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  • Hindawi
  • National Academy of Sciences
  • 2020-2023  (32)
  • 2020-2020
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  • 1
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    High (3)He/(4)He in central Panama reveals a distal connection to the Galápagos plume (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bekaert, D. V., Gazel, E., Turner, S., Behn, M. D., de Moor, J. M., Zahirovic, S., Manea, V. C., Hoernle, K., Fischer, T. P., Hammerstrom, A., Seltzer, A. M., Kulongoski, J. T., Patel, B. S., Schrenk, M. O., Halldórsson, S. A., Nakagawa, M., Ramírez, C. J., Krantz, J. A., Yücel, M., Ballentine, C. J., Giovannelli, D., Lloyd, K. G., Barry, P. H. High (3)He/(4)He in central Panama reveals a distal connection to the Galápagos plume. Proceedings of the National Academy of Sciences of the United States of America, 118(47), (2021): e2110997118, https://doi.org/10.1073/pnas.2110997118.
    Description: It is well established that mantle plumes are the main conduits for upwelling geochemically enriched material from Earth's deep interior. The fashion and extent to which lateral flow processes at shallow depths may disperse enriched mantle material far (〉1,000 km) from vertical plume conduits, however, remain poorly constrained. Here, we report He and C isotope data from 65 hydrothermal fluids from the southern Central America Margin (CAM) which reveal strikingly high 3He/4He (up to 8.9RA) in low-temperature (≤50 °C) geothermal springs of central Panama that are not associated with active volcanism. Following radiogenic correction, these data imply a mantle source 3He/4He 〉10.3RA (and potentially up to 26RA, similar to Galápagos hotspot lavas) markedly greater than the upper mantle range (8 ± 1RA). Lava geochemistry (Pb isotopes, Nb/U, and Ce/Pb) and geophysical constraints show that high 3He/4He values in central Panama are likely derived from the infiltration of a Galápagos plume–like mantle through a slab window that opened ∼8 Mya. Two potential transport mechanisms can explain the connection between the Galápagos plume and the slab window: 1) sublithospheric transport of Galápagos plume material channeled by lithosphere thinning along the Panama Fracture Zone or 2) active upwelling of Galápagos plume material blown by a “mantle wind” toward the CAM. We present a model of global mantle flow that supports the second mechanism, whereby most of the eastward transport of Galápagos plume material occurs in the shallow asthenosphere. These findings underscore the potential for lateral mantle flow to transport mantle geochemical heterogeneities thousands of kilometers away from plume conduits.
    Description: This work was principally supported by Grant G-2016-7206 from the Alfred P. Sloan Foundation and the Deep Carbon Observatory to P.H.B. We also acknowledge the NSF awards (1144559, 1923915, and 2015789) to P.H.B., which partially supported this work. S.Z. was supported by the Australian Research Council Grant DE210100084 and a University of Sydney Robinson Fellowship. D.G. was partially supported by funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program Grant Agreement No. 948972—COEVOLVE—ERC-2020-STG. This study was also supported in part by NSF award No. EAR 1826673 to E.G. Folkmar Hauff is acknowledged for contributing to the analysis of the La Providencia samples at GEOMAR.
    Keywords: Helium ; Mantle plume ; Slab window ; Mantle flow ; Geochemistry
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  • 2
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    The evolution of synaptic and cognitive capacity: insights from the nervous system transcriptome of Aplysia (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-11-10
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Orvis, J., Albertin, C., Shrestha, P., Chen, S., Zheng, M., Rodriguez, C., Tallon, L., Mahurkar, A., Zimin, A., Kim, M., Liu, K., Kandel, E., Fraser, C., Sossin, W., & Abrams, T. The evolution of synaptic and cognitive capacity: insights from the nervous system transcriptome of Aplysia. Proceedings of the National Academy of Sciences of the United States of America, 119(28), (2022): e2122301119, https://doi.org/10.1073/pnas.2122301119.
    Description: The gastropod mollusk Aplysia is an important model for cellular and molecular neurobiological studies, particularly for investigations of molecular mechanisms of learning and memory. We developed an optimized assembly pipeline to generate an improved Aplysia nervous system transcriptome. This improved transcriptome enabled us to explore the evolution of cognitive capacity at the molecular level. Were there evolutionary expansions of neuronal genes between this relatively simple gastropod Aplysia (20,000 neurons) and Octopus (500 million neurons), the invertebrate with the most elaborate neuronal circuitry and greatest behavioral complexity? Are the tremendous advances in cognitive power in vertebrates explained by expansion of the synaptic proteome that resulted from multiple rounds of whole genome duplication in this clade? Overall, the complement of genes linked to neuronal function is similar between Octopus and Aplysia. As expected, a number of synaptic scaffold proteins have more isoforms in humans than in Aplysia or Octopus. However, several scaffold families present in mollusks and other protostomes are absent in vertebrates, including the Fifes, Lev10s, SOLs, and a NETO family. Thus, whereas vertebrates have more scaffold isoforms from select families, invertebrates have additional scaffold protein families not found in vertebrates. This analysis provides insights into the evolution of the synaptic proteome. Both synaptic proteins and synaptic plasticity evolved gradually, yet the last deuterostome-protostome common ancestor already possessed an elaborate suite of genes associated with synaptic function, and critical for synaptic plasticity.
    Description: This work was supported by NSF EAGER Award IOS-1255695 and NIH grant R01 MH 55880 grant to T.W.A.; by a Natural Sciences and Engineering Research Council of Canada Discovery grant and Canadian Institutes of Health Research project grant 340328 to W.S.; by funding from the HHMI to E.R.K.; and by a Hibbitt Early Career Fellowship to C.A. W.S. is James McGill Professor at McGill University.
    Keywords: Neural plasticity ; Synaptic plasticity ; Evolution ; Neuromodulation ; Aplysia
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  • 3
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    Discovery of active off-axis hydrothermal vents at 9° 54’N East Pacific Rise (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-11-10
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in McDermott, J. M., Parnell-Turner, R., Barreyre, T., Herrera, S., Downing, C. C., Pittoors, N. C., Pehr, K., Vohsen, S. A., Dowd, W. S., Wu, J.-N., Marjanović, M., & Fornari, D. J. Discovery of active off-axis hydrothermal vents at 9° 54’N East Pacific Rise. Proceedings of the National Academy of Sciences of the United States of America, 119(30), (2022): e2205602119, https://doi.org/10.1073/pnas.2205602119.
    Description: Comprehensive knowledge of the distribution of active hydrothermal vent fields along midocean ridges is essential to understanding global chemical and heat fluxes and endemic faunal distributions. However, current knowledge is biased by a historical preference for on-axis surveys. A scarcity of high-resolution bathymetric surveys in off-axis regions limits vent identification, which implies that the number of vents may be underestimated. Here, we present the discovery of an active, high-temperature, off-axis hydrothermal field on a fast-spreading ridge. The vent field is located 750 m east of the East Pacific Rise axis and ∼7 km north of on-axis vents at 9° 50′N, which are situated in a 50- to 100-m-wide trough. This site is currently the largest vent field known on the East Pacific Rise between 9 and 10° N. Its proximity to a normal fault suggests that hydrothermal fluid pathways are tectonically controlled. Geochemical evidence reveals deep fluid circulation to depths only 160 m above the axial magma lens. Relative to on-axis vents at 9° 50′N, these off-axis fluids attain higher temperatures and pressures. This tectonically controlled vent field may therefore exhibit greater stability in fluid composition, in contrast to more dynamic, dike-controlled, on-axis vents. The location of this site indicates that high-temperature convective circulation cells extend to greater distances off axis than previously realized. Thorough high-resolution mapping is necessary to understand the distribution, frequency, and physical controls on active off-axis vent fields so that their contribution to global heat and chemical fluxes and role in metacommunity dynamics can be determined.
    Description: Financial support was provided by the NSF Awards OCE-1949938 (to J.M.M.), OCE-1948936 (to R.P.-T.), and OCE-1949485 (to D.J.F. and T.B.).
    Keywords: Hydrothermal activity ; Midocean ridge ; Ocean chemistry ; Chemosynthetic ecosystem ; East Pacific Rise
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  • 4
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    Hox gene expression predicts tetrapod-like axial regionalization in the skate, Leucoraja erinacea (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Criswell, K. E., Roberts, L. E., Koo, E. T., Head, J. J., & Gillis, J. A. Hox gene expression predicts tetrapod-like axial regionalization in the skate, Leucoraja erinacea. Proceedings of the National Academy of Sciences of the United States of America, 118(51), (2021): e2114563118, https://doi.org/10.1073/pnas.2114563118.
    Description: The axial skeleton of tetrapods is organized into distinct anteroposterior regions of the vertebral column (cervical, trunk, sacral, and caudal), and transitions between these regions are determined by colinear anterior expression boundaries of Hox5/6, -9, -10, and -11 paralogy group genes within embryonic paraxial mesoderm. Fishes, conversely, exhibit little in the way of discrete axial regionalization, and this has led to scenarios of an origin of Hox-mediated axial skeletal complexity with the evolutionary transition to land in tetrapods. Here, combining geometric morphometric analysis of vertebral column morphology with cell lineage tracing of hox gene expression boundaries in developing embryos, we recover evidence of at least five distinct regions in the vertebral skeleton of a cartilaginous fish, the little skate (Leucoraja erinacea). We find that skate embryos exhibit tetrapod-like anteroposterior nesting of hox gene expression in their paraxial mesoderm, and we show that anterior expression boundaries of hox5/6, hox9, hox10, and hox11 paralogy group genes predict regional transitions in the differentiated skate axial skeleton. Our findings suggest that hox-based axial skeletal regionalization did not originate with tetrapods but rather has a much deeper evolutionary history than was previously appreciated.
    Description: This research was funded by a Natural Environment Research Council Grant (to J.J.H., J.A.G., and K.E.C.: NE/S000739/1) and a Royal Society University Research Fellowship (UF130182 and URF\R\191007), Royal Society Research Grant (RG140377), and University of Cambridge Sir Isaac Newton Trust Grant (14.23z) (to J.A.G.).
    Keywords: Hox genes ; Regionalization ; Chondrichthyan ; Vertebral column
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  • 5
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    Holocene bidirectional river system along the Kenya Rift and its influence on East African faunal exchange and diversity gradients (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-19
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Dommain, R., Riedl, S., Olaka, L. A., deMenocal, P., Deino, A. L., Owen, R. B., Muiruri, V., Müller, J., Potts, R., & Strecker, M. R. Holocene bidirectional river system along the Kenya Rift and its influence on East African faunal exchange and diversity gradients. Proceedings of the National Academy of Sciences of the United States of America, 119(28),(2022): e2121388119, https://doi.org/10.1073/pnas.2121388119.
    Description: East Africa is a global biodiversity hotspot and exhibits distinct longitudinal diversity gradients from west to east in freshwater fishes and forest mammals. The assembly of this exceptional biodiversity and the drivers behind diversity gradients remain poorly understood, with diversification often studied at local scales and less attention paid to biotic exchange between Afrotropical regions. Here, we reconstruct a river system that existed for several millennia along the now semiarid Kenya Rift Valley during the humid early Holocene and show how this river system influenced postglacial dispersal of fishes and mammals due to its dual role as a dispersal corridor and barrier. Using geomorphological, geochronological, isotopic, and fossil analyses and a synthesis of radiocarbon dates, we find that the overflow of Kenyan rift lakes between 12 and 8 ka before present formed a bidirectional river system consisting of a “Northern River” connected to the Nile Basin and a “Southern River,” a closed basin. The drainage divide between these rivers represented the only viable terrestrial dispersal corridor across the rift. The degree and duration of past hydrological connectivity between adjacent river basins determined spatial diversity gradients for East African fishes. Our reconstruction explains the isolated distribution of Nilotic fish species in modern Kenyan rift lakes, Guineo-Congolian mammal species in forests east of the Kenya Rift, and recent incipient vertebrate speciation and local endemism in this region. Climate-driven rearrangements of drainage networks unrelated to tectonic activity contributed significantly to the assembly of species diversity and modern faunas in the East African biodiversity hotspot.
    Description: R.D. was funded by a Smithsonian Human Origins Postdoctoral Fellowship and by Geo.X—the Research Network for Geosciences in Berlin and Potsdam. Fig. 1 D, E, and G and SI Appendix, Figs. S1 and S3 are based on the TanDEM-X Science DEM granted to L.A.O. and S.R. by the German Aerospace Center (DLR) in 2017. L.A.O. acknowledges the Volkswagen Foundation for funding this study with Grant No. 89369. M.R.S. and S.R. were supported by funds from Potsdam University and the Geothermal Development Company of Kenya, and R.B.O. and V.M. were supported by the Hong Kong General Research Fund. We acknowledge support from the National Museums of Kenya and the Kenya Government permission granted by the Ministry of Sports, Culture and the Arts, and by the National Commission for Science, Technology and Innovation (NACOSTI) Permits P/14/7709/683 (to R.P.) and P/16/11924/11448 (to L.A.O.). This work is a contribution of the Olorgesailie Drilling Project, for which support from the National Museums of Kenya, the Oldonyo Nyokie Group Ranch, the Peter Buck Fund for Human Origins Research (Smithsonian Institution), the William H. Donner Foundation, the Ruth and Vernon Taylor Foundation, Whitney and Betty MacMillan, and the Smithsonian Human Origins Program is gratefully acknowledged. LacCore is acknowledged for support in drilling and core storage.
    Keywords: East Africa ; Biogeography ; Biodiversity ; Hydrological connectivity ; Holocene
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  • 6
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    Nutrient availability and senescence spatially structure the dynamics of a foundation species (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-20
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bell, T. W., & Siegel, D. A. Nutrient availability and senescence spatially structure the dynamics of a foundation species. Proceedings of the National Academy of Sciences of the United States of America, 119(1), (2021): e2105135118, https://doi.org/10.1073/pnas.2105135118.
    Description: Disentangling the roles of the external environment and internal biotic drivers of plant population dynamics is challenging due to the absence of relevant physiological and abundance information over appropriate space and time scales. Remote observations of giant kelp biomass and photosynthetic pigment concentrations are used to show that spatiotemporal patterns of physiological condition, and thus growth and production, are regulated by different processes depending on the scale of observation. Nutrient supply was linked to regional scale (〉1 km) physiological condition dynamics, and kelp forest stands were more persistent where nutrient levels were consistently high. However, on local scales (〈1 km), internal senescence processes related to canopy age demographics determined patterns of biomass loss across individual kelp forests despite uniform nutrient conditions. Repeat measurements of physiology over continuous spatial fields can provide insights into complex dynamics that are unexplained by the environmental drivers thought to regulate abundance. Emerging remote sensing technologies that provide simultaneous estimates of abundance and physiology can quantify the roles of environmental change and demographics governing plant population dynamics for a wide range of aquatic and terrestrial ecosystems.
    Description: This work was supported by the US NSF (Grants OCE 1232779 and 1831937), by the US Department of Energy (Cooperative Agreement DE-AR0000922), and by NASA (Grant NNX14AR62A) and the NASA Earth and Space Sciences Fellowship program in support of T.W.B.
    Keywords: Physiology ; Population ; Biomass ; Hyperspectral ; Giant kelp
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  • 7
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    Trivalent chromium isotopes in the eastern tropical North Pacific oxygen-deficient zone (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2021. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 118(8), (2021): e1918605118, https://doi.org/10.1073/pnas.1918605118.
    Description: Changes in chromium (Cr) isotope ratios due to fractionation between trivalent [Cr(III)] and hexavalent [Cr(VI)] are being utilized by geologists to infer oxygen conditions in past environments. However, there is little information available on Cr in the modern ocean to ground-truth these inferences. Transformations between the two chromium species are important processes in oceanic Cr cycling. Here we present profiles of hexavalent and trivalent Cr concentrations and stable isotope ratios from the eastern tropical North Pacific (ETNP) oxygen-deficient zone (ODZ) which support theoretical and experimental studies that predict that lighter Cr is preferentially reduced in low-oxygen environments and that residual dissolved Cr becomes heavier due to removal of particle-reactive Cr(III) on sinking particles. The Cr(III) maximum dominantly occurs in the upper portion of the ODZ, implying that microbial activity (dependent on the sinking flux of organic matter) may be the dominant mechanism for this transformation, rather than a simple inorganic chemical conversion between the species depending on the redox potential.
    Description: We thank chief scientist Gabrielle Rocap for accommodating us on cruises Roger Revelle 1804-5 and Kilo Moana 19-20 (sponsored by NSF Grant DEB-1542240 to G. Rocap, A. Devol, R. Kiel, and C. Deutch), Jim Moffett for helping with sampling on these cruises, and Mark Altabet and Frank Stewart for collecting the samples from station 2T on cruise New Horizon 1410. This research was supported by NSF Grant OCE-1736996 (to E.A.B.) and by a fellowship from the Massachusetts Institute of Technology/Woods Hole Oceanographic Institution Joint Program in Oceanography.
    Keywords: Chromium isotopes ; Oxygen-deficient zones ; Trace elements ; Trivalent chromium ; Hexavalent ; Chromium
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  • 8
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    Global collision-risk hotspots of marine traffic and the world’s largest fish, the whale shark (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-08-15
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Womersley, F. C., Humphries, N. E., Queiroz, N., Vedor, M., da Costa, I., Furtado, M., Tyminski, J. P., Abrantes, K., Araujo, G., Bach, S. S., Barnett, A., Berumen, M. L., Bessudo Lion, S., Braun, C. D., Clingham, E., Cochran, J. E. M., de la Parra, R., Diamant, S., Dove, A. D. M., Dudgeon, C. L., Erdmann, M. V., Espinoza, E., Fitzpatrick, R., González Cano, J., Green, J. R., Guzman, H. M., Hardenstine, R., Hasan, A., Hazin, F. H. V., Hearn, A. R., Hueter, R. E., Jaidah, M. Y., Labaja, J., Ladinol, F., Macena, B. C. L., Morris Jr., J. J., Norman, B. M., Peñaherrera-Palmav, C., Pierce, S. J., Quintero, L. M., Ramırez-Macías, D., Reynolds, S. D., Richardson, A. J., Robinson, D. P., Rohner, C. A., Rowat, D. R. L., Sheaves, M., Shivji, M. S., Sianipar, A. B., Skomal, G. B., Soler, G., Syakurachman, I., Thorrold, S. R., Webb, D. H., Wetherbee, B. M., White, T. D., Clavelle, T., Kroodsma, D. A., Thums, M., Ferreira, L. C., Meekan, M. G., Arrowsmith, L. M., Lester, E. K., Meyers, M. M., Peel, L. R., Sequeira, A. M. M., Eguıluz, V. M., Duarte, C. M., & Sims, D. W. Global collision-risk hotspots of marine traffic and the world’s largest fish, the whale shark. Proceedings of the National Academy of Sciences of the United States of America, 119(20), (2022): e2117440119, https://doi.org/10.1073/pnas.2117440119.
    Description: Marine traffic is increasing globally yet collisions with endangered megafauna such as whales, sea turtles, and planktivorous sharks go largely undetected or unreported. Collisions leading to mortality can have population-level consequences for endangered species. Hence, identifying simultaneous space use of megafauna and shipping throughout ranges may reveal as-yet-unknown spatial targets requiring conservation. However, global studies tracking megafauna and shipping occurrences are lacking. Here we combine satellite-tracked movements of the whale shark, Rhincodon typus, and vessel activity to show that 92% of sharks’ horizontal space use and nearly 50% of vertical space use overlap with persistent large vessel (〉300 gross tons) traffic. Collision-risk estimates correlated with reported whale shark mortality from ship strikes, indicating higher mortality in areas with greatest overlap. Hotspots of potential collision risk were evident in all major oceans, predominantly from overlap with cargo and tanker vessels, and were concentrated in gulf regions, where dense traffic co-occurred with seasonal shark movements. Nearly a third of whale shark hotspots overlapped with the highest collision-risk areas, with the last known locations of tracked sharks coinciding with busier shipping routes more often than expected. Depth-recording tags provided evidence for sinking, likely dead, whale sharks, suggesting substantial “cryptic” lethal ship strikes are possible, which could explain why whale shark population declines continue despite international protection and low fishing-induced mortality. Mitigation measures to reduce ship-strike risk should be considered to conserve this species and other ocean giants that are likely experiencing similar impacts from growing global vessel traffic.
    Description: Funding for data analysis was provided by the UK Natural Environment Research Council (NERC) through a University of Southampton INSPIRE DTP PhD Studentship to F.C.W. Additional funding for data analysis was provided by NERC Discovery Science (NE/R00997/X/1) and the European Research Council (ERC-AdG-2019 883583 OCEAN DEOXYFISH) to D.W.S., Fundação para a Ciência e a Tecnologia (FCT) under PTDC/BIA/28855/2017 and COMPETE POCI-01–0145-FEDER-028855, and MARINFO–NORTE-01–0145-FEDER-000031 (funded by Norte Portugal Regional Operational Program [NORTE2020] under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund–ERDF) to N.Q. FCT also supported N.Q. (CEECIND/02857/2018) and M.V. (PTDC/BIA-COM/28855/2017). D.W.S. was supported by a Marine Biological Association Senior Research Fellowship. All tagging procedures were approved by institutional ethical review bodies and complied with all relevant ethical regulations in the jurisdictions in which they were performed. Details for individual research teams are given in SI Appendix, section 8. Full acknowledgments for tagging and field research are given in SI Appendix, section 7. This research is part of the Global Shark Movement Project (https://www.globalsharkmovement.org).
    Keywords: ship strike ; marine megafauna ; conservation ; movement ecology ; human impact
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  • 9
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    Phosphonate production by marine microbes: exploring new sources and potential function (2022)
    National Academy of Sciences
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    Publication Date: 2022-06-10
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Acker, M., Hogle, S. L., Berube, P. M., Hackl, T., Coe, A., Stepanauskas, R., Chisholm, S. W., & Repeta, D. J. Phosphonate production by marine microbes: exploring new sources and potential function. Proceedings of the National Academy of Sciences of the United States of America, 119(11), (2022): e2113386119, https://doi.org/10.1073/pnas.2113386119.
    Description: Phosphonates are organophosphorus metabolites with a characteristic C-P bond. They are ubiquitous in the marine environment, their degradation broadly supports ecosystem productivity, and they are key components of the marine phosphorus (P) cycle. However, the microbial producers that sustain the large oceanic inventory of phosphonates as well as the physiological and ecological roles of phosphonates are enigmatic. Here, we show that phosphonate synthesis genes are rare but widely distributed among diverse bacteria and archaea, including Prochlorococcus and SAR11, the two major groups of bacteria in the ocean. In addition, we show that Prochlorococcus can allocate over 40% of its total cellular P-quota toward phosphonate production. However, we find no evidence that Prochlorococcus uses phosphonates for surplus P storage, and nearly all producer genomes lack the genes necessary to degrade and assimilate phosphonates. Instead, we postulate that phosphonates are associated with cell-surface glycoproteins, suggesting that phosphonates mediate ecological interactions between the cell and its surrounding environment. Our findings indicate that the oligotrophic surface ocean phosphonate pool is sustained by a relatively small fraction of the bacterioplankton cells allocating a significant portion of their P quotas toward secondary metabolism and away from growth and reproduction.
    Description: This work was supported in part by grants from the NSF (OCE-1153588 and DBI-0424599 to S.W.C.; OCE-1335810 and OIA-1826734 to R.S.; and OCE-1634080 to D.J.R.), the Gordon and Betty Moore Foundation (no. 6000 to D.J.R.), and the Simons Foundation (Life Sciences Project Award IDs 337262 and 647135 to S.W.C.; 510023 to R.S.; and Simons Collaboration on Ocean Processes and Ecology [SCOPE] Award ID 329108 to S.W.C. and D.J.R.).
    Keywords: phosphonate ; Prochlorococcus ; marine ; biogeochemistry ; phosphorus
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  • 10
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    The Earth BioGenome Project 2020: starting the clock (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-27
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Lewin, H. A., Richards, S., Lieberman Aiden, E., Allende, M. L., Archibald, J. M., Bálint, M., Barker, K. B., Baumgartner, B., Belov, K., Bertorelle, G., Blaxter, Mark L., Cai, J., Caperello, N. D., Carlson, K., Castilla-Rubio, J. C., Chaw, S-M., Chen, L., Childers, A. K., Coddington, J. A., Conde, D. A., Corominas, M., Crandall, K. A., Crawford, A. J., DiPalma, F., Durbin, R., Ebenezer, T. E., Edwards, S. V., Fedrigo, O., Flicek, P., Formenti, G., Gibbs, R. A., Gilbert, M. Thomas P., Goldstein, M. M., Graves, J. M., Greely, H. T., Grigoriev, I. V., Hackett, K. J., Hall, N., Haussler, D., Helgen, K. M., Hogg, C. J., Isobe, S., Jakobsen, K. S., Janke, A., Jarvis, E. D., Johnson, W. E., Jones, S. J. M., Karlsson, E. K., Kersey, P. J., Kim, J-H., Kress, W. J., Kuraku, S., Lawniczak, M. K. N., Leebens-Mack, J. H., Li, X., Lindblad-Toh, K., Liu, X., Lopez, J. V., Marques-Bonet, T., Mazard, S., Mazet, J. A. K., Mazzoni, C. J., Myers, E. W., O’Neill, R. J., Paez, S., Park, H., Robinson, G. E., Roquet, C., Ryder, O. A., Sabir, J. S. M., Shaffer, H. B., Shank, T. M., Sherkow, J. S., Soltis, P. S., Tang, B., Tedersoo, L., Uliano-Silva, M., Wang, K., Wei, X., Wetzer, R., Wilson, J. L., Xu, X., Yang, H., Yoder, A. D., Zhang, G. The Earth BioGenome Project 2020: starting the clock. Proceedings of the National Academy of Sciences of the United States of America, 119(4), (2022): e2115635118, https://doi.org/10.1073/pnas.2115635118.
    Description: November 2020 marked 2 y since the launch of the Earth BioGenome Project (EBP), which aims to sequence all known eukaryotic species in a 10-y timeframe. Since then, significant progress has been made across all aspects of the EBP roadmap, as outlined in the 2018 article describing the project’s goals, strategies, and challenges (1). The launch phase has ended and the clock has started on reaching the EBP’s major milestones. This Special Feature explores the many facets of the EBP, including a review of progress, a description of major scientific goals, exemplar projects, ethical legal and social issues, and applications of biodiversity genomics. In this Introduction, we summarize the current status of the EBP, held virtually October 5 to 9, 2020, including recent updates through February 2021. References to the nine Perspective articles included in this Special Feature are cited to guide the reader toward deeper understanding of the goals and challenges facing the EBP.
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  • 11
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    Climate control on terrestrial biospheric carbon turnover (2021)
    National Academy of Sciences
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    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Eglinton, T. I., Galy, V. V., Hemingway, J. D., Feng, X., Bao, H., Blattmann, T. M., Dickens, A. F., Gies, H., Giosan, L., Haghipour, N., Hou, P., Lupker, M., McIntyre, C. P., Montluçon, D. B., Peucker-Ehrenbrink, B., Ponton, C., Schefuß, E., Schwab, M. S., Voss, B. M., Wacker, L., Wu, Y., & Zhao, M. Climate control on terrestrial biospheric carbon turnover. Proceedings of the National Academy of Sciences of the United States of America, 118(8), (2021): e2011585118, htps://doi.org/ 10.1073/pnas.2011585118.
    Description: Terrestrial vegetation and soils hold three times more carbon than the atmosphere. Much debate concerns how anthropogenic activity will perturb these surface reservoirs, potentially exacerbating ongoing changes to the climate system. Uncertainties specifically persist in extrapolating point-source observations to ecosystem-scale budgets and fluxes, which require consideration of vertical and lateral processes on multiple temporal and spatial scales. To explore controls on organic carbon (OC) turnover at the river basin scale, we present radiocarbon (14C) ages on two groups of molecular tracers of plant-derived carbon—leaf-wax lipids and lignin phenols—from a globally distributed suite of rivers. We find significant negative relationships between the 14C age of these biomarkers and mean annual temperature and precipitation. Moreover, riverine biospheric-carbon ages scale proportionally with basin-wide soil carbon turnover times and soil 14C ages, implicating OC cycling within soils as a primary control on exported biomarker ages and revealing a broad distribution of soil OC reactivities. The ubiquitous occurrence of a long-lived soil OC pool suggests soil OC is globally vulnerable to perturbations by future temperature and precipitation increase. Scaling of riverine biospheric-carbon ages with soil OC turnover shows the former can constrain the sensitivity of carbon dynamics to environmental controls on broad spatial scales. Extracting this information from fluvially dominated sedimentary sequences may inform past variations in soil OC turnover in response to anthropogenic and/or climate perturbations. In turn, monitoring riverine OC composition may help detect future climate-change–induced perturbations of soil OC turnover and stocks.
    Description: This work was supported by grants from the US NSF (OCE-0928582 to T.I.E. and V.V.G.; OCE-0851015 to B.P.-E., T.I.E., and V.V.G.; and EAR-1226818 to B.P.-E.), Swiss National Science Foundation (200021_140850, 200020_163162, and 200020_184865 to T.I.E.), and National Natural Science Foundation of China (41520104009 to M.Z.).
    Keywords: Radiocarbon ; Plant biomarkers ; Carbon turnover times ; Fluvial carbon ; Carbon cycle
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  • 12
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    Human arrival and landscape dynamics in the northern Bahamas (2021)
    National Academy of Sciences
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    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Fall, P. L., van Hengstum, P. J., Lavold-Foote, L., Donnelly, J. P., Albury, N. A., & Tamalavage, A. E. Human arrival and landscape dynamics in the northern Bahamas. Proceedings of the National Academy of Sciences of the United States of America, 118(10), (2021): e2015764118, https://doi.org/10.1073/pnas.2015764118.
    Description: The first Caribbean settlers were Amerindians from South America. Great Abaco and Grand Bahama, the final islands colonized in the northernmost Bahamas, were inhabited by the Lucayans when Europeans arrived. The timing of Lucayan arrival in the northern Bahamas has been uncertain because direct archaeological evidence is limited. We document Lucayan arrival on Great Abaco Island through a detailed record of vegetation, fire, and landscape dynamics based on proxy data from Blackwood Sinkhole. From about 3,000 to 1,000 y ago, forests dominated by hardwoods and palms were resilient to the effects of hurricanes and cooling sea surface temperatures. The arrival of Lucayans by about 830 CE (2σ range: 720 to 920 CE) is demarcated by increased burning and followed by landscape disturbance and a time-transgressive shift from hardwoods and palms to the modern pine forest. Considering that Lucayan settlements in the southern Bahamian archipelago are dated to about 750 CE (2σ range: 600 to 900 CE), these results demonstrate that Lucayans spread rapidly through the archipelago in less than 100 y. Although precontact landscapes would have been influenced by storms and climatic trends, the most pronounced changes follow more directly from landscape burning and ecosystem shifts after Lucayan arrival. The pine forests of Abaco declined substantially between 1500 and 1670 CE, a period of increased regional hurricane activity, coupled with fires on an already human-impacted landscape. Any future intensification of hurricane activity in the tropical North Atlantic Ocean threatens the sustainability of modern pine forests in the northern Bahamas.
    Description: This research was supported by NSF Awards GSS-1118340 (P.L.F.), OCE-1356509 (P.J.v.H.), OCE-1703087 (P.J.v.H.), and OCE-1356708 (J.P.D.).
    Keywords: Anthropogenic burning ; Lucayan ; Caribbean ; Pollen ; Vegetation change
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  • 13
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    Thermodynamic feasibility of shipboard conversion of marine plastics to blue diesel for self-powered ocean cleanup (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Belden, E. R., Kazantzis, N. K., Reddy, C. M., Kite-Powell, H., Timko, M. T., Italiani, E., & Herschbach, D. R. Thermodynamic feasibility of shipboard conversion of marine plastics to blue diesel for self-powered ocean cleanup. Proceedings of the National Academy of Sciences of the United States of America, 118(46),(2021): e2107250118, https://doi.org/10.1073/pnas.2107250118.
    Description: Collecting and removing ocean plastics can mitigate their environmental impacts; however, ocean cleanup will be a complex and energy-intensive operation that has not been fully evaluated. This work examines the thermodynamic feasibility and subsequent implications of hydrothermally converting this waste into a fuel to enable self-powered cleanup. A comprehensive probabilistic exergy analysis demonstrates that hydrothermal liquefaction has potential to generate sufficient energy to power both the process and the ship performing the cleanup. Self-powered cleanup reduces the number of roundtrips to port of a waste-laden ship, eliminating the need for fossil fuel use for most plastic concentrations. Several cleanup scenarios are modeled for the Great Pacific Garbage Patch (GPGP), corresponding to 230 t to 11,500 t of plastic removed yearly; the range corresponds to uncertainty in the surface concentration of plastics in the GPGP. Estimated cleanup times depends mainly on the number of booms that can be deployed in the GPGP without sacrificing collection efficiency. Self-powered cleanup may be a viable approach for removal of plastics from the ocean, and gaps in our understanding of GPGP characteristics should be addressed to reduce uncertainty.
    Description: The US NSF supported this work as part of its 2026 Idea Machine initiative (Chemical, Bioengineering, Environmental, and Transport Systems, EArly-concept Grants for Exploratory Research Award #2032621). E.R.B.’s contribution was funded, in part, by the NSF Graduate Research Fellowship Program under Grant No. 2038257.
    Keywords: Ocean plastic ; Hydrothermal liquefaction ; Exergy analysis ; Monte Carlo simulation
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  • 14
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    Neuromechanical wave resonance in jellyfish swimming (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-27
    Description: Author Posting. © National Academy of Sciences, 2021. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 118(11), (2021): e2020025118, https://doi.org/10.1073/pnas.2020025118.
    Description: For organisms to have robust locomotion, their neuromuscular organization must adapt to constantly changing environments. In jellyfish, swimming robustness emerges when marginal pacemakers fire action potentials throughout the bell’s motor nerve net, which signals the musculature to contract. The speed of the muscle activation wave is dictated by the passage times of the action potentials. However, passive elastic material properties also influence the emergent kinematics, with time scales independent of neuromuscular organization. In this multimodal study, we examine the interplay between these two time scales during turning. A three-dimensional computational fluid–structure interaction model of a jellyfish was developed to determine the resulting emergent kinematics, using bidirectional muscular activation waves to actuate the bell rim. Activation wave speeds near the material wave speed yielded successful turns, with a 76-fold difference in turning rate between the best and worst performers. Hyperextension of the margin occurred only at activation wave speeds near the material wave speed, suggesting resonance. This hyperextension resulted in a 34-fold asymmetry in the circulation of the vortex ring between the inside and outside of the turn. Experimental recording of the activation speed confirmed that jellyfish actuate within this range, and flow visualization using particle image velocimetry validated the corresponding fluid dynamics of the numerical model. This suggests that neuromechanical wave resonance plays an important role in the robustness of an organism’s locomotory system and presents an undiscovered constraint on the evolution of flexible organisms. Understanding these dynamics is essential for developing actuators in soft body robotics and bioengineered pumps.
    Description: This research was funded by the NSF Division of Mathematical Sciences, under Faculty Early Career Development Program Grant 1151478 (to L.A.M.).
    Description: 2021-09-16
    Keywords: Jellyfish ; Propulsion ; Neuromechanics ; Fluid-structure interaction ; Maneuverability
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  • 15
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    Teamwork in the viscous oceanic microscale (2021)
    National Academy of Sciences
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    Publication Date: 2022-10-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Kanso, E. A., Lopes, R. M., Strickler, J. R., Dabiri, J. O., & Costello, J. H. Teamwork in the viscous oceanic microscale. Proceedings of the National Academy of Sciences of the United States of America, 118(29), (2021): e2018193118, https://doi.org/10.1073/pnas.2018193118.
    Description: Nutrient acquisition is crucial for oceanic microbes, and competitive solutions to solve this challenge have evolved among a range of unicellular protists. However, solitary solutions are not the only approach found in natural populations. A diverse array of oceanic protists form temporary or even long-lasting attachments to other protists and marine aggregates. Do these planktonic consortia provide benefits to their members? Here, we use empirical and modeling approaches to evaluate whether the relationship between a large centric diatom, Coscinodiscus wailesii, and a ciliate epibiont, Pseudovorticella coscinodisci, provides nutrient flux benefits to the host diatom. We find that fluid flows generated by ciliary beating can increase nutrient flux to a diatom cell surface four to 10 times that of a still cell without ciliate epibionts. This cosmopolitan species of diatom does not form consortia in all environments but frequently joins such consortia in nutrient-depleted waters. Our results demonstrate that symbiotic consortia provide a cooperative alternative of comparable or greater magnitude to sinking for enhancement of nutrient acquisition in challenging environments.
    Description: We are grateful to Y. Garcia for help with organism sampling and sorting. E.A.K. is funded by NSF-2100209, NSF RAISE IOS-2034043 and NIH R01 HL 153622-01A1. R.M.L. is a CNPq research fellow (grant # 310642/2017-5). J.H.C. and J.O.D. are funded by Grant NSF-2100705.
    Keywords: Phytoplankton ; Nutrient limitation ; Symbiosis ; Diffusion limitation ; Cell size
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  • 16
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    Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Reysenbach, A. L., St John, E., Meneghin, J., Flores, G. E., Podar, M., Dombrowski, N., Spang, A., L'Haridon, S., Humphris, S. E., de Ronde, C. E. J., Caratori Tontini, F., Tivey, M., Stucker, V. K., Stewart, L. C., Diehl, A., & Bach, W. Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities. Proceedings of the National Academy of Sciences of the United States of America, 117(51), (2020): 202019021, doi:10.1073/pnas.2019021117.
    Description: Hydrothermally active submarine volcanoes are mineral-rich biological oases contributing significantly to chemical fluxes in the deep sea, yet little is known about the microbial communities inhabiting these systems. Here we investigate the diversity of microbial life in hydrothermal deposits and their metagenomics-inferred physiology in light of the geological history and resulting hydrothermal fluid paths in the subsurface of Brothers submarine volcano north of New Zealand on the southern Kermadec arc. From metagenome-assembled genomes we identified over 90 putative bacterial and archaeal genomic families and nearly 300 previously unknown genera, many potentially endemic to this submarine volcanic environment. While magmatically influenced hydrothermal systems on the volcanic resurgent cones of Brothers volcano harbor communities of thermoacidophiles and diverse members of the superphylum “DPANN,” two distinct communities are associated with the caldera wall, likely shaped by two different types of hydrothermal circulation. The communities whose phylogenetic diversity primarily aligns with that of the cone sites and magmatically influenced hydrothermal systems elsewhere are characterized predominately by anaerobic metabolisms. These populations are probably maintained by fluids with greater magmatic inputs that have interacted with different (deeper) previously altered mineral assemblages. However, proximal (a few meters distant) communities with gene-inferred aerobic, microaerophilic, and anaerobic metabolisms are likely supported by shallower seawater-dominated circulation. Furthermore, mixing of fluids from these two distinct hydrothermal circulation systems may have an underlying imprint on the high microbial phylogenomic diversity. Collectively our results highlight the importance of considering geologic evolution and history of subsurface processes in studying microbial colonization and community dynamics in volcanic environments.
    Description: We thank the captain and crew of the R/V Thompson and the engineers from Woods Hole Oceanographic Institution for the successful operation of ROV Jason. The project was funded by NSF grants OCE‐1558356 (Principal Investigator S.E.H.) and OCE-1558795 (Principal Investigator A.-L.R.). S.L. received a grant from the University of Brest to work in the A.-L.R. laboratory. A travel fund from Interridge enabled A.D. to participate on the R/V Thompson cruise. Funding for this work for C.E.J.d.R., F.C.T., V.K.S., and L.C.S. was provided by the New Zealand government. A.S. was supported by the Swedish Research Council (Vetenskapsrådet starting grant 2016-03559 to A.S.) and the Nederlandse Organisatie voor Wetenschappelijk Onderzoek (Dutch Research Council) Foundation of the Netherlands Organization for Scientific Research (Women In Science Excel [WISE] fellowship to A.S.). A.-L.R. and E.S.J. thank Rika Anderson for helpful methodological discussions and Sean Sylva for assistance in shipboard geochemical analysis.
    Keywords: Metagenomics ; Deep-sea hydrothermal ; Thermophiles ; Archaea ; Volcanics
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    Diel transcriptional oscillations of light-sensitive regulatory elements in open-ocean eukaryotic plankton communities (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Coesel, S. N., Durham, B. P., Groussman, R. D., Hu, S. K., Caron, D. A., Morales, R. L., Ribalet, F., & Armbrust, E. V. Diel transcriptional oscillations of light-sensitive regulatory elements in open-ocean eukaryotic plankton communities. Proceedings of the National Academy of Sciences of the United States of America, 118(6), (2021): e2011038118, https://doi.org/10.1073./pnas.2011038118.
    Description: The 24-h cycle of light and darkness governs daily rhythms of complex behaviors across all domains of life. Intracellular photoreceptors sense specific wavelengths of light that can reset the internal circadian clock and/or elicit distinct phenotypic responses. In the surface ocean, microbial communities additionally modulate nonrhythmic changes in light quality and quantity as they are mixed to different depths. Here, we show that eukaryotic plankton in the North Pacific Subtropical Gyre transcribe genes encoding light-sensitive proteins that may serve as light-activated transcription factors, elicit light-driven electrical/chemical cascades, or initiate secondary messenger-signaling cascades. Overall, the protistan community relies on blue light-sensitive photoreceptors of the cryptochrome/photolyase family, and proteins containing the Light-Oxygen-Voltage (LOV) domain. The greatest diversification occurred within Haptophyta and photosynthetic stramenopiles where the LOV domain was combined with different DNA-binding domains and secondary signal-transduction motifs. Flagellated protists utilize green-light sensory rhodopsins and blue-light helmchromes, potentially underlying phototactic/photophobic and other behaviors toward specific wavelengths of light. Photoreceptors such as phytochromes appear to play minor roles in the North Pacific Subtropical Gyre. Transcript abundance of environmental light-sensitive protein-encoding genes that display diel patterns are found to primarily peak at dawn. The exceptions are the LOV-domain transcription factors with peaks in transcript abundances at different times and putative phototaxis photoreceptors transcribed throughout the day. Together, these data illustrate the diversity of light-sensitive proteins that may allow disparate groups of protists to respond to light and potentially synchronize patterns of growth, division, and mortality within the dynamic ocean environment.
    Description: This work was supported by a grant from the Simons Foundation (SCOPE Award 329108 [to E.V.A.]) and XSEDE Grant Allocation OCE160019 (to R.D.G.).
    Keywords: Photoreceptors ; Microbial eukaryotes ; Oligotrophic gyre ; Diel cycles ; Metatranscriptomics
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    Evidence for massive and recurrent toxic blooms of Alexandrium catenella in the Alaskan Arctic (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Anderson, D. M., Fachon, E., Pickart, R. S., Lin, P., Fischer, A. D., Richlen, M. L., Uva, V., Brosnahan, M. L., McRaven, L., Bahr, F., Lefebvre, K., Grebmeier, J. M., Danielson, S. L., Lyu, Y., & Fukai, Y. Evidence for massive and recurrent toxic blooms of Alexandrium catenella in the Alaskan Arctic. Proceedings of the National Academy of Sciences of the United States of America, 118(41) (2021): e2107387118, https://doi.org/10.1073/pnas.2107387118.
    Description: Among the organisms that spread into and flourish in Arctic waters with rising temperatures and sea ice loss are toxic algae, a group of harmful algal bloom species that produce potent biotoxins. Alexandrium catenella, a cyst-forming dinoflagellate that causes paralytic shellfish poisoning worldwide, has been a significant threat to human health in southeastern Alaska for centuries. It is known to be transported into Arctic regions in waters transiting northward through the Bering Strait, yet there is little recognition of this organism as a human health concern north of the Strait. Here, we describe an exceptionally large A. catenella benthic cyst bed and hydrographic conditions across the Chukchi Sea that support germination and development of recurrent, locally originating and self-seeding blooms. Two prominent cyst accumulation zones result from deposition promoted by weak circulation. Cyst concentrations are among the highest reported globally for this species, and the cyst bed is at least 6× larger in area than any other. These extraordinary accumulations are attributed to repeated inputs from advected southern blooms and to localized cyst formation and deposition. Over the past two decades, warming has likely increased the magnitude of the germination flux twofold and advanced the timing of cell inoculation into the euphotic zone by 20 d. Conditions are also now favorable for bloom development in surface waters. The region is poised to support annually recurrent A. catenella blooms that are massive in scale, posing a significant and worrisome threat to public and ecosystem health in Alaskan Arctic communities where economies are subsistence based.
    Description: Funding for D.M.A., R.S.P., E.F., P.L., A.D.F., V.U., M.L.B., L.M., F.B., and M.L.R. was provided by grants from the NSF Office of Polar Programs (Grants OPP-1823002 and OPP-1733564) and the National Ocanic and Atmospheric Administration (NOAA) Arctic Research program (through the Cooperative Institute for the North Atlantic Region [CINAR; Grants NA14OAR4320158 and NA19OAR4320074]), for J.M.G. through CINAR 22309.07 UMCES (University of Maryland Center for Environmental Science), and for D.M.A. and K.L. through NOAA’s Center for Coastal and Ocean Studies Ecology and Oceanography of Harmful Algal Blooms (ECOHAB) Program (NA20NOS4780195). Funding for D.M.A., M.L.R., M.L.B., E.F., V.U., and A.D.F. was also provided by NSF (Grant OCE-1840381) and NIH (Grant 1P01-ES028938-01) through the Woods Hole Center for Oceans and Human Health. S.L.D. was supported by North Pacific Research Board IERP Grants A91-99a and A91-00a. This is IERP publication ArcticIERP-41 and ECOHAB Contribution No. ECO983.
    Keywords: Harmful algal bloom ; HAB ; Alexandrium ; Alaskan Arctic ; Climate
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  • 19
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    Unifying chemical and biological perspectives of carbon accumulation in the environment (2021)
    National Academy of Sciences
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    Publication Date: 2022-05-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Repeta, D. J. Unifying chemical and biological perspectives of carbon accumulation in the environment. Proceedings of the National Academy of Sciences of the United States of America, 118(11), (2021); e2100935118, https://doi.org/10.1073/pnas.2100935118.
    Description: Heterotrophic microorganisms are fiendishly clever at degrading all shapes and sizes of organic compounds to extract the energy they need to build biomass. Every year marine phytoplankton fix ∼50 billion tons of carbon dioxide into organic matter, and every year marine heterotrophs respire nearly all of this organic matter back to carbon dioxide (1). Nearly all, but not all. With each spin of this carbon cycle, a small amount of organic matter escapes respiration and becomes sequestered in seawater, sediments, and soils. Over time, this small “leak” in the system leads to the accumulation of a vast reservoir of carbon; some 5 × 1019 kg of organic matter are thought to be sequestered in sedimentary rocks (2). This carbon sequestration has immense consequences for life on Earth, as illustrated by the change in climate we are now experiencing due in part to the transfer of a minute portion of this inventory from geologic reservoirs into the atmosphere.
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  • 20
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    Origin of interannual variability in global mean sea level (2020)
    National Academy of Sciences
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    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2020. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 117(25), (2020): 13983-13990, doi: 10.1073/pnas.1922190117.
    Description: The two dominant drivers of the global mean sea level (GMSL) variability at interannual timescales are steric changes due to changes in ocean heat content and barystatic changes due to the exchange of water mass between land and ocean. With Gravity Recovery and Climate Experiment (GRACE) satellites and Argo profiling floats, it has been possible to measure the relative steric and barystatic contributions to GMSL since 2004. While efforts to “close the GMSL budget” with satellite altimetry and other observing systems have been largely successful with regards to trends, the short time period covered by these records prohibits a full understanding of the drivers of interannual to decadal variability in GMSL. One particular area of focus is the link between variations in the El Niño−Southern Oscillation (ENSO) and GMSL. Recent literature disagrees on the relative importance of steric and barystatic contributions to interannual to decadal variability in GMSL. Here, we use a multivariate data analysis technique to estimate variability in barystatic and steric contributions to GMSL back to 1982. These independent estimates explain most of the observed interannual variability in satellite altimeter-measured GMSL. Both processes, which are highly correlated with ENSO variations, contribute about equally to observed interannual GMSL variability. A theoretical scaling analysis corroborates the observational results. The improved understanding of the origins of interannual variability in GMSL has important implications for our understanding of long-term trends in sea level, the hydrological cycle, and the planet’s radiation imbalance.
    Description: The research was carried out at JPL, California Institute of Technology, under a contract with NASA. This study was funded by NASA Grants NNX17AH35G (Ocean Surface Topography Science Team), 80NSSC17K0564, and 80NSSC17K0565 (NASA Sea Level Change Team). The efforts of J.T.F. in this work were also supported by NSF Award AGS-1419571, and by the Regional and Global Model Analysis component of the Earth and Environmental System Modeling Program of the US Department of Energy's Office of Biological & Environmental Research via National Science Foundation Grant IA 1844590. C.G.P. was supported by the J. Lamar Worzel Assistant Scientist Fund and the Penzance Endowed Fund in Support of Assistant Scientists at the Woods Hole Oceanographic Institution.
    Description: 2020-12-08
    Keywords: Sea level ; Climate variability ; Global mean sea level ; Satellite altimetry
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  • 21
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    Identification of chondritic krypton and xenon in Yellowstone gases and the timing of terrestrial volatile accretion (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), [year]. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Broadley, M. W., Barry, P. H., Bekaert, D. V., Byrne, D. J., Caracausi, A., Ballentine, C. J., & Marty, B. Identification of chondritic krypton and xenon in Yellowstone gases and the timing of terrestrial volatile accretion. Proceedings of the National Academy of Sciences of the United States of America, 117 (25), (2020): 13997-14004, doi: 10.1073/pnas.2003907117.
    Description: Identifying the origin of noble gases in Earth’s mantle can provide crucial constraints on the source and timing of volatile (C, N, H2O, noble gases, etc.) delivery to Earth. It remains unclear whether the early Earth was able to directly capture and retain volatiles throughout accretion or whether it accreted anhydrously and subsequently acquired volatiles through later additions of chondritic material. Here, we report high-precision noble gas isotopic data from volcanic gases emanating from, in and around, the Yellowstone caldera (Wyoming, United States). We show that the He and Ne isotopic and elemental signatures of the Yellowstone gas requires an input from an undegassed mantle plume. Coupled with the distinct ratio of 129Xe to primordial Xe isotopes in Yellowstone compared with mid-ocean ridge basalt (MORB) samples, this confirms that the deep plume and shallow MORB mantles have remained distinct from one another for the majority of Earth’s history. Krypton and xenon isotopes in the Yellowstone mantle plume are found to be chondritic in origin, similar to the MORB source mantle. This is in contrast with the origin of neon in the mantle, which exhibits an isotopic dichotomy between solar plume and chondritic MORB mantle sources. The co-occurrence of solar and chondritic noble gases in the deep mantle is thought to reflect the heterogeneous nature of Earth’s volatile accretion during the lifetime of the protosolar nebula. It notably implies that the Earth was able to retain its chondritic volatiles since its earliest stages of accretion, and not only through late additions.
    Description: Samples were collected as part of Study YELL-08056: Xenon Anomalies in the Yellowstone Hotspot. We thank Annie Carlson and all of the rangers at the Yellowstone National Park for providing invaluable advice and help when collecting the samples. M.W.B., D.V.B., D.J.B., and B.M. were supported by the European Research Council (PHOTONIS Project Grant 695618). This work was partially supported by Grants G-2016-7206 and G-2017-9696 from the Alfred P. Sloan Foundation and the Deep Carbon Observatory (to P.H.B.) and UK National Environment Research Council Deep Volatile Grant NE/M000427/1 (to C.J.B.). We also thank Laurent Zimmerman for providing help with the analysis. Finally, we thank the editor for efficient handling of our manuscript and the two anonymous reviewers for their insightful comments. This is CRPG contribution 2998.
    Keywords: Origin of Earth’s volatiles ; Accretion ; Mantle plume ; Noble gases ; Yellowstone
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    Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Sutherland, K. M., Wankel, S. D., & Hansel, C. M. Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen. Proceedings of the National Academy of Sciences of the United States of America, 117(7), (2020): 3433-3439, doi:10.1073/pnas.1912313117.
    Description: The balance between sources and sinks of molecular oxygen in the oceans has greatly impacted the composition of Earth’s atmosphere since the evolution of oxygenic photosynthesis, thereby exerting key influence on Earth’s climate and the redox state of (sub)surface Earth. The canonical source and sink terms of the marine oxygen budget include photosynthesis, respiration, photorespiration, the Mehler reaction, and other smaller terms. However, recent advances in understanding cryptic oxygen cycling, namely the ubiquitous one-electron reduction of O2 to superoxide by microorganisms outside the cell, remains unexplored as a potential player in global oxygen dynamics. Here we show that dark extracellular superoxide production by marine microbes represents a previously unconsidered global oxygen flux and sink comparable in magnitude to other key terms. We estimate that extracellular superoxide production represents a gross oxygen sink comprising about a third of marine gross oxygen production, and a net oxygen sink amounting to 15 to 50% of that. We further demonstrate that this total marine dark extracellular superoxide flux is consistent with concentrations of superoxide in marine environments. These findings underscore prolific marine sources of reactive oxygen species and a complex and dynamic oxygen cycle in which oxygen consumption and corresponding carbon oxidation are not necessarily confined to cell membranes or exclusively related to respiration. This revised model of the marine oxygen cycle will ultimately allow for greater reconciliation among estimates of primary production and respiration and a greater mechanistic understanding of redox cycling in the ocean.
    Description: This work was supported by NASA Earth and Space Science Fellowship NNX15AR62H to K.M.S., NASA Exobiology grant NNX15AM04G to S.D.W. and C.M.H., and NSF Division of Ocean Sciences grant 1355720 to C.M.H. This research was further supported in part by Hanse-Wissenschaftskolleg Institute of Advanced Study fellowships to C.M.H. and S.D.W. We thank Danielle Hicks for assistance with figures and Community Earth Systems Model (CESM) Large Ensemble Project for the availability and use of its data product. The CESM project is primarily supported by the NSF.
    Keywords: Microbial superoxide ; Reactive oxygen species ; Marine dissolved oxygen
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  • 23
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    Shared up-regulation and contrasting down-regulation of gene expression distinguish desiccation-tolerant from intolerant green algae (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-27
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Peredo, E. L., & Cardon, Z. G. Shared up-regulation and contrasting down-regulation of gene expression distinguish desiccation-tolerant from intolerant green algae. Proceedings of the National Academy of Sciences of the United States of America, 117(29), 1(2020): 7438-17445, doi:10.1073/pnas.1906904117.
    Description: Among green plants, desiccation tolerance is common in seeds and spores but rare in leaves and other vegetative green tissues. Over the last two decades, genes have been identified whose expression is induced by desiccation in diverse, desiccation-tolerant (DT) taxa, including, e.g., late embryogenesis abundant proteins (LEA) and reactive oxygen species scavengers. This up-regulation is observed in DT resurrection plants, mosses, and green algae most closely related to these Embryophytes. Here we test whether this same suite of protective genes is up-regulated during desiccation in even more distantly related DT green algae, and, importantly, whether that up-regulation is unique to DT algae or also occurs in a desiccation-intolerant relative. We used three closely related aquatic and desert-derived green microalgae in the family Scenedesmaceae and capitalized on extraordinary desiccation tolerance in two of the species, contrasting with desiccation intolerance in the third. We found that during desiccation, all three species increased expression of common protective genes. The feature distinguishing gene expression in DT algae, however, was extensive down-regulation of gene expression associated with diverse metabolic processes during the desiccation time course, suggesting a switch from active growth to energy-saving metabolism. This widespread downshift did not occur in the desiccation-intolerant taxon. These results show that desiccation-induced up-regulation of expression of protective genes may be necessary but is not sufficient to confer desiccation tolerance. The data also suggest that desiccation tolerance may require induced protective mechanisms operating in concert with massive down-regulation of gene expression controlling numerous other aspects of metabolism.
    Description: Dr. Louise Lewis (University of Connecticut) provided F. rotunda and A. deserticola. Suzanne Thomas and Jordan Stark provided expert technical assistance. This work was supported by the NSF, Division of Integrative Organismal Systems (1355085 to Z.G.C.), and an anonymous donor (to Z.G.C.).
    Keywords: Aquatic green algae ; Desert-evolved green algae ; Extremophiles ; Microbiotic ; Crusts ; Scenedesmaceae
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    Molecular profiling of single neurons of known identity in two ganglia from the crab Cancer borealis (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-31
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Northcutt, A. J., Kick, D. R., Otopalik, A. G., Goetz, B. M., Harris, R. M., Santin, J. M., Hofmann, H. A., Marder, E., & Schulz, D. J. Molecular profiling of single neurons of known identity in two ganglia from the crab Cancer borealis. Proceedings of the National Academy of Sciences of the United States of America, 116 (52) (2019): 26980-26990, doi: 10.1073/pnas.1911413116.
    Description: Understanding circuit organization depends on identification of cell types. Recent advances in transcriptional profiling methods have enabled classification of cell types by their gene expression. While exceptionally powerful and high throughput, the ground-truth validation of these methods is difficult: If cell type is unknown, how does one assess whether a given analysis accurately captures neuronal identity? To shed light on the capabilities and limitations of solely using transcriptional profiling for cell-type classification, we performed 2 forms of transcriptional profiling—RNA-seq and quantitative RT-PCR, in single, unambiguously identified neurons from 2 small crustacean neuronal networks: The stomatogastric and cardiac ganglia. We then combined our knowledge of cell type with unbiased clustering analyses and supervised machine learning to determine how accurately functionally defined neuron types can be classified by expression profile alone. The results demonstrate that expression profile is able to capture neuronal identity most accurately when combined with multimodal information that allows for post hoc grouping, so analysis can proceed from a supervised perspective. Solely unsupervised clustering can lead to misidentification and an inability to distinguish between 2 or more cell types. Therefore, this study supports the general utility of cell identification by transcriptional profiling, but adds a caution: It is difficult or impossible to know under what conditions transcriptional profiling alone is capable of assigning cell identity. Only by combining multiple modalities of information such as physiology, morphology, or innervation target can neuronal identity be unambiguously determined.
    Description: We thank members of the D.J.S., H.A.H., and E.M. laboratories for helpful discussions. We thank the Genomic Sequencing and Analysis Facility (The University of Texas [UT] at Austin) for library preparation and sequencing and the bioinformatics consulting team at the UT Austin Center for Computational Biology and Bioinformatics for helpful advice. This work was supported by National Institutes of Health grant R01MH046742-29 (to E.M. and D.J.S.) and the National Institute of General Medical Sciences T32GM008396 (support for A.J.N.) and National Institute of Mental Health grant 5R25MH059472-18 and the Grass Foundation (support for Neural Systems and Behavior Course at the Marine Biological Laboratory).
    Keywords: qPCR ; RNA-seq ; Stomatogastric ; Expression profiling
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    Global variability in seawater Mg:Ca and Sr:Ca ratios in the modern ocean (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Lebrato, M., Garbe-Schönberg, D., Müller, M. N., Blanco-Ameijeiras, S., Feely, R. A., Lorenzoni, L., Molinero, J. C., Bremer, K., Jones, D. O. B., Iglesias-Rodriguez, D., Greeley, D., Lamare, M. D., Paulmier, A., Graco, M., Cartes, J., Barcelos E Ramos, J., de Lara, A., Sanchez-Leal, R., Jimenez, P., Paparazzo, F. E., Hartman, S. E., Westernströer, U., Küter, M., Benavides, R., da Silva, A. F., Bell, S., Payne, C., Olafsdottir, S., Robinson, K., Jantunen, L. M., Korablev, A., Webster, R. J., Jones, E. M., Gilg, O., Bailly du Bois, P., Beldowski, J., Ashjian, C., Yahia, N. D., Twining, B., Chen, X. G., Tseng, L. C., Hwang, J. S., Dahms, H. U., & Oschlies, A. Global variability in seawater Mg:Ca and Sr:Ca ratios in the modern ocean. Proceedings of the National Academy of Sciences of the United States of America, 117(36), (2020): 22281-22292, doi:10.1073/pnas.1918943117.
    Description: Seawater Mg:Ca and Sr:Ca ratios are biogeochemical parameters reflecting the Earth–ocean–atmosphere dynamic exchange of elements. The ratios’ dependence on the environment and organisms' biology facilitates their application in marine sciences. Here, we present a measured single-laboratory dataset, combined with previous data, to test the assumption of limited seawater Mg:Ca and Sr:Ca variability across marine environments globally. High variability was found in open-ocean upwelling and polar regions, shelves/neritic and river-influenced areas, where seawater Mg:Ca and Sr:Ca ratios range from ∼4.40 to 6.40 mmol:mol and ∼6.95 to 9.80 mmol:mol, respectively. Open-ocean seawater Mg:Ca is semiconservative (∼4.90 to 5.30 mol:mol), while Sr:Ca is more variable and nonconservative (∼7.70 to 8.80 mmol:mol); both ratios are nonconservative in coastal seas. Further, the Ca, Mg, and Sr elemental fluxes are connected to large total alkalinity deviations from International Association for the Physical Sciences of the Oceans (IAPSO) standard values. Because there is significant modern seawater Mg:Ca and Sr:Ca ratios variability across marine environments we cannot absolutely assume that fossil archives using taxa-specific proxies reflect true global seawater chemistry but rather taxa- and process-specific ecosystem variations, reflecting regional conditions. This variability could reconcile secular seawater Mg:Ca and Sr:Ca ratio reconstructions using different taxa and techniques by assuming an error of 1 to 1.50 mol:mol, and 1 to 1.90 mmol:mol, respectively. The modern ratios’ variability is similar to the reconstructed rise over 20 Ma (Neogene Period), nurturing the question of seminonconservative behavior of Ca, Mg, and Sr over modern Earth geological history with an overlooked environmental effect.
    Description: We thank the researchers, staff, students, and volunteers in all the expeditions around the world for their contributions. One anonymous referee and Bernhard Peucker-Ehenbrink, Woods Hole Oceanographic Institution, contributed significantly to the final version of the manuscript. This study was developed under a grant from the Federal Ministry of Education and Research to D.G.-S. under contract 03F0722A, by the Kiel Cluster of Excellence “The Future Ocean” (D1067/87) to A.O. and M.L., and by the “European project on Ocean Acidification” (European Community’s Seventh Framework Programme FP7/2007-2013, grant agreement 211384) to A.O. and M.L. Additional funding was provided from project DOSMARES CTM2010-21810-C03-02, by the UK Natural Environment Research Council, to the National Oceanography Centre. This is Pacific Marine Environmental Laboratory contribution number 5046.
    Keywords: global ; seawater ; Mg:Ca ; Sr:Ca ; biogeochemistry
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    Hydrocarbon seepage in the deep seabed links subsurface and seafloor biospheres (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-27
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Chakraborty, A., Ruff, S. E., Dong, X., Ellefson, E. D., Li, C., Brooks, J. M., McBee, J., Bernard, B. B., & Hubert, C. R. J. Hydrocarbon seepage in the deep seabed links subsurface and seafloor biospheres. Proceedings of the National Academy of Sciences of the United States of America, 117(20), (2020): 11029-11037, doi: 10.1073/pnas.2002289117.
    Description: Marine cold seeps transmit fluids between the subseafloor and seafloor biospheres through upward migration of hydrocarbons that originate in deep sediment layers. It remains unclear how geofluids influence the composition of the seabed microbiome and if they transport deep subsurface life up to the surface. Here we analyzed 172 marine surficial sediments from the deep-water Eastern Gulf of Mexico to assess whether hydrocarbon fluid migration is a mechanism for upward microbial dispersal. While 132 of these sediments contained migrated liquid hydrocarbons, evidence of continuous advective transport of thermogenic alkane gases was observed in 11 sediments. Gas seeps harbored distinct microbial communities featuring bacteria and archaea that are well-known inhabitants of deep biosphere sediments. Specifically, 25 distinct sequence variants within the uncultivated bacterial phyla Atribacteria and Aminicenantes and the archaeal order Thermoprofundales occurred in significantly greater relative sequence abundance along with well-known seep-colonizing members of the bacterial genus Sulfurovum, in the gas-positive sediments. Metabolic predictions guided by metagenome-assembled genomes suggested these organisms are anaerobic heterotrophs capable of nonrespiratory breakdown of organic matter, likely enabling them to inhabit energy-limited deep subseafloor ecosystems. These results point to petroleum geofluids as a vector for the advection-assisted upward dispersal of deep biosphere microbes from subsurface to surface environments, shaping the microbiome of cold seep sediments and providing a general mechanism for the maintenance of microbial diversity in the deep sea.
    Description: We wish to thank Jody Sandel as well as the crew of R/V GeoExplorer for collection of piston cores, onboard core processing, sample preservation, and shipment. Cynthia Kwan and Oliver Horanszky are thanked for assistance with amplicon library preparation. We also wish to thank Jayne Rattray, Daniel Gittins, and Marc Strous for valuable discussions and suggestions, and Rhonda Clark for research support. Collaborations with Andy Mort from the Geological Survey of Canada, and Richard Hatton from Geoscience Wales are also gratefully acknowledged. This work was financially supported by a Mitacs Elevate Postdoctoral Fellowship awarded to A.C.; an Alberta Innovates-Technology Futures/Eyes High Postdoctoral Fellowship to S.E.R.; and a Natural Sciences and Engineering Research Council Strategic Project Grant, a Genome Canada Genomics Applications Partnership Program grant, a Canada Foundation for Innovation grant (CFI-JELF 33752) for instrumentation, and Campus Alberta Innovates Program Chair funding to C.R.J.H.
    Keywords: Deep biosphere ; Microbiome ; Dispersal
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    A demographic and evolutionary analysis of maternal effect senescence (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-27
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in MBL Hernandez, C. M., van Daalen, S. F., Caswell, H., Neubert, M. G., & Gribble, K. E. A demographic and evolutionary analysis of maternal effect senescence. Proceedings of the National Academy of Sciences of the United States of America, 17(28), (2020):16431-16437, doi: 10.1073/pnas.1919988117.
    Description: Maternal effect senescence—a decline in offspring survival or fertility with maternal age—has been demonstrated in many taxa, including humans. Despite decades of phenotypic studies, questions remain about how maternal effect senescence impacts evolutionary fitness. To understand the influence of maternal effect senescence on population dynamics, fitness, and selection, we developed matrix population models in which individuals are jointly classified by age and maternal age. We fit these models to data from individual-based culture experiments on the aquatic invertebrate, Brachionus manjavacas (Rotifera). By comparing models with and without maternal effects, we found that maternal effect senescence significantly reduces fitness for B. manjavacas and that this decrease arises primarily through reduced fertility, particularly at maternal ages corresponding to peak reproductive output. We also used the models to estimate selection gradients, which measure the strength of selection, in both high growth rate (laboratory) and two simulated low growth rate environments. In all environments, selection gradients on survival and fertility decrease with increasing age. They also decrease with increasing maternal age for late maternal ages, implying that maternal effect senescence can evolve through the same process as in Hamilton’s theory of the evolution of age-related senescence. The models we developed are widely applicable to evaluate the fitness consequences of maternal effect senescence across species with diverse aging and fertility schedule phenotypes.
    Description: K.E.G. was supported by Grant 5K01AG049049 from the National Institute on Aging and by the Bay and Paul Foundations. H.C. and S.F.v.D. were supported by the European Research Council through Advanced Grants 322829 and 788195 and by the Dutch Research Council through Grant ALWOP.2015.100. C.M.H. was supported by a National Science Foundation Graduate Research Fellowship. M.G.N. received funding from The Paul MacDonald Fye Chair for Excellence in Oceanography at the Woods Hole Oceanographic Institution.
    Keywords: Aging ; Demography ; Fitness ; Maternal effects ; Selection gradients
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    Dynamics and functional diversity of the smallest phytoplankton on the Northeast US shelf (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2020. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 117(22), (2020): 12215-12221, doi: 10.1073/pnas.1918439117.
    Description: Picophytoplankton are the most abundant primary producers in the ocean. Knowledge of their community dynamics is key to understanding their role in marine food webs and global biogeochemical cycles. To this end, we analyzed a 16-y time series of observations of a phytoplankton community at a nearshore site on the Northeast US Shelf. We used a size-structured population model to estimate in situ division rates for the picoeukaryote assemblage and compared the dynamics with those of the picocyanobacteria Synechococcus at the same location. We found that the picoeukaryotes divide at roughly twice the rate of the more abundant Synechococcus and are subject to greater loss rates (likely from viral lysis and zooplankton grazing). We describe the dynamics of these groups across short and long timescales and conclude that, despite their taxonomic differences, their populations respond similarly to changes in the biotic and abiotic environment. Both groups appear to be temperature limited in the spring and light limited in the fall and to experience greater mortality during the day than at night. Compared with Synechococcus, the picoeukaryotes are subject to greater top-down control and contribute more to the region’s primary productivity than their standing stocks suggest.
    Description: We thank E. T. Crockford, E. E. Peacock, J. Fredericks, Z. Sandwith, the MVCO Operations Team, and divers of the Woods Hole Oceanographic Institution diving program. This work was supported by NSF Grants OCE-0119915 (to R.J.O. and H.M.S.) and OCE-1655686 (to M.G.N., R.J.O., A.R.S., and H.M.O.); NASA Grants NNX11AF07G (to H.M.S.) and NNX13AC98G (to H.M.S.); Gordon and Betty Moore Foundation Grant GGA#934 (to H.M.S.); and Simons Foundation Grant 561126 (to H.M.S.).
    Description: 2020-11-15
    Keywords: Picoeukaryotes ; Flow cytometry ; Matrix model ; Primary productivity
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    Abiotic redox reactions in hydrothermal mixing zones: decreased energy availability for the subsurface biosphere (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 202. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in McDermott, J. M., Sylva, S. P., Ono, S., German, C. R., & Seewald, J. S. Abiotic redox reactions in hydrothermal mixing zones: decreased energy availability for the subsurface biosphere. Proceedings of the National Academy of Sciences of the United States of America, 117(34), (2020): 20453-20461, doi:10.1073/pnas.2003108117.
    Description: Subseafloor mixing of high-temperature hot-spring fluids with cold seawater creates intermediate-temperature diffuse fluids that are replete with potential chemical energy. This energy can be harnessed by a chemosynthetic biosphere that permeates hydrothermal regions on Earth. Shifts in the abundance of redox-reactive species in diffuse fluids are often interpreted to reflect the direct influence of subseafloor microbial activity on fluid geochemical budgets. Here, we examine hydrothermal fluids venting at 44 to 149 °C at the Piccard hydrothermal field that span the canonical 122 °C limit to life, and thus provide a rare opportunity to study the transition between habitable and uninhabitable environments. In contrast with previous studies, we show that hydrocarbons are contributed by biomass pyrolysis, while abiotic sulfate (SO42−) reduction produces large depletions in H2. The latter process consumes energy that could otherwise support key metabolic strategies employed by the subseafloor biosphere. Available Gibbs free energy is reduced by 71 to 86% across the habitable temperature range for both hydrogenotrophic SO42− reduction to hydrogen sulfide (H2S) and carbon dioxide (CO2) reduction to methane (CH4). The abiotic H2 sink we identify has implications for the productivity of subseafloor microbial ecosystems and is an important process to consider within models of H2 production and consumption in young oceanic crust.
    Description: Financial support was provided by the National Aeronautics and Space Administration (NASA) Astrobiology program (Awards NNX09AB75G and 80NSSC19K1427 to C.R.G. and J.S.S.) and the NSF (Award OCE-1061863 to C.R.G. and J.S.S.). Ship and vehicle time for cruise FK008 was provided by the Schmidt Ocean Institute. We thank the ROV Jason II and HROV Nereus groups, and the captain, officers, and crew of R/V Atlantis (AT18-16) and R/V Falkor (FK008) for their dedication to skillful operations at sea. We thank our scientific colleagues from both cruises, as well as Meg Tivey, Frieder Klein, and Scott Wankel for insightful discussions. We are grateful to the editor and two anonymous reviewers for providing helpful comments and suggestions.
    Keywords: Hydrothermal vent ; Subsurface biosphere ; Bioenergetics ; Biogeochemistry
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    Aseismic transient slip on the Gofar transform fault, East Pacific Rise (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2020. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences (2020): 201913625, doi: 10.1073/pnas.1913625117.
    Description: Oceanic transform faults display a unique combination of seismic and aseismic slip behavior, including a large globally averaged seismic deficit, and the local occurrence of repeating magnitude (M) ∼6 earthquakes with abundant foreshocks and seismic swarms, as on the Gofar transform of the East Pacific Rise and the Blanco Ridge in the northeast Pacific Ocean. However, the underlying mechanisms that govern the partitioning between seismic and aseismic slip and their interaction remain unclear. Here we present a numerical modeling study of earthquake sequences and aseismic transient slip on oceanic transform faults. In the model, strong dilatancy strengthening, supported by seismic imaging that indicates enhanced fluid-filled porosity and possible hydrothermal circulation down to the brittle–ductile transition, effectively stabilizes along-strike seismic rupture propagation and results in rupture barriers where aseismic transients arise episodically. The modeled slow slip migrates along the barrier zones at speeds ∼10 to 600 m/h, spatiotemporally correlated with the observed migration of seismic swarms on the Gofar transform. Our model thus suggests the possible prevalence of episodic aseismic transients in M ∼6 rupture barrier zones that host active swarms on oceanic transform faults and provides candidates for future seafloor geodesy experiments to verify the relation between aseismic fault slip, earthquake swarms, and fault zone hydromechanical properties.
    Description: We thank Joan Gomberg, Ruth Harris, Steve Hickman, Shane Detweiler, Mike Diggles, and two anonymous external reviewers for their thoughtful comments that helped to improve the manuscript. This study was supported by Natural Sciences and Engineering Research Council of Canada Discovery Grants RGPIN/418338-2012 and RGPIN-2018-05389; and NSF Grants OCE-10-61203 and OCE-18-33279.
    Description: 2020-10-28
    Keywords: Oceanic transform faults ; Earthquake rupture segmentation ; Aseismic transients ; Seismic swarms
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    Metrics that matter for assessing the ocean biological carbon pump (2020)
    National Academy of Sciences
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    Publication Date: 2022-10-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Buesseler, K. O., Boyd, P. W., Black, E. E., & Siegel, D. A. Metrics that matter for assessing the ocean biological carbon pump. Proceedings of the National Academy of Sciences of the United States of America, (2020): 201918114, doi: 10.1073/pnas.1918114117.
    Description: The biological carbon pump (BCP) comprises wide-ranging processes that set carbon supply, consumption, and storage in the oceans’ interior. It is becoming increasingly evident that small changes in the efficiency of the BCP can significantly alter ocean carbon sequestration and, thus, atmospheric CO2 and climate, as well as the functioning of midwater ecosystems. Earth system models, including those used by the United Nation’s Intergovernmental Panel on Climate Change, most often assess POC (particulate organic carbon) flux into the ocean interior at a fixed reference depth. The extrapolation of these fluxes to other depths, which defines the BCP efficiencies, is often executed using an idealized and empirically based flux-vs.-depth relationship, often referred to as the “Martin curve.” We use a new compilation of POC fluxes in the upper ocean to reveal very different patterns in BCP efficiencies depending upon whether the fluxes are assessed at a fixed reference depth or relative to the depth of the sunlit euphotic zone (Ez). We find that the fixed-depth approach underestimates BCP efficiencies when the Ez is shallow, and vice versa. This adjustment alters regional assessments of BCP efficiencies as well as global carbon budgets and the interpretation of prior BCP studies. With several international studies recently underway to study the ocean BCP, there are new and unique opportunities to improve our understanding of the mechanistic controls on BCP efficiencies. However, we will only be able to compare results between studies if we use a common set of Ez-based metrics.
    Description: We thank the many scientists whose ideas and contributions over the years are the foundation of this paper. This includes A. Martin, who led the organization of the BIARRITZ group (now JETZON) workshop in July 2019, discussions at which helped to motivate this article. We thank D. Karl for pointing us in the right direction for this paper format at PNAS and two thoughtful reviewers who through their comments helped to improve this manuscript. Support for writing this piece is acknowledged from several sources, including the Woods Hole Oceanographic Institution’s Ocean Twilight Zone project (K.O.B.); NASA as part of the EXport Processes in the global Ocean from RemoTe Sensing (EXPORTS) program (K.O.B. and D.A.S.). E.E.B. was supported by a postdoctoral fellowship through the Ocean Frontier Institute at Dalhousie University. P.W.B. was supported by the Australian Research Council through a Laureate (FL160100131).
    Keywords: Biological carbon pump ; Twilight zone ; Particle flux
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    Opinion: we need better data about the environmental persistence of plastic goods (2020)
    National Academy of Sciences
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    Publication Date: 2022-05-26
    Description: Author Posting. © National Academy of Sciences, 2020. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 117(26), (2020): 14618-14621, doi:10.1073/pnas.2008009117.
    Description: Plastic pollution is one of the most visible and complex environmental issues today. Interested and concerned parties include researchers, governmental agencies, nongovernmental organizations, industry, media, and the general public. One key assumption behind the issue and the public outcry is that plastics last indefinitely in the environment, resulting in chronic exposure that harms animals and humans. But the data supporting this assumption are scant.
    Description: We thank Briana Prado, Cassia Armstrong, and Anna Walsh for their help with the review, Kenneth Kostel, Katie Linehan, Daniel Ward, and Rose Cory for feedback on an earlier version of this piece, John Furfey for assistance with tracking down the original sources of the environmental lifetime estimates, and Natalie Reiner for help with Fig. 1. We acknowledge financial support from Woods Hole Oceanographic Institution (Woods Hole, MA) and the Seaver Institute (Los Angeles, CA).
    Description: 2020-12-10
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    Peptidoglycan hydrolase of an unusual cross-link cleavage specificity contributes to bacterial cell wall synthesis (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-02
    Description: Bacteria are surrounded by a protective exoskeleton, peptidoglycan (PG), a cross-linked mesh-like macromolecule consisting of glycan strands interlinked by short peptides. Because PG completely encases the cytoplasmic membrane, cleavage of peptide cross-links is a prerequisite to make space for incorporation of nascent glycan strands for its successful expansion during cell growth. In most bacteria, the peptides consist of l-alanine, d-glutamate, meso-diaminopimelic acid (mDAP) and d-alanine (d-Ala) with cross-links occurring either between d-Ala and mDAP or two mDAP residues. In Escherichia coli, the d-Ala−mDAP cross-links whose cleavage by specialized endopeptidases is crucial for expansion of PG predominate. However, a small proportion of mDAP−mDAP cross-links also exist, yet their role in the context of PG expansion or the hydrolase(s) capable of catalyzing their cleavage is not known. Here, we identified an ORF of unknown function, YcbK (renamed MepK), as an mDAP−mDAP cross-link cleaving endopeptidase working in conjunction with other elongation-specific endopeptidases to make space for efficient incorporation of nascent PG strands into the sacculus. E. coli mutants lacking mepK and another d-Ala−mDAP–specific endopeptidase (mepS) were synthetic sick, and the defects were abrogated by lack of l,d-transpeptidases, enzymes catalyzing the formation of mDAP cross-links. Purified MepK was able to cleave the mDAP cross-links of soluble muropeptides and of intact PG sacculi. Overall, this study describes a PG hydrolytic enzyme with a hitherto unknown substrate specificity that contributes to expansion of the PG sacculus, emphasizing the fundamental importance of cross-link cleavage in bacterial peptidoglycan synthesis.
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    Shockley–Queisser triangle predicts the thermodynamic efficiency limits of arbitrarily complex multijunction bifacial solar cells (2019)
    National Academy of Sciences
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    Publication Date: 2019-11-12
    Description: As monofacial, single-junction solar cells approach their fundamental limits, there has been significant interest in tandem solar cells in the presence of concentrated sunlight or tandem bifacial solar cells with back-reflected albedo. The bandgap sequence and thermodynamic efficiency limits of these complex cell configurations require sophisticated numerical calculation. Therefore, the analyses of specialized cases are scattered throughout the literature. In this paper, we show that a powerful graphical approach called the normalized “Shockley–Queisser (S-Q) triangle” (i.e., imp=1−vmp) is sufficient to calculate the bandgap sequence and efficiency limits of arbitrarily complex photovoltaic (PV) topologies. The results are validated against a wide variety of specialized cases reported in the literature and are accurate within a few percent. We anticipate that the widespread use of the S-Q triangle will illuminate the deeper physical principles and design trade-offs involved in the design of bifacial tandem solar cells under arbitrary concentration and series resistance.
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    Insulin signaling in the hippocampus and amygdala regulates metabolism and neurobehavior (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-14
    Description: Previous studies have shown that insulin and IGF-1 signaling in the brain, especially the hypothalamus, is important for regulation of systemic metabolism. Here, we develop mice in which we have specifically inactivated both insulin receptors (IRs) and IGF-1 receptors (IGF1Rs) in the hippocampus (Hippo-DKO) or central amygdala (CeA-DKO) by stereotaxic delivery of AAV-Cre into IRlox/lox/IGF1Rlox/loxmice. Consequently, both Hippo-DKO and CeA-DKO mice have decreased levels of the GluA1 subunit of glutamate AMPA receptor and display increased anxiety-like behavior, impaired cognition, and metabolic abnormalities, including glucose intolerance. Hippo-DKO mice also display abnormal spatial learning and memory whereas CeA-DKO mice have impaired cold-induced thermogenesis. Thus, insulin/IGF-1 signaling has common roles in the hippocampus and central amygdala, affecting synaptic function, systemic glucose homeostasis, behavior, and cognition. In addition, in the hippocampus, insulin/IGF-1 signaling is important for spatial learning and memory whereas insulin/IGF-1 signaling in the central amygdala controls thermogenesis via regulation of neural circuits innervating interscapular brown adipose tissue.
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    A fully resolved backbone phylogeny reveals numerous dispersals and explosive diversifications throughout the history of Asteraceae (2019)
    National Academy of Sciences
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    Publication Date: 2019-06-17
    Description: The sunflower family, Asteraceae, comprises 10% of all flowering plant species and displays an incredible diversity of form. Asteraceae are clearly monophyletic, yet resolving phylogenetic relationships within the family has proven difficult, hindering our ability to understand its origin and diversification. Recent molecular clock dating has suggested a Cretaceous origin, but the lack of deep sampling of many genes and representative taxa from across the family has impeded the resolution of migration routes and diversifications that led to its global distribution and tremendous diversity. Here we use genomic data from 256 terminals to estimate evolutionary relationships, timing of diversification(s), and biogeographic patterns. Our study places the origin of Asteraceae at ∼83 MYA in the late Cretaceous and reveals that the family underwent a series of explosive radiations during the Eocene which were accompanied by accelerations in diversification rates. The lineages that gave rise to nearly 95% of extant species originated and began diversifying during the middle Eocene, coincident with the ensuing marked cooling during this period. Phylogenetic and biogeographic analyses support a South American origin of the family with subsequent dispersals into North America and then to Asia and Africa, later followed by multiple worldwide dispersals in many directions. The rapid mid-Eocene diversification is aligned with the biogeographic range shift to Africa where many of the modern-day tribes appear to have originated. Our robust phylogeny provides a framework for future studies aimed at understanding the role of the macroevolutionary patterns and processes that generated the enormous species diversity of Asteraceae.
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    Science, health, and cultural literacy in a rapidly changing communications landscape (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-15
    Description: There is a gap between how many scientists communicate and how most people understand and interpret messages. This article argues that the extensive science communications literature needs to be joined by the health literacy literature and anthropological work on cultural variations in hearing and understanding messages. Rapid changes and differences in how people in the United States get information are also discussed. Better understanding of how people get and perceive messages, and how access to information and to health services affects their behavior, should be an iterative and interdisciplinary effort. Community involvement in developing communication strategies is strongly encouraged.
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    A functional enrichment test for molecular convergent evolution finds a clear protein-coding signal in echolocating bats and whales (2019)
    National Academy of Sciences
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    Publication Date: 2019-09-30
    Description: Distantly related species entering similar biological niches often adapt by evolving similar morphological and physiological characters. How much genomic molecular convergence (particularly of highly constrained coding sequence) contributes to convergent phenotypic evolution, such as echolocation in bats and whales, is a long-standing fundamental question. Like others, we find that convergent amino acid substitutions are not more abundant in echolocating mammals compared to their outgroups. However, we also ask a more informative question about the genomic distribution of convergent substitutions by devising a test to determine which, if any, of more than 4,000 tissue-affecting gene sets is most statistically enriched with convergent substitutions. We find that the gene set most overrepresented (q-value = 2.2e-3) with convergent substitutions in echolocators, affecting 18 genes, regulates development of the cochlear ganglion, a structure with empirically supported relevance to echolocation. Conversely, when comparing to nonecholocating outgroups, no significant gene set enrichment exists. For aquatic and high-altitude mammals, our analysis highlights 15 and 16 genes from the gene sets most affected by molecular convergence which regulate skin and lung physiology, respectively. Importantly, our test requires that the most convergence-enriched set cannot also be enriched for divergent substitutions, such as in the pattern produced by inactivated vision genes in subterranean mammals. Showing a clear role for adaptive protein-coding molecular convergence, we discover nearly 2,600 convergent positions, highlight 77 of them in 3 organs, and provide code to investigate other clades across the tree of life.
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    Tubulin lattice in cilia is in a stressed form regulated by microtubule inner proteins (2019)
    National Academy of Sciences
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    Publication Date: 2019-09-16
    Description: Cilia, the hair-like protrusions that beat at high frequencies to propel a cell or move fluid around are composed of radially bundled doublet microtubules. In this study, we present a near-atomic resolution map of the Tetrahymena doublet microtubule by cryoelectron microscopy. The map demonstrates that the network of microtubule inner proteins weaves into the tubulin lattice and forms an inner sheath. From mass spectrometry data and de novo modeling, we identified Rib43a proteins as the filamentous microtubule inner proteins in the protofilament ribbon region. The Rib43a–tubulin interaction leads to an elongated tubulin dimer distance every 2 dimers. In addition, the tubulin lattice structure with missing microtubule inner proteins (MIPs) by sarkosyl treatment shows significant longitudinal compaction and lateral angle change between protofilaments. These results are evidence that the MIPs directly affect and stabilize the tubulin lattice. It suggests that the doublet microtubule is an intrinsically stressed filament and that this stress could be manipulated in the regulation of ciliary waveforms.
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    Interspecies analysis of MYC targets identifies tRNA synthetases as mediators of growth and survival in MYC-overexpressing cells (2019)
    National Academy of Sciences
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    Publication Date: 2019-07-01
    Description: Aberrant MYC oncogene activation is one of the most prevalent characteristics of cancer. By overlapping datasets of Drosophila genes that are insulin-responsive and also regulate nucleolus size, we enriched for Myc target genes required for cellular biosynthesis. Among these, we identified the aminoacyl tRNA synthetases (aaRSs) as essential mediators of Myc growth control in Drosophila and found that their pharmacologic inhibition is sufficient to kill MYC-overexpressing human cells, indicating that aaRS inhibitors might be used to selectively target MYC-driven cancers. We suggest a general principle in which oncogenic increases in cellular biosynthesis sensitize cells to disruption of protein homeostasis.
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    Optimizing organic electrosynthesis through controlled voltage dosing and artificial intelligence (2019)
    National Academy of Sciences
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    Publication Date: 2019-08-21
    Description: Organic electrosynthesis can transform the chemical industry by introducing electricity-driven processes that are more energy efficient and that can be easily integrated with renewable energy sources. However, their deployment is severely hindered by the difficulties of controlling selectivity and achieving a large energy conversion efficiency at high current density due to the low solubility of organic reactants in practical electrolytes. This control can be improved by carefully balancing the mass transport processes and electrocatalytic reaction rates at the electrode diffusion layer through pulsed electrochemical methods. In this study, we explore these methods in the context of the electrosynthesis of adiponitrile (ADN), the largest organic electrochemical process in industry. Systematically exploring voltage pulses in the timescale between 5 and 150 ms led to a 20% increase in production of ADN and a 250% increase in relative selectivity with respect to the state-of-the-art constant voltage process. Moreover, combining this systematic experimental investigation with artificial intelligence (AI) tools allowed us to rapidly discover drastically improved electrosynthetic conditions, reaching improvements of 30 and 325% in ADN production rates and selectivity, respectively. This powerful AI-enhanced experimental approach represents a paradigm shift in the design of electrified chemical transformations, which can accelerate the deployment of more sustainable electrochemical manufacturing processes.
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    Parallel spatial channels converge at a bottleneck in anterior word-selective cortex (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-08
    Description: In most environments, the visual system is confronted with many relevant objects simultaneously. That is especially true during reading. However, behavioral data demonstrate that a serial bottleneck prevents recognition of more than one word at a time. We used fMRI to investigate how parallel spatial channels of visual processing converge into a serial bottleneck for word recognition. Participants viewed pairs of words presented simultaneously. We found that retinotopic cortex processed the two words in parallel spatial channels, one in each contralateral hemisphere. Responses were higher for attended than for ignored words but were not reduced when attention was divided. We then analyzed two word-selective regions along the occipitotemporal sulcus (OTS) of both hemispheres (subregions of the visual word form area, VWFA). Unlike retinotopic regions, each word-selective region responded to words on both sides of fixation. Nonetheless, a single region in the left hemisphere (posterior OTS) contained spatial channels for both hemifields that were independently modulated by selective attention. Thus, the left posterior VWFA supports parallel processing of multiple words. In contrast, activity in a more anterior word-selective region in the left hemisphere (mid OTS) was consistent with a single channel, showing (i) limited spatial selectivity, (ii) no effect of spatial attention on mean response amplitudes, and (iii) sensitivity to lexical properties of only one attended word. Therefore, the visual system can process two words in parallel up to a late stage in the ventral stream. The transition to a single channel is consistent with the observed bottleneck in behavior.
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    Histone H2B monoubiquitination regulates heart development via epigenetic control of cilia motility (2019)
    National Academy of Sciences
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    Publication Date: 2019-06-24
    Description: Genomic analyses of patients with congenital heart disease (CHD) have identified significant contribution from mutations affecting cilia genes and chromatin remodeling genes; however, the mechanism(s) connecting chromatin remodeling to CHD is unknown. Histone H2B monoubiquitination (H2Bub1) is catalyzed by the RNF20 complex consisting of RNF20, RNF40, and UBE2B. Here, we show significant enrichment of loss-of-function mutations affecting H2Bub1 in CHD patients (enrichment 6.01,P= 1.67 × 10−03), some of whom had abnormal laterality associated with ciliary dysfunction. InXenopus, knockdown ofrnf20andrnf40results in abnormal heart looping, defective development of left–right (LR) asymmetry, and impaired cilia motility. Rnf20, Rnf40, and Ube2b affect LR patterning and cilia synergistically. Examination of global H2Bub1 level inXenopusembryos shows that H2Bub1 is developmentally regulated and requires Rnf20. To examine gene-specific H2Bub1, we performed ChIP-seq of mouse ciliated and nonciliated tissues and showed tissue-specific H2Bub1 marks significantly enriched at cilia genes including the transcription factorRfx3. Rnf20 knockdown results in decreased levels ofrfx3mRNA inXenopus, and exogenousrfx3can rescue the Rnf20 depletion phenotype. These data suggest that Rnf20 functions at theRfx3locus regulating cilia motility and cardiac situs and identify H2Bub1 as an upstream transcriptional regulator controlling tissue-specific expression of cilia genes. Our findings mechanistically link the two functional gene ontologies that have been implicated in human CHD: chromatin remodeling and cilia function.
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    Deep learning predicts path-dependent plasticity (2019)
    National Academy of Sciences
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    Publication Date: 2019-12-16
    Description: Plasticity theory aims at describing the yield loci and work hardening of a material under general deformation states. Most of its complexity arises from the nontrivial dependence of the yield loci on the complete strain history of a material and its microstructure. This motivated 3 ingenious simplifications that underpinned a century of developments in this field: 1) yield criteria describing yield loci location; 2) associative or nonassociative flow rules defining the direction of plastic flow; and 3) effective stress–strain laws consistent with the plastic work equivalence principle. However, 2 key complications arise from these simplifications. First, finding equations that describe these 3 assumptions for materials with complex microstructures is not trivial. Second, yield surface evolution needs to be traced iteratively, i.e., through a return mapping algorithm. Here, we show that these assumptions are not needed in the context of sequence learning when using recurrent neural networks, diverting the above-mentioned complications. This work offers an alternative to currently established plasticity formulations by providing the foundations for finding history- and microstructure-dependent constitutive models through deep learning.
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    Graphene-like monolayer monoxides and monochlorides (2019)
    National Academy of Sciences
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    Publication Date: 2019-08-12
    Description: Two-dimensional monolayer materials, with thicknesses of up to several atoms, can be obtained from almost every layer-structured material. It is believed that the catalogs of known 2D materials are almost complete, with fewer new graphene-like materials being discovered. Here, we report 2D graphene-like monolayers from monoxides such as BeO, MgO, CaO, SrO, BaO, and rock-salt structured monochlorides such as LiCl, and NaCl using first-principle calculations. Two-dimensional materials containing d-orbital atoms such as HfO, CdO, and AgCl are predicted. Adopting the same strategy, 2D graphene-like monolayers from mononitrides such as scandium nitride (ScN) and monoselenides such as cadmium selenide (CdSe) are discovered. Stress engineering is found to help stabilize 2D monolayers, through canceling the imaginary frequency of phonon dispersion relation. These 2D monolayers show high dynamic, thermal, kinetic, and mechanic stabilities due to atomic hybridization, and electronic delocalization.
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    Light-triggered thermal conductivity switching in azobenzene polymers (2019)
    National Academy of Sciences
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    Publication Date: 2019-03-08
    Description: Materials that can be switched between low and high thermal conductivity states would advance the control and conversion of thermal energy. Employing in situ time-domain thermoreflectance (TDTR) and in situ synchrotron X-ray scattering, we report a reversible, light-responsive azobenzene polymer that switches between high (0.35 W m−1K−1) and low thermal conductivity (0.10 W m−1K−1) states. This threefold change in the thermal conductivity is achieved by modulation of chain alignment resulted from the conformational transition between planar (trans) and nonplanar (cis) azobenzene groups under UV and green light illumination. This conformational transition leads to changes in the π-π stacking geometry and drives the crystal-to-liquid transition, which is fully reversible and occurs on a time scale of tens of seconds at room temperature. This result demonstrates an effective control of the thermophysical properties of polymers by modulating interchain π-π networks by light.
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    Cell contact and Nf2/Merlin-dependent regulation of TEAD palmitoylation and activity (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-01
    Description: The Hippo pathway is involved in regulating contact inhibition of proliferation and organ size control and responds to various physical and biochemical stimuli. It is a kinase cascade that negatively regulates the activity of cotranscription factors YAP and TAZ, which interact with DNA binding transcription factors including TEAD and activate the expression of target genes. In this study, we show that the palmitoylation of TEAD, which controls the activity and stability of TEAD proteins, is actively regulated by cell density independent of Lats, the key kinase of the Hippo pathway. The expression of fatty acid synthase and acetyl-CoA carboxylase involved in de novo biosynthesis of palmitate is reduced by cell density in an Nf2/Merlin-dependent manner. Depalmitoylation of TEAD is mediated by depalmitoylases including APT2 and ABHD17A. Palmitoylation-deficient TEAD4 mutant is unstable and degraded by proteasome through the activity of the E3 ubiquitin ligase CHIP. These findings show that TEAD activity is tightly controlled through the regulation of palmitoylation and stability via the orchestration of FASN, depalmitoylases, and E3 ubiquitin ligase in response to cell contact.
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    Self-regulation and theforaginggene (PRKG1) in humans (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-19
    Description: Foraging is a goal-directed behavior that balances the need to explore the environment for resources with the need to exploit those resources. InDrosophila melanogaster, distinct phenotypes have been observed in relation to theforaginggene (for), labeled the rover and sitter. Adult rovers explore their environs more extensively than do adult sitters. We explored whether this distinction would be conserved in humans. We made use of a distinction from regulatory mode theory between those who “get on with it,” so-called locomotors, and those who prefer to ensure they “do the right thing,” so-called assessors. In this logic, rovers and locomotors share similarities in goal pursuit, as do sitters and assessors. We showed that genetic variation inPRKG1, the human ortholog offor, is associated with preferential adoption of a specific regulatory mode. Next, participants performed a foraging task to see whether genetic differences associated with distinct regulatory modes would be associated with distinct goal pursuit patterns. Assessors tended to hug the boundary of the foraging environment, much like behaviors seen inDrosophilaadult sitters. In a patchy foraging environment, assessors adopted more cautious search strategies maximizing exploitation. These results show that distinct patterns of goal pursuit are associated with particular genotypes ofPRKG1, the human ortholog offor.
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    Intragenomic variability and extended sequence patterns in the mutational signature of ultraviolet light (2019)
    National Academy of Sciences
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    Publication Date: 2019-09-23
    Description: Mutational signatures can reveal properties of underlying mutational processes and are important when assessing signals of selection in cancer. Here, we describe the sequence characteristics of mutations induced by ultraviolet (UV) light, a major mutagen in several human cancers, in terms of extended (longer than trinucleotide) patterns as well as variability of the signature across chromatin states. Promoter regions display a distinct UV signature with reduced TCG 〉 TTG transitions, and genome-wide mapping of UVB-induced DNA photoproducts (pyrimidine dimers) showed that this may be explained by decreased damage formation at hypomethylated promoter CpG sites. Further, an extended signature model encompassing additional information from longer contextual patterns improves modeling of UV mutations, which may enhance discrimination between drivers and passenger events. Our study presents a refined picture of the UV signature and underscores that the characteristics of a single mutational process may vary across the genome.
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    OAS-RNase L innate immune pathway mediates the cytotoxicity of a DNA-demethylating drug (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-27
    Description: Drugs that reverse epigenetic silencing, such as the DNA methyltransferase inhibitor (DNMTi) 5-azacytidine (AZA), have profound effects on transcription and tumor cell survival. AZA is an approved drug for myelodysplastic syndromes and acute myeloid leukemia, and is under investigation for different solid malignant tumors. AZA treatment generates self, double-stranded RNA (dsRNA), transcribed from hypomethylated repetitive elements. Self dsRNA accumulation in DNMTi-treated cells leads to type I IFN production and IFN-stimulated gene expression. Here we report that cell death in response to AZA treatment occurs through the 2′,5′-oligoadenylate synthetase (OAS)-RNase L pathway. OASs are IFN-induced enzymes that synthesize the RNase L activator 2-5A in response to dsRNA. Cells deficient in RNase L or OAS1 to 3 are highly resistant to AZA, as are wild-type cells treated with a small-molecule inhibitor of RNase L. A small-molecule inhibitor of c-Jun NH2-terminal kinases (JNKs) also antagonizes RNase L-dependent cell death in response to AZA, consistent with a role for JNK in RNase L-induced apoptosis. In contrast, the rates of AZA-induced and RNase L-dependent cell death were increased by transfection of 2-5A, by deficiencies in ADAR1 (which edits and destabilizes dsRNA), PDE12 or AKAP7 (which degrade 2-5A), or by ionizing radiation (which induces IFN-dependent signaling). Finally, OAS1 expression correlates with AZA sensitivity in the NCI-60 set of tumor cell lines, suggesting that the level of OAS1 can be a biomarker for predicting AZA sensitivity of tumor cells. These studies may eventually lead to pharmacologic strategies for regulating the antitumor activity and toxicity of AZA and related drugs.
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    Thermalization and possible signatures of quantum chaos in complex crystalline materials (2019)
    National Academy of Sciences
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    Publication Date: 2019-09-12
    Description: Analyses of thermal diffusivity data on complex insulators and on strongly correlated electron systems hosted in similar complex crystal structures suggest that quantum chaos is a good description for thermalization processes in these systems, particularly in the high-temperature regime where the many phonon bands and their interactions dominate the thermal transport. Here we observe that for these systems diffusive thermal transport is controlled by a universal Planckian timescale τ∼ℏ/kBT and a unique velocity vE. Specifically, vE≈vph for complex insulators, and vph≲vE≪vF in the presence of strongly correlated itinerant electrons (vph and vF are the phonon and electron velocities, respectively). For the complex correlated electron systems we further show that charge diffusivity, while also reaching the Planckian relaxation bound, is largely dominated by the Fermi velocity of the electrons, hence suggesting that it is only the thermal (energy) diffusivity that describes chaos diffusivity.
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    Cyclic-di-GMP regulation promotes survival of a slow-replicating subpopulation of intracellularSalmonellaTyphimurium (2019)
    National Academy of Sciences
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    Publication Date: 2019-03-12
    Description: SalmonellaTyphimurium can invade and survive within macrophages where the bacterium encounters a range of host environmental conditions. Like many bacteria,S.Typhimurium rapidly responds to changing environments by the use of second messengers such as cyclic di-GMP (c-di-GMP). Here, we generate a fluorescent biosensor to measure c-di-GMP concentrations in thousands of individual bacteria during macrophage infection and to define the sensor enzymes important to c-di-GMP regulation. Three sensor phosphodiesterases were identified as critical to maintaining low c-di-GMP concentrations generated after initial phagocytosis by macrophages. Maintenance of low c-di-GMP concentrations by these phosphodiesterases was required to promote survival within macrophages and virulence for mice. Attenuation ofS. Typhimurium virulence was due to overproduction of c-di-GMP−regulated cellulose, as deletion of the cellulose synthase machinery restored virulence to a strain lacking enzymatic activity of the three phosphodiesterases. We further identified that the cellulose-mediated reduction in survival was constrained to a slow-replicating persister population ofS.Typhimurium induced within the macrophage intracellular environment. As utilization of glucose has been shown to be required forS.Typhimurium macrophage survival, one possible hypothesis is that this persister population requires the glucose redirected to the synthesis of cellulose to maintain a slow-replicating, metabolically active state.
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    MZB1 promotes the secretion of J-chain–containing dimeric IgA and is critical for the suppression of gut inflammation (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-24
    Description: IgA is the most abundantly produced antibody in the body and plays a crucial role in gut homeostasis and mucosal immunity. IgA forms a dimer that covalently associates with the joining (J) chain, which is essential for IgA transport into the mucosa. Here, we demonstrate that the marginal zone B and B-1 cell-specific protein (MZB1) interacts with IgA through the α-heavy-chain tailpiece dependent on the penultimate cysteine residue and prevents the intracellular degradation of α-light-chain complexes. Moreover, MZB1 promotes J-chain binding to IgA and the secretion of dimeric IgA. MZB1-deficient mice are impaired in secreting large amounts of IgA into the gut in response to acute inflammation and develop severe colitis. Oral administration of a monoclonal IgA significantly ameliorated the colitis, accompanied by normalization of the gut microbiota composition. The present study identifies a molecular chaperone that promotes J-chain binding to IgA and reveals an important mechanism that controls the quantity, quality, and function of IgA.
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    Vortex-induced dispersal of a plant pathogen by raindrop impact (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-25
    Description: Raindrop impact on infected plants can disperse micron-sized propagules of plant pathogens (e.g., spores of fungi). Little is known about the mechanism of how plant pathogens are liberated and transported due to raindrop impact. We used high-speed photography to observe thousands of dry-dispersed spores of the rust fungus Puccinia triticina being liberated from infected wheat plants following the impact of a single raindrop. We revealed that an air vortex ring was formed during the raindrop impact and carried the dry-dispersed spores away from the surface of the host plant. The maximum height and travel distance of the airborne spores increased with the aid of the air vortex. This unique mechanism of vortex-induced dispersal dynamics was characterized to predict trajectories of spores. Finally, we found that the spores transported by the air vortex can reach beyond the laminar boundary layer of leaves, which would enable the long-distance transport of plant pathogens through the atmosphere.
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    Origin of the avian predentary and evidence of a unique form of cranial kinesis in Cretaceous ornithuromorphs (2019)
    National Academy of Sciences
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    Publication Date: 2019-11-18
    Description: The avian predentary is a small skeletal structure located rostral to the paired dentaries found only in Mesozoic ornithuromorphs. The evolution and function of this enigmatic element is unknown. Skeletal tissues forming the predentary and the lower jaws in the basal ornithuromorph Yanornis martini are identified using computed-tomography, scanning electron microscopy, and histology. On the basis of these data, we propose hypotheses for the development, structure, and function of this element. The predentary is composed of trabecular bone. The convex caudal surface articulates with rostromedial concavities on the dentaries. These articular surfaces are covered by cartilage, which on the dentaries is divided into 3 discrete patches: 1 rostral articular cartilage and 2 symphyseal cartilages. The mechanobiology of avian cartilage suggests both compression and kinesis were present at the predentary–dentary joint, therefore suggesting a yet unknown form of avian cranial kinesis. Ontogenetic processes of skeletal formation occurring within extant taxa do not suggest the predentary originates within the dentaries, nor Meckel’s cartilage. We hypothesize that the predentary is a biomechanically induced sesamoid that arose within the soft connective tissues located rostral to the dentaries. The mandibular canal hosting the alveolar nerve suggests that the dentary teeth and predentary of Yanornis were proprioceptive. This whole system may have increased foraging efficiency. The Mesozoic avian predentary apparently coevolved with an edentulous portion of the premaxilla, representing a unique kinetic morphotype that combined teeth with a small functional beak and persisted successfully for ∼60 million years.
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    The functional importance of human foot muscles for bipedal locomotion (2019)
    National Academy of Sciences
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    Publication Date: 2019-01-17
    Description: Human feet have evolved to facilitate bipedal locomotion, losing an opposable digit that grasped branches in favor of a longitudinal arch (LA) that stiffens the foot and aids bipedal gait. Passive elastic structures are credited with supporting the LA, but recent evidence suggests that plantar intrinsic muscles (PIMs) within the foot actively contribute to foot stiffness. To test the functional significance of the PIMs, we compared foot and lower limb mechanics with and without a tibial nerve block that prevented contraction of these muscles. Comparisons were made during controlled limb loading, walking, and running in healthy humans. An inability to activate the PIMs caused slightly greater compression of the LA when controlled loads were applied to the lower limb by a linear actuator. However, when greater loads were experienced during ground contact in walking and running, the stiffness of the LA was not altered by the block, indicating that the PIMs’ contribution to LA stiffness is minimal, probably because of their small size. With the PIMs blocked, the distal joints of the foot could not be stiffened sufficiently to provide normal push-off against the ground during late stance. This led to an increase in stride rate and compensatory power generated by the hip musculature, but no increase in the metabolic cost of transport. The results reveal that the PIMs have a minimal effect on the stiffness of the LA when absorbing high loads, but help stiffen the distal foot to aid push-off against the ground when walking or running bipedally.
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    Electrochemical nanoimprinting of silicon (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-08
    Description: Scalable nanomanufacturing enables the commercialization of nanotechnology, particularly in applications such as nanophotonics, silicon photonics, photovoltaics, and biosensing. Nanoimprinting lithography (NIL) was the first scalable process to introduce 3D nanopatterning of polymeric films. Despite efforts to extend NIL’s library of patternable media, imprinting of inorganic semiconductors has been plagued by concomitant generation of crystallography defects during imprinting. Here, we use an electrochemical nanoimprinting process—called Mac-Imprint—for directly patterning electronic-grade silicon with 3D microscale features. It is shown that stamps made of mesoporous metal catalysts allow for imprinting electronic-grade silicon without the concomitant generation of porous silicon damage while introducing mesoscale roughness. Unlike most NIL processes, Mac-Imprint does not rely on plastic deformation, and thus, it allows for replicating hard and brittle materials, such as silicon, from a reusable polymeric mold, which can be manufactured by almost any existing microfabrication technique.
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    Steering CO2electroreduction toward ethanol production by a surface-bound Ru polypyridyl carbene catalyst on N-doped porous carbon (2019)
    National Academy of Sciences
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    Publication Date: 2019-12-10
    Description: Electrochemical reduction of CO2to multicarbon products is a significant challenge, especially for molecular complexes. We report here CO2reduction to multicarbon products based on a Ru(II) polypyridyl carbene complex that is immobilized on an N-doped porous carbon (RuPC/NPC) electrode. The catalyst utilizes the synergistic effects of the Ru(II) polypyridyl carbene complex and the NPC interface to steer CO2reduction toward C2 production at low overpotentials. In 0.5 M KHCO3/CO2aqueous solutions, Faradaic efficiencies of 31.0 to 38.4% have been obtained for C2 production at −0.87 to −1.07 V (vs. normal hydrogen electrode) with 21.0 to 27.5% for ethanol and 7.1 to 12.5% for acetate. Syngas is also produced with adjustable H2/CO mole ratios of 2.0 to 2.9. The RuPC/NPC electrocatalyst maintains its activity during 3-h CO2-reduction periods.
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    Impact of jamming criticality on low-temperature anomalies in structural glasses (2019)
    National Academy of Sciences
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    Publication Date: 2019-06-24
    Description: We present a mechanism for the anomalous behavior of the specific heat in low-temperature amorphous solids. The analytic solution of a mean-field model belonging to the same universality class as high-dimensional glasses, the spherical perceptron, suggests that there exists a cross-over temperature above which the specific heat scales linearly with temperature, while below it, a cubic scaling is displayed. This relies on two crucial features of the phase diagram: (i) the marginal stability of the free-energy landscape, which induces a gapless phase responsible for the emergence of a power-law scaling; and (ii) the vicinity of the classical jamming critical point, as the cross-over temperature gets lowered when approaching it. This scenario arises from a direct study of the thermodynamics of the system in the quantum regime, where we show that, contrary to crystals, the Debye approximation does not hold.
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    Observation of Rydberg exciton polaritons and their condensate in a perovskite cavity (2019)
    National Academy of Sciences
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    Publication Date: 2019-09-23
    Description: The condensation of half-light half-matter exciton polaritons in semiconductor optical cavities is a striking example of macroscopic quantum coherence in a solid-state platform. Quantum coherence is possible only when there are strong interactions between the exciton polaritons provided by their excitonic constituents. Rydberg excitons with high principal value exhibit strong dipole–dipole interactions in cold atoms. However, polaritons with the excitonic constituent that is an excited state, namely Rydberg exciton polaritons (REPs), have not yet been experimentally observed. Here, we observe the formation of REPs in a single crystal CsPbBr3 perovskite cavity without any external fields. These polaritons exhibit strong nonlinear behavior that leads to a coherent polariton condensate with a prominent blue shift. Furthermore, the REPs in CsPbBr3 are highly anisotropic and have a large extinction ratio, arising from the perovskite’s orthorhombic crystal structure. Our observation not only sheds light on the importance of many-body physics in coherent polariton systems involving higher-order excited states, but also paves the way for exploring these coherent interactions for solid-state quantum optical information processing.
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    Outflanking immunodominance to target subdominant broadly neutralizing epitopes (2019)
    National Academy of Sciences
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    Publication Date: 2019-06-18
    Description: A major obstacle to vaccination against antigenically variable viruses is skewing of antibody responses to variable immunodominant epitopes. For influenza virus hemagglutinin (HA), the immunodominance of the variable head impairs responses to the highly conserved stem. Here, we show that head immunodominance depends on the physical attachment of head to stem. Stem immunogenicity is enhanced by immunizing with stem-only constructs or by increasing local HA concentration in the draining lymph node. Surprisingly, coimmunization of full-length HA and stem alters stem-antibody class switching. Our findings delineate strategies for overcoming immunodominance, with important implications for human vaccination.
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    L-type voltage-gated Ca2+ channel CaV1.2 regulates chondrogenesis during limb development (2019)
    National Academy of Sciences
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    Publication Date: 2019-10-07
    Description: All cells, including nonexcitable cells, maintain a discrete transmembrane potential (Vmem), and have the capacity to modulate Vmem and respond to their own and neighbors’ changes in Vmem. Spatiotemporal variations have been described in developing embryonic tissues and in some cases have been implicated in influencing developmental processes. Yet, how such changes in Vmem are converted into intracellular inputs that in turn regulate developmental gene expression and coordinate patterned tissue formation, has remained elusive. Here we document that the Vmem of limb mesenchyme switches from a hyperpolarized to depolarized state during early chondrocyte differentiation. This change in Vmem increases intracellular Ca2+ signaling through Ca2+ influx, via CaV1.2, 1 of L-type voltage-gated Ca2+ channels (VGCCs). We find that CaV1.2 activity is essential for chondrogenesis in the developing limbs. Pharmacological inhibition by an L-type VGCC specific blocker, or limb-specific deletion of CaV1.2, down-regulates expression of genes essential for chondrocyte differentiation, including Sox9, Col2a1, and Agc1, and thus disturbs proper cartilage formation. The Ca2+-dependent transcription factor NFATc1, which is a known major transducer of intracellular Ca2+ signaling, partly rescues Sox9 expression. These data reveal instructive roles of CaV1.2 in limb development, and more generally expand our understanding of how modulation of membrane potential is used as a mechanism of developmental regulation.
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    A large-scale analysis of task switching practice effects across the lifespan (2019)
    National Academy of Sciences
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    Publication Date: 2019-08-19
    Description: An important feature of human cognition is the ability to flexibly and efficiently adapt behavior in response to continuously changing contextual demands. We leverage a large-scale dataset from Lumosity, an online cognitive-training platform, to investigate how cognitive processes involved in cued switching between tasks are affected by level of task practice across the adult lifespan. We develop a computational account of task switching that specifies the temporal dynamics of activating task-relevant representations and inhibiting task-irrelevant representations and how they vary with extended task practice across a number of age groups. Practice modulates the level of activation of the task-relevant representation and improves the rate at which this information becomes available, but has little effect on the task-irrelevant representation. While long-term practice improves performance across all age groups, it has a greater effect on older adults. Indeed, extensive task practice can make older individuals functionally similar to less-practiced younger individuals, especially for cognitive measures that focus on the rate at which task-relevant information becomes available.
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    Equilibrium structure and deformation response of 2D kinetoplast sheets (2019)
    National Academy of Sciences
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    Publication Date: 2019-12-06
    Description: The considerable interest in two-dimensional (2D) materials and complex molecular topologies calls for a robust experimental system for single-molecule studies. In this work, we study the equilibrium properties and deformation response of a complex DNA structure called a kinetoplast, a 2D network of thousands of linked rings akin to molecular chainmail. Examined in good solvent conditions, kinetoplasts appear as a wrinkled hemispherical sheet. The conformation of each kinetoplast is dictated by its network topology, giving it a unique shape, which undergoes small-amplitude thermal fluctuations at subsecond timescales, with a wide separation between fluctuation and diffusion timescales. They deform elastically when weakly confined and swell to their equilibrium dimensions when the confinement is released. We hope that, in the same way that linear DNA became a canonical model system on the first investigations of its polymer-like behavior, kinetoplasts can serve that role for 2D and catenated polymer systems.
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    Spontaneous mutations in maize pollen are frequent in some lines and arise mainly from retrotranspositions and deletions (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-16
    Description: While studying spontaneous mutations at the maize bronze (bz) locus, we made the unexpected discovery that specific low-copy number retrotransposons are mobile in the pollen of some maize lines, but not of others. We conducted large-scale genetic experiments to isolate new bz mutations from several Bz stocks and recovered spontaneous stable mutations only in the pollen parent in reciprocal crosses. Most of the new stable bz mutations resulted from either insertions of low-copy number long terminal repeat (LTR) retrotransposons or deletions, the same two classes of mutations that predominated in a collection of spontaneous wx mutations [Wessler S (1997) The Mutants of Maize, pp 385–386]. Similar mutations were recovered at the closely linked sh locus. These events occurred with a frequency of 2–4 × 10−5 in two lines derived from W22 and in 4Co63, but not at all in B73 or Mo17, two inbreds widely represented in Corn Belt hybrids. Surprisingly, the mutagenic LTR retrotransposons differed in the active lines, suggesting differences in the autonomous element make-up of the lines studied. Some active retrotransposons, like Hopscotch, Magellan, and Bs2, a Bs1 variant, were described previously; others, like Foto and Focou in 4Co63, were not. By high-throughput sequencing of retrotransposon junctions, we established that retrotranposition of Hopscotch, Magellan, and Bs2 occurs genome-wide in the pollen of active lines, but not in the female germline or in somatic tissues. We discuss here the implications of these results, which shed light on the source, frequency, and nature of spontaneous mutations in maize.
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    Mapping hole hopping escape routes in proteins (2019)
    National Academy of Sciences
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    Publication Date: 2019-07-24
    Description: A recently proposed oxidative damage protection mechanism in proteins relies on hole hopping escape routes formed by redox-active amino acids. We present a computational tool to identify the dominant charge hopping pathways through these residues based on the mean residence times of the transferring charge along these hopping pathways. The residence times are estimated by combining a kinetic model with well-known rate expressions for the charge-transfer steps in the pathways. We identify the most rapid hole hopping escape routes in cytochrome P450 monooxygenase, cytochrome c peroxidase, and benzylsuccinate synthase (BSS). This theoretical analysis supports the existence of hole hopping chains as a mechanism capable of providing hole escape from protein catalytic sites on biologically relevant timescales. Furthermore, we find that pathways involving the [4Fe4S] cluster as the terminal hole acceptor in BSS are accessible on the millisecond timescale, suggesting a potential protective role of redox-active cofactors for preventing protein oxidative damage.
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    Insights into the origin of the high energy-conversion efficiency of F1-ATPase (2019)
    National Academy of Sciences
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    Publication Date: 2019-07-24
    Description: Our understanding of the rotary-coupling mechanism of F1-ATPase has been greatly enhanced in the last decade by advances in X-ray crystallography, single-molecular imaging, and theoretical models. Recently, Volkán-Kacsó and Marcus [S. Volkán-Kacsó, R. A. Marcus, Proc. Natl. Acad. Sci. U.S.A. 112, 14230 (2015)] presented an insightful thermodynamic model based on the Marcus reaction theory coupled with an elastic structural deformation term to explain the observed γ-rotation angle dependence of the adenosine triphosphate (ATP)/adenosine diphosphate (ADP) exchange rates of F1-ATPase. Although the model is successful in correlating single-molecule data, it is not in agreement with the available theoretical results. We describe a revision of the model, which leads to consistency with the simulation results and other experimental data on the F1-ATPase rotor compliance. Although the free energy liberated on ATP hydrolysis by F1-ATPase is rapidly dissipated as heat and so cannot contribute directly to the rotation, we show how, nevertheless, F1-ATPase functions near the maximum possible efficiency. This surprising result is a consequence of the differential binding of ATP and its hydrolysis products ADP and Pi along a well-defined pathway.
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    Homotypic cooperativity and collective binding are determinants of bHLH specificity and function (2019)
    National Academy of Sciences
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    Publication Date: 2019-07-24
    Description: Eukaryotic cells express transcription factor (TF) paralogues that bind to nearly identical DNA sequences in vitro but bind at different genomic loci and perform different functions in vivo. Predicting how 2 paralogous TFs bind in vivo using DNA sequence alone is an important open problem. Here, we analyzed 2 yeast bHLH TFs, Cbf1p and Tye7p, which have highly similar binding preferences in vitro, yet bind at almost completely nonoverlapping target loci in vivo. We dissected the determinants of specificity for these 2 proteins by making a number of chimeric TFs in which we swapped different domains of Cbf1p and Tye7p and determined the effects on in vivo binding and cellular function. From these experiments, we learned that the Cbf1p dimer achieves its specificity by binding cooperatively with other Cbf1p dimers bound nearby. In contrast, we found that Tye7p achieves its specificity by binding cooperatively with 3 other DNA-binding proteins, Gcr1p, Gcr2p, and Rap1p. Remarkably, most promoters (63%) that are bound by Tye7p do not contain a consensus Tye7p binding site. Using this information, we were able to build simple models to accurately discriminate bound and unbound genomic loci for both Cbf1p and Tye7p. We then successfully reprogrammed the human bHLH NPAS2 to bind Cbf1p in vivo targets and a Tye7p target intergenic region to be bound by Cbf1p. These results demonstrate that the genome-wide binding targets of paralogous TFs can be discriminated using sequence information, and provide lessons about TF specificity that can be applied across the phylogenetic tree.
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    Agency plus automation: Designing artificial intelligence into interactive systems (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-04
    Description: Much contemporary rhetoric regards the prospects and pitfalls of using artificial intelligence techniques to automate an increasing range of tasks, especially those once considered the purview of people alone. These accounts are often wildly optimistic, understating outstanding challenges while turning a blind eye to the human labor that undergirds and sustains ostensibly “automated” services. This long-standing focus on purely automated methods unnecessarily cedes a promising design space: one in which computational assistance augments and enriches, rather than replaces, people’s intellectual work. This tension between human agency and machine automation poses vital challenges for design and engineering. In this work, we consider the design of systems that enable rich, adaptive interaction between people and algorithms. We seek to balance the often-complementary strengths and weaknesses of each, while promoting human control and skillful action. We share case studies of interactive systems we have developed in three arenas—data wrangling, exploratory analysis, and natural language translation—that integrate proactive computational support into interactive systems. To improve outcomes and support learning by both people and machines, we describe the use of shared representations of tasks augmented with predictive models of human capabilities and actions. We conclude with a discussion of future prospects and scientific frontiers for intelligence augmentation research.
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    Histone H2AX promotes neuronal health by controlling mitochondrial homeostasis (2019)
    National Academy of Sciences
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    Publication Date: 2019-03-25
    Description: Phosphorylation of histone H2AX is a major contributor to efficient DNA repair. We recently reported neurobehavioral deficits in mice lacking H2AX. Here we establish that this neural failure stems from impairment of mitochondrial function and repression of the mitochondrial biogenesis gene PGC-1α. H2AX loss leads to reduced levels of the major subunits of the mitochondrial respiratory complexes in mouse embryonic fibroblasts and in the striatum, a brain region particularly vulnerable to mitochondrial damage. These defects are substantiated by disruption of the mitochondrial shape in H2AX mutant cells. Ectopic expression of PGC-1α restores mitochondrial oxidative phosphorylation complexes and mitigates cell death. H2AX knockout mice display increased neuronal death in the brain when challenged with 3-nitropronionic acid, which targets mitochondria. This study establishes a role for H2AX in mitochondrial homeostasis associated with neuroprotection.
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    SIP/CacyBP promotes autophagy by regulating levels of BRUCE/Apollon, which stimulates LC3-I degradation (2019)
    National Academy of Sciences
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    Publication Date: 2019-06-18
    Description: BRUCE/Apollon is a membrane-associated inhibitor of apoptosis protein that is essential for viability and has ubiquitin-conjugating activity. On initiation of apoptosis, the ubiquitin ligase Nrdp1/RNF41 promotes proteasomal degradation of BRUCE. Here we demonstrate that BRUCE together with the proteasome activator PA28γ causes proteasomal degradation of LC3-I and thus inhibits autophagy. LC3-I on the phagophore membrane is conjugated to phosphatidylethanolamine to form LC3-II, which is required for the formation of autophagosomes and selective recruitment of substrates. SIP/CacyBP is a ubiquitination-related protein that is highly expressed in neurons and various tumors. Under normal conditions, SIP inhibits the ubiquitination and degradation of BRUCE, probably by blocking the binding of Nrdp1 to BRUCE. On DNA damage by topoisomerase inhibitors, Nrdp1 causes monoubiquitination of SIP and thus promotes apoptosis. However, on starvation, SIP together with Rab8 enhances the translocation of BRUCE into the recycling endosome, formation of autophagosomes, and degradation of BRUCE by optineurin-mediated autophagy. Accordingly, deletion of SIP in cultured cells reduces the autophagic degradation of damaged mitochondria and cytosolic protein aggregates. Thus, by stimulating proteasomal degradation of LC3-I, BRUCE also inhibits autophagy. Conversely, SIP promotes autophagy by blocking BRUCE-dependent degradation of LC3-I and by enhancing autophagosome formation and autophagic destruction of BRUCE. These actions of BRUCE and SIP represent mechanisms that link the regulation of autophagy and apoptosis under different conditions.
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    Learning the space-time phase diagram of bacterial swarm expansion (2019)
    National Academy of Sciences
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    Publication Date: 2019-01-11
    Description: Coordinated dynamics of individual components in active matter are an essential aspect of life on all scales. Establishing a comprehensive, causal connection between intracellular, intercellular, and macroscopic behaviors has remained a major challenge due to limitations in data acquisition and analysis techniques suitable for multiscale dynamics. Here, we combine a high-throughput adaptive microscopy approach with machine learning, to identify key biological and physical mechanisms that determine distinct microscopic and macroscopic collective behavior phases which develop as Bacillus subtilis swarms expand over five orders of magnitude in space. Our experiments, continuum modeling, and particle-based simulations reveal that macroscopic swarm expansion is primarily driven by cellular growth kinetics, whereas the microscopic swarming motility phases are dominated by physical cell–cell interactions. These results provide a unified understanding of bacterial multiscale behavioral complexity in swarms.
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    Quantum parity Hall effect in Bernal-stacked trilayer graphene (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-03
    Description: The quantum Hall effect has recently been generalized from transport of conserved charges to include transport of other approximately conserved-state variables, including spin and valley, via spin- or valley-polarized boundary states with different chiralities. Here, we report a class of quantum Hall effect in Bernal- or ABA-stacked trilayer graphene (TLG), the quantum parity Hall (QPH) effect, in which boundary channels are distinguished by even or odd parity under the system’s mirror reflection symmetry. At the charge neutrality point, the longitudinal conductance σxx is first quantized to 4e2/h at a small perpendicular magnetic field B⊥, establishing the presence of four edge channels. As B⊥ increases, σxx first decreases to 2e2/h, indicating spin-polarized counterpropagating edge states, and then, to approximately zero. These behaviors arise from level crossings between even- and odd-parity bulk Landau levels driven by exchange interactions with the underlying Fermi sea, which favor an ordinary insulator ground state in the strong B⊥ limit and a spin-polarized state at intermediate fields. The transitions between spin-polarized and -unpolarized states can be tuned by varying Zeeman energy. Our findings demonstrate a topological phase that is protected by a gate-controllable symmetry and sensitive to Coulomb interactions.
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    Motional dynamics of single Patched1 molecules in cilia are controlled by Hedgehog and cholesterol (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-28
    Description: The Hedgehog-signaling pathway is an important target in cancer research and regenerative medicine; yet, on the cellular level, many steps are still poorly understood. Extensive studies of the bulk behavior of the key proteins in the pathway established that during signal transduction they dynamically localize in primary cilia, antenna-like solitary organelles present on most cells. The secreted Hedgehog ligand Sonic Hedgehog (SHH) binds to its receptor Patched1 (PTCH1) in primary cilia, causing its inactivation and delocalization from cilia. At the same time, the transmembrane protein Smoothened (SMO) is released of its inhibition by PTCH1 and accumulates in cilia. We used advanced, single molecule-based microscopy to investigate these processes in live cells. As previously observed for SMO, PTCH1 molecules in cilia predominantly move by diffusion and less frequently by directional transport, and spend a fraction of time confined. After treatment with SHH we observed two major changes in the motional dynamics of PTCH1 in cilia. First, PTCH1 molecules spend more time as confined, and less time freely diffusing. This result could be mimicked by a depletion of cholesterol from cells. Second, after treatment with SHH, but not after cholesterol depletion, the molecules that remain in the diffusive state showed a significant increase in the diffusion coefficient. Therefore, PTCH1 inactivation by SHH changes the diffusive motion of PTCH1, possibly by modifying the membrane microenvironment in which PTCH1 resides.
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    Segregation through the multiscalar lens (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-30
    Description: We introduce a mathematical framework that allows one to carry out multiscalar and multigroup spatial exploratory analysis across urban regions. By producing coefficients that integrate information across all scales and that are normalized with respect to theoretical maximally segregated configurations, this framework provides a practical and powerful tool for the comparative empirical analysis of urban segregation. We illustrate our method with a study of ethnic mixing in the Los Angeles metropolitan area.
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    Large bandgap of pressurized trilayer graphene (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-19
    Description: Graphene-based nanodevices have been developed rapidly and are now considered a strong contender for postsilicon electronics. However, one challenge facing graphene-based transistors is opening a sizable bandgap in graphene. The largest bandgap achieved so far is several hundred meV in bilayer graphene, but this value is still far below the threshold for practical applications. Through in situ electrical measurements, we observed a semiconducting character in compressed trilayer graphene by tuning the interlayer interaction with pressure. The optical absorption measurements demonstrate that an intrinsic bandgap of 2.5 ± 0.3 eV could be achieved in such a semiconducting state, and once opened could be preserved to a few GPa. The realization of wide bandgap in compressed trilayer graphene offers opportunities in carbon-based electronic devices.
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    Macromolecules with programmable shape, size, and chemistry (2019)
    National Academy of Sciences
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    Publication Date: 2019-01-17
    Description: Shape, size, and composition are the most fundamental design features, enabling highly complex functionalities. Despite recent advances, the independent control of shape, size, and chemistry of macromolecules remains a synthetic challenge. We report a scalable methodology to produce large, well-defined macromolecules with programmable shape, size, and chemistry that combines reactor engineering principles and controlled polymerizations. Specifically, bottlebrush polymers with conical, ellipsoidal, and concave architectures are synthesized using two orthogonal polymerizations. The chemical versatility is highlighted by the synthesis of a compositional asymmetric cone. The strong agreement between predictions and experiments validates the precision that this methodology offers.
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    ANO1/TMEM16A regulates process maturation in radial glial cells in the developing brain (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-30
    Description: Neural stem cells (NSCs) are primary progenitor cells in the early developmental stage in the brain that initiate a diverse lineage of differentiated neurons and glia. Radial glial cells (RGCs), a type of neural stem cell in the ventricular zone, are essential for nurturing and delivering new immature neurons to the appropriate cortical target layers. Here we report that Anoctamin 1 (ANO1)/TMEM16A, a Ca2+-activated chloride channel, mediates the Ca2+-dependent process extension of RGCs. ANO1 is highly expressed and functionally active in RGCs of the mouse embryonic ventricular zone. Knockdown of ANO1 suppresses RGC process extension and protrusions, whereas ANO1 overexpression stimulates process extension. Among various trophic factors, brain-derived neurotrophic factor (BDNF) activates ANO1, which is required for BDNF-induced process extension in RGCs. More importantly, Ano1-deficient mice exhibited disrupted cortical layers and reduced cortical thickness. We thus conclude that the regulation of RGC process extension by ANO1 contributes to the normal formation of mouse embryonic brain.
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    Quantitative imaging of anion exchange kinetics in halide perovskites (2019)
    National Academy of Sciences
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    Publication Date: 2019-06-12
    Description: Ion exchange, as a postsynthetic transformation strategy, offers more flexibilities in controlling material compositions and structures beyond direct synthetic methodology. Observation of such transformation kinetics on the single-particle level with rich spatial and spectroscopic information has never been achieved. We report the quantitative imaging of anion exchange kinetics in individual single-crystalline halide perovskite nanoplates using confocal photoluminescence microscopy. We have systematically observed a symmetrical anion exchange pathway on the nanoplates with dependence on reaction time and plate thickness, which is governed by the crystal structure and the diffusion-limited transformation mechanism. Based on a reaction–diffusion model, the halide diffusion coefficient was estimated to be on the order of10−14cm2⋅s−1. This diffusion-controlled mechanism leads to the formation of 2D perovskite heterostructures with spatially resolved coherent interface through the precisely controlled anion exchange reaction, offering a design protocol for tailoring functionalities of semiconductors at the nano-/microscale.
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    Breaking tolerance with engineered class I antigen-presenting molecules (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-06
    Description: Successful efforts to activate T cells capable of recognizing weak cancer-associated self-antigens have employed altered peptide antigens to activate T cell responses capable of cross-reacting on native tumor-associated self. A limitation of this approach is the requirement for detailed knowledge about the altered self-peptide ligands used in these vaccines. In the current study we considered allorecognition as an approach for activating CTL capable of recognizing weak or self-antigens in the context of self-MHC. Nonself antigen-presenting molecules typically contain polymorphisms that influence interactions with the bound peptide and TCR interface. Recognition of these nonself structures results in peptide-dependent alloimmunity. Alloreactive T cells target their inducing alloantigens as well as third-party alloantigens but generally fail to target self-antigens. Certain residues located on the alpha-1/2 domains of class I antigen-presenting molecules primarily interface with TCR. These residues are more conserved within and across species than are residues that determine peptide antigen binding properties. Class I variants designed with amino acid substitutions at key positions within the conserved helical structures are shown to provide strong activating signals to alloreactive CD8 T cells while avoiding changes in naturally bound peptide ligands. Importantly, CTL activated in this manner can break self-tolerance by reacting to self-peptides presented by native MHC. The ability to activate self-tolerant T cells capable of cross-reacting on self-peptide-MHC in vivo represents an approach for inducing autoimmunity, with possible application in cancer vaccines.
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    Directional coupling of slow and fast hippocampal gamma with neocortical alpha/beta oscillations in human episodic memory (2019)
    National Academy of Sciences
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    Publication Date: 2019-10-09
    Description: Episodic memories hinge upon our ability to process a wide range of multisensory information and bind this information into a coherent, memorable representation. On a neural level, these 2 processes are thought to be supported by neocortical alpha/beta desynchronization and hippocampal theta/gamma synchronization, respectively. Intuitively, these 2 processes should couple to successfully create and retrieve episodic memories, yet this hypothesis has not been tested empirically. We address this by analyzing human intracranial electroencephalogram data recorded during 2 associative memory tasks. We find that neocortical alpha/beta (8 to 20 Hz) power decreases reliably precede and predict hippocampal “fast” gamma (60 to 80 Hz) power increases during episodic memory formation; during episodic memory retrieval, however, hippocampal “slow” gamma (40 to 50 Hz) power increases reliably precede and predict later neocortical alpha/beta power decreases. We speculate that this coupling reflects the flow of information from the neocortex to the hippocampus during memory formation, and hippocampal pattern completion inducing information reinstatement in the neocortex during memory retrieval.
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    The deaminase APOBEC3B triggers the death of cells lacking uracil DNA glycosylase (2019)
    National Academy of Sciences
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    Publication Date: 2019-10-14
    Description: Human cells express up to 9 active DNA cytosine deaminases with functions in adaptive and innate immunity. Many cancers manifest an APOBEC mutation signature and APOBEC3B (A3B) is likely the main enzyme responsible. Although significant numbers of APOBEC signature mutations accumulate in tumor genomes, the majority of APOBEC-catalyzed uracil lesions are probably counteracted in an error-free manner by the uracil base excision repair pathway. Here, we show that A3B-expressing cells can be selectively killed by inhibiting uracil DNA glycosylase 2 (UNG) and that this synthetic lethal phenotype requires functional mismatch repair (MMR) proteins and p53. UNG knockout human 293 and MCF10A cells elicit an A3B-dependent death. This synthetic lethal phenotype is dependent on A3B catalytic activity and reversible by UNG complementation. A3B expression in UNG-null cells causes a buildup of genomic uracil, and the ensuing lethality requires processing of uracil lesions (likely U/G mispairs) by MSH2 and MLH1 (likely noncanonical MMR). Cancer cells expressing high levels of endogenous A3B and functional p53 can also be killed by expressing an UNG inhibitor. Taken together, UNG-initiated base excision repair is a major mechanism counteracting genomic mutagenesis by A3B, and blocking UNG is a potential strategy for inducing the selective death of tumors.
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    Sublethal antibiotics collapse gut bacterial populations by enhancing aggregation and expulsion (2019)
    National Academy of Sciences
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    Publication Date: 2019-10-07
    Description: Antibiotics induce large and highly variable changes in the intestinal microbiome even at sublethal concentrations, through mechanisms that remain elusive. Using gnotobiotic zebrafish, which allow high-resolution examination of microbial dynamics, we found that sublethal doses of the common antibiotic ciprofloxacin cause severe drops in bacterial abundance. Contrary to conventional views of antimicrobial tolerance, disruption was more pronounced for slow-growing, aggregated bacteria than for fast-growing, planktonic species. Live imaging revealed that antibiotic treatment promoted bacterial aggregation and increased susceptibility to intestinal expulsion. Intestinal mechanics therefore amplify the effects of antibiotics on resident bacteria. Microbial dynamics are captured by a biophysical model that connects antibiotic-induced collapses to gelation phase transitions in soft materials, providing a framework for predicting the impact of antibiotics on the intestinal microbiome.
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    RAMP3 determines rapid recycling of atypical chemokine receptor-3 for guided angiogenesis (2019)
    National Academy of Sciences
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    Publication Date: 2019-11-11
    Description: Receptor-activity–modifying proteins (RAMPs) are single transmembrane-spanning proteins which serve as molecular chaperones and allosteric modulators of G-protein–coupled receptors (GPCRs) and their signaling pathways. Although RAMPs have been previously studied in the context of their effects on Family B GPCRs, the coevolution of RAMPs with many GPCR families suggests an expanded repertoire of potential interactions. Using bioluminescence resonance energy transfer-based and cell-surface expression approaches, we comprehensively screen for RAMP interactions within the chemokine receptor family and identify robust interactions between RAMPs and nearly all chemokine receptors. Most notably, we identify robust RAMP interaction with atypical chemokine receptors (ACKRs), which function to establish chemotactic gradients for directed cell migration. Specifically, RAMP3 association with atypical chemokine receptor 3 (ACKR3) diminishes adrenomedullin (AM) ligand availability without changing G-protein coupling. Instead, RAMP3 is required for the rapid recycling of ACKR3 to the plasma membrane through Rab4-positive vesicles following either AM or SDF-1/CXCL12 binding, thereby enabling formation of dynamic spatiotemporal chemotactic gradients. Consequently, genetic deletion of either ACKR3 or RAMP3 in mice abolishes directed cell migration of retinal angiogenesis. Thus, RAMP association with chemokine receptor family members represents a molecular interaction to control receptor signaling and trafficking properties.
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    KRAS G13D sensitivity to neurofibromin-mediated GTP hydrolysis (2019)
    National Academy of Sciences
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    Publication Date: 2019-10-14
    Description: KRAS mutations occur in ∼35% of colorectal cancers and promote tumor growth by constitutively activating the mitogen-activated protein kinase (MAPK) pathway. KRAS mutations at codons 12, 13, or 61 are thought to prevent GAP protein-stimulated GTP hydrolysis and render KRAS-mutated colorectal cancers unresponsive to epidermal growth factor receptor (EGFR) inhibitors. We report here that KRAS G13-mutated cancer cells are frequently comutated with NF1 GAP but NF1 is rarely mutated in cancers with KRAS codon 12 or 61 mutations. Neurofibromin protein (encoded by the NF1 gene) hydrolyzes GTP directly in complex with KRAS G13D, and KRAS G13D-mutated cells can respond to EGFR inhibitors in a neurofibromin-dependent manner. Structures of the wild type and G13D mutant of KRAS in complex with neurofibromin (RasGAP domain) provide the structural basis for neurofibromin-mediated GTP hydrolysis. These results reveal that KRAS G13D is responsive to neurofibromin-stimulated hydrolysis and suggest that a subset of KRAS G13-mutated colorectal cancers that are neurofibromin-competent may respond to EGFR therapies.
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    A portrait of wellbore leakage in northeastern British Columbia, Canada (2019)
    National Academy of Sciences
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    Publication Date: 2019-11-18
    Description: Oil and gas well leakage is of public concern primarily due to the perceived risks of aquifer contamination and greenhouse gas (GHG) emissions. This study examined well leakage data from the British Columbia Oil and Gas Commission (BC OGC) to identify leakage pathways and initially quantify incident rates of leakage and GHG emissions from leaking wells. Three types of leakage are distinguished: “surface casing vent flow” (SCVF), “outside the surface casing leakage” (OSCL), and “cap leakage” (CL). In British Columbia (BC), the majority of reported incidents involve SCVF of gases, which does not pose a risk of aquifer contamination but does contribute to GHG emissions. Reported liquid leakage of brines and hydrocarbons is rarer. OSCL and CL of gas are more serious problems due to the risk of long-term leakage from abandoned wells; some were reported to be leaking gas several decades after they were permanently abandoned. According to the requirements of provincial regulation, 21,525 have been tested for leakage. In total, 2,329 wells in BC have had reported leakage during the lifetime of the well. This represents 10.8% of all wells in the assumed test population. However, it seems likely that wells drilled and/or abandoned before 2010 have unreported leakage. In BC, the total GHG emission from gas SCVF is estimated to reach about 75,000 t/y based on the existing inventory calculation; however, this number is likely higher due to underreporting.
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    Direct visualization of cAMP signaling in primary cilia reveals up-regulation of ciliary GPCR activity following Hedgehog activation (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-29
    Description: The primary cilium permits compartmentalization of specific signaling pathways, including elements of the Hedgehog (Hh) pathway. Hh transcriptional activity is thought to be negatively regulated by constitutively high ciliary cAMP maintained by the Gα(s)-coupled GPCR, GPR161. However, cilia also sequester many other Gα(s)-coupled GPCRs with unknown potential to regulate Hh. Here we used biosensors optimized for ciliary cAMP and strategies to isolate signals in the cilium from the cell body and neighboring cells. We found that ciliary cAMP was not elevated relative to cellular cAMP, inconsistent with constitutive cAMP production. Gα(s)-coupled GPCRs (e.g., the 5-HT6 serotonin and D1R dopamine receptor) had reduced ability to generate cAMP upon trafficking to the ciliary membrane. However, activation of the Hh pathway restored or amplified GPCR function to permit cAMP elevation selectively in the cilium. Hh therefore enables its own local GPCR-dependent cAMP regulatory circuit. Considering that GPCRs comprise much of the druggable genome, these data suggest alternative strategies to modify Hh signaling.
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    Revisiting the protomotive vectorial motion of F0-ATPase (2019)
    National Academy of Sciences
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    Publication Date: 2019-09-11
    Description: The elucidation of the detailed mechanism used by F0 to convert proton gradient to torque and rotational motion presents a major puzzle despite significant biophysical and structural progress. Although the conceptual model has advanced our understanding of the working principles of such systems, it is crucial to explore the actual mechanism using structure-based models that actually reproduce a unidirectional proton-driven rotation. Our previous work used a coarse-grained (CG) model to simulate the action of F0. However, the simulations were based on a very tentative structural model of the interaction between subunit a and subunit c. Here, we again use a CG model but with a recent cryo-EM structure of cF1F0 and also explore the proton path using our water flooding and protein dipole Langevin dipole semimacroscopic formalism with its linear response approximation version (PDLD/S-LRA) approaches. The simulations are done in the combined space defined by the rotational coordinate and the proton transport coordinate. The study reproduced the effect of the protomotive force on the rotation of the F0 while establishing the electrostatic origin of this effect. Our landscape reproduces the correct unidirectionality of the synthetic direction of the F0 rotation and shows that it reflects the combined electrostatic coupling between the proton transport path and the c-ring conformational change. This work provides guidance for further studies in other proton-driven mechanochemical systems and should lead (when combined with studies of F1) to a complete energy transduction picture of the F0F1-ATPase system.
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    Divergent kinase regulates membrane ultrastructure of theToxoplasmaparasitophorous vacuole (2019)
    National Academy of Sciences
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    Publication Date: 2019-03-08
    Description: Apicomplexan parasites replicate within a protective organelle, called the parasitophorous vacuole (PV). TheToxoplasma gondiiPV is filled with a network of tubulated membranes, which are thought to facilitate trafficking of effectors and nutrients. Despite being critical to parasite virulence, there is scant mechanistic understanding of the network’s functions. Here, we identify the parasite-secreted kinase WNG1 (With-No-Gly-loop) as a critical regulator of tubular membrane biogenesis. WNG1 family members adopt an atypical protein kinase fold lacking the glycine rich ATP-binding loop that is required for catalysis in canonical kinases. Unexpectedly, we find that WNG1 is an active protein kinase that localizes to the PV lumen and phosphorylates PV-resident proteins, several of which are essential for the formation of a functional intravacuolar network. Moreover, we show that WNG1-dependent phosphorylation of these proteins is required for their membrane association, and thus their ability to tubulate membranes. Consequently, WNG1 knockout parasites have an aberrant PV membrane ultrastructure. Collectively, our results describe a unique family ofToxoplasmakinases and implicate phosphorylation of secreted proteins as a mechanism of regulating PV development during parasite infection.
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    Prp8 impacts cryptic but not alternative splicing frequency (2019)
    National Academy of Sciences
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    Publication Date: 2019-01-23
    Description: Pre-mRNA splicing must occur with extremely high fidelity. Spliceosomes assemble onto pre-mRNA guided by specific sequences (5′ splice site, 3′ splice site, and branchpoint). When splice sites are mutated, as in many hereditary diseases, the spliceosome can aberrantly select nearby pseudo- or “cryptic” splice sites, often resulting in nonfunctional protein. How the spliceosome distinguishes authentic splice sites from cryptic splice sites is poorly understood. We performed aCaenorhabditis elegansgenetic screen to find cellular factors that affect the frequency with which the spliceosome uses cryptic splice sites and identified two alleles in core spliceosome component Prp8 that alter cryptic splicing frequency. Subsequent complementary genetic and structural analyses in yeast implicate these alleles in the stability of the spliceosome’s catalytic core. However, despite a clear effect on cryptic splicing, high-throughput mRNA sequencing of theseprp-8mutantC. elegansreveals that overall alternative splicing patterns are relatively unchanged. Our data suggest the spliceosome evolved intrinsic mechanisms to reduce the occurrence of cryptic splicing and that these mechanisms are distinct from those that impact alternative splicing.
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    Reply to Yang et al.: Multilayer network switching and behavior (2019)
    National Academy of Sciences
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    Publication Date: 2019-08-13
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    Propagation of pop ups in kirigami shells (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-08
    Description: Kirigami-inspired metamaterials are attracting increasing interest because of their ability to achieve extremely large strains and shape changes via out-of-plane buckling. While in flat kirigami sheets, the ligaments buckle simultaneously as Euler columns, leading to a continuous phase transition; here, we demonstrate that kirigami shells can also support discontinuous phase transitions. Specifically, we show via a combination of experiments, numerical simulations, and theoretical analysis that, in cylindrical kirigami shells, the snapping-induced curvature inversion of the initially bent ligaments results in a pop-up process that first localizes near an imperfection and then, as the deformation is increased, progressively spreads through the structure. Notably, we find that the width of the transition zone as well as the stress at which propagation of the instability is triggered can be controlled by carefully selecting the geometry of the cuts and the curvature of the shell. Our study significantly expands the ability of existing kirigami metamaterials and opens avenues for the design of the next generation of responsive surfaces as demonstrated by the design of a smart skin that significantly enhances the crawling efficiency of a simple linear actuator.
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    Electronic ISSN: 1091-6490
    Topics: Biology , Medicine , Natural Sciences in General
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    Programmable active kirigami metasheets with more freedom of actuation (2019)
    National Academy of Sciences
    Details
    Publication Date: 2019-12-16
    Description: Kirigami (cutting and/or folding) offers a promising strategy to reconfigure metamaterials. Conventionally, kirigami metamaterials are often composed of passive cut unit cells to be reconfigured under mechanical forces. The constituent stimuli-responsive materials in active kirigami metamaterials instead will enable potential mechanical properties and functionality, arising from the active control of cut unit cells. However, the planar features of hinges in conventional kirigami structures significantly constrain the degrees of freedom (DOFs) in both deformation and actuation of the cut units. To release both constraints, here, we demonstrate a universal design of implementing folds to reconstruct sole-cuts–based metamaterials. We show that the supplemented folds not only enrich the structural reconfiguration beyond sole cuts but also enable more DOFs in actuating the kirigami metasheets into 3 dimensions (3D) in response to environmental temperature. Utilizing the multi-DOF in deformation of unit cells, we demonstrate that planar metasheets with the same cut design can self-fold into programmable 3D kirigami metastructures with distinct mechanical properties. Last, we demonstrate potential applications of programmable kirigami machines and easy-turning soft robots.
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    Electronic ISSN: 1091-6490
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    Geographically divergent evolutionary and ecological legacies shape mammal biodiversity in the global tropics and subtropics (2019)
    National Academy of Sciences
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    Publication Date: 2019-12-16
    Description: Studies of the factors governing global patterns of biodiversity are key to predicting community responses to ongoing and future abiotic and biotic changes. Although most research has focused on present-day climate, a growing body of evidence indicates that modern ecological communities may be significantly shaped by paleoclimatic change and past anthropogenic factors. However, the generality of this pattern is unknown, as global analyses are lacking. Here we quantify the phylogenetic and functional trait structure of 515 tropical and subtropical large mammal communities and predict their structure from past and present climatic and anthropogenic factors. We find that the effects of Quaternary paleoclimatic change are strongest in the Afrotropics, with communities in the Indomalayan realm showing mixed effects of modern climate and paleoclimate. Malagasy communities are poorly predicted by any single factor, likely due to the atypical history of the island compared with continental regions. Neotropical communities are mainly codetermined by modern climate and prehistoric and historical human impacts. Overall, our results indicate that the factors governing tropical and subtropical mammalian biodiversity are complex, with the importance of past and present factors varying based on the divergent histories of the world’s biogeographic realms and their native biotas. Consideration of the evolutionary and ecological legacies of both the recent and ancient past are key to understanding the forces shaping global patterns of present-day biodiversity and its response to ongoing and future abiotic and biotic changes in the 21st century.
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    The impact of income, land, and wealth inequality on agricultural expansion in Latin America (2019)
    National Academy of Sciences
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    Publication Date: 2019-01-24
    Description: Agricultural expansion remains the most prominent proximate cause of tropical deforestation in Latin America, a region characterized by deforestation rates substantially above the world average and extremely high inequality. This paper deploys several multivariate statistical models to test whether different aspects of inequality, within a context of increasing agricultural productivity, promote agricultural expansion (Jevons paradox) or contraction (land-sparing) in 10 Latin American countries over 1990–2010. Here I show the existence of distinct patterns between the instantaneous and the overall (i.e., accounting for temporal lags) effect of increasing agricultural productivity, conditional on the degree of income, land, and wealth inequality. In a context of perfect equality, the instantaneous effect of increases in agricultural productivity is to promote agricultural expansion (Jevons paradox). When temporal lags are accounted for, agricultural productivity appears to be mainly land-sparing. Increases in the level of inequality, in all its forms, promote agricultural expansion, thus eroding the land-sparing effects of increasing productivity. The results also suggest that the instantaneous impact of inequality is larger than the overall effect (accounting for temporal lags) and that the effects of income inequality are stronger than those of land and wealth inequality, respectively. Reaping the benefits of increasing agricultural productivity, and achieving sustainable agricultural intensification in Latin America, requires policy interventions that specifically address inequality.
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    Protein stability engineering insights revealed by domain-wide comprehensive mutagenesis (2019)
    National Academy of Sciences
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    Publication Date: 2019-08-01
    Description: The accurate prediction of protein stability upon sequence mutation is an important but unsolved challenge in protein engineering. Large mutational datasets are required to train computational predictors, but traditional methods for collecting stability data are either low-throughput or measure protein stability indirectly. Here, we develop an automated method to generate thermodynamic stability data for nearly every single mutant in a small 56-residue protein. Analysis reveals that most single mutants have a neutral effect on stability, mutational sensitivity is largely governed by residue burial, and unexpectedly, hydrophobics are the best tolerated amino acid type. Correlating the output of various stability-prediction algorithms against our data shows that nearly all perform better on boundary and surface positions than for those in the core and are better at predicting large-to-small mutations than small-to-large ones. We show that the most stable variants in the single-mutant landscape are better identified using combinations of 2 prediction algorithms and including more algorithms can provide diminishing returns. In most cases, poor in silico predictions were tied to compositional differences between the data being analyzed and the datasets used to train the algorithm. Finally, we find that strategies to extract stabilities from high-throughput fitness data such as deep mutational scanning are promising and that data produced by these methods may be applicable toward training future stability-prediction tools.
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    Mode-of-action profiling reveals glutamine synthetase as a collateral metabolic vulnerability of M. tuberculosis to bedaquiline (2019)
    National Academy of Sciences
    Details
    Publication Date: 2019-09-09
    Description: Combination chemotherapy can increase treatment efficacy and suppress drug resistance. Knowledge of how to engineer rational, mechanism-based drug combinations, however, remains lacking. Although studies of drug activity have historically focused on the primary drug–target interaction, growing evidence has emphasized the importance of the subsequent consequences of this interaction. Bedaquiline (BDQ) is the first new drug for tuberculosis (TB) approved in more than 40 y, and a species-selective inhibitor of the Mycobacterium tuberculosis (Mtb) ATP synthase. Curiously, BDQ-mediated killing of Mtb lags significantly behind its inhibition of ATP synthase, indicating a mode of action more complex than the isolated reduction of ATP pools. Here, we report that BDQ-mediated inhibition of Mtb’s ATP synthase triggers a complex metabolic response indicative of a specific hierarchy of ATP-dependent reactions. We identify glutamine synthetase (GS) as an enzyme whose activity is most responsive to changes in ATP levels. Chemical supplementation with exogenous glutamine failed to affect BDQ’s antimycobacterial activity. However, further inhibition of Mtb’s GS synergized with and accelerated the onset of BDQ-mediated killing, identifying Mtb’s glutamine synthetase as a collateral, rather than directly antimycobacterial, metabolic vulnerability of BDQ. These findings reveal a previously unappreciated physiologic specificity of ATP and a facet of mode-of-action biology we term collateral vulnerability, knowledge of which has the potential to inform the development of rational, mechanism-based drug combinations.
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    Correction for Tang et al., Electronic-cigarette smoke induces lung adenocarcinoma and bladder urothelial hyperplasia in mice (2019)
    National Academy of Sciences
    Details
    Publication Date: 2019-10-28
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    Disease mortality in domesticated animals is predicted by host evolutionary relationships (2019)
    National Academy of Sciences
    Details
    Publication Date: 2019-03-29
    Description: Infectious diseases of domesticated animals impact human well-being via food insecurity, loss of livelihoods, and human infections. While much research has focused on parasites that infect single host species, most parasites of domesticated mammals infect multiple species. The impact of multihost parasites varies across hosts; some rarely result in death, whereas others are nearly always fatal. Despite their high ecological and societal costs, we currently lack theory for predicting the lethality of multihost parasites. Here, using a global dataset of 〉4,000 case-fatality rates for 65 infectious diseases (caused by microparasites and macroparasites) and 12 domesticated host species, we show that the average evolutionary distance from an infected host to other mammal host species is a strong predictor of disease-induced mortality. We find that as parasites infect species outside of their documented phylogenetic host range, they are more likely to result in lethal infections, with the odds of death doubling for each additional 10 million years of evolutionary distance. Our results for domesticated animal diseases reveal patterns in the evolution of highly lethal parasites that are difficult to observe in the wild and further suggest that the severity of infectious diseases may be predicted from evolutionary relationships among hosts.
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    A neural signature of pattern separation in the monkey hippocampus (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-22
    Description: The CA3 and dentate gyrus (DG) regions of the hippocampus are considered key for disambiguating sensory inputs from similar experiences in memory, a process termed pattern separation. The neural mechanisms underlying pattern separation, however, have been difficult to compare across species: rodents offer robust recording methods with less human-centric tasks, while humans provide complex behavior with less recording potential. To overcome these limitations, we trained monkeys to perform a visual pattern separation task similar to those used in humans while recording activity from single CA3/DG neurons. We find that, when animals discriminate recently seen novel images from similar (lure) images, behavior indicative of pattern separation, CA3/DG neurons respond to lure images more like novel than repeat images. Using a population of these neurons, we are able to classify novel, lure, and repeat images from each other using this pattern of firing rates. Notably, one subpopulation of these neurons is more responsible for distinguishing lures and repeats—the key discrimination indicative of pattern separation.
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