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  • National Academy of Sciences  (181,892)
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  • 1
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    The strength of the Earth's magnetic field from Pre-Pottery to Pottery Neolithic, Jordan (2023)
    National Academy of Sciences
    Details
    Publication Date: 2023-10-26
    Description: Constraining secular variation of the Earth's magnetic field strength in the past is fundamental to understanding short-term processes of the geodynamo. Such records also constitute a powerful and independent dating tool for archaeological sites and geological formations. In this study, we present 11 robust archaeointensity results from Pre-Pottery to Pottery Neolithic Jordan that are based on both clay and flint (chert) artifacts. Two of these results constitute the oldest archaeointensity data for the entire Levant, ancient Egypt, Turkey, and Mesopotamia, extending the archaeomagnetic reference curve for the Holocene. Virtual Axial Dipole Moments (VADMs) show that the Earth's magnetic field in the Southern Levant was weak (about two-thirds the present field) at around 7600 BCE, recovering its strength to greater than the present field around 7000 BCE, and gradually weakening again around 5200 BCE. In addition, successful results obtained from burnt flint demonstrate the potential of this very common, and yet rarely used, material in archaeomagnetic research, in particular for prehistoric periods from the first use of fire to the invention of pottery.
    Description: Published
    Description: e2100995118
    Description: 1A. Geomagnetismo e Paleomagnetismo
    Description: JCR Journal
    Keywords: Jordan ; Neolithic ; Pre-Pottery Neolithic ; archaeointensity
    Repository Name: Istituto Nazionale di Geofisica e Vulcanologia (INGV)
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  • 2
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    Microbial functional diversity across biogeochemical provinces in the central Pacific Ocean (2023)
    National Academy of Sciences
    Details
    Publication Date: 2023-03-08
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Saunders, J. K., McIlvin, M. R., Dupont, C. L., Kaul, D., Moran, D. M., Horner, T., Laperriere, S. M., Webb, E. A., Bosak, T., Santoro, A. E., & Saito, M. A. Microbial functional diversity across biogeochemical provinces in the central Pacific Ocean. Proceedings of the National Academy of Sciences of the United States of America, 119(37),(2022): e2200014119, https://doi.org/10.1073/pnas.2200014119.
    Description: Enzymes catalyze key reactions within Earth’s life-sustaining biogeochemical cycles. Here, we use metaproteomics to examine the enzymatic capabilities of the microbial community (0.2 to 3 µm) along a 5,000-km-long, 1-km-deep transect in the central Pacific Ocean. Eighty-five percent of total protein abundance was of bacterial origin, with Archaea contributing 1.6%. Over 2,000 functional KEGG Ontology (KO) groups were identified, yet only 25 KO groups contributed over half of the protein abundance, simultaneously indicating abundant key functions and a long tail of diverse functions. Vertical attenuation of individual proteins displayed stratification of nutrient transport, carbon utilization, and environmental stress. The microbial community also varied along horizontal scales, shaped by environmental features specific to the oligotrophic North Pacific Subtropical Gyre, the oxygen-depleted Eastern Tropical North Pacific, and nutrient-rich equatorial upwelling. Some of the most abundant proteins were associated with nitrification and C1 metabolisms, with observed interactions between these pathways. The oxidoreductases nitrite oxidoreductase (NxrAB), nitrite reductase (NirK), ammonia monooxygenase (AmoABC), manganese oxidase (MnxG), formate dehydrogenase (FdoGH and FDH), and carbon monoxide dehydrogenase (CoxLM) displayed distributions indicative of biogeochemical status such as oxidative or nutritional stress, with the potential to be more sensitive than chemical sensors. Enzymes that mediate transformations of atmospheric gases like CO, CO2, NO, methanethiol, and methylamines were most abundant in the upwelling region. We identified hot spots of biochemical transformation in the central Pacific Ocean, highlighted previously understudied metabolic pathways in the environment, and provided rich empirical data for biogeochemical models critical for forecasting ecosystem response to climate change.
    Description: Funding for this research was provided by the Gordon and Betty Moore Foundation (grants 3782 and 8453), the US NSF (NSF grants OCE-1924554, 2123055, 2125063, 2048774, and 2026933), the Center for Chemical Currencies on a Microbial Planet (NSF grant OCE-2019589), and the US NIH General Medicine (grant GM135709-01A1). J.K.S. was supported by a NASA Postdoctoral Program Fellowship with the NASA Astrobiology Program, administered by Universities Space Research Association under contract with NASA. A.E.S. was supported by the Sloan Foundation, the Simons Foundation, and NSF grant OCE-1437310. A portion of this research used resources at the US Department of Energy JGI sponsored by the Office of Biological and Environmental Research and operated under contract DE-AC02-05CH11231 (JGI). C.L.D. and D.K. were supported by NSF grants OCE-1558453 and OCE-2049299. T.H. was supported by NSF grant OCE-2023456.
    Keywords: Marine microbial ecology ; Metaproteomics ; Mesopelagic ; Nitrification ; Methylotrophy
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  • 3
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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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  • 4
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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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  • 5
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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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  • 6
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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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  • 7
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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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  • 8
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    Phosphonate production by marine microbes: exploring new sources and potential function (2022)
    National Academy of Sciences
    Details
    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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  • 9
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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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  • 10
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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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  • 11
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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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  • 12
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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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  • 13
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    Diverse methylotrophic methanogenic archaea cause high methane emissions from seagrass meadows (2022)
    National Academy of Sciences
    Details
    Publication Date: 2023-03-08
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Schorn, S., Ahmerkamp, S., Bullock, E., Weber, M., Lott, C., Liebeke, M., Lavik, G., Kuypers, M. M. M., Graf, J. S., & Milucka, J. Diverse methylotrophic methanogenic archaea cause high methane emissions from seagrass meadows. Proceedings of the National Academy of Sciences of the United States of America, 119(9), (2022): e2106628119, https://doi.org/10.1073/pnas.2106628119.
    Description: Marine coastlines colonized by seagrasses are a net source of methane to the atmosphere. However, methane emissions from these environments are still poorly constrained, and the underlying processes and responsible microorganisms remain largely unknown. Here, we investigated methane turnover in seagrass meadows of Posidonia oceanica in the Mediterranean Sea. The underlying sediments exhibited median net fluxes of methane into the water column of ca. 106 µmol CH4 ⋅ m−2 ⋅ d−1. Our data show that this methane production was sustained by methylated compounds produced by the plant, rather than by fermentation of buried organic carbon. Interestingly, methane production was maintained long after the living plant died off, likely due to the persistence of methylated compounds, such as choline, betaines, and dimethylsulfoniopropionate, in detached plant leaves and rhizomes. We recovered multiple mcrA gene sequences, encoding for methyl-coenzyme M reductase (Mcr), the key methanogenic enzyme, from the seagrass sediments. Most retrieved mcrA gene sequences were affiliated with a clade of divergent Mcr and belonged to the uncultured Candidatus Helarchaeota of the Asgard superphylum, suggesting a possible involvement of these divergent Mcr in methane metabolism. Taken together, our findings identify the mechanisms controlling methane emissions from these important blue carbon ecosystems.
    Description: This project was funded by theMax Planck Society.
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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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  • 17
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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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  • 18
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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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    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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  • 21
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    Human arrival and landscape dynamics in the northern Bahamas (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 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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    Thermodynamic feasibility of shipboard conversion of marine plastics to blue diesel for self-powered ocean cleanup (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 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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    Electrochemical implications of modulating the solvation shell around redox active organic species in aqueous organic redox flow batteries (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Organic and organometallic reactants in aqueous electrolytes, being composed of earth-abundant elements, are promising redox active candidates for cost-effective organic redox flow batteries (ORFBs). Various compounds of ferrocene and methyl viologen have been examined as promising redox actives for this application. Herein, we examined the influence of the electrolyte pH and the salt anion on model redox active organic cations, bis((3-trimethylammonio) propyl)- ferrocene dichloride (BTMAP-Fc) and bis(3-trimethylammonio) propyl viologen tetrachloride (BTMAP-Vi), which have exhibited excellent cycling stability and capacity retention at ≥1.00 M concentration [E. S. Beh, et al. ACS Energy Lett. 2, 639–644 (2017)]. We examined the solvation shell around BTMAP-Fc and BTMAP-Vi at acidic and neutral pH with SO42-, Cl−, and CH3SO3− counterions and elucidated their impact on cation diffusion coefficient, first electron transfer rate constant, and thereby the electrochemical Thiele modulus. The electrochemical Thiele modulus was found to be exponentially correlated with the solvent reorganizational energy (λ) in both neutral and acidic pH. Thus, λ is proposed as a universal descriptor and selection criteria for organic redox flow battery electrolyte compositions. In the specific case of the BTMAP-Fc/BTMAP-Vi ORFB, low pH electrolytes with methanesulfonate or chloride counterions were identified as offering the best balance of transport and kinetic requirements.
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    An in vivo selection-derived d-peptide for engineering erythrocyte-binding antigens that promote immune tolerance (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: When displayed on erythrocytes, peptides and proteins can drive antigen-specific immune tolerance. Here, we investigated a straightforward approach based on erythrocyte binding to promote antigen-specific tolerance to both peptides and proteins. We first identified a robust erythrocyte-binding ligand. A pool of one million fully d-chiral peptides was injected into mice, blood cells were isolated, and ligands enriched on these cells were identified using nano-liquid chromatography–tandem mass spectrometry. One round of selection yielded a murine erythrocyte-binding ligand with an 80 nM apparent dissociation constant, Kd. We modified an 83-kDa bacterial protein and a peptide antigen derived from ovalbumin (OVA) with the identified erythrocyte-binding ligand. An administration of the engineered bacterial protein led to decreased protein-specific antibodies in mice. Similarly, mice given the engineered OVA-derived peptide had decreased inflammatory anti-OVA CD8+ T cell responses. These findings suggest that our tolerance-induction strategy is applicable to both peptide and protein antigens and that our in vivo selection strategy can be used for de novo discovery of robust erythrocyte-binding ligands.
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    The trisulfur radical ion S3•− controls platinum transport by hydrothermal fluids (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Platinum group elements (PGE) are considered to be very poorly soluble in aqueous fluids in most natural hydrothermal–magmatic contexts and industrial processes. Here, we combined in situ X-ray absorption spectroscopy and solubility experiments with atomistic and thermodynamic simulations to demonstrate that the trisulfur radical ion S3•− forms very stable and soluble complexes with both PtII and PtIV in sulfur-bearing aqueous solution at elevated temperatures (∼300 °C). These Pt-bearing species enable (re)mobilization, transfer, and focused precipitation of platinum up to 10,000 times more efficiently than any other common inorganic ligand, such as hydroxide, chloride, sulfate, or sulfide. Our results imply a far more important contribution of sulfur-bearing hydrothermal fluids to PGE transfer and accumulation in the Earth’s crust than believed previously. This discovery challenges traditional models of PGE economic concentration from silicate and sulfide melts and provides new possibilities for resource prospecting in hydrothermal shallow crust settings. The exceptionally high capacity of the S3•− ion to bind platinum may also offer new routes for PGE selective extraction from ore and hydrothermal synthesis of noble metal nanomaterials.
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    Structural insights into a novel family of integral membrane siderophore reductases (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Gram-negative bacteria take up the essential ion Fe3+ as ferric-siderophore complexes through their outer membrane using TonB-dependent transporters. However, the subsequent route through the inner membrane differs across many bacterial species and siderophore chemistries and is not understood in detail. Here, we report the crystal structure of the inner membrane protein FoxB (from Pseudomonas aeruginosa) that is involved in Fe-siderophore uptake. The structure revealed a fold with two tightly bound heme molecules. In combination with in vitro reduction assays and in vivo iron uptake studies, these results establish FoxB as an inner membrane reductase involved in the release of iron from ferrioxamine during Fe-siderophore uptake.
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    Counting equilibria of large complex systems by instability index (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: We consider a nonlinear autonomous system of N≫1 degrees of freedom randomly coupled by both relaxational (“gradient”) and nonrelaxational (“solenoidal”) random interactions. We show that with increased interaction strength, such systems generically undergo an abrupt transition from a trivial phase portrait with a single stable equilibrium into a topologically nontrivial regime of “absolute instability” where equilibria are on average exponentially abundant, but typically, all of them are unstable, unless the dynamics is purely gradient. When interactions increase even further, the stable equilibria eventually become on average exponentially abundant unless the interaction is purely solenoidal. We further calculate the mean proportion of equilibria that have a fixed fraction of unstable directions.
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    On randomly changing conformity bias in cultural transmission (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Humans and nonhuman animals display conformist as well as anticonformist biases in cultural transmission. Whereas many previous mathematical models have incorporated constant conformity coefficients, empirical research suggests that the extent of (anti)conformity in populations can change over time. We incorporate stochastic time-varying conformity coefficients into a widely used conformity model, which assumes a fixed number n of “role models” sampled by each individual. We also allow the number of role models to vary over time (nt). Under anticonformity, nonconvergence can occur in deterministic and stochastic models with different parameter values. Even if strong anticonformity may occur, if conformity or random copying (i.e., neither conformity nor anticonformity) is expected, there is convergence to one of the three equilibria seen in previous deterministic models of conformity. Moreover, this result is robust to stochastic variation in nt. However, dynamic properties of these equilibria may be different from those in deterministic models. For example, with random conformity coefficients, all equilibria can be stochastically locally stable simultaneously. Finally, we study the effect of randomly changing weak selection. Allowing the level of conformity, the number of role models, and selection to vary stochastically may produce a more realistic representation of the wide range of group-level properties that can emerge under (anti)conformist biases. This promises to make interpretation of the effect of conformity on differences between populations, for example those connected by migration, rather difficult. Future research incorporating finite population sizes and migration would contribute added realism to these models.
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    Structure of Usutu virus SAAR-1776 displays fusion loop asymmetry (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Usutu virus (USUV) is an emerging arbovirus in Europe that has been increasingly identified in asymptomatic humans and donated blood samples and is a cause of increased incidents of neuroinvasive human disease. Treatment or prevention options for USUV disease are currently nonexistent, the result of a lack of understanding of the fundamental elements of USUV pathogenesis. Here, we report two structures of the mature USUV virus, determined at a resolution of 2.4 Å, using single-particle cryogenic electron microscopy. Mature USUV is an icosahedral shell of 180 copies of envelope (E) and membrane (M) proteins arranged in the classic herringbone pattern. However, unlike previous reports of flavivirus structures, we observe virus subpopulations and differences in the fusion loop disulfide bond. Presence of a second, unique E glycosylation site could elucidate host interactions, contributing to the broad USUV tissue tropism. The structures provide a basis for exploring USUV interactions with glycosaminoglycans and lectins, the role of the RGD motif as a receptor, and the inability of West Nile virus therapeutic antibody E16 to neutralize the mature USUV strain SAAR-1776. Finally, we identify three lipid binding sites and predict key residues that likely participate in virus stability and flexibility during membrane fusion. Our findings provide a framework for the development of USUV therapeutics and expand the current knowledge base of flavivirus biology.
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    A dynamic electrically driven soft valve for control of soft hydraulic actuators (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Regulation systems for fluid-driven soft robots predominantly consist of inflexible and bulky components. These rigid structures considerably limit the adaptability and mobility of these robots. Soft valves in various forms for fluidic actuators have been developed, primarily fluidically or electrically driven. However, fluidic soft valves require external pressure sources that limit robot locomotion. State-of-the-art electrostatic valves are unable to modulate pressure beyond 3.5 kPa with a sufficient flow rate (〉6 mL⋅min−1). In this work, we present an electrically powered soft valve for hydraulic actuators with mesoscale channels based on a different class of ultrahigh-power density dynamic dielectric elastomer actuators. The dynamic dielectric elastomer actuators (DEAs) are actuated at 500 Hz or above. These DEAs generate 300% higher blocked force compared with the dynamic DEAs in previous works and their loaded power density reaches 290 W⋅kg−1 at operating conditions. The soft valves are developed with compact (7 mm tall) and lightweight (0.35 g) dynamic DEAs, and they allow effective control of up to 51 kPa of pressure and a 40 mL⋅min−1 flow rate with a response time less than 0.1 s. The valves can also tune flow rates based on their driving voltages. Using the DEA soft valves, we demonstrate control of hydraulic actuators of different volumes and achieve independent control of multiple actuators powered by a single pressure source. This compact and lightweight DEA valve is capable of unprecedented electrical control of hydraulic actuators, showing the potential for future onboard motion control of soft fluid-driven robots.
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    Metapopulation capacity determines food chain length in fragmented landscapes (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Metapopulation capacity provides an analytic tool to quantify the impact of landscape configuration on metapopulation persistence, which has proven powerful in biological conservation. Yet surprisingly few efforts have been made to apply this approach to multispecies systems. Here, we extend metapopulation capacity theory to predict the persistence of trophically interacting species. Our results demonstrate that metapopulation capacity could be used to predict the persistence of trophic systems such as prey–predator pairs and food chains in fragmented landscapes. In particular, we derive explicit predictions for food chain length as a function of metapopulation capacity, top-down control, and population dynamical parameters. Under certain assumptions, we show that the fraction of empty patches for the basal species provides a useful indicator to predict the length of food chains that a fragmented landscape can support and confirm this prediction for a host–parasitoid interaction. We further show that the impact of habitat changes on biodiversity can be predicted from changes in metapopulation capacity or approximately by changes in the fraction of empty patches. Our study provides an important step toward a spatially explicit theory of trophic metacommunities and a useful tool for predicting their responses to habitat changes.
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    Topological braiding and virtual particles on the cell membrane (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Braiding of topological structures in complex matter fields provides a robust framework for encoding and processing information, and it has been extensively studied in the context of topological quantum computation. In living systems, topological defects are crucial for the localization and organization of biochemical signaling waves, but their braiding dynamics remain unexplored. Here, we show that the spiral wave cores, which organize the Rho-GTP protein signaling dynamics and force generation on the membrane of starfish egg cells, undergo spontaneous braiding dynamics. Experimentally measured world line braiding exponents and topological entropy correlate with cellular activity and agree with predictions from a generic field theory. Our analysis further reveals the creation and annihilation of virtual quasi-particle excitations during defect scattering events, suggesting phenomenological parallels between quantum and living matter.
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    Synergistic dispersal of plant pathogen spores by jumping-droplet condensation and wind (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Plant pathogens are responsible for the annual yield loss of crops worldwide and pose a significant threat to global food security. A necessary prelude to many plant disease epidemics is the short-range dispersal of spores, which may generate several disease foci within a field. New information is needed on the mechanisms of plant pathogen spread within and among susceptible plants. Here, we show that self-propelled jumping dew droplets, working synergistically with low wind flow, can propel spores of a fungal plant pathogen (wheat leaf rust) beyond the quiescent boundary layer and disperse them onto neighboring leaves downwind. An array of horizontal water-sensitive papers was used to mimic healthy wheat leaves and showed that up to 25 spores/h may be deposited on a single leaf downwind of the infected leaf during a single dew cycle. These findings reveal that a single dew cycle can disperse copious numbers of fungal spores to other wheat plants, even in the absence of rain splash or strong gusts of wind.
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    Replication across space and time must be weak in the social and environmental sciences (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Replicability takes on special meaning when researching phenomena that are embedded in space and time, including phenomena distributed on the surface and near surface of the Earth. Two principles, spatial dependence and spatial heterogeneity, are generally characteristic of such phenomena. Various practices have evolved in dealing with spatial heterogeneity, including the use of place-based models. We review the rapidly emerging applications of artificial intelligence to phenomena distributed in space and time and speculate on how the principle of spatial heterogeneity might be addressed. We introduce a concept of weak replicability and discuss possible approaches to its measurement.
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    Stephen T. Warren: Human geneticist who advanced understanding of mutational mechanisms and developmental disorders (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
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    Mitochondrial fatty acid utilization increases chromatin oxidative stress in cardiomyocytes (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: The inability of adult mammalian cardiomyocytes to proliferate underpins the development of heart failure following myocardial injury. Although the newborn mammalian heart can spontaneously regenerate for a short period of time after birth, this ability is lost within the first week after birth in mice, partly due to increased mitochondrial reactive oxygen species (ROS) production which results in oxidative DNA damage and activation of DNA damage response. This increase in ROS levels coincides with a postnatal switch from anaerobic glycolysis to fatty acid (FA) oxidation by cardiac mitochondria. However, to date, a direct link between mitochondrial substrate utilization and oxidative DNA damage is lacking. Here, we generated ROS-sensitive fluorescent sensors targeted to different subnuclear compartments (chromatin, heterochromatin, telomeres, and nuclear lamin) in neonatal rat ventricular cardiomyocytes, which allowed us to determine the spatial localization of ROS in cardiomyocyte nuclei upon manipulation of mitochondrial respiration. Our results demonstrate that FA utilization by the mitochondria induces a significant increase in ROS detection at the chromatin level compared to other nuclear compartments. These results indicate that mitochondrial metabolic perturbations directly alter the nuclear redox status and that the chromatin appears to be particularly sensitive to the prooxidant effect of FA utilization by the mitochondria.
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    Two-dimensional electronic–vibrational sum frequency spectroscopy for interactions of electronic and nuclear motions at interfaces (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Interactions of electronic and vibrational degrees of freedom are essential for understanding excited-states relaxation pathways of molecular systems at interfaces and surfaces. Here, we present the development of interface-specific two-dimensional electronic–vibrational sum frequency generation (2D-EVSFG) spectroscopy for electronic–vibrational couplings for excited states at interfaces and surfaces. We demonstrate this 2D-EVSFG technique by investigating photoexcited interface-active (E)-4-((4-(dihexylamino) phenyl)diazinyl)-1-methylpyridin-1- lum (AP3) molecules at the air–water interface as an example. Our 2D-EVSFG experiments show strong vibronic couplings of interfacial AP3 molecules upon photoexcitation and subsequent relaxation of a locally excited (LE) state. Time-dependent 2D-EVSFG experiments indicate that the relaxation of the LE state, S2, is strongly coupled with two high-frequency modes of 1,529.1 and 1,568.1 cm−1. Quantum chemistry calculations further verify that the strong vibronic couplings of the two vibrations promote the transition from the S2 state to the lower excited state S1. We believe that this development of 2D-EVSFG opens up an avenue of understanding excited-state dynamics related to interfaces and surfaces.
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    Inactivation of Hedgehog signal transduction in adult astrocytes results in region-specific blood–brain barrier defects (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: In this study, we use molecular genetic approaches to clarify the role of the Hedgehog (Hh) pathway in regulating the blood–brain/spinal cord barrier (BBB) in the adult mouse central nervous system (CNS). Our work confirms and extends prior studies to demonstrate that astrocytes are the predominant cell type in the adult CNS that transduce Hh signaling, revealed by the expression of Gli1, a target gene of the canonical pathway that is activated in cells receiving Hh, and other key pathway transduction components. Gli1+ (Hh-responsive) astrocytes are distributed in specific regions of the CNS parenchyma, including layers 4/5/6 of the neocortex, hypothalamus, thalamus, and spinal cord, among others. Notably, although BBB properties in endothelial cells are normally regulated by both paracellular and transcellular mechanisms, conditional inactivation of Hh signaling in astrocytes results in transient, region-specific BBB defects that affect transcytosis but not paracellular diffusion. These findings stand in contrast to prior studies that implicated astrocytes as a source of Sonic hedgehog that limited extravasation via both mechanisms [J. I. Alvarez et al., Science 334, 1727–1731 (2011)]. Furthermore, using three distinct Cre driver lines as well as pharmacological approaches to inactivate Hh-pathway transduction globally in CNS astrocytes, we find that these specific BBB defects are only detected in the rostral hypothalamus and spinal cord but not the cortex or other regions where Gli1+ astrocytes are found. Together, our data show that Gli1+ Hh-responsive astrocytes have regionally distinct molecular and functional properties and that the pathway is required to maintain BBB properties in specific regions of the adult mammalian CNS.
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    Droplet tilings for rapid exploration of spatially constrained many-body systems (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Geometry in materials is a key concept which can determine material behavior in ordering, frustration, and fragmentation. More specifically, the behavior of interacting degrees of freedom subject to arbitrary geometric constraints has the potential to be used for engineering materials with exotic phase behavior. While advances in lithography have allowed for an experimental exploration of geometry on ordering that has no precedent in nature, many of these methods are low throughput or the underlying dynamics remain difficult to observe directly. Here, we introduce an experimental system that enables the study of interacting many-body dynamics by exploiting the physics of multidroplet evaporation subject to two-dimensional spatial constraints. We find that a high-energy initial state of this system settles into frustrated, metastable states with relaxation on two timescales. We understand this process using a minimal dynamical model that simulates the overdamped dynamics of motile droplets by identifying the force exerted on a given droplet as being proportional to the two-dimensional vapor gradients established by its neighbors. Finally, we demonstrate the flexibility of this platform by presenting experimental realizations of droplet−lattice systems representing different spin degrees of freedom and lattice geometries. Our platform enables a rapid and low-cost means to directly visualize dynamics associated with complex many-body systems interacting via long-range interactions. More generally, this platform opens up the rich design space between geometry and interactions for rapid exploration with minimal resources.
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    Assisted assembly of bacteriophage T7 core components for genome translocation across the bacterial envelope (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: In most bacteriophages, genome transport across bacterial envelopes is carried out by the tail machinery. In viruses of the Podoviridae family, in which the tail is not long enough to traverse the bacterial wall, it has been postulated that viral core proteins assembled inside the viral head are translocated and reassembled into a tube within the periplasm that extends the tail channel. Bacteriophage T7 infects Escherichia coli, and despite extensive studies, the precise mechanism by which its genome is translocated remains unknown. Using cryo-electron microscopy, we have resolved the structure of two different assemblies of the T7 DNA translocation complex composed of the core proteins gp15 and gp16. Gp15 alone forms a partially folded hexamer, which is further assembled upon interaction with gp16 into a tubular structure, forming a channel that could allow DNA passage. The structure of the gp15–gp16 complex also shows the location within gp16 of a canonical transglycosylase motif involved in the degradation of the bacterial peptidoglycan layer. This complex docks well in the tail extension structure found in the periplasm of T7-infected bacteria and matches the sixfold symmetry of the phage tail. In such cases, gp15 and gp16 that are initially present in the T7 capsid eightfold-symmetric core would change their oligomeric state upon reassembly in the periplasm. Altogether, these results allow us to propose a model for the assembly of the core translocation complex in the periplasm, which furthers understanding of the molecular mechanism involved in the release of T7 viral DNA into the bacterial cytoplasm.
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    A recombinant herpes virus expressing influenza hemagglutinin confers protection and induces antibody-dependent cellular cytotoxicity (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Despite widespread yearly vaccination, influenza leads to significant morbidity and mortality across the globe. To make a more broadly protective influenza vaccine, it may be necessary to elicit antibodies that can activate effector functions in immune cells, such as antibody-dependent cellular cytotoxicity (ADCC). There is growing evidence supporting the necessity for ADCC in protection against influenza and herpes simplex virus (HSV), among other infectious diseases. An HSV-2 strain lacking the essential glycoprotein D (gD), was used to create ΔgD-2, which is a highly protective vaccine against lethal HSV-1 and HSV-2 infection in mice. It also elicits high levels of IgG2c antibodies that bind FcγRIV, a receptor that activates ADCC. To make an ADCC-eliciting influenza vaccine, we cloned the hemagglutinin (HA) gene from an H1N1 influenza A strain into the ΔgD-2 HSV vector. Vaccination with ΔgD-2::HAPR8 was protective against homologous influenza challenge and elicited an antibody response against HA that inhibits hemagglutination (HAI+), is predominantly IgG2c, strongly activates FcγRIV, and protects against influenza challenge following passive immunization of naïve mice. Prior exposure of mice to HSV-1, HSV-2, or a replication-defective HSV-2 vaccine (dl5-29) does not reduce protection against influenza by ΔgD-2::HAPR8. This vaccine also continues to elicit protection against both HSV-1 and HSV-2, including high levels of IgG2c antibodies against HSV-2. Mice lacking the interferon-α/β receptor and mice lacking the interferon-γ receptor were also protected against influenza challenge by ΔgD-2::HAPR8. Our results suggest that ΔgD-2 can be used as a vaccine vector against other pathogens, while also eliciting protective anti-HSV immunity.
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    Metabolism drives demography in an experimental field test (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Metabolism should drive demography by determining the rates of both biological work and resource demand. Long-standing “rules” for how metabolism should covary with demography permeate biology, from predicting the impacts of climate change to managing fisheries. Evidence for these rules is almost exclusively indirect and in the form of among-species comparisons, while direct evidence is exceptionally rare. In a manipulative field experiment on a sessile marine invertebrate, we created experimental populations that varied in population size (density) and metabolic rate, but not body size. We then tested key theoretical predictions regarding relationships between metabolism and demography by parameterizing population models with lifetime performance data from our field experiment. We found that populations with higher metabolisms had greater intrinsic rates of increase and lower carrying capacities, in qualitative accordance with classic theory. We also found important departures from theory—in particular, carrying capacity declined less steeply than predicted, such that energy use at equilibrium increased with metabolic rate, violating the long-standing axiom of energy equivalence. Theory holds that energy equivalence emerges because resource supply is assumed to be independent of metabolic rate. We find this assumption to be violated under real-world conditions, with potentially far-reaching consequences for the management of biological systems.
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    Regulation of metamorphosis in neopteran insects is conserved in the paleopteran Cloeon dipterum (Ephemeroptera) (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: In the Paleozoic era, more than 400 Ma, a number of insect groups continued molting after forming functional wings. Today, however, flying insects stop molting after metamorphosis when they become fully winged. The only exception is the mayflies (Paleoptera, Ephemeroptera), which molt in the subimago, a flying stage between the nymph and the adult. However, the identity and homology of the subimago still is underexplored. Debate remains regarding whether this stage represents a modified nymph, an adult, or a pupa like that of butterflies. Another relevant question is why mayflies have the subimago stage despite the risk of molting fragile membranous wings. These questions have intrigued numerous authors, but nonetheless, clear answers have not yet been found. By combining morphological studies, hormonal treatments, and molecular analysis in the mayfly Cloeon dipterum, we found answers to these old questions. We observed that treatment with a juvenile hormone analog in the last nymphal instar stimulated the expression of the Kr-h1 gene and reduced that of E93, which suppress and trigger metamorphosis, respectively. The regulation of metamorphosis thus follows the MEKRE93 pathway, as in neopteran insects. Moreover, the treatment prevented the formation of the subimago. These findings suggest that the subimago must be considered an instar of the adult mayfly. We also observed that the forelegs dramatically grow between the last nymphal instar, the subimago, and the adult. This necessary growth spread over the last two stages could explain, at least in part, the adaptive sense of the subimago.
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    Correction for Kim et al., The mechanics and dynamics of cancer cells sensing noisy 3D contact guidance (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
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    Pro-inflammatory T helper 17 directly harms oligodendrocytes in neuroinflammation (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: T helper (Th)17 cells are considered to contribute to inflammatory mechanisms in diseases such as multiple sclerosis (MS). However, the discussion persists regarding their true role in patients. Here, we visualized central nervous system (CNS) inflammatory processes in models of MS live in vivo and in MS brains and discovered that CNS-infiltrating Th17 cells form prolonged stable contact with oligodendrocytes. Strikingly, compared to Th2 cells, direct contact with Th17 worsened experimental demyelination, caused damage to human oligodendrocyte processes, and increased cell death. Importantly, we found that in comparison to Th2 cells, both human and murine Th17 cells express higher levels of the integrin CD29, which is linked to glutamate release pathways. Of note, contact of human Th17 cells with oligodendrocytes triggered release of glutamate, which induced cell stress and changes in biosynthesis of cholesterol and lipids, as revealed by single-cell RNA-sequencing analysis. Finally, exposure to glutamate decreased myelination, whereas blockade of CD29 preserved oligodendrocyte processes from Th17-mediated injury. Our data provide evidence for the direct and deleterious attack of Th17 cells on the myelin compartment and show the potential for therapeutic opportunities in MS.
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    Oculo-retinal dynamics can explain the perception of minimal recognizable configurations (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Natural vision is a dynamic and continuous process. Under natural conditions, visual object recognition typically involves continuous interactions between ocular motion and visual contrasts, resulting in dynamic retinal activations. In order to identify the dynamic variables that participate in this process and are relevant for image recognition, we used a set of images that are just above and below the human recognition threshold and whose recognition typically requires 〉2 s of viewing. We recorded eye movements of participants while attempting to recognize these images within trials lasting 3 s. We then assessed the activation dynamics of retinal ganglion cells resulting from ocular dynamics using a computational model. We found that while the saccadic rate was similar between recognized and unrecognized trials, the fixational ocular speed was significantly larger for unrecognized trials. Interestingly, however, retinal activation level was significantly lower during these unrecognized trials. We used retinal activation patterns and oculomotor parameters of each fixation to train a binary classifier, classifying recognized from unrecognized trials. Only retinal activation patterns could predict recognition, reaching 80% correct classifications on the fourth fixation (on average, ∼2.5 s from trial onset). We thus conclude that the information that is relevant for visual perception is embedded in the dynamic interactions between the oculomotor sequence and the image. Hence, our results suggest that ocular dynamics play an important role in recognition and that understanding the dynamics of retinal activation is crucial for understanding natural vision.
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    Cryo-EM structures of Escherichia coli cytochrome bo3 reveal bound phospholipids and ubiquinone-8 in a dynamic substrate binding site (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Two independent structures of the proton-pumping, respiratory cytochrome bo3 ubiquinol oxidase (cyt bo3) have been determined by cryogenic electron microscopy (cryo-EM) in styrene–maleic acid (SMA) copolymer nanodiscs and in membrane scaffold protein (MSP) nanodiscs to 2.55- and 2.19-Å resolution, respectively. The structures include the metal redox centers (heme b, heme o3, and CuB), the redox-active cross-linked histidine–tyrosine cofactor, and the internal water molecules in the proton-conducting D channel. Each structure also contains one equivalent of ubiquinone-8 (UQ8) in the substrate binding site as well as several phospholipid molecules. The isoprene side chain of UQ8 is clamped within a hydrophobic groove in subunit I by transmembrane helix TM0, which is only present in quinol oxidases and not in the closely related cytochrome c oxidases. Both structures show carbonyl O1 of the UQ8 headgroup hydrogen bonded to D75I and R71I. In both structures, residue H98I occupies two conformations. In conformation 1, H98I forms a hydrogen bond with carbonyl O4 of the UQ8 headgroup, but in conformation 2, the imidazole side chain of H98I has flipped to form a hydrogen bond with E14I at the N-terminal end of TM0. We propose that H98I dynamics facilitate proton transfer from ubiquinol to the periplasmic aqueous phase during oxidation of the substrate. Computational studies show that TM0 creates a channel, allowing access of water to the ubiquinol headgroup and to H98I.
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    Wnt signaling recruits KIF2A to the spindle to ensure chromosome congression and alignment during mitosis (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Canonical Wnt signaling plays critical roles in development and tissue renewal by regulating β-catenin target genes. Recent evidence showed that β-catenin–independent Wnt signaling is also required for faithful execution of mitosis. However, the targets and specific functions of mitotic Wnt signaling still remain uncharacterized. Using phosphoproteomics, we identified that Wnt signaling regulates the microtubule depolymerase KIF2A during mitosis. We found that Dishevelled recruits KIF2A via its N-terminal and motor domains, which is further promoted upon LRP6 signalosome formation during cell division. We show that Wnt signaling modulates KIF2A interaction with PLK1, which is critical for KIF2A localization at the spindle. Accordingly, inhibition of basal Wnt signaling leads to chromosome misalignment in somatic cells and pluripotent stem cells. We propose that Wnt signaling monitors KIF2A activity at the spindle poles during mitosis to ensure timely chromosome alignment. Our findings highlight a function of Wnt signaling during cell division, which could have important implications for genome maintenance, notably in stem cells.
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    Dynamic localization of a helper NLR at the plant–pathogen interface underpins pathogen recognition (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Plants employ sensor–helper pairs of NLR immune receptors to recognize pathogen effectors and activate immune responses. Yet, the subcellular localization of NLRs pre- and postactivation during pathogen infection remains poorly understood. Here, we show that NRC4, from the “NRC” solanaceous helper NLR family, undergoes dynamic changes in subcellular localization by shuttling to and from the plant–pathogen haustorium interface established during infection by the Irish potato famine pathogen Phytophthora infestans. Specifically, prior to activation, NRC4 accumulates at the extrahaustorial membrane (EHM), presumably to mediate response to perihaustorial effectors that are recognized by NRC4-dependent sensor NLRs. However, not all NLRs accumulate at the EHM, as the closely related helper NRC2 and the distantly related ZAR1 did not accumulate at the EHM. NRC4 required an intact N-terminal coiled-coil domain to accumulate at the EHM, whereas the functionally conserved MADA motif implicated in cell death activation and membrane insertion was dispensable for this process. Strikingly, a constitutively autoactive NRC4 mutant did not accumulate at the EHM and showed punctate distribution that mainly associated with the plasma membrane, suggesting that postactivation, NRC4 may undergo a conformation switch to form clusters that do not preferentially associate with the EHM. When NRC4 is activated by a sensor NLR during infection, however, NRC4 forms puncta mainly at the EHM and, to a lesser extent, at the plasma membrane. We conclude that following activation at the EHM, NRC4 may spread to other cellular membranes from its primary site of activation to trigger immune responses.
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    SAMD9L autoinflammatory or ataxia pancytopenia disease mutations activate cell-autonomous translational repression (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Sterile α motif domain-containing protein 9-like (SAMD9L) is encoded by a hallmark interferon-induced gene with a role in controlling virus replication that is not well understood. Here, we analyze SAMD9L function from the perspective of human mutations causing neonatal-onset severe autoinflammatory disease. Whole-genome sequencing of two children with leukocytoclastic panniculitis, basal ganglia calcifications, raised blood inflammatory markers, neutrophilia, anemia, thrombocytopaenia, and almost no B cells revealed heterozygous de novo SAMD9L mutations, p.Asn885Thrfs*6 and p.Lys878Serfs*13. These frameshift mutations truncate the SAMD9L protein within a domain a region of homology to the nucleotide-binding and oligomerization domain (NOD) of APAF1, ∼80 amino acids C-terminal to the Walker B motif. Single-cell analysis of human cells expressing green fluorescent protein (GFP)-SAMD9L fusion proteins revealed that enforced expression of wild-type SAMD9L repressed translation of red fluorescent protein messenger RNA and globally repressed endogenous protein translation, cell autonomously and in proportion to the level of GFP-SAMD9L in each cell. The children’s truncating mutations dramatically exaggerated translational repression even at low levels of GFP-SAMD9L per cell, as did a missense Arg986Cys mutation reported recurrently as causing ataxia pancytopenia syndrome. Autoinflammatory disease associated with SAMD9L truncating mutations appears to result from an interferon-induced translational repressor whose activity goes unchecked by the loss of C-terminal domains that may normally sense virus infection.
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    Benzofuran sulfonates and small self-lipid antigens activate type II NKT cells via CD1d (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Natural killer T (NKT) cells detect lipids presented by CD1d. Most studies focus on type I NKT cells that express semi-invariant αβ T cell receptors (TCR) and recognize α-galactosylceramides. However, CD1d also presents structurally distinct lipids to NKT cells expressing diverse TCRs (type II NKT cells), but our knowledge of the antigens for type II NKT cells is limited. An early study identified a nonlipidic NKT cell agonist, phenyl pentamethyldihydrobenzofuransulfonate (PPBF), which is notable for its similarity to common sulfa drugs, but its mechanism of NKT cell activation remained unknown. Here, we demonstrate that a range of pentamethylbenzofuransulfonates (PBFs), including PPBF, activate polyclonal type II NKT cells from human donors. Whereas these sulfa drug–like molecules might have acted pharmacologically on cells, here we demonstrate direct contact between TCRs and PBF-treated CD1d complexes. Further, PBF-treated CD1d tetramers identified type II NKT cell populations expressing αβTCRs and γδTCRs, including those with variable and joining region gene usage (TRAV12-1–TRAJ6) that was conserved across donors. By trapping a CD1d–type II NKT TCR complex for direct mass-spectrometric analysis, we detected molecules that allow the binding of CD1d to TCRs, finding that both selected PBF family members and short-chain sphingomyelin lipids are present in these complexes. Furthermore, the combination of PPBF and short-chain sphingomyelin enhances CD1d tetramer staining of PPBF-reactive T cell lines over either molecule alone. This study demonstrates that nonlipidic small molecules, which resemble sulfa drugs implicated in systemic hypersensitivity and drug allergy reactions, are targeted by a polyclonal population of type II NKT cells in a CD1d-restricted manner.
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    Band gaps of crystalline solids from Wannier-localization–based optimal tuning of a screened range-separated hybrid functional (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-20
    Description: Accurate prediction of fundamental band gaps of crystalline solid-state systems entirely within density functional theory is a long-standing challenge. Here, we present a simple and inexpensive method that achieves this by means of nonempirical optimal tuning of the parameters of a screened range-separated hybrid functional. The tuning involves the enforcement of an ansatz that generalizes the ionization potential theorem to the removal of an electron from an occupied state described by a localized Wannier function in a modestly sized supercell calculation. The method is benchmarked against experiment for a set of systems ranging from narrow band-gap semiconductors to large band-gap insulators, spanning a range of fundamental band gaps from 0.2 to 14.2 electronvolts (eV), and is found to yield quantitative accuracy across the board, with a mean absolute error of ∼0.1 eV and a maximal error of ∼0.2 eV.
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    Measuring the scientific effectiveness of contact tracing: Evidence from a natural experiment (2021)
    National Academy of Sciences
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    Publication Date: 2021-08-12
    Description: Contact tracing has for decades been a cornerstone of the public health approach to epidemics, including Ebola, severe acute respiratory syndrome, and now COVID-19. It has not yet been possible, however, to causally assess the method’s effectiveness using a randomized controlled trial of the sort familiar throughout other areas of science. This study provides evidence that comes close to that ideal. It exploits a large-scale natural experiment that occurred by accident in England in late September 2020. Because of a coding error involving spreadsheet data used by the health authorities, a total of 15,841 COVID-19 cases (around 20% of all cases) failed to have timely contact tracing. By chance, some areas of England were much more severely affected than others. This study finds that the random breakdown of contact tracing led to more illness and death. Conservative causal estimates imply that, relative to cases that were initially missed by the contact tracing system, cases subject to proper contact tracing were associated with a reduction in subsequent new infections of 63% and a reduction insubsequent COVID-19–related deaths of 66% across the 6 wk following the data glitch.
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    Vaccinating the oldest against COVID-19 saves both the most lives and most years of life (2021)
    National Academy of Sciences
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    Publication Date: 2021-02-25
    Description: Many competing criteria are under consideration for prioritizing COVID-19 vaccination. Two criteria based on age are demographic: lives saved and years of future life saved. Vaccinating the very old against COVID-19 saves the most lives, but, since older age is accompanied by falling life expectancy, it is widely supposed that these two goals are in conflict. We show this to be mistaken. The age patterns of COVID-19 mortality are such that vaccinating the oldest first saves the most lives and, surprisingly, also maximizes years of remaining life expectancy. We demonstrate this relationship empirically in the United States, Germany, and South Korea and with mathematical analysis of life tables. Our age-risk results, under usual conditions, also apply to health risks.
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    Effects of fluorinated solvents on electrolyte solvation structures and electrode/electrolyte interphases for lithium metal batteries (2021)
    National Academy of Sciences
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    Publication Date: 2021-02-25
    Description: Electrolyte is very critical to the performance of the high-voltage lithium (Li) metal battery (LMB), which is one of the most attractive candidates for the next-generation high-density energy-storage systems. Electrolyte formulation and structure determine the physical properties of the electrolytes and their interfacial chemistries on the electrode surfaces. Localized high-concentration electrolytes (LHCEs) outperform state-of-the-art carbonate electrolytes in many aspects in LMBs due to their unique solvation structures. Types of fluorinated cosolvents used in LHCEs are investigated here in searching for the most suitable diluent for high-concentration electrolytes (HCEs). Nonsolvating solvents (including fluorinated ethers, fluorinated borate, and fluorinated orthoformate) added in HCEs enable the formation of LHCEs with high-concentration solvation structures. However, low-solvating fluorinated carbonate will coordinate with Li+ ions and form a second solvation shell or a pseudo-LHCE which diminishes the benefits of LHCE. In addition, it is evident that the diluent has significant influence on the electrode/electrolyte interphases (EEIs) beyond retaining the high-concentration solvation structures. Diluent molecules surrounding the high-concentration clusters could accelerate or decelerate the anion decomposition through coparticipation of diluent decomposition in the EEI formation. The varied interphase features lead to significantly different battery performance. This study points out the importance of diluents and their synergetic effects with the conductive salt and the solvating solvent in designing LHCEs. These systematic comparisons and fundamental insights into LHCEs using different types of fluorinated solvents can guide further development of advanced electrolytes for high-voltage LMBs.
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    Transcriptional regulation of intermolecular Ca2+ signaling in hibernating ground squirrel cardiomyocytes: The myocardin–junctophilin axis (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: The contraction of heart cells is controlled by the intermolecular signaling between L-type Ca2+ channels (LCCs) and ryanodine receptors (RyRs), and the nanodistance between them depends on the interaction between junctophilin-2 (JPH2) in the sarcoplasmic reticulum (SR) and caveolin-3 (CAV3) in the transversal tubule (TT). In heart failure, decreased expression of JPH2 compromises LCC–RyR communication leading to deficient blood-pumping power. In the present study, we found that JPH2 and CAV3 transcription was concurrently regulated by serum response factor (SRF) and myocardin. In cardiomyocytes from torpid ground squirrels, compared with those from euthermic counterparts, myocardin expression was up-regulated, which boosted both JPH2 and CAV3 expression. Transmission electron microscopic imaging showed that the physical coupling between TTs and SRs was tightened during hibernation and after myocardin overexpression. Confocal Ca2+ imaging under the whole-cell patch clamp condition revealed that these changes enhanced the efficiency of LCC–RyR intermolecular signaling and fully compensated the adaptive down-regulation of LCCs, maintaining the power of heart contraction while avoiding the risk of calcium overload during hibernation. Our finding not only revealed an essential molecular mechanism underlying the survival of hibernating mammals, but also demonstrated a “reverse model of heart failure” at the molecular level, suggesting a strategy for treating heart diseases.
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    A unique Malpighian tubule architecture in Tribolium castaneum informs the evolutionary origins of systemic osmoregulation in beetles (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: Maintaining internal salt and water balance in response to fluctuating external conditions is essential for animal survival. This is particularly true for insects as their high surface-to-volume ratio makes them highly susceptible to osmotic stress. However, the cellular and hormonal mechanisms that mediate the systemic control of osmotic homeostasis in beetles (Coleoptera), the largest group of insects, remain largely unidentified. Here, we demonstrate that eight neurons in the brain of the red flour beetle Tribolium castaneum respond to internal changes in osmolality by releasing diuretic hormone (DH) 37 and DH47—homologs of vertebrate corticotropin-releasing factor (CRF) hormones—to control systemic water balance. Knockdown of the gene encoding the two hormones (Urinate, Urn8) reduces Malpighian tubule secretion and restricts organismal fluid loss, whereas injection of DH37 or DH47 reverses these phenotypes. We further identify a CRF-like receptor, Urinate receptor (Urn8R), which is exclusively expressed in a functionally unique secondary cell in the beetle tubules, as underlying this response. Activation of Urn8R increases K+ secretion, creating a lumen-positive transepithelial potential that drives fluid secretion. Together, these data show that beetle Malpighian tubules operate by a fundamentally different mechanism than those of other insects. Finally, we adopt a fluorescent labeling strategy to identify the evolutionary origin of this unusual tubule architecture, revealing that it evolved in the last common ancestor of the higher beetle families. Our work thus uncovers an important homeostatic program that is key to maintaining osmotic control in beetles, which evolved parallel to the radiation of the “advanced” beetle lineages.
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    Signal transduction through Cys-loop receptors is mediated by the nonspecific bumping of closely apposed domains (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: One of the most fundamental questions in the field of Cys-loop receptors (pentameric ligand-gated ion channels, pLGICs) is how the affinity for neurotransmitters and the conductive/nonconductive state of the transmembrane pore are correlated despite the ∼60-Å distance between the corresponding domains. Proposed mechanisms differ, but they all converge into the idea that interactions between wild-type side chains across the extracellular–transmembrane-domain (ECD–TMD) interface are crucial for this phenomenon. Indeed, the successful design of fully functional chimeras that combine intact ECD and TMD modules from different wild-type pLGICs has commonly been ascribed to the residual conservation of sequence that exists at the level of the interfacial loops even between evolutionarily distant parent channels. Here, using mutagenesis, patch-clamp electrophysiology, and radiolabeled-ligand binding experiments, we studied the effect of eliminating this residual conservation of sequence on ion-channel function and cell-surface expression. From our results, we conclude that proper state interconversion (“gating”) does not require conservation of sequence—or even physicochemical properties—across the ECD–TMD interface. Wild-type ECD and TMD side chains undoubtedly interact with their surroundings, but the interactions between them—straddling the interface—do not seem to be more important for gating than those occurring elsewhere in the protein. We propose that gating of pLGICs requires, instead, that the overall structure of the interfacial loops be conserved, and that their relative orientation and distance be the appropriate ones for changes in one side to result in changes in the other, in a phenomenon akin to the nonspecific “bumping” of closely apposed domains.
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    Structural analyses of an RNA stability element interacting with poly(A) (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: Cis-acting RNA elements are crucial for the regulation of polyadenylated RNA stability. The element for nuclear expression (ENE) contains a U-rich internal loop flanked by short helices. An ENE stabilizes RNA by sequestering the poly(A) tail via formation of a triplex structure that inhibits a rapid deadenylation-dependent decay pathway. Structure-based bioinformatic studies identified numerous ENE-like elements in evolutionarily diverse genomes, including a subclass containing two ENE motifs separated by a short double-helical region (double ENEs [dENEs]). Here, the structure of a dENE derived from a rice transposable element (TWIFB1) before and after poly(A) binding (∼24 kDa and ∼33 kDa, respectively) is investigated. We combine biochemical structure probing, small angle X-ray scattering (SAXS), and cryo‐electron microscopy (cryo-EM) to investigate the dENE structure and its local and global structural changes upon poly(A) binding. Our data reveal 1) the directionality of poly(A) binding to the dENE, and 2) that the dENE-poly(A) interaction involves a motif that protects the 3ʹ-most seven adenylates of the poly(A). Furthermore, we demonstrate that the dENE does not undergo a dramatic global conformational change upon poly(A) binding. These findings are consistent with the recently solved crystal structure of a dENE+poly(A) complex [S.-F. Torabi et al., Science 371, eabe6523 (2021)]. Identification of additional modes of poly(A)–RNA interaction opens new venues for better understanding of poly(A) tail biology.
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    Selective autophagy of AKAP11 activates cAMP/PKA to fuel mitochondrial metabolism and tumor cell growth (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: Autophagy is a catabolic pathway that provides self-nourishment and maintenance of cellular homeostasis. Autophagy is a fundamental cell protection pathway through metabolic recycling of various intracellular cargos and supplying the breakdown products. Here, we report an autophagy function in governing cell protection during cellular response to energy crisis through cell metabolic rewiring. We observe a role of selective type of autophagy in direct activation of cyclic AMP protein kinase A (PKA) and rejuvenation of mitochondrial function. Mechanistically, autophagy selectively degrades the inhibitory subunit RI of PKA holoenzyme through A-kinase–anchoring protein (AKAP) 11. AKAP11 acts as an autophagy receptor that recruits RI to autophagosomes via LC3. Glucose starvation induces AKAP11-dependent degradation of RI, resulting in PKA activation that potentiates PKA-cAMP response element-binding signaling, mitochondria respiration, and ATP production in accordance with mitochondrial elongation. AKAP11 deficiency inhibits PKA activation and impairs cell survival upon glucose starvation. Our results thus expand the view of autophagy cytoprotection mechanism by demonstrating selective autophagy in RI degradation and PKA activation that fuels the mitochondrial metabolism and confers cell resistance to glucose deprivation implicated in tumor growth.
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    The myosin II coiled-coil domain atomic structure in its native environment (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: The atomic structure of the complete myosin tail within thick filaments isolated from Lethocerus indicus flight muscle is described and compared to crystal structures of recombinant, human cardiac myosin tail segments. Overall, the agreement is good with three exceptions: the proximal S2, in which the filament has heads attached but the crystal structure doesn’t, and skip regions 2 and 4. At the head–tail junction, the tail α-helices are asymmetrically structured encompassing well-defined unfolding of 12 residues for one myosin tail, ∼4 residues of the other, and different degrees of α-helix unwinding for both tail α-helices, thereby providing an atomic resolution description of coiled-coil “uncoiling” at the head–tail junction. Asymmetry is observed in the nonhelical C termini; one C-terminal segment is intercalated between ribbons of myosin tails, the other apparently terminating at Skip 4 of another myosin tail. Between skip residues, crystal and filament structures agree well. Skips 1 and 3 also agree well and show the expected α-helix unwinding and coiled-coil untwisting in response to skip residue insertion. Skips 2 and 4 are different. Skip 2 is accommodated in an unusual manner through an increase in α-helix radius and corresponding reduction in rise/residue. Skip 4 remains helical in one chain, with the other chain unfolded, apparently influenced by the acidic myosin C terminus. The atomic model may shed some light on thick filament mechanosensing and is a step in understanding the complex roles that thick filaments of all species undergo during muscle contraction.
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    Potent neutralization of Rift Valley fever virus by human monoclonal antibodies through fusion inhibition (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Rift Valley fever virus (RVFV), an emerging arboviral and zoonotic bunyavirus, causes severe disease in livestock and humans. Here, we report the isolation of a panel of monoclonal antibodies (mAbs) from the B cells of immune individuals following natural infection in Kenya or immunization with MP-12 vaccine. The B cell responses of individuals who were vaccinated or naturally infected recognized similar epitopes on both Gc and Gn proteins. The Gn-specific mAbs and two mAbs that do not recognize either monomeric Gc or Gn alone but recognized the hetero-oligomer glycoprotein complex (Gc+Gn) when Gc and Gn were coexpressed exhibited potent neutralizing activities in vitro, while Gc-specific mAbs exhibited relatively lower neutralizing capacity. The two Gc+Gn–specific mAbs and the Gn domain A-specific mAbs inhibited RVFV fusion to cells, suggesting that mAbs can inhibit the exposure of the fusion loop in Gc, a class II fusion protein, and thus prevent fusion by an indirect mechanism without direct fusion loop contact. Competition-binding analysis with coexpressed Gc/Gn and mutagenesis library screening indicated that these mAbs recognize four major antigenic sites, with two sites of vulnerability for neutralization on Gn. In experimental models of infection in mice, representative mAbs recognizing three of the antigenic sites reduced morbidity and mortality when used at a low dose in both prophylactic and therapeutic settings. This study identifies multiple candidate mAbs that may be suitable for use in humans against RVFV infection and highlights fusion inhibition against bunyaviruses as a potential contributor to potent antibody-mediated neutralization.
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    A coupled human–natural system analysis of freshwater security under climate and population change (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Limited water availability, population growth, and climate change have resulted in freshwater crises in many countries. Jordan’s situation is emblematic, compounded by conflict-induced population shocks. Integrating knowledge across hydrology, climatology, agriculture, political science, geography, and economics, we present the Jordan Water Model, a nationwide coupled human–natural-engineered systems model that is used to evaluate Jordan’s freshwater security under climate and socioeconomic changes. The complex systems model simulates the trajectory of Jordan’s water system, representing dynamic interactions between a hierarchy of actors and the natural and engineered water environment. A multiagent modeling approach enables the quantification of impacts at the level of thousands of representative agents across sectors, allowing for the evaluation of both systemwide and distributional outcomes translated into a suite of water-security metrics (vulnerability, equity, shortage duration, and economic well-being). Model results indicate severe, potentially destabilizing, declines in freshwater security. Per capita water availability decreases by approximately 50% by the end of the century. Without intervening measures, 〉90% of the low-income household population experiences critical insecurity by the end of the century, receiving
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    The consequences of online partisan media (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: What role do ideologically extreme media play in the polarization of society? Here we report results from a randomized longitudinal field experiment embedded in a nationally representative online panel survey (N = 1,037) in which participants were incentivized to change their browser default settings and social media following patterns, boosting the likelihood of encountering news with either a left-leaning (HuffPost) or right-leaning (Fox News) slant during the 2018 US midterm election campaign. Data on ≈ 19 million web visits by respondents indicate that resulting changes in news consumption persisted for at least 8 wk. Greater exposure to partisan news can cause immediate but short-lived increases in website visits and knowledge of recent events. After adjusting for multiple comparisons, however, we find little evidence of a direct impact on opinions or affect. Still, results from later survey waves suggest that both treatments produce a lasting and meaningful decrease in trust in the mainstream media up to 1 y later. Consistent with the minimal-effects tradition, direct consequences of online partisan media are limited, although our findings raise questions about the possibility of subtle, cumulative dynamics. The combination of experimentation and computational social science techniques illustrates a powerful approach for studying the long-term consequences of exposure to partisan news.
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    Presynaptic α2δ subunits are key organizers of glutamatergic synapses (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: In nerve cells the genes encoding for α2δ subunits of voltage-gated calcium channels have been linked to synaptic functions and neurological disease. Here we show that α2δ subunits are essential for the formation and organization of glutamatergic synapses. Using a cellular α2δ subunit triple-knockout/knockdown model, we demonstrate a failure in presynaptic differentiation evidenced by defective presynaptic calcium channel clustering and calcium influx, smaller presynaptic active zones, and a strongly reduced accumulation of presynaptic vesicle-associated proteins (synapsin and vGLUT). The presynaptic defect is associated with the downscaling of postsynaptic AMPA receptors and the postsynaptic density. The role of α2δ isoforms as synaptic organizers is highly redundant, as each individual α2δ isoform can rescue presynaptic calcium channel trafficking and expression of synaptic proteins. Moreover, α2δ-2 and α2δ-3 with mutated metal ion-dependent adhesion sites can fully rescue presynaptic synapsin expression but only partially calcium channel trafficking, suggesting that the regulatory role of α2δ subunits is independent from its role as a calcium channel subunit. Our findings influence the current view on excitatory synapse formation. First, our study suggests that postsynaptic differentiation is secondary to presynaptic differentiation. Second, the dependence of presynaptic differentiation on α2δ implicates α2δ subunits as potential nucleation points for the organization of synapses. Finally, our results suggest that α2δ subunits act as transsynaptic organizers of glutamatergic synapses, thereby aligning the synaptic active zone with the postsynaptic density.
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    Disentangling perceptual awareness from nonconscious processing in rhesus monkeys (Macaca mulatta) (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: Scholars have long debated whether animals, which display impressive intelligent behaviors, are consciously aware or not. Yet, because many complex human behaviors and high-level functions can be performed without conscious awareness, it was long considered impossible to untangle whether animals are aware or just conditionally or nonconsciously behaving. Here, we developed an empirical approach to address this question. We harnessed a well-established cross-over double dissociation between nonconscious and conscious processing, in which people perform in completely opposite ways when they are aware of stimuli versus when they are not. To date, no one has explored if similar performance dissociations exist in a nonhuman species. In a series of seven experiments, we first established these signatures in humans using both known and newly developed nonverbal double-dissociation tasks and then identified similar signatures in rhesus monkeys (Macaca mulatta). These results provide robust evidence for two distinct modes of processing in nonhuman primates. This empirical approach makes it feasible to disentangle conscious visual awareness from nonconscious processing in nonhuman species; hence, it can be used to strip away ambiguity when exploring the processes governing intelligent behavior across the animal kingdom. Taken together, these results strongly support the existence of both nonconscious processing as well as functional human-like visual awareness in nonhuman animals.
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    Crossover interference: Just ZYP it (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
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    Sums of integer cubes (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
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    A molecular link between cell wall biosynthesis, translation fidelity, and stringent response in Streptococcus pneumoniae (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: Survival in the human host requires bacteria to respond to unfavorable conditions. In the important Gram-positive pathogen Streptococcus pneumoniae, cell wall biosynthesis proteins MurM and MurN are tRNA-dependent amino acyl transferases which lead to the production of branched muropeptides. We demonstrate that wild-type cells experience optimal growth under mildly acidic stressed conditions, but ΔmurMN strain displays growth arrest and extensive lysis. Furthermore, these stress conditions compromise the efficiency with which alanyl-tRNAAla synthetase can avoid noncognate mischarging of tRNAAla with serine, which is toxic to cells. The observed growth defects are rescued by inhibition of the stringent response pathway or by overexpression of the editing domain of alanyl-tRNAAla synthetase that enables detoxification of tRNA misacylation. Furthermore, MurM can incorporate seryl groups from mischarged Seryl-tRNAAlaUGC into cell wall precursors with exquisite specificity. We conclude that MurM contributes to the fidelity of translation control and modulates the stress response by decreasing the pool of mischarged tRNAs. Finally, we show that enhanced lysis of ΔmurMN pneumococci is caused by LytA, and the murMN operon influences macrophage phagocytosis in a LytA-dependent manner. Thus, MurMN attenuates stress responses with consequences for host–pathogen interactions. Our data suggest a causal link between misaminoacylated tRNA accumulation and activation of the stringent response. In order to prevent potential corruption of translation, consumption of seryl-tRNAAla by MurM may represent a first line of defense. When this mechanism is overwhelmed or absent (ΔmurMN), the stringent response shuts down translation to avoid toxic generation of mistranslated/misfolded proteins.
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    Subthalamic low-frequency oscillations predict vulnerability to cocaine addiction (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: Identifying vulnerable individuals before they transition to a compulsive pattern of drug seeking and taking is a key challenge in addiction to develop efficient prevention strategies. Oscillatory activity within the subthalamic nucleus (STN) has been associated with compulsive-related disorders. To study compulsive cocaine-seeking behavior, a core component of drug addiction, we have used a rat model in which cocaine seeking despite a foot-shock contingency only emerges in some vulnerable individuals having escalated their cocaine intake. We show that abnormal oscillatory activity within the alpha/theta and low-beta bands during the escalation of cocaine intake phase predicts the subsequent emergence of compulsive-like seeking behavior. In fact, mimicking STN pathological activity in noncompulsive rats during cocaine escalation turns them into compulsive ones. We also find that 30 Hz, but not 130 Hz, STN deep brain stimulation (DBS) reduces pathological cocaine seeking in compulsive individuals. Our results identify an early electrical signature of future compulsive-like cocaine-seeking behavior and further advocates the use of frequency-dependent STN DBS for the treatment of addiction.
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    TBK1 recruitment to STING activates both IRF3 and NF-κB that mediate immune defense against tumors and viral infections (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: The induction of type I interferons through the transcription factor interferon regulatory factor 3 (IRF3) is considered a major outcome of stimulator of interferon genes (STING) activation that drives immune responses against DNA viruses and tumors. However, STING activation can also trigger other downstream pathways such as nuclear factor κB (NF-κB) signaling and autophagy, and the roles of interferon (IFN)-independent functions of STING in infectious diseases or cancer are not well understood. Here, we generated a STING mouse strain with a mutation (S365A) that disrupts IRF3 binding and therefore type I interferon induction but not NF-κB activation or autophagy induction. We also generated STING mice with mutations that disrupt the recruitment of TANK-binding kinase 1 (TBK1), which is important for both IRF3 and NF-κB activation but not autophagy induction (L373A or ∆CTT, which lacks the C-terminal tail). The STING-S365A mutant mice, but not L373A or ∆CTT mice, were still resistant to herpes simplex virus 1 (HSV-1) infections and mounted an antitumor response after cyclic guanosine monophosphate-adenosine monophosphate (cGAMP) treatment despite the absence of STING-induced interferons. These results demonstrate that STING can function independently of type I interferons and autophagy, and that TBK1 recruitment to STING is essential for antiviral and antitumor immunity.
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    ICAM-1 orchestrates the abscopal effect of tumor radiotherapy (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: Compelling evidence indicates that radiotherapy (RT) has a systemic inhibitory effect on nonirradiated lesions (abscopal effect) in addition to the ablation of irradiated tumors. However, this effect occurs only in rare circumstances in clinical practice, and mechanisms underlying the abscopal effect of RT are neither fully understood nor therapeutically utilized. Here we identified that intercellular adhesion molecule-1 (ICAM-1), an inducible glycoprotein of the immunoglobulin superfamily, is up-regulated in nonirradiated tumors responsive to RT. ICAM-1 expression in preclinical animal models can be noninvasively detected by optical imaging and positron emission tomography (PET) using near-infrared fluorescence dye- and 64Cu-labeled imaging probes that we synthesized, respectively. Importantly, the expression levels of ICAM-1 determined by quantitative PET imaging showed a strong negative linear correlation with the growth of nonirradiated tumors. Moreover, genetic or pharmacologic up-regulation of ICAM-1 expression by either an intratumoral injection of engineered recombinant adenovirus or systemic administration of a Toll-like receptor 7 agonist-capsulated nanodrug could induce markedly increased abscopal responses to local RT in animal models. Mechanistic investigation revealed that ICAM-1 expression can enhance both the activation and tumor infiltration of CD8+ T cells to improve the responses of the nonirradiated tumors to RT. Together, our findings suggest that noninvasive PET imaging of ICAM-1 expression could be a powerful means to predict the responses of nonirradiated tumors to RT, which could facilitate the exploration of new combination RT strategies for effective ablation of primary and disseminated lesions.
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    Synchronous caregiving from birth to adulthood tunes humans’ social brain (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: Mammalian young are born with immature brain and rely on the mother’s body and caregiving behavior for maturation of neurobiological systems that sustain adult sociality. While research in animal models indicated the long-term effects of maternal contact and caregiving on the adult brain, little is known about the effects of maternal–newborn contact and parenting behavior on social brain functioning in human adults. We followed human neonates, including premature infants who initially lacked or received maternal–newborn skin-to-skin contact and full-term controls, from birth to adulthood, repeatedly observing mother–child social synchrony at key developmental nodes. We tested the brain basis of affect-specific empathy in young adulthood and utilized multivariate techniques to distinguish brain regions sensitive to others’ distinct emotions from those globally activated by the empathy task. The amygdala, insula, temporal pole (TP), and ventromedial prefrontal cortex (VMPFC) showed high sensitivity to others’ distinct emotions. Provision of maternal–newborn contact enhanced social synchrony across development from infancy and up until adulthood. The experience of synchrony, in turn, predicted the brain’s sensitivity to emotion-specific empathy in the amygdala and insula, core structures of the social brain. Social synchrony linked with greater empathic understanding in adolescence, which was longitudinally associated with higher neural sensitivity to emotion-specific empathy in TP and VMPFC. Findings demonstrate the centrality of synchronous caregiving, by which infants practice the detection and sharing of others’ affective states, for tuning the human social brain, particularly in regions implicated in salience detection, interoception, and mentalization that underpin affect sharing and human attachment.
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    In situ small-angle X-ray scattering reveals solution phase discharge of Li–O2 batteries with weakly solvating electrolytes (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: Electrodepositing insulating lithium peroxide (Li2O2) is the key process during discharge of aprotic Li–O2 batteries and determines rate, capacity, and reversibility. Current understanding states that the partition between surface adsorbed and dissolved lithium superoxide governs whether Li2O2 grows as a conformal surface film or larger particles, leading to low or high capacities, respectively. However, better understanding governing factors for Li2O2 packing density and capacity requires structural sensitive in situ metrologies. Here, we establish in situ small- and wide-angle X-ray scattering (SAXS/WAXS) as a suitable method to record the Li2O2 phase evolution with atomic to submicrometer resolution during cycling a custom-built in situ Li–O2 cell. Combined with sophisticated data analysis, SAXS allows retrieving rich quantitative structural information from complex multiphase systems. Surprisingly, we find that features are absent that would point at a Li2O2 surface film formed via two consecutive electron transfers, even in poorly solvating electrolytes thought to be prototypical for surface growth. All scattering data can be modeled by stacks of thin Li2O2 platelets potentially forming large toroidal particles. Li2O2 solution growth is further justified by rotating ring-disk electrode measurements and electron microscopy. Higher discharge overpotentials lead to smaller Li2O2 particles, but there is no transition to an electronically passivating, conformal Li2O2 coating. Hence, mass transport of reactive species rather than electronic transport through a Li2O2 film limits the discharge capacity. Provided that species mobilities and carbon surface areas are high, this allows for high discharge capacities even in weakly solvating electrolytes. The currently accepted Li–O2 reaction mechanism ought to be reconsidered.
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    CD11c+CD88+CD317+ myeloid cells are critical mediators of persistent CNS autoimmunity (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: Natalizumab, a humanized monoclonal antibody (mAb) against α4-integrin, reduces the number of dendritic cells (DC) in cerebral perivascular spaces in multiple sclerosis (MS). Selective deletion of α4-integrin in CD11c+ cells should curtail their migration to the central nervous system (CNS) and ameliorate experimental autoimmune encephalomyelitis (EAE). We generated CD11c.Cre+/−ITGA4fl/fl C57BL/6 mice to selectively delete α4-integrin in CD11c+ cells. Active immunization and adoptive transfer EAE models were employed and compared with WT controls. Multiparameter flow cytometry was utilized to immunophenotype leukocyte subsets. Single-cell RNA sequencing was used to profile individual cells. α4-Integrin expression by CD11c+ cells was significantly reduced in primary and secondary lymphoid organs in CD11c.Cre+/−ITGA4fl/fl mice. In active EAE, a delayed disease onset was observed in CD11c.Cre+/−ITGA4fl/fl mice, during which CD11c+CD88+ cells were sequestered in the blood. Upon clinical EAE onset, CD11c+CD88+ cells appeared in the CNS and expressed CD317+. In adoptive transfer experiments, CD11c.Cre+/−ITGA4fl/fl mice had ameliorated clinical disease phenotype associated with significantly diminished numbers of CNS CD11c+CD88+CD317+ cells. In human cerebrospinal fluid from subjects with neuroinflammation, microglia-like cells display coincident expression of ITGAX (CD11c), C5AR1 (CD88), and BST2 (CD317). In mice, we show that only activated, but not naïve microglia expressed CD11c, CD88, and CD317. Finally, anti-CD317 treatment prior to clinical EAE substantially enhanced recovery in mice.
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    A single-cell resolution developmental atlas of hematopoietic stem and progenitor cell expansion in zebrafish (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: During vertebrate embryogenesis, fetal hematopoietic stem and progenitor cells (HSPCs) exhibit expansion and differentiation properties in a supportive hematopoietic niche. To profile the developmental landscape of fetal HSPCs and their local niche, here, using single-cell RNA-sequencing, we deciphered a dynamic atlas covering 28,777 cells and 9 major cell types (23 clusters) of zebrafish caudal hematopoietic tissue (CHT). We characterized four heterogeneous HSPCs with distinct lineage priming and metabolic gene signatures. Furthermore, we investigated the regulatory mechanism of CHT niche components for HSPC development, with a focus on the transcription factors and ligand–receptor networks involved in HSPC expansion. Importantly, we identified an endothelial cell-specific G protein–coupled receptor 182, followed by in vivo and in vitro functional validation of its evolutionally conserved role in supporting HSPC expansion in zebrafish and mice. Finally, comparison between zebrafish CHT and human fetal liver highlighted the conservation and divergence across evolution. These findings enhance our understanding of the regulatory mechanism underlying hematopoietic niche for HSPC expansion in vivo and provide insights into improving protocols for HSPC expansion in vitro.
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    Pre-Columbian transregional captive rearing of Amazonian parrots in the Atacama Desert (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: The feathers of tropical birds were one of the most significant symbols of economic, social, and sacred status in the pre-Columbian Americas. In the Andes, finely produced clothing and textiles containing multicolored feathers of tropical parrots materialized power, prestige, and distinction and were particularly prized by political and religious elites. Here we report 27 complete or partial remains of macaws and amazon parrots from five archaeological sites in the Atacama Desert of northern Chile to improve our understanding of their taxonomic identity, chronology, cultural context, and mechanisms of acquisition. We conducted a multiproxy archaeometric study that included zooarchaeological analysis, isotopic dietary reconstruction, accelerated mass spectrometry radiocarbon dating, and paleogenomic analysis. The results reveal that during the Late Intermediate Period (1100 to 1450 CE), Atacama oasis communities acquired scarlet macaws (Ara macao) and at least five additional translocated parrot species through vast exchange networks that extended more than 500 km toward the eastern Amazonian tropics. Carbon and nitrogen stable isotopes indicate that Atacama aviculturalists sustained these birds on diets rich in marine bird guano-fertilized maize-based foods. The captive rearing of these colorful, exotic, and charismatic birds served to unambiguously signal relational wealth in a context of emergent intercommunity competition.
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    Associations between adolescent cannabis use and young-adult functioning in three longitudinal twin studies (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Observational studies have linked cannabis use to an array of negative outcomes, including psychiatric symptoms, cognitive impairment, and educational and occupational underachievement. These associations are particularly strong when cannabis use occurs in adolescence. Nevertheless, causality remains unclear. The purpose of the present study was thus to examine associations between prospectively assessed adolescent cannabis use and young-adult outcomes (psychiatric, cognitive, and socioeconomic) in three longitudinal studies of twins (n = 3,762). Twins reporting greater cumulative cannabis use in adolescence reported higher levels of psychopathology as well as poorer socioeconomic outcomes in young adulthood. However, cannabis use remained associated only with socioeconomic outcomes (i.e., educational attainment, occupational status, and income) in monozygotic-cotwin control analyses, which account fully for shared genetic and environmental confounding. Follow-up analyses examining associations between twin differences in adolescent cannabis use and longitudinal change in academic functioning during the middle- and high-school years provided a possible mechanism for these associations, indicating that greater cannabis use during this period was associated with decreases in grade point average and academic motivation as well as increases in academic problem behavior and school disciplinary problems. Our findings thus suggest that cannabis use in adolescence has potentially causal, deleterious effects on adolescent academic functioning and young-adult socioeconomic outcomes despite little evidence suggesting a strong, causal influence on adult mental health or cognitive ability.
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    Reconciling early Deccan Traps CO2 outgassing and pre-KPB global climate (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: A 2 to 4 °C warming episode, known as the Latest Maastrichtian warming event (LMWE), preceded the Cretaceous–Paleogene boundary (KPB) mass extinction at 66.05 ± 0.08 Ma and has been linked with the onset of voluminous Deccan Traps volcanism. Here, we use direct measurements of melt-inclusion CO2 concentrations and trace-element proxies for CO2 to test the hypothesis that early Deccan magmatism triggered this warming interval. We report CO2 concentrations from NanoSIMS and Raman spectroscopic analyses of melt-inclusion glass and vapor bubbles hosted in magnesian olivines from pre-KPB Deccan primitive basalts. Reconstructed melt-inclusion CO2 concentrations range up to 0.23 to 1.2 wt% CO2 for lavas from the Saurashtra Peninsula and the Thakurvadi Formation in the Western Ghats region. Trace-element proxies for CO2 concentration (Ba and Nb) yield estimates of initial melt concentrations of 0.4 to 1.3 wt% CO2 prior to degassing. Our data imply carbon saturation and degassing of Deccan magmas initiated at high pressures near the Moho or in the lower crust. Furthermore, we find that the earliest Deccan magmas were more CO2 rich, which we hypothesize facilitated more efficient flushing and outgassing from intrusive magmas. Based on carbon cycle modeling and estimates of preserved lava volumes for pre-KPB lavas, we find that volcanic CO2 outgassing alone remains insufficient to account for the magnitude of the observed latest Maastrichtian warming. However, accounting for intrusive outgassing can reconcile early carbon-rich Deccan Traps outgassing with observed changes in climate and atmospheric pCO2.
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    The diversity of stomatal development regulation in Callitriche is related to the intrageneric diversity in lifestyles (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Stomata, the gas exchange structures of plants, are formed by the division and differentiation of stem cells, or meristemoids. Although diverse patterns of meristemoid behavior have been observed among different lineages of land plants, the ecological significance and diversification processes of these different patterns are not well understood. Here we describe an intrageneric diversity in the patterns of meristemoid division within the ecologically diverse genus Callitriche (Plantaginaceae). Meristemoids underwent a series of divisions before differentiating into stomata in the terrestrial species of Callitriche, but these divisions did not occur in amphibious species, which can grow in both air and water, in which meristemoids differentiated directly into stomata. These findings imply the adaptive significance of diversity in meristemoid division. Molecular genetic analyses showed that the different expression times of the stomatal key transcription factors SPEECHLESS and MUTE, which maintain and terminate the meristemoid division, respectively, underlie the different division patterns of meristemoids. Unlike terrestrial species, amphibious species prematurely expressed MUTE immediately after expressing SPEECHLESS, which corresponded to their early termination of stomatal division. By linking morphological, ecological, and genetic elements of stomatal development, this study provides significant insight that should aid ecological evolutionary developmental biology investigations of stomata.
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    Virus-induced cell gigantism and asymmetric cell division in archaea (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Archaeal viruses represent one of the most mysterious parts of the global virosphere, with many virus groups sharing no evolutionary relationship to viruses of bacteria or eukaryotes. How these viruses interact with their hosts remains largely unexplored. Here we show that nonlytic lemon-shaped virus STSV2 interferes with the cell cycle control of its host, hyperthermophilic and acidophilic archaeon Sulfolobus islandicus, arresting the cell cycle in the S phase. STSV2 infection leads to transcriptional repression of the cell division machinery, which is homologous to the eukaryotic endosomal sorting complexes required for transport (ESCRT) system. The infected cells grow up to 20-fold larger in size, have 8,000-fold larger volume compared to noninfected cells, and accumulate massive amounts of viral and cellular DNA. Whereas noninfected Sulfolobus cells divide symmetrically by binary fission, the STSV2-infected cells undergo asymmetric division, whereby giant cells release normal-sized cells by budding, resembling the division of budding yeast. Reinfection of the normal-sized cells produces a new generation of giant cells. If the CRISPR-Cas system is present, the giant cells acquire virus-derived spacers and terminate the virus spread, whereas in its absence, the cycle continues, suggesting that CRISPR-Cas is the primary defense system in Sulfolobus against STSV2. Collectively, our results show how an archaeal virus manipulates the cell cycle, transforming the cell into a giant virion-producing factory.
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    Invariant plastic deformation mechanism in paramagnetic nickel–iron alloys (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: The Invar anomaly is one of the most fascinating phenomena observed in magnetically ordered materials. Invariant thermal expansion and elastic properties have attracted substantial scientific attention and led to important technological solutions. By studying planar faults in the high-temperature magnetically disordered state of Ni1−cFec, here we disclose a completely different anomaly. An invariant plastic deformation mechanism is characterized by an unchanged stacking fault energy with temperature within wide concentration and temperature ranges. This anomaly emerges from the competing stability between the face-centered cubic and hexagonal close-packed structures and occurs in other paramagnetic or nonmagnetic systems whenever the structural balance exists. The present findings create a platform for tailoring high-temperature properties of technologically relevant materials toward plastic stability at elevated temperatures.
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    Mapping temperature-dependent conformational change in the voltage-sensing domain of an engineered heat-activated K+ channel (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Temperature-dependent regulation of ion channel activity is critical for a variety of physiological processes ranging from immune response to perception of noxious stimuli. Our understanding of the structural mechanisms that underlie temperature sensing remains limited, in part due to the difficulty of combining high-resolution structural analysis with temperature stimulus. Here, we use NMR to compare the temperature-dependent behavior of Shaker potassium channel voltage sensor domain (WT-VSD) to its engineered temperature sensitive (TS-VSD) variant. Further insight into the molecular basis for temperature-dependent behavior is obtained by analyzing the experimental results together with molecular dynamics simulations. Our studies reveal that the overall secondary structure of the engineered TS-VSD is identical to the wild-type channels except for local changes in backbone torsion angles near the site of substitution (V369S and F370S). Remarkably however, these structural differences result in increased hydration of the voltage-sensing arginines and the S4–S5 linker helix in the TS-VSD at higher temperatures, in contrast to the WT-VSD. These findings highlight how subtle differences in the primary structure can result in large-scale changes in solvation and thereby confer increased temperature-dependent activity beyond that predicted by linear summation of solvation energies of individual substituents.
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    An ancient, conserved gene regulatory network led to the rise of oral venom systems (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Oral venom systems evolved multiple times in numerous vertebrates enabling the exploitation of unique predatory niches. Yet how and when they evolved remains poorly understood. Up to now, most research on venom evolution has focused strictly on the toxins. However, using toxins present in modern day animals to trace the origin of the venom system is difficult, since they tend to evolve rapidly, show complex patterns of expression, and were incorporated into the venom arsenal relatively recently. Here we focus on gene regulatory networks associated with the production of toxins in snakes, rather than the toxins themselves. We found that overall venom gland gene expression was surprisingly well conserved when compared to salivary glands of other amniotes. We characterized the “metavenom network,” a network of ∼3,000 nonsecreted housekeeping genes that are strongly coexpressed with the toxins, and are primarily involved in protein folding and modification. Conserved across amniotes, this network was coopted for venom evolution by exaptation of existing members and the recruitment of new toxin genes. For instance, starting from this common molecular foundation, Heloderma lizards, shrews, and solenodon, evolved venoms in parallel by overexpression of kallikreins, which were common in ancestral saliva and induce vasodilation when injected, causing circulatory shock. Derived venoms, such as those of snakes, incorporated novel toxins, though still rely on hypotension for prey immobilization. These similarities suggest repeated cooption of shared molecular machinery for the evolution of oral venom in mammals and reptiles, blurring the line between truly venomous animals and their ancestors.
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    Deep genetic affinity between coastal Pacific and Amazonian natives evidenced by Australasian ancestry (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Different models have been proposed to elucidate the origins of the founding populations of America, along with the number of migratory waves and routes used by these first explorers. Settlements, both along the Pacific coast and on land, have been evidenced in genetic and archeological studies. However, the number of migratory waves and the origin of immigrants are still controversial topics. Here, we show the Australasian genetic signal is present in the Pacific coast region, indicating a more widespread signal distribution within South America and implicating an ancient contact between Pacific and Amazonian dwellers. We demonstrate that the Australasian population contribution was introduced in South America through the Pacific coastal route before the formation of the Amazonian branch, likely in the ancient coastal Pacific/Amazonian population. In addition, we detected a significant amount of interpopulation and intrapopulation variation in this genetic signal in South America. This study elucidates the genetic relationships of different ancestral components in the initial settlement of South America and proposes that the migratory route used by migrants who carried the Australasian ancestry led to the absence of this signal in the populations of Central and North America.
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    The crystal structure of a 250-kDa heterotetrameric particle explains inhibition of sheddase meprin β by endogenous fetuin-B (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Meprin β (Mβ) is a multidomain type-I membrane metallopeptidase that sheds membrane-anchored substrates, releasing their soluble forms. Fetuin-B (FB) is its only known endogenous protein inhibitor. Herein, we analyzed the interaction between the ectodomain of Mβ (MβΔC) and FB, which stabilizes the enzyme and inhibits it with subnanomolar affinity. The MβΔC:FB crystal structure reveals a ∼250-kDa, ∼160-Å polyglycosylated heterotetrameric particle with a remarkable glycan structure. Two FB moieties insert like wedges through a “CPDCP trunk” and two hairpins into the respective peptidase catalytic domains, blocking the catalytic zinc ions through an “aspartate switch” mechanism. Uniquely, the active site clefts are obstructed from subsites S4 to S10′, but S1 and S1′ are spared, which prevents cleavage. Modeling of full-length Mβ reveals an EGF-like domain between MβΔC and the transmembrane segment that likely serves as a hinge to transit between membrane-distal and membrane-proximal conformations for inhibition and catalysis, respectively.
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    A scalable empathic supervision intervention to mitigate recidivism from probation and parole (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Incarceration is a pervasive issue in the United States that is enormously costly to families, communities, and society at large. The path from prison back to prison may depend on the relationship a person has with their probation or parole officer (PPO). If the relationship lacks appropriate care and trust, violations and recidivism (return to jail or prison) may be more likely to occur. Here, we test whether an “empathic supervision” intervention with PPOs—that aims to reduce collective blame against and promote empathy for the perspectives of adults on probation or parole (APPs)—can reduce rates of violations and recidivism. The intervention highlights the unreasonable expectation that all APPs will reoffend (collective blame) and the benefits of empathy—valuing APPs’ perspectives. Using both within-subject (monthly official records for 10 mo) and between-subject (treatment versus control) comparisons in a longitudinal study with PPOs in a large US city (NPPOs = 216; NAPPs=∼20,478), we find that the empathic supervision intervention reduced collective blame against APPs 10 mo postintervention and reduced between-subject violations and recidivism, a 13% reduction that would translate to less taxpayer costs if scaled. Together, these findings illustrate that very low-cost psychological interventions that target empathy in relationships can be cost effective and combat important societal outcomes in a lasting manner.
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    Fluid-like elastic response of superionic NH3 in Uranus and Neptune (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Nondipolar magnetic fields exhibited at Uranus and Neptune may be derived from a unique geometry of their icy mantle with a thin convective layer on top of a stratified nonconvective layer. The presence of superionic H2O and NH3 has been thought as an explanation to stabilize such nonconvective regions. However, a lack of experimental data on the physical properties of those superionic phases has prevented the clarification of this matter. Here, our Brillouin measurements for NH3 show a two-stage reduction in longitudinal wave velocity (Vp) by ∼9% and ∼20% relative to the molecular solid in the temperature range of 1,500 K and 2,000 K above 47 GPa. While the first Vp reduction observed at the boundary to the superionic α phase was most likely due to the onset of the hydrogen diffusion, the further one was likely attributed to the transition to another superionic phase, denoted γ phase, exhibiting the higher diffusivity. The reduction rate of Vp in the superionic γ phase, comparable to that of the liquid, implies that this phase elastically behaves almost like a liquid. Our measurements show that superionic NH3 becomes convective and cannot contribute to the internal stratification.
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    Using random assignment to measure court accessibility for low-income divorce seekers (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-30
    Description: We conducted a field experiment in which 311 low-income individuals seeking a divorce were randomly assigned to receive access to a pro bono lawyer (versus minimal help) to assist with filing for divorce. Examining court records, we found that assignment to an attorney made a large difference in whether participants filed for and obtained a divorce. Three years after randomization, 46% of the treated group had terminated their marriages in the proper legal venue, compared to 9% of the control group. Among “compliers”—participants who obtained representation only if assigned to receive it—those with lawyers were far more likely to file for and obtain a divorce than those not assigned lawyers. Because divorce implicates fundamental constitutional interests and can be effectuated only by resort to the courts, the US Constitution requires that dissolution of marriage be made achievable regardless of ability to pay. Yet, we observed few low-income individuals who were able to initiate divorce suits on their own. Through interviews and archival research, we identified barriers that low-income litigants faced in navigating the divorce system, including mandatory wait times, limited hours at important facilities, and burdensome paperwork sometimes requiring access to photocopiers and typewriters. This study therefore documents a salient instance in which a civil legal process was inaccessible to those without lawyers, even though their legal issues were straightforward, involving few if any matters for courts to adjudicate.
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    Modeling DNA trapping of anticancer therapeutic targets using missense mutations identifies dominant synthetic lethal interactions (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Genetic screens can identify synthetic lethal (SL) interactions and uncover potential anticancer therapeutic targets. However, most SL screens have utilized knockout or knockdown approaches that do not accurately mimic chemical inhibition of a target protein. Here, we test whether missense mutations can be utilized as a model for a type of protein inhibition that creates a dominant gain-of-function cytotoxicity. We expressed missense mutations in the FEN1 endonuclease and the replication-associated helicase, CHL1, that inhibited enzymatic activity but retained substrate binding, and found that these mutations elicited a dominant SL phenotype consistent with the generation of cytotoxic protein–DNA or protein–protein intermediates. Genetic screens with nuclease-defective hFEN1 and helicase-deficient yCHL1 captured dominant SL interactions, in which ectopic expression of the mutant form, in the presence of the wild-type form, caused SL in specific mutant backgrounds. Expression of nuclease-defective hFEN1 in yeast elicited DNA binding-dependent dominant SL with homologous recombination mutants. In contrast, dominant SL interactions with helicase-deficient yCHL1 were observed in spindle-associated, Ctf18-alternative replication factor C (Ctf18-RFC) clamp loader complex, and cohesin mutant backgrounds. These results highlight the different mechanisms underlying SL interactions that occur in the presence of an inhibited form of the target protein and point to the utility of modeling trapping mutations in pursuit of more clinically relevant SL interactions.
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    Upgraded CRISPR/Cas9 tools for tissue-specific mutagenesis in Drosophila (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: CRISPR/Cas9 has emerged as a powerful technology for tissue-specific mutagenesis. However, tissue-specific CRISPR/Cas9 tools currently available in Drosophila remain deficient in three significant ways. First, many existing gRNAs are inefficient, such that further improvements of gRNA expression constructs are needed for more efficient and predictable mutagenesis in both somatic and germline tissues. Second, it has been difficult to label mutant cells in target tissues with current methods. Lastly, application of tissue-specific mutagenesis at present often relies on Gal4-driven Cas9, which hampers the flexibility and effectiveness of the system. Here, we tackle these deficiencies by building upon our previous CRISPR-mediated tissue-restricted mutagenesis (CRISPR-TRiM) tools. First, we significantly improved gRNA efficiency in somatic tissues by optimizing multiplexed gRNA design. Similarly, we also designed efficient dual-gRNA vectors for the germline. Second, we developed methods to positively and negatively label mutant cells in tissue-specific mutagenesis by incorporating co-CRISPR reporters into gRNA expression vectors. Lastly, we generated genetic reagents for convenient conversion of existing Gal4 drivers into tissue-specific Cas9 lines based on homology-assisted CRISPR knock-in. In this way, we expand the choices of Cas9 for CRISPR-TRiM analysis to broader tissues and developmental stages. Overall, our upgraded CRISPR/Cas9 tools make tissue-specific mutagenesis more versatile, reliable, and effective in Drosophila. These improvements may be also applied to other model systems.
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    A limited role of NKCC1 in telencephalic glutamatergic neurons for developing hippocampal network dynamics and behavior (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: NKCC1 is the primary transporter mediating chloride uptake in immature principal neurons, but its role in the development of in vivo network dynamics and cognitive abilities remains unknown. Here, we address the function of NKCC1 in developing mice using electrophysiological, optical, and behavioral approaches. We report that NKCC1 deletion from telencephalic glutamatergic neurons decreases in vitro excitatory actions of γ-aminobutyric acid (GABA) and impairs neuronal synchrony in neonatal hippocampal brain slices. In vivo, it has a minor impact on correlated spontaneous activity in the hippocampus and does not affect network activity in the intact visual cortex. Moreover, long-term effects of the developmental NKCC1 deletion on synaptic maturation, network dynamics, and behavioral performance are subtle. Our data reveal a neural network function of NKCC1 in hippocampal glutamatergic neurons in vivo, but challenge the hypothesis that NKCC1 is essential for major aspects of hippocampal development.
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    Molecular mechanism of abnormally large nonsoftening deformation in a tough hydrogel (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Tough soft materials usually show strain softening and inelastic deformation. Here, we study the molecular mechanism of abnormally large nonsoftening, quasi-linear but inelastic deformation in tough hydrogels made of hyperconnective physical network and linear polymers as molecular glues to the network. The interplay of hyperconnectivity of network and effective load transfer by molecular glues prevents stress concentration, which is revealed by an affine deformation of the network to the bulk deformation up to sample failure. The suppression of local stress concentration and strain amplification plays a key role in avoiding necking or strain softening and endows the gels with a unique large nonsoftening, quasi-linear but inelastic deformation.
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    Turn-on mode diarylethenes for bioconjugation and fluorescence microscopy of cellular structures (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: The use of photoswitchable fluorescent diarylethenes (fDAEs) as protein labels in fluorescence microscopy and nanoscopy has been limited by labeling inhomogeneity and the need for ultraviolet light for fluorescence activation (on-switching). To overcome these drawbacks, we prepared “turn-on mode” fDAEs featuring thienyl substituents, multiple polar residues, and a reactive maleimide group in the core structure. Conjugates with antibodies and nanobodies displayed complete on-switching and excitation with violet (405 nm) and yellow-green (
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    Tuning interactions between spins in a superconductor (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Novel many-body and topological electronic phases can be created in assemblies of interacting spins coupled to a superconductor, such as one-dimensional topological superconductors with Majorana zero modes (MZMs) at their ends. Understanding and controlling interactions between spins and the emergent band structure of the in-gap Yu–Shiba–Rusinov (YSR) states they induce in a superconductor are fundamental for engineering such phases. Here, by precisely positioning magnetic adatoms with a scanning tunneling microscope (STM), we demonstrate both the tunability of exchange interaction between spins and precise control of the hybridization of YSR states they induce on the surface of a bismuth (Bi) thin film that is made superconducting with the proximity effect. In this platform, depending on the separation of spins, the interplay among Ruderman–Kittel–Kasuya–Yosida (RKKY) interaction, spin–orbit coupling, and surface magnetic anisotropy stabilizes different types of spin alignments. Using high-resolution STM spectroscopy at millikelvin temperatures, we probe these spin alignments through monitoring the spin-induced YSR states and their energy splitting. Such measurements also reveal a quantum phase transition between the ground states with different electron number parity for a pair of spins in a superconductor tuned by their separation. Experiments on larger assemblies show that spin–spin interactions can be mediated in a superconductor over long distances. Our results show that controlling hybridization of the YSR states in this platform provides the possibility of engineering the band structure of such states for creating topological phases.
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    Interplays of electron and nuclear motions along CO dissociation trajectory in myoglobin revealed by ultrafast X-rays and quantum dynamics calculations (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Ultrafast structural dynamics with different spatial and temporal scales were investigated during photodissociation of carbon monoxide (CO) from iron(II)–heme in bovine myoglobin during the first 3 ps following laser excitation. We used simultaneous X-ray transient absorption (XTA) spectroscopy and X-ray transient solution scattering (XSS) at an X-ray free electron laser source with a time resolution of 80 fs. Kinetic traces at different characteristic X-ray energies were collected to give a global picture of the multistep pathway in the photodissociation of CO from heme. In order to extract the reaction coordinates along different directions of the CO departure, XTA data were collected with parallel and perpendicular relative polarizations of the laser pump and X-ray probe pulse to isolate the contributions of electronic spin state transition, bond breaking, and heme macrocycle nuclear relaxation. The time evolution of the iron K-edge X-ray absorption near edge structure (XANES) features along the two major photochemical reaction coordinates, i.e., the iron(II)–CO bond elongation and the heme macrocycle doming relaxation were modeled by time-dependent density functional theory calculations. Combined results from the experiments and computations reveal insight into interplays between the nuclear and electronic structural dynamics along the CO photodissociation trajectory. Time-resolved small-angle X-ray scattering data during the same process are also simultaneously collected, which show that the local CO dissociation causes a protein quake propagating on different spatial and temporal scales. These studies are important for understanding gas transport and protein deligation processes and shed light on the interplay of active site conformational changes and large-scale protein reorganization.
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    Use of NAD tagSeq II to identify growth phase-dependent alterations in E. coli RNA NAD+ capping (2021)
    National Academy of Sciences
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    Publication Date: 2021-03-29
    Description: Recent findings regarding nicotinamide adenine dinucleotide (NAD+)-capped RNAs (NAD-RNAs) indicate that prokaryotes and eukaryotes employ noncanonical RNA capping to regulate gene expression. Two methods for transcriptome-wide analysis of NAD-RNAs, NAD captureSeq and NAD tagSeq, are based on copper-catalyzed azide-alkyne cycloaddition (CuAAC) click chemistry to label NAD-RNAs. However, copper ions can fragment/degrade RNA, interfering with the analyses. Here we report development of NAD tagSeq II, which uses copper-free, strain-promoted azide-alkyne cycloaddition (SPAAC) for labeling NAD-RNAs, followed by identification of tagged RNA by single-molecule direct RNA sequencing. We used this method to compare NAD-RNA and total transcript profiles of Escherichia coli cells in the exponential and stationary phases. We identified hundreds of NAD-RNA species in E. coli and revealed genome-wide alterations of NAD-RNA profiles in the different growth phases. Although no or few NAD-RNAs were detected from some of the most highly expressed genes, the transcripts of some genes were found to be primarily NAD-RNAs. Our study suggests that NAD-RNAs play roles in linking nutrient cues with gene regulation in E. coli.
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    miR-218-2 regulates cognitive functions in the hippocampus through complement component 3–dependent modulation of synaptic vesicle release (2021)
    National Academy of Sciences
    Details
    Publication Date: 2021-03-29
    Description: microRNA-218 (miR-218) has been linked to several cognition related neurodegenerative and neuropsychiatric disorders. However, whether miR-218 plays a direct role in cognitive functions remains unknown. Here, using the miR-218 knockout (KO) mouse model and the sponge/overexpression approaches, we showed that miR-218-2 but not miR-218-1 could bidirectionally regulate the contextual and spatial memory in the mice. Furthermore, miR-218-2 deficiency induced deficits in the morphology and presynaptic neurotransmitter release in the hippocampus to impair the long term potentiation. Combining the RNA sequencing analysis and luciferase reporter assay, we identified complement component 3 (C3) as a main target gene of miR-218 in the hippocampus to regulate the presynaptic functions. Finally, we showed that restoring the C3 activity in the miR-218-2 KO mice could rescue the synaptic and learning deficits. Therefore, miR-218-2 played an important role in the cognitive functions of mice through C3, which can be a mechanism for the defective cognition of miR-218 related neuronal disorders.
    Print ISSN: 0027-8424
    Electronic ISSN: 1091-6490
    Topics: Biology , Medicine , Natural Sciences in General
    Published by National Academy of Sciences
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    Substrate discrimination and quality control require each catalytic activity of TRAMP and the nuclear RNA exosome (2021)
    National Academy of Sciences
    Details
    Publication Date: 2021-03-29
    Description: Quality control requires discrimination between functional and aberrant species to selectively target aberrant substrates for destruction. Nuclear RNA quality control in Saccharomyces cerevisiae includes the TRAMP complex that marks RNA for decay via polyadenylation followed by helicase-dependent 3′ to 5′ degradation by the RNA exosome. Using reconstitution biochemistry, we show that polyadenylation and helicase activities of TRAMP cooperate with processive and distributive exoribonuclease activities of the nuclear RNA exosome to protect stable RNA from degradation while selectively targeting and degrading less stable RNA. Substrate discrimination is lost when the distributive exoribonuclease activity of Rrp6 is inactivated, leading to degradation of stable and unstable RNA species. These data support a proofreading mechanism in which deadenylation by Rrp6 competes with Mtr4-dependent degradation to protect stable RNA while selectively targeting and degrading unstable RNA.
    Print ISSN: 0027-8424
    Electronic ISSN: 1091-6490
    Topics: Biology , Medicine , Natural Sciences in General
    Published by National Academy of Sciences
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    ZYP1 is required for obligate cross-over formation and cross-over interference in Arabidopsis (2021)
    National Academy of Sciences
    Details
    Publication Date: 2021-03-29
    Description: The synaptonemal complex is a tripartite proteinaceous ultrastructure that forms between homologous chromosomes during prophase I of meiosis in the majority of eukaryotes. It is characterized by the coordinated installation of transverse filament proteins between two lateral elements and is required for wild-type levels of crossing over and meiotic progression. We have generated null mutants of the duplicated Arabidopsis transverse filament genes zyp1a and zyp1b using a combination of T-DNA insertional mutants and targeted CRISPR/Cas mutagenesis. Cytological and genetic analysis of the zyp1 null mutants reveals loss of the obligate chiasma, an increase in recombination map length by 1.3- to 1.7-fold and a virtual absence of cross-over (CO) interference, determined by a significant increase in the number of double COs. At diplotene, the numbers of HEI10 foci, a marker for Class I interference-sensitive COs, are twofold greater in the zyp1 mutant compared to wild type. The increase in recombination in zyp1 does not appear to be due to the Class II interference-insensitive COs as chiasmata were reduced by ∼52% in msh5/zyp1 compared to msh5. These data suggest that ZYP1 limits the formation of closely spaced Class I COs in Arabidopsis. Our data indicate that installation of ZYP1 occurs at ASY1-labeled axial bridges and that loss of the protein disrupts progressive coalignment of the chromosome axes.
    Print ISSN: 0027-8424
    Electronic ISSN: 1091-6490
    Topics: Biology , Medicine , Natural Sciences in General
    Published by National Academy of Sciences
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