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  • 1
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    Consequences of strain variability and calcification in Emiliania huxleyi on microzooplankton grazing (2016)
    Details
    Publication Date: 2022-05-25
    Description: Author Posting. © The Author(s), 2015. This is the author's version of the work. It is posted here by permission of Oxford University Press for personal use, not for redistribution. The definitive version was published in Journal of Plankton Research (2015), doi:10.1093/plankt/fbv081.
    Description: Microzooplankton are the main consumers of marine phytoplankton. Intrinsic traits of phytoplankton can reduce grazing mortality, directly influencing phytoplankton population dynamics, food web ecology, and biogeochemical cycling. We examined the impact of calcification in mediating the functional grazing response of three heterotrophic dinoflagellates, on the coccolithophore, Emilania huxleyi. A variety of parameters, including predator grazing and growth rates, were examined over a 24-48 h period, at 1-5 prey concentrations for five isolates of E. huxleyi that fell along a gradient of calcification states. Significant differences in ingestion and clearance rate were strain-specific, and no apparent trends were observed in relation to calcification. However, predators had, on average, a had a 60% slower growth rate on calcified strains relative to naked strains; furthermore, gross growth efficiency was reduced when ingesting calcified strains. A growth rate model demonstrated a positive feedback from grazing interactions whereby decreased predator growth rate on calcified strains resulted in the accumulation of E. huxleyi. This study highlights the complexity involved in understanding the role of prey phenotype on grazing rates, and emphasizes the importance in considering morphological traits when deciphering predator-prey interactions in the plankton.
    Description: This research was funded by the Gordon and Betty Moore Foundation through Grant GBMF3301 to MDJ and KDB.
    Description: 2016-09-30
    Keywords: Grazing ; Microzooplankton ; Emiliania huxleyi ; Intra-specific variability
    Repository Name: Woods Hole Open Access Server
    Type: Preprint
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  • 2
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    A bacterial quorum-sensing precursor induces mortality in the marine coccolithophore, Emiliania huxleyi (2016)
    Frontiers Media
    Details
    Publication Date: 2022-05-25
    Description: © The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 7 (2016): 59, doi:10.3389/fmicb.2016.00059.
    Description: Interactions between phytoplankton and bacteria play a central role in mediating biogeochemical cycling and food web structure in the ocean. However, deciphering the chemical drivers of these interspecies interactions remains challenging. Here, we report the isolation of 2-heptyl-4-quinolone (HHQ), released by Pseudoalteromonas piscicida, a marine gamma-proteobacteria previously reported to induce phytoplankton mortality through a hitherto unknown algicidal mechanism. HHQ functions as both an antibiotic and a bacterial signaling molecule in cell–cell communication in clinical infection models. Co-culture of the bloom-forming coccolithophore, Emiliania huxleyi with both live P. piscicida and cell-free filtrates caused a significant decrease in algal growth. Investigations of the P. piscicida exometabolome revealed HHQ, at nanomolar concentrations, induced mortality in three strains of E. huxleyi. Mortality of E. huxleyi in response to HHQ occurred slowly, implying static growth rather than a singular loss event (e.g., rapid cell lysis). In contrast, the marine chlorophyte, Dunaliella tertiolecta and diatom, Phaeodactylum tricornutum were unaffected by HHQ exposures. These results suggest that HHQ mediates the type of inter-domain interactions that cause shifts in phytoplankton population dynamics. These chemically mediated interactions, and other like it, ultimately influence large-scale oceanographic processes.
    Description: This research was support through funding from the Gordon and Betty Moore Foundation through Grant GBMF3301 to MJ and TM; NIH grant from the National Institute of Allergy and Infectious Disease (NIAID – 1R21Al119311-01) to TM and KW; the National Science Foundation (OCE – 1313747) and US National Institute of Environmental Health Science (P01-ES021921) through the Oceans and Human Health Program to BM. Additional financial support was provided to TM from the Flatley Discovery Lab.
    Keywords: Infochemicals ; Algicidal compound ; Bacteria–phytoplankton interaction ; HHQ ; Pseudoalteromonas ; Emiliania huxleyi ; IC50 ; Mortality
    Repository Name: Woods Hole Open Access Server
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  • 3
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    The possession of coccoliths fails to deter microzooplankton grazers (2021)
    Frontiers Media
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Mayers, K. M. J., Poulton, A. J., Bidle, K., Thamatrakoln, K., Schieler, B., Giering, S. L. C., Wells, S. R., Tarran, G. A., Mayor, D., Johnson, M., Riebesell, U., Larsen, A., Vardi, A., & Harvey, E. L. The possession of coccoliths fails to deter microzooplankton grazers. Frontiers in Marine Science, 7, (2020): 562020, doi:10.3389/fmars.2020.569896.
    Description: Phytoplankton play a central role in the regulation of global carbon and nutrient cycles, forming the basis of the marine food webs. A group of biogeochemically important phytoplankton, the coccolithophores, produce calcium carbonate scales that have been hypothesized to deter or reduce grazing by microzooplankton. Here, a meta-analysis of mesocosm-based experiments demonstrates that calcification of the cosmopolitan coccolithophore, Emiliania huxleyi, fails to deter microzooplankton grazing. The median grazing to growth ratio for E. huxleyi (0.56 ± 0.40) was not significantly different among non-calcified nano- or picoeukaryotes (0.71 ± 0.31 and 0.55 ± 0.34, respectively). Additionally, the environmental concentration of E. huxleyi did not drive preferential grazing of non-calcified groups. These results strongly suggest that the possession of coccoliths does not provide E. huxleyi effective protection from microzooplankton grazing. Such indiscriminate consumption has implications for the dissolution and fate of CaCO3 in the ocean, and the evolution of coccoliths.
    Description: Mesocosm experiments in 2015 were supported by the Kiel Excellence Cluster “The Future Ocean” (CP1540) and the Leibniz Award to UR, in 2017 the MESOHUX experiment was supported by NSF (OCE-1559179) to KT and KB, NSF (OCE-1537951 and OCE-1459200) to KB, NSF (OCE-1459190, 1657808, and DBI-1624593) to EH, and in 2018 by AQUACOSM (EU H2020-INFRAIA-project No 731065). KM was supported by a NERC Doctoral Training Partnership (DTP) studentship as part of the Southampton Partnership for Innovative Training of Future Investigators Researching the Environment (SPITFIRE, grant number NE/L002531/1) and Research Council of Norway project (#280414) MIXsTRUCT.
    Keywords: coccolithophore ; phytoplankton ; microzooplankton ; biomineralisation ; predation ; evolution
    Repository Name: Woods Hole Open Access Server
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  • 4
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    Dynamic regulation of extracellular superoxide production by the coccolithophore Emiliania huxleyi (CCMP 374) (2019)
    Frontiers Media
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Plummeer, S., Taylor, A. E., Harvey, E. L., Hansel, C. M., & Diaz, J. M. Dynamic regulation of extracellular superoxide production by the coccolithophore Emiliania huxleyi (CCMP 374). Frontiers in Microbiology, 10, (2019): 1546, doi: 10.3389/fmicb.2019.01546.
    Description: In marine waters, ubiquitous reactive oxygen species (ROS) drive biogeochemical cycling of metals and carbon. Marine phytoplankton produce the ROS superoxide (O2−) extracellularly and can be a dominant source of O2− in natural aquatic systems. However, the cellular regulation, biological functioning, and broader ecological impacts of extracellular O2− production by marine phytoplankton remain mysterious. Here, we explored the regulation and potential roles of extracellular O2− production by a noncalcifying strain of the cosmopolitan coccolithophorid Emiliania huxleyi, a key species of marine phytoplankton that has not been examined for extracellular O2− production previously. Cell-normalized extracellular O2− production was the highest under presumably low-stress conditions during active proliferation and inversely related to cell density during exponential growth phase. Removal of extracellular O2− through addition of the O2− scavenger superoxide dismutase (SOD), however, increased growth rates, growth yields, cell biovolume, and photosynthetic efficiency (Fv/Fm) indicating an overall physiological improvement. Thus, the presence of extracellular O2− does not directly stimulate E. huxleyi proliferation, as previously suggested for other phytoplankton, bacteria, fungi, and protists. Extracellular O2− production decreased in the dark, suggesting a connection with photosynthetic processes. Taken together, the tight regulation of this stress independent production of extracellular O2− by E. huxleyi suggests that it could be involved in fundamental photophysiological processes.
    Description: This research was supported by a Junior Faculty Seed Grant from the University of Georgia Research Foundation (JD), a National Science Foundation (NSF) Graduate Research Fellowship (SP), and NSF grant OCE-1355720 (CH). The FlowCam® and FIRe were purchased through a NSF Equipment Improvement Grant (1624593).
    Keywords: Reactive oxygen species ; Superoxide ; Emiliania huxleyi ; Photophysiology ; Oxidative stress ; Redox homeostasis ; Biogeochemical cycling
    Repository Name: Woods Hole Open Access Server
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  • 5
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    Transparent exopolymer particle (TEP) measurements from the MesoHux mesocosm experiment held in May 2017 (2021)
    Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu
    Details
    Publication Date: 2022-05-27
    Description: Dataset: MesoHux TEP
    Description: Transparent exopolymer particle (TEP) measurements from the MesoHux mesocosm experiment held in May 2017. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/748500
    Description: NSF Division of Ocean Sciences (NSF OCE) OCE-1459190
    Repository Name: Woods Hole Open Access Server
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  • 6
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    Chlorophyll measurements from the MesoHux mesocosm experiment held in May 2017 (2021)
    Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu
    Details
    Publication Date: 2022-05-27
    Description: Dataset: MesoHux Chlorophyll
    Description: Chlorophyll measurements from the MesoHux mesocosm experiment held in May 2017. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/748471
    Description: NSF Division of Ocean Sciences (NSF OCE) OCE-1459190
    Repository Name: Woods Hole Open Access Server
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  • 7
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    Flow cytometry measurements from HHQ experiments conducted during the MesoHux mesocosm experiment, May 2017, Bergen, Norway (2019)
    Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu
    Details
    Publication Date: 2022-05-26
    Description: Dataset: HHQ Flow Cytometry
    Description: This dataset includes flow cytometry measurements from HHQ experiments conducted during the MesoHux mesocosm experiment, May 2017, Bergen, Norway. Microbial mesocosms were spiked with 2-heptyl-4-quinolone (HHQ). For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/753431
    Description: NSF Division of Ocean Sciences (NSF OCE) OCE-1657898
    Repository Name: Woods Hole Open Access Server
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  • 8
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    Bacterial quorum-sensing signal arrests phytoplankton cell division and impacts virus-induced mortality (2021)
    American Society for Microbiology
    Details
    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 Pollara, S. B., Becker, J. W., Nunn, B. L., Boiteau, R., Repeta, D., Mudge, M. C., Downing, G., Chase, D., Harvey, E. L., & Whalen, K. E. Bacterial quorum-sensing signal arrests phytoplankton cell division and impacts virus-induced mortality. Msphere, 6(3), (2021): e00009-21, https://doi.org/10.1128/mSphere.00009-21.
    Description: Interactions between phytoplankton and heterotrophic bacteria fundamentally shape marine ecosystems by controlling primary production, structuring marine food webs, mediating carbon export, and influencing global climate. Phytoplankton-bacterium interactions are facilitated by secreted compounds; however, linking these chemical signals, their mechanisms of action, and their resultant ecological consequences remains a fundamental challenge. The bacterial quorum-sensing signal 2-heptyl-4-quinolone (HHQ) induces immediate, yet reversible, cellular stasis (no cell division or mortality) in the coccolithophore Emiliania huxleyi; however, the mechanism responsible remains unknown. Using transcriptomic and proteomic approaches in combination with diagnostic biochemical and fluorescent cell-based assays, we show that HHQ exposure leads to prolonged S-phase arrest in phytoplankton coincident with the accumulation of DNA damage and a lack of repair despite the induction of the DNA damage response (DDR). While this effect is reversible, HHQ-exposed phytoplankton were also protected from viral mortality, ascribing a new role of quorum-sensing signals in regulating multitrophic interactions. Furthermore, our data demonstrate that in situ measurements of HHQ coincide with areas of enhanced micro- and nanoplankton biomass. Our results suggest bacterial communication signals as emerging players that may be one of the contributing factors that help structure complex microbial communities throughout the ocean.
    Description: Funding for this work was supported by an NSF grant (OCE-1657808) awarded to K.E.W. and E.L.H. K.E.W. was also supported by a faculty research grant from Haverford College as well as funding from the Koshland Integrated Natural Science Center and Green Fund at Haverford College. E.L.H. was also supported by a Sloan Foundation research fellowship. B.L.N. was supported by an NSF grant (OCE-1633939). M.C.M. was supported by an NIH training grant (T32 HG000035). Mass spectrometry was partially supported by the University of Washington Proteomics Resource (UWPR95794). D.R. was supported by funding through the Gordon and Betty Moore Foundation (grant 6000), a Simons Collaboration for Ocean Processes and Ecology grant (329108), and an NSF grant (OCE-1736280). R.B. was supported by an NSF graduate research fellowship and an NSF grant (OCE-1829761).
    Repository Name: Woods Hole Open Access Server
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  • 9
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    NCBI accession numbers and related metadata from a study of transcriptomic response of Emiliania huxleyi to 2-heptyl-4-quinolone (HHQ) (2020)
    Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu
    Details
    Publication Date: 2022-05-26
    Description: Dataset: Transcriptomic response of Emiliania huxleyi to HHQ
    Description: NCBI accession numbers and related metadata from a study of transcriptomic response of Emiliania huxleyi to 2-heptyl-4-quinolone (HHQ). Sequences from this study are available at the NCBI GEO under accession series GSE131846 https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?&acc=GSE131846 For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/773272
    Description: NSF Division of Ocean Sciences (NSF OCE) OCE-1657808, NSF Division of Ocean Sciences (NSF OCE) OCE-1657818
    Repository Name: Woods Hole Open Access Server
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  • 10
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    Evidence for strain-specific exometabolomic responses of the coccolithophore Emiliania huxleyi to grazing by the dinoflagellate oxyrrhis marina (2017)
    Frontiers Media
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Marine Science 3 (2016): 1, doi:10.3389/fmars.2016.00001.
    Description: The coccolithophore Emiliania huxleyi forms massive blooms and plays a critical role in global elemental cycles, sequestering significant amounts of atmospheric carbon dioxide on geological time scales via production of calcium carbonate coccoliths and emitting dimethyl sulfoniopropionate (DMSP), which has the potential for increasing atmosph-eric albedo. Because grazing in pelagic systems is a major top-down force structuring microbial communities, the influence of grazers on E. huxleyi populations has been of interest to researchers. Roles of DMSP (and related metabolites) in interactions between E. huxleyi and protist grazers have been investigated, however, little is known about the release of other metabolites that may influence, or be influenced by, such grazing interactions. We used high-resolution mass spectrometry in an untargeted approach to survey the suite of low molecular weight compounds released by four different E. huxleyi strains in response to grazing by the dinoflagellate Oxyrrhis marina. Overall, a strikingly small number of metabolites were detected from E. huxleyi and O. marina cells, but these were distinctly informative to construct metabolic footprints. At most, E. huxleyi strains shared 25% of released metabolites. Furthermore, there appeared to be no unified metabolic response in E. huxleyi strains to grazing; rather, these responses were strain specific. Concentrations of several metabolites also positively correlated with grazer activities, including grazing, ingestion, and growth rates; however, no single metabolite responded uniformly across all strains of E. huxleyi tested. Regardless, grazing clearly transformed the constituents of dissolved organic matter produced by these marine microbes. This study addresses several technical challenges, and presents a platform to further study the influence of chemical cues in aquatic systems and demonstrates the impact of strain diversity and grazing on the complexity of dissolved organic matter in marine systems.
    Description: Funding for this work was provided by the Gordon and Betty Moore Foundation, Grant #3301 awarded to A Vardi, BAS. Van Mooy, K Bidle, MJ, and TM. Additional funding for this work was provided by an award from the Flatley Discovery Lab to TM.
    Keywords: Dissolved organic matter ; Environmental metabolomics ; Grazing ; Metabolic footprinting ; Phytoplankton
    Repository Name: Woods Hole Open Access Server
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