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ArticleThe mutual interplay between calcification and coccolithovirus infection(Wiley, 2018-07-24) Johns, Christopher T. ; Grubb, Austin R. ; Nissimov, Jozef I. ; Natale, Frank ; Knapp, Viki ; Mui, Alwin ; Fredricks, Helen F. ; Van Mooy, Benjamin A. S. ; Bidle, Kay D.Two prominent characteristics of marine coccolithophores are their secretion of coccoliths and their susceptibility to infection by coccolithoviruses (EhVs), both of which display variation among cells in culture and in natural populations. We examined the impact of calcification on infection by challenging a variety of Emiliania huxleyi strains at different calcification states with EhVs of different virulence. Reduced cellular calcification was associated with increased infection and EhV production, even though calcified cells and associated coccoliths had significantly higher adsorption coefficients than non‐calcified (naked) cells. Sialic acid glycosphingolipids, molecules thought to mediate EhV infection, were generally more abundant in calcified cells and enriched in purified, sorted coccoliths, suggesting a biochemical link between calcification and adsorption rates. In turn, viable EhVs impacted cellular calcification absent of lysis by inducing dramatic shifts in optical side scatter signals and a massive release of detached coccoliths in a subpopulation of cells, which could be triggered by resuspension of healthy, calcified host cells in an EhV‐free, ‘induced media’. Our findings show that calcification is a key component of the E. huxleyi‐EhV arms race and an aspect that is critical both to the modelling of these host–virus interactions in the ocean and interpreting their impact on the global carbon cycle.
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ArticleVirus infection of Haptolina ericina and Phaeocystis pouchetii implicates evolutionary conservation of programmed cell death induction in marine haptophyte–virus interactions(Oxford University Press, 2014-05-05) Ray, Jessica L. ; Haramaty, Liti ; Thyrhaug, Runar ; Fredricks, Helen F. ; Van Mooy, Benjamin A. S. ; Larsen, Aud ; Bidle, Kay D. ; Sandaa, Ruth-AnneThe mechanisms by which phytoplankton cope with stressors in the marine environment are neither fully characterized nor understood. As viruses are the most abundant entities in the global ocean and represent a strong top-down regulator of phytoplankton abundance and diversity, we sought to characterize the cellular response of two marine haptophytes to virus infection in order to gain more knowledge about the nature and diversity of microalgal responses to this chronic biotic stressor. We infected laboratory cultures of the haptophytes Haptolina ericina and Phaeocystis pouchetii with CeV-01B or PpV-01B dsDNA viruses, respectively, and assessed the extent to which host cellular responses resemble programmed cell death (PCD) through the activation of diagnostic molecular and biochemical markers. Pronounced DNA fragmentation and activation of cysteine aspartate-specific proteases (caspases) were only detected in virus-infected cultures of these phytoplankton. Inhibition of host caspase activity by addition of the pan-caspase inhibitor z-VAD-fmk did not impair virus production in either host–virus system, differentiating it from the Emiliania huxleyi-Coccolithovirus model of haptophyte–virus interactions. Nonetheless, our findings point to a general conservation of PCD-like activation during virus infection in ecologically diverse haptophytes, with the subtle heterogeneity of cell death biochemical responses possibly exerting differential regulation on phytoplankton abundance and diversity.
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DatasetDissolved nutrients from Espelandsvegen Fjord, Bergen Norway, May 2017(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2021-01-06) Thamatrakoln, Kimberlee ; Bidle, Kay D.This dataset includes dissolved nutrient concentrations from seawater collected in the Norwegian National Mesocosm Centre at the Espegrend (Espeland) Marine Biological Station near Bergen, Norway, 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/752737
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DatasetNiskin bottle data, including salinity, O2, temperature, conductivity, etc, from R/V Knorr cruise KN207-03 in the North Atlantic (transect from Ponta Delgada, Azores to Reykjavik, Iceland) in 2012 (NA-VICE project)(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2019-10-28) Bidle, Kay D ; DiTullio, Giacomo ; Van Mooy, Benjamin A.S. ; Coolen, Marco ; Vardi, AssafNiskin bottle data, including salinity, O2, temperature, conductivity, etc, from R/V Knorr cruise KN207-03 in the North Atlantic (transect from Ponta Delgada, Azores to Reykjavik, Iceland) in 2012 (NA-VICE project). 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/3902
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DatasetTransparent exopolymer particle (TEP) measurements from the MesoHux mesocosm experiment held in May 2017(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2021-05-19) Johnson, Matthew D. ; Bidle, Kay D. ; Harvey, ElizabethTransparent 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
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ArticleThe possession of coccoliths fails to deter microzooplankton grazers(Frontiers Media, 2020-12-02) Mayers, Kyle M. J. ; Poulton, Alex J. ; Bidle, Kay D. ; Thamatrakoln, Kimberlee ; Schieler, Brittany ; Giering, Sarah L. C. ; Wells, Seona R. ; Tarran, Glen A. ; Mayor, Daniel J. ; Johnson, Matthew D. ; Riebesell, Ulf ; Larsen, Aud ; Vardi, Assaf ; Harvey, Elizabeth L.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.
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DatasetBacteria cell counts and virus-like particle abundances from Espelandsvegen Fjord, Bergen Norway, May 2017(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2021-01-06) Thamatrakoln, Kimberlee ; Bidle, Kay D.This dataset includes bacterial and virus abundances using flow cytometry from seawater collected in the Norwegian National Mesocosm Centre at the Espegrend (Espeland) Marine Biological Station near Bergen, Norway, 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/752722
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PreprintConsequences of strain variability and calcification in Emiliania huxleyi on microzooplankton grazing( 2015-08-04) Harvey, Elizabeth L. ; Bidle, Kay D. ; Johnson, Matthew D.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.
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ArticleThe Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP) : illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing(Public Library of Science, 2014-06-24) Keeling, Patrick J. ; Burki, Fabien ; Wilcox, Heather M. ; Allam, Bassem ; Allen, Eric E. ; Amaral-Zettler, Linda A. ; Armbrust, E. Virginia ; Archibald, John M. ; Bharti, Arvind K. ; Bell, Callum J. ; Beszteri, Bank ; Bidle, Kay D. ; Cameron, Connor T. ; Campbell, Lisa ; Caron, David A. ; Cattolico, Rose Ann ; Collier, Jackie L. ; Coyne, Kathryn J. ; Davy, Simon K. ; Deschamps, Phillipe ; Dyhrman, Sonya T. ; Edvardsen, Bente ; Gates, Ruth D. ; Gobler, Christopher J. ; Greenwood, Spencer J. ; Guida, Stephanie M. ; Jacobi, Jennifer L. ; Jakobsen, Kjetill S. ; James, Erick R. ; Jenkins, Bethany D. ; John, Uwe ; Johnson, Matthew D. ; Juhl, Andrew R. ; Kamp, Anja ; Katz, Laura A. ; Kiene, Ronald P. ; Kudryavtsev, Alexander N. ; Leander, Brian S. ; Lin, Senjie ; Lovejoy, Connie ; Lynn, Denis ; Marchetti, Adrian ; McManus, George ; Nedelcu, Aurora M. ; Menden-Deuer, Susanne ; Miceli, Cristina ; Mock, Thomas ; Montresor, Marina ; Moran, Mary Ann ; Murray, Shauna A. ; Nadathur, Govind ; Nagai, Satoshi ; Ngam, Peter B. ; Palenik, Brian ; Pawlowski, Jan ; Petroni, Giulio ; Piganeau, Gwenael ; Posewitz, Matthew C. ; Rengefors, Karin ; Romano, Giovanna ; Rumpho, Mary E. ; Rynearson, Tatiana A. ; Schilling, Kelly B. ; Schroeder, Declan C. ; Simpson, Alastair G. B. ; Slamovits, Claudio H. ; Smith, David R. ; Smith, G. Jason ; Smith, Sarah R. ; Sosik, Heidi M. ; Stief, Peter ; Theriot, Edward ; Twary, Scott N. ; Umale, Pooja E. ; Vaulot, Daniel ; Wawrik, Boris ; Wheeler, Glen L. ; Wilson, William H. ; Xu, Yan ; Zingone, Adriana ; Worden, Alexandra Z.Microbial ecology is plagued by problems of an abstract nature. Cell sizes are so small and population sizes so large that both are virtually incomprehensible. Niches are so far from our everyday experience as to make their very definition elusive. Organisms that may be abundant and critical to our survival are little understood, seldom described and/or cultured, and sometimes yet to be even seen. One way to confront these problems is to use data of an even more abstract nature: molecular sequence data. Massive environmental nucleic acid sequencing, such as metagenomics or metatranscriptomics, promises functional analysis of microbial communities as a whole, without prior knowledge of which organisms are in the environment or exactly how they are interacting. But sequence-based ecological studies nearly always use a comparative approach, and that requires relevant reference sequences, which are an extremely limited resource when it comes to microbial eukaryotes. In practice, this means sequence databases need to be populated with enormous quantities of data for which we have some certainties about the source. Most important is the taxonomic identity of the organism from which a sequence is derived and as much functional identification of the encoded proteins as possible. In an ideal world, such information would be available as a large set of complete, well-curated, and annotated genomes for all the major organisms from the environment in question. Reality substantially diverges from this ideal, but at least for bacterial molecular ecology, there is a database consisting of thousands of complete genomes from a wide range of taxa, supplemented by a phylogeny-driven approach to diversifying genomics. For eukaryotes, the number of available genomes is far, far fewer, and we have relied much more heavily on random growth of sequence databases, raising the question as to whether this is fit for purpose.
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ArticleThe multiple fates of sinking particles in the North Atlantic Ocean(John Wiley & Sons, 2015-09-25) Collins, James R. ; Edwards, Bethanie R. ; Thamatrakoln, Kimberlee ; Ossolinski, Justin E. ; DiTullio, Giacomo R. ; Bidle, Kay D. ; Doney, Scott C. ; Van Mooy, Benjamin A. S.The direct respiration of sinking organic matter by attached bacteria is often invoked as the dominant sink for settling particles in the mesopelagic ocean. However, other processes, such as enzymatic solubilization and mechanical disaggregation, also contribute to particle flux attenuation by transferring organic matter to the water column. Here we use observations from the North Atlantic Ocean, coupled to sensitivity analyses of a simple model, to assess the relative importance of particle-attached microbial respiration compared to the other processes that can degrade sinking particles. The observed carbon fluxes, bacterial production rates, and respiration by water column and particle-attached microbial communities each spanned more than an order of magnitude. Rates of substrate-specific respiration on sinking particle material ranged from 0.007 ± 0.003 to 0.173 ± 0.105 day−1. A comparison of these substrate-specific respiration rates with model results suggested sinking particle material was transferred to the water column by various biological and mechanical processes nearly 3.5 times as fast as it was directly respired. This finding, coupled with strong metabolic demand imposed by measurements of water column respiration (729.3 ± 266.0 mg C m−2 d−1, on average, over the 50 to 150 m depth interval), suggested a large fraction of the organic matter evolved from sinking particles ultimately met its fate through subsequent remineralization in the water column. At three sites, we also measured very low bacterial growth efficiencies and large discrepancies between depth-integrated mesopelagic respiration and carbon inputs.
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ArticleTemperature-induced viral resistance in Emiliania huxleyi (Prymnesiophyceae)(Public Library of Science, 2014-11-18) Kendrick, B. Jacob ; DiTullio, Giacomo R. ; Cyronak, Tyler J. ; Fulton, James M. ; Van Mooy, Benjamin A. S. ; Bidle, Kay D.Annual Emiliania huxleyi blooms (along with other coccolithophorid species) play important roles in the global carbon and sulfur cycles. E. huxleyi blooms are routinely terminated by large, host-specific dsDNA viruses, (Emiliania huxleyi Viruses; EhVs), making these host-virus interactions a driving force behind their potential impact on global biogeochemical cycles. Given projected increases in sea surface temperature due to climate change, it is imperative to understand the effects of temperature on E. huxleyi’s susceptibility to viral infection and its production of climatically active dimethylated sulfur species (DSS). Here we demonstrate that a 3°C increase in temperature induces EhV-resistant phenotypes in three E. huxleyi strains and that successful virus infection impacts DSS pool sizes. We also examined cellular polar lipids, given their documented roles in regulating host-virus interactions in this system, and propose that alterations to membrane-bound surface receptors are responsible for the observed temperature-induced resistance. Our findings have potential implications for global biogeochemical cycles in a warming climate and for deciphering the particular mechanism(s) by which some E. huxleyi strains exhibit viral resistance.
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DatasetChlorophyll measurements from the MesoHux mesocosm experiment held in May 2017(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2021-05-19) Johnson, Matthew D. ; Bidle, Kay D. ; Harvey, ElizabethChlorophyll 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
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DatasetScientific sampling event log from R/V Knorr cruise KN207-03 in the North Atlantic (transect from Ponta Delgada, Azores to Reykjavik, Iceland) in 2012 (NA-VICE project)(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2019-03-05) Bidle, Kay DScientific sampling event log from R/V Knorr cruise KN207-03 in the North Atlantic (transect from Ponta Delgada, Azores to Reykjavik, Iceland) in 2012. The scientific sampling event log was created using v1.0 of the Rolling Deck to Repository (R2R) event log application. 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/3739
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ArticleSeasonal mixed layer depth shapes phytoplankton physiology, viral production, and accumulation in the North Atlantic(Nature Research, 2021-11-17) Diaz, Ben P. ; Knowles, Benjamin ; Johns, Christopher T. ; Laber, Christien P. ; Bondoc, Karen Grace V. ; Haramaty, Liti ; Natale, Frank ; Harvey, Elizabeth L. ; Kramer, Sasha J. ; Bolaños, Luis M. ; Lowenstein, Daniel P. ; Fredricks, Helen F. ; Graff, Jason R. ; Westberry, Toby K. ; Mojica, Kristina D. A. ; Haëntjens, Nils ; Baetge, Nicholas ; Gaube, Peter ; Boss, Emmanuel S. ; Carlson, Craig A. ; Behrenfeld, Michael J. ; Van Mooy, Benjamin A. S. ; Bidle, Kay D.Seasonal shifts in phytoplankton accumulation and loss largely follow changes in mixed layer depth, but the impact of mixed layer depth on cell physiology remains unexplored. Here, we investigate the physiological state of phytoplankton populations associated with distinct bloom phases and mixing regimes in the North Atlantic. Stratification and deep mixing alter community physiology and viral production, effectively shaping accumulation rates. Communities in relatively deep, early-spring mixed layers are characterized by low levels of stress and high accumulation rates, while those in the recently shallowed mixed layers in late-spring have high levels of oxidative stress. Prolonged stratification into early autumn manifests in negative accumulation rates, along with pronounced signatures of compromised membranes, death-related protease activity, virus production, nutrient drawdown, and lipid markers indicative of nutrient stress. Positive accumulation renews during mixed layer deepening with transition into winter, concomitant with enhanced nutrient supply and lessened viral pressure.