Chisholm
Sallie W.
Chisholm
Sallie W.
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PreprintCorrigendum "Portal protein diversity and phage ecology"( 2011-10) Sullivan, Matthew B. ; Coleman, Maureen L. ; Quinlivan, Vanessa ; Rosenkrantz, Jessica E. ; DeFrancesco, Alicia S. ; Tan, G. ; Fu, Ross ; Lee, Jessica A. ; Waterbury, John B. ; Bielawski, Joseph P. ; Chisholm, Sallie W.
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ArticleTemporal dynamics of Prochlorococcus cells with the potential for nitrate assimilation in the subtropical Atlantic and Pacific oceans(Elsevier B.V., 2015-10-30) Berube, Paul M. ; Coe, Allison ; Roggensack, Sara E. ; Chisholm, Sallie W.
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ArticleThree Prochlorococcus cyanophage genomes : signature features and ecological interpretations(Public Library of Science (PLoS), 2005-04-19) Sullivan, Matthew B. ; Coleman, Maureen L. ; Weigele, Peter ; Rohwer, Forest ; Chisholm, Sallie W.The oceanic cyanobacteria Prochlorococcus are globally important, ecologically diverse primary producers. It is thought that their viruses (phages) mediate population sizes and affect the evolutionary trajectories of their hosts. Here we present an analysis of genomes from three Prochlorococcus phages: a podovirus and two myoviruses. The morphology, overall genome features, and gene content of these phages suggest that they are quite similar to T7-like (P-SSP7) and T4-like (P-SSM2 and P-SSM4) phages. Using the existing phage taxonomic framework as a guideline, we examined genome sequences to establish ‘‘core’’ genes for each phage group. We found the podovirus contained 15 of 26 core T7-like genes and the two myoviruses contained 43 and 42 of 75 core T4-like genes. In addition to these core genes, each genome contains a significant number of ‘‘cyanobacterial’’ genes, i.e., genes with significant best BLAST hits to genes found in cyanobacteria. Some of these, we speculate, represent ‘‘signature’’ cyanophage genes. For example, all three phage genomes contain photosynthetic genes (psbA, hliP) that are thought to help maintain host photosynthetic activity during infection, as well as an aldolase family gene (talC) that could facilitate alternative routes of carbon metabolism during infection. The podovirus genome also contains an integrase gene (int) and other features that suggest it is capable of integrating into its host. If indeed it is, this would be unprecedented among cultured T7-like phages or marine cyanophages and would have significant evolutionary and ecological implications for phage and host. Further, both myoviruses contain phosphate-inducible genes (phoH and pstS) that are likely to be important for phage and host responses to phosphate stress, a commonly limiting nutrient in marine systems. Thus, these marine cyanophages appear to be variations of two well-known phages—T7 and T4—but contain genes that, if functional, reflect adaptations for infection of photosynthetic hosts in low-nutrient oceanic environments.
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DatasetProchlorococcus cell concentrations during the BiG-RAPA expedition (Cruise MV1015) in the Peru Current and Eastern South Pacific Subtropical Gyre between November and December of 2010(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2023-01-30) Berube, Paul ; Berta-Thompson, Jessica ; Coe, Allison ; Chisholm, Sallie W.These data include Prochlorococcus cell concentrations (total cell densities by flow cytometry and cell densities for specific ecotypes/clades determined by quantitative PCR). Samples were collected during the C-MORE Biogeochemical Gradients Role in Arranging Planktonic Assemblages (BiG-RAPA) expedition (Cruise MV1015) in the Peru Current and Eastern South Pacific Subtropical Gyre between dates 2010-11-19 and 2010-12-10 along a zonal transect from the northern coast of Chile to the island of Rapa Nui. Prochlorococcus is an important primary producer in the oligotrophic South Pacific Gyre and these data facilitate studies examining Prochlorococcus' ecology. 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/886299
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ArticleResolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences(American Society for Microbiology, 2002-03) Rocap, Gabrielle ; Distel, Daniel L. ; Waterbury, John B. ; Chisholm, Sallie W.Cultured isolates of the marine cyanobacteria Prochlorococcus and Synechococcus vary widely in their pigment compositions and growth responses to light and nutrients, yet show greater than 96% identity in their 16S ribosomal DNA (rDNA) sequences. In order to better define the genetic variation that accompanies their physiological diversity, sequences for the 16S-23S rDNA internal transcribed spacer (ITS) region were determined in 32 Prochlorococcus isolates and 25 Synechococcus isolates from around the globe. Each strain examined yielded one ITS sequence that contained two tRNA genes. Dramatic variations in the length and G+C content of the spacer were observed among the strains, particularly among Prochlorococcus strains. Secondary-structure models of the ITS were predicted in order to facilitate alignment of the sequences for phylogenetic analyses. The previously observed division of Prochlorococcus into two ecotypes (called high and low-B/A after their differences in chlorophyll content) were supported, as was the subdivision of the high-B/A ecotype into four genetically distinct clades. ITS-based phylogenies partitioned marine cluster A Synechococcus into six clades, three of which can be associated with a particular phenotype (motility, chromatic adaptation, and lack of phycourobilin). The pattern of sequence divergence within and between clades is suggestive of a mode of evolution driven by adaptive sweeps and implies that each clade represents an ecologically distinct population. Furthermore, many of the clades consist of strains isolated from disparate regions of the world's oceans, implying that they are geographically widely distributed. These results provide further evidence that natural populations of Prochlorococcus and Synechococcus consist of multiple coexisting ecotypes, genetically closely related but physiologically distinct, which may vary in relative abundance with changing environmental conditions.
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ArticlePortal protein diversity and phage ecology(Society for Applied Microbiology and Blackwell Publishing, 2008-07-31) Sullivan, Matthew B. ; Coleman, Maureen L. ; Quinlivan, Vanessa ; Rosenkrantz, Jessica E. ; DeFrancesco, Alicia S. ; Tan, G. ; Fu, Ross ; Lee, Jessica A. ; Waterbury, John B. ; Bielawski, Joseph P. ; Chisholm, Sallie W.Oceanic phages are critical components of the global ecosystem, where they play a role in microbial mortality and evolution. Our understanding of phage diversity is greatly limited by the lack of useful genetic diversity measures. Previous studies, focusing on myophages that infect the marine cyanobacterium Synechococcus, have used the coliphage T4 portal-protein-encoding homologue, gene 20 (g20), as a diversity marker. These studies revealed 10 sequence clusters, 9 oceanic and 1 freshwater, where only 3 contained cultured representatives. We sequenced g20 from 38 marine myophages isolated using a diversity of Synechococcus and Prochlorococcus hosts to see if any would fall into the clusters that lacked cultured representatives. On the contrary, all fell into the three clusters that already contained sequences from cultured phages. Further, there was no obvious relationship between host of isolation, or host range, and g20 sequence similarity. We next expanded our analyses to all available g20 sequences (769 sequences), which include PCR amplicons from wild uncultured phages, non-PCR amplified sequences identified in the Global Ocean Survey (GOS) metagenomic database, as well as sequences from cultured phages, to evaluate the relationship between g20 sequence clusters and habitat features from which the phage sequences were isolated. Even in this meta-data set, very few sequences fell into the sequence clusters without cultured representatives, suggesting that the latter are very rare, or sequencing artefacts. In contrast, sequences most similar to the culture-containing clusters, the freshwater cluster and two novel clusters, were more highly represented, with one particular culture-containing cluster representing the dominant g20 genotype in the unamplified GOS sequence data. Finally, while some g20 sequences were non-randomly distributed with respect to habitat, there were always numerous exceptions to general patterns, indicating that phage portal proteins are not good predictors of a phage's host or the habitat in which a particular phage may thrive.
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ArticlePhosphonate production by marine microbes: exploring new sources and potential function(National Academy of Sciences, 2022-03-07) Acker, Marianne ; Hogle, Shane L. ; Berube, Paul M. ; Hackl, Thomas ; Coe, Allison ; Stepanauskas, Ramunas ; Chisholm, Sallie W. ; Repeta, Daniel J.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.
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ArticleClosely related phytoplankton species produce similar suites of dissolved organic matter(Frontiers Media, 2014-03-28) Becker, Jamie W. ; Berube, Paul M. ; Follett, Christopher L. ; Waterbury, John B. ; Chisholm, Sallie W. ; DeLong, Edward F. ; Repeta, Daniel J.Production of dissolved organic matter (DOM) by marine phytoplankton supplies the majority of organic substrate consumed by heterotrophic bacterioplankton in the sea. This production and subsequent consumption converts a vast quantity of carbon, nitrogen, and phosphorus between organic and inorganic forms, directly impacting global cycles of these biologically important elements. Details regarding the chemical composition of DOM produced by marine phytoplankton are sparse, and while often assumed, it is not currently known if phylogenetically distinct groups of marine phytoplankton release characteristic suites of DOM. To investigate the relationship between specific phytoplankton groups and the DOM they release, hydrophobic phytoplankton-derived dissolved organic matter (DOMP) from eight axenic strains was analyzed using high-performance liquid chromatography coupled to mass spectrometry (HPLC-MS). Identification of DOM features derived from Prochlorococcus, Synechococcus, Thalassiosira, and Phaeodactylum revealed DOMP to be complex and highly strain dependent. Connections between DOMP features and the phylogenetic relatedness of these strains were identified on multiple levels of phylogenetic distance, suggesting that marine phytoplankton produce DOM that in part reflects its phylogenetic origin. Chemical information regarding the size and polarity ranges of features from defined biological sources was also obtained. Our findings reveal DOMP composition to be partially conserved among related phytoplankton species, and implicate marine DOM as a potential factor influencing microbial diversity in the sea by acting as a link between autotrophic and heterotrophic microbial community structures.
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ArticleProchlorococcus extracellular vesicles: molecular composition and adsorption to diverse microbes(Society for Applied Microbiology, 2021-11-12) Biller, Steven J. ; Lundeen, Rachel A. ; Hmelo, Laura R. ; Becker, Kevin W. ; Arellano, Aldo A. ; Dooley, Keven ; Heal, Katherine R. ; Carlson, Laura Truxal ; Van Mooy, Benjamin A. S. ; Ingalls, Anitra ; Chisholm, Sallie W.Extracellular vesicles are small (~50–200 nm diameter) membrane-bound structures released by cells from all domains of life. While vesicles are abundant in the oceans, their functions, both for cells themselves and the emergent ecosystem, remain a mystery. To better characterize these particles – a prerequisite for determining function – we analysed the lipid, protein, and metabolite content of vesicles produced by the marine cyanobacterium Prochlorococcus. We show that Prochlorococcus exports a diverse array of cellular compounds into the surrounding seawater enclosed within discrete vesicles. Vesicles produced by two different strains contain some materials in common, but also display numerous strain-specific differences, reflecting functional complexity within vesicle populations. The vesicles contain active enzymes, indicating that they can mediate extracellular biogeochemical reactions in the ocean. We further demonstrate that vesicles from Prochlorococcus and other bacteria associate with diverse microbes including the most abundant marine bacterium, Pelagibacter. Together, our data point toward hypotheses concerning the functional roles of vesicles in marine ecosystems including, but not limited to, possibly mediating energy and nutrient transfers, catalysing extracellular biochemical reactions, and mitigating toxicity of reactive oxygen species.
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DatasetThe abundance of Prochlorococcus cells containing the nitrate reductase gene (narB) at the HOT and BATS sites in the Pacific and Atlantic Oceans between October 2005 and January 2008(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2016-05-10) Chisholm, Sallie W.Two year time series of the abundance of Prochlorococcus cells containing the nitrate reductase gene (narB) at the HOT and BATS sites in the Pacific and Atlantic Oceans. The goal was to collect long-term, high-resolution data on the temporal and spatial variability of Prochlorococcus narB genotypes belonging to the HLII and LLI clades. The abundance of Prochlorococcus cells containing narB for each of these clades was determined by quantitative PCR at 12 depths every month from October 2005 to December 2007 at two locations: BATS location (5 nautical mile radius around 31 40'N, 64 10'W) and HOT Station ALOHA (5 nautical mile radius around 22 45'N, 158 00' W). For a complete list of measurements, refer to the supplemental document 'Field_names.pdf', and a full dataset description is included in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: http://www.bco-dmo.org/dataset/641495
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ArticleChitin utilization by marine picocyanobacteria and the evolution of a planktonic lifestyle(National Academy of Sciences, 2023-05-16) Capovilla, Giovanna ; Braakman, Rogier ; Fournier, Gregory P. ; Hackl, Thomas ; Schwartzman, Julia ; Lu, Xinda ; Yelton, Alexis ; Longnecker, Krista ; Soule, Melissa C. Kido ; Thomas, Elaina ; Swarr, Gretchen ; Mongera, Alessandro ; Payette, Jack G. ; Castro, Kurt G. ; Waldbauer, Jacob R. ; Kujawinski, Elizabeth B. ; Cordero, Otto X. ; Chisholm, Sallie W.Marine picocyanobacteria Prochlorococcus and Synechococcus, the most abundant photosynthetic cells in the oceans, are generally thought to have a primarily single-celled and free-living lifestyle. However, while studying the ability of picocyanobacteria to supplement photosynthetic carbon fixation with the use of exogenous organic carbon, we found the widespread occurrence of genes for breaking down chitin, an abundant source of organic carbon that exists primarily as particles. We show that cells that encode a chitin degradation pathway display chitin degradation activity, attach to chitin particles, and show enhanced growth under low light conditions when exposed to chitosan, a partially deacetylated soluble form of chitin. Marine chitin is largely derived from arthropods, which underwent major diversifications 520 to 535 Mya, close to when marine picocyanobacteria are inferred to have appeared in the ocean. Phylogenetic analyses confirm that the chitin utilization trait was acquired at the root of marine picocyanobacteria. Together this leads us to postulate that attachment to chitin particles allowed benthic cyanobacteria to emulate their mat-based lifestyle in the water column, initiating their expansion into the open ocean, seeding the rise of modern marine ecosystems. Subsequently, transitioning to a constitutive planktonic life without chitin associations led to cellular and genomic streamlining along a major early branch within Prochlorococcus. Our work highlights how the emergence of associations between organisms from different trophic levels, and their coevolution, creates opportunities for colonizing new environments. In this view, the rise of ecological complexity and the expansion of the biosphere are deeply intertwined processes.