Metatranscriptome analyses indicate resource partitioning between diatoms in the field
Diverse communities of marine phytoplankton carry out half of global primary production. The vast diversity of the phytoplankton has long perplexed ecologists because these organisms coexist in an isotropic environment while competing for the same basic resources (e.g., inorganic nutrients). Differe...
Gespeichert in:
Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2015-04, Vol.112 (17), p.E2182-E2190 |
---|---|
Hauptverfasser: | , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | E2190 |
---|---|
container_issue | 17 |
container_start_page | E2182 |
container_title | Proceedings of the National Academy of Sciences - PNAS |
container_volume | 112 |
creator | Alexander, Harriet Jenkins, Bethany D. Rynearson, Tatiana A. Dyhrman, Sonya T. |
description | Diverse communities of marine phytoplankton carry out half of global primary production. The vast diversity of the phytoplankton has long perplexed ecologists because these organisms coexist in an isotropic environment while competing for the same basic resources (e.g., inorganic nutrients). Differential niche partitioning of resources is one hypothesis to explain this “paradox of the plankton,” but it is difficult to quantify and track variation in phytoplankton metabolism in situ. Here, we use quantitative metatranscriptome analyses to examine pathways of nitrogen (N) and phosphorus (P) metabolism in diatoms that cooccur regularly in an estuary on the east coast of the United States (Narragansett Bay). Expression of known N and P metabolic pathways varied between diatoms, indicating apparent differences in resource utilization capacity that may prevent direct competition. Nutrient amendment incubations skewed N/P ratios, elucidating nutrient-responsive patterns of expression and facilitating a quantitative comparison between diatoms. The resource-responsive (RR) gene sets deviated in composition from the metabolic profile of the organism, being enriched in genes associated with N and P metabolism. Expression of the RR gene set varied over time and differed significantly between diatoms, resulting in opposite transcriptional responses to the same environment. Apparent differences in metabolic capacity and the expression of that capacity in the environment suggest that diatom-specific resource partitioning was occurring in Narragansett Bay. This high-resolution approach highlights the molecular underpinnings of diatom resource utilization and how cooccurring diatoms adjust their cellular physiology to partition their niche space.
Significance Nutrient availability plays a central role in driving the activities and large-scale distributions of phytoplankton, yet there are still fundamental gaps in understanding how phytoplankton metabolize nutrients, like nitrogen (N) and phosphorus (P), and how this metabolic potential is modulated in field populations. Here, we show that cooccurring diatoms in a dynamic coastal marine system have apparent differences in their metabolic capacity to use N and P. Further, bioinformatic approaches enabled the identification and species-specific comparison of resource-responsive (RR) genes. Variation of these RR gene sets highlights the disparate transcriptional responses these species have to the same environment, which likel |
doi_str_mv | 10.1073/pnas.1421993112 |
format | Article |
fullrecord | <record><control><sourceid>jstor_pubme</sourceid><recordid>TN_cdi_jstor_primary_26462605</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>26462605</jstor_id><sourcerecordid>26462605</sourcerecordid><originalsourceid>FETCH-LOGICAL-c525t-53b653d8291fbfb1555f9d7e19cad99df849a07e9f7bf4ecb061c584f0bf402b3</originalsourceid><addsrcrecordid>eNqNkU1v1DAQhiMEokvhzAmIxIVL2hnHju0LEqrKh1TEAcrVcpLx1qtsEmwvqP8eh122wImTZc0zj8fzFsVThDMEWZ_Po41nyBlqXSOye8UKQWPVcA33ixUAk5XijJ8Uj2LcAIAWCh4WJ0woCUzrVfH1IyWbgh1jF_ycpi2VdrTDbaRY-rH3nU1UBorTLnRUzjYkn_w0-nFdtpR-EI1l723uW_Ay3VDpPA394-KBs0OkJ4fztLh-e_nl4n119endh4s3V1UnmEiVqNtG1L1iGl3rWhRCON1LQt3ZXuveKa4tSNJOto5T10KDnVDcQb4Ca-vT4vXeO-_aLfUdjfkvg5mD39pwaybrzd-V0d-Y9fTdcI5KNTwLXh0EYfq2o5jM1seOhsGONO2iwUbJRkPe1n-gUtZSoVAZffkPuskLzHv9Jcwuxvjy9vme6sIUYyB3nBvBLPGaJV5zF2_ueP7nd4_87zwzUB6ApfOoQ2ZQmkuGanE82yObmKZwp2h4wxoQuf5iX3d2MnYdfDTXnxlgA4C1EnmKn6DIv_I</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1680232244</pqid></control><display><type>article</type><title>Metatranscriptome analyses indicate resource partitioning between diatoms in the field</title><source>PubMed (Medline)</source><source>MEDLINE</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><source>JSTOR</source><creator>Alexander, Harriet ; Jenkins, Bethany D. ; Rynearson, Tatiana A. ; Dyhrman, Sonya T.</creator><creatorcontrib>Alexander, Harriet ; Jenkins, Bethany D. ; Rynearson, Tatiana A. ; Dyhrman, Sonya T.</creatorcontrib><description>Diverse communities of marine phytoplankton carry out half of global primary production. The vast diversity of the phytoplankton has long perplexed ecologists because these organisms coexist in an isotropic environment while competing for the same basic resources (e.g., inorganic nutrients). Differential niche partitioning of resources is one hypothesis to explain this “paradox of the plankton,” but it is difficult to quantify and track variation in phytoplankton metabolism in situ. Here, we use quantitative metatranscriptome analyses to examine pathways of nitrogen (N) and phosphorus (P) metabolism in diatoms that cooccur regularly in an estuary on the east coast of the United States (Narragansett Bay). Expression of known N and P metabolic pathways varied between diatoms, indicating apparent differences in resource utilization capacity that may prevent direct competition. Nutrient amendment incubations skewed N/P ratios, elucidating nutrient-responsive patterns of expression and facilitating a quantitative comparison between diatoms. The resource-responsive (RR) gene sets deviated in composition from the metabolic profile of the organism, being enriched in genes associated with N and P metabolism. Expression of the RR gene set varied over time and differed significantly between diatoms, resulting in opposite transcriptional responses to the same environment. Apparent differences in metabolic capacity and the expression of that capacity in the environment suggest that diatom-specific resource partitioning was occurring in Narragansett Bay. This high-resolution approach highlights the molecular underpinnings of diatom resource utilization and how cooccurring diatoms adjust their cellular physiology to partition their niche space.
Significance Nutrient availability plays a central role in driving the activities and large-scale distributions of phytoplankton, yet there are still fundamental gaps in understanding how phytoplankton metabolize nutrients, like nitrogen (N) and phosphorus (P), and how this metabolic potential is modulated in field populations. Here, we show that cooccurring diatoms in a dynamic coastal marine system have apparent differences in their metabolic capacity to use N and P. Further, bioinformatic approaches enabled the identification and species-specific comparison of resource-responsive (RR) genes. Variation of these RR gene sets highlights the disparate transcriptional responses these species have to the same environment, which likely reflects the role resource partitioning has in facilitating the vast diversity of the phytoplankton.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1421993112</identifier><identifier>PMID: 25870299</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Algae ; Bacillariophyceae ; Bays - microbiology ; Biological Sciences ; Diatoms - physiology ; Marine ecology ; Metabolism ; Metagenomics ; Nitrogen ; Nitrogen - metabolism ; Phosphorus ; Phosphorus - metabolism ; Physical Sciences ; Phytoplankton - physiology ; Plankton ; PNAS Plus ; Transcriptome - physiology ; United States</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2015-04, Vol.112 (17), p.E2182-E2190</ispartof><rights>Volumes 1–89 and 106–112, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Apr 28, 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c525t-53b653d8291fbfb1555f9d7e19cad99df849a07e9f7bf4ecb061c584f0bf402b3</citedby><cites>FETCH-LOGICAL-c525t-53b653d8291fbfb1555f9d7e19cad99df849a07e9f7bf4ecb061c584f0bf402b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/112/17.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26462605$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26462605$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,728,781,785,804,886,27926,27927,53793,53795,58019,58252</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25870299$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Alexander, Harriet</creatorcontrib><creatorcontrib>Jenkins, Bethany D.</creatorcontrib><creatorcontrib>Rynearson, Tatiana A.</creatorcontrib><creatorcontrib>Dyhrman, Sonya T.</creatorcontrib><title>Metatranscriptome analyses indicate resource partitioning between diatoms in the field</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Diverse communities of marine phytoplankton carry out half of global primary production. The vast diversity of the phytoplankton has long perplexed ecologists because these organisms coexist in an isotropic environment while competing for the same basic resources (e.g., inorganic nutrients). Differential niche partitioning of resources is one hypothesis to explain this “paradox of the plankton,” but it is difficult to quantify and track variation in phytoplankton metabolism in situ. Here, we use quantitative metatranscriptome analyses to examine pathways of nitrogen (N) and phosphorus (P) metabolism in diatoms that cooccur regularly in an estuary on the east coast of the United States (Narragansett Bay). Expression of known N and P metabolic pathways varied between diatoms, indicating apparent differences in resource utilization capacity that may prevent direct competition. Nutrient amendment incubations skewed N/P ratios, elucidating nutrient-responsive patterns of expression and facilitating a quantitative comparison between diatoms. The resource-responsive (RR) gene sets deviated in composition from the metabolic profile of the organism, being enriched in genes associated with N and P metabolism. Expression of the RR gene set varied over time and differed significantly between diatoms, resulting in opposite transcriptional responses to the same environment. Apparent differences in metabolic capacity and the expression of that capacity in the environment suggest that diatom-specific resource partitioning was occurring in Narragansett Bay. This high-resolution approach highlights the molecular underpinnings of diatom resource utilization and how cooccurring diatoms adjust their cellular physiology to partition their niche space.
Significance Nutrient availability plays a central role in driving the activities and large-scale distributions of phytoplankton, yet there are still fundamental gaps in understanding how phytoplankton metabolize nutrients, like nitrogen (N) and phosphorus (P), and how this metabolic potential is modulated in field populations. Here, we show that cooccurring diatoms in a dynamic coastal marine system have apparent differences in their metabolic capacity to use N and P. Further, bioinformatic approaches enabled the identification and species-specific comparison of resource-responsive (RR) genes. Variation of these RR gene sets highlights the disparate transcriptional responses these species have to the same environment, which likely reflects the role resource partitioning has in facilitating the vast diversity of the phytoplankton.</description><subject>Algae</subject><subject>Bacillariophyceae</subject><subject>Bays - microbiology</subject><subject>Biological Sciences</subject><subject>Diatoms - physiology</subject><subject>Marine ecology</subject><subject>Metabolism</subject><subject>Metagenomics</subject><subject>Nitrogen</subject><subject>Nitrogen - metabolism</subject><subject>Phosphorus</subject><subject>Phosphorus - metabolism</subject><subject>Physical Sciences</subject><subject>Phytoplankton - physiology</subject><subject>Plankton</subject><subject>PNAS Plus</subject><subject>Transcriptome - physiology</subject><subject>United States</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU1v1DAQhiMEokvhzAmIxIVL2hnHju0LEqrKh1TEAcrVcpLx1qtsEmwvqP8eh122wImTZc0zj8fzFsVThDMEWZ_Po41nyBlqXSOye8UKQWPVcA33ixUAk5XijJ8Uj2LcAIAWCh4WJ0woCUzrVfH1IyWbgh1jF_ycpi2VdrTDbaRY-rH3nU1UBorTLnRUzjYkn_w0-nFdtpR-EI1l723uW_Ay3VDpPA394-KBs0OkJ4fztLh-e_nl4n119endh4s3V1UnmEiVqNtG1L1iGl3rWhRCON1LQt3ZXuveKa4tSNJOto5T10KDnVDcQb4Ca-vT4vXeO-_aLfUdjfkvg5mD39pwaybrzd-V0d-Y9fTdcI5KNTwLXh0EYfq2o5jM1seOhsGONO2iwUbJRkPe1n-gUtZSoVAZffkPuskLzHv9Jcwuxvjy9vme6sIUYyB3nBvBLPGaJV5zF2_ueP7nd4_87zwzUB6ApfOoQ2ZQmkuGanE82yObmKZwp2h4wxoQuf5iX3d2MnYdfDTXnxlgA4C1EnmKn6DIv_I</recordid><startdate>20150428</startdate><enddate>20150428</enddate><creator>Alexander, Harriet</creator><creator>Jenkins, Bethany D.</creator><creator>Rynearson, Tatiana A.</creator><creator>Dyhrman, Sonya T.</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>5PM</scope></search><sort><creationdate>20150428</creationdate><title>Metatranscriptome analyses indicate resource partitioning between diatoms in the field</title><author>Alexander, Harriet ; Jenkins, Bethany D. ; Rynearson, Tatiana A. ; Dyhrman, Sonya T.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c525t-53b653d8291fbfb1555f9d7e19cad99df849a07e9f7bf4ecb061c584f0bf402b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Algae</topic><topic>Bacillariophyceae</topic><topic>Bays - microbiology</topic><topic>Biological Sciences</topic><topic>Diatoms - physiology</topic><topic>Marine ecology</topic><topic>Metabolism</topic><topic>Metagenomics</topic><topic>Nitrogen</topic><topic>Nitrogen - metabolism</topic><topic>Phosphorus</topic><topic>Phosphorus - metabolism</topic><topic>Physical Sciences</topic><topic>Phytoplankton - physiology</topic><topic>Plankton</topic><topic>PNAS Plus</topic><topic>Transcriptome - physiology</topic><topic>United States</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Alexander, Harriet</creatorcontrib><creatorcontrib>Jenkins, Bethany D.</creatorcontrib><creatorcontrib>Rynearson, Tatiana A.</creatorcontrib><creatorcontrib>Dyhrman, Sonya T.</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Alexander, Harriet</au><au>Jenkins, Bethany D.</au><au>Rynearson, Tatiana A.</au><au>Dyhrman, Sonya T.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Metatranscriptome analyses indicate resource partitioning between diatoms in the field</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2015-04-28</date><risdate>2015</risdate><volume>112</volume><issue>17</issue><spage>E2182</spage><epage>E2190</epage><pages>E2182-E2190</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Diverse communities of marine phytoplankton carry out half of global primary production. The vast diversity of the phytoplankton has long perplexed ecologists because these organisms coexist in an isotropic environment while competing for the same basic resources (e.g., inorganic nutrients). Differential niche partitioning of resources is one hypothesis to explain this “paradox of the plankton,” but it is difficult to quantify and track variation in phytoplankton metabolism in situ. Here, we use quantitative metatranscriptome analyses to examine pathways of nitrogen (N) and phosphorus (P) metabolism in diatoms that cooccur regularly in an estuary on the east coast of the United States (Narragansett Bay). Expression of known N and P metabolic pathways varied between diatoms, indicating apparent differences in resource utilization capacity that may prevent direct competition. Nutrient amendment incubations skewed N/P ratios, elucidating nutrient-responsive patterns of expression and facilitating a quantitative comparison between diatoms. The resource-responsive (RR) gene sets deviated in composition from the metabolic profile of the organism, being enriched in genes associated with N and P metabolism. Expression of the RR gene set varied over time and differed significantly between diatoms, resulting in opposite transcriptional responses to the same environment. Apparent differences in metabolic capacity and the expression of that capacity in the environment suggest that diatom-specific resource partitioning was occurring in Narragansett Bay. This high-resolution approach highlights the molecular underpinnings of diatom resource utilization and how cooccurring diatoms adjust their cellular physiology to partition their niche space.
Significance Nutrient availability plays a central role in driving the activities and large-scale distributions of phytoplankton, yet there are still fundamental gaps in understanding how phytoplankton metabolize nutrients, like nitrogen (N) and phosphorus (P), and how this metabolic potential is modulated in field populations. Here, we show that cooccurring diatoms in a dynamic coastal marine system have apparent differences in their metabolic capacity to use N and P. Further, bioinformatic approaches enabled the identification and species-specific comparison of resource-responsive (RR) genes. Variation of these RR gene sets highlights the disparate transcriptional responses these species have to the same environment, which likely reflects the role resource partitioning has in facilitating the vast diversity of the phytoplankton.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>25870299</pmid><doi>10.1073/pnas.1421993112</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0027-8424 |
ispartof | Proceedings of the National Academy of Sciences - PNAS, 2015-04, Vol.112 (17), p.E2182-E2190 |
issn | 0027-8424 1091-6490 |
language | eng |
recordid | cdi_jstor_primary_26462605 |
source | PubMed (Medline); MEDLINE; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry; JSTOR |
subjects | Algae Bacillariophyceae Bays - microbiology Biological Sciences Diatoms - physiology Marine ecology Metabolism Metagenomics Nitrogen Nitrogen - metabolism Phosphorus Phosphorus - metabolism Physical Sciences Phytoplankton - physiology Plankton PNAS Plus Transcriptome - physiology United States |
title | Metatranscriptome analyses indicate resource partitioning between diatoms in the field |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-17T22%3A37%3A35IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Metatranscriptome%20analyses%20indicate%20resource%20partitioning%20between%20diatoms%20in%20the%20field&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Alexander,%20Harriet&rft.date=2015-04-28&rft.volume=112&rft.issue=17&rft.spage=E2182&rft.epage=E2190&rft.pages=E2182-E2190&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.1421993112&rft_dat=%3Cjstor_pubme%3E26462605%3C/jstor_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1680232244&rft_id=info:pmid/25870299&rft_jstor_id=26462605&rfr_iscdi=true |