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Metagenomic evidence for reciprocal particle exchange between the mainstem estuary and lateral bay sediments of the lower Columbia River

Identifieur interne : 000087 ( Pmc/Checkpoint ); précédent : 000086; suivant : 000088

Metagenomic evidence for reciprocal particle exchange between the mainstem estuary and lateral bay sediments of the lower Columbia River

Auteurs : Maria W. Smith [États-Unis] ; Richard E. Davis [États-Unis] ; Nicholas D. Youngblut [États-Unis] ; Tuomas K Rn [États-Unis] ; Lydie Herfort [États-Unis] ; Rachel J. Whitaker [États-Unis] ; William W. Metcalf [États-Unis] ; Bradley M. Tebo [États-Unis] ; Ant Nio M. Baptista [États-Unis] ; Holly M. Simon [États-Unis]

Source :

RBID : PMC:4589670

Abstract

Lateral bays of the lower Columbia River estuary are areas of enhanced water retention that influence net ecosystem metabolism through activities of their diverse microbial communities. Metagenomic characterization of sediment microbiota from three disparate sites in two brackish lateral bays (Baker and Youngs) produced ∼100 Gbp of DNA sequence data analyzed subsequently for predicted SSU rRNA and peptide-coding genes. The metagenomes were dominated by Bacteria. A large component of Eukaryota was present in Youngs Bay samples, i.e., the inner bay sediment was enriched with the invasive New Zealand mudsnail, Potamopyrgus antipodarum, known for high ammonia production. The metagenome was also highly enriched with an archaeal ammonia oxidizer closely related to Nitrosoarchaeum limnia. Combined analysis of sequences and continuous, high-resolution time series of biogeochemical data from fixed and mobile platforms revealed the importance of large-scale reciprocal particle exchanges between the mainstem estuarine water column and lateral bay sediments. Deposition of marine diatom particles in sediments near Youngs Bay mouth was associated with a dramatic enrichment of Bacteroidetes (58% of total Bacteria) and corresponding genes involved in phytoplankton polysaccharide degradation. The Baker Bay sediment metagenome contained abundant Archaea, including diverse methanogens, as well as functional genes for methylotrophy and taxonomic markers for syntrophic bacteria, suggesting that active methane cycling occurs at this location. Our previous work showed enrichments of similar anaerobic taxa in particulate matter of the mainstem estuarine water column. In total, our results identify the lateral bays as both sources and sinks of biogenic particles significantly impacting microbial community composition and biogeochemical activities in the estuary.


Url:
DOI: 10.3389/fmicb.2015.01074
PubMed: 26483785
PubMed Central: 4589670


Affiliations:


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PMC:4589670

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<p>Lateral bays of the lower Columbia River estuary are areas of enhanced water retention that influence net ecosystem metabolism through activities of their diverse microbial communities. Metagenomic characterization of sediment microbiota from three disparate sites in two brackish lateral bays (Baker and Youngs) produced ∼100 Gbp of DNA sequence data analyzed subsequently for predicted SSU rRNA and peptide-coding genes. The metagenomes were dominated by Bacteria. A large component of Eukaryota was present in Youngs Bay samples, i.e., the inner bay sediment was enriched with the invasive New Zealand mudsnail,
<italic>Potamopyrgus antipodarum</italic>
, known for high ammonia production. The metagenome was also highly enriched with an archaeal ammonia oxidizer closely related to
<italic>Nitrosoarchaeum limnia</italic>
. Combined analysis of sequences and continuous, high-resolution time series of biogeochemical data from fixed and mobile platforms revealed the importance of large-scale reciprocal particle exchanges between the mainstem estuarine water column and lateral bay sediments. Deposition of marine diatom particles in sediments near Youngs Bay mouth was associated with a dramatic enrichment of Bacteroidetes (58% of total Bacteria) and corresponding genes involved in phytoplankton polysaccharide degradation. The Baker Bay sediment metagenome contained abundant Archaea, including diverse methanogens, as well as functional genes for methylotrophy and taxonomic markers for syntrophic bacteria, suggesting that active methane cycling occurs at this location. Our previous work showed enrichments of similar anaerobic taxa in particulate matter of the mainstem estuarine water column. In total, our results identify the lateral bays as both sources and sinks of biogenic particles significantly impacting microbial community composition and biogeochemical activities in the estuary.</p>
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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Front Microbiol</journal-id>
<journal-id journal-id-type="iso-abbrev">Front Microbiol</journal-id>
<journal-id journal-id-type="publisher-id">Front. Microbiol.</journal-id>
<journal-title-group>
<journal-title>Frontiers in Microbiology</journal-title>
</journal-title-group>
<issn pub-type="epub">1664-302X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">26483785</article-id>
<article-id pub-id-type="pmc">4589670</article-id>
<article-id pub-id-type="doi">10.3389/fmicb.2015.01074</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Microbiology</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Metagenomic evidence for reciprocal particle exchange between the mainstem estuary and lateral bay sediments of the lower Columbia River</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Smith</surname>
<given-names>Maria W.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/75948/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Davis</surname>
<given-names>Richard E.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/182485/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Youngblut</surname>
<given-names>Nicholas D.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/63352/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kärnä</surname>
<given-names>Tuomas</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/260376/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Herfort</surname>
<given-names>Lydie</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/179465/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Whitaker</surname>
<given-names>Rachel J.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/54914/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Metcalf</surname>
<given-names>William W.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/54876/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Tebo</surname>
<given-names>Bradley M.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/18550/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Baptista</surname>
<given-names>António M.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/256816/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Simon</surname>
<given-names>Holly M.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/25158/overview"></uri>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Center for Coastal Margin Observation and Prediction and Institute of Environmental Health, Oregon Health & Science University, Portland</institution>
<country>OR, USA</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Department of Crop and Soil Sciences, Cornell University, Ithaca</institution>
<country>NY, USA</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Department of Microbiology, University of Illinois at Urbana-Champaign, Urbana</institution>
<country>IL, USA</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by:
<italic>Hongyue Dang, Xiamen University, China</italic>
</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by:
<italic>Jennifer F. Biddle, University of Delaware, USA; Ian Salter, Alfred Wegener Institute, Germany</italic>
</p>
</fn>
<corresp id="fn001">*Correspondence:
<italic>Holly M. Simon, Center for Coastal Margin Observation and Prediction and Institute of Environmental Health, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, OR 97239, USA,
<email xlink:type="simple">simonh@ohsu.edu</email>
</italic>
</corresp>
<fn fn-type="other" id="fn002">
<p>This article was submitted to Aquatic Microbiology, a section of the journal Frontiers in Microbiology</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>01</day>
<month>10</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<year>2015</year>
</pub-date>
<volume>6</volume>
<elocation-id>1074</elocation-id>
<history>
<date date-type="received">
<day>27</day>
<month>5</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>18</day>
<month>9</month>
<year>2015</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2015 Smith, Davis, Youngblut, Kärnä, Herfort, Whitaker, Metcalf, Tebo, Baptista and Simon.</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>Smith, Davis, Youngblut, Kärnä, Herfort, Whitaker, Metcalf, Tebo, Baptista and Simon</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p>
</license>
</permissions>
<abstract>
<p>Lateral bays of the lower Columbia River estuary are areas of enhanced water retention that influence net ecosystem metabolism through activities of their diverse microbial communities. Metagenomic characterization of sediment microbiota from three disparate sites in two brackish lateral bays (Baker and Youngs) produced ∼100 Gbp of DNA sequence data analyzed subsequently for predicted SSU rRNA and peptide-coding genes. The metagenomes were dominated by Bacteria. A large component of Eukaryota was present in Youngs Bay samples, i.e., the inner bay sediment was enriched with the invasive New Zealand mudsnail,
<italic>Potamopyrgus antipodarum</italic>
, known for high ammonia production. The metagenome was also highly enriched with an archaeal ammonia oxidizer closely related to
<italic>Nitrosoarchaeum limnia</italic>
. Combined analysis of sequences and continuous, high-resolution time series of biogeochemical data from fixed and mobile platforms revealed the importance of large-scale reciprocal particle exchanges between the mainstem estuarine water column and lateral bay sediments. Deposition of marine diatom particles in sediments near Youngs Bay mouth was associated with a dramatic enrichment of Bacteroidetes (58% of total Bacteria) and corresponding genes involved in phytoplankton polysaccharide degradation. The Baker Bay sediment metagenome contained abundant Archaea, including diverse methanogens, as well as functional genes for methylotrophy and taxonomic markers for syntrophic bacteria, suggesting that active methane cycling occurs at this location. Our previous work showed enrichments of similar anaerobic taxa in particulate matter of the mainstem estuarine water column. In total, our results identify the lateral bays as both sources and sinks of biogenic particles significantly impacting microbial community composition and biogeochemical activities in the estuary.</p>
</abstract>
<kwd-group>
<kwd>metagenome analysis</kwd>
<kwd>Columbia River estuary</kwd>
<kwd>lateral bay sediments</kwd>
<kwd>particle exchange</kwd>
<kwd>methane cycling</kwd>
</kwd-group>
<funding-group>
<award-group>
<funding-source id="cn001">National Science Foundation
<named-content content-type="fundref-id">10.13039/100000001</named-content>
</funding-source>
<award-id rid="cn001">OCE 0424602, MCB 0644468</award-id>
</award-group>
</funding-group>
<counts>
<fig-count count="12"></fig-count>
<table-count count="3"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="84"></ref-count>
<page-count count="20"></page-count>
<word-count count="0"></word-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>États-Unis</li>
</country>
</list>
<tree>
<country name="États-Unis">
<noRegion>
<name sortKey="Smith, Maria W" sort="Smith, Maria W" uniqKey="Smith M" first="Maria W." last="Smith">Maria W. Smith</name>
</noRegion>
<name sortKey="Baptista, Ant Nio M" sort="Baptista, Ant Nio M" uniqKey="Baptista A" first="Ant Nio M." last="Baptista">Ant Nio M. Baptista</name>
<name sortKey="Davis, Richard E" sort="Davis, Richard E" uniqKey="Davis R" first="Richard E." last="Davis">Richard E. Davis</name>
<name sortKey="Herfort, Lydie" sort="Herfort, Lydie" uniqKey="Herfort L" first="Lydie" last="Herfort">Lydie Herfort</name>
<name sortKey="K Rn, Tuomas" sort="K Rn, Tuomas" uniqKey="K Rn T" first="Tuomas" last="K Rn">Tuomas K Rn</name>
<name sortKey="Metcalf, William W" sort="Metcalf, William W" uniqKey="Metcalf W" first="William W." last="Metcalf">William W. Metcalf</name>
<name sortKey="Simon, Holly M" sort="Simon, Holly M" uniqKey="Simon H" first="Holly M." last="Simon">Holly M. Simon</name>
<name sortKey="Tebo, Bradley M" sort="Tebo, Bradley M" uniqKey="Tebo B" first="Bradley M." last="Tebo">Bradley M. Tebo</name>
<name sortKey="Whitaker, Rachel J" sort="Whitaker, Rachel J" uniqKey="Whitaker R" first="Rachel J." last="Whitaker">Rachel J. Whitaker</name>
<name sortKey="Youngblut, Nicholas D" sort="Youngblut, Nicholas D" uniqKey="Youngblut N" first="Nicholas D." last="Youngblut">Nicholas D. Youngblut</name>
</country>
</tree>
</affiliations>
</record>

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