Transcriptional Changes Underlying Elemental Stoichiometry Shifts in a Marine Heterotrophic Bacterium
Identifieur interne : 000370 ( Pmc/Checkpoint ); précédent : 000369; suivant : 000371Transcriptional Changes Underlying Elemental Stoichiometry Shifts in a Marine Heterotrophic Bacterium
Auteurs : Leong-Keat Chan [États-Unis] ; Ryan J. Newton [États-Unis] ; Shalabh Sharma [États-Unis] ; Christa B. Smith [États-Unis] ; Pratibha Rayapati [États-Unis] ; Alexander J. Limardo [États-Unis] ; Christof Meile [États-Unis] ; Mary Ann Moran [États-Unis]Source :
- Frontiers in Microbiology [ 1664-302X ] ; 2012.
Abstract
Marine bacteria drive the biogeochemical processing of oceanic dissolved organic carbon (DOC), a 750-Tg C reservoir that is a critical component of the global C cycle. Catabolism of DOC is thought to be regulated by the biomass composition of heterotrophic bacteria, as cells maintain a C:N:P ratio of ∼50:10:1 during DOC processing. Yet a complicating factor in stoichiometry-based analyses is that bacteria can change the C:N:P ratio of their biomass in response to resource composition. We investigated the physiological mechanisms of resource-driven shifts in biomass stoichiometry in continuous cultures of the marine heterotrophic bacterium
Url:
DOI: 10.3389/fmicb.2012.00159
PubMed: 22783226
PubMed Central: 3390766
Affiliations:
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Transcriptional Changes Underlying Elemental Stoichiometry Shifts in a Marine Heterotrophic Bacterium</title>
<author><name sortKey="Chan, Leong Keat" sort="Chan, Leong Keat" uniqKey="Chan L" first="Leong-Keat" last="Chan">Leong-Keat Chan</name>
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<country>Milwaukee, WI, USA</country>
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<author><name sortKey="Rayapati, Pratibha" sort="Rayapati, Pratibha" uniqKey="Rayapati P" first="Pratibha" last="Rayapati">Pratibha Rayapati</name>
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<author><name sortKey="Meile, Christof" sort="Meile, Christof" uniqKey="Meile C" first="Christof" last="Meile">Christof Meile</name>
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<author><name sortKey="Moran, Mary Ann" sort="Moran, Mary Ann" uniqKey="Moran M" first="Mary Ann" last="Moran">Mary Ann Moran</name>
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<series><title level="j">Frontiers in Microbiology</title>
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<front><div type="abstract" xml:lang="en"><p>Marine bacteria drive the biogeochemical processing of oceanic dissolved organic carbon (DOC), a 750-Tg C reservoir that is a critical component of the global C cycle. Catabolism of DOC is thought to be regulated by the biomass composition of heterotrophic bacteria, as cells maintain a C:N:P ratio of ∼50:10:1 during DOC processing. Yet a complicating factor in stoichiometry-based analyses is that bacteria can change the C:N:P ratio of their biomass in response to resource composition. We investigated the physiological mechanisms of resource-driven shifts in biomass stoichiometry in continuous cultures of the marine heterotrophic bacterium <italic>Ruegeria pomeroyi</italic>
(a member of the <italic>Roseobacter</italic>
clade) under four element limitation regimes (C, N, P, and S). Microarray analysis indicated that the bacterium scavenged for alternate sources of the scarce element when cells were C-, N-, or P-limited; reworked the ratios of biomolecules when C- and P- limited; and exerted tighter control over import/export and cytoplasmic pools when N-limited. Under S limitation, a scenario not existing naturally for surface ocean microbes, stress responses dominated transcriptional changes. Resource-driven changes in C:N ratios of up to 2.5-fold and in C:P ratios of up to sixfold were measured in <italic>R. pomeroyi</italic>
biomass. These changes were best explained if the C and P content of the cells was flexible in the face of shifting resources but N content was not, achieved through the net balance of different transcriptional strategies. The cellular-level metabolic trade-offs that govern biomass stoichiometry in <italic>R. pomeroyi</italic>
may have implications for global carbon cycling if extendable to other heterotrophic bacteria. Strong homeostatic responses to N limitation by marine bacteria would intensify competition with autotrophs. Modification of cellular inventories in C- and P-limited heterotrophs would vary the elemental ratio of particulate organic matter sequestered in the deep ocean.</p>
</div>
</front>
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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. Microbio.</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 Research Foundation</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">22783226</article-id>
<article-id pub-id-type="pmc">3390766</article-id>
<article-id pub-id-type="doi">10.3389/fmicb.2012.00159</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>Transcriptional Changes Underlying Elemental Stoichiometry Shifts in a Marine Heterotrophic Bacterium</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Chan</surname>
<given-names>Leong-Keat</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn002"><sup>†</sup>
</xref>
<xref ref-type="author-notes" rid="fn003"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Newton</surname>
<given-names>Ryan J.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn003"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sharma</surname>
<given-names>Shalabh</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Smith</surname>
<given-names>Christa B.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rayapati</surname>
<given-names>Pratibha</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn002"><sup>†</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Limardo</surname>
<given-names>Alexander J.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Meile</surname>
<given-names>Christof</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Moran</surname>
<given-names>Mary Ann</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">*</xref>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup>
<institution>Department of Marine Sciences, University of Georgia</institution>
<country>Athens, GA, USA</country>
</aff>
<aff id="aff2"><sup>2</sup>
<institution>Great Lakes WATER Institute, University of Wisconsin-Milwaukee</institution>
<country>Milwaukee, WI, USA</country>
</aff>
<author-notes><fn fn-type="edited-by"><p>Edited by: James Cotner, University of Minnesota, USA</p>
</fn>
<fn fn-type="edited-by"><p>Reviewed by: Katherine McMahon, University of Wisconsin-Madison, USA; Edward Hall, United States Geological Survey, USA</p>
</fn>
<corresp id="fn001">*Correspondence: Mary Ann Moran, Department of Marine Sciences, University of Georgia, Athens, GA 30602-3636, USA. e-mail: <email>mmoran@uga.edu</email>
</corresp>
<fn fn-type="present-address" id="fn002"><p><sup>†</sup>
Present address: Leong-Keat Chan, DOE Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA, USA; Pratibha Rayapati, Georgia Health Sciences University, Augusta, GA, USA.</p>
</fn>
<fn fn-type="other" id="fn003"><p><sup>‡</sup>
Leong-Keat Chan and Ryan J. Newton have contributed equally to this work.</p>
</fn>
<fn fn-type="other" id="fn004"><p>This article was submitted to Frontiers in Aquatic Microbiology, a specialty of Frontiers in Microbiology.</p>
</fn>
</author-notes>
<pub-date pub-type="epub"><day>16</day>
<month>5</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="collection"><year>2012</year>
</pub-date>
<volume>3</volume>
<elocation-id>159</elocation-id>
<history><date date-type="received"><day>31</day>
<month>12</month>
<year>2011</year>
</date>
<date date-type="accepted"><day>09</day>
<month>4</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2012 Chan, Newton, Sharma, Smith, Rayapati, Limardo, Meile and Moran.</copyright-statement>
<copyright-year>2012</copyright-year>
<license license-type="open-access" xlink:href="http://www.frontiersin.org/licenseagreement"><license-p>This is an open-access article distributed under the terms of the <uri xlink:type="simple" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/">Creative Commons Attribution Non Commercial License</uri>
, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.</license-p>
</license>
</permissions>
<abstract><p>Marine bacteria drive the biogeochemical processing of oceanic dissolved organic carbon (DOC), a 750-Tg C reservoir that is a critical component of the global C cycle. Catabolism of DOC is thought to be regulated by the biomass composition of heterotrophic bacteria, as cells maintain a C:N:P ratio of ∼50:10:1 during DOC processing. Yet a complicating factor in stoichiometry-based analyses is that bacteria can change the C:N:P ratio of their biomass in response to resource composition. We investigated the physiological mechanisms of resource-driven shifts in biomass stoichiometry in continuous cultures of the marine heterotrophic bacterium <italic>Ruegeria pomeroyi</italic>
(a member of the <italic>Roseobacter</italic>
clade) under four element limitation regimes (C, N, P, and S). Microarray analysis indicated that the bacterium scavenged for alternate sources of the scarce element when cells were C-, N-, or P-limited; reworked the ratios of biomolecules when C- and P- limited; and exerted tighter control over import/export and cytoplasmic pools when N-limited. Under S limitation, a scenario not existing naturally for surface ocean microbes, stress responses dominated transcriptional changes. Resource-driven changes in C:N ratios of up to 2.5-fold and in C:P ratios of up to sixfold were measured in <italic>R. pomeroyi</italic>
biomass. These changes were best explained if the C and P content of the cells was flexible in the face of shifting resources but N content was not, achieved through the net balance of different transcriptional strategies. The cellular-level metabolic trade-offs that govern biomass stoichiometry in <italic>R. pomeroyi</italic>
may have implications for global carbon cycling if extendable to other heterotrophic bacteria. Strong homeostatic responses to N limitation by marine bacteria would intensify competition with autotrophs. Modification of cellular inventories in C- and P-limited heterotrophs would vary the elemental ratio of particulate organic matter sequestered in the deep ocean.</p>
</abstract>
<kwd-group><kwd>elemental stoichiometry</kwd>
<kwd>element limitation</kwd>
<kwd>microarray</kwd>
<kwd>chemostat</kwd>
<kwd><italic>Ruegeria pomeroyi</italic>
DSS-3</kwd>
</kwd-group>
<counts><fig-count count="6"></fig-count>
<table-count count="9"></table-count>
<equation-count count="1"></equation-count>
<ref-count count="81"></ref-count>
<page-count count="24"></page-count>
<word-count count="12180"></word-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>États-Unis</li>
</country>
</list>
<tree><country name="États-Unis"><noRegion><name sortKey="Chan, Leong Keat" sort="Chan, Leong Keat" uniqKey="Chan L" first="Leong-Keat" last="Chan">Leong-Keat Chan</name>
</noRegion>
<name sortKey="Limardo, Alexander J" sort="Limardo, Alexander J" uniqKey="Limardo A" first="Alexander J." last="Limardo">Alexander J. Limardo</name>
<name sortKey="Meile, Christof" sort="Meile, Christof" uniqKey="Meile C" first="Christof" last="Meile">Christof Meile</name>
<name sortKey="Moran, Mary Ann" sort="Moran, Mary Ann" uniqKey="Moran M" first="Mary Ann" last="Moran">Mary Ann Moran</name>
<name sortKey="Newton, Ryan J" sort="Newton, Ryan J" uniqKey="Newton R" first="Ryan J." last="Newton">Ryan J. Newton</name>
<name sortKey="Newton, Ryan J" sort="Newton, Ryan J" uniqKey="Newton R" first="Ryan J." last="Newton">Ryan J. Newton</name>
<name sortKey="Rayapati, Pratibha" sort="Rayapati, Pratibha" uniqKey="Rayapati P" first="Pratibha" last="Rayapati">Pratibha Rayapati</name>
<name sortKey="Sharma, Shalabh" sort="Sharma, Shalabh" uniqKey="Sharma S" first="Shalabh" last="Sharma">Shalabh Sharma</name>
<name sortKey="Smith, Christa B" sort="Smith, Christa B" uniqKey="Smith C" first="Christa B." last="Smith">Christa B. Smith</name>
</country>
</tree>
</affiliations>
</record>
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