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Litter Breakdown and Microbial Succession on Two Submerged Leaf Species in a Small Forested Stream

Identifieur interne : 000031 ( Pmc/Checkpoint ); précédent : 000030; suivant : 000032

Litter Breakdown and Microbial Succession on Two Submerged Leaf Species in a Small Forested Stream

Auteurs : Molli M. Newman ; Mark R. Liles ; Jack W. Feminella

Source :

RBID : PMC:4476575

Abstract

Microbial succession during leaf breakdown was investigated in a small forested stream in west-central Georgia, USA, using multiple culture-independent techniques. Red maple (Acer rubrum) and water oak (Quercus nigra) leaf litter were incubated in situ for 128 days, and litter breakdown was quantified by ash-free dry mass (AFDM) method and microbial assemblage composition using phospholipid fatty acid analysis (PLFA), ribosomal intergenic spacer analysis (RISA), denaturing gradient gel electrophoresis (DGGE), and bar-coded next-generation sequencing of 16S rRNA gene amplicons. Leaf breakdown was faster for red maple than water oak. PLFA revealed a significant time effect on microbial lipid profiles for both leaf species. Microbial assemblages on maple contained a higher relative abundance of bacterial lipids than oak, and oak microbial assemblages contained higher relative abundance of fungal lipids than maple. RISA showed that incubation time was more important in structuring bacterial assemblages than leaf physicochemistry. DGGE profiles revealed high variability in bacterial assemblages over time, and sequencing of DGGE-resolved amplicons indicated several taxa present on degrading litter. Next-generation sequencing revealed temporal shifts in dominant taxa within the phylum Proteobacteria, whereas γ-Proteobacteria dominated pre-immersion and α- and β-Proteobacteria dominated after 1 month of instream incubation; the latter groups contain taxa that are predicted to be capable of using organic material to fuel further breakdown. Our results suggest that incubation time is more important than leaf species physicochemistry in influencing leaf litter microbial assemblage composition, and indicate the need for investigation into seasonal and temporal dynamics of leaf litter microbial assemblage succession.


Url:
DOI: 10.1371/journal.pone.0130801
PubMed: 26098687
PubMed Central: 4476575


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PMC:4476575

Le document en format XML

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<p>Microbial succession during leaf breakdown was investigated in a small forested stream in west-central Georgia, USA, using multiple culture-independent techniques. Red maple (
<italic>Acer rubrum</italic>
) and water oak (
<italic>Quercus nigra</italic>
) leaf litter were incubated
<italic>in situ</italic>
for 128 days, and litter breakdown was quantified by ash-free dry mass (AFDM) method and microbial assemblage composition using phospholipid fatty acid analysis (PLFA), ribosomal intergenic spacer analysis (RISA), denaturing gradient gel electrophoresis (DGGE), and bar-coded next-generation sequencing of 16S rRNA gene amplicons. Leaf breakdown was faster for red maple than water oak. PLFA revealed a significant time effect on microbial lipid profiles for both leaf species. Microbial assemblages on maple contained a higher relative abundance of bacterial lipids than oak, and oak microbial assemblages contained higher relative abundance of fungal lipids than maple. RISA showed that incubation time was more important in structuring bacterial assemblages than leaf physicochemistry. DGGE profiles revealed high variability in bacterial assemblages over time, and sequencing of DGGE-resolved amplicons indicated several taxa present on degrading litter. Next-generation sequencing revealed temporal shifts in dominant taxa within the phylum
<italic>Proteobacteria</italic>
, whereas γ-
<italic>Proteobacteria</italic>
dominated pre-immersion and α- and β-
<italic>Proteobacteria</italic>
dominated after 1 month of instream incubation; the latter groups contain taxa that are predicted to be capable of using organic material to fuel further breakdown. Our results suggest that incubation time is more important than leaf species physicochemistry in influencing leaf litter microbial assemblage composition, and indicate the need for investigation into seasonal and temporal dynamics of leaf litter microbial assemblage succession.</p>
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<journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
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<issn pub-type="epub">1932-6203</issn>
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<publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, CA USA</publisher-loc>
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<article-id pub-id-type="pmid">26098687</article-id>
<article-id pub-id-type="pmc">4476575</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0130801</article-id>
<article-id pub-id-type="publisher-id">PONE-D-14-54995</article-id>
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<subj-group subj-group-type="heading">
<subject>Research Article</subject>
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<title-group>
<article-title>Litter Breakdown and Microbial Succession on Two Submerged Leaf Species in a Small Forested Stream</article-title>
<alt-title alt-title-type="running-head">Microbial Succession on Leaf Litter during Instream Litter Breakdown</alt-title>
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<contrib contrib-type="author">
<name>
<surname>Newman</surname>
<given-names>Molli M.</given-names>
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<xref rid="cor001" ref-type="corresp">*</xref>
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<contrib contrib-type="author">
<name>
<surname>Liles</surname>
<given-names>Mark R.</given-names>
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<contrib contrib-type="author">
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<surname>Feminella</surname>
<given-names>Jack W.</given-names>
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</contrib-group>
<aff id="aff001">
<addr-line>Department of Biological Sciences, Auburn University, Auburn, Alabama, United States of America</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Smidt</surname>
<given-names>Hauke</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">
<addr-line>Wageningen University, NETHERLANDS</addr-line>
</aff>
<author-notes>
<fn fn-type="conflict" id="coi001">
<p>
<bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con" id="contrib001">
<p>Conceived and designed the experiments: MMN MRL JWF. Performed the experiments: MMN. Analyzed the data: MMN. Contributed reagents/materials/analysis tools: MRL JWF. Wrote the paper: MMN MRL JWF.</p>
</fn>
<corresp id="cor001">* E-mail:
<email>ramsemm@auburn.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>22</day>
<month>6</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<year>2015</year>
</pub-date>
<volume>10</volume>
<issue>6</issue>
<elocation-id>e0130801</elocation-id>
<history>
<date date-type="received">
<day>12</day>
<month>12</month>
<year>2014</year>
</date>
<date date-type="accepted">
<day>25</day>
<month>5</month>
<year>2015</year>
</date>
</history>
<permissions>
<copyright-year>2015</copyright-year>
<copyright-holder>Newman et al</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
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="pone.0130801.pdf"></self-uri>
<abstract>
<p>Microbial succession during leaf breakdown was investigated in a small forested stream in west-central Georgia, USA, using multiple culture-independent techniques. Red maple (
<italic>Acer rubrum</italic>
) and water oak (
<italic>Quercus nigra</italic>
) leaf litter were incubated
<italic>in situ</italic>
for 128 days, and litter breakdown was quantified by ash-free dry mass (AFDM) method and microbial assemblage composition using phospholipid fatty acid analysis (PLFA), ribosomal intergenic spacer analysis (RISA), denaturing gradient gel electrophoresis (DGGE), and bar-coded next-generation sequencing of 16S rRNA gene amplicons. Leaf breakdown was faster for red maple than water oak. PLFA revealed a significant time effect on microbial lipid profiles for both leaf species. Microbial assemblages on maple contained a higher relative abundance of bacterial lipids than oak, and oak microbial assemblages contained higher relative abundance of fungal lipids than maple. RISA showed that incubation time was more important in structuring bacterial assemblages than leaf physicochemistry. DGGE profiles revealed high variability in bacterial assemblages over time, and sequencing of DGGE-resolved amplicons indicated several taxa present on degrading litter. Next-generation sequencing revealed temporal shifts in dominant taxa within the phylum
<italic>Proteobacteria</italic>
, whereas γ-
<italic>Proteobacteria</italic>
dominated pre-immersion and α- and β-
<italic>Proteobacteria</italic>
dominated after 1 month of instream incubation; the latter groups contain taxa that are predicted to be capable of using organic material to fuel further breakdown. Our results suggest that incubation time is more important than leaf species physicochemistry in influencing leaf litter microbial assemblage composition, and indicate the need for investigation into seasonal and temporal dynamics of leaf litter microbial assemblage succession.</p>
</abstract>
<funding-group>
<funding-statement>This work was funded by the Auburn University Graduate School. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts>
<fig-count count="6"></fig-count>
<table-count count="1"></table-count>
<page-count count="22"></page-count>
</counts>
<custom-meta-group>
<custom-meta id="data-availability">
<meta-name>Data Availability</meta-name>
<meta-value>All relevant data, excluding sequences, can be found within the paper. All sequence files are currently available from the Sequence Read Archive (accession number SRP033423).</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes>
<title>Data Availability</title>
<p>All relevant data, excluding sequences, can be found within the paper. All sequence files are currently available from the Sequence Read Archive (accession number SRP033423).</p>
</notes>
</front>
</pmc>
<affiliations>
<list></list>
<tree>
<noCountry>
<name sortKey="Feminella, Jack W" sort="Feminella, Jack W" uniqKey="Feminella J" first="Jack W." last="Feminella">Jack W. Feminella</name>
<name sortKey="Liles, Mark R" sort="Liles, Mark R" uniqKey="Liles M" first="Mark R." last="Liles">Mark R. Liles</name>
<name sortKey="Newman, Molli M" sort="Newman, Molli M" uniqKey="Newman M" first="Molli M." last="Newman">Molli M. Newman</name>
</noCountry>
</tree>
</affiliations>
</record>

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