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Widespread Occurrence of Expressed Fungal Secretory Peroxidases in Forest Soils

Identifieur interne : 000061 ( Pmc/Checkpoint ); précédent : 000060; suivant : 000062

Widespread Occurrence of Expressed Fungal Secretory Peroxidases in Forest Soils

Auteurs : Harald Kellner [Allemagne] ; Patricia Luis [France] ; Marek J. Pecyna [Allemagne] ; Florian Barbi [France] ; Danuta Kapturska [Allemagne] ; Dirk Krüger [Allemagne] ; Donald R. Zak [États-Unis] ; Roland Marmeisse [France] ; Micheline Vandenbol [Belgique] ; Martin Hofrichter [Allemagne]

Source :

RBID : PMC:3999038

Abstract

Fungal secretory peroxidases mediate fundamental ecological functions in the conversion and degradation of plant biomass. Many of these enzymes have strong oxidizing activities towards aromatic compounds and are involved in the degradation of plant cell wall (lignin) and humus. They comprise three major groups: class II peroxidases (including lignin peroxidase, manganese peroxidase, versatile peroxidase and generic peroxidase), dye-decolorizing peroxidases, and heme-thiolate peroxidases (e.g. unspecific/aromatic peroxygenase, chloroperoxidase). Here, we have repeatedly observed a widespread expression of all major peroxidase groups in leaf and needle litter across a range of forest ecosystems (e.g. Fagus, Picea, Acer, Quercus, and Populus spp.), which are widespread in Europe and North America. Manganese peroxidases and unspecific peroxygenases were found expressed in all nine investigated forest sites, and dye-decolorizing peroxidases were observed in five of the nine sites, thereby indicating biological significance of these enzymes for fungal physiology and ecosystem processes. Transcripts of selected secretory peroxidase genes were also analyzed in pure cultures of several litter-decomposing species and other fungi. Using this information, we were able to match, in environmental litter samples, two manganese peroxidase sequences to Mycena galopus and Mycena epipterygia and one unspecific peroxygenase transcript to Mycena galopus, suggesting an important role of this litter- and coarse woody debris-dwelling genus in the disintegration and transformation of litter aromatics and organic matter formation.


Url:
DOI: 10.1371/journal.pone.0095557
PubMed: 24763280
PubMed Central: 3999038


Affiliations:


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PMC:3999038

Le document en format XML

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<name sortKey="Zak, Donald R" sort="Zak, Donald R" uniqKey="Zak D" first="Donald R." last="Zak">Donald R. Zak</name>
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<region type="province" nuts="1">Province de Liège</region>
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<name sortKey="Hofrichter, Martin" sort="Hofrichter, Martin" uniqKey="Hofrichter M" first="Martin" last="Hofrichter">Martin Hofrichter</name>
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<addr-line>Department of Bio- and Environmental Sciences, International Institute Zittau, Technische Universität Dresden, Zittau, Germany</addr-line>
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<title level="j">PLoS ONE</title>
<idno type="eISSN">1932-6203</idno>
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<date when="2014">2014</date>
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<div type="abstract" xml:lang="en">
<p>Fungal secretory peroxidases mediate fundamental ecological functions in the conversion and degradation of plant biomass. Many of these enzymes have strong oxidizing activities towards aromatic compounds and are involved in the degradation of plant cell wall (lignin) and humus. They comprise three major groups: class II peroxidases (including lignin peroxidase, manganese peroxidase, versatile peroxidase and generic peroxidase), dye-decolorizing peroxidases, and heme-thiolate peroxidases (e.g. unspecific/aromatic peroxygenase, chloroperoxidase). Here, we have repeatedly observed a widespread expression of all major peroxidase groups in leaf and needle litter across a range of forest ecosystems (e.g.
<italic>Fagus</italic>
,
<italic>Picea</italic>
,
<italic>Acer</italic>
,
<italic>Quercus</italic>
, and
<italic>Populus</italic>
spp.), which are widespread in Europe and North America. Manganese peroxidases and unspecific peroxygenases were found expressed in all nine investigated forest sites, and dye-decolorizing peroxidases were observed in five of the nine sites, thereby indicating biological significance of these enzymes for fungal physiology and ecosystem processes. Transcripts of selected secretory peroxidase genes were also analyzed in pure cultures of several litter-decomposing species and other fungi. Using this information, we were able to match, in environmental litter samples, two manganese peroxidase sequences to
<italic>Mycena galopus</italic>
and
<italic>Mycena epipterygia</italic>
and one unspecific peroxygenase transcript to
<italic>Mycena galopus</italic>
, suggesting an important role of this litter- and coarse woody debris-dwelling genus in the disintegration and transformation of litter aromatics and organic matter formation.</p>
</div>
</front>
<back>
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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
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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>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group>
<journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher>
<publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">24763280</article-id>
<article-id pub-id-type="pmc">3999038</article-id>
<article-id pub-id-type="publisher-id">PONE-D-13-51780</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0095557</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2">
<subject>Biology and Life Sciences</subject>
<subj-group>
<subject>Biochemistry</subject>
<subj-group>
<subject>Enzymology</subject>
<subj-group>
<subject>Enzymes</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group>
<subject>Ecology</subject>
<subj-group>
<subject>Ecosystems</subject>
<subj-group>
<subject>Ecosystem Functioning</subject>
</subj-group>
</subj-group>
<subj-group>
<subject>Microbial Ecology</subject>
</subj-group>
</subj-group>
<subj-group>
<subject>Microbiology</subject>
<subj-group>
<subject>Microbial Physiology</subject>
<subj-group>
<subject>Fungal Physiology</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group>
<subject>Mycology</subject>
<subj-group>
<subject>Fungal Biochemistry</subject>
</subj-group>
</subj-group>
<subj-group>
<subject>Organisms</subject>
<subj-group>
<subject>Fungi</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2">
<subject>Ecology and Environmental Sciences</subject>
<subj-group>
<subject>Soil Science</subject>
<subj-group>
<subject>Soil Ecology</subject>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Widespread Occurrence of Expressed Fungal Secretory Peroxidases in Forest Soils</article-title>
<alt-title alt-title-type="running-head">Fungal Secretory Peroxidases in Forest Soils</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Kellner</surname>
<given-names>Harald</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>*</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Luis</surname>
<given-names>Patricia</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pecyna</surname>
<given-names>Marek J.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Barbi</surname>
<given-names>Florian</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kapturska</surname>
<given-names>Danuta</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Krüger</surname>
<given-names>Dirk</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zak</surname>
<given-names>Donald R.</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Marmeisse</surname>
<given-names>Roland</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Vandenbol</surname>
<given-names>Micheline</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hofrichter</surname>
<given-names>Martin</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1">
<label>1</label>
<addr-line>Department of Bio- and Environmental Sciences, International Institute Zittau, Technische Universität Dresden, Zittau, Germany</addr-line>
</aff>
<aff id="aff2">
<label>2</label>
<addr-line>Ecologie Microbienne, UMR CNRS 5557, USC INRA 1364, Université de Lyon, Université Lyon 1, Villeurbanne, France</addr-line>
</aff>
<aff id="aff3">
<label>3</label>
<addr-line>Department of Soil Ecology, UFZ - Helmholtz Center for Environmental Research, Halle/Saale, Germany</addr-line>
</aff>
<aff id="aff4">
<label>4</label>
<addr-line>School of Natural Resources and Environment, University of Michigan, Ann Arbor, Michigan, United States of America</addr-line>
</aff>
<aff id="aff5">
<label>5</label>
<addr-line>Unité de Microbiologie et Génomique, Gembloux Agro-Bio Tech, Université de Liège, Gembloux, Belgium</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Martins</surname>
<given-names>Ligia O.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">
<addr-line>Universidade Nova de Lisboa, Portugal</addr-line>
</aff>
<author-notes>
<corresp id="cor1">* E-mail:
<email>mail@haraldkellner.com</email>
</corresp>
<fn fn-type="conflict">
<p>
<bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con">
<p>Conceived and designed the experiments: HK. Performed the experiments: D. Kapturska FB HK MP PL. Analyzed the data: HK PL FB MP. Contributed reagents/materials/analysis tools: D. Kapturska D. Krüger DZ MV MH RM. Wrote the paper: HK PL MP FB D. Kapturska D. Krüger DZ RM MV MH.</p>
</fn>
</author-notes>
<pub-date pub-type="collection">
<year>2014</year>
</pub-date>
<pub-date pub-type="epub">
<day>24</day>
<month>4</month>
<year>2014</year>
</pub-date>
<volume>9</volume>
<issue>4</issue>
<elocation-id>e95557</elocation-id>
<history>
<date date-type="received">
<day>23</day>
<month>12</month>
<year>2013</year>
</date>
<date date-type="accepted">
<day>28</day>
<month>3</month>
<year>2014</year>
</date>
</history>
<permissions>
<copyright-year>2014</copyright-year>
<copyright-holder>Kellner et al</copyright-holder>
<license>
<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>
<abstract>
<p>Fungal secretory peroxidases mediate fundamental ecological functions in the conversion and degradation of plant biomass. Many of these enzymes have strong oxidizing activities towards aromatic compounds and are involved in the degradation of plant cell wall (lignin) and humus. They comprise three major groups: class II peroxidases (including lignin peroxidase, manganese peroxidase, versatile peroxidase and generic peroxidase), dye-decolorizing peroxidases, and heme-thiolate peroxidases (e.g. unspecific/aromatic peroxygenase, chloroperoxidase). Here, we have repeatedly observed a widespread expression of all major peroxidase groups in leaf and needle litter across a range of forest ecosystems (e.g.
<italic>Fagus</italic>
,
<italic>Picea</italic>
,
<italic>Acer</italic>
,
<italic>Quercus</italic>
, and
<italic>Populus</italic>
spp.), which are widespread in Europe and North America. Manganese peroxidases and unspecific peroxygenases were found expressed in all nine investigated forest sites, and dye-decolorizing peroxidases were observed in five of the nine sites, thereby indicating biological significance of these enzymes for fungal physiology and ecosystem processes. Transcripts of selected secretory peroxidase genes were also analyzed in pure cultures of several litter-decomposing species and other fungi. Using this information, we were able to match, in environmental litter samples, two manganese peroxidase sequences to
<italic>Mycena galopus</italic>
and
<italic>Mycena epipterygia</italic>
and one unspecific peroxygenase transcript to
<italic>Mycena galopus</italic>
, suggesting an important role of this litter- and coarse woody debris-dwelling genus in the disintegration and transformation of litter aromatics and organic matter formation.</p>
</abstract>
<funding-group>
<funding-statement>The work has been funded by the Deutsche Forschungsgemeinschaft - DFG Priority Program 1374 “Infrastructure-Biodiversity-Exploratories” (HO 1961/4-1, KR 3587/1-1), Gembloux Agro-Bio Tech and Fonds de la Recherche Scientific - FNRS (Grant No 2.4503.08), French Research Foundation (EC2CO program MicrobiEn 2009 and project ANR-06-BDIV- 006 Fundiv), US National Science Foundation's Long-Term Research in Environmental Biology program and the US Department of Energy's Biological and Environmental Research Division, and European Union integrated project “Peroxicats” (KBBE-2010-4-265397). 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>
<page-count count="11"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>Belgique</li>
<li>France</li>
<li>États-Unis</li>
</country>
<region>
<li>Auvergne-Rhône-Alpes</li>
<li>District de Dresde</li>
<li>Michigan</li>
<li>Province de Liège</li>
<li>Rhône-Alpes</li>
<li>Région wallonne</li>
<li>Saxe (Land)</li>
</region>
<settlement>
<li>Dresde</li>
<li>Liège</li>
<li>Lyon</li>
<li>Villeurbanne</li>
</settlement>
<orgName>
<li>Université de Liège</li>
<li>Université technique de Dresde</li>
</orgName>
</list>
<tree>
<country name="Allemagne">
<region name="Saxe (Land)">
<name sortKey="Kellner, Harald" sort="Kellner, Harald" uniqKey="Kellner H" first="Harald" last="Kellner">Harald Kellner</name>
</region>
<name sortKey="Hofrichter, Martin" sort="Hofrichter, Martin" uniqKey="Hofrichter M" first="Martin" last="Hofrichter">Martin Hofrichter</name>
<name sortKey="Kapturska, Danuta" sort="Kapturska, Danuta" uniqKey="Kapturska D" first="Danuta" last="Kapturska">Danuta Kapturska</name>
<name sortKey="Kapturska, Danuta" sort="Kapturska, Danuta" uniqKey="Kapturska D" first="Danuta" last="Kapturska">Danuta Kapturska</name>
<name sortKey="Kruger, Dirk" sort="Kruger, Dirk" uniqKey="Kruger D" first="Dirk" last="Krüger">Dirk Krüger</name>
<name sortKey="Pecyna, Marek J" sort="Pecyna, Marek J" uniqKey="Pecyna M" first="Marek J." last="Pecyna">Marek J. Pecyna</name>
</country>
<country name="France">
<region name="Auvergne-Rhône-Alpes">
<name sortKey="Luis, Patricia" sort="Luis, Patricia" uniqKey="Luis P" first="Patricia" last="Luis">Patricia Luis</name>
</region>
<name sortKey="Barbi, Florian" sort="Barbi, Florian" uniqKey="Barbi F" first="Florian" last="Barbi">Florian Barbi</name>
<name sortKey="Marmeisse, Roland" sort="Marmeisse, Roland" uniqKey="Marmeisse R" first="Roland" last="Marmeisse">Roland Marmeisse</name>
</country>
<country name="États-Unis">
<region name="Michigan">
<name sortKey="Zak, Donald R" sort="Zak, Donald R" uniqKey="Zak D" first="Donald R." last="Zak">Donald R. Zak</name>
</region>
</country>
<country name="Belgique">
<region name="Région wallonne">
<name sortKey="Vandenbol, Micheline" sort="Vandenbol, Micheline" uniqKey="Vandenbol M" first="Micheline" last="Vandenbol">Micheline Vandenbol</name>
</region>
</country>
</tree>
</affiliations>
</record>

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