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Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi.

Identifieur interne : 000222 ( Main/Exploration ); précédent : 000221; suivant : 000223

Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi.

Auteurs : Carolyn A. Zeiner [États-Unis] ; Samuel O. Purvine [États-Unis] ; Erika M. Zink [États-Unis] ; Ljiljana Paša-Toli [États-Unis] ; Dominique L. Chaput [États-Unis] ; Sajeet Haridas [États-Unis] ; Si Wu [États-Unis] ; Kurt Labutti [États-Unis] ; Igor V. Grigoriev [États-Unis] ; Bernard Henrissat [France, Arabie saoudite] ; Cara M. Santelli [États-Unis] ; Colleen M. Hansel [États-Unis]

Source :

RBID : pubmed:27434633

Descripteurs français

English descriptors

Abstract

Fungal secretomes contain a wide range of hydrolytic and oxidative enzymes, including cellulases, hemicellulases, pectinases, and lignin-degrading accessory enzymes, that synergistically drive litter decomposition in the environment. While secretome studies of model organisms such as Phanerochaete chrysosporium and Aspergillus species have greatly expanded our knowledge of these enzymes, few have extended secretome characterization to environmental isolates or conducted side-by-side comparisons of diverse species. Thus, the mechanisms of carbon degradation by many ubiquitous soil fungi remain poorly understood. Here we use a combination of LC-MS/MS, genomic, and bioinformatic analyses to characterize and compare the protein composition of the secretomes of four recently isolated, cosmopolitan, Mn(II)-oxidizing Ascomycetes (Alternaria alternata SRC1lrK2f, Stagonospora sp. SRC1lsM3a, Pyrenochaeta sp. DS3sAY3a, and Paraconiothyrium sporulosum AP3s5-JAC2a). We demonstrate that the organisms produce a rich yet functionally similar suite of extracellular enzymes, with species-specific differences in secretome composition arising from unique amino acid sequences rather than overall protein function. Furthermore, we identify not only a wide range of carbohydrate-active enzymes that can directly oxidize recalcitrant carbon, but also an impressive suite of redox-active accessory enzymes that suggests a role for Fenton-based hydroxyl radical formation in indirect, non-specific lignocellulose attack. Our findings highlight the diverse oxidative capacity of these environmental isolates and enhance our understanding of the role of filamentous Ascomycetes in carbon turnover in the environment.

DOI: 10.1371/journal.pone.0157844
PubMed: 27434633
PubMed Central: PMC4951024


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Le document en format XML

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<term>Ascomycota (enzymology)</term>
<term>Biodegradation, Environmental (MeSH)</term>
<term>Carbon (metabolism)</term>
<term>Cations, Divalent (MeSH)</term>
<term>Cellulases (classification)</term>
<term>Cellulases (metabolism)</term>
<term>Computational Biology (MeSH)</term>
<term>Glycoside Hydrolases (classification)</term>
<term>Glycoside Hydrolases (metabolism)</term>
<term>Hydroxyl Radical (metabolism)</term>
<term>Lignin (metabolism)</term>
<term>Manganese (metabolism)</term>
<term>Molecular Sequence Annotation (MeSH)</term>
<term>Oxidation-Reduction (MeSH)</term>
<term>Polygalacturonase (classification)</term>
<term>Polygalacturonase (metabolism)</term>
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<term>Species Specificity (MeSH)</term>
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<term>Annotation de séquence moléculaire (MeSH)</term>
<term>Ascomycota (enzymologie)</term>
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<term>Carbone (métabolisme)</term>
<term>Cations divalents (MeSH)</term>
<term>Cellulases (classification)</term>
<term>Cellulases (métabolisme)</term>
<term>Dépollution biologique de l'environnement (MeSH)</term>
<term>Glycosidases (classification)</term>
<term>Glycosidases (métabolisme)</term>
<term>Lignine (métabolisme)</term>
<term>Manganèse (métabolisme)</term>
<term>Microbiologie du sol (MeSH)</term>
<term>Oxydoréduction (MeSH)</term>
<term>Polygalacturonase (classification)</term>
<term>Polygalacturonase (métabolisme)</term>
<term>Radical hydroxyle (métabolisme)</term>
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<term>Glycosidases</term>
<term>Lignine</term>
<term>Manganèse</term>
<term>Polygalacturonase</term>
<term>Radical hydroxyle</term>
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<div type="abstract" xml:lang="en">Fungal secretomes contain a wide range of hydrolytic and oxidative enzymes, including cellulases, hemicellulases, pectinases, and lignin-degrading accessory enzymes, that synergistically drive litter decomposition in the environment. While secretome studies of model organisms such as Phanerochaete chrysosporium and Aspergillus species have greatly expanded our knowledge of these enzymes, few have extended secretome characterization to environmental isolates or conducted side-by-side comparisons of diverse species. Thus, the mechanisms of carbon degradation by many ubiquitous soil fungi remain poorly understood. Here we use a combination of LC-MS/MS, genomic, and bioinformatic analyses to characterize and compare the protein composition of the secretomes of four recently isolated, cosmopolitan, Mn(II)-oxidizing Ascomycetes (Alternaria alternata SRC1lrK2f, Stagonospora sp. SRC1lsM3a, Pyrenochaeta sp. DS3sAY3a, and Paraconiothyrium sporulosum AP3s5-JAC2a). We demonstrate that the organisms produce a rich yet functionally similar suite of extracellular enzymes, with species-specific differences in secretome composition arising from unique amino acid sequences rather than overall protein function. Furthermore, we identify not only a wide range of carbohydrate-active enzymes that can directly oxidize recalcitrant carbon, but also an impressive suite of redox-active accessory enzymes that suggests a role for Fenton-based hydroxyl radical formation in indirect, non-specific lignocellulose attack. Our findings highlight the diverse oxidative capacity of these environmental isolates and enhance our understanding of the role of filamentous Ascomycetes in carbon turnover in the environment. </div>
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<Year>2017</Year>
<Month>07</Month>
<Day>18</Day>
</DateCompleted>
<DateRevised>
<Year>2018</Year>
<Month>12</Month>
<Day>02</Day>
</DateRevised>
<Article PubModel="Electronic-eCollection">
<Journal>
<ISSN IssnType="Electronic">1932-6203</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>11</Volume>
<Issue>7</Issue>
<PubDate>
<Year>2016</Year>
</PubDate>
</JournalIssue>
<Title>PloS one</Title>
<ISOAbbreviation>PLoS One</ISOAbbreviation>
</Journal>
<ArticleTitle>Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi.</ArticleTitle>
<Pagination>
<MedlinePgn>e0157844</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pone.0157844</ELocationID>
<Abstract>
<AbstractText>Fungal secretomes contain a wide range of hydrolytic and oxidative enzymes, including cellulases, hemicellulases, pectinases, and lignin-degrading accessory enzymes, that synergistically drive litter decomposition in the environment. While secretome studies of model organisms such as Phanerochaete chrysosporium and Aspergillus species have greatly expanded our knowledge of these enzymes, few have extended secretome characterization to environmental isolates or conducted side-by-side comparisons of diverse species. Thus, the mechanisms of carbon degradation by many ubiquitous soil fungi remain poorly understood. Here we use a combination of LC-MS/MS, genomic, and bioinformatic analyses to characterize and compare the protein composition of the secretomes of four recently isolated, cosmopolitan, Mn(II)-oxidizing Ascomycetes (Alternaria alternata SRC1lrK2f, Stagonospora sp. SRC1lsM3a, Pyrenochaeta sp. DS3sAY3a, and Paraconiothyrium sporulosum AP3s5-JAC2a). We demonstrate that the organisms produce a rich yet functionally similar suite of extracellular enzymes, with species-specific differences in secretome composition arising from unique amino acid sequences rather than overall protein function. Furthermore, we identify not only a wide range of carbohydrate-active enzymes that can directly oxidize recalcitrant carbon, but also an impressive suite of redox-active accessory enzymes that suggests a role for Fenton-based hydroxyl radical formation in indirect, non-specific lignocellulose attack. Our findings highlight the diverse oxidative capacity of these environmental isolates and enhance our understanding of the role of filamentous Ascomycetes in carbon turnover in the environment. </AbstractText>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Zeiner</LastName>
<ForeName>Carolyn A</ForeName>
<Initials>CA</Initials>
<AffiliationInfo>
<Affiliation>School of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Purvine</LastName>
<ForeName>Samuel O</ForeName>
<Initials>SO</Initials>
<AffiliationInfo>
<Affiliation>Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zink</LastName>
<ForeName>Erika M</ForeName>
<Initials>EM</Initials>
<AffiliationInfo>
<Affiliation>Biological Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Paša-Tolić</LastName>
<ForeName>Ljiljana</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chaput</LastName>
<ForeName>Dominique L</ForeName>
<Initials>DL</Initials>
<AffiliationInfo>
<Affiliation>Department of Mineral Sciences, National Museum of Natural History, Smithsonian Institution, Washington, DC, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Haridas</LastName>
<ForeName>Sajeet</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wu</LastName>
<ForeName>Si</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>LaButti</LastName>
<ForeName>Kurt</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Grigoriev</LastName>
<ForeName>Igor V</ForeName>
<Initials>IV</Initials>
<AffiliationInfo>
<Affiliation>U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Henrissat</LastName>
<ForeName>Bernard</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>Architecture et Fonction des Macromolécules Biologiques, UMR7257, Centre National de la Recherche Scientifique and Aix-Marseille Université, 13288 Marseille Cedex 9, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Biological Sciences, King Abdulaziz University, P.O. Box 80203, Jeddah, 21589, Saudi Arabia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Santelli</LastName>
<ForeName>Cara M</ForeName>
<Initials>CM</Initials>
<AffiliationInfo>
<Affiliation>Department of Earth Sciences, University of Minnesota, Minneapolis, Minnesota, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hansel</LastName>
<ForeName>Colleen M</ForeName>
<Initials>CM</Initials>
<AffiliationInfo>
<Affiliation>Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2016</Year>
<Month>07</Month>
<Day>19</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>PLoS One</MedlineTA>
<NlmUniqueID>101285081</NlmUniqueID>
<ISSNLinking>1932-6203</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D002413">Cations, Divalent</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>11132-73-3</RegistryNumber>
<NameOfSubstance UI="C036909">lignocellulose</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>3352-57-6</RegistryNumber>
<NameOfSubstance UI="D017665">Hydroxyl Radical</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>42Z2K6ZL8P</RegistryNumber>
<NameOfSubstance UI="D008345">Manganese</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>7440-44-0</RegistryNumber>
<NameOfSubstance UI="D002244">Carbon</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>9005-53-2</RegistryNumber>
<NameOfSubstance UI="D008031">Lignin</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 3.2.1.-</RegistryNumber>
<NameOfSubstance UI="D044602">Cellulases</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 3.2.1.-</RegistryNumber>
<NameOfSubstance UI="D006026">Glycoside Hydrolases</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 3.2.1.-</RegistryNumber>
<NameOfSubstance UI="C023305">hemicellulase</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 3.2.1.15</RegistryNumber>
<NameOfSubstance UI="D011096">Polygalacturonase</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D001203" MajorTopicYN="N">Ascomycota</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D001673" MajorTopicYN="N">Biodegradation, Environmental</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002244" MajorTopicYN="N">Carbon</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002413" MajorTopicYN="N">Cations, Divalent</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D044602" MajorTopicYN="N">Cellulases</DescriptorName>
<QualifierName UI="Q000145" MajorTopicYN="N">classification</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D019295" MajorTopicYN="N">Computational Biology</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006026" MajorTopicYN="N">Glycoside Hydrolases</DescriptorName>
<QualifierName UI="Q000145" MajorTopicYN="N">classification</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017665" MajorTopicYN="N">Hydroxyl Radical</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008031" MajorTopicYN="N">Lignin</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008345" MajorTopicYN="N">Manganese</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D058977" MajorTopicYN="N">Molecular Sequence Annotation</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010084" MajorTopicYN="N">Oxidation-Reduction</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011096" MajorTopicYN="N">Polygalacturonase</DescriptorName>
<QualifierName UI="Q000145" MajorTopicYN="N">classification</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012988" MajorTopicYN="Y">Soil Microbiology</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013045" MajorTopicYN="N">Species Specificity</DescriptorName>
</MeshHeading>
</MeshHeadingList>
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<Year>2016</Year>
<Month>02</Month>
<Day>26</Day>
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<PubMedPubDate PubStatus="accepted">
<Year>2016</Year>
<Month>06</Month>
<Day>06</Day>
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<li>Arabie saoudite</li>
<li>France</li>
<li>États-Unis</li>
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<li>Californie</li>
<li>District de Columbia</li>
<li>Massachusetts</li>
<li>Minnesota</li>
<li>Provence-Alpes-Côte d'Azur</li>
<li>Washington (État)</li>
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<name sortKey="Zeiner, Carolyn A" sort="Zeiner, Carolyn A" uniqKey="Zeiner C" first="Carolyn A" last="Zeiner">Carolyn A. Zeiner</name>
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<name sortKey="Chaput, Dominique L" sort="Chaput, Dominique L" uniqKey="Chaput D" first="Dominique L" last="Chaput">Dominique L. Chaput</name>
<name sortKey="Grigoriev, Igor V" sort="Grigoriev, Igor V" uniqKey="Grigoriev I" first="Igor V" last="Grigoriev">Igor V. Grigoriev</name>
<name sortKey="Hansel, Colleen M" sort="Hansel, Colleen M" uniqKey="Hansel C" first="Colleen M" last="Hansel">Colleen M. Hansel</name>
<name sortKey="Haridas, Sajeet" sort="Haridas, Sajeet" uniqKey="Haridas S" first="Sajeet" last="Haridas">Sajeet Haridas</name>
<name sortKey="Labutti, Kurt" sort="Labutti, Kurt" uniqKey="Labutti K" first="Kurt" last="Labutti">Kurt Labutti</name>
<name sortKey="Pasa Toli, Ljiljana" sort="Pasa Toli, Ljiljana" uniqKey="Pasa Toli L" first="Ljiljana" last="Paša-Toli">Ljiljana Paša-Toli</name>
<name sortKey="Purvine, Samuel O" sort="Purvine, Samuel O" uniqKey="Purvine S" first="Samuel O" last="Purvine">Samuel O. Purvine</name>
<name sortKey="Santelli, Cara M" sort="Santelli, Cara M" uniqKey="Santelli C" first="Cara M" last="Santelli">Cara M. Santelli</name>
<name sortKey="Wu, Si" sort="Wu, Si" uniqKey="Wu S" first="Si" last="Wu">Si Wu</name>
<name sortKey="Zink, Erika M" sort="Zink, Erika M" uniqKey="Zink E" first="Erika M" last="Zink">Erika M. Zink</name>
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<country name="France">
<region name="Provence-Alpes-Côte d'Azur">
<name sortKey="Henrissat, Bernard" sort="Henrissat, Bernard" uniqKey="Henrissat B" first="Bernard" last="Henrissat">Bernard Henrissat</name>
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<country name="Arabie saoudite">
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<name sortKey="Henrissat, Bernard" sort="Henrissat, Bernard" uniqKey="Henrissat B" first="Bernard" last="Henrissat">Bernard Henrissat</name>
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