Regulation of fungal decomposition at single-cell level.
Identifieur interne : 000211 ( Main/Corpus ); précédent : 000210; suivant : 000212Regulation of fungal decomposition at single-cell level.
Auteurs : Michiel Op De Beeck ; Carl Troein ; Syahril Siregar ; Luigi Gentile ; Giuseppe Abbondanza ; Carsten Peterson ; Per Persson ; Anders TunlidSource :
- The ISME journal [ 1751-7370 ] ; 2020.
English descriptors
- KwdEn :
- MESH :
- chemical , chemistry : Soil.
- physiology : Basidiomycota, Fungi, Mycelium, Mycorrhizae.
- Agaricales, Environmental Microbiology, Hyphae, Nutrients.
Abstract
Filamentous fungi play a key role as decomposers in Earth's nutrient cycles. In soils, substrates are heterogeneously distributed in microenvironments. Hence, individual hyphae of a mycelium may experience very different environmental conditions simultaneously. In the current work, we investigated how fungi cope with local environmental variations at single-cell level. We developed a method based on infrared spectroscopy that allows the direct, in-situ chemical imaging of the decomposition activity of individual hyphal tips. Colonies of the ectomycorrhizal Basidiomycete Paxillus involutus were grown on liquid media, while parts of colonies were allowed to colonize lignin patches. Oxidative decomposition of lignin by individual hyphae growing under different conditions was followed for a period of seven days. We identified two sub-populations of hyphal tips: one with low decomposition activity and one with much higher activity. Active cells secreted more extracellular polymeric substances and oxidized lignin more strongly. The ratio of active to inactive hyphae strongly depended on the environmental conditions in lignin patches, but was further mediated by the decomposition activity of entire mycelia. Phenotypic heterogeneity occurring between genetically identical hyphal tips may be an important strategy for filamentous fungi to cope with heterogeneous and constantly changing soil environments.
DOI: 10.1038/s41396-019-0583-9
PubMed: 31896790
PubMed Central: PMC7082364
Links to Exploration step
pubmed:31896790Le document en format XML
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Siregar</name><affiliation><nlm:affiliation>Department of Astronomy and Theoretical Physics, Computational Biology and Biological Physics, Lund University, Sölvegatan 14A, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation></author><author><name sortKey="Gentile, Luigi" sort="Gentile, Luigi" uniqKey="Gentile L" first="Luigi" last="Gentile">Luigi Gentile</name><affiliation><nlm:affiliation>Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Department of Chemistry and CSGI, University of Bari Aldo Moro, IT- 701 21, Bari, Italy.</nlm:affiliation></affiliation></author><author><name sortKey="Abbondanza, Giuseppe" sort="Abbondanza, Giuseppe" uniqKey="Abbondanza G" first="Giuseppe" last="Abbondanza">Giuseppe Abbondanza</name><affiliation><nlm:affiliation>Department of Physics, Synchrotron Radiation Research, Lund University, SE- 223 62, Lund, Sweden.</nlm:affiliation></affiliation></author><author><name sortKey="Peterson, Carsten" sort="Peterson, Carsten" uniqKey="Peterson C" first="Carsten" last="Peterson">Carsten Peterson</name><affiliation><nlm:affiliation>Department of Astronomy and Theoretical Physics, Computational Biology and Biological Physics, Lund University, Sölvegatan 14A, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation></author><author><name sortKey="Persson, Per" sort="Persson, Per" uniqKey="Persson P" first="Per" last="Persson">Per Persson</name><affiliation><nlm:affiliation>Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Centre for Environmental and Climate Research (CEC), Lund University, Ecology Building, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation></author><author><name sortKey="Tunlid, Anders" sort="Tunlid, Anders" uniqKey="Tunlid A" first="Anders" last="Tunlid">Anders Tunlid</name><affiliation><nlm:affiliation>Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:31896790</idno><idno type="pmid">31896790</idno><idno type="doi">10.1038/s41396-019-0583-9</idno><idno type="pmc">PMC7082364</idno><idno type="wicri:Area/Main/Corpus">000211</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000211</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Regulation of fungal decomposition at single-cell level.</title><author><name sortKey="Op De Beeck, Michiel" sort="Op De Beeck, Michiel" uniqKey="Op De Beeck M" first="Michiel" last="Op De Beeck">Michiel Op De Beeck</name><affiliation><nlm:affiliation>Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden. michiel.op_de_beeck@biol.lu.se.</nlm:affiliation></affiliation></author><author><name sortKey="Troein, Carl" sort="Troein, Carl" uniqKey="Troein C" first="Carl" last="Troein">Carl Troein</name><affiliation><nlm:affiliation>Department of Astronomy and Theoretical Physics, Computational Biology and Biological Physics, Lund University, Sölvegatan 14A, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation></author><author><name sortKey="Siregar, Syahril" sort="Siregar, Syahril" uniqKey="Siregar S" first="Syahril" last="Siregar">Syahril Siregar</name><affiliation><nlm:affiliation>Department of Astronomy and Theoretical Physics, Computational Biology and Biological Physics, Lund University, Sölvegatan 14A, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation></author><author><name sortKey="Gentile, Luigi" sort="Gentile, Luigi" uniqKey="Gentile L" first="Luigi" last="Gentile">Luigi Gentile</name><affiliation><nlm:affiliation>Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Department of Chemistry and CSGI, University of Bari Aldo Moro, IT- 701 21, Bari, Italy.</nlm:affiliation></affiliation></author><author><name sortKey="Abbondanza, Giuseppe" sort="Abbondanza, Giuseppe" uniqKey="Abbondanza G" first="Giuseppe" last="Abbondanza">Giuseppe Abbondanza</name><affiliation><nlm:affiliation>Department of Physics, Synchrotron Radiation Research, Lund University, SE- 223 62, Lund, Sweden.</nlm:affiliation></affiliation></author><author><name sortKey="Peterson, Carsten" sort="Peterson, Carsten" uniqKey="Peterson C" first="Carsten" last="Peterson">Carsten Peterson</name><affiliation><nlm:affiliation>Department of Astronomy and Theoretical Physics, Computational Biology and Biological Physics, Lund University, Sölvegatan 14A, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation></author><author><name sortKey="Persson, Per" sort="Persson, Per" uniqKey="Persson P" first="Per" last="Persson">Per Persson</name><affiliation><nlm:affiliation>Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Centre for Environmental and Climate Research (CEC), Lund University, Ecology Building, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation></author><author><name sortKey="Tunlid, Anders" sort="Tunlid, Anders" uniqKey="Tunlid A" first="Anders" last="Tunlid">Anders Tunlid</name><affiliation><nlm:affiliation>Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.</nlm:affiliation></affiliation></author></analytic><series><title level="j">The ISME journal</title><idno type="eISSN">1751-7370</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Agaricales (MeSH)</term><term>Basidiomycota (physiology)</term><term>Environmental Microbiology (MeSH)</term><term>Fungi (physiology)</term><term>Hyphae (MeSH)</term><term>Mycelium (physiology)</term><term>Mycorrhizae (physiology)</term><term>Nutrients (MeSH)</term><term>Soil (chemistry)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Soil</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Basidiomycota</term><term>Fungi</term><term>Mycelium</term><term>Mycorrhizae</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Agaricales</term><term>Environmental Microbiology</term><term>Hyphae</term><term>Nutrients</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Filamentous fungi play a key role as decomposers in Earth's nutrient cycles. In soils, substrates are heterogeneously distributed in microenvironments. Hence, individual hyphae of a mycelium may experience very different environmental conditions simultaneously. In the current work, we investigated how fungi cope with local environmental variations at single-cell level. We developed a method based on infrared spectroscopy that allows the direct, in-situ chemical imaging of the decomposition activity of individual hyphal tips. Colonies of the ectomycorrhizal Basidiomycete Paxillus involutus were grown on liquid media, while parts of colonies were allowed to colonize lignin patches. Oxidative decomposition of lignin by individual hyphae growing under different conditions was followed for a period of seven days. We identified two sub-populations of hyphal tips: one with low decomposition activity and one with much higher activity. Active cells secreted more extracellular polymeric substances and oxidized lignin more strongly. The ratio of active to inactive hyphae strongly depended on the environmental conditions in lignin patches, but was further mediated by the decomposition activity of entire mycelia. Phenotypic heterogeneity occurring between genetically identical hyphal tips may be an important strategy for filamentous fungi to cope with heterogeneous and constantly changing soil environments.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" IndexingMethod="Curated" Owner="NLM"><PMID Version="1">31896790</PMID><DateCompleted><Year>2020</Year><Month>10</Month><Day>15</Day></DateCompleted><DateRevised><Year>2020</Year><Month>10</Month><Day>15</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1751-7370</ISSN><JournalIssue CitedMedium="Internet"><Volume>14</Volume><Issue>4</Issue><PubDate><Year>2020</Year><Month>04</Month></PubDate></JournalIssue><Title>The ISME journal</Title><ISOAbbreviation>ISME J</ISOAbbreviation></Journal><ArticleTitle>Regulation of fungal decomposition at single-cell level.</ArticleTitle><Pagination><MedlinePgn>896-905</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41396-019-0583-9</ELocationID><Abstract><AbstractText>Filamentous fungi play a key role as decomposers in Earth's nutrient cycles. In soils, substrates are heterogeneously distributed in microenvironments. Hence, individual hyphae of a mycelium may experience very different environmental conditions simultaneously. In the current work, we investigated how fungi cope with local environmental variations at single-cell level. We developed a method based on infrared spectroscopy that allows the direct, in-situ chemical imaging of the decomposition activity of individual hyphal tips. Colonies of the ectomycorrhizal Basidiomycete Paxillus involutus were grown on liquid media, while parts of colonies were allowed to colonize lignin patches. Oxidative decomposition of lignin by individual hyphae growing under different conditions was followed for a period of seven days. We identified two sub-populations of hyphal tips: one with low decomposition activity and one with much higher activity. Active cells secreted more extracellular polymeric substances and oxidized lignin more strongly. The ratio of active to inactive hyphae strongly depended on the environmental conditions in lignin patches, but was further mediated by the decomposition activity of entire mycelia. Phenotypic heterogeneity occurring between genetically identical hyphal tips may be an important strategy for filamentous fungi to cope with heterogeneous and constantly changing soil environments.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Op De Beeck</LastName><ForeName>Michiel</ForeName><Initials>M</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-8727-0999</Identifier><AffiliationInfo><Affiliation>Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden. michiel.op_de_beeck@biol.lu.se.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Troein</LastName><ForeName>Carl</ForeName><Initials>C</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-9729-8891</Identifier><AffiliationInfo><Affiliation>Department of Astronomy and Theoretical Physics, Computational Biology and Biological Physics, Lund University, Sölvegatan 14A, SE-223 62, Lund, Sweden.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Siregar</LastName><ForeName>Syahril</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Astronomy and Theoretical Physics, Computational Biology and Biological Physics, Lund University, Sölvegatan 14A, SE-223 62, Lund, Sweden.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gentile</LastName><ForeName>Luigi</ForeName><Initials>L</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-6854-2963</Identifier><AffiliationInfo><Affiliation>Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Chemistry and CSGI, University of Bari Aldo Moro, IT- 701 21, Bari, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Abbondanza</LastName><ForeName>Giuseppe</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Department of Physics, Synchrotron Radiation Research, Lund University, SE- 223 62, Lund, Sweden.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Peterson</LastName><ForeName>Carsten</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Department of Astronomy and Theoretical Physics, Computational Biology and Biological Physics, Lund University, Sölvegatan 14A, SE-223 62, Lund, Sweden.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Persson</LastName><ForeName>Per</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Centre for Environmental and Climate Research (CEC), Lund University, Ecology Building, SE-223 62, Lund, Sweden.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tunlid</LastName><ForeName>Anders</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Biology, Microbial Ecology Group, Lund University, Ecology Building, SE-223 62, Lund, Sweden.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>01</Month><Day>02</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>ISME J</MedlineTA><NlmUniqueID>101301086</NlmUniqueID><ISSNLinking>1751-7362</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D012987">Soil</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000363" MajorTopicYN="N">Agaricales</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D001487" MajorTopicYN="N">Basidiomycota</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D004783" MajorTopicYN="N">Environmental Microbiology</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005658" MajorTopicYN="N">Fungi</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D025301" MajorTopicYN="N">Hyphae</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D025282" MajorTopicYN="N">Mycelium</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000078622" MajorTopicYN="N">Nutrients</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D012987" MajorTopicYN="N">Soil</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName></MeshHeading></MeshHeadingList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>09</Month><Day>27</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>12</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2019</Year><Month>12</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>1</Month><Day>4</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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