Symbiont selection via alcohol benefits fungus farming by ambrosia beetles.
Identifieur interne : 000096 ( Main/Exploration ); précédent : 000095; suivant : 000097Symbiont selection via alcohol benefits fungus farming by ambrosia beetles.
Auteurs : Christopher M. Ranger [États-Unis] ; Peter H W. Biedermann [Allemagne] ; Vipaporn Phuntumart [États-Unis] ; Gayathri U. Beligala [États-Unis] ; Satyaki Ghosh [États-Unis] ; Debra E. Palmquist [États-Unis] ; Robert Mueller [Allemagne, Australie] ; Jenny Barnett [États-Unis] ; Peter B. Schultz [États-Unis] ; Michael E. Reding [États-Unis] ; J Philipp Benz [Allemagne]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 1091-6490 ] ; 2018.
Descripteurs français
- KwdFr :
- MESH :
- effets des médicaments et des substances chimiques : Symbiose.
- microbiologie : Coléoptères.
- métabolisme : Éthanol.
- pharmacologie : Éthanol.
- physiologie : Aspergillus, Penicillium, Symbiose.
- Animaux.
English descriptors
- KwdEn :
- MESH :
- chemical , metabolism : Ethanol.
- drug effects : Symbiosis.
- microbiology : Coleoptera.
- chemical , pharmacology : Ethanol.
- physiology : Aspergillus, Penicillium, Symbiosis.
- Animals.
Abstract
Animal-microbe mutualisms are typically maintained by vertical symbiont transmission or partner choice. A third mechanism, screening of high-quality symbionts, has been predicted in theory, but empirical examples are rare. Here we demonstrate that ambrosia beetles rely on ethanol within host trees for promoting gardens of their fungal symbiont and producing offspring. Ethanol has long been known as the main attractant for many of these fungus-farming beetles as they select host trees in which they excavate tunnels and cultivate fungal gardens. More than 300 attacks by Xylosandrus germanus and other species were triggered by baiting trees with ethanol lures, but none of the foundresses established fungal gardens or produced broods unless tree tissues contained in vivo ethanol resulting from irrigation with ethanol solutions. More X. germanus brood were also produced in a rearing substrate containing ethanol. These benefits are a result of increased food supply via the positive effects of ethanol on food-fungus biomass. Selected Ambrosiella and Raffaelea fungal isolates from ethanol-responsive ambrosia beetles profited directly and indirectly by (i) a higher biomass on medium containing ethanol, (ii) strong alcohol dehydrogenase enzymatic activity, and (iii) a competitive advantage over weedy fungal garden competitors (Aspergillus, Penicillium) that are inhibited by ethanol. As ambrosia fungi both detoxify and produce ethanol, they may maintain the selectivity of their alcohol-rich habitat for their own purpose and that of other ethanol-resistant/producing microbes. This resembles biological screening of beneficial symbionts and a potentially widespread, unstudied benefit of alcohol-producing symbionts (e.g., yeasts) in other microbial symbioses.
DOI: 10.1073/pnas.1716852115
PubMed: 29632193
PubMed Central: PMC5924889
Affiliations:
- Allemagne, Australie, États-Unis
- Bavière, District de Basse-Franconie, District de Haute-Bavière, Illinois, Ohio, Virginie
- Munich, Wurtzbourg
- Université Louis-et-Maximilien de Munich
Links toward previous steps (curation, corpus...)
Le document en format XML
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Ranger</name><affiliation wicri:level="2"><nlm:affiliation>Horticultural Insects Research Laboratory, US Department of Agriculture-Agricultural Research Service, Wooster, OH 44691; christopher.ranger@ars.usda.gov peter.biedermann@uni-wuerzburg.de.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Ohio</region></placeName><wicri:cityArea>Horticultural Insects Research Laboratory, US Department of Agriculture-Agricultural Research Service, Wooster</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Entomology, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Ohio</region></placeName><wicri:cityArea>Department of Entomology, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster</wicri:cityArea></affiliation></author><author><name sortKey="Biedermann, Peter H W" sort="Biedermann, Peter H W" uniqKey="Biedermann P" first="Peter H W" last="Biedermann">Peter H W. Biedermann</name><affiliation><nlm:affiliation>Department of Biochemistry, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany; christopher.ranger@ars.usda.gov peter.biedermann@uni-wuerzburg.de.</nlm:affiliation><wicri:noCountry code="subField">Germany; christopher.ranger@ars.usda.gov</wicri:noCountry></affiliation><affiliation wicri:level="3"><nlm:affiliation>Department of Animal Ecology and Tropical Biology, Biozentrum, Julius Maximilian University Würzburg, 97074 Würzburg, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Animal Ecology and Tropical Biology, Biozentrum, Julius Maximilian University Würzburg, 97074 Würzburg</wicri:regionArea><placeName><region type="land" nuts="1">Bavière</region><region type="district" nuts="2">District de Basse-Franconie</region><settlement type="city">Wurtzbourg</settlement></placeName></affiliation></author><author><name sortKey="Phuntumart, Vipaporn" sort="Phuntumart, Vipaporn" uniqKey="Phuntumart V" first="Vipaporn" last="Phuntumart">Vipaporn Phuntumart</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Ohio</region></placeName><wicri:cityArea>Department of Biological Sciences, Bowling Green State University, Bowling Green</wicri:cityArea></affiliation></author><author><name sortKey="Beligala, Gayathri U" sort="Beligala, Gayathri U" uniqKey="Beligala G" first="Gayathri U" last="Beligala">Gayathri U. Beligala</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Ohio</region></placeName><wicri:cityArea>Department of Biological Sciences, Bowling Green State University, Bowling Green</wicri:cityArea></affiliation></author><author><name sortKey="Ghosh, Satyaki" sort="Ghosh, Satyaki" uniqKey="Ghosh S" first="Satyaki" last="Ghosh">Satyaki Ghosh</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Ohio</region></placeName><wicri:cityArea>Department of Biological Sciences, Bowling Green State University, Bowling Green</wicri:cityArea></affiliation></author><author><name sortKey="Palmquist, Debra E" sort="Palmquist, Debra E" uniqKey="Palmquist D" first="Debra E" last="Palmquist">Debra E. Palmquist</name><affiliation wicri:level="2"><nlm:affiliation>US Department of Agriculture-Agricultural Research Service Midwest Area, Peoria, IL 61604.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Illinois</region></placeName><wicri:cityArea>US Department of Agriculture-Agricultural Research Service Midwest Area, Peoria</wicri:cityArea></affiliation></author><author><name sortKey="Mueller, Robert" sort="Mueller, Robert" uniqKey="Mueller R" first="Robert" last="Mueller">Robert Mueller</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Biochemistry, Max Planck Institute for Chemical Ecology, 07745 Jena</wicri:regionArea><wicri:noRegion>07745 Jena</wicri:noRegion><wicri:noRegion>07745 Jena</wicri:noRegion><wicri:noRegion>07745 Jena</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW 2751, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW 2751</wicri:regionArea><wicri:noRegion>NSW 2751</wicri:noRegion></affiliation></author><author><name sortKey="Barnett, Jenny" sort="Barnett, Jenny" uniqKey="Barnett J" first="Jenny" last="Barnett">Jenny Barnett</name><affiliation wicri:level="2"><nlm:affiliation>Horticultural Insects Research Laboratory, US Department of Agriculture-Agricultural Research Service, Wooster, OH 44691.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Ohio</region></placeName><wicri:cityArea>Horticultural Insects Research Laboratory, US Department of Agriculture-Agricultural Research Service, Wooster</wicri:cityArea></affiliation></author><author><name sortKey="Schultz, Peter B" sort="Schultz, Peter B" uniqKey="Schultz P" first="Peter B" last="Schultz">Peter B. Schultz</name><affiliation wicri:level="2"><nlm:affiliation>Hampton Roads Agricultural Research and Extension Center, Virginia Polytechnic Institute and State University, Virginia Beach, VA 23455.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Virginie</region></placeName><wicri:cityArea>Hampton Roads Agricultural Research and Extension Center, Virginia Polytechnic Institute and State University, Virginia Beach</wicri:cityArea></affiliation></author><author><name sortKey="Reding, Michael E" sort="Reding, Michael E" uniqKey="Reding M" first="Michael E" last="Reding">Michael E. Reding</name><affiliation wicri:level="2"><nlm:affiliation>Horticultural Insects Research Laboratory, US Department of Agriculture-Agricultural Research Service, Wooster, OH 44691.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Ohio</region></placeName><wicri:cityArea>Horticultural Insects Research Laboratory, US Department of Agriculture-Agricultural Research Service, Wooster</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Entomology, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Ohio</region></placeName><wicri:cityArea>Department of Entomology, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster</wicri:cityArea></affiliation></author><author><name sortKey="Benz, J Philipp" sort="Benz, J Philipp" uniqKey="Benz J" first="J Philipp" last="Benz">J Philipp Benz</name><affiliation wicri:level="4"><nlm:affiliation>School of Life Sciences Weihenstephan, Technical University of Munich, D-85354 Freising, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>School of Life Sciences Weihenstephan, Technical University of Munich, D-85354 Freising</wicri:regionArea><wicri:noRegion>85354 Freising</wicri:noRegion><orgName type="university">Université Louis-et-Maximilien de Munich</orgName><placeName><settlement type="city">Munich</settlement><region type="land" nuts="1">Bavière</region><region type="district" nuts="2">District de Haute-Bavière</region></placeName></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="eISSN">1091-6490</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals (MeSH)</term><term>Aspergillus (physiology)</term><term>Coleoptera (microbiology)</term><term>Ethanol (metabolism)</term><term>Ethanol (pharmacology)</term><term>Penicillium (physiology)</term><term>Symbiosis (drug effects)</term><term>Symbiosis (physiology)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animaux (MeSH)</term><term>Aspergillus (physiologie)</term><term>Coléoptères (microbiologie)</term><term>Penicillium (physiologie)</term><term>Symbiose (effets des médicaments et des substances chimiques)</term><term>Symbiose (physiologie)</term><term>Éthanol (métabolisme)</term><term>Éthanol (pharmacologie)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Ethanol</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Symbiosis</term></keywords><keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr"><term>Symbiose</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Coléoptères</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Coleoptera</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Éthanol</term></keywords><keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr"><term>Éthanol</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Ethanol</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Aspergillus</term><term>Penicillium</term><term>Symbiose</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Aspergillus</term><term>Penicillium</term><term>Symbiosis</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Animal-microbe mutualisms are typically maintained by vertical symbiont transmission or partner choice. A third mechanism, screening of high-quality symbionts, has been predicted in theory, but empirical examples are rare. Here we demonstrate that ambrosia beetles rely on ethanol within host trees for promoting gardens of their fungal symbiont and producing offspring. Ethanol has long been known as the main attractant for many of these fungus-farming beetles as they select host trees in which they excavate tunnels and cultivate fungal gardens. More than 300 attacks by <i>Xylosandrus germanus</i> and other species were triggered by baiting trees with ethanol lures, but none of the foundresses established fungal gardens or produced broods unless tree tissues contained in vivo ethanol resulting from irrigation with ethanol solutions. More <i>X. germanus</i> brood were also produced in a rearing substrate containing ethanol. These benefits are a result of increased food supply via the positive effects of ethanol on food-fungus biomass. Selected <i>Ambrosiella</i> and <i>Raffaelea</i> fungal isolates from ethanol-responsive ambrosia beetles profited directly and indirectly by (<i>i</i>) a higher biomass on medium containing ethanol, (<i>ii</i>) strong alcohol dehydrogenase enzymatic activity, and (<i>iii</i>) a competitive advantage over weedy fungal garden competitors (<i>Aspergillus</i>, <i>Penicillium</i>) that are inhibited by ethanol. As ambrosia fungi both detoxify and produce ethanol, they may maintain the selectivity of their alcohol-rich habitat for their own purpose and that of other ethanol-resistant/producing microbes. This resembles biological screening of beneficial symbionts and a potentially widespread, unstudied benefit of alcohol-producing symbionts (e.g., yeasts) in other microbial symbioses.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">29632193</PMID><DateCompleted><Year>2018</Year><Month>08</Month><Day>13</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>14</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1091-6490</ISSN><JournalIssue CitedMedium="Internet"><Volume>115</Volume><Issue>17</Issue><PubDate><Year>2018</Year><Month>04</Month><Day>24</Day></PubDate></JournalIssue><Title>Proceedings of the National Academy of Sciences of the United States of America</Title><ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation></Journal><ArticleTitle>Symbiont selection via alcohol benefits fungus farming by ambrosia beetles.</ArticleTitle><Pagination><MedlinePgn>4447-4452</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1716852115</ELocationID><Abstract><AbstractText>Animal-microbe mutualisms are typically maintained by vertical symbiont transmission or partner choice. A third mechanism, screening of high-quality symbionts, has been predicted in theory, but empirical examples are rare. Here we demonstrate that ambrosia beetles rely on ethanol within host trees for promoting gardens of their fungal symbiont and producing offspring. Ethanol has long been known as the main attractant for many of these fungus-farming beetles as they select host trees in which they excavate tunnels and cultivate fungal gardens. More than 300 attacks by <i>Xylosandrus germanus</i> and other species were triggered by baiting trees with ethanol lures, but none of the foundresses established fungal gardens or produced broods unless tree tissues contained in vivo ethanol resulting from irrigation with ethanol solutions. More <i>X. germanus</i> brood were also produced in a rearing substrate containing ethanol. These benefits are a result of increased food supply via the positive effects of ethanol on food-fungus biomass. Selected <i>Ambrosiella</i> and <i>Raffaelea</i> fungal isolates from ethanol-responsive ambrosia beetles profited directly and indirectly by (<i>i</i>) a higher biomass on medium containing ethanol, (<i>ii</i>) strong alcohol dehydrogenase enzymatic activity, and (<i>iii</i>) a competitive advantage over weedy fungal garden competitors (<i>Aspergillus</i>, <i>Penicillium</i>) that are inhibited by ethanol. As ambrosia fungi both detoxify and produce ethanol, they may maintain the selectivity of their alcohol-rich habitat for their own purpose and that of other ethanol-resistant/producing microbes. This resembles biological screening of beneficial symbionts and a potentially widespread, unstudied benefit of alcohol-producing symbionts (e.g., yeasts) in other microbial symbioses.</AbstractText><CopyrightInformation>Copyright © 2018 the Author(s). Published by PNAS.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Ranger</LastName><ForeName>Christopher M</ForeName><Initials>CM</Initials><AffiliationInfo><Affiliation>Horticultural Insects Research Laboratory, US Department of Agriculture-Agricultural Research Service, Wooster, OH 44691; christopher.ranger@ars.usda.gov peter.biedermann@uni-wuerzburg.de.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Entomology, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Biedermann</LastName><ForeName>Peter H W</ForeName><Initials>PHW</Initials><Identifier Source="ORCID">0000-0003-4234-5659</Identifier><AffiliationInfo><Affiliation>Department of Biochemistry, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany; christopher.ranger@ars.usda.gov peter.biedermann@uni-wuerzburg.de.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Animal Ecology and Tropical Biology, Biozentrum, Julius Maximilian University Würzburg, 97074 Würzburg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Phuntumart</LastName><ForeName>Vipaporn</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Beligala</LastName><ForeName>Gayathri U</ForeName><Initials>GU</Initials><AffiliationInfo><Affiliation>Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ghosh</LastName><ForeName>Satyaki</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Palmquist</LastName><ForeName>Debra E</ForeName><Initials>DE</Initials><AffiliationInfo><Affiliation>US Department of Agriculture-Agricultural Research Service Midwest Area, Peoria, IL 61604.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mueller</LastName><ForeName>Robert</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW 2751, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Barnett</LastName><ForeName>Jenny</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Horticultural Insects Research Laboratory, US Department of Agriculture-Agricultural Research Service, Wooster, OH 44691.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schultz</LastName><ForeName>Peter B</ForeName><Initials>PB</Initials><AffiliationInfo><Affiliation>Hampton Roads Agricultural Research and Extension Center, Virginia Polytechnic Institute and State University, Virginia Beach, VA 23455.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Reding</LastName><ForeName>Michael E</ForeName><Initials>ME</Initials><AffiliationInfo><Affiliation>Horticultural Insects Research Laboratory, US Department of Agriculture-Agricultural Research Service, Wooster, OH 44691.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Entomology, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Benz</LastName><ForeName>J Philipp</ForeName><Initials>JP</Initials><AffiliationInfo><Affiliation>School of Life Sciences Weihenstephan, Technical University of Munich, D-85354 Freising, Germany.</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><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>04</Month><Day>09</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Proc Natl Acad Sci U S A</MedlineTA><NlmUniqueID>7505876</NlmUniqueID><ISSNLinking>0027-8424</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>3K9958V90M</RegistryNumber><NameOfSubstance UI="D000431">Ethanol</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D001230" MajorTopicYN="N">Aspergillus</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D001517" MajorTopicYN="N">Coleoptera</DescriptorName><QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000431" MajorTopicYN="N">Ethanol</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName><QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010407" MajorTopicYN="N">Penicillium</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">fungus-farming insects</Keyword><Keyword MajorTopicYN="Y">host screening</Keyword><Keyword MajorTopicYN="Y">insect–fungus mutualism</Keyword><Keyword MajorTopicYN="Y">plant–insect–microbe interactions</Keyword><Keyword MajorTopicYN="Y">symbiosis</Keyword></KeywordList><CoiStatement>The authors declare no conflict of interest.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>4</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2018</Year><Month>8</Month><Day>14</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2018</Year><Month>4</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId 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