The Gut Microbiota in Camellia Weevils Are Influenced by Plant Secondary Metabolites and Contribute to Saponin Degradation.
Identifieur interne : 000005 ( Main/Exploration ); précédent : 000004; suivant : 000006The Gut Microbiota in Camellia Weevils Are Influenced by Plant Secondary Metabolites and Contribute to Saponin Degradation.
Auteurs : Shouke Zhang [République populaire de Chine] ; Jinping Shu [Oman] ; Huaijun Xue [République populaire de Chine] ; Wei Zhang [République populaire de Chine] ; Yabo Zhang [République populaire de Chine] ; Yaning Liu [République populaire de Chine] ; Linxin Fang [République populaire de Chine] ; Yangdong Wang [Oman, République populaire de Chine] ; Haojie Wang [République populaire de Chine]Source :
- mSystems [ 2379-5077 ] ; 2020.
Abstract
The camellia weevil (CW [Curculio chinensis]) is a notorious host-specific predator of the seeds of Camellia species in China, causing seed losses of up to 60%. The weevil is capable of overcoming host tree chemical defenses, while the mechanisms of how these beetles contend with the toxic compounds are still unknown. Here, we examined the interaction between the gut microbes of CW and camellia seed chemistry and found that beetle-associated bacterial symbionts mediate tea saponin degradation. We demonstrate that the gut microbial community profile of CW was significantly plant associated, and the gut bacterial community associated with CW feeding on Camellia oleifera seeds is enriched with genes involved in tea saponin degradation compared with those feeding on Camellia sinensis and Camellia reticulata seeds. Twenty-seven bacteria from the genera Enterobacter, Serratia, Acinetobacter, and Micrococcus subsisted on tea saponin as a sole source of carbon and nitrogen, and Acinetobacter species are identified as being involved in the degradation of tea saponin. Our results provide the first metagenome of gut bacterial communities associated with a specialist insect pest of Camellia trees, and the results are consistent with a potential microbial contribution to the detoxification of tree-defensive chemicals.IMPORTANCE The gut microbiome may play an important role in insect-plant interactions mediated by plant secondary metabolites, but the microbial communities and functions of toxic plant feeders are still poorly characterized. In the present study, we provide the first metagenome of gut bacterial communities associated with a specialist weevil feeding on saponin-rich and saponin-low camellia seeds, and the results reveal the correlation between bacterial diversity and plant allelochemicals. We also used cultured microbes to establish their saponin-degradative capacity outside the insect. Our results provide new experimental context to better understand how gut microbial communities are influenced by plant secondary metabolites and how the resistance mechanisms involving microbes have evolved to deal with the chemical defenses of plants.
DOI: 10.1128/mSystems.00692-19
PubMed: 32184361
PubMed Central: PMC7380582
Affiliations:
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The Gut Microbiota in Camellia Weevils Are Influenced by Plant Secondary Metabolites and Contribute to Saponin Degradation.</title><author><name sortKey="Zhang, Shouke" sort="Zhang, Shouke" uniqKey="Zhang S" first="Shouke" last="Zhang">Shouke Zhang</name><affiliation wicri:level="3"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de 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last="Fang">Linxin Fang</name><affiliation wicri:level="1"><nlm:affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang</wicri:regionArea><wicri:noRegion>Zhejiang</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Yangdong" sort="Wang, Yangdong" uniqKey="Wang Y" first="Yangdong" last="Wang">Yangdong Wang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing, People's Republic of China shu_jinping001@163.com wyd11111@126.com.</nlm:affiliation><country wicri:rule="url">Oman</country></affiliation><affiliation wicri:level="1"><nlm:affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, 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China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang</wicri:regionArea><wicri:noRegion>Zhejiang</wicri:noRegion></affiliation></author><author><name sortKey="Shu, Jinping" sort="Shu, Jinping" uniqKey="Shu J" first="Jinping" last="Shu">Jinping Shu</name><affiliation wicri:level="1"><nlm:affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China shu_jinping001@163.com wyd11111@126.com.</nlm:affiliation><country wicri:rule="url">Oman</country></affiliation></author><author><name sortKey="Xue, Huaijun" sort="Xue, Huaijun" uniqKey="Xue H" first="Huaijun" last="Xue">Huaijun Xue</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Zhang, Wei" sort="Zhang, Wei" uniqKey="Zhang W" first="Wei" last="Zhang">Wei Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang</wicri:regionArea><wicri:noRegion>Zhejiang</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Yabo" sort="Zhang, Yabo" uniqKey="Zhang Y" first="Yabo" last="Zhang">Yabo Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang</wicri:regionArea><wicri:noRegion>Zhejiang</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Yaning" sort="Liu, Yaning" uniqKey="Liu Y" first="Yaning" last="Liu">Yaning Liu</name><affiliation wicri:level="1"><nlm:affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang</wicri:regionArea><wicri:noRegion>Zhejiang</wicri:noRegion></affiliation></author><author><name sortKey="Fang, Linxin" sort="Fang, Linxin" uniqKey="Fang L" first="Linxin" last="Fang">Linxin Fang</name><affiliation wicri:level="1"><nlm:affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang</wicri:regionArea><wicri:noRegion>Zhejiang</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Yangdong" sort="Wang, Yangdong" uniqKey="Wang Y" first="Yangdong" last="Wang">Yangdong Wang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing, People's Republic of China shu_jinping001@163.com wyd11111@126.com.</nlm:affiliation><country wicri:rule="url">Oman</country></affiliation><affiliation wicri:level="1"><nlm:affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang</wicri:regionArea><wicri:noRegion>Zhejiang</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Haojie" sort="Wang, Haojie" uniqKey="Wang H" first="Haojie" last="Wang">Haojie Wang</name><affiliation wicri:level="1"><nlm:affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang</wicri:regionArea><wicri:noRegion>Zhejiang</wicri:noRegion></affiliation></author></analytic><series><title level="j">mSystems</title><idno type="ISSN">2379-5077</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The camellia weevil (CW [<i>Curculio chinensis</i>]) is a notorious host-specific predator of the seeds of <i>Camellia</i> species in China, causing seed losses of up to 60%. The weevil is capable of overcoming host tree chemical defenses, while the mechanisms of how these beetles contend with the toxic compounds are still unknown. Here, we examined the interaction between the gut microbes of CW and camellia seed chemistry and found that beetle-associated bacterial symbionts mediate tea saponin degradation. We demonstrate that the gut microbial community profile of CW was significantly plant associated, and the gut bacterial community associated with CW feeding on <i>Camellia oleifera</i> seeds is enriched with genes involved in tea saponin degradation compared with those feeding on <i>Camellia sinensis</i> and <i>Camellia reticulata</i> seeds. Twenty-seven bacteria from the genera <i>Enterobacter</i>, <i>Serratia</i>, <i>Acinetobacter</i>, and <i>Micrococcus</i> subsisted on tea saponin as a sole source of carbon and nitrogen, and <i>Acinetobacter</i> species are identified as being involved in the degradation of tea saponin. Our results provide the first metagenome of gut bacterial communities associated with a specialist insect pest of <i>Camellia</i> trees, and the results are consistent with a potential microbial contribution to the detoxification of tree-defensive chemicals.<b>IMPORTANCE</b> The gut microbiome may play an important role in insect-plant interactions mediated by plant secondary metabolites, but the microbial communities and functions of toxic plant feeders are still poorly characterized. In the present study, we provide the first metagenome of gut bacterial communities associated with a specialist weevil feeding on saponin-rich and saponin-low camellia seeds, and the results reveal the correlation between bacterial diversity and plant allelochemicals. We also used cultured microbes to establish their saponin-degradative capacity outside the insect. Our results provide new experimental context to better understand how gut microbial communities are influenced by plant secondary metabolites and how the resistance mechanisms involving microbes have evolved to deal with the chemical defenses of plants.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">32184361</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>28</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Print">2379-5077</ISSN><JournalIssue CitedMedium="Print"><Volume>5</Volume><Issue>2</Issue><PubDate><Year>2020</Year><Month>Mar</Month><Day>17</Day></PubDate></JournalIssue><Title>mSystems</Title><ISOAbbreviation>mSystems</ISOAbbreviation></Journal><ArticleTitle>The Gut Microbiota in Camellia Weevils Are Influenced by Plant Secondary Metabolites and Contribute to Saponin Degradation.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">e00692-19</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1128/mSystems.00692-19</ELocationID><Abstract><AbstractText>The camellia weevil (CW [<i>Curculio chinensis</i>]) is a notorious host-specific predator of the seeds of <i>Camellia</i> species in China, causing seed losses of up to 60%. The weevil is capable of overcoming host tree chemical defenses, while the mechanisms of how these beetles contend with the toxic compounds are still unknown. Here, we examined the interaction between the gut microbes of CW and camellia seed chemistry and found that beetle-associated bacterial symbionts mediate tea saponin degradation. We demonstrate that the gut microbial community profile of CW was significantly plant associated, and the gut bacterial community associated with CW feeding on <i>Camellia oleifera</i> seeds is enriched with genes involved in tea saponin degradation compared with those feeding on <i>Camellia sinensis</i> and <i>Camellia reticulata</i> seeds. Twenty-seven bacteria from the genera <i>Enterobacter</i>, <i>Serratia</i>, <i>Acinetobacter</i>, and <i>Micrococcus</i> subsisted on tea saponin as a sole source of carbon and nitrogen, and <i>Acinetobacter</i> species are identified as being involved in the degradation of tea saponin. Our results provide the first metagenome of gut bacterial communities associated with a specialist insect pest of <i>Camellia</i> trees, and the results are consistent with a potential microbial contribution to the detoxification of tree-defensive chemicals.<b>IMPORTANCE</b> The gut microbiome may play an important role in insect-plant interactions mediated by plant secondary metabolites, but the microbial communities and functions of toxic plant feeders are still poorly characterized. In the present study, we provide the first metagenome of gut bacterial communities associated with a specialist weevil feeding on saponin-rich and saponin-low camellia seeds, and the results reveal the correlation between bacterial diversity and plant allelochemicals. We also used cultured microbes to establish their saponin-degradative capacity outside the insect. Our results provide new experimental context to better understand how gut microbial communities are influenced by plant secondary metabolites and how the resistance mechanisms involving microbes have evolved to deal with the chemical defenses of plants.</AbstractText><CopyrightInformation>Copyright © 2020 Zhang et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Shouke</ForeName><Initials>S</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-7941-2029</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing, People's Republic of China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shu</LastName><ForeName>Jinping</ForeName><Initials>J</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-3685-9349</Identifier><AffiliationInfo><Affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China shu_jinping001@163.com wyd11111@126.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xue</LastName><ForeName>Huaijun</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, People's Republic of China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Wei</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Yabo</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Yaning</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fang</LastName><ForeName>Linxin</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Yangdong</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing, People's Republic of China shu_jinping001@163.com wyd11111@126.com.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Haojie</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, Zhejiang, People's Republic of China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>03</Month><Day>17</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>mSystems</MedlineTA><NlmUniqueID>101680636</NlmUniqueID><ISSNLinking>2379-5077</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Camellia weevil</Keyword><Keyword MajorTopicYN="N">degradation</Keyword><Keyword MajorTopicYN="N">diversity</Keyword><Keyword MajorTopicYN="N">gut microbiome</Keyword><Keyword MajorTopicYN="N">phytophagous insect</Keyword><Keyword MajorTopicYN="N">plant secondary metabolites</Keyword><Keyword MajorTopicYN="N">tea saponin</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>3</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>3</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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Chine</li></country><settlement><li>Pékin</li></settlement></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Zhang, Shouke" sort="Zhang, Shouke" uniqKey="Zhang S" first="Shouke" last="Zhang">Shouke Zhang</name></noRegion><name sortKey="Fang, Linxin" sort="Fang, Linxin" uniqKey="Fang L" first="Linxin" last="Fang">Linxin Fang</name><name sortKey="Liu, Yaning" sort="Liu, Yaning" uniqKey="Liu Y" first="Yaning" last="Liu">Yaning Liu</name><name sortKey="Wang, Haojie" sort="Wang, Haojie" uniqKey="Wang H" first="Haojie" last="Wang">Haojie Wang</name><name sortKey="Wang, Yangdong" sort="Wang, Yangdong" uniqKey="Wang Y" first="Yangdong" last="Wang">Yangdong Wang</name><name sortKey="Xue, Huaijun" sort="Xue, Huaijun" uniqKey="Xue H" first="Huaijun" last="Xue">Huaijun Xue</name><name sortKey="Zhang, Shouke" sort="Zhang, Shouke" uniqKey="Zhang S" first="Shouke" last="Zhang">Shouke Zhang</name><name sortKey="Zhang, Wei" sort="Zhang, Wei" uniqKey="Zhang W" first="Wei" last="Zhang">Wei Zhang</name><name sortKey="Zhang, Yabo" sort="Zhang, Yabo" uniqKey="Zhang Y" first="Yabo" last="Zhang">Yabo Zhang</name></country><country name="Oman"><noRegion><name sortKey="Shu, Jinping" sort="Shu, Jinping" uniqKey="Shu J" first="Jinping" last="Shu">Jinping Shu</name></noRegion><name sortKey="Wang, Yangdong" sort="Wang, Yangdong" uniqKey="Wang Y" first="Yangdong" last="Wang">Yangdong Wang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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