The Promoting Effect of Gut Microbiota on Growth and Development of Red Palm Weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Dryophthoridae) by Modulating Its Nutritional Metabolism.
Identifieur interne : 000056 ( Main/Exploration ); précédent : 000055; suivant : 000057The Promoting Effect of Gut Microbiota on Growth and Development of Red Palm Weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Dryophthoridae) by Modulating Its Nutritional Metabolism.
Auteurs : Prosper Habineza [République populaire de Chine] ; Abrar Muhammad [République populaire de Chine] ; Tianliang Ji [République populaire de Chine] ; Rong Xiao [République populaire de Chine] ; Xianyuan Yin [République populaire de Chine] ; Youming Hou [République populaire de Chine] ; Zhanghong Shi [République populaire de Chine]Source :
- Frontiers in microbiology [ 1664-302X ] ; 2019.
Abstract
Red palm weevil (RPW), Rhynchophorus ferrugineus Olivier, is a destructive pest for palm trees worldwide. Recent studies have shown that RPW gut is colonized by microbes and alterations in gut microbiota can significantly modify its hemolymph nutrition content. However, the exact effects of gut microbiota on RPW phenotype and the underlying mechanisms remain elusive. Here germ-free (GF) RPW larvae were generated from dechorionated eggs which were reared on sterilized artificial food under axenic conditions. Compared with controls, the larval development of GF RPW individuals was markedly depressed and their body mass was reduced as well. Furthermore, the content of hemolymph protein, glucose and triglyceride were dropped significantly in GF RPW larvae. Interestingly, introducing gut microbiota into GF individuals could significantly increase the levels of the three nutrition indices. Additionally, it has also been demonstrated that RPW larvae monoassociated with Lactococcus lactis exhibited the same level of protein content with the CR (conventionally reared) insects while feeding Enterobacter cloacae to GF larvae increased their hemolymph triglyceride and glucose content markedly. Consequently, our findings suggest that gut microbiota profoundly affect the development of this pest by regulating its nutrition metabolism and different gut bacterial species show distinct impact on host physiology. Taken together, the establishment of GF and gnotobiotic RPW larvae will advance the elucidation of molecular mechanisms behind the interactions between RPW and its gut microbiota.
DOI: 10.3389/fmicb.2019.01212
PubMed: 31191510
PubMed Central: PMC6549218
Affiliations:
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Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Hou, Youming" sort="Hou, Youming" uniqKey="Hou Y" first="Youming" last="Hou">Youming Hou</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Shi, Zhanghong" 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Prosper" sort="Habineza, Prosper" uniqKey="Habineza P" first="Prosper" last="Habineza">Prosper Habineza</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Muhammad, Abrar" sort="Muhammad, Abrar" uniqKey="Muhammad A" first="Abrar" last="Muhammad">Abrar Muhammad</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Ji, Tianliang" sort="Ji, Tianliang" uniqKey="Ji T" first="Tianliang" last="Ji">Tianliang Ji</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Xiao, Rong" sort="Xiao, Rong" uniqKey="Xiao R" first="Rong" last="Xiao">Rong Xiao</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Yin, Xianyuan" sort="Yin, Xianyuan" uniqKey="Yin X" first="Xianyuan" last="Yin">Xianyuan Yin</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Hou, Youming" sort="Hou, Youming" uniqKey="Hou Y" first="Youming" last="Hou">Youming Hou</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author><author><name sortKey="Shi, Zhanghong" sort="Shi, Zhanghong" uniqKey="Shi Z" first="Zhanghong" last="Shi">Zhanghong Shi</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian</wicri:regionArea><wicri:noRegion>Fujian</wicri:noRegion></affiliation></author></analytic><series><title level="j">Frontiers in microbiology</title><idno type="ISSN">1664-302X</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Red palm weevil (RPW), <i>Rhynchophorus ferrugineus</i> Olivier, is a destructive pest for palm trees worldwide. Recent studies have shown that RPW gut is colonized by microbes and alterations in gut microbiota can significantly modify its hemolymph nutrition content. However, the exact effects of gut microbiota on RPW phenotype and the underlying mechanisms remain elusive. Here germ-free (GF) RPW larvae were generated from dechorionated eggs which were reared on sterilized artificial food under axenic conditions. Compared with controls, the larval development of GF RPW individuals was markedly depressed and their body mass was reduced as well. Furthermore, the content of hemolymph protein, glucose and triglyceride were dropped significantly in GF RPW larvae. Interestingly, introducing gut microbiota into GF individuals could significantly increase the levels of the three nutrition indices. Additionally, it has also been demonstrated that RPW larvae monoassociated with <i>Lactococcus lactis</i> exhibited the same level of protein content with the CR (conventionally reared) insects while feeding <i>Enterobacter cloacae</i> to GF larvae increased their hemolymph triglyceride and glucose content markedly. Consequently, our findings suggest that gut microbiota profoundly affect the development of this pest by regulating its nutrition metabolism and different gut bacterial species show distinct impact on host physiology. Taken together, the establishment of GF and gnotobiotic RPW larvae will advance the elucidation of molecular mechanisms behind the interactions between RPW and its gut microbiota.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">31191510</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>01</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-302X</ISSN><JournalIssue CitedMedium="Print"><Volume>10</Volume><PubDate><Year>2019</Year></PubDate></JournalIssue><Title>Frontiers in microbiology</Title><ISOAbbreviation>Front Microbiol</ISOAbbreviation></Journal><ArticleTitle>The Promoting Effect of Gut Microbiota on Growth and Development of Red Palm Weevil, <i>Rhynchophorus ferrugineus</i> (Olivier) (Coleoptera: Dryophthoridae) by Modulating Its Nutritional Metabolism.</ArticleTitle><Pagination><MedlinePgn>1212</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fmicb.2019.01212</ELocationID><Abstract><AbstractText>Red palm weevil (RPW), <i>Rhynchophorus ferrugineus</i> Olivier, is a destructive pest for palm trees worldwide. Recent studies have shown that RPW gut is colonized by microbes and alterations in gut microbiota can significantly modify its hemolymph nutrition content. However, the exact effects of gut microbiota on RPW phenotype and the underlying mechanisms remain elusive. Here germ-free (GF) RPW larvae were generated from dechorionated eggs which were reared on sterilized artificial food under axenic conditions. Compared with controls, the larval development of GF RPW individuals was markedly depressed and their body mass was reduced as well. Furthermore, the content of hemolymph protein, glucose and triglyceride were dropped significantly in GF RPW larvae. Interestingly, introducing gut microbiota into GF individuals could significantly increase the levels of the three nutrition indices. Additionally, it has also been demonstrated that RPW larvae monoassociated with <i>Lactococcus lactis</i> exhibited the same level of protein content with the CR (conventionally reared) insects while feeding <i>Enterobacter cloacae</i> to GF larvae increased their hemolymph triglyceride and glucose content markedly. Consequently, our findings suggest that gut microbiota profoundly affect the development of this pest by regulating its nutrition metabolism and different gut bacterial species show distinct impact on host physiology. Taken together, the establishment of GF and gnotobiotic RPW larvae will advance the elucidation of molecular mechanisms behind the interactions between RPW and its gut microbiota.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Habineza</LastName><ForeName>Prosper</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Muhammad</LastName><ForeName>Abrar</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ji</LastName><ForeName>Tianliang</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xiao</LastName><ForeName>Rong</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yin</LastName><ForeName>Xianyuan</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hou</LastName><ForeName>Youming</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shi</LastName><ForeName>Zhanghong</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fujian, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>05</Month><Day>29</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Microbiol</MedlineTA><NlmUniqueID>101548977</NlmUniqueID><ISSNLinking>1664-302X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Rhynchophorus ferrugineus</Keyword><Keyword MajorTopicYN="N">germ-free larvae</Keyword><Keyword MajorTopicYN="N">gut microbiota</Keyword><Keyword MajorTopicYN="N">insect symbiosis</Keyword><Keyword MajorTopicYN="N">nutrition metabolism</Keyword><Keyword MajorTopicYN="N">symbiotic invasion</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>01</Month><Day>07</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>05</Month><Day>14</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>6</Month><Day>14</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>6</Month><Day>14</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>6</Month><Day>14</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31191510</ArticleId><ArticleId IdType="doi">10.3389/fmicb.2019.01212</ArticleId><ArticleId IdType="pmc">PMC6549218</ArticleId></ArticleIdList><ReferenceList><Reference><Citation>Genome Res. 2001 May;11(5):731-53</Citation><ArticleIdList><ArticleId IdType="pubmed">11337471</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Ecol. 2005 Aug;14(9):2637-43</Citation><ArticleIdList><ArticleId IdType="pubmed">16029466</ArticleId></ArticleIdList></Reference><Reference><Citation>Can J Microbiol. 2006 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