Intestinal Microbiota Confer Protection by Priming the Immune System of Red Palm Weevil Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae).
Identifieur interne : 000072 ( Main/Exploration ); précédent : 000071; suivant : 000073Intestinal Microbiota Confer Protection by Priming the Immune System of Red Palm Weevil Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae).
Auteurs : Abrar Muhammad [République populaire de Chine] ; Prosper Habineza [République populaire de Chine] ; Tianliang Ji [République populaire de Chine] ; Youming Hou [République populaire de Chine] ; Zhanghong Shi [République populaire de Chine]Source :
- Frontiers in physiology [ 1664-042X ] ; 2019.
Abstract
The immune system of animals, including insects, is the vital factor to maintain the symbiotic interactions between animals and their associated microbes. However, the effects of gut microbiota on insect immunity remain mostly elusive. Red palm weevil (RPW), Rhynchophorus ferrugineus Olivier, is a destructive pest of palm trees worldwide, which has forged alliances with its gut microbiota. Here, we found that the aposymbiotic insects succumbed at a significantly faster rate than conventionally reared (CR) ones upon bacterial infection. Physiological assays confirmed that CR insects had stronger antimicrobial activity and higher phenoloxidase activity in contrast to germfree (GF) ones, indicating that the systemic immune responses of GF individuals were compromised markedly. Interestingly, under the bacterial challenge conditions, the reassociation of gut microbiota with GF insects could enhance their survival rate by rescuing their immunocompetence. Furthermore, comparative transcriptome analysis uncovered that 35 immune-related genes, including pathogen recognition receptors, effectors and immune signaling pathway, were significantly downregulated in GF insects as compared to CR ones. Collectively, our findings corrobate that intestinal commensal bacteria have profound immunostimulatory effects on RPW larvae. Therefore, knowledge on the effects of gut microbiota on RPW immune defenses may contribute to of set up efficient control strategies of this pest.
DOI: 10.3389/fphys.2019.01303
PubMed: 31681013
PubMed Central: PMC6805723
Affiliations:
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Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, 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, Fuzhou</wicri:regionArea><placeName><settlement type="city">Fuzhou</settlement><region type="province">Fujian</region></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, 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, Fuzhou</wicri:regionArea><placeName><settlement type="city">Fuzhou</settlement><region type="province">Fujian</region></placeName></affiliation></author><author><name sortKey="Hou, Youming" sort="Hou, Youming" uniqKey="Hou Y" first="Youming" last="Hou">Youming Hou</name><affiliation wicri:level="3"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, 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, Fuzhou</wicri:regionArea><placeName><settlement type="city">Fuzhou</settlement><region type="province">Fujian</region></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, 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, Fuzhou</wicri:regionArea><placeName><settlement type="city">Fuzhou</settlement><region type="province">Fujian</region></placeName></affiliation></author><author><name sortKey="Shi, Zhanghong" sort="Shi, Zhanghong" uniqKey="Shi Z" first="Zhanghong" last="Shi">Zhanghong Shi</name><affiliation wicri:level="3"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, 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, Fuzhou</wicri:regionArea><placeName><settlement type="city">Fuzhou</settlement><region type="province">Fujian</region></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, 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, Fuzhou</wicri:regionArea><placeName><settlement type="city">Fuzhou</settlement><region type="province">Fujian</region></placeName></affiliation></author></analytic><series><title level="j">Frontiers in physiology</title><idno type="ISSN">1664-042X</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">The immune system of animals, including insects, is the vital factor to maintain the symbiotic interactions between animals and their associated microbes. However, the effects of gut microbiota on insect immunity remain mostly elusive. Red palm weevil (RPW), <i>Rhynchophorus ferrugineus</i> Olivier, is a destructive pest of palm trees worldwide, which has forged alliances with its gut microbiota. Here, we found that the aposymbiotic insects succumbed at a significantly faster rate than conventionally reared (CR) ones upon bacterial infection. Physiological assays confirmed that CR insects had stronger antimicrobial activity and higher phenoloxidase activity in contrast to germfree (GF) ones, indicating that the systemic immune responses of GF individuals were compromised markedly. Interestingly, under the bacterial challenge conditions, the reassociation of gut microbiota with GF insects could enhance their survival rate by rescuing their immunocompetence. Furthermore, comparative transcriptome analysis uncovered that 35 immune-related genes, including pathogen recognition receptors, effectors and immune signaling pathway, were significantly downregulated in GF insects as compared to CR ones. Collectively, our findings corrobate that intestinal commensal bacteria have profound immunostimulatory effects on RPW larvae. Therefore, knowledge on the effects of gut microbiota on RPW immune defenses may contribute to of set up efficient control strategies of this pest.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">31681013</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>01</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-042X</ISSN><JournalIssue CitedMedium="Print"><Volume>10</Volume><PubDate><Year>2019</Year></PubDate></JournalIssue><Title>Frontiers in physiology</Title><ISOAbbreviation>Front Physiol</ISOAbbreviation></Journal><ArticleTitle>Intestinal Microbiota Confer Protection by Priming the Immune System of Red Palm Weevil <i>Rhynchophorus ferrugineus</i> Olivier (Coleoptera: Dryophthoridae).</ArticleTitle><Pagination><MedlinePgn>1303</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fphys.2019.01303</ELocationID><Abstract><AbstractText>The immune system of animals, including insects, is the vital factor to maintain the symbiotic interactions between animals and their associated microbes. However, the effects of gut microbiota on insect immunity remain mostly elusive. Red palm weevil (RPW), <i>Rhynchophorus ferrugineus</i> Olivier, is a destructive pest of palm trees worldwide, which has forged alliances with its gut microbiota. Here, we found that the aposymbiotic insects succumbed at a significantly faster rate than conventionally reared (CR) ones upon bacterial infection. Physiological assays confirmed that CR insects had stronger antimicrobial activity and higher phenoloxidase activity in contrast to germfree (GF) ones, indicating that the systemic immune responses of GF individuals were compromised markedly. Interestingly, under the bacterial challenge conditions, the reassociation of gut microbiota with GF insects could enhance their survival rate by rescuing their immunocompetence. Furthermore, comparative transcriptome analysis uncovered that 35 immune-related genes, including pathogen recognition receptors, effectors and immune signaling pathway, were significantly downregulated in GF insects as compared to CR ones. Collectively, our findings corrobate that intestinal commensal bacteria have profound immunostimulatory effects on RPW larvae. Therefore, knowledge on the effects of gut microbiota on RPW immune defenses may contribute to of set up efficient control strategies of this pest.</AbstractText><CopyrightInformation>Copyright © 2019 Muhammad, Habineza, Ji, Hou and Shi.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><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, Fuzhou, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China.</Affiliation></AffiliationInfo></Author><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, Fuzhou, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, 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, Fuzhou, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, 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, Fuzhou, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, 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, Fuzhou, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>10</Month><Day>16</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Physiol</MedlineTA><NlmUniqueID>101549006</NlmUniqueID><ISSNLinking>1664-042X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Rhynchophorus ferrugineus</Keyword><Keyword MajorTopicYN="N">gut microbiota</Keyword><Keyword MajorTopicYN="N">insect immunity</Keyword><Keyword MajorTopicYN="N">invasive biology</Keyword><Keyword MajorTopicYN="N">symbiosis</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>05</Month><Day>14</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>09</Month><Day>27</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>11</Month><Day>5</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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first="Prosper" last="Habineza">Prosper Habineza</name><name sortKey="Hou, Youming" sort="Hou, Youming" uniqKey="Hou Y" first="Youming" last="Hou">Youming Hou</name><name sortKey="Hou, Youming" sort="Hou, Youming" uniqKey="Hou Y" first="Youming" last="Hou">Youming Hou</name><name sortKey="Ji, Tianliang" sort="Ji, Tianliang" uniqKey="Ji T" first="Tianliang" last="Ji">Tianliang Ji</name><name sortKey="Ji, Tianliang" sort="Ji, Tianliang" uniqKey="Ji T" first="Tianliang" last="Ji">Tianliang Ji</name><name sortKey="Muhammad, Abrar" sort="Muhammad, Abrar" uniqKey="Muhammad A" first="Abrar" last="Muhammad">Abrar Muhammad</name><name sortKey="Shi, Zhanghong" sort="Shi, Zhanghong" uniqKey="Shi Z" first="Zhanghong" last="Shi">Zhanghong Shi</name><name sortKey="Shi, Zhanghong" sort="Shi, Zhanghong" uniqKey="Shi Z" first="Zhanghong" last="Shi">Zhanghong Shi</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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