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Antimicrobial Peptides Keep Insect Endosymbionts Under Control
Vertically transmitted endosymbionts persist for millions of years in invertebrates and play an important role in animal evolution. However, the functional basis underlying the maintenance of these long-term resident bacteria is unknown. We report that the weevil coleoptericin-A (ColA) antimicrobial...
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Published in: | Science (American Association for the Advancement of Science) 2011-10, Vol.334 (6054), p.362-365 |
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description | Vertically transmitted endosymbionts persist for millions of years in invertebrates and play an important role in animal evolution. However, the functional basis underlying the maintenance of these long-term resident bacteria is unknown. We report that the weevil coleoptericin-A (ColA) antimicrobial peptide selectively targets endosymbionts within the bacteriocytes and regulates their growth through the inhibition of cell division. Silencing the colA gene with RNA interference resulted in a decrease in size of the giant filamentous endosymbionts, which escaped from the bacteriocytes and spread into insect tissues. Although this family of peptides is commonly linked with microbe clearance, this work shows that endosymbiosis benefits from ColA, suggesting that long-term host-symbiont coevolution might have shaped immune effectors for symbiont maintenance. |
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However, the functional basis underlying the maintenance of these long-term resident bacteria is unknown. We report that the weevil coleoptericin-A (ColA) antimicrobial peptide selectively targets endosymbionts within the bacteriocytes and regulates their growth through the inhibition of cell division. Silencing the colA gene with RNA interference resulted in a decrease in size of the giant filamentous endosymbionts, which escaped from the bacteriocytes and spread into insect tissues. Although this family of peptides is commonly linked with microbe clearance, this work shows that endosymbiosis benefits from ColA, suggesting that long-term host-symbiont coevolution might have shaped immune effectors for symbiont maintenance.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.1209728</identifier><identifier>PMID: 22021855</identifier><identifier>CODEN: SCIEAS</identifier><language>eng</language><publisher>Washington, DC: American Association for the Advancement of Science</publisher><subject>Animal and plant ecology ; Animal, plant and microbial ecology ; Animals ; Antimicrobials ; Autoecology ; Bacteria ; Bacterial Outer Membrane Proteins - metabolism ; Bacterial Proteins - metabolism ; Bacteriocytes ; Biological and medical sciences ; Cellular Biology ; Chaperonin 60 - genetics ; Chaperonin 60 - metabolism ; Cytoplasm - metabolism ; Endosymbionts ; Epithelial cells ; Epithelial Cells - metabolism ; Escherichia coli - cytology ; Escherichia coli - drug effects ; Fat body ; Fat Body - metabolism ; Fundamental and applied biological sciences. Psychology ; Gammaproteobacteria - cytology ; Gammaproteobacteria - drug effects ; Gammaproteobacteria - metabolism ; Gammaproteobacteria - physiology ; Genomes ; Insect genetics ; Insect larvae ; Insect Proteins - genetics ; Insect Proteins - metabolism ; Insect Proteins - pharmacology ; Insects ; Life Sciences ; Microbial corrosion ; Micrococcus luteus - drug effects ; Oocytes - metabolism ; Peptides ; Protozoa. 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However, the functional basis underlying the maintenance of these long-term resident bacteria is unknown. We report that the weevil coleoptericin-A (ColA) antimicrobial peptide selectively targets endosymbionts within the bacteriocytes and regulates their growth through the inhibition of cell division. Silencing the colA gene with RNA interference resulted in a decrease in size of the giant filamentous endosymbionts, which escaped from the bacteriocytes and spread into insect tissues. Although this family of peptides is commonly linked with microbe clearance, this work shows that endosymbiosis benefits from ColA, suggesting that long-term host-symbiont coevolution might have shaped immune effectors for symbiont maintenance.</description><subject>Animal and plant ecology</subject><subject>Animal, plant and microbial ecology</subject><subject>Animals</subject><subject>Antimicrobials</subject><subject>Autoecology</subject><subject>Bacteria</subject><subject>Bacterial Outer Membrane Proteins - metabolism</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriocytes</subject><subject>Biological and medical sciences</subject><subject>Cellular Biology</subject><subject>Chaperonin 60 - genetics</subject><subject>Chaperonin 60 - metabolism</subject><subject>Cytoplasm - metabolism</subject><subject>Endosymbionts</subject><subject>Epithelial cells</subject><subject>Epithelial Cells - metabolism</subject><subject>Escherichia coli - cytology</subject><subject>Escherichia coli - drug effects</subject><subject>Fat body</subject><subject>Fat Body - metabolism</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gammaproteobacteria - cytology</subject><subject>Gammaproteobacteria - drug effects</subject><subject>Gammaproteobacteria - metabolism</subject><subject>Gammaproteobacteria - physiology</subject><subject>Genomes</subject><subject>Insect genetics</subject><subject>Insect larvae</subject><subject>Insect Proteins - genetics</subject><subject>Insect Proteins - metabolism</subject><subject>Insect Proteins - pharmacology</subject><subject>Insects</subject><subject>Life Sciences</subject><subject>Microbial corrosion</subject><subject>Micrococcus luteus - drug effects</subject><subject>Oocytes - metabolism</subject><subject>Peptides</subject><subject>Protozoa. Invertebrata</subject><subject>RNA Interference</subject><subject>Saccharomyces cerevisiae - drug effects</subject><subject>Symbiosis</subject><subject>Weevils</subject><subject>Weevils - cytology</subject><subject>Weevils - metabolism</subject><subject>Weevils - microbiology</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNqF0c9LHDEUB_AgFd1qz55aBqGUHkZfJr8vwrLYKi7oQc8hm8lglplkm8wK_vfNdqcKvfSUkPdJ8pIvQmcYLjBu-GW23gXrLnADSjTyAM0wKFarBsgHNAMgvJYg2DH6mPMaoNQUOULHTQMNlozN0NU8jH7wNsWVN3314Dajb12u7pzbVLchOztW16GN-XVY-RjGXD2F1qVqUeYp9qfosDN9dp-m8QQ9_bh-XNzUy_uft4v5srYMxFhjrgzuWmmdtUoSThiXirZdQyWhxrS8FRQTyqXkwnIlpCFcsU45XGqKG3KCvu_PfTa93iQ_mPSqo_H6Zr7UuzXAgKWS9AUX-21vNyn-2ro86sFn6_reBBe3WSssgQpM2f8lAC-NwE6e_yPXcZtCebKWSnFCCZEFXe5R-c2ck-veOsWgd3HpKS49xVV2fJmO3a4G1775v_kU8HUCJlvTd8kE6_O7owKE_HP1571b5zGm9zqBEjjD5Dcvv6UT</recordid><startdate>20111021</startdate><enddate>20111021</enddate><creator>Login, Frédéric H.</creator><creator>Balmand, Séverine</creator><creator>Vallier, Agnès</creator><creator>Vincent-Monégat, Carole</creator><creator>Vigneron, Aurélien</creator><creator>Weiss-Gayet, Michèle</creator><creator>Rochat, Didier</creator><creator>Heddi, Abdelaziz</creator><general>American Association for the Advancement of Science</general><general>The American Association for the Advancement of Science</general><general>American Association for the Advancement of Science (AAAS)</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QF</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TK</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-1909-3556</orcidid><orcidid>https://orcid.org/0000-0003-4986-6465</orcidid><orcidid>https://orcid.org/0000-0001-6377-5573</orcidid></search><sort><creationdate>20111021</creationdate><title>Antimicrobial Peptides Keep Insect Endosymbionts Under Control</title><author>Login, Frédéric H. ; Balmand, Séverine ; Vallier, Agnès ; Vincent-Monégat, Carole ; Vigneron, Aurélien ; Weiss-Gayet, Michèle ; Rochat, Didier ; Heddi, Abdelaziz</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c507t-169a1fd8cecc9836356894df24834aad6d7413468867c6978a3695f9e1ad696a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Animal and plant ecology</topic><topic>Animal, plant and microbial ecology</topic><topic>Animals</topic><topic>Antimicrobials</topic><topic>Autoecology</topic><topic>Bacteria</topic><topic>Bacterial Outer Membrane Proteins - metabolism</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteriocytes</topic><topic>Biological and medical sciences</topic><topic>Cellular Biology</topic><topic>Chaperonin 60 - genetics</topic><topic>Chaperonin 60 - metabolism</topic><topic>Cytoplasm - metabolism</topic><topic>Endosymbionts</topic><topic>Epithelial cells</topic><topic>Epithelial Cells - metabolism</topic><topic>Escherichia coli - cytology</topic><topic>Escherichia coli - drug effects</topic><topic>Fat body</topic><topic>Fat Body - metabolism</topic><topic>Fundamental and applied biological sciences. 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Invertebrata</topic><topic>RNA Interference</topic><topic>Saccharomyces cerevisiae - drug effects</topic><topic>Symbiosis</topic><topic>Weevils</topic><topic>Weevils - cytology</topic><topic>Weevils - metabolism</topic><topic>Weevils - microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Login, Frédéric H.</creatorcontrib><creatorcontrib>Balmand, Séverine</creatorcontrib><creatorcontrib>Vallier, Agnès</creatorcontrib><creatorcontrib>Vincent-Monégat, Carole</creatorcontrib><creatorcontrib>Vigneron, Aurélien</creatorcontrib><creatorcontrib>Weiss-Gayet, Michèle</creatorcontrib><creatorcontrib>Rochat, Didier</creatorcontrib><creatorcontrib>Heddi, Abdelaziz</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Login, Frédéric H.</au><au>Balmand, Séverine</au><au>Vallier, Agnès</au><au>Vincent-Monégat, Carole</au><au>Vigneron, Aurélien</au><au>Weiss-Gayet, Michèle</au><au>Rochat, Didier</au><au>Heddi, Abdelaziz</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Antimicrobial Peptides Keep Insect Endosymbionts Under Control</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2011-10-21</date><risdate>2011</risdate><volume>334</volume><issue>6054</issue><spage>362</spage><epage>365</epage><pages>362-365</pages><issn>0036-8075</issn><eissn>1095-9203</eissn><coden>SCIEAS</coden><abstract>Vertically transmitted endosymbionts persist for millions of years in invertebrates and play an important role in animal evolution. However, the functional basis underlying the maintenance of these long-term resident bacteria is unknown. We report that the weevil coleoptericin-A (ColA) antimicrobial peptide selectively targets endosymbionts within the bacteriocytes and regulates their growth through the inhibition of cell division. Silencing the colA gene with RNA interference resulted in a decrease in size of the giant filamentous endosymbionts, which escaped from the bacteriocytes and spread into insect tissues. 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subjects | Animal and plant ecology Animal, plant and microbial ecology Animals Antimicrobials Autoecology Bacteria Bacterial Outer Membrane Proteins - metabolism Bacterial Proteins - metabolism Bacteriocytes Biological and medical sciences Cellular Biology Chaperonin 60 - genetics Chaperonin 60 - metabolism Cytoplasm - metabolism Endosymbionts Epithelial cells Epithelial Cells - metabolism Escherichia coli - cytology Escherichia coli - drug effects Fat body Fat Body - metabolism Fundamental and applied biological sciences. Psychology Gammaproteobacteria - cytology Gammaproteobacteria - drug effects Gammaproteobacteria - metabolism Gammaproteobacteria - physiology Genomes Insect genetics Insect larvae Insect Proteins - genetics Insect Proteins - metabolism Insect Proteins - pharmacology Insects Life Sciences Microbial corrosion Micrococcus luteus - drug effects Oocytes - metabolism Peptides Protozoa. Invertebrata RNA Interference Saccharomyces cerevisiae - drug effects Symbiosis Weevils Weevils - cytology Weevils - metabolism Weevils - microbiology |
title | Antimicrobial Peptides Keep Insect Endosymbionts Under Control |
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