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Pleiotropic Role of Quorum-Sensing Autoinducer 2 in Photorhabdus luminescens
Bacterial virulence is an integrative process that may involve quorum sensing. In this work, we compared by global expression profiling the wild-type entomopathogenic Photorhabdus luminescens subsp. laumondii TT01 to a luxS-deficient mutant unable to synthesize the type 2 quorum-sensing inducer AI-2...
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Published in: | Applied and Environmental Microbiology 2006-10, Vol.72 (10), p.6439-6451 |
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creator | Krin, Evelyne Chakroun, Nesrine Turlin, Evelyne Givaudan, Alain Gaboriau, François Bonne, Isabelle Rousselle, Jean-Claude Frangeul, Lionel Lacroix, Céline Hullo, Marie-Françoise Marisa, Laetitia Danchin, Antoine Derzelle, Sylviane |
description | Bacterial virulence is an integrative process that may involve quorum sensing. In this work, we compared by global expression profiling the wild-type entomopathogenic Photorhabdus luminescens subsp. laumondii TT01 to a luxS-deficient mutant unable to synthesize the type 2 quorum-sensing inducer AI-2. AI-2 was shown to regulate more than 300 targets involved in most compartments and metabolic pathways of the cell. AI-2 is located high in the hierarchy, as it controls the expression of several transcriptional regulators. The regulatory effect of AI-2 appeared to be dose dependent. The luxS-deficient strain exhibited decreased biofilm formation and increased type IV/V pilus-dependent twitching motility. AI-2 activated its own synthesis and transport. It also modulated bioluminescence by regulating the synthesis of spermidine. AI-2 was further shown to increase oxidative stress resistance, which is necessary to overcome part of the innate immune response of the host insect involving reactive oxygen species. Finally, we showed that the luxS-deficient strain had attenuated virulence against the lepidopteran Spodoptera littoralis. We concluded that AI-2 is involved mainly in early steps of insect invasion in P. luminescens. |
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In this work, we compared by global expression profiling the wild-type entomopathogenic Photorhabdus luminescens subsp. laumondii TT01 to a luxS-deficient mutant unable to synthesize the type 2 quorum-sensing inducer AI-2. AI-2 was shown to regulate more than 300 targets involved in most compartments and metabolic pathways of the cell. AI-2 is located high in the hierarchy, as it controls the expression of several transcriptional regulators. The regulatory effect of AI-2 appeared to be dose dependent. The luxS-deficient strain exhibited decreased biofilm formation and increased type IV/V pilus-dependent twitching motility. AI-2 activated its own synthesis and transport. It also modulated bioluminescence by regulating the synthesis of spermidine. AI-2 was further shown to increase oxidative stress resistance, which is necessary to overcome part of the innate immune response of the host insect involving reactive oxygen species. Finally, we showed that the luxS-deficient strain had attenuated virulence against the lepidopteran Spodoptera littoralis. We concluded that AI-2 is involved mainly in early steps of insect invasion in P. luminescens.</description><identifier>ISSN: 0099-2240</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/AEM.00398-06</identifier><identifier>PMID: 17021191</identifier><identifier>CODEN: AEMIDF</identifier><language>eng</language><publisher>Washington, DC: American Society for Microbiology</publisher><subject>autoinducer 2 ; Bacteria ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Bacterial Proteins - physiology ; biofilm ; Biofilms ; Biological and medical sciences ; bioluminescence ; Carbon-Sulfur Lyases - deficiency ; Carbon-Sulfur Lyases - genetics ; Carbon-Sulfur Lyases - metabolism ; cell communication ; cell motility ; Ecology, environment ; entomopathogenic bacteria ; Fundamental and applied biological sciences. Psychology ; Gene expression ; Gene Expression Profiling ; gene expression regulation ; genes ; Genetics and Molecular Biology ; global expression profiling ; Homoserine - analogs & derivatives ; Homoserine - physiology ; insect pests ; Lactones ; Lepidoptera ; Life Sciences ; microbial physiology ; Microbiology ; oxidative stress ; Oxidative Stress - physiology ; Photorhabdus - chemistry ; Photorhabdus - pathogenicity ; Photorhabdus - physiology ; Photorhabdus luminescens ; Polyamines - metabolism ; Protein synthesis ; quorum sensing ; Remote sensing ; Signal Transduction - physiology ; spermidine ; Spodoptera littoralis ; stress tolerance ; Studies ; transcription factors ; virulence ; Virulence - physiology ; Viruses</subject><ispartof>Applied and Environmental Microbiology, 2006-10, Vol.72 (10), p.6439-6451</ispartof><rights>2007 INIST-CNRS</rights><rights>Copyright American Society for Microbiology Oct 2006</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Copyright © 2006, American Society for Microbiology 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c517t-54d8b9bfb04c9e5ba1adc96da8f95873d034f9d9d6cbf4188e850745e47253b73</citedby><cites>FETCH-LOGICAL-c517t-54d8b9bfb04c9e5ba1adc96da8f95873d034f9d9d6cbf4188e850745e47253b73</cites><orcidid>0000-0002-2302-2291 ; 0000-0002-3901-5133 ; 0000-0002-0992-8775</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC1610301/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC1610301/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,3174,3175,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=18178581$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17021191$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02664186$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Krin, Evelyne</creatorcontrib><creatorcontrib>Chakroun, Nesrine</creatorcontrib><creatorcontrib>Turlin, Evelyne</creatorcontrib><creatorcontrib>Givaudan, Alain</creatorcontrib><creatorcontrib>Gaboriau, François</creatorcontrib><creatorcontrib>Bonne, Isabelle</creatorcontrib><creatorcontrib>Rousselle, Jean-Claude</creatorcontrib><creatorcontrib>Frangeul, Lionel</creatorcontrib><creatorcontrib>Lacroix, Céline</creatorcontrib><creatorcontrib>Hullo, Marie-Françoise</creatorcontrib><creatorcontrib>Marisa, Laetitia</creatorcontrib><creatorcontrib>Danchin, Antoine</creatorcontrib><creatorcontrib>Derzelle, Sylviane</creatorcontrib><title>Pleiotropic Role of Quorum-Sensing Autoinducer 2 in Photorhabdus luminescens</title><title>Applied and Environmental Microbiology</title><addtitle>Appl Environ Microbiol</addtitle><description>Bacterial virulence is an integrative process that may involve quorum sensing. In this work, we compared by global expression profiling the wild-type entomopathogenic Photorhabdus luminescens subsp. laumondii TT01 to a luxS-deficient mutant unable to synthesize the type 2 quorum-sensing inducer AI-2. AI-2 was shown to regulate more than 300 targets involved in most compartments and metabolic pathways of the cell. AI-2 is located high in the hierarchy, as it controls the expression of several transcriptional regulators. The regulatory effect of AI-2 appeared to be dose dependent. The luxS-deficient strain exhibited decreased biofilm formation and increased type IV/V pilus-dependent twitching motility. AI-2 activated its own synthesis and transport. It also modulated bioluminescence by regulating the synthesis of spermidine. AI-2 was further shown to increase oxidative stress resistance, which is necessary to overcome part of the innate immune response of the host insect involving reactive oxygen species. Finally, we showed that the luxS-deficient strain had attenuated virulence against the lepidopteran Spodoptera littoralis. We concluded that AI-2 is involved mainly in early steps of insect invasion in P. luminescens.</description><subject>autoinducer 2</subject><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacterial Proteins - physiology</subject><subject>biofilm</subject><subject>Biofilms</subject><subject>Biological and medical sciences</subject><subject>bioluminescence</subject><subject>Carbon-Sulfur Lyases - deficiency</subject><subject>Carbon-Sulfur Lyases - genetics</subject><subject>Carbon-Sulfur Lyases - metabolism</subject><subject>cell communication</subject><subject>cell motility</subject><subject>Ecology, environment</subject><subject>entomopathogenic bacteria</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>gene expression regulation</subject><subject>genes</subject><subject>Genetics and Molecular Biology</subject><subject>global expression profiling</subject><subject>Homoserine - analogs & derivatives</subject><subject>Homoserine - physiology</subject><subject>insect pests</subject><subject>Lactones</subject><subject>Lepidoptera</subject><subject>Life Sciences</subject><subject>microbial physiology</subject><subject>Microbiology</subject><subject>oxidative stress</subject><subject>Oxidative Stress - physiology</subject><subject>Photorhabdus - chemistry</subject><subject>Photorhabdus - pathogenicity</subject><subject>Photorhabdus - physiology</subject><subject>Photorhabdus luminescens</subject><subject>Polyamines - metabolism</subject><subject>Protein synthesis</subject><subject>quorum sensing</subject><subject>Remote sensing</subject><subject>Signal Transduction - physiology</subject><subject>spermidine</subject><subject>Spodoptera littoralis</subject><subject>stress tolerance</subject><subject>Studies</subject><subject>transcription factors</subject><subject>virulence</subject><subject>Virulence - physiology</subject><subject>Viruses</subject><issn>0099-2240</issn><issn>1098-5336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><recordid>eNqFkc1v1DAUxCMEokvhxhkiJCohkfKev2JfkFZVS5EWUSg9W07ibFwl8WInRfz3eNkVC71wsmX_PPM8k2XPEU4RiXy3PP90CkCVLEA8yBYIaccpFQ-zBYBSBSEMjrInMd4CAAMhH2dHWAJBVLjIVle9dX4KfuPq_Kvvbe7b_MvswzwU13aMblzny3nybmzm2oac5G7Mrzo_-dCZqplj3s-DG22sE_w0e9SaPtpn-_U4u7k4_3Z2Waw-f_h4tlwVNcdyKjhrZKWqtgJWK8srg6aplWiMbBWXJW2AslY1qhF11TKU0koOJeOWlYTTqqTH2fud7mauBtsk6ymYXm-CG0z4qb1x-t-b0XV67e80CgQKmATe7AS6e88ulyu9PQMiRHIWd1v2ZG8W_PfZxkkPLv22781o_Ry1kIooCf8HUVGuqCQJfHUPvPVzGFNimgBPEShGE_R2B9XBxxhs-2dOBL0tXqfi9e_iNYiEv_g7kgO8bzoBr_eAibXp22DG2sUDJ7GUXOJhuM6tux8uWG3ioI0ddEm21oJRlaCXO6g1Xpt1SEI31yRlAIggUBH6C8mtyS0</recordid><startdate>20061001</startdate><enddate>20061001</enddate><creator>Krin, Evelyne</creator><creator>Chakroun, Nesrine</creator><creator>Turlin, Evelyne</creator><creator>Givaudan, Alain</creator><creator>Gaboriau, François</creator><creator>Bonne, Isabelle</creator><creator>Rousselle, Jean-Claude</creator><creator>Frangeul, Lionel</creator><creator>Lacroix, Céline</creator><creator>Hullo, Marie-Françoise</creator><creator>Marisa, Laetitia</creator><creator>Danchin, Antoine</creator><creator>Derzelle, Sylviane</creator><general>American Society for Microbiology</general><scope>FBQ</scope><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>7QL</scope><scope>7QO</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7QR</scope><scope>7X8</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2302-2291</orcidid><orcidid>https://orcid.org/0000-0002-3901-5133</orcidid><orcidid>https://orcid.org/0000-0002-0992-8775</orcidid></search><sort><creationdate>20061001</creationdate><title>Pleiotropic Role of Quorum-Sensing Autoinducer 2 in Photorhabdus luminescens</title><author>Krin, Evelyne ; Chakroun, Nesrine ; Turlin, Evelyne ; Givaudan, Alain ; Gaboriau, François ; Bonne, Isabelle ; Rousselle, Jean-Claude ; Frangeul, Lionel ; Lacroix, Céline ; Hullo, Marie-Françoise ; Marisa, Laetitia ; Danchin, Antoine ; Derzelle, Sylviane</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c517t-54d8b9bfb04c9e5ba1adc96da8f95873d034f9d9d6cbf4188e850745e47253b73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>autoinducer 2</topic><topic>Bacteria</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacterial Proteins - physiology</topic><topic>biofilm</topic><topic>Biofilms</topic><topic>Biological and medical sciences</topic><topic>bioluminescence</topic><topic>Carbon-Sulfur Lyases - deficiency</topic><topic>Carbon-Sulfur Lyases - genetics</topic><topic>Carbon-Sulfur Lyases - metabolism</topic><topic>cell communication</topic><topic>cell motility</topic><topic>Ecology, environment</topic><topic>entomopathogenic bacteria</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>gene expression regulation</topic><topic>genes</topic><topic>Genetics and Molecular Biology</topic><topic>global expression profiling</topic><topic>Homoserine - analogs & derivatives</topic><topic>Homoserine - physiology</topic><topic>insect pests</topic><topic>Lactones</topic><topic>Lepidoptera</topic><topic>Life Sciences</topic><topic>microbial physiology</topic><topic>Microbiology</topic><topic>oxidative stress</topic><topic>Oxidative Stress - physiology</topic><topic>Photorhabdus - chemistry</topic><topic>Photorhabdus - pathogenicity</topic><topic>Photorhabdus - physiology</topic><topic>Photorhabdus luminescens</topic><topic>Polyamines - metabolism</topic><topic>Protein synthesis</topic><topic>quorum sensing</topic><topic>Remote sensing</topic><topic>Signal Transduction - physiology</topic><topic>spermidine</topic><topic>Spodoptera littoralis</topic><topic>stress tolerance</topic><topic>Studies</topic><topic>transcription factors</topic><topic>virulence</topic><topic>Virulence - physiology</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Krin, Evelyne</creatorcontrib><creatorcontrib>Chakroun, Nesrine</creatorcontrib><creatorcontrib>Turlin, Evelyne</creatorcontrib><creatorcontrib>Givaudan, Alain</creatorcontrib><creatorcontrib>Gaboriau, François</creatorcontrib><creatorcontrib>Bonne, Isabelle</creatorcontrib><creatorcontrib>Rousselle, Jean-Claude</creatorcontrib><creatorcontrib>Frangeul, Lionel</creatorcontrib><creatorcontrib>Lacroix, Céline</creatorcontrib><creatorcontrib>Hullo, Marie-Françoise</creatorcontrib><creatorcontrib>Marisa, Laetitia</creatorcontrib><creatorcontrib>Danchin, Antoine</creatorcontrib><creatorcontrib>Derzelle, Sylviane</creatorcontrib><collection>AGRIS</collection><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>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Applied and Environmental Microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Krin, Evelyne</au><au>Chakroun, Nesrine</au><au>Turlin, Evelyne</au><au>Givaudan, Alain</au><au>Gaboriau, François</au><au>Bonne, Isabelle</au><au>Rousselle, Jean-Claude</au><au>Frangeul, Lionel</au><au>Lacroix, Céline</au><au>Hullo, Marie-Françoise</au><au>Marisa, Laetitia</au><au>Danchin, Antoine</au><au>Derzelle, Sylviane</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pleiotropic Role of Quorum-Sensing Autoinducer 2 in Photorhabdus luminescens</atitle><jtitle>Applied and Environmental Microbiology</jtitle><addtitle>Appl Environ Microbiol</addtitle><date>2006-10-01</date><risdate>2006</risdate><volume>72</volume><issue>10</issue><spage>6439</spage><epage>6451</epage><pages>6439-6451</pages><issn>0099-2240</issn><eissn>1098-5336</eissn><coden>AEMIDF</coden><abstract>Bacterial virulence is an integrative process that may involve quorum sensing. In this work, we compared by global expression profiling the wild-type entomopathogenic Photorhabdus luminescens subsp. laumondii TT01 to a luxS-deficient mutant unable to synthesize the type 2 quorum-sensing inducer AI-2. AI-2 was shown to regulate more than 300 targets involved in most compartments and metabolic pathways of the cell. AI-2 is located high in the hierarchy, as it controls the expression of several transcriptional regulators. The regulatory effect of AI-2 appeared to be dose dependent. The luxS-deficient strain exhibited decreased biofilm formation and increased type IV/V pilus-dependent twitching motility. AI-2 activated its own synthesis and transport. It also modulated bioluminescence by regulating the synthesis of spermidine. AI-2 was further shown to increase oxidative stress resistance, which is necessary to overcome part of the innate immune response of the host insect involving reactive oxygen species. 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subjects | autoinducer 2 Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacterial Proteins - physiology biofilm Biofilms Biological and medical sciences bioluminescence Carbon-Sulfur Lyases - deficiency Carbon-Sulfur Lyases - genetics Carbon-Sulfur Lyases - metabolism cell communication cell motility Ecology, environment entomopathogenic bacteria Fundamental and applied biological sciences. Psychology Gene expression Gene Expression Profiling gene expression regulation genes Genetics and Molecular Biology global expression profiling Homoserine - analogs & derivatives Homoserine - physiology insect pests Lactones Lepidoptera Life Sciences microbial physiology Microbiology oxidative stress Oxidative Stress - physiology Photorhabdus - chemistry Photorhabdus - pathogenicity Photorhabdus - physiology Photorhabdus luminescens Polyamines - metabolism Protein synthesis quorum sensing Remote sensing Signal Transduction - physiology spermidine Spodoptera littoralis stress tolerance Studies transcription factors virulence Virulence - physiology Viruses |
title | Pleiotropic Role of Quorum-Sensing Autoinducer 2 in Photorhabdus luminescens |
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