Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid–Vibrio symbiosis
Summary Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host–microbe associations are less well recognized. During the early st...
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| Veröffentlicht in: | Molecular microbiology 2010-11, Vol.78 (4), p.903-915 |
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| creator | Wang, Yanling Dunn, Anne K. Wilneff, Jacqueline McFall‐Ngai, Margaret J. Spiro, Stephen Ruby, Edward G. |
| description | Summary
Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host–microbe associations are less well recognized. During the early stages of the squid–vibrio symbiosis, the bacterial symbiont Vibrio fischeri encounters host‐derived NO, which has been hypothesized to serve as a specificity determinant. We demonstrate here that the flavohaemoglobin, Hmp, of V. fischeri protects against NO, both in culture and during colonization of the squid host. Transcriptional analyses indicate that hmp expression is highly responsive to NO, principally through the repressor, NsrR. Hmp protects V. fischeri from NO inhibition of aerobic respiration, and removes NO under both oxic and anoxic conditions. A Δhmp mutant of V. fischeri initiates squid colonization less effectively than wild type, but is rescued by the presence of an NO synthase inhibitor. The hmp promoter is activated during the initial stage of colonization, during which the Δhmp strain fails to form normal‐sized aggregates of colonizing cells. Taken together, these results suggest that the sensing of host‐derived NO by NsrR, and the subsequent removal of NO by Hmp, influence aggregate size and, thereby, V. fischeri colonization efficiency. |
| doi_str_mv | 10.1111/j.1365-2958.2010.07376.x |
| format | Article |
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Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host–microbe associations are less well recognized. During the early stages of the squid–vibrio symbiosis, the bacterial symbiont Vibrio fischeri encounters host‐derived NO, which has been hypothesized to serve as a specificity determinant. We demonstrate here that the flavohaemoglobin, Hmp, of V. fischeri protects against NO, both in culture and during colonization of the squid host. Transcriptional analyses indicate that hmp expression is highly responsive to NO, principally through the repressor, NsrR. Hmp protects V. fischeri from NO inhibition of aerobic respiration, and removes NO under both oxic and anoxic conditions. A Δhmp mutant of V. fischeri initiates squid colonization less effectively than wild type, but is rescued by the presence of an NO synthase inhibitor. The hmp promoter is activated during the initial stage of colonization, during which the Δhmp strain fails to form normal‐sized aggregates of colonizing cells. Taken together, these results suggest that the sensing of host‐derived NO by NsrR, and the subsequent removal of NO by Hmp, influence aggregate size and, thereby, V. fischeri colonization efficiency.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2010.07376.x</identifier><identifier>PMID: 20815823</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Aerobiosis ; Aliivibrio fischeri - immunology ; Aliivibrio fischeri - physiology ; Anaerobiosis ; Animals ; Bacterial Proteins - metabolism ; Bacteriology ; Biological and medical sciences ; Decapodiformes - immunology ; Decapodiformes - microbiology ; Fundamental and applied biological sciences. Psychology ; Gene expression ; Gene Expression Profiling ; Gram-negative bacteria ; Hemeproteins - metabolism ; Microbiology ; Miscellaneous ; Mutation ; Nitric oxide ; Nitric Oxide - metabolism ; Nitric Oxide - toxicity ; Oxidative stress ; Repressor Proteins - metabolism ; Signal transduction ; Symbiosis ; Vibrio fischeri</subject><ispartof>Molecular microbiology, 2010-11, Vol.78 (4), p.903-915</ispartof><rights>2010 Blackwell Publishing Ltd</rights><rights>2015 INIST-CNRS</rights><rights>2010 Blackwell Publishing Ltd.</rights><rights>Copyright Blackwell Publishing Ltd. Nov 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5246-d604204b254d7a49ec152e889a8c839b88b7d60ca02739356446477bb92cdabd3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1365-2958.2010.07376.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1365-2958.2010.07376.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,777,781,1412,1428,27905,27906,45555,45556,46390,46814</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=23411568$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20815823$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Yanling</creatorcontrib><creatorcontrib>Dunn, Anne K.</creatorcontrib><creatorcontrib>Wilneff, Jacqueline</creatorcontrib><creatorcontrib>McFall‐Ngai, Margaret J.</creatorcontrib><creatorcontrib>Spiro, Stephen</creatorcontrib><creatorcontrib>Ruby, Edward G.</creatorcontrib><title>Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid–Vibrio symbiosis</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host–microbe associations are less well recognized. During the early stages of the squid–vibrio symbiosis, the bacterial symbiont Vibrio fischeri encounters host‐derived NO, which has been hypothesized to serve as a specificity determinant. We demonstrate here that the flavohaemoglobin, Hmp, of V. fischeri protects against NO, both in culture and during colonization of the squid host. Transcriptional analyses indicate that hmp expression is highly responsive to NO, principally through the repressor, NsrR. Hmp protects V. fischeri from NO inhibition of aerobic respiration, and removes NO under both oxic and anoxic conditions. A Δhmp mutant of V. fischeri initiates squid colonization less effectively than wild type, but is rescued by the presence of an NO synthase inhibitor. The hmp promoter is activated during the initial stage of colonization, during which the Δhmp strain fails to form normal‐sized aggregates of colonizing cells. Taken together, these results suggest that the sensing of host‐derived NO by NsrR, and the subsequent removal of NO by Hmp, influence aggregate size and, thereby, V. fischeri colonization efficiency.</description><subject>Aerobiosis</subject><subject>Aliivibrio fischeri - immunology</subject><subject>Aliivibrio fischeri - physiology</subject><subject>Anaerobiosis</subject><subject>Animals</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriology</subject><subject>Biological and medical sciences</subject><subject>Decapodiformes - immunology</subject><subject>Decapodiformes - microbiology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gram-negative bacteria</subject><subject>Hemeproteins - metabolism</subject><subject>Microbiology</subject><subject>Miscellaneous</subject><subject>Mutation</subject><subject>Nitric oxide</subject><subject>Nitric Oxide - metabolism</subject><subject>Nitric Oxide - toxicity</subject><subject>Oxidative stress</subject><subject>Repressor Proteins - metabolism</subject><subject>Signal transduction</subject><subject>Symbiosis</subject><subject>Vibrio fischeri</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkctu1DAUhi0EokPhFZCFhFhl8DWxFyxQxaVSKzaA2Fm248ycURJP7aTM7HgH3pAnwaFDkfDG1jmfjv7jDyFMyZqW83q3pryWFdNSrRkpVdLwpl4fHqDVfeMhWhEtScUV-3aGnuS8I4RyUvPH6IwRRaVifIX2X8EliLiD7LchAe56exu3Ngxx00cHI96nOAU_ZWw3FsY84RGmBB7HA7QBt3OCcYOhFMFOEEccOzxtA843M7S_fvw8zc_HwUHMkJ-iR53tc3h2us_Rl_fvPl98rK4-fbi8eHtVeclEXbU1EYwIx6RoGyt08FSyoJS2yiuunVKuKYy3hDVcc1kLUYumcU4z31rX8nP06m5uyX8zhzyZoawY-t6OIc7ZKElFzQjjhXzxH7mLcxpLONPoEkZQvUDPT9DshtCafYLBpqP5-5MFeHkCbPa275IdPeR_HBeUyloV7s0d9x36cLzvU2IWs2ZnFoFmEWgWs-aPWXMw19eXy4v_BlPwmEY</recordid><startdate>201011</startdate><enddate>201011</enddate><creator>Wang, Yanling</creator><creator>Dunn, Anne K.</creator><creator>Wilneff, Jacqueline</creator><creator>McFall‐Ngai, Margaret J.</creator><creator>Spiro, Stephen</creator><creator>Ruby, Edward G.</creator><general>Blackwell Publishing Ltd</general><general>Blackwell</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</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>7TN</scope><scope>F1W</scope><scope>H95</scope><scope>H98</scope><scope>L.G</scope></search><sort><creationdate>201011</creationdate><title>Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid–Vibrio symbiosis</title><author>Wang, Yanling ; Dunn, Anne K. ; Wilneff, Jacqueline ; McFall‐Ngai, Margaret J. ; Spiro, Stephen ; Ruby, Edward G.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5246-d604204b254d7a49ec152e889a8c839b88b7d60ca02739356446477bb92cdabd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Aerobiosis</topic><topic>Aliivibrio fischeri - immunology</topic><topic>Aliivibrio fischeri - physiology</topic><topic>Anaerobiosis</topic><topic>Animals</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteriology</topic><topic>Biological and medical sciences</topic><topic>Decapodiformes - immunology</topic><topic>Decapodiformes - microbiology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gram-negative bacteria</topic><topic>Hemeproteins - metabolism</topic><topic>Microbiology</topic><topic>Miscellaneous</topic><topic>Mutation</topic><topic>Nitric oxide</topic><topic>Nitric Oxide - metabolism</topic><topic>Nitric Oxide - toxicity</topic><topic>Oxidative stress</topic><topic>Repressor Proteins - metabolism</topic><topic>Signal transduction</topic><topic>Symbiosis</topic><topic>Vibrio fischeri</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Yanling</creatorcontrib><creatorcontrib>Dunn, Anne K.</creatorcontrib><creatorcontrib>Wilneff, Jacqueline</creatorcontrib><creatorcontrib>McFall‐Ngai, Margaret J.</creatorcontrib><creatorcontrib>Spiro, Stephen</creatorcontrib><creatorcontrib>Ruby, Edward G.</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>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</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>Oceanic Abstracts</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Aquaculture Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Yanling</au><au>Dunn, Anne K.</au><au>Wilneff, Jacqueline</au><au>McFall‐Ngai, Margaret J.</au><au>Spiro, Stephen</au><au>Ruby, Edward G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid–Vibrio symbiosis</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2010-11</date><risdate>2010</risdate><volume>78</volume><issue>4</issue><spage>903</spage><epage>915</epage><pages>903-915</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host–microbe associations are less well recognized. During the early stages of the squid–vibrio symbiosis, the bacterial symbiont Vibrio fischeri encounters host‐derived NO, which has been hypothesized to serve as a specificity determinant. We demonstrate here that the flavohaemoglobin, Hmp, of V. fischeri protects against NO, both in culture and during colonization of the squid host. Transcriptional analyses indicate that hmp expression is highly responsive to NO, principally through the repressor, NsrR. Hmp protects V. fischeri from NO inhibition of aerobic respiration, and removes NO under both oxic and anoxic conditions. A Δhmp mutant of V. fischeri initiates squid colonization less effectively than wild type, but is rescued by the presence of an NO synthase inhibitor. The hmp promoter is activated during the initial stage of colonization, during which the Δhmp strain fails to form normal‐sized aggregates of colonizing cells. Taken together, these results suggest that the sensing of host‐derived NO by NsrR, and the subsequent removal of NO by Hmp, influence aggregate size and, thereby, V. fischeri colonization efficiency.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>20815823</pmid><doi>10.1111/j.1365-2958.2010.07376.x</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Aerobiosis Aliivibrio fischeri - immunology Aliivibrio fischeri - physiology Anaerobiosis Animals Bacterial Proteins - metabolism Bacteriology Biological and medical sciences Decapodiformes - immunology Decapodiformes - microbiology Fundamental and applied biological sciences. Psychology Gene expression Gene Expression Profiling Gram-negative bacteria Hemeproteins - metabolism Microbiology Miscellaneous Mutation Nitric oxide Nitric Oxide - metabolism Nitric Oxide - toxicity Oxidative stress Repressor Proteins - metabolism Signal transduction Symbiosis Vibrio fischeri |
| title | Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid–Vibrio symbiosis |
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