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Mutation of the Sensor Kinase chvG in Rhizobium leguminosarum Negatively Impacts Cellular Metabolism, Outer Membrane Stability, and Symbiosis
Two-component signal transduction systems (TCS) are a main strategy used by bacteria to sense and adapt to changes in their environment. In the legume symbiont Rhizobium leguminosarum biovar viciae VF39, mutation of chvG, a histidine kinase, caused a number of pleiotropic phenotypes. ChvG mutants ar...
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Published in: | Journal of Bacteriology 2012-02, Vol.194 (4), p.768-777 |
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description | Two-component signal transduction systems (TCS) are a main strategy used by bacteria to sense and adapt to changes in their environment. In the legume symbiont Rhizobium leguminosarum biovar viciae VF39, mutation of chvG, a histidine kinase, caused a number of pleiotropic phenotypes. ChvG mutants are unable to grow on proline, glutamate, histidine, or arginine as the sole carbon source. The chvG mutant secreted smaller amounts of acidic and neutral surface polysaccharides and accumulated abnormally large amounts of poly-ss-hydroxybutyrate. Mutation of chvG caused symbiotic defects on peas, lentils, and vetch; nodules formed by the chvG mutant were small and white and contained only a few cells that had failed to differentiate into bacteroids. Mutation of chvG also destabilized the outer membrane of R. leguminosarum, resulting in increased sensitivity to membrane stressors. Constitutive expression of ropB, the outer membrane protein-encoding gene, restored membrane stability and rescued the sensitivity phenotypes described above. Similar phenotypes have been described for mutations in other ChvG-regulated genes encoding a conserved operon of unknown function and in the fabXL genes required for synthesis of the lipid A very-long-chain fatty acid, suggesting that ChvG is a key component of the envelope stress response in Rhizobium leguminosarum. Collectively, the results of this study demonstrate the important and unique role the ChvG/ChvI TCS plays in the physiology, metabolism, and symbiotic competency of R. leguminosarum. |
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In the legume symbiont Rhizobium leguminosarum biovar viciae VF39, mutation of chvG, a histidine kinase, caused a number of pleiotropic phenotypes. ChvG mutants are unable to grow on proline, glutamate, histidine, or arginine as the sole carbon source. The chvG mutant secreted smaller amounts of acidic and neutral surface polysaccharides and accumulated abnormally large amounts of poly-ss-hydroxybutyrate. Mutation of chvG caused symbiotic defects on peas, lentils, and vetch; nodules formed by the chvG mutant were small and white and contained only a few cells that had failed to differentiate into bacteroids. Mutation of chvG also destabilized the outer membrane of R. leguminosarum, resulting in increased sensitivity to membrane stressors. Constitutive expression of ropB, the outer membrane protein-encoding gene, restored membrane stability and rescued the sensitivity phenotypes described above. Similar phenotypes have been described for mutations in other ChvG-regulated genes encoding a conserved operon of unknown function and in the fabXL genes required for synthesis of the lipid A very-long-chain fatty acid, suggesting that ChvG is a key component of the envelope stress response in Rhizobium leguminosarum. Collectively, the results of this study demonstrate the important and unique role the ChvG/ChvI TCS plays in the physiology, metabolism, and symbiotic competency of R. leguminosarum.</description><identifier>ISSN: 0021-9193</identifier><identifier>EISSN: 1098-5530</identifier><identifier>EISSN: 1067-8832</identifier><identifier>DOI: 10.1128/JB.06357-11</identifier><identifier>PMID: 22155778</identifier><identifier>CODEN: JOBAAY</identifier><language>eng</language><publisher>Washington, DC: American Society for Microbiology</publisher><subject>Agronomy. Soil science and plant productions ; arginine ; Arginine - metabolism ; bacteria ; Bacterial Outer Membrane Proteins - genetics ; Bacterial Proteins - biosynthesis ; Bacterial Proteins - genetics ; Bacteriology ; Biological and medical sciences ; carbon ; Cell Membrane - genetics ; Cell Membrane - physiology ; DNA, Bacterial - genetics ; Economic plant physiology ; Fundamental and applied biological sciences. Psychology ; gene expression ; Genes, Bacterial - genetics ; glutamic acid ; Glutamic Acid - metabolism ; Gram-negative bacteria ; histidine ; Histidine - metabolism ; histidine kinase ; Hydroxybutyrates - metabolism ; Kinases ; Lens Plant - microbiology ; lentils ; Membranes ; Metabolism ; Microbiology ; Miscellaneous ; mutants ; Mutation ; operon ; peas ; phenotype ; Pisum sativum - microbiology ; Polyesters - metabolism ; polysaccharides ; Polysaccharides - metabolism ; proline ; Proline - metabolism ; Protein Kinases - genetics ; Rhizobium leguminosarum - genetics ; Rhizobium leguminosarum - growth & development ; Rhizobium leguminosarum - metabolism ; Rhizobium leguminosarum bv. viciae ; signal transduction ; Signal Transduction - genetics ; stress response ; Stress, Physiological - genetics ; symbionts ; symbiosis ; Symbiosis (nodules, symbiotic nitrogen fixation, mycorrhiza...) ; Symbiosis - genetics ; Symbiosis - physiology ; Transcription Factors - genetics ; very long chain fatty acids ; Vicia ; Vicia - microbiology</subject><ispartof>Journal of Bacteriology, 2012-02, Vol.194 (4), p.768-777</ispartof><rights>2015 INIST-CNRS</rights><rights>Copyright American Society for Microbiology Feb 2012</rights><rights>Copyright © 2012, American Society for Microbiology. All Rights Reserved. 2012 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c519t-ccffc642742c2c7ef5a071747dbc89a18d9f64693db2042b5d2731f39b51b81c3</citedby><cites>FETCH-LOGICAL-c519t-ccffc642742c2c7ef5a071747dbc89a18d9f64693db2042b5d2731f39b51b81c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3272964/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3272964/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,724,777,781,882,3175,3176,27905,27906,53772,53774</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25505659$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22155778$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Vanderlinde, Elizabeth M</creatorcontrib><creatorcontrib>Yost, Christopher K</creatorcontrib><title>Mutation of the Sensor Kinase chvG in Rhizobium leguminosarum Negatively Impacts Cellular Metabolism, Outer Membrane Stability, and Symbiosis</title><title>Journal of Bacteriology</title><addtitle>J Bacteriol</addtitle><description>Two-component signal transduction systems (TCS) are a main strategy used by bacteria to sense and adapt to changes in their environment. In the legume symbiont Rhizobium leguminosarum biovar viciae VF39, mutation of chvG, a histidine kinase, caused a number of pleiotropic phenotypes. ChvG mutants are unable to grow on proline, glutamate, histidine, or arginine as the sole carbon source. The chvG mutant secreted smaller amounts of acidic and neutral surface polysaccharides and accumulated abnormally large amounts of poly-ss-hydroxybutyrate. Mutation of chvG caused symbiotic defects on peas, lentils, and vetch; nodules formed by the chvG mutant were small and white and contained only a few cells that had failed to differentiate into bacteroids. Mutation of chvG also destabilized the outer membrane of R. leguminosarum, resulting in increased sensitivity to membrane stressors. Constitutive expression of ropB, the outer membrane protein-encoding gene, restored membrane stability and rescued the sensitivity phenotypes described above. Similar phenotypes have been described for mutations in other ChvG-regulated genes encoding a conserved operon of unknown function and in the fabXL genes required for synthesis of the lipid A very-long-chain fatty acid, suggesting that ChvG is a key component of the envelope stress response in Rhizobium leguminosarum. Collectively, the results of this study demonstrate the important and unique role the ChvG/ChvI TCS plays in the physiology, metabolism, and symbiotic competency of R. leguminosarum.</description><subject>Agronomy. Soil science and plant productions</subject><subject>arginine</subject><subject>Arginine - metabolism</subject><subject>bacteria</subject><subject>Bacterial Outer Membrane Proteins - genetics</subject><subject>Bacterial Proteins - biosynthesis</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacteriology</subject><subject>Biological and medical sciences</subject><subject>carbon</subject><subject>Cell Membrane - genetics</subject><subject>Cell Membrane - physiology</subject><subject>DNA, Bacterial - genetics</subject><subject>Economic plant physiology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>gene expression</subject><subject>Genes, Bacterial - genetics</subject><subject>glutamic acid</subject><subject>Glutamic Acid - metabolism</subject><subject>Gram-negative bacteria</subject><subject>histidine</subject><subject>Histidine - metabolism</subject><subject>histidine kinase</subject><subject>Hydroxybutyrates - metabolism</subject><subject>Kinases</subject><subject>Lens Plant - microbiology</subject><subject>lentils</subject><subject>Membranes</subject><subject>Metabolism</subject><subject>Microbiology</subject><subject>Miscellaneous</subject><subject>mutants</subject><subject>Mutation</subject><subject>operon</subject><subject>peas</subject><subject>phenotype</subject><subject>Pisum sativum - microbiology</subject><subject>Polyesters - metabolism</subject><subject>polysaccharides</subject><subject>Polysaccharides - metabolism</subject><subject>proline</subject><subject>Proline - metabolism</subject><subject>Protein Kinases - genetics</subject><subject>Rhizobium leguminosarum - genetics</subject><subject>Rhizobium leguminosarum - growth & development</subject><subject>Rhizobium leguminosarum - metabolism</subject><subject>Rhizobium leguminosarum bv. viciae</subject><subject>signal transduction</subject><subject>Signal Transduction - genetics</subject><subject>stress response</subject><subject>Stress, Physiological - genetics</subject><subject>symbionts</subject><subject>symbiosis</subject><subject>Symbiosis (nodules, symbiotic nitrogen fixation, mycorrhiza...)</subject><subject>Symbiosis - genetics</subject><subject>Symbiosis - physiology</subject><subject>Transcription Factors - genetics</subject><subject>very long chain fatty acids</subject><subject>Vicia</subject><subject>Vicia - microbiology</subject><issn>0021-9193</issn><issn>1098-5530</issn><issn>1067-8832</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><recordid>eNp9kk1v1DAQhiMEokvhxB2sSggkmuJx7Di-INEVlJaWSiw9W47jbLxK4sVOFi3_gf-Mwy7l48DBssbz-J0Z-02Sx4BPAEjx6uL0BOcZ4ynAnWQGWBQpYxm-m8wwJpAKENlB8iCEFcZAKSP3kwNCgDHOi1ny_Woc1GBdj1yNhsaghemD8-iD7VUwSDebM2R79Kmx31xpxw61Zjl2tndB-Rh9NMt4e2PaLTrv1koPAc1N246t8ujKDKp0rQ3dMboeBzOddKVXfSwSM7a1w_YYqb5Ci21XWhdseJjcq1UbzKP9fpjcvHv7ef4-vbw-O5-_uUw1AzGkWte1zinhlGiiuamZwhw45VWpC6GgqESd01xkVUkwJSWrCM-gzkTJoCxAZ4fJ653ueiw7U2nTD161cu1tp_xWOmXl35neNnLpNjIjnIicRoHnewHvvowmDLKzQcfJ43RuDFJAgTNa5DiSL_5LQs4LRiihIqJH_6ArN_o-PoQUBCAXnEGEXu4g7V0I3tS3XQOWkx_kxan86YcYRfrJn4Pesr8MEIFne0AFrdo6fo-24TfHGGY5m3pDO66xy-ar9Uaq0MlVKUFQSSXPJ6mnO6RWTqqljzI3C4KB4WmRIst-ADwN0tU</recordid><startdate>20120201</startdate><enddate>20120201</enddate><creator>Vanderlinde, Elizabeth M</creator><creator>Yost, Christopher K</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>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>7S9</scope><scope>L.6</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20120201</creationdate><title>Mutation of the Sensor Kinase chvG in Rhizobium leguminosarum Negatively Impacts Cellular Metabolism, Outer Membrane Stability, and Symbiosis</title><author>Vanderlinde, Elizabeth M ; Yost, Christopher K</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c519t-ccffc642742c2c7ef5a071747dbc89a18d9f64693db2042b5d2731f39b51b81c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Agronomy. Soil science and plant productions</topic><topic>arginine</topic><topic>Arginine - metabolism</topic><topic>bacteria</topic><topic>Bacterial Outer Membrane Proteins - genetics</topic><topic>Bacterial Proteins - biosynthesis</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacteriology</topic><topic>Biological and medical sciences</topic><topic>carbon</topic><topic>Cell Membrane - genetics</topic><topic>Cell Membrane - physiology</topic><topic>DNA, Bacterial - genetics</topic><topic>Economic plant physiology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>gene expression</topic><topic>Genes, Bacterial - genetics</topic><topic>glutamic acid</topic><topic>Glutamic Acid - metabolism</topic><topic>Gram-negative bacteria</topic><topic>histidine</topic><topic>Histidine - metabolism</topic><topic>histidine kinase</topic><topic>Hydroxybutyrates - metabolism</topic><topic>Kinases</topic><topic>Lens Plant - microbiology</topic><topic>lentils</topic><topic>Membranes</topic><topic>Metabolism</topic><topic>Microbiology</topic><topic>Miscellaneous</topic><topic>mutants</topic><topic>Mutation</topic><topic>operon</topic><topic>peas</topic><topic>phenotype</topic><topic>Pisum sativum - microbiology</topic><topic>Polyesters - metabolism</topic><topic>polysaccharides</topic><topic>Polysaccharides - metabolism</topic><topic>proline</topic><topic>Proline - metabolism</topic><topic>Protein Kinases - genetics</topic><topic>Rhizobium leguminosarum - genetics</topic><topic>Rhizobium leguminosarum - growth & development</topic><topic>Rhizobium leguminosarum - metabolism</topic><topic>Rhizobium leguminosarum bv. viciae</topic><topic>signal transduction</topic><topic>Signal Transduction - genetics</topic><topic>stress response</topic><topic>Stress, Physiological - genetics</topic><topic>symbionts</topic><topic>symbiosis</topic><topic>Symbiosis (nodules, symbiotic nitrogen fixation, mycorrhiza...)</topic><topic>Symbiosis - genetics</topic><topic>Symbiosis - physiology</topic><topic>Transcription Factors - genetics</topic><topic>very long chain fatty acids</topic><topic>Vicia</topic><topic>Vicia - microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Vanderlinde, Elizabeth M</creatorcontrib><creatorcontrib>Yost, Christopher K</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>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>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of Bacteriology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Vanderlinde, Elizabeth M</au><au>Yost, Christopher K</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mutation of the Sensor Kinase chvG in Rhizobium leguminosarum Negatively Impacts Cellular Metabolism, Outer Membrane Stability, and Symbiosis</atitle><jtitle>Journal of Bacteriology</jtitle><addtitle>J Bacteriol</addtitle><date>2012-02-01</date><risdate>2012</risdate><volume>194</volume><issue>4</issue><spage>768</spage><epage>777</epage><pages>768-777</pages><issn>0021-9193</issn><eissn>1098-5530</eissn><eissn>1067-8832</eissn><coden>JOBAAY</coden><abstract>Two-component signal transduction systems (TCS) are a main strategy used by bacteria to sense and adapt to changes in their environment. In the legume symbiont Rhizobium leguminosarum biovar viciae VF39, mutation of chvG, a histidine kinase, caused a number of pleiotropic phenotypes. ChvG mutants are unable to grow on proline, glutamate, histidine, or arginine as the sole carbon source. The chvG mutant secreted smaller amounts of acidic and neutral surface polysaccharides and accumulated abnormally large amounts of poly-ss-hydroxybutyrate. Mutation of chvG caused symbiotic defects on peas, lentils, and vetch; nodules formed by the chvG mutant were small and white and contained only a few cells that had failed to differentiate into bacteroids. Mutation of chvG also destabilized the outer membrane of R. leguminosarum, resulting in increased sensitivity to membrane stressors. Constitutive expression of ropB, the outer membrane protein-encoding gene, restored membrane stability and rescued the sensitivity phenotypes described above. Similar phenotypes have been described for mutations in other ChvG-regulated genes encoding a conserved operon of unknown function and in the fabXL genes required for synthesis of the lipid A very-long-chain fatty acid, suggesting that ChvG is a key component of the envelope stress response in Rhizobium leguminosarum. Collectively, the results of this study demonstrate the important and unique role the ChvG/ChvI TCS plays in the physiology, metabolism, and symbiotic competency of R. leguminosarum.</abstract><cop>Washington, DC</cop><pub>American Society for Microbiology</pub><pmid>22155778</pmid><doi>10.1128/JB.06357-11</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Agronomy. Soil science and plant productions arginine Arginine - metabolism bacteria Bacterial Outer Membrane Proteins - genetics Bacterial Proteins - biosynthesis Bacterial Proteins - genetics Bacteriology Biological and medical sciences carbon Cell Membrane - genetics Cell Membrane - physiology DNA, Bacterial - genetics Economic plant physiology Fundamental and applied biological sciences. Psychology gene expression Genes, Bacterial - genetics glutamic acid Glutamic Acid - metabolism Gram-negative bacteria histidine Histidine - metabolism histidine kinase Hydroxybutyrates - metabolism Kinases Lens Plant - microbiology lentils Membranes Metabolism Microbiology Miscellaneous mutants Mutation operon peas phenotype Pisum sativum - microbiology Polyesters - metabolism polysaccharides Polysaccharides - metabolism proline Proline - metabolism Protein Kinases - genetics Rhizobium leguminosarum - genetics Rhizobium leguminosarum - growth & development Rhizobium leguminosarum - metabolism Rhizobium leguminosarum bv. viciae signal transduction Signal Transduction - genetics stress response Stress, Physiological - genetics symbionts symbiosis Symbiosis (nodules, symbiotic nitrogen fixation, mycorrhiza...) Symbiosis - genetics Symbiosis - physiology Transcription Factors - genetics very long chain fatty acids Vicia Vicia - microbiology |
title | Mutation of the Sensor Kinase chvG in Rhizobium leguminosarum Negatively Impacts Cellular Metabolism, Outer Membrane Stability, and Symbiosis |
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