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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
Main Authors: Vanderlinde, Elizabeth M, Yost, Christopher K
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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 &amp; 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&amp;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 &amp; 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 &amp; 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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source ASM Journals; PubMed Central
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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