Cyclic GMP controls Rhodospirillum centenum cyst development
Adenylyl cyclases are widely distributed across all kingdoms whereas guanylyl cyclases are generally thought to be restricted to eukaryotes. Here we report that the α-proteobacterium Rhodospirillum centenum secretes cGMP when developing cysts and that a guanylyl cyclase deletion strain fails to synt...
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| Veröffentlicht in: | Molecular microbiology 2011-02, Vol.79 (3), p.600-615 |
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| creator | Marden, Jeremiah N Dong, Qian Roychowdhury, Sugata Berleman, James E Bauer, Carl E |
| description | Adenylyl cyclases are widely distributed across all kingdoms whereas guanylyl cyclases are generally thought to be restricted to eukaryotes. Here we report that the α-proteobacterium Rhodospirillum centenum secretes cGMP when developing cysts and that a guanylyl cyclase deletion strain fails to synthesize cGMP and is defective in cyst formation. The R. centenum cyclase was purified and shown to effectively synthesize cGMP from GTP in vitro, demonstrating that it is a functional guanylyl cyclase. A homologue of the Escherichia coli cAMP receptor protein (CRP) is linked to the guanylyl cyclase and when deleted is deficient in cyst development. Isothermal calorimetry (ITC) and differential scanning fluorimetry (DSF) analyses demonstrate that the recombinant CRP homologue preferentially binds to, and is stabilized by cGMP, but not cAMP. This study thus provides evidence that cGMP has a crucial role in regulating prokaryotic development. The involvement of cGMP in regulating bacterial development has broader implications as several plant-interacting bacteria contain a similar cyclase coupled by the observation that Azospirillum brasilense also synthesizes cGMP when inducing cysts. |
| doi_str_mv | 10.1111/j.1365-2958.2010.07513.x |
| format | Article |
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Here we report that the α-proteobacterium Rhodospirillum centenum secretes cGMP when developing cysts and that a guanylyl cyclase deletion strain fails to synthesize cGMP and is defective in cyst formation. The R. centenum cyclase was purified and shown to effectively synthesize cGMP from GTP in vitro, demonstrating that it is a functional guanylyl cyclase. A homologue of the Escherichia coli cAMP receptor protein (CRP) is linked to the guanylyl cyclase and when deleted is deficient in cyst development. Isothermal calorimetry (ITC) and differential scanning fluorimetry (DSF) analyses demonstrate that the recombinant CRP homologue preferentially binds to, and is stabilized by cGMP, but not cAMP. This study thus provides evidence that cGMP has a crucial role in regulating prokaryotic development. The involvement of cGMP in regulating bacterial development has broader implications as several plant-interacting bacteria contain a similar cyclase coupled by the observation that Azospirillum brasilense also synthesizes cGMP when inducing cysts.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2010.07513.x</identifier><identifier>PMID: 21214648</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Amino Acid Sequence ; Bacteria ; Bacteriology ; Biochemistry ; Biological and medical sciences ; Chemical synthesis ; Chromatography, High Pressure Liquid ; Conserved Sequence - genetics ; Cyclic AMP Receptor Protein - metabolism ; Cyclic GMP - metabolism ; Cysts ; Fundamental and applied biological sciences. 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Here we report that the α-proteobacterium Rhodospirillum centenum secretes cGMP when developing cysts and that a guanylyl cyclase deletion strain fails to synthesize cGMP and is defective in cyst formation. The R. centenum cyclase was purified and shown to effectively synthesize cGMP from GTP in vitro, demonstrating that it is a functional guanylyl cyclase. A homologue of the Escherichia coli cAMP receptor protein (CRP) is linked to the guanylyl cyclase and when deleted is deficient in cyst development. Isothermal calorimetry (ITC) and differential scanning fluorimetry (DSF) analyses demonstrate that the recombinant CRP homologue preferentially binds to, and is stabilized by cGMP, but not cAMP. This study thus provides evidence that cGMP has a crucial role in regulating prokaryotic development. The involvement of cGMP in regulating bacterial development has broader implications as several plant-interacting bacteria contain a similar cyclase coupled by the observation that Azospirillum brasilense also synthesizes cGMP when inducing cysts.</description><subject>Amino Acid Sequence</subject><subject>Bacteria</subject><subject>Bacteriology</subject><subject>Biochemistry</subject><subject>Biological and medical sciences</subject><subject>Chemical synthesis</subject><subject>Chromatography, High Pressure Liquid</subject><subject>Conserved Sequence - genetics</subject><subject>Cyclic AMP Receptor Protein - metabolism</subject><subject>Cyclic GMP - metabolism</subject><subject>Cysts</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Guanylate Cyclase - chemistry</subject><subject>Guanylate Cyclase - metabolism</subject><subject>Medical sciences</subject><subject>Microbiology</subject><subject>Miscellaneous</subject><subject>Models, Biological</subject><subject>Molecular biology</subject><subject>Molecular Sequence Data</subject><subject>Multigene Family - genetics</subject><subject>Mutation - genetics</subject><subject>Open Reading Frames - genetics</subject><subject>Protein Binding</subject><subject>Regulatory Sequences, Nucleic Acid - genetics</subject><subject>Rhodospirillum centenum - enzymology</subject><subject>Rhodospirillum centenum - genetics</subject><subject>Rhodospirillum centenum - growth & development</subject><subject>Rhodospirillum centenum - metabolism</subject><subject>Sequence Homology, Amino Acid</subject><subject>Signal Transduction</subject><subject>Soil Microbiology</subject><subject>Species Specificity</subject><subject>Spores, Bacterial - cytology</subject><subject>Spores, Bacterial - metabolism</subject><subject>Substrate Specificity</subject><subject>Suppression, Genetic</subject><subject>Transition Temperature</subject><subject>Tumors</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpFkFFLwzAQx4Mobk6_ghbBx84k16Qp6IMMnYMNRR34FtJrph1dO5tOt29v6qbmJcfd7_InP0ICRvvMn8t5n4EUIU-E6nPquzQWDPrrPdL9G-yTLk0EDUHx1w45cm5OKQMq4ZB0OOMskpHqkqvBBoscg-HkMcCqbOqqcMHTe5VVbpnXeVGsFgHasrFlW2xcE2T20xbVcuGbx-RgZgpnT3Z3j0zvbl8G9-H4YTga3IxDFExCiMgVt1xJjhSlTEFwJkycpMakyiBkCUUlEkxUmggAKVEyE0cZIHCDsxh65Hz77rKuPlbWNXpererSR2olQMVRDNxDpztolS5sppd1vjD1Rv_-1QMXO8A4NMWsNiXm7p8DFUHs83vkest95YXd_M0Z1a17PdetYt0q1q17_eNer_VkMmorv3-23Z-ZSpu32mdMn3nrniXAqOTwDVivfwc</recordid><startdate>201102</startdate><enddate>201102</enddate><creator>Marden, Jeremiah N</creator><creator>Dong, Qian</creator><creator>Roychowdhury, Sugata</creator><creator>Berleman, James E</creator><creator>Bauer, Carl E</creator><general>Blackwell Publishing Ltd</general><general>Blackwell</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>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></search><sort><creationdate>201102</creationdate><title>Cyclic GMP controls Rhodospirillum centenum cyst development</title><author>Marden, Jeremiah N ; Dong, Qian ; Roychowdhury, Sugata ; Berleman, James E ; Bauer, Carl E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5163-cc282e2862c0c66b35215a79baab8ac3d90c859c98b953366c61a74d3c32acf73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Amino Acid Sequence</topic><topic>Bacteria</topic><topic>Bacteriology</topic><topic>Biochemistry</topic><topic>Biological and medical sciences</topic><topic>Chemical synthesis</topic><topic>Chromatography, High Pressure Liquid</topic><topic>Conserved Sequence - genetics</topic><topic>Cyclic AMP Receptor Protein - metabolism</topic><topic>Cyclic GMP - metabolism</topic><topic>Cysts</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Guanylate Cyclase - chemistry</topic><topic>Guanylate Cyclase - metabolism</topic><topic>Medical sciences</topic><topic>Microbiology</topic><topic>Miscellaneous</topic><topic>Models, Biological</topic><topic>Molecular biology</topic><topic>Molecular Sequence Data</topic><topic>Multigene Family - genetics</topic><topic>Mutation - genetics</topic><topic>Open Reading Frames - genetics</topic><topic>Protein Binding</topic><topic>Regulatory Sequences, Nucleic Acid - genetics</topic><topic>Rhodospirillum centenum - enzymology</topic><topic>Rhodospirillum centenum - genetics</topic><topic>Rhodospirillum centenum - growth & development</topic><topic>Rhodospirillum centenum - metabolism</topic><topic>Sequence Homology, Amino Acid</topic><topic>Signal Transduction</topic><topic>Soil Microbiology</topic><topic>Species Specificity</topic><topic>Spores, Bacterial - cytology</topic><topic>Spores, Bacterial - metabolism</topic><topic>Substrate Specificity</topic><topic>Suppression, Genetic</topic><topic>Transition Temperature</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Marden, Jeremiah N</creatorcontrib><creatorcontrib>Dong, Qian</creatorcontrib><creatorcontrib>Roychowdhury, Sugata</creatorcontrib><creatorcontrib>Berleman, James E</creatorcontrib><creatorcontrib>Bauer, Carl E</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>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><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Marden, Jeremiah N</au><au>Dong, Qian</au><au>Roychowdhury, Sugata</au><au>Berleman, James E</au><au>Bauer, Carl E</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cyclic GMP controls Rhodospirillum centenum cyst development</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2011-02</date><risdate>2011</risdate><volume>79</volume><issue>3</issue><spage>600</spage><epage>615</epage><pages>600-615</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Adenylyl cyclases are widely distributed across all kingdoms whereas guanylyl cyclases are generally thought to be restricted to eukaryotes. Here we report that the α-proteobacterium Rhodospirillum centenum secretes cGMP when developing cysts and that a guanylyl cyclase deletion strain fails to synthesize cGMP and is defective in cyst formation. The R. centenum cyclase was purified and shown to effectively synthesize cGMP from GTP in vitro, demonstrating that it is a functional guanylyl cyclase. A homologue of the Escherichia coli cAMP receptor protein (CRP) is linked to the guanylyl cyclase and when deleted is deficient in cyst development. Isothermal calorimetry (ITC) and differential scanning fluorimetry (DSF) analyses demonstrate that the recombinant CRP homologue preferentially binds to, and is stabilized by cGMP, but not cAMP. This study thus provides evidence that cGMP has a crucial role in regulating prokaryotic development. The involvement of cGMP in regulating bacterial development has broader implications as several plant-interacting bacteria contain a similar cyclase coupled by the observation that Azospirillum brasilense also synthesizes cGMP when inducing cysts.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>21214648</pmid><doi>10.1111/j.1365-2958.2010.07513.x</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Amino Acid Sequence Bacteria Bacteriology Biochemistry Biological and medical sciences Chemical synthesis Chromatography, High Pressure Liquid Conserved Sequence - genetics Cyclic AMP Receptor Protein - metabolism Cyclic GMP - metabolism Cysts Fundamental and applied biological sciences. Psychology Guanylate Cyclase - chemistry Guanylate Cyclase - metabolism Medical sciences Microbiology Miscellaneous Models, Biological Molecular biology Molecular Sequence Data Multigene Family - genetics Mutation - genetics Open Reading Frames - genetics Protein Binding Regulatory Sequences, Nucleic Acid - genetics Rhodospirillum centenum - enzymology Rhodospirillum centenum - genetics Rhodospirillum centenum - growth & development Rhodospirillum centenum - metabolism Sequence Homology, Amino Acid Signal Transduction Soil Microbiology Species Specificity Spores, Bacterial - cytology Spores, Bacterial - metabolism Substrate Specificity Suppression, Genetic Transition Temperature Tumors |
| title | Cyclic GMP controls Rhodospirillum centenum cyst development |
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