Nitric Oxide Modulates Bacterial Biofilm Formation through a Multicomponent Cyclic-di-GMP Signaling Network

Molecular Cell

Volumn 46, Issue 4, 2012, Pages 449-460

  Plate, Lars ^a   Marletta, Michael A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC DIGUANOSINE MONOPHOSPHATE; CYCLIC GMP; NITRIC OXIDE; PHOSPHODIESTERASE; PHOSPHOTRANSFERASE; PROTEIN HISTIDINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; BIOFILM; CELL ADHESION; ENZYME ACTIVITY; FEEDBACK SYSTEM; GAMMAPROTEOBACTERIA; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; OPERON; PHENOTYPE; PROTECTION; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; SHEWANELLA ONEIDENSIS; SIGNAL TRANSDUCTION; THERMOTOGA MARITIMA; ULTRAVIOLET SPECTROSCOPY;

3',5'-CYCLIC-GMP PHOSPHODIESTERASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BIOFILMS; CYCLIC GMP; GAMMAPROTEOBACTERIA; GUANYLATE CYCLASE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SECOND MESSENGER SYSTEMS; SEQUENCE HOMOLOGY, AMINO ACID; SHEWANELLA; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); SHEWANELLA ONEIDENSIS; VERTEBRATA;

EID: 84861456040     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.03.023     Document Type: Article

References (57)

1. Barends T.R.M., Hartmann E., Griese J.J., Beitlich T., Kirienko N.V., Ryjenkov D.A., Reinstein J., Shoeman R.L., Gomelsky M., Schlichting I. Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 2009, 459:1015-1018.
2. Beyhan S., Tischler A.D., Camilli A., Yildiz F.H. Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level. J. Bacteriol. 2006, 188:3600-3613.
3. Boehm A., Kaiser M., Li H., Spangler C., Kasper C.A., Ackermann M., Kaever V., Sourjik V., Roth V., Jenal U. Second messenger-mediated adjustment of bacterial swimming velocity. Cell 2010, 141:107-116.
4. Boon E.M., Davis J.H., Tran R., Karow D.S., Huang S.H., Pan D., Miazgowicz M.M., Mathies R.A., Marletta M.A. Nitric oxide binding to prokaryotic homologs of the soluble guanylate cyclase beta1 H-NOX domain. J. Biol. Chem. 2006, 281:21892-21902.
5. Borziak K., Zhulin I.B. FIST: a sensory domain for diverse signal transduction pathways in prokaryotes and ubiquitin signaling in eukaryotes. Bioinformatics 2007, 23:2518-2521.
6. Brons H.J., Hagen W.R., Zehnder A.J. Ferrous iron dependent nitric oxide production in nitrate reducing cultures of Escherichia coli. Arch. Microbiol. 1991, 155:341-347.
7. Carlson H.K., Vance R.E., Marletta M.A. H-NOX regulation of c-di-GMP metabolism and biofilm formation in Legionella pneumophila. Mol. Microbiol. 2010, 77:930-942.
8. Christen M., Christen B., Folcher M., Schauerte A., Jenal U. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 2005, 280:30829-30837.
9. Davies K.M., Lowe E.D., Vénien-Bryan C., Johnson L.N. The HupR receiver domain crystal structure in its nonphospho and inhibitory phospho states. J. Mol. Biol. 2009, 385:51-64.
10. Davies B.W., Bogard R.W., Dupes N.M., Gerstenfeld T.A.I., Simmons L.A., Mekalanos J.J. DNA damage and reactive nitrogen species are barriers to Vibrio cholerae colonization of the infant mouse intestine. PLoS Pathog. 2011, 7:e1001295.
11. Derbyshire E.R., Marletta M.A. Biochemistry of soluble guanylate cyclase. Handbook of Experimental Pharmacology 2009, 17-31. Springer, Berlin. H.H.H.W. Schmidt, F. Hofmann, J.-P. Stasch (Eds.).
12. Donlan R.M., Costerton J.W. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 2002, 15:167-193.
13. Duncan C., Dougall H., Johnston P., Green S., Brogan R., Leifert C., Smith L., Golden M., Benjamin N. Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate. Nat. Med. 1995, 1:546-551.
14. Faruque S.M., Biswas K., Udden S.M.N., Ahmad Q.S., Sack D.A., Nair G.B., Mekalanos J.J. Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc. Natl. Acad. Sci. USA 2006, 103:6350-6355.
15. Galperin M.Y. Diversity of structure and function of response regulator output domains. Curr. Opin. Microbiol. 2010, 13:150-159.
16. Galperin M.Y., Natale D.A., Aravind L., Koonin E.V. A specialized version of the HD hydrolase domain implicated in signal transduction. J. Mol. Microbiol. Biotechnol. 1999, 1:303-305.
17. Gao R., Stock A.M. Molecular strategies for phosphorylation-mediated regulation of response regulator activity. Curr. Opin. Microbiol. 2010, 13:160-167.
18. Hammer B.K., Bassler B.L. Distinct sensory pathways in Vibrio cholerae El Tor and classical biotypes modulate cyclic dimeric GMP levels to control biofilm formation. J. Bacteriol. 2009, 191:169-177.
19. Hengge R. Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol. 2009, 7:263-273.
20. Iyer L.M., Anantharaman V., Aravind L. Ancient conserved domains shared by animal soluble guanylyl cyclases and bacterial signaling proteins. BMC Genomics 2003, 4:5.
21. Jenal U., Malone J. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet. 2006, 40:385-407.
22. Karow D.S., Pan D., Tran R., Pellicena P., Presley A., Mathies R.A., Marletta M.A. Spectroscopic characterization of the soluble guanylate cyclase-like heme domains from Vibrio cholerae and Thermoanaerobacter tengcongensis. Biochemistry 2004, 43:10203-10211.
23. Krasteva P.V., Fong J.C.N., Shikuma N.J., Beyhan S., Navarro M.V.A.S., Yildiz F.H., Sondermann H. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 2010, 327:866-868.
24. Lassak J., Henche A.-L., Binnenkade L., Thormann K.M. ArcS, the cognate sensor kinase in an atypical Arc system of Shewanella oneidensis MR-1. Appl. Environ. Microbiol. 2010, 76:3263-3274.
25. Laub M.T., Goulian M. Specificity in two-component signal transduction pathways. Annu. Rev. Genet. 2007, 41:121-145.
26. Laub M.T., Biondi E.G., Skerker J.M. Phosphotransfer profiling: systematic mapping of two-component signal transduction pathways and phosphorelays. Methods Enzymol. 2007, 423:531-548.
27. Lauriano C.M., Ghosh C., Correa N.E., Klose K.E. The sodium-driven flagellar motor controls exopolysaccharide expression in Vibrio cholerae. J. Bacteriol. 2004, 186:4864-4874.
28. Lee S.Y., Cho H.S., Pelton J.G., Yan D., Henderson R.K., King D.S., Huang L., Kustu S., Berry E.A., Wemmer D.E. Crystal structure of an activated response regulator bound to its target. Nat. Struct. Biol. 2001, 8:52-56.
29. Liu N., Xu Y., Hossain S., Huang N., Coursolle D., Gralnick J.A., Boon E.M. Nitric oxide regulation of cyclic di-GMP synthesis and hydrolysis in Shewanella woodyi. Biochemistry 2012, 51:2087-2099.
30. Lovering A.L., Capeness M.J., Lambert C., Hobley L., Sockett R.E. The structure of an unconventional HD-GYP protein from Bdellovibrio reveals the roles of conserved residues in this class of cyclic-di-GMP phosphodiesterases. MBio. 2011, 2. e00163-11.
31. MacMicking J., Xie Q.W., Nathan C. Nitric oxide and macrophage function. Annu. Rev. Immunol. 1997, 15:323-350.
32. Mangan S., Alon U. Structure and function of the feed-forward loop network motif. Proc. Natl. Acad. Sci. USA 2003, 100:11980-11985.
33. Mikkelsen H., Sivaneson M., Filloux A. Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. Environ. Microbiol. 2011, 13:1666-1681.
34. Mitrophanov A.Y., Groisman E.A. Signal integration in bacterial two-component regulatory systems. Genes Dev. 2008, 22:2601-2611.
35. Myers C.R., Nealson K.H. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 1988, 240:1319-1321.
36. Navarro M.V.A.S., De N., Bae N., Wang Q., Sondermann H. Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure 2009, 17:1104-1116.
37. Ng W.-L., Bassler B.L. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 2009, 43:197-222.
38. Paul R., Jaeger T., Abel S., Wiederkehr I., Folcher M., Biondi E.G., Laub M.T., Jenal U. Allosteric regulation of histidine kinases by their cognate response regulator determines cell fate. Cell 2008, 133:452-461.
39. Poole R.K. Nitric oxide and nitrosative stress tolerance in bacteria. Biochem. Soc. Trans. 2005, 33:176-180.
40. Price M.S., Chao L.Y., Marletta M.A. Shewanella oneidensis MR-1 H-NOX regulation of a histidine kinase by nitric oxide. Biochemistry 2007, 46:13677-13683.
41. Ryan R.P., Fouhy Y., Lucey J.F., Dow J.M. Cyclic di-GMP signaling in bacteria: recent advances and new puzzles. J. Bacteriol. 2006, 188:8327-8334.
42. Ryan R.P., Lucey J., O'Donovan K., McCarthy Y., Yang L., Tolker-Nielsen T., Dow J.M. HD-GYP domain proteins regulate biofilm formation and virulence in Pseudomonas aeruginosa. Environ. Microbiol. 2009, 11:1126-1136.
43. Ryan R.P., McCarthy Y., Andrade M., Farah C.S., Armitage J.P., Dow J.M. Cell-cell signal-dependent dynamic interactions between HD-GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris. Proc. Natl. Acad. Sci. USA 2010, 107:5989-5994.
44. Schirmer T., Jenal U. Structural and mechanistic determinants of c-di-GMP signalling. Nat. Rev. Microbiol. 2009, 7:724-735.
45. Sivaneson M., Mikkelsen H., Ventre I., Bordi C., Filloux A. Two-component regulatory systems in Pseudomonas aeruginosa: an intricate network mediating fimbrial and efflux pump gene expression. Mol. Microbiol. 2011, 79:1353-1366.
46. Skerker J.M., Prasol M.S., Perchuk B.S., Biondi E.G., Laub M.T. Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol. 2005, 3:e334.
47. Skerker J.M., Perchuk B.S., Siryaporn A., Lubin E.A., Ashenberg O., Goulian M., Laub M.T. Rewiring the specificity of two-component signal transduction systems. Cell 2008, 133:1043-1054.
48. Spiro S. Regulators of bacterial responses to nitric oxide. FEMS Microbiol. Rev. 2007, 31:193-211.
49. Stock A.M., Robinson V.L., Goudreau P.N. Two-component signal transduction. Annu. Rev. Biochem. 2000, 69:183-215.
50. Tamayo R., Tischler A.D., Camilli A. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 2005, 280:33324-33330.
51. Thormann K.M., Saville R.M., Shukla S., Pelletier D.A., Spormann A.M. Initial Phases of biofilm formation in Shewanella oneidensis MR-1. J. Bacteriol. 2004, 186:8096-8104.
52. Thormann K.M., Duttler S., Saville R.M., Hyodo M., Shukla S., Hayakawa Y., Spormann A.M. Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J. Bacteriol. 2006, 188:2681-2691.
53. Wang Y., Dufour Y.S., Carlson H.K., Donohue T.J., Marletta M.A., Ruby E.G. H-NOX-mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri. Proc. Natl. Acad. Sci. USA 2010, 107:8375-8380.
54. Waters C.M., Lu W., Rabinowitz J.D., Bassler B.L. Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J. Bacteriol. 2008, 190:2527-2536.
55. Wolf Y.I., Rogozin I.B., Kondrashov A.S., Koonin E.V. Genome alignment, evolution of prokaryotic genome organization, and prediction of gene function using genomic context. Genome Res. 2001, 11:356-372.
56. Yan D., Cho H.S., Hastings C.A., Igo M.M., Lee S.Y., Pelton J.G., Stewart V., Wemmer D.E., Kustu S. Beryllofluoride mimics phosphorylation of NtrC and other bacterial response regulators. Proc. Natl. Acad. Sci. USA 1999, 96:14789-14794.
57. Zhu J., Mekalanos J.J. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell 2003, 5:647-656.