Cyclic-diGMP signal transduction systems in Vibrio cholerae: Modulation of rugosity and biofilm formation

Molecular Microbiology

Volumn 60, Issue 2, 2006, Pages 331-348

  Lim, Bentley ^a   Beyhan, Sinem ^a   Meir, James ^a   Yildiz, Fitnat H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC DIGMP; DIGUANYLATE CYCLASE; EXOPOLYSACCHARIDE; GUANOSINE DERIVATIVE; LYASE; PHOSPHODIESTERASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIUM COLONY; BACTERIUM MUTANT; BIOFILM; CARBOHYDRATE SYNTHESIS; CELL LEVEL; CELL MOTILITY; CELL SURFACE; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC EPISTASIS; MORPHOLOGICAL TRAIT; NONHUMAN; NULL ALLELE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SECOND MESSENGER; SIGNAL TRANSDUCTION; SURFACE PROPERTY; VIBRIO CHOLERAE;

BACTERIAL PROTEINS; BIOFILMS; CELL MOVEMENT; CYCLIC GMP; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MUTATION; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS); VIBRIO CHOLERAE;

EID: 33645296297     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05106.x     Document Type: Article

References (60)

1. Ali A. Morris J.G. Jr and Johnson J.A. 2005 Sugars inhibit expression of the rugose phenotype of Vibrio cholerae. J Clin Microbiol 43 1426 1429.
2. Aravind L. Ponting C.P. 1997 The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 22 458 459.
3. Aravind L. Ponting C.P. 1999 The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol Lett 176 111 116.
4. Bao Y. Lies D.P. Fu H. Roberts G.P. 1991 An improved Tn7-based system for the single-copy insertion of cloned genes into chromosomes of gram-negative bacteria. Gene 109 167 168.
5. Bochner B.R. Ames B.N. 1982 Complete analysis of cellular nucleotides by two-dimensional thin layer chromatography. J Biol Chem 257 9759 9769.
6. Boles B.R. McCarter L.L. 2002 Vibrio parahaemolyticus scrABC, a novel operon affecting swarming and capsular polysaccharide regulation. J Bacteriol 184 5946 5954.
7. Bomchil N. Watnick P. Kolter R. 2003 Identification and characterization of a Vibrio cholerae gene, mbaA, involved in maintenance of biofilm architecture. J Bacteriol 185 1384 1390.
8. Casper-Lindley C. Yildiz F.H. 2004 VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J Bacteriol 186 1574 1578.
9. Choy W.K. Zhou L. Syn C.K. Zhang L.H. Swarup S. 2004 MorA defines a new class of regulators affecting flagellar development and biofilm formation in diverse Pseudomonas species. J Bacteriol 186 7221 7228.
10. Christen M. Christen B. Folcher M. Schauerte A. Jenal U. 2005 Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J Biol Chem 280 30829 30837.
11. D'Argenio D.A. Miller S.I. 2004 Cyclic di-GMP as a bacterial second messenger. Microbiology 150 2497 2502.
12. D'Argenio D.A. Calfee M.W. Rainey P.B. Pesci E.C. 2002 Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J Bacteriol 184 6481 6489.
13. Drenkard E. Ausubel F.M. 2002 Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416 740 743.
14. Faruque S.M. Albert M.J. Mekalanos J.J. 1998 Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev 62 1301 1314.
15. Fullner K.J. Mekalanos J.J. 1999 Genetic characterization of a new type IV-A pilus gene cluster found in both classical and El Tor biotypes of Vibrio cholerae. Infect Immun 67 1393 1404.
16. Galperin M.Y. 2004 Bacterial signal transduction network in a genomic perspective. Environ Microbiol 6 552 567.
17. Galperin M.Y. Nikolskaya A.N. Koonin E.V. 2001 Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203 11 21.
18. Garcia B. Latasa C. Solano C. Garcia-del Portillo F. Gamazo C. Lasa I. 2004 Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol Microbiol 54 264 277.
19. Gilles-Gonzalez M.A. Gonzalez G. 2004 Signal transduction by heme-containing PAS-domain proteins. J Appl Physiol 96 774 783.
20. Gronewold T.M. Kaiser D. 2001 The act operon controls the level and time of C-signal production for Myxococcus xanthus development. Mol Microbiol 40 744 756.
21. Guvener Z.T. McCarter L.L. 2003 Multiple regulators control capsular polysaccharide production in Vibrio parahaemolyticus. J Bacteriol 185 5431 5441.
22. Guzman L.M. Belin D. Carson M.J. Beckwith J. 1995 Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177 4121 4130.
23. Hammer B.K. Bassler B.L. 2003 Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50 101 104.
24. Haugo A.J. Watnick P.I. 2002 Vibrio cholerae CytR is a repressor of biofilm development. Mol Microbiol 45 471 483.
25. Herrero M. de Lorenzo V. Timmis K.N. 1990 Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172 6557 6567.
26. Hickman J.W. Tifrea D.F. Harwood C.S. 2005 A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA 102 14422 14427.
27. Horton R.M. Ho S.N. Pullen J.K. Hunt H.D. Cai Z. Pease L.R. 1993 Gene splicing by overlap extension. Methods Enzymol 217 270 279.
28. Islam M. Drasar B. Sack R. 1993 The aquatic environment as a reservoir of Vibrio-cholerae - a review. J Diarrhoeal Dis Res 11 197 206.
29. Jenal U. 2004 Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr Opin Microbiol 7 185 191.
30. Jones H.A. Lillard J.W. Jr and Perry R.D. 1999 HmsT, a protein essential for expression of the haemin storage (Hms+) phenotype of Yersinia pestis. Microbiology 145 2117 2128.
31. Karatan E. Duncan T.R. Watnick P.I. 2005 NspS, a predicted polyamine pensor, mediates activation of Vibrio cholerae biofilm formation by norspermidine. J Bacteriol 187 7434 7443.
32. Kovacikova G. Lin W. Skorupski K. 2005 Dual regulation of genes involved in acetoin biosynthesis and motility/biofilm formation by the virulence activator AphA and the acetate-responsive LysR-type regulator AlsR in Vibrio cholerae. Mol Microbiol 57 420 433.
33. Lefebvre B. Formstecher P. Lefebvre P. 1995 Improvement of the gene splicing overlap (SOE) method. Biotechniques 19 186 188.
34. Lipp E.K. Huq A. Colwell R.R. 2002 Effects of global climate on infectious disease: the cholera model. Clin Microbiol Rev 15 757 770.
35. de Lorenzo V. Timmis K.N. 1994 Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol 235 386 405.
36. Meibom K.L. Li X.B. Nielsen A.T. Wu C.Y. Roseman S. Schoolnik G.K. 2004 The Vibrio cholerae chitin utilization program. Proc Natl Acad Sci USA 101 2524 2529.
37. Merrell D.S. Butler S.M. Qadri F. Dolganov N.A. Alam A. Cohen M.B. et al. 2002 Host-induced epidemic spread of the cholera bacterium. Nature 417 642 645.
38. Miller J.H. 1972 Assay of β-Galactosidase. Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press.
39. Morris J.G. Jr Sztein M.B. Rice E.W. Nataro J.P. Losonsky G.A. Panigrahi P. et al. 1996 Vibrio cholerae O1 can assume a chlorine-resistant rugose survival form that is virulent for humans. J Infect Dis 174 1364 1368.
40. Paul R. Weiser S. Amiot N.C. Chan C. Schirmer T. Giese B. Jenal U. 2004 Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18 715 727.
41. Rashid M.H. Rajanna C. Ali A. Karaolis D.K. 2003 Identification of genes involved in the switch between the smooth and rugose phenotypes of Vibrio cholerae. FEMS Microbiol Lett 227 113 119.
42. Rice E.W. Johnson C.J. Clark R.M. Fox K.R. Reasoner D.J. Dunnigan M.E. et al. 1992 Chlorine and survival of 'rugose'Vibrio cholerae. Lancet 340 740.
43. Romling U. Rohde M. Olsen A. Normark S. Reinkoster J. 2000 AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36 10 23.
44. Romling U. Gomelsky M. Galperin M.Y. 2005 C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57 629 639.
45. Ross P. Aloni Y. Weinhouse H. Michaeli D. Weinbergerohana P. Mayer R. Benziman M. 1986 Control of cellulose synthesis in Acetobacter-xylinum - a unique guanyl oligonucleotide is the immediate activator of the cellulose synthase. Carbohydr Res 149 101 117.
46. Ryjenkov D.A. Tarutina M. Moskvin O.V. Gomelsky M. 2005 Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J Bacteriol 187 1792 1798.
47. Sardiwal S. Kendall S.L. Movahedzadeh F. Rison S.C. Stoker N.G. Djordjevic S. 2005 A GAF domain in the hypoxia/NO-inducible Mycobacterium tuberculosis DosS protein binds haem. J Mol Biol 353 929 936.
48. Schmidt A.J. Ryjenkov D.A. Gomelsky M. 2005 The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol 187 4774 4781.
49. Simm R. Morr M. Kader A. Nimtz M. Romling U. 2004 GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53 1123 1134.
50. Spiers A.J. Bohannon J. Gehrig S.M. Rainey P.B. 2003 Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 50 15 27.
51. Tamayo R. Tischler A.D. Camilli A. 2005 The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J Biol Chem 280 33324 33330.
52. Tischler A.D. Camilli A. 2004 Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53 857 869.
53. Tischler A.D. Camilli A. 2005 Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun 73 5873 5882.
54. Tischler A.D. Lee S.H. Camilli A. 2002 The Vibrio cholerae vieSAB locus encodes a pathway contributing to cholera toxin production. J Bacteriol 184 4104 4113.
55. Wai S.N. Mizunoe Y. Takade A. Kawabata S.I. Yoshida S.I. 1998 Vibrio cholerae O1 strain TSI-4 produces the exopolysaccharide materials that determine colony morphology, stress resistance, and biofilm formation. Appl Environ Microbiol 64 3648 3655.
56. White P.B. 1938 The rugose variant of Vibrios. J Pathol 46 1 6.
57. Yildiz F.H. Schoolnik G.K. 1999 Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci USA 96 4028 4033.
58. Yildiz F.H. Liu X.S. Heydorn A. Schoolnik G.K. 2004 Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol Microbiol 53 497 515.
59. Zhang Z. Gaffney B.L. Jones R.A. 2004 c-di-GMP displays a monovalent metal ion-dependent polymorphism. J Am Chem Soc 126 16700 16701.
60. Zhu J. Mekalanos J.J. 2003 Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5 647 656.