C-di-GMP: The dawning of a novel bacterial signalling system

Molecular Microbiology

Volumn 57, Issue 3, 2005, Pages 629-639

  Römling, Ute ^a   Gomelsky, Mark ^b   Galperin, Michael Y ^c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF WYOMING   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIS (3' 5') CYCLIC DIMERIC GUANOSINE MONOPHOSPHATE; GUANOSINE PHOSPHATE; UNCLASSIFIED DRUG;

BACTERIAL GENOME; BACTERIAL METABOLISM; CELL DIFFERENTIATION; CELL FUNCTION; GENOMICS; GLUCONACETOBACTER XYLINUS; HOST PATHOGEN INTERACTION; NONHUMAN; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; SHORT SURVEY; SIGNAL TRANSDUCTION;

BACTERIA; BACTERIAL PROTEINS; CYCLIC GMP; GENE EXPRESSION REGULATION, BACTERIAL; SECOND MESSENGER SYSTEMS;

BACTERIA (MICROORGANISMS); EUKARYOTA; GLUCONACETOBACTER XYLINUS;

EID: 22644438480     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04697.x     Document Type: Short Survey

References (69)

1. Aldridge, P., and Jenal, U. (1999) Cell cycle-dependent degradation of a flagellar motor component requires a novel-type response regulator. Mol Microbiol 32: 379-391.
2. Aldridge, P., Paul, R., Goymer, P., Rainey, P., and Jenal, U. (2003) Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus. Mol Microbiol 47: 1695-1708.
3. Altman, S., Bassler, B.L., Beckwith, J., Belfort, M., Berg, H.C., Bloom, B., et al. (2005) An open letter to Elias Zerhouni. Science 307: 1409-1410.
4. Amikam, D., Steinberger, O., Shkolnik, T., and Ben-Ishai, Z. (1995) The novel cyclic dinucleotide 3′-5′-cyclic diguanylic acid binds to p21 ras and enhances DNA synthesis but not cell replication in the Molt 4 cell line. Biochem J 311: 921-927.
5. Ausmees, N., Jonsson, H., Hoglund, S., Ljunggren, H., and Lindberg, M. (1999) Structural and putative regulatory genes involved in cellulose synthesis in Rhizobium leguminosarum bv. trifolii. Microbiology 145: 1253-1262.
6. Ausmees, N., Mayer, R., Weinhouse, H., Volman, G., Amikam, D., Benziman, M., et al. (2001) Genetic data indicate that proteins containing the GGDEF domain possess diguanylate cyclase activity. FEMS Microbiol Lett 204: 163-167.
7. Bae, S.O., Sugano, Y., Ohi, K., and Shoda, M. (2004) Features of bacterial cellulose synthesis in a mutant generated by disruption of the diguanylate cyclase 1 gene of Acetobacter xylinum BPR 2001. Appl Microbiol Biotechnol 65: 315-322.
8. Boles, B.R., and McCarter, L.L. (2002) Vibrio parahaemolyticus scrABC, a novel operon affecting swarming and capsular polysaccharide regulation. J Bacteriol 184: 5946-5954.
9. Bomchil, N., Watnick, P., and Kolter, R. (2003) Identification and characterization of a Vibrio cholerae gene, mbaA, involved in maintenance of biofilm architecture. J Bacteriol 185: 1384-1390.
10. Brown, N.L., Misra, T.K., Winnie, J.N., Schmidt, A., Seiff, M., and Silver, S. (1986) The nucleotide sequence of the mercuric resistance operons of plasmid R100 and transposon Tn501: further evidence for mer genes which enhance the activity of the mercuric ion detoxification system. Mol Gen Genet 202: 143-151.
11. Camilli, A., and Mekalanos, J.J. (1995) Use of recombinase gene fusions to identify Vibrio cholerae genes induced during infection. Mol Microbiol 18: 671-683.
12. Chae, K.S., and Yoo, O.J. (1986) Cloning of the lambda resistant genes from Brevibacterium albidum and Proteus vulgaris into Escherichia coli. Biochem Biophys Res Commun 140: 1101-1105.
13. Chan, C., Paul, R., Samoray, D., Amiot, N.C., Giese, B., Jenal, U., et al. (2004) Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci USA 101: 17084-17089.
14. Chang, A.L., Tuckerman, J.R., Gonzalez, G., Mayer, R., Weinhouse, H., Volman, G., et al. (2001) Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40: 3420-3426.
15. Crooks, G.E., Hon, G., Chandonia, J.M., and Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
16. D'Argenio, D.A., and Miller, S.I. (2004) Cyclic di-GMP as a bacterial second messenger. Microbiology 150: 2497-2502.
17. D'Argenio, D.A., Calfee, M.W., Rainey, P.B., and Pesci, E.G. (2002) Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J Bacteriol 184: 6481-6489.
18. Delgado-Nixon, V.M., Gonzalez, G., and Gilles-Gonzalez, M.A. (2000) Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. Biochemistry 39: 2685-2691.
19. Drenkard, E., and Ausubel, P.M. (2002) Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416: 740-743.
20. Galperin, M.Y. (2004) Bacterial signal transduction network in a genomic perspective. Environ Microbiol 6: 552-567.
21. Galperin, M.Y., Natale, D.A., Aravind, L., and Koonin, E.V. (1999) A specialized version of the HD hydrolase domain implicated in signal transduction. J Mol Microbiol Biotechnol 1: 303-305.
22. Galperin, M.Y., Nikolskaya, A.N., and Koonin, E.V. (2001) Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203: 11-21.
23. Garcia, B., Latasa, C., Solano, C., Portillo, F.G., Gamazo, C., and Lasa, I. (2004) Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol Microbiol 54: 264-277.
24. Gralla, J.D. (2005) Escherichia coli ribosomal RNA transcription: regulatory roles for ppGpp, NTPs, architectural proteins and a polymerase-binding protein. Mol Microbiol 55: 973-977.
25. Gronewold, T.M., and Kaiser, D. (2001) The act operon controls the level and time of C-signal production for Myxococcus xanthus development. Mol Microbiol 40: 744-756.
26. Hecht, G.B., and Newton, A. (1995) Identification of a novel response regulator required for the swarmer-to-stalked-cell transition in Caulobacter crescentus. J Bacteriol 177: 6223-6229.
27. Huber, B., Riedel, K., Kothe, M., Givskov, M., Molin, S., and Eberl, L. (2002) Genetic analysis of functions involved in the late stages of biofilm development in Burkholderia cepacia H111. Mol Microbiol 46: 411-426.
28. Hurley, J.H. (2003) GAF domains: cyclic nucleotides come full circle. Sci STKE 2003: PE1.
29. Ismail, T.M., Hart, C.A., and McLennan, A.G. (2003) Regulation of dinucleoside polyphosphate pools by the YgdP and ApaH hydrolases is essential for the ability of Salmonella enterica serovar typhimurium to invade cultured mammalian cells. J Biol Chem 278: 32602-32607.
30. 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.
31. Johnson, M.R., Montera, C.I., Conners, S.B., Shockley, K.R., Bridger, S.L., and Kelly, R.M. (2005) Population density-dependent regulation of exopolysaccharide formation in the hyperthermophilic bacterium Thermotoga maritima. Mol Microbiol 55: 664-674.
32. 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.
33. Karaolis, D.K., Rashid, M.H., Chythanya, R., Luo, W., Hyodo, M., and Hayakawa, Y. (2005a) c-di-GMP (3′-5′-cyclic diguanylic acid) inhibits Staphylococcus aureus cell-cell interactions and biofilm formation. Antimicrob Agents Chemother 49: 1029-1038.
34. Karaolis, D.K., Cheng, K., Lipsky, M., Elnabawi, A., Catalano, J., Hyodo, M., et al. (2005b) 3′,5′-Cyclic diguanylic acid (c-di-GMP) inhibits basal and growth factor-stimulated human colon cancer cell proliferation. Biochem Biophys Res Commun 329: 40-45.
35. Kearns, D.B., Chu, F., Branda, S.S., Kolter, R., and Losick, R. (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol 55: 739-749.
36. Kim, Y.R., Lee, S.E., Kim, C.M., Kim, S.Y., Shin, E.K., Shin, D.H., et al. (2003) Characterization and pathogenic significance of Vibrio vulnificus antigens preferentially expressed in septicemic patients. Infect Immun 71: 5461-5471.
37. Kirillina, O., Fetherston, J.D., Bobrov, A.G., Abney, J., and Perry, R.D. (2004) HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis. Mol Microbiol 54: 75-88.
38. Klausen, M., Aaes-Jorgensen, A., Molin, S., and Tolker-Nielsen, T. (2003) Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol 50: 61-68.
39. Ko, M., and Park, C. (2000) Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli. J Mol Biol 303: 371-382.
40. Kulasekara, H.D., Ventre, I., Kulasekara, B.R., Lazdunski, A., Filloux, A., and Lory, S. (2005) A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol Microbid 55: 368-380.
41. Lee, S.H., Butler, S.M., and Camilli, A. (2001) Selection for in vivo regulators of bacterial virulence. Proc Natl Acad Sci USA 98: 6889-6894.
42. Mayer, R., Ross, P., Weinhouse, H., Amikam, D., Volman, G., Ohana, P., et al. (1991) Polypeptide composition of bacterial cyclic diguanylic acid-dependent cellulose synthase and the occurrence of immunologically crossreacting proteins in higher plants. Proc Natl Acad Sci USA 88: 5472-5476.
43. Merket, T.J., and Stibitz, S. (1995) Identification of a locus required for the regulation of bvg-repressed genes in Bordetella pertussis. J Bacteriol 177: 2727-2736.
44. Merkel, T.J., Stibitz, S., Keith, J.M., Leef, M., and Shahin, R. (1998a) Contribution of regulation by the bvg locus to respiratory infection of mice by Bordetella pertussis. Infect Immun 66: 4367-4373.
45. Merkel, T.J., Barros, C., and Stibitz, S. (1998b) Characterization of the bvgR locus of Bordetella pertussis. J Bacteriol 180: 1682-1690.
46. Milton, D.L., Norqvist, A., and Wolf-Watz, H. (1995) Sequence of a novel virulence-mediating gene, virC, from Vibrio anguillarum. Gene 164: 95-100.
47. Nikolskaya, A.N., Mulkidjanian, A.Y., Beech, I.B., and Galperin, M.Y. (2003) MASE1 and MASE2: two novel integral membrane sensory domains. J Mol Microbiol Biotechnol 5: 11-16.
48. Paul, R., Weiser, S., Amiot, N.C., Chan, C., Schirmer, T., Giese, B., et al. (2004) Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18: 715-727.
49. Pei, J., and Grishin, N.V. (2001) GGDEF domain is homologous to adenylyl cyclase. Proteins 42: 210-216.
50. Perry, R.D., Bobrov, A.G., Kirillina, O., Jones, H.A., Pedersen, L., Abney, J., et al. (2004) Temperature regulation of the hemin storage (Hms+) phenotype of Yersinia pestis is posttranscriptional. J Bacteriol 186: 1638-1647.
51. Rashid, M.H., Rajanna, C., Ali, A., and Karaolis, O.K. (2003) Identification of genes involved in the switch between the smooth and rugose phenotypes of Vibrio cholerae. FEMS Microbiol Lett 227: 113-119.
52. Römling, U. (2005) Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. CLMS 62: 1-13.
53. Römling, U., Bian, Z., Hammar, M., Sierralta, W.D., and Normark, S. (1998) Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180: 722-731.
54. Römling, U., Rohde, M., Olsen, A., Normark, S., and Reinköster, J. (2000) AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36: 10-23.
55. Ross, P., Weinhouse, H., Aloni, Y., Michaeli, D., Weinberger-Ohana, P., Mayer, R., et al. (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325: 279-281.
56. Rychlik, I., Martin, G., Methner, U., Lovell, M., Cardova, L., Sebkova, A., et al. (2002) Identification of Salmonella enterica serovar Typhimurium genes associated with growth suppression in stationary-phase nutrient broth cultures and in the chicken intestine. Arch Microbiol 178: 411-420.
57. Ryjenkov, D.A., Tarutina, M., Moskvin, O.M., and 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.
58. Sasakura, Y., Hirata, S., Sugiyama, S., Suzuki, S., Taguchi, S., Watanabe, M., et al. (2002) Characterization of a direct oxygen sensor heme protein from Escherichia coli. Effects of the heme redox states and mutations at the heme-binding site on catalysis and structure. J Biol Chem 277: 23821-23827.
59. Schmidt, A.J., Ryjenkov, D.A., and Gomelsky, M. (2005) Ubiquitous protein domain EAL encodes cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol (in press).
60. Simm, R., Morr, M., Kader, A., Nimtz, M., and Römling, U. (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53: 1123-1134.
61. Spiers, A.J., Kahn, S.G., Bohannon, J., Travisano, M., and Rainey, P.B. (2002) Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 161: 33-46.
62. Steinberger, O., Lapidot, Z., Ben-Ishai, Z., and Amikam, D. (1999) Elevated expression of the CD4 receptor and cell cycle arrest are induced in Jurkat cells by treatment with the novel cyclic dinucleotide 3′,5′-cyclic diguanylic acid. FEBS Lett 444: 125-129.
63. Tal, R., Wong, H.C., Calhoon, R., Gelfand, D., Fear, A.L., Volman, G., et al. (1998) Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 180: 4416-4425.
64. Taylor, B.L., and Zhulin, I.B. (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63: 479-506.
65. Thomas, C., Andersson, C.R., Canales, S.R., and Golden, S.S. (2004) PsfR, a factor that stimulates psbAI expression in the cyanobacterium Synechococcus elongatus PCC 7942. Microbiology 150: 1031-1040.
66. Tischler, A.D., and Camilli, A. (2004) Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53: 857-869.
67. Weinhouse, H., Sapir, S., Amikam, D., Shilo, Y., Volman, G., Ghana, P., et al. (1997) c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett 416: 207-211.
68. Zhulin, I.B., Nikolskaya, A.N., and Galperin, M.Y. (2003) Common extracellular sensory domains in transmembrane receptors for diverse signal transduction pathways in bacteria and archaea. J Bacteriol 185: 285-294.
69. Zogaj, X., Nimtz, M., Rohde, M., Bokranz, W., and Römling, U. (2001) The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39: 1452-1463.