Comparative genomics of cyclic-di-GMP signalling in bacteria: Post-translational regulation and catalytic activity

Nucleic Acids Research

Volumn 38, Issue 18, 2010, Pages 5970-5981

  Seshasayee, Aswin S N ^a   Fraser, Gillian M ^b   Luscombe, Nicholas M ^a,c  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC DIMERIC GUANOSINE PHOSPHATE; CYCLIC NUCLEOTIDE; HYBRID PROTEIN; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; BACTERIAL PROTEIN; BIS(3',5') CYCLIC DIGUANYLIC ACID; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CYCLIC GMP; DIGUANYLATE CYCLASE; DRUG DERIVATIVE; LYASE; MEMBRANE PROTEIN; PHOSPHODIESTERASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENETICS; BIOCHEMISTRY; CELL SURFACE; COMPUTER PROGRAM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GENETIC CONSERVATION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; ARCHAEAL GENOME; BACTERIAL GENOME; BACTERIUM; BIOCATALYSIS; CHEMISTRY; COMPARATIVE STUDY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; SECOND MESSENGER;

BACTERIA (MICROORGANISMS); PROKARYOTA;

ARCHAEAL PROTEINS; BACTERIA; BACTERIAL PROTEINS; BIOCATALYSIS; CATALYTIC DOMAIN; CYCLIC GMP; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, ARCHAEAL; GENOME, BACTERIAL; GENOMICS; MEMBRANE PROTEINS; PHOSPHORIC DIESTER HYDROLASES; PHOSPHORUS-OXYGEN LYASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; SECOND MESSENGER SYSTEMS;

EID: 78049426911     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq382     Document Type: Article

References (62)

1. Pesavento, C. and Hengge, R. (2009) Bacterial nucleotide-based second messengers. Curr. Opin. Microbiol., 12, 170-176.
2. Amikam, D. and Benziman, M. (1989) Cyclic diguanylic acid and cellulose synthesis in Agrobacterium tumefaciens. J. Bacteriol., 171, 6649-6655.
3. Tal, R., Wong, H.C., Calhoon, R., Gelfand, D., Fear, A.L., Volman, G., Mayer, R., Ross, P., Amikam, D., Weinhouse, H. 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.
4. Jenal, U. and Malone, J. (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet., 40, 385-407.
5. Hengge, R. (2009) Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol., 7, 263-273.
6. Tamayo, R., Pratt, J.T. and Camilli, A. (2007) Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu. Rev. Microbiol., 61, 131-148.
7. Kumar, M. and Chatterji, D. (2008) Cyclic di-GMP: a second messenger required for long-term survival, but not for biofilm formation, in Mycobacterium smegmatis. Microbiology, 154, 2942-2955.
8. Ryan, R.P., Fouhy, Y., Lucey, J.F. and Dow, J.M. (2006) Cyclic di-GMP signaling in bacteria: recent advances and new puzzles. J. Bacteriol., 188, 8327-8334.
9. Ferreira, R.B., Antunes, L.C., Greenberg, E.P. and McCarter, L.L. (2008) Vibrio parahaemolyticus ScrC modulates cyclic dimeric GMP regulation of gene expression relevant to growth on surfaces. J. Bacteriol., 190, 851-860.
10. Tarutina, M., Ryjenkov, D.A. and Gomelsky, M. (2006) An unorthodox bacteriophytochrome from Rhodobacter sphaeroides involved in turnover of the second messenger c-di-GMP. J. Biol. Chem., 281, 34751-34758.
11. 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.
12. Sommerfeldt, N., Possling, A., Becker, G., Pesavento, C., Tschowri, N. and Hengge, R. (2009) Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology, 155, 1318-1331.
13. 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, 1695-708.
14. Paul, R., Weiser, S., Amiot, N.C., Chan, C., Schirmer, T., Giese, B. and 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.
15. Kanehisa, M., Goto, S., Furumichi, M., Tanabe, M. and Hirakawa, M. (2010) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res., 38, D355-D360.
16. Finn, R.D., Tate, J., Mistry, J., Coggill, P.C., Sammut, S.J., Hotz, H.R., Ceric, G., Forslund, K., Eddy, S.R., Sonnhammer, E.L.L. et al. (2008) The Pfam protein families database. Nucleic Acids Res., 36, D281-D288.
17. Moreno-Hagelsieb, G. and Collado-Vides, J. (2002) A powerful non-homology method for the prediction of operons in prokaryotes. Bioinformatics, 18, S329-S336.
18. Aravind, L. and Koonin, E.V. (1998) The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem. Sci., 23, 469-472.
19. 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.
20. Marchler-Bauer, A. and Bryant, S.H. (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res., 32(W), 327-331.
21. Krogh, A., Larsson, B., von Heijne, G. and Sonnhammer, E.L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol., 305, 567-580.
22. Bendtsen, J.D., Nielsen, H., von Heijne, G. and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol., 340, 783-795.
23. Juncker, A.S., Willenbrock, H., Heijne, G.V., Brunak, S., Nielsen, H. and Krogh, A. (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci., 12, 1652-1662.
24. Bendtsen, J.D., Nielsen, H., Widdick, D., Palmer, T. and Brunak, S. (2005) Prediction of twin-arginine signal peptides. BMC Bioinformatics, 6, 167.
25. Emanuelsson, O., Brunak, S., von Heijne, G. and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protocol., 2, 953-971.
26. Needleman, S.B. and Wunsch, C.D. (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol., 48, 443-453.
27. Henikoff, J.G. (1992) Amino acid substitution matrices from protein blocks. Proc. Natl Acad. Sci. USA, 89, 10915-10919.
28. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797.
29. Malone, J.G., Williams, R., Christen, M., Jenal, U., Spiers, A.J. and Rainey, P.B. (2007) The structure-function relationship of WspR, a Pseudomonas fluorescens response regulator with a GGDEF output domain. Microbiology, 153, 980-994.
30. Christen, B., Christen, M., Paul, R., Schmid, F., Folcher, M., Jenoe, P., Meuwly, M. and Jenal, U. (2006) Allosteric control of cyclic di-GMP signaling. J. Biol. Chem., 281, 32015-32024.
31. Rao, F., Yang, Y., Qi, Y. and Liang, Z.X. (2008) Catalytic mechanism of cyclic di-GMP-specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J. Bacteriol., 190, 3622-3631.
32. Weber, H., Pesavento, C., Possling, A., Tischendorf, G. and Hengge, R. (2006) Cyclic-di-GMP-mediated signalling within the sigma network of Escherichia coli. Mol. Microbiol., 62, 1014-1034.
33. Kulasakara, H., Lee, V., Brencic, A., Liberati, N., Urbach, J., Miyata, S., Lee, D.G., Neely, A.N., Hyodo, M., Hayakawa, Y. et al. (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-′)-cyclic-GMP in virulence. Proc. Natl Acad. Sci. USA, 103, 2839-2844.
34. Pearson, M.M., Sebaihia, M., Churcher, C., Quail, M.A., Seshasayee, A.S., Luscombe, N.M., Abdellah, Z., Arrosmith, C., Atkin, B., Chillingworth, T. et al. (2008) Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J. Bacteriol., 190, 4027-4037.
35. Rather, P.N. (2005) Swarmer cell differentiation in Proteus mirabilis. Environ. Microbiol., 7, 1065-1073.
36. Holland, L.M., O'Donnell, S.T., Ryjenkov, D.A., Gomelsky, L., Slater, S.R., Fey, P.D., Gomelsky, M. and O'Gara, J.P. (2008) A staphylococcal GGDEF domain protein regulates biofilm formation independently of cyclic dimeric GMP. J. Bacteriol., 190, 5178-5189.
37. Lai, T.H., Kumagai, Y., Hyodo, M., Hayakawa, Y. and Rikihisa, Y. (2009) The Anaplasma phagocytophilum PleC histidine kinase and PleD diguanylate cyclase two-component system and role of cyclic Di-GMP in host cell infection. J. Bacteriol., 191, 693-700.
38. Ulrich, L.E., Koonin, E.V. and Zhulin, I.B. (2005) One-component systems dominate signal transduction in prokaryotes. Trends Microbiol., 13, 52-56.
39. Garcia, B., Latasa, C., Solano, C., Garcia-del Portillo, F., Gamazo, C. and Lasa, I. (2004) Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol. Microbiol., 54, 264-277.
40. 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.
41. Güvener, Z.T. and Harwood, C.S. (2007) Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol. Microbiol., 66, 1459-1473.
42. Shapiro, L., McAdams, H.H. and Losick, R. (2009) Why and how bacteria localize proteins. Science, 326, 1225-1228.
43. Bendtsen, J.D., Binnewies, T.T., Hallin, P.F. and Ussery, D.W. (2005) Genome update: prediction of membrane proteins in prokaryotic genomes. Microbiology, 151, 2119-2121.
44. Ponting, C.P. and Aravind, L. (1997) PAS: a multifunctional domain family comes to light. Curr. Biol., 7, R674-R677.
45. Qui, Y., Rao, F., Luo, Z. and Liang, Z.X. (2009) A flavin cofactor-binding PAS domain regulates c-di-GMP synthesis in AxDGC2 from Acetobacter xylinum. Biochemistry, 48, 10275-10285.
46. Aravind, L. and 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.
47. Aravind, L. and Ponting, C.P. (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem. Sci., 22, 458-459.
48. Skerker, J.M., Perchuk, B.S., Siryaporn, A., Lubin, E.A., Ashenberg, O., Goulian, M. and Laub, M.T. (2008) Rewiring the specificity of two-component signal transduction systems. Cell, 133, 1043-1054.
49. Vogel, C., Bashton, M., Kerrison, N.D., Chothia, C. and Teichmann, S.A. (2004) Structure, function and evolution of multidomain proteins. Curr. Opin. Struct. Biol., 14, 208-216.
50. Christen, M., Christen, B., Folcher, M., Schauerte, A. and 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.
51. Huang, B., Whitchurch, C.B. and Mattick, J.S. (2003) FimX, a multidomain protein connecting environmental signals to twitching motility in Pseudomonas aeruginosa. J. Bacteriol., 185, 7068-7076.
52. Kazmierczak, B.I., Lebron, M.B. and Murray, T.S. (2006) Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol. Microbiol., 60, 1026-1043.
53. Duerig, A., Abel, S., Folcher, M., Nicollier, M., Schwede, T., Amiot, N., Giese, B. and Jenal, U. (2009) Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev., 23, 93-104.
54. Jonas, K., Tomenius, H., Romling, U., Georgellis, D. and Melefors, O. (2006) Identification of YhdA as a regulator of the Escherichia coli carbon storage regulation system. Microbiol. Lett., 264, 232-237.
55. Tschowri, N., Busse, S. and Hengge, R. (2009) The BLUF-EAL protein YcgF acts as a direct anti-repressor in a blue-light response of Escherichia coli. Genes Dev., 23, 522-534.
56. Ryan, R.P., Fouhy, Y., Lucey, J.F., Crossman, L.C., Spiro, S., He, Y.W., Zhang, L.H., Heeb, S., Camara, M., Williams, P. et al. (2006) Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl Acad. Sci. USA, 103, 6712-6717.
57. Camilli, A. and Bassler, B.L. (2006) Bacterial small-molecule signaling pathways. Science, 311, 1113-1116.
58. Römling, U. (2009) Cyclic Di-GMP (c-Di-GMP) goes into host cells-c-Di-GMP signaling in the obligate intracellular pathogen Anaplasma phagocytophilum. J. Bacteriol., 191, 683-686.
59. Amikam, D. and Galperin, M.Y. (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics, 22, 3-6.
60. Pratt, J.T., Tamayo, R., Tischler, A.D. and Camilli, A. (2007) PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae. J. Biol. Chem., 282, 12860-12870.
61. Ryjenkov, D.A., Simm, R., Romling, U. and Gomelsky, M. (2006) The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J. Biol. Chem., 281, 30310-30314.
62. Sudarsan, N., Lee, E.R., Weinberg, Z., Moy, R.H., Kim, J.N., Link, K.H. and Breaker, R.R. (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science, 321, 411-413.