Chapter 3 : Ubiquity of Cyclic Di-GMP Pathways: a Bioinformatic Analysis

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Ubiquity of Cyclic Di-GMP Pathways: a Bioinformatic Analysis, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816667/9781555814991_Chap03-1.gif /docserver/preview/fulltext/10.1128/9781555816667/9781555814991_Chap03-2.gif


In this chapter, the author shows how the bioinformatic tools have contributed to the studies of the c-di-GMP-mediated signaling pathways—and continue to do so. A brief discussion of the roles of the GGDEF, EAL, and HD-GYP domains in c-di-GMP turnover and the role of the PilZ domain as a c-di-GMP adaptor protein is followed by an analysis of the phylogenetic distribution of these domains and a listing of the most common domain architectures that involve these four domains. The identification of the GGDEF domain as a component of DGCs and c-di-GMP-specific phosphodiesterases, participating in c-di-GMP turnover, by Benziman and his colleagues was a watershed event in at least three important aspects. This work provided the first evidence of an enzymatic function for this widespread protein domain and paved the way to the experimental demonstration that the GGDEF domain alone was responsible for the DGC activity. Second, linking this widespread domain with c-di-GMP turnover provided evidence for the participation of c-di-GMP in a variety of signaling processes. Third, the presence of the GGDEF domain in DGCs and in c-di-GMP-specific phosphodiesterases, two kinds of enzymes with opposing activities, suggested that this domain had allosteric functions that regulate c-di-GMP turnover. Experimental characterization of the most widespread combinations of c-di- GMP-related domains, including those described above, remains a promising venue of research that can be expected to provide much-needed insights into the functioning of this fascinating signaling system and its role in bacterial adaptation mechanisms.

Citation: Galperin M. 2010. Ubiquity of Cyclic Di-GMP Pathways: a Bioinformatic Analysis, p 24-36. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch3
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1.
Figure 1.

Growth of the number of c-di-GMP-related protein domains in the public protein databases. The numbers of proteins containing GGDEF domains but no EAL domains (open circles), both GGDEF and EAL domains (grey circles), only EAL domains (open squares), HD-GYP domains (diamonds), and PilZ domains (triangles) are indicated.

Citation: Galperin M. 2010. Ubiquity of Cyclic Di-GMP Pathways: a Bioinformatic Analysis, p 24-36. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch3
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Alm, R. A.,, A. J. Bodero,, P. D. Free, and, J. S. Mattick. 1996. Identification of a novel gene, pilZ, essential for type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J. Bacteriol. 178: 4653.
2. Amikam, D., and, M. Y. Galperin. 2006. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22: 36.
3. Anantharaman, V., and, L. Aravind. 2003. Application of comparative genomics in the identification and analysis of novel families of membrane-associated receptors in bacteria. BMC Genomics 4: 34.
4. Aravind, L., and, E. V. Koonin. 1998. The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem. Sci. 23: 469472.
5. Ausmees, N.,, H. Jonsson,, S. Hoglund,, H. Ljunggren, and, M. Lindberg. 1999. Structural and putative regulatory genes involved in cellulose synthesis in Rhizobium leguminosarum bv. trifolii. Microbiology 145: 12531262.
6. Benach, J.,, S. S. Swaminathan,, R. Tamayo,, S. K. Handelman,, E. Folta-Stogniew,, J. E. Ramos,, F. Forouhar,, H. Neely,, J. Seetharaman,, A. Camilli, and, J. F. Hunt. 2007. The structural basis of cyclic diguanylate signal transduction by PilZ domains. EMBO J. 26: 51535166.
7. Bobrov, A. G.,, O. Kirillina, and, R. D. Perry. 2005. The phosphodiesterase activity of the HmsP EAL domain is required for negative regulation of biofilm formation in Yersinia pestis. FEMS Microbiol. Lett. 247: 123130.
8. Brown, N. L.,, T. K. Misra,, J. N. Winnie,, A. Schmidt,, M. Seiff, and, S. Silver. 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: 143151.
9. Chan, C.,, R. Paul,, D. Samoray,, N. C. Amiot,, B. Giese,, U. Jenal, and, T. Schirmer. 2004. Structural basis of activity and allosteric control of diguanylate cyclase. Proc. Natl. Acad. Sci. USA 101: 1708417089.
10. Chang, A. L.,, J. R. Tuckerman,, G. Gonzalez,, R. Mayer,, H. Weinhouse,, G. Volman,, D. Amikam,, M. Benziman, and, M. A. Gilles-Gonzalez. 2001. Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40: 34203426.
11. Christen, B.,, M. Christen,, R. Paul,, F. Schmid,, M. Folcher,, P. Jenoe,, M. Meuwly, and, U. Jenal. 2006. Allosteric control of cyclic di-GMP signaling. J. Biol. Chem. 281: 3201532024.
12. Christen, M.,, B. Christen,, M. G. Allan,, M. Folcher,, P. Jeno,, S. Grzesiek, and, U. Jenal. 2007. DgrA is a member of a new family of cyclic diguanosine monophosphate receptors and controls flagellar motor function in Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 104: 41124117.
13. Claret, L.,, S. Miquel,, N. Vieille,, D. A. Ryjenkov,, M. Gomelsky, and, A. Darfeuille-Michaud. 2007. The flagellar sigma factor FliA regulates adhesion and invasion of Crohn disease-associated Escherichia coli via a cyclic dimeric GMP-dependent pathway. J. Biol. Chem. 282: 3327533283.
14. D’Argenio,, D. A.,, M. W. Calfee,, P. B. Rainey, and, E. C. Pesci. 2002. Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J. Bacteriol. 184: 64816489.
15. De, N.,, M. Pirruccello,, P. V. Krasteva,, N. Bae,, R. V. Raghavan, and, H. Sondermann. 2008. Phosphorylation-independent regulation of the diguanylate cyclase WspR. PLoS Biol. 6: e67.
16. Delgado-Nixon,, V. M.,, G. Gonzalez, and, M. A. Gilles-Gonzalez. 2000. Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. Biochemistry 39: 26852691.
17. Drenkard, E., and, F. M. Ausubel. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416: 740743.
18. Finn, R. D.,, J. Tate,, J. Mistry,, P. C. Coggill,, S. J. Sammut,, H. R. Hotz,, G. Ceric,, K. Forslund,, S. R. Eddy,, E. L. Sonn-hammer, and, A. Bateman. 2008. The Pfam protein families database. Nucleic Acids Res. 36: D281D288.
19. Freitas, T. A.,, S. Hou, and, M. Alam. 2003. The diversity of globin-coupled sensors. FEBS Lett. 552: 99104.
20. Galperin, M. Y. 2004. Bacterial signal transduction network in a genomic perspective. Environ. Microbiol. 6: 552567.
21. Galperin, M. Y. 2005. A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol. 5: 35.
22. Galperin, M. Y.,, A. N. Nikolskaya, and, E. V. Koonin. 2001. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 203: 1121.
23. Galperin, M. Y.,, D. A. Natale,, L. Aravind, and, E. V. Koonin. 1999. A specialized version of the HD hydrolase domain implicated in signal transduction. J. Mol. Microbiol. Biotechnol. 1: 303305.
24. Galperin, M. Y.,, T. A. Gaidenko,, A. Y. Mulkidjanian,, M. Nakano, and, C. W. Price. 2001. MHYT, a new integral membrane sensor domain. FEMS Microbiol. Lett. 205: 1723.
25. Girgis, H. S.,, Y. Liu,, W. S. Ryu, and, S. Tavazoie. 2007. A comprehensive genetic characterization of bacterial motility. PLoS Genet. 3: 16441660.
26. Gjermansen, M.,, P. Ragas, and, T. Tolker-Nielsen. 2006. Proteins with GGDEF and EAL domains regulate Pseudomonas putida biofilm formation and dispersal. FEMS Microbiol. Lett. 265: 215224.
27. Gomelsky, M., and, S. Kaplan. 1998. AppA, a redox regulator of photosystem formation in Rhodobacter sphaeroides 2.4.1, is a flavoprotein. Identification of a novel FAD-binding domain. J. Biol. Chem. 273: 3531935325.
28. Goymer, P.,, S. G. Kahn,, J. G. Malone,, S. M. Gehrig,, A. J. Spiers, and, P. B. Rainey. 2006. Adaptive divergence in experimental populations of Pseudomonas fluorescens. II. Role of the GGDEF regulator WspR in evolution and development of the wrinkly spreader phenotype. Genetics 173: 515526.
29. Hecht, G. B., and, A. Newton. 1995. Identification of a novel response regulator required for the swarmer-to-stalked-cell transition in Caulobacter crescentus. J. Bacteriol. 177: 62236229.
30. Henrick, K.,, Z. Feng,, W. F. Bluhm,, D. Dimitropoulos,, J. F. Doreleijers,, S. Dutta,, J. L. Flippen-Anderson,, J. Ionides,, C. Kamada,, E. Krissinel,, C. L. Lawson,, J. L. Markley,, H. Nakamura,, R. Newman,, Y. Shimizu,, J. Swaminathan,, S. Velankar,, J. Ory,, E. L. Ulrich,, W. Vranken,, J. Westbrook,, R. Yamashita,, H. Yang,, J. Young,, M. Yousufuddin, and, H. M. Berman. 2008. Remediation of the protein data bank archive. Nucleic Acids Res. 36: D426D433.
31. Hickman, J. W., and, C. S. Harwood. 2008. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Microbiol. 69: 376389.
32. Hickman, J. W.,, D. F. Tifrea, and, C. S. Harwood. 2005. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. USA 102: 1442214427.
33. Jenal, U., and, M. Y. Galperin. 2009. Single-domain response regulators: molecular switches with emerging roles in cell organization and dynamics. Curr. Opin. Microbiol. 12: 152160.
34. Kader, A.,, R. Simm,, U. Gerstel,, M. Morr, and, U. Römling. 2006. Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 60: 602616.
35. Kazmierczak, B. I.,, M. B. Lebron, and, T. S. Murray. 2006. Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol. Microbiol. 60: 10261043.
36. Kim, Y. K., and, L. L. McCarter. 2007. ScrG, a GGDEF-EAL protein, participates in regulating swarming and sticking in Vibrio parahaemolyticus. J. Bacteriol. 189: 40944107.
37. Ko, M., and, C. Park. 2000. Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli. J. Mol. Biol. 303: 371382.
38. Kulasekara, H. D.,, I. Ventre,, B. R. Kulasekara,, A. Lazdunski,, A. Filloux, and, S. Lory. 2005. A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol. Microbiol. 55: 368380.
39. Lai, T. H.,, Y. Kumagai,, M. Hyodo,, Y. Hayakawa, and, Y. Rikihisa. 2008. 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: 693700.
40. Lee, V. T.,, J. M. Matewish,, J. L. Kessler,, M. Hyodo,, Y. Hayakawa, and, S. Lory. 2007. A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol. Microbiol. 65: 14741484.
41. Maharaj, R.,, T. B. May,, S. K. Wang, and, A. M. Chakrabarty. 1993. Sequence of the alg8 and alg44 genes involved in the synthesis of alginate by Pseudomonas aeruginosa. Gene 136: 267269.
42. Malone, J. G.,, R. Williams,, M. Christen,, U. Jenal,, A. J. Spiers, and, P. B. Rainey. 2007. The structure-function relationship of WspR, a Pseudomonas fluorescens response regulator with a GGDEF output domain. Microbiology 153: 980994.
43. Marchler-Bauer,, A.,, J. B. Anderson,, F. Chitsaz,, M. K. Derbyshire,, C. DeWeese-Scott,, J. H. Fong,, L. Y. Geer,, R. C. Geer,, N. R. Gonzales,, M. Gwadz,, S. He,, D. I. Hurwitz,, J. D. Jackson,, Z. Ke,, C. J. Lanczycki,, C. A. Liebert,, C. Liu,, F. Lu,, S. Lu,, G. H. Marchler,, M. Mullokandov,, J. S. Song,, A. Tasneem,, N. Thanki,, R. A. Yamashita,, D. Zhang,, N. Zhang, and, S. H. Bryant. 2009. CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37: D205D210.
44. Mayer, R.,, P. Ross,, H. Weinhouse,, D. Amikam,, G. Volman,, P. Ohana,, R. D. Calhoon,, H. C. Wong,, A. W. Emerick, and, M. Benziman. 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: 54725476.
45. Meissner, A.,, V. Wild,, R. Simm,, M. Rohde,, C. Erck,, F. Bredenbruch,, M. Morr,, U. Römling, and, S. Haussler. 2007. Pseudomonas aeruginosa cupA-encoded fimbriae expression is regulated by a GGDEF and EAL domain-dependent modulation of the intracellular level of cyclic diguanylate. Environ. Microbiol. 9: 24752485.
46. Mejia-Ruiz,, H.,, J. Guzman,, S. Moreno,, G. Soberon-Chavez, and, G. Espin. 1997. The Azotobacter vinelandii alg8 and alg44 genes are essential for alginate synthesis and can be transcribed from an algD-independent promoter. Gene 199: 271277.
47. Merighi, M.,, V. T. Lee,, M. Hyodo,, Y. Hayakawa, and, S. Lory. 2007. The second messenger bis-(3′-5′)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol. Microbiol. 65: 876895.
48. Merkel, T. J., and, S. Stibitz. 1995. Identification of a locus required for the regulation of bvg-repressed genes in Bordetella pertussis. J. Bacteriol. 177: 27272736.
49. Merkel, T. J.,, C. Barros, and, S. Stibitz. 1998. Characterization of the bvgR locus of Bordetella pertussis. J. Bacteriol. 180: 16821690.
50. Nikolskaya, A. N.,, A. Y. Mulkidjanian,, I. B. Beech, and, M. Y. Galperin. 2003. MASE1 and MASE2: two novel integral membrane sensory domains. J. Mol. Microbiol. Biotechnol. 5: 1116.
51. Oglesby, L. L.,, S. Jain, and, D. E. Ohman. 2008. Membrane topology and roles of Pseudomonas aeruginosa Alg8 and Alg44 in alginate polymerization. Microbiology 154: 16051615.
52. Paul, R.,, S. Abel,, P. Wassmann,, A. Beck,, H. Heerklotz, and, U. Jenal. 2007. Activation of the diguanylate cyclase PleD by phosphorylation-mediated dimerization. J. Biol. Chem. 282: 2917029177.
53. Paul, R.,, S. Weiser,, N. C. Amiot,, C. Chan,, T. Schirmer,, B. Giese, and, U. Jenal. 2004. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel diguanylate cyclase output domain. Genes Dev. 18: 715727.
54. Pratt, J. T.,, R. Tamayo,, A. D. Tischler, and, A. Camilli. 2007. PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae. J. Biol. Chem. 282: 1286012870.
55. Pruitt, K. D.,, T. Tatusova,, W. Klimke, and, D. R. Maglott. 2009. NCBI Reference Sequences: current status, policy and new initiatives. Nucleic Acids Res. 37: D32D36.
56. Rahman, M.,, R. Simm,, A. Kader,, E. Basseres,, U. Römling, and, R. Mollby. 2007. The role of c-di-GMP signaling in an Aeromonas veronii biovar sobria strain. FEMS Microbiol. Lett. 273: 172179.
57. Raivio, T. L.,, D. Hoffer,, R. W. Prince,, M. L. Vasil, and, D. G. Storey. 1996. Linker insertion scanning of regA, an activator of exotoxin A production in Pseudomonas aeruginosa. Mol. Microbiol. 22: 239254.
58. Rajagopal, S.,, J. M. Key,, E. B. Purcell,, D. J. Boerema, and, K. Moffat. 2004. Purification and initial characterization of a putative blue light-regulated phosphodiesterase from Escherichia coli. Photochem. Photobiol. 80: 542547.
59. Römling, U.,, M. Rohde,, A. Olsen,, S. Normark, and, J. Reinkoster. 2000. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol. Microbiol. 36: 1023.
60. Ryan, R. P.,, Y. Fouhy,, J. F. Lucey,, B. L. Jiang,, Y. Q. He,, J. X. Feng,, J. L. Tang, and, J. M. Dow. 2007. Cyclic di-GMP signalling in the virulence and environmental adaptation of Xanthomonas campestris. Mol. Microbiol. 63: 429442.
61. Ryan, R. P.,, Y. Fouhy,, J. F. Lucey,, L. C. Crossman,, S. Spiro,, Y. W. He,, L. H. Zhang,, S. Heeb,, M. Camara,, P. Williams, and, J. M. Dow. 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: 67126717.
62. Ryjenkov, D. A.,, M. Tarutina,, O. M. Moskvin, and M. Gomelsky. 2005. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187: 17921798.
63. Ryjenkov, D. A.,, R. Simm,, U. Römling, and, M. Gomelsky. 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: 3031030314.
64. Sarand, I.,, S. Osterberg,, S. Holmqvist,, P. Holmfeldt,, E. Skarfstad,, R. E. Parales, and, V. Shingler. 2008. Metabolism-dependent taxis towards (methyl)phenols is coupled through the most abundant of three polar localized Aer-like proteins of Pseudomonas putida. Environ. Microbiol. 10: 13201334.
65. Sasakura, Y.,, S. Hirata,, S. Sugiyama,, S. Suzuki,, S. Taguchi,, M. Watanabe,, T. Matsui,, I. Sagami, and, T. Shimizu. 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: 2382123827.
66. Schmidt, A. J.,, D. A. Ryjenkov, and, M. Gomelsky. 2005. Ubiquitous protein domain EAL encodes cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 187: 47744781.
67. Simm, R.,, M. Morr,, A. Kader,, M. Nimtz, and, U. Römling. 2004. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol. Microbiol. 53: 11231134.
68. Simm, R.,, J. D. Fetherston,, A. Kader,, U. Römling, and, R. D. Perry. 2005. Phenotypic convergence mediated by GGDEF-domain-containing proteins. J. Bacteriol. 187: 68166823.
69. Slater, H.,, A. Alvarez-Morales,, C. E. Barber,, M. J. Daniels, and, J. M. Dow. 2000. A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol. Microbiol. 38: 9861003.
70. Spiers, A. J.,, J. Bohannon,, S. M. Gehrig, and, P. B. Rainey. 2003. Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol. Microbiol. 50: 1527.
71. Sudarsan, N.,, E. R. Lee,, Z. Weinberg,, R. H. Moy,, J. N. Kim,, K. H. Link, and, R. R. Breaker. 2008. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321: 411413.
72. Swartz, T. E.,, T. S. Tseng,, M. A. Frederickson,, G. Paris,, D. J. Comerci,, G. Rajashekara,, J. G. Kim,, M. B. Mudgett,, G. A. Splitter,, R. A. Ugalde,, F. A. Goldbaum,, W. R. Briggs, and, R. A. Bogomolni. 2007. Blue-light-activated histidine kinases: two-component sensors in bacteria. Science 317: 10901093.
73. Tal, R.,, H. C. Wong,, R. Calhoon,, D. Gelfand,, A. L. Fear,, G. Volman,, R. Mayer,, P. Ross,, D. Amikam,, H. Weinhouse,, A. Cohen,, S. Sapir,, P. Ohana, and, M. Benziman. 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: 44164425.
74. Tamayo, R.,, A. D. Tischler, and, A. Camilli. 2005. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 280: 3332433330.
75. Taylor, B. L., and, I. B. Zhulin. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63: 479506.
76. Tischler, A. D., and, A. Camilli. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 53: 857869.
77. Tischler, A. D., and, A. Camilli. 2005. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun. 73: 58735882.
78. Walker, S. L.,, L. S. Hiremath, and, D. R. Galloway. 1995. ToxR (RegA) activates Escherichia coli RNA polymerase to initiate transcription of Pseudomonas aeruginosa toxA. Gene 154: 1521.
79. Walker, S. L.,, L. S. Hiremath,, D. J. Wozniak, and, D. R. Galloway. 1994. ToxR (RegA)-mediated in vitro transcription of Pseudomonas aeruginosa toxA. Gene 150: 8792.
80. Wan, X.,, J. R. Tuckerman,, J. A. Saito,, T. A. Freitas,, J. S. Newhouse,, J. R. Denery,, M. Y. Galperin,, G. Gonzalez,, M. A. Gilles-Gonzalez, and, M. Alam. 2009. Globins synthesize the second messenger bis-(3′-5′)-cyclic diguanosine monophosphate in bacteria. J. Mol. Biol. 388: 262270.
81. Wassmann, P.,, C. Chan,, R. Paul,, A. Beck,, H. Heerklotz,, U. Jenal, and, T. Schirmer. 2007. Structure of BeF3— -modified response regulator PleD: implications for diguanylate cyclase activation, catalysis, and feedback inhibition. Structure 15: 915927.
82. Weinhouse, H.,, S. Sapir,, D. Amikam,, Y. Shilo,, G. Volman,, P. Ohana, and, M. Benziman. 1997. c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett. 416: 207211.
83. Wozniak, D. J.,, D. C. Cram,, C. J. Daniels, and, D. R. Galloway. 1987. Nucleotide sequence and characterization of toxR: a gene involved in exotoxin A regulation in Pseudomonas aeruginosa. Nucleic Acids Res. 15: 21232135.
84. Yoshimura-Suzuki,, T.,, I. Sagami,, N. Yokota,, H. Kurokawa, and, T. Shimizu. 2005. DOS(Ec), a heme-regulated phosphodiesterase, plays an important role in the regulation of the cyclic AMP level in Escherichia coli. J. Bacteriol. 187: 66786682.
85. Zhulin, I. B.,, A. N. Nikolskaya, and, M. Y. Galperin. 2003. Common extracellular sensory domains in transmembrane receptors for diverse signal transduction pathways in Bacteria and Archaea. J. Bacteriol. 185: 285294.
86. Zogaj, X.,, M. Nimtz,, M. Rohde,, W. Bokranz, and, U. Römling. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39: 14521463.


Generic image for table
Table 1

General properties of c-di-GMP-related signaling domains

Citation: Galperin M. 2010. Ubiquity of Cyclic Di-GMP Pathways: a Bioinformatic Analysis, p 24-36. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch3
Generic image for table
Table 2

Distribution of genes encoding GGDEF, EAL, HD-GYP, and PilZ domain proteins in completely sequenced genomes of selected model organisms

Citation: Galperin M. 2010. Ubiquity of Cyclic Di-GMP Pathways: a Bioinformatic Analysis, p 24-36. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch3

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error