Cyclic di-GMP: a second messenger required for long-term survival, but not for biofilm formation, in Mycobacterium smegmatis

References

1. Aldridge P., Paul R., Goymer P., Rainey P., Jenal U. 2003; Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus . Mol Microbiol 47:1695–1708
   [Google Scholar]
2. Beyhan S., Tischler A. D., Camilli A., Yildiz F. H. 2006; Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level. J Bacteriol 188:3600–3613
   [Google Scholar]
3. Bloom B. R., Murray C. J. L. 1992; Tuberculosis: commentary on a reemergent killer. Science 257:1055–1064
   [Google Scholar]
4. Brouillette E., Hyodo M., Hayakawa Y., Karaolis D. K., Malouin F. 2005; 3′,5′-cyclic diguanylic acid reduces the virulence of biofilm-forming Staphylococcus aureus strains in a mouse model of mastitis infection. Antimicrob Agents Chemother 49:3109–3113
   [Google Scholar]
5. Camilli A., Bassler B. L. 2006; Bacterial small-molecule signaling pathways. Science 311:1113–1116
   [Google Scholar]
6. Cashel M., Gentry D. R., Hernandez V. J., Vinella D. others 1996; The stringent response. In Escherichia coli and Salmonella: Cellular and Molecular Biology , 2nd edn. pp 1458–1496 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
   [Google Scholar]
7. Chan C., Paul R., Samoray D., Amiot N. C., Giese B., Jenal U., Schirmer T. 2004; Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci U S A 101:17084–17089
   [Google Scholar]
8. Chatterji D., Ojha A. K. 2001; Revisiting the stringent response, ppGpp and starvation signaling. Curr Opin Microbiol 4:160–165
   [Google Scholar]
9. 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
   [Google Scholar]
10. Dahl J. L., Arora K., Boshoff H. I., Whiteford D. C., Pacheco S. A., Walsh O. J., Lau-Bonilla D., Davis W. B., Garza A. G. 2005; The relA homolog of Mycobacterium smegmatis affects cell appearance, viability, and gene expression. J Bacteriol 187:2439–2447
    [Google Scholar]
11. 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
    [Google Scholar]
12. Ferreira R. B., Antunes L. C., Greenberg E. P., McCarter L. L. 2008; Vibrio parahaemolyticus ScrC modulates c-di-GMP regulation of gene expression relevant to growth on surfaces. J Bacteriol 190:851–860
    [Google Scholar]
13. 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
    [Google Scholar]
14. Hall-Stoodley L., Costerton J. W., Stoodley P. 2004; Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108
    [Google Scholar]
15. 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 U S A 102:14422–14427
    [Google Scholar]
16. Hisert K. B., MacCoss M., Shiloh M. U., Darwin K. H., Singh S., Jones R. A., Ehrt S., Zhang Z., Gaffney B. L. other authors 2005; A glutamate–alanine–leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defence and killing of macrophages: role of cyclic diGMP. Mol Microbiol 56:1234–1245
    [Google Scholar]
17. Huitema E., Pritchard S., Matteson D., Radhakrishnan S. K., Viollier P. H. 2006; Bacterial birth scar proteins mark future flagellum assembly site. Cell 124:1025–1037
    [Google Scholar]
18. Hurley J. H. 2003; GAF domains: cyclic nucleotides come full circle. Sci STKE 164:PE1
    [Google Scholar]
19. Jacobs W. R. Jr, Tuckman M., Bloom B. R. 1987; Introduction of foreign DNA into mycobacteria using a shuttle phasmid. Nature 327:532–535
    [Google Scholar]
20. Jain V., Kumar M., Chatterji D. 2006a; ppGpp: stringent response and survival. J Microbiol 44:1–10
    [Google Scholar]
21. Jain V., Saleem-Batcha R., China A., Chatterji D. 2006b; Molecular dissection of the mycobacterial stringent response protein Rel. Protein Sci 15:1449–1464
    [Google Scholar]
22. Jenal U., Malone J. 2006; Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40:385–407
    [Google Scholar]
23. Karaolis D. K., Rashid M. H., Chythanya R., Luo W., Hyodo M., Hayakawa Y. 2005; c-di-GMP (3′-5′-cyclic diguanylic acid) inhibits Staphylococcus aureus cell–cell interactions and biofilm formation. Antimicrob Agents Chemother 49:1029–1038
    [Google Scholar]
24. Kazmierczak B. I., Lebron M. B., Murray T. S. 2006; Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa . Mol Microbiol 60:1026–1043
    [Google Scholar]
25. Kirillina O., Fetherston J. D., Bobrov A. G., Abney J., 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
    [Google Scholar]
26. Klebensberger J., Lautenschlager K., Bressler D., Wingender J., Philipp B. 2007; Detergent-induced cell aggregation in subpopulations of Pseudomonas aeruginosa as a preadaptive survival strategy. Environ Microbiol 9:2247–2259
    [Google Scholar]
27. Kuchma S. L., Connolly J. P., O'Toole G. A. 2005; A three-component regulatory system regulates biofilm maturation and type III secretion in Pseudomonas aeruginosa . J Bacteriol 187:1441–1454
    [Google Scholar]
28. Kuchma S. L., Brothers K. M., Merritt J. H., Liberati N. T., Ausubel F. M., O'Toole G. A. 2007; BifA, a cyclic-di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189:8165–8178
    [Google Scholar]
29. Kulasakara H., Lee V., Brencic A., Liberati N., Urbach J., Miyata S., Lee D. G., Neely A. N., Hyodo M. other authors 2006; Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterase reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci U S A 103:2839–2844
    [Google Scholar]
30. Lestrate P., Dricot A., Delrue R. M., Lambert C., Martinelli V., De Bolle X., Letesson J. J., Tibor A. 2003; Attenuated signature-tagged mutagenesis mutants of Brucella melitensis identified during the acute phase of infection in mice. Infect Immun 71:7053–7060
    [Google Scholar]
31. Mathew R., Mukherjee R., Balachandar R., Chatterji D. 2006; Deletion of the rpoZ gene, encoding the ω subunit of RNA polymerase, results in pleiotropic surface-related phenotypes in Mycobacterium smegmatis . Microbiology 152:1741–1750
    [Google Scholar]
32. Méndez-Ortiz M. M., Hyodo M., Hayakawa Y., Membrillo-Hernández J. 2006; Genome-wide transcriptional profile of Escherichia coli in response to high levels of the second messenger 3′,5′-cyclic diguanylic acid. J Biol Chem 281:8090–8099
    [Google Scholar]
33. Merkel T. J., Stibitz S., Keith J. M., Leef M., Shahin R. 1998; Contribution of regulation by the bvg locus to respiratory infection of mice by Bordetella pertussis . Infect Immun 66:4367–4373
    [Google Scholar]
34. Merritt J. H., Brothers K. M., Kuchma S. L., O'Toole G. A. 2007; SadC reciprocally influences biofilm formation and swarming motility via modulation of exopolysaccharide production and flagellar function. J Bacteriol 189:8154–8164
    [Google Scholar]
35. Miller M. B., Bassler B. L. 2001; Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199
    [Google Scholar]
36. Nyka W. 1974; Studies on the effect of starvation on mycobacteria. Infect Immun 9:843–850
    [Google Scholar]
37. Ojha A., Hatfull G. F. 2007; The role of iron in Mycobacterium smegmatis biofilm formation: the exochelin siderophore is essential in limiting iron conditions for biofilm formation but not for planktonic growth. Mol Microbiol 66:468–483
    [Google Scholar]
38. Ojha A. K., Mukherjee T. K., Chatterji D. 2000; High intracellular level of guanosine tetraphosphate in Mycobacterium smegmatis changes the morphology of the bacterium. Infect Immun 68:4084–4091
    [Google Scholar]
39. O'Toole G. A., Pratt L. A., Watnick P. I., Newman D. K., Weaver V. B., Kolter R. 1999; Genetic approaches to study of biofilms. Methods Enzymol 310:91–109
    [Google Scholar]
40. Parrish N. M., Dick J. D., Bishai W. R. 1998; Mechanisms of latency in Mycobacterium tuberculosis . Trends Microbiol 6:107–112
    [Google Scholar]
41. 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
    [Google Scholar]
42. Pei J., Grishin N. V. 2001; GGDEF domain is homologous to adenylyl cyclase. Proteins 42:210–216
    [Google Scholar]
43. Pelicic V., Jackson M., Reyrat J. M., Jacobs W. R. Jr, Gicquel B., Guilhot C. 1997; Efficient allelic exchange and transposon mutagenesis in Mycobacterium tuberculosis . Proc Natl Acad Sci U S A 94:10955–10960
    [Google Scholar]
44. Primm T. P., Andersen S. J., Mizrahi V., Avarbock D., Rubin H., Barry C. E. III 2000; The stringent response of Mycobacterium tuberculosis is required for long-term survival. J Bacteriol 182:4889–4898
    [Google Scholar]
45. Römling U., Gomelsky M., Galperin M. Y. 2005; c-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57:629–639
    [Google Scholar]
46. Ross P., Weinhouse H., Aloni Y., Michaeli D., Weinberger-Ohana P., Mayer R., Braun S., De Vroom E., Van der Marel G. A. other authors 1987; Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325:279–281
    [Google Scholar]
47. Ryan R. P., Fouhy Y., Lucey J. F., Crossman L. C., Spiro S., He Y. W., Zhang L. H., Heeb S., Cámara M. other authors 2006; Cell–cell signaling in Xanthomonas campestris involves an HD–GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A 103:6712–6717
    [Google Scholar]
48. 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
    [Google Scholar]
49. 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
    [Google Scholar]
50. Shenoy A. R., Visweswariah S. S. 2006; New messages from old messengers: cAMP and mycobacteria. Trends Microbiol 14:543–550
    [Google Scholar]
51. Simm R., Morr M., Kader A., Nimtz M., Römling U. 2004; GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53:1123–1134
    [Google Scholar]
52. Smeulders M. J., Keer J., Speight R. A., Williams H. D. 1999; Adaptation of Mycobacterium smegmatis to stationary phase. J Bacteriol 181:270–283
    [Google Scholar]
53. Stover C. K., de la Cruz V. F., Fuerst T. R., Burlein J. E., Benson L. A., Bennett L. T., Bansal G. P., Young J. F., Lee M. H. other authors 1991; New use of BCG for recombinant vaccines. Nature 351:456–460
    [Google Scholar]
54. Tal R., Wong H. C., Calhoon R., Gelfand D., Fear A. L., Volman G., Mayer R., Ross P., Amikam D. other authors 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
    [Google Scholar]
55. Tamayo R., Tischler A. D., Camilli A. 2005; The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J Biol Chem 280:33324–33330
    [Google Scholar]
56. Tamayo R., Pratt J. T., Camilli A. 2007; Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61:131–148
    [Google Scholar]
57. Tarutina M., Ryjenkov D. A., 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
    [Google Scholar]
58. Teng R., Dick T. 2003; Isoniazid resistance of exponentially growing Mycobacterium smegmatis biofilm culture. FEMS Microbiol Lett 227:171–174
    [Google Scholar]
59. Thormann K. M., Duttler S., Saville R. M., Hyodo M., Shukla S., Hayakawa Y., Spormann A. M. 2006; Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J Bacteriol 188:2681–2691
    [Google Scholar]
60. Tischler A. D., Camilli A. 2004; Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53:857–869
    [Google Scholar]
61. Tischler A. D., Camilli A. 2005; Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun 73:5873–5882
    [Google Scholar]
62. Weinhouse H., Sapir S., Amikam D., Shilo Y., Volman G., Ohana P., Benziman M. 1997; c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum . FEBS Lett 416:207–211
    [Google Scholar]