Systematic analysis of diguanylate cyclases that promote biofilm formation by Pseudomonas fluorescens Pf0-1

Journal of Bacteriology

Volumn 193, Issue 18, 2011, Pages 4685-4698

  Newell, Peter D ^a   Yoshioka, Shiro ^a,b   Hvorecny, Kelli L ^a   Monds, Russell D ^a,c   O'Toole, George A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b INSTITUTE FOR MOLECULAR SCIENCE   (Japan)

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP DERIVATIVE; DIGUANYLATE CYCLASE; LAPA PROTEIN; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOFILM; CELL SURFACE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME DEGRADATION; ENZYME PURIFICATION; ENZYME SYNTHESIS; EXPRESSION VECTOR; GENE DELETION; GENE INSERTION; GENE MUTATION; MICROARRAY ANALYSIS; MUTAGENESIS; NONHUMAN; PHENOTYPE; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PSEUDOMONAS FLUORESCENS; REGULATORY MECHANISM; TRANSPOSON;

BIOFILMS; CYCLIC GMP; DNA TRANSPOSABLE ELEMENTS; ESCHERICHIA COLI PROTEINS; GENE KNOCKOUT TECHNIQUES; MUTAGENESIS, INSERTIONAL; PHOSPHORUS-OXYGEN LYASES; PSEUDOMONAS FLUORESCENS;

PSEUDOMONAS FLUORESCENS;

EID: 80052519940     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05483-11     Document Type: Article

References (53)

1. An, S., J. Wu, and L. H. Zhang. 2010. Modulation of Pseudomonas aeruginosa biofilm dispersal by a cyclic-Di-GMP phosphodiesterase with a putative hypoxia-sensing domain. Appl. Environ. Microbiol. 76:8160-8173.
2. Banin, E., M. L. Vasil, and E. P. Greenberg. 2005. Iron and Pseudomonas aeruginosa biofilm formation. Proc. Natl. Acad. Sci. U. S. A. 102:11076-11081.
3. Bantinaki, E., et al. 2007. Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of wrinkly spreader diversity. Genetics 176:441-453.
4. Choy, W. K., L. Zhou, C. K. Syn, L. H. Zhang, and S. Swarup. 2004. MorA defines a new class of regulators affecting flagellar development and biofilm formation in diverse Pseudomonas species. J. Bacteriol. 186:7221-7228.
5. Christen, M., B. Christen, M. Folcher, A. Schauerte, and U. Jenal. 2005. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 280:30829-30837.
6. 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. 184:6481-6489.
7. Davey, M. E., and A. G. O'Toole. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64:847-867.
8. De, N., et al. 2008. Phosphorylation-independent regulation of the diguanylate cyclase WspR. PLoS Biol. 6:e67.
9. Galperin, M. Y., A. N. Nikolskaya, and E. V. Koonin. 2001. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 203:11-21.
10. Haas, D., and G. Defago. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3:307-319.
11. Hay, I. D., U. Remminghorst, and B. H. Rehm. 2009. MucR, a novel membrane-associated regulator of alginate biosynthesis in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 75:1110-1120.
12. 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. U. S. A. 102:14422-14427.
13. Hinsa, S. M., M. Espinosa-Urgel, J. L. Ramos, and G. A. O'Toole. 2003. Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol. Microbiol. 49:905-918.
14. Hinsa, S. M., and G. A. O'Toole. 2006. Biofilm formation by Pseudomonas fluorescens WCS365: a role for LapD. Microbiology 152:1375-1383.
15. Jackson, D. W., et al. 2002. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J. Bacteriol. 184: 290-301.
16. Kader, A., R. Simm, U. Gerstel, M. Morr, and U. Romling. 2006. Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 60:602-616.
17. Kulasakara, H., et al. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3'-5')-cyclic-GMP in virulence. Proc. Natl. Acad. Sci. U. S. A. 103:2839-2844.
18. Lukat, G. S., W. R. McCleary, A. M. Stock, and J. B. Stock. 1992. Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc. Natl. Acad. Sci. U. S. A. 89:718-722.
19. Malone, J. G., et al. 2010. YfiBNR mediates cyclic di-GMP dependent small colony variant formation and persistence in Pseudomonas aeruginosa. PLoS Pathog. 6:e1000804.
20. Malone, J. G., et al. 2007. The structure-function relationship of WspR, a Pseudomonas fluorescens response regulator with a GGDEF output domain. Microbiology 153:980-994.
21. McDonald, M. J., S. M. Gehrig, P. L. Meintjes, X. X. Zhang, and P. B. Rainey. 2009. Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics 183:1041-1053.
22. Merritt, J. H., K. M. Brothers, S. L. Kuchma, and G. A. O'Toole. 2007. SadC reciprocally influences biofilm formation and swarming motility via modulation of exopolysaccharide production and flagellar function. J. Bacteriol. 189:8154-8164.
23. Merritt, J. H., et al. 2010. Specific control of Pseudomonas aeruginosa surface-associated behaviors by two c-di-GMP diguanylate cyclases. mBio 1:e00183.
24. Monds, R. D., P. D. Newell, R. H. Gross, and G. A. O'Toole. 2007. Phosphatedependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol. Microbiol. 63:656-679.
25. Monds, R. D., P. D. Newell, J. A. Schwartzman, and G. A. O'Toole. 2006. Conservation of the Pho regulon in Pseudomonas fluorescens Pf0-1. Appl. Environ. Microbiol. 72:1910-1924.
26. Monds, R. D., et al. 2010. Di-adenosine tetraphosphate (Ap4A) metabolism impacts biofilm formation by Pseudomonas fluorescens via modulation of c-di-GMP-dependent pathways. J. Bacteriol. 192:3011-3023.
27. Monds, R. D., and G. A. O'Toole. 2009. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol. 17:73-87.
28. Müsken, M., S. Di Fiore, A. Dotsch, R. Fischer, and S. Haussler. 2010. Genetic determinants of Pseudomonas aeruginosa biofilm establishment. Microbiology 156:431-441.
29. Navarro, M. V., et al. 2011. Structural basis for c-di-GMP-mediated insideout signaling controlling periplasmic proteolysis. PLoS Biol. 9:e1000588.
30. Navazo, A., et al. 2009. Three independent signalling pathways repress motility in Pseudomonas fluorescens F113. Microb. Biotechnol. 2:489-498.
31. Newell, P. D., C. D. Boyd, H. Sondermann, and G. A. O'Toole. 2011. A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol. 9:e1000587.
32. Newell, P. D., and G. A. O'Toole. 2010. Environmental control of cyclic di-GMP signaling in Pseudomonas fluorescens: from signal to output, p. 282-290. In A. J. Wolfe and K. L. Visick (ed.), The second messenger cyclic Di-GMP. ASM Press, Washington DC.
33. Newell, P. D., R. D. Monds, and G. A. O'Toole. 2009. LapD is a bis-(3',5')-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc. Natl. Acad. Sci. U. S. A. 106:3461-3466.
34. O'Toole, G. A. 2008. How Pseudomonas aeruginosa regulates surface behaviors. Microbe 3:65-71.
35. O'Toole, G. A., K. A. Gibbs, P. W. Hager, P. V. Phibbs, Jr., and R. Kolter. 2000. The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J. Bacteriol. 182:425-431.
36. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
37. Paul, R., et al. 2007. Activation of the diguanylate cyclase PleD by phosphorylation-mediated dimerization. J. Biol. Chem. 282:29170-29177.
38. Paul, R., 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.
39. Pratt, J. T., E. McDonough, and A. Camilli. 2009. PhoB regulates motility, biofilms, and cyclic di-GMP in Vibrio cholerae. J. Bacteriol. 191:6632-6642.
40. Rao, F., et al. 2009. The functional role of a conserved loop in EAL domainbased cyclic di-GMP-specific phosphodiesterase. J. Bacteriol. 191:4722-4731.
41. Ryan, R. 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. U. S. A. 103:6712-6717.
42. Ryjenkov, D. A., M. Tarutina, O. V. Moskvin, and M. Gomelsky. 2005. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187:1792-1798.
43. Sawai, H., et al. 2010. Molecular oxygen regulates the enzymatic activity of a heme-containing diguanylate cyclase (HemDGC) for the synthesis of cyclic di-GMP. Biochim. Biophys. Acta 1804:166-172.
44. Schmidt, A. J., D. A. Ryjenkov, and M. Gomelsky. 2005. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 187:4774-4781.
45. Seshasayee, A. S., G. M. Fraser, and N. M. Luscombe. 2010. Comparative genomics of cyclic-di-GMP signalling in bacteria: post-translational regulation and catalytic activity. Nucleic Acids Res. 38:5970-5981.
46. Shanks, R. M., N. C. Caiazza, S. M. Hinsa, C. M. Toutain, and G. A. O'Toole. 2006. Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl. Environ. Microbiol. 72:5027-5036.
47. Silby, M. W., et al. 2009. Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol. 10:R51.
48. Stanley, N. R., and B. A. Lazazzera. 2004. Environmental signals and regulatory pathways that influence biofilm formation. Mol. Microbiol. 52:917-924.
49. Tarutina, M., D. A. Ryjenkov, and M. Gomelsky. 2006. An unorthodox bacteriophytochrome from Rhodobacter sphaeroides involved in turnover of the second messenger c-di-GMP. J. Biol. Chem. 281:34751-34758.
50. Tuckerman, J. R., et al. 2009. An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48:9764-9774.
51. Wagner, V. E., L. L. Li, V. M. Isabella, and B. H. Iglewski. 2007. Analysis of the hierarchy of quorum-sensing regulation in Pseudomonas aeruginosa. Anal. Bioanal. Chem. 387:469-479.
52. Wolfe, A. J., and K. L. Visick. 2008. Get the message out: cyclic-Di-GMP regulates multiple levels of flagellum-based motility. J. Bacteriol. 190:463-475.
53. Wu, H., et al. 2000. Identification and characterization of two chemotactic transducers for inorganic phosphate in Pseudomonas aeruginosa. J. Bacteriol. 182:3400-3404.