Specific control of Pseudomonas aeruginosa surface-associated behaviors by two c-di-GMP diguanylate cyclases

mBio

Volumn 1, Issue 4, 2010, Pages

  Merritt, Judith H ^a,c   Ha, Dae Gon ^a   Cowles, Kimberly N ^b   Lu, Wenyun ^b   Morales, Diana K ^a   Rabinowitz, Joshua ^b   Gitai, Zemer ^b   O'Toole, George A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c Glycobia Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; CYCLIC DIGUANYLATE CYCLASE; PROTEIN ROEA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOFILM; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME METABOLISM; ENZYME REGULATION; ENZYME SYNTHESIS; EXTRACELLULAR MATRIX; FLAGELLUM; GENE MUTATION; GENE OVEREXPRESSION; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; NONHUMAN; OPEN READING FRAME; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 79952168685     PISSN: None     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00183-10     Document Type: Article

References (46)

1. Römling, U., M. Gomelsky, and M. Y. Galperin. 2005. c-di-GMP: the dawning of a novel bacterial signaling system. Mol. Microbiol. 57:629-639.
2. Miller, J. H. 1992. A short course in bacterial genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. 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.
4. Garcia, B., C. Latasa, C. Solano, F. Garcia-del Portillo, C. Gamazo, and I. Lasa. 2004. Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol. Microbiol. 54:264-277.
5. 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. 65:1474-1484.
6. Lim, B., S. Beyhan, J. Meir, and F. H. Yildiz. 2006. Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol. Microbiol. 60:331-348.
7. 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. 177:6223-6229.
8. 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. 60:1026-1043.
9. 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.
10. 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 di-guanylate cyclase output domain. Genes Dev. 18:715-727.
11. 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.
12. 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. U. S. A. 103:6712-6717.
13. Kulasekara, H., V. Lee, A. Brencic, N. Liberati, J. Urbach, S. Miyata, D. G. Lee, A. N. Neely, M. Hyodo, Y. Hayakawa, F. M. Ausubel, and S. Lory. 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.
14. 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.
15. Liberati, N. T., J. M. Urbach, S. Miyata, D. G. Lee, E. Drenkard, G. Wu, J. Villanueva, T. Wei, and F. M. Ausubel. 2006. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc. Natl. Acad. Sci. U. S. A. 103:2833-2838.
16. 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.
17. Kuchma, S. L., K. M. Brothers, J. H. Merritt, N. T. Liberati, F. M. Ausubel, and G. A. O'Toole. 2007. BifA, a cyclic-di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J. Bacteriol. 189:8165-8178.
18. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
19. Dunne, W. M., Jr. 2002. Bacterial adhesion: seen any good biofilms lately? Clin. Microbiol. Rev. 15:155-166.
20. Friedman, L., and R. Kolter. 2004. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol. Microbiol. 51:675-690.
21. Vasseur, P., I. Vallet-Gely, C. Soscia, S. Genin, and A. Filloux. 2005. The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology 151:985-997.
22. Zogaj, X., M. Nimtz, M. Rohde, W. Bokranz, and U. Romling. 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.
23. Merighi, M., V. T. Lee, M. Hyodo, Y. Hayakawa, and S. Lory. 2007. The second messenger bis-(3=-5=)-cyclic-GMP and its PilZ domaincontaining receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol. Microbiol. 65:876-895.
24. Caiazza, N. C., J. H. Merritt, K. M. Brothers, and G. A. O'Toole. 2007. Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J. Bacteriol. 189:3603-3612.
25. O'Toole, G. A. 2008. How Pseudomonas aeruginosa regulates surface behaviors. Microbe 3:65-71.
26. Toutain, C. M., N. C. Caiazza, M. E. Zegans, and G. A. O'Toole. 2007. Roles for the flagellar stators in biofilm formation by Pseudomonas aeruginosa. Res. Microbiol. 158:471-477.
27. Gitai, Z., N. Dye, and L. Shapiro. 2004. An actin-like gene can determine cell polarity in bacteria. Proc. Natl. Acad. Sci. U. S. A. 101:8643-8648.
28. Schuster, M., and E. P. Greenberg. 2006. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296:73-81.
29. Yahr, T. L., and M. C. Wolfgang. 2006. Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 62:631-640.
30. Hengge, R. 2009. Principles of c-di-GMP signaling in bacteria. Nat. Rev. Microbiol. 7:263-273.
31. Christen, M., H. D. Kulasekara, B. Christen, B. R. Kulasekara, L. R. Hoffman, and S. I. Miller. 2010. Asymmetrical distribution of the second messenger c-di-GMP upon bacterial cell division. Science 328:1295-1297.
32. 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.
33. Kohler, T., L. K. Curty, F. Barja, C. van Delden, and J. C. Pechere. 2000. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J. Bacteriol. 182:5990-5996.
34. Schweizer, H. P. 1992. Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker. Mol. Microbiol. 6:1195-1204.
35. Choi, K. H., J. B. Gaynor, K. G. White, C. Lopez, C. M. Bosio, R. R. Karkhoff-Schweizer, and H. P. Schweizer. 2005. A Tn7-based broadrange bacterial cloning and expression system. Nat. Methods 2:443-448.
36. Merritt, J. H., D. E. Kadouri, and G. A. O'Toole. 2005. Growing and analyzing static biofilms, p.1B.1.2. In R. Coico, T. Kowalik, J. Quarles, B. Stevenson, and R. Taylor (ed.), Current protocols in microbiology. John Wiley and Sons, Hoboken, NJ.
37. Toutain, C. M., M. E. Zegans, and G. A. O'Toole. 2005. Evidence for two flagellar stators and their role in the motility of Pseudomonas aeruginosa. J. Bacteriol. 187:771-777.
38. O'Toole, G. A., and R. Kolter. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis. Mol. Microbiol. 28:449-461.
39. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
40. Monds, R. D., P. D. Newell, R. H. Gross, and G. A. O'Toole. 2007. Phosphate-dependent 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.
41. Monds, R. D., P. D. Newell, J. C. Wagner, J. A. Schwartzman, W. Lu, J. D. Rabinowitz, and G. A. O'Toole. 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.
42. Shebelut, C. W., R. B. Jensen, and Z. Gitai. 2009. Growth conditions regulate the requirements for Caulobacter chromosome segregation. J. Bacteriol. 191:1097-1100.
43. Nunn, D., and S. Lory. 1993. Cleavage, methylation, and localization of the Pseudomonas aeruginosa export proteins XcpT, -U, -V, and -W. J. Bacteriol. 175:4375-4382.
44. Caiazza, N. C., and G. A. O'Toole. 2004. SadB is required for the transition from reversible to irreversible attachment during biofilm formation by Pseudomonas aeruginosa PA14. J. Bacteriol. 186:4476-4485.
45. Hinsa, S. M., and G. A. O'Toole. 2006. Biofilm formation by Pseudomonas fluorescens WCS365: a role for LapD. Microbiology 152:1375-1383.
46. MacEachran, D. P., S. Ye, J. M. Bomberger, D. A. Hogan, A. Swiatecka- Urban, B. A. Stanton, and G. A. O'Toole. 2007. The Pseudomonas aeruginosa secreted protein PA2934 decreases apical membrane expression of the cystic fibrosis transmembrane conductance regulator. Infect. Immun. 75:3902-3912.