Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation

Journal of Bacteriology

Volumn 186, Issue 14, 2004, Pages 4466-4475

  Jackson, Kara D ^a   Starkey, Melissa ^b   Kremer, Stefanie ^a   Parsek, Matthew R ^b   Wozniak, Daniel J ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; ANTIINFECTIVE AGENT; BIOCIDE; EXOPOLYSACCHARIDE; POLYSACCHARIDE;

ARTICLE; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIAL STRAIN; BIOFILM; BIOSYNTHESIS; CELL MOTILITY; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE CLUSTER; GENE DISRUPTION; GENE FUNCTION; GENE LOCUS; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSL GENE; SEQUENCE HOMOLOGY;

BACTERIAL PROTEINS; BIOFILMS; COLONY COUNT, MICROBIAL; GENE DELETION; GENE ORDER; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; LIPOPOLYSACCHARIDES; MOVEMENT; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; MUTATION; OPEN READING FRAMES; OPERON; POLYSACCHARIDES, BACTERIAL; PSEUDOMONAS AERUGINOSA;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PROKARYOTA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 3042856626     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.14.4466-4475.2004     Document Type: Article

References (65)

1. Arora, S. K., B. W. Ritchings, E. C. Almira, S. Lory, and R. Ramphal. 1998. The Pseudomonas aeruginosa flagellar cap protein, FliD, is responsible for mucin adhesion. Infect. Immun. 66:1000-1007.
2. Arora, S. K., B. W. Ritchings, E. C. Almira, S. Lory, and R. Ramphal. 1997. A transcriptional activator, FleQ, regulates mucin adhesion and flagellar gene expression in Pseudomonas aeruginosa in a cascade manner. J. Bacteriol. 179:5574-5581.
3. Baynham, P. J., and D. J. Wozniak. 1996. Identification and characterization of AlgZ, an AlgT-dependent DNA binding protein required for Pseudomonas aeruginosa algD transcription. Mol. Microbiol. 22:97-108.
4. Bjorn, M. J., O. R. Pavloskis, M. R. Thompson, and B. H. Iglewski. 1979. Production of exoenzyme S during Pseudomonas aeruginosa infections of burned mice. Infect. Immun. 24:837-842.
5. Christensen, B., C. Sternberg, J. B. Andersen, R. J. Palmer, A. T. Nielsen, M. Givskov, and S. Molin. 1999. Molecular tools to study biofilm physiology. Methods Enzymol. 310:20-42.
6. Christensen, G., W. Simpson, J. Younger, L. Baddour, F. Barrett, D. Melton, and E. Beachey. 1985. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for adherence of staphylococci to medical devices. J. Clin. Microbiol. 22:996-1006.
7. Costerton, J. W. 2001. Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends Microbiol. 9:50-52.
8. Costerton, J. W., Z. Lewandowski, D. E. Caldwell, D. R. Korber, and H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711-745.
9. Coyne, M. J., K. S. Russell, C. L. Coyle, and J. B. Goldberg. 1994. The Pseudomonas aeruginosa algC gene encodes phosphoglucomutase required for the synthesis of a complete lipopolysaccharide core. J. Bacteriol. 176: 3500-3507.
10. Danese, P. N., L. A. Pratt, and R. Kolter. 2000. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J. Bacteriol. 182:3593-3596.
11. Davies, D. G., M. R. Parsek, J. P. Pearson, B. H. Iglewski, J. W. Costerton, and E. P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295-298.
12. Evans, L. R., and A. Linker. 1973. Production and characterization of the slime polysaccharide of Pseudomonas aeruginosa. J. Bacteriol. 116:915-924.
13. Figurski, D., and D. R. Helinski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76:1648-1652.
14. Friedman, L., and R. Kolter. 2004. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol. Microbiol. 51:675-690.
15. Friedman, L., and R. Kolter. 2004. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J. Bacteriol. 186:4457-4465.
16. Goldberg, J. B., W. L. Gorman, J. L. Flynn, and D. E. Ohman. 1993. A mutation in algN permits transactivation of alginate production by algT in Pseudomonas species. J. Bacteriol. 175:1303-1308.
17. Govan, J. R. W., and V. Deretic. 1996. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60:539-574.
18. Guvener, Z. T., and L. L. McCarter. 2003. Multiple regulators control capsular polysaccharide production in Vibrio parahaemolyticus. J. Bacteriol. 185: 5431-5441.
19. Hentzer, M., G. M. Teitzel, G. J. Balzer, A. Heydorn, S. Molin, M. Givskov, and M. R. Parsek. 2001. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J. Bacteriol. 183:5395-5401.
20. Hitchcock, P. J., and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide types in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277.
21. Hoang, T. T., R. R. Karkhoff-Schweizer, A. J. Kutchma, and H. Schweizer. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: applications for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
22. Huang, B., C. B. Whitchurch, L. Croft, S. A. Beatson, and J. S. Mattick. 2000. A minimal tiling path cosmid library for functional analysis of the Pseudomonas aeruginosa PAO1 genome. Microb. Comp. Genomics 5:189-203.
23. Jensen, S. E., I. T. Facycz, and J. N. Campbell. 1980. Nutritional factors controlling exocellular protease production by Pseudomonas aeruginosa. J. Bacteriol. 144:844-847.
24. Kao, C. C., E. Barlow, and L. Sequeira. 1992. Extracellular polysaccharide is required for wild-type virulence of Pseudomonas solanacearum. J. Bacteriol. 174:1068-1071.
25. Klausen, M., A. Heydorn, P. Ragas, L. Lambertsen, A. Aaes-Jorgensen, S. Molin, and T. Tolker-Nielsen. 2003. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol. Microbiol. 48:1511-1524.
26. Kocharova, N., K. Hatano, A. Shaskov, Y. Knirel, N. Kochetkov, and G. Pier. 1989. The structure and serologic distribution of an extracellular neutral polysaccharide from Pseudomonas aeruginosa immunotype 3. J. Biol. Chem. 264:15569-15573.
27. Lam, J., R. Chan, K. Lam, and J. R. W. Costerton. 1980. Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Infect. Immun. 28:546-556.
28. Langille, S. E., and R. M. Weiner. 1998. Spatial and temporal deposition of Hyphomonas strain VP-6 capsules involved in biofilm formation. Appl. Environ. Microbiol. 64:2906-2913.
29. Liu, P. V. 1966. The roles of various fractions of Pseudomonas aeruginosa on its pathogenesis. II. Effects of lecithinase and protease. J. Infect. Dis. 116: 481-489.
30. Lyczak, J. B., C. Cannon, and G. B. Pier. 2000. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2:1051-1060.
31. Ma, S., U. Selvaraj, D. E. Ohman, R. Quarless, D. J. Hassett, and D. J. Wozniak. 1998. Phosphorylation-independent activity of the response regulators AlgB and AlgR in promoting alginate biosynthesis in mucoid Pseudomonas aeruginosa. J. Bacteriol. 180:956-968.
32. Mack, D., W. Fischer, A. Krokotsch, K. Leopold, R. Hartmann, H. Egge, and R. Laufs. 1996. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear β-1,6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol. 178:175-183.
33. Mah, T. C., and G. A. O'Toole. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9:34-39.
34. Matsukawa, M., and E. P. Greenberg. 2004. Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J. Bacteriol. 186:4449-4456.
35. McKenney, D., J. Hubner, E. Muller, Y. Wang, D. A. Goldmann, and G. Pier. 1998. The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide/adhesin. Infect. Immun. 66:4711-4720.
36. Nimtz, M., A. Mort, T. Domke, V. Wray, Y. Zhang, F. Qiu, D. Coplin, and K. Geider. 1996. Structure of amylovoran, the capsular exopolysaccharide from the fire blight pathogen Erwinia amylovora. Carbohydr. Res. 287:59-76.
37. Nivens, D. E., D. E. Ohman, J. Williams, and M. J. Franklin. 2001. Role of alginate and its O acetylation in formation of Pseudomonas aeruginosa microcolonies and biofilms. J. Bacteriol. 183:1047-1057.
38. Ohman, D. E., and A. M. Chakrabarty. 1981. Genetic mapping of chromosomal determinants for the production of the exopolysaccharide alginate in a Pseudomonas aeruginosa cystic fibrosis isolate. Infect. Immun. 33:142-148.
39. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
40. O'Toole, G., L. A. Pratt, P. I. Watnick, D. K. Newman, V. B. Weaver, and R. Kolter. 1999. Genetic approaches to study biofilms. Methods Enzymol. 310: 91-109.
41. O'Toole, G. A. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461.
42. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motilities are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
43. Pier, G. B. 1998. Pseudomonas aeruginosa: a key problem in cystic fibrosis. ASM News 6:339-347.
44. Rocchetta, H. L., L. L. Burrows, and J. S. Lam. 1999. Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev. 63:523-553.
45. Rocchetta, H. L., J. C. Pacan, and J. S. Lam. 1998. Synthesis of the A-band polysaccharide sugar D-rhamnose requires Rmd and WbpW: identification of multiple AlgA homologues, WbpW and ORF488, in Pseudomonas aeruginosa. Mol. Microbiol. 29:1419-1434.
46. Sauer, K., A. K. Camper, G. D. Ehrlich, J. W. Costerton, and D. G. Davies. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184:1140-1154.
47. Schaefer, A. L., E. P. Greenberg, and M. R. Parsek. 2001. Acylated homoserine lactone detection in Pseudomonas aeruginosa biofilms by radiolabel assay, p. 41-47. In R. J. Doyle (ed.), Microbial growth in biofilms, part A: developmental and molecular biological aspects. Academic Press, New York, N.Y.
48. Schweizer, H. P. 1993. Small broad-host-range gentamycin resistance cassettes for site-specific insertion and deletion mutagenesis. BioTechniques 15:831-833.
49. Schweizer, H. P., and T. T. Hoang. 1995. An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158: 15-22.
50. Semmler, A., C. B. Whitchurch, and J. S. Mattick. 1999. A re-examination of twitching motility in Pseudomonas aeruginosa. Microbiology 145:2863-2873.
51. Singh, P. K., A. L. Schaefer, M. R. Parsek, T. O. Moninger, M. J. Welsh, and E. P. Greenberg. 2000. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762-764.
52. Stephens, C. 2002. Microbiology: breaking down biofilms. Curr. Biol. 12: R132-R134.
53. Stewart, P. S., and J. W. Costerton. 2001. Antibiotic resistance of bacteria in biofilms. Lancet 358:135-138.
54. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. L. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, R. L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L. L. Brody, S. N. Coulter, K. R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G. K.-S. Wong, Z. Wu, I. T. Paulsenk, J. Reizer, M. H. Saier, R. E. W. Hancock, S. Lory, and M. V. Olson. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959-964.
55. Strevett, K., and G. Chen. 2003. Microbial surface thermodynamics and applications. Res. Microbiol. 154:329-335.
56. Tsuneda, S., H. Aikawa, H. Hayaski, A. Yuasa, and A. Hirata. 2003. Extracellular polymeric substances responsible for bacterial adhesion onto solid surface. FEMS Microbiol. Lett. 223:287-292.
57. Vieira, J., and J. Messing. 1991. New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene 100:189-194.
58. Whitchurch, C. B., T. Tolker-Nielsen, P. C. Ragas, and J. S. Mattick. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295: 1487.
59. Wolfgang, M. C., B. R. Kulasekara, X. Liang, D. Boyd, K. Wu, Q. Yang, C. G. Miyada, and S. Lory. 2003. Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 100:8484-8489.
60. Woolwine, S., and D. J. Wozniak. 1999. Identification of an Escherichia coli pepA homolog and its involvement in suppression of the algB phenotype in mucoid Pseudomonas aeruginosa. J. Bacteriol. 181:107-116.
61. Wozniak, D. J., A. B. Sprinkle, and P. J. Baynham. 2003. Control of Pseudomonas aeruginosa algZ expression by the alternative sigma factor AlgT. J. Bacteriol. 185:7297-7300.
62. Wozniak, D. J., T. J. O. Wyckoff, M. Starkey, R. Keyser, P. Azadi, G. A. O'Toole, and M. R. Parsek. 2003. Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms. Proc. Natl. Acad. Sci. USA 100:7907-7912.
63. Wyckoff, T. J. O., B. Thomas, D. J. Hassett, and D. J. Wozniak. 2002. Static growth of mucoid Pseudomonas aeruginosa selects for non-mucoid variants that have acquired flagellum-dependent motility. Microbiology 148:3423-3430.
64. Wyckoff, T. J. O., and D. J. Wozniak. 2001. Transcriptional analysis of genes involved in Pseudomonas aeruginosa biofilms. Methods Enzymol. 336:144-151.
65. Yildiz, F. H., and G. K. Schoolnik. 1999. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc. Natl. Acad. Sci. USA 96:4028-4033.