Pattern formation in Pseudomonas aeruginosa biofilms

Current Opinion in Microbiology

Volumn 11, Issue 6, 2008, Pages 560-566

  Parsek, Matthew R ^a   Tolker Nielsen, Tim ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSURFACTANT; DNA; POLYSACCHARIDE;

BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BACTERIUM COLONY; BIOFILM; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONFOCAL LASER MICROSCOPY; ENVIRONMENTAL PARAMETERS; GENE EXPRESSION; METABOLIC ACTIVATION; NONHUMAN; NUTRIENT; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; REVIEW;

BIOFILMS; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS AERUGINOSA;

EID: 56949084551     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2008.09.015     Document Type: Review

References (54)

1. Blair D.F. How bacteria sense and swim. Annu Rev Microbiol 49 (1995) 489-522
2. Golden J.W., and Yoon H.-S. Heterocyst formation in Anabaena. Curr Opin Microbiol 1 (1998) 623-629
3. Jelsbak L., and Søgaard-Andersen L. Pattern formation: fruiting body morphogenesis in Myxococcus xanthus. Curr Opin Microbiol 3 (2000) 637-642
4. Klausen M., Aaes-Jorgensen A., Molin S., and Tolker-Nielsen T. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol 50 (2003) 61-68
5. Singh P.K., Parsek M.R., Greenberg E.P., and Welsh M.J. A component of innate immunity prevents bacterial biofilm development. Nature 417 (2002) 552-555
6. Klausen M., Heydorn A., Ragas P., Lambertsen L., Aaes-Jorgensen A., Molin S., and Tolker-Nielsen T. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48 (2003) 1511-1524
7. Banin E., Vasil M.L., and Greenberg E.P. Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 102 (2005) 11076-11081
8. Shrout J.D., Chopp D.L., Just C.L., Hentzer M., Givskov M., and Parsek M.R. The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol Microbiol 62 (2006) 1264-1277. This paper provides evidence that the impact of quorum sensing on pattern formation in P. aeruginosa biofilms is nutritionally conditional, and thus explains previously conflicting reports on the role of quorum sensing in P. aeruginosa biofilm formation.
9. Landry R.M., An D., Hupp J.T., Singh P.K., and Parsek M.R. Mucin-Pseudomonas aeruginosa interactions promote biofilm formation and antibiotic resistance. Mol Microbiol 59 (2006) 142-151
10. Thompson L.S., Webb J.S., Rice S.A., and Kjelleberg S. The alternative sigma factor RpoN regulates the quorum sensing gene rhlI in Pseudomonas aeruginosa. FEMS Microbiol Lett 220 (2003) 187-195
11. Monds R.D., Newell P.D., Gross R.H., and O'Toole G.A. 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 (2007) 656-679
12. Davies D.G., Parsek M.R., Pearson J.P., Iglewski B.H., Costerton J.W., and Greenberg E.P. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280 (1998) 295-298
13. Heydorn A., Ersbøll B., Kato J., Hentzer M., Parsek M., Tolker-Nielsen T., Givskov M., and Molin S. Statistical analysis of Pseudomonas aeruginosa biofilm development: impact of mutations in genes involved in twitching motility, cell-to-cell signaling, and stationary-phase sigma factor expression. Appl Environ Microbiol 68 (2002) 2008-2017
14. Purevdorj-Gage B., Costerton J.W., and Stoodley P. Influence of hydrodynamics and cell signaling on the structure and behavior of Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 68 (2002) 4457-4464
15. Hentzer M., Riedel K., Rasmussen T.B., Heydorn A., Andersen J.B., Parsek M.R., Rice S.A., Eberl L., Molin S., Høiby N., et al. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148 (2002) 87-102
16. Patriquin G.M., Banin E., Gilmour C., Tuchman R., Greenberg E.P., and Poole K. Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 190 (2008) 662-671
17. Haagensen J.A., Klausen M., Ernst R.K., Miller S.I., Folkesson A., Tolker-Nielsen T., and Molin S. Differentiation and distribution of colistin- and sodium dodecyl sulfate-tolerant cells in Pseudomonas aeruginosa biofilms. J Bacteriol 189 (2007) 28-37
18. Barken K.B., Pamp S.J., Yang L., Gjermansen M., Bertrand J.J., Klausen M., Givskov M., Whitchurch C.B., Engel J.N., and Tolker-Nielsen T. Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ Microbiol 10 (2008) 2331-2343. This study provides evidence that type IV pili, flagella, and extracellular DNA all play roles in cell migration dependent pattern formation in P. aeruginosa biofilms.
19. Whitchurch C.B., Tolker-Nielsen T., Ragas P.C., and Mattick J.S. Extracellular DNA required for bacterial biofilm formation. Science 295 (2002) 1487
20. Allesen-Holm M., Barken K.B., Yang L., Klausen M., Webb J.S., Kjelleberg S., Molin S., Givskov M., and Tolker-Nielsen T. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59 (2006) 1114-1128. This study shows that the generation of large amounts of extracellular DNA occurs at distinct locations in P. aeruginosa biofilms and depends on the PQS quorum sensing system.
21. Köhler T., Curty L.K., Barja F., van Delden C., and Pechere J.C. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182 (2000) 5990-5996
22. Pamp S.J., and Tolker-Nielsen T. Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J Bacteriol 189 (2007) 2531-2539
23. Hickman J.W., Tifrea D.F., and Harwood C.S. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102 (2005) 14422-14427
24. Merritt J.H., Brothers K.M., Kuchma S.L., and O'Toole G.A. SadC reciprocally influences biofilm formation and swarming motility via modulation of exopolysaccharide production and flagellar function. J Bacteriol 189 (2007) 8154-8164
25. Kuchma S.L., Brothers K.M., Merritt J.H., Liberati N.T., Ausubel F.M., and O'Toole G.A. BifA, a cyclic-Di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189 (2007) 8165-8178
26. Kearns D.B., Robinson J., and Shimkets L.J. Pseudomonas aeruginosa exhibits directed twitching motility up phosphatidylethanolamine gradients. J Bacteriol 183 (2001) 763-767
27. Tremblay J., Richardson A.P., Lépine F., and Déziel E. Self-produced extracellular stimuli modulate the Pseudomonas aeruginosa swarming motility behaviour. Environ Microbiol 9 (2007) 2622-2630
28. Pamp S.J., Gjermansen M., and Tolker-Nielsen T. The biofilm matrix-a sticky framework. In: Kjelleberg S., and Givskov M. (Eds). Bacterial Biofilm Formation and Adaptation (2007), Horizon BioSci 37-69
29. Lu A., Cho K., Black W.P., Duan X.Y., Lux R., Yang Z., Kaplan H.B., Zusman D.R., and Shi W. Exopolysaccharide biosynthesis genes required for social motility in Myxococcus xanthus. Mol Microbiol 55 (2005) 206-220
30. Stapper A.P., Narasimhan G., Ohman D.E., Barakat J., Hentzer M., Molin S., Kharazmi A., Høiby N., and Mathee K. Alginate production affects Pseudomonas aeruginosa biofilm development and architecture, but is not essential for biofilm formation. J Med Microbiol 53 (2004) 679-690
31. Govan J.R.W., and Deretic V. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60 (1996) 539-574
32. Wozniak D.J., Wyckoff T.J.O., Starkey M., Keyser R., Azadi P., O'Toole G.A., and Parsek M.R. Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms. Proc Natl Acad Sci U S A 100 (2003) 7907-7912
33. Worlitzsch D., Tarran R., Ulrich M., Schwab U., Cekici A., Meyer K., Birrer P., Bellon G., Berger J., Weiss T., et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109 (2002) 317-325
34. Sarkisova S., Patrauchan M.A., Berglund D., Nivens D.E., and Franklin M.J. Calcium-induced virulence factors associated with the extracellular matrix of mucoid Pseudomonas aeruginosa biofilms. J Bacteriol 187 (2005) 4327-4337
35. Hentzer M., Teitzel G.M., Balzer G.J., Heydorn A., Molin S., Givskov M., and Parsek M.R. Alginate over-production affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 183 (2001) 5395-5401
36. Friedman L., and Kolter R. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aerguinosa biofilm matrix. J Bacteriol 186 (2004) 4457-4465
37. Jackson K.D., Starkey M., Kremer S., Parsek M.R., and Wozniak D.J. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186 (2004) 4466-4475
38. Matsukawa M., and Greenberg E.P. Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J Bacteriol 186 (2004) 4449-4456
39. Ma L., Lu H., Sprinkle A., Parsek M.R., and Wozniak D.J. Pseudomonas aeruginosa Psl is a galactose- and mannose-rich exopolysaccharide. J Bacteriol 189 (2007) 8353-8356
40. Ma L., Jackson K.D., Landry R.M., Parsek M.R., and Wozniak D.J. Analysis of Pseudomonas aeruginosa conditional psl variants reveals roles for the psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J Bacteriol 188 (2006) 8213-8221. Through the use of a psl-inducible P. aeruginosa strain, it was shown that expression of the psl operon is required to maintain biofilm structure at steps postattachment.
41. Haussler S., Ziegler I., Lottel A., Gotz Fv, Rohde M., Wehmhohner D., Saravanamuthu S., Tummler B., and Steinmetz I. Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J Med Microbiol 52 (2003) 295-301
42. Smith E.E., Buckley D.G., Wu Z., Saenphimmachak C., Hoffman L.R., D'Argenio D.A., Miller S.I., Ramsey B.W., Speert D.P., Moskowitz S.M., et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A 103 (2006) 8487-8492. This study shows that virulence factors that are required for the initiation of acute infections often are selected against during chronic infections.
43. Kirisits M.J., Prost L., Starkey M., and Parsek M.R. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71 (2005) 4809-4821
44. Friedman L., and Kolter R. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51 (2004) 675-690
45. Vasseur P., Vallet-Gely I., Soscia C., Genin S., and Filloux A. The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology 151 (2005) 985-997
46. Aas F.E., Wolfgang M., Frye S., Dunham S., Lovold C., and Koomey M. Competence for natural transformation in Neisseria gonorrhoeae: components of DNA binding and uptake linked to type IV pilus expression. Mol Microbiol 46 (2002) 749-760
47. van Schaik E.J., Giltner C.L., Audette G.F., Keizer D.W., Bautista D.L., Slupsky C.M., Sykes B.D., and Irvin R.T. DNA binding: a novel function of Pseudomonas aeruginosa type IV pili. J Bacteriol 187 (2005) 1455-1464
48. Yang L., Barken K.B., Skindersoe M.E., Christensen A.B., Givskov M., and Tolker-Nielsen T. Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153 (2007) 1318-1328
49. Pamp S.J., Gjermansen M., Johansen H.K., and Tolker-Nielsen T. Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes. Mol Microbiol 68 (2008) 223-240. This study highlights the role of physiological heterogeneity in the ability of P. aeruginosa biofilms to tolerate antimicrobial treatment.
50. Lequette Y., and Greenberg E.P. Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J Bacteriol 187 (2005) 37-44
51. Kaneko Y., Thoendel M., Olakanmi O., Britigan B.E., and Singh P.K. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest 117 (2007) 877-888. This study provides evidence that gallium can be used as a potent antimicrobial targeting P. aeruginosa biofilm-based infections.
52. Lenz A.P., Williamson K.S., Pitts B., Stewart P.S., and Franklin M.J. Localized gene expression in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 74 (2008) 4463-4471. This study uses laser capture microdissection microscopy combined with multiplex quantitative real-time reverse transcriptase PCR to isolate and quantify RNA transcripts from small groups of cells at spatially resolved sites within P. aeruginosa biofilms.
53. Bjarnsholt T., Jensen P.O., Burmolle M., Hentzer M., Haagensen J.A., Hougen H.P., Calum H., Madsen K.G., Moser C., Molin S., et al. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151 (2005) 373-383
54. Banin E., Brady K.M., and Greenberg E.P. Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl Environ Microbiol 72 (2006) 2064-2069