Biofilms and type III secretion are not mutually exclusive in Pseudomonas aeruginosa

Microbiology

Volumn 155, Issue 3, 2009, Pages 687-698

  Mikkelsen, H ^a   Bond, N J ^a   Skindersoe, M E ^c   Givskov, M ^b   Lilley, K S ^a   Welch, M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c ChemoMetec A/S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOFILM; CONTROLLED STUDY; DOWN REGULATION; GENE ACTIVATION; GENE EXPRESSION PROFILING; GENETIC VARIABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLANKTON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PSEUDOMONAS AERUGINOSA; TRANSCRIPTOMICS; TYPE III SECRETION SYSTEM; UPREGULATION; BIOSYNTHESIS; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEIN; BACTERIAL RNA; VIRULENCE FACTOR;

BACTERIAL PROTEINS; BIOFILMS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PSEUDOMONAS AERUGINOSA; RNA, BACTERIAL; VIRULENCE FACTORS;

EID: 64049084921     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.025551-0     Document Type: Article

References (68)

1. Alvarez-Ortega, C. & Harwood, C. S. (2007). Responses of Pseudomonas aeruginosa to low oxygen indicate that growth in the cystic fibrosis lung is by aerobic respiration. Mol Microbiol 65, 153-165.
2. Ando, H., Abe, H., Sugimoto, N. & Tobe, T. (2007). Maturation of functional type III secretion machinery by activation of anaerobic respiration in enterohaemorrhagic Escherichia coli. Microbiology 153, 464-473.
3. Augustin, D. K., Song, Y., Baek, M. S., Sawa, Y., Singh, G., Taylor, B., Rubio-Mills, A., Flanagan, J. L., Wiener-Kronish, J. P. & Lynch, S. V. (2007). Presence or absence of lipopolysaccharide O antigens affects type III secretion by Pseudomonas aeruginosa. J Bacteriol 189, 2203-2209.
4. Bleves, S., Soscia, C., Nogueira-Orlandi, P., Lazdunski, A. & Filloux, A. (2005). Quorum sensing negatively controls type III secretion regulon expression in Pseudomonas aeruginosa PAO1. J Bacteriol 187, 3898-3902.
5. Boes, N., Schreiber, K., Hartig, E., Jaensch, L. & Schobert, M. (2006). The Pseudomonas aeruginosa universal stress protein PA4352 is essential for surviving anaerobic energy stress. J Bacteriol 188, 6529-6538.
6. Collins, F. S. (1992). Cystic fibrosis: molecular biology and therapeutic implications. Science 256, 774-779.
7. Corbett, M., Virtue, S., Bell, K., Birch, P., Burr, T., Hyman, L., Lilley, K., Poock, S., Toth, I. & Salmond, G. (2005). Identification of a new quorum-sensing-controlled virulence factor in Erwinia carotovora subsp. atroseptica secreted via the type II targeting pathway. Mol Plant Microbe Interact 18, 334-342.
8. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. (1999). Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322.
9. 2+ and host cell contact proceeds through two distinct signaling pathways. Infect Immun 74, 3334-3341.
10. Drenkard, E. (2003). Antimicrobial resistance of Pseudomonas aeruginosa biofilms. Microbes Infect 5, 1213-1219.
11. Filiatrault, M. J., Wagner, V. E., Bushnell, D., Haidaris, C. G., Iglewski, B. H. & Passador, L. (2005). Effect of anaerobiosis and nitrate on gene expression in Pseudomonas aeruginosa. Infect Immun 73, 3764-3772.
12. Filiatrault, M. J., Picardo, K. F., Ngai, H., Passador, L. & Iglewski, B. H. (2006). Identification of Pseudomonas aeruginosa genes involved in virulence and anaerobic growth. Infect Immun 74, 4237-4245.
13. Filloux, A., Hachani, A. & Bleves, S. (2008). The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154, 1570-1583.
14. Furukawa, S., Kuchma, S. L. & O'Toole, G. A. (2006). Keeping their options open: acute versus persistent infections. J Bacteriol 188, 1211-1217.
15. Goodman, A. L., Kulasekara, B., Rietsch, A., Boyd, D., Smith, R. S. & Lory, S. (2004). A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7, 745-754.
16. Hancock, R. E. & Speert, D. P. (2000). Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug Resist Updat 3, 247-255.
17. Hauser, A. R., Cobb, E., Bodi, M., Mariscal, D., Valles, J., Engel, J. N. & Rello, J. (2002). Type III protein secretion is associated with poor clinical outcomes in patients with ventilator-associated pneumonia caused by Pseudomonas aeruginosa. Crit Care Med 30, 521-528.
18. Hentzer, M., Wu, H., Andersen, J. B., Riedel, K., Rasmussen, T. B., Bagge, N., Kumar, N., Schembri, M. A., Song, Z. & other authors (2003). Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22, 3803-3815.
19. Hentzer, M., Eberl, L. & Givskov, M. (2005). Transcriptome analysis of Pseudomonas aeruginosa biofilm development: anaerobic respiration and iron limitation. Biofilms 2, 37-61.
20. Hogardt, M., Roeder, M., Schreff, A. M., Eberl, L. & Heesemann, J. (2004). Expression of Pseudomonas aeruginosa exoS is controlled by quorum sensing and RpoS. Microbiology 150, 843-851.
21. Hornef, M. W., Roggenkamp, A., Geiger, A. M., Hogardt, M., Jacobi, C. A. & Heesemann, J. (2000). Triggering the ExoS regulon of Pseudomonas aeruginosa: a GFP-reporter analysis of exoenzyme (Exo) S, ExoT and ExoU synthesis. Microb Pathog 29, 329-343.
22. Jelsbak, L., Johansen, H. K., Frost, A. L., Thogersen, R., Thomsen, L. E., Ciofu, O., Yang, L., Haagensen, J. A., Hoiby, N. & Molin, S. (2007). Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients. Infect Immun 75, 2214-2224.
23. Kirisits, M. J., Margolis, J. J., Purevdorj-Gage, B. L., Vaughan, B., Chopp, D. L., Stoodley, P. & Parsek, M. R. (2007). Influence of the hydrodynamic environment on quorum sensing in Pseudomonas aeruginosa biofilms. J Bacteriol 189, 8357-8360.
24. Klausen, M., Heydorn, A., Ragas, P., Lambertsen, L., Aaes-Jorgensen, A., Molin, S. & Tolker-Nielsen, T. (2003). Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48, 1511-1524.
25. 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.
26. Lam, J., Chan, R., Lam, K. & Costerton, J. W. (1980). Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Infect Immun 28, 546-556.
27. Lee, B., Haagensen, J. A., Ciofu, O., Andersen, J. B., Hoiby, N. & Molin, S. (2005). Heterogeneity of biofilms formed by nonmucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. J Clin Microbiol 43, 5247-5255
28. Lee, D. G., Urbach, J. M., Wu, G., Liberati, N. T., Feinbaum, R. L., Miyata, S., Diggins, L. T., He, J., Saucier, M. & other authors (2006). Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol 7, R90.
29. Lyczak, J. B., Cannon, C. L. & Pier, G. B. (2000). Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2, 1051-1060.
30. Lyczak, J. B., Cannon, C. L. & Pier, G. B. (2002). Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15, 194-222.
31. Ma, Q., Zhai, Y., Schneider, J. C., Ramseier, T. M. & Saier, M. H., Jr (2003). Protein secretion systems of Pseudomonas aeruginosa and P. fluorescens. Biochim Biophys Acta 1611, 223-233.
32. Ma, L., Jackson, K. D., Landry, R. M., Parsek, M. R. & Wozniak, D. J. (2006). Analysis of Pseudomonas aeruginosa conditional psl variants reveals roles for the Psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J Bacteriol 188, 8213-8221.
33. Ma, L., Lu, H., Sprinkle, A., Parsek, M. R. & Wozniak, D. J. (2007). Pseudomonas aeruginosa Psl is a galactose- and mannose-rich exopolysaccharide. J Bacteriol 189, 8353-8356.
34. Matz, C., Moreno, A. M., Alhede, M., Manefield, M., Hauser, A. R., Givskov, M. & Kjelleberg, S. (2008). Pseudomonas aeruginosa uses type III secretion system to kill biofilm-associated amoebae. ISME J 2, 843-852.
35. Mikkelsen, H., Duck, Z., Lilley, K. S. & Welch, M. (2007). Interrelationships between colonies, biofilms, and planktonic cells of Pseudomonas aeruginosa. J Bacteriol 189, 2411-2416.
36. Mougous, J. D., Cuff, M. E., Raunser, S., Shen, A., Zhou, M., Gifford, C. A., Goodman, A. L., Joachimiak, G., Ordoñez, C. L. & other authors (2006). A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312, 1526-1530.
37. Palmer, K. L., Mashburn, L. M., Singh, P. K. & Whiteley, M. (2005). Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology. J Bacteriol 187, 5267-5277.
38. Palmer, K. L., Brown, S. A. & Whiteley, M. (2007). Membrane-bound nitrate reductase is required for anaerobic growth in cystic fibrosis sputum. J Bacteriol 189, 4449-4455.
39. Parsek, M. R. & Singh, P. K. (2003). Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 57, 677-701.
40. Platt, M. D., Schurr, M. J., Sauer, K., Vazquez, G., Kukavica-Ibrulj, I., Potvin, E., Levesque, R. C., Fedynak, A., Brinkman, F. S. & other authors (2008). Proteomic, microarray, and signature-tagged mutagenesis analyses of anaerobic Pseudomonas aeruginosa at pH 6.5, likely representing chronic, late-stage cystic fibrosis airway conditions. J Bacteriol 190, 2739-2758.
41. Rietsch, A. & Mekalanos, J. J. (2006). Metabolic regulation of type III secretion gene expression in Pseudomonas aeruginosa. Mol Microbiol 59, 807-820.
42. Rowntree, R. K. & Harris, A. (2003). The phenotypic consequences of CFTR mutations. Ann Hum Genet 67, 471-485.
43. Roy-Burman, A., Savel, R. H., Racine, S., Swanson, B. L., Revadigar, N. S., Fujimoto, J., Sawa, T., Frank, D. W. & Wiener-Kronish, J. P. (2001). Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections. J Infect Dis 183, 1767-1774.
44. Rumbaugh, K. P., Griswold, J. A. & Hamood, A. N. (2000). The role of quorum sensing in the in vivo virulence of Pseudomonas aeruginosa. Microbes Infect 2, 1721-1731.
45. Sakuragi, Y. & Kolter, R. (2007). Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J Bacteriol 189, 5383-5386.
46. Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W. & Davies, D. G. (2002). Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184, 1140-1154.
47. Schaber, J. A., Triffo, W. J., Suh, S. J., Oliver, J. W., Hastert, M. C., Griswold, J. A., Auer, M., Hamood, A. N. & Rumbaugh, K. P. (2007). Pseudomonas aeruginosa forms biofilms in acute infection independent of cell-to-cell signaling. Infect Immun 75, 3715-3721.
48. Schreiber, K., Boes, N., Eschbach, M., Jaensch, L., Wehland, J., Bjarnsholt, T., Givskov, M., Hentzer, M. & Schobert, M. (2006). Anaerobic survival of Pseudomonas aeruginosa by pyruvate fermentation requires an Usp-type stress protein. J Bacteriol 188, 659-668.
49. Schuster, M., Lostroh, C. P., Ogi, T. & Greenberg, E. P. (2003). Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185, 2066-2079.
50. Singh, P. K., Parsek, M. R., Greenberg, E. P. & Welsh, M. J. (2002). A component of innate immunity prevents bacterial biofilm development. Nature 417, 552-555.
51. 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. & other authors (2006). Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A 103, 8487-8492.
52. Smyth, G. K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3
53. Somerville, G., Mikoryak, C. A. & Reitzer, L. (1999). Physiological characterization of Pseudomonas aeruginosa during exotoxin A synthesis: glutamate, iron limitation, and aconitase activity. J Bacteriol 181, 1072-1078.
54. Spoering, A. L. & Lewis, K. (2001). Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 183, 6746-6751.
55. Van Alst, N. E., Picardo, K. F., Iglewski, B. H. & Haidaris, C. G. (2007). Nitrate sensing and metabolism modulate motility, biofilm formation, and virulence in Pseudomonas aeruginosa. Infect Immun 75, 3780-3790.
56. Van Delden, C. (2004). Virulence Factors in Pseudomonas aeruginosa. New York: Kluwer Academic/Plenum Publishers.
57. Ventre, I., Goodman, A. L., Vallet-Gely, I., Vasseur, P., Soscia, C., Molin, S., Bleves, S., Lazdunski, A., Lory, S. & Filloux, A. (2006). Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci U S A 103, 171-176.
58. Wagner, V. E., Bushnell, D., Passador, L., Brooks, A. I. & Iglewski, B. H. (2003). Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 185, 2080-2095.
59. Waite, R. D., Papakonstantinopoulou, A., Littler, E. & Curtis, M. A. (2005). Transcriptome analysis of Pseudomonas aeruginosa growth: comparison of gene expression in planktonic cultures and developing and mature biofilms. J Bacteriol 187, 6571-6576.
60. Waite, R. D., Paccanaro, A., Papakonstantinopoulou, A., Hurst, J. M., Saqi, M., Littler, E. & Curtis, M. A. (2006). Clustering of Pseudomonas aeruginosa transcriptomes from planktonic cultures, developing and mature biofilms reveals distinct expression profiles. BMC Genomics 7, 162.
61. Whiteley, M., Bangera, M. G., Bumgarner, R. E., Parsek, M. R., Teitzel, G. M., Lory, S. & Greenberg, E. P. (2001). Gene expression in Pseudomonas aeruginosa biofilms. Nature 413, 860-864.
62. Williams, H. D., Zlosnik, J. E. & Ryall, B. (2007). Oxygen, cyanide and energy generation in the cystic fibrosis pathogen Pseudomonas aeruginosa. Adv Microb Physiol 52, 1-71.
63. Worlitzsch, D., Tarran, R., Ulrich, M., Schwab, U., Cekici, A., Meyer, K. C., Birrer, P., Bellon, G., Berger, J. & other authors (2002). Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109, 317-325.
64. Wu, M., Guina, T., Brittnacher, M., Nguyen, H., Eng, J. & Miller, S. I. (2005). The Pseudomonas aeruginosa proteome during anaerobic growth. J Bacteriol 187, 8185-8190.
65. Yahr, T. L. & Greenberg, E. P. (2004). The genetic basis for the commitment to chronic versus acute infection in Pseudomonas aeruginosa. Mol Cell 16, 497-498.
66. Yang, L., Haagensen, J. A., Jelsbak, L., Johansen, H. K., Sternberg, C., Hoiby, N. & Molin, S. (2008). In situ growth rates and biofilm development of Pseudomonas aeruginosa populations in chronic lung infections. J Bacteriol 190, 2767-2776.
67. Yoon, S. S., Hennigan, R. F., Hilliard, G. M., Ochsner, U. A., Parvatiyar, K., Kamani, M. C., Allen, H. L., DeKievit, T. R., Gardner, P. R. & other authors (2002). Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev Cell 3, 593-603.
68. Zumft, W. G. (2004). Denitrification by pseudomonads: control and assembly processes. In Pseudomonas; Biosynthesis of Macromolecules and Molecular Metabolism, pp. 193-227. Edited by J. L. Ramos. New York: Kluwer Academic/Plenum Publishers.