Evolution of Pseudomonas aeruginosa Pathogenicity: From Acute to Chronic Infections

Antonio Oliver; Ana Mena; María D. Maciá

doi:10.1128/9781555815639.ch36

Chapter 36 : Evolution of Pseudomonas aeruginosa Pathogenicity: From Acute to Chronic Infections

Authors: Antonio Oliver¹, Ana Mena², María D. Maciá³

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Affiliations: 1: Servicio de Microbiología, Hospital Son Dureta, Palma de Mallorca, Spain; 2: Servicio de Microbiología, Hospital Son Dureta, Palma de Mallorca, Spain; 3: Servicio de Microbiología, Hospital Son Dureta, Palma de Mallorca, Spain

Content Type: Monograph

Publication Year: 2008

Category: Fungi and Fungal Pathogenesis; Bacterial Pathogenesis

Book DOI: 10.1128/9781555815639

Chapter DOI: 10.1128/9781555815639.ch36

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Abstract:

This chapter focuses on the analysis of the factors driving the evolutive transition of Pseudomonas aeruginosa populations from the acute to the chronic infection scenario and the underlying consequences in terms of virulence, persistence (adaptation), and antimicrobial resistance. The transcendence of P. aeruginosa biofilms in the persistence of chronic infections demonstrates both its increased resistance to the host defense mechanisms, including the mechanical clearance and that mediated by complement, antibodies, or phagocytes, and its increased resistance to the antimicrobials action, reported to be over 100-fold higher than in planktonic cells. A nice example of how mutator cells can be amplified in a bacterial population by hitchhiking with adapting mutations was provided by Mao et al. In this work it was found that when E. coli populations are subjected to a one-step mutation selection process, hypermutable variants were amplified in the population from approximately 0.001 to 0.5%, and when they were subjected to two consecutive steps of mutants selection, the amplification reached 25 to 100%. A link between P. aeruginosa hypermutation and antibiotic resistance has also been documented for other chronic infections such as those occurring in patients with bronchiectasis or chronic obstructive pulmonary disease (COPD). The establishment of P. aeruginosa chronic infections is the result of a complex adaptation process that includes both physiological and genetic changes, ultimately leading to the selection of highly persistent bacterial populations.

Citation: Oliver A, Mena A, Maciá M. 2008. Evolution of Pseudomonas aeruginosa Pathogenicity: From Acute to Chronic Infections, p 433-444. In Baquero F, Nombela C, Cassell G, Gutiérrez-Fuentes J (ed), Evolutionary Biology of Bacterial and Fungal Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815639.ch36

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Evolution of Pseudomonas aeruginosa Pathogenicity: From Acute to Chronic Infections

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/content/10.1128/9781555815639.ch36.ch36fig01

Figure 1.

Model of the sequential adaptive process for long-term persistence taking place in P. aeruginosa chronic lung infections.

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Figure 1.

Model of the sequential adaptive process for long-term persistence taking place in P. aeruginosa chronic lung infections.

/content/10.1128/9781555815639.ch36.ch36fig02

Figure 2.

(A) Imipenem (8 μg/ml) killing-kinetics for strain PAO1 and its hypermutable derivative PAOΔmutS. PAO1 is represented by dashed lines, and PAOΔmutS by full lines, squares indicate strains grown in Müller-Hinton broth without antibiotic, and diamonds indicate strains grown in 8 μg/ml imipenem Müller-Hinton broth. Displayed data were obtained from Ventre et al., 2006. (B) Imipenem Etest and disk diffusion susceptibility tests of strains PAO1 and PAOΔmutS showing the presence of RMS for the hypermutable strain.

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Figure 2.

References

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1. Alonso, A.,, F. Rojo, and, J. L. Martinez. 1999. Environmental and clinical isolates of Pseudomonas aeruginosa show pathogenic and biodegradative properties irrespective of their origin. Environ. Microbiol. 1:421–430.

2. Bagge, N.,, M. Morten,, J. B. Andersen,, O. Ciofu,, M. Givskov, and, N. Hoiby. 2004. Dynamics and spatial distribution of β-lactamase expression in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 48:1168–1174.

3. Barbieri, J. T., and, J. Sun. 2004. Pseudomonas aeruginosa ExoS and ExoT. Rev. Physiol. Biochem. Pharmacol. 152:79–92.

4. Blazquez, J. 2003. Hypermutation as a factor contributing to the acquisition of antimicrobial resistance. Clin. Infect. Dis. 37:1201–1209.

5. Boles, B. R.,, M. Thoendel, and, P. K. Singh. 2004. Self-generated diversity produces “insurance effects” in biofilm communities. Proc. Natl. Acad. Sci. USA 101:16630–16635.

6. Bragonzi, A.,, D. Worlitzsch,, G. B. Pier,, P. Timpert,, M. Ulrich,, M. Hentzer,, J. B. Andersen,, M. Givskov,, M. Conese, and, G. Doring. 2005. Nonmucoid Pseudomonas aeruginosa expresses alginate in the lungs of patients with cystic fibrosis and in a mouse model. J. Infect. Dis. 192:410–419.

7. Chopra, I.,, A. J. O’Neill, and, K. Miller. 2003. The role of mutators in the emergence of antibiotic-resistant bacteria. Drug Resist. Updates 6:137–145.

8. Ciofu, O.,, B. Riis,, P. Pressler,, H. P. Poulsen, and, N. Hoiby. 2005. Ocurrence of hypermutable Pseudomonas aeruginosa in cystic fibrosis patients is associated with the oxidative stress caused by chronic lung inflamation. Antimicrob. Agents Chemother. 49:2276–2282.

9. Comolli, J. C.,, A. R. Hauser,, L. Waite,, C. B. Whitchurch,, J. S. Mattick, and, J. N. Engel. 1999. Pseudomonas aeruginosa gene products PilT and PilU are required for cytotoxicity in vitro and virulence in a mouse model of acute pneumonia. Infect. Immun. 67:3625–3630.

10. Costerton, J. W.,, P. S. Stewart, and, E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322.

11. Cox, E. C., and, T. C. Gibson. 1974. Selection for high mutation rates in chemostats. Genetics 77:169–184.

12. Curran, B.,, D. Jonas,, H. Grundmann,, T. Pitt, and, C. G. Dowson. 2004. Development of a multilocus sequence typing scheme for the oportunistic pathogen Pseudomonas aeruginosa. J. Clin. Microbiol. 42:5644–5649.

13. Davies, D. G.,, M. R. Parsek,, J. P. Pearson,, B. H. Iglewski,, J. W. Costerton, and, E. P. Greeberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–297.

14. Ernst, R. K.,, E. C. Yi,, L. Guo,, K. B. Lim,, J. L. Burns,, M. Hackett, and, S. I. Miller. 1999. Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aeruginosa. Science 286:1561–1565.

15. Evans, S. A.,, S. M. Turner,, B. J. Bosch,, C. C. Hardy, and, M. A. Woodhead. 1996. Lung function in bronchiectasis: the influence of Pseudomonas aeruginosa. Eur. Respir. J. 9:1601–1604.

16. Feldman, M.,, R. Bryan,, S. Rajan,, L. Scheffler,, S. Brunnert,, H. Tang, and, A. Prince. 1998. Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect. Immun. 66:43–51.

17. Funchain, P.,, A. Yeung,, J. Stewart,, W. M. Clendenin, and, J. H. Miller. 2001. Amplification of mutator cells in a population as a result of horizontal transfer. J. Bacteriol. 183:3737–3741.

18. Gibson, R. L.,, J. L. Burns, and, B. W. Rammsey. 2003. Pathophysiology and management of pulmonary infections in cystic fibrosis. Am. J. Respir. Crit. Care Med. 168:918–951.

19. Giraud, A.,, I. Matic,, O. Tenaillon,, A. Clara,, M. Radman,, M. Fons, et al. 2001. Cost and benfits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science 291:2606–2608.

20. Goldman, M. J.,, G. M. Anderson,, E. D. Stolzenberg,, U. P. Kari,, M. Zasloff, and, J. M. Wilson. 1997. Human β-defensin-1 is a salt sensitive antibiotic in lung that is inactivated in cystic fibrosis. Cell 88:553–560.

21. Govan, J. R., and, V. Deretic. 1996. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60:539–574.

22. Gutiérrez, O.,, C. Juan,, J. L. Pérez, and, A. Oliver. 2004. Lack of association between hypermutation and antibiotic resistance development in Pseudomonas aeruginosa isolates from intensive care unit patients. Antimicrob. Agents Chemother. 48:3573–3575.

23. Hanage, W. P.,, E. J. Feil,, A. B. Brueggemann, and, B. G. Spratt. 2004. Multilocus sequence typing: strain characterization, population biology, and patterns of evolutionary descent. In D. H. Persing,, F. C. Tenover,, J. Versalovic,, Y. W. Tang,, E. R. Unger,, D. A. Relman, and, T. J. White (ed.), Molecular Microbiology: Diagnostic Principles and Practise. Washington, DC.

24. Hancock, R. E.,, L. M. Mutharia,, L. Chan,, R. P. Darveau,, D. P. Speert, and, G. B. Pier. 1983. Pseudomonas aeruginosa isolates from patients with cystic fibrosis: a class of serum-sensitive, nontypable strains defficient in lipopolysaccharide O side chains. Infect. Immun. 42:170–177.

25. Hatch, R. A., and, N. L. Schiller. 1998. Alginate lyase promotes diffusion of aminoglycosides through the extracellular polysaccharide of mucoid Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 42:974–977.

26. Häußler, S.,, B. Tümmler,, H. Weissbrodt,, M. Rohde, and, I. Steinmetz. 1999. Small colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin. Infect. Dis. 29:621–625.

27. Häußler, S.,, I. Ziegler,, A. Löttel,, F. V. Götz,, M. Rohde,, D. Wehmhöhner,, S. Saravanamuthu,, B. Tümmler, and, I. Steinmetz. 2003. Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J. Med. Microbiol. 52:295–301.

28. He, J.,, R. L. Baldini,, E. Déziel,, M. Saucir,, Q. Zhang,, N. T. Libertari,, D. Lee,, J. Urbach,, H. M. Goodman, and, L. C. Rahme. 2004. The broad host range pathogen Pseudomonas aeruginosa strain PA14 carries two pathogenicity islands harboring plant and animal virulence genes. Proc. Natl. Acad. Sci. USA 101:2530–2535.

29. Henwood, C. J.,, D. M. Livermore,, D. James,, M. Warner, andthe Pseudomonas study group. 2001. Antimicrobial susceptibility of Pseudomonas aeruginosa: results of a UK survey and evaluation of the British society for antimicrobial chemotherapy disc susceptibility test. J. Antimicrob. Chemother. 47:789–799.

30. Hill, A. T.,, E. J. Campbell,, S. L. Hill,, D. L. Bayley, and, R. A. Stockley. 2000. Markers of airway inflammation in patients with stable chronic bronchitis. Am. J. Med. 109:288–295.

31. Hogardt, M.,, C. Hoboth,, S. Schmoldt,, C. Henke,, L. Bader, and, J. Heesemann. 2007. Stage-specific adaptation of hypermutable Pseudomonas aeruginosa isolates during chronic pulmonary infection in patients with cystic fibrosis. J. Infect. Dis. 195:70–80.

32. Imundo, L.,, J. Barasch,, A. Prince, and, A. Al-awqati. 1995. Cystic fibrosis epithelial cells have a receptor for pathogenic bacteria on their apical surface. Proc. Natl. Acad. Sci. USA 92:3019–3023.

33. Kiewitz, C., and, B. Tümmler. 2000. Sequence diversity of Pseudomonas aeruginosa: impact on population structure and genome evolution. J. Bacteriol. 182:3125–3135.

34. Kounnas, M. Z.,, R. E. Morris,, M. R. Thompson,, D. J. FitzGerald,, D. K. Strickland, and, C. B. Saelinger. 1992. The alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein binds and internalizes Pseudomonas exotoxin A. J. Biol. Chem. 267:12420–12423.

35. Lau, G. W.,, D. J. Hassett,, H. Ran, and, F. Kong. 2004. The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol. Med. 10:599–606.

36. Leach, F. S.,, N. C. Nicolaides,, N. Papadopoulos,, B. Liu,, J. Jen,, R. Parsons,, P. Peltomäki,, P. Sistonen,, L. A. Aaltonen,, M. Nyström-Lahti,, X. Y. Guan,, J. Zhang,, P. S. Meltzer,, J. W. Yu,, F. T. Kao,, D. J. Chen,, K. M. Cerosaletti,, R. E. K. Fournier,, S. Todd,, T. Lewis,, R. J. Leach,, S. L. Naylor,, J. Weissenbach,, J. P. Mecklin,, H. Järvinen,, G. M. Petersen,, S. R. Hamilton,, J. Green,, J. Jass,, P. Watson,, H. T. Lynch,, J. M. Trent,, A. de la Chapelle,, K. W. Kinzler, and, B. Vogel-stein. 1993. Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell 75:1215–1225.

37. LeClerc, J. E.,, B. Li,, W. L. Payne, and, T. A. Cebula. 1996. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274:1208–1211.

38. Lieberman, D., and, D. Lieberman. 2003. Pseudomonal infections in patients with COPD: epidemiology and management. Am.J. Respir. Med. 2:459–468.

39. Livermore, D. M. 2002. Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin. Infect. Dis. 34:634–640.

40. Lujan, A. M.,, A. J. Moyano,, I. Segura,, C. E. Argaraña, and, A. M. Smania. 2007. Quorom-sensing-deficient (lasR) mutants emerge at high frequency from a Pseudomonas aeruginosa mutS strain. Microbiology 153:225–237.

41. Lyczak, J. B.,, C. L. Cannon, and, G. B. Pier. 2002. Lung infections associated with cystic fibrois. Clin. Microbiol. Rev. 15:194–222.

42. Lynch, J. P. 2001. Hospital-acquired pneumonia: risk factors, microbiology, and treatment. Chest 119(Suppl. 2): 373–384.

43. Macia, M. D.,, D. Blanquer,, B. Togores,, J. Sauleda,, J. L. Pérez, and, A. Oliver. 2005. Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrob. Agents Chemother. 49:3382–3386.

44. Macia, M. D.,, N. Borrell,, J. L. Perez, and, A. Oliver. 2004. Detection and susceptibility testing of hypermutable Pseudomonas aeruginosa strains with the Etest and disk diffusion. Antimicrob. Agents Chemother. 48:2665–2672.

45. Maciá, M. D.,, N. Borrell,, M. Segura,, G. Gómez,, J. L. Pérez, and, A. Oliver. 2006. Efficacy and potential for resistance selection of anti-pseudomonal treatments in a mouse model of lung infection by hypermutable Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 50:975–983.

46. Mah, T. F. C., and, G. A. O’Toole. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9:34–39.

47. Mahenthiralingam, E.,, M. E. Campbell, and, D. P. Speert. 1994. Nonmotility and phagocytic resistance of Pseudomonas aeruginosa isolates from chronically colonized patients with cystic fibrosis. Infect. Immun. 62:596–605.

48. Mao, E. F.,, L. Lane,, J. Lee, and, J. H. Miller. 1997. Proliferation of mutators in a cell population. J. Bacteriol. 179:417–422.

49. Mariencheck, W. I.,, J. F. Alcorn,, S. M. Palmer, and, J. R. Wright. 2003. Pseudomonas aeruginosa elastase degrades surfactant proteins A and D. Am. J. Respir. Cell Mol. Biol. 28:528–537.

50. Matic, I.,, M. Radman,, F. Taddei,, B. Picard,, C. Doit,, E. Bingen,, E. Denamur, and, J. Elion. 1997. High variable mutation rates in commensal and pathogenic Escherichia coli. Science 277:1833–1834.

51. Matic, I.,, C. Rayssiguer, and, M. Radman. 1995. Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species. Cell 80:507–515.

52. Mena, A.,, M. D. Maciá,, N. Borrell,, B. Moya,, T. de Francisco,, J. L. Pérez, and, A. Oliver. 2007. Inactivation of the mismatch repair system in Pseudomonas aeruginosa attenuates virulence but favors persistence of oropharyngeal colonization in cystic fibrosis mice. J. Bacteriol. 189:3665–3668.

53. Meyer, J. M.,, A. Neely,, A. Stintzi,, C. Georges, and, I. A. Holder. 1996. Pyoverdin is essential for virulence of Pseudomonas aeruginosa. Infect. Immun. 64:518–523.

54. Miller, J. H. 1996. Spontaneous mutators in bacteria: insights into pathways of mutagenesis and repair. Annu. Rev. Microbiol. 50:625–643.

55. Montanari, S.,, A. Oliver,, P. Salerno,, A. Mena,, G. Bertoni,, B. Tummler,, L. Cariani,, M. Conese,, G. Doring, and, A. Bragonzi. 2007. Biological cost of hypermutation in Pseudomonas aeruginosa strains from patients with cystic fibrosis. Microbiology 153:1445–1454.

56. Moyano, A. J.,, A. M. Lujan,, C. E. Argaraña, and, A. M. Smania. 2007. MutS deficiency and activity of the error-prone DNA polymerase IV are crucial for determining mucA as the main target for mucoid conversion in Pseudomonas aeruginosa. Mol. Microbiol. 64:547–559.

57. Nagaki, M.,, S. Shimura,, Y. Tanno,, T. Ishibashi,, H. Sasaki, and, T. Takishima. 1992. Role of chronic Pseudomonas aeruginosa infection in the development of bronchiectasis. Chest 102:1464–1469.

58. Nicotra, M. B.,, M. Rivera,, A. M. Dale,, R. Shepherd, and, R. Carter. 1995. Clinical, pathophysiologic, and microbiologic characterization of bronchiectasis in an aging cohort. Chest 108:955–961.

59. Oliver, A.,, F. Baquero, and, J. Blazquez. 2002. The mismatch repair system (mutS, mutL and uvrD genes) in Pseudomonas aeruginosa: molecular characterization of naturally occurring mutants. Mol. Microbiol. 43:1641–1650.

60. Oliver, A.,, R. Cantón,, P. Campo,, F. Baquero, and, J. Blázquez. 2000. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251–1253.

61. Oliver, A.,, B. R. Levin,, C. Juan,, F. Baquero, and, J. Blázquez. 2004. Hypermutation and the pre-existence of antibiotic resistance Pseudomonas aeruginosa mutants: implications for susceptibility testing and treatment of chronic infections. Antimicrob. Agents Chemother. 48:4226–4233.

62. Oliver, A. M., and, D. M. Weir. 1985. The effect of Pseudomonas aeruginosa alginate on rat alveolar macrophage phagocytosis and bacterial opsonization. Clin. Exp. Immunol. 59:190–196.

63. Parad, R. B.,, C. J. Gerard,, D. Zurakowski,, D. P. Nichols, and, G. B. Pier. 1999. Pulmonary outcome in cystic fibrosis is influenced primarily by mucoid Pseudomonas aeruginosa infection and immune status and only modestly by genotype. Infect. Immun. 67:4744–4750.

64. Pedersen, S.,, S. A. Kharazmi,, F. Espersen, and, N. Hoiby. 1990. Pseudomonas aeruginosa alginate in cystic fibrosis sputum and the inflamatory response. Infect. Immun. 58:3363–3368.

65. Pier, G. B.,, M. Grout,, T. S. Zaidi,, J. C. Olsen,, L. G. Johnson,, J. R. Yankaskas, and, J. B. Goldberg. 1996. Role of mutant CFTR in hypersusceptibility of cystic fibrosis to lung infections. Science 271:64–67.

66. Pirnay, J. P.,, D. De Vos,, C. Cochez,, F. Bilocq,, A. Vanderkelen,, M. Zizi,, B. Ghysels, and, P. Cornellis. 2002. Pseudomonas aeruginosa displays an epidemic population structure. Environ. Microbiol. 4:898–911.

67. Prunier, A. L.,, B. Malbruny,, M. Laurans,, J. Brouard,, J. F. Duhamel, and, R. Leclerc. 2003. High rate of macrolide resistance in Staphylococcus aureus strains from patients with cystic fibrosis reveals high proportions of hypermutable strains. J. Infect. Dis. 187:1709–1716.

68. Rainey, P. B., and, M. Travisano. 1998. Adaptive radiation in a heterogeneous environment. Nature 394:69–72.

69. Román, F.,, R. Cantón,, M. Pérez-Vazquez,, F. Baquero, and, F. Campos. 2004. Dynamics of long-term colonization of respiratory tract by Haemophilus influenzae in cystic fibrosis patients shows a marked increase in hypermutable strains. J. Clin. Microbiol. 42:1450–1459.

70. Romling, U.,, B. Fiedler,, J. Bobhammer,, D. Grothues,, J. Greipel,, H. Von der Hardt, and, B. Tummler. 1994a. Epidemiology of chronic Pseudomonas aeruginosa infections in cystic fibrosis. J. Infect. Dis. 170:1616–1621.

71. Römling, U.,, J. Wingender,, H. Müller, and, B. Tümmler. 1994b. A major Pseudomonas aeruginosa clone common to patients and aquatic habitats. Appl. Environ. Microbiol. 60:1734–1738.

72. Salyers, A. A., and, D. D. Whitt. 2002. Pseudomonas aeruginosa and related species, a lesson of versatility, p. 247–262. In A. Salyers, and, D. D. Whitt (ed.), Bacterial Pathogenesis: a Molecular Approach, 2nd ed. ASM Press, Washington, DC.

73. Sato, H., and, D. W. Frank. 2004. ExoU is a potent intracellular phospholipase. Mol. Microbiol. 53:1279–1290.

74. 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.

75. Silo-Suh, L.,, S. Suh,, P. V. Phibbis, and, D. E. Ohman. 2005. Adaptations of Pseudomonas aeruginosa to the cystic fibrosis lung environment can include deregulation of zwf, encoding glucose-6-phosphate dehydrogenase. J. Bacteriol. 187:7561–7568.

76. Simpson, J. A.,, S. E. Smith, and, R. T. Dean. 1989. Scavenging by alginate of free radicals released by macrophages. Free Radic. Biol. Med. 6:347–353.

77. Smania, A. M.,, I. Segura,, R. J. Pezza,, C. Becerra,, I. Albesa, and, C. E. Argaraña. 2004. Emergence of phenotypic variants upon mismatch repair disruption in Pseudomonas aeruginosa. Microbiology 150:1327–1338.

78. Smith, E. E.,, D. G. Buckley,, Z. Wu,, C. Saenphimmachack,, L. R. Hoffman,, D. A. D`Argenio,, S. I. Miller,, B. W. Ramsey,, D. P. Speert,, S. M. Moskowitz,, J. L. Burns,, R. Kaul, and, M. V. Olson. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. USA 103:8487–8492.

79. Sniegowski, P. D.,, P. J. Gerrish, and, R. E. Lenski. 1997. Evolution of high mutation rates in experimental populations of E. coli. Nature 387:703–705.

80. Spencer, D. H.,, A. Kas,, E. E. Smith,, C. K. Raymond,, E. H. Sims,, M. Hastings,, J. L. Burns,, R. Kaul, and, M. V. Olson. 2003. Whole-genome sequence variation among multiple isolates of Pseudomonas aeruginosa. J. Bacteriol. 185:1316–1325.

81. Stover, C. K.,, X. Q. Pham,, A. L. Erwin,, S. D. Mizoguchi,, P. Warrener,, M. J. Hickey,, F. S. 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. Wong,, Z. Wu,, I. T. Paulsen,, J. Reizer,, M. H. Saier,, R. E. Hancock,, S. Lory, and, M. V. Olson. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959–964.

82. Taddei, F.,, M. Radman,, J. Maynard-Smith,, B. Toupance,, P. H. Gouyon, and, B. Godellete. 1997. Role of mutator alleles in adaptive evolution. Nature 387:700–702.

83. Taylor, R. F.,, M. E. Hodson, and, T. L. Pitt. 1993a. Adult cystic fibrosis: association of acute pulmonary exacerbations and increasing severity of lung disease with auxotrophic mutants of Pseudomonas aeruginosa. Thorax 48:1002–1005.

84. Taylor, R. F.,, M. Warner,, R. C. George,, M. E. Hodson, and, T. L. Pitt. 1993b. Auxotrophic mutants of Pseudomonas aeruginosa: increased resistance to antipseudomonal antibiotics in cystic fibrosis. Med. Microbiol. Lett. 2:25–32.

85. Ventre, I.,, A. L. Goodman,, I. Vallet-Gey,, P. Vasseur,, C. Soscia,, S. Molin,, S. Bleves,, A. Lazdunski,, S. Lory, and, A. Filloux. 2006. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc. Natl. Acad. Sci. USA 103:171–176.

86. Vincent, J. L. 2003. Nosocomial infections in adult intensive-care units. Lancet 361:2068–2077.

87. Whiteley, M.,, M. G. Bangera,, R. E. Bumgamer,, M. R. Parsek,, G. M. Teitzel,, S. Lory, and, E. P. Greenberg. 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860–864.

88. Wilson, C. B.,, P. W. Jones,, C. J. O’Leary,, D. M. Hansell,, P. J. Cole, and, R. Wilson. 1997. Effect of sputum bacteriology on the quality of life of patients with bronchiectasis. Eur. Respir. J. 10:1754–1760.

89. Yahr, T. L.,, A. J. Vallis,, M. K. Hancock,, J. T. Barbieri, and, D. W. Frank. 1998. ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc. Natl. Acad. Sci. USA 95:13899–13904.

90. Yoon, S. S.,, R. F. Hennigan,, G. M. Hilliard,, U. A. Ochsner,, K. Parvatiyar,, M. C. Kamani,, H. L. Allen,, T. R. DeKievit,, P. R. Garder,, U. Schwab,, J. J. Rowe,, B. H. Iglewski,, T. R. McDermott,, R. P. Mason,, D. J. Wozniak,, R. E. Hancock,, M. R. Parsek,, T. L. Noah,, R. C. Boucher, and, D. J. Hassett. 2002. Pseudomonas aeruginosa anaerobic respiration in biofilms. Dev. Cell 3:593–610.

91. Yu, H.,, M. Hanes,, C. E. Chrisp,, J. C. Boucher, and, V. Deretic. 1998. Microbial pathogenesis in cystic fibrosis: pulmonary clearance of mucoid Pseudomonas aeruginosa and inflammation in a mouse model of repeated respiratory challenge. Infect. Immun. 66:280–288.

Tables

Evolution of Pseudomonas aeruginosa Pathogenicity: From Acute to Chronic Infections

/content/10.1128/9781555815639.ch36.ch36tab01

Table 1.

Pseudomonas aeruginosa virulence determinants

Table 1.

Pseudomonas aeruginosa virulence determinants