Adaptation of Pseudomonas aeruginosa in cystic fibrosis airways influences virulence of Staphylococcus aureus in vitro and murine models of co-infection

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Baldan, Rossella ^a   Cigana, Cristina ^a   Testa, Francesca ^a   Bianconi, Irene ^a   De Simone, Maura ^a   Pellin, Danilo ^b   Di Serio, Clelia ^b   Bragonzi, Alessandra ^a   Cirillo, Daniela M ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BIOFILM; COCULTURE; CONTROLLED STUDY; CYSTIC FIBROSIS; DISEASE COURSE; GROWTH INHIBITION; IN VITRO STUDY; IN VIVO STUDY; INFECTIOUS PNEUMONIA; MALE; MIXED INFECTION; MOUSE; MURINE MODEL; NONHUMAN; ORGANISMAL INTERACTION; PHENOTYPIC VARIATION; PLANKTON; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; ANIMAL; ANTIBIOSIS; C57BL MOUSE; CLASSIFICATION; DISEASE MODEL; HOST PATHOGEN INTERACTION; LUNG; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; RESPIRATORY SYSTEM; SPECIES DIFFERENCE; VIRULENCE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIBIOSIS; BACTERIOLOGICAL TECHNIQUES; BIOFILMS; COINFECTION; CYSTIC FIBROSIS; DISEASE MODELS, ANIMAL; HOST-PATHOGEN INTERACTIONS; LUNG; MALE; MICE, INBRED C57BL; PSEUDOMONAS AERUGINOSA; RESPIRATORY SYSTEM; SPECIES SPECIFICITY; STAPHYLOCOCCUS AUREUS; VIRULENCE;

EID: 84897382832     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089614     Document Type: Article

References (49)

1. Sibley CD, Rabin H, Surette MG (2006) Cystic fibrosis: a polymicrobial infectious disease. Future Microbiol 1: 53-61
2. Cystic Fibrosis Foundation Patient Registry: Annual Data Report 2008. Available: http://www.cff.org. Accessed 2014 Feb 12.
3. Rogers GB, Hoffman LR, Whiteley M, Daniels TW, Carroll MP, et al. (2010) Revealing the dynamics of polymicrobial infections: implications for antibiotic therapy. Trends Microbiol 18(8):357-64.
4. Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8(1):15-25.
5. Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K, et al. (2008) Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol Microbiol 68:75-86. (Pubitemid 351363777)
6. Nocker A, Burr M, Camper AK (2007) Genotypic microbial community profiling: a critical technical review. Microb Ecol 54:276-289. (Pubitemid 47197901)
7. Rogers GB, Carroll MP, Bruce KD (2009) Studying bacterial infections through culture-independent approaches. J Med Microbiol 58:1401-1418.
8. Sibley CD, Parkins MD, Rabin HR, Duan K, Norgaard JC, et al. (2008) A polymicrobial perspective of pulmonary infections exposes an enigmatic pathogen in cystic fibrosis patients. Proc Natl Acad Sci U S A 105:15070-15075.
9. Bittar F, Richet H, Dubus JC, Reynaud-Gaubert M, Stremler N, et al. (2008) Molecular detection of multiple emerging pathogens in sputa from cystic fibrosis patients. PLoS One 3:e2908.
10. Bouchara JP, Hsieh HY, Croquefer S, Barton R, Marchais V, et al. (2009) Development of an oligonucleotide array for direct detection of fungi in sputum samples from patients with cystic fibrosis. J Clin Microbiol 47:142-152.
11. Armougom F, Bittar F, Stremler N, Rolain JM, Robert C, et al. (2009) Microbial diversity in the sputum of a cystic fibrosis patient studied with 16S rDNA pyrosequencing. Eur J Clin Microbiol Infect Dis 28:1151-1154.
12. Ecker DJ, Sampath R, Massire C, Blyn LB, Hall TA, et al. (2008) Ibis T5000: a universal biosensor approach for microbiology. Nat Rev Microbiol 6:553-558. (Pubitemid 351850978)
13. Rogers GB, Stressmann FA, Walker AW, Carroll MP, Bruce KD (2010) Lung infections in cystic fibrosis; deriving clinical insight from microbial complexity. Exp Rev Mol Diag 10:187-196.
14. Brogden KA, Guthmiller JM, Taylor CE (2005) Human polymicrobial infections. Lancet 365(9455):253-255. 6.
15. Peters BM, Jabra-Rizk MA, O'May GA, Costerton JW, Shirtliff ME (2012) Polymicrobial interactions: impact on pathogenesis and human disease. Clin Microbiol Rev 25(1):193-213.
16. Döring G (1997) Staphylococcus aureus in cystic fibrosis: implications for prognosis and treatment. Pediatr Pulmonol Suppl 16:235-6.
17. Razvi S, Quittell L, Sewall A, Quinton H, Marshall B, et al. (2009) Respiratory microbiology of patients with cystic fibrosis in the United States, 1995 to 2005. Chest 136(6):1554-60.
18. Goss CH, Muhlebach MS (2011) Review: Staphylococcus aureus and MRSA in cystic fibrosis. J Cyst Fibros 10(5):298-306.
19. Johnson AP (2011) Methicillin-resistant Staphylococcus aureus: the European landscape. J Antimicrob Chemother 66 Suppl 4:iv43-iv48.
20. Baldan R, Testa F, Lorè NI, Bragonzi A, Cichero P, et al. (2012) Factors contributing to epidemic MRSA clones replacement in a hospital setting. PLoS One 7(8):e43153.
21. Ratjen F, McColley SA (2012) Update in cystic fibrosis 2011. Am J Respir Crit Care Med 1;185(9):933-6.
22. Döring G, Hoiby N, Consensus Study Group (2004) Early intervention and prevention of lung disease in cystic fibrosis: a European consensus. J Cyst Fibros 3(2):67-91. (Pubitemid 38987019)
23. Bragonzi A, Paroni M, Nonis A, Cramer N, Montanari S, et al. (2009) Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am J Respir Crit Care Med 15;180(2):138-45.
24. Jarry TM, Cheung AL (2006) Staphylococcus aureus escapes more efficiently from the phagosome of a cystic fibrosis bronchial epithelial cell line than from its normal counterpart. Infect Immun 74(5):2568-77. (Pubitemid 43672964)
25. Hoffman LR, Deziel E, D'Argenio DA, Lepine F, Emerson J, et al. (2006) Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 103(52):19890-19895. (Pubitemid 46037526)
26. Maselli J, Sontag MK, Norris JM, MacKenzie T, Wagener JS, et al. (2003) Risk factors for initial acquisition of Pseudomonas aeruginosa in children with cystic fibrosis identified by newborn screening. Pediatr Pulmonol 35(4):257-262. (Pubitemid 36397675)
27. Yang L, Liu Y, Markussen T, Høiby N, Tolker-Nielsen T, et al. (2011) Pattern differentiation in co-culture biofilms formed by Staphylococcus aureus and Pseudomonas aeruginosa. FEMS Immunol Med Microbiol 62(3):339-47.
28. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35(4):322-32.
29. Lipuma JJ (2010) The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 23:299-323.
30. Lorè NI, Cigana C, De Fino I, Riva C, Juhas M, et al. (2012) Cystic fibrosis-niche adaptation of Pseudomonas aeruginosa reduces virulence in multiple infection hosts. PLoS One 7(4):e35648.
31. Montanari S, Oliver A, Salerno P, Mena A, Bertoni G, et al. (2007) Biological cost of hypermutation in Pseudomonas aeruginosa strains from patients with cystic fibrosis. Microbiology 153(Pt 5):1445-54. (Pubitemid 46780000)
32. Bragonzi A, Wiehlmann L, Klockgether J, Cramer N, Worlitzsch D, et al. (2006) Sequence diversity of the mucABD locus in Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology 152(Pt 11):3261-9. (Pubitemid 44734330)
33. Cigana C, Curcurù L, Leone MR, Ieranò T, Lorè NI, et al. (2009) Pseudomonas aeruginosa exploits lipid A and muropeptides modification as a strategy to lower innate immunity during cystic fibrosis lung infection. PLoS One 23;4(12):e8439.
34. Bragonzi A, Farulla I, Paroni M, Twomey KB, Pirone L, et al. (2012) Modelling co-infection of the cystic fibrosis lung by Pseudomonas aeruginosa and Burkholderia cenocepacia reveals influences on biofilm formation and host response. PLoS One 7(12):e52330.
35. Bianconi I, Milani A, Cigana C, Paroni M, Levesque RC, et al. (2011) Positive signature-tagged mutagenesis in Pseudomonas aeruginosa: tracking patho-adaptive mutations promoting airways chronic infection. PLoS Pathog 3;7(2):e1001270.
36. Harrison F (2007) Microbial ecology of the cystic fibrosis lung. Microbiology 153(Pt 4):917-23.
37. Folkesson A, Jelsbak L, Yang L, Johansen HK, Ciofu O, et al. (2012) Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol 10(12):841-51.
38. Mashburn LM, Jett AM, Akins DR, Whiteley M (2005) Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture. J Bacteriol 187(2):554-66. (Pubitemid 40096244)
39. Biswas L, Biswas R, Schlag M, Bertram R, Götz F (2009) Small-colony variant selection as a survival strategy for Staphylococcus aureus in the presence of Pseudomonas aeruginosa. Appl Environ Microbiol 75(21):6910-2.
40. Mann EE, Wozniak DJ (2012) Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36(4):893-916.
41. Qazi S, Middleton B, Muharram SH, Cockayne A, Hill P, et al. (2006) N-acylhomoserine lactones antagonize virulence gene expression and quorum sensing in Staphylococcus aureus. Infect Immun 74(2):910-9. (Pubitemid 43185524)
42. Pastar I, Nusbaum AG, Gil J, Patel SB, Chen J, et al. (2013) Interactions of methicillin resistant Staphylococcus aureus USA300 and Pseudomonas aeruginosa in polymicrobial wound infection. PLoS One 8(2):e56846.
43. Qin Z, Yang L, Qu D, Molin S, Tolker-Nielsen T (2009) Pseudomonas aeruginosa extracellular products inhibit staphylococcal growth, and disrupt established biofilms produced by Staphylococcus epidermidis. Microbiology 155(Pt 7):2148-56.
44. Dalton T, Dowd SE, Wolcott RD, Sun Y, Watters C, et al. (2011) An in vivo polymicrobial biofilm wound infection model to study interspecies interactions. PLoS One 6(11):e27317.
45. Baba T, Bae T, Schneewind O, Takeuchi F, Hiramatsu K (2008) Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J Bacteriol 190(1):300-10.
46. Horsburgh MJ, Aish JL, White IJ, Shaw L, Lithgow JK, et al. (2002) SigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184(19):5457-67. (Pubitemid 35024393)
47. Liberati NT, Urbach JM, Miyata S, Lee DG, Drenkard E, et al. (2006) An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci U S A 21;103(8):2833-8.
48. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406(6799):959-64.
49. Macho AP, Zumaquero A, Ortiz-Martín I, Beuzón CR (2007) Competitive index in mixed infections: a sensitive and accurate assay for the genetic analysis of Pseudomonas syringae - plant interactions. Mol Plant Pathol 8(4):437-50.pone.0089614.