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Review Article

Chronic pulmonary pseudomonal infection in patients with cystic fibrosis: A model for early phase symbiotic evolution

Pages 144-157 | Received 03 Feb 2014, Accepted 18 Mar 2014, Published online: 25 Apr 2014

References

  • Aaron SD, Ramotar K, Ferris W, et al. (2004). Adult cystic fibrosis exacerbations and new strains of Pseudomonas aeruginosa. Am J Respir Crit Care Med 169:811–5
  • Aaron SD, Vandemheen KL, Ramotar K, et al. (2010). Infection with transmissible strains of Pseudomonas aeruginosa and clinical outcomes in adults with cystic fibrosis. JAMA 304:2145–53
  • Abraham EH, Vos P, Kahn J, et al. (1996). Cystic fibrosis hetero- and homozygosity is associated with inhibition of breast cancer growth. Nat Med 2:593–6
  • Agarwal G, Kapil A, Kabra SK, et al. (2005). Characterization of Pseudomonas aeruginosa isolated from chronically infected children with cystic fibrosis in India. BMC Microbiol 5:43
  • Anderson SW, Stapp JR, Burns JL, Qin X. (2007). Characterization of small-colony-variant Stenotrophomonas maltophilia isolated from the sputum specimens of five patients with cystic fibrosis. J Clin Microbiol 45:529–35
  • Atkinson S, Williams P. (2009). Quorum sensing and social networking in the microbial world. J R Soc Interface 6:959–78
  • Bals R, Weiner DJ, Wilson JM. (1999). The innate immune system in cystic fibrosis lung disease. J Clin Invest 103:303–7
  • Barben J, Hafen G, Schmid J. (2005). Pseudomonas aeruginosa in public swimming pools and bathroom water of patients with cystic fibrosis. J Cyst Fibros 4:227–31
  • Barth AL, Pitt TL. (1995a). Auxotrophic variants of Pseudomonas aeruginosa are selected from prototrophic wild-type strains in respiratory infections in patients with cystic fibrosis. J Clin Microbiol 33:37–40
  • Barth AL, Pitt TL. (1995b). Auxotrophy of Burkholderia (Pseudomonas) cepacia from cystic fibrosis patients. J Clin Microbiol 33:2192–4
  • Barth AL, Pitt TL. (1996). The high amino-acid content of sputum from cystic fibrosis patients promotes growth of auxotrophic Pseudomonas aeruginosa. J Med Microbiol 45:110–19
  • Barth AL, Woodford N, Pitt TL. (1998). Complementation of methionine auxotrophs of Pseudomonas aeruginosa from cystic fibrosis. Curr Microbiol 36:190–5
  • Belda E, Moya A, Bentley S, Silva FJ. (2010). Mobile genetic element proliferation and gene inactivation impact over the genome structure and metabolic capabilities of Sodalis glossinidius, the secondary endosymbiont of tsetse flies. BMC Genomics 11:449
  • Blaser MJ, Kirschner D. (2007). The equilibria that allow bacterial persistence in human hosts. Nature 449:843–9
  • Borderon E, Horodniceanu T. (1978). Metabolically deficient dwarf-colony mutants of Escherichia coli: deficiency and resistance to antibiotics of strains isolated from urine culture. J Clin Microbiol 8:629–34
  • Boucher RC. (2004). New concepts of the pathogenesis of cystic fibrosis lung disease. Eur Respir J 23:146–58
  • Bragonzi A, Paroni M, Nonis A, et al. (2009). Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am J Respir Crit Care Med 180:138–45
  • Brandt LJ, Aroniadis OC. (2013). An overview of fecal microbiota transplantation: techniques, indications, and outcomes. Gastrointest Endos 78:240–9
  • Burns JL, Emerson J, Stapp JR, et al. (1998). Microbiology of sputum from patients at cystic fibrosis centers in the United States. Clin Infect Dis 27:158–63
  • Burns JL, Gibson RL, McNamara S, et al. (2001). Longitudinal assessment of Pseudomonas aeruginosa in young children with cystic fibrosis. J Infect Dis 183:444–52
  • Cigana C, Lore NI, Bernardini ML, Bragonzi A. (2011). Dampening Host Sensing and Avoiding Recognition in Pseudomonas aeruginosa Pneumonia. J Biomed Biotechnol 2011:852513(1–10)
  • Ciofu O, Riis B, Pressler T, et al. (2005). Occurrence of hypermutable Pseudomonas aeruginosa in cystic fibrosis patients is associated with the oxidative stress caused by chronic lung inflammation. Antimicrob Agents Chemother 49:2276–82
  • Ciofu O, Mandsberg LF, Bjarnsholt T, et al. (2010). Genetic adaptation of Pseudomonas aeruginosa during chronic lung infection of patients with cystic fibrosis: strong and weak mutators with heterogeneous genetic backgrounds emerge in mucA and/or lasR mutants. Microbiology 156:1108–19
  • Cox MJ, Allgaier M, Taylor B, et al. (2010). Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS One 5:e11044
  • Dacheux D, Toussaint B, Richard M, et al. (2000). Pseudomonas aeruginosa cystic fibrosis isolates induce rapid, type III secretion-dependent, but ExoU-independent, oncosis of macrophages and polymorphonuclear neutrophils. Infect Immun 68:2916–24
  • Dacheux D, Attree I, Toussaint B. (2001). Expression of ExsA in trans confers type III secretion system-dependent cytotoxicity on noncytotoxic Pseudomonas aeruginosa cystic fibrosis isolates. Infect Immun 69:538–42
  • Dakin CJ, Numa AH, Wang H, et al. (2002). Inflammation, infection, and pulmonary function in infants and young children with cystic fibrosis. Am J Respir Crit Care Med 165:904–10
  • Dale C, Moran NA. (2006). Molecular interactions between bacterial symbionts and their hosts. Cell 126:453–65
  • Damman CJ, Miller SI, Surawicz CM, Zisman TL. (2012). The microbiome and inflammatory bowel disease: is there a therapeutic role for fecal microbiota transplantation? Am J Gastroenterol 107:1452–9
  • Diggle SP, Crusz SA, Camara M. (2007). Quorum sensing. Curr Biol 17:R907–10
  • Doring G, Conway SP, Heijerman HG, et al. (2000). Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus. Eur Respir J 16:749–67
  • Doring G. (2010). Prevention of Pseudomonas aeruginosa infection in cystic fibrosis patients. Int J Med Microbiol 300:573–7
  • Duan K, Dammel C, Stein J, et al. (2003). Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 50:1477–91
  • Emmett M, Kloos WE. (1975). Amino acid requirements of staphylococci isolated from human skin. Can J Microbiol 21:729–33
  • Emmett M, Kloos WE. (1979). The nature of arginine auxotrophy in cutaneous populations of staphylococci. J Gen Microbiol 110:305–14
  • Fang FC. (1997). Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest 99:2818–25
  • Feary TW, Williams B, Calhoun DH, Walker TA. (1969). An analysis of arginine requiring mutants in Pseudomonas aeruginosa. Genetics 62:673–86
  • Feliziani S, Lujan AM, Moyano AJ, et al. (2010). Mucoidy, quorum sensing, mismatch repair and antibiotic resistance in Pseudomonas aeruginosa from cystic fibrosis chronic airways infections. PLoS One 5:e12669(1–12)
  • FitzSimmons SC. (1993). The changing epidemiology of cystic fibrosis. J Pediatr 122:1–9
  • Flume PA, Van Devanter DR. (2012). State of progress in treating cystic fibrosis respiratory disease. BMC Med 10:88
  • Foweraker J. (2009). Recent advances in the microbiology of respiratory tract infection in cystic fibrosis. Br Med Bull 89:93–110
  • Furukawa S, Kuchma SL, O'Toole GA. (2006). Keeping their options open: acute versus persistent infections. J Bacteriol 188:1211–7
  • Fux CA, Shirtliff M, Stoodley P, Costerton JW. (2005). Can laboratory reference strains mirror “real-world” pathogenesis? Trends Microbiol 13:58–63
  • Geng H, Belas R. (2010). Molecular mechanisms underlying roseobacter-phytoplankton symbioses. Current Opin Biotechnol 21:332–8
  • Georgiades K, Raoult D. (2010). Defining pathogenic bacterial species in the genomic era. Frontiers Microbiol 1:151(1–13)
  • Gibson RL, Burns JL, Ramsey BW. (2003a). Pathophysiology and management of pulmonary infections in cystic fibrosis. Am J Respir Crit Care Med 168:918–51
  • Gibson RL, Emerson J, McNamara S, et al. (2003b). Significant microbiological effect of inhaled tobramycin in young children with cystic fibrosis. Am J Respir Crit Care Med 167:841–9
  • Gibson DG, Glass JI, Lartigue C, et al. (2010). Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329:52–6
  • Giles TN, Fisher DJ, Graham DE. (2009). Independent inactivation of arginine decarboxylase genes by nonsense and missense mutations led to pseudogene formation in Chlamydia trachomatis serovar L2 and D strains. BMC Evol Biol 9:166
  • Goldberg JB, Hancock RE, Parales RE, et al. (2008). Pseudomonas 2007. J Bacteriol 190:2649–62
  • Grasemann H, Michler E, Wallot M, Ratjen F. (1997). Decreased concentration of exhaled nitric oxide (NO) in patients with cystic fibrosis. Pediatr Pulmonol 24:173–7
  • Grasemann H, Grasemann C, Kurtz F, et al. (2005a). Oral l-arginine supplementation in cystic fibrosis patients: a placebo-controlled study. Eur Respir J 25:62–8
  • Grasemann H, Schwiertz R, Matthiesen S, et al. (2005b). Increased arginase activity in cystic fibrosis airways. Am J Respir Crit Care Med 172:1523–8
  • Grasemann H, Kurtz F, Ratjen F. (2006a). Inhaled l-arginine improves exhaled nitric oxide and pulmonary function in patients with cystic fibrosis. Am J Respir Crit Care Med 174:208–12
  • Grasemann H, Schwiertz R, Grasemann C, et al. (2006b). Decreased systemic bioavailability of l-arginine in patients with cystic fibrosis. Respir Res 7:87(1–7)
  • Grasemann H. (2010). l-Arginine deficiency in cystic fibrosis lung disease. Open Nitric Oxide J 2:37–40
  • Green SK, Schroth MN, Cho JJ, et al. (1974). Agricultural plants and soil as a reservoir for Pseudomonas aeruginosa. Appl Microbiol 28:987–91
  • Haussler S, Tummler B, Weissbrodt H, et al. (1999). Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin Infect Dis 29:621–5
  • Haussler S, Lehmann C, Breselge C, et al. (2003a). Fatal outcome of lung transplantation in cystic fibrosis patients due to small-colony variants of the Burkholderia cepacia complex. Eur J Clin Microbiol Infect Dis 22:249–53
  • Haussler S, Ziegler I, Lottel A, et al. (2003b). Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J Med Microbiol 52:295–301
  • Head NE, Yu H. (2004). Cross-sectional analysis of clinical and environmental isolates of Pseudomonas aeruginosa: biofilm formation, virulence, and genome diversity. Infect Immun 72:133–44
  • Heurlier K, Denervaud V, Haenni M, et al. (2005). Quorum-sensing-negative (lasR) mutants of Pseudomonas aeruginosa avoid cell lysis and death. J Bacteriol 187:4875–83
  • Heurlier K, Denervaud V, Haas D. (2006). Impact of quorum sensing on fitness of Pseudomonas aeruginosa. Int J Med Microbiol 296:93–102
  • Hewlett AW. (1916). Monographic medicine, Vol. 1. New York and London: Appleton and Company
  • Hoboth C, Hoffmann R, Eichner A, et al. (2009). Dynamics of adaptive microevolution of hypermutable Pseudomonas aeruginosa during chronic pulmonary infection in patients with cystic fibrosis. J Infect Dis 200:118–30
  • Hoffman LR, Kulasekara HD, Emerson J, et al. (2009). Pseudomonas aeruginosa lasR mutants are associated with cystic fibrosis lung disease progression. J Cyst Fibros 8:66–70
  • Hoffmann N, Rasmussen TB, Jensen PO, et al. (2005). Novel mouse model of chronic Pseudomonas aeruginosa lung infection mimicking cystic fibrosis. Infect Immun 73:2504–14
  • Hogardt M, Heesemann J. (2010). Adaptation of Pseudomonas aeruginosa during persistence in the cystic fibrosis lung. Int J Med Microbiol 300:557–62
  • Hogardt M, Hoboth C, Schmoldt S, et al. (2007). Stage-specific adaptation of hypermutable Pseudomonas aeruginosa isolates during chronic pulmonary infection in patients with cystic fibrosis. J Infect Dis 195:70–80
  • Hoiby N, Koch C. (2000). Maintenance treatment of chronic pseudomonas aeruginosa infection in cystic fibrosis. Thorax 55:349–50
  • Hoiby N, Ciofu O, Bjarnsholt T. (2010). Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol 5:1663–74
  • Hoiby N, Ciofu O, Johansen HK, et al. (2011). The clinical impact of bacterial biofilms. Int J Oral Sci 3:55–65
  • Hoiby N, Krogh Johansen H, Moser C, et al. (2001). Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect 3:23–35
  • Huse HK, Kwon T, Zlosnik JE, et al. (2010). Parallel evolution in Pseudomonas aeruginosa over 39 000 generations in vivo. MBio 1:e00199–10
  • Irvin RT, Govan JW, Fyfe JA, Costerton JW. (1981). Heterogeneity of antibiotic resistance in mucoid isolates of Pseudomonas aeruginosa obtained from cystic fibrosis patients: role of outer membrane proteins. Antimicrob Agents Chemother 19:1056–63
  • Jacques I, Derelle J, Weber M, Vidailhet M. (1998). Pulmonary evolution of cystic fibrosis patients colonized by Pseudomonas aeruginosa and/or Burkholderia cepacia. Eur J Pediatr 157:427–31
  • Jelsbak L, Johansen HK, Frost AL, et al. (2007). Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients. Infect Immun 75:2214–24
  • Kau AL, Ahern PP, Griffin NW, et al. (2011). Human nutrition, the gut microbiome and the immune system. Nature 474:327–36
  • Kinkel LL, Bakker MG, Schlatter DC. (2011). A coevolutionary framework for managing disease-suppressive soils. Ann Rev Phytopathol 49:47–67
  • Kinkel LL, Schlatter DC, Bakker MG, Arenz BE. (2012). Streptomyces competition and co-evolution in relation to plant disease suppression. Res Microbiol 163:490–9
  • Kohler T, Buckling A, van Delden C. (2009). Cooperation and virulence of clinical Pseudomonas aeruginosa populations. Proc Natl Acad Sci USA 106:6339–44
  • Lane N, Martin W. (2010). The energetics of genome complexity. Nature 467:929–34
  • Laursen BS, Sorensen HP, Mortensen KK, Sperling-Petersen HU. (2005). Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev 69:101–23
  • Lee DG, Urbach JM, Wu G, et al. (2006). Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol 7:R90
  • Lemon KP, Armitage GC, Relman DA, Fischbach MA. (2012). Microbiota-targeted therapies: an ecological perspective. Science translational medicine 4:137rv135
  • Levin BR, Antia R. (2001). Why we don't get sick: the within-host population dynamics of bacterial infections. Science 292:1112–5
  • Ley RE, Peterson DA, Gordon JI. (2006). Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–48
  • Ley RE, Hamady M, Lozupone C, et al. (2008). Evolution of mammals and their gut microbes. Science 320:1647–51
  • Li Z, Kosorok MR, Farrell PM, et al. (2005). Longitudinal development of mucoid Pseudomonas aeruginosa infection and lung disease progression in children with cystic fibrosis. JAMA 293:581–8
  • Livermore DM. (2002). Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin Infect Dis 34:634–40
  • Lore NI, Cigana C, De Fino I, et al. (2012). Cystic fibrosis-niche adaptation of Pseudomonas aeruginosa reduces virulence in multiple infection hosts. PLoS One 7:e35648
  • Luiking YC, Poeze M, Dejong CH, et al. (2004). Sepsis: an arginine deficiency state? Crit Care Med 32:2135–45
  • Luzar MA, Montie TC. (1985). Avirulence and altered physiological properties of cystic fibrosis strains of Pseudomonas aeruginosa. Infect Immun 50:572–6
  • Luzar MA, Thomassen MJ, Montie TC. (1985). Flagella and motility alterations in Pseudomonas aeruginosa strains from patients with cystic fibrosis: relationship to patient clinical condition. Infect Immun 50:577–82
  • Lyczak JB, Cannon CL, Pier GB. (2002). Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15:194–222
  • Macia MD, Blanquer D, Togores B, et al. (2005). Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrob Agents Chemother 49:3382–6
  • Mahadeva R, Webb K, Westerbeek RC, et al. (1998). Clinical outcome in relation to care in centres specialising in cystic fibrosis: cross sectional study. BMJ 316:1771–5
  • Manos J, Arthur J, Rose B, et al. (2008). Transcriptome analyses and biofilm-forming characteristics of a clonal Pseudomonas aeruginosa from the cystic fibrosis lung. J Med Microbiol 57:1454–65
  • Mathee K, Narasimhan G, Valdes C, et al. (2008). Dynamics of Pseudomonas aeruginosa genome evolution. Proc Natl Acad Sci USA 105:3100–5
  • Mavrodi DV, Bonsall RF, Delaney SM, et al. (2001). Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183:6454–65
  • May TB, Shinabarger D, Maharaj R, et al. (1991). Alginate synthesis by Pseudomonas aeruginosa: a key pathogenic factor in chronic pulmonary infections of cystic fibrosis patients. Clin Microbiol Rev 4:191–206
  • McCutcheon JP, Moran NA. (2012). Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10:13–26
  • Mena A, Macia MD, Borrell N, et al. (2007). Inactivation of the mismatch repair system in Pseudomonas aeruginosa attenuates virulence but favors persistence of oropharyngeal colonization in cystic fibrosis mice. J Bacteriol 189:3665–8
  • Mena A, Smith EE, Burns JL, et al. (2008). Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J Bacteriol 190:7910–7
  • Meyer KF. (1936). Latent infections. J Bacteriol 31:109–35
  • Montanari S, Oliver A, Salerno P, et al. (2007). Biological cost of hypermutation in Pseudomonas aeruginosa strains from patients with cystic fibrosis. Microbiology 153:1445–54
  • Moran NA, McCutcheon JP, Nakabachi A. (2008). Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–90
  • Moran NA. (2006). Symbiosis. Curr Biol 16:R866–871
  • Moran NA. (2007). Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci USA 104:8627–33
  • Mowat E, Paterson S, Fothergill JL, et al. (2011). Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Am J Respir Crit Care Med 183:1674–9
  • Munder M. (2009). Arginase: an emerging key player in the mammalian immune system. Br J Pharmacol 158:638–51
  • Munson MA, Baumann P, Clark MA, et al. (1991). Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol 173:6321–4
  • Murray TS, Egan M, Kazmierczak BI. (2007). Pseudomonas aeruginosa chronic colonization in cystic fibrosis patients. Curr Opin Pediatr 19:83–8
  • Nappi AJaEV. (2001). Phylogenetic perspectives on the vertebrate immune system. Vol. 484. Springer. 329–348
  • Nixon GM, Armstrong DS, Carzino R, et al. (2001). Clinical outcome after early Pseudomonas aeruginosa infection in cystic fibrosis. J Pediatr 138:699–704
  • Noah TL, Black HR, Cheng PW, et al. (1997). Nasal and bronchoalveolar lavage fluid cytokines in early cystic fibrosis. J Infect Dis 175:638–47
  • Oberhardt MA, Goldberg JB, Hogardt M, Papin JA. (2010). Metabolic network analysis of Pseudomonas aeruginosa during chronic cystic fibrosis lung infection. J Bacteriol 192:5534–48
  • Oliver A. (2010). Mutators in cystic fibrosis chronic lung infection: prevalence, mechanisms, and consequences for antimicrobial therapy. Int J Med Microbiol 300:563–72
  • Oliver A, Baquero F, Blazquez J. (2002). The mismatch repair system (mutS, mutL and uvrD genes) in Pseudomonas aeruginosa: molecular characterization of naturally occurring mutants. Mol Microbiol 43:1641–50
  • Oliver A, Mena A. (2010). Bacterial hypermutation in cystic fibrosis, not only for antibiotic resistance. Clin Microbiol Infect 16:798–808
  • O'Sullivan BP, Freedman SD. (2009). Cystic fibrosis. Lancet 373:1891–904
  • Palmer KL, Mashburn LM, Singh PK, Whiteley M. (2005). Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology. J Bacteriol 187:5267–77
  • Palmer KL, Aye LM, Whiteley M. (2007). Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J Bacteriol 189:8079–87
  • Palmer JN. (2005). Bacterial biofilms: do they play a role in chronic sinusitis? Otolaryngol Clin North Am 38:1193–201, viii
  • Patel HM, Walsh CT. (2001). In vitro reconstitution of the Pseudomonas aeruginosa nonribosomal peptide synthesis of pyochelin: characterization of backbone tailoring thiazoline reductase and N-methyltransferase activities. Biochemistry 40:9023–31
  • Payne SH, Loomis WF. (2006). Retention and loss of amino acid biosynthetic pathways based on analysis of whole-genome sequences. Eukaryot Cell 5:272–6
  • Piddock LJ. (2006). Multidrug-resistance efflux pumps - not just for resistance. Nat Rev Microbiol 4:629–36
  • Pirnay JP, Bilocq F, Pot B, et al. (2009). Pseudomonas aeruginosa population structure revisited. PLoS One 4:e7740
  • Pitt TL, Sparrow M, Warner M, Stefanidou M. (2003). Survey of resistance of Pseudomonas aeruginosa from UK patients with cystic fibrosis to six commonly prescribed antimicrobial agents. Thorax 58:794–6
  • Pollack M. (2000). Pseudomonas aeruginosa. In: Mandell GL BJ, Dolin R, eds. Principles and practice of infectious diseases, 5th ed. New York, NY: Churchill Livingstone, 2310–27
  • Poole K. (2001). Multidrug efflux pumps and antimicrobial resistance in Pseudomonas aeruginosa and related organisms. J Mol Microbiol Biotechnol 3:255–64
  • Poulsen M, Erhardt DP, Molinaro DJ, et al. (2007). Antagonistic bacterial interactions help shape host-symbiont dynamics within the fungus-growing ant-microbe mutualism. PLoS One 2:e960
  • Proctor RA, von Eiff C, Kahl BC, et al. (2006). Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4:295–305
  • Qin X, Zerr DM, McNutt MA, et al. (2012). Pseudomonas aeruginosa syntrophy in chronically colonized airways of cystic fibrosis patients. Antimicrob Agents Chemother 56:5971–81
  • Racey D, Inglis RF, Harrison F, et al. (2010). The effect of elevated mutation rates on the evolution of cooperation and virulence of Pseudomonas aeruginosa. Evolution 64:515–21
  • Ratcliff WC, Denison RF. (2011). Microbiology. Alternative actions for antibiotics. Science 332:547–8
  • Rau MH, Hansen SK, Johansen HK, et al. (2010). Early adaptive developments of Pseudomonas aeruginosa after the transition from life in the environment to persistent colonization in the airways of human cystic fibrosis hosts. Environ Microbiol 12:1643–58
  • Regnath T, Kreutzberger M, Illing S, et al. (2004). Prevalence of Pseudomonas aeruginosa in households of patients with cystic fibrosis. Int J Hyg Environ Health 207:585–8
  • Ricciardolo FL, Sterk PJ, Gaston B, Folkerts G. (2004). Nitric oxide in health and disease of the respiratory system. Physiol Rev 84:731–65
  • Rosenfeld M, Ramsey BW, Gibson RL. (2003). Pseudomonas acquisition in young patients with cystic fibrosis: pathophysiology, diagnosis, and management. Curr Opin Pulm Med 9:492–7
  • Roy PH, Tetu SG, Larouche A, et al. (2010). Complete genome sequence of the multiresistant taxonomic outlier Pseudomonas aeruginosa PA7. PLoS One 5:e8842
  • Roy-Burman A, Savel RH, Racine S, et al. (2001). Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections. J Infect Dis 183:1767–74
  • Ruby EG. (2008). Symbiotic conversations are revealed under genetic interrogation. Nat Rev Microbiol 6:752–62
  • Sheldon CD, Hodson ME, Carpenter LM, Swerdlow AJ. (1993). A cohort study of cystic fibrosis and malignancy. Br J Cancer 68:1025–8
  • Smith EE, Buckley DG, Wu Z, et al. (2006). Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103:8487–92
  • Son MS, Matthews WJ Jr, Kang Y, et al. (2007). In vivo evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infect Immun 75:5313–24
  • Starkey M, Hickman JH, Ma L, et al. (2009). Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol 191:3492–503
  • Starner TD, McCray PB Jr. (2005). Pathogenesis of early lung disease in cystic fibrosis: a window of opportunity to eradicate bacteria. Ann Intern Med 143:816–22
  • Strausbaugh SD, Davis PB. (2007). Cystic fibrosis: a review of epidemiology and pathobiology. Clin Chest Med 28:279–88
  • Tangney M, Gahan CG. (2010). Editorial [Hot Topic: Bacterial Vectors for Gene & Cell Therapy]. Curr Gene Ther 10:1–2
  • Taylor RF, Hodson ME, Pitt TL. (1992). Auxotrophy of Pseudomonas aeruginosa in cystic fibrosis. FEMS Microbiol Lett 71:243–6
  • Thomas SR, Ray A, Hodson ME, Pitt TL. (2000). Increased sputum amino acid concentrations and auxotrophy of Pseudomonas aeruginosa in severe cystic fibrosis lung disease. Thorax 55:795–7
  • Valderrey AD, Pozuelo MJ, Jimenez PA, et al. (2010). Chronic colonization by Pseudomonas aeruginosa of patients with obstructive lung diseases: cystic fibrosis, bronchiectasis, and chronic obstructive pulmonary disease. Diagn Microbiol Infect Dis 68:20–7
  • Vendeville A, Winzer K, Heurlier K, et al. (2005). Making ‘sense' of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat Rev Microbiol 3:383–96
  • von Eiff C, Peters G, Becker K. (2006). The small colony variant (SCV) concept – the role of staphylococcal SCVs in persistent infections. Injury 37:S26–33
  • Waters CM, Bassler BL. (2005). Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–46
  • Whiteley M, Bangera MG, Bumgarner RE, et al. (2001). Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860–4
  • Williams P, Camara M. (2009). Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12:182–91
  • Williams BJ, Dehnbostel J, Blackwell TS. (2010). Pseudomonas aeruginosa: host defence in lung diseases. Respirology 15:1037–56
  • Williams P, Winzer K, Chan WC, Camara M. (2007). Look who's talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond. Ser B, Biol Sci 362:1119–34
  • Willcox MD, Zhu H, Conibear TC, et al. (2008). Role of quorum sensing by Pseudomonas aeruginosa in microbial keratitis and cystic fibrosis. Microbiology 154:2184–94
  • Winstanley C, Fothergill JL. (2009). The role of quorum sensing in chronic cystic fibrosis Pseudomonas aeruginosa infections. FEMS Microbiol Lett 290:1–9
  • Wolter DJ, Emerson JC, McNamara S, et al. (2013). Staphylococcus aureus small-colony variants are independently associated with worse lung disease in children with cystic fibrosis. Clin Infect Dis 57:384–91
  • Wu H, Song Z, Givskov M, et al. (2001). Pseudomonas aeruginosa mutations in lasI and rhlI quorum sensing systems result in milder chronic lung infection. Microbiology 147:1105–13
  • Xavier JB, Kim W, Foster KR. (2011). A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Mol Microbiol 79:166–79
  • Yang L, Haagensen JA, Jelsbak L, et al. (2008). In situ growth rates and biofilm development of Pseudomonas aeruginosa populations in chronic lung infections. J Bacteriol 190:2767–76
  • Yim G, Wang HH, Davies JFRS. (2007). Antibiotics as signalling molecules. Philos Trans R Soc Lond B Biol Sci 362:1195–200
  • Zierdt CH, Schmidt PJ. (1964). Dissociation in Pseudomonas aeruginosa. J Bacteriol 87:1003–10