1887

Abstract

is one of the main microbial species colonizing the lungs of cystic fibrosis patients and is responsible for the decline in respiratory function. Despite the hostile pulmonary environment, is able to establish chronic infections thanks to its strong adaptive capacity. Various longitudinal studies have attempted to compare the strains of early infection with the adapted strains of chronic infection. Thanks to new ‘-omics’ techniques, convergent genetic mutations, as well as transcriptomic and proteomic dysregulations have been identified. As a consequence of this evolution, the adapted strains of have particular phenotypes that promote persistent infection.

Funding
This study was supported by the:
  • Association Gregory Lemarchal
    • Principle Award Recipient: KarenMoreau
  • Association Vaincre la Mucoviscidose
    • Principle Award Recipient: KarenMoreau
  • Fondation Innovations en Infectiologie
    • Principle Award Recipient: KarenMoreau
  • FRM (Award ECO20170637499)
    • Principle Award Recipient: LauraCamus
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2021-02-02
2024-04-24
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References

  1. Moradali MF, Ghods S, Rehm BHA. Pseudomonas aeruginosa lifestyle: a paradigm for adaptation, survival, and persistence. Front Cell Infect Microbiol 2017; 7:39 [View Article]
    [Google Scholar]
  2. Elabed H, González-Tortuero E, Ibacache-Quiroga C, Bakhrouf A, Johnston P et al. Seawater salt-trapped Pseudomonas aeruginosa survives for years and gets primed for salinity tolerance. BMC Microbiol 2019; 19:142 [View Article]
    [Google Scholar]
  3. Lewenza S, Abboud J, Poon K, Kobryn M, Humplik I et al. Pseudomonas aeruginosa displays a dormancy phenotype during long-term survival in water. PLoS One 2018; 13:e0198384 [View Article]
    [Google Scholar]
  4. Kung VL, Ozer EA, Hauser AR. The accessory genome of Pseudomonas aeruginosa . Microbiol Mol Biol Rev 2010; 74:621–641 [View Article]
    [Google Scholar]
  5. Parkins MD, Somayaji R, Waters VJ. Epidemiology, biology, and impact of clonal Pseudomonas aeruginosa infections in cystic fibrosis. Clin Microbiol Rev 2018; 31:e00019-18 [View Article]
    [Google Scholar]
  6. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 2006; 103:8487–8492 [View Article]
    [Google Scholar]
  7. Cramer N, Klockgether J, Wrasman K, Schmidt M, Davenport CF et al. Microevolution of the major common Pseudomonas aeruginosa clones C and PA14 in cystic fibrosis lungs. Environ Microbiol 2011; 13:1690–1704 [View Article]
    [Google Scholar]
  8. Feliziani S, Marvig RL, Luján AM, Moyano AJ, Di Rienzo JA et al. Coexistence and within-host evolution of diversified lineages of hypermutable Pseudomonas aeruginosa in long-term cystic fibrosis infections. PLoS Genet 2014; 10:e1004651 [View Article]
    [Google Scholar]
  9. Markussen T, Marvig RL, Gómez-Lozano M, Aanæs K, Burleigh AE et al. Environmental heterogeneity drives within-host diversification and evolution of Pseudomonas aeruginosa . mBio 2014; 5:e01592-14 [View Article][PubMed]
    [Google Scholar]
  10. Bianconi I, Jeukens J, Freschi L, Alcalá-Franco B, Facchini M et al. Comparative genomics and biological characterization of sequential Pseudomonas aeruginosa isolates from persistent airways infection. BMC Genomics 2015; 16:1105 [View Article]
    [Google Scholar]
  11. Bianconi I, D’Arcangelo S, Esposito A, Benedet M, Piffer E et al. Persistence and microevolution of Pseudomonas aeruginosa in the cystic fibrosis lung: a single-patient longitudinal genomic study. Front Microbiol 2018; 9:3242 [View Article]
    [Google Scholar]
  12. van Mansfeld R, de Been M, Paganelli F, Yang L, Bonten M et al. Within-host evolution of the Dutch high-prevalent Pseudomonas aeruginosa clone ST406 during chronic colonization of a patient with cystic fibrosis. PLoS One 2016; 11:e0158106 [View Article]
    [Google Scholar]
  13. Yang L, Jelsbak L, Marvig RL, Damkiaer S, Workman CT et al. Evolutionary dynamics of bacteria in a human host environment. Proc Natl Acad Sci USA 2011; 108:7481–7486 [View Article]
    [Google Scholar]
  14. Marvig RL, Johansen HK, Molin S, Jelsbak L. Genome analysis of a transmissible lineage of Pseudomonas aeruginosa reveals pathoadaptive mutations and distinct evolutionary paths of hypermutators. PLoS Genet 2013; 9:e1003741 [View Article]
    [Google Scholar]
  15. Wee BA, Tai AS, Sherrard LJ, Ben Zakour NL, Hanks KR et al. Whole genome sequencing reveals the emergence of a Pseudomonas aeruginosa shared strain sub-lineage among patients treated within a single cystic fibrosis centre. BMC Genomics 2018; 19:644 [View Article]
    [Google Scholar]
  16. Marvig RL, Sommer LM, Molin S, Johansen HK. Convergent evolution and adaptation of Pseudomonas aeruginosa within patients with cystic fibrosis. Nat Genet 2015; 47:57–64 [View Article]
    [Google Scholar]
  17. Klockgether J, Cramer N, Fischer S, Wiehlmann L, Tümmler B. Long-term microevolution of Pseudomonas aeruginosa differs between mildly and severely affected cystic fibrosis lungs. Am J Respir Cell Mol Biol 2018; 59:246–256 [View Article]
    [Google Scholar]
  18. Marvig RL, Dolce D, Sommer LM, Petersen B, Ciofu O et al. Within-host microevolution of Pseudomonas aeruginosa in Italian cystic fibrosis patients. BMC Microbiol 2015; 15:218 [View Article]
    [Google Scholar]
  19. Qiu X, Kulasekara BR, Lory S. Role of horizontal gene transfer in the evolution of Pseudomonas aeruginosa virulence. Genome Dyn 2009; 6:126–139 [View Article][PubMed]
    [Google Scholar]
  20. Brockhurst MA, Buckling A, Rainey PB. The effect of a bacteriophage on diversification of the opportunistic bacterial pathogen, Pseudomonas aeruginosa . Proc Biol Sci 2005; 272:1385–1391 [View Article]
    [Google Scholar]
  21. Winstanley C, Langille MGI, Fothergill JL, Kukavica-Ibrulj I, Paradis-Bleau C et al. Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool epidemic strain of Pseudomonas aeruginosa . Genome Res 2009; 19:12–23 [View Article]
    [Google Scholar]
  22. Harrison EM, Carter MEK, Luck S, Ou H-Y, He X et al. Pathogenicity islands PAPI-1 and PAPI-2 contribute individually and synergistically to the virulence of Pseudomonas aeruginosa strain PA14. Infect Immun 2010; 78:1437–1446 [View Article]
    [Google Scholar]
  23. Dettman JR, Rodrigue N, Aaron SD, Kassen R. Evolutionary genomics of epidemic and nonepidemic strains of Pseudomonas aeruginosa . Proc Natl Acad Sci USA 2013; 110:21065–21070 [View Article]
    [Google Scholar]
  24. Lemieux A-A, Jeukens J, Kukavica-Ibrulj I, Fothergill JL, Boyle B et al. Genes required for free phage production are essential for Pseudomonas aeruginosa chronic lung infections. J Infect Dis 2016; 213:395–402 [View Article]
    [Google Scholar]
  25. Subedi D, Vijay AK, Kohli GS, Rice SA, Willcox M. Comparative genomics of clinical strains of Pseudomonas aeruginosa strains isolated from different geographic sites. Sci Rep 2018; 8:15668 [View Article]
    [Google Scholar]
  26. Qiu X, Gurkar AU, Lory S. Interstrain transfer of the large pathogenicity island (PAPI-1) of Pseudomonas aeruginosa . Proc Natl Acad Sci USA 2006; 103:19830–19835 [View Article]
    [Google Scholar]
  27. Klockgether J, Würdemann D, Reva O, Wiehlmann L, Tümmler B. Diversity of the abundant pKLC102/PAGI-2 family of genomic islands in Pseudomonas aeruginosa . J Bacteriol 2007; 189:2443–2459 [View Article]
    [Google Scholar]
  28. Mathee K, Narasimhan G, Valdes C, Qiu X, Matewish JM et al. Dynamics of Pseudomonas aeruginosa genome evolution. Proc Natl Acad Sci USA 2008; 105:3100–3105 [View Article]
    [Google Scholar]
  29. Carter MQ, Chen J, Lory S. The Pseudomonas aeruginosa pathogenicity island PAPI-1 is transferred via a novel type IV pilus. J Bacteriol 2010; 192:3249–3258 [View Article]
    [Google Scholar]
  30. James CE, Fothergill JL, Kalwij H, Hall AJ, Cottell J et al. Differential infection properties of three inducible prophages from an epidemic strain of Pseudomonas aeruginosa . BMC Microbiol 2012; 12:216 [View Article]
    [Google Scholar]
  31. Rau MH, Marvig RL, Ehrlich GD, Molin S, Jelsbak L. Deletion and acquisition of genomic content during early stage adaptation of Pseudomonas aeruginosa to a human host environment. Environ Microbiol 2012; 14:2200–2211 [View Article]
    [Google Scholar]
  32. Bezuidt OKI, Klockgether J, Elsen S, Attree I, Davenport CF et al. Intraclonal genome diversity of Pseudomonas aeruginosa clones CHA and TB. BMC Genomics 2013; 14:416 [View Article]
    [Google Scholar]
  33. Sharma P, Gupta SK, Rolain J-M. Whole genome sequencing of bacteria in cystic fibrosis as a model for bacterial genome adaptation and evolution. Expert Rev Anti Infect Ther 2014; 12:343–355 [View Article]
    [Google Scholar]
  34. Fothergill JL, Mowat E, Ledson MJ, Walshaw MJ, Winstanley C. Fluctuations in phenotypes and genotypes within populations of Pseudomonas aeruginosa in the cystic fibrosis lung during pulmonary exacerbations. J Med Microbiol 2010; 59:472–481 [View Article]
    [Google Scholar]
  35. Römling U, Schmidt KD, Tümmler B. Large genome rearrangements discovered by the detailed analysis of 21 Pseudomonas aeruginosa clone C isolates found in environment and disease habitats. J Mol Biol 1997; 271:386–404 [View Article]
    [Google Scholar]
  36. Harmer C, Alnassafi K, Hu H, Elkins M, Bye P et al. Modulation of gene expression by Pseudomonas aeruginosa during chronic infection in the adult cystic fibrosis lung. Microbiology 2013; 159:2354–2363 [View Article]
    [Google Scholar]
  37. Andersen SB, Ghoul M, Griffin AS, Petersen B, Johansen HK et al. Diversity, prevalence, and longitudinal occurrence of type II toxin-antitoxin systems of Pseudomonas aeruginosa infecting cystic fibrosis lungs. Front Microbiol 2017; 8:1180 [View Article]
    [Google Scholar]
  38. England WE, Kim T, Whitaker RJ. Metapopulation structure of CRISPR-Cas immunity in Pseudomonas aeruginosa and its viruses. mSystems 2018; 3:e00075-18 [View Article]
    [Google Scholar]
  39. Kresse AU, Dinesh SD, Larbig K, Römling U. Impact of large chromosomal inversions on the adaptation and evolution of Pseudomonas aeruginosa chronically colonizing cystic fibrosis lungs. Mol Microbiol 2003; 47:145–158 [View Article]
    [Google Scholar]
  40. Dorman CJ, Bogue MM. The interplay between DNA topology and accessory factors in site-specific recombination in bacteria and their bacteriophages. Sci Prog 2016; 99:420–437 [View Article]
    [Google Scholar]
  41. Darch SE, McNally A, Harrison F, Corander J, Barr HL et al. Recombination is a key driver of genomic and phenotypic diversity in a Pseudomonas aeruginosa population during cystic fibrosis infection. Sci Rep 2015; 5:7649 [View Article]
    [Google Scholar]
  42. Williams D, Paterson S, Brockhurst MA, Winstanley C. Refined analyses suggest that recombination is a minor source of genomic diversity in Pseudomonas aeruginosa chronic cystic fibrosis infections. Microb Genom 2016; 2:e000051 [View Article]
    [Google Scholar]
  43. Darch SE, McNally A, Corander J, Diggle SP. Response to ‘Refined analyses suggest that recombination is a minor source of genomic diversity in Pseudomonas aeruginosa chronic cystic fibrosis infections’ by Williams et al. (2016). Microb Genom 2016; 2:e000054
    [Google Scholar]
  44. Oliver A. Mutators in cystic fibrosis chronic lung infection: prevalence, mechanisms, and consequences for antimicrobial therapy. Int J Med Microbiol 2010; 300:563–572 [View Article]
    [Google Scholar]
  45. Colque CA, Albarracín Orio AG, Feliziani S, Marvig RL, Tobares AR et al. Hypermutator Pseudomonas aeruginosa exploits multiple genetic pathways to develop multidrug resistance during long-term infections in the airways of cystic fibrosis patients. Antimicrob Agents Chemother 2020; 64:e02142-19 [View Article][PubMed]
    [Google Scholar]
  46. Winstanley C, O’Brien S, Brockhurst MA. Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol 2016; 24:327–337 [View Article]
    [Google Scholar]
  47. Clark ST, Guttman DS, Hwang DM. Diversification of Pseudomonas aeruginosa within the cystic fibrosis lung and its effects on antibiotic resistance. FEMS Microbiol Lett 2018; 365:fny026 [View Article]
    [Google Scholar]
  48. Davies EV, James CE, Brockhurst MA, Winstanley C. Evolutionary diversification of Pseudomonas aeruginosa in an artificial sputum model. BMC Microbiol 2017; 17:3 [View Article]
    [Google Scholar]
  49. Mehta HH, Prater AG, Beabout K, Elworth RAL, Karavis M. The essential role of hypermutation in rapid adaptation to antibiotic stress. Antimicrob Agents Chemother 2019; 63:e00744-19 [View Article]
    [Google Scholar]
  50. Cabot G, Zamorano L, Moyà B, Juan C, Navas A et al. Evolution of Pseudomonas aeruginosa antimicrobial resistance and fitness under low and high mutation rates. Antimicrob Agents Chemother 2016; 60:1767–1778 [View Article]
    [Google Scholar]
  51. Khil PP, Dulanto Chiang A, Ho J, Youn J-H, Lemon JK et al. Dynamic emergence of mismatch repair deficiency facilitates rapid evolution of ceftazidime-avibactam resistance in Pseudomonas aeruginosa acute infection. mBio 2019; 10:e01822-19 [View Article][PubMed]
    [Google Scholar]
  52. Hall LMC, Henderson-Begg SK. Hypermutable bacteria isolated from humans – a critical analysis. Microbiology 2006; 152:2505–2514 [View Article]
    [Google Scholar]
  53. Oliver A, Mena A. Bacterial hypermutation in cystic fibrosis, not only for antibiotic resistance. Clin Microbiol Infect 2010; 16:798–808 [View Article]
    [Google Scholar]
  54. Rees VE, Deveson Lucas DS, López-Causapé C, Huang Y, Kotsimbos T. Characterization of hypermutator Pseudomonas aeruginosa isolates from patients with cystic osis in Australia. Antimicrob Agents Chemother 2019; 63:e02538-18 [View Article]
    [Google Scholar]
  55. Auerbach A, Kerem E, Assous MV, Picard E, Bar-Meir M. Is infection with hypermutable Pseudomonas aeruginosa clinically significant?. J Cyst Fibros 2015; 14:347–352 [View Article]
    [Google Scholar]
  56. Waine DJ, Honeybourne D, Smith EG, Whitehouse JL, Dowson CG. Association between hypermutator phenotype, clinical variables, mucoid phenotype, and antimicrobial resistance in Pseudomonas aeruginosa . J Clin Microbiol 2008; 46:3491–3493 [View Article]
    [Google Scholar]
  57. Ferroni A, Guillemot D, Moumile K, Bernede C, Le Bourgeois M et al. Effect of mutator P. aeruginosa on antibiotic resistance acquisition and respiratory function in cystic fibrosis. Pediatr Pulmonol 2009; 44:820–825 [View Article]
    [Google Scholar]
  58. Wang K, Chen Y-Q, Salido MM, Kohli GS, Kong J-L et al. The rapid in vivo evolution of Pseudomonas aeruginosa in ventilator-associated pneumonia patients leads to attenuated virulence. Open Biol 2017; 7:170029 [View Article][PubMed]
    [Google Scholar]
  59. Persyn E, Sassi M, Aubry M, Broly M, Delanou S et al. Rapid genetic and phenotypic changes in Pseudomonas aeruginosa clinical strains during ventilator-associated pneumonia. Sci Rep 2019; 9:4720 [View Article]
    [Google Scholar]
  60. Fischer S, Klockgether J, Morán Losada P, Chouvarine P, Cramer N et al. Intraclonal genome diversity of the major Pseudomonas aeruginosa clones C and PA14. Environ Microbiol Rep 2016; 8:227–234 [View Article]
    [Google Scholar]
  61. Wiehlmann L, Wagner G, Cramer N, Siebert B, Gudowius P et al. Population structure of Pseudomonas aeruginosa . Proc Natl Acad Sci USA 2007; 104:8101–8106 [View Article]
    [Google Scholar]
  62. Damkiaer S, Yang L, Molin S, Jelsbak L. Evolutionary remodeling of global regulatory networks during long-term bacterial adaptation to human hosts. Proc Natl Acad Sci USA 2013; 110:7766–7771 [View Article]
    [Google Scholar]
  63. Feltner JB, Wolter DJ, Pope CE, Groleau M-C, Smalley NE et al. LasR variant cystic fibrosis isolates reveal an adaptable quorum-sensing hierarchy in Pseudomonas aeruginosa . mBio 2016; 7:e01513-16 [View Article][PubMed]
    [Google Scholar]
  64. Chen R, Déziel E, Groleau M-C, Schaefer AL, Greenberg EP. Social cheating in a Pseudomonas aeruginosa quorum-sensing variant. Proc Natl Acad Sci USA 2019; 116:7021–7026 [View Article]
    [Google Scholar]
  65. Kostylev M, Kim DY, Smalley NE, Salukhe I, Greenberg EP et al. Evolution of the Pseudomonas aeruginosa quorum-sensing hierarchy. Proc Natl Acad Sci USA 2019; 116:7027–7032 [View Article]
    [Google Scholar]
  66. Cruz RL, Asfahl KL, Van den Bossche S, Coenye T, Crabbé A. RhlR-regulated acyl-homoserine lactone quorum sensing in a cystic fibrosis isolate of Pseudomonas aeruginosa . mMBio 2020; 11:e00532-20 [View Article]
    [Google Scholar]
  67. Jorth P, Staudinger BJ, Wu X, Hisert KB, Hayden H et al. Regional isolation drives bacterial diversification within cystic fibrosis lungs. Cell Host Microbe 2015; 18:307–319 [View Article]
    [Google Scholar]
  68. Williams D, Evans B, Haldenby S, Walshaw MJ, Brockhurst MA et al. Divergent, coexisting Pseudomonas aeruginosa lineages in chronic cystic fibrosis lung infections. Am J Respir Crit Care Med 2015; 191:775–785 [View Article]
    [Google Scholar]
  69. Williams D, Fothergill JL, Evans B, Caples J, Haldenby S et al. Transmission and lineage displacement drive rapid population genomic flux in cystic fibrosis airway infections of a Pseudomonas aeruginosa epidemic strain. Microb Genom 2018; 4:000167 [View Article][PubMed]
    [Google Scholar]
  70. Anthony M, Rose B, Pegler MB, Elkins M, Service H et al. Genetic analysis of Pseudomonas aeruginosa isolates from the sputa of Australian adult cystic fibrosis patients. J Clin Microbiol 2002; 40:2772–2778 [View Article]
    [Google Scholar]
  71. Bragonzi A, Wiehlmann L, Klockgether J, Cramer N, Worlitzsch D et al. Sequence diversity of the mucABD locus in Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology 2006; 152:3261–3269 [View Article]
    [Google Scholar]
  72. Ciofu O, Lee B, Johannesson M, Hermansen NO, Meyer P et al. Investigation of the algT operon sequence in mucoid and non-mucoid Pseudomonas aeruginosa isolates from 115 Scandinavian patients with cystic fibrosis and in 88 in vitro non-mucoid revertants. Microbiology 2008; 154:103–113 [View Article]
    [Google Scholar]
  73. Pulcrano G, Iula DV, Raia V, Rossano F, Catania MR. Different mutations in mucA gene of Pseudomonas aeruginosa mucoid strains in cystic fibrosis patients and their effect on algU gene expression. New Microbiol 2012; 35:295–305
    [Google Scholar]
  74. Candido Caçador N, Paulino da Costa Capizzani C, Gomes Monteiro Marin Torres LA, Galetti R, Ciofu O et al. Adaptation of Pseudomonas aeruginosa to the chronic phenotype by mutations in the algTmucABD operon in isolates from Brazilian cystic fibrosis patients. PLoS One 2018; 13:e0208013 [View Article][PubMed]
    [Google Scholar]
  75. Panmanee W, Su S, Schurr MJ, Lau GW, Zhu X et al. The anti-sigma factor MucA of Pseudomonas aeruginosa: dramatic differences of a mucA22 vs. a ΔmucA mutant in anaerobic acidified nitrite sensitivity of planktonic and biofilm bacteria in vitro and during chronic murine lung infection. PLoS One 2019; 14:e0216401 [View Article]
    [Google Scholar]
  76. Brule CE, Grayhack EJ. Synonymous codons: choose wisely for expression. Trends Genet 2017; 33:283–297 [View Article]
    [Google Scholar]
  77. Kristofich J, Morgenthaler AB, Kinney WR, Ebmeier CC, Snyder DJ et al. Synonymous mutations make dramatic contributions to fitness when growth is limited by a weak-link enzyme. PLoS Genet 2018; 14:e1007615 [View Article]
    [Google Scholar]
  78. Bailey SF, Hinz A, Kassen R. Adaptive synonymous mutations in an experimentally evolved Pseudomonas fluorescens population. Nat Commun 2014; 5:4076 [View Article]
    [Google Scholar]
  79. Lebeuf-Taylor E, McCloskey N, Bailey SF, Hinz A, Kassen R. The distribution of fitness effects among synonymous mutations in a gene under directional selection. Elife 2019; 8:e45952 [View Article][PubMed]
    [Google Scholar]
  80. Thorpe HA, Bayliss SC, Hurst LD, Feil EJ. Comparative analyses of selection operating on nontranslated intergenic regions of diverse bacterial species. Genetics 2017; 206:363–376 [View Article]
    [Google Scholar]
  81. Khademi SMH, Sazinas P, Jelsbak L. Within-host adaptation mediated by intergenic evolution in Pseudomonas aeruginosa . Genome Biol Evol 2019; 11:1385–1397 [View Article]
    [Google Scholar]
  82. Ernst RK, D′Argenio DA, Ichikawa JK, Bangera MG, Selgrade S et al. Genome mosaicism is conserved but not unique in Pseudomonas aeruginosa isolates from the airways of young children with cystic fibrosis. Environ Microbiol 2003; 5:1341–1349 [View Article]
    [Google Scholar]
  83. Huse HK, Kwon T, Zlosnik JEA, Speert DP, Marcotte EM et al. Parallel evolution in Pseudomonas aeruginosa over 39,000 generations in vivo. mBio 2010; 1:e00199-10 [View Article][PubMed]
    [Google Scholar]
  84. Rau MH, Hansen SK, Johansen HK, Thomsen LE, Workman CT et al. 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 2010; 12:1643–1658
    [Google Scholar]
  85. Lee B, Schjerling CK, Kirkby N, Hoffmann N, Borup R et al. Mucoid Pseudomonas aeruginosa isolates maintain the biofilm formation capacity and the gene expression profiles during the chronic lung infection of CF patients. APMIS 2011; 119:263–274 [View Article]
    [Google Scholar]
  86. Schuster M, Lostroh CP, Ogi T, Greenberg EP. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 2003; 185:2066–2079 [View Article][PubMed]
    [Google Scholar]
  87. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 2003; 185:2080–2095 [View Article]
    [Google Scholar]
  88. Damron FH, Owings JP, Okkotsu Y, Varga JJ, Schurr JR et al. Analysis of the Pseudomonas aeruginosa regulon controlled by the sensor kinase KinB and sigma factor RpoN. J Bacteriol 2012; 194:1317–1330 [View Article]
    [Google Scholar]
  89. Schultz A, Stick S. Early pulmonary inflammation and lung damage in children with cystic fibrosis: early inflammation and lung damage in CF. Respirology 2015; 20:569–578
    [Google Scholar]
  90. Gifford AH, Willger SD, Dolben EL, Moulton LA, Dorman DB et al. Use of a multiplex transcript method for analysis of Pseudomonas aeruginosa gene expression profiles in the cystic fibrosis lung. Infect Immun 2016; 84:2995–3006 [View Article]
    [Google Scholar]
  91. Rossi E, Falcone M, Molin S, Johansen HK. High-resolution in situ transcriptomics of Pseudomonas aeruginosa unveils genotype independent patho-phenotypes in cystic fibrosis lungs. Nat Commun 2018; 9:3459 [View Article]
    [Google Scholar]
  92. Cornforth DM, Dees JL, Ibberson CB, Huse HK, Mathiesen IH et al. Pseudomonas aeruginosa transcriptome during human infection. Proc Natl Acad Sci USA 2018; 115:E5125–E5134 [View Article]
    [Google Scholar]
  93. Kordes A, Preusse M, Willger SD, Braubach P, Jonigk D et al. Genetically diverse Pseudomonas aeruginosa populations display similar transcriptomic profiles in a cystic fibrosis explanted lung. Nat Commun 2019; 10:3397 [View Article]
    [Google Scholar]
  94. Kumar SS, Tandberg JI, Penesyan A, Elbourne LDH, Suarez-Bosche N et al. Dual transcriptomics of host-pathogen interaction of cystic fibrosis isolate Pseudomonas aeruginosa PASS1 with zebrafish. Front Cell Infect Microbiol 2018; 8:406 [View Article]
    [Google Scholar]
  95. Damron FH, Oglesby-Sherrouse AG, Wilks A, Barbier M. Dual-seq transcriptomics reveals the battle for iron during Pseudomonas aeruginosa acute murine pneumonia. Sci Rep 2016; 16:39172
    [Google Scholar]
  96. Hare NJ, Cordwell SJ. Proteomics of bacterial pathogens: Pseudomonas aeruginosa infections in cystic fibrosis - a case study. Proteomics Clin Appl 2010; 4:228–248 [View Article][PubMed]
    [Google Scholar]
  97. Kamath KS, Kumar SS, Kaur J, Venkatakrishnan V, Paulsen IT et al. Proteomics of hosts and pathogens in cystic fibrosis. Proteomics Clin Appl 2015; 9:134–146 [View Article]
    [Google Scholar]
  98. Penesyan A, Kumar SS, Kamath K, Shathili AM, Venkatakrishnan V et al. Genetically and phenotypically distinct Pseudomonas aeruginosa cystic fibrosis isolates share a core proteomic signature. PLoS One 2015; 10:e0138527 [View Article]
    [Google Scholar]
  99. Kamath KS, Pascovici D, Penesyan A, Goel A, Venkatakrishnan V et al. Pseudomonas aeruginosa cell membrane protein expression from phenotypically diverse cystic fibrosis isolates demonstrates host-specific adaptations. J Proteome Res 2016; 15:2152–2163 [View Article][PubMed]
    [Google Scholar]
  100. Kamath KS, Krisp C, Chick J, Pascovici D, Gygi SP et al. Pseudomonas aeruginosa proteome under hypoxic stress conditions mimicking the cystic fibrosis lung. J Proteome Res 2017; 16:3917–3928 [View Article]
    [Google Scholar]
  101. Wu X, Siehnel RJ, Garudathri J, Staudinger BJ, Hisert KB et al. In vivo proteome of Pseudomonas aeruginosa in airways of cystic fibrosis patients. J Proteome Res 2019; 18:2601–2612 [View Article][PubMed]
    [Google Scholar]
  102. Hare NJ, Solis N, Harmer C, Marzook NB, Rose B et al. Proteomic profiling of Pseudomonas aeruginosa AES-1R, PAO1 and PA14 reveals potential virulence determinants associated with a transmissible cystic fibrosis-associated strain. BMC Microbiol 2012; 12:16 [View Article][PubMed]
    [Google Scholar]
  103. Hare NJ, Soe CZ, Rose B, Harbour C, Codd R et al. Proteomics of Pseudomonas aeruginosa Australian epidemic strain 1 (AES-1) cultured under conditions mimicking the cystic fibrosis lung reveals increased iron acquisition via the siderophore pyochelin. J Proteome Res 2012; 11:776–795 [View Article][PubMed]
    [Google Scholar]
  104. Sousa AM, Pereira MO. Pseudomonas aeruginosa diversification during infection development in cystic fibrosis lungs – a review. Pathogens 2014; 3:680–703 [View Article][PubMed]
    [Google Scholar]
  105. Klockgether J, Miethke N, Kubesch P, Bohn Y-S, Brockhausen I et al. Intraclonal diversity of the Pseudomonas aeruginosa cystic fibrosis airway isolates TBCF10839 and TBCF121838: distinct signatures of transcriptome, proteome, metabolome, adherence and pathogenicity despite an almost identical genome sequence. Environ Microbiol 2013; 15:191–210 [View Article][PubMed]
    [Google Scholar]
  106. Faure E, Kwong K, Nguyen D. Pseudomonas aeruginosa in chronic lung infections: how to adapt within the host?. Front Immunol 2018; 9:2416 [View Article][PubMed]
    [Google Scholar]
  107. La Rosa R, Johansen HK, Molin S. Adapting to the airways: metabolic requirements of Pseudomonas aeruginosa during the infection of cystic fibrosis patients. Metabolites 2019; 9:234 [View Article][PubMed]
    [Google Scholar]
  108. Riquelme SA, Wong Fok Lung T, Prince A. Pulmonary pathogens adapt to immune signaling metabolites in the airway. Front Immunol 2020; 11:385 [View Article][PubMed]
    [Google Scholar]
  109. Schick A, Kassen R. Rapid diversification of Pseudomonas aeruginosa in cystic fibrosis lung-like conditions. Proc Natl Acad Sci USA 2018; 115:10714–10719 [View Article][PubMed]
    [Google Scholar]
  110. La Rosa R, Johansen HK, Molin S. Convergent metabolic specialization through distinct evolutionary paths in Pseudomonas aeruginosa . mBio 2018; 9:e00269-18 [View Article][PubMed]
    [Google Scholar]
  111. Palmer KL, Aye LM, Whiteley M. Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J Bacteriol 2007; 189:8079–8087 [View Article][PubMed]
    [Google Scholar]
  112. Barth AL, Pitt TL. The high amino-acid content of sputum from cystic fibrosis patients promotes growth of auxotrophic Pseudomonas aeruginosa . J Med Microbiol 1996; 45:110–119 [View Article][PubMed]
    [Google Scholar]
  113. Kumar SS, Penesyan A, Elbourne LDH, Gillings MR, Paulsen IT. Catabolism of nucleic acids by a cystic fibrosis Pseudomonas aeruginosa isolate: an adaptive pathway to cystic fibrosis sputum environment. Front Microbiol 2019; 10:1199 [View Article][PubMed]
    [Google Scholar]
  114. Cramer N, Fischer S, Hedtfeld S, Dorda M, Tümmler B. Intraclonal competitive fitness of longitudinal cystic fibrosis Pseudomonas aeruginosa airway isolates in liquid cultures. Environ Microbiol 2020; 22:25362549 [View Article][PubMed]
    [Google Scholar]
  115. Evans TJ. Small colony variants of Pseudomonas aeruginosa in chronic bacterial infection of the lung in cystic fibrosis. Future Microbiol 2015; 10:231–239 [View Article][PubMed]
    [Google Scholar]
  116. Mangiaterra G, Amiri M, Di Cesare A, Pasquaroli S, Manso E et al. Detection of viable but non-culturable Pseudomonas aeruginosa in cystic fibrosis by qPCR: a validation study. BMC Infect Dis 2018; 18:701 [View Article][PubMed]
    [Google Scholar]
  117. Al Ahmar R, Kirby BD, Yu HD. Culture of small colony variant of Pseudomonas aeruginosa and quantitation of its alginate. J Vis Exp 2020; 156:e60466 [View Article][PubMed]
    [Google Scholar]
  118. López-Causapé C, Cabot G, Del Barrio-Tofiño E, Oliver A. The versatile mutational resistome of Pseudomonas aeruginosa . Front Microbiol 2018; 9:685 [View Article][PubMed]
    [Google Scholar]
  119. Suresh M, Nithya N, Jayasree PR, Vimal KP, Manish Kumar PR. Mutational analyses of regulatory genes, mexR, nalC, nalD and mexZ of mexAB-oprM and mexXY operons, in efflux pump hyperexpressing multidrug-resistant clinical isolates of Pseudomonas aeruginosa . World J Microbiol Biotechnol 2018; 34:83 [View Article][PubMed]
    [Google Scholar]
  120. Huszczynski SM, Lam JS, Khursigara CM. The role of Pseudomonas aeruginosa lipopolysaccharide in bacterial pathogenesis and physiology. Pathogens 2019; 9:6 [View Article][PubMed]
    [Google Scholar]
  121. Maldonado RF, Sá-Correia I, Valvano MA. Lipopolysaccharide modification in Gram-negative bacteria during chronic infection. FEMS Microbiol Rev 2016; 40:480–493 [View Article][PubMed]
    [Google Scholar]
  122. Bricio-Moreno L, Sheridan VH, Goodhead I, Armstrong S, Wong JKL et al. Evolutionary trade-offs associated with loss of PmrB function in host-adapted Pseudomonas aeruginosa . Nat Commun 2018; 9:2635 [View Article][PubMed]
    [Google Scholar]
  123. Poon KKH, Westman EL, Vinogradov E, Jin S, Lam JS. Functional characterization of MigA and WapR: putative rhamnosyltransferases involved in outer core oligosaccharide biosynthesis of Pseudomonas aeruginosa . J Bacteriol 2008; 190:1857–1865 [View Article][PubMed]
    [Google Scholar]
  124. Dößelmann B, Willmann M, Steglich M, Bunk B, Nübel U et al. Rapid and consistent evolution of colistin resistance in extensively drug-resistant Pseudomonas aeruginosa during morbidostat culture. Antimicrob Agents Chemother 2017; 61:e00043-17 [View Article][PubMed]
    [Google Scholar]
  125. Cullen L, Weiser R, Olszak T, Maldonado RF, Moreira AS et al. Phenotypic characterization of an international Pseudomonas aeruginosa reference panel: strains of cystic fibrosis (CF) origin show less in vivo virulence than non-CF strains. Microbiology 2015; 161:1961–1977 [View Article][PubMed]
    [Google Scholar]
  126. Römling U, Fiedler B, Bosshammer J, Grothues D, Greipel J et al. Epidemiology of chronic Pseudomonas aeruginosa infections in cystic fibrosis. J Infect Dis 1994; 170:1616–1621 [View Article][PubMed]
    [Google Scholar]
  127. Ghoul M, West SA, Johansen HK, Molin S, Harrison OB et al. Bacteriocin-mediated competition in cystic fibrosis lung infections. Proc Biol Sci 2015; 282:20150972 [View Article][PubMed]
    [Google Scholar]
  128. Redero M, López-Causapé C, Aznar J, Oliver A, Blázquez J et al. Susceptibility to R-pyocins of Pseudomonas aeruginosa clinical isolates from cystic fibrosis patients. J Antimicrob Chemother 2018; 73:2770–2776 [View Article][PubMed]
    [Google Scholar]
  129. Franklin MJ, Nivens DE, Weadge JT, Howell PL. Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front Microbiol 2011; 2:167 [View Article][PubMed]
    [Google Scholar]
  130. Colvin KM, Irie Y, Tart CS, Urbano R, Whitney JC et al. The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ Microbiol 2012; 14:1913–1928 [View Article][PubMed]
    [Google Scholar]
  131. Colvin KM, Gordon VD, Murakami K, Borlee BR, Wozniak DJ et al. The Pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa . PLoS Pathog 2011; 7:e1001264 [View Article][PubMed]
    [Google Scholar]
  132. Billings N, Millan M, Caldara M, Rusconi R, Tarasova Y et al. The extracellular matrix component Psl provides fast-acting antibiotic defense in Pseudomonas aeruginosa biofilms. PLoS Pathog 2013; 9:e1003526 [View Article][PubMed]
    [Google Scholar]
  133. Harrison JJ, Almblad H, Irie Y, Wolter DJ, Eggleston HC et al. Elevated exopolysaccharide levels in Pseudomonas aeruginosa flagellar mutants have implications for biofilm growth and chronic infections. PLoS Genet 2020; 16:e1008848 [View Article][PubMed]
    [Google Scholar]
  134. Starkey M, Hickman JH, Ma L, Zhang N, De Long S et al. Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol 2009; 191:3492–3503 [View Article][PubMed]
    [Google Scholar]
  135. Henry RL, Mellis CM, Petrovic L. Mucoid Pseudomonas aeruginosa is a marker of poor survival in cystic fibrosis. Pediatr Pulmonol 1992; 12:158–161 [View Article][PubMed]
    [Google Scholar]
  136. Parad RB, Gerard CJ, Zurakowski D, Nichols DP, Pier GB. Pulmonary outcome in cystic fibrosis is influenced primarily by mucoid Pseudomonas aeruginosa infection and immune status and only modestly by genotype. Infect Immun 1999; 67:4744–4750 [View Article][PubMed]
    [Google Scholar]
  137. Hengzhuang W, Wu H, Ciofu O, Song Z, Høiby N. Pharmacokinetics/pharmacodynamics of colistin and imipenem on mucoid and nonmucoid Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 2011; 55:4469–4474 [View Article][PubMed]
    [Google Scholar]
  138. Malhotra S, Hayes D, Wozniak DJ. Mucoid Pseudomonas aeruginosa and regional inflammation in the cystic fibrosis lung. J Cyst Fibros 2019; 18:796–803 [View Article][PubMed]
    [Google Scholar]
  139. Cornelis P, Dingemans J. Pseudomonas aeruginosa adapts its iron uptake strategies in function of the type of infections. Front Cell Infect Microbiol 2013; 3:75 [View Article][PubMed]
    [Google Scholar]
  140. Minandri F, Imperi F, Frangipani E, Bonchi C, Visaggio D et al. Role of iron uptake systems in Pseudomonas aeruginosa virulence and airway infection. Infect Immun 2016; 84:2324–2335 [View Article][PubMed]
    [Google Scholar]
  141. Marvig RL, Damkiær S, Khademi SMH, Markussen TM, Molin S et al. Within-host evolution of Pseudomonas aeruginosa reveals adaptation toward iron acquisition from hemoglobin. mBio 2014; 5:e00966-14 [View Article][PubMed]
    [Google Scholar]
  142. Ballarini A, Scalet G, Kos M, Cramer N, Wiehlmann L et al. Molecular typing and epidemiological investigation of clinical populations of Pseudomonas aeruginosa using an oligonucleotide-microarray. BMC Microbiol 2012; 12:152 [View Article][PubMed]
    [Google Scholar]
  143. Shaver CM, Hauser AR. Relative contributions of Pseudomonas aeruginosa ExoU, ExoS, and ExoT to virulence in the lung. Infect Immun 2004; 72:6969–6977 [View Article][PubMed]
    [Google Scholar]
  144. Sawa T, Shimizu M, Moriyama K, Wiener-Kronish JP. Association between Pseudomonas aeruginosa type III secretion, antibiotic resistance, and clinical outcome: a review. Crit Care 2014; 18:668 [View Article][PubMed]
    [Google Scholar]
  145. Sarges EDSNF, Rodrigues YC, Furlaneto IP, de Melo MVH, Brabo GLDC et al. Pseudomonas aeruginosa type III secretion system virulotypes and their association with clinical features of cystic fibrosis patients. Infect Drug Resist 2020; 13:3771–3781 [View Article][PubMed]
    [Google Scholar]
  146. Tognon M, Köhler T, Gdaniec BG, Hao Y, Lam JS et al. Co-evolution with Staphylococcus aureus leads to lipopolysaccharide alterations in Pseudomonas aeruginosa . ISME J 2017; 11:2233–2243 [View Article][PubMed]
    [Google Scholar]
  147. Zhao K, Du L, Lin J, Yuan Y, Wang X et al. Pseudomonas aeruginosa quorum-sensing and type vi secretion system can direct interspecific coexistence during evolution. Front Microbiol 2018; 9:2287 [View Article][PubMed]
    [Google Scholar]
  148. Diggle SP, Griffin AS, Campbell GS, West SA. Cooperation and conflict in quorum-sensing bacterial populations. Nature 2007; 450:411–414 [View Article][PubMed]
    [Google Scholar]
  149. Sandoz KM, Mitzimberg SM, Schuster M. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci USA 2007; 104:15876–15881 [View Article][PubMed]
    [Google Scholar]
  150. Dandekar AA, Chugani S, Greenberg EP. Bacterial quorum sensing and metabolic incentives to cooperate. Science 2012; 338:264–266 [View Article][PubMed]
    [Google Scholar]
  151. Tashiro Y, Yawata Y, Toyofuku M, Uchiyama H, Nomura N. Interspecies interaction between Pseudomonas aeruginosa and other microorganisms. Microbes Environ 2013; 28:13–24 [View Article][PubMed]
    [Google Scholar]
  152. Sana TG, Berni B, Bleves S. The T6SSs of Pseudomonas aeruginosa strain PAO1 and their effectors: beyond bacterial-cell targeting. Front Cell Infect Microbiol 2016; 6:61 [View Article][PubMed]
    [Google Scholar]
  153. Nguyen AT, Oglesby-Sherrouse AG. Interactions between Pseudomonas aeruginosa and Staphylococcus aureus during co-cultivations and polymicrobial infections. Appl Microbiol Biotechnol 2016; 100:6141–6148 [View Article][PubMed]
    [Google Scholar]
  154. Hotterbeekx A, Kumar-Singh S, Goossens H, Malhotra-Kumar S. In vivo and In vitro interactions between Pseudomonas aeruginosa and Staphylococcus spp. Front Cell Infect Microbiol 2017; 7:106 [View Article][PubMed]
    [Google Scholar]
  155. Fourie R, Pohl CH. Beyond Antagonism: The Interaction Between Candida Species and Pseudomonas aeruginosa . J Fungi 2019; 5:34 [View Article][PubMed]
    [Google Scholar]
  156. Baldan R, Cigana C, Testa F, Bianconi I, De Simone M et al. Adaptation of Pseudomonas aeruginosa in cystic fibrosis airways influences virulence of Staphylococcus aureus in vitro and murine models of co-infection. PLoS One 2014; 9:e89614 [View Article][PubMed]
    [Google Scholar]
  157. Michelsen CF, Christensen A-MJ, Bojer MS, Høiby N, Ingmer H et al. Staphylococcus aureus alters growth activity, autolysis, and antibiotic tolerance in a human host-adapted Pseudomonas aeruginosa lineage. J Bacteriol 2014; 196:3903–3911 [View Article][PubMed]
    [Google Scholar]
  158. Frydenlund Michelsen C, Hossein Khademi SM, Krogh Johansen H, Ingmer H, Dorrestein PC et al. Evolution of metabolic divergence in Pseudomonas aeruginosa during long-term infection facilitates a proto-cooperative interspecies interaction. ISME J 2016; 10:1323–1336 [View Article][PubMed]
    [Google Scholar]
  159. Briaud P, Camus L, Bastien S, Doléans-Jordheim A, Vandenesch F et al. Coexistence with Pseudomonas aeruginosa alters Staphylococcus aureus transcriptome, antibiotic resistance and internalization into epithelial cells. Sci Rep 2019; 9:16564 [View Article][PubMed]
    [Google Scholar]
  160. Camus L, Briaud P, Bastien S, Elsen S, Doléans-Jordheim A et al. Trophic cooperation promotes bacterial survival of Staphylococcus aureus and Pseudomonas aeruginosa . ISME J 2020; 14:3093–3105 [View Article][PubMed]
    [Google Scholar]
  161. Flynn JM, Cameron LC, Wiggen TD, Dunitz JM, Harcombe WR et al. Disruption of cross-feeding inhibits pathogen growth in the sputa of patients with cystic fibrosis. mSphere 2020; 5:e00343-20 [View Article][PubMed]
    [Google Scholar]
  162. Scott JE, O’Toole GA. The yin and yang of Streptococcus lung infections in cystic fibrosis: a model for studying polymicrobial interactions. J Bacteriol 2019; 201:e00115-19 [View Article]
    [Google Scholar]
  163. Cigana C, Bianconi I, Baldan R, De Simone M, Riva C et al. Staphylococcus aureus impacts Pseudomonas aeruginosa chronic respiratory disease in murine models. J Infect Dis 2018; 217:933–942 [View Article][PubMed]
    [Google Scholar]
  164. Granchelli AM, Adler FR, Keogh RH, Kartsonaki C, Cox DR. Microbial interactions in the cystic fibrosis airway. J Clin Microbiol 2018; 56:e00354-18 [View Article][PubMed]
    [Google Scholar]
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