1887

Abstract

Pseudomonas aeruginosa is a highly adaptive opportunistic pathogen that can have serious health consequences in patients with lung disorders. Taxonomic outliers of P. aeruginosa of environmental origin have recently emerged as infectious for humans. Here, we present the first genome-wide analysis of an isolate that caused fatal haemorrhagic pneumonia. In two clones, CLJ1 and CLJ3, sequentially recovered from a patient with chronic pulmonary disease, insertion of a mobile genetic element into the P. aeruginosa chromosome affected major virulence-associated phenotypes and led to increased resistance to the antibiotics used to combat the infection. Comparative genome, proteome and transcriptome analyses revealed that this ISL3-family insertion sequence disrupted the genes for flagellar components, type IV pili, O-specific antigens, translesion polymerase and enzymes producing hydrogen cyanide. Seven-fold more insertions were detected in the later isolate, CLJ3, than in CLJ1, some of which modified strain susceptibility to antibiotics by disrupting the genes for the outer-membrane porin OprD and the regulator of β-lactamase expression AmpD. In the Galleria mellonella larvae model, the two strains displayed different levels of virulence, with CLJ1 being highly pathogenic. This study revealed insertion sequences to be major players in enhancing the pathogenic potential of a P. aeruginosa taxonomic outlier by modulating both its virulence and its resistance to antimicrobials, and explains how this bacterium adapts from the environment to a human host.

Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000265
2019-04-04
2019-09-18
Loading full text...

Full text loading...

/deliver/fulltext/mgen/mgen.000265.zip/mgen000265.html?itemId=/content/journal/mgen/10.1099/mgen.0.000265&mimeType=html&fmt=ahah

References

  1. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D et al. Global trends in emerging infectious diseases. Nature 2008;451: 990– 993 [CrossRef] [PubMed]
    [Google Scholar]
  2. Bartoli C, Roux F, Lamichhane JR. Molecular mechanisms underlying the emergence of bacterial pathogens: an ecological perspective. Mol Plant Pathol 2016;17: 303– 310 [CrossRef] [PubMed]
    [Google Scholar]
  3. Diard M, Hardt WD. Evolution of bacterial virulence. FEMS Microbiol Rev 2017;41: 679– 697 [CrossRef] [PubMed]
    [Google Scholar]
  4. Aujoulat F, Roger F, Bourdier A, Lotthé A, Lamy B et al. From environment to man: genome evolution and adaptation of human opportunistic bacterial pathogens. Genes 2012;3: 191– 232 [CrossRef] [PubMed]
    [Google Scholar]
  5. Silby MW, Winstanley C, Godfrey SA, Levy SB, Jackson RW. Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev 2011;35: 652– 680 [CrossRef] [PubMed]
    [Google Scholar]
  6. Xin XF, Kvitko B, He SY. Pseudomonas syringae: what it takes to be a pathogen. Nat Rev Microbiol 2018;16: 316– 328 [CrossRef] [PubMed]
    [Google Scholar]
  7. Cullen L, McClean S. Bacterial adaptation during chronic respiratory infections. Pathogens 2015;4: 66– 89 [CrossRef] [PubMed]
    [Google Scholar]
  8. Folkesson A, Jelsbak L, Yang L, Johansen HK, Ciofu O et al. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol 2012;10: 841– 851 [CrossRef] [PubMed]
    [Google Scholar]
  9. Hilliam Y, Moore MP, Lamont IL, Bilton D, Haworth CS et al. Pseudomonas aeruginosa adaptation and diversification in the non-cystic fibrosis bronchiectasis lung. Eur Respir J 2017;49: 1602108 [CrossRef] [PubMed]
    [Google Scholar]
  10. Marvig RL, Damkiær S, Khademi SM, Markussen TM, Molin S et al. Within-host evolution of Pseudomonas aeruginosa reveals adaptation toward iron acquisition from hemoglobin. mBio 2014;5: e00966 00914 [CrossRef] [PubMed]
    [Google Scholar]
  11. 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 [CrossRef] [PubMed]
    [Google Scholar]
  12. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. PNAS USA 2006;103: 8487– 8492 [CrossRef]
    [Google Scholar]
  13. Kos VN, Déraspe M, McLaughlin RE, Whiteaker JD, Roy PH et al. The resistome of Pseudomonas aeruginosa in relationship to phenotypic susceptibility. Antimicrob Agents Chemother 2015;59: 427– 436 [CrossRef] [PubMed]
    [Google Scholar]
  14. Thrane SW, Taylor VL, Freschi L, Kukavica-Ibrulj I, Boyle B et al. The widespread multidrug-resistant serotype O12 Pseudomonas aeruginosa clone emerged through concomitant horizontal transfer of serotype antigen and antibiotic resistance gene clusters. mBio 2015;6: e01396 01315 [CrossRef] [PubMed]
    [Google Scholar]
  15. Hauser AR. The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat Rev Microbiol 2009;7: 654– 665 [CrossRef] [PubMed]
    [Google Scholar]
  16. Elsen S, Huber P, Bouillot S, Couté Y, Fournier P et al. A type III secretion negative clinical strain of Pseudomonas aeruginosa employs a two-partner secreted exolysin to induce hemorrhagic pneumonia. Cell Host Microbe 2014;15: 164– 176 [CrossRef] [PubMed]
    [Google Scholar]
  17. Roy PH, Tetu SG, Larouche A, Elbourne L, Tremblay S et al. Complete genome sequence of the multiresistant taxonomic outlier Pseudomonas aeruginosa PA7. PLoS One 2010;5: e8842 [CrossRef] [PubMed]
    [Google Scholar]
  18. Selezska K, Kazmierczak M, Müsken M, Garbe J, Schobert M et al. Pseudomonas aeruginosa population structure revisited under environmental focus: impact of water quality and phage pressure. Environ Microbiol 2012;14: 1952– 1967 [CrossRef] [PubMed]
    [Google Scholar]
  19. Wiehlmann L, Cramer N, Tümmler B. Habitat-associated skew of clone abundance in the Pseudomonas aeruginosa population. Environ Microbiol Rep 2015;7: 955– 960 [CrossRef] [PubMed]
    [Google Scholar]
  20. Huber P, Basso P, Reboud E, Attrée I. Pseudomonas aeruginosa renews its virulence factors. Environ Microbiol Rep 2016;8: 564– 571 [CrossRef] [PubMed]
    [Google Scholar]
  21. Reboud E, Basso P, Maillard AP, Huber P, Attrée I. Exolysin shapes the virulence of Pseudomonas aeruginosa clonal outliers. Toxins 2017;9: 364 [CrossRef] [PubMed]
    [Google Scholar]
  22. Reboud E, Elsen S, Bouillot S, Golovkine G, Basso P et al. Phenotype and toxicity of the recently discovered exlA-positive Pseudomonas aeruginosa strains collected worldwide. Environ Microbiol 2016;18: 3425– 3439 [CrossRef] [PubMed]
    [Google Scholar]
  23. Basso P, Wallet P, Elsen S, Soleilhac E, Henry T et al. Multiple Pseudomonas species secrete exolysin-like toxins and provoke Caspase-1-dependent macrophage death. Environ Microbiol 2017;19: 4045– 4064 [CrossRef]
    [Google Scholar]
  24. Huber P, Basso P, Reboud E, Attrée I. Pseudomonas aeruginosa renews its virulence factors. Environ Microbiol Rep 2016;8: 564– 571 [CrossRef] [PubMed]
    [Google Scholar]
  25. Bouillot S, Munro P, Gallet B, Reboud E, Cretin F et al. Pseudomonas aeruginosa Exolysin promotes bacterial growth in lungs, alveolar damage and bacterial dissemination. Sci Rep 2017;7: 2120 [CrossRef] [PubMed]
    [Google Scholar]
  26. Choi KH, Kumar A, Schweizer HP. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 2006;64: 391– 397 [CrossRef] [PubMed]
    [Google Scholar]
  27. Aziz RK, Bartels D, Best AA, Dejongh M, Disz T et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008;9: 75 [CrossRef] [PubMed]
    [Google Scholar]
  28. Winsor GL, Griffiths EJ, Lo R, Dhillon BK, Shay JA et al. Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the Pseudomonas genome database. Nucleic Acids Res 2016;44: D646– D653 [CrossRef] [PubMed]
    [Google Scholar]
  29. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R et al. Circos: an information aesthetic for comparative genomics. Genome Res 2009;19: 1639– 1645 [CrossRef] [PubMed]
    [Google Scholar]
  30. Treepong P, Guyeux C, Meunier A, Couchoud C, Hocquet D et al. panISa: ab initio detection of insertion sequences in bacterial genomes from short read sequence data. Bioinformatics 2018;34: 3795-3800 [CrossRef] [PubMed]
    [Google Scholar]
  31. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv 2013; 1303.3997
    [Google Scholar]
  32. Han K, Tjaden B, Lory S. GRIL-seq provides a method for identifying direct targets of bacterial small regulatory RNA by in vivo proximity ligation. Nat Microbiol 2017;2: 16239 [CrossRef] [PubMed]
    [Google Scholar]
  33. Casabona MG, Vandenbrouck Y, Attree I, Couté Y. Proteomic characterization of Pseudomonas aeruginosa PAO1 inner membrane. Proteomics 2013;13: 2419– 2423 [CrossRef] [PubMed]
    [Google Scholar]
  34. Wieczorek S, Combes F, Lazar C, Giai Gianetto Q, Gatto L et al. DAPAR & ProStaR: software to perform statistical analyses in quantitative discovery proteomics. Bioinformatics 2017;33: 135– 136 [CrossRef] [PubMed]
    [Google Scholar]
  35. Vizcaíno JA, Csordas A, del-Toro N, Dianes JA, Griss J et al. 2016 update of the PRIDE database and its related tools. Nucleic Acids Res 2016;44: D447– D456 [CrossRef] [PubMed]
    [Google Scholar]
  36. Rybtke MT, Borlee BR, Murakami K, Irie Y, Hentzer M et al. Fluorescence-based reporter for gauging cyclic di-GMP levels in Pseudomonas aeruginosa. Appl Environ Microbiol 2012;78: 5060– 5069 [CrossRef] [PubMed]
    [Google Scholar]
  37. Zlosnik JE, Gunaratnam LC, Speert DP. Serum susceptibility in clinical isolates of Burkholderia cepacia complex bacteria: development of a growth-based assay for high throughput determination. Front Cell Infect Microbiol 2012;2: 67 [CrossRef] [PubMed]
    [Google Scholar]
  38. Berry A, Han K, Trouillon J, Robert-Genthon M, Ragno M et al. cAMP and Vfr Control Exolysin Expression and Cytotoxicity of Pseudomonas aeruginosa Taxonomic Outliers. J Bacteriol 2018;200: [CrossRef] [PubMed]
    [Google Scholar]
  39. Mathee K, Narasimhan G, Valdes C, Qiu X, Matewish JM et al. Dynamics of Pseudomonas aeruginosa genome evolution. PNAS USA 2008;105: 3100– 3105 [CrossRef] [PubMed]
    [Google Scholar]
  40. Smith DJ, Park J, Tiedje JM, Mohn WW. A large gene cluster in Burkholderia xenovorans encoding abietane diterpenoid catabolism. J Bacteriol 2007;189: 6195– 6204 [CrossRef] [PubMed]
    [Google Scholar]
  41. Kung VL, Ozer EA, Hauser AR. The accessory genome of Pseudomonas aeruginosa. Microbiol Mol Biol Rev 2010;74: 621– 641 [CrossRef] [PubMed]
    [Google Scholar]
  42. Klockgether J, Cramer N, Wiehlmann L, Davenport CF, Tümmler B. Pseudomonas aeruginosa Genomic Structure and Diversity. Front Microbiol 2011;2: 150 [CrossRef] [PubMed]
    [Google Scholar]
  43. Kus JV, Tullis E, Cvitkovitch DG, Burrows LL. Significant differences in type IV pilin allele distribution among Pseudomonas aeruginosa isolates from cystic fibrosis (CF) versus non-CF patients. Microbiology 2004;150: 1315– 1326 [CrossRef] [PubMed]
    [Google Scholar]
  44. 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 [CrossRef] [PubMed]
    [Google Scholar]
  45. Giraud C, Bernard CS, Calderon V, Yang L, Filloux A et al. The PprA-PprB two-component system activates CupE, the first non-archetypal Pseudomonas aeruginosa chaperone-usher pathway system assembling fimbriae. Environ Microbiol 2011;13: 666– 683 [CrossRef] [PubMed]
    [Google Scholar]
  46. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007;57: 81– 91 [CrossRef] [PubMed]
    [Google Scholar]
  47. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 2006;34: D32– D36 [CrossRef] [PubMed]
    [Google Scholar]
  48. Castro-Jaimes S, Salgado-Camargo AD, Graña-Miraglia L, Lozano L, Bocanegra-Ibarias P et al. Complete genome sequence of a multidrug-resistant Acinetobacter baumannii isolate obtained from a mexican hospital (sequence type 422). Genome Announc 2016;4: [CrossRef] [PubMed]
    [Google Scholar]
  49. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 2017;45: D200– D203 [CrossRef] [PubMed]
    [Google Scholar]
  50. Siguier P, Gourbeyre E, Chandler M. Bacterial insertion sequences: their genomic impact and diversity. FEMS Microbiol Rev 2014;38: 865– 891 [CrossRef] [PubMed]
    [Google Scholar]
  51. Vandecraen J, Chandler M, Aertsen A, van Houdt R. The impact of insertion sequences on bacterial genome plasticity and adaptability. Crit Rev Microbiol 2017;43: 709– 730 [CrossRef] [PubMed]
    [Google Scholar]
  52. Martinez E, Pérez JE, Márquez C, Vilacoba E, Centrón D et al. Emerging and existing mechanisms co-operate in generating diverse β-lactam resistance phenotypes in geographically dispersed and genetically disparate Pseudomonas aeruginosa strains. J Glob Antimicrob Resist 2013;1: 135– 142 [CrossRef] [PubMed]
    [Google Scholar]
  53. Sun Q, Ba Z, Wu G, Wang W, Lin S et al. Insertion sequence ISRP10 inactivation of the oprD gene in imipenem-resistant Pseudomonas aeruginosa clinical isolates. Int J Antimicrob Agents 2016;47: 375– 379 [CrossRef] [PubMed]
    [Google Scholar]
  54. Vassilara F, Galani I, Souli M, Papanikolaou K, Giamarellou H et al. Mechanisms responsible for imipenem resistance among Pseudomonas aeruginosa clinical isolates exposed to imipenem concentrations within the mutant selection window. Diagn Microbiol Infect Dis 2017;88: 276– 281 [CrossRef] [PubMed]
    [Google Scholar]
  55. Wołkowicz T, Patzer JA, Kamińska W, Gierczyński R, Dzierżanowska D. Distribution of carbapenem resistance mechanisms in Pseudomonas aeruginosa isolates among hospitalised children in Poland: characterisation of two novel insertion sequences disrupting the oprD gene. J Glob Antimicrob Resist 2016;7: 119– 125 [CrossRef] [PubMed]
    [Google Scholar]
  56. Lindberg F, Lindquist S, Normark S. Inactivation of the ampD gene causes semiconstitutive overproduction of the inducible Citrobacter freundii beta-lactamase. J Bacteriol 1987;169: 1923– 1928 [CrossRef] [PubMed]
    [Google Scholar]
  57. Pérez-Gallego M, Torrens G, Castillo-vera J, Moya B, Zamorano L et al. Impact of AmpC derepression on fitness and virulence: the mechanism or the pathway?. mBio 2016;7: [CrossRef] [PubMed]
    [Google Scholar]
  58. Lee M, Artola-Recolons C, Carrasco-López C, Martínez-Caballero S, Hesek D et al. Cell-wall remodeling by the zinc-protease AmpDh3 from Pseudomonas aeruginosa. J Am Chem Soc 2013;135: 12604– 12607 [CrossRef] [PubMed]
    [Google Scholar]
  59. Vollmer W, von Rechenberg M, Höltje JV. Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J Biol Chem 1999;274: 6726– 6734 [CrossRef] [PubMed]
    [Google Scholar]
  60. Li XZ, Plésiat P, Nikaido H. The challenge of efflux-mediated antibiotic resistance in Gram-negative bacteria. Clin Microbiol Rev 2015;28: 337– 418 [CrossRef] [PubMed]
    [Google Scholar]
  61. Shah P, Swiatlo E. A multifaceted role for polyamines in bacterial pathogens. Mol Microbiol 2008;68: 4– 16 [CrossRef] [PubMed]
    [Google Scholar]
  62. Dean CR, Goldberg JB. Pseudomonas aeruginosa galU is required for a complete lipopolysaccharide core and repairs a secondary mutation in a PA103 (serogroup O11) wbpM mutant. FEMS Microbiol Lett 2002;210: 277– 283 [CrossRef] [PubMed]
    [Google Scholar]
  63. Priebe GP, Dean CR, Zaidi T, Meluleni GJ, Coleman FT et al. The galU Gene of Pseudomonas aeruginosa is required for corneal infection and efficient systemic spread following pneumonia but not for infection confined to the lung. Infect Immun 2004;72: 4224– 4232 [CrossRef] [PubMed]
    [Google Scholar]
  64. Arora SK, Bangera M, Lory S, Ramphal R. A genomic island in Pseudomonas aeruginosa carries the determinants of flagellin glycosylation. PNAS USA 2001;98: 9342– 9347 [CrossRef] [PubMed]
    [Google Scholar]
  65. Feuillet V, Medjane S, Mondor I, Demaria O, Pagni PP et al. Involvement of toll-like receptor 5 in the recognition of flagellated bacteria. PNAS USA 2006;103: 12487– 12492 [CrossRef] [PubMed]
    [Google Scholar]
  66. Tammam S, Sampaleanu LM, Koo J, Manoharan K, Daubaras M et al. PilMNOPQ from the Pseudomonas aeruginosa type IV pilus system form a transenvelope protein interaction network that interacts with PilA. J Bacteriol 2013;195: 2126– 2135 [CrossRef] [PubMed]
    [Google Scholar]
  67. Basso P, Ragno M, Elsen S, Reboud E, Golovkine G et al. Pseudomonas aeruginosa Pore-Forming exolysin and Type IV Pili cooperate to induce host cell lysis. mBio 2017;8: [CrossRef] [PubMed]
    [Google Scholar]
  68. Borlee BR, Goldman AD, Murakami K, Samudrala R, Wozniak DJ et al. Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 2010;75: 827– 842 [CrossRef] [PubMed]
    [Google Scholar]
  69. Faure LM, Garvis S, de Bentzmann S, Bigot S. Characterization of a novel two-partner secretion system implicated in the virulence of Pseudomonas aeruginosa. Microbiology 2014;160: 1940– 1952 [CrossRef] [PubMed]
    [Google Scholar]
  70. Kida Y, Higashimoto Y, Inoue H, Shimizu T, Kuwano K. A novel secreted protease from Pseudomonas aeruginosa activates NF-kappaB through protease-activated receptors. Cell Microbiol 2008;10: 1491– 1504 [CrossRef] [PubMed]
    [Google Scholar]
  71. Melvin JA, Gaston JR, Phillips SN, Springer MJ, Marshall CW et al. Pseudomonas aeruginosa Contact-Dependent Growth Inhibition Plays Dual Role in Host-Pathogen Interactions. mSphere 2017;2: [CrossRef] [PubMed]
    [Google Scholar]
  72. Mercy C, Ize B, Salcedo SP, de Bentzmann S, Bigot S. Functional characterization of Pseudomonas Contact dependent growth inhibition (CDI) Systems. PLoS One 2016;11: e0147435 [CrossRef] [PubMed]
    [Google Scholar]
  73. Blumer C, Haas D. Iron regulation of the hcnABC genes encoding hydrogen cyanide synthase depends on the anaerobic regulator ANR rather than on the global activator GacA in Pseudomonas fluorescens CHA0. Microbiology 2000;146: 2417– 2424 [CrossRef] [PubMed]
    [Google Scholar]
  74. Carterson AJ, Morici LA, Jackson DW, Frisk A, Lizewski SE et al. The transcriptional regulator AlgR controls cyanide production in Pseudomonas aeruginosa. J Bacteriol 2004;186: 6837– 6844 [CrossRef] [PubMed]
    [Google Scholar]
  75. Carroll W, Lenney W, Wang T, Spanel P, Alcock A et al. Detection of volatile compounds emitted by Pseudomonas aeruginosa using selected ion flow tube mass spectrometry. Pediatr Pulmonol 2005;39: 452– 456 [CrossRef] [PubMed]
    [Google Scholar]
  76. Ryall B, Davies JC, Wilson R, Shoemark A, Williams HD. Pseudomonas aeruginosa, cyanide accumulation and lung function in CF and non-CF bronchiectasis patients. Eur Respir J 2008;32: 740– 747 [CrossRef] [PubMed]
    [Google Scholar]
  77. Frangipani E, Pérez-Martínez I, Williams HD, Cherbuin G, Haas D. A novel cyanide-inducible gene cluster helps protect Pseudomonas aeruginosa from cyanide. Environ Microbiol Rep 2014;6: 28– 34 [CrossRef] [PubMed]
    [Google Scholar]
  78. Hirai T, Osamura T, Ishii M, Arai H. Expression of multiple cbb 3 cytochrome c oxidase isoforms by combinations of multiple isosubunits in Pseudomonas aeruginosa. PNAS USA 2016;113: 12815– 12819
    [Google Scholar]
  79. Firoved AM, Ornatowski W, Deretic V. Microarray analysis reveals induction of lipoprotein genes in mucoid Pseudomonas aeruginosa: implications for inflammation in cystic fibrosis. Infect Immun 2004;72: 5012– 5018 [CrossRef] [PubMed]
    [Google Scholar]
  80. Damron FH, Napper J, Teter MA, Yu HD. Lipotoxin F of Pseudomonas aeruginosa is an AlgU-dependent and alginate-independent outer membrane protein involved in resistance to oxidative stress and adhesion to A549 human lung epithelia. Microbiology 2009;155: 1028– 1038 [CrossRef] [PubMed]
    [Google Scholar]
  81. Fortier LC, Sekulovic O. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 2013;4: 354– 365 [CrossRef] [PubMed]
    [Google Scholar]
  82. Winstanley C, Langille MG, 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 [CrossRef] [PubMed]
    [Google Scholar]
  83. Matsui H, Sano Y, Ishihara H, Shinomiya T. Regulation of pyocin genes in Pseudomonas aeruginosa by positive (prtN) and negative (prtR) regulatory genes. J Bacteriol 1993;175: 1257– 1263 [CrossRef] [PubMed]
    [Google Scholar]
  84. McFarland KA, Dolben EL, Leroux M, Kambara TK, Ramsey KM et al. A self-lysis pathway that enhances the virulence of a pathogenic bacterium. PNAS USA 2015;112: 8433– 8438 [CrossRef] [PubMed]
    [Google Scholar]
  85. Jatsenko T, Sidorenko J, Saumaa S, Kivisaar M. DNA polymerases ImuC and DinB are involved in DNA alkylation damage tolerance in Pseudomonas aeruginosa and Pseudomonas putida. PLoS One 2017;12: e0170719 [CrossRef] [PubMed]
    [Google Scholar]
  86. Oliver A, Cantón R, Campo P, Baquero F, Blázquez J. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 2000;288: 1251– 1253 [CrossRef] [PubMed]
    [Google Scholar]
  87. Boukerb AM, Decor A, Ribun S, Tabaroni R, Rousset A et al. Genomic rearrangements and functional diversification of lecA and lecB lectin-coding regions impacting the efficacy of glycomimetics directed against Pseudomonas aeruginosa. Front Microbiol 2016;7: 811 [CrossRef] [PubMed]
    [Google Scholar]
  88. Boukerb AM, Marti R, Cournoyer B. Genome sequences of three strains of the Pseudomonas aeruginosa PA7 clade. Genome Announc 2015;3: [CrossRef] [PubMed]
    [Google Scholar]
  89. Hilker R, Munder A, Klockgether J, Losada PM, Chouvarine P et al. Interclonal gradient of virulence in the Pseudomonas aeruginosa pangenome from disease and environment. Environ Microbiol 2015;17: 29– 46 [CrossRef] [PubMed]
    [Google Scholar]
  90. 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 [CrossRef] [PubMed]
    [Google Scholar]
  91. Gaffé J, McKenzie C, Maharjan RP, Coursange E, Ferenci T et al. Insertion sequence-driven evolution of Escherichia coli in chemostats. J Mol Evol 2011;72: 398– 412 [CrossRef] [PubMed]
    [Google Scholar]
  92. Raeside C, Gaffé J, Deatherage DE, Tenaillon O, Briska AM et al. Large chromosomal rearrangements during a long-term evolution experiment with Escherichia coli. mBio 2014;5: e01377 01314 [CrossRef] [PubMed]
    [Google Scholar]
  93. 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 [CrossRef] [PubMed]
    [Google Scholar]
  94. Roach DJ, Burton JN, Lee C, Stackhouse B, Butler-Wu SM et al. A year of infection in the intensive care unit: prospective whole genome sequencing of bacterial clinical isolates reveals cryptic transmissions and novel microbiota. PLoS Genet 2015;11: e1005413 [CrossRef] [PubMed]
    [Google Scholar]
  95. Vincent AT, Freschi L, Jeukens J, Kukavica-Ibrulj I, Emond-Rheault JG et al. Genomic characterisation of environmental Pseudomonas aeruginosa isolated from dental unit waterlines revealed the insertion sequence ISPa11 as a chaotropic element. FEMS Microbiol Ecol 2017;93: [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000265
Loading
/content/journal/mgen/10.1099/mgen.0.000265
Loading

Data & Media loading...

Supplementary File 1

PDF

Supplementary File 2

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error