Genome Analysis of a Transmissible Lineage of Pseudomonas aeruginosa Reveals Pathoadaptive Mutations and Distinct Evolutionary Paths of Hypermutators

PLoS Genetics

Volumn 9, Issue 9, 2013, Pages

  Marvig, Rasmus Lykke ^a   Johansen, Helle Krogh ^a,b   Molin, Søren ^a   Jelsbak, Lars ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b Rigshospitalet   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIUM ISOLATE; BACTERIUM ISOLATION; CELL LINEAGE; CLINICAL ARTICLE; CLONE; CONTROLLED STUDY; CYSTIC FIBROSIS; DANISH; DISEASE TRANSMISSION; DK2 GENE; ETHNIC GROUP; GENE IDENTIFICATION; GENE MUTATION; GENE SEQUENCE; GENE TARGETING; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENOME; HOMOZYGOTE; HUMAN; HYPERMUTATOR GENE; MUTL GENE; MUTS GENE; MUTY GENE; NONHUMAN; PATHOADAPTIVE MUTATION; PATHOGENESIS; PHYLOGENY; PREVALENCE; PSEUDOMONAS AERUGINOSA; RETROSPECTIVE STUDY;

CYSTIC FIBROSIS; DRUG RESISTANCE, MICROBIAL; EVOLUTION, MOLECULAR; GENOME; HUMANS; MUTATION; MUTATION RATE; PHENOTYPE; PHYLOGENY; PSEUDOMONAS AERUGINOSA;

EID: 84884679783     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003741     Document Type: Article

References (47)

1. Lieberman TD, Michel JB, Aingaran M, Potter-Bynoe G, Roux D, et al. (2011) Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 43: 1275-1280.
2. Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH, et al. (2011) Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477: 462-465.
3. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, et al. (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A 103: 8487-8492.
4. Harris SR, Clarke IN, Seth-Smith HM, Solomon AW, Cutcliffe LT, et al. (2012) Whole-genome analysis of diverse Chlamydia trachomatis strains identifies phylogenetic relationships masked by current clinical typing. Nat Genet 44: 413-419, S411.
5. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, et al. (2011) Rapid pneumococcal evolution in response to clinical interventions. Science 331: 430-434.
6. Morelli G, Song Y, Mazzoni CJ, Eppinger M, Roumagnac P, et al. (2010) Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nat Genet 42: 1140-1143.
7. Holt KE, Baker S, Weill FX, Holmes EC, Kitchen A, et al. (2012) Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat Genet 44: 1056-1059.
8. Sokurenko EV, Hasty DL, Dykhuizen DE, (1999) Pathoadaptive mutations: gene loss and variation in bacterial pathogens. Trends Microbiol 7: 191-195.
9. Rau MH, Marvig RL, Ehrlich GD, Molin S, Jelsbak L, (2012) Deletion and acquisition of genomic content during early stage adaptation of Pseudomonas aeruginosa to a human host environment. Environ Microbiol 14: 2200-2211.
10. Yang L, Jelsbak L, Marvig RL, Damkiaer S, Workman CT, et al. (2011) Evolutionary dynamics of bacteria in a human host environment. Proc Natl Acad Sci U S A 108: 7481-7486.
11. Oliver A, Canton R, Campo P, Baquero F, Blazquez J, (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288: 1251-1254.
12. Matic I, Radman M, Taddei F, Picard B, Doit C, et al. (1997) Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277: 1833-1834.
13. Mao EF, Lane L, Lee J, Miller JH, (1997) Proliferation of mutators in A cell population. J Bacteriol 179: 417-422.
14. LeClerc JE, Li B, Payne WL, Cebula TA, (1996) High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274: 1208-1211.
15. Richardson AR, Yu Z, Popovic T, Stojiljkovic I, (2002) Mutator clones of Neisseria meningitidis in epidemic serogroup A disease. Proc Natl Acad Sci U S A 99: 6103-6107.
16. Sniegowski PD, Gerrish PJ, Lenski RE, (1997) Evolution of high mutation rates in experimental populations of E. coli. Nature 387: 703-705.
17. Chung JC, Becq J, Fraser L, Schulz-Trieglaff O, Bond NJ, et al. (2012) Genomic Variation among Contemporary Pseudomonas aeruginosa Isolates from Chronically Infected Cystic Fibrosis Patients. J Bacteriol 194: 4857-4866.
18. 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: 1641-1650.
19. Schaaper RM, Dunn RL, (1987) Spectra of spontaneous mutations in Escherichia coli strains defective in mismatch correction: the nature of in vivo DNA replication errors. Proc Natl Acad Sci U S A 84: 6220-6224.
20. Bichara M, Wagner J, Lambert IB, (2006) Mechanisms of tandem repeat instability in bacteria. Mutat Res 598: 144-163.
21. Strand M, Prolla TA, Liskay RM, Petes TD, (1993) Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 365: 274-276.
22. Levinson G, Gutman GA, (1987) High frequencies of short frameshifts in poly-CA/TG tandem repeats borne by bacteriophage M13 in Escherichia coli K-12. Nucleic Acids Res 15: 5323-5338.
23. Moxon ER, Rainey PB, Nowak MA, Lenski RE, (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 4: 24-33.
24. Moyano AJ, Smania AM, (2009) Simple sequence repeats and mucoid conversion: biased mucA mutagenesis in mismatch repair-deficient Pseudomonas aeruginosa. PLoS One 4: e8203.
25. Liberati NT, Urbach JM, Miyata S, Lee DG, Drenkard E, et al. (2006) An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci U S A 103: 2833-2838.
26. Yang L, Haagensen JA, Jelsbak L, Johansen HK, Sternberg C, et al. (2008) In situ growth rates and biofilm development of Pseudomonas aeruginosa populations in chronic lung infections. J Bacteriol 190: 2767-2776.
27. Harris SR, Feil EJ, Holden MT, Quail MA, Nickerson EK, et al. (2010) Evolution of MRSA during hospital transmission and intercontinental spread. Science 327: 469-474.
28. Marvig RL, Sondergaard MS, Damkiaer S, Hoiby N, Johansen HK, et al. (2012) Mutations in 23S rRNA confer resistance against azithromycin in Pseudomonas aeruginosa. Antimicrob Agents Chemother 56: 4519.
29. Severinov K, Markov D, Severinova E, Nikiforov V, Landick R, et al. (1995) Streptolydigin-resistant mutants in an evolutionarily conserved region of the beta' subunit of Escherichia coli RNA polymerase. J Biol Chem 270: 23926-23929.
30. Yee YC, Kisslinger B, Yu VL, Jin DJ, (1996) A mechanism of rifamycin inhibition and resistance in Pseudomonas aeruginosa. J Antimicrob Chemother 38: 133-137.
31. Liao X, Hancock RE, (1995) Cloning and characterization of the Pseudomonas aeruginosa pbpB gene encoding penicillin-binding protein 3. Antimicrob Agents Chemother 39: 1871-1874.
32. Lomovskaya O, Lewis K, (1992) Emr, an Escherichia coli locus for multidrug resistance. Proc Natl Acad Sci U S A 89: 8938-8942.
33. Bielecki P, Lukat P, Husecken K, Dotsch A, Steinmetz H, et al. (2012) Mutation in elongation factor G confers resistance to the antibiotic argyrin in the opportunistic pathogen Pseudomonas aeruginosa. Chembiochem 13: 2339-2345.
34. Hancock RE, (1998) Resistance mechanisms in Pseudomonas aeruginosa and other nonfermentative gram-negative bacteria. Clin Infect Dis 27 Suppl 1: S93-99.
35. Strateva T, Yordanov D, (2009) Pseudomonas aeruginosa- a phenomenon of bacterial resistance. J Med Microbiol 58: 1133-1148.
36. Moskowitz SM, Ernst RK, Miller SI, (2004) PmrAB, a two-component regulatory system of Pseudomonas aeruginosa that modulates resistance to cationic antimicrobial peptides and addition of aminoarabinose to lipid A. J Bacteriol 186: 575-579.
37. Wang Y, Ha U, Zeng L, Jin S, (2003) Regulation of membrane permeability by a two-component regulatory system in Pseudomonas aeruginosa. Antimicrob Agents Chemother 47: 95-101.
38. Nguyen D, Singh PK, (2006) Evolving stealth: genetic adaptation of Pseudomonas aeruginosa during cystic fibrosis infections. Proc Natl Acad Sci U S A 103: 8305-8306.
39. Moskowitz SM, Brannon MK, Dasgupta N, Pier M, Sgambati N, et al. (2012) PmrB mutations promote polymyxin resistance of Pseudomonas aeruginosa isolated from colistin-treated cystic fibrosis patients. Antimicrob Agents Chemother 56: 1019-1030.
40. Philippe N, Crozat E, Lenski RE, Schneider D, (2007) Evolution of global regulatory networks during a long-term experiment with Escherichia coli. Bioessays 29: 846-860.
41. Waine DJ, Honeybourne D, Smith EG, Whitehouse JL, Dowson CG, (2008) Association between hypermutator phenotype, clinical variables, mucoid phenotype, and antimicrobial resistance in Pseudomonas aeruginosa. J Clin Microbiol 46: 3491-3493.
42. Ferroni A, Guillemot D, Moumile K, Bernede C, Le Bourgeois M, et al. (2009) Effect of mutator P. aeruginosa on antibiotic resistance acquisition and respiratory function in cystic fibrosis. Pediatr Pulmonol 44: 820-825.
43. Ciofu O, Riis B, Pressler T, Poulsen HE, Hoiby N, (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: 2276-2282.
44. Hoiby N, Frederiksen B (2000) Microbiology of cystic fibrosis. In: Hodson M, Geddes D, editors. Cystic fibrosis. 2nd ed. London, United Kingdom: Arnold. pp. 83-107.
45. Krawitz P, Rodelsperger C, Jager M, Jostins L, Bauer S, et al. (2010) Microindel detection in short-read sequence data. Bioinformatics 26: 722-729.
46. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
47. Drummond AJ, Suchard MA, Xie D, Rambaut A, (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29: 1969-1973.