Evolutionary insight from whole-genome sequencing of Pseudomonas aeruginosa from cystic fibrosis patients

Future Microbiology

Volumn 10, Issue 4, 2015, Pages 599-611

  Marvig, Rasmus Lykke ^a   Sommer, Lea M ^b,c   Jelsbak, Lars ^b   Molin, Søren ^b,c   Johansen, Helle Krogh ^a,c  

^a University of Copenhagen   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c Chalmers University of Technology   (Denmark)

Author keywords

bacteria; cystic fibrosis; genome sequencing; pathogen evolution; pathogenomics; Pseudomonas aeruginosa

Indexed keywords

BACTERIAL GENOME; CYSTIC FIBROSIS; EVOLUTION; EVOLUTIONARY ADAPTATION; GENE MUTATION; GENOME ANALYSIS; GENOMICS; HUMAN; MORBIDITY; MORTALITY; NONHUMAN; POPULATION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; REVIEW; ADAPTATION; CLASSIFICATION; COMPLICATION; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EVOLUTION; PSEUDOMONAS INFECTION; RESPIRATORY TRACT INFECTION;

PSEUDOMONAS AERUGINOSA;

ADAPTATION, BIOLOGICAL; CYSTIC FIBROSIS; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; HUMANS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RESPIRATORY TRACT INFECTIONS; SEQUENCE ANALYSIS, DNA;

EID: 84927768646     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.15.3     Document Type: Review

References (73)

1. Pallen MJ, Wren BW. Bacterial pathogenomics. Nature 449(7164), 835-842 (2007).
2. Stover CK, Pham XQ, Erwin AL et al. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406(6799), 959-964 (2000).
3. Holloway BW, Krishnapillai V, Morgan AF. Chromosomal genetics of Pseudomonas. Microbiol. Rev. 43(1), 73-102 (1979).
4. Parkhill J. What has high-throughput sequencing ever done for us Nat. Rev. Microbiol. 11(10), 664-665 (2013).
5. Lee DG, Urbach JM, Wu G et al. Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol. 7(10), R90 (2006).
6. Smith EE, Buckley DG, Wu Z et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl Acad. Sci. USA 103(22), 8487-8492 (2006).
7. Winstanley C, Langille MG, Fothergill JL et al. Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool Epidemic Strain of Pseudomonas aeruginosa. Genome Res. 19(1), 12-23 (2009).
8. Roy PH, Tetu SG, Larouche A et al. Complete genome sequence of the multiresistant taxonomic outlier Pseudomonas aeruginosa PA7. PLoS ONE 5(1), e8842 (2010).
9. 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. 14(8), 2200-2211 (2012).
10. Wu DQ, Ye J, Ou HY et al. Genomic analysis and temperature-dependent transcriptome profiles of the rhizosphere originating strain Pseudomonas aeruginosa M18. BMC Genomics 12, 438 (2011).
11. Miyoshi-Akiyama T, Kuwahara T, Tada T, Kitao T, Kirikae T. Complete genome sequence of highly multidrug-resistant Pseudomonas aeruginosa NCGM2.S1, a representative strain of a cluster endemic to Japan. J. Bacteriol. 193(24), 7010 (2011).
12. Jeukens J, Boyle B, Bianconi I et al. Complete genome sequence of persistent cystic fibrosis isolate Pseudomonas aeruginosa strain RP73. Genome Announc. 1(4), pii: e00568 (2013).
13. Cheng K, Smyth RL, Govan JR et al. Spread of beta-lactam-resistant Pseudomonas aeruginosa in a cystic fibrosis clinic. Lancet 348(9028), 639-642 (1996).
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. 9(9), e1003741 (2013).
15. Wiehlmann L, Wagner G, Cramer N et al. Population structure of Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 104(19), 8101-8106 (2007).
16. Mathee K, Narasimhan G, Valdes C et al. Dynamics of Pseudomonas aeruginosa genome evolution. Proc. Natl Acad. Sci. USA 105(8), 3100-3105 (2008).
17. Klockgether J, Cramer N, Wiehlmann L, Davenport CF, Tummler B. Pseudomonas aeruginosa genomic structure and diversity. Front. Microbiol. 2, 150 (2011).
18. Kung VL, Ozer EA, Hauser AR. The accessory genome of Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev. 74(4), 621-641 (2010).
19. Hilker R, Munder A, Klockgether J et al. Interclonal gradient of virulence in the Pseudomonas aeruginosa pangenome from disease and environment. Environ. Microbiol.17(1) 29-46 (2014). representative genomes
20. Koonin EV, Wolf YI. Evolution of microbes and viruses: a paradigm shift in evolutionary biology Front. Cell. Infect. Microbiol. 2, 119 (2012).
21. Stewart RM, Wiehlmann L, Ashelford KE et al. Genetic characterization indicates that a specific subpopulation of Pseudomonas aeruginosa is associated with keratitis infections. J. Clin. Microbiol. 49(3), 993-1003 (2011).
22. Spencer DH, Kas A, Smith EE et al. Whole-genome sequence variation among multiple isolates of Pseudomonas aeruginosa. J. Bacteriol. 185(4), 1316-1325 (2003).
23. Stewart L, Ford A, Sangal V et al. Draft genomes of 12 host-Adapted and environmental isolates of Pseudomonas aeruginosa and their positions in the core genome phylogeny. Pathog. Dis. 71(1), 20-25 (2014).
24. Yang L, Jelsbak L, Marvig RL et al. Evolutionary dynamics of bacteria in a human host environment. Proc. Natl Acad. Sci. USA 108(18), 7481-7486 (2011).
25. Cramer N, Klockgether J, Wrasman K, Schmidt M, Davenport CF, Tummler B. Microevolution of the major common Pseudomonas aeruginosa clones C and PA14 in cystic fibrosis lungs. Environ. Microbiol. 13(7), 1690-1704 (2011).
26. Klockgether J, Miethke N, Kubesch P 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.15(1) 191-200 (2013).
27. Marvig RL, Damkiaer S, Khademi SM, Markussen TM, Molin S, Jelsbak L. Within-host evolution of Pseudomonas aeruginosa reveals adaptation toward iron acquisition from hemoglobin. mBio 5(3), e00966-14 (2014).
28. Marvig RL, Sondergaard MS, Damkiaer S et al. Mutations in 23S rRNA confer resistance against azithromycin in Pseudomonas aeruginosa. Antimicrob. Agents Chemother.56(8), 4519-4521(2012).
29. 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 110(19), 7766-7771 (2013).
30. Markussen T, Marvig RL, Gomez-Lozano M et al. Environmental heterogeneity drives within-host diversification and evolution of Pseudomonas aeruginosa. mBio 5(5), e01592-e01514 (2014).
31. Marvig RL, Sommer LM, Molin S, Johansen HK. Convergent evolution and adaptation of Pseudomonas aeruginosa within patients with cystic fibrosis. Nat. Genet. 47(1), 57-64 (2014).
32. Feliziani S, Marvig RL, Lujan AM et al. Coexistence and within-host evolution of diversified lineages of hypermutable Pseudomonas aeruginosa in long-term cystic fibrosis infections. PLoS Genet. 10(10), e1004651 (2014).
33. Chung JC, Becq J, Fraser L et al. Genomic variation among contemporary Pseudomonas aeruginosa isolates from chronically infected cystic fibrosis patients. J. Bacteriol. 194(18), 4857-4866 (2012).
34. Snyder LA, Loman NJ, Faraj LA et al. Epidemiological investigation of Pseudomonas aeruginosa isolates from a six-year-long hospital outbreak using high-throughput whole genome sequencing. Euro Surveill. 18(42), pii: 20611 (2013).
35. Jeukens J, Boyle B, Kukavica-Ibrulj I et al. Comparative genomics of isolates of a Pseudomonas aeruginosa epidemic strain associated with chronic lung infections of cystic fibrosis patients. PLoS ONE 9(2), e87611 (2014).
36. Dettman JR, Rodrigue N, Aaron SD, Kassen R. Evolutionary genomics of epidemic and nonepidemic strains of Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 110(52), 21065-21070 (2013).
37. Bezuidt OK, Klockgether J, Elsen S, Attree I, Davenport CF, Tummler B. Intraclonal genome diversity of Pseudomonas aeruginosa clones CHA and TB. BMC Genomics 14, 416 (2013).
38. Yang L, Haagensen JA, Jelsbak L et al. In situ growth rates and biofilm development of Pseudomonas aeruginosa populations in chronic lung infections. J. Bacteriol. 190(8), 2767-2776 (2008).
39. Langergraber KE, Prufer K, Rowney C et al. Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc. Natl Acad. Sci. USA 109(39), 15716-15721 (2012).
40. Dingemans J, Ye L, Hildebrand F et al. The deletion of TonB-dependent receptor genes is part of the genome reduction process that occurs during adaptation of Pseudomonas aeruginosa to the cystic fibrosis lung. Pathog. Dis. 71(1), 26-38 (2014).
41. Oliver A, Canton R, Campo P, Baquero F, Blazquez J. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288(5469), 1251-1254 (2000).
42. Ciofu O, Riis B, Pressler T, Poulsen HE, Hoiby N. Occurrence of hypermutable Pseudomonas aeruginosa in cystic fibrosis patients is associated with the oxidative stress caused by chronic lung inflammation. Antimicrob. Agents Chemother. 49(6), 2276-2282 (2005).
43. 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. 46(10), 3491-3493 (2008).
44. Oliver A, Mena A. Bacterial hypermutation in cystic fibrosis, not only for antibiotic resistance. Clin. Microbiol. Infect. 16(7), 798-808 (2010).
45. Mena A, Smith EE, Burns JL et al. Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J. Bacteriol. 190(24), 7910-7917 (2008).
46. Wielgoss S, Barrick JE, Tenaillon O et al. Mutation rate dynamics in a bacterial population reflect tension between adaptation and genetic load. Proc. Natl Acad. Sci. USA 110(1), 222-227 (2013).
47. Mao EF, Lane L, Lee J, Miller JH. Proliferation of mutators in A cell population. J. Bacteriol. 179(2), 417-422 (1997).
48. Tenaillon O, Le Nagard H, Godelle B, Taddei F. Mutators and sex in bacteria: conflict between adaptive strategies. Proc. Natl Acad. Sci. USA 97(19), 10465-10470 (2000).
49. Ferroni A, Guillemot D, Moumile K et al. Effect of mutator P. aeruginosa on antibiotic resistance acquisition and respiratory function in cystic fibrosis. Pediatr. Pulmonol. 44(8), 820-825 (2009).
50. Moyano AJ, Lujan AM, Argarana CE, Smania AM. MutS deficiency and activity of the error-prone DNA polymerase IV are crucial for determining mucA as the main target for mucoid conversion in Pseudomonas aeruginosa. Mol. Microbiol. 64(2), 547-559 (2007).
51. Hardin G. The competitive exclusion principle. Science 131(3409), 1292-1297 (1960).
52. Kassen R, Rainey PB. The ecology and genetics of microbial diversity. Annu. Rev. Microbiol. 58, 207-231 (2004).
53. Rainey PB, Travisano M. Adaptive radiation in a heterogeneous environment. Nature 394(6688), 69-72 (1998).
54. Yang Z, Bielawski JP. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15(12), 496-503 (2000).
55. Jelsbak L, Johansen HK, Frost AL et al. Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients. Infect. Immun. 75(5), 2214-2224 (2007).
56. Koser CU, Holden MT, Ellington MJ et al. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N. Engl. J. Med. 366(24), 2267-2275 (2012).
57. Harris SR, Clarke IN, Seth-Smith HM et al. Whole-genome analysis of diverse Chlamydia trachomatis strains identifies phylogenetic relationships masked by current clinical typing. Nat. Genet. 44(4), 413-419, S411 (2012).
58. Sun G, Luo T, Yang C et al. Dynamic population changes in Mycobacterium tuberculosis during acquisition and fixation of drug resistance in patients. J. Infect. Dis. 206(11), 1724-1733 (2012).
59. Mcadam PR, Templeton KE, Edwards GF et al. Molecular tracing of the emergence, adaptation, and transmission of hospitalassociated methicillin-resistant Staphylococcus aureus. Proc. Natl Acad. Sci. USA 109(23), 9107-9112 (2012).
60. Mutreja A, Kim DW, Thomson NR et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477(7365), 462-465 (2011).
61. Morelli G, Song Y, Mazzoni CJ et al. Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nat. Genet. 42(12), 1140-1143 (2010).
62. Mowat E, Paterson S, Fothergill JL et al. Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Am. J. Respir. Crit. Care Med. 183(12), 1674-1679 (2011).
63. Workentine ML, Sibley CD, Glezerson B et al. Phenotypic heterogeneity of Pseudomonas aeruginosa populations in a cystic fibrosis patient. PLoS ONE 8(4), e60225 (2013).
64. Barrick JE, Yu DS, Yoon SH et al. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461(7268), 1243-1247 (2009).
65. Palmer KL, Daniel A, Hardy C, Silverman J, Gilmore MS. Genetic basis for daptomycin resistance in enterococci. Antimicrob. Agents Chemother. 55(7), 3345-3356 (2011).
66. Linkevicius M, Sandegren L, Andersson DI. Mechanisms and fitness costs of tigecycline resistance in Escherichia coli. J. Antimicrob. Chemother. 68(12), 2809-2819 (2013).
67. Wong A, Rodrigue N, Kassen R. Genomics of adaptation during experimental evolution of the opportunistic pathogen Pseudomonas aeruginosa. PLoS Genet. 8(9), e1002928 (2012).
68. Ensminger AW, Yassin Y, Miron A, Isberg RR. Experimental evolution of Legionella pneumophila in mouse macrophages leads to strains with altered determinants of environmental survival. PLoS Pathog. 8(5), e1002731 (2012).
69. Elena SF, Lenski RE. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4(6), 457-469 (2003).
70. Raeside C, Gaffe J, Deatherage DE et al. Large chromosomal rearrangements during a long-term evolution experiment with Escherichia coli. mBio 5(5), (2014).
71. Kresse AU, Blocker H, Romling U. ISPa20 advances the individual evolution of Pseudomonas aeruginosa clone C subclone C13 strains isolated from cystic fibrosis patients by insertional mutagenesis and genomic rearrangements. Arch. Microbiol. 185(4), 245-254 (2006).
72. Philippe N, Crozat E, Lenski RE, Schneider D. Evolution of global regulatory networks during a long-term experiment with Escherichia coli. Bioessays 29(9), 846-860 (2007).
73. Sniegowski PD, Gerrish PJ, Lenski RE. Evolution of high mutation rates in experimental populations of E. coli. Nature 387(6634), 703-705 (1997).