Testing the role of genetic background in parallel evolution using the comparative experimental evolution of antibiotic resistance

Molecular Biology and Evolution

Volumn 31, Issue 12, 2014, Pages 3314-3323

  Vogwill, Tom ^a   Kojadinovic, Mila ^b   Furió, Victoria ^a   Maclean, R Craig ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

adaptation; antibiotic resistance; comparative biology; experimental evolution; Pseudomonas; selection experiment

Indexed keywords

RIFAMPICIN; BACTERIAL PROTEIN; TUBERCULOSTATIC AGENT;

AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; ARTICLE; COMPARATIVE STUDY; EVOLUTIONARY ADAPTATION; GENETIC VARIABILITY; GENOTYPE; GROWTH RATE; MOLECULAR EVOLUTION; MUTATION RATE; NONHUMAN; PARALLEL EVOLUTION; PHENOTYPE; PHENOTYPIC VARIATION; PSEUDOMONAS; SINGLE NUCLEOTIDE POLYMORPHISM; STRAIN DIFFERENCE; ADAPTATION; BACTERIAL GENE; DRUG EFFECTS; GENETIC DRIFT; GENETIC SELECTION; GENETICS; MUTATION; PHYLOGENY;

PSEUDOMONAS;

ADAPTATION, BIOLOGICAL; ANTIBIOTICS, ANTITUBERCULAR; BACTERIAL PROTEINS; DRUG RESISTANCE, MICROBIAL; EVOLUTION, MOLECULAR; GENES, BACTERIAL; GENETIC DRIFT; MUTATION; PHENOTYPE; PHYLOGENY; PSEUDOMONAS; RIFAMPIN; SELECTION, GENETIC;

EID: 84924973674     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu262     Document Type: Article

References (66)

1. Andersson DI, Hughes D. 2010. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol. 8: 260-271.
2. Angst D, Hall A. 2013. The cost of antibiotic resistance depends on evolutionary history in Escherichia coli. BMC Evol Biol. 13:163.
3. Bernasconi P, Woodworth AR, Rosen BA, Subramanian MV, Siehl DL. 1995. A naturally occurring point mutation confers broad range tolerance to herbicides that target acetolactate synthase. J Biol Chem. 270:17381-17385.
4. Bollback JP, Huelsenbeck JP. 2009. Parallel genetic evolution within and between bacteriophage species of varying degrees of divergence. Genetics 181:225-234.
5. Borrell S, Teo Y, Giardina F, Streicher EM, Klopper M, Feldmann J, Muller., Victor TC, Gagneux S. 2013. Epistasis between antibiotic resistance mutations drives the evolution of extensively drug-resistant tuberculosis. Evol Med Public Health. 2013:65-74.
6. Brandis G, Hughes D. 2013. Genetic characterization of compensatory evolution in strains carrying rpoB Ser531Leu, the rifampicin resistance mutation most frequently found in clinical isolates. J Antimicrob Chemother. 68:2493-2497.
7. Brandis G, Wrande M, Liljas L, Hughes D. 2012. Fitness-compensatory mutations in rifampicin-resistant RNA polymerase. Mol Microbiol. 85:142-151.
8. Breen MS, Kemena C, Vlasov PK, Notredame C, Kondrashov FA. 2012. Epistasis as the primary factor in molecular evolution. Nature 490: 535-538.
9. Campbell EA, Korzheva N, Mustaev A, Murakami K, Nair S, Goldfarb A, Darst SA. 2001. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104:901-912.
10. Carata E, Peano C, Tredici S, Ferrari F, Tala A, Corti G, Bicciato S, De Bellis G, Alifano P. 2009. Phenotypes and gene expression profiles of Saccharopolyspora erythraea rifampicin-resistant (rif) mutants affected in erythromycin production. Microb Cell Fact. 8:18.
11. Casali N, Nikolayevskyy V, Balabanova Y, Ignatyeva O, Kontsevaya I, Harris SR, Bentley SD, Parkhill J, Nejentsev S, Hoffner SE, et al. 2012. Microevolution of extensively drug-resistant tuberculosis in Russia. Genome Res. 22:735-745.
12. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 17: 540-552.
13. Comas I, Borrell S, Roetzer A, Rose G,Malla B, Kato-MaedaM, Galagan J, Niemann S, Gagneux S. 2012. Whole-genome sequencing of rifampicin-resistant Mycobacterium tuberculosis strains identifies compensatory mutations in RNA polymerase genes. Nat Genet. 44: 106-110.
14. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JLY, Toufighi K, Mostafavi S, et al. 2010. The genetic landscape of a cell. Science 327:425-431.
15. Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 9: 772-772.
16. de Vos M, Muller B, Borrell S, Black PA, van Helden PD, Warren RM, Gagneux S, Victor TC. 2013. Putative compensatory mutations in the rpoC gene of rifampin-resistant Mycobacterium tuberculosis are associated with ongoing transmission. Antimicrob Agents Chemother. 57:827-832.
17. Dettman JR, Rodrigue N, Aaron SD, Kassen R. 2013. Evolutionary genomics of epidemic and nonepidemic strains of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 110:21065-21070.
18. Drake JW. 1991. A constant rate of spontaneous mutation in DNAbased microbes. Proc Natl Acad Sci U S A. 88:7160-7164.
19. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
20. Fajardo A, Martinez-Martin N, Mercadillo M, Galian JC, Ghysels B, Matthijs S, Cornelis P, Wiehlmann L, Tummler B, Baquero F, et al. 2008. The neglected intrinsic resistome of bacterial pathogens. PLoS One 3:e1619.
21. Felsenstein J. 1985. Phylogenies and the comparative method. Am Nat. 125:1-15.
22. ffrench-Constant RH, Daborn PJ, Goff GL. 2004. The genetics and genomics of insecticide resistance. Trends Genet. 20:163-170.
23. Gagneux S, Long CD, Small PM, Van T, Schoolnik GK, Bohannan BJM. 2006. The competitive cost of antibiotic resistance in Mycobacterium tuberculosis. Science 312:1944-1946.
24. Gao W, Cameron DR, Davies JK, Kostoulias X, Stepnell J, Tuck KL, Yeaman MR, Peleg AY, Stinear TP, Howden BP. 2013. The RpoB H481Y rifampicin resistance mutation and an active stringent response reduce virulence and increase resistance to innate immune responses in Staphylococcus aureus. J Infect Dis. 207: 929-939.
25. Garibyan L, Huang T, KimM,Wolff E, Nguyen A, Nguyen T, Diep A, Hu K, Iverson A, Yang H, et al. 2003. Use of the rpoB gene to determine the specificity of base substitution mutations on the Escherichia coli chromosome. DNA Repair. 2:593-608.
26. Garland T, Midford PE, Ives AR. 1999. An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral values. Am Zool. 39:374-388.
27. Girgis HS, Hottes AK, Tavazoie S. 2009. Genetic architecture of intrinsic antibiotic susceptibility. PLoS One 4:e5629.
28. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximumlikelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 59:307-321.
29. Hall AR. 2013. Genotype-by-environment interactions due to antibiotic resistance and adaptation in Escherichia coli. J Evol Biol. 26: 1655-1664.
30. Hall AR, Iles JC, MacLean RC. 2011. The fitness cost of rifampicin resistance in Pseudomonas aeruginosa depends on demand for RNA polymerase. Genetics 187:817-822.
31. Hall AR, MacLean RC. 2011. Epistasis buffers the fitness effects of rifampicin-resistance mutations in Pseudomonas aeruginosa. Evolution 65: 2370-2379.
32. Harms MJ, Thornton JW. 2013. Evolutionary biochemistry: revealing the historical and physical causes of protein properties. Nat Rev Genet. 14:559-571.
33. Hedrick PW, Goodnight C. 2005. A standardized genetic differentiation measure. Evolution 59:1633-1638.
34. Holder KK, Bull JJ. 2001. Profiles of adaptation in two similar viruses. Genetics 159:1393-1404.
35. Humphrey B, Thomson N, Thomas C, Brooks K, Sanders M, Delsol A, Roe J, Bennett P, Enne V. 2012. Fitness of Escherichia coli strains carrying expressed and partially silent IncN and IncP1 plasmids. BMC Microbiol. 12:53.
36. Jatsenko T, Tover A, Tegova R, Kivisaar M. 2010. Molecular characterization of Rifr mutations in Pseudomonas aeruginosa and Pseudomonas putida. Mutat Res. 683:106-114.
37. Khan AI, Dinh DM, Schneider D, Lenski RE, Cooper TF. 2011. Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332:1193-1196.
38. Lieberman TD, Michel JB, Aingaran M, Potter-Bynoe G, Roux D, Davis MR, Skurnik D, Leiby N, LiPuma JJ, Goldberg JB, et al. 2011. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet. 43:1275-1280.
39. MacLean RC, Buckling A. 2009. The Distribution of fitness effects of beneficial mutations in Pseudomonas aeruginosa. PLoS Genet. 5: e1000406.
40. MacLean RC, Perron GG, Gardner A. 2010. Diminishing returns from beneficial mutations and pervasive epistasis shape the fitness landscape for rifampicin resistance in Pseudomonas aeruginosa. Genetics 186:1345-1354.
41. Markowitz VM, Chen IMA, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang J, Williams P, et al. 2012. IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res. 40:D115-D122.
42. McCracken KG, Barger CP, Bulgarella M, Johnson KP, Sonsthagen SA, Trucco J, Valqui TH, Wilson RE, Winker K, Sorenson MD. 2009. Parallel evolution in the major haemoglobin genes of eight species of Andean waterfowl. Mol Ecol. 18:3992-4005.
43. Mongkolrattanothai K, Pumfrey L, Mankin P, Gray BM. 2009. Acquisition of high-level mupirocin resistance and its fitness cost among methicillin-resistant Staphylococcus aureus strains with lowlevel mupirocin resistance. J Clin Microbiol. 47:4158-4160.
44. Nei M. 1973. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci U S A. 70:3321-3323.
45. Nguyen AH, Molineux IJ, Springman R, Bull J. 2012. Multiple genetic pathways to similar fitness limits during viral adaptation to a new host. Evolution 66:363-374.
46. Ostrowski EA, Woods RJ, Lenski RE. 2008. The genetic basis of parallel and divergent phenotypic responses in evolving populations of Escherichia coli. Proc R Soc Lond B Biol Sci. 275:277.
47. Ozen A, Ussery D. 2012. Defining the Pseudomonas genus: where do we draw the line with Azotobacter? Microb Ecol. 63:239-248.
48. Pelz HJ, Rost S, Hunerberg M, Fregin A, Heiberg AC, Baert K, MacNicoll AD, Prescott CV, Walker AS, Oldenburg J, et al. 2005. The genetic basis of resistance to anticoagulants in rodents. Genetics 170: 1839-1847.
49. Powles SB, Yu Q. 2010. Evolution in action: plants resistant to herbicides. Ann Rev Plant Biol. 61:317-347.
50. Rodriguez-Verdugo A, Gaut B, Tenaillon O. 2013. Evolution of Escherichia coli rifampicin resistance in an antibiotic-free environment during thermal stress. BMC Evol Biol. 13:50.
51. Rokas A, Carroll SB. 2008. Frequent and widespread parallel evolution of protein sequences. Mol Biol Evol. 25:1943-1953.
52. Sandegren L, Linkevicius M, Lytsy B, Melhus A, Andersson DI. 2012. Transfer of an Escherichia coli ST131 multiresistance cassette has created a Klebsiella pneumoniae-specific plasmid associated with a major nosocomial outbreak. J Antimicrob Chemother 67: 74-83.
53. Sandgren A, Strong M, Muthukrishnan P, Weiner BK, Church GM, Murray MB. 2009. Tuberculosis drug resistance mutation database. PLoS Med. 6:e1000002.
54. Simpson EH. 1949. Measurement of diversity. Nature 163:688-688.
55. Travisano M, Mongold JA, Bennett AF, Lenski RE. 1995. Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267:87-90.
56. Vaidya G, Lohman DJ, Meier R. 2011. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27:171-180.
57. Wichelhaus TA, Boddinghaus B, Besier S, Schafer V, Brade V, Ludwig A. 2002. Biological cost of rifampin resistance from the perspective of Staphylococcus aureus. Antimicrob Agents Chemother. 46: 3381-3385.
58. Wichman HA, Scott LA, Yarber CD, Bull JJ. 2000. Experimental evolution recapitulates natural evolution. Philos Trans R Soc Lond B Biol Sci. 355:1677-1684.
59. Wong A, Kassen R. 2011. Parallel evolution and local differentiation in quinolone resistance in Pseudomonas aeruginosa. Microbiology 157: 937-944.
60. Wong A, Rodrigue N, Kassen R. 2012. Genomics of adaptation during experimental evolution of the opportunistic pathogen Pseudomonas aeruginosa. PLoS Genet. 8:e1002928.
61. Wood T, Burke J, Rieseberg L. 2005. Parallel genotypic adaptation: when evolution repeats itself. In:Mauricio R, editor. genetics of adaptation. Netherlands: Springer. p. 157-170.
62. Woods R, Schneider D, Winkworth CL, Riley MA, Lenski RE. 2006. Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc Natl Acad Sci U S A. 103:9107.
63. Wrande M, Roth JR, Hughes D. 2008. Accumulation of mutants in "aging" bacterial colonies is due to growth under selection, not stress-induced mutagenesis. Proc Natl Acad Sci U S A. 105: 11863-11868.
64. Xu J, Tozawa Y, Lai C, Hayashi H, Ochi K. 2002. A rifampicin resistance mutation in the rpoB gene confers ppGpp-independent antibiotic production in Streptomyces coelicolor A3(2). Mol Genet Genomics. 268:179-189.
65. Zaczek A, Brzostek A, Augustynowicz-Kopec E, Zwolska Z, Dziadek J. 2009. Genetic evaluation of relationship between mutations in rpoB and resistance of Mycobacterium tuberculosis to rifampin. BMC Microbiol. 9:1-8.
66. Zhang J, Kumar S. 1997. Detection of convergent and parallel evolution at the amino acid sequence level. Mol Biol Evol. 14:527-536.