Quantifying the adaptive potential of an antibiotic resistance enzyme

PLoS Genetics

Volumn 8, Issue 6, 2012, Pages

  Schenk, Martijn F ^a,b   Szendro, Ivan G ^a   Krug, Joachim ^a   de Visser, J Arjan G M ^b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE TEM 1; CEFOTAXIME; BETA LACTAMASE; BETA-LACTAMASE TEM-1;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL SURVIVAL; BASE PAIRING; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME LOCALIZATION; ESCHERICHIA COLI; EVOLUTIONARY ADAPTATION; GENE FREQUENCY; GENE MUTATION; GENETIC SCREENING; MOLECULAR EVOLUTION; NONHUMAN; POLYMERASE CHAIN REACTION; PREDICTION; QUANTITATIVE ANALYSIS; REPRODUCTIVE FITNESS; SEQUENCE ANALYSIS; WILD TYPE; ADAPTATION; AMINO ACID SUBSTITUTION; BACTERIUM; DOSE RESPONSE; ENZYMOLOGY; GENE VECTOR; GENETICS; METABOLISM; MUTAGENESIS; MUTATION;

BACTERIA (MICROORGANISMS);

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SUBSTITUTION; BACTERIA; BETA-LACTAMASES; CEFOTAXIME; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENETIC VECTORS; MUTAGENESIS; MUTATION;

EID: 84864070833     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002783     Document Type: Article

References (62)

1. Toprak E, Veres A, Michel J-B, Chait R, Hartl DL, et al. (2012) Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nat Genet 44: 101-105.
2. Salverda MLM, Dellus E, Gorter FA, Debets AJM, Van der Oost J, et al. (2011) Initial mutations direct alternative pathways of protein evolution. PLoS Genet 7: e1001321 doi:10.1371/journal.pgen.1001321.
3. Sniegowski PD, Gerrish PJ, (2010) Beneficial mutations and the dynamics of adaptation in asexual populations. Phil Trans R Soc B 365: 1255-1263.
4. Weinreich DM, Delaney NF, DePristo MA, Hartl DL, (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111-114.
5. Orr HA, (1998) Testing natural selection versus genetic drift in phenotypic evolution using quantitative trait locus data. Genetics 149: 2099-2104.
6. Orr HA, (2003) The distribution of fitness effects among beneficial mutations. Genetics 163: 1519-1526.
7. Orr HA, (2010) The population genetics of beneficial mutations. Phil Trans R Soc B 365: 1195-1201.
8. Gillespie JH, (1984) Molecular evolution over the mutational landscape. Evolution 38: 1116-1129.
9. Kassen R, Bataillon T, (2006) Distribution of fitness effects among beneficial mutations prior to selection in experimental populations of bacteria. Nat Genet 38: 484-488.
10. MacLean RC, Buckling A, (2009) The distribution of fitness effects of beneficial mutations in Pseudomonas aeruginosa. PLoS Genet 5: e1000406 doi:10.1371/journal.pgen.1000406.
11. Rokyta DR, Joyce P, Caudle SB, Wichman HA, (2005) An empirical test of the mutational landscape model of adaptation using a single-stranded DNA virus. Nat Genet 37: 441-444.
12. Sanjuán R, Moya A, Elena SF, (2004) The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc Natl Acad Sci U S A 101: 8396-8401.
13. McDonald MJ, Cooper TF, Beaumont HJE, Rainey PB, (2010) The distribution of fitness effects of new beneficial mutations in Pseudomonas fluorescence. Biol Lett 7: 98-100.
14. Joyce P, Rokyta DR, Beisel CJ, Orr HA, (2008) A General Extreme Value Theory Model for the Adaptation of DNA Sequences Under Strong Selection and Weak Mutation. Genetics 180: 1627-1643.
15. Bataillon T, Zhang T, Kassen R, (2011) Cost of Adaptation and Fitness Effects of Beneficial Mutations in Pseudomonas fluorescens. Genetics 189: 939-949.
16. Rokyta DR, Beisel CJ, Joyce P, Ferris MT, Burch CL, et al. (2008) Beneficial Fitness Effects Are Not Exponential for Two Viruses. J Mol Evol 67: 368-376.
17. Jain K, Seetharaman S, (2011) Multiple Adaptive Substitutions During Evolution in Novel Environments. Genetics 189: 1029-1043.
18. Neidhart J, Krug J, (2011) Adaptive Walks and Extreme Value Theory. Phys Rev Lett 107: 178102.
19. Jain K, (2011) Number of adaptive steps to a local fitness peak. EPL 96: 58006.
20. Orr HA, (2005) The probability of parallel evolution. Evolution 59: 216-220.
21. Orr HA, (2003) A minimum on the mean number of steps taken in adaptive walks. J Theor Biol 220: 241-247.
22. Fogle CA, Nagle JL, Desai MM, (2008) Clonal Interference, Multiple Mutations and Adaptation in Large Asexual Populations. Genetics 180: 2163-2173.
23. Park S-C, Simon D, Krug J, (2010) The speed of evolution in large asexual populations. J Stat Phys 138: 381-410.
24. Perfeito L, Fernandes L, Mota C, Gordo I, (2007) Adaptive mutations in bacteria: high rate and small effects. Science 317: 813-815.
25. Salverda MLM, de Visser JAGM, Barlow M, (2010) Natural evolution of TEM-1 beta-lactamase: experimental reconstruction and clinical relevance. FEMS Microbiol Rev 34: 1015-1036.
26. Barlow M, Hall BG, (2002) Predicting evolutionary potential: In vitro evolution accurately reproduces natural evolution of the TEM beta-lactamase. Genetics 160: 823-832.
27. Stemmer WPC, (1994) Rapid evolution of a protein in vitro by DNA shuffling. Nature 370: 389-391.
28. Davison AC, Smith RL, (1990) Models for exeedances over high thresholds. J R Stat Soc B (Methodological) 52: 393-442.
29. Stevens KE, Sebert ME, (2011) Frequent Beneficial Mutations during Single-Colony Serial Transfer of Streptococcus pneumoniae. PLoS Genet 7: e1002232 doi:10.1371/journal.pgen.1002232.
30. Lalic J, Cuevas JM, Elena SF, (2011) Effect of Host Species on the Distribution of Mutational Fitness Effects for an RNA Virus. PLoS Genet 7: e1002378 doi:10.1371/journal.pgen.1002378.
31. Romero PA, Arnold FH, (2009) Exploring protein fitness landscapes by directed evolution. Nat Rev Mol Cell Biol 10: 866-876.
32. Hall AR, Griffiths VF, MacLean RC, Colegrave N, (2010) Mutational neighbourhood and mutation supply rate constrain adaptation in Pseudomonas aeruginosa. Proc R Soc B 277: 643-650.
33. DePristo MA, Weinreich DM, Hartl DL, (2005) Missense meanderings in sequence space: a biophysical view of protein evolution. Nat Rev Genet 6: 678-687.
34. Huang W, Petrosino J, Hirsch M, Shenkin PS, Palzkill T, (1996) Amino acid sequence determinants of beta-lactamase structure and activity. J Mol Biol 258: 688-703.
35. Soskine M, Tawfik DS, (2010) Mutational effects and the evolution of new protein functions. Nat Rev Genet 11: 572-582.
36. Kryazhimskiy S, Rice DP, Desai MM, (2012) Population Subdivision and Adaptation in Asexual Populations of Saccharomyces cerevisiae. Evolution in press.
37. Wang X, Minasov G, Shoichet BK, (2002) Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs. J Mol Biol 320: 85-95.
38. Goldsmith M, Tawfik DS, (2009) Potential role of phenotypic mutations in the evolution of protein expression and stability. Proc Natl Acad Sci U S A 106: 6197-6202.
39. Deana A, Ehrlich R, Reiss C, (1996) Synonymous codon selection controls in vivo turnover and mount of mRNA in Escherichia coli bla and ompA genes. J Bacteriol 178: 2718-2720.
40. Zalucki YM, Gittins KL, Jennings MP, (2008) Secretory sequence signal non-optimal codons are required for expression and export of beta-lactamase. Biochem Biophys Res Comm 366: 135-141.
41. Duan JB, Wainwright MS, Comeron JM, Saitou N, Sanders AR, et al. (2003) Synonymous mutations in the human dopamine receptor D2 (DRD2) affect mRNA stability and synthesis of the receptor. Hum Mol Genet 12: 205-216.
42. Lind PA, Berg OG, Andersson DI, (2010) Mutational Robustness of Ribosomal Protein Genes. Science 330: 825-827.
43. Vakulenko SB, Taibi-Tronche P, Toth M, Massova I, Lerner SA, et al. (1999) Effects on substrate profile by mutational substitutions at positions 164 and 179 of the class A TEMpUC19 beta-lactamase from Escherichia coli. J Biol Chem 274: 23052-23060.
44. Orencia MC, Yoon JS, Ness JE, Stemmer WPC, Stevens RC, (2001) Predicting the emergence of antibiotic resistance by directed evolution and structural analysis. Nat Struct Biol 8: 238-242.
45. Negri M-C, Lipsitch M, Blázquez J, Levin BR, Baquero F, (2000) Concentration-dependent selection of small phenotypic differences in TEM beta-lactamase-mediated antibiotic resistance. Antimicrob Agents Chemother 44: 2485-2491.
46. Paulander W, Pennhag A, Andersson DI, Maisnier-Patin S, (2007) Caenorhabditis elegans as a model to determine fitness of antibiotic-resistant Salmonella enterica serovar typhimuriu. Antimicrob Agents Chemother 51: 766-769.
47. Andersson DI, Hughes D, (2010) Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microb 8: 260-271.
48. Medeiros AA, (1997) Evolution and dissemniation of beta-lactamases accelerated by generations of beta-lactam antibiotics. Clin Infect Dis 24: S19-S45.
49. Derrida B, (1994) Non-self averaging effects in sums of random variables, spin glasses, random maps and random walks. In: Fannes M, Maes C, Verbeure A, editors. On three levels: Micro-, meso- and macro-approaches in physics New York Plenum Press pp. 125-137.
50. Gifford DR, Schoustra SE, Kassen R, (2011) The length of adaptive walks is insensitive to starting fitness in Aspergillus nidulans. Evolution 65: 3070-3078.
51. Schoustra SE, Bataillon T, Gifford DR, Kassen R, (2009) The Properties of Adaptive Walks in Evolving Populations of Fungus. PLOS Biol 7: e1000250 doi:10.1371/journal.pbio.1000250.
52. Sun F, (1995) The polymerase chain reaction and branching processes. J Comp Biol 2: 63-86.
53. Patrick WM, Firth AE, Blackburn JM, (2003) User-friendly algorithms for estimating completeness and diversity in randomized protein-encoding libraries. Protein Eng 16: 451-457.
54. Ambler RP, Coulson AFW, Frere JM, Ghuysen JM, Joris B, et al. (1991) A standard numbering scheme for the class A beta-lactamase. Biochem J 276: 269-270.
55. DeLano WL, (2002) The PyMOL Molecular Graphics System Palo Alto, CA DeLano Scientific.
56. Jaffe A, Chabbert YA, Semonin O, (1982) Role of porin proteins OmpF and OmpC in the permeation of beta-lactams. Antimicrob Agents Chemother 22: 942-948.
57. Finkelstein M, Tucker HG, Veeh JA, (1998) Confidence intervals for the number of unseen types. Stat Prob Lett 37: 423-430.
58. Beisel CJ, Rokyta DR, Wichman HA, Joyce P, (2007) Testing the extreme value domain of attraction for distributions of beneficial fitness effects. Genetics 176: 2441-2449.
59. Pickands J, (1975) Statistical inference using extreme order statistics. Ann Stat 3: 119-131.
60. Choulakian V, Stephens MA, (2001) Goodness-of-fit tests for the generalized pareto distribution. Technometrics 43: 478-484.
61. Lang M, Ouarda TBMJ, Bobée B, (1999) Towards operational guidelines for over-threshold modeling. J Hydrol 225: 103-117.
62. Haldane JBS, (1927) The mathematical theory of natural and artificial selection. Proc Cambridge Phil Soc 23: 838-844.