Genotype-by-environment interactions due to antibiotic resistance and adaptation in Escherichia coli

Journal of Evolutionary Biology

Volumn 26, Issue 8, 2013, Pages 1655-1664

  Hall, A R ^a,b  

^a ETH ZURICH   (Switzerland)

^b Eawag Dübendorf ^*  (Switzerland)

Author keywords

Antibiotic resistance; Escherichia coli; Experimental evolution; Pleiotropy

Indexed keywords

ADAPTATION; ANTIBIOTIC RESISTANCE; COLIFORM BACTERIUM; ECOLOGICAL MODELING; FITNESS; GENOTYPE; GROWTH RATE; HETEROGENEITY; MUTATION; PHENOTYPE; PLEIOTROPY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ESCHERICHIA COLI PROTEIN; RIFAMPICIN; RPOB PROTEIN, E COLI;

ADAPTATION; ANTIBIOTIC RESISTANCE; ARTICLE; CULTURE MEDIUM; ENVIRONMENT; ESCHERICHIA COLI; EVOLUTION; EXPERIMENTAL EVOLUTION; GENETICS; GENOTYPE; MUTATION; PHENOTYPE; PLEIOTROPY; PREDICTIVE VALUE;

ANTIBIOTIC RESISTANCE; ESCHERICHIA COLI; EXPERIMENTAL EVOLUTION; PLEIOTROPY;

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; CULTURE MEDIA; DRUG RESISTANCE, BACTERIAL; ENVIRONMENT; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENOTYPE; MUTATION; PHENOTYPE; PREDICTIVE VALUE OF TESTS; RIFAMPIN;

EID: 84881025768     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12172     Document Type: Article

References (46)

1. Applebee, M.K., Herrgård, M.J. & Palsson, B.O. 2008. Impact of individual mutations on increased fitness in adaptively evolved strains of Escherichia coli. J. Bacteriol. 190: 5087-5094.
2. Baev, M.V., Baev, D., Radek, A.J. & Campbell, J.W. 2006a. Growth of Escherichia coli MG1655 on LB medium: determining metabolic strategy with transcriptional microarrays. Appl. Microbiol. Biotechnol. 71: 323-328.
3. Baev, M.V., Baev, D., Radek, A.J. & Campbell, J.W. 2006b. Growth of Escherichia coli MG1655 on LB medium: monitoring utilization of sugars, alcohols, and organic acids with transcriptional microarrays. Appl. Microbiol. Biotechnol. 71: 310-316.
4. Barrick, J.E., Kauth, M.R., Strelioff, C.C. & Lenski, R.E. 2010. Escherichia coli rpoB mutants have increased evolvability in proportion to their fitness defects. Mol. Biol. Evol. 27: 1338-1347.
5. Bataillon, T., Zhang, T. & Kassen, R. 2011. Cost of adaptation and fitness effects of beneficial mutations in Pseudomonas fluorescens. Genetics 189: 939-949.
6. Björkman, J., Nagaev, I., Berg, O.G., Hughes, D. & Andersson, D.I. 2000. Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287: 1479-1482.
7. Brandis, G., Wrande, M., Liljas, L. & Hughes, D. 2012. Fitness-compensatory mutations in rifampicin-resistant RNA polymerase. Mol. Microbiol. 85: 142-151.
8. Campbell, E.A., Korzheva, N., Mustaev, A., Murakami, K., Nair, S., Goldfarb, A. et al. 2001. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104: 901-912.
9. Cohan, F.M., King, E.C. & Zawadzki, P. 1994. Amelioration of the deleterious pleiotropic effects of an adaptive mutation in Bacillus subtilis. Evolution 48: 81-95.
10. Comas, I., Borrell, S., Roetzer, A., Rose, G., Malla, B., Kato-Maeda, M. et al. 2012. Whole-genome sequencing of rifampicin-resistant Mycobacterium tuberculosis strains identifies compensatory mutations in RNA polymerase genes. Nat. Genet. 44: 106-112.
11. Conrad, T.M., Frazier, M., Joyce, A.R., Cho, B.K., Knight, E.M., Lewis, N.E. et al. 2010. RNA polymerase mutants found through adaptive evolution reprogram Escherichia coli for optimal growth in minimal media. Proc. Natl. Acad. Sci. USA 107: 20500-20505.
12. Cooper, V.S. 2002. Long-term experimental evolution in Escherichia coli. X. Quantifying the fundamental and realized niche. BMC Evol. Biol. 2: 12.
13. Cooper, V.S. & Lenski, R.E. 2000. The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736-739.
14. Derewacz, D.K., Goodwin, C.R., McNees, C.R., McLean, J.A. & Bachmann, B.O. 2013. Antimicrobial drug resistance affects broad changes in metabolomic phenotype in addition to secondary metabolism. Proc. Natl. Acad. Sci. USA 110: 2336-2341.
15. Garibyan, L., Huang, T., Kim, M., Wolff, E., Nguyen, A., Nguyen, T. 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.
16. Gullberg, E., Cao, S., Berg, O.G., Ilbäck, C., Sandegren, L., Hughes, D. et al. 2011. Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog. 7: e1002158.
17. Hall, A.R., Griffiths, V.F., MacLean, R.C. & Colegrave, N. 2010. Mutational neighbourhood and mutation supply rate constrain adaptation in Pseudomonas aeruginosa. Proc. Biol. Sci. 277: 643-650.
18. Hall, A.R., Iles, J.C. & MacLean, R.C. 2011. The fitness cost of rifampicin resistance in Pseudomonas aeruginosa depends on demand for RNA polymerase. Genetics 187: 44-53.
19. Herring, C.D., Raghunathan, A., Honisch, C., Patel, T., Applebee, M.K., Joyce, A.R. et al. 2006. Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat. Genet. 38: 1406-1412.
20. Jin, D.J. & Gross, C.A. 1989. Characterization of the pleiotropic phenotypes of rifampin-resistant rpoB mutants of Escherichia coli. J. Bacteriol. 171: 5229-5231.
21. Lenski, R.E., Rose, M.R., Simpson, S.C. & Tadler, S.C. 1991. Long-term experimental evolution in Escherichia coli 1. Adaptation and divergence during 2000 generations. Am. Nat. 138: 1315-1341.
22. Lessells, C.M. & Boag, P.T. 1987. Unrepeatable repeatabilities - a common mistake. Auk 104: 116-121.
23. MacLean, R.C. & Bell, G. 2003. Divergent evolution during an experimental adaptive radiation. Proc. Biol. Sci. 270: 1645-1650.
24. Maisnier-Patin, S., Berg, O.G., Liljas, L. & Andersson, D.I. 2002. Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Mol. Microbiol. 46: 355-366.
25. Maisnier-Patin, S., Paulander, W., Pennhag, A. & Andersson, D.I. 2007. Compensatory evolution reveals functional interactions between ribosomal proteins S12 L14 and L19. J. Mol. Biol. 366: 207-215.
26. Nagaev, I., Björkman, J., Andersson, D.I. & Hughes, D. 2001. Biological cost and compensatory evolution in fusidic acid-resistant Staphylococcus aureus. Mol. Microbiol. 40: 433-439.
27. Ostrowski, E.A., Rozen, D.E. & Lenski, R.E. 2005. Pleiotropic effects of beneficial mutations in Escherichia coli. Evolution 59: 2343-2352.
28. Paulander, W., Maisnier-Patin, S. & Andersson, D.I. 2007. Multiple mechanisms to ameliorate the fitness burden of mupirocin resistance in Salmonella typhimurium. Mol. Microbiol. 64: 1038-1048.
29. Paulander, W., Maisnier-Patin, S. & Andersson, D.I. 2009. The fitness cost of streptomycin resistance depends on rpsL mutation, carbon source and rpoS (σ(s)). Genetics 183: 539-546.
30. Perkins, A.E. & Nicholson, W.L. 2008. Uncovering new metabolic capabilities of Bacillus subtilis using phenotype profiling of rifampin-resistant rpoB mutants. J. Bacteriol. 190: 807-814.
31. Pozzi, G., Meloni, M., Iona, E., Orrù, G., Thoresen, O.F., Ricci, M.L. et al. 1999. rpoB mutations in multidrug-resistant strains of Mycobacterium tuberculosis isolated in Italy. J. Clin. Microbiol. 37: 1197-1199.
32. Reynolds, M.G. 2000. Compensatory evolution in rifampin-resistant Escherichia coli. Genetics 156: 1471-1481.
33. Rozen, D.E., McGee, L., Levin, B.R. & Klugman, K.P. 2007. Fitness costs of fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 51: 412-416.
34. Ryu, J.I. 1978. Pleiotropic effect of a rifampin-resistant mutation in Bacillus subtilis. J. Bacteriol. 135: 408-414.
35. Schrag, S.J., Perrot, V. & Levin, B.R. 1997. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc. Biol. Sci. 264: 1287-1291.
36. Severinov, K., Soushko, M., Goldfarb, A. & Nikiforov, V. 1993. Rifampicin region revisited - new rifampicin-resistant and streptolydigin-resistant mutants in the beta subunit of Escherichia coli RNA polymerase. J. Biol. Chem. 268: 14820-14825.
37. Sezonov, G., Joseleau-Petit, D. & D'Ari, R. 2007. Escherichia coli physiology in Luria-Bertani broth. J. Bacteriol. 189: 8746-8749.
38. Sokal, R.R. & Rohlf, J. 1995. Biometry, 3rd edn. W.H. Freeman and Company, New York.
39. Sousa, A., Magalhães, S. & Gordo, I. 2012. Cost of antibiotic resistance and the geometry of adaptation. Mol. Biol. Evol. 29: 1417-1428.
40. Tenaillon, O., Rodríguez-Verdugo, A., Gaut, R.L., McDonald, P., Bennett, A.F., Long, A.D. et al. 2012. The molecular diversity of adaptive convergence. Science 335: 457-461.
41. Travisano, M. & Lenski, R.E. 1995. Long-term experimental evolution in Escherichia coli. III. Variation among replicate populations in correlated responses to novel environments. Evolution 49: 189-200.
42. Travisano, M. & Lenski, R.E. 1996. Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation. Genetics 143: 15-26.
43. Travisano, M., Mongold, J.A., Bennett, A.F. & Lenski, R.E. 1995. Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267: 87-90.
44. Trindade, S., Sousa, A., Xavier, K.B., Dionisio, F., Ferreira, M.G. & Gordo, I. 2009. Positive epistasis drives the acquisition of multidrug resistance. PLoS Genet. 5: e1000578.
45. Trindade, S., Sousa, A. & Gordo, I. 2012. Antibiotic resistance and stress in the light of Fisher's model. Evolution 66: 3815-3824.
46. Trinh, V., Langelier, M.F., Archambault, J. & Coulombe, B. 2006. Structural perspective on mutations affecting the function of multisubunit RNA polymerases. Microbiol. Mol. Biol. Rev. 70: 12-36.