Plasmid copy number underlies adaptive mutability in bacteria

Genetics

Volumn 198, Issue 3, 2014, Pages 919-933

  Sano, Emiko ^a,b   Maisnier Patin, Sophie ^a   Aboubechara, John Paul ^a,c   Quiñones Soto, Semarhy ^a,d   Roth, John R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MONTANA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANHYDROTETRACYCLINE; LACTOSE; 4-EPIANHYDROTETRACYCLINE; TETRACYCLINE DERIVATIVE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL MUTATION; BACTERIAL STRAIN; COPY NUMBER VARIATION; CULTURE MEDIUM; ESCHERICHIA COLI; GENE AMPLIFICATION; GROWTH INHIBITION; GROWTH RATE; MOLECULAR CLONING; MUTAGENESIS; NONHUMAN; PLASMID; REVERTANT; SALMONELLA TYPHIMURIUM; ADAPTATION; BACTERIAL GENE; DRUG EFFECTS; GENE DOSAGE; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LACTOSE OPERON; MUTATION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

ADAPTATION, BIOLOGICAL; DNA COPY NUMBER VARIATIONS; ESCHERICHIA COLI; GENE AMPLIFICATION; GENE DOSAGE; GENE DUPLICATION; GENES, BACTERIAL; LAC OPERON; MUTAGENESIS, INSERTIONAL; MUTATION; PLASMIDS; SALMONELLA TYPHIMURIUM; TETRACYCLINES;

EID: 84908632179     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.170068     Document Type: Article

References (54)

1. Andersson, D. I., E. S. Slechta, and J. R. Roth, 1998 Evidence that gene amplification underlies adaptive mutability of the bacterial lac operon. Science 282: 1133-1135.
2. Bergthorsson, U., D. I. Andersson, and J. R. Roth, 2007 Ohno’s dilemma: evolution of new genes under continuous selection. Proc. Natl. Acad. Sci. USA 104: 17004-17009.
3. Berkowitz, D., J. M. Hushon, H. J. Whitfield, J. R. Roth, and B. N. Ames, 1968 Procedures for identifying nonsense mutations. J. Bacteriol. 96: 215-220.
4. Bochner, B. R., H. C. Huang, G. L. Schieven, and B. N. Ames, 1980 Positive selection for loss of tetracycline resistance. J. Bacteriol. 143: 926-933.
5. Cairns, J., and P. L. Foster, 1991 Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128: 695-701.
6. Cairns, J., J. Overbaugh, and S. Miller, 1988 The origin of mutants. Nature 335: 142-145.
7. Churchward, G., D. Belin, and Y. Nagamine, 1984 A pSC101-derived plasmid which shows no sequence homology to other commonly used cloning vectors. Gene 31: 165-171.
8. Cohen, A., and A. J. Clark, 1986 Synthesis of linear plasmid multimers in Escherichia coli K-12. J. Bacteriol. 167: 327-335.
9. Coleman, D. C., I. Chopra, S. W. Shales, T. G. Howe, and T. J. Foster, 1983 Analysis of tetracycline resistance encoded by transposon Tn10: deletion mapping of tetracycline-sensitive point mutations and identification of two structural genes. J. Bacteriol. 153: 921-929.
10. Davis, R. W., D. Botstein, and J. R. Roth, 1980 Advanced Bacterial Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
11. Eckert, B., and C. F. Beck, 1989 Overproduction of transposon Tn10-encoded tetracycline resistance protein results in cell death and loss of membrane potential. J. Bacteriol. 171: 3557-3559.
12. Elde, N. C., S. J. Child, M. T. Eickbush, J. O. Kitzman, K. S. Rogers et al., 2012 Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. Cell 150: 831-841.
13. Foster, P. L., 1994 Population dynamics of a Lac2 strain of Escherichia coli during selection for lactose utilization. Genetics 138: 253-261.
14. Foster, P. L., 1997 Nonadaptive mutations occur on the F’ episome during adaptive mutation conditions in Escherichia coli. J. Bacteriol. 179: 1550-1554.
15. Foster, P. L., and J. Cairns, 1992 Mechanisms of directed mutation. Genetics 131: 783-789.
16. Foster, P. L., and J. M. Trimarchi, 1994 Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science 265: 407-409.
17. Foster, P. L., and J. M. Trimarchi, 1995a Adaptive reversion of an episomal frameshift mutation in Escherichia coli requires conjugal functions but not actual conjugation. Proc. Natl. Acad. Sci. USA 92: 5487-5490.
18. Foster, P. L., and J. M. Trimarchi, 1995b Conjugation is not required for adaptive reversion of an episomal frameshift mutation in Escherichia coli. J. Bacteriol. 177: 6670-6671.
19. Galitski, T., and J. R. Roth, 1995 Evidence that F plasmid transfer replication underlies apparent adaptive mutation. Science 268: 421-423.
20. Godoy, V. G., and M. S. Fox, 2000 Transposon stability and a role for conjugational transfer in adaptive mutability. Proc. Natl. Acad. Sci. USA 97: 7393-7398.
21. Hall, B. G., 1990 Spontaneous point mutations that occur more often when advantageous than when neutral. Genetics 126: 5-16.
22. Hastings, P. J., H. J. Bull, J. R. Klump, and S. M. Rosenberg, 2000 Adaptive amplification: an inducible chromosomal instability mechanism. Cell 103: 723-731.
23. Hendrickson, H., E. S. Slechta, U. Bergthorsson, D. I. Andersson, and J. R. Roth, 2002 Amplification-mutagenesis: evidence that “directed” adaptive mutation and general hypermutability result from growth with a selected gene amplification. Proc. Natl. Acad. Sci. USA 99: 2164-2169.
24. Kleckner, N., J. Bender, and S. Gottesman, 1991 Uses of transposons with emphasis on Tn10. Methods Enzymol. 204: 139-180.
25. Kugelberg, E., E. Kofoid, A. B. Reams, D. I. Andersson, and J. R. Roth, 2006 Multiple pathways of selected gene amplification during adaptive mutation. Proc. Natl. Acad. Sci. USA 103: 17319-17324.
26. Kugelberg, E., E. Kofoid, D. I. Andersson, Y. Lu, J. Mellor et al., 2010 The tandem inversion duplication in Salmonella enterica: selection drives unstable precursors to final mutation types. Genetics 185: 65-80.
27. Larsen, J. E., K. Gerdes, J. Light, and S. Molin, 1984 Low-copynumber plasmid-cloning vectors amplifiable by derepression of an inserted foreign promoter. Gene 28: 45-54.
28. Luria, S. E., and M. Delbruck, 1943 Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28: 491-511.
29. Lyu, Y. L., C. T. Lin, and L. F. Liu, 1999 Inversion/dimerization of plasmids mediated by inverted repeats. J. Mol. Biol. 285: 1485-1501.
30. Mann, B. A., and J. M. Slauch, 1997 Transduction of low-copy number plasmids by bacteriophage P22. Genetics 146: 447-456.
31. McKenzie, G., P. Lee, M.-J. Lombardo, P. Hastings, and S. Rosenberg, 2001 SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Mol. Cell 7: 571-579.
32. Moyed, H. S., T. T. Nguyen, and K. P. Bertrand, 1983 Multicopy Tn10 tet plasmids confer sensitivity to induction of tet gene expression. J. Bacteriol. 155: 549-556.
33. Näsvall, J., L. Sun, J. R. Roth, and D. I. Andersson, 2012 Real-time evolution of new genes by innovation, amplification, and divergence. Science 338: 384-387.
34. Nguyen, T. N., Q. G. Phan, L. P. Duong, K. P. Bertrand, and R. E. Lenski, 1989 Effects of carriage and expression of the Tn10 tetracycline-resistance operon on the fitness of Escherichia coli K12. Mol. Biol. Evol. 6: 213-225.
35. Peters, J. E., I. M. Bartoszyk, S. Dheer, and S. A. Benson, 1996 Redundant homosexual F transfer facilitates selectioninduced reversion of plasmid mutations. J. Bacteriol. 178: 3037-3043.
36. Pinkel, D., R. Segraves, D. Sudar, S. Clark, I. Poole et al., 1998 High resolution analysis of DNA copy number variation using comparative genomic hybridization to microarrays. Nat. Genet. 20: 207-211.
37. Pranting, M., and D. I. Andersson, 2011 Escape from growth restriction in small colony variants of Salmonella typhimurium by gene amplification and mutation. Mol. Microbiol. 79: 305-315.
38. Projan, S. J., S. Carleton, and R. P. Novick, 1983 Determination of plasmid copy number by fluorescence densitometry. Plasmid 9: 182-190.
39. Quinones-Soto, S., A. B. Reams, and J. R. Roth, 2012 Pathways of genetic adaptation: multistep origin of mutants under selection without induced mutagenesis in Salmonella enterica. Genetics 192: 987-999.
40. Radicella, J. P., P. U. Park, and M. S. Fox, 1995 Adaptive mutation in Escherichia coli: a role for conjugation. Science 268: 418-420.
41. Reams, A. B., E. Kofoid, E. Kugelberg, and J. R. Roth, 2012 Multiple pathways of duplication formation with and without recombination (RecA) in Salmonella enterica. Genetics 192: 397-415.
42. Reams, A. B., E. Kofoid, M. Savageau, and J. R. Roth, 2010 Duplication frequency in a population of Salmonella enterica rapidly approaches steady state with or without recombination. Genetics 184: 1077-1094.
43. Rosche, W. A., and P. L. Foster, 1999 The role of transient hypermutators in adaptive mutation in Escherichia coli. Proc. Natl. Acad. Sci. USA 96: 6862-6867.
44. Rosenberg, S. M., S. Longerich, P. Gee, and R. S. Harris, 1994 Adaptive mutation by deletions in small mononucleotide repeats. Science 265: 405-407.
45. Roth, J. R., 2011 The joys and terrors of fast adaptation: new findings elucidate antibiotic resistance and natural selection. Mol. Microbiol. 79: 279-282.
46. Roth, J. R., E. Kofoid, F. P. Roth, O. G. Berg, J. Seger et al., 2003 Regulating general mutation rates: examination of the hypermutable state model for Cairnsian adaptive mutation. Genetics 163: 1483-1496.
47. Slack, A., P. C. Thornton, D. B. Magner, S. M. Rosenberg, and P. J. Hastings, 2006 On the mechanism of gene amplification induced under stress in Escherichia coli. PLoS Genet. 2: e48.
48. Slechta, E. S., K. L. Bunny, E. Kugelberg, E. Kofoid, D. I. Andersson et al., 2003 Adaptive mutation: general mutagenesis is not a programmed response to stress but results from rare coamplification of dinB with lac. Proc. Natl. Acad. Sci. USA 100: 12847-12852.
49. Stahl, F. W., 1988 News and views: a unicorn in the garden. Nature 355: 112-113.
50. + in Escherichia coli. J. Bacteriol. 189: 2291-2299.
51. Sun, S., O. G. Berg, J. R. Roth, and D. I. Andersson, 2009 Contribution of gene amplification to evolution of increased antibiotic resistance in Salmonella typhimurium. Genetics 182: 1183-1195.
52. Torkelson, J., R. S. Harris, M.-J. Lombardo, J. Nagendran, C. Thulin et al., 1997 Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation. EMBO J. 16: 3303-3311.
53. Viret, J. F., A. Bravo, and J. C. Alonso, 1991 Recombinationdependent concatemeric plasmid replication. Microbiol. Rev. 55: 675-683.
54. Way, J. C., M. A. Davis, D. Morisato, D. E. Roberts, and N. Kleckner, 1984 New Tn10 derivatives for transposon mutagenesis and for construction of lacZ operon fusions by transposition. Gene 32: 369-379.