Mutational heterogeneity: A key ingredient of bet-hedging and evolutionary divergence?: The broad spectrum of mutations and their flexible frequency in populations provides a source of risk avoidance and alternative evolutionary strategies

BioEssays

Volumn 37, Issue 2, 2015, Pages 123-130

  Ferenci, Thomas ^a   Maharjan, Ram ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Double strand DNA breaks (DSBs); E. coli; Evolutionary divergence; Experimental evolution; Mutational spectrum; Population heterogeneity

Indexed keywords

ADAPTIVE RADIATION; DNA TRANSPOSITION; EVOLUTION; EVOLUTIONARY ADAPTATION; FREQUENCY DEPENDENT SELECTION; GENE DELETION; GENE DUPLICATION; GENE INSERTION; GENE INSERTION SEQUENCE; GENE MUTATION; GENETIC HETEROGENEITY; NONHUMAN; NOTE; PHENOTYPE; POINT MUTATION; ADAPTATION; DOUBLE STRANDED DNA BREAK; ESCHERICHIA COLI; GENETIC SELECTION; GENETICS; MUTATION; PHYSIOLOGY;

BACTERIA (MICROORGANISMS);

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; DNA BREAKS, DOUBLE-STRANDED; ESCHERICHIA COLI; MUTATION; SELECTION, GENETIC;

EID: 84921474588     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201400153     Document Type: Note

References (61)

1. Merlin F. 2010. Evolutionary chance mutation: A defense of the modern synthesis' consensus view. Philos Theor Biol 2, DOI: 10.3998/ptb.6959004.0002.003.
2. Ninio J. 2010. Frail hypotheses in evolutionary biology. PLoS Genet 6: e1001067.
3. Drake JW, Charlesworth B, Charlesworth D, Crow JF. 1998. Rates of spontaneous mutation. Genetics 148: 1667-86.
4. Radman M, Matic I, Taddei F. 1999. Evolution of evolvability. Ann N Y Acad Sci 870: 146-55.
5. Taddei F, Radman M, Maynardsmith J, Toupance B, et al. 1997. Role of mutator alleles in adaptive evolution. Nature 387: 700-2.
6. Martincorena I, Seshasayee ASN, Luscombe NM. 2012. Evidence of non-random mutation rates suggests an evolutionary risk management strategy. Nature 485: 95-8.
7. Foster PL, Hanson AJ, Lee H, Popodi EM, et al. 2013. On the mutational topology of the bacterial genome. G3 (Bethesda) 3: 399-407.
8. King DG, Kashi Y. 2007. Indirect selection for mutability. Heredity 99: 123-4.
9. Lee H, Popodi E, Tang HX, Foster PL. 2012. Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing. Proc Natl Acad Sci USA 109: E2774-83.
10. Roth JR. 2010. Genetic adaptation: A new piece for a very old puzzle. Curr Biol 20: R15-7.
11. Ryall B, Eydallin G, Ferenci T. 2012. Culture history and population heterogeneity as determinants of bacterial adaptation: The adaptomics of a single environmental transition. Microbiol Mol Biol Rev 76: 597-625.
12. Ferenci T. 2003. What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli? Trends Microbiol 11: 457-61.
13. Miller JH. 1996. Spontaneous mutators in bacteria - Insights into pathways of mutagenesis and repair. Annu Rev Microbiol 50: 625-43.
14. Gutierrez A, Laureti L, Crussard S, Abida H, et al. 2013. beta-lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nat Commun 4: 1610.
15. Al Mamun AAM, Lombardo M-J, Shee C, Lisewski AM. et al. 2012. Identity and function of a large gene network underlying mutagenic repair of DNA breaks. Science 338: 1344-8.
16. Kobayashi S, Valentine MR, Pham P, O'Donnell M, et al. 2002. Fidelity of Escherichia coli DNA polymerase IV: Preferential generation of small deletion mutations by dNTP-stabilized misalignment. J Biol Chem 277: 34198-207.
17. Foti JJ, Devadoss B, Winkler JA, Collins JJ, et al. 2012. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science 336: 315-9.
18. Matic I. 2013. Stress-induced mutagenesis in bacteria. In: Mittelman D, ed; Stress-Induced Mutagenesis. New York: Springer. p. 1-19.
19. Hastings PJ. 2007. Adaptive amplification. Crit Rev Biochem Mol Biol 42: 271-83.
20. Twiss E, Coros AM, Tavakoli NP, Derbyshire KM. 2005. Transposition is modulated by a diverse set of host factors in Escherichia coli and is stimulated by nutritional stress. Mol Microbiol 57: 1593-607.
21. Sousa A, Bourgard C, Wahl LM, Gordo I. 2013. Rates of transposition in Escherichia coli. Biol Lett 9: 30838.
22. Maki H. 2002. Origins of spontaneous mutations: Specificity and directionality of base-substitution, frameshift, and sequence-substitution mutageneses. Annu Rev Genet 36: 279-303.
23. Andersson DI, Hughes D. 2009. Gene amplification and adaptive evolution in bacteria. Annu Rev Genet 43: 167-95.
24. Goldsmith M, Tawfik S. 2009. Potential role of phenotypic mutations in the evolution of protein expression and stability. Proc Natl Acad Sci USA 106: 6197-202.
25. De Wals PY, Doucet N, Pelletier JN. 2009. High tolerance to simultaneous active-site mutations in TEM-1 β-lactamase: Distinct mutational paths provide more generalized β-lactam recognition. Protein Sci 18: 147-60.
26. Stoebel DM, Dorman CJ. 2010. The effect of mobile element IS10 on experimental regulatory evolution in Escherichia coli. Mol Biol Evol 27: 2105-12.
27. Hottes AK, Freddolino PL, Khare A, Donnell ZN, et al. 2013. Bacterial adaptation through loss of function. PLoS Genet 9: e1003617.
28. Dhar R, Bergmiller T, Wagner A. 2014. Increased gene dosage plays a predominant role in the initial stages of evolution of duplicate TEM-1 beta lactamase genes. Evolution 68: 1775-91.
29. Maharjan RP, Gaffe J, Plucain J, Schliep M, et al. 2013. A case of adaptation through a mutation in a tandem duplication during experimental evolution in Escherichia coli. BMC Genomics 14: 441.
30. Glover SW. 1962. Valine-resistant mutants of Escherichia coli K-12. Genet Res 3: 448-60.
31. De Felice M, Levinthal M, Iaccarino M, Guardiola J. 1979. Growth inhibition as a consequence of antagonism between related amino acids: Effect of valine in Escherichia coli K-12. Microbiol Rev 43: 42-58.
32. Umenhoffer K, Fehér T, Balikó G, Ayaydin F, et al. 2010. Reduced evolvability of Escherichia coli MDS42, an IS-less cellular chassis for molecular and synthetic biology applications. Microb Cell Fact 9: 38.
33. Hall BG. 1998. Activation of the bgl operon by adaptive mutation. Mol Biol Evol 15: 1-15.
34. Notley-McRobb L, Pinto R, Seeto S, Ferenci T. 2002. Regulation of mutY and nature of mutator mutations in Escherichia coli populations under nutrient limitation. J Bacteriol 184: 739-45.
35. Notley-McRobb L, Seeto S, Ferenci T. 2002. Enrichment and elimination of mutY mutators in Escherichia coli populations. Genetics 162: 1055-62.
36. Csoergo B, Fehér T, Tímár E, Blattner FR, et al. 2012. Low-mutation-rate, reduced-genome Escherichia coli: An improved host for faithful maintenance of engineered genetic constructs. Microb Cell Fact 11: 11.
37. Wagner J, Nohmi T. 2000. Escherichia coli DNA polymerase IV mutator activity: Genetic requirements and mutational specificity. J Bacteriol 182: 4587-95.
38. Barrick JE, Lenski RE. 2013. Genome dynamics during experimental evolution. Nat Rev Genet 14: 827-39.
39. Conrad TM, Lewis NE, Palsson BO. 2011. Microbial laboratory evolution in the era of genome-scale science. Mol Syst Biol 7: 509.
40. Dettman JR, Rodrigue N, Melnyk AH, Wong A, et al. 2012. Evolutionary insight from whole-genome sequencing of experimentally evolved microbes. Mol Ecol 21: 2058-77.
41. Tenaillon O, Rodriguez-Verdugo A, Gaut RL, McDonald P, et al. 2012. The molecular diversity of adaptive convergence. Science 335: 457-61.
42. Maharjan R, Seeto S, Notley-McRobb L, Ferenci T. 2006. Clonal adaptive radiation in a constant environment. Science 313: 514-7.
43. Kinnersley MA, Holben WE, Rosenzweig F. 2009. E unibus plurum: Genomic analysis of an experimentally evolved polymorphism in Escherichia coli. PLoS Genet 5: e1000713.
44. Kvitek DJ, Sherlock G. 2013. Whole genome, whole population sequencing reveals that loss of signaling networks is the major adaptive strategy in a constant environment. PLoS Genet 9: e1003972.
45. Maharjan R, Seeto S, Ferenci T. 2007. Divergence and redundancy of transport and metabolic rate-yield strategies in a single Escherichia coli population. J Bacteriol 189: 2350-8.
46. Wang L, Spira B, Zhou ZM, Feng L, et al. 2010. Divergence involving global regulatory gene mutations in an Escherichia coli population evolving under phosphate limitation. Genome Biol Evol 2: 478-87.
47. Ferenci T. 2008. Bacterial physiology, regulation and mutational adaptation in a chemostat environment. Adv Microb Physiol 53: 169-229.
48. Maharjan R, Ferenci T, Reeves P, Li Y, et al. 2012. The multiplicity of divergence mechanisms in a single evolving population. Genome Biol 13: R41.
49. Maharjan RP, Ferenci T. 2013. Epistatic interactions determine the mutational pathways and coexistence of lineages in clonal Escherichia coli populations. Evolution 67: 2762-8.
50. Maharjan R, Zhou ZM, Ren Y, Li Y, et al. 2010. Genomic identification of a novel mutation in hfq that provides multiple benefits in evolving glucose-limited populations of Escherichia coli. J Bacteriol 192: 4517-21.
51. Notley-McRobb L, Ferenci T. 1999. The generation of multiple coexisting mal-regulatory mutations through polygenic evolution in glucose-limited populations of Escherichia coli. Environ Microbiol 1: 45-52.
52. Gaffe J, McKenzie C, Maharjan RP, Coursange E, et al. 2011. Insertion sequence-driven evolution of Escherichia coli in chemostats. J Mol Evol 72: 398-412.
53. Ostrowski EA, Woods RJ, Lenski RE. 2008. The genetic basis of parallel and divergent phenotypic responses in evolving populations of Escherichia coli. Proc Biol Sci 275: 277-84.
54. Gresham D, Desai MM, Tucker CM, Jenq HT, et al. 2008. The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet 4: e1000303.
55. Wenger JW, Piotrowski J, Nagarajan S, Chiotti K, et al. 2011. Hunger artists: Yeast adapted to carbon limitation show trade-offs under carbon sufficiency. PLoS Genet 7: e1002202.
56. Nei M. 2007. The new mutation theory of phenotypic evolution. Proc Natl Acad Sci USA 104: 12235-42.
57. de Jong IG, Haccou P, Kuipers OP. 2011. Bet hedging or not? A guide to proper classification of microbial survival strategies. BioEssays 33: 215-23.
58. Lewis K. 2010. Persister cells. Annu Rev Microbiol 64: 357-72.
59. Veening JW, Smits WK, Kuipers OP. 2008. Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol 62: 193-210.
60. Maharjan R, McKenzie C, Yeung A, Ferenci T. 2013. The basis of antagonistic pleiotropy in hfq mutations that have opposite effects on fitness at slow and fast growth rates. Heredity 110: 10-8.
61. Pennington JM, Rosenberg SM. 2007. Spontaneous DNA breakage in single living Escherichia coli cells. Nat Genet 39: 797-802.