#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Frequent Beneficial Mutations during Single-Colony Serial Transfer of


The appearance of new mutations within a population provides the raw material for evolution. The consistent decline in fitness observed in classical mutation accumulation studies has provided support for the long-held view that deleterious mutations are more common than beneficial mutations. Here we present results of a study using a mutation accumulation design with the bacterium Streptococcus pneumoniae in which the fitness of the derived populations increased. This rise in fitness was associated specifically with adaptation to survival during brief stationary phase periods between single-colony population bottlenecks. To understand better the population dynamics behind this unanticipated adaptation, we developed a maximum likelihood model describing the processes of mutation and stationary-phase selection in the context of frequent population bottlenecks. Using this model, we estimate that the rate of beneficial mutations may be as high as 4.8×10−4 events per genome for each time interval corresponding to the pneumococcal generation time. This rate is several orders of magnitude higher than earlier estimates of beneficial mutation rates in bacteria but supports recent results obtained through the propagation of small populations of Escherichia coli. Our findings indicate that beneficial mutations may be relatively frequent in bacteria and suggest that in S. pneumoniae, which develops natural competence for transformation, a steady supply of such mutations may be available for sampling by recombination.


Vyšlo v časopise: Frequent Beneficial Mutations during Single-Colony Serial Transfer of. PLoS Genet 7(8): e32767. doi:10.1371/journal.pgen.1002232
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002232

Souhrn

The appearance of new mutations within a population provides the raw material for evolution. The consistent decline in fitness observed in classical mutation accumulation studies has provided support for the long-held view that deleterious mutations are more common than beneficial mutations. Here we present results of a study using a mutation accumulation design with the bacterium Streptococcus pneumoniae in which the fitness of the derived populations increased. This rise in fitness was associated specifically with adaptation to survival during brief stationary phase periods between single-colony population bottlenecks. To understand better the population dynamics behind this unanticipated adaptation, we developed a maximum likelihood model describing the processes of mutation and stationary-phase selection in the context of frequent population bottlenecks. Using this model, we estimate that the rate of beneficial mutations may be as high as 4.8×10−4 events per genome for each time interval corresponding to the pneumococcal generation time. This rate is several orders of magnitude higher than earlier estimates of beneficial mutation rates in bacteria but supports recent results obtained through the propagation of small populations of Escherichia coli. Our findings indicate that beneficial mutations may be relatively frequent in bacteria and suggest that in S. pneumoniae, which develops natural competence for transformation, a steady supply of such mutations may be available for sampling by recombination.


Zdroje

1. FryJDKeightleyPDHeinsohnSLNuzhdinSV 1999 New estimates of the rates and effects of mildly deleterious mutation in Drosophila melanogaster. Proc Nat Acad Sci U S A 96 574 579

2. ChavarríasDLópez-FanjulCGarcía-DoradoA 2001 The rate of mutation and the homozygous and heterozygous mutational effects for competitive viability: a long-term experiment with Drosophila melanogaster. Genetics 158 681 693

3. KibotaTTLynchM 1996 Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature 381 694 696

4. TrindaleSPerfeitoLGordoI 2010 Rate and effects of spontaneous mutations that affect fitness in mutator Escherichia coli. Phil Trans R Soc B 365 1177 1186

5. KeightleyPDCaballeroA 1997 Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans. Proc Nat Acad Sci U S A 94 3823 3827

6. VassilievaLLHookAMLynchM 2000 The fitness effects of spontaneous mutations in Caenorhabditis elegans. Evolution 54 1234 1246

7. SchultzSTLynchMWillisJH 1999 Spontaneous deleterious mutation in Arabidopsis thaliana. Proc Nat Acad Sci U S A 96 11393 11398

8. BritoPHGuilhermeESoaresHGordoI 2010 Mutation accumulation in Tetrahymena. BMC Evol Biol 10 354

9. ZeylCde VisserJAGM 2001 Estimates of the rate and distribution of fitness effects of spontaneous mutation in Saccharomyces cerevisiae. Genetics 157 53 61

10. AnderssonDIHughesD 1996 Muller's ratchet decreases fitness of a DNA-based microbe. Proc Natl Acad Sci U S A 93 906 907

11. GerrishPJLenskiRE 1998 The fate of competing beneficial mutations in an asexual population. Genetica 102/ 103 127 144

12. ImhofMSchlöttererC 2001 Fitness effects of advantageous mutations in evolving Escherichia coli populations. Proc Nat Acad Sci U S A 98 1113 1117

13. SniegowskiPDGerrishPJ 2010 Beneficial mutations and the dynamics of adaptation in asexual populations. Phil Trans R Soc B 365 1255 1263

14. PerfeitoLFernandesLMotaCGordoI 2007 Adaptive mutations in bacteria: high rate and small effects. Science 317 813 815

15. WhitneyCGFarleyMMHadlerJHarrisonLHLexauC 2000 Increasing prevalence of multidrug-resistant Streptococcus pneumoniae in the United States. New Eng J Med 343 1917 1924

16. HicksLAHarrisonLHFlanneryBHandlerJLSchaffnerW 2007 Incidence of pneumococcal disease due to non-pneumococcal conjugate vaccine (PCV7) serotypes in the United Statess during the era of widespread PCV7 vaccination, 1998–2004. J Infect Dis 196 1346 1354

17. FeilEJMaynard SmithJEnrightMCSprattBG 2000 Estimating recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. Genetics 154 1439 1450

18. HanageWPFraserCSprattBG 2006 The impact of homologous recombination on the generation of diversity in bacteria. J Theor Biol 239 210 219

19. AveryOTMacLeodCMMcCartyM 1944 Studies on the nature of the chemical nature of the substance inducing transformation of pneumococcal types. J Exp Med 79 137 157

20. ClaverysJ-PMartinBPolardP 2009 The genetic transformation machinery: composition, localization, and mechanism. FEMS Microbiol Rev 33 643 656

21. VasiFKLenskiRE 1999 Ecological strategies and fitness tradeoffs in Escherichia coli mutants adapted to prolonged starvation. J Genet 78 43 49

22. LenskiRERoseMRSimpsonSCTadlerSC 1991 Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Nat 138 1315 1341

23. de VisserJAGMZeylCWGerrishPJBlanchardJLLenskiRE 1999 Diminishing returns from mutation supply rate in asexual populations. Science 283 404 406

24. SniegowskiPDGerrishPJLenskiRE 1997 Evolution of high mutation rates in experimental populations of E. coli. Nature 387 703 705

25. CairnsJFosterPL 1991 Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128 695 701

26. WrandeMRothJRHughesD 2008 Accumulation of mutants in “aging” bacterial colonies is due to growth under selection, not stress-induced mutagenesis. Proc Nat Acad Sci U S A 105 11863 11868

27. PonderRGFonvilleNCRosenbergSM 2005 A switch from high-fidelity to error-prone DNA double-strand break repair underlies stress-induced mutation. Mol Cell 19 791 804

28. BatemanAJ 1959 The viability of near-normal irradiated chromosomes. Int J Radiat Biol 1 170 180

29. MukaiT 1964 The genetic structure of natural populations of Drosophila melanogaster. I. Spontaneous mutation rate of polygenes controlling viability. Genetics 50 1 19

30. JosephSBHallDW 2004 Spontaneous mutations in diploid Saccharomyces cerevisiae: more beneficial than expected. Genetics 168 1817 1825

31. HallDWJosephSB 2010 A high frequency of beneficial mutations across multiple fitness components in Saccharomyces cerevisiae. Genetics 185 1397 1409

32. ShawFHGeyerCJShawRG 2002 A comprehensive model of mutations affecting fitness and inferences for Arabidopsis thaliana. Evolution 56 453 463

33. FerenciT 2005 Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Mol Microbiol 57 1 8

34. LevertMZamfirOClermontOBouvetOLespinatsS 2010 Molecular and evolutionary bases of within-patient genotypic and phenotypic diversity in Escherichia coli extraintestinal infections. PLoS Pathog 6 e1001125 doi:10.1371/journal.ppat.1001125

35. PericoneCDBaeDShchepetovMMcCoolTWeiserJN 2002 Short-sequence tandem and nontandem DNA repeats and endogenous hydrogen peroxide production contribute to genetic instability of Streptococcus pneumoniae. J Bacteriol 184 4392 4399

36. GouldCVSniegowskiPDShchepetovMMetlayJPWeiserJN 2007 Identifying mutator phenotypes among fluoroquinolone-resistant strains of Streptococcus pneumoniae using fluctuation analysis. Antimicrob Agents Chemother 51 3225 3229

37. BjedovITenaillonOGérardBSouzaVDenamurE 2003 Sress-induced mutagenesis in bacteria. Science 300 1404 1409

38. LoeweLTextorVSchererS 2003 High deleterious genomic mutation rate in stationary phase of Escherichia coli. Science 302 1558 1560

39. de VisserJAGMRozenDE 2004 Comment on “High deleterious genomic mutation rate in stationary phase of Escherichia coli”. Science 304 518

40. FisherRA 1930 The Genetical Theory of Natural Selection Oxford Oxford University Press

41. OrrHA 1998 The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52 935 949

42. SilanderOKTenaillonOChaoL 2007 Understanding the evolutionary fate of finite populations: the dynamics of mutational effects. PLoS Biol 5 e94 doi:10.1371/journal.pbio.0050094

43. ZambranoMMKolterR 1996 GASPing for life in stationary phase. Cell 86 181 184

44. MirallesRGerrishPJMoyaAElenaSF 1999 Clonal interference and the evolution of RNA viruses. Science 285 1745 1747

45. SungCKLiHClaverysJPMorrisonDA 2001 An rpsL cassette, Janus, for gene replacement through negative selection in Streptococcus pneumoniae. App Env Microbiol 67 5190 5196

46. LauPCYSungCKLeeJHMorrisonDACvitkovitchDG 2002 PCR ligation mutagenesis in transformable streptococci: application and efficiency. J Microbiol Methods 49 193 205

47. SebertMEPatelKPPlotnickMWeiserJN 2005 Pneumococcal HtrA protease mediates inhibition of competence by the CiaRH two-component signaling system. J Bacteriol 187 3969 3979

48. RozenDEde VisserJAGMGerrishPJ 2002 Fitness effects of fixed beneficial mutations in microbial populations. Curr Biol 12 1040 1045

49. OrrHA 2003 The distribution of fitness effects among beneficial mutations. Genetics 163 1519 1526

50. KassenRBataillonT 2006 Distribution of fitness effects among beneficial mutations before selection in experimental populations of bacteria. Nat Genet 38 484 488

51. LuriaSEDelbrückM 1943 Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28 491 511

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 8
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#