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Transition from Positive to Neutral in Mutation Fixation along with Continuing Rising Fitness in Thermal Adaptive Evolution


It remains to be determined experimentally whether increasing fitness is related to positive selection, while stationary fitness is related to neutral evolution. Long-term laboratory evolution in Escherichia coli was performed under conditions of thermal stress under defined laboratory conditions. The complete cell growth data showed common continuous fitness recovery to every 2°C or 4°C stepwise temperature upshift, finally resulting in an evolved E. coli strain with an improved upper temperature limit as high as 45.9°C after 523 days of serial transfer, equivalent to 7,560 generations, in minimal medium. Two-phase fitness dynamics, a rapid growth recovery phase followed by a gradual increasing growth phase, was clearly observed at diverse temperatures throughout the entire evolutionary process. Whole-genome sequence analysis revealed the transition from positive to neutral in mutation fixation, accompanied with a considerable escalation of spontaneous substitution rate in the late fitness recovery phase. It suggested that continually increasing fitness not always resulted in the reduction of genetic diversity due to the sequential takeovers by fit mutants, but caused the accumulation of a considerable number of mutations that facilitated the neutral evolution.


Vyšlo v časopise: Transition from Positive to Neutral in Mutation Fixation along with Continuing Rising Fitness in Thermal Adaptive Evolution. PLoS Genet 6(10): e32767. doi:10.1371/journal.pgen.1001164
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001164

Souhrn

It remains to be determined experimentally whether increasing fitness is related to positive selection, while stationary fitness is related to neutral evolution. Long-term laboratory evolution in Escherichia coli was performed under conditions of thermal stress under defined laboratory conditions. The complete cell growth data showed common continuous fitness recovery to every 2°C or 4°C stepwise temperature upshift, finally resulting in an evolved E. coli strain with an improved upper temperature limit as high as 45.9°C after 523 days of serial transfer, equivalent to 7,560 generations, in minimal medium. Two-phase fitness dynamics, a rapid growth recovery phase followed by a gradual increasing growth phase, was clearly observed at diverse temperatures throughout the entire evolutionary process. Whole-genome sequence analysis revealed the transition from positive to neutral in mutation fixation, accompanied with a considerable escalation of spontaneous substitution rate in the late fitness recovery phase. It suggested that continually increasing fitness not always resulted in the reduction of genetic diversity due to the sequential takeovers by fit mutants, but caused the accumulation of a considerable number of mutations that facilitated the neutral evolution.


Zdroje

1. FongSS

JoyceAR

PalssonBO

2005 Parallel adaptive evolution cultures of Escherichia coli lead to convergent growth phenotypes with different gene expression states. Genome Res 15 1365 1372

2. HerringCD

RaghunathanA

HonischC

PatelT

ApplebeeMK

2006 Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat Genet 38 1406 1412

3. BarrickJE

YuDS

YoonSH

JeongH

OhTK

2009 Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461 1243 1247

4. KimuraM

1983 The neutral theory of molecular evolution. Cambridge Oxford Univeristy Press

5. YuraT

NagaiH

MoriH

1993 Regulation of the heat-shock response in bacteria. Annu Rev Microbiol 47 321 350

6. BukauB

WeissmanJ

HorwichA

2006 Molecular chaperones and protein quality control. Cell 125 443 451

7. HartlFU

Hayer-HartlM

2002 Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295 1852 1858

8. BradfordMA

DaviesCA

FreySD

MaddoxTR

MelilloJM

2008 Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11 1316 1327

9. MongoldJA

BennettAF

LenskiRE

1999 Evolutionary adaptation to temperature. VII. Extension of the upper thermal limit of Escherichia coli. Evolution 53 386 394

10. BennettAF

LenskiRE

2007 An experimental test of evolutionary trade-offs during temperature adaptation. Proc Natl Acad Sci U S A 104 Suppl 1 8649 8654

11. BergthorssonU

OchmanH

1999 Chromosomal changes during experimental evolution in laboratory populations of Escherichia coli. J Bacteriol 181 1360 1363

12. RiehleMM

BennettAF

LongAD

2001 Genetic architecture of thermal adaptation in Escherichia coli. Proc Natl Acad Sci U S A 98 525 530

13. RiehleMM

BennettAF

LenskiRE

LongAD

2003 Evolutionary changes in heat-inducible gene expression in lines of Escherichia coli adapted to high temperature. Physiol Genomics 14 47 58

14. LenskiRE

TravisanoM

1994 Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci U S A 91 6808 6814

15. AzumaY

HosoyamaA

MatsutaniM

FuruyaN

HorikawaH

2009 Whole-genome analyses reveal genetic instability of Acetobacter pasteurianus. Nucleic Acids Res 37 5768 5783

16. DrakeJW

CharlesworthB

CharlesworthD

CrowJF

1998 Rates of spontaneous mutation. Genetics 148 1667 1686

17. NeiM

GojoboriT

1986 Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3 418 426

18. NeiM

2005 Selectionism and neutralism in molecular evolution. Mol Biol Evol 22 2318 2342

19. ComeronJM

1995 A method for estimating the numbers of synonymous and nonsynonymous substitutions per site. J Mol Evol 41 1152 1159

20. BennettAF

LenskiRE

MittlterJE

1992 Evolutionary adaptation to temperature. I. Fitness responses of Escherichia coli to changes in its thermal environment. Evolution 46 16 30

21. SniegowskiPD

GerrishPJ

LenskiRE

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

22. TaddeiF

RadmanM

Maynard-SmithJ

ToupanceB

GouyonPH

1997 Role of mutator alleles in adaptive evolution. Nature 387 700 702

23. OchmanH

ElwynS

MoranNA

1999 Calibrating bacterial evolution. Proc Natl Acad Sci U S A 96 12638 12643

24. LenskiRE

WinkworthCL

RileyMA

2003 Rates of DNA sequence evolution in experimental populations of Escherichia coli during 20,000 generations. J Mol Evol 56 498 508

25. DenamurE

MaticI

2006 Evolution of mutation rates in bacteria. Mol Microbiol 60 820 827

26. DuretL

2002 Evolution of synonymous codon usage in metazoans. Curr Opin Genet Dev 12 640 649

27. MaruyamaT

KimuraM

1980 Genetic variability and effective population size when local extinction and recolonization of subpopulations are frequent. Proc Natl Acad Sci U S A 77 6710 6714

28. BergOG

1996 Selection intensity for codon bias and the effective population size of Escherichia coli. Genetics 142 1379 1382

29. DePristoMA

WeinreichDM

HartlDL

2005 Missense meanderings in sequence space: a biophysical view of protein evolution. Nat Rev Genet 6 678 687

30. Maisnier-PatinS

RothJR

FredrikssonA

NystromT

BergOG

2005 Genomic buffering mitigates the effects of deleterious mutations in bacteria. Nat Genet 37 1376 1379

31. TokurikiN

TawfikDS

2009 Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459 668 673

32. WarneckeT

HurstLD

2010 GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution. Mol Syst Biol 6 340

33. FontanaW

SchusterP

1998 Continuity in evolution: on the nature of transitions. Science 280 1451 1455

34. SchultesEA

BartelDP

2000 One sequence, two ribozymes: implications for the emergence of new ribozyme folds. Science 289 448 452

35. DePristoMA

HartlDL

WeinreichDM

2007 Mutational reversions during adaptive protein evolution. Mol Biol Evol 24 1608 1610

36. SuzukiT

KashiwagiA

UrabeI

YomoT

2006 Inherent characteristics of gene expression for buffering environmental changes without the corresponding transcriptional regulations. Biophysics 2 63 77

37. DatsenkoKA

WannerBL

2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97 6640 6645

38. KashiwagiA

SakuraiT

TsuruS

YingBW

MoriK

2009 Construction of Escherichia coli gene expression level perturbation collection. Metab Eng 11 56 63

39. BjedovI

TenaillonO

GerardB

SouzaV

DenamurE

2003 Stress-induced mutagenesis in bacteria. Science 300 1404 1409

40. SkarstadK

BoyeE

SteenHB

1986 Timing of initiation of chromosome replication in individual Escherichia coli cells. EMBO J 5 1711 1717

41. OnoN

SuzukiS

FurusawaC

AgataT

KashiwagiA

2008 An improved physico-chemical model of hybridization on high-density oligonucleotide microarrays. Bioinformatics 24 1278 1285

42. SuzukiS

OnoN

FurusawaC

KashiwagiA

YomoT

2007 Experimental optimization of probe length to increase the sequence specificity of high-density oligonucleotide microarrays. BMC Genomics 8 373

43. FurusawaC

OnoN

SuzukiS

AgataT

ShimizuH

2009 Model-based analysis of non-specific binding for background correction of high-density oligonucleotide microarrays. Bioinformatics 25 36 41

44. ZhangL

MilesMF

AldapeKD

2003 A model of molecular interactions on short oligonucleotide microarrays. Nat Biotechnol 21 818 821

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