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
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 10
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Genome-Wide Identification of Targets and Function of Individual MicroRNAs in Mouse Embryonic Stem Cells
- Common Genetic Variants and Modification of Penetrance of -Associated Breast Cancer
- Allele-Specific Down-Regulation of Expression Induced by Retinoids Contributes to Climate Adaptations
- Simultaneous Disruption of Two DNA Polymerases, Polη and Polζ, in Avian DT40 Cells Unmasks the Role of Polη in Cellular Response to Various DNA Lesions