Evidence That Mutation Is Universally Biased towards AT in Bacteria
Mutation is the engine that drives evolution and adaptation forward in that it generates the variation on which natural selection acts. Mutation is a random process that nevertheless occurs according to certain biases. Elucidating mutational biases and the way they vary across species and within genomes is crucial to understanding evolution and adaptation. Here we demonstrate that clonal pathogens that evolve under severely relaxed selection are uniquely suitable for studying mutational biases in bacteria. We estimate mutational patterns using sequence datasets from five such clonal pathogens belonging to four diverse bacterial clades that span most of the range of genomic nucleotide content. We demonstrate that across different types of sites and in all four clades mutation is consistently biased towards AT. This is true even in clades that have high genomic GC content. In all studied cases the mutational bias towards AT is primarily due to the high rate of C/G to T/A transitions. These results suggest that bacterial mutational biases are far less variable than previously thought. They further demonstrate that variation in nucleotide content cannot stem entirely from variation in mutational biases and that natural selection and/or a natural selection-like process such as biased gene conversion strongly affect nucleotide content.
Vyšlo v časopise:
Evidence That Mutation Is Universally Biased towards AT in Bacteria. PLoS Genet 6(9): e32767. doi:10.1371/journal.pgen.1001115
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001115
Souhrn
Mutation is the engine that drives evolution and adaptation forward in that it generates the variation on which natural selection acts. Mutation is a random process that nevertheless occurs according to certain biases. Elucidating mutational biases and the way they vary across species and within genomes is crucial to understanding evolution and adaptation. Here we demonstrate that clonal pathogens that evolve under severely relaxed selection are uniquely suitable for studying mutational biases in bacteria. We estimate mutational patterns using sequence datasets from five such clonal pathogens belonging to four diverse bacterial clades that span most of the range of genomic nucleotide content. We demonstrate that across different types of sites and in all four clades mutation is consistently biased towards AT. This is true even in clades that have high genomic GC content. In all studied cases the mutational bias towards AT is primarily due to the high rate of C/G to T/A transitions. These results suggest that bacterial mutational biases are far less variable than previously thought. They further demonstrate that variation in nucleotide content cannot stem entirely from variation in mutational biases and that natural selection and/or a natural selection-like process such as biased gene conversion strongly affect nucleotide content.
Zdroje
1. LynchM
2007 The origins of Genome Architecture Sunderland, MA Sinauer Associates, Inc
2. SueokaN
1962 On the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci U S A 48 582 592
3. BentleySD
ParkhillJ
2004 Comparative genomic structure of prokaryotes. Annu Rev Genet 38 771 792
4. MutoA
OsawaS
1987 The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci U S A 84 166 169
5. ChenSL
LeeW
HottesAK
ShapiroL
McAdamsHH
2004 Codon usage between genomes is constrained by genome-wide mutational processes. Proc Natl Acad Sci U S A 101 3480 3485
6. ShieldsDC
1990 Switches in species-specific codon preferences: the influence of mutation biases. J Mol Evol 31 71 80
7. AnderssonSG
SharpPM
1996 Codon usage and base composition in Rickettsia prowazekii. J Mol Evol 42 525 536
8. GraurD
LiW
2000 Fundementals of molecular evolution Sunderland, MA Sinauer Associaes, Inc 412 415
9. DuretL
GaltierN
2009 Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 10 285 311
10. NagylakiT
PetesTD
1982 Intrachromosomal gene conversion and the maintenance of sequence homogeneity among repeated genes. Genetics 100 315 337
11. TouchonM
HoedeC
TenaillonO
BarbeV
BaeriswylS
2009 Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5 e1000344
12. ElenaSF
LenskiRE
2003 Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4 457 469
13. SchaaperRM
DunnRL
1991 Spontaneous mutation in the Escherichia coli lacI gene. Genetics 129 317 326
14. HudsonRE
BergthorssonU
OchmanH
2003 Transcription increases multiple spontaneous point mutations in Salmonella enterica. Nucleic Acids Res 31 4517 4522
15. GalhardoRS
HastingsPJ
RosenbergSM
2007 Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol Biol 42 399 435
16. BullHJ
LombardoMJ
RosenbergSM
2001 Stationary-phase mutation in the bacterial chromosome: recombination protein and DNA polymerase IV dependence. Proc Natl Acad Sci U S A 98 8334 8341
17. MitchellA
GraurD
2005 Inferring the pattern of spontaneous mutation from the pattern of substitution in unitary pseudogenes of Mycobacterium leprae and a comparison of mutation patterns among distantly related organisms. J Mol Evol 61 795 803
18. RochaEP
TouchonM
FeilEJ
2006 Similar compositional biases are caused by very different mutational effects. Genome Res 16 1537 1547
19. AkashiH
1995 Inferring weak selection from patterns of polymorphism and divergence at “silent” sites in Drosophila DNA. Genetics 139 1067 1076
20. MesserPW
2009 Measuring the Rates of Spontaneous Mutation from Deep and Large-Scale Polymorphism Data. Genetics
21. HaddrillPR
CharlesworthB
2008 Non-neutral processes drive the nucleotide composition of non-coding sequences in Drosophila. Biol Lett 4 438 441
22. WebsterMT
SmithNG
EllegrenH
2003 Compositional evolution of noncoding DNA in the human and chimpanzee genomes. Mol Biol Evol 20 278 286
23. LercherMJ
SmithNG
Eyre-WalkerA
HurstLD
2002 The evolution of isochores: evidence from SNP frequency distributions. Genetics 162 1805 1810
24. DoolittleWF
ZhaxybayevaO
2009 On the origin of prokaryotic species. Genome Res 19 744 756
25. HershbergR
LipatovM
SmallPM
ShefferH
NiemannS
2008 High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol 6 e311
26. LynchM
2010 Rate, molecular spectrum, and consequences of human mutation. Proc Natl Acad Sci U S A 107 961 968
27. PetrovDA
HartlDL
1999 Patterns of nucleotide substitution in Drosophila and mammalian genomes. Proc Natl Acad Sci U S A 96 1475 1479
28. OssowskiS
SchneebergerK
Lucas-LledoJI
WarthmannN
ClarkRM
2009 The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327 92 94
29. DenverDR
DolanPC
WilhelmLJ
SungW
Lucas-LledoJI
2009 A genome-wide view of Caenorhabditis elegans base-substitution mutation processes. Proc Natl Acad Sci U S A 106 16310 16314
30. KeightleyPD
TrivediU
ThomsonM
OliverF
KumarS
2009 Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines. Genome Res 19 1195 1201
31. LynchM
SungW
MorrisK
CoffeyN
LandryCR
2008 A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc Natl Acad Sci U S A 105 9272 9277
32. BalbiKJ
RochaEP
FeilEJ
2009 The temporal dynamics of slightly deleterious mutations in Escherichia coli and Shigella spp. Mol Biol Evol 26 345 355
33. LindPA
AnderssonDI
2008 Whole-genome mutational biases in bacteria. Proc Natl Acad Sci U S A 105 17878 17883
34. SprattBG
2004 Exploring the concept of clonality in bacteria. Methods Mol Biol 266 323 352
35. NeiM
GojoboriT
1986 Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3 418 426
36. FayJC
WuCI
2003 Sequence divergence, functional constraint, and selection in protein evolution. Annu Rev Genomics Hum Genet 4 213 235
37. HershbergR
TangH
PetrovDA
2007 Reduced selection leads to accelerated gene loss in Shigella. Genome Biol 8 R164
38. MoranNA
McCutcheonJP
NakabachiA
2008 Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42 165 190
39. LiWH
1987 Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. J Mol Evol 24 337 345
40. HershbergR
PetrovDA
2008 Selection on codon bias. Annu Rev Genet 42 287 299
41. HildebrandF
MeyerA
Eyre-WalkerA
2010 Evidence of Selection upon Genomic GC-content in Bacteria. PLoS Genet 6 e1001107
42. HershbergR
PetrovDA
2009 General rules for optimal codon choice. PLoS Genet 5 e1000556
43. McCutcheonJP
McDonaldBR
MoranNA
2009 Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Genet 5 e1000565
44. GaltierN
LobryJR
1997 Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J Mol Evol 44 632 636
45. MustoH
NayaH
ZavalaA
RomeroH
Alvarez-ValinF
2004 Correlations between genomic GC levels and optimal growth temperatures in prokaryotes. FEBS Lett 573 73 77
46. NayaH
RomeroH
ZavalaA
AlvarezB
MustoH
2002 Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. J Mol Evol 55 260 264
47. McEwanCE
GathererD
McEwanNR
1998 Nitrogen-fixing aerobic bacteria have higher genomic GC content than non-fixing species within the same genus. Hereditas 128 173 178
48. WangHC
SuskoE
RogerAJ
2006 On the correlation between genomic G+C content and optimal growth temperature in prokaryotes: data quality and confounding factors. Biochem Biophys Res Commun 342 681 684
49. ZhaoX
ZhangZ
YanJ
YuJ
2007 GC content variability of eubacteria is governed by the pol III alpha subunit. Biochem Biophys Res Commun 356 20 25
50. MarashiSA
GhalanborZ
2004 Correlations between genomic GC levels and optimal growth temperatures are not ‘robust’. Biochem Biophys Res Commun 325 381 383
51. BasakS
MandalS
GhoshTC
2005 Correlations between genomic GC levels and optimal growth temperatures: some comments. Biochem Biophys Res Commun 327 969 970
52. HoltKE
ParkhillJ
MazzoniCJ
RoumagnacP
WeillFX
2008 High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Genet 40 987 993
53. GreeneJM
CollinsF
LefkowitzEJ
RoosD
ScheuermannRH
2007 National Institute of Allergy and Infectious Diseases bioinformatics resource centers: new assets for pathogen informatics. Infect Immun 75 3212 3219
54. PearsonWR
LipmanDJ
1988 Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A 85 2444 2448
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 9
- 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
- Synthesizing and Salvaging NAD: Lessons Learned from
- Optimal Strategy for Competence Differentiation in Bacteria
- Long- and Short-Term Selective Forces on Malaria Parasite Genomes
- Identifying Signatures of Natural Selection in Tibetan and Andean Populations Using Dense Genome Scan Data