Evidence of Selection upon Genomic GC-Content in Bacteria
The genomic GC-content of bacteria varies dramatically, from less than 20% to more than 70%. This variation is generally ascribed to differences in the pattern of mutation between bacteria. Here we test this hypothesis by examining patterns of synonymous polymorphism using datasets from 149 bacterial species. We find a large excess of synonymous GC→AT mutations over AT→GC mutations segregating in all but the most AT-rich bacteria, across a broad range of phylogenetically diverse species. We show that the excess of GC→AT mutations is inconsistent with mutation bias, since it would imply that most GC-rich bacteria are declining in GC-content; such a pattern would be unsustainable. We also show that the patterns are probably not due to translational selection or biased gene conversion, because optimal codons tend to be AT-rich, and the excess of GC→AT SNPs is observed in datasets with no evidence of recombination. We therefore conclude that there is selection to increase synonymous GC-content in many species. Since synonymous GC-content is highly correlated to genomic GC-content, we further conclude that there is selection on genomic base composition in many bacteria.
Vyšlo v časopise:
Evidence of Selection upon Genomic GC-Content in Bacteria. PLoS Genet 6(9): e32767. doi:10.1371/journal.pgen.1001107
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001107
Souhrn
The genomic GC-content of bacteria varies dramatically, from less than 20% to more than 70%. This variation is generally ascribed to differences in the pattern of mutation between bacteria. Here we test this hypothesis by examining patterns of synonymous polymorphism using datasets from 149 bacterial species. We find a large excess of synonymous GC→AT mutations over AT→GC mutations segregating in all but the most AT-rich bacteria, across a broad range of phylogenetically diverse species. We show that the excess of GC→AT mutations is inconsistent with mutation bias, since it would imply that most GC-rich bacteria are declining in GC-content; such a pattern would be unsustainable. We also show that the patterns are probably not due to translational selection or biased gene conversion, because optimal codons tend to be AT-rich, and the excess of GC→AT SNPs is observed in datasets with no evidence of recombination. We therefore conclude that there is selection to increase synonymous GC-content in many species. Since synonymous GC-content is highly correlated to genomic GC-content, we further conclude that there is selection on genomic base composition in many bacteria.
Zdroje
1. NakabachiA
YamashitaA
TohH
IshikawaH
DunbarHE
2006 The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314 267
2. BernardiG
BernardiG
1985 Codon usage and genome composition. J Mol Evol 22 363 365
3. GuX
Hewett-EmmettD
LiWH
1998 Directional mutational pressure affects the amino acid composition and hydrophobicity of proteins in bacteria. Genetica 102–103 383 391
4. SharpPM
BailesE
GrocockRJ
PedenJF
SockettRE
2005 Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res 33 1141 1153
5. Haywood-FarmerE
OttoSP
2003 The evolution of genomic base composition in bacteria. Evolution 57 1783 1792
6. BentleySD
ParkhillJ
2004 Comparative genomic structure of prokaryotes. Annu Rev Genet 38 771 792
7. SueokaN
1961 Compositional correlation between deoxyribonucleic acid and protein. Cold Spring Harb Symp Quant Biol 26 35 43
8. FreeseE
1962 On the evolution of base composition of DNA. J Theor Biol 3 82 101
9. RochaEP
DanchinA
2002 Base composition bias might result from competition for metabolic resources. Trends Genet 18 291 294
10. WoolfitM
BromhamL
2003 Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes. Mol Biol Evol 20 1545 1555
11. FoerstnerKU
von MeringC
HooperSD
BorkP
2005 Environments shape the nucleotide composition of genomes. EMBO Rep 6 1208 1213
12. NayaH
RomeroH
ZavalaA
AlvarezB
MustoH
2002 Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. J Mol Evol 55 260 264
13. 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
14. MustoH
NayaH
ZavalaA
RomeroH
Alvarez-ValinF
2006 Genomic GC level, optimal growth temperature, and genome size in prokaryotes. Biochem Biophys Res Commun 347 1 3
15. GaltierN
LobryJ
1997 Relationships between genomic G+C content, RNA secondary structures and optimal growth temperature in prokaryotes. J Mol Evol 44 632 636
16. HurstLD
MerchantAR
2001 High guanine-cytosine content is not an adaptation to high temperature: a comparative analysis amongst prokaryotes. Proc Biol Sci 268 493 497
17. 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
18. SargentiniNJ
SmithKC
1994 DNA sequence analysis of gamma-radiation (anoxic)-induced and spontaneous lacId mutations in Escherichia coli K-12. Mutat Res 309 147 163
19. SchaaperRM
DunnRL
1991 Spontaneous mutation in the Escherichia coli lacI gene. Genetics 129 317 326
20. LynchM
2007 The origins of genome architecture Sunderland Sinauer
21. DeschavannmeP
FilipskiJ
1995 Correlation of GC content with replication timing and repair mechanisms in weakly expressed E.coli genes. Nucl Acids Res 23 1350 1353
22. BalbiKJ
RochaEP
FeilEJ
2009 The temporal dynamics of slightly deleterious mutations in Escherichia coli and Shigella spp. Mol Biol Evol 26 345 355
23. 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
24. AkashiH
1995 Inferring weak selection from patterns of polymorphism and divergence at “silent” sites in Drosophila DNA. Genetics 139 1067 1076
25. Eyre-WalkerA
1997 Differentiating selection and mutation bias. Genetics 147 1983 1987
26. HeyJ
2001 The mind of the species problem. Trends Ecol Evol 16 326 329
27. Eyre-WalkerA
1998 Problems with parsimony in sequences of biased base composition. J Mol Evol 47 686 690
28. SharpPM
BurgessCJ
LloydAT
MitchellKJ
1992 Selective use of termination and variation in codon choice.
HatfieldDL
LeeBJ
PirtleRM
Transfer RNA in protein synthesis Boca Raton CRC Press
29. BirdsellJA
2002 Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. Mol Biol Evol 19 1181 1197
30. DuretL
GaltierN
2009 Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 10 285 311
31. MaraisG
2003 Biased gene conversion: implications for genome and sex evolution. Trends Genet 19 330 338
32. NagylakiT
1983 Evolution of a finite population under gene conversion. Proc Natl Acad Sci USA 80 6278 6281
33. Eyre-WalkerA
1999 Evidence of selection on silent site base composition in mammals: potential implications for the evolution of isochores and junk DNA. Genetics 152 675 683
34. HudsonRR
KaplanNL
1985 Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111 147 164
35. VosM
DidelotX
2009 A comparison of homologous recombination rates in bacteria and archaea. ISME J 3 199 208
36. GogartenJP
TownsendJP
2005 Horizontal gene transfer, genome innovation and evolution. Nature Rev Microbiol 3 679 687
37. DaubinV
LeratE
PerriereG
2003 The source of laterally transferred genes in bacterial genomes. Genome Biol 4 R57
38. McClellandM
SandersonKE
SpiethJ
CliftonSW
LatreilleP
2001 Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413 852 856
39. LawrenceJG
OchmanH
1997 Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol 44 383 397
40. BernM
GoldbergD
2005 Automatic selection of representative proteins for bacterial phylogeny. BMC Evol Biol 5 34
41. Maynard SmithJM
1992 Analyzing the mosaic structure of genes. J Mol Evol 34 126 129
42. HershbergR
PetrovP
2010 Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet 6 e1001115
43. LynchM
ConeryJS
2003 The origins of genome complexity. Science 302 1401 1404
44. LynchM
2010 Rate, molecular spectrum, and consequences of human mutation. Proc Natl Acad Sci USA 107 961 968
45. TouchonM
HoedeC
TenaillonO
BarbeV
BaeriswylS
2009 Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5 e1000344
46. MoranNA
McCutcheonJP
NakabachiA
2008 Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42 165 190
47. MoranNA
McLaughlinHJ
SorekR
2009 The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323 379 382
48. WernegreenJJ
FunkDJ
2004 Mutation exposed: a neutral explanation for extreme base composition of an endosymbiont genome. J Mol Evol 59 849 858
49. 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
50. EdgarRC
2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 1792 1797
51. DesperR
GascuelO
2002 Fast and accurate phylogeny reconstruction algorithms based on the minimum-evolution principle. J Comput Biol 9 687 705
52. PiganeauG
GardnerMJ
Eyre-WalkerA
2004 A broad survey of recombination in animal mitochondrial DNA. Mol Biol Evol 21 2319 2325
53. WrightS
1931 Evolution in Mendelian populations. Genetics 16 97 159
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 9
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- Optimal Strategy for Competence Differentiation in Bacteria
- Synthesizing and Salvaging NAD: Lessons Learned from
- 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