Forces that influence the evolution of codon bias

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1544, 2010, Pages 1203-1212

  Sharp, Paul M ^a   Emery, Laura R ^a   Zeng, Kai ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Bacteria; Codon usage; Mutation bias; Population genetics; Selection

Indexed keywords

ADAPTATION; COLIFORM BACTERIUM; GENE; GENOME; GROWTH RATE; MUTATION; NATURAL SELECTION; POLYMORPHISM; POPULATION GENETICS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 77951570815     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0305     Document Type: Article

References (71)

1. Achtman, M. et al. 2004 Microevolution and history of the pague bacillus, Yersinia pestis. Proc. Natl Acad. Sci. USA 101, 17 837-17 842. (doi:10.1073/pnas.0408026101)
2. Akashi, H. 1994 Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136, 927-935. (Pubitemid 24085643)
3. Andersson, S. G. E. & Kurland, C. G. 1990 Codon preferences in free-living microorganisms. Microbiol. Rev. 54, 198-210.
4. Belozersky, A. N. & Spirin, A. S. 1958 A correlation between the compositions of deoxyribonucleic and ribonucleic acids. Nature 182, 111-112. (doi:10.1038/182111a0)
5. Berg, O. G. & Martelius, M. 1995 Synonymous substitution-rate constants in Escherichia coli and Salmonella typhimurium and their relationship to gene expression and selection pressure. J. Mol. Evol. 41, 449-456. (doi:10.1007/BF00160316)
6. Berg, O. G. & Silva, P. J. N. 1997 Codon bias in Escherichia coli: the influence of codon context on mutation and selection. Nucleic Acids Res. 25, 1397-1404. (doi:10.1093/nar/25.7.1397)
7. Bernardi, G. & Bernardi, G. 1986 Compositional constraints and genome evolution. J. Mol. Evol. 24, 1-11. (doi: 10.1007/BF02099946)
8. Bibb, M. J., Findlay, P. R. & Johnson, M. W. 1984 The relationship between base composition and codon usage in bacterial genes and its use for the simple and reliable identification of protein-coding sequences. Gene 30, 157-166. (doi:10.1016/0378-l119(84)90116-1)
9. Brewer, B. J. 1988 When polymerases collide: replication and the transcriptional organization of the E. coli chromosome. Cell 53, 679-686. (doi:10.1016/00928674(88)90086-4)
10. Bulmer, M. 1991 The selection-mutation-drift theory of synonymous codon usage. Genetics 129, 897-907.
11. Chen, S. L., Lee, W., Hottes, A. K., Shapiro, L. & McAdams, H. H. 2004 Codon usage between genomes is constrained by genome-wide mutational processes. Proc. Natl Acad. Sci. USA 101, 3480-3485. (doi: 10.1073/pnas. 0307827100) (Pubitemid 38338220)
12. Coutourier, E. & Rocha, E. P. C. 2006 Replicationassociated gene dosage effects shape the genomes of fast-growing bacteria but only for transcription and translation genes. Mol. Microbiol. 59, 1506-1518. (doi:10.1111/j.1365-2958.2006.05046.X)
13. Cutter, A. D. 2008 Multilocus patterns of polymorphism and selection across the X chromosome of Caenorhabditis remanei. Genetics 178, 1661-1672. (doi:10.1534/genetics.107.085803)
14. Cutter, A. D. & Charlesworth, B. 2006 Selection intensity on preferred codons correlates with overall codon usage bias in Caenorhabditis remannei. Curr. Biol. 16, 2053-2057. (doi:10.1016/j.cub.2006.08.067)
15. dos Reis, M. & Wernisch, L. 2009 Estimating translational selection in eukaryotic genomes. Mol. Biol. Evol. 26, 451-461. (doi:10.1093/molbev/msn272)
16. Drummond, D. A. & Wilke, C. O. 2008 Mistranslationinduced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134, 341-352. (doi:10.1016/j.cell.2008.05.042)
17. Duret, L. & Mouchiroud, D. 1999 Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila and Arabidopsis. Proc. Natl Acad. Sci. USA 96, 4482-4487. (doi:10.1073/pnas.96.8.4482) (Pubitemid 29190362)
18. Ehrenberg, M. & Kurland, C. G. 1984 Costs of accuracy determined by a maximal growth rate constraint. Quart. Rev. Biophys. 17, 45-82. (doi:10.1017/S0033583500005254)
19. Eyre-Walker, A. & Bulmer, M. 1993 Reduced synonymous substitution rate at the start of enterobacterial genes. Nucleic Acids Res. 21, 4599-4603. (doi:10.1093/nar/21. 19, 4599)
20. Eyre-Walker, A. & Bulmer, M. 1995 Synonymous substitution rates in Enterobacteria. Genetics 140, 1407-1412.
21. Felsenstein, J. 1985 Phytogenies and the comparative method. Am. Nat. 125, 1-15. (doi: 10.1086/284325)
22. Fijalkowska, I. J., Jonczyk, P., Tkaczyk, M. M., Bialoskorska, M. & Schaaper, R. M. 1998 Unequal fidelity of leading strand and lagging strand DNA replication on the Escherichia coli chromosome. Proc. Natl Acad. Sci. USA 95, 10020-10025. (doi: 10.1073/pnas.95.17.10020) (Pubitemid 28415287)
23. Francino, M. P., Chao, L., Riley, M. A. & Ochman, H. 1996 Asymmetries generated by transcription-coupled repair in Enterobacterial genes. Science 111, 107-109. (doi:10.1126/science.272.5258.107) (Pubitemid 26110761)
24. Galtier, N. & Lobry, J. R. 1997 Relationships between genomic G + C content, RNA secondary structures, and optimal growth temperatures in prokaryotes. J. Mol. Evol. 44, 632-636. (doi:10.1007/PL00006186) (Pubitemid 27240856)
25. Gouy, M. & Gautier, C. 1982 Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res. 10, 7055-7074. (doi:10.1093/nar/10.22. 7055)
26. Grantham, R., Gautier, C., Gouy, M., Mercier, R. & Pave, A. 1980 Codon catalog usage and the genome hypothesis. Nucleic Acids Res. 8, r49-r62. (Pubitemid 10154683)
27. Henry, I. & Sharp, P. M. 2007 Predicting gene expression level from codon usage bias. Mol. Biol. Evol. 14, 10-12. (doi: 10.1093/molbev/ms1148)
28. Herbeck, J. T., Degnan, P. H. & Wernegreen, J. J. 2005 -Nonhomogeneous model of sequence evolution indicates independent origins of primary endosymbionts within the Enterobacteriales (gamma-Proetobacteria). Mol. Biol. Evol. 11, 520-532. (doi:10.1093/molbev/msi036)
29. Hill, W. G. & Robertson, A. 1966 The effect of linkage in limits to artificial selection. Genet. Res. 8, 269-294. (doi:10.1017/S0016672300010156)
30. Ikemura, T. 1985 Codon usage and tRNA content in unicellular and multicellular organisms. Mol. Biol. Evol. 2, 13-34. (Pubitemid 15152046)
31. Ishihama, Y., Schmidt, T., Rappsilber, J., Mann, M., Hartl, F. U., Kerner, M. J. & Frishman, D. 2008 Protein abundance profiling of the Escherichia coli cytosol. BMC Genom. 9, 102. (doi:10.1186/1471-2164-9-102) (Pubitemid 351517450)
32. Kaiser, V. B. & Charlesworth, B. 2009 The effects of deleterious mutations on evolution in non-recombining genomes. Trends Genet. 25, 9-12. (doi:10.1016/j.tig. 2008.10.009)
33. Kanaya, S., Yamada, Y., Kudo, Y. & Ikemura, T. 1999 Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene 238, 143-155. (doi:10.1016/S0378- 1119(99)00225-5) (Pubitemid 29436104)
34. Kloster, M. & Tang, C. 2008 SCUMBLE: a method for systematic and accurate detection of codon usage bias by maximum likelihood estimation. Nucleic Acids Res. 36, 3819-3827. (doi:10.1093/nar/gkn288) (Pubitemid 351940555)
35. Kudla, G., Murray, A. W, Tollervey, D. & Plotkin, J. B. 2009 Coding-sequence determinants of gene expression in Escherichia coli. Science 324, 255-258. (doi: 10.1126/science. 1170160)
36. Labbe, R. G. & Huang, T. H. 1995 Generation times and modeling of enterotoxin-positive and enterotoxinnegative strains of Clostridium perfringens in laboratory media and ground beef. J. Food Prot. 58, 1303-1306.
37. Lafay, B., Lloyd, A. T., McLean, M. J., Devine, K. M., Sharp, P. M. & Wolfe, K. H. 1999 Proteome composition and codon usage in spirochaetes, species-specific and DNA strand-specific mutational biases. Nucleic Acids Res. 11, 1642-1649. (doi:10.1093/nar/27.7.1642) (Pubitemid 29209540)
38. Lafay, B., Atherton, J. C. & Sharp, P. M. 2000 Absence of translationally selected codon usage bias in Helicobacter pylori. Microbiology 146, 851-860.
39. Lawrence, J. G. & Ochman, H. 1997 Amelioration of bacterial genomes: rates of change and exchange. J. Mol. Evol. 44, 383-397. (doi:10.1007/ PL00006158) (Pubitemid 27161335)
40. Li, H. 1987 Models of nearly neutral mutations with particular implications for the nonrandom usage of synonymous codons. J. Mol. Evol. 24, 337-345. (doi:10.1007/BF02134132)
41. Lobry, J. R. 1996 Asymmetric substitution patterns in the two DNA strands of bacteria. Mol. Biol. Evol. 13, 660-665.
42. Lynch, M. 2007 The origins of genome architecture. MA, USA: Sinauer Associates.
43. Lynn, D. J., Singer, G. A. C. & Hickey, D. A. 2002 Synonymous codon usage is subject to selection in thermophilic bacteria. Nucleic Acids Res. 30, 4272-4277. (doi:10.1093/nar/gkf546)
44. Maside, X., Lee, A. W. & Charlesworth, B. 2004 Selection on codon usage in Drosophila americana. Curr. Biol. 14, 150-154. (doi:10.1016/j.cub.2003. 12.055)
45. Maynard Smith, J. & Smith, N. H. 1996 Site-specific codon bias in bacteria. Genetics 142, 1037-1043.
46. McLean, M., Wolfe, K. H. & Devine, K. M. 1998 Base composition skews, replication orientation, and gene orientation in 12 prokaryote genomes. J. Mol. Evol. 47, 691-696. (doi: 10.1007/PL00006428) (Pubitemid 29008772)
47. McVean, G. A. T. & Charlesworth, B. 1999 A population genetic model for the evolution of synonymous codon usage: patterns and predictions. Genet. Res. 74, 145-158. (doi:10.1017/S0016672399003912) (Pubitemid 29507353)
48. McVean, G. A. T. & Charlesworth, B. 2000 The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics 155, 929-944. (Pubitemid 30397140)
49. Moran, N. A. & Wernegreen, J. J. 2000 Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15, 321-326. (doi:10.1016/S0169-5347(00) 01902-9)
50. Musto, H., Romero, H. & Zavala, A. 2003 Translational selection is operative for synonymous codon usage in Clostridium perfringens and Clostridium acetobutylicum. Microbiology 149, 855-863. (Pubitemid 37352760)
51. Musto, H., Naya, H., Zavala, A., Romero, H., Alvarez-Valin, F. & Bernardi, G. 2004 Correlations between genomic GC levels and optimal growth temperatures in prokaryotes. FEBS Lett. 573, 73-77. (doi:10.1016/j.febslet. 2004.07.056) (Pubitemid 39141038)
52. Muto, A. & Osawa, S. 1987 The guanine and cytosine content of genomic DNA and bacterial evolution. Proc. Natl Acad Sci. USA 84, 166-169. (doi:10.1073/pnas.84.1.166) (Pubitemid 17013595)
53. Nakabachi, A., Yamashita, A., Toh, H., Ishikawa, H., Dunbar, H. E., Moran, N. A. & Hattori, M. 2006 The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314, 267. (doi:10.1126/science.H34196)
54. Normand, P. et al. 2007 Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res. 17, 7-15. (doi:10.1101/gr.5798407) (Pubitemid 46041660)
55. Pedersen, S., Bloch, P. L., Reeh, S. & Neidhardt, F. C. 1978 Patterns of protein synthesis in E. coli: a catalog of the amount of 140 individual proteins at different growth rates. Cell 14, 179-190. (doi:10.1016/0092-8674(78) 90312-4) (Pubitemid 8340445)
56. Post, L. E. & Nomura, M. 1980 DNA sequences from the str operon of Escherichia coli. J. Biol. Chem. 255, 4660-4666.
57. Rocha, E. P. C. 2004 Codon usage bias from tRNA's point of view: redundancy, specialization, and efficient coding for translation optimization. Genome Res. 14, 2279-2286. (doi:10.1101/gr.2896904)
58. Rooney, A. P., Swezey, J. L., Friedman, R., Hecht, D. W. & Maddox, C. W. 2006 Analysis of core housekeeping and virulence genes reveals cryptic lineages of Clostridium perfringens that are associated with distina disease presentations. Genetics 111, 2081-2092. (doi:10.1534/genetics. 105.054601)
59. Sharp, P. M. 1991 Determinants of DNA sequence divergence between Escherichia coli and Salmonella typhimurium, codon usage, map position and concerted evolution. J. Mol. Evol. 33, 23-33. (doi:10.1007/BF02100192)
60. Sharp, P. M. & Li, W.-H. 1987 The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 15, 1281-1295. (doi:10.1093/nar/15.3.1281)
61. Sharp, P. M., Shields, D. C., Wolfe, K. H. & Li, W.-H. 1989 Chromosomal location and evolutionary rate variation in Enterobacterial genes. Science 246, 808-810.(doi:10.1126/science.2683084)
62. Sharp, P. M., Bailes, E., Grocock, R. J., Peden, J. F. & Sockett, R. E. 2005 Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res. 33, 1141-1153. (doi:10.1093/nar/gki242) (Pubitemid 41439907)
63. Shields, D. C. 1990 Switches in species-specific codon preferences: the influence of mutation biases. J. Mol. Evol. 31, 71-80. (doi:10.1007/BF02109476)
64. Shields, D. C., Sharp, P. M., Higgins, D. G. & Wright, F. 1988 'Silent' sites in Drosophila genes are not neutral: evidence of selection among alternative synonymous codons. Mol. Biol. Evol. 5, 704-716.
65. Sorensen, M. A. & Pedersen, S. 1991 Absolute in vivo translation rates of individual codons in Escherichia coli: the two glutamic acid codons GAA and GAG are translated with a threefold difference in rate. J. Mol. Biol. 222, 265-280. (doi:10.1016/0022-2836(91)90211-N) (Pubitemid 121004006)
66. Stoletzki, N. & Eyre-Walker, A. 2006 Synonymous codon usage in Escherichia coli: selection for translational accuracy. Mol. Biol. Evol. 24, 374-381. (doi:10.1093/molbev/msll66) (Pubitemid 46204370)
67. Suerbaum, S., Maynard Smith, J., Bapumia, K., Morelli, G., Smith, N. H., Kunstmann, E., Dyrek, I. & Achtman, M. 1998 Free recombination within Helicobacter pylori. Proc. Natl Acad. Sci. USA 95, 12619-12624. (doi:10.1073/pnas.95.21.12619)
68. Sueoka, N. 1962 On the genetic basis of variation and heterogeneity of DNA base composition. Proc. Natl Acad. Sci. USA 48, 582-592.
69. Tillier, E. R. M. & Collins, R. A. 2000 The contributions of replication orientation, gene direction, and signal sequences to base-composition asymmetries in bacterial genomes. J. Mol. Evol. 50, 249-257.
70. Wernegreen, J. J. & Funk, D. J. 2004 Mutation exposed: a neutral explanation for extreme base composition of an endosymbiont genome. J. Mol. Evol. 59, 849-858. (doi:10.1007/s00239-003-0192-z)
71. Zeng, K. & Charlesworth, B. 2009 Estimating selection intensity on synonymous codon usage in a non-equilibrium population. Genetics 183, 651-662. (doi: 10.1534/genetics.109.101782)