Mutation exposed: A neutral explanation for extreme base composition of an endosymbiont genome

Journal of Molecular Evolution

Volumn 59, Issue 6, 2004, Pages 849-858

  Wernegreen, Jennifer J ^a   Funk, Daniel J ^b  

^a MARINE BIOLOGICAL LABORATORY   (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

Base composition; Buchnera; DNA repair; Drift; Mutation; Neutrality; Selection

Indexed keywords

AMINO ACID SUBSTITUTION; APHID; ARTICLE; BUCHNERA APHIDICOLA; CONTROLLED STUDY; DNA BASE COMPOSITION; ENDOSYMBIONT; GENE MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY;

ANIMALS; APHIDS; BASE COMPOSITION; BASE SEQUENCE; BUCHNERA; DATABASES, NUCLEIC ACID; DNA PRIMERS; EVOLUTION, MOLECULAR; GENETICS, POPULATION; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; MUTATION; SELECTION (GENETICS); SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

APHIDIDAE; BACTERIA (MICROORGANISMS); BUCHNERA APHIDICOLA; MAMMALIA; NEGIBACTERIA; PROKARYOTA;

EID: 11944272022     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-003-0192-z     Document Type: Article

References (88)

1. Abbot P, Moran NA (2002) Extremely low levels of genetic polymorphism in endosymbionts (Buchnera) of aphids (Pemphigus). Mol Ecol 11:2649-2660
2. Akashi H (1995) Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. Genetics 139:1067-1076
3. Akashi H (1996) Molecular evolution between Drosophila melanogaster and D simulans: Reduced codon bias faster rates of amino acid substitution and larger proteins in D melanogaster. Genetics 144:1297-1307
4. Akashi H (1999a) Inferring the fitness effects of DNA mutations from polymorphism and divergence data: Statistical power to detect directional selection under stationarity and free recombination. Genetics 151:221-238
5. Akashi H (1999b) Within- and between-species DNA sequence variation and the 'footprint' of natural selection. Gene 238:39-51
6. Akashi H, Schaeffer SW (1997) Natural selection and the frequency distributions of "silent" DNA polymorphism in Drosophila. Genetics 146:295-307
7. Akashi H, Kliman M, Eyre-Walker A (1998) Mutation pressure natural selection and the evolution of base composition in Drosophila. Genetica 102-103:49-60
8. Andersson SG, Kurland CG (1998) Reductive evolution of resident genomes. Trends Microbiol 6:263-268
9. Argos P, Rossman MG, Grau UM, Zuber H, Frand G, Tratschin JD (1979) Thermal stability and protein structure. Biochemistry 18:5698-5703
10. Ballard JW, Kreitman M (1994) Unraveling selection in the mitochondrial genome of Drosophila. Genetics 138:757-772
11. Baumann P, Baumann L, Lai CY et al. (1995) Genetics physiology and evolutionary relationships of the genus Buchnera: Intracellular symbionts of aphids. Annu Rev Microbiol 49:55-94
12. Bulmer M (1991) The selection-mutation-drift theory of synonymous codon usage. Genetics 129:897-907
13. Clark MA, Moran NA, Baumann P (1999) Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol Biol Evol 16:1586-1598
14. Clark MA, Moran NA, Baumann P, Wernegreen JJ (2000) Co-speciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54:517-525
15. Cohan FM (2002) What are bacterial species?. Annu Rev Microbiol 56:457-487
16. Collins T, Wimberger P, Naylor G (1994) Compositional bias character state bias and character state reconstruction using parsimony. Syst Biol 43:482-496
17. Comeron JM, Kreitman M (2000) The correlation between intron length and recombination in Drosophila: Dynamic equilibrium between mutational and selective forces. Genetics 156:1175-1190
18. Eisen JA, Hanawalt PC (1999) A phylogenomic study of DNA repair genes proteins and processes. Mutat Res 435:171-213
19. Ellegren H, Smith NG, Webster MT (2003) Mutation rate variation in the mammalian genome. Curr Opin Genet Dev 13:562-568
20. Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186-194
21. Eyre-Walker A (1994) DNA mismatch repair and synonymous codon evolution in mammals. Mol Biol Evol 11:88-98
22. Eyre-Walker A (1997) Differentiating between selection and mutation bias. Genetics 147:1983-1987
23. Eyre-Walker A (1998) Problems with parsimony in sequences of biased base composition. J Mol Evol 47:686-690
24. Eyre-Walker A (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
25. Francino MP, Ochman H (2001) Deamination as the basis of strand-asymmetric evolution in transcribed Escherichia coli sequences. Mol Biol Evol 18:1147-1150
26. Francino MP, Chao L, Riley MA, Ochman H (1996) Asymmetries generated by transcription-coupled repair in enterobacterial genes. Science 272:107-109
27. Fromme JC, Verdine GL (2003) DNA lesion recognition by the bacterial repair enzyme MutM. J Biol Chem 218:51543-51548
28. Funk DJ, Helbling L, Wernegreen JJ, Moran NA (2000) Intraspecific phylogenetic congruence among multiple symbiont. Proc R Soc Lond B Biol Sci 267:2517-2521
29. Funk DJ, Wernegreen JJ, Moran NA (2001) Intraspecific variation in symbiont genomes: Bottlenecks and the aphid-Buchnera association. Genetics 157:477-489
30. Gautier C (2000) Compositional bias in DNA. Curr Opin Genet Dev 10:656-661
31. Galtier N, Boursot P (2000) A new method for locating changes in a tree reveals distinct nucleotide polymorphism vs divergence patterns in mouse mitochondrial control region. J Mol Evol 50:224-231
32. Galtier N, Lobry JR (1997) Relationships between genomic G + C content RNA secondary structures and optimal growth temperature in prokaryotes. J Mol Evol 44:632-636
33. Gil R, Sabater-Munoz B, Latorre A, Silva FJ, Moya A (2002) Extreme genome reduction in Buchnera spp: Toward the minimal genome needed for symbiotic life. Proc Natl Acad Sci USA 99:4454-4458
34. Gordon D, Abajian C, Green P (1998) Consed: A graphical tool for sequence finishing. Genome Res 8:195-202
35. Gouy M, Gautier C (1982) Codon usage in bacteria: Correlation with gene expressivity. Nucleic Acids Res 10:7055-7074
36. Hartl DL, Moriyama EN, Sawyer SA (1994) Selection intensity for codon bias. Genetics 138:227-234
37. Haywood-Farmer E, Otto SP (2003) The evolution of genomic base composition in bacteria. Evolution 57:1783-1792
38. Herbeck JT, Funk DJ, Degnan PH, Wernegreen JJ (2003) A conservative test of genetic drift in the endosymbiotic bacterium Buchnera: Slightly deleterious mutations in the chaperonin groEL. Genetics 165:1651-1660
39. Hey J, Wakeley J (1997) A coalescent estimator of the population recombination rate. Genetics 145:833-846
40. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755
41. Ikemura T (1981) Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: A proposal for a synonymous codon choice that is optimal for the E. coli translational system. J Mol Biol 151:389-409
42. Ishikawa H (1989) Biochemical and molecular aspects of endosymbiosis in insects. Int Rev Cytol 116:1-45
43. 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
44. Karlin S, Mrazek J, Campbell AM (1998) Codon usages in different gene classes of the Escherichia coli genome. Mol Microbiol 29:1341-1355
45. Kimura M (1968) Evolutionary rate at the molecular level. Nature 217:624-626
46. Kimura M (1983) The Neutral Theory of Molecular Evolution. Cambridge University Press, Cambridge
47. Kliman RM, Hey J (1993) Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol Biol Evol 10:1239-1258
48. Lambert JD, Moran NA (1998) Deleterious mutations destabilize ribosomal RNA in endosymbiotic bacteria. Proc Natl Acad Sci USA 95:4458-4462
49. Marais G, Mouchiroud D, Duret L (2001) Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci USA 98:5688-5692
50. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654
51. Miller JH (1996) Spontaneous mutators in bacteria: Insights into pathways of mutagenesis and repair. Annu Rev Microbiol 50:625-643
52. Mira A, Moran NA (2002) Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb Ecol 44:137-143
53. Moran NA (1996) Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci USA 93:2873-2878
54. Moran NA (2002) Microbial minimalism: Genome reduction in bacterial pathogens. Cell 108:583-586
55. Moran NA, Wernegreen JJ (2000) Lifestyle evolution in symbiotic bacteria: insights from genomics. Tr Ecol Evol 15:321-326
56. Moran NA, Munson MA, Baumann P, Ishikawa H (1993) A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc Roy Soc Lond B 253:167-171
57. Moran NA, Kaplan M, Gelsey M, Murphy T, Scholes E (1999) Phylogenetics and evolution of the aphid genus Uroleucon based on mitochondrial and nuclear DNA sequences. Syst Entomol 24:85-93
58. Moya A, Latorre A, Sabater-Munoz B, Silva FJ (2002) Comparative molecular evolution of primary (Buchnera) and secondary symbionts of aphids based on two protein-coding genes. J Mol Evol 55(2):127-137
59. Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84:166-169
60. Naya H, Romero H, Zavala A, Alvarez B, Musto H (2002) Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. J Mol Evol 55:260-264
61. Ochman H, Elwyn S, Moran NA (1999) Calibrating bacterial evolution. Proc Natl Acad Sci USA 96:12638-12643
62. Ohta T (1973) Slightly deleterious mutant substitutions in evolution. Nature 246:96-98
63. Ohta T (1992) The nearly neutral theory of molecular evolution. Annu Rev Evol Syst 23:263-286
64. Pan A, Dutta C, Das J (1998) Codon usage in highly expressed genes of Haemophilus influenzae and Mycobacterium tuberculosis: Translational selection versus mutational bias. Gene 215:405-413
65. Powell JR, Moriyama EN (1997) Evolution of codon usage bias in Drosophila. Proc Natl Acad Sci USA 94:7784-7790
66. Rispe C, Delmotte F, van Ham RCHJ, Moya A (2004) Mutational and selective pressures on codon and amino acid usage in Buchnera the endosymbiotic bacteria of aphids. Genome Res 14(1):44-53
67. Rocha EP, Danchin A (2002) Base composition bias might result from competition for metabolic resources. Trends Genet 18:291-294
68. Rodriguez-Trelles F, Tarrio R, Ayala AJ (1999) Molecular evolution and phylogeny of the Drosophila saltans species group inferred from the Xdh gene. Mol Phylogenet Evol 13:110-121
69. Rodriguez-Trelles F, Tarrio R, Ayala AJ (2000) Fluctuating mutation bias and the evolution of base composition in Drosophila. J Mol Evol 50:1-10
70. Sawyer SA, Hard DL (1992) Population genetics of polymorphism and divergence. Genetics 132:1161-1176
71. Sharp PM, Matassi G (1994) Codon usage and genome evolution. Curr Opin Genet Dev 4:851-860
72. Sharp PM, Cowe E, Higgins DG et al. (1988) Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster, and Homo sapiens: A review of the considerable within-species diversity. Nucleic Acids Res 16:8207-8211
73. Shields DC, Sharp PM, Higgins SG, Wright F (1988) "Silent" sites in Drosophila genes are not neutral: Evidence of selection among synonymous codons. Mol Biol Evol 5:704-716
74. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp APS. Nature 407:81-86
75. Smith NG, Eyre-Walker A (2002) The compositional evolution of the murid genome. J Mol Evol 55:197-201
76. Smith NG, Webster MT, Ellegren H (2002) Deterministic mutation rate variation in the human genome. Genome Res 12:1350-1356
77. Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85:2653-2657
78. Sueoka N (1993) Directional mutational pressure mutator mutations and dynamics of molecular evolution. J Mol Evol 37:137-153
79. Sueoka N (1999) Translation-coupled violation of Parity Rule 2 in human genes is not the cause of heterogeneity of the DNA G + C content of third codon position. Gene 238:53-58
80. Suoeka N (1961) Correlation between base composition of DNA and amino acid composition of proteins. Proc Natl Acad Sci USA 47:1141-1149
81. Takano-Shimizu T (2001) Local changes in GC/AT substitution biases and in crossover frequencies on Drosophila chromosomes. Mol Biol Evol 18:606-619
82. Tamas I, Klasson L, Canback B et al. (2002) 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376-2379
83. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512-526
84. Wada A, Suyama A (1986) Local stability of DNA and RNA secondary structure and its relation to biological functions. Prog Biophys Mol Biol 47:113-157
85. Wang D, Kreutzer DA, Essigmann JM (1998) Mutagenicity and repair of oxidative DNA damage:insights from studies using defined lesions. Mutat Res 400:99-115
86. Wernegreen JJ, Moran NA (1999) Evidence for genetic drift in endosymbionts (Buchnera): Analyses of protein-coding genes. Mol Biol Evol 16:83-97
87. Wernegreen JJ, Moran NA (2001) Vertical transmission of biosynthetic plasmids in aphid endosymbionts (Buchnera). J Bacteriol 183:785-790
88. Yang Z (1997) PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555-556