A strong effect of AT mutational bias on amino acid usage in Buchnera is mitigated at high-expression genes

Molecular Biology and Evolution

Volumn 19, Issue 9, 2002, Pages 1575-1584

  Palacios, Carmen ^a   Wernegreen, Jennifer J ^a  

^a MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

Amino acid usage; Endosymbiosis; Escherichia coli; Gene expression; Multivariate analysis; Mutational bias; Selection

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BUCHNERA; CODON; ESCHERICHIA COLI; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; GENETIC DRIFT; GENOME; HYDROPHOBICITY; MOLECULAR EVOLUTION; MULTIVARIATE ANALYSIS; MUTATIONAL ANALYSIS; NONHUMAN; SEQUENCE ANALYSIS; CHEMISTRY; DNA BASE COMPOSITION; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; POINT MUTATION;

BACTERIA (MICROORGANISMS); BUCHNERA; ESCHERICHIA COLI; NEGIBACTERIA; PROKARYOTA;

ADENINE; AMINO ACID; BACTERIAL PROTEIN; THYMINE;

ADENINE; AMINO ACIDS; BACTERIAL PROTEINS; BASE COMPOSITION; BASE SEQUENCE; BUCHNERA; CODON; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HYDROPHOBICITY; MULTIVARIATE ANALYSIS; POINT MUTATION; THYMINE; VARIATION (GENETICS);

EID: 0036730186     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.molbev.a004219     Document Type: Article

References (61)

1. AKASHI, H., and A. EYRE-WALKER. 1998. Translational selection and molecular evolution. Curr. Opin. Genet. Dev. 8:688-693.
2. AKASHI, H., and T. GOJOBORI. 2002. Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc. Natl. Acad. Sci. USA 99:3695-3700.
3. AKSOY, S. 1995. Molecular analysis of the endosymbionts of tsetse fiies: 16S rDNA locus and over-expression of a chaperonin. Insect Mol. Biol. 4:23-29.
4. ANDERSSON, S. G. E., and C. G. KURLAND. 1998. Reductive evolution of resident genomes. Trends Microbiol. 6:263-268.
5. ANDERSSON, S. G. E., and P. M. SHARP. 1996. Codon usage and base composition in Rickettsia prowazekii. J. Mol. Evol. 42:525-536.
6. BAUMANN, P., L. BAUMANN, M. A. CLARK, and M. L. THAO. 1998. Genetic properties and adaptations of Buchnera aphidicola to an endosymbiotic association with aphids. ASM News 64:203-208.
7. BELETSKII, A., and A. S. BHAGWAT. 1996. Transcription-induced mutations: increase in C to T mutations in the nontranscribed strand during transcription in Escherichia coli. Proc. Natl. Acad. Sci. USA 93:13919-13924.
8. BENNETZEN, J. L., and B. D. HALL. 1982. Codon selection in yeast. J. Biol. Chem. 257:3026-3031.
9. BLATTNER, E R., G. PLUNKETT, III, C. A. BLOCH et al. (17 coauthors). 1997. The complete genome sequence of Escherichia coli K-12. Science. 277:1453-1474.
10. BRACHO, A. M., D. MARTINEZ-TORRES, A. MOYA, and A. LATORRE. 1995. Discovery and molecular characterization of a plasmid localized in Buchnera sp. bacterial endosymbiont of the aphid Rhopalosiphum padi. J. Mol. Evol. 41:67-73.
11. BREWER, B. 1988. When polymerases collide: replication and the transcriptional organization of the E. coli chromosome. Cell 53:679-686.
12. BRYNNEL, E. U., C. G. KURLAND, N. A. MORAN, and S. G. E. ANDERSSON. 1998. Evolutionary rates for tuf genes in endosymbionts of aphids. Mol. Biol. Evol. 15:574-582.
13. BUCHNER, P. 1965. Endosymbiosis of animals with plant microorganisms. Interscience-Wiley, New York.
14. CLARK, M. A., L. BAUMANN, and P. BAUMANN. 1998. Sequence analysis of a 34.7-kb DNA segment from the genome of Buchnera aphidicola (endosymbiont of aphids) containing groEL, dnaA, the atp operon, gidA, and rho. Curr. Microbiol. 36:158-163.
15. CLARK, M. A., N. A. MORAN, and E BAUMANN. 1999. Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol. Biol. Evol. 16:1586-1598.
16. CRAIG, C. L., and R. S. WEBER. 1998. Selection costs of amino acid substitutions in ColE1 and Colla gene clusters harbored by Escherichia coli. Mol. Biol. Evol. 15:774-776.
17. DE MIRANDA, A. B., E. ALVAREZ-VALIN, K. JABBARI, W. M. DEGRAVE, and G. BERNARDI. 2000. Gene expression, amino acid conservation, and hydrophobicity are the main factors shaping codon preferences in Mycobacterium tuberculosis and Mycobacterium leprae. J. Mol. Evol. 50:45-55.
18. DONG, H., L. NILSSON, and C. G. KURLAND. 1996. Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. J. Mol. Biol. 260:649-663.
19. DOUGLAS, A. E. 1995. The ecology of symbiotic micro-organisms. Adv. Ecol. Res. 26:69-103.
20. DOUGLAS, A. E., and W. A. PROSSER. 1992. Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. J. Insect Physiol. 38:565-568.
21. FRANCINO, M. P., and H. OCHMAN. 1999. A comparative genomics approach to DNA asymmetry. Ann. N. Y. Acad. Sci. 870:428-431.
22. FUNK, D. J., L. HELBLING, J. J. WERNEGREEN, and N. A. MORAN. 2000. Intraspecific phylogenetic congruence among multiple symbiont genomes. Proc. R. Soc. Lond. B 267:2517-2521.
23. GREENACRE, M. J. 1984. Theory and applications of correspondence analysis. Academic Press, London.
24. GUTIERREZ, G., L. MARQUEZ, and A. MARIN. 1996. Preference for guanosine at first codon position in highly expressed Escherichia coli genes. A relationship with translational efficiency. Nucleic Acids Res. 24:2525-2527.
25. 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.
26. ISHIKAWA, H. 1984. Characterization of the protein species synthesized in vivo and in vitro by an aphid endosymbiont. Insect Biochem. 14:417-425.
27. KARLIN, S., A. M. CAMPBELL, and J. MRAZEK. 1998. Comparative DNA analysis across diverse genomes. Annu. Rev. Genet. 32:185-225.
28. KYTE, J., and R. E. DOOLITTLE. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
29. LAFAY, B., A. T. LLOYD, M. J. MCLEAN, K. M. DEWNE, P. M. SHARP, and K. H. WOLFE. 1999. Proteome composition and codon usage in spirochaetes: species-specific and DNA strand-specific mutational biases. Nucleic Acids Res. 27:1642-1649.
30. LOBRY, J. R. 1996. Origin of replication of Mycoplasma genitalium. Science. 272:745-746.
31. LOBRY, J. R., and C. GAUTIER. 1994. Hydrophobicity, expressivity and aromaticity ate the major trends of amino-acid usage in 999 Escherichia coli chromosome-encoded genes. Nucleic Acids Res. 22:3174-3180.
32. MACKIEWICZ, P., A. GIERLIK, M. KOWALCZUK, M. DUDEK, and S. CEBRAT. 1999. How does replication-associated mutational pressure influence amino acid composition of proteins? Genome Res. 9:409-416.
33. MCINERNEY, J. O. 1997. Prokaryotic genome evolution as assessed by multivariate analysis of codon usage patterns. Microb. Comparat. Genomics 2:89-97.
34. -. 1998. Replication and transcriptional selection on codon usage in Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA 95:10698-10703
35. MCLEAN, D. L., and E. J. HOUK. 1973. Phase contrast and electron microscopy of the mycetocytes and symbiontes of the pea aphid Acyrtosiphon pisum. J. Insect Physiol. 19:625-633.
36. MIRA, A., H. OCHMAN, and N. A. MORAN. 2001. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17:589-596.
37. MORAN, N. 1996. Accelerated evolution and Muller's ratchet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93:2873-2878.
38. MORAN, N., and P. BAUMANN. 1994. Phylogenetics of cytoplasmically inherited microorganisms of arthropods. Trends Ecol. Evol. 9:15-20.
39. MORAN, N. A., M. A. MUNSON, P. BAUMANN, and H. ISHIKAWA. 1993. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc. R. Soc. Lond. B. 253:167-171.
40. MULLER, J. 1964. The relation of recombination to mutational advance. Mutat. Res. 1:2-9.
41. MUNSON, M. A., E BAUMANN, M. A. CLARK, L. BAUMANN, N. A. MORAN, D. J. VOEGTLIN, and B. C. CAMPBELL. 1991. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J. Bacteriol. 173:6321-6324.
42. OHTA, T 1973. Slightly deleterious mutant substitutions in evolution. Nature. 246:96-98.
43. OHTAKA, C., and H. ISHIKAWA. 1993. Accumulation of adenine and thymine in a groE-homologous operon of an intracellular symbiont. J. Mol. Evol. 36:121-126.
44. RISPE, C., and N. A. MORAN. 2000. Accumulation of deleterious mutations in endosymbionts: Muller's ratchet with two levels of selection. Am. Nat. 156:425-441.
45. ROCHA, E., A. DANCHIN, and A. VIARI. 1999. Universal replication biases in bacteria. Mol. Microbiol. 32:11.
46. ROMERO, H., A. ZAVAKA, and H. MUSTO. 2000. Codon usage in Chlamydia trachomatis is the result of strand-specific mutational biases and a complex pattern of selective forces. Nucleic. Acids. Res. 28:2084-2090.
47. SATO, S., and H. ISHIKAWA. 1997. Expression and control of an operon from an intracellular symbiont which is homologous to the groE operon. J. Bacteriol. 179:2300-2304.
48. SELANDER, R. K., D. A. CAUGANT, and T. S. WHITTAM. 1987. Genetic structure and variation in natural populations of Escherichia coli. Pp. 1625-1648 in E C. NUIDHARDT, J. L. INGRAHAM, K. B. LOW, G. MAGASANIK, M. SCHAECHTER, and H. E. UMBARGER, eds. Escherichia coli and Salmonella o'phimurium: cellular and molecular Biology. American Society of Microbiology, Washington, D.C.
49. SELOSSE, M., B. ALBERT, and B. GODELLE. 2001. Reducing the genome size of organelles favours gene transfer to the nucleus. Trends Ecol. Evol. 16:135-141.
50. SHARP, P. M., and W. H. LI. 1987. The codon Adaptation Index - a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 15:1281-1295.
51. SHIGENOBU, S., H. WATANABE, M. HATTORI, Y. SAKAKI, and H. ISHIKAWA. 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera APS. Nature. 407:81-86.
52. SHIGENOBU, S., H. WATANABE, Y. SAKAKI, and H. ISHIKAWA. 2001. Accumulation of species-specific amino acid replacements that cause loss of particular functions in Buchnera, an endocellular bacterial symbiont. J. Mol. Evol. 53:377-386.
53. SILVA, E. J., A. LATORRE, and A. MOYA. 2001. Genome size reduction through multiple events of gene disintegration in Buchnera APS. Trends Genet. 17:615-618.
54. SINGER, G. A. C., and D. A. HICKEY. 2000. Nucleotide bias causes a genomewide bias in the amino acid composition of proteins. Mol. Biol. Evol. 17:1581-1588.
55. SOKAL, R. R., and E J. ROHLF. 1995. Biometry. W.H. Freeman and Co., New York.
56. SRIVASTAVA, A. K., and D. SCHLESSINGER. 1990. Mechanism and regulation of bacterial ribosomal RNA processing. Annu. Rev. Microbiol. 44:105-129.
57. UNTERMAN, B. M., P. BAUMANN, and D. L. MCLEAN. 1989. Pea aphid symbiont relationships established by analysis of 16S rRNAs. J. Bacteriol. 171:2970-2974.
58. WERNEGREEN, J. J., and N. A. MORAN. 1999. Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes. Mol. Biol. Evol. 16:83-97.
59. -. 2001. Vertical transmission of biosynthetic plasmids in aphid endosymbionts (Buchnera). J. Bacteriol. 183(2):785-790.
60. YAMAO, F, Y. ANDACHI, A. MUTO, T. IKEMURA, and S. OSAWA. 1991. Levels of tRNAs in bacterial cells as affected by amino acid usage in proteins. Nucleic Acids Res. 19:6119-6122.
61. YOSHIKAWA, H., and N. OGASAWARA. 1991. Structure and function of DnaA and the DnaA-box in eubacteria: evolutionary relationships of bacterial replication origins. Mol. Microbiol. 5:2589-2597.