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Determinants of DNA sequence divergence betweenEscherichia coli andSalmonella typhimurium: Codon usage, map position, and concerted evolution

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Summary

The nature and extent of DNA sequence divergence between homologous proteincoding genes fromEscherichia coli andSalmonella typhimurium have been examined. The degree of divergence varies greatly among genes at both synonymous (silent) and nonsynonymous sites. Much of the variation in silent substitution rates can be explained by natural selection on synonymous codon usage, varying in intensity with gene expression level. Silent substitution rates also vary significantly with chromosomal location, with genes nearoriC having lower divergence. Certain genes have been examined in more detail. In particular, the duplicate genes encoding elongation factor Tu,tufA andtufB, fromS. typhimurium have been compared to theirE. coli homologues. As expected these very highly expressed genes have high codon usage bias and have diverged very little between the two species. Interestingly, these genes, which are widely spaced on the bacterial chromosome, also appear to be undergoing concerted evolution, i.e., there has been exchange between the loci subsequent to the divergence of the two species.

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References

  • An G, Friesen JD (1980) The nucleotide sequence oftufB and four nearby tRNA structural genes ofE. coli. Gene 12:33–39

    Article  PubMed  Google Scholar 

  • Andersson SGE, Kurland CG (1990) Codon preferences in free-living microorganisms. Microbiol Rev 54:198–210

    Google Scholar 

  • Bachmann B (1990) Linkage map ofEscherichia coli K-12, ed 8. Microbiol Rev 54: 130–197

    Google Scholar 

  • Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J, Cuny G Meunier-Rotival M, Rodier F (1985) The mosaic genome of warm-blooded vertebrates. Science 228:953–958

    PubMed  Google Scholar 

  • Bulmer M (1988) Are codon usage patterns in unicellular organisms determined by selection-mutation balance. J Evol Biol 1:15–26

    Article  Google Scholar 

  • Bulmer M, Wolfe KH, Sharp PM (1991) Synonymous nucleotide substitution rates in mammalian genes: implications for the molecular clock and the relationships of mammalian orders. Proc Natl Acad Sci USA (in press)

  • DuBose RF, Dykhuizen DE, Hartl DL (1988) Genetic exchange among natural isolates of bacteria: recombination within thephoA gene ofEscherichia coli. Proc Natl Acad Sci USA 85:7036–7040

    PubMed  Google Scholar 

  • Fitch WM (1977) On the problem of discovering the most parsimonious tree. Am Nat 111:223–257

    Article  Google Scholar 

  • Gouy M, Gautier C (1982) Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res 10:7055–7074

    PubMed  Google Scholar 

  • Gouy M, Gautier C, Attimonelli M, Lanave C, di Paola G (1985) ACNUC—a protable retrieval system for nucleic acid sequence databases: logical and physical designs and usage. CABIOS 1:167–172

    PubMed  Google Scholar 

  • Grantham R, Gautier C, Gouy M, Mercier R, Pave A (1980) Codon catalog usage and the genome hypothesis. Nucleic Acids Res 8:r49-r62

    PubMed  Google Scholar 

  • Holck A, Kleppe K (1988) Cloning and sequencing of the gene for the DNA-binding 17 K protein fromEscherichia coli. Gene 67:117–124

    Article  PubMed  Google Scholar 

  • Hulton CSJ, Seirafi A, Hinton JCD, Sidebotham JM, Waddell L, Pavitt GD, Owen-Hughes T, Spassky A, Buc H, Higgins CF (1990) Histone-like protein H1 (H-NS), DNA supercoiling and gene expression in bacteria. Cell 63:631–642

    PubMed  Google Scholar 

  • Hulton CSJ, Higgins CF, Sharp PM (1991) ERIC sequences: a novel family of repetitive elements in the genomes ofEscherichia coli, Salmonella typhimurium and other enterobacteria. Mol Microbiol 5:825–834

    PubMed  Google Scholar 

  • Ikemura T (1981) Correlation between the abundance ofEscherichia 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 theE. coli translational system. J Mol Biol 151:389–409

    Article  PubMed  Google Scholar 

  • Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34

    PubMed  Google Scholar 

  • Ikemura T, Aota S-i (1988) Global variation in G+C content along vertebrate genome DNA. J Mol Biol 203:1–13

    Article  PubMed  Google Scholar 

  • Iwabe N, Kuma K-i, Hasegawa M, Osawa S, Miyata T (1989) Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci USA 86:9355–9359

    PubMed  Google Scholar 

  • Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275–276

    Article  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge, England

    Google Scholar 

  • Kimura M (1986) DNA and the neutral theory. Phil Trans R Soc Lond B 312:343–354

    Google Scholar 

  • Koski P, Rhen M, Kantele J, Vaara M (1989) Isolation, cloning and primary structure of a cationic 16-kDa outer membrane protein ofSalmonella typhimurium. J Biol Chem 264:18973–18980

    PubMed  Google Scholar 

  • Kröger M, Wahl R, Rice P (1990) Compilation of DNA sequences ofEscherichia coli (update 1990). Nucleic Acids Res 18:2549–2587

    PubMed  Google Scholar 

  • Li W-H, Wu C-I, Luo C-C (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2:150–174

    PubMed  Google Scholar 

  • Li W-H, Gouy M, Sharp PM, OhUigin C, Yang Y-W (1990) Molecular phylogeny of Rodentia, Lagomorpha, Primates, Artiodactyla, and Carnivora and molecular clocks. Proc Natl Acad Sci USA 87:6703–6707

    PubMed  Google Scholar 

  • Lipman DJ, Wilbur WJ (1985) Interaction of silent and replacement changes in eucaryotic coding sequences. J Mol Evol 21:161–167

    Google Scholar 

  • Milkman R, Crawford IP (1983) Clustered third-base substitutions among wild strains ofEscherichia coli. Science 221: 378–380

    PubMed  Google Scholar 

  • Mouchiroud D, Gautier C (1990) Codon usage changes and sequence dissimilarity between human and rat. J Mol Evol 31:81–91

    PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nichols BP, Yanofsky C (1979) Nucleotide sequences oftrpA ofSalmonella typhimurium andEscherichia coli: an evolutionary comparison. Proc Natl Acad Sci USA 76:5244–5248

    PubMed  Google Scholar 

  • Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26:74–86

    PubMed  Google Scholar 

  • Ohta T (1987) Very slightly deleterious mutations and the molecular clock. J Mol Evol 26:1–6

    Google Scholar 

  • Post LE, Strycharz GD, Nomura M, Lewis H, Dennis PP (1979) Nucleotide sequence of the ribosomal protein gene cluster adjacent to the gene for RNA polymerase subunit beta inEscherichia coli. Proc Natl Acad Sci USA 76:1697–1701

    PubMed  Google Scholar 

  • Rayssiguier C, Thaler DS, Radman M (1989) The barrier to recombination betweenEscherichia coli andSalmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342:396–401

    Article  PubMed  Google Scholar 

  • Reeves P, Stevenson G (1989) Cloning and nucleotide sequence of theSalmonella typhimurium LT2gnd gene and its homology with the corresponding sequence ofEscherichia coli K12. Mol Gen Genet 217:182–184

    Article  PubMed  Google Scholar 

  • Riley M, Krawiec S (1987) Genome organization. In: Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds)Escherichia coli andSalmonella typhimurium. American Society for Microbiology, Washington DC, pp 967–981

    Google Scholar 

  • Sanderson KE, Roth JR (1988) Linkage map ofSalmonella typhimurium, ed VII. Microbiol Rev 52:485–532

  • Sawyer SA, Dykhuizen DE, Hartl DL (1987) Confidence interval for the number of selectively neutral amino acid polymorphisms. Proc Natl Acad Sci USA 84:6225–6228

    PubMed  Google Scholar 

  • Schmid MB, Roth JR (1987) Gene location affects expression level inSalmonella typhimurium. J Bacteriol 169:2872–2875

    PubMed  Google Scholar 

  • Sharp PM (1989) Evolution at ‘silent’ sites in DNA. In: Hill WG, Mackay TFC (eds) Evolution and animal breeding; reviews on molecular and quantitative approaches in honour of Alan Robertson. C.A.B. International, Wallingford, UK, pp 24–32

    Google Scholar 

  • Sharp PM (1990) Processes of genome evolution reflected by base composition differences amongSerratia marcescens genes. Mol Microbiol 4:119–122

    PubMed  Google Scholar 

  • Sharp PM, Li W-H (1986a) Codon usage in regulatory genes inEscherichia coli does not reflect selection for “rare” codons. Nucleic Acids Res 14:7737–7749

    PubMed  Google Scholar 

  • Sharp PM, Li W-H (1986b) An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24:28–38

    PubMed  Google Scholar 

  • Sharp PM, Li W-H (1987a) The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295

    PubMed  Google Scholar 

  • Sharp PM, Li W-H (1987b) The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol Biol Evol 4:222–230

    PubMed  Google Scholar 

  • Sharp PM, Li W-H (1989) On the rate of DNA sequence evolution inDrosophila. J Mol Evol 28:398–402

    PubMed  Google Scholar 

  • Sharp PM, Cowe E, Higgins DG, Shields DC, Wolfe KH, Wright F (1988) Codon usage inEscherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster andHomo sapiens; a review of the considerable within-species diversity. Nucleic Acids Res 16:8207–8211

    PubMed  Google Scholar 

  • Sharp PM, Shields DC, Wolfe KH, Li W-H (1989) Chromosomal location and evolutionary rate variation in enterobacterial genes. Science 246:808–810

    PubMed  Google Scholar 

  • Smith CM, Koch WH, Franklin SB, Foster PL, Cebula TA, Eisenstadt E (1990) Sequence analysis and mapping of theSalmonella typhimurium LT2umuDC operon. J Bacteriol 172:4964–4978

    PubMed  Google Scholar 

  • Thomas SM, Crowne HM, Pidsley SC, Sedgwick SG (1990) Structural characterization of theSalmonella typhimurium LT2umu operon. J Bacteriol 172:4979–4987

    PubMed  Google Scholar 

  • Tuohy TMF, Thompson S, Gesteland RF, Hughes D, Atkins JF (1990) The role of EF-Tu and other translation components in determining translocation step size. Biochim Biophys Acta 1050:274–278

    PubMed  Google Scholar 

  • Wolfe KH, Sharp PM, Li W-H (1989) Mutation rates differ among regions of the mammalian genome. Nature 337:283–285

    Article  PubMed  Google Scholar 

  • Yokota T, Sugisaka H, Takanami M, Kaziro Y (1980) The nucleotide sequence of the clonedtufA gene ofEscherichia coli. Gene 12:25–31

    Article  PubMed  Google Scholar 

  • Zimmer EA, Martin SL, Beverley SM, Kan YW, Wilson AC (1980) Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. Proc Natl Acad Sci USA 77:2158–2162

    PubMed  Google Scholar 

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Sharp, P.M. Determinants of DNA sequence divergence betweenEscherichia coli andSalmonella typhimurium: Codon usage, map position, and concerted evolution. J Mol Evol 33, 23–33 (1991). https://doi.org/10.1007/BF02100192

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  • DOI: https://doi.org/10.1007/BF02100192

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