Journal of Molecular Evolution

, Volume 33, Issue 3, pp 241–250 | Cite as

Molecular considerations in the evolution of bacterial genes

  • Jeffrey G. Lawrence
  • Daniel L. Hartl
  • Howard Ochman


Synonymous and nonsynonymous substitution rates at the loci encoding glyceraldehyde-3-phosphate dehydrogenase (gap) and outer membrane protein 3A (ompA) were examined in 12 species of enteric bacteria. By examining homologous sequences in species of varying degrees of relatedness and of known phylogenetic relationships, we analyzed the patterns of synonymous and nonsynonymous substitutions within and among these genes. Although both loci accumulate synonymous substitutions at reduced rates due to codon usage bias, portions of thegap andompA reading frames show significant deviation in synonymous substitution rates not attributable to local codon bias. A paucity of synonymous substitutions in portions of theompA gene may reflect selection for a novel mRNA secondary structure. In addition, these studies allow comparisons of homologous protein-coding sequences (gap) in plants, animals, and bacteria, revealing differences in evolutionary constraints on this glycolytic enzyme in these lineages.

Key words

Enteric bacteria Codon usage bias Synonymous substitution Glyceraldehyde-3-phosphate dehydrogenase Outer membrane protein 3A 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bachmann BJ (1990) Linkage map ofEscherichia coli K-12, ed 8. Microbiol Rev 54:130–197PubMedGoogle Scholar
  2. Beale D, Feinstein A (1976) Structure and function of the constant regions of immunoglobins. Quart Rev Biophys 9:135–180Google Scholar
  3. Beck E, Bremer E (1980) Nucleotide sequence of the geneompA coding the outer membrane protein II* ofEscherichia coli K-12. Nucleic Acids Res 8:3011–3024PubMedGoogle Scholar
  4. Biesecker G, Harris JI, Thierry JC, Walker JE, Wonacott AJ (1977) Sequence and structure ofd-glyceraldehyde-3-phosphate dehydrogenase fromBacillus stearothermophilus. Nature 266:328–333CrossRefPubMedGoogle Scholar
  5. Bossi L (1983) Context effects: translation of UAG codon by suppressor tRNA is affected by the sequence following UAG in the message. J Mol Biol 164:73–87CrossRefPubMedGoogle Scholar
  6. Branlant G, Branlant C (1985) Nucleotide sequence of theEscherichia coli gap gene: different evolutionary behavior of the NAD+-binding domain and of the catalytic domain of thed-glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 150:61–66CrossRefPubMedGoogle Scholar
  7. Braun G, Cole ST (1984) DNA sequence analysis of theSerratia marcescens ompA gene: implication for the organisation of an enterobacterial outer membrane protein. Mol Gen Genet 195:321–328CrossRefPubMedGoogle Scholar
  8. Brenner DJ, Falkow S (1971) Molecular relationships among members of the Enterobacteriaceae. Adv Genet 16:81–118PubMedGoogle Scholar
  9. Bulmer M (1988) Codon usage and intragenic position. J Theor Biol 133:67–71PubMedGoogle Scholar
  10. Bychkova VE, Pain RH, Ptitsyn OB (1988) The ‘molten globule’ state is involved in the translocation of proteins across membranes. FEBS Lett 238:231–234CrossRefPubMedGoogle Scholar
  11. Chen R, Schmidmayr W, Kramer C, Chen-Schmeisser U, Henning U (1980) Primary structure of outer membrane protein II (ompA protein) ofEscherichia coli K12. Proc Natl Acad Sci USA 77:4592–4596PubMedGoogle Scholar
  12. Cocks GT, Wilson AC (1972) Enzyme evolution in the Enterobacteriaceae. J Bacteriol 110:793–802PubMedGoogle Scholar
  13. Conway T, Sewell GW, Ingram LO (1987) Glyceraldehyde-3-phosphate dehydrogenase gene fromZymomonas mobilis: cloning, sequencing, and identification of promoter region. J Bacteriol 169:5653–5662PubMedGoogle Scholar
  14. Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395PubMedGoogle Scholar
  15. DuBose RF, Hartl DL (1990) The molecular evolution of alkaline phosphatase: correlating variation among enteric bacteria to experimental manipulations of the protein. Mol Biol Evol 7:547–577PubMedGoogle Scholar
  16. Edelman GM, Cunningham BA, Gall WE, Gottlieb PD, Rutishauser U, Waxdal MJ (1969) The covalent structure of an entire γG immunoglobin molecule. Proc Natl Acad Sci USA 63:78–85PubMedGoogle Scholar
  17. Felsenstein J (1985) Confidence limits, on phylogenies with a molecular clock. Syst Zool 34:152–161Google Scholar
  18. Fitch WM (1976) The molecular evolution of cytochrome c in eukaryotes. J Mol Evol 8:13–40CrossRefPubMedGoogle Scholar
  19. Freudl R, Cole ST (1983) Cloning and molecular characterization of theompA gene fromSalmonella typhimurium. Eur J Biochem 134:497–502CrossRefPubMedGoogle Scholar
  20. Freudl R, Braun G, Hindennach I, Henning U (1985) Lethal mutations in the structural gene of an outer membrane, protein (OmpA) ofEscherichia coli K-12. Mol Gen Genet 201:76–81CrossRefPubMedGoogle Scholar
  21. Freudl R, Schwarz H, Stierhof Y-D, Gamon K, Hindenach I, Henning U (1986) An outer membrane protein (OmpA) ofEscherichia coli K-12 undergoes a conformational change during export. J Biol Chem 261:11355–11361PubMedGoogle Scholar
  22. Gouy M, Gautier C (1982) Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res 10:7055–7074PubMedGoogle Scholar
  23. Green PJ, Pines O, Inouye M (1986) The role of antisense RNA in gene regulation. Annu Rev Biochem 55:569–597CrossRefPubMedGoogle Scholar
  24. Gross G, Mielke C, Hollatz I, Blöcker H, Frank R (1990) RNA primary sequence or secondary structure in the translational initiation region controls expression of two variant interferon-β genes fromEscherichia coli. J Biol Chem 265:17627–17636PubMedGoogle Scholar
  25. Huck S, Lefrane G, Lefrane M-P (1989) A human immunoglobinIGHG3 allele (Gmbo, b1, c3, c5, u) with anIGHG4 converted region and three hinge exons. Immunogenetics 30:250–257PubMedGoogle Scholar
  26. Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–33PubMedGoogle Scholar
  27. Kaplan JB, Nichols BP (1983) Nucleotide sequence ofEscherichia coli pabA and its evolutionary relationship to thetrp(G)D. J Mol Biol 168:451–468PubMedGoogle Scholar
  28. Kaplan JB, Merkel WK, Nichols BP (1985) Evolution of the glutamine amidotransferase genes: nucleotide sequences of thepabA genes fromSalmonella typhimurium, Klebsiella aerogenes, andSerratia marcescens. J Mol Biol 183:327–340CrossRefPubMedGoogle Scholar
  29. Keller EB, Calvo JM (1979) Alternative, secondary structures of leader operons and the regulation of thetrp, phe, thr, andleu operons. Proc Natl Acad Sci USA 76:6186–6190PubMedGoogle Scholar
  30. Kuwajima K (1989) The molten globule state as a clue for understanding the folding and cooperativity of glubular-protein structure. Proteins 6:87–103CrossRefPubMedGoogle Scholar
  31. Lawrence JG, Hartl DL (1991) Unusual codon usage bias occurring within insertion sequences inEscherichia coli. Genetica (in press)Google Scholar
  32. Lawrence JG, Ochman H, Hartl DL (1991) Molecular and evolutinary relationships among enteric bacteria. J Gen Microbiol (in press)Google Scholar
  33. Li W-H, Graur D (1991) Molecular evolution. Sinauer Associate, Sunderland MAGoogle Scholar
  34. Li W-H, Tanimura M (1987) The molecular clock runs more slowly in man than in apes and monkeys. Nature 326:93–96CrossRefPubMedGoogle Scholar
  35. Li W-H, Wu C-I, Luo CC (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 2:150–174PubMedGoogle Scholar
  36. Li W-H, Gouy M, Sharp PM, O'hUigin C, Yang Y-W (1990) Molecular phylogeny of Rodentia, Lagomorpha, Primates, Artiodactyla, and Carnivora and molecular clocks. Proc Natl Acad Sci USA 87:6703–6707Google Scholar
  37. Liljenström H, von Heijne G (1987) Translation rate modification by preferential codon usage: intragenic position effects. J Theor Biol 124:43–55PubMedGoogle Scholar
  38. Liu Y-SV, Low TLK, Infante A, Putnam FW (1976) Complete covalent structure of a human IgA1 immunoglobin. Science 193:1017–1019PubMedGoogle Scholar
  39. MacDonald PM (1990)bicoid mRNA localization signal: phylogenetic conservation of function and RNA secondary structure. Development 110:161–171PubMedGoogle Scholar
  40. Manning PA, Pugsley AP, Reeves P (1977) Defective growth functions in mutants ofEscherichia coli K12, lacking a major outer membrane protein. J Mol Biol 116:285–300CrossRefPubMedGoogle Scholar
  41. Martin W, Gierl A, Saedler H (1989) Molecular evidence for pre-Cretaceous angiosperm origins. Nature 339:46–48CrossRefGoogle Scholar
  42. Nakamura K, Mizushima S (1976) Effects of heating in dodecyl sulfate solution on the conformation and electrophoretic mobility of isolated major outer membrane proteins fromEscherichia coli K-12. J Biochem (Tokyo) 80:1411–1422Google Scholar
  43. Nakamura K, Ostrovsky DN, Miyazawa T, Mizushima S (1974) Infrared spectra of outer and cytoplasmic membranes ofEscherichia coli Biochim. Biophys Acta 332:329–335Google Scholar
  44. Nichols BP, Miozzari GF, VanCleemput M, Bennett GN, Yanofsky C (1980) Nucleotide sequences of the trpG region ofEscherichia coli, Shigella dysenteriae, Salmonella typhimurium, andSerratia marcescens J Mol Biol 142:503–517CrossRefPubMedGoogle Scholar
  45. Nikaido H, Song SA, Shaltiel L, Nurminen M (1977) Outer membrane ofSalmonella. XIV. Reduced transmembrane diffusion rates in porin deficient mutants. Biochem Biophys. Res Commun 76:324–330CrossRefGoogle Scholar
  46. Ochman H, Wilson AC (1987a) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26:74–76PubMedGoogle Scholar
  47. Ochman H, Wilson AC (1987b) Evolutionary history of enteric bacteria. In: Niedhardt FD (ed)Escherichia coli andSalmonella typhimurium: cellular and molecular biology. American Society of Microbiology, Washington DC, pp 1649–1654Google Scholar
  48. Oxender DL, Zurawski G, Yanofsky C (1979) Attenuation in theEscherichia coli tryptophan operon: role of RNA secondary structure involving the tryptophan codon region. Proc Natl Acad Sci USA 76:5524–5528PubMedGoogle Scholar
  49. Perler F, Efstratiadis A, Lomedico P, Gilbert W, Kolodner R, Dodgson J (1980) The evolution of genes: the chicken preproinsulin gene. Cell 20:555–566CrossRefPubMedGoogle Scholar
  50. Ptitsyn OB, Pain RH, Semisotnov GV, Zerovnik E, Razgulyaev OI (1990) Evidence for the molten globule state as a general intermediate in protein folding. FEBS Lett 262:20–24CrossRefPubMedGoogle Scholar
  51. Reid G, Henning U (1987) A unique amino acid substitution in the outer membrane protein OmpA causes conjugation deficiency inEscherichia coli K-12. FEBS Lett 223:387–390CrossRefPubMedGoogle Scholar
  52. Roy P, Rondeau SB, Vézina C, Boileau G (1990) Effect of mRNA secondary structure on their efficiency of translation initiation by eukaryotic ribosomes. FEBS Lett 191:647–651Google Scholar
  53. Saiki RK, Scharf S, Fallona F, Mullis KB, Horn GT, Erlich HA, Arnheim NA (1985) Enzymatic amplification of, beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230:1350–1354PubMedGoogle Scholar
  54. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491PubMedGoogle Scholar
  55. Schluter D (1988) Estimating the form of natural selction on a quantitative trait. Evolution 42:849–861Google Scholar
  56. Sharp PM (1990) Processes of genome evolution reflected by base frequency differences amongSerratia marcescens genes. Mol Microbiol 4:119–122PubMedGoogle Scholar
  57. Sharp PM, Li W-H (1987a) Rate of synonymous substitution in enterobacterial genes in inversely related to codon usage bias. Mol Biol Evol 4:222–230PubMedGoogle Scholar
  58. Sharp PM, Li W-H (1987b) The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295PubMedGoogle Scholar
  59. Sharp PM, Shields DC, Wolfe KH, Li W-H (1989) Chromosomal location and evolutionary rate variation in enterobacterial genes. Science 246:808–810PubMedGoogle Scholar
  60. Sørensen MA, Kurland CG, Pedersen S (1989) Codon usage determines translation rate inEscherichia coli. J Mol Biol 207:365–377CrossRefPubMedGoogle Scholar
  61. Tso JY, Sun X-H, Kao T-H, Reese KS, Wu R (1985) Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene. Nucleic Acids Res 13:2485–2502PubMedGoogle Scholar
  62. Vogel H, Jähnig F (1986) Models for the structure of outer membrane proteins ofEscherichia coli derived from Raman spectroscopy and prediction models. J Mol Biol 190:191–199CrossRefPubMedGoogle Scholar
  63. Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639CrossRefPubMedGoogle Scholar
  64. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579PubMedGoogle Scholar
  65. Wolfe KH, Gouy M, Yang Y-W, Sharp PM, Li W-H (1989) Date of monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc. Natl Acad Sci USA 86:6201–6205PubMedGoogle Scholar
  66. Wu C-I, Li W-H (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–1745PubMedGoogle Scholar
  67. Yanofsky C (1988) Transcription attenuation. J Biol Chem 263: 609–612PubMedGoogle Scholar
  68. Zuckerkandl E, Pauling L (1962) Molecular disease, evolution, and genetic heterogeneity. In: Kasha M, Pullman B (eds) Horizons in biochemistry. Academic Press, New York, pp 189–225Google Scholar
  69. Zuker M, Stiegler P (1981) Optimal computer folding of large RNA sequence using thermodynamics and auxiliary information. Nucleic Acids Res 9:133–148PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1991

Authors and Affiliations

  • Jeffrey G. Lawrence
    • 1
  • Daniel L. Hartl
    • 1
  • Howard Ochman
    • 1
  1. 1.Department of GeneticsWashington University School of MedicineSt. LouisUSA

Personalised recommendations