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Molecular considerations in the evolution of bacterial genes

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Summary

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.

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References

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

    PubMed  Google Scholar 

  • Beale D, Feinstein A (1976) Structure and function of the constant regions of immunoglobins. Quart Rev Biophys 9:135–180

    Google Scholar 

  • Beck E, Bremer E (1980) Nucleotide sequence of the geneompA coding the outer membrane protein II* ofEscherichia coli K-12. Nucleic Acids Res 8:3011–3024

    PubMed  Google Scholar 

  • Biesecker G, Harris JI, Thierry JC, Walker JE, Wonacott AJ (1977) Sequence and structure ofd-glyceraldehyde-3-phosphate dehydrogenase fromBacillus stearothermophilus. Nature 266:328–333

    Article  PubMed  Google Scholar 

  • 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 164:73–87

    Article  PubMed  Google Scholar 

  • 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 150:61–66

    Article  PubMed  Google Scholar 

  • 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 195:321–328

    Article  PubMed  Google Scholar 

  • Brenner DJ, Falkow S (1971) Molecular relationships among members of the Enterobacteriaceae. Adv Genet 16:81–118

    PubMed  Google Scholar 

  • Bulmer M (1988) Codon usage and intragenic position. J Theor Biol 133:67–71

    PubMed  Google Scholar 

  • Bychkova VE, Pain RH, Ptitsyn OB (1988) The ‘molten globule’ state is involved in the translocation of proteins across membranes. FEBS Lett 238:231–234

    Article  PubMed  Google Scholar 

  • 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 77:4592–4596

    PubMed  Google Scholar 

  • Cocks GT, Wilson AC (1972) Enzyme evolution in the Enterobacteriaceae. J Bacteriol 110:793–802

    PubMed  Google Scholar 

  • Conway T, Sewell GW, Ingram LO (1987) Glyceraldehyde-3-phosphate dehydrogenase gene fromZymomonas mobilis: cloning, sequencing, and identification of promoter region. J Bacteriol 169:5653–5662

    PubMed  Google Scholar 

  • Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395

    PubMed  Google Scholar 

  • 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 7:547–577

    PubMed  Google Scholar 

  • 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 63:78–85

    PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits, on phylogenies with a molecular clock. Syst Zool 34:152–161

    Google Scholar 

  • Fitch WM (1976) The molecular evolution of cytochrome c in eukaryotes. J Mol Evol 8:13–40

    Article  PubMed  Google Scholar 

  • Freudl R, Cole ST (1983) Cloning and molecular characterization of theompA gene fromSalmonella typhimurium. Eur J Biochem 134:497–502

    Article  PubMed  Google Scholar 

  • 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 201:76–81

    Article  PubMed  Google Scholar 

  • 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 261:11355–11361

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Green PJ, Pines O, Inouye M (1986) The role of antisense RNA in gene regulation. Annu Rev Biochem 55:569–597

    Article  PubMed  Google Scholar 

  • 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 265:17627–17636

    PubMed  Google Scholar 

  • 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 30:250–257

    PubMed  Google Scholar 

  • Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–33

    PubMed  Google Scholar 

  • Kaplan JB, Nichols BP (1983) Nucleotide sequence ofEscherichia coli pabA and its evolutionary relationship to thetrp(G)D. J Mol Biol 168:451–468

    PubMed  Google Scholar 

  • 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 183:327–340

    Article  PubMed  Google Scholar 

  • 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 76:6186–6190

    PubMed  Google Scholar 

  • Kuwajima K (1989) The molten globule state as a clue for understanding the folding and cooperativity of glubular-protein structure. Proteins 6:87–103

    Article  PubMed  Google Scholar 

  • Lawrence JG, Hartl DL (1991) Unusual codon usage bias occurring within insertion sequences inEscherichia coli. Genetica (in press)

  • Lawrence JG, Ochman H, Hartl DL (1991) Molecular and evolutinary relationships among enteric bacteria. J Gen Microbiol (in press)

  • Li W-H, Graur D (1991) Molecular evolution. Sinauer Associate, Sunderland MA

    Google Scholar 

  • Li W-H, Tanimura M (1987) The molecular clock runs more slowly in man than in apes and monkeys. Nature 326:93–96

    Article  PubMed  Google Scholar 

  • 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 2:150–174

    PubMed  Google Scholar 

  • 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 87:6703–6707

    Google Scholar 

  • Liljenström H, von Heijne G (1987) Translation rate modification by preferential codon usage: intragenic position effects. J Theor Biol 124:43–55

    PubMed  Google Scholar 

  • Liu Y-SV, Low TLK, Infante A, Putnam FW (1976) Complete covalent structure of a human IgA1 immunoglobin. Science 193:1017–1019

    PubMed  Google Scholar 

  • MacDonald PM (1990)bicoid mRNA localization signal: phylogenetic conservation of function and RNA secondary structure. Development 110:161–171

    PubMed  Google Scholar 

  • Manning PA, Pugsley AP, Reeves P (1977) Defective growth functions in mutants ofEscherichia coli K12, lacking a major outer membrane protein. J Mol Biol 116:285–300

    Article  PubMed  Google Scholar 

  • Martin W, Gierl A, Saedler H (1989) Molecular evidence for pre-Cretaceous angiosperm origins. Nature 339:46–48

    Article  Google Scholar 

  • 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) 80:1411–1422

    Google Scholar 

  • Nakamura K, Ostrovsky DN, Miyazawa T, Mizushima S (1974) Infrared spectra of outer and cytoplasmic membranes ofEscherichia coli Biochim. Biophys Acta 332:329–335

    Google Scholar 

  • 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 142:503–517

    Article  PubMed  Google Scholar 

  • 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 76:324–330

    Article  Google Scholar 

  • Ochman H, Wilson AC (1987a) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26:74–76

    PubMed  Google Scholar 

  • 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 1649–1654

    Google Scholar 

  • 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 76:5524–5528

    PubMed  Google Scholar 

  • Perler F, Efstratiadis A, Lomedico P, Gilbert W, Kolodner R, Dodgson J (1980) The evolution of genes: the chicken preproinsulin gene. Cell 20:555–566

    Article  PubMed  Google Scholar 

  • 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 262:20–24

    Article  PubMed  Google Scholar 

  • 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 223:387–390

    Article  PubMed  Google Scholar 

  • 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 191:647–651

    Google Scholar 

  • 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 230:1350–1354

    PubMed  Google Scholar 

  • 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 239:487–491

    PubMed  Google Scholar 

  • Schluter D (1988) Estimating the form of natural selction on a quantitative trait. Evolution 42:849–861

    Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • 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 15:1281–1295

    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 

  • Sørensen MA, Kurland CG, Pedersen S (1989) Codon usage determines translation rate inEscherichia coli. J Mol Biol 207:365–377

    Article  PubMed  Google Scholar 

  • 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 13:2485–2502

    PubMed  Google Scholar 

  • 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 190:191–199

    Article  PubMed  Google Scholar 

  • Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639

    Article  PubMed  Google Scholar 

  • 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 87:4576–4579

    PubMed  Google Scholar 

  • 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 86:6201–6205

    PubMed  Google Scholar 

  • Wu C-I, Li W-H (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–1745

    PubMed  Google Scholar 

  • Yanofsky C (1988) Transcription attenuation. J Biol Chem 263: 609–612

    PubMed  Google Scholar 

  • 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 189–225

    Google Scholar 

  • Zuker M, Stiegler P (1981) Optimal computer folding of large RNA sequence using thermodynamics and auxiliary information. Nucleic Acids Res 9:133–148

    PubMed  Google Scholar 

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  1. Department of Genetics, Washington University School of Medicine, Box 8232, 63110, St. Louis, MO, USA

    Jeffrey G. Lawrence, Daniel L. Hartl & Howard Ochman

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  1. Jeffrey G. Lawrence
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  2. Daniel L. Hartl
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Lawrence, J.G., Hartl, D.L. & Ochman, H. Molecular considerations in the evolution of bacterial genes. J Mol Evol 33, 241–250 (1991). https://doi.org/10.1007/BF02100675

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