• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Feb 15, 1994; 91(4): 1280–1284.
PMCID: PMC43141

Molecular genetic basis of allelic polymorphism in malate dehydrogenase (mdh) in natural populations of Escherichia coli and Salmonella enterica.

Abstract

Nucleotide sequences of the mdh gene encoding the metabolic enzyme malate dehydrogenase (MDH) were determined for 44 strains representing the major lineages of Escherichia coli and the eight subspecies of Salmonella enterica. Sequence diversity was four times greater in S. enterica than in E. coli, and in both species the rate of amino acid substitution was lower in the NAD(+)-binding domain than in the catalytic domain. Divergence of the mdh genes of the two species apparently has not involved excess nonsynonymous substitutions resulting from the fixation of adaptive amino acid mutations. Allozyme analysis detected 57% of the distinctive amino acid sequences. Statistical tests of the distribution of polymorphic synonymous nucleotide sites identified four possible intragenic recombination events, one involving a single allele of E. coli and three involving alleles of the three subspecies of S. enterica. But recombination at mdh has not occurred with sufficient frequency to obscure the phylogenetic relationships among strains indicated by multilocus enzyme electrophoresis, total DNA hybridization, and sequence analysis of the gapA and putP genes. These findings provide further evidence that the effective (realized) rates of horizontal transfer and recombination for metabolic enzyme and other housekeeping genes are generally low in these species, in contrast to those for loci encoding or mediating the structure of cell-surface and other macromolecules for which recombinants may be subject to strong balancing, directional, or diversifying selection.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.0M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Barcak GJ, Wolf RE., Jr Comparative nucleotide sequence analysis of growth-rate-regulated gnd alleles from natural isolates of Escherichia coli and from Salmonella typhimurium LT-2. J Bacteriol. 1988 Jan;170(1):372–379. [PMC free article] [PubMed]
  • Sawyer S. Statistical tests for detecting gene conversion. Mol Biol Evol. 1989 Sep;6(5):526–538. [PubMed]
  • Bisercić M, Feutrier JY, Reeves PR. Nucleotide sequences of the gnd genes from nine natural isolates of Escherichia coli: evidence of intragenic recombination as a contributing factor in the evolution of the polymorphic gnd locus. J Bacteriol. 1991 Jun;173(12):3894–3900. [PMC free article] [PubMed]
  • Dykhuizen DE, Green L. Recombination in Escherichia coli and the definition of biological species. J Bacteriol. 1991 Nov;173(22):7257–7268. [PMC free article] [PubMed]
  • Nelson K, Whittam TS, Selander RK. Nucleotide polymorphism and evolution in the glyceraldehyde-3-phosphate dehydrogenase gene (gapA) in natural populations of Salmonella and Escherichia coli. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6667–6671. [PMC free article] [PubMed]
  • Nelson K, Selander RK. Evolutionary genetics of the proline permease gene (putP) and the control region of the proline utilization operon in populations of Salmonella and Escherichia coli. J Bacteriol. 1992 Nov;174(21):6886–6895. [PMC free article] [PubMed]
  • Hall BG, Sharp PM. Molecular population genetics of Escherichia coli: DNA sequence diversity at the celC, crr, and gutB loci of natural isolates. Mol Biol Evol. 1992 Jul;9(4):654–665. [PubMed]
  • Ochman H, Selander RK. Standard reference strains of Escherichia coli from natural populations. J Bacteriol. 1984 Feb;157(2):690–693. [PMC free article] [PubMed]
  • Herzer PJ, Inouye S, Inouye M, Whittam TS. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol. 1990 Nov;172(11):6175–6181. [PMC free article] [PubMed]
  • Boyd EF, Wang FS, Beltran P, Plock SA, Nelson K, Selander RK. Salmonella reference collection B (SARB): strains of 37 serovars of subspecies I. J Gen Microbiol. 1993 Jun;139(Pt 6):1125–1132. [PubMed]
  • Selander RK, Caugant DA, Ochman H, Musser JM, Gilmour MN, Whittam TS. Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl Environ Microbiol. 1986 May;51(5):873–884. [PMC free article] [PubMed]
  • McAlister-Henn L, Blaber M, Bradshaw RA, Nisco SJ. Complete nucleotide sequence of the Escherichia coli gene encoding malate dehydrogenase. Nucleic Acids Res. 1987 Jun 25;15(12):4993–4993. [PMC free article] [PubMed]
  • Vogel RF, Entian KD, Mecke D. Cloning and sequence of the mdh structural gene of Escherichia coli coding for malate dehydrogenase. Arch Microbiol. 1987;149(1):36–42. [PubMed]
  • Lu CD, Abdelal AT. Complete sequence of the Salmonella typhimurium gene encoding malate dehydrogenase. Gene. 1993 Jan 15;123(1):143–144. [PubMed]
  • Higuchi RG, Ochman H. Production of single-stranded DNA templates by exonuclease digestion following the polymerase chain reaction. Nucleic Acids Res. 1989 Jul 25;17(14):5865–5865. [PMC free article] [PubMed]
  • Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. [PubMed]
  • Stephens JC. Statistical methods of DNA sequence analysis: detection of intragenic recombination or gene conversion. Mol Biol Evol. 1985 Nov;2(6):539–556. [PubMed]
  • Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. [PubMed]
  • Nei M, Jin L. Variances of the average numbers of nucleotide substitutions within and between populations. Mol Biol Evol. 1989 May;6(3):290–300. [PubMed]
  • Hall MD, Levitt DG, Banaszak LJ. Crystal structure of Escherichia coli malate dehydrogenase. A complex of the apoenzyme and citrate at 1.87 A resolution. J Mol Biol. 1992 Aug 5;226(3):867–882. [PubMed]
  • McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. [PubMed]
  • Caugant DA, Frøholm LO, Bøvre K, Holten E, Frasch CE, Mocca LF, Zollinger WD, Selander RK. Intercontinental spread of a genetically distinctive complex of clones of Neisseria meningitidis causing epidemic disease. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4927–4931. [PMC free article] [PubMed]
  • Reeves PR. Variation in O-antigens, niche-specific selection and bacterial populations. FEMS Microbiol Lett. 1992 Dec 15;100(1-3):509–516. [PubMed]
  • Wang JF, Caugant DA, Li X, Hu X, Poolman JT, Crowe BA, Achtman M. Clonal and antigenic analysis of serogroup A Neisseria meningitidis with particular reference to epidemiological features of epidemic meningitis in the People's Republic of China. Infect Immun. 1992 Dec;60(12):5267–5282. [PMC free article] [PubMed]
  • Whittam TS, Wolfe ML, Wachsmuth IK, Orskov F, Orskov I, Wilson RA. Clonal relationships among Escherichia coli strains that cause hemorrhagic colitis and infantile diarrhea. Infect Immun. 1993 May;61(5):1619–1629. [PMC free article] [PubMed]
  • Tibayrenc M, Neubauer K, Barnabé C, Guerrini F, Skarecky D, Ayala FJ. Genetic characterization of six parasitic protozoa: parity between random-primer DNA typing and multilocus enzyme electrophoresis. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1335–1339. [PMC free article] [PubMed]
  • Istock CA, Duncan KE, Ferguson N, Zhou X. Sexuality in a natural population of bacteria--Bacillus subtilis challenges the clonal paradigm. Mol Ecol. 1992 Aug;1(2):95–103. [PubMed]
  • Lenski RE. Assessing the genetic structure of microbial populations. Proc Natl Acad Sci U S A. 1993 May 15;90(10):4334–4336. [PMC free article] [PubMed]
  • Smith JM, Smith NH, O'Rourke M, Spratt BG. How clonal are bacteria? Proc Natl Acad Sci U S A. 1993 May 15;90(10):4384–4388. [PMC free article] [PubMed]
  • Eardly BD, Materon LA, Smith NH, Johnson DA, Rumbaugh MD, Selander RK. Genetic structure of natural populations of the nitrogen-fixing bacterium Rhizobium meliloti. Appl Environ Microbiol. 1990 Jan;56(1):187–194. [PMC free article] [PubMed]
  • Milkman R, Bridges MM. Molecular evolution of the Escherichia coli chromosome. IV. Sequence comparisons. Genetics. 1993 Mar;133(3):455–468. [PMC free article] [PubMed]
  • Achtman M, Pluschke G. Clonal analysis of descent and virulence among selected Escherichia coli. Annu Rev Microbiol. 1986;40:185–210. [PubMed]
  • Smith NH, Selander RK. Molecular genetic basis for complex flagellar antigen expression in a triphasic serovar of Salmonella. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):956–960. [PMC free article] [PubMed]
  • Marklund BI, Tennent JM, Garcia E, Hamers A, Båga M, Lindberg F, Gaastra W, Normark S. Horizontal gene transfer of the Escherichia coli pap and prs pili operons as a mechanism for the development of tissue-specific adhesive properties. Mol Microbiol. 1992 Aug;6(16):2225–2242. [PubMed]
  • Murray NE, Daniel AS, Cowan GM, Sharp PM. Conservation of motifs within the unusually variable polypeptide sequences of type I restriction and modification enzymes. Mol Microbiol. 1993 Jul;9(1):133–143. [PubMed]
  • Feavers IM, Heath AB, Bygraves JA, Maiden MC. Role of horizontal genetic exchange in the antigenic variation of the class 1 outer membrane protein of Neisseria meningitidis. Mol Microbiol. 1992 Feb;6(4):489–495. [PubMed]
  • Harbaugh MP, Podbielski A, Hügl S, Cleary PP. Nucleotide substitutions and small-scale insertion produce size and antigenic variation in group A streptococcal M1 protein. Mol Microbiol. 1993 May;8(5):981–991. [PubMed]
  • Spratt BG, Bowler LD, Zhang QY, Zhou J, Smith JM. Role of interspecies transfer of chromosomal genes in the evolution of penicillin resistance in pathogenic and commensal Neisseria species. J Mol Evol. 1992 Feb;34(2):115–125. [PubMed]
  • Laible G, Spratt BG, Hakenbeck R. Interspecies recombinational events during the evolution of altered PBP 2x genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Mol Microbiol. 1991 Aug;5(8):1993–2002. [PubMed]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

Formats:

Related citations in PubMed

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...