Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Nov;179(21):6551–6559. doi: 10.1128/jb.179.21.6551-6559.1997

Evolutionary genetics of the isocitrate dehydrogenase gene (icd) in Escherichia coli and Salmonella enterica.

F S Wang 1, T S Whittam 1, R K Selander 1
PMCID: PMC179578  PMID: 9352899

Abstract

Sequences of the icd gene, encoding isocitrate dehydrogenase (IDH), were obtained for 33 strains representing the major phylogenetic lineages of Escherichia coli and Salmonella enterica. Evolutionary relationships of the strains based on variation in icd are generally similar to those previously obtained for several other housekeeping and for invasion genes, but the sequences of S. enterica subspecies V strains are unusual in being almost intermediate between those of the other S. enterica subspecies and E. coli. For S. enterica, the ratio of synonymous (silent) to nonsynonymous (replacement) nucleotide substitutions between pairs of strains was larger than comparable values for 12 other housekeeping and invasion genes, reflecting unusually strong purifying selection against amino acid replacement in the IDH enzyme. All amino acids involved in the catalytic activity and conformational changes of IDH are strictly conserved within and between species. In E. coli, the level of variation at the 3' end of the gene is elevated by the presence in some strains of a 165-bp replacement sequence supplied by the integration of either lambdoid phage 21 or defective prophage element e14. The 72 members of the E. coli Reference Collection (ECOR) and five additional E. coli strains were surveyed for the presence of phage 21 (as prophage) by PCR amplification of a phage 21-specific fragment in and adjacent to the host icd, and the sequence of the phage 21 segment extending from the 3' end of icd through the integrase gene (int) was determined in nine strains of E. coli. Phage 21 was found in 39% of E. coli strains, and its distribution among the ECOR strains is nonrandom. In two ECOR strains, the phage 21 int gene is interrupted by a 1,313-bp insertion element that has 99.3% nucleotide sequence identity with IS3411 of E. coli. The phylogenetic relationships of phage 21 strains derived from sequences of two different genomic regions were strongly incongruent, providing evidence of frequent recombination.

Full Text

The Full Text of this article is available as a PDF (1.8 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baker J., Limberger R., Schneider S. J., Campbell A. Recombination and modular exchange in the genesis of new lambdoid phages. New Biol. 1991 Mar;3(3):297–308. [PubMed] [Google Scholar]
  2. Borthwick A. C., Holms W. H., Nimmo H. G. Amino acid sequence round the site of phosphorylation in isocitrate dehydrogenase from Escherichia coli ML308. FEBS Lett. 1984 Aug 20;174(1):112–115. doi: 10.1016/0014-5793(84)81087-x. [DOI] [PubMed] [Google Scholar]
  3. Boyd E. F., Li J., Ochman H., Selander R. K. Comparative genetics of the inv-spa invasion gene complex of Salmonella enterica. J Bacteriol. 1997 Mar;179(6):1985–1991. doi: 10.1128/jb.179.6.1985-1991.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boyd E. F., Nelson K., Wang F. S., Whittam T. S., Selander R. K. Molecular genetic basis of allelic polymorphism in malate dehydrogenase (mdh) in natural populations of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1280–1284. doi: 10.1073/pnas.91.4.1280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boyd E. F., Wang F. S., Whittam T. S., Selander R. K. Molecular genetic relationships of the salmonellae. Appl Environ Microbiol. 1996 Mar;62(3):804–808. doi: 10.1128/aem.62.3.804-808.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brody H., Greener A., Hill C. W. Excision and reintegration of the Escherichia coli K-12 chromosomal element e14. J Bacteriol. 1985 Mar;161(3):1112–1117. doi: 10.1128/jb.161.3.1112-1117.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brody H., Hill C. W. Attachment site of the genetic element e14. J Bacteriol. 1988 May;170(5):2040–2044. doi: 10.1128/jb.170.5.2040-2044.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cabot E. L., Beckenbach A. T. Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Comput Appl Biosci. 1989 Jul;5(3):233–234. doi: 10.1093/bioinformatics/5.3.233. [DOI] [PubMed] [Google Scholar]
  9. Campbell A. M. Chromosomal insertion sites for phages and plasmids. J Bacteriol. 1992 Dec;174(23):7495–7499. doi: 10.1128/jb.174.23.7495-7499.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Campbell A., Schneider S. J., Song B. Lambdoid phages as elements of bacterial genomes (integrase/phage21/Escherichia coli K-12/icd gene). Genetica. 1992;86(1-3):259–267. doi: 10.1007/BF00133724. [DOI] [PubMed] [Google Scholar]
  11. Dean A. M., Golding G. B. Protein engineering reveals ancient adaptive replacements in isocitrate dehydrogenase. Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3104–3109. doi: 10.1073/pnas.94.7.3104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dean A. M., Koshland D. E., Jr Electrostatic and steric contributions to regulation at the active site of isocitrate dehydrogenase. Science. 1990 Aug 31;249(4972):1044–1046. doi: 10.1126/science.2204110. [DOI] [PubMed] [Google Scholar]
  13. Dean A. M., Lee M. H., Koshland D. E., Jr Phosphorylation inactivates Escherichia coli isocitrate dehydrogenase by preventing isocitrate binding. J Biol Chem. 1989 Dec 5;264(34):20482–20486. [PubMed] [Google Scholar]
  14. Eyre-Walker A., Bulmer M. Reduced synonymous substitution rate at the start of enterobacterial genes. Nucleic Acids Res. 1993 Sep 25;21(19):4599–4603. doi: 10.1093/nar/21.19.4599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Greener A., Hill C. W. Identification of a novel genetic element in Escherichia coli K-12. J Bacteriol. 1980 Oct;144(1):312–321. doi: 10.1128/jb.144.1.312-321.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Herzer P. J., Inouye S., Inouye M., Whittam T. S. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol. 1990 Nov;172(11):6175–6181. doi: 10.1128/jb.172.11.6175-6181.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Highton P. J., Chang Y., Myers R. J. Evidence for the exchange of segments between genomes during the evolution of lambdoid bacteriophages. Mol Microbiol. 1990 Aug;4(8):1329–1340. doi: 10.1111/j.1365-2958.1990.tb00712.x. [DOI] [PubMed] [Google Scholar]
  18. Higuchi R. G., 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. doi: 10.1093/nar/17.14.5865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hill C. W., Gray J. A., Brody H. Use of the isocitrate dehydrogenase structural gene for attachment of e14 in Escherichia coli K-12. J Bacteriol. 1989 Jul;171(7):4083–4084. doi: 10.1128/jb.171.7.4083-4084.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hurley J. H., Dean A. M., Koshland D. E., Jr, Stroud R. M. Catalytic mechanism of NADP(+)-dependent isocitrate dehydrogenase: implications from the structures of magnesium-isocitrate and NADP+ complexes. Biochemistry. 1991 Sep 3;30(35):8671–8678. doi: 10.1021/bi00099a026. [DOI] [PubMed] [Google Scholar]
  21. Hurley J. H., Dean A. M., Sohl J. L., Koshland D. E., Jr, Stroud R. M. Regulation of an enzyme by phosphorylation at the active site. Science. 1990 Aug 31;249(4972):1012–1016. doi: 10.1126/science.2204109. [DOI] [PubMed] [Google Scholar]
  22. Hurley J. H., Thorsness P. E., Ramalingam V., Helmers N. H., Koshland D. E., Jr, Stroud R. M. Structure of a bacterial enzyme regulated by phosphorylation, isocitrate dehydrogenase. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8635–8639. doi: 10.1073/pnas.86.22.8635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ishiguro N., Sato G. Nucleotide sequence of insertion sequence IS3411, which flanks the citrate utilization determinant of transposon Tn3411. J Bacteriol. 1988 Apr;170(4):1902–1906. doi: 10.1128/jb.170.4.1902-1906.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kutsukake K., Nakao T., Iino T. A gene for DNA invertase and an invertible DNA in Escherichia coli K-12. Gene. 1985;34(2-3):343–350. doi: 10.1016/0378-1119(85)90143-x. [DOI] [PubMed] [Google Scholar]
  25. Li J., Ochman H., Groisman E. A., Boyd E. F., Solomon F., Nelson K., Selander R. K. Relationship between evolutionary rate and cellular location among the Inv/Spa invasion proteins of Salmonella enterica. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7252–7256. doi: 10.1073/pnas.92.16.7252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Matsutani S., Ohtsubo E. Complete sequence of IS629. Nucleic Acids Res. 1990 Apr 11;18(7):1899–1899. doi: 10.1093/nar/18.7.1899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
  28. Miyazaki K., Eguchi H., Yamagishi A., Wakagi T., Oshima T. Molecular cloning of the isocitrate dehydrogenase gene of an extreme thermophile, Thermus thermophilus HB8. Appl Environ Microbiol. 1992 Jan;58(1):93–98. doi: 10.1128/aem.58.1.93-98.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Muro-Pastor M. I., Florencio F. J. NADP(+)-isocitrate dehydrogenase from the cyanobacterium Anabaena sp. strain PCC 7120: purification and characterization of the enzyme and cloning, sequencing, and disruption of the icd gene. J Bacteriol. 1994 May;176(9):2718–2726. doi: 10.1128/jb.176.9.2718-2726.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
  31. 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. doi: 10.1093/oxfordjournals.molbev.a040547. [DOI] [PubMed] [Google Scholar]
  32. Nelson K., Selander R. K. Analysis of genetic variation by polymerase chain reaction-based nucleotide sequencing. Methods Enzymol. 1994;235:174–183. doi: 10.1016/0076-6879(94)35139-2. [DOI] [PubMed] [Google Scholar]
  33. Nelson K., Selander R. K. 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. doi: 10.1128/jb.174.21.6886-6895.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Nelson K., Selander R. K. Intergeneric transfer and recombination of the 6-phosphogluconate dehydrogenase gene (gnd) in enteric bacteria. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):10227–10231. doi: 10.1073/pnas.91.21.10227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Nelson K., Whittam T. S., Selander R. K. 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. doi: 10.1073/pnas.88.15.6667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ochman H., Selander R. K. Standard reference strains of Escherichia coli from natural populations. J Bacteriol. 1984 Feb;157(2):690–693. doi: 10.1128/jb.157.2.690-693.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Paton A. W., Paton J. C. Characterization of IS1203, an insertion sequence in Escherichia coli O111:H-. Gene. 1994 Dec 2;150(1):67–70. doi: 10.1016/0378-1119(94)90859-1. [DOI] [PubMed] [Google Scholar]
  38. Reeves M. W., Evins G. M., Heiba A. A., Plikaytis B. D., Farmer J. J., 3rd Clonal nature of Salmonella typhi and its genetic relatedness to other salmonellae as shown by multilocus enzyme electrophoresis, and proposal of Salmonella bongori comb. nov. J Clin Microbiol. 1989 Feb;27(2):313–320. doi: 10.1128/jcm.27.2.313-320.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  40. Sawyer S. A., Hartl D. L. Population genetics of polymorphism and divergence. Genetics. 1992 Dec;132(4):1161–1176. doi: 10.1093/genetics/132.4.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sharp P. M. Determinants of DNA sequence divergence between Escherichia coli and Salmonella typhimurium: codon usage, map position, and concerted evolution. J Mol Evol. 1991 Jul;33(1):23–33. doi: 10.1007/BF02100192. [DOI] [PubMed] [Google Scholar]
  42. Stephens J. C. Statistical methods of DNA sequence analysis: detection of intragenic recombination or gene conversion. Mol Biol Evol. 1985 Nov;2(6):539–556. doi: 10.1093/oxfordjournals.molbev.a040371. [DOI] [PubMed] [Google Scholar]
  43. Thorsness P. E., Koshland D. E., Jr Inactivation of isocitrate dehydrogenase by phosphorylation is mediated by the negative charge of the phosphate. J Biol Chem. 1987 Aug 5;262(22):10422–10425. [PubMed] [Google Scholar]
  44. Walsh K., Koshland D. E., Jr Determination of flux through the branch point of two metabolic cycles. The tricarboxylic acid cycle and the glyoxylate shunt. J Biol Chem. 1984 Aug 10;259(15):9646–9654. [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES