Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Oct 11;91(21):10227–10231. doi: 10.1073/pnas.91.21.10227

Intergeneric transfer and recombination of the 6-phosphogluconate dehydrogenase gene (gnd) in enteric bacteria.

K Nelson 1, R K Selander 1
PMCID: PMC44991  PMID: 7937867

Abstract

The gnd gene, encoding 6-phosphogluconate dehydrogenase (EC 1.1.1.44), was sequenced in 87 strains of 15 species assigned to five nominal genera of the Enterobacteriaceae, including 36 isolates of Salmonella enterica and 32 strains of Escherichia coli. In S. enterica, the effective (realized) rate of recombination of horizontally transferred gnd sequences is only moderately higher than the rates for other chromosomal housekeeping genes. In contrast, recombination at gnd has occurred with such high frequency in Escherichia coli that the indicated evolutionary relationships among strains are not congruent with those estimated by sequence analysis of other genes and by multilocus enzyme electrophoresis. E. coli and S. enterica apparently have not exchanged gnd sequences, but those of several strains of E. coli have been imported from species of Citrobacter and Klebsiella. The relatively frequent exchange of gnd within and among taxonomic groups of the Enterobacteriaceae, compared with other housekeeping genes, apparently results from its close linkage with genes that are subject to diversifying selection, including those of the rfb region determining the structure of the O antigen polysaccharide.

Full text

PDF
10227

Selected References

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

  1. Achtman M. Clonal spread of serogroup A meningococci: a paradigm for the analysis of microevolution in bacteria. Mol Microbiol. 1994 Jan;11(1):15–22. doi: 10.1111/j.1365-2958.1994.tb00285.x. [DOI] [PubMed] [Google Scholar]
  2. Achtman M., Pluschke G. Clonal analysis of descent and virulence among selected Escherichia coli. Annu Rev Microbiol. 1986;40:185–210. doi: 10.1146/annurev.mi.40.100186.001153. [DOI] [PubMed] [Google Scholar]
  3. Barcak G. J., Wolf R. E., 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. doi: 10.1128/jb.170.1.372-379.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bastin D. A., Stevenson G., Brown P. K., Haase A., Reeves P. R. Repeat unit polysaccharides of bacteria: a model for polymerization resembling that of ribosomes and fatty acid synthetase, with a novel mechanism for determining chain length. Mol Microbiol. 1993 Mar;7(5):725–734. doi: 10.1111/j.1365-2958.1993.tb01163.x. [DOI] [PubMed] [Google Scholar]
  5. Batchelor R. A., Alifano P., Biffali E., Hull S. I., Hull R. A. Nucleotide sequences of the genes regulating O-polysaccharide antigen chain length (rol) from Escherichia coli and Salmonella typhimurium: protein homology and functional complementation. J Bacteriol. 1992 Aug;174(16):5228–5236. doi: 10.1128/jb.174.16.5228-5236.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Beltran P., Musser J. M., Helmuth R., Farmer J. J., 3rd, Frerichs W. M., Wachsmuth I. K., Ferris K., McWhorter A. C., Wells J. G., Cravioto A. Toward a population genetic analysis of Salmonella: genetic diversity and relationships among strains of serotypes S. choleraesuis, S. derby, S. dublin, S. enteritidis, S. heidelberg, S. infantis, S. newport, and S. typhimurium. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7753–7757. doi: 10.1073/pnas.85.20.7753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bisercić M., Feutrier J. Y., Reeves P. R. 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. doi: 10.1128/jb.173.12.3894-3900.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Boyd E. F., Wang F. S., Beltran P., Plock S. A., Nelson K., Selander R. K. Salmonella reference collection B (SARB): strains of 37 serovars of subspecies I. J Gen Microbiol. 1993 Jun;139(Pt 6):1125–1132. doi: 10.1099/00221287-139-6-1125. [DOI] [PubMed] [Google Scholar]
  10. Brenner D. J., Grimont P. A., Steigerwalt A. G., Fanning G. R., Ageron E., Riddle C. F. Classification of citrobacteria by DNA hybridization: designation of Citrobacter farmeri sp. nov., Citrobacter youngae sp. nov., Citrobacter braakii sp. nov., Citrobacter werkmanii sp. nov., Citrobacter sedlakii sp. nov., and three unnamed Citrobacter genomospecies. Int J Syst Bacteriol. 1993 Oct;43(4):645–658. doi: 10.1099/00207713-43-4-645. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Caugant D. A., Levin B. R., Selander R. K. Genetic diversity and temporal variation in the E. coli population of a human host. Genetics. 1981 Jul;98(3):467–490. doi: 10.1093/genetics/98.3.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dykhuizen D. E., Green L. Recombination in Escherichia coli and the definition of biological species. J Bacteriol. 1991 Nov;173(22):7257–7268. doi: 10.1128/jb.173.22.7257-7268.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Groisman E. A., Sturmoski M. A., Solomon F. R., Lin R., Ochman H. Molecular, functional, and evolutionary analysis of sequences specific to Salmonella. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):1033–1037. doi: 10.1073/pnas.90.3.1033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hashimoto Y., Li N., Yokoyama H., Ezaki T. Complete nucleotide sequence and molecular characterization of ViaB region encoding Vi antigen in Salmonella typhi. J Bacteriol. 1993 Jul;175(14):4456–4465. doi: 10.1128/jb.175.14.4456-4465.1993. [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. Jayaratne P., Bronner D., MacLachlan P. R., Dodgson C., Kido N., Whitfield C. Cloning and analysis of duplicated rfbM and rfbK genes involved in the formation of GDP-mannose in Escherichia coli O9:K30 and participation of rfb genes in the synthesis of the group I K30 capsular polysaccharide. J Bacteriol. 1994 Jun;176(11):3126–3139. doi: 10.1128/jb.176.11.3126-3139.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Karaolis D. K., Lan R., Reeves P. R. Sequence variation in Shigella sonnei (Sonnei), a pathogenic clone of Escherichia coli, over four continents and 41 years. J Clin Microbiol. 1994 Mar;32(3):796–802. doi: 10.1128/jcm.32.3.796-802.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Keenleyside W. J., Perry M., Maclean L., Poppe C., Whitfield C. A plasmid-encoded rfbO:54 gene cluster is required for biosynthesis of the O:54 antigen in Salmonella enterica serovar Borreze. Mol Microbiol. 1994 Feb;11(3):437–448. doi: 10.1111/j.1365-2958.1994.tb00325.x. [DOI] [PubMed] [Google Scholar]
  20. Lawrence J. G., Ochman H., Hartl D. L. Molecular and evolutionary relationships among enteric bacteria. J Gen Microbiol. 1991 Aug;137(8):1911–1921. doi: 10.1099/00221287-137-8-1911. [DOI] [PubMed] [Google Scholar]
  21. Le Minor L., Popoff M. Y., Laurent B., Hermant D. Individualisation d'une septième sous-espèce de Salmonella: S. choleraesuis subsp. indica subsp. nov. Ann Inst Pasteur Microbiol. 1986 Sep-Oct;137B(2):211–217. [PubMed] [Google Scholar]
  22. Le Minor L., Véron M., Popoff M. Taxonomie des Salmonella. Ann Microbiol (Paris) 1982 Sep-Oct;133(2):223–243. [PubMed] [Google Scholar]
  23. Li J., Musser J. M., Beltran P., Kline M. W., Selander R. K. Genotypic heterogeneity of strains of Citrobacter diversus expressing a 32-kilodalton outer membrane protein associated with neonatal meningitis. J Clin Microbiol. 1990 Aug;28(8):1760–1765. doi: 10.1128/jcm.28.8.1760-1765.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Li J., Nelson K., McWhorter A. C., Whittam T. S., Selander R. K. Recombinational basis of serovar diversity in Salmonella enterica. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2552–2556. doi: 10.1073/pnas.91.7.2552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Li J., Smith N. H., Nelson K., Crichton P. B., Old D. C., Whittam T. S., Selander R. K. Evolutionary origin and radiation of the avian-adapted non-motile salmonellae. J Med Microbiol. 1993 Feb;38(2):129–139. doi: 10.1099/00222615-38-2-129. [DOI] [PubMed] [Google Scholar]
  26. Murray N. E., Daniel A. S., Cowan G. M., Sharp P. M. Conservation of motifs within the unusually variable polypeptide sequences of type I restriction and modification enzymes. Mol Microbiol. 1993 Jul;9(1):133–143. doi: 10.1111/j.1365-2958.1993.tb01675.x. [DOI] [PubMed] [Google Scholar]
  27. Musser J. M., Bemis D. A., Ishikawa H., Selander R. K. Clonal diversity and host distribution in Bordetella bronchiseptica. J Bacteriol. 1987 Jun;169(6):2793–2803. doi: 10.1128/jb.169.6.2793-2803.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nasoff M. S., Baker H. V., 2nd, Wolf R. E., Jr DNA sequence of the Escherichia coli gene, gnd, for 6-phosphogluconate dehydrogenase. Gene. 1984 Mar;27(3):253–264. doi: 10.1016/0378-1119(84)90070-2. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. 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]
  32. 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]
  33. 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]
  34. Ochman H., Whittam T. S., Caugant D. A., Selander R. K. Enzyme polymorphism and genetic population structure in Escherichia coli and Shigella. J Gen Microbiol. 1983 Sep;129(9):2715–2726. doi: 10.1099/00221287-129-9-2715. [DOI] [PubMed] [Google Scholar]
  35. Reeves P. Evolution of Salmonella O antigen variation by interspecific gene transfer on a large scale. Trends Genet. 1993 Jan;9(1):17–22. doi: 10.1016/0168-9525(93)90067-R. [DOI] [PubMed] [Google Scholar]
  36. Reeves P., Stevenson G. Cloning and nucleotide sequence of the Salmonella typhimurium LT2 gnd gene and its homology with the corresponding sequence of Escherichia coli K12. Mol Gen Genet. 1989 May;217(1):182–184. doi: 10.1007/BF00330960. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Selander R. K., Beltran P., Smith N. H., Helmuth R., Rubin F. A., Kopecko D. J., Ferris K., Tall B. D., Cravioto A., Musser J. M. Evolutionary genetic relationships of clones of Salmonella serovars that cause human typhoid and other enteric fevers. Infect Immun. 1990 Jul;58(7):2262–2275. doi: 10.1128/iai.58.7.2262-2275.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Selander R. K., Smith N. H., Li J., Beltran P., Ferris K. E., Kopecko D. J., Rubin F. A. Molecular evolutionary genetics of the cattle-adapted serovar Salmonella dublin. J Bacteriol. 1992 Jun;174(11):3587–3592. doi: 10.1128/jb.174.11.3587-3592.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sharp P. M., Kelleher J. E., Daniel A. S., Cowan G. M., Murray N. E. Roles of selection and recombination in the evolution of type I restriction-modification systems in enterobacteria. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9836–9840. doi: 10.1073/pnas.89.20.9836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Smith J. M., Smith N. H., O'Rourke M., Spratt B. G. How clonal are bacteria? Proc Natl Acad Sci U S A. 1993 May 15;90(10):4384–4388. doi: 10.1073/pnas.90.10.4384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Smith N. H., Beltran P., Selander R. K. Recombination of Salmonella phase 1 flagellin genes generates new serovars. J Bacteriol. 1990 May;172(5):2209–2216. doi: 10.1128/jb.172.5.2209-2216.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. Stevenson G., Neal B., Liu D., Hobbs M., Packer N. H., Batley M., Redmond J. W., Lindquist L., Reeves P. Structure of the O antigen of Escherichia coli K-12 and the sequence of its rfb gene cluster. J Bacteriol. 1994 Jul;176(13):4144–4156. doi: 10.1128/jb.176.13.4144-4156.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Sugiyama T., Kido N., Komatsu T., Ohta M., Jann K., Jann B., Saeki A., Kato N. Genetic analysis of Escherichia coli O9 rfb: identification and DNA sequence of phosphomannomutase and GDP-mannose pyrophosphorylase genes. Microbiology. 1994 Jan;140(Pt 1):59–71. doi: 10.1099/13500872-140-1-59. [DOI] [PubMed] [Google Scholar]
  46. Van Vliet F., Boyen A., Glansdorff N. On interspecies gene transfer: the case of the argF gene of Escherichia coli. Ann Inst Pasteur Microbiol. 1988 Jul-Aug;139(4):493–496. doi: 10.1016/0769-2609(88)90111-1. [DOI] [PubMed] [Google Scholar]
  47. Waxin H., Virlogeux I., Kolyva S., Popoff M. Y. Identification of six open reading frames in the Salmonella enterica subsp. enterica ser. Typhi viaB locus involved in Vi antigen production. Res Microbiol. 1993 Jun;144(5):363–371. doi: 10.1016/0923-2508(93)90193-6. [DOI] [PubMed] [Google Scholar]
  48. Whittam T. S., Ochman H., Selander R. K. Multilocus genetic structure in natural populations of Escherichia coli. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1751–1755. doi: 10.1073/pnas.80.6.1751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Whittam T. S., Wolfe M. L., Wachsmuth I. K., Orskov F., Orskov I., Wilson R. A. Clonal relationships among Escherichia coli strains that cause hemorrhagic colitis and infantile diarrhea. Infect Immun. 1993 May;61(5):1619–1629. doi: 10.1128/iai.61.5.1619-1629.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES