Skip to main content
Log in

A comparison of the nucleotide sequences of theadk andrecA genes of pathogenic and commensalNeisseria species: Evidence for extensive interspecies recombination withinadk

  • Articles
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The sequences of the adenylate kinase gene (adk) and the RecA gene (recA) were determined from the same isolates ofNeisseria gonorrhoeae, N. meningitidis, N. lactamica, N. polysaccharea, N. cinerea, N. mucosa, N. pharyngis var.flava, N. flavescens, andN. animalis. The patterns of sequence divergence observed atadk andrecA were very different. Dendrograms constructed from therecA data using two different algorithms were statistically robust and were congruent with each other and with the relationships between the species previously proposed using other data. In contrast, the dendrograms derived from theadk data were noncongruent with each other, and with those from therecA data, and were statistically poorly supported. These results, along with the uniform distribution of pairwise sequence divergences between the species atadk, suggest there has been a history of interspecies recombination within theadk gene of the humanNeisseria species which has obscured the phylogenetic relationships between the species. This view was supported by Sawyer's runs test, and the Index of Association (IA) between codons, which provided significant evidence for interspecies recombination between theadk genes from the humanNeisseria species, but no evidence of interspecies recombination between therecA sequences.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Achtman M (1994) Clonal spread of serogroup A meningococci: a paradigm for the analysis of microevolution in bacteria. Mol Microbiol 11:15–22

    Google Scholar 

  • Barrett SJ, Sneath PHA (1994) A numerical phenotypic taxonomic study of the genusNeisseria. Microbiol 140:2867–2891

    Google Scholar 

  • Bowler LD, Zhang Q-Y, Riou J-Y, Spratt BG (1994) Inter-species recombination between thepenA genes ofNeisseria meningitidis and commensalNeisseria species during the emergence of penicillin resistance inN. meningitidis: natural events and laboratory simulation. J Bacteriol 176:333–337

    Google Scholar 

  • Boyd EF, Nelson K, Wang F-S, Whittam TS, Selander RK (1994) Molecular genetic basis of allelic polymorphism in malatedehydrogenase (mdh) in natural-populations ofEscherichia coli andSalmonella enterica. Proc Natl Acad Sci USA 91:1280–1284

    Google Scholar 

  • Brown AHD, Feldman MW, Nevo E (1980) Multilocus structure of natural populations ofHordeum spontanium. Genetics 96:523–536

    Google Scholar 

  • Cohan FM (1995) Does recombination constrain neutral divergence among bacterial taxa. Evolution 49:164–175

    Google Scholar 

  • Dykhuizen DE, Green L (1991) Recombination inEscherichia coli and the definition of biological species. J Bacteriol 173:7257–7268

    Google Scholar 

  • Feil E, Carpenter G, Spratt BG (1995) Electrophoretic variation in adenylate kinase ofNeisseria meningitidis is due to inter- and intra-species recombination. Proc Natl Acad Sci USA 92:10535–10539

    Google Scholar 

  • Frosch M, Meyer TF (1992) Transformation-mediated exchange of virulence determinants by co-cultivation of pathogenicNeisseria. FEMS Microbiol Lett 100:345–350

    Google Scholar 

  • Fyfe JAM, Davies JK (1990) Nucleotide sequence and expression inEscherichia coli of therecA gene ofNeisseria gonorrhoeae. Gene 93:151–156

    Google Scholar 

  • Graves JF, Biswas GD, Sparling PF (1982) Sequence-specific DNA uptake in transformation ofNeisseria gonorrhoeae. J Bacteriol 152:1071–1077

    Google Scholar 

  • Guibourdenche M, Popoff MY, Riou JY (1986) Deoxyribonucleic acid relatedness amongNeisseria gonorrhoeae, N. meningitidis, N. lactamica, N. cinerea and “Neisseria polysaccharea.” Ann Inst Pasteur Microbiol 137B:177–185

    Google Scholar 

  • Guttman DS, Dykhuizen DE (1994) Clonal divergence inEscherichia coli as a result of recombination, not mutation. Science 266:1380–1383

    Google Scholar 

  • Higuchi RG, Ochman H (1989) Production of single-stranded DNA templates by exonuclease digestion following the polymerase chain reaction. Nucleic Acids Res 17:5865

    Google Scholar 

  • Hobbs MM, Seiler A, Achtman M, Cannon JG (1994) Microevolution within a clonal population of pathogenic bacteria—recombination, gene duplication and horizontal genetic exchange in theopa gene family ofNeisseria meningitidis. Mol Microbiol 12:171–180

    Google Scholar 

  • Istock CA, Duncan KE, Ferguson N, Zhou X (1992) Sexuality in a natural population of bacteria—Bacillus subtilis challenges the clonal paradigm. Mol Ecol 1:95–103

    Google Scholar 

  • Knapp JS (1988) Historical perspectives and identification ofNeisseria and related species. Clin Microbiol Rev 1:415–431

    Google Scholar 

  • Kumar S, Tamura K, Nei M (1993) MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers. Comput Appl Biosci 10:189–191

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Google Scholar 

  • Maiden MCJ (1993) Population genetics of a transformable bacterium: the influence of horizontal genetic exchange on the biology ofNeisseria meningitidis. FEMS Microbiol Lett 112:243–250

    Google Scholar 

  • Maynard Smith J, Dowson CG, Spratt BG (1991) Localised sex in bacteria. Nature 349:29–31

    Google Scholar 

  • Maynard Smith J, Smith NH, O'Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci USA 90:4384–4388

    Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426

    Google Scholar 

  • Nelson K, Selander RK (1994) Intergeneric transfer and recombination of the 6-phosphogluconate gene (gnd) in enteric bacteria. Proc Natl Acad Sci USA 91:10227–10231

    Google Scholar 

  • Olyhoek T, Crowe BA, Achtman M (1987) Clonal population structure ofNeisseria meningitidis serogroup A isolated from epidemics and pandemics between 1915 and 1983. Rev Infect Dis 9:665–682

    Google Scholar 

  • O'Rourke M, Stevens E (1993) Genetic structure ofNeisseria gonorrhoeae populations: a non-clonal pathogen. J Gen Microbiol 139:2603–2611

    Google Scholar 

  • Reeves PR, Farnell L, Lan R (1994) Multicomp: a program for preparing sequence data for phylogenetic analysis. Comput Appl Biosci 10:281–284

    Google Scholar 

  • Roberts MS, Cohan FM (1993) The effect of DNA sequence divergence on sexual isolation inBacillus. Genetics 134:402–408

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

  • Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538

    Google Scholar 

  • Spratt BG, Zhou J (1994) Recombination in nature between chromosomal genes of pathogenic and commensalNeisseria species. In: Conde-Glez CJ, Morse S, Rice P, Sparling F, Calderon E (eds) Pathobiology and immunobiology ofNeisseriaceae. INSP, Cuernavaca, Mexico, pp 575–581

    Google Scholar 

  • Spratt BG, Bowler LD, Zhang Q-Y, Zhou J, Maynard Smith J (1992) Role of inter-species transfer of chromosomal genes in the evolution of penicillin resistance in pathogenic and commensalNeisseria species. J Mol Evol 34:115–125

    Google Scholar 

  • Spratt BG, Smith NH, Zhou J, O'Rourke M, Feil E (1995) The population genetics of the pathogenicNeisseria. In: Baumberg S, Young JPW, Wellington EMH, Saunders JR (eds) The population genetics of bacteria. SGM Symposium No. 52, Cambridge University Press, Cambridge, pp 143–160

    Google Scholar 

  • Vázquez JA, de la Fuente L, Berrón S, O'Rourke M, Smith NH, Zhou J, Spratt BG (1993) Ecological separation and genetic isolation ofNeisseria gonorrhoeae andNeisseria meningitidis. Curr Biol 3:567–572

    Google Scholar 

  • Vázquez JA, Berrón S, O'Rourke M, Carpenter G, Feil E, Smith NH, Spratt BG (1995) Interspecies recombination in nature: a meningococcus that has acquired a gonococcal PIB porin. Mol Microbiol 15:1001–1007

    Google Scholar 

  • Ward MJ, Lambden PR, Heckels JE (1992) Sequence analysis and relationships between meningococcal class 3 serotype proteins and other porins from pathogenic and non-pathogenicNeisseria species. FEMS Microbiol Lett 94:283–290

    Google Scholar 

  • Zhou J, Spratt BG (1992) Sequence diversity within theargF, fbp andrecA genes of natural isolates ofNeisseria meningitidis: interspecies recombination within theargF gene. Mol Microbiol 6:2135–2146

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Feil, E., Zhou, J., Smith, J.M. et al. A comparison of the nucleotide sequences of theadk andrecA genes of pathogenic and commensalNeisseria species: Evidence for extensive interspecies recombination withinadk . J Mol Evol 43, 631–640 (1996). https://doi.org/10.1007/BF02202111

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02202111

Key words

Navigation