1887

Abstract

Acquisition of genetic information through horizontal gene transfer (HGT) is an important evolutionary process by which micro-organisms gain novel phenotypic characteristics. In pathogenic bacteria, for example, it facilitates maintenance and enhancement of virulence and spread of drug resistance. In the genus , to which several primary human pathogens belong, HGT has not been clearly demonstrated. The few existing reports suggesting this process are based on circumstantial evidence of similarity of sequences found in distantly related species. Here, direct evidence of HGT between strains of representing two different serotypes is presented. Conflicting evolutionary histories of genes encoding elements of the glycopeptidolipid (GPL) biosynthesis pathway led to an analysis of the GPL cluster genomic sequences from four strains. The sequence of strain 2151 appeared to be a mosaic consisting of three regions having alternating identities to either strains 724 or 104. Maximum-likelihood estimation of two breakpoints allowed a ∼4100 bp region horizontally transferred into the strain 2151 genome to be pinpointed with confidence. The maintenance of sequence continuity at both breakpoints and the lack of insertional elements at these sites strongly suggest that the integration of foreign DNA occurred by homologous recombination. To our knowledge, this is the first report to demonstrate naturally occurring homologous recombination in . This previously undiscovered mechanism of genetic exchange may have major implications for the understanding of pathogenesis.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27088-0
2004-06-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/6/mic1501707.html?itemId=/content/journal/micro/10.1099/mic.0.27088-0&mimeType=html&fmt=ahah

References

  1. Aldovini A., Husson R. N., Young R. A. 1993; The uraA locus and homologous recombination in Mycobacterium bovis. BCG. J Bacteriol 175:7282–7289
    [Google Scholar]
  2. Balasubramanian V., Pavelka M. S. J., Bardarov S. S., Martin J., Weisbrod T. R., McAdam R. A., Bloom B. R., Jacobs W. R., Jr. 1996; Allelic exchange in Mycobacterium tuberculosis with long linear recombination substrates. J Bacteriol 178:273–279
    [Google Scholar]
  3. Bardarov S., Kriakov J., Carriere C.7 other authors 1997; Conditionally replicating mycobacteriophages: a system for transposon delivery to Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 94:10961–10966 [CrossRef]
    [Google Scholar]
  4. Bhatt A., Kieser H. M., Melton R. E., Kieser T. 2002; Plasmid transfer from Streptomyces to Mycobacterium smegmatis by spontaneous transformation. Mol Microbiol 43:135–146 [CrossRef]
    [Google Scholar]
  5. Boshoff H. I., Reed M. B., Barry C. E. 2003; DnaE2 polymerase contributes to in vivo survival and the emergence of drug resistance inMycobacterium tuberculosis. Cell 113:183–193 [CrossRef]
    [Google Scholar]
  6. Braden C. R., Morlock G. P., Woodley C. L.7 other authors 2001; Simultaneous infection with multiple strains of Mycobacterium tuberculosis. Clin Infect Dis 33:42–47 [CrossRef]
    [Google Scholar]
  7. David H. L., Newman C. M. 1971; Some observations on the genetics of isoniazid resistance in the tubercle bacilli. Am Rev Respir Dis 104:508–515
    [Google Scholar]
  8. Davis E. O., Sedgwick S. G., Colston M. J. 1991; Novel structure of the recA locus of Mycobacterium tuberculosis implies processing of the gene product. J Bacteriol 173:5653–5662
    [Google Scholar]
  9. Davis E. O., Jenner P. J., Brooks P. C., Colston M. J., Sedgwick S. G. 1992; Protein splicing in the maturation of M. tuberculosis RecA protein: a mechanism for tolerating a novel class of intervening sequence. Cell 71:201–210 [CrossRef]
    [Google Scholar]
  10. Espinal M. A., Kim S. J., Suarez P. G.7 other authors 2000; Standard short-course chemotherapy for drug-resistant tuberculosis: treatment outcomes in 6 countries. JAMA 283:2537–2545 [CrossRef]
    [Google Scholar]
  11. Gamieldien J., Ptitsyn A., Hide W. 2002; Eukaryotic genes in Mycobacterium tuberculosis could have a role in pathogenesis and immunomodulation. Trends Genet 18:5–8 [CrossRef]
    [Google Scholar]
  12. Gordon S. V., Heym B., Parkhill J., Barrell B., Cole S. T. 1999; New insertion sequences and a novel repeated sequence in the genome of Mycobacterium tuberculosis H37Rv. Microbiology 145:881–892 [CrossRef]
    [Google Scholar]
  13. Gormley E. P., Davies J. 1991; Transfer of plasmid RSF1010 by conjugation from Escherichia coli to Streptomyces lividans and Mycobacterium smegmatis. J Bacteriol 173:6705–6708
    [Google Scholar]
  14. Hatfull G. F., Jacobs W. R. J. 1994; Mycobacteriophages: cornerstones of mycobacterial research. In Tuberculosis: Pathogenesis, Protection and Control pp 165–183 Edited by Bloom B. R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  15. Hellyer T. J., Brown I. N., Dale J. W., Easmon C. S. 1991; Plasmid analysis of Mycobacterium avium-intracellulare (MAI) isolated in the United Kingdom from patients with and without AIDS. J Med Microbiol 34:225–231 [CrossRef]
    [Google Scholar]
  16. Holmes E. C., Worobey M., Rambaut A. 1999; Phylogenetic evidence for recombination in dengue virus. Mol Biol Evol 16:405–409 [CrossRef]
    [Google Scholar]
  17. Howard S. T., Byrd T. F., Lyons C. R. 2002; A polymorphic region in Mycobacterium abscessus contains a novel insertion sequence element. Microbiology 148:2987–2996
    [Google Scholar]
  18. Husson R. N., James B. E., Young R. A. 1990; Gene replacement and expression of foreign DNA in mycobacteria. J Bacteriol 172:519–524
    [Google Scholar]
  19. Jucker M. T., Falkinham J. O. 1990; Epidemiology of infection by nontuberculous mycobacteria IX. Evidence for two DNA homology groups among small plasmids in Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum. Am Rev Respir Dis 142:858–862 [CrossRef]
    [Google Scholar]
  20. Kinsella R. J., McInerney J. O. 2003; Eukaryotic genes in Mycobacterium tuberculosis? Possible alternative explanations. Trends Genet 19:687–689 [CrossRef]
    [Google Scholar]
  21. Kinsella R. J., Fitzpatrick D. A., Creevey C. J., McInerney J. O. 2003; Fatty acid biosynthesis in Mycobacterium tuberculosis: lateral gene transfer, adaptive evolution, and gene duplication. Proc Natl Acad Sci U S A 100:10320–10325 [CrossRef]
    [Google Scholar]
  22. Kirby C., Waring A., Griffin T. J., Falkinham J. O. 2002; Cryptic plasmids of Mycobacterium avium: Tn552 to the rescue. Mol Microbiol 43:173–186 [CrossRef]
    [Google Scholar]
  23. Krzywinska E., Schorey J. S. 2003; Characterization of genetic differences between Mycobacterium avium subsp.avium strains of diverse virulence with a focus on the glycopeptidolipid biosynthesis cluster. Vet Microbiol 91:249–264 [CrossRef]
    [Google Scholar]
  24. Krzywinska E., Krzywinski J., Schorey J. S. 2004; Phylogeny of Mycobacterium avium strains inferred from glycopeptidolipid biosynthesis pathway genes. Microbiology 150:1699–1706 [CrossRef]
    [Google Scholar]
  25. Kulakova A. N., Larkin M. J., Kulakov L. A. 1997; The plasmid-located haloalkane dehalogenase gene from Rhodococcus rhodochrous NCIMB13064. Microbiology 143:109–115 [CrossRef]
    [Google Scholar]
  26. Kumar S., Tamura K., Jakobsen I. B., Nei M. 2001; MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245 [CrossRef]
    [Google Scholar]
  27. Le Dantec C., Winter N., Gicquel B., Vincent V., Picardeau M. 2001; Genomic sequence and transcriptional analysis of a 23-kilobase mycobacterial linear plasmid: evidence for horizontal transfer and identification of plasmid maintenance systems. J Bacteriol 183:2157–2164 [CrossRef]
    [Google Scholar]
  28. Maslow J. N., Irani V. R., Lee S. H., Eckstein T. M., Inamine J. M., Belisle J. T. 2003; Biosynthetic specificity of the rhamnosyltransferase gene of Mycobacterium avium serovar 2 as determined by allelic exchange mutagenesis. Microbiology 149:3193–3202 [CrossRef]
    [Google Scholar]
  29. McFadden J. 1996; Recombination in mycobacteria. Mol Microbiol 21:205–211 [CrossRef]
    [Google Scholar]
  30. Meissner P. S., Falkinham J. O. 3rd (1986; Plasmid DNA profiles as epidemiological markers for clinical and environmental isolates of Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum. J Infect Dis 153:325–331 [CrossRef]
    [Google Scholar]
  31. Morschhauser J., Kohler G., Ziebuhr W., Blum-Oehler G., Dobrindt U., Hacker J. 2000; Evolution of microbial pathogens. Philos Trans R Soc Lond B Biol Sci 355:695–704 [CrossRef]
    [Google Scholar]
  32. Musser J. M. 1995; Antimicrobial agent resistance in mycobacteria: molecular genetic insights. Clin Microbiol Rev 8:496–514
    [Google Scholar]
  33. Ochman H. 2001; Lateral and oblique gene transfer. Curr Opin Genet Dev 11:616–619 [CrossRef]
    [Google Scholar]
  34. Ochman H., Lawrence J. G., Groisman E. A. 2000; Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304 [CrossRef]
    [Google Scholar]
  35. Otero J., Jacobs W. R. J., Glickman M. S. 2003; Efficient allelic exchange and transposon mutagenesis in Mycobacterium avium by specialized transduction. Appl Environ Microbiol 69:5039–5044 [CrossRef]
    [Google Scholar]
  36. Papavinasasundaram K. G., Colston M. J., Davis E. O. 1998; Construction and complementation of a recA deletion mutant of Mycobacterium smegmatis reveals that the intein in Mycobacterium tuberculosis recA does not affect RecA function. Mol Microbiol 30:525–534 [CrossRef]
    [Google Scholar]
  37. Parsons L. M., Jankowski C. S., Derbyshire K. M. 1998; Conjugal transfer of chromosomal DNA in Mycobacterium smegmatis. Mol Microbiol 28:571–582 [CrossRef]
    [Google Scholar]
  38. Pavelka M. S. J., Jacobs W. R. J. 1999; Comparison of the construction of unmarked deletion mutations in Mycobacterium smegmatis, Mycobacterium bovis bacillus Calmette-Guerin, and Mycobacterium tuberculosis H37Rv by allelic exchange. J Bacteriol 181:4780–4789
    [Google Scholar]
  39. Pedulla M. L., Ford M. E., Houtz J. M.17 other authors 2003; Origins of highly mosaic mycobacteriophage genomes. Cell 113:171–182 [CrossRef]
    [Google Scholar]
  40. Poelarends G. J., Kulakov L. A., Larkin M. J., van Hylckama Vlieg J. E., Janssen D. B. 2000; Roles of horizontal gene transfer and gene integration in evolution of 1,3-dichloropropene- and 1,2-dibromoethane-degradative pathways. J Bacteriol 182:2191–2199 [CrossRef]
    [Google Scholar]
  41. Ragan M. A. 2001; Detection of lateral gene transfer among microbial genomes. Curr Opin Genet Dev 11:620–626 [CrossRef]
    [Google Scholar]
  42. Rambaut A., Grassly N. C. 1997; Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Comput Appl Biosci 13:235–238
    [Google Scholar]
  43. Smith N. H., Dale J., Inwald J., Palmer S., Gordon S. V., Hewinson R. G., Smith J. M. 2003; The population structure of Mycobacterium bovis in Great Britain: clonal expansion. Proc Natl Acad Sci U S A 100:15271–15275 [CrossRef]
    [Google Scholar]
  44. Snider D. E. J. 1994; Global burden of tuberculosis. In Tuberculosis: Pathogenesis, Protection, and Control pp . 3–59 Edited by Bloom B. R. Washington DC: American Society for Microbiology;
    [Google Scholar]
  45. Stinear T. P., Mve-Obiang A., Small P. L. C.12 other authors 2004; Giant plasmid-encoded polyketide synthases produce the macrolide toxin of Mycobacterium ulcerans. Proc Natl Acad Sci U S A 101:1345–1349 [CrossRef]
    [Google Scholar]
  46. Supply P., Warren R. M., Banuls A. L.6 other authors 2003; Linkage disequilibrium between minisatellite loci supports clonal evolution of Mycobacterium tuberculosis in a high tuberculosis incidence area. Mol Microbiol 47:529–538 [CrossRef]
    [Google Scholar]
  47. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882 [CrossRef]
    [Google Scholar]
  48. Tsukamura M., Hashimoto H., Noda Y. 1960; Transformation of isoniazid and streptomycin resistance in Mycobacterium avium by desoxyribonucleate derived from isoniazid- and streptomycin-double-resistant cultures. Am Rev Respir Dis 81:403–406
    [Google Scholar]
  49. von Reyn C. F., Jacobs N. J. R., Arbeit D., Maslow J. N., Niemczyk S. 1995; Polyclonal Mycobacterium avium infections in patients with AIDS: variations in antimicrobial susceptibilities of different strains ofM. avium isolated from the same patient. J Clin Microbiol 33:1008–1010
    [Google Scholar]
  50. Walker G. C. 1984; Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Rev 48:60–93
    [Google Scholar]
  51. Weigel L. M., Clewell D. B., Gill S. R.7 other authors 2003; Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science 302:1569–1571 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27088-0
Loading
/content/journal/micro/10.1099/mic.0.27088-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error