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Lateral gene transfer and the nature of bacterial innovation

Nature volume 405, pages 299–304 (2000)Cite this article

Abstract

Unlike eukaryotes, which evolve principally through the modification of existing genetic information, bacteria have obtained a significant proportion of their genetic diversity through the acquisition of sequences from distantly related organisms. Horizontal gene transfer produces extremely dynamic genomes in which substantial amounts of DNA are introduced into and deleted from the chromosome. These lateral transfers have effectively changed the ecological and pathogenic character of bacterial species.

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Figure 1: Evolutionary relationships and phenotypic profiles of representative enteric bacteria.
Figure 2: Distribution of horizontally acquired (foreign) DNA in sequenced bacterial genomes.
Figure 3: Gene capture and expression by integrons.
Figure 4: Succession of genetic events contributing to virulence in Shigella .

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References

  1. Lawrence, J. G. & Ochman, H. Molecular archaeology of the Escherichia coli genome. Proc. Natl Acad. Sci. USA 95, 9413–9417 ( 1998).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  2. Davies, J. Origins and evolution of antibiotic resistance. Microbiologia 12, 9–16 (1996).

    CAS  PubMed  Google Scholar 

  3. Doolittle, W. F. Phylogenetic classification and the universal tree. Science 284, 2124–2129 (1999).

    Article  CAS  PubMed  Google Scholar 

  4. Swofford, D. L., Olsen, G. J., Wadell, P. J. & Hillis, D. M. in Molecular Systematics (eds Hillis, D. M., Moritz, C. & Mable, B. K.) 407–514 (Sinauer Associates, Sunderland, Massachusetts, 1996).

    Google Scholar 

  5. Sueoka, N. On the genetic basis of variation and heterogeneity in base composition. Proc. Natl Acad. Sci. USA 48, 582– 592 (1962).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  6. Muto, A. & Osawa, S. The guanine and cytosine content of genomic DNA and bacterial evolution. Proc. Natl Acad. Sci. USA 84, 166–169 ( 1987).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  7. Karlin, S., Campbell, A. M. & Mrázek, J. Comparative DNA analysis across diverse genomes. Annu. Rev. Genet. 32, 185–225 (1998).

    Article  CAS  PubMed  Google Scholar 

  8. Groisman, E. A., Saier, M. H. Jr & Ochman, H. Horizontal transfer of a phosphatase gene as evidence for the mosaic structure of the Salmonella genome. EMBO J. 11, 1309–1316 ( 1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Lawrence, J. G. & Ochman, H. Amelioration of bacterial genomes: rates of change and exchange. J. Mol. Evol. 44, 383–397 ( 1997).

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Lan, R. & Reeves, P. R. Gene transfer is a major factor in bacterial evolution. Mol. Biol. Evol. 13, 47–55 (1996).

    Article  CAS  PubMed  Google Scholar 

  11. Maynard Smith, J. The detection and measurement of recombination from sequence data. Genetics 153, 1021–1027 (1999).

    Google Scholar 

  12. Vulic, M., Dionisio, F., Taddei, F. & Radman, M. Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in Enterobacteria. Proc. Natl Acad. Sci. USA 94, 9763– 9767 (1997).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  13. Rayssiguier, C., Thaler, D. S. & Radman, M. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342, 396– 399 (1989).

    Article  ADS  CAS  PubMed  Google Scholar 

  14. Medigue, C., Rouxel, T., Vigier, P., Henaut, A. & Danchin, A. Evidence for horizontal gene transfer in Escherichia coli speciation. J. Mol. Biol. 222, 851–856 (1991).

    Article  CAS  PubMed  Google Scholar 

  15. Whittam, T. S. & Ake, S. in Mechanisms of Molecular Evolution (eds Takahata, N. & Clark, A. G.) 223– 246 (Japan Scientific Society Press, Tokyo, 1992).

  16. Riley, M. & Anilionis, A. Evolution of the bacterial genome. Annu. Rev. Microbiol. 32, 519– 560 (1978).

    Article  CAS  PubMed  Google Scholar 

  17. Wolf, Y. I., Aravind, L., Grishin, N. V. & Koonin, E. V. Evolution of aminoacyl-tRNA synthetases—analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res. 9, 689– 710 (1999).

    CAS  PubMed  Google Scholar 

  18. Aravind, L., Tatusov, R. L., Wolf, Y. I., Walker, D. R. & Koonin, E. V. Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends Genet. 14, 442–444 ( 1998).

    Article  CAS  PubMed  Google Scholar 

  19. Nelson, K. E. et al. Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima. Nature 399, 323–329 (1999).

    Article  ADS  CAS  PubMed  Google Scholar 

  20. Logsdon, J. M. Jr & Fuguy, D. M. Thermotoga heats up lateral gene transfer. Curr. Biol. 9, R747–R751 (1999).

    Article  CAS  PubMed  Google Scholar 

  21. Gaasterland, T. Archaeal genomics. Curr. Opin. Microbiol. 2, 542–547 (1999).

    Article  CAS  PubMed  Google Scholar 

  22. Dubnau, D. DNA uptake in bacteria. Annu. Rev. Microbiol. 53, 217–244 (1999).

    Article  CAS  PubMed  Google Scholar 

  23. Goodman, S. D. & Scocca, J. J. Identification and arrangement of the DNA sequence recognized in specific transformation of Neisseria gonorrhoeae. Proc. Natl Acad. Sci. USA 85, 6982–6986 (1988).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  24. Elkins, C., Thomas, C. E., Seifert, H. S. & Sparling, P. F. Species-specific uptake of DNA by gonococci is mediated by a 10-base-pair sequence. J. Bacteriol. 173, 3911– 3913 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Smith, H. O., Tomb, J. -F., Dougherty, B. A., Fleischmann, R. D. & Venter, J. C. Frequency and distribution of DNA uptake signal sequences in the Haemophilus influenzae Rd genome. Science 269, 538– 540 (1985).

    Article  ADS  Google Scholar 

  26. Davison, J. Genetic exchange between bacteria in the environment. Plasmid 42, 73–91 (1999).

    Article  CAS  PubMed  Google Scholar 

  27. Jiang, S. C. & Paul, J. H. Gene transfer by transduction in the marine environment. Appl. Environ. Microbiol. 64 , 2780–2787 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Schicklmaier, P. & Schmieger, H. Frequency of generalized transducing phages in natural isolates of the Salmonella typhimurium complex. Appl. Environ. Microbiol. 61, 1637–1640 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Buchanan-Wollaston, V., Passiatore, J. E. & Canon, F. The mob and oriT mobilization functions of a bacterial plasmid promote its transfer to plants. Nature 328, 170–175 (1987).

    Article  ADS  Google Scholar 

  30. Heinemann, J. A. & Sprague, G. F. J. Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature 340, 205–209 ( 1989).

    Article  ADS  CAS  PubMed  Google Scholar 

  31. Ricchetti, M., Fairhead, C. & Dujon, B. Mitochondrial DNA repairs double-strand breaks in yeast chromosomes. Nature 402, 96– 100 (1999).

    Article  ADS  CAS  PubMed  Google Scholar 

  32. Kleckner, N. in Mobile DNA (eds Berg, D. E. & Howe, M. M.) 227– 268 (American Society for Microbiology, Washington DC, 1989).

    Google Scholar 

  33. Berg, D. E. in Mobile DNA (eds Berg, D. E. & Howe, M. M.) 185– 210 (American Society for Microbiology, Washington DC. 1989).

    Google Scholar 

  34. Hall, R. M. Mobile gene cassettes and integrons: moving antibiotic resistance genes in Gram-negative bacteria. CIBA Found. Symp. 207, 192–205 (1997).

    CAS  PubMed  Google Scholar 

  35. Rowe-Magnus, D. A. & Mazel, D. Resistance gene capture. Curr. Opin. Microbiol. 2, 483– 488 (1999).

    Article  CAS  PubMed  Google Scholar 

  36. Hall, R. M. & Collis, C. M. Mobile gene cassettes and integrons: capture and spread of genes by site-specific recombination. Mol. Microbiol. 15, 593–600 ( 1995).

    Article  CAS  PubMed  Google Scholar 

  37. Mazel, D., Dychinco, B., Webb, V. A. & Davies, J. A distinctive class of integron in the Vibrio cholerae genome. Science 280, 605–608 ( 1998).

    Article  ADS  CAS  PubMed  Google Scholar 

  38. Portnoy, D. A., Moseley, S. L. & Falkow, S. Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Infect. Immun. 31, 775–782 ( 1981).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Maurelli, A. T., Baudry, B., d’Hauteville, H., Hale, T. L. & Sansonetti, P. J. Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri. Infect. Immun. 49, 164–171 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Sasakawa, C. et al. Virulence-associated genetic regions comprising 31 kilobases of the 230-kilobase plasmid in Shigella flexneri 2a. J. Bacteriol. 170, 2480–2484 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Gemski, P., Lazere, J. R., Casey, T. & Wohlhieter, J. A. Presence of virulence-associated plasmid in Yersinia pseudotuberculosis. Infect. Immun. 28, 1044–1047 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Isberg, R. R. & Falkow, S. A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature 317, 19–25 (1985).

    Article  Google Scholar 

  43. McDaniel, T. K. & Kaper, J. B. A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol. Microbiol. 23, 399–407 ( 1997).

    Article  CAS  PubMed  Google Scholar 

  44. Groisman, E. A. & Ochman, H. Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87, 791–794 (1996).

    Article  CAS  PubMed  Google Scholar 

  45. Hacker, J., Blum-Oehler, G., Muhldorfer, I. & Tschape, H. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol. Microbiol. 23, 1089–1097 (1997).

    Article  CAS  PubMed  Google Scholar 

  46. Ritter, A. et al. tRNA genes and pathogenicity islands: influence on virulence and metabolic properties of uropathogenic Escherichia coli. Mol. Microbiol. 17, 109–121 (1995).

    Article  CAS  PubMed  Google Scholar 

  47. Blum, G et al. Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect. Immun. 62, 606– 614 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Moss, J. E., Cardozo, T. J., Zychlinsky, A. & Groisman, E. A. The selC-associated SHI-2 pathogenicity island of Shigella flexneri . Mol. Microbiol. 33, 74– 83 (1999).

    Article  CAS  PubMed  Google Scholar 

  49. Vokes, S. A., Reeves, S. A., Torres, A. G. & Payne, S. M. The aerobactin iron transport system genes in Shigella flexneri are present within a pathogenicity island. Mol. Microbiol. 33, 63–73 (1999).

    Article  CAS  PubMed  Google Scholar 

  50. Blanc-Potard, A. B. & Groisman, E. A. The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J. 16, 5376– 5385 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Sun, J., Inouye, M. & Inouye, S. Association of a retroelement with a P4-like cryptic prophage (retronphage Theta;R73) integrated into the selenocystyl-tRNA gene of Escherichia coli. J. Bacteriol. 173, 171–181 (1991).

    Google Scholar 

  52. Cheetham, B. F. & Katz, M. E. A role for bacteriophages in the evolution and transfer of bacterial virulence determinants. Mol. Microbiol. 18, 201–208 (1995).

    Article  CAS  PubMed  Google Scholar 

  53. Lindsay, J. A., Ruzin, A., Ross, H. F., Kurepina, N. & Novick, R. P. The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol. Microbiol. 29, 527–543 (1998).

    Article  CAS  PubMed  Google Scholar 

  54. Weeks, C. R. & Ferretti, J. J. The gene for type A streptococcal exotoxin (erythrogenic toxin) is located in bacteriophage T12. Infect. Immun. 46, 531–536 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Jackson, M. P., Neill, R. J., O'Brien, A. D., Holmes, R. K. & Newland, J. W. Nucleotide sequence analysis and comparison of the structural genes for Shiga-like toxin-I and Shiga-like toxin II encoded by bacteriophages from Escherichia coli. FEMS Microbiol. Lett. 44, 109–114 (1987).

    Article  CAS  Google Scholar 

  56. Mirold, S. Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc. Natl Acad. Sci. USA 96, 9845–9850.

  57. Waldor, M. K. & Mekalanos, J. J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910–1914 (1996).

    Article  ADS  CAS  PubMed  Google Scholar 

  58. Karaolis, D. K., Somara, S., Maneval, D. R. J., Johnson, J. A. & Kaper, J. B. A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature 399, 675–679 ( 1999).

    Article  Google Scholar 

  59. Nakata, N. et al. The absence of a surface protease, OmpT, determines the intercellular spreading ability of Shigella: the relationship between the ompT and kcpA loci. Mol. Microbiol. 9, 459–468 (1993).

    Article  CAS  PubMed  Google Scholar 

  60. Maurelli, A. T., Fernández, R. E., Bloch, C. A., Rode, C. K. & Fasano, A. “Black holes” and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc. Natl Acad. Sci. USA 95, 3943– 3948 (1998).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  61. Riley, M. & Sanderson, K. E. in The Bacterial Chromosome (eds Riley, M. & Drlica, K.) 85–96 (American Society for Microbiology, Washington DC, 1990).

    Google Scholar 

  62. Lawrence, J. G. & Roth, J. R. Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics 143, 1843–1860 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Wolf, Y. I., Aravind, L. & Koonin, E. V. Rickettsiae and Chlamydia: evidence of horizontal gene transfer and gene exchange. Trends Genet. 14, 442–444 (1998).

    Article  PubMed  Google Scholar 

  64. Groisman, E. A. & Ochman, H. How Salmonella became a pathogen. Trends Microbiol. 5, 343–349 (1997).

    Article  CAS  PubMed  Google Scholar 

  65. Groisman, E. A. The ins and outs of virulence gene expression: Mg2+ as a regulatory signal. Bioessays 20, 96– 101 (1998).

    Article  CAS  PubMed  Google Scholar 

  66. Deiwick, J., Nikolaus, T., Erdogan, S. & Hensel, M. Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol. Microbiol. 31, 1759– 1773 (1999).

    Article  CAS  PubMed  Google Scholar 

  67. Casjens, S. The diverse and dynamic structure of bacterial genomes. Annu. Rev. Genet. 32, 339–377 ( 1998).

    Article  CAS  PubMed  Google Scholar 

  68. Andersson, S. G. E. & Kurland, C. G. Reductive evolution of resident genomes. Trends Microbiol. 6, 263–268 (1998).

    Article  CAS  PubMed  Google Scholar 

  69. Andersson, J. O. & Andersson, S. G. E. Insights into the evolutionary process of genome degradation. Curr. Opin. Genet. Dev. 9, 664–671 ( 1999).

    Article  CAS  PubMed  Google Scholar 

  70. Lawrence, J. G. Gene transfer, speciation, and the evolution of bacterial genomes. Curr. Opin. Microbiol. 2, 519–523 (1999).

    Article  CAS  PubMed  Google Scholar 

  71. Lawrence, J. G. & Roth, J. R. in Organization of the Prokaryotic Genome (ed. Charlebois, R. L.) 263– 289 (American Society for Microbiology, Washington, DC, 1999).

    Book  Google Scholar 

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, 85721-0088, Arizona, USA

    Howard Ochman

  2. Department of Biological Sciences, University of Pittsburgh, Pittsburgh, 15260, Pennsylvania, USA

    Jeffrey G. Lawrence

  3. Department of Molecular Microbiology, Howard Hughes Medical Institute, Washington University School of Medicine, St Louis, 63110, Missouri, USA

    Eduardo A. Groisman

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  2. Jeffrey G. Lawrence
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  3. Eduardo A. Groisman
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Ochman, H., Lawrence, J. & Groisman, E. Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304 (2000). https://doi.org/10.1038/35012500

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