1887

Abstract

The bacterial genome projects have suggested a central role for horizontal transfer in bacterial adaptation, but it is difficult to rule out an adaptive role for ordinary genetic change in existing genes. The bacterial systematics literature can readily address the importance of gene acquisition in adaptive evolution, since phenotypic characterization typically assesses presence versus absence of metabolic capabilities, and metabolic gains and losses are most likely due to horizontal transfer and/or gene loss. Bacterial systematists have not geared their studies toward quantitative differences in metabolic capabilities, which are more likely to involve adjustments of existing genes. Here, quantitative variation in metabolism within and between three closely related taxa has been assayed. While these taxa show no qualitative (i.e. presence versus absence) differences in resource utilization, they are quantitatively different in utilization of 8 % of 95 resources tested. Moreover, 93 % of the resources tested showed significant quantitative variation among strains within a single taxon. These results suggest that ordinary genetic changes in existing genes may play an important role in adaptation. If these results are typical, future genomically based assays of quantitative variation in phenotype (e.g. microarray analysis of mRNA concentrations) may identify hundreds of genes whose expression has been modified. A protocol is presented for identifying those modifications of gene expression and those gene acquisitions that are most likely to have played a role in adaptive evolution.

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2003-12-01
2019-11-15
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References

  1. Achtman, M., van der Ende, A., Zhu, P. & 8 other authors ( 2001; ). Molecular epidemiology of serogroup a meningitis in Moscow, 1969 to 1997. Emerg Infect Dis 7, 420–427.[CrossRef]
    [Google Scholar]
  2. Akashi, H. & Gojobori, T. ( 2002; ). Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci U S A 99, 3695–3700.[CrossRef]
    [Google Scholar]
  3. Alm, R. A., Ling, L. S., Moir, D. T. & 20 other authors ( 1999; ). Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397, 176–180.[CrossRef]
    [Google Scholar]
  4. Baba, T., Takeuchi, F., Kuroda, M. & 11 other authors ( 2002; ). Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359, 1819–1827.[CrossRef]
    [Google Scholar]
  5. Baumler, A. J., Gilde, A. J., Tsolis, R. M., van der Velden, A. W., Ahmer, B. M. & Heffron, F. ( 1997; ). Contribution of horizontal gene transfer and deletion events to development of distinctive patterns of fimbrial operons during evolution of Salmonella serotypes. J Bacteriol 179, 317–322.
    [Google Scholar]
  6. Beres, S. B., Sylva, G. L., Barbian, K. D. & 13 other authors ( 2002; ). Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc Natl Acad Sci U S A 99, 10078–10083.[CrossRef]
    [Google Scholar]
  7. Bochner, B. R. ( 1989; ). Sleuthing out bacterial identities. Nature 339, 157–158.[CrossRef]
    [Google Scholar]
  8. Bouma, J. E. & Lenski, R. E. ( 1988; ). Evolution of a bacteria/plasmid association. Nature 335, 351–352.[CrossRef]
    [Google Scholar]
  9. Cavalieri, D., Townsend, J. P. & Hartl, D. L. ( 2000; ). Manifold anomalies in gene expression in a vineyard isolate of Saccharomyces cerevisiae revealed by DNA microarray analysis. Proc Natl Acad Sci U S A 97, 12369–12374.[CrossRef]
    [Google Scholar]
  10. Chan, M. S., Maiden, M. C. & Spratt, B. G. ( 2001; ). Database-driven multi locus sequence typing (MLST) of bacterial pathogens. Bioinformatics 17, 1077–1083.[CrossRef]
    [Google Scholar]
  11. Cohan, F. M. ( 1994a; ). The effects of rare but promiscuous genetic exchange on evolutionary divergence in prokaryotes. Am Nat 143, 965–986.[CrossRef]
    [Google Scholar]
  12. Cohan, F. M. ( 1994b; ). Genetic exchange and evolutionary divergence in prokaryotes. Trends Ecol Evol 9, 175–180.[CrossRef]
    [Google Scholar]
  13. Cohan, F. M. ( 2002a; ). Clonal structure: an overview. In Encyclopedia of Evolution, pp. 159–161. Edited by M. Pagel. New York: Oxford University Press.
  14. Cohan, F. M. ( 2002b; ). What are bacterial species? Annu Rev Microbiol 56, 457–487.[CrossRef]
    [Google Scholar]
  15. Cohan, F. M. ( 2002c; ). Population structure and clonality of bacteria. In Encyclopedia of Evolution, pp. 161–163. Edited by M. Pagel. New York: Oxford University Press.
  16. Cohan, F. M. ( 2004; ). Periodic selection and ecological diversity in bacteria. In Selective Sweep. Edited by D. Nurminsky. Georgetown, Texas: Landes Bioscience.
  17. Cohan, F. M., King, E. C. & Zawadzki, P. ( 1994; ). Amelioration of the deleterious pleiotropic effects of an adaptive mutation in Bacillus subtilis. Evolution 48, 81–95.[CrossRef]
    [Google Scholar]
  18. Cooper, T. F., Rozen, D. E. & Lenski, R. E. ( 2003; ). Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc Natl Acad Sci U S A 100, 1072–1077.[CrossRef]
    [Google Scholar]
  19. Dillon, W. R. M. G. ( 1984; ). Multivariate Analysis: Methods and Applications. Chichester: Wiley.
  20. Duncan, K. E., Ferguson, N., Kimura, K., Zhou, X. & Istock, C. A. ( 1994; ). Fine-scale genetic and phenotypic structures in natural populations of Bacillus subtilis and Bacillus licheniformis: important implications for bacterial evolution and speciation. Evolution 48, 2002–2025.[CrossRef]
    [Google Scholar]
  21. Dykhuizen, D. E. ( 1998; ). Santa Rosalia revisited: why are there so many species of bacteria? Antonie Van Leeuwenhoek 73, 25–33.[CrossRef]
    [Google Scholar]
  22. Feil, E. J., Maiden, M. C., Achtman, M. & Spratt, B. G. ( 1999; ). The relative contributions of recombination and mutation to the divergence of clones of Neisseria meningitidis. Mol Biol Evol 16, 1496–1502.[CrossRef]
    [Google Scholar]
  23. Feil, E. J., Smith, J. M., Enright, M. C. & Spratt, B. G. ( 2000; ). Estimating recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. Genetics 154, 1439–1450.
    [Google Scholar]
  24. Feldgarden, M., Brisson, D., Stoebel, D. M. & Dykhuizen, D. E. ( 2003; ). Size doesn't matter: microbial selection experiments address ecological phenomena. Ecology 84, 1679–1687.[CrossRef]
    [Google Scholar]
  25. Ferea, T. L., Botstein, D., Brown, P. O. & Rosenzweig, R. F. ( 1999; ). Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc Natl Acad Sci U S A 96, 9721–9726.[CrossRef]
    [Google Scholar]
  26. Hall, B. G. ( 1999; ). Experimental evolution of Ebg enzyme provides clues about the evolution of catalysis and to evolutionary potential. FEMS Microbiol Lett 174, 1–8.[CrossRef]
    [Google Scholar]
  27. Hall, B. G. & Malik, H. S. ( 1998; ). Determining the evolutionary potential of a gene. Mol Biol Evol 15, 1055–1061.[CrossRef]
    [Google Scholar]
  28. Hamilton, B. A. ( 2002; ). Variations in abundance: genome-wide responses to genetic variation and vice versa. Genome Biol 3, reviews1029.
    [Google Scholar]
  29. Holt, R. D. ( 1987; ). On the relationship between niche overlap and competition: the effect of incommensurable niche dimensions. Oikos 48, 110–114.[CrossRef]
    [Google Scholar]
  30. Istock, C. A., Bell, J. A., Ferguson, N. & Istock, N. L. ( 1996; ). Bacterial species and evolution: theoretical and practical perspectives. J Ind Microbiol 17, 137–150.[CrossRef]
    [Google Scholar]
  31. Johnson, J. ( 1973; ). Use of nucleic-acid homologies in the taxonomy of anaerobic bacteria. Int J Syst Bacteriol 23, 308–315.[CrossRef]
    [Google Scholar]
  32. Katz, L. & Burge, C. B. ( 2003; ). Widespread selection for local RNA secondary structure in coding regions of bacterial genes. Genome Res 13, 2042–2051.[CrossRef]
    [Google Scholar]
  33. Keim, P. & Smith, K. L. ( 2002; ). Bacillus anthracis evolution and epidemiology. Curr Top Microbiol Immunol 271, 21–32.
    [Google Scholar]
  34. Klevytska, A. M., Price, L. B., Schupp, J. M., Worsham, P. L., Wong, J. & Keim, P. ( 2001; ). Identification and characterization of variable-number tandem repeats in the Yersinia pestis genome. J Clin Microbiol 39, 3179–3185.[CrossRef]
    [Google Scholar]
  35. Koch, A. L. ( 1974; ). The pertinence of the periodic selection phenomenon to prokaryote evolution. Genetics 77, 127–142.
    [Google Scholar]
  36. Kunst, F., Ogasawara, N., Moszer, I. & 148 other authors ( 1997; ). The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390, 249–256.[CrossRef]
    [Google Scholar]
  37. Lan, R. & Reeves, P. R. ( 1996; ). Gene transfer is a major factor in bacterial evolution. Mol Biol Evol 13, 47–55.[CrossRef]
    [Google Scholar]
  38. Lawrence, J. G. ( 1997; ). Selfish operons and speciation by gene transfer. Trends Microbiol 5, 355–359.[CrossRef]
    [Google Scholar]
  39. Lawrence, J. G. ( 1999; ). Gene transfer, speciation, and the evolution of bacterial genomes. Curr Opin Microbiol 2, 519–523.[CrossRef]
    [Google Scholar]
  40. Lawrence, J. G. ( 2002; ). Gene transfer in bacteria: speciation without species? Theor Popul Biol 61, 449–460.[CrossRef]
    [Google Scholar]
  41. Levin, B. R. ( 1981; ). Periodic selection, infectious gene exchange and the genetic structure of E. coli populations. Genetics 99, 1–23.
    [Google Scholar]
  42. Lunzer, M., Natarajan, A., Dykhuizen, D. E. & Dean, A. M. ( 2002; ). Enzyme kinetics, substitutable resources and competition: from biochemistry to frequency-dependent selection in lac. Genetics 162, 485–499.
    [Google Scholar]
  43. Maiden, M. C., Bygraves, J. A., Feil, E. & 10 other authors ( 1998; ). Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95, 3140–3145.[CrossRef]
    [Google Scholar]
  44. Maynard Smith, J. M., Dowson, C. G. & Spratt, B. G. ( 1991; ). Localized sex in bacteria. Nature 349, 29–31.[CrossRef]
    [Google Scholar]
  45. Maynard Smith, J., Smith, N. H., O'Rourke, M. & Spratt, B. G. ( 1993; ). How clonal are bacteria? Proc Natl Acad Sci U S A 90, 4384–4388.[CrossRef]
    [Google Scholar]
  46. Nakamura, L. K. ( 1998; ). Bacillus pseudomycoides sp. nov. Int J Syst Bacteriol 48, 1031–1035.[CrossRef]
    [Google Scholar]
  47. Nakamura, L. K., Roberts, M. S. & Cohan, F. M. ( 1999; ). Relationship of Bacillus subtilis clades associated with strains 168 and W23: a proposal for Bacillus subtilis subsp. subtilis subsp. nov. and Bacillus subtilis subsp. spizizenii subsp. nov. Int J Syst Bacteriol 49, 1211–1215.[CrossRef]
    [Google Scholar]
  48. Ochman, H. & Groisman, E. A. ( 1996; ). Distribution of pathogenicity islands in Salmonella spp. Infect Immun 64, 5410–5412.
    [Google Scholar]
  49. 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]
  50. Oleksiak, M. F., Churchill, G. A. & Crawford, D. L. ( 2002; ). Variation in gene expression within and among natural populations. Nat Genet 32, 261–266.[CrossRef]
    [Google Scholar]
  51. Palys, T., Nakamura, L. K. & Cohan, F. M. ( 1997; ). Discovery and classification of ecological diversity in the bacterial world: the role of DNA sequence data. Int J Syst Bacteriol 47, 1145–1156.[CrossRef]
    [Google Scholar]
  52. Perna, N. T., Plunkett, G., 3rd, Burland, V. & 25 other authors ( 2001; ). Genome sequence of enterohaemorrhagic Escherichia coli O157 : H7. Nature 409, 529–533.[CrossRef]
    [Google Scholar]
  53. Rainey, P. B. & Travisano, M. ( 1998; ). Adaptive radiation in a heterogeneous environment. Nature 394, 69–72.[CrossRef]
    [Google Scholar]
  54. Rice, W. R. ( 1989; ). Analyzing tables of statistical tests. Evolution 43, 223–225.[CrossRef]
    [Google Scholar]
  55. Roberts, M. S. & Cohan, F. M. ( 1995; ). Recombination and migration rates in natural populations of Bacillus subtilis and Bacillus mojavensis. Evolution 49, 1081–1094.[CrossRef]
    [Google Scholar]
  56. Roberts, M. S., Nakamura, L. K. & Cohan, F. M. ( 1994; ). Bacillus mojavensis sp. nov., distinguishable from Bacillus subtilis by sexual isolation, divergence in DNA sequence, and differences in fatty acid composition. Int J Syst Bacteriol 44, 256–264.[CrossRef]
    [Google Scholar]
  57. Roberts, M. S., Nakamura, L. K. & Cohan, F. M. ( 1996; ). Bacillus vallismortis sp. nov., a close relative of Bacillus subtilis, isolated from soil in Death Valley, California. Int J Syst Bacteriol 46, 470–475.[CrossRef]
    [Google Scholar]
  58. Rozen, D. E. & Lenski, R. E. ( 2000; ). Long-term experimental evolution in Escherichia coli. VIII. Dynamics of a balanced polymorphism. Am Nat 155, 24–35.[CrossRef]
    [Google Scholar]
  59. Schrag, S. J., Perrot, V. & Levin, B. R. ( 1997; ). Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc R Soc Lond B Biol Sci 264, 1287–1291.[CrossRef]
    [Google Scholar]
  60. Seligmann, H. ( 2003; ). Cost-minimization of amino acid usage. J Mol Evol 56, 151–161.[CrossRef]
    [Google Scholar]
  61. Shirai, M., Hirakawa, H., Kimoto, M. & 8 other authors ( 2000; ). Comparison of whole genome sequences of Chlamydia pneumoniae J138 from Japan and CWL029 from USA. Nucleic Acids Res 28, 2311–2314.[CrossRef]
    [Google Scholar]
  62. Sokurenko, E. V., Chesnokova, V., Dykhuizen, D. E., Ofek, I., Wu, X. R., Krogfelt, K. A., Struve, C., Schembri, M. A. & Hasty, D. L. ( 1998; ). Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc Natl Acad Sci U S A 95, 8922–8926.[CrossRef]
    [Google Scholar]
  63. Spiers, A. J., Kahn, S. G., Bohannon, J., Travisano, M. & Rainey, P. B. ( 2002; ). Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 161, 33–46.
    [Google Scholar]
  64. Stackebrandt, E., Frederiksen, W., Garrity, G. M. & 10 other authors ( 2002; ). Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52, 1043–1047.[CrossRef]
    [Google Scholar]
  65. Treves, D. S., Manning, S. & Adams, J. ( 1998; ). Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol Biol Evol 15, 789–797.[CrossRef]
    [Google Scholar]
  66. Zhu, P., van der Ende, A., Falush, D. & 13 other authors ( 2001; ). Fit genotypes and escape variants of subgroup III Neisseria meningitidis during three pandemics of epidemic meningitis. Proc Natl Acad Sci U S A 98, 5234–5239.[CrossRef]
    [Google Scholar]
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Results of a principal component analysis for utilization of the 95 substrates examined in this study are available when you click here. (PDF format)



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