The Bacterial Species Challenge: Making Sense of Genetic and Ecological Diversity
Abstract
The Bacteria and Archaea are the most genetically diverse superkingdoms of life, and techniques for exploring that diversity are only just becoming widespread. Taxonomists classify these organisms into species in much the same way as they classify eukaryotes, but differences in their biology—including horizontal gene transfer between distantly related taxa and variable rates of homologous recombination—mean that we still do not understand what a bacterial species is. This is not merely a semantic question; evolutionary theory should be able to explain why species exist at all levels of the tree of life, and we need to be able to define species for practical applications in industry, agriculture, and medicine. Recent studies have emphasized the need to combine genetic diversity and distinct ecology in an attempt to define species in a coherent and convincing fashion. The resulting data may help to discriminate among the many theories of prokaryotic species that have been produced to date.
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References and Notes
1
J. Handelsman, Microbiol. Mol. Biol. Rev.68, 669 (2004).
2
W. P. Hanage, C. Fraser, B. G. Spratt, Philos. Trans. R. Soc. London Ser. B361, 1917 (2006).
3
M. Achtman, M. Wagner, Nat. Rev. Microbiol.6, 431 (2008).
4
F. M. Cohan, Annu. Rev. Microbiol.56, 457 (2002).
5
W. F. Doolittle, R. T. Papke, Genome Biol.7, 116 (2006).
6
D. Geverset al., Nat. Rev. Microbiol.3, 733 (2005).
7
M. F. Polz, D. E. Hunt, S. P. Preheim, D. M. Weinreich, Philos. Trans. R. Soc. London Ser. B361, 2009 (2006).
8
D. B. Ruschet al., PLoS Biol.5, e77 (2007).
9
C. Darwin, The Origin of Species (Penguin Classics, London, 1985).
10
E. Stackebrandtet al., Int. J. Syst. Evol. Microbiol.52, 1043 (2002).
11
R. Facklam, Clin. Microbiol. Rev.15, 613 (2002).
12
J. C. Arbiqueet al., J. Clin. Microbiol.42, 4686 (2004).
13
D. E. Huntet al., Science320, 1081 (2008).
14
See supplementary information in (16) for a statistical comparison of the ecotype model with an effective neutral model and an implicit estimate of Ne.
15
C. Fraser, W. P. Hanage, B. G. Spratt, Science315, 476 (2007).
16
A. Koeppelet al., Proc. Natl. Acad. Sci. U.S.A.105, 2504 (2008).
17
J. Maynard Smith, Proc. R. Soc. London Ser. B245, 37 (1991).
18
H. Ochman, A. C. Wilson, in Escherichia coli and Salmonella typhimurium:Cellular and Molecular Biology, F. C. Neidhart, Ed. (ASM Press, Washington, DC, 1987), pp. 1649–1654.
19
J. R. Thompsonet al., Appl. Environ. Microbiol.70, 4103 (2004).
20
M. Kimura, Trends Biochem. Sci.1, N152 (1976).
21
R. Milkman, Trends Biochem. Sci.1, N152 (1976).
22
K. C. Atwood, L. K. Schneider, F. J. Ryan, Proc. Natl. Acad. Sci. U.S.A.37, 146 (1951).
23
B. R. Levin, Genetics99, 1 (1981).
24
F. M. Cohan, E. B. Perry, Curr. Biol.17, R373 (2007).
25
A. Rambautet al., Nature453, 615 (2008).
26
R. A. Fisher, E. B. Ford, Heredity1, 143 (1947).
27
M. Slatkin, Theor. Popul. Biol.12, 253 (1977).
28
J. Majewski, F. M. Cohan, Genetics152, 1459 (1999).
29
E. J. Feil, B. G. Spratt, Annu. Rev. Microbiol.55, 561 (2001).
30
J. Majewski, F. M. Cohan, Genetics153, 1525 (1999).
31
J. Majewski, P. Zawadzki, P. Pickerill, F. M. Cohan, C. G. Dowson, J. Bacteriol.182, 1016 (2000).
32
S. T. Cowan, in Microbial Classification, 12th Symposium of the Society for General Microbiology, G. C. Ainsworth, P. H. A. Sneath, Eds. (Cambridge Univ. Press, Cambridge, 1962), pp. 433–455.
33
S. K. Sheppard, N. D. McCarthy, D. Falush, M. C. J. Maiden, Science320, 237 (2008).
34
A. C. Retchless, J. G. Lawrence, Science317, 1093 (2007).
35
K. Vetsigian, N. Goldenfeld, Proc. Natl. Acad. Sci. U.S.A.102, 7332 (2005).
36
A. Tuanyoket al., BMC Genomics9, 566 (2008).
37
U. Dobrindt, B. Hochhut, U. Hentschel, J. Hacker, Nat. Rev. Microbiol.2, 414 (2004).
38
P. Wilmes, S. L. Simmons, V. J. Denef, J. F. Banfield, FEMS Microbiol. Rev.33, 109 (2009).
39
V. J. Denefet al., Environ. Microbiol.11, 313 (2008).
40
E. Bantinakiet al., Genetics176, 441 (2007).
41
R. A. Welchet al., Proc. Natl. Acad. Sci. U.S.A.99, 17020 (2002).
42
J. Maynard Smith, N. H. Smith, M. O'Rourke, B. G. Spratt, Proc. Natl. Acad. Sci. U.S.A.90, 4384 (1993).
43
K. H. Hoffmannet al., FEMS Microbiol. Lett.273, 224 (2007).
44
We thank T. Connor and S. Deeny for useful discussions. Supported by University Research Fellowships from the Royal Society (C.F. and W.P.H.), a program grant from the Wellcome Trust (B.G.S.), grants from the U.S. Department of Energy Genomes to Life program (M.F.P. and E.J.A.), and the NSF/National Institute of Environmental Health Sciences Woods Hole Centre for Oceans and Human Health, the NSF Biological Oceanography Program, and the Moore Foundation (M.F.P.).
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Volume 323 | Issue 5915
6 February 2009
6 February 2009
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