[go: up one dir, main page]
More Web Proxy on the site http://driver.im/
Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

Re-evaluating prokaryotic species

Nature Reviews Microbiology volume 3, pages 733–739 (2005)Cite this article

Abstract

There is no widely accepted concept of species for prokaryotes, and assignment of isolates to species is based on measures of phenotypic or genome similarity. The current methods for defining prokaryotic species are inadequate and incapable of keeping pace with the levels of diversity that are being uncovered in nature. Prokaryotic taxonomy is being influenced by advances in microbial population genetics, ecology and genomics, and by the ease with which sequence data can be obtained. Here, we review the classical approaches to prokaryotic species definition and discuss the current and future impact of multilocus nucleotide-sequence-based approaches to prokaryotic systematics. We also consider the potential, and difficulties, of assigning species status to biologically or ecologically meaningful sequence clusters.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Failure of threshold methods in delineating prokaryotic species.

Similar content being viewed by others

References

  1. Stackebrandt, E. et al. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int. J. Syst. Evol. Microbiol. 52, 1043–1047 (2002).

    CAS  PubMed  Google Scholar 

  2. Vandamme, P. et al. Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol. Rev. 60, 407–438 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Amann, R. I., Ludwig, W. & Schleifer, K. H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59, 143–169 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Cohan, F. M. What are bacterial species? Annu. Rev. Microbiol. 56, 457–487 (2002).

    Article  CAS  PubMed  Google Scholar 

  5. Woese, C. R. The Use of Ribosomal RNA in Reconstructing Evolutionary Relationships Among Bacteria. in Evolution at the Molecular Level (eds Selander, R. K., Clark, A. G. & Whittam, T. S.) Ch. 1, 1–24 (Sinauer Associates Inc., Sunderland, 1991).

    Google Scholar 

  6. Fox, G. E., Wisotzkey, J. D. & Jurtshuk, P. Jr. How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int. J. Syst. Bacteriol. 42, 166–170 (1992).

    Article  CAS  PubMed  Google Scholar 

  7. Stackebrandt, E. & Goebel, B. M. A place for DNA–DNA reassociation and 16S ribosomal-RNA sequence-analysis in the present species definition in bacteriology. Int. J. Syst. Bacteriol. 44, 846–849 (1994).

    Article  CAS  Google Scholar 

  8. Gogarten, J. P., Doolittle, W. F. & Lawrence, J. G. Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 19, 2226–2238 (2002).

    Article  CAS  PubMed  Google Scholar 

  9. Boucher, Y., Douady, C. J., Sharma, A. K., Kamekura, M. & Doolittle, W. F. Intragenomic heterogeneity and intergenomic recombination among haloarchaeal rRNA genes. J. Bacteriol. 186, 3980–3990 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Maiden, M. C. J. et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl Acad. Sci. USA 95, 3140–3145 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Cooper, J. E. & Feil, E. J. Multilocus sequence typing — what is resolved? Trends Microbiol. 12, 373–377 (2004).

    Article  CAS  PubMed  Google Scholar 

  12. Zeigler, D. R. Gene sequences useful for predicting relatedness of whole genomes in bacteria. Int. J. Syst. Evol. Microbiol. 53, 1893–1900 (2003).

    Article  CAS  PubMed  Google Scholar 

  13. Santos, S. R. & Ochman, H. Identification and phylogenetic sorting of bacterial lineages with universally conserved genes and proteins. Environ. Microbiol. 6, 754–759 (2004).

    Article  CAS  PubMed  Google Scholar 

  14. Thompson, F. L. et al. Phylogeny and molecular identification of vibrios based on multilocus sequence analysis. Appl. Environ. Microbiol. (in the press).

  15. Devulder, G., Perouse de Montclos, M. & Flandrois, J. P. A multigene approach to phylogenetic analysis using the genus Mycobacterium as a model. Int. J. Syst. Evol. Microbiol. 55, 293–302 (2005).

    Article  CAS  PubMed  Google Scholar 

  16. Kotetishvili, M. et al. Multilocus sequence typing for studying genetic relationships among Yersinia species. J. Clin. Microbiol. 43, 2674–2684 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Priest, F. G., Barker, M., Baillie, L. W. J., Holmes, E. C. & Maiden, M. C. J. Population structure and evolution of the Bacillus cereus group. J. Bacteriol. 186, 7959–7970 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Godoy, D. et al. Multilocus sequence typing and evolutionary relationships among the causative agents of melioidosis and glanders, Burkholderia pseudomallei and Burkholderia mallei. J. Clin. Microbiol. 41, 2068–2079 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Feldgarden, M., Byrd, N. & Cohan, F. M. Gradual evolution in bacteria: evidence from Bacillus systematics. Microbiology 149, 3565–3573 (2003).

    Article  CAS  PubMed  Google Scholar 

  20. Welch, R. A. et al. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl Acad. Sci. USA 99, 17020–17024 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Schloter, M., Lebuhn, M., Heulin, T. & Hartmann, A. Ecology and evolution of bacterial microdiversity. FEMS Microbiol. Rev. 24, 647–660 (2000).

    Article  CAS  PubMed  Google Scholar 

  22. Jolley, K. A. et al. Carried meningococci in the Czech Republic: a diverse recombining population. J. Clin. Microbiol. 38, 4492–4498 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Enright, M. C., Spratt, B. G., Kalia, A., Cross, J. H. & Bessen, D. E. Multilocus sequence typing of Streptococcus pyogenes and the relationships between emm type and clone. Infect. Immun. 69, 2416–2427 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Sreevatsan, S. et al. Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc. Natl Acad. Sci. USA 94, 9869–9874 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Godreuil, S., Cohan, F. M., Shah, H. & Tibayrenc, M. Which species concept for pathogenic bacteria?: an e-debate. Infect. Genet. Evol. 20 Jan 2005 (doi/10.1016/j.meegid.2004.03.004).

  26. de Queiroz, K. in Endless Forms: Species and Speciation (eds Howard, D. J. & Berlocher, S. H.) Ch. 5, 57–75 (Oxford University Press, Oxford, 1998).

    Google Scholar 

  27. Ward, D. M. & Cohan, F. M. Microbial Diversity in Hot Spring Cyanobacterial Mats: Pattern and Prediction. in Geothermal Biology and Geochemistry in Yellowstone National Park (eds Inskeep, W. P. & McDermott, T.) in the press (Thermal Biology Institute, Bozeman).

  28. Hanage, W. P., Fraser, C. & Spratt, B. G. Fuzzy species among recombinogenic bacteria. BMC Biol. 3, 6 (2005).

  29. Feil, E. J. et al. Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc. Natl Acad. Sci. USA 98, 182–187 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Field, D., Feil, E. J. & Wilson, G. Databases and software for the comparative genomic study of collections of genomes. Microbiology (in the press).

  31. Welch, D. F. Applications of cellular fatty acid analysis. Clin. Microbiol. Rev. 4, 422–438 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Vos, P. et al. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23, 4407–4414 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. van Belkum, A. DNA fingerprinting of medically important microorganisms by use of PCR. Clin. Microbiol. Rev. 7, 174–184 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Coenye, T. & Vandamme, P. Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ. Microbiol. 5, 719–729 (2003).

    Article  CAS  PubMed  Google Scholar 

  35. Holden, M. T. G. et al. Genornic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc. Natl Acad. Sci. USA 101, 14240–14245 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Nierman, W. C. et al. Structural flexibility in the Burkholderia mallei genome. Proc. Natl Acad. Sci. USA 101, 14246–14251 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Brett, P. J., Deshazer, D., & Woods, D. E. Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. Int. J. Syst. Bacteriol. 48, 317–320 (1998).

    Article  CAS  PubMed  Google Scholar 

  38. Rogul, M., Brendle, J. J., Haapala, D. K. & Alexander, A. D. Nucleic acid similarities among Pseudomonas pseudomallei, Pseudomonas multivorans, and Actinobacillus mallei. J. Bacteriol. 101, 827–835 (1970).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Yabuuchi, E. et al. Burkholderia uboniae sp. nov., L-arabinose-assimilating but different from Burkholderia thailandensis and Burkholderia vietnamiensis. Microbiol. Immunol. 44, 307–317 (2000).

    Article  CAS  PubMed  Google Scholar 

  40. Cohan, F. M. Concepts of Bacterial Biodiversity for the Age of Genomics. in Microbial Genomes (eds Fraser, C. M., Read, T. D. & Nelson, K. E.) Ch. 11, 175–194 (Humana Press, Totowa, 2004).

    Google Scholar 

  41. Lawrence, J. G. Gene transfer in bacteria: speciation without species. Theor. Popul. Biol. 61, 449–460 (2002).

    Article  PubMed  Google Scholar 

  42. Palys, T., Nakamura, L. K. & Cohan, F. M. Discovery and classification of ecological diversity in the bacterial world: the role of DNA sequence data. Int. J. Syst. Bacteriol. 47, 1145–1156 (1997).

    Article  CAS  PubMed  Google Scholar 

  43. Papke, R. T., Ramsing, N. B., Bateson, M. M. & Ward, D. M. Geographical isolation in hot spring cyanobacteria. Environ. Microbiol. 5, 650–659 (2003).

    Article  CAS  PubMed  Google Scholar 

  44. Fraser, C., Hanage, W. P. & Spratt, B. G. Neutral microepidemic evolution of bacterial pathogens? Proc. Natl Acad. Sci. USA 102, 1968–1973 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Cohan, F. M. Does recombination constrain neutral divergence among bacterial taxa. Evolution 49, 164–175 (1995).

    Article  PubMed  Google Scholar 

  46. Keim, P. et al. Anthrax molecular epidemiology and forensics: using the appropriate marker for different evolutionary scales. Infect. Genet. Evol. 4, 205–213 (2004).

    Article  CAS  PubMed  Google Scholar 

  47. Dunlap, P. V. and Ast, J. C. Genomic and phylogenetic characterization of luminous bacteria symbiotic with the deep-sea fish Chlorophthalmus albatrossis (Aulopiformes: Chlorophthalmidae). Appl. Environ. Microbiol. 71, 930–939 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This paper is the outcome of a workshop entitled ‘The prokaryotic species: genome plasticity, microevolution and taxonomy’, organized by F. Thompson and J. Swings in Ghent, Belgium, 25 October 2004, and has the intention to stir up the interdisciplinary debate on the prokaryotic species. We thank all participants as well as D. Mazel, G. Manfio and T. Iida for their contributions. T.C., P.V. and J.S. are indebted to the Fund for Scientific Research — Flanders (Belgium) for a position as postdoctoral fellow and research funding, respectively. F.M.C. acknowledges funding from the National Science Foundation.

Author information

Authors and Affiliations

  1. Laboratory of Microbiology and the Bioinformatics and Evolutionary Genomics Research Group, Ghent University/VIB, Ghent, Belgium

    Dirk Gevers

  2. Department of Biology, Wesleyan University, Middletown, Connecticut, USA

    Frederick M. Cohan

  3. Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, USA

    Jeffrey G. Lawrence

  4. Department of Infectious Disease Epidemiology, Imperial College London, London, UK

    Brian G. Spratt

  5. Laboratory of Microbiology, Ghent University, Ghent, Belgium

    Tom Coenye & Peter Vandamme

  6. Department of Biology and Biochemistry, University of Bath, Bath, UK

    Edward J. Feil

  7. Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Braunschweig, Germany

    Erko Stackebrandt

  8. Bioinformatics and Evolutionary Genomics Research Group, Ghent University/VIB, Ghent, Belgium

    Yves Van de Peer

  9. Centro Pluridisciplinar de Pesquisas Químicas, Biológicas e Agrícolas, Universidade Estadual de Campinas, Campinas, Brazil

    Fabiano L. Thompson

  10. Laboratory of Microbiology and the BCCM™/LMG Bacteria Collection, Ghent University, Ghent, Belgium

    Jean Swings

Authors
  1. Dirk Gevers
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Frederick M. Cohan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeffrey G. Lawrence
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Brian G. Spratt
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tom Coenye
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Edward J. Feil
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Erko Stackebrandt
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yves Van de Peer
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Peter Vandamme
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Fabiano L. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jean Swings
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dirk Gevers.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Get into the debate on the prokaryotic species here

Glossary

MLST

Multilocus sequence typing, a method for the genotypic characterization of prokaryotes at the infraspecific level, using the allelic mismatches of a small number (usually 7) of housekeeping genes. Designed as a tool in molecular epidemiology and used for recognizing distinct strains within named species.

MLSA

Multilocus sequence analysis, a method for the genotypic characterization of a more diverse group of prokaryotes (including entire genera) using the sequences of multiple protein-coding genes.

SPECIES CONCEPT

A framework to understand how and why an observer can sort organisms into species; that is, what kind of unit do we think the term species embraces, and what characteristics are shared between all members of a species.

SPECIES DEFINITION

A more practical outline of how to assign isolates to a named species or identify new species.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gevers, D., Cohan, F., Lawrence, J. et al. Re-evaluating prokaryotic species. Nat Rev Microbiol 3, 733–739 (2005). https://doi.org/10.1038/nrmicro1236

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro1236

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing