Systematics of prokaryotes: the state of the art

Abstract

The term taxonomy is often used synonymously with systematics but it should be regarded more as a specific part of the latter and comprises the orderly arrangements of (defined) units in addition to the nomenclature, i.e. labelling of these units defined by classification, and also identification of these units defined by classification and labeled by nomenclature. Similar to all biological disciplines, taxonomic approaches in microbiology aim at the establishment of a system that mirrors the “order in nature” as closely as possible with the ultimate goal to describe the whole evolutionary order back to the origin of life. With the recognition of molecular markers present in all organisms (here in particular the small subunit rRNAs, ssRNSs), the achievement of this goal has become more and more feasible and the generation of gene and increasing numbers of genome sequences allow nowadays the generation of large amounts of data and often a very detailed insight into the genetic potential of prokaryotes. The possibility to generate whole genome sequences in a very short period of time leads to a strong tendency to base the taxonomic system more and more on sequence data. However, a comprehensive understanding of all the information behind sequence data is lagging far behind their accumulation. Genes and genomes may (or may not) function only in a given “environment”, with the cell as basic entity for the display of this potential. Prokaryotic taxonomy still has its focus on the whole organism. In this context, natural selection drives evolution selecting the existing phenotypes and it is the phenotype that “exhibits” this process both in a given cellular and also environmental context. The term polyphasic taxonomy, which was coined almost 40 years ago and aimed at the integration of many levels of information (from molecular to ecological data) thereby allowing a more holistic view, should be revisited in the light of the enormous potential of the novel information associated with large data sets.

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

References

  1. Bapteste E, Boucher Y (2008) Lateral gene transfer challenges principles of microbial systematics. Trends Microbiol 16:200–207

    PubMed  Article  CAS  Google Scholar 

  2. Bapteste E, O’Malley MA, Beiko RG, Ereshefky M, Gogarten JP, Franklin-Hall L et al (2009) Prokaryotic evolution and the tree of life are two different things. Biology Direct 4:34. doi:101186/1745-6150-4-34

    PubMed  Article  Google Scholar 

  3. Brenner DJ, Staley JT, Krieg NR (2001) Classification of prokaryotic organisms and the concept of bacterial speciation. In: Garrity GM (ed) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn. Springer, New York, pp 27–31

    Google Scholar 

  4. Brenner S (2010) Sequences and consequences. Phil Trans R Soc B 365:207–212

    PubMed  Article  Google Scholar 

  5. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287

    PubMed  Article  CAS  Google Scholar 

  6. Cole JR, Konstinidis K, Farris RJ, Tiedje JM (2010) Microbial diversity phylogeny: extending from rRNAs to genomes. In: Liu W-T, Jackson JK (eds) Environmental molecular microbiology. Caister Academic Press, Norfolk, pp 1–19

    Google Scholar 

  7. Colwell RR (1970) Polyphasic taxonomy of bacteria. In: Iizuka H, Hazegawa T (eds) Culture collections of microorganisms. University of Tokyo Press, Tokyo, pp 421–436

    Google Scholar 

  8. Cowan ST (1978) A dictionary of microbial taxonomy. Cambridge University Press, Cambridge

    Google Scholar 

  9. Dagan T, Artzy-Rrandup Y, Martin W (2008) Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proc Nat Acad Sci USA 105:10039–10044

    PubMed  Article  CAS  Google Scholar 

  10. De Vos P, Trüper HG (2000) Judicial Commission of the International Committee of Systematic Bacteriology. IXth International (IUMS) Congress of Bacteriology and Applied Microbiology. Minutes of the meetings, 14, 15, 18 August 1999, Sydney, Australia. Int J Syst Evol Microbiol 50:2239–2244

    Article  Google Scholar 

  11. Doroghazi JR, Buckley DH (2010) Widespread homologous recombination within and between Streptomyces species. ISME J 4:136–1143

    Article  Google Scholar 

  12. Euzéby JP (1997) List of bacterial names with standing in nomenclature: a folder available on the Internet. Int J Syst Bacteriol 47:590–592

    PubMed  Article  Google Scholar 

  13. Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ et al (2005) Re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739

    PubMed  Article  CAS  Google Scholar 

  14. Giffard P (2010) Bioinformatics of microbial sequences. In: Sintchenko V (ed) Infectious diseases informatics. Springer, New York, pp 27–52

    Google Scholar 

  15. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91

    PubMed  Article  CAS  Google Scholar 

  16. Harayama S, Kasai H (2006) Bacterial phylogeny reconstruction from molecular sequences. In: Stackebrandt E (ed) Molecular identification, systematics, and population structure of prokaryotes. Springer, Berlin, pp 105–140

    Google Scholar 

  17. Kämpfer P (2010) Certificates of deposit—a key element of the bacteriological code and an indispensable prerequisite for comparative taxonomic research. Report of a case of falsification and a reply to the letter to the editor by Tindall (2008). Int J Syst Evol Microbiol 60:475–477

    PubMed  Article  Google Scholar 

  18. Kämpfer P, Glaeser S (2011a) Prokaryotic taxonomy in the sequencing era and the role of MLSA in classification. Microbiology Australia 32:66–70

    Google Scholar 

  19. Kämpfer P, Glaeser S. (2011b) Prokaryotic taxonomy in the sequencing era—the polyphasic approach revisited. Env Microbiol (in press)

  20. Klenk H-P, Göker M (2010) En route to a genome-based classification of Archaea and Bacteria? Syst Appl Microbiol 33:175–182

    PubMed  Article  CAS  Google Scholar 

  21. Konstantinidis KT, Ramette A, Tiedje JM (2006) The bacterial species definition in the genomic era. Philos Trans R Soc Lond B Biol Sci 361:1929–1940

    PubMed  Article  Google Scholar 

  22. Konstantinidis KT, Tiedje JM (2005) Genomic insights into the species definition for prokaryotes. Proc Natl Acad Sci USA 102:2567–2572

    PubMed  Article  CAS  Google Scholar 

  23. Konstantinidis KT, Tiedje JM (2007) Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 10:504–509

    PubMed  Article  CAS  Google Scholar 

  24. Koonin EV (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol 1:27–136

    Article  Google Scholar 

  25. Krichevsky MI (2011) What is a bacterial species? I will know it when I see it. The Bulletin of BISMiS 2:17–23

    Google Scholar 

  26. Kubatko LS, Degnan JH (2007) Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst Biol 56:17–24

    PubMed  Article  CAS  Google Scholar 

  27. Labeda DP (2000) International committee on systematic bacteriology. IXth International (IUMS) Congress of Bacteriology and Applied Microbiology. Minutes of the meetings, 14 and 17 August 1999, Sydney, Australia. Int J Syst Evol Microbiol 50:2245–2247

    Article  Google Scholar 

  28. Lapage SP, Sneath PHA, Lessel EF, Skerman VBD, Seeliger HPR, Clark WA (1992) International code of nomenclature of bacteria (1990 Revision). American Society for Microbiology, Washington

    Google Scholar 

  29. Ludwig W (2010) Molecular phylogeny of microorganisms: is rRNA still a useful marker? In: Oren A, Papke RT (eds) Molecular phylogeny of microorganisms. Caister Academic Press, Norfolk, pp 65–84

    Google Scholar 

  30. Ludwig W, Klenk H-P (2001) Overview: a phylogenetic backbone and taxonomic framework of prokaryotes. In: Garrity GM (ed) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York, pp 49–65

    Google Scholar 

  31. Maiden MC, Bygraves JA, Feil E, Morelli G, Russel JE, Urwin R et al (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA 95:3140–3145

    PubMed  Article  CAS  Google Scholar 

  32. Moore ERB, Mihaylova SA, Vandamme P, Krichevsky MI, Dijkshoorn L (2010) Microbial systematics and taxonomy: relevance for a microbial commons. Res Microbiol 161:430–438

    PubMed  Article  Google Scholar 

  33. Murray RGE, Brenner DJ, Colwell RR, De Vos P, Goodfellow M, Grimont PAD et al (1990) Report of the ad hoc committee on approaches to taxonomy within the Proteobacteria. Int J Syst Bacteriol 40:213–215

    Article  Google Scholar 

  34. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 45:19126–19131

    Article  Google Scholar 

  35. Sneath PHA (1989) Analysis and interpretation of sequence data for bacterial systematics—the view of a numerical taxonomist. Syst Appl Microbiol 12:15–31

    Article  Google Scholar 

  36. Sneath PHA (2007) The species concept. Microbiol Today 34:45

    Google Scholar 

  37. Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155

    Google Scholar 

  38. Stackebrandt E, Frederiksen W, Garrity GM, Grimont PAD, Kämpfer P, Maiden MCJ et al (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

    PubMed  Article  CAS  Google Scholar 

  39. Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  CAS  Google Scholar 

  40. Stackebrandt E, Woese CR (1981) Towards a phylogeny of the actinomycetes and related organism. Curr Microbiol 5:197–202

    Article  CAS  Google Scholar 

  41. Tindall BJ (2008) Confirmation of deposit, but confirmation of what? Int J Syst Evol Microbiol 58:1785–1787

    PubMed  Article  CAS  Google Scholar 

  42. Tindall BJ, De Vos P, Trüper HG (2008a) Judicial Commission of the International Committee of Systematics of Prokaryotes. XIth International (IUMS) Congress of Bacteriology and Applied Microbiology. Minutes of the meetings, 23, 24, 27 July 2005, San Francisco, CA, USA. Int J Syst Evol Microbiol 58:1737–1745

    Article  Google Scholar 

  43. Tindall BJ, Garrity GM (2008) Proposals to clarify how type strains are deposited and made available to the scientific community for the purpose of systematic research. Int J Syst Evol Microbiol 58:1987–1990

    PubMed  Article  CAS  Google Scholar 

  44. Tindall BJ, Kämpfer P, Euzéby JP, Oren A (2006) Valid publication of names of prokaryotes according to the rules of nomenclature: past history and current practice. Int J Syst Evol Microbiol 56:2715–2720

    PubMed  Article  Google Scholar 

  45. Tindall BJ, Rosselló-Móra R, Busse H-J, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266

    PubMed  Article  CAS  Google Scholar 

  46. Tindall BJ, Sikorski J, Smibert RA, Krieg NL (2008b) Phenotypic characterization and the principles of comparative systematics. In: Garrity GM (ed) Methods for general and molecular microbiology, 3rd Ed. ASM Press, Washington, pp 330–393

    Google Scholar 

  47. Vinuesa P (2010) Multilocus sequence analysis and bacterial species phylogeny estimation. In: Oren A, Papke RT (eds) Molecular phylogeny of microorganisms. Caister Academic Press, norfolk, pp 41–64

    Google Scholar 

  48. Wayne LG, Brenner DJ, Colwell RR et al (1987) International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464

    Article  Google Scholar 

  49. Welker M, Moore ER (2011) Applications of whole-cell matrix-assisted laser-desorption/ionization time-of-flight mass spectrometry in systematic microbiology. Syst Appl Microbiol 34:2–11

    Google Scholar 

  50. Williams D, Andam CP, Gogarten JP (2010) Horizontal gene transfer and the formation of groups of microorganisms. In: Oren A, Papke RT (eds) Molecular phylogeny of microorganisms. Caister Academic Press, Norfolk, pp 167–184

    Google Scholar 

  51. Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    PubMed  CAS  Google Scholar 

  52. Woese CR, Fox E (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Nat Acad Sci USA 74:5088–5090

    PubMed  Article  CAS  Google Scholar 

  53. Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer KH, Ludwig W, Glöckner FO, Rosselló-Móra R (2008) The all-species living tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31:241–250

    PubMed  Article  CAS  Google Scholar 

  54. Young JM (2001) Implications of alternative classifications and horizontal gene transfer for bacterial taxonomy. Int J Syst Evol Microbiol 51:945–953

    PubMed  Article  CAS  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Peter Kämpfer.

Additional information

This paper is dedicated to Prof. P.H.A. Sneath, who passed away on 9. September 2011. His work on Bacterial Nomenclature and the Code will have a long standing influence on our taxonomic system. His approach to computers for taxonomic studies was the first and although most of the analyses in bacterial systematics today use molecular data, their bases are essentially the same as the approaches that Peter Sneath developed more than 50 years ago.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kämpfer, P. Systematics of prokaryotes: the state of the art. Antonie van Leeuwenhoek 101, 3–11 (2012). https://doi.org/10.1007/s10482-011-9660-4

Download citation

Keywords

  • Systematics
  • Taxonomy
  • Polyphasic approach
  • State of the art