Antonie van Leeuwenhoek

, Volume 101, Issue 1, pp 67–72 | Cite as

The 3Cs provide a novel concept of bacterial species: messages from the genome as illustrated by Salmonella



A key issue troubling bacterial taxonomy and systematics is the lack of a biological species definition. Criteria to be used for defining bacterial species on genetic and biological bases should be able to reveal clear-cut boundaries among clusters of bacteria. To date, DNA–DNA re-association assays and ribosomal RNA sequence comparison have been useful in determining relative evolutionary distances among bacteria but the data are continuous and thus cannot define bacterial clusters as taxonomic units to be called species. Using Salmonella as models, we have looked for definite genetic and biologic uniqueness of clusters of bacteria. Based on our findings that each Salmonella lineage has a unique genome structure shared by strains of the same lineage but not overlapping with strains of other Salmonella lineages, we conclude that this is a result of genetic isolation following divergence of the bacteria. We propose that there should be genetic boundaries between different species of bacteria at the genomic level, which awaits further genomic information for validation.


Bacterial species Bacterial systematics Bacterial taxonomy Bacterial nomenclature Salmonella genome 


  1. Bennett AF, Lenski RE (2007) An experimental test of evolutionary trade-offs during temperature adaptation. Proc Natl Acad Sci USA 104(1):8649–8654. doi: 10.1073/pnas.0702117104 PubMedCrossRefGoogle Scholar
  2. Brenner DJ, McWhorter AC, Knutson JK, Steigerwalt AG (1982) Escherichia vulneris: a new species of Enterobacteriaceae associated with human wounds. J Clin Microbiol 15(6):1133–1140PubMedGoogle Scholar
  3. Chen F, Liu WQ, Eisenstark A, Johnston RN, Liu GR, Liu SL (2010a) Multiple genetic switches spontaneously modulating bacterial mutability. BMC Evol Biol 10:277. doi: 10.1186/1471-2148-10-277 PubMedCrossRefGoogle Scholar
  4. Chen F, Liu WQ, Liu ZH, Zou QH, Wang Y, Li YG, Zhou J, Eisenstark A, Johnston RN, Liu GR, Yang BF, Liu SL (2010b) mutL as a genetic switch of bacterial mutability: turned on or off through repeat copy number changes. FEMS Microbiol Lett 312(2):126–132. doi: 10.1111/j.1574-6968.2010.02107.x PubMedCrossRefGoogle Scholar
  5. Chiu CH, Tang P, Chu C, Hu S, Bao Q, Yu J, Chou YY, Wang HS, Lee YS (2005) The genome sequence of Salmonella enterica serovar Choleraesuis, a highly invasive and resistant zoonotic pathogen. Nucleic Acids Res 33(5):1690–1698PubMedCrossRefGoogle Scholar
  6. Cohan FM (2002) What are bacterial species? Annu Rev Microbiol 56:457–487PubMedCrossRefGoogle Scholar
  7. Cooke FJ, Brown DJ, Fookes M, Pickard D, Ivens A, Wain J, Roberts M, Kingsley RA, Thomson NR, Dougan G (2008) Characterization of the genomes of a diverse collection of Salmonella enterica serovar Typhimurium definitive phage type 104. J Bacteriol 190(24):8155–8162PubMedCrossRefGoogle Scholar
  8. Crosa JH, Brenner DJ, Ewing WH, Falkow S (1973) Molecular relationships among the Salmonelleae. J Bacteriol 115(1):307–315PubMedGoogle Scholar
  9. DeLong EF, Pace NR (2001) Environmental diversity of bacteria and archaea. Syst Biol 50(4):470–478PubMedCrossRefGoogle Scholar
  10. Deng W, Liou SR, Plunkett G 3rd, Mayhew GF, Rose DJ, Burland V, Kodoyianni V, Schwartz DC, Blattner FR (2003) Comparative genomics of Salmonella enterica serovar Typhi strains Ty2 and CT18. J Bacteriol 185(7):2330–2337PubMedCrossRefGoogle Scholar
  11. Doolittle RF, Feng DF, Tsang S, Cho G, Little E (1996) Determining divergence times of the major kingdoms of living organisms with a protein clock. Science 271(5248):470–477PubMedCrossRefGoogle Scholar
  12. Feng DF, Cho G, Doolittle RF (1997) Determining divergence times with a protein clock: update and reevaluation. Proc Natl Acad Sci USA 94(24):13028–13033PubMedCrossRefGoogle Scholar
  13. Feng Y, Liu W-Q, Sanderson KE, Liu S-L (2011) Comparison of Salmonella genomes. In: Porwollik S (ed) Salmonella from genome to function. Caister Academic Press, Norfolk, pp 49–67Google Scholar
  14. Fox GE, Stackebrandt E, Hespell RB, Gibson J, Maniloff J, Dyer TA, Wolfe RS, Balch WE, Tanner RS, Magrum LJ, Zablen LB, Blakemore R, Gupta R, Bonen L, Lewis BJ, Stahl DA, Luehrsen KR, Chen KN, Woese CR (1980) The phylogeny of prokaryotes. Science 209(4455):457–463PubMedCrossRefGoogle Scholar
  15. Gao B, Gupta RS (2012) Microbial Systematics in the post-genomics Era. Antonie van Leeuwenhoek (in press)Google Scholar
  16. Gong J, Liu WQ, Liu GR, Chen F, Li JQ, Xu GM, Wang L, Johnston RN, Eisenstark A, Liu SL (2007) Spontaneous conversion between mutL and 6 bpDeltamutL in Salmonella typhimurium LT7: association with genome diversification and possible roles in bacterial adaptation. Genomics 90(4):542–549. doi: 10.1016/j.ygeno.2007.06.009 PubMedCrossRefGoogle Scholar
  17. Holt JG (1984) Bergey’s manual of systematic bacteriology. The Williams & Wilkins, BaltimoreGoogle Scholar
  18. Holt JG, Krieg NR, Sneath PH, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology, 9th edn. The Williams & Wilkins, BaltimoreGoogle Scholar
  19. Holt KE, Parkhill J, Mazzoni CJ, Roumagnac P, Weill FX, Goodhead I, Rance R, Baker S, Maskell DJ, Wain J, Dolecek C, Achtman M, Dougan G (2008) High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Genet 40(8):987–993PubMedCrossRefGoogle Scholar
  20. Kauffmann F, Edwards PR (1957) A revised, simplified Kauffmann-White schema. Acta Pathol Microbiol Scand 41(3):242–246PubMedCrossRefGoogle Scholar
  21. Le Minor L (1988) Typing of Salmonella species. Eur J Clin Microbiol Infect Dis 7(2):214–218PubMedCrossRefGoogle Scholar
  22. Liu SL, Sanderson KE (1995a) I-CeuI reveals conservation of the genome of independent strains of Salmonella typhimurium. J Bacteriol 177(11):3355–3357PubMedGoogle Scholar
  23. Liu SL, Sanderson KE (1995b) Rearrangements in the genome of the bacterium Salmonella typhi. Proc Natl Acad Sci USA 92(4):1018–1022PubMedCrossRefGoogle Scholar
  24. Liu SL, Schryvers AB, Sanderson KE, Johnston RN (1999) Bacterial phylogenetic clusters revealed by genome structure. J Bacteriol 181(21):6747–6755PubMedGoogle Scholar
  25. Liu GR, Rahn A, Liu WQ, Sanderson KE, Johnston RN, Liu SL (2002) The evolving genome of Salmonella enterica serovar Pullorum. J Bacteriol 184(10):2626–2633PubMedCrossRefGoogle Scholar
  26. Liu WQ, Feng Y, Wang Y, Zou QH, Chen F, Guo JT, Peng YH, Jin Y, Li YG, Hu SN, Johnston RN, Liu GR, Liu SL (2009) Salmonella paratyphi C: genetic divergence from Salmonella choleraesuis and pathogenic convergence with Salmonella typhi. PLoS ONE 4(2):e4510PubMedCrossRefGoogle Scholar
  27. Mayr E (1944) Systematics and the origin of species from the viewpoint of a zoologist. Columbia University Press, New YorkGoogle Scholar
  28. Mayr E (1996) What is a species, and what is not? Philos Sci 63:262–277CrossRefGoogle Scholar
  29. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, Porwollik S, Ali J, Dante M, Du F, Hou S, Layman D, Leonard S, Nguyen C, Scott K, Holmes A, Grewal N, Mulvaney E, Ryan E, Sun H, Florea L, Miller W, Stoneking T, Nhan M, Waterston R, Wilson RK (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413(6858):852–856PubMedCrossRefGoogle Scholar
  30. McClelland M, Sanderson KE, Clifton SW, Latreille P, Porwollik S, Sabo A, Meyer R, Bieri T, Ozersky P, McLellan M, Harkins CR, Wang C, Nguyen C, Berghoff A, Elliott G, Kohlberg S, Strong C, Du F, Carter J, Kremizki C, Layman D, Leonard S, Sun H, Fulton L, Nash W, Miner T, Minx P, Delehaunty K, Fronick C, Magrini V, Nhan M, Warren W, Florea L, Spieth J, Wilson RK (2004) Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid. Nat Genet 36(12):1268–1274PubMedCrossRefGoogle Scholar
  31. Ochman H, Selander RK (1984) Standard reference strains of Escherichia coli from natural populations. J Bacteriol 157(2):690–693PubMedGoogle Scholar
  32. Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26(1–2):74–86PubMedCrossRefGoogle Scholar
  33. Olsen GJ, Larsen N, Woese CR (1991) The ribosomal RNA database project. Nucleic Acids Res 19:2017–2021PubMedGoogle Scholar
  34. Palys T, Nakamura LK, Cohan FM (1997) Discovery and classification of ecological diversity in the bacterial world: the role of DNA sequence data. Int J Syst Bacteriol 47(4):1145–1156PubMedCrossRefGoogle Scholar
  35. Palys T, Berger E, Mitrica I, Nakamura LK, Cohan FM (2000) Protein-coding genes as molecular markers for ecologically distinct populations: the case of two Bacillus species. Int J Syst Evol Microbiol 50(Pt 3):1021–1028PubMedCrossRefGoogle Scholar
  36. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, Churcher C, Mungall KL, Bentley SD, Holden MT, Sebaihia M, Baker S, Basham D, Brooks K, Chillingworth T, Connerton P, Cronin A, Davis P, Davies RM, Dowd L, White N, Farrar J, Feltwell T, Hamlin N, Haque A, Hien TT, Holroyd S, Jagels K, Krogh A, Larsen TS, Leather S, Moule S, O’Gaora P, Parry C, Quail M, Rutherford K, Simmonds M, Skelton J, Stevens K, Whitehead S, Barrell BG (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413(6858):848–852PubMedCrossRefGoogle Scholar
  37. Parry CM, Hien TT, Dougan G, White NJ, Farrar JJ (2002) Typhoid fever. N Engl J Med 347(22):1770–1782PubMedCrossRefGoogle Scholar
  38. Popoff MY, Bockemuhl J, Gheesling LL (2004) Supplement 2002 (no. 46) to the Kauffmann–White scheme. Res Microbiol 155(7):568–570PubMedCrossRefGoogle Scholar
  39. Ravin AW (1960) The origin of bacterial species. Genetic recombination and factors limiting it between bacterial populations. Bacteriol Rev 24(2):201–220PubMedGoogle Scholar
  40. Reeves MW, Evins GM, Heiba AA, Plikaytis BD, Farmer JJ 3rd (1989) Clonal nature of Salmonella typhi and its genetic relatedness to other salmonellae as shown by multilocus enzyme electrophoresis, and proposal of Salmonella bongori comb. nov. J Clin Microbiol 27(2):313–320PubMedGoogle Scholar
  41. Roumagnac P, Weill F-X, Dolecek C, Baker S, Brisse S, Chinh NT, Le TAH, Acosta CJ, Farrar J, Dougan G, Achtman M (2006) Evolutionary history of Salmonella Typhi. Science 314:1301–1304PubMedCrossRefGoogle Scholar
  42. Schleifer KH, Ludwig W (1989) Phylogenetic relationships of bacteria. In: Fernholm B, Bremer K, Jornvall H (eds) The hierarchy of life. Elsevier Science Publishers BV, Amsterdam, pp 103–117Google Scholar
  43. Sokal RR, Crovello TJ (1970) The biological species concept: a critical evaluation. Am Nat 104:127–153CrossRefGoogle Scholar
  44. Souza V, Rocha M, Valera A, Eguiarte LE (1999) Genetic structure of natural populations of Escherichia coli in wild hosts on different continents. Appl Environ Microbiol 65(8):3373–3385PubMedGoogle Scholar
  45. Stackebrandt E, Woese CR (1984) The phylogeny of prokaryotes. Microbiol Sci 1(5):117–122PubMedGoogle Scholar
  46. Staley JT (2006) The bacterial species dilemma and the genomic-phylogenetic species concept. Philos Trans R Soc Lond B 361(1475):1899–1909CrossRefGoogle Scholar
  47. Thomson NR, Clayton DJ, Windhorst D, Vernikos G, Davidson S, Churcher C, Quail MA, Stevens M, Jones MA, Watson M, Barron A, Layton A, Pickard D, Kingsley RA, Bignell A, Clark L, Harris B, Ormond D, Abdellah Z, Brooks K, Cherevach I, Chillingworth T, Woodward J, Norberczak H, Lord A, Arrowsmith C, Jagels K, Moule S, Mungall K, Sanders M, Whitehead S, Chabalgoity JA, Maskell D, Humphrey T, Roberts M, Barrow PA, Dougan G, Parkhill J (2008) Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res 18(10):1624–1637PubMedCrossRefGoogle Scholar
  48. Vandamme P, Pot B, Gillis M, de Vos P, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60(2):407–438PubMedGoogle Scholar
  49. Vos M (2011) A species concept for bacteria based on adaptive divergence. Trends Microbiol 19(1):1–7. doi: 10.1016/j.tim.2010.10.003 PubMedCrossRefGoogle Scholar
  50. Woese CR (1987) Bacterial evolution. Microbiol Rev 51(2):221–271PubMedGoogle Scholar
  51. Woese CR (2000) Interpreting the universal phylogenetic tree. Proc Natl Acad Sci USA 97(15):8392–8396PubMedCrossRefGoogle Scholar
  52. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87(12):4576–4579PubMedCrossRefGoogle Scholar
  53. Wu KY, Liu GR, Liu WQ, Wang AQ, Zhan S, Sanderson KE, Johnston RN, Liu SL (2005) The genome of Salmonella enterica serovar gallinarum: distinct insertions/deletions and rare rearrangements. J Bacteriol 187(14):4720–4727PubMedCrossRefGoogle Scholar
  54. Zahrt TC, Mora GC, Maloy S (1994) Inactivation of mismatch repair overcomes the barrier to transduction between Salmonella typhimurium and Salmonella typhi. J Bacteriol 176(5):1527–1529PubMedGoogle Scholar
  55. Zuckerkandl E, Pauling L (1965) Molecules as documents of evolutionary history. J Theor Biol 8(2):357–366PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Genomics Research Center (One of the State-Province Key Laboratories of Biomedicine-Pharmaceutics of China)Harbin Medical UniversityHarbinChina
  2. 2.Genetic Detection Center of First Affiliated Hospital, Harbin Medical UniversityHarbinChina
  3. 3.Department of Microbiology and Infectious DiseasesUniversity of CalgaryCalgaryCanada
  4. 4.Department of MicrobiologyPeking University Health Science CenterBeijingChina

Personalised recommendations