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Defining Taxonomic Ranks

  • Konstantinos T. Konstantinidis
  • Erko Stackebrandt

Abstract

Taxonomic ranks are subjectively defined constructs based on dissimilarities between individuals or groups of organisms, with higher ranks representing higher-order groupings. The establishment of a Linnaeus-type hierarchy and binomial nomenclature for bacteria originated from the botanical background of the first microbiologists in the nineteenth century and the desire to establish a system comparable to those of plants and animals. Anatomical/morphological similarities, reflecting evolutionary relationships, are common among plants and animals, allowing their classification into a hierarchic structure. In contrast, as bacterial relatedness is not typically characterized by distinctive morphological and physiological similarities, the first 100 years of bacteriology witnessed several different hierarchic structures, often discussed in parallel, depending upon the emerging discoveries at the time. It was not until the semantic nature of DNA, RNA, and proteins was described that scientists were able to present the outline of a hierarchic structure of the prokaryotes. This structure is primarily based on the phylogenetic tree of the small subunit ribosomal RNA gene, a universally present molecule of about 1,500 nucleotides long, and so far represents the most convincing reflection of the evolutionary relationships among prokaryotic taxa. Although the evolution of several housekeeping genes is in support of the rRNA gene tree, indicating that an average “consensus” phylogeny may have been obtained, the phylogenies of many other genes depart from the rRNA phylogeny due to extensive horizontal gene transfer, making it clear that the true evolutionary history of organisms is probably not reflected by the present prokaryotic tree. It must also be remembered that taxonomy is not fixed but prone to changes as a result of research on established and new taxa. Only the naming of taxa but not the science of classification is regulated, resulting in taxonomy in flux with regular changes of ranks due to their splitting and merging and introduction of novel ranks at all levels as new information becomes available.

This chapter describes the main principles underlying the delineation of the higher ranks (phylum-class-order-family) and discusses the finding that not all taxa related at the same rank are comparable units in terms of intrataxon genetic relatedness. Special attention is given to the species rank, the fundamental unit of biological organization, and the recent advances in genomics and ecology that call into question the pragmatic but artificial species definition that is in use today. Only when these issues will be addressed, the promise for a more predictive, genome-based prokaryotic taxonomy will be realized. We believe time and technology needed may have arrived.

Keywords

Horizontal Gene Transfer Species Concept Average Nucleotide Identity Prokaryotic Species Average Amino Acid Identity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Achtman M (1998) Microevolution during epidemic spread of Neisseria meningitidis. Electrophoresis 19:593–596PubMedGoogle Scholar
  2. Achtman M, Wagner M (2008) Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 6:431–440PubMedGoogle Scholar
  3. Acinas SG, Klepac-Ceraj V, Hunt DE, Pharino C, Ceraj I, Distel DL, Polz MF (2004) Fine-scale phylogenetic architecture of a complex bacterial community. Nature 430:551–554PubMedGoogle Scholar
  4. Alperi A, Martínez-Murcia AJ, Monera A, Saavedra MJ, Figueras MJ (2010) Aeromonas fluvialis sp. nov., isolated from a Spanish river. Int J Syst Evol Microbiol 60:72–77PubMedGoogle Scholar
  5. Amann R, Ludwig W, Schleifer KH (1988) Beta-subunit of ATP-synthase: a useful marker for studying the phylogenetic relationship of eubacteria. J Gen Microbiol 134:2815–2821PubMedGoogle Scholar
  6. Amann RI, Lin C, Key R, Montgomery L, Stahl DA (1992) Diversity among Fibrobacter strains: towards a phylogenetic classification. Syst Appl Microbiol 15:23–31Google Scholar
  7. Ash C, Farrow JAE, Wallbanks S, Collins MD (1991) Phylogenetic heterogeneity of the genus Bacillus revealed by comparative analysis of small-subunit ribosomal RNA sequences. Lett Appl Microbiol 13:202–206Google Scholar
  8. Bachmann K (1998) Species as units of diversity: an outdated concept. Theor Biosci 117:213–230Google Scholar
  9. Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogens: reevaluation of a unique biological group. Micribiol Rev 43:260–296Google Scholar
  10. Barraclough TG, Hughes M, Ashford-Hodges N, Fujisawa T (2009) Inferring evolutionarily significant units of bacterial diversity from broad environmental surveys of single-locus data. Biol Lett 23:425–428Google Scholar
  11. Baumann P, Baumann L, Woolkalis MJ, Bang SS (1983) Evolutionary relationships in Vibrio and Photobacterium a basis for a natural classification. Annu Rev Microbiol 37:369–398PubMedGoogle Scholar
  12. Bautz EKF, Bautz FA (1964) The influence of non-complementary bases on the stability of ordered polynucleotides. Proc Natl Acad Sci USA 52:1476–1481PubMedGoogle Scholar
  13. Beiko RG, Harlow TJ, Ragan MA (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci USA 102:14332–14337PubMedGoogle Scholar
  14. Beres SB, Carroll RK, Shea PR, Sitkiewicz I, Martinez-Gutierrez JC et al (2009) Molecular complexity of successive bacterial epidemics deconvoluted by comparative pathogenomics. Proc Natl Acad Sci USA 107:4371–4376Google Scholar
  15. Borriss R, Chen X, Rueckert C, Blom J, Becker A, Baumgarth B, Fan B, Pukall R, Schumann P, Spröer C, Junge H, Vater J, Pühler A, Klenk H-P (2010)Relationship of Bacillus amyloliquefaciens clades associated with strains DSM7T and FZB42: a proposal for Bacillus amyloliquefaciens subsp. amyloliquefaciens subsp. nov. and Bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on their discriminating complete genome sequences. Int J Syst Evol Microbiol. First published on Sep 3, 2010 as doi: 10.1099/ijs.0.023267-0Google Scholar
  16. Brenner DJ (1991) Additional genera of the Enterobacteriaceae. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes. A handbook on the biology of bacteria: ecophysiology, isolation, applications. Springer, New York, pp 2922–2937Google Scholar
  17. Britten RJ, Kohne DE (1968) Repeated sequences in DNA. Science 161:529–540PubMedGoogle Scholar
  18. Buchanan RE (1916) Studies in the nomenclature and classification of the bacteria I. The problem of bacterial nomenclature. J Bacteriol 1:591–596PubMedGoogle Scholar
  19. Buchanan RE (1918) Studies in the nomenclature and classification of the bacteria V. Subgroups and genera of the Bacteriaceae. J Bacteriol 3:27–61PubMedGoogle Scholar
  20. Buckley M, Roberts RJ (2007) Reconciling microbial systematics and genomics. Colloquium Report. The American Society for Microbiology, Washington, DCGoogle Scholar
  21. Caro-Quintero A, Rodriguez-Castano GP, Konstantinidis KT (2009) Genomic insights into the convergence and pathogenicity factors of Campylobacter jejuni and Campylobacter coli species. J Bacteriol 191:5824–5831PubMedGoogle Scholar
  22. Caro-Quintero A, Deng J, Auchtung J, Brettar I, Höfle MG, Klappenbach J, Konstantinidis KT (2011) Unprecedented levels of horizontal gene transfer among spatially co-occurring Shewanella bacteria from the Baltic Sea. ISME J 5:131–140PubMedGoogle Scholar
  23. Cavalier-Smith T (2002) The neomuran origin of archaebacteria, the negibacterial root of the universal tree, and bacterial mega classification. Int J Syst Evol Microbiol 52:7–76PubMedGoogle Scholar
  24. Christensen H, Kuhnert P, Busse H-J, Frederiksen WC, Bisgaard M (2007) Proposed minimal standards for the description of genera, species and subspecies of the Pasteurellaceae. Int J Syst Evol Microbiol 57:166–178PubMedGoogle Scholar
  25. Cicarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287Google Scholar
  26. Cohan FM (2002) What are bacterial species? Annu Rev Microbiol 56:457–487PubMedGoogle Scholar
  27. Cohan FM (2006) Towards a conceptual and operational union of bacterial systematics, ecology, and evolution. Philos Trans R Soc Lond B Biol Sci 361:1985–1996PubMedGoogle Scholar
  28. Cohan FM, Koeppel AF (2008) The origins of ecological diversity in prokaryotes. Curr Biol 18R:1024–1034Google Scholar
  29. Cohn F (1872) Untersuchungen über Bacterien. Beitr Biol Pfl 2:127–224Google Scholar
  30. Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J, Garcia P, Cai J, Hippe H, Farrow JAE (1994) The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44:812–826PubMedGoogle Scholar
  31. Colwell RR (1970) Polyphasic taxonomy of the genus Vibrio: numerica taxonomy of Vibrio cholerae, Vibrio parahaemolyticus, and related Vibrio species. J Bacteriol 104:410–433PubMedGoogle Scholar
  32. Cousin S, Brambilla E, Yang J, Stackebrandt E (2008) Culturable aerobic bacteria from the upstream region of a karst water rivulet. Int Microbiol 11:91–100PubMedGoogle Scholar
  33. Cowan ST (1968) A dictionary of microbial taxonomic usage. Oliver & Boyd, EdinburghGoogle Scholar
  34. Cracraft J (1983) Species concept and speciation analysis. Current ornithology. Plenum Press, New York, pp 159–187Google Scholar
  35. Darwin C (1859) On the origin of species. Murray, LondonGoogle Scholar
  36. De Ley J (1970) Reexamination of the association between melting point, buoyant density, and chemical base composition of deoxyribonucleic acid. J Bacteriol 101:738–754PubMedGoogle Scholar
  37. DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard NU, Martinez A, Sullivan MB, Edwards R, Brito BR, Chisholm SW, Karl DM (2006) Community genomics among stratified microbial assemblages in the ocean’s interior. Science 311:496–503PubMedGoogle Scholar
  38. Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  39. Doolittle WF, Bapteste E (2007) Pattern pluralism and the tree of life hypothesis. Proc Natl Acad Sci USA 104:2043–2049PubMedGoogle Scholar
  40. Doolittle WF, Zhaxybayeva O (2009) On the origin of prokaryotic species. Genome Res 19:744–756PubMedGoogle Scholar
  41. Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37PubMedGoogle Scholar
  42. Dykhuizen DE, Green L (1991) Recombination in Escherichia coli and the definition of biological species. J Bacteriol 173:7257–7268PubMedGoogle Scholar
  43. Dzink JL, Sheehan MT, Socransky SS (1990) Proposal of three subspecies of Fusobacterium nucleatum Knorr 1922: Fusobacterium nucleatum subsp. nucleatum subsp. nov., comb. nov.; Fusobacterium nucleatum subsp. polymorphum subsp. nov., nom. rev., comb. nov.; and Fusobacterium nucleatum subsp. vincentii subsp. nov., nom. rev., comb. nov. Int J Syst Bacteriol 40:74–78PubMedGoogle Scholar
  44. Embley MT, Stackebrandt E (1994) The molecular phylogeny and systematics of the Actinomycetes. Annu Rev Microbiol 48:257–289PubMedGoogle Scholar
  45. Eppley JM, Tyson GW, Getz WM, Banfield JF (2007) Genetic exchange across a species boundary in the archaeal genus Ferroplasma. Genetics 177:407–416PubMedGoogle Scholar
  46. Ezaki T, Hashimoto Y, Yabuuchi E (1989) Fluorimetric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39:224–229Google Scholar
  47. Farelly V, Rainey FA, Stackebrandt E (1995) Effect of genomic size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species. Appl Environ Microbiol 61:2798–2801Google Scholar
  48. Farmer JJ III, Janda JM, Brenner FW, Cameron DN, Birkhead KM (2005) Genus 1. Vibrio Pacini 1854, 411AL. In: Brenner DJ, Krieg NR, Staley JR (eds) Bergey’s manual systematic bacteriology: the proteobacteria, 2nd edn. Springer, New York, pp 494–546Google Scholar
  49. Fowler VJ, Widdel F, Pfennig N, Stackebrandt E (1986) Phylogenetic relationships of sulfate- and sulfur-reducing eubacteria. Syst Appl Microbiol 8:32–41Google Scholar
  50. Fox GE, Stackebrandt E, Hespell RB, Gibson J, Maniloff J, Dyer TA, Wolfe RS, Balch WE, Tanner R, Magrum L, Zablen L-B, Blakemore R, Gupta R, Lewis BJ, Stahl DA, Luehrsen R, Chen KN, Woese CR (1980) The phylogeny of prokaryotes. Science 209:457–463PubMedGoogle Scholar
  51. Fox GE, Wisotzkey JD, Jurtshuk P Jr (1992) How close is close: 16S RNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Bacteriol 42:166–170PubMedGoogle Scholar
  52. Fraser C, Hanage WP, Spratt BG (2007) Recombination and the nature of bacterial speciation. Science 315:476–480PubMedGoogle Scholar
  53. Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP (2009) The bacterial species challenge: making sense of genetic and ecological diversity. Science 323:741–746PubMedGoogle Scholar
  54. Garrity GM, Holt JG (2001a) Class I. Deinococci class. nov. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn, The Archaea and the deeply branching and phototrophic bacteria. Springer, New York, p 395Google Scholar
  55. Garrity GM, Holt JG (2001b) Phylum BVIII. Nitrospirae phy. nov. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology. Springer, New York, pp 451–464Google Scholar
  56. Garrity GM, Holt JG (2001c) Phylum BVI. Chloroflexi phy. nov. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn, The Archaea and the deeply branching and phototrophic bacteria. Springer, New York, pp 427–446Google Scholar
  57. Garrity GM, Garrity GM, Bell JA, Lilburn T (2005) Phylum XIV. Proteobacteria phyl. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 2, 2nd edn, The proteobacteria, part B: the gammaproteobacteria. Springer, New York, p 1Google Scholar
  58. Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL, Swings J (2005) Re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739PubMedGoogle Scholar
  59. Gharbia SE, Shah HN (1992) Fusobacterium nucleatum subsp. fusiforme subsp. nov. and Fusobacterium nucleatum subsp. animalis subsp. nov. as additional subspecies within Fusobacterium nucleatum. Int J Syst Bacteriol 42:296–298PubMedGoogle Scholar
  60. Gibbons NE, Murray RGE (1978) Proposals concerning the higher taxa of bacteria. Int J Syst Bacteriol 28:1–6Google Scholar
  61. Gibson J, Ludwig W, Stackebrandt E, Woese CR (1985) The phylogeny of the green photosynthetic bacteria: absence of a close relationship between Chlorobium and Chloroflexus. Syst Appl Microbiol 6:152–156Google Scholar
  62. Gogarten JP, Townsend JP (2005) Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3:679–687PubMedGoogle Scholar
  63. Goris J, Suzuki K, De Vos P, Nakase T, Kersters K (1999) Evaluation of a microplate DNA-DNA hybridization method compared to the initial renaturation method. Can J Microbiol 44:1148–1153Google Scholar
  64. Goris J, Konstantinidis KT, Coenye T, Vandamme P, Tiedje JM (2007) DNA-DNA hybridization values and their relation to whole genome sequence. Int J Syst Evol Microbiol 57:81–91PubMedGoogle Scholar
  65. Grimont PAD, Popoff MY, Grimont F, Coynault C, Lemelin M (1980) Reproducibility and correlation study of three deoxyribonucleic acid hybridization procedures. Curr Microbiol 4:325–330Google Scholar
  66. Gupta RS, Golding GB (1993) Evolution of HSP70 gene and its implications regarding relationships between Archaebacteria, Eubacteria and Eukaryotes. J Mol Evol 37:573–582PubMedGoogle Scholar
  67. Gürtler V, Mayall BC (2001) Genomic approaches to typing, taxonomy and evolution of bacterial isolates. Int J Syst Evol Microbiol 51:3–16PubMedGoogle Scholar
  68. Guttman DS, Dykhuizen DE (1994) Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266:1380–1383PubMedGoogle Scholar
  69. Handelsman J, Tiedje J, Alvarez-Cohen L, Ashburner M, Cann I, Delong E, Doolittle W, Fraser-Ligget C, Godzik A, Gordon J, Riley M, Schmidt T (2007) The news of metagenomics: revealing the secrets of our microbial planet. The National Academies Press, Washington, DCGoogle Scholar
  70. Hara T, Shimoda T, Nonaka K, Ogata S (1991) Colorimetric detection of DNA-DNA hybridization in microdilution wells for taxonomic application on bacteria strains. J Ferment Bioeng 72:122–124Google Scholar
  71. Harris LG, El-Bouri K, Johnston S, Rees E, Frommelt L, Siemssen N, Christner M, Davies AP, Rohde H, Mack D (2010) Rapid identification of staphylococci from prosthetic joint infections using MALDI-TOF mass-spectrometry. Int J Artif Organs 33:568–574PubMedGoogle Scholar
  72. He Y, Li H, Lu X, Stratton CW, Tang YW (2010) Mass spectrometry biotyper system identifies enteric bacterial pathogens directly from colonies grown on selective stool culture media. J Clin Microbiol 48:3888–3892PubMedGoogle Scholar
  73. Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology, 9th edn. Williams & Wilkins, BaltimoreGoogle Scholar
  74. Hsieh S-Y, Tseng C-L, Lee Y-S, Kuo A-J, Sun C-F, Lin Y-H, Chen J-K (2008) Highly efficient classification and identification of human pathogenic bacteria by MALDI-TOF MS. Mol Cell Proteomics 7:448–456PubMedGoogle Scholar
  75. Hull D (1976) Are species really individuals? Syst Zool 25:174–191Google Scholar
  76. Huss VAR, Festl H, Schleifer KH (1983) Studies on the spectrophotometric determination of DNA hybridization from renaturation rates. Syst Appl Microbiol 4:184–192PubMedGoogle Scholar
  77. Huys G, Kämpfer P, Albert MJ, Kuhn I, Denys R, Swings J (2002) Aeromonas hydrophila subsp. dhakensis subsp. nov., isolated from children with diarrhoea in Bangladesh, and extended description of Aeromonas hydrophila subsp. hydrophila Chester 1901 Stanier 1943 Approved Lists 1980. Int J Syst Evol Microbiol 52:705–712PubMedGoogle Scholar
  78. Iino T, Mori K, Uchino Y, Nakagawa T, Harayama S, Suzuki KI (2010) Ignavibacterium album gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from microbial mats at a terrestrial hot spring and proposal of Ignavibacteria classis nov., for a novel lineage at the periphery of green sulfur bacteria. Int J Syst Evol Microbiol 60:1376–1382PubMedGoogle Scholar
  79. Imhoff JF, Süling J, Petri R (1998a) Phylogenetic relationships among the Chromatiaceae, their taxomonic reclassification and description of the new genera Allochromatium, Halochromatium, Isochromatium, Marichromatium, Thiococcus, Thiohalocapsa and Thermochromatium. Int J Syst Bacteriol 48:1129–1143PubMedGoogle Scholar
  80. Imhoff JF, Petri R, Süling J (1998b) Reclassification of species of the spiral-shaped phototrophic purple non-sulfur bacteria of the γ-Proteobacteria: description of the genera Phaeospirillum gen. nov., Rhodovibrio gen. nov., Rhodothalassium gen. nov. and Roseospiragen nov., as well as transfer of Rhodospirillum fulvum to Phaeospirillum fulvum comb. nov., of Rhodospirillum molischianum to Phaeospirillum molischianum comb. nov., of Rhodospirillum salinarum to Rhodovibrion salinarum comb. nov., of Rhodospirillum sodomense to Rhodovibrio sodomensis comb. nov., of Rhodospirillum salexigens to Rhodothalassium salexigens comb. nov. and of Rhodospirillum medosalinum to Roseospira mediosalina. Int J Syst Bacteriol 48:793–798PubMedGoogle Scholar
  81. Istock CA, Bell JA, Ferguson N, Istock NL (1996) Bacterial species and evolution: theoretical and practical perspectives. J Ind Microbiol 17:137–150Google Scholar
  82. Johnson JL (1973) The use of nucleic acid homologies in the taxonomy of anaerobic bacteria. Int J Syst Bacteriol 23:308–315Google Scholar
  83. Kandler O, König H (1985) Cell envelopes of archaebacteria. In: Woese CR, Wolfe RS (eds) Archaebacteria (The bacteria. A treatise on structure and function), vol VIII. Academic, New York, pp 413–457Google Scholar
  84. Kaznowski A (1995) A method of colorimetric DNA-DNA hybridization in microplates with covalently immobilized DNA for identification of Aeromonas sp. Med Microbiol Lett 4:362–369Google Scholar
  85. Klenk HP, Zillig W (1994) DNA-dependent RNA polymerase subunit B as a tool for phylogenetic reconstructions: branching topology of the archaeal domain. J Mol Evol 38:4420–4432Google Scholar
  86. Kloos WE, Mohapatra N, Dobrogosz J, Ezell JW, Manclark CR (1981) Deoxyribonucleotide sequence relatioships among Bordetella species. Int J Syst Bacteriol 31:173–176Google Scholar
  87. Kluyver AJ, van Niel CB (1936) Prospects for a natural system of classification of bacteria. Zbl Bakt Abt 2(94):369–403Google Scholar
  88. Konstantinidis KT, DeLong EF (2008) Genomic patterns of recombination, clonal divergence and environment in marine microbial populations. ISME J 2:1052–1065PubMedGoogle Scholar
  89. Konstantinidis KT, Tiedje JM (2005a) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187:6258–6264PubMedGoogle Scholar
  90. Konstantinidis KT, Tiedje JM (2005b) Genomic insights that advance the species concept for prokaryotes. Proc Natl Acad Sci USA 102:2567–2572PubMedGoogle Scholar
  91. Konstantinidis KT, Tiedje JM (2007) Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 105:504–509Google Scholar
  92. Konstantinidis KT, Ramette A, Tiedje JM (2006) Toward a more robust assessment of intra-species diversity using fewer genetic markers. Appl Environ Microbiol 72:7286–7293PubMedGoogle Scholar
  93. Konstantinidis KT, Braff J, Karl DM, DeLong EF (2009) Comparative metagenomic analysis of a microbial community residing at a depth of 4,000 meters at station ALOHA in the North Pacific subtropical gyre. Appl Environ Microbiol 75:5345–5355PubMedGoogle Scholar
  94. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD (2006) Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23:1891–1901PubMedGoogle Scholar
  95. Lapage SP, Sneath PHA, Lessel EF, Skerman VBD, Seeliger HPR, Clark WA (eds) (1975) International code of nomenclature of bacteria (1975 revision). American Society for Microbiology, Washington, DCGoogle Scholar
  96. Lawrence JG (2002) Gene transfer in bacteria: speciation without species? Theor Popul Biol 61:449–460PubMedGoogle Scholar
  97. Lawrence JG, Ochman H (1998) Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA 95:9413–9417PubMedGoogle Scholar
  98. Lawrence JG, Retchless AC (2009) The interplay of homologous recombination and horizontal gene transfer in bacterial speciation. Methods Mol Biol 532:29–53PubMedGoogle Scholar
  99. Lay JO Jr (2001) MALDI-TOF mass spectrometry of bacteria. Mass Spectrom Rev 20(4):172–194PubMedGoogle Scholar
  100. Lehmann KB, Neumann R (1896) Atlas und Grundriss der Bakteriologie und Lehrbuch der speziellen Bakteriologischen Diagnostik, 1st edn. Munich J.F, LehmannGoogle Scholar
  101. Lester CH, Sandvang D, Olsen SS, Schønheyder HC, Jarløv JO, Bangsborg J, Hansen DS, Jensen TG, Frimodt-Møller N, Hammerum AM, Lester CH, Sandvang D, Olsen SS, Schønheyder HC, Jarløv JO, Bangsborg J, Hansen DS, Jensen TG, Frimodt-Møller N, Hammerum AM, DANRES Study Group (2008) Emergence of ampicillin-resistant Enterococcus faecium in Danish hospitals. J Antimicrob Chemother 62:1203–1206PubMedGoogle Scholar
  102. Lilburn TG, Harrison SH, Cole JR, Garrity GM (2006) Computational aspects of systematic biology. Brief Bioinform 7:186–195PubMedGoogle Scholar
  103. Lind E, Ursing J (1986) Clinical strains of Enterobacter aggomeruns synonyms: Erwinia herbicola,Envinia milletiae identified by DNA-DNA-hybridization. Acta Pathol Microbiol Scand B Microbiol Immunol 94:205–213Google Scholar
  104. Linnaeus C (1753) Species plantarum. HolmiaeGoogle Scholar
  105. Maiden CJM, Dingle KC (2008) Campylobacter. In: Nachamkin I, Szymanski CM, Blaser MJ (eds) Population biology of Campylobacter jejuni and related organisms, 3rd edn. American Society for Microbiology Press, Washington, DC, pp 27–40Google Scholar
  106. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA, Feavers IM, Achtman M, Spratt BG (1996) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA 95:3140–3145Google Scholar
  107. Margulis L (1981) Symbiosis in cell evolution. W.H. Freeman, San FranciscoGoogle Scholar
  108. Maynart-Smith J, Smith NH, O’Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci USA 90:4384–4388Google Scholar
  109. McVean G, Awadalla P, Fearnhead P (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231–1241PubMedGoogle Scholar
  110. Migula W (1900) System der Bakterien. Gustav Fischer, JenaGoogle Scholar
  111. Miller SR, Augustine S, Olson TL, Blankenship RE, Selker J, Wood AM (2005) Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. Proc Natl Acad Sci USA 102:850–855PubMedGoogle Scholar
  112. Moran NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci USA 104:8627–8633PubMedGoogle Scholar
  113. Moreno E (1997) In search of a bacterial species definition. Rev Biol Trop 45:753–771PubMedGoogle Scholar
  114. Naser SM, Thompson FL, Hoste B, Gevers D, Dawyndt P, Vancanneyt M, Swings J (2005) Application of multilocus sequence analysis MLSA for rapid identification of Enterococcus species based on rpoA and pheS genes. Microbiol (Reading) 151:2141–2150Google Scholar
  115. O`Hara RJ (1994) Evolutionary history and the species problem. Amer Zool 34:12–22Google Scholar
  116. Orla-Jensen S (1909) Die Hauptlinien des natürlichen Bakteriensystems. Zbl Bakt Abt 2(22):305–346Google Scholar
  117. Peix A, Valverde A, Rivas R, Igual JM, Ramırez-Bahena M-H, Mateos PF, Santa-Regina I, Rodrıguez-Barrueco C, Martınez-Molina E, Velazquez C (2007) Reclassification of Pseudomonas aurantiaca as a synonym of Pseudomonas chlororaphis and proposal of three subspecies, P. chlororaphis subsp. chlororaphis subsp. nov., P. chlororaphis subsp. aureofaciens subsp. nov., comb. nov. and P. chlororaphis subsp. aurantiaca subsp. nov., comb. nov. Int J Syst Evol Microbiol 57:1286–1290PubMedGoogle Scholar
  118. Prévot AR (1938) Études de systématique bactérienne. Ann Inst Pasteur 60:285–307Google Scholar
  119. Pringsheim EG (1923) Zur Kritik der Bakteriensystematik. Lotus 71:357–377Google Scholar
  120. Prod’hom G, Bizzini A, Durussel C, Bille J, Gilbert Greub G (2011) MALDI-TOF mass spectrometry for direct bacterial identification from positive ammonium chloride lysed blood culture pellets. J Clin Microbiol. doi:10.1128/JCM.01780-09Google Scholar
  121. Rademaker JLW, Hoste B, Louws FJ, Kersters K, Swings J, Vauterin L, Vauterin P, de Bruijn FJ (2000) Comparison of AFLP and rep-PCR genomic fingerprinting with DNA–DNA homology studies: Xanthomonas as a model system. Int J Syst Evol Microbiol 50:665–677PubMedGoogle Scholar
  122. Rainey FA, Stackebrandt E (1993) Phylogenetic evidence for the relationship of Saccharococcus thermophilus to Bacillus thermoglucosidasius, Bacillus kaustophilus and Bacillus stearothermophilus. Syst Appl Microbiol 16:224–226Google Scholar
  123. Relman DA, Strauss E (1999) Microbial genomes: blueprint for life. American Society for Microbiology Press, Washington, DCGoogle Scholar
  124. Reysenbach A-L (2001) Phylum BI. Aquificae phy. nov. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn, The Archaea and the deeply branching and phototrophic bacteria. Springer, New York, pp 359–367Google Scholar
  125. Richter M, Rossello-Mora R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131PubMedGoogle Scholar
  126. Riley M, Buckley M (2008) Large-scale sequencing: the future of genomic sciences? American Society for Microbiology Press, Washington, DCGoogle Scholar
  127. Rodas AM, Ferrer S, Pardo I (2005) Polyphasic study of wine Lactobacillus strains: taxonomic implications. Int J Syst Evol Microbiol 55:197–207PubMedGoogle Scholar
  128. Rong X, Huang Y (2010) Taxonomic evaluation of the Streptomyces griseus clade using multilocus sequence analysis and DNA-DNA hybridization, with proposal to combine 29 species and three subspecies as 11 genomic species. Int J Syst Evol Microbiol 60:696–703PubMedGoogle Scholar
  129. Rong X, Guop Y, Huag Y (2009) Proposal to reclassify the Streptomyces albidoflavus clade on the basis of multilocus sequence analysis and DNA-DNA hybridization, and taxonomic elucidation of Streptomyces griseus subsp. solvifaciens. Syst Appl Microbiol 32:314–322PubMedGoogle Scholar
  130. Rossello-Mora R (2005) Updating prokaryotic taxonomy. J Bacteriol 187:6255–6257PubMedGoogle Scholar
  131. Rosselló-Móra R (2006) DNA-DNA reassociation methods applied to microbial taxonomy and their critical evaluation. In: Stackebrandt E (ed) Molecular identification, systematics, and population structure of prokaryotes. Springer, Berlin, pp 23–50Google Scholar
  132. Rosselló-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67PubMedGoogle Scholar
  133. Rothschild LJ, Ragan A, Coleman AW, Heywood P, Gerbi SA (1986) Are rRNA sequence comparisons the Rosetta stone of phylogeny? Cell 47(5):640PubMedGoogle Scholar
  134. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K et al (2007) The sorcerer II global ocean sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol 5:e77PubMedGoogle Scholar
  135. Scheldeman P, Goossens K, Rodriguez-Diaz M, Pil A, Goris J, Herman L, De Vos P, Logan NA, Heyndrickx M (2004) Paenibacillus lactis sp. nov. isolated from raw and heat-treated milk. Int J Syst Evol Microbiol 54:885–891PubMedGoogle Scholar
  136. Schleifer K-H, Kandler O (1972) The peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477PubMedGoogle Scholar
  137. Schleifer K-H, Stackebrandt E (1983) Molecular systematics of prokaryotes. Annu Rev Microbiol 37:143–187PubMedGoogle Scholar
  138. Schleifer K-H, Leuteritz M, Weiss N, Ludwig W, Kirchhof G, Seidel-Rüfer H (1990) Taxonomic study of anaerobic, Gram-negative, rod-shaped bacteria from breweries: emended description of Pectinatus cerevisiiphilus and description of Pectinatus frisingensis sp. nov., Selenomonas lacticifex sp. nov., Zymophilus raffinosivorans gen. nov., sp. nov., and Zymophilus paucivorans sp. nov. Int J Syst Bacteriol 40:19–27PubMedGoogle Scholar
  139. Schroeter J (1886) Microspira comma. In: Cohn F (ed) Kryprogamen-Flora von Schlesien 3:168Google Scholar
  140. Seewaldt E, Schleifer K-H, Bock E, Stackebrandt E (1982) The close phylogenetic relationship of Nitrobacter and Rhodopseudomonas palustris. Arch Microbiol 131:287–290Google Scholar
  141. Selander RK, Li J, Boyd F, Wang F-S, Nelson K (1994) DNA sequence analysis of the genetic structure of populations of Salmonella enterica and Escherichia coli. In: Priest FG, Ramos-Cormenzana A, Tindall R (eds) Bacterial systematics and diversity. Plenum Press, New York, pp 17–50Google Scholar
  142. Shah HN, Keys CJ, Schmid O, Gharbia SE (2002) Matrix-assisted laser desorption/ionisation time of flight mass spectrometry and proteomics; a new era in anaerobic microbiology. Clin Infect Dis 35:58–64Google Scholar
  143. Sibley CG, Comstock JA, Ahlquist JE (1990) DNA hybridization evidence of homoid phylogeny: a reanalysis of the data. J Mol Evol 30:202–236PubMedGoogle Scholar
  144. Sneath PAH (1989) Analysis and interpretation of sequence data for bacterial systematics: the view of a numerical taxonomist. Syst Appl Microbiol 12:15–31Google Scholar
  145. Stackebrandt E (1992) The prokaryotes. a handbook on the biology of bacteria: ecophysiology, isolation, identification, applications. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) Unifying phylogeny and phenotypic properties. Springer, New York, pp 19–47Google Scholar
  146. Stackebrandt E (2000) The prokaryotes: an evolving electronic resource for the microbiological community. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) Defining taxonomic ranks. Springer, New York, pp 29–57Google Scholar
  147. Stackebrandt E (2010) Diversification and focusing: strategies of microbial culture collections. Trends Microbiol 18:283–287PubMedGoogle Scholar
  148. Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155Google Scholar
  149. Stackebrandt E, Goebel BM (1994) A place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849Google Scholar
  150. Stackebrandt E, Rainey FA (1997) Phylogenetic relationships. In: Rood IJ, McClane BA, Songer JB, Titball RW (eds) The clostridia: molecular biology and pathogenesis. Academic, New York, pp 3–19Google Scholar
  151. Stackebrandt E, Woese CR (1984) The phylogeny of prokaryotes. Microbiol Sci 1:117–122PubMedGoogle Scholar
  152. Stackebrandt E (1985) The significance of "wall types" in phylogenetically based taxonomic studies on actinomycetes. In: Szabó G, Biró S. Goodfellow M (eds) Sixth Int Symp on Actinomycete Biology. Akademiai Kiado, Budapest, pp 497–606Google Scholar
  153. Stackebrandt E, Embley M, Weckesser J (1988) Phylogenetic, evolutionary, and taxonomic aspects of phototrophic eubacteria. In: Olson JM, Ormerod JG, Amesz J, Stackebrandt E, Trüper HG (eds) Green photosynthetic bacteria. Plenum Press, New York, pp 201–215Google Scholar
  154. Stackebrandt E, Tindall B, Ludwig W, Goodfellow M (1999) Prokaryotic diversity and systematics. In: Lengeler J, Drews G, Schlegel HG (eds) Biology of the prokaryotes. Thieme, Stuttgart, pp 675–720Google Scholar
  155. Stackebrandt E, Frederiksen W, Garrity GM, Grimont PAD, Kämpfer P, Maiden MC, Nesme X, Rossello-Mora R, Swings J, Trüper HG, Vauterin L, Ward AC, Whitman WB (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1052PubMedGoogle Scholar
  156. Stackebrandt E, Päuker O, Erhard M (2005) Grouping myxococci (Corallococcus) strains by matrix-assisted laser desorption ionization time-of-flight MALDI TOF mass spectrometry: comparison with gene sequence phylogenies. Curr Microbiol 50:71–77PubMedGoogle Scholar
  157. Staley JT (1997) Biodiversity: are microbial species threatened? Curr Opin Biotechnol 8:340–345PubMedGoogle Scholar
  158. Staley J (2009) The phylogenomics species concept. Microbiol Today 36:82–83Google Scholar
  159. Staley JT, Krieg NR (1984) Bacterial classification I. Classification of prokaryotic organisms: an overview. In: Williams ST, Sharpe ME, Holt JG (eds) Bergey’s manual of systematic bacteriology. Williams & Wilkins, Baltimore, pp 1–4Google Scholar
  160. Stanier RY, van Niel CB (1941) The main outlines of bacterial classification. J Bacteriol 42:437–466PubMedGoogle Scholar
  161. Steigerwalt AG, Fanning GR, Fife-Ashbury MA, Brenner DJ (1976) DNA relatedness among species of Enterobacter and Serratia. Can J Microbiol 22:121–137PubMedGoogle Scholar
  162. Szabados F, Woloszyn J, Richter C, Kaase M, Gatermann SG (2010) A Biotyper 2.0 Bruker Daltonics-based score cut-off of actually 2 is superior to molecular Staphylococcus aureus identification. J Med Microbiol 59:787–790PubMedGoogle Scholar
  163. Thane PR (2009) A critique of prokaryotic species concepts. Methods Mol Biol 532:379–395Google Scholar
  164. Thompson CC, Thompson FL, Vicente ACP (2008) Identification of Vibrio cholerae and Vibrio mimicus by multilocus sequence analysis MLSA. Int J Syst Evol Microbiol 58:617–621PubMedGoogle Scholar
  165. 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 60:249–266PubMedGoogle Scholar
  166. Turenne CY, Collins DM, Alexander DC, Behr MA (2008) Mycobacterium avium subsp. paratuberculosis and M. avium subsp. avium are independently evolved pathogenic clones of a much broader group of M. avium organisms. J Bacteriol 190:2479–2487PubMedGoogle Scholar
  167. Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43PubMedGoogle Scholar
  168. Ullman JS, McCarthy BJ (1973) The relationship between mismatched base pairs and the thermal stability of DNA duplexes. Biochim Biophys Acta 294:416–424PubMedGoogle Scholar
  169. van Baar BL (2000) Characterisation of bacteria by matrix-assisted laser desorption/ionisation and electrospray mass spectrometry. FEMS Microbiol Rev 24:193–219PubMedGoogle Scholar
  170. van Berkum P, Terefework Z, Paulin L, Suomalainen S, Lindström K, Eardly BD (2003) Discordant phylogenies within the rrnl of rhizobia. J Bacteriol 185:2988–2998PubMedGoogle Scholar
  171. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D et al (2004) Environmental genome shotgun sequencing of the Sargasso sea. Science 304:66–74PubMedGoogle Scholar
  172. Wagner M (2009) Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. Annu Rev Microbiol 63:411–429PubMedGoogle Scholar
  173. Ward DM (1998) A natural species concept for prokaryotes. Curr Opin Microbiol 1:271–277PubMedGoogle Scholar
  174. Ward DM (2006) A macrobiological perspective on microbial species. Microbe 1:269–278Google Scholar
  175. Walker DH (1989) Rocky Mountain spotted fever: a new disease in need of microbiological concern. Clin Microbiol Rev 2:227–240PubMedGoogle Scholar
  176. Wayne L, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) International committee on systematic bacteriology: report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464Google Scholar
  177. Winslow C-EA, Broadhurst J, Buchanan RE (1920) The families and genera of the bacteria. J Bacteriol 3:191–229Google Scholar
  178. Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271PubMedGoogle Scholar
  179. Woese CR, Debrunner-Vossbrinck B, Oyaizu H, Stackebrandt E, Ludwig W (1985) Gram-positive bacteria: possible photosynthetic ancestry. Science 229:762–765PubMedGoogle Scholar
  180. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains archaea, bacteria and eucaryas. Proc Natl Acad Sci USA 87:4576–4579PubMedGoogle Scholar
  181. Wolf YI, Rogozin IB, Grishin NV, Tatusov RL, Koonin EV (2001) Genome trees constructed using five different approaches suggest new major bacterial clades. BMC Evol Biol 1:8–28PubMedGoogle Scholar
  182. Yanagida F, Suzuki K-I, Kozaki M, Komagata K (1997) Proposal of Sporolactobacillus nakayamae subsp. nakayamae sp. nov., subsp. nov., Sporolactobacillus nakayamae subsp. racemicus subsp. nov., Sporolactobacillus terrae sp. nov., Sporolactobacillus kofuensis sp. nov., and Sporolactobacillus lactosus sp. nov. Int J Syst Bacteriol 47:499–504Google Scholar
  183. Zawadzki P, Roberts MS, Cohan FM (1995) The log-linear relationship between sexual isolation and sequence divergence in Bacillus transformation is robust. Genetics 140:917–932PubMedGoogle Scholar
  184. Zhu Y, Fournier PE, Eremeeva M, Raoult D (2005) Proposal to create subspecies of Rickettsia conorii based on multi-locus sequence typing and an emended description of Rickettsia conorii. BMC Microbiol 5:11. doi:10.1186/1471-2180-5-11PubMedGoogle Scholar
  185. Ziemke F, Höfle MG, Lalucat J, Rosello-Mora R (1998) Reclassification of Owen’s genomic group II as Shewanella baltica sp. nov. Int J Syst Bacteriol 48:179–186PubMedGoogle Scholar
  186. Zuckerkandl E, Pauling L (1965) Molecules as documents of evolutionary history. J Theor Biol 8:357–366PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Konstantinos T. Konstantinidis
    • 1
  • Erko Stackebrandt
    • 2
  1. 1.School of Civil and Environmental Engineering and School of BiologyGeorgia Institute of TechnologyAtlantaUSA
  2. 2.Leibniz Institute DSMZ-German Collection of Microorganisms and Cell CulturesBraunschweigGermany

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