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. 2013 Jul 19;4(9):664–676. doi: 10.1007/s13238-013-3050-9

Romance of the three domains: how cladistics transformed the classification of cellular organisms

Chi-Chun Ho 1, Susanna K P Lau 1,2,3,4,✉, Patrick C Y Woo 1,2,3,4,✉
PMCID: PMC4875529  PMID: 23873078

Abstract

Cladistics is a biological philosophy that uses genealogical relationship among species and an inferred sequence of divergence as the basis of classification. This review critically surveys the chronological development of biological classification from Aristotle through our postgenomic era with a central focus on cladistics. In 1957, Julian Huxley coined cladogenesis to denote splitting from subspeciation. In 1960, the English translation of Willi Hennig’s 1950 work, Systematic Phylogenetics, was published, which received strong opposition from pheneticists, such as numerical taxonomists Peter Sneath and Robert Sokal, and evolutionary taxonomist, Ernst Mayr, and sparked acrimonious debates in 1960–1980. In 1977–1990, Carl Woese pioneered in using small subunit rRNA gene sequences to delimitate the three domains of cellular life and established major prokaryotic phyla. Cladistics has since dominated taxonomy. Despite being compatible with modern microbiological observations, i.e. organisms with unusual phenotypes, restricted expression of characteristics and occasionally being uncultivable, increasing recognition of pervasiveness and abundance of horizontal gene transfer has challenged relevance and validity of cladistics. The mosaic nature of eukaryotic and prokaryotic genomes was also gradually discovered. In the mid-2000s, high-throughput and whole-genome sequencing became routine and complex geneologies of organisms have led to the proposal of a reticulated web of life. While genomics only indirectly leads to understanding of functional adaptations to ecological niches, computational modeling of entire organisms is underway and the gap between genomics and phenetics may soon be bridged. Controversies are not expected to settle as taxonomic classifications shall remain subjective to serve the human scientist, not the classified.

Keywords: cladistics, phenetics, phylogeny, classification, evolution

Contributor Information

Susanna K. P. Lau, Email: skplau@hkucc.hku.hk

Patrick C. Y. Woo, Email: pcywoo@hkucc.hku.hk

References

  1. (161 1). THE HOLY BIBLE, Conteyning the Old Testament, AND THE NEW: Newly Translated out of the Originall tongues: & with the former Translations diligently compared and revised, by his Majesties speciall Comandement. Appointed to be read in Churches. (London, Robert Barker).
  2. Abby SS, Tannier E, Gouy M, Daubin V. Detecting lateral gene transfers by statistical reconciliation of phylogenetic forests. BMC Bioinformatics. 2010;11:324. doi: 10.1186/1471-2105-11-324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Abby SS, Tannier E, Gouy M, Daubin V. Lateral gene transfer as a support for the tree of life. Proc Natl Acad Sci U S A. 2012;109:4962–4967. doi: 10.1073/pnas.1116871109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Achenbach-Richter L, Gupta R, Zillig W, Woese CR. Rooting the archaebacterial tree: the pivotal role of Thermococcus celer in archaebacterial evolution. Syst Appl Microbiol. 1988;10:231–240. doi: 10.1016/s0723-2020(88)80007-9. [DOI] [PubMed] [Google Scholar]
  5. Adl SM, Leander BS, Simpson AG, Archibald JM, Anderson OR, Bass D, Bowser SS, Brugerolle G, Farmer MA, Karpov S, et al. Diversity, nomenclature, and taxonomy of protists. Syst Biol. 2007;56:684–689. doi: 10.1080/10635150701494127. [DOI] [PubMed] [Google Scholar]
  6. Ashlock PD. The uses of cladistics. Annu Rev Ecol Systemat. 1974;5:81–99. [Google Scholar]
  7. Avise JC. Systematic value of electrophoretic data. Syst Biol. 1974;23:465–481. [Google Scholar]
  8. Balch WE, Magrum LJ, Fox GE, Wolfe RS, Woese CR. An ancient divergence among the bacteria. J Mol Evol. 1977;9:305–311. doi: 10.1007/BF01796092. [DOI] [PubMed] [Google Scholar]
  9. Baldauf SL, Palmer JD, Doolittle WF. The root of the universal tree and the origin of eukaryotes based on elongation factor phylogeny. Proc Natl Acad Sci U S A. 1996;93:7749–7754. doi: 10.1073/pnas.93.15.7749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bapteste E, Brochier C. On the conceptual difficulties in rooting the tree of life. Trends Microbiol. 2004;12:9–13. doi: 10.1016/j.tim.2003.11.002. [DOI] [PubMed] [Google Scholar]
  11. Bapteste E, Walsh DA. Does the ‘Ring of Life’ ring true? Trends Microbiol. 2005;13:256–261. doi: 10.1016/j.tim.2005.03.012. [DOI] [PubMed] [Google Scholar]
  12. Boyden A. Homology and analogy. a critical review of the meanings and implications of these concepts in biology. Amer Mid Natur. 1947;37:648–669. [Google Scholar]
  13. Branfield P, Potter S. Edexcel IGCSE biology. Pearson: Harlow; 2009. [Google Scholar]
  14. Brenner D, Staley J, Krieg N. Classification of prokaryotic organisms and the concept of bacterial speciation. In: Brenner D, Krieg N, Staley J, Garrity G, editors. Bergey’s manual of systematic bacteriology. 2005. pp. 27–32. [Google Scholar]
  15. Bridge PD, Sneath PH. Numerical taxonomy of Streptococcus. J Gen Microbiol. 1983;129:565–597. doi: 10.1099/00221287-129-3-565. [DOI] [PubMed] [Google Scholar]
  16. Broom A, Sneath PH. Numerical taxonomy of Haemophilus. J Gen Microbiol. 1981;126:123–149. doi: 10.1099/00221287-126-1-123. [DOI] [PubMed] [Google Scholar]
  17. Brown JR, Doolittle WF. Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications. Proc Natl Acad Sci U S A. 1995;92:2441–2445. doi: 10.1073/pnas.92.7.2441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Brundin L. With a monograph of the subfamilies Podonominae and Aphroteniinae and the austral Heptagyiae. 1966. Transantarctic relationships and their significance, as evidenced by chironomid midges. [Google Scholar]
  19. Burggraf S, Fricke H, Neuner A, Kristjansson J, Rouvier P, Mandelco L, Woese CR, Stetter KO. Methanococcus igneus sp. nov., a novel hyperthermophilic methanogen from a shallow submarine hydrothermal system. Syst Appl Microbiol. 1990;13:263–269. doi: 10.1016/s0723-2020(11)80197-9. [DOI] [PubMed] [Google Scholar]
  20. Burkholder JM, Glasgow HB., Jr. Trophic controls on stage transformations of a toxic ambush-predator dinoflagellate. J Eukaryot Microbiol. 1997;44:200–205. doi: 10.1111/j.1550-7408.1997.tb05700.x. [DOI] [PubMed] [Google Scholar]
  21. Caetano-Anolles G. Evolved RNA secondary structure and the rooting of the universal tree of life. J Mol Evol. 2002;54:333–345. doi: 10.1007/s00239-001-0048-3. [DOI] [PubMed] [Google Scholar]
  22. Cammarano P, Palm P, Creti R, Ceccarelli E, Sanangelantoni AM, Tiboni O. Early evolutionary relationships among known life forms inferred from elongation factor EF-2/EF-G sequences: phylogenetic coherence and structure of the archaeal domain. J Mol Evol. 1992;34:396–405. doi: 10.1007/BF00162996. [DOI] [PubMed] [Google Scholar]
  23. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–552. doi: 10.1093/oxfordjournals.molbev.a026334. [DOI] [PubMed] [Google Scholar]
  24. Cavalier-Smith T. Only six kingdoms of life. Proc Biol Sci. 2004;271:1251–1262. doi: 10.1098/rspb.2004.2705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Chan JF, Lau SK, Curreem SO, To KK, Leung SS, Cheng VC, Yuen KY, Woo PC. First report of spontaneous intrapartum Atopobium vaginae bacteremia. J Clin Microbiol. 2012;50:2525–2528. doi: 10.1128/JCM.00212-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009;37:D141–145. doi: 10.1093/nar/gkn879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Colwell RR. Polyphasic taxonomy of the genus vibrio: numerical taxonomy of Vibrio cholerae, Vibrio parahaemolyticus, and related Vibrio species. J Bacteriol. 1970;104:410–433. doi: 10.1128/jb.104.1.410-433.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Dagan T, Roettger M, Bryant D, Martin W. Genome networks root the tree of life between prokaryotic domains. Genome Biol Evol. 2010;2:379–392. doi: 10.1093/gbe/evq025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Darwin C. On the origin of species by means of natural selection. 1859. [Google Scholar]
  30. Deppenmeier U, Johann A, Hartsch T, Merkl R, Schmitz RA, Martinez-Arias R, Henne A, Wiezer A, Baumer S, Jacobi C, et al. The genome of Methanosarcina mazei: evidence for lateral gene transfer between bacteria and archaea. J Mol Microbiol Biotechnol. 2002;4:453–461. [PubMed] [Google Scholar]
  31. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–5072. doi: 10.1128/AEM.03006-05. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Doolittle WF, Brown JR. Tempo, mode, the progenote, and the universal root. Proc Natl Acad Sci U S A. 1994;91:6721–6728. doi: 10.1073/pnas.91.15.6721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Edgar R, Asimenos G, Batzoglou S, Sidow A. Evolver: a whole-genome sequence evolution simulator. 2013. [Google Scholar]
  34. Federhen S. The NCBI Taxonomy database. Nucleic Acids Res. 2012;40:D136–143. doi: 10.1093/nar/gkr1178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Field KG, Olsen GJ, Lane DJ, Giovannoni SJ, Ghiselin MT, Raff EC, Pace NR, Raff RA. Molecular phylogeny of the animal kingdom. Science. 1988;239:748–753. doi: 10.1126/science.3277277. [DOI] [PubMed] [Google Scholar]
  36. Forterre P, Philippe H. Where is the root of the universal tree of life? Bioessays. 1999;21:871–879. doi: 10.1002/(SICI)1521-1878(199910)21:10<871::AID-BIES10>3.0.CO;2-Q. [DOI] [PubMed] [Google Scholar]
  37. Fournier GP, Gogarten JP. Rooting the ribosomal tree of life. Mol Biol Evol. 2010;27:1792–1801. doi: 10.1093/molbev/msq057. [DOI] [PubMed] [Google Scholar]
  38. Fox GE, Magrum LJ, Balch WE, Wolfe RS, Woese CR. Classification of methanogenic bacteria by 16S ribosomal RNA characterization. Proc Natl Acad Sci U S A. 1977;74:4537–4541. doi: 10.1073/pnas.74.10.4537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Golding GB, Gupta RS. Protein-based phylogenies support a chimeric origin for the eukaryotic genome. Mol Biol Evol. 1995;12:1–6. doi: 10.1093/oxfordjournals.molbev.a040178. [DOI] [PubMed] [Google Scholar]
  40. Graur D, Li W-H. Fundamentals of molecular evolution. 2nd edn. Sunderland, Massachusetts, USA.: Sinauer Associates; 2000. [Google Scholar]
  41. Gribaldo S, Cammarano P. The root of the universal tree of life inferred from anciently duplicated genes encoding components of the protein-targeting machinery. J Mol Evol. 1998;47:508–516. doi: 10.1007/pl00006407. [DOI] [PubMed] [Google Scholar]
  42. Gribaldo S, Philippe H. Ancient phylogenetic relationships. Theor Popul Biol. 2002;61:391–408. doi: 10.1006/tpbi.2002.1593. [DOI] [PubMed] [Google Scholar]
  43. Gupta R, Lanter JM, Woese CR. Sequence of the 16S ribosomal RNA from Halobacterium volcanii, an archaebacterium. Science. 1983;221:656–659. doi: 10.1126/science.221.4611.656. [DOI] [PubMed] [Google Scholar]
  44. Gupta RS. Protein phylogenies and signature sequences: A reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev. 1998;62:1435–1491. doi: 10.1128/mmbr.62.4.1435-1491.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y, Sugahara J, Preston C, de la Torre J, Richardson PM, DeLong EF. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci U S A. 2006;103:18296–18301. doi: 10.1073/pnas.0608549103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Hennig W. Grundzüge einer Theorie der phylogenetischen Systematik. Berlin: Deutscher zentralverlag; 1950. [Google Scholar]
  47. Hennig W. Phylogenetic Systematics. Annu Rev Entomol. 1965;10:97–116. [Google Scholar]
  48. Hennig W. Phylogenetic systematics. Urbana: University of Illinois Press; 1966. [Google Scholar]
  49. Ho CC, Wu AK, Tse CW, Yuen KY, Lau SK, Woo PC. Automated pangenomic analysis in target selection for PCR detection and identification of bacteria by use of ssGeneFinder Webserver and its application to Salmonella enterica serovar Typhi. J Clin Microbiol. 2012;50:1905–1911. doi: 10.1128/JCM.06843-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Ho CC, Yuen KY, Lau SK, Woo PC. Rapid identification and validation of specific molecular targets for detection of Escherichia coli O104:H4 outbreak strain by use of high-throughput sequencing data from nine genomes. J Clin Microbiol. 2011;49:3714–3716. doi: 10.1128/JCM.05062-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Hongoh Y, Sharma VK, Prakash T, Noda S, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M, Ohkuma M. Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. Proc Natl Acad Sci U S A. 2008;105:5555–5560. doi: 10.1073/pnas.0801389105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Hongoh Y, Sharma VK, Prakash T, Noda S, Toh H, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M, et al. Genome of an endosymbiont coupling N2 fixation to cellulolysis within protest cells in termite gut. Science. 2008;322:1108–1109. doi: 10.1126/science.1165578. [DOI] [PubMed] [Google Scholar]
  53. Hubbs CL. Concepts of homology and analogy. Amer Nat. 1944;78:289–307. [Google Scholar]
  54. Huxley J. The three types of evolutionary process. Nature. 1957;180:454–455. [Google Scholar]
  55. Huxley, J. (1959). Clades and grades. in function and taxonomic importance: a symposium. Cain, A.J. ed. (London, Systematics Association).
  56. Hyer BH, McCarthy BJ, Bolton ET. A molecular approach in the systematics of higher organisms. dna interactions provide a basis for detecting common polynucleotide sequences among diverse organisms. Science. 1964;144:959–967. doi: 10.1126/science.144.3621.959. [DOI] [PubMed] [Google Scholar]
  57. Iwabe N, Kuma K, Hasegawa M, Osawa S, Miyata T. Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci U S A. 1989;86:9355–9359. doi: 10.1073/pnas.86.23.9355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Johnson ML, Wicks MJ. Serum Protein Electrophoresis in Mammals-Taxonomic Implications. Syst Biol. 1959;8:88–95. [Google Scholar]
  59. Jones JH, Card W, Chapman M, Lennard-Jones JE, Morson BC, Sackin MJ, Sneath PH. The application of numerical taxonomy to the separation of cllonic inflammatory disease. Gut. 1970;11:1062. [PubMed] [Google Scholar]
  60. Jones JH, Lennard-Jones JE, Morson BC, Chapman M, Sackin MJ, Sneath PH, Spicer CC, Card WI. Numerical taxonomy and discriminant analysis applied to non-specific colitis. Q J Med. 1973;42:715–732. [PubMed] [Google Scholar]
  61. Karr JR, Sanghvi JC, Macklin DN, Gutschow MV, Jacobs JM, Bolival B, Jr., Assad-Garcia N, Glass JI, Covert MW. A whole-cell computational model predicts phenotype from genotype. Cell. 2012;150:389–401. doi: 10.1016/j.cell.2012.05.044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, Roger AJ, Gray MW. The tree of eukary otes. Trends Ecol Evol. 2005;20:670–676. doi: 10.1016/j.tree.2005.09.005. [DOI] [PubMed] [Google Scholar]
  63. Kennedy SP, Ng WV, Salzberg SL, Hood L, DasSarma S. Understanding the adaptation of Halobacterium species NRC-1 to its extreme environment through computational analysis of its genome sequence. Genome Res. 2001;11:1641–1650. doi: 10.1101/gr.190201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Koonin EV, Wolf YI. Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res. 2008;36:6688–6719. doi: 10.1093/nar/gkn668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Kunin V, Goldovsky L, Darzentas N, Ouzounis CA. The net of life: reconstructing the microbial phylogenetic network. Genome Res. 2005;15:954–959. doi: 10.1101/gr.3666505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Lake JA, Rivera MC. Deriving the genomic tree of life in the presence of horizontal gene transfer: conditioned reconstruction. Mol Biol Evol. 2004;21:681–690. doi: 10.1093/molbev/msh061. [DOI] [PubMed] [Google Scholar]
  67. Lake JA, Servin JA, Herbold CW, Skophammer RG. Evidence for a new root of the tree of life. Syst Biol. 2008;57:835–843. doi: 10.1080/10635150802555933. [DOI] [PubMed] [Google Scholar]
  68. Lake JA, Skophammer RG, Herbold CW, Servin JA. Genome beginnings: rooting the tree of life. Philos. Trans R Soc Lond B Biol Sci. 2009;364:2177–2185. doi: 10.1098/rstb.2009.0035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Lau SK, Curreem SO, Ngan AH, Yeung CK, Yuen KY, Woo PC. First report of disseminated Mycobacterium skin infections in two liver transplant recipients and rapid diagnosis by hsp65 gene sequencing. J Clin Microbiol. 2011;49:3733–3738. doi: 10.1128/JCM.05088-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Lau SK, Lee P, Tsang AK, Yip CC, Tse H, Lee RA, So LY, Lau YL, Chan KH, Woo PC, et al. Molecular epidemiology of human coronavirus OC43 reveals evolution of different genotypes over time and recent emergence of a novel genotype due to natural recombination. J Virol. 2011;85:11325–11337. doi: 10.1128/JVI.05512-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Lau SK, Li KS, Huang Y, Shek CT, Tse H, Wang M, Choi GK, Xu H, Lam CS, Guo R, et al. Ecoepidemiology and complete genome comparison of different strains of severe acute respiratory syndrome-related Rhinolophus bat coronavirus in China reveal bats as a reservoir for acute, self-limiting infection that allows recombination events. J Virol. 2010;84:2808–2819. doi: 10.1128/JVI.02219-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Lau SK, Ng KH, Woo PC, Yip KT, Fung AM, Woo GK, Chan KM, Que TL, Yuen KY. Usefulness of the Micro-Seq 500 16S rDNA bacterial identification system for identification of anaerobic Gram positive bacilli isolated from blood cultures. J Clin Pathol. 2006;59:219–222. doi: 10.1136/jcp.2004.025247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Lau SK, Woo PC, Chan CY, Woo WL, Woo GK, Yuen KY. Typhoid fever associated with acute appendicitis caused by an H1-j strain of Salmonella enterica serotype Typhi. J Clin Microbiol. 2005;43:1470–1472. doi: 10.1128/JCM.43.3.1470-1472.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Lau SK, Woo PC, Luk WK, Fung AM, Hui WT, Fong AH, Chow CW, Wong SS, Yuen KY. Clinical isolates of Streptococcus iniae from Asia are more mucoid and beta-hemolytic than those from North America. Diagn Microbiol Infect Dis. 2006;54:177–181. doi: 10.1016/j.diagmicrobio.2005.09.012. [DOI] [PubMed] [Google Scholar]
  75. Lau SK, Woo PC, Yip CC, Li KS, Fu CT, Huang Y, Chan KH, Yuen KY. Co-existence of multiple strains of two novel porcine bocaviruses in the same pig, a previously undescribed phenomenon in members of the family Parvoviridae, and evidence for inter- and intra-host genetic diversity and recombination. J Gen Virol. 2011;92:2047–2059. doi: 10.1099/vir.0.033688-0. [DOI] [PubMed] [Google Scholar]
  76. Lawson FS, Charlebois RL, Dillon JA. Phylogenetic analysis of carbamoylphosphate synthetase genes: complex evolutionary history includes an internal duplication within a gene which can root the tree of life. Mol Biol Evol. 1996;13:970–977. doi: 10.1093/oxfordjournals.molbev.a025665. [DOI] [PubMed] [Google Scholar]
  77. Li WH, Tanimura M. The molecular clock runs more slowly in man than in apes and monkeys. Nature. 1987;326:93–96. doi: 10.1038/326093a0. [DOI] [PubMed] [Google Scholar]
  78. Linnaeus C. The root of the tree of life in the light of the covarion model. J Mol Evol. 1751;49:496–508. doi: 10.1007/pl00006572. [DOI] [PubMed] [Google Scholar]
  79. Ludwig W, Klenk H-P. Overview: a phylogenetic backbone and taxonomic framework for procaryotic systematics. In: Brenner D, Krieg N, Staley J, Garrity G, editors. Bergey’s manual of systematic bacteriology. 2005. pp. 49–66. [Google Scholar]
  80. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363–1371. doi: 10.1093/nar/gkh293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Magrum LJ, Luehrsen KR, Woese CR. Are extreme halophiles actually “bacteria”? J Mol Evol. 1978;11:1–8. doi: 10.1007/BF01768019. [DOI] [PubMed] [Google Scholar]
  82. Margoliash E, Smith EL, Kreil G, Tuppy H. Amino-acid sequence of horse heart cytochrome c. Nature. 1961;192:1125–1127. doi: 10.1038/1921125a0. [DOI] [PubMed] [Google Scholar]
  83. Mayr E. Cladistic analysis or cladistic classification. Zeitschrift für zoologische Systematik und Evolutionsforschung. 1974;12:94–128. [Google Scholar]
  84. Mayr E. Biological classification: toward a synthesis of opposing methodologies. Science. 1981;214:510–516. doi: 10.1126/science.214.4520.510. [DOI] [PubMed] [Google Scholar]
  85. McCarthy BJ, Bolton ET. An approach to the measurement of genetic relatedness among organisms. Proc Natl Acad Sci U S A. 1963;50:156–164. doi: 10.1073/pnas.50.1.156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. McDade L. Hybrids and phylogenetic systematics i. patterns of character expression in hybrids and their implications for cladistic analysis. Evolution. 1990;44:1685–1700. doi: 10.1111/j.1558-5646.1990.tb03856.x. [DOI] [PubMed] [Google Scholar]
  87. McDade LA. Hybrids and phylogenetic systematics ii. the impact of hybrids on cladistic analysis. Evolution. 1992;46:1329–1346. doi: 10.1111/j.1558-5646.1992.tb01127.x. [DOI] [PubMed] [Google Scholar]
  88. Medlin L, Elwood HJ, Stickel S, Sogin ML. The characterization of enzymatically amplified eukaryotic 16S-like rRNAcoding regions. Gene. 1988;71:491–499. doi: 10.1016/0378-1119(88)90066-2. [DOI] [PubMed] [Google Scholar]
  89. Myers GS. The nature of systematic biology and of a species description. Syst Zool. 1952;1:106–111. [Google Scholar]
  90. Noller HF, Woese CR. Secondary structure of 16S ribosomal RNA. Science. 1981;212:403–411. doi: 10.1126/science.6163215. [DOI] [PubMed] [Google Scholar]
  91. Olsen GJ, Overbeek R, Larsen N, Marsh TL, McCaughey MJ, Maciukenas MA, Kuan WM, Macke TJ, Xing Y, Woese CR. The ribosomal database project. Nucleic Acids Res. 1992;20(Suppl):2199–2200. doi: 10.1093/nar/20.suppl.2199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Olsen GJ, Pace NR, Nuell M, Kaine BP, Gupta R, Woese CR. Sequence of the 16S rRNA gene from the thermoacidophilic archaebacterium Sulfolobus solfataricus and its evolutionary implications. J Mol Evol. 1985;22:301–307. doi: 10.1007/BF02115685. [DOI] [PubMed] [Google Scholar]
  93. Oyaizu H, Debrunner-Vossbrinck B, Mandelco L, Studier JA, Woese CR. The green non-sulfur bacteria: A deep branching in the eubacterial line of descent. Syst Appl Microbiol. 1987;9:47–53. doi: 10.1016/s0723-2020(87)80055-3. [DOI] [PubMed] [Google Scholar]
  94. Oyaizu H, Woese CR. Phylogenetic relationships among the sulfate respiring bacteria, myxobacteria and purple bacteria. Syst Appl Microbiol. 1985;6:257–263. [Google Scholar]
  95. Page RDM, Holmes EC. Molecular evolution: a phylogenetic approach. Oxford; Malden, MA: Blackwell Science; 1998. [Google Scholar]
  96. Paster BJ, Ludwig W, Weisburg WG, Stackebrandt E, Hespell RB, Hahn CM, Reichenbach H, Stetter KO, Woese CR. A phylogenetic grouping of the Bacteroides, Cytophagas, and certain Flavobacteria. Syst Appl Microbiol. 1985;6:34–42. [Google Scholar]
  97. Paster BJ, Stackebrandt E, Hespell RB, Hahn CM, Woese CR. The phylogeny of the spirochetes. Syst Appl Microbiol. 1984;5:337–351. doi: 10.1016/s0723-2020(84)80034-x. [DOI] [PubMed] [Google Scholar]
  98. Philippe H, Forterre P. The rooting of the universal tree of life is not reliable. J Mol Evol. 1999;49:509–523. doi: 10.1007/pl00006573. [DOI] [PubMed] [Google Scholar]
  99. Posada D, Crandall KA. Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol. 2001;16:37–45. doi: 10.1016/s0169-5347(00)02026-7. [DOI] [PubMed] [Google Scholar]
  100. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35:7188–7196. doi: 10.1093/nar/gkm864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Puigbo P, Wolf YI, Koonin EV. Search for a ‘Tree of Life’ in the thicket of the phylogenetic forest. J Biol. 2009;8:59. doi: 10.1186/jbiol159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Razin S. Comparative genomics of mycoplasmas. Wien Klin Wochenschr. 1997;109:551–556. [PubMed] [Google Scholar]
  103. Rensch B. Neuere Probleme der Abstammungslehre: die transspezifische Evolution, 2., stark verä nderte Aufl. edn. Stuttgart: F. Enke; 1954. [Google Scholar]
  104. Ribeiro S, Golding GB. The mosaic nature of the eukaryotic nucleus. Mol Biol Evol. 1998;15:779–788. doi: 10.1093/oxfordjournals.molbev.a025983. [DOI] [PubMed] [Google Scholar]
  105. Saccone C, Gissi C, Lanave C, Pesole G. Molecular classification of living organisms. J Mol Evol. 1995;40:273–279. doi: 10.1007/BF00163232. [DOI] [PubMed] [Google Scholar]
  106. Salichos L, Rokas A. Inferring ancient divergences requires genes with strong phylogenetic signals. Nature. 2013;497:327–331. doi: 10.1038/nature12130. [DOI] [PubMed] [Google Scholar]
  107. Sanger F, Donelson JE, Coulson AR, Kossel H, Fischer D. Use of DNA polymerase I primed by a synthetic oligonucleotide to determine a nucleotide sequence in phage flDNA. Proc Natl Acad Sci U S A. 1973;70:1209–1213. doi: 10.1073/pnas.70.4.1209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977;74:5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Schliep K, Lopez P, Lapointe FJ, Bapteste E. Harvesting evolutionary signals in a forest of prokaryotic gene trees. Mol Biol Evol. 2011;28:1393–1405. doi: 10.1093/molbev/msq323. [DOI] [PubMed] [Google Scholar]
  110. Sicheritz-Ponten T, Andersson SG. A phylogenomic approach to microbial evolution. Nucleic Acids Res. 2001;29:545–552. doi: 10.1093/nar/29.2.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. Simpson AGB, Roger AJ. The real’ kingdoms’ of eukaryotes. Curr Biol. 2004;14:R693–R696. doi: 10.1016/j.cub.2004.08.038. [DOI] [PubMed] [Google Scholar]
  112. Sneath PH, Sokal RR. Numerical taxonomy. Nature. 1962;193:855–860. doi: 10.1038/193855a0. [DOI] [PubMed] [Google Scholar]
  113. Sneath PH, Stevens M, Sackin MJ. Numerical taxonomy of Pseudomonas based on published records of substrate utilization. Antonie van Leeuwenhoek. 1981;47:423–448. doi: 10.1007/BF00426004. [DOI] [PubMed] [Google Scholar]
  114. Sneath PHA. Thirty years of numerical taxonomy. Syst Biol. 1995;44:281–298. [Google Scholar]
  115. Sokal RRSPHA. Principles of numerical taxonomy. San Francisco: Freeman; 1963. [Google Scholar]
  116. Sun FJ, Caetano-Anolles G. The evolutionary history of the structure of 5S ribosomal RNA. J Mol Evol. 2009;69:430–443. doi: 10.1007/s00239-009-9264-z. [DOI] [PubMed] [Google Scholar]
  117. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56:564–577. doi: 10.1080/10635150701472164. [DOI] [PubMed] [Google Scholar]
  118. Theißen G. Orthology: secret life of genes. Nature. 2002;415:741–741. doi: 10.1038/415741a. [DOI] [PubMed] [Google Scholar]
  119. Titsworth E, Grunberg E, Beskid G, Cleeland R, Jr., Delorenzo WF. Efficiency of a multitest system (Enterotube) for rapid identification of Enterobacteriaceae. Appl Microbiol. 1969;18:207–213. doi: 10.1128/am.18.2.207-213.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Tse H, Tsang AK, Tsoi HW, Leung AS, Ho CC, Lau SK, Woo PC, Yuen KY. Identification of a novel bat papillomavirus by metagenomics. PLoS ONE. 2012;7:e43986. doi: 10.1371/journal.pone.0043986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. US National Library of Medicine (2006). Genetic Speciation.
  122. Valas RE, Bourne PE. The origin of a derived superkingdom: how a gram-positive bacterium crossed the desert to become an archaeon. Biol Direct. 2011;6:16. doi: 10.1186/1745-6150-6-16. [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. Washington JA, 2nd, Yu PK, Martin WJ. Evaluation of accuracy of multitest micromethod system for identification of Enterobacteriaceae. Appl Microbiol. 1971;22:267–269. doi: 10.1128/am.22.3.267-269.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  124. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991;173:697–703. doi: 10.1128/jb.173.2.697-703.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  125. Weisburg WG, Giovannoni SJ, Woese CR. The Deinococcus-Thermus phylum and the effect of rRNA composition on phylogenetic tree construction. Syst Appl Microbiol. 1989;11:128–134. doi: 10.1016/s0723-2020(89)80051-7. [DOI] [PubMed] [Google Scholar]
  126. Williams DM, Ebach MC. What, exactly, is cladistics? Re-writing the history of systematics and biogeography. Acta Biotheor. 2009;57:249–268. doi: 10.1007/s10441-008-9058-5. [DOI] [PubMed] [Google Scholar]
  127. Woese CR. A proposal concerning the origin of life on the planet earth. J Mol Evol. 1979;13:95–101. doi: 10.1007/BF01732865. [DOI] [PubMed] [Google Scholar]
  128. Woese CR. Interpreting the universal phylogenetic tree. Proc Natl Acad Sci U S A. 2000;97:8392–8396. doi: 10.1073/pnas.97.15.8392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Woese CR, Fox GE. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A. 1977;74:5088–5090. doi: 10.1073/pnas.74.11.5088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Woese CR, Gupta R, Hahn CM, Zillig W, Tu J. The phylogenetic relationships of three sulfur dependent archaebacteria. Syst Appl Microbiol. 1984;5:97–105. doi: 10.1016/s0723-2020(84)80054-5. [DOI] [PubMed] [Google Scholar]
  131. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990;87:4576–4579. doi: 10.1073/pnas.87.12.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  132. Woese CR, Magrum LJ, Fox GE. Archaebacteria. J Mol Evol. 1978;11:245–251. doi: 10.1007/BF01734485. [DOI] [PubMed] [Google Scholar]
  133. Woese CR, Magrum LJ, Gupta R, Siegel RB, Stahl DA, Kop J, Crawford N, Brosius J, Gutell R, Hogan JJ, et al. Secondary structure model for bacterial 16S ribosomal RNA: phylogenetic, enzymatic and chemical evidence. Nucleic Acids Res. 1980;8:2275–2293. doi: 10.1093/nar/8.10.2275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  134. Woese CR, Maloy S, Mandelco L, Raj HD. Phylogenetic placement of the Spirosomaceae. Syst Appl Microbiol. 1990;13:19–23. doi: 10.1016/S0723-2020(11)80175-X. [DOI] [PubMed] [Google Scholar]
  135. Woese CR, Mandelco L, Yang D, Gherna R, Madigan MT. The case for relationship of the flavobacteria and their relatives to the green sulfur bacteria. Syst Appl Microbiol. 1990;13:258–262. doi: 10.1016/s0723-2020(11)80196-7. [DOI] [PubMed] [Google Scholar]
  136. Woese CR, Maniloff J, Zablen LB. Phylogenetic analysis of the mycoplasmas. Proc Natl Acad Sci U S A. 1980;77:494–498. doi: 10.1073/pnas.77.1.494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Woese CR, Stackebrandt E, Weisburg WG, Paster BJ, Madigan MT, Fowler VJ, Hahn CM, Blanz P, Gupta R, Nealson KH, et al. The phylogeny of purple bacteria: The alpha subdivision. Syst Appl Microbiol. 1984;5:315–326. doi: 10.1016/s0723-2020(84)80034-x. [DOI] [PubMed] [Google Scholar]
  138. Woese CR, Weisburg WG, Hahn CM, Paster BJ, Zablen LB, Lewis BJ, Macke TJ, Ludwig W, Stackebrandt E. The phylogeny of purple bacteria: The gamma subdivision. Syst Appl Microbiol. 1985;6:25–33. [Google Scholar]
  139. Woese CR, Yang D, Mandelco L, Stetter KO. The flexibacter-flavobacter connection. Syst Appl Microbiol. 1990;13:161–165. [Google Scholar]
  140. Woo PC, Chong KT, Tse H, Cai JJ, Lau CC, Zhou AC, Lau SK, Yuen KY. Genomic and experimental evidence for a potential sexual cycle in the pathogenic thermal dimorphic fungus Penicillium marneffei. FEBS Lett. 2006;580:3409–3416. doi: 10.1016/j.febslet.2006.05.014. [DOI] [PubMed] [Google Scholar]
  141. Woo PC, Fung AM, Wong SS, Tsoi HW, Yuen KY. Isolation and characterization of a Salmonella enterica serotype Typhi variant and its clinical and public health implications. J Clin Microbiol. 2001;39:1190–1194. doi: 10.1128/JCM.39.3.1190-1194.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. Woo PC, Lam CW, Tam EW, Leung CK, Wong SS, Lau SK, Yuen KY. First discovery of two polyketide synthase genes for mitorubrinic acid and mitorubrinol yellow pigment biosynthesis and implications in virulence of Penicillium marneffei. PLoS Negl Trop Dis. 2012;6:e1871. doi: 10.1371/journal.pntd.0001871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  143. Woo PC, Lau SK, Huang Y, Yuen KY. Coronavirus diversity, phylogeny and interspecies jumping. Exp Biol Med (Maywood) 2009;234:1117–1127. doi: 10.3181/0903-MR-94. [DOI] [PubMed] [Google Scholar]
  144. Woo PC, Lau SK, Teng JL, Tse H, Yuen KY. Then and now: use of 16S rDNA gene sequencing for bacterial identification and discovery of novel bacteria in clinical microbiology laboratories. Clin Microbiol Infect. 2008;14:908–934. doi: 10.1111/j.1469-0691.2008.02070.x. [DOI] [PubMed] [Google Scholar]
  145. Woo PC, Lau SK, Woo GK, Fung AM, Ngan AH, Hui WT, Yuen KY. Seronegative bacteremic melioidosis caused by Burkholderia pseudomallei with ambiguous biochemical profile: clinical importance of accurate identification by 16S rRNA gene and groEL gene sequencing. J Clin Microbiol. 2003;41:3973–3977. doi: 10.1128/JCM.41.8.3973-3977.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  146. Woo PC, Leung PK, Leung KW, Yuen KY. Identification by 16S ribosomal RNA gene sequencing of an Enterobacteriaceae species from a bone marrow transplant recipient. Mol Pathol. 2000;53:211–215. doi: 10.1136/mp.53.4.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  147. Woo PC, Leung PK, Wong SS, Ho PL, Yuen KY. groEL encodes a highly antigenic protein in Burkholderia pseudomallei. Clin Diagn Lab Immunol. 2001;8:832–836. doi: 10.1128/CDLI.8.4.832-836.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  148. Woo PC, Ng KH, Lau SK, Yip KT, Fung AM, Leung KW, Tam DM, Que TL, Yuen KY. Usefulness of the MicroSeq 500 16S ribosomal DNA-based bacterial identification system for identification of clinically significant bacterial isolates with ambiguous biochemical profiles. J Clin Microbiol. 2003;41:1996–2001. doi: 10.1128/JCM.41.5.1996-2001.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  149. Woo PC, Tam EW, Chong KT, Cai JJ, Tung ET, Ngan AH, Lau SK, Yuen KY. High diversity of polyketide synthase genes and the melanin biosynthesis gene cluster in Penicillium marneffei. FEBS J. 2010;277:3750–3758. doi: 10.1111/j.1742-4658.2010.07776.x. [DOI] [PubMed] [Google Scholar]
  150. Woo PC, Teng JL, Yeung JM, Tse H, Lau SK, Yuen KY. Automated identification of medically important bacteria by 16S rRNA gene sequencing using a novel comprehensive database, 16SpathDB. J Clin Microbiol. 2011;49:1799–1809. doi: 10.1128/JCM.02350-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  151. Woo PC, Wong SS, Lum PN, Hui WT, Yuen KY. Cell-wall-deficient bacteria and culture-negative febrile episodes in bone-marrow-transplant recipients. Lancet. 2001;357:675–679. doi: 10.1016/S0140-6736(00)04131-3. [DOI] [PubMed] [Google Scholar]
  152. Woo PC, Zhen H, Cai JJ, Yu J, Lau SK, Wang J, Teng JL, Wong SS, Tse RH, Chen R, et al. The mitochondrial genome of the thermal dimorphic fungus Penicillium marneffei is more closely related to those of molds than yeasts. FEBS Lett. 2003;555:469–477. doi: 10.1016/s0014-5793(03)01307-3. [DOI] [PubMed] [Google Scholar]
  153. Woolley SM, Posada D, Crandall KA. A comparison of phylogenetic network methods using computer simulation. PLoS ONE. 2008;3:e1913. doi: 10.1371/journal.pone.0001913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  154. Yang D, Kaine BP, Woese CR. The phylogeny of Archaebacteria. Syst Appl Microbiol. 1985;6:251–256. [Google Scholar]
  155. Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR. Mitochondrial origins. Proc Natl Acad Sci U S A. 1985;82:4443–4447. doi: 10.1073/pnas.82.13.4443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  156. Yang D, Woese CR. Phylogenetic sructure of the “Leuconostocs”: an interesting case of a rapidly evolving organism. Syst Appl Microbiol. 1989;12:145–149. [Google Scholar]
  157. Yang Z, Rannala B. Molecular phylogenetics: principles and practice. Nat Rev Genet. 2012;13:303–314. doi: 10.1038/nrg3186. [DOI] [PubMed] [Google Scholar]
  158. Yang Z, Roberts D. On the use of nucleic acid sequences to infer early branchings in the tree of life. Mol Biol Evol. 1995;12:451–458. doi: 10.1093/oxfordjournals.molbev.a040220. [DOI] [PubMed] [Google Scholar]
  159. Yip CC, Lau SK, Woo PC, Chan KH, Yuen KY. Complete genome sequence of a coxsackievirus A22 strain in Hong Kong reveals a natural intratypic recombination event. J Virol. 2011;85:12098–12099. doi: 10.1128/JVI.05944-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  160. Zablen LB, Kissil MS, Woese CR, Buetow DE. Phylogenetic origin of the chloroplast and prokaryotic nature of its ribosomal RNA. Proc Natl Acad Sci U S A. 1975;72:2418–2422. doi: 10.1073/pnas.72.6.2418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  161. Zuckerkandl E, Pauling L. Molecules as documents of evolutionary history. J Theor Biol. 1965;8:357–366. doi: 10.1016/0022-5193(65)90083-4. [DOI] [PubMed] [Google Scholar]

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