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. 2004 Jun 22;271(1545):1251–1262. doi: 10.1098/rspb.2004.2705

Only six kingdoms of life.

Thomas Cavalier-Smith 1
PMCID: PMC1691724  PMID: 15306349

Abstract

There are many more phyla of microbes than of macro-organisms, but microbial biodiversity is poorly understood because most microbes are uncultured. Phylogenetic analysis of rDNA sequences cloned after PCR amplification of DNA extracted directly from environmental samples is a powerful way of exploring our degree of ignorance of major groups. As there are only five eukaryotic kingdoms, two claims using such methods for numerous novel 'kingdom-level' lineages among anaerobic eukaryotes would be remarkable, if true. By reanalysing those data with 167 known species (not merely 8-37), I identified relatives for all 8-10 'mysterious' lineages. All probably belong to one of five already recognized phyla (Amoebozoa, Cercozoa, Apusozoa, Myzozoa, Loukozoa) within the basal kingdom Protozoa, mostly in known classes, sometimes even in known orders, families or genera. This strengthens the idea that the ancestral eukaryote was a mitochondrial aerobe. Analogous claims of novel bacterial divisions or kingdoms may reflect the weak resolution and grossly non-clock-like evolution of ribosomal rRNA, not genuine phylum-level biological disparity. Critical interpretation of environmental DNA sequences suggests that our overall picture of microbial biodiversity at phylum or division level is already rather good and comprehensive and that there are no uncharacterized kingdoms of life. However, immense lower-level diversity remains to be mapped, as does the root of the tree of life.

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Selected References

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  1. Archibald John M., O'Kelly Charles J., Doolittle W. Ford. The chaperonin genes of jakobid and jakobid-like flagellates: implications for eukaryotic evolution. Mol Biol Evol. 2002 Apr;19(4):422–431. doi: 10.1093/oxfordjournals.molbev.a004097. [DOI] [PubMed] [Google Scholar]
  2. Baldauf S. L., Roger A. J., Wenk-Siefert I., Doolittle W. F. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science. 2000 Nov 3;290(5493):972–977. doi: 10.1126/science.290.5493.972. [DOI] [PubMed] [Google Scholar]
  3. Bapteste Eric, Brinkmann Henner, Lee Jennifer A., Moore Dorothy V., Sensen Christoph W., Gordon Paul, Duruflé Laure, Gaasterland Terry, Lopez Philippe, Müller Miklós. The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1414–1419. doi: 10.1073/pnas.032662799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barns S. M., Delwiche C. F., Palmer J. D., Pace N. R. Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9188–9193. doi: 10.1073/pnas.93.17.9188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bolivar I., Fahrni J. F., Smirnov A., Pawlowski J. SSU rRNA-based phylogenetic position of the genera Amoeba and Chaos (Lobosea, Gymnamoebia): the origin of gymnamoebae revisited. Mol Biol Evol. 2001 Dec;18(12):2306–2314. doi: 10.1093/oxfordjournals.molbev.a003777. [DOI] [PubMed] [Google Scholar]
  6. Cavalier-Smith T. A revised six-kingdom system of life. Biol Rev Camb Philos Soc. 1998 Aug;73(3):203–266. doi: 10.1017/s0006323198005167. [DOI] [PubMed] [Google Scholar]
  7. Cavalier-Smith T. Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Philos Trans R Soc Lond B Biol Sci. 2003 Jan 29;358(1429):109–134. doi: 10.1098/rstb.2002.1194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cavalier-Smith T. Kingdom protozoa and its 18 phyla. Microbiol Rev. 1993 Dec;57(4):953–994. doi: 10.1128/mr.57.4.953-994.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cavalier-Smith T. The excavate protozoan phyla Metamonada Grassé emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa. Int J Syst Evol Microbiol. 2003 Nov;53(Pt 6):1741–1758. doi: 10.1099/ijs.0.02548-0. [DOI] [PubMed] [Google Scholar]
  10. Cavalier-Smith T. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int J Syst Evol Microbiol. 2002 Jan;52(Pt 1):7–76. doi: 10.1099/00207713-52-1-7. [DOI] [PubMed] [Google Scholar]
  11. Cavalier-Smith T. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol. 2002 Mar;52(Pt 2):297–354. doi: 10.1099/00207713-52-2-297. [DOI] [PubMed] [Google Scholar]
  12. Cavalier-Smith Thomas, Chao Ema E-Y. Molecular phylogeny of centrohelid heliozoa, a novel lineage of bikont eukaryotes that arose by ciliary loss. J Mol Evol. 2003 Apr;56(4):387–396. doi: 10.1007/s00239-002-2409-y. [DOI] [PubMed] [Google Scholar]
  13. Cavalier-Smith Thomas, Chao Ema E-Y. Phylogeny of choanozoa, apusozoa, and other protozoa and early eukaryote megaevolution. J Mol Evol. 2003 May;56(5):540–563. doi: 10.1007/s00239-002-2424-z. [DOI] [PubMed] [Google Scholar]
  14. Cavalier-Smith Thomas, Chao Ema E. Y. Phylogeny and classification of phylum Cercozoa (Protozoa). Protist. 2003 Oct;154(3-4):341–358. doi: 10.1078/143446103322454112. [DOI] [PubMed] [Google Scholar]
  15. Dawson Scott C., Pace Norman R. Novel kingdom-level eukaryotic diversity in anoxic environments. Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):8324–8329. doi: 10.1073/pnas.062169599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Edgcomb Virginia P., Kysela David T., Teske Andreas, de Vera Gomez Alvin, Sogin Mitchell L. Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc Natl Acad Sci U S A. 2002 May 28;99(11):7658–7662. doi: 10.1073/pnas.062186399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Embley T. M., Hirt R. P. Early branching eukaryotes? Curr Opin Genet Dev. 1998 Dec;8(6):624–629. doi: 10.1016/s0959-437x(98)80029-4. [DOI] [PubMed] [Google Scholar]
  18. Gaucher Eric A., Thomson J. Michael, Burgan Michelle F., Benner Steven A. Inferring the palaeoenvironment of ancient bacteria on the basis of resurrected proteins. Nature. 2003 Sep 18;425(6955):285–288. doi: 10.1038/nature01977. [DOI] [PubMed] [Google Scholar]
  19. Giovannoni S. J., Britschgi T. B., Moyer C. L., Field K. G. Genetic diversity in Sargasso Sea bacterioplankton. Nature. 1990 May 3;345(6270):60–63. doi: 10.1038/345060a0. [DOI] [PubMed] [Google Scholar]
  20. Gribaldo Simonetta, Philippe Hervé. Ancient phylogenetic relationships. Theor Popul Biol. 2002 Jun;61(4):391–408. doi: 10.1006/tpbi.2002.1593. [DOI] [PubMed] [Google Scholar]
  21. Harper James T., Keeling Patrick J. Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol Biol Evol. 2003 Jul 28;20(10):1730–1735. doi: 10.1093/molbev/msg195. [DOI] [PubMed] [Google Scholar]
  22. Hugenholtz P., Pitulle C., Hershberger K. L., Pace N. R. Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol. 1998 Jan;180(2):366–376. doi: 10.1128/jb.180.2.366-376.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Keeling Patrick J. Congruent evidence from alpha-tubulin and beta-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genet Biol. 2003 Apr;38(3):298–309. doi: 10.1016/s1087-1845(02)00537-6. [DOI] [PubMed] [Google Scholar]
  24. Lang B. F., O'Kelly C., Nerad T., Gray M. W., Burger G. The closest unicellular relatives of animals. Curr Biol. 2002 Oct 15;12(20):1773–1778. doi: 10.1016/s0960-9822(02)01187-9. [DOI] [PubMed] [Google Scholar]
  25. Leadbetter Jared R. Cultivation of recalcitrant microbes: cells are alive, well and revealing their secrets in the 21st century laboratory. Curr Opin Microbiol. 2003 Jun;6(3):274–281. doi: 10.1016/s1369-5274(03)00041-9. [DOI] [PubMed] [Google Scholar]
  26. Leander Brian S., Clopton Richard E., Keeling Patrick J. Phylogeny of gregarines (Apicomplexa) as inferred from small-subunit rDNA and beta-tubulin. Int J Syst Evol Microbiol. 2003 Jan;53(Pt 1):345–354. doi: 10.1099/ijs.0.02284-0. [DOI] [PubMed] [Google Scholar]
  27. López-García P., Rodríguez-Valera F., Pedrós-Alió C., Moreira D. Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature. 2001 Feb 1;409(6820):603–607. doi: 10.1038/35054537. [DOI] [PubMed] [Google Scholar]
  28. López-García Purificación, Philippe Hervé, Gail Françoise, Moreira David. Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge. Proc Natl Acad Sci U S A. 2003 Jan 9;100(2):697–702. doi: 10.1073/pnas.0235779100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Milyutina I. A., Aleshin V. V., Mikrjukov K. A., Kedrova O. S., Petrov N. B. The unusually long small subunit ribosomal RNA gene found in amitochondriate amoeboflagellate Pelomyxa palustris: its rRNA predicted secondary structure and phylogenetic implication. Gene. 2001 Jul 11;272(1-2):131–139. doi: 10.1016/s0378-1119(01)00556-x. [DOI] [PubMed] [Google Scholar]
  30. Moon-van der Staay S. Y., De Wachter R., Vaulot D. Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature. 2001 Feb 1;409(6820):607–610. doi: 10.1038/35054541. [DOI] [PubMed] [Google Scholar]
  31. Moreira David, López-García Purificación. The molecular ecology of microbial eukaryotes unveils a hidden world. Trends Microbiol. 2002 Jan;10(1):31–38. doi: 10.1016/s0966-842x(01)02257-0. [DOI] [PubMed] [Google Scholar]
  32. Morris Robert M., Rappé Michael S., Connon Stephanie A., Vergin Kevin L., Siebold William A., Carlson Craig A., Giovannoni Stephen J. SAR11 clade dominates ocean surface bacterioplankton communities. Nature. 2002 Dec 19;420(6917):806–810. doi: 10.1038/nature01240. [DOI] [PubMed] [Google Scholar]
  33. Philippe H., Lopez P., Brinkmann H., Budin K., Germot A., Laurent J., Moreira D., Müller M., Le Guyader H. Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc Biol Sci. 2000 Jun 22;267(1449):1213–1221. doi: 10.1098/rspb.2000.1130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Philippe H. Opinion: long branch attraction and protist phylogeny. Protist. 2000 Dec;151(4):307–316. doi: 10.1078/S1434-4610(04)70029-2. [DOI] [PubMed] [Google Scholar]
  35. Roger AJ. Reconstructing Early Events in Eukaryotic Evolution. Am Nat. 1999 Oct;154(S4):S146–S163. doi: 10.1086/303290. [DOI] [PubMed] [Google Scholar]
  36. Sait Michelle, Hugenholtz Philip, Janssen Peter H. Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys. Environ Microbiol. 2002 Nov;4(11):654–666. doi: 10.1046/j.1462-2920.2002.00352.x. [DOI] [PubMed] [Google Scholar]
  37. Silberman Jeffrey D., Simpson Alastair G. B., Kulda Jaroslav, Cepicka Ivan, Hampl Vladimir, Johnson Patricia J., Roger Andrew J. Retortamonad flagellates are closely related to diplomonads--implications for the history of mitochondrial function in eukaryote evolution. Mol Biol Evol. 2002 May;19(5):777–786. doi: 10.1093/oxfordjournals.molbev.a004135. [DOI] [PubMed] [Google Scholar]
  38. Simpson Alastair G. B., Roger Andrew J. Eukaryotic evolution: getting to the root of the problem. Curr Biol. 2002 Oct 15;12(20):R691–R693. doi: 10.1016/s0960-9822(02)01207-1. [DOI] [PubMed] [Google Scholar]
  39. Simpson Alastair G. B., Roger Andrew J., Silberman Jeffrey D., Leipe Detlef D., Edgcomb Virginia P., Jermiin Lars S., Patterson David J., Sogin Mitchell L. Evolutionary history of "early-diverging" eukaryotes: the excavate taxon Carpediemonas is a close relative of Giardia. Mol Biol Evol. 2002 Oct;19(10):1782–1791. doi: 10.1093/oxfordjournals.molbev.a004000. [DOI] [PubMed] [Google Scholar]
  40. Stechmann Alexandra, Cavalier-Smith Thomas. Phylogenetic analysis of eukaryotes using heat-shock protein Hsp90. J Mol Evol. 2003 Oct;57(4):408–419. doi: 10.1007/s00239-003-2490-x. [DOI] [PubMed] [Google Scholar]
  41. Stechmann Alexandra, Cavalier-Smith Thomas. Rooting the eukaryote tree by using a derived gene fusion. Science. 2002 Jul 5;297(5578):89–91. doi: 10.1126/science.1071196. [DOI] [PubMed] [Google Scholar]
  42. Stechmann Alexandra, Cavalier-Smith Thomas. The root of the eukaryote tree pinpointed. Curr Biol. 2003 Sep 2;13(17):R665–R666. doi: 10.1016/s0960-9822(03)00602-x. [DOI] [PubMed] [Google Scholar]
  43. Stoeck Thorsten, Epstein Slava. Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen-depleted marine environments. Appl Environ Microbiol. 2003 May;69(5):2657–2663. doi: 10.1128/AEM.69.5.2657-2663.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Stoeck Thorsten, Taylor Gordon T., Epstein Slava S. Novel eukaryotes from the permanently anoxic Cariaco Basin (Caribbean Sea). Appl Environ Microbiol. 2003 Sep;69(9):5656–5663. doi: 10.1128/AEM.69.9.5656-5663.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tovar Jorge, León-Avila Gloria, Sánchez Lidya B., Sutak Robert, Tachezy Jan, van der Giezen Mark, Hernández Manuel, Müller Miklós, Lucocq John M. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature. 2003 Nov 13;426(6963):172–176. doi: 10.1038/nature01945. [DOI] [PubMed] [Google Scholar]
  46. Van de Peer Y., Ben Ali A., Meyer A. Microsporidia: accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi. Gene. 2000 Apr 4;246(1-2):1–8. doi: 10.1016/s0378-1119(00)00063-9. [DOI] [PubMed] [Google Scholar]
  47. Vossbrinck C. R., Maddox J. V., Friedman S., Debrunner-Vossbrinck B. A., Woese C. R. Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. 1987 Mar 26-Apr 1Nature. 326(6111):411–414. doi: 10.1038/326411a0. [DOI] [PubMed] [Google Scholar]
  48. Williams Bryony A. P., Hirt Robert P., Lucocq John M., Embley T. Martin. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature. 2002 Aug 22;418(6900):865–869. doi: 10.1038/nature00949. [DOI] [PubMed] [Google Scholar]
  49. Zhang Hui, Sekiguchi Yuji, Hanada Satoshi, Hugenholtz Philip, Kim Hongik, Kamagata Yoichi, Nakamura Kazunori. Gemmatimonas aurantiaca gen. nov., sp. nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol. 2003 Jul;53(Pt 4):1155–1163. doi: 10.1099/ijs.0.02520-0. [DOI] [PubMed] [Google Scholar]

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