pmc logo imageJournal ListSearchpmc logo image
Logo of microrevMicrobiol Mol Biol Rev ArchiveMicrobiol Rev Archive
Microbiol Rev. 1993 December; 57(4): 953–994.
PMCID: PMC372943
Kingdom protozoa and its 18 phyla.
T Cavalier-Smith
Department of Botany, University of British Columbia, Vancouver, Canada.
Abstract
The demarcation of protist kingdoms is reviewed, a complete revised classification down to the level of subclass is provided for the kingdoms Protozoa, Archezoa, and Chromista, and the phylogenetic basis of the revised classification is outlined. Removal of Archezoa because of their ancestral absence of mitochondria, peroxisomes, and Golgi dictyosomes makes the kingdom Protozoa much more homogeneous: they all either have mitochondria and peroxisomes or have secondarily lost them. Predominantly phagotrophic, Protozoa are distinguished from the mainly photosynthetic kingdom Chromista (Chlorarachniophyta, Cryptista, Heterokonta, and Haptophyta) by the absence of epiciliary retronemes (rigid thrust-reversing tubular ciliary hairs) and by the lack of two additional membranes outside their chloroplast envelopes. The kingdom Protozoa has two subkingdoms: Adictyozoa, without Golgi dictyosomes, containing only the phylum Percolozoa (flagellates and amoeboflagellates); and Dictyozoa, made up of 17 phyla with Golgi dictyosomes. Dictyozoa are divided into two branches: (i) Parabasalia, a single phylum with hydrogenosomes and 70S ribosomes but no mitochondria, Golgi dictyosomes associated with striated roots, and a kinetid of four or five cilia; and (ii) Bikonta (16 unicellular or plasmodial phyla with mitochondria and bikinetids and in which Golgi dictyosomes are not associated with striated ciliary roots), which are divided into two infrakingdoms: Euglenozoa (flagellates with discoid mitochondrial cristae and trans-splicing of miniexons for all nuclear genes) and Neozoa (15 phyla of more advanced protozoa with tubular or flat [usually nondiscoid] mitochondrial cristae and cis-spliced spliceosomal introns). Neozoa are divided into seven parvkingdoms: (i) Ciliomyxa (three predominantly ciliated phyla with tubular mitochondrial cristae but no cortical alveoli, i.e., Opalozoa [flagellates with tubular cristae], Mycetozoa [slime molds], and Choanozoa [choanoflagellates, with flattened cristae]); (ii) Alveolata (three phyla with cortical alveoli and tubular mitochondrial cristae, i.e., Dinozoa [Dinoflagellata and Protalveolata], Apicomplexa, and Ciliophora); (iii) Neosarcodina (phyla Rhizopoda [lobose and filose amoebae] and Reticulosa [foraminifera; reticulopodial amoebae], usually with tubular cristae); (iv) Actinopoda (two phyla with axopodia: Heliozoa and Radiozoa [Radiolaria, Acantharia]); (v) Entamoebia (a single phylum of amoebae with no mitochondria, peroxisomes, hydrogenosomes, or cilia and with transient intranuclear centrosomes); (vi) Myxozoa (three endoparasitic phyla with multicellular spores, mitochondria, and no cilia: Myxosporidia, Haplosporidia, and Paramyxia); and (vii) Mesozoa (multicells with tubular mitochondrial cristae, included in Protozoa because, unlike animals, they lack collagenous connective tissue).
Full text
Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (9.3M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
  • Ashkin, A; Schütze, K; Dziedzic, JM; Euteneuer, U; Schliwa, M. Force generation of organelle transport measured in vivo by an infrared laser trap. Nature. 1990 Nov 22;348(6299):346–348. [PubMed]
  • Bakker-Grunwald, T; Wöstmann, C. Entamoeba histolytica as a model for the primitive eukaryotic cell. Parasitol Today. 1993 Jan;9(1):27–31. [PubMed]
  • Belcher, JH; Swale, EM. Luffisphaera gen.nov., an enigmatic scaly micro-organism. Proc R Soc Lond B Biol Sci. 1975 Mar 11;188(1093):495–499. [PubMed]
  • Bowman, BH; Taylor, JW; Brownlee, AG; Lee, J; Lu, SD; White, TJ. Molecular evolution of the fungi: relationship of the Basidiomycetes, Ascomycetes, and Chytridiomycetes. Mol Biol Evol. 1992 Mar;9(2):285–296. [PubMed]
  • Cavalier-Smith, T. Eukaryote kingdoms: seven or nine? Biosystems. 1981;14(3-4):461–481. [PubMed]
  • Cavalier-Smith, T. The evolutionary origin and phylogeny of eukaryote flagella. Symp Soc Exp Biol. 1982;35:465–493. [PubMed]
  • Cavalier-Smith, T. The kingdoms of organisms. Nature. 1986 Dec 4;324(6096):416–417. [PubMed]
  • Cavalier-Smith, T. The origin of cells: a symbiosis between genes, catalysts, and membranes. Cold Spring Harb Symp Quant Biol. 1987;52:805–824. [PubMed]
  • Cavalier-Smith, T. The origin of eukaryotic and archaebacterial cells. Ann N Y Acad Sci. 1987;503:17–54. [PubMed]
  • Cavalier-Smith, T. The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. Ann N Y Acad Sci. 1987;503:55–71. [PubMed]
  • Cavalier-Smith, T. Eukaryotes with no mitochondria. Nature. 326(6111):332–333. [PubMed]
  • Cavalier-Smith, T. Origin of the cell nucleus. Bioessays. 1988 9(2-3):72–78.Aug–Sep; [PubMed]
  • Cavalier-Smith, T. Archamoebae: the ancestral eukaryotes? Biosystems. 1991;25(1-2):25–38. [PubMed]
  • Cavalier-Smith, T. Intron phylogeny: a new hypothesis. Trends Genet. 1991 May;7(5):145–148. [PubMed]
  • Cavalier-Smith, T. The number of symbiotic origins of organelles. Biosystems. 1992;28(1-3):91–108. [PubMed]
  • Cavalier-Smith, T. Origins of secondary metabolism. Ciba Found Symp. 1992;171:64–87. [PubMed]
  • Christen, R; Ratto, A; Baroin, A; Perasso, R; Grell, KG; Adoutte, A. An analysis of the origin of metazoans, using comparisons of partial sequences of the 28S RNA, reveals an early emergence of triploblasts. EMBO J. 1991 Mar;10(3):499–503. [PubMed]
  • Corliss, JO. What are the taxonomic and evolutionary relationships of the Protozoa to the Protista? Biosystems. 1981;14(3-4):445–449. [PubMed]
  • Corliss, JO. The kingdom Protista and its 45 phyla. Biosystems. 1984;17(2):87–126. [PubMed]
  • Corliss, JO. Should there be a separate code of nomenclature for the protists? Biosystems. 1992;28(1-3):1–14. [PubMed]
  • Douglas, SE. Eukaryote-eukaryote endosymbioses: insights from studies of a cryptomonad alga. Biosystems. 1992;28(1-3):57–68. [PubMed]
  • Douglas, SE; Murphy, CA; Spencer, DF; Gray, MW. Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature. 1991 Mar 14;350(6314):148–151. [PubMed]
  • Edman, JC; Kovacs, JA; Masur, H; Santi, DV; Elwood, HJ; Sogin, ML. Ribosomal RNA sequence shows Pneumocystis carinii to be a member of the fungi. Nature. 1988 Aug 11;334(6182):519–522. [PubMed]
  • Ferat, JL; Michel, F. Group II self-splicing introns in bacteria. Nature. 1993 Jul 22;364(6435):358–361. [PubMed]
  • Flavin, M; Nerad, TA. Reclinomonas americana N. G., N. Sp., a new freshwater heterotrophic flagellate. J Eukaryot Microbiol. 1993 40(2):172–179.Mar–Apr; [PubMed]
  • Gray, MW. The endosymbiont hypothesis revisited. Int Rev Cytol. 1992;141:233–357. [PubMed]
  • Hasegawa, M; Hashimoto, T; Adachi, J; Iwabe, N; Miyata, T. Early branchings in the evolution of eukaryotes: ancient divergence of entamoeba that lacks mitochondria revealed by protein sequence data. J Mol Evol. 1993 Apr;36(4):380–388. [PubMed]
  • Heywood, P. Structure, function and terminology of microtubule- and microfilament-containing structures. Cell Biol Int Rep. 1987 Dec;11(12):837–847. [PubMed]
  • Higgins, DG; Sharp, PM. Fast and sensitive multiple sequence alignments on a microcomputer. Comput Appl Biosci. 1989 Apr;5(2):151–153. [PubMed]
  • 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 Dec;86(23):9355–9359. [PubMed]
  • Johnson, PJ; d'Oliveira, CE; Gorrell, TE; Müller, M. Molecular analysis of the hydrogenosomal ferredoxin of the anaerobic protist Trichomonas vaginalis. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6097–6101. [PubMed]
  • Keller, GA; Krisans, S; Gould, SJ; Sommer, JM; Wang, CC; Schliebs, W; Kunau, W; Brody, S; Subramani, S. Evolutionary conservation of a microbody targeting signal that targets proteins to peroxisomes, glyoxysomes, and glycosomes. J Cell Biol. 1991 Sep;114(5):893–904. [PubMed]
  • Lee, RE; Kugrens, P. Relationship between the flagellates and the ciliates. Microbiol Rev. 1992 Dec;56(4):529–542. [PubMed]
  • Leipe, DD; Gunderson, JH; Nerad, TA; Sogin, ML. Small subunit ribosomal RNA+ of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol Biochem Parasitol. 1993 May;59(1):41–48. [PubMed]
  • Lenaers, G; Scholin, C; Bhaud, Y; Saint-Hilaire, D; Herzog, M. A molecular phylogeny of dinoflagellate protists (pyrrhophyta) inferred from the sequence of 24S rRNA divergent domains D1 and D8. J Mol Evol. 1991 Jan;32(1):53–63. [PubMed]
  • Levine, ND; Corliss, JO; Cox, FE; Deroux, G; Grain, J; Honigberg, BM; Leedale, GF; Loeblich, AR, 3rd; Lom, J; Lynn, D; Merinfeld, EG; Page, FC; Poljansky, G; Sprague, V; Vavra, J; Wallace, FG. A newly revised classification of the protozoa. J Protozool. 1980 Feb;27(1):37–58. [PubMed]
  • Maier, UG. The four genomes of the alga Pyrenomonas salina (Cryptophyta). Biosystems. 1992;28(1-3):69–73. [PubMed]
  • Maier, UG; Hofmann, CJ; Eschbach, S; Wolters, J; Igloi, GL. Demonstration of nucleomorph-encoded eukaryotic small subunit ribosomal RNA in cryptomonads. Mol Gen Genet. 1991 Nov;230(1-2):155–160. [PubMed]
  • Marvin-Sikkema, FD; Kraak, MN; Veenhuis, M; Gottschal, JC; Prins, RA. The hydrogenosomal enzyme hydrogenase from the anaerobic fungus Neocallimastix sp. L2 is recognized by antibodies, directed against the C-terminal microbody protein targeting signal SKL. Eur J Cell Biol. 1993 Jun;61(1):86–91. [PubMed]
  • Medlin, L; Elwood, HJ; Stickel, S; Sogin, ML. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene. 1988 Nov 30;71(2):491–499. [PubMed]
  • Morden, CW; Delwiche, CF; Kuhsel, M; Palmer, JD. Gene phylogenies and the endosymbiotic origin of plastids. Biosystems. 1992;28(1-3):75–90. [PubMed]
  • Muchhal, US; Schwartzbach, SD. Characterization of a Euglena gene encoding a polyprotein precursor to the light-harvesting chlorophyll a/b-binding protein of photosystem II. Plant Mol Biol. 1992 Jan;18(2):287–299. [PubMed]
  • Müller, M. Energy metabolism of ancestral eukaryotes: a hypothesis based on the biochemistry of amitochondriate parasitic protists. Biosystems. 1992;28(1-3):33–40. [PubMed]
  • Patterson, DJ. The evolution of protozoa. Mem Inst Oswaldo Cruz. 1988 Nov;83 Suppl 1:580–600. [PubMed]
  • Raikov, IB. Unusual extrusive organelles in karyorelictid ciliates: an argument for the ancient origin of this group. Biosystems. 1992;28(1-3):195–201. [PubMed]
  • SABATINI, DD; BENSCH, K; BARRNETT, RJ. Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J Cell Biol. 1963 Apr;17:19–58. [PubMed]
  • Saffo, MB. The enigmatic protist Nephromyces. Biosystems. 1981;14(3-4):487–490. [PubMed]
  • Saitou, N; Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. [PubMed]
  • Sogin, ML; Gunderson, JH; Elwood, HJ; Alonso, RA; Peattie, DA. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science. 1989 Jan 6;243(4887):75–77. [PubMed]
  • Swanton, MT; Heumann, JM; Prescott, DM. Gene-sized DNA molecules of the macronuclei in three species of hypotrichs: size distributions and absence of nicks. DNA of ciliated protozoa. VIII. Chromosoma. 1980;77(2):217–227. [PubMed]
  • Taylor, FJ. Problems in the development of an explicit hypothetical phylogeny of the lower eukaryotes. Biosystems. 1978 Apr;10(1-2):67–89. [PubMed]
  • Tessier, LH; Keller, M; Chan, RL; Fournier, R; Weil, JH; Imbault, P. Short leader sequences may be transferred from small RNAs to pre-mature mRNAs by trans-splicing in Euglena. EMBO J. 1991 Sep;10(9):2621–2625. [PubMed]
  • Turner, S; Burger-Wiersma, T; Giovannoni, SJ; Mur, LR; Pace, NR. The relationship of a prochlorophyte Prochlorothrix hollandica to green chloroplasts. Nature. 1989 Jan 26;337(6205):380–382. [PubMed]
  • Viscogliosi, E; Philippe, H; Baroin, A; Perasso, R; Brugerolle, G. Phylogeny of trichomonads based on partial sequences of large subunit rRNA and on cladistic analysis of morphological data. J Eukaryot Microbiol. 1993 40(4):411–421.Jul–Aug; [PubMed]
  • Vossbrinck, CR; Maddox, JV; Friedman, S; Debrunner-Vossbrinck, BA; Woese, CR. Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature. 326(6111):411–414. [PubMed]
  • Vossbrinck, CR; Woese, CR. Eukaryotic ribosomes that lack a 5.8S RNA. Nature. 1986 Mar 20;320(6059):287–288. [PubMed]
  • Wainright, PO; Hinkle, G; Sogin, ML; Stickel, SK. Monophyletic origins of the metazoa: an evolutionary link with fungi. Science. 1993 Apr 16;260(5106):340–342. [PubMed]
  • Whatley, JM; John, P; Whatley, FR. From extracellular to intracellular: the establishment of mitochondria and chloroplasts. Proc R Soc Lond B Biol Sci. 1979 Apr 11;204(1155):165–187. [PubMed]
  • WHITTAKER, RH. On the broad classification of organisms. Q Rev Biol. 1959 Sep;34:210–226. [PubMed]
  • Whittaker, RH. New concepts of kingdoms or organisms. Evolutionary relations are better represented by new classifications than by the traditional two kingdoms. Science. 1969 Jan 10;163(863):150–160. [PubMed]
  • Woese, CR; Fox, GE. The concept of cellular evolution. J Mol Evol. 1977 Sep 20;10(1):1–6. [PubMed]
  • 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 Jun;87(12):4576–4579. [PubMed]
  • Wolf, Ken; Markiw, Maria E. Biology Contravenes Taxonomy in the Myxozoa: New Discoveries Show Alternation of Invertebrate and Vertebrate Hosts. Science. 1984 Sep 28;225(4669):1449–1452. [PubMed]
  • Wolters, J. The troublesome parasites--molecular and morphological evidence that Apicomplexa belong to the dinoflagellate-ciliate clade. Biosystems. 1991;25(1-2):75–83. [PubMed]