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Kingdom Protozoa and Its 18Phyla

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Kingdom Protozoa and Its 18Phyla MICROBIOLOGICAL REVIEWS, Dec. 1993, p. 953-994 Vol. 57, No. 4 0146-0749/93/040953-42$02.00/0 Copyright © 1993, American Society for Microbiology Kingdom Protozoa and Its 18 Phyla T. CAVALIER-SMITH Evolutionary Biology Program of the Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 INTRODUCTION .......................................................................... 954 Changing Views of Protozoa as a Taxon.......................................................................... 954 EXCESSIVE BREADTH OF PROTISTA OR PROTOCTISTA ......................................................955 DISTINCTION BETWEEN PROTOZOA AND PLANTAE............................................................956 DISTINCTION BETWEEN PROTOZOA AND FUNGI ................................................................957 DISTINCTION BETWEEN PROTOZOA AND CHROMISTA .......................................................960 DISTINCTION BETWEEN PROTOZOA AND ANIMALIA ..........................................................962 DISTINCTION BETWEEN PROTOZOA AND ARCHEZOA.........................................................962 Transitional Problems in Narrowing the Definition of Protozoa ....................................................963 Exclusion of Parabasalia from Archezoa .......................................................................... 964 Exclusion of Entamoebia from Archezoa .......................................................................... 964 Are Microsporidia Archezoa or Protozoa?.......................................................................... 964 DIAGNOSIS OF THE KINGDOM PROTOZOA .........................................................................965 THE TWO SUBKINGDOMS, TWO BRANCHES, TWO INFRAKINGDOMS, AND SEVEN PARVKINGDOMS OF PROTOZOA .......................................................................... 967 Subkingdoms Adictyozoa and Dictyozoa.......................................................................... 967 New Dictyozoan Branches: Parabasalia and Bikonta..................................................................967 Infrakingdoms Euglenozoa and Neozoa .......................................................................... 967 The New Category Parvkingdom .......................................................................... 968 Mesozoa as Multicellular Protozoa .......................................................................... 968 Myxozoa are Protozoa, not Animalia.......................................................................... 968 The New Parvkingdom Entamoebia .......................................................................... 968 Four Other New Parvkingdoms: Alveolata, Actinopoda, Neosarcodina, and Ciliomyxa ....................968 PHYLUM PERCOLOZOA ......................................................................... 969 PHYLUM AND INFRAKINGDOM EUGLENOZOA ....................................................................969 PARVKINGDOM ALVEOLATA AND ITS THREE PHYLA .........................................................969 Superphylum Heterokaryota and its Sole Phylum, Ciliophora......................................................969 Superphylum Miozoa .......................................................................... 973 Phylum Dinozoa Emended .......................................................................... 973 Phylum Apicomplexa Emended .......................................................................... 973 NEW SUPERPHYLUM OPALOMYXA AND ITS TWO PHYLA....................................................974 Phylum Opalozoa .......................................................................... 974 Phylum Mycetozoa .......................................................................... 976 PARVKINGDOM ACTINOPODA AND ITS TWO PHYLA...........................................................977 Phylum Radiozoa Emended .......................................................................... 977 Phylum Heliozoa Emended.......................................................................... 977 NEW PARVKINGDOM NEOSARCODINA.......................................................................... 978 Phylum Rhizopoda Emended .......................................................................... 978 Neosarcodina incertae sedes.......................................................................... 978 New Phylum Reticulosa .......................................................................... 978 PHYLUM AND SUPERPHYLUM CHOANOZOA .......................................................................979 New Parvkingdom Ciliomyxa.......................................................................... 979 NEW PARVKINGDOM MYXOZOA .......................................................................... 979 Phylum Myxosporidia .......................................................................... 979 Phylum Haplosporidia .......................................................................... 979 Phylum Paramyxia .......................................................................... 979 NEW PROTOZOAN SUBPHYLA, CLASSES, SUBCLASSES, AND ORDERS..................................980 Percolozoa .......................................................................... 980 Euglenozoa .......................................................................... 980 Opalozoa.......................................................................... 980 Dinozoa.......................................................................... 981 Apicomplexa .......................................................................... 981 Radiozoa ......................................................................... 982 Heliozoa.......................................................................... 982 DISCUSSION......................................................................... 982 ENVOI .......................................................................... 983 953 954 CAVALIER-SMITH MICROBIOL. REV. APPENDIX 1. DIAGNOSES OF SUBKINGDOMS, BRANCHES, INFRAKINGDOMS, PARVKINGDOMS, SUPERPHYLA, PHYLA, SUBPHYLA, AND INFRAPHYIA OF THE KINGDOM PROTOZOA........................................................................... 983 APPENDIX 2. DIAGNOSES OF THE NEW PROTOZOAN SUPERCLASSES, CLASSES, SUBCLASSES, ORDERS, AND FAMILIES ...........................................................*0*00000000000986 APPENDIX 3. DIAGNOSES OF NEW CHROMIST TAXA...........................................................988 ACKNOWLEDGMENTS............................................................................989 ADDENDUM IN PROOF ........................................................................... 989 REFERENCES ........................................................................... 989 INTRODUCTION new criteria for this demarcation and helped to reinforce a The classification of eukaryotic microorganisms, usually growing preference for multikingdom systems of classifica- referred to as protists, has been in flux for over two tion over the old animal-or-vegetable dichotomy (16, 17, 19, centuries. During the past 20 years, there has been an 21, 31, 52, 76, 77, 90, 95, 96, 99, 101, 124, 147). Though it is increasing tendency to divide them into several kingdoms widely agreed that Protozoa are too diverse to constitute a rather than to place them all in a single kingdom, as was single phylum and must be distributed among a fairly large proposed by the 19th century authors Owen (kingdom Pro- number ofphyla (17, 31, 52, 77, 83, 89, 90, 98, 124), there has tozoa, 1858), Hogg (kingdom Primigenum, 1860), and been no general consensus as to how this should be done or, Haeckel (kingdom Protista, 1866). (These earlier kingdoms indeed, whether or not Protozoa should even remain a formal included bacteria, which were first formally removed as a taxon. At present, three fundamentally different viewpoints separate kingdom by Copeland [48] in 1938.) Earlier at- are enjoying an uneasy coexistence. The most conservative tempts to subdivide protists simply into plants and animals, approach is to treat Protozoa as a subkingdom, but not to on the basis of the presence or absence of chloroplasts or specify whether it belongs to Animalia or Protista, and to phagotrophy (feeding by phagocytosis), were abandoned sidestep the problem of demarcation by failing to provide a because three well-defined taxa (dinoflagellates, euglenoids, diagnosis (89) or by providing a diagnosis that is too vague to and heterokonts) have some members of each type, and in be effective (83). The most radical approach is to abandon the case of dinoflagellates and heterokonts (and hapto- Protozoa altogether as a taxon (51, 90) and either to subsume phytes) many species are both photosynthetic and phag- its phyla into a broader kingdom, whether Protista (48, 52, otrophic. Since the early 1970s, new insights into protist 95, 96, 147), Protoctista Copeland 1947 (49, 97-99), or even ultrastructure arising from electron microscopic studies have Phytobiota (= Plantae) (77), or alternatively to subdivide it been increasingly used to propose explicit phylogenies for into several narrower kingdoms (86, 90, 101). A more protists (16-19, 21, 25-27, 29, 32, 34-43, 132, 133) and to eclectic middle way is to refine the concept of protozoa more apply more rigorous phylogenetic principles to the large- precisely so as to produce a phylogenetically sound taxon scale classification of protists.
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