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A Revised Six-Kingdom System of Life

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A Revised Six-Kingdom System of Life Hi ul. R iv. ' 1998,', 73, p p . 203-266 printed in the United Kingdom © Cambridge Philosophical Society 203 A revised six-kingdom system of life T. CAVALIER-SMITH Evolutionary Biology Programme, Canadian Institute for Advanced Research , Department o f Botany , University o f British Columbia, Vancouver, BC, Canada V6T If4 (.Received 27 M arch 1 9 9 6 ; revised 15 December 1 9 9 7 ; accepted 18 December 1997) ABSTRACT A revised six-kingdom system of life is presented, down to the level of infraphylum. As in my 1983 system Bacteria are treated as a single kingdom, and eukaryotes are divided into only five kingdoms: Protozoa, Animalia, Fungi, Plantae and Chromista. Interm ediate high level categories (superkingdom, subkingdom, branch, infrakingdom, supcrphylum, subphylum and infraphylum) arc extensively used lo avoid splitting organisms into an excessive num ber of kingdoms and phyla (60 only being recognized). The two ‘zoological ’ kingdoms. Protozoa and Animalia, are subject to the International Code of Zoological Nomenclature, the kingdom Bacteria to the International Code of Bacteriological Nomenclature, and the three ‘botanical’ kingdoms (Plantae, Fungi, Chromista) lo the International Code of Botanical Nomenclature, Circumscrip­ tions of the kingdoms Bacteria and Plantae remain unchanged since Cavalicr-Smith (1981). The kingdom Fungi is expanded by adding M icrosporidia, because of protein sequence evidence that these amitochondrial intracellular parasites are related to conventional Fungi, not Protozoa. Fungi arc subdivided into four phyla and 20 classes; fungal classification at the rank of subclass and above is comprehensively revised. The kingdoms Protozoa and Animalia are modified in the light of molecular phylogenetic evidence that Myxozoa arc actually Animalia, not Protozoa, and that mesozoans arc related lo bilaterian animals. Animalia are divided into four subkingdoms: Radiata (phyla Porifera, Cnidaria, Placozoa, Ctenophora), Myxozoa, Mesozoa and Bilatcria (bilateral animals: all other phyla). Several new higher level groupings are made in the animal kingdom including three new phyla: Acanthognatha (rotifers, acanthoccphalans. gastrotrichs, gnathostomulids), Brachiozoa (brachiopods and phoronids) and Lobopoda (onychophorans and tardi- grades), so only 23 animal phyla are recognized. Archczoa, here restricted to the phyla M etam onada and Trichozoa, are treated as a subkingdom within Protozoa, as in my 1983 six-kingdom system, not as a separate kingdom. The recently revised phylum Rhizopoda is modified further by adding more flagellates and removing some ‘rhizopods’ and is therefore renamed Cercozoa. The num ber of protozoan phyla is reduced by grouping Mycetozoa and Archamoebae (both now infraphyla) as a new subphylum Conosa within the phylum Amoebozoa alongside the subphylum Lobosa, which now includes both the traditional aerobic lobosean amoebae and Multicilia. Haplosporidia and the (formerly microsporidian) melchnikovcllids are now both placed within the phylum Sporozoa. These changes make a total of only 13 currently recognized protozoan phyla, which arc grouped into two subkingdoms : Archezoa and Neozoa ; the latior is modified in circumscription by adding the Discicristata, a new infrakingdom comprising the phyla Percolozoa and Euglenozoa). These changes are discussed in relation to the principles of megasvstematics, here defined as systematics that concentrates on the higher levels of classes, phyla, and kingdoms. These principles also make it desirable to rank Archacbactcria as an infrakingdom of the kingdom Bacteria, not as a separate kingdom. Archaebacteria arc grouped with the infrakingdom Posibactcria to form a new subkingdom, Unibactcria, comprising all bacteria bounded by a single membrane. The bacterial subkingdom Negibacteria, with separate cytoplasmic and outer membranes, is subdivided into two infrakingdoms: Llpobacleria, which lack lipopolysaecharide and have only phospholipids in the outer membrane, and Glycobac.tcria, with lipopolysaccharides in the outer leaflet of the outer membrane and phospholipids in Its inner leaflet. This primary grouping of the 10 bacterial phyla into subkingdoms is based on the number of ccll-cnvclope membranes, whilst their subdivision into infrakingdoms emphasises their mem brane chemistry; definition of the ncgibacterial phyla, five at least partly photosynthetic, relies chiefly on pholosynthelic mechanism and ccll-cnvelope structure and chemistry corroborated by ribosomal RNA phylogeny. The kingdoms Protozoa and Chromista are slightly changed in circumscription by transferring subphylum Opalinata (classes Opalinea, Proteromonadea, Blastocystea cl. nov.) from Protozoa into infrakingdom Heterokonta of the 204 T. Cavalier-Smith kingdom Chromista. Opalinata arc grouped with the subphylum Pseudofungi and the zoofiagcllate Developayella elegans (in a new subphylum Bigvromonada) to form a new botanical phylum (Bigyra) of hctcrotrophs with a double ciliary transitional helix, making it necessary to abandon the phylum name phylogenetic evidence. Key winds : M cgasystematics, Bacteria, Protozoa, Anthozoa, Fungi, Animalia, Plantae, Chromista, Eumycota, M y c e to z o a . CONTENTS I. Introduction ................................................................................................................................................................................ 205 II. Philosophic preliminaries.................................................................................................................................................... 2 1 0 11 ') Darwinian evolutionary classification contrasted with H cnnigian cladification ...................... 2 1 0 (2) Naming taxa and clades.......................................................................................................................................... 213 (3) Principles of ranking taxa....................................................................................................................................... 214 (4) The need to weigh and integrate phylogenetic evidence from diverse sources....................... 215 III. In defence of Bacteria: the sole primary kingdom of life.................................................................................. 215 (1) The concept of a bacterium (synonym : prokaryote)............................................................................. 215 (2) Changing views on Archaebacteria .................................................................................................................... 216 (3) The importance of cell structure in bacterial classification ................................................................ 217 (4) Characters im portant in the high-level classification of Bacteria................................................... 220 (5) Bacterial subkingdoms and infrakingdoms .................................................................................................... 222 IV. Protozoa, the basal eukaryotic kingdom .................................................................................................................... 226 ¡1) Status of Archezoa, early diverging amitochondrial eukaryotes ..................................................... 2 2 6 (a) Changes in circumscription of the Archezoa ....................................................................................... 226 (2) The protozoan subkingdoms : Archezoa and Neozoa ............................................................................. 229 (3) Demarcation between the two zoological kingdoms: Protozoa and Anim alia ......................... 231 (4) Classification of the Neozoa ..................................................................................................................................... 234 (a) The infrakingdom Sarcomastigota ................................................................................................... 234 (b) The infrakingdom Alveolata ................................................................................................................ 238 (r) The infrakingdom Adinopoda ............................................................................................................ 238 V. The kingdom Animalia and its 23 phyla.................................................................................................................. 239 (1) Radiata, the ancestral animal subkingdom ................................................................................................... 239 (2) The derived subkingdom Mesozoa ..................................................................................................................... 2 3 9 (3) The number of animal phyla ................................................................................................................................ 239 (4) A broadened phylum Annelida ............................................................................................................................ 240 (5) The pseudococlomatc phyla Nemathelminthcs and Acanthognatha phvl. nov........................ 2 4 0 (6) The new phyla Brachiozoa and Lobopoda.................................................................................................. 241 (7) Phylogenetic assumptions behind the new bilaterian infrakingdoms and superphyla 241 (8) N e w a n im a l s u b p h v la a n d in f r a p h y la .............................................................................................................. 243 VI. The
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