Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.)

The protozoan infrakingdom Alveolata comprises the phyla Ciliophora and Miozoa. The name Myzozoa—sucking life—is introduced here to replace Miozoa (protalveolates, dinoflagellates, Sporozoa, apicomonads) as both subphyla (Dinozoa, Apicomplexa) are commonly or ancestrally myzocytotic feeders. We studied ultrastructurally two contrasting myzocytotic flagellates: Colpodella tetrahymenae sp. n. (predatory on Tetrahymena), with an inner membrane complex like Sporozoa, and Voromonas (=Colpodella) pontica gen. et comb. nov., with discrete cortical alveoli like Dinozoa; we also sequenced 18S rDNA of both of these flagellates and of two highly divergent isolates of Oxyrrhis. Phylogenetic analysis shows early divergence between Colpodella, Voromonas and Alphamonas edax and supports the independent origin of dinoflagellates, Perkinsea and Apicomplexa (Sporozoa, Apicomonadea) from myzocytotic protalveolate flagellates. Oxyrrhis is probably a highly modified dinoflagellate, not a protalveolate with primitive chromatin and ciliary organization. The rapid basal radiation of Myzozoa is poorly resolved; the predatory colpodellids sensu stricto are probably sisters of Sporozoa. We discuss early cellular diversification of Myzozoa (=Miozoa) and revise its classification, establishing a new class Myzomonadea for Voromonas, Alphamonas and Chilovora (=Bodo) perforans gen. et comb. nov., three new peridinean subclasses (Oxyrrhia, Gonaulacoidia, Suessioidia), and five new orders: Acrocoelida for Acrocoelus; Voromonadida for Voromonas and Alphamonas; Chilovorida for Chilovora; Rastromonadida for Rastromonas and Parvilucifera; and Algovorida for Algovora, a new genus for Colpodella turpis and Colpodella pugnax sensu Simpson and Patterson. We suggest that the flattened inner membrane complex of Apicomplexa evolved in association with trichocyst loss by fusion of already flattened myzomonad cortical alveoli as an adaptation for actomyosin-based host penetration and gliding motility.