Amoeboflagellates and mitochondrial cristae in eukaryote evolution: megasystematics of the new protozoan subkingdoms eozoa and neozoa

Abstract

Recent molecular and ultrastructural discoveries necessitate major changes in the higher level classification of the kingdom Protozoa. A new class Anaeromonadea and subphylum Anaeromonada are created for the anaerobic tetrakont flagellate Trimastix, which is grouped with Parabasala, ranked as a subphylum, to form the new protozoan phylum Trichozoa. To simplify the supraphyletic classification of Protozoa I dispense with the category parvkingdom by increasing Neozoa in rank from infrakingdom to subkingdom and creating a new subkingdom Eozoa for the eokaryote phyla Trichozoa, Percolozoa and Euglenozoa.

The subkingdom Neozoa, containing all neokaryote Protozoa, is divided into four infrakingdoms: Sarcodina infrak. nov.; Alveolata Cavalier-Smith 1991; Actinopoda Calkins 1902, stat. nov.; and Neomonada infrak. nov. Sarcodina are subdivided into three superphyla: Eosarcodina superph. nov. (phyla Reticulosa and Mycetozoa); Neosarcodina (phyla Amoebozoa and Rhizopoda); and Haplosporidia (phylum Haplosporidia). Paramyxia are treated as a superclass within infraphylum Sporozoa of the Apicomplexa, not as a separate phylum.

Major changes are made to the tubulicristate phylum Opalozoa: I transfer the partially pseudopodial opalozoan groups into Rhizopoda; I move Proteromonadida into the subphylum Opalinata, and group the remaining non-opalinate opalozoans with the Choanozoa as a new zooflagellate phylum Neomonada, leaving only the revised Opalinata in the Opalozoa; these residual Opalozoa are left as protists incertae sedis, as it is unclear whether they belong in the kingdom Protozoa or Chromista. Neomonada are divided into four subphyla: Choanozoa stat. nov. (classes Choanoflagellea, Coral lochytrea); Hemimastigophora; Apusozoa subphyl. nov. (classes Thecomonadea, Anisomonadea, Jacobea cl. nov., Ebridea) and Isomita subphyl. nov. (classes Telonemea and Cyathobodonea).

Commation is transferred from Heterokonta to Apusozoa. Three apusozoan orders (Discocelida; Caecitellida; and Commatiida) are created. Within the revised Rhizopoda I group Sarcomonadea (revised by excluding proteomyxids and Jakoba) and Filosea together as a new subphylum Monadofilosa, and group Chlorarachnea with the formerly opalozoan class Proteomyxidea as a second new rhizopod subphylum, Reticulofilosa; Phytomyxea are removed from Opalozoa and treated as a third new rhizopod subphylum, Phytomyxa.

Lobose amoebae are excluded from Rhizopoda and placed in the separate sarcodine phylum Amoebozoa as a subphylum (Lobosa) comprising the classes Amoebaea and Testacealobosea. A new amoebozoan subphylum (Holomastiga) and class (Holomastigea) are created for Multicilia, and Archamoebae (classes Pelobiontea and Entamoebea) are treated as a third subphylum of Amoebozoa.

A central role for amoeboflagellates in eukaryote cell evolution is proposed. I suggest that ancestral eukaryotes were non-amoeboid zooflagellates and that the amoeboflagellate condition originated only once in a percolozoan that evolved eruptive pseudopodia to create the Heterolobosea. Later, by evolving graded spatial fine-tuning of cortical properties, these evolved into the non-eruptive pseudopodia of Sarcodina. The non-amoeboid flagellate groups Euglenozoa, Neomonada, and Alveolata may have evolved secondarily by the independent suppression of the amoeboid phase of amoeboflagellates, just as the non-ciliated sarcodine groups evolved polyphyletically from amoeboflagellates by several independent losses of cilia. It is argued that Actinopoda arose from neosarcodine amoeboflagellates by evolving axopodia. The four higher kingdoms did not evolve directly from amoeboflagellates (Animalia and Fungi arose independently from the neomonad Choanozoa, and Plantae and Chromista probably from early alveolates); but, as the neomonads and alveolates themselves evolved from amoeboflagellates, the ancestors of all four higher kingdoms were indirectly descended from amoeboflagellates, and their descendants retained the potential to re-evolve a controlled amoeboid motility. The evolutionary significance of pseudophytoplankton for neokaryote evolution is discussed.

An evolutionary explanation for the rare changes in the form of mitochondrial cristae during eukaryote cell evolution is proposed: cristal morphology coevolves with plasma membrane properties through the pleiotropic effects of genes affecting membrane composition. Selection acts primarily on plasma membrane properties, and cristal form is a basically neutral response accounted for by correlations of growth. Origin of non-eruptive pseudopods in the ancestral sarcodine could have caused the changeover from discoid to tubular cristae in the ancestral sarcodine, and converse changes in cell cortical properties may account for the polyphyletic flattening of cristae in Plantae, Cryptista, and Opisthokonta.