Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree

Abstract

I discuss eukaryotic deep phylogeny and reclassify the basal eukaryotic kingdom Protozoa and derived kingdom Chromista in the light of multigene trees. I transfer the formerly protozoan Heliozoa and infrakingdoms Alveolata and Rhizaria into Chromista, which is sister to kingdom Plantae and arguably originated by synergistic double internal enslavement of green algal and red algal cells. I establish new subkingdoms (Harosa; Hacrobia) for the expanded Chromista. The protozoan phylum Euglenozoa differs immensely from other eukaryotes in its nuclear genome organization (trans-spliced multicistronic transcripts), mitochondrial DNA organization, cytochrome c-type biogenesis, cell structure and arguably primitive mitochondrial protein-import and nuclear DNA prereplication machineries. The bacteria-like absence of mitochondrial outer-membrane channel Tom40 and DNA replication origin-recognition complexes from trypanosomatid Euglenozoa roots the eukaryotic tree between Euglenozoa and all other eukaryotes (neokaryotes), or within Euglenozoa. Given their unique properties, I segregate Euglenozoa from infrakingdom Excavata (now comprising only phyla Percolozoa, Loukozoa, Metamonada), grouping infrakingdoms Euglenozoa and Excavata as the ancestral protozoan subkingdom Eozoa. I place phylum Apusozoa within the derived protozoan subkingdom Sarcomastigota. Clarifying early eukaryote evolution requires intensive study of properties distinguishing Euglenozoa from neokaryotes and Eozoa from neozoa (eukaryotes except Eozoa; ancestrally defined by haem lyase).

Figure 1.

Evolutionary relationships of the six kingdoms. Chromist taxa with chlorophyll c are in brown (constituting the paraphyletic ‘chromalveolates’); unlike previous classifications, Rhizaria and Heliozoa are within Chromista not Protozoa. Nm denotes retention as nucleomorphs by chlorarachnean Rhizaria of the green-algal and by Cryptophyceae of the red-algal nuclei from two ancestral secondary symbiogeneses that generated chromists. Cytochrome c/c1 biogenesis mechanisms are highlighted in yellow. The ancestral bacterial cytochrome c/c1 biogenesis mechanism (Ccm) is argued to have been inherited by excavate protozoa from the α-proteobacterial ancestor of mitochondria, and replaced by the novel haem lyase in the ancestor of neozoa. The complex pattern within corticates (ancestrally with both Ccms and haem lyase but later differentially lost) is omitted for clarity. The deepest branch having mitochondrial protein-import receptor Tom40 and origin recognition complex (ORC) is Percolozoa (electronic supplementary material, note 2). Taxa ranked as kingdoms or above are in upper case; clades not treated as taxa have lower-case initial. Diagnosis of new subkingdom Harosa: having Rab1A; typically with cortical alveoli or tripartite ciliary hairs or reticulose/filose pseudopods or ciliary gliding. The Alveolata/Heterokonta grouping (new clade halvaria) and likely eventual need to transfer Alveolata into Chromista were long foreseen (Cavalier-Smith 1995).