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The Origin of Eukaryote and Archaebacterial Cells

Ultrastructural and molecular data have recently so rejuvenated the study of organismic diversity that we may soon have a clear understanding of the overall phylogeny of the living world, and even of the major steps in its diversification. Of these, the transition from the prokaryote to the eukaryote cell is certainly the most profound, ’ so much so that Prokaryota and Eukaryota are now generally ranked as superkingdoms (TABLE 1). To explain the origin of the eukaryote cell one has to determine the properties of the most primitive eukaryote, identify its likely prokaryotic ancestor, and explain in detail how the latter evolved into the former. That is the object of this paper. Identifying the most primitive eukaryote depends upon a proper understanding of the diversity and phylogenetic relationships within the most primitive eukaryote kingdom, the Protozoa. TABLE 2 indicates the protozoan classification and nomenclature that will be used in this paper: those protozoa recently separated as the subkingdom Archezoa are of special significance for early eukaryote evolution. All four archezoan phyla, though fully eukaryotic, completely lack any trace of mitochondria; the first three of them, especially, have a variety of other apparently primitive characters suggesting that they are living representatives of the earliest phases of eukaryote evolution. I argue that the most primitive eukaryote was a phagotrophic archezoan, with no chloroplasts, no mitochondria, no microbodies, and no stacked smooth cisternae forming a Golgi dictyosome, but possessing a single cilium with a sheaf of rootlet microtubules surrounding the single nucleus that divided by a closed mitosis in which the ciliary kinetosome was attached to the centrosome. The present day Mastigamoebea closely fit this description and may be “living fossils.” I suggest that this first eukaryote had a single chromosome and could form a resting cyst or spore in which (as in modem Anaxostylea) the ciliary axoneme and rootlets were not disassembled, and that with the origin of sexual syngamy allopolyploidy led to the formation of a cell with two chromosomes and two dissimilar (i.e., “anisokont”) cilia. This ancestral two-chromosomed anisokont perfected a primitive one-step meiosis and was the ancestor not only of the amitochondrial Metamonada and Parabasalia but also of all eukaryotes with mitochondria and chloroplasts, which it acquired by endosymbiosis of purple nonsulfur bacteria6 and cyanobacteria’ respectively. The