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Molecular phylogeny of the free-living archezoanTrepomonas agilis and the nature of the first eukaryote

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Abstract

We have sequenced the small ribosomal subunit RNA gene of the diplozoanTrepomonas agilis. This provides the first molecular information on a free-living archezoan. We have performed a phylogenetic analysis by maximum likelihood, parsimony, and distance methods for all available nearly complete archezoan small subunit ribosomal RNA genes and for representatives of all major groups of more advanced eukaryotes (metakaryotes). These show Diplozoa as the earliest-diverging eukaryotic lineage, closely followed by microsporidia.Trepomonas proves to be much more closely related toHexamita, and, to a lesser degree, toSpironucleus, than toGiardia. The close relationship between the free-livingTrepomonas on our trees and the parasitesHexamita inflata andSpironucleus refutes the idea that the early divergence of the amitochondrial Archezoa is an artefact caused by parasitism. The deep molecular divergence between the three phagotrophic genera with two cytostomes (Hexamita, Trepomonas, Spironucleus) and the saprotrophicGiardia that lacks cytostomes is in keeping with the classical evidence for a fundamental difference in the symmetry of the cytoskeleton between the two groups. We accordingly separate the two groups as two orders: Distomatida for those with two cytostomes/cytopharynxes and Giardiida ord. nov. forGiardia andOctomitus that lack these, and divide each order into two families. We suggest that this fundamental divergence in manner of feeding and in the symmetry of the cytoskeleton evolved in a free-living diplozoan very early indeed in the evolution of the eukaryotic cell, possibly very soon after the origin of the diplokaryotic state (having two nuclei linked together firmly by the cytoskeleton) and before the evolution of parasitism by distomatids and giardiids, which may have colonized animal guts independently. We discuss the possible relationship between the two archezoan phyla (Metamonada and Microsporidia) and the nature of the first eukaryotic cell in the light of our results and other recent molecular data.

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  1. Evolutionary Biology Program, Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, V6T 1Z4, Vancouver, Canada

    T. Cavalier-Smith & E. E. Chao

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Cavalier-Smith, T., Chao, E.E. Molecular phylogeny of the free-living archezoanTrepomonas agilis and the nature of the first eukaryote. J Mol Evol 43, 551–562 (1996). https://doi.org/10.1007/BF02202103

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