Multigene phylogenies of diverse Carpediemonas-like organisms identify the closest relatives of 'amitochondriate' diplomonads and retortamonads

Abstract

Diplomonads, retortamonads, and "Carpediemonas-like" organisms (CLOs) are a monophyletic group of protists that are microaerophilic/anaerobic and lack typical mitochondria. Most diplomonads and retortamonads are parasites, and the pathogen Giardia intestinalis is known to possess reduced mitochondrion-related organelles (mitosomes) that do not synthesize ATP. By contrast, free-living CLOs have larger organelles that superficially resemble some hydrogenosomes, organelles that in other protists are known to synthesize ATP anaerobically. This group represents an excellent system for studying the evolution of parasitism and anaerobic, mitochondrion-related organelles. Understanding these evolutionary transitions requires a well-resolved phylogeny of diplomonads, retortamonads and CLOs. Unfortunately, until now the deep relationships amongst these taxa were unresolved due to limited data for almost all of the CLO lineages. To address this, we assembled a dataset of up to six protein-coding genes that includes representatives from all six CLO lineages, and complements existing rRNA datasets. Multigene phylogenetic analyses place CLOs as well as the retortamonad Chilomastix as a paraphyletic basal assemblage to the lineage comprising diplomonads and the retortamonad Retortamonas. In particular, the CLO Dysnectes was shown to be the closest relative of the diplomonads + Retortamonas clade, with strong support. This phylogeny is consistent with a drastic degeneration of mitochondrion-related organelles during the evolution from a free-living organism resembling extant CLOs to a probable parasite/commensal common ancestor of diplomonads and Retortamonas.