Transcriptome and evolutionary analysis of Pseudotrichomonas keilini, a free-living anaerobic eukaryote

Abstract

The early evolution of eukaryotes and their adaptations to low-oxygen environments are fascinating open questions in biology. Genome-scale data from novel eukaryotes, and particularly from free-living lineages, are key to answering these questions. The Parabasalia are an ancient lineage of anaerobes, and the most speciose lineage of Metamonada, a major lineage of eukaryotes. The most well-studied metamonads are parasitic parabasalids including Trichomonas vaginalis, Tritrichomonas foetus, and Giardia intestinalis, but very little genome-scale data is available for free-living members of the group. Here, we sequenced the transcriptome of Pseudotrichomonas keilini, a free-living parabasalian. Comparative genomic analysis indicated that P. keilini possesses a metabolism and gene complement that are in many respects similar to its parasitic relative Trichomonas vaginalis, and that in the time since their most recent common ancestor, it is the Trichomonas vaginalis lineage that has experienced more genomic change, likely due to the transition to a parasitic lifestyle. Features shared between P. keilini and Trichomonas vaginalis include a hydrogenosome (anaerobic mitochondrial homologue) that we predict to function much as in Trichomonas vaginalis, and a complete glycolytic pathway that is likely to represent one of the primary means by which P. keilini obtains ATP. Phylogenomic analysis indicates that P. keilini branches within a clade of endobiotic parabasalids, consistent with the hypothesis that different parabasalid lineages evolved towards parasitic or free-living lifestyles from an endobiotic, anaerobic or microaerophilic common ancestor.