Genomics of Preaxostyla Flagellates Illuminates the Path Towards the Loss of Mitochondria

Abstract

Until recently, mitochondria were considered essential organelles impossible to truly lose in a lineage. This view changed in 2016, with the report that the oxymonadMonocercomonoides exilis, was the first known eukaryote without any mitochondrion. Questions remain, however, about whether this extends to the entire lineage and how this transition took place. Oxymonadida are a group of gut endobionts of insects, reptiles, and mammals. They are housed in the Preaxostyla (Metamonada), a protistan group that also contains free-living flagellates of generaTrimastixandParatrimastix. These latter two taxa harbor conspicuous mitochondrion-related organelles (MROs), while no mitochondria were reported for any oxymonad. Here we report genomic data sets of two Preaxostyla representatives, the free-livingParatrimastix pyriformisand the oxymonadBlattamonas nauphoetae. We note thatP. pyriformispossesses a set of unique or ancestral features among metamonads or eukaryotes, e.g.,p-cresol synthesis, UFMylation system, NAD+synthesis, selenium volatilization, or mercury methylation, demonstrating the biochemical versatility of this protist lineage. We performed thorough comparisons among all available genomic and transcriptomic data of Preaxostyla to corroborate both the absence of MRO in Oxymonadida and the nature of MROs present in other Preaxostyla and to decipher the evolutionary transition towards amitochondriality and endobiosis. Our results provide insights into the metabolic and endomembrane evolution, but most strikingly the data confirm the complete loss of mitochondria and every protein that has ever participated in the mitochondrion function for all three oxymonad species (M. exilis,B. nauphoetae, andStreblomastix strix) extending the amitochondriate status to the whole Oxymonadida.

A mitochondrion-free eukaryote contains proteins capable of import into an exogenous mitochondrion-related organelle

“…The potential caveat is the secondary amitochondriate status of M. exilis , due to which it cannot be strictly excluded that features of some proteins are still affected by the past presence of the mitochondrion. This is, however, very unlikely, as the loss of mitochondria in the oxymonad lineage happened at least a 100 Ma, and more importantly, there is no evidence for the presence of any originally mitochondrial protein in the current proteome of M. exilis (Novak et al in prep [34]). The hydrogenosome of T. vaginalis is obviously remote from the original mitochondrial endosymbiont, but its translocation system is arguably simpler than the one in aerobic mitochondria [26], so it may mimic the primitive situation well.…”

Protist symbionts of termites: diversity, distribution, and coevolution

“…Metamonada prefer low-oxygen environments, either living free in anaerobic sediments or, more commonly, living inside animals as parasites or commensals (Adam, 2017;Kulda, Nohýnkov a & Čepička, 2017). They tend to have reduced mitochondria that lack genomes (hydrogenosomes or mitosomes) or lack mitochondria completely in the case of Monocercomonoides and relatives (Preaxostyla) (Karnkowska et al, 2016;Hampl, 2017;Nov ak et al, 2023). The bestknown Metamonada are the human parasites Trichomonas vaginalis (Parabasalia, Trichomonadida) and Giardia lamblia (Fornicata, Diplomonadida).…”

“…Blattamonas, Monocercomonoides) (Brugerolle & Lee, 2000a;Hampl, 2017;Treitli et al, 2018). Mitochondria-like organelles have been secondarily lost in this lineage (Karnkowska et al, 2016(Karnkowska et al, , 2019Nov ak et al, 2023). The axostyle is a rod made of interlinked rows of microtubules (the parabasalian axostyle is a rolled microtubular sheet or a bundle of rolled sheets), and in some of the larger termite-associated genera it can be flexible and motile (e.g.…”