Extreme mitochondrial reduction in a novel group of free-living metamonads

Abstract

AbstractMetamonads are a diverse group of heterotrophic microbial eukaryotes adapted to living in hypoxic environments. All metamonads but one harbour metabolically altered ‘mitochondrion-related organelles’ (MROs) with reduced functions relative to aerobic mitochondria, however the degree of reduction varies markedly over the metamonad tree. To further investigate metamonad MRO diversity, we generated high quality draft genomes, transcriptomes, and predicted proteomes for five recently discovered free-living metamonads. Phylogenomic analyses place these organisms in a clade sister to the Fornicata – a group of metamonads that includes parasitic and free-living diplomonads andCarpediemonas-like organisms. Extensive bioinformatic analyses of the manually curated gene models showed that these organisms have extremely reduced MROs in comparison to other free-living metamonads. Loss of the mitochondrial iron-sulfur cluster (ISC) assembly system in some organisms in this group appears to be linked to the acquisition in their common ancestral lineage of a SUF-like minimal system (SMS) Fe/S cluster pathway through lateral gene transfer (LGT). One of the isolates, named ‘RC’, appears to have undergone even more drastic mitochondrial reduction losing almost all other detectable MRO-related functions. The extreme mitochondrial reduction observed within this free-living anaerobic protistan clade is unprecedented and demonstrates that mitochondrial functions, under some conditions, can be almost completely lost even in free-living organisms.