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

• Published in: Nature communications 2024-08, Vol.15 (1), p.6805-14, Article 6805
• Main Authors: Williams, Shelby K., Jerlström Hultqvist, Jon, Eglit, Yana, Salas-Leiva, Dayana E., Curtis, Bruce, Orr, Russell J. S., Stairs, Courtney W., Atalay, Tuğba N., MacMillan, Naomi, Simpson, Alastair G. B., Roger, Andrew J.
• Format: Article
• Language: English
• Subjects: 45; 45/22; 45/91; 631/181/735; 631/181/757; 631/208/212/2304; 631/80/642/333/1465; Biologi; Biological Sciences; Clusters; Eukaryota - classification; Eukaryota - genetics; Eukaryota - metabolism; Eukaryotes; Flagellates; Gene transfer; Gene Transfer, Horizontal; Humanities and Social Sciences; Hypoxia; Iron; Iron-Sulfur Proteins - genetics; Iron-Sulfur Proteins - metabolism; Microbiology; Microorganisms; Mikrobiologi; Mitochondria; Mitochondria - genetics; Mitochondria - metabolism; multidisciplinary; Natural Sciences; Naturvetenskap; Organelles; Organisms; Phylogeny; Plastic foam; Proteome - genetics; Proteome - metabolism; Proteomes; Science; Science (multidisciplinary); Sulfur; Transcriptome; Transcriptomes
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-50991-w

Metamonads 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, however the degree of reduction varies. Here, we generate high-quality draft genomes, transcriptomes, and predicted proteomes for five recently discovered free-living metamonads. Phylogenomic analyses placed these organisms in a group we name the ‘BaSk’ (Barthelonids+Skoliomonads) clade, a deeply branching sister group to the Fornicata, a phylum that includes parasitic and free-living flagellates. Bioinformatic analyses of gene models shows that these organisms are predicted to have extremely reduced MRO proteomes in comparison to other free-living metamonads. Loss of the mitochondrial iron-sulfur cluster 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 Fe/S cluster pathway by lateral gene transfer. One of the isolates, Skoliomonas litria , appears to have lost all other known MRO pathways. No proteins were confidently assigned to the predicted MRO proteome of this organism suggesting that the organelle has been lost. The extreme mitochondrial reduction observed within this free-living anaerobic protistan clade demonstrates that mitochondrial functions may be completely lost even in free-living organisms. Mitochondria are essential cellular components that are found in animals, plants, fungi, and protists. This study reports what is believed to be the first example of complete mitochondrial loss in a free-living organism, providing insights into the evolutionary plasticity of eukaryotic cells.