The Earliest Stages of Mitochondrial Adaptation to Low Oxygen Revealed in a Novel Rhizarian.
Mitochondria exist on a functional and evolutionary continuum that includes anaerobic mitochondrion-related organelles (MROs), such as hydrogenosomes. Hydrogenosomes lack many classical mitochondrial features, including conspicuous cristae, mtDNA, the tricarboxylic acid (TCA) cycle, and ATP synthesis powered by an electron transport chain (ETC); instead, they produce ATP anaerobically, liberating H2and CO2gas in the process. However, our understanding of the evolutionary transformation from aerobic mitochondria to various MRO types remains incomplete. Here we describe a novel MRO from a cercomonad (Brevimastigomonas motovehiculus n. sp.; Rhizaria). We have sequenced its 30,608-bp mtDNA and characterized organelle function through a combination of transcriptomic, genomic, and cell biological approaches. B. motovehiculus MROs are metabolically versatile, retaining mitochondrial metabolic pathways, such as a TCA cycle and ETC-driven ATP synthesis, but also possessing hydrogenosomal-type pyruvate metabolism and substrate-level phosphorylation. Notably, the B. motovehiculus ETC is degenerate and appears to be losing cytochrome-based electron transport (complexes III and IV). Furthermore, the F1FoATP synthase (complex V) is unique, with the highly conserved Atpα subunit fragmented into four separate pieces. The B. motovehiculus MRO appears to be in the process of losing aerobic metabolic capacities. Our findings shed light on the transition between organelle types, specifically the early stages of mitochondrial adaptation to anaerobiosis.
Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS B3H 4R2, Canada; Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS B3H 4R2, Canada.
Ryan M R
RMR
Gawryluk
Graduate School of Human and Environmental Studies, Kyoto University, Kyoto 606-8501, Japan; Graduate School of Global Environmental Studies, Kyoto University, Kyoto 606-8501, Japan.
Ryoma
R
Kamikawa
Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS B3H 4R2, Canada; Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS B3H 4R2, Canada.
Courtney W
CW
Stairs
Department of Biological Sciences, University of Arkansas, Fayetteville, AR 72701, USA.
Jeffrey D
JD
Silberman
Department of Biological Sciences, Mississippi State University, Mississippi State, MS 39762, USA; Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA.
Matthew W
MW
Brown
Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS B3H 4R2, Canada; Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS B3H 4R2, Canada; Program in Integrated Microbial Biodiversity, Canadian Institute for Advanced Research, Halifax, NS B3H 4R2, Canada. Electronic address: andrew.roger@dal.ca.
Andrew J
AJ
Roger
D000220:Adaptation, Biological; D000595:Amino Acid Sequence; D000693:Anaerobiosis; D005075:Biological Evolution; D056907:Cercozoa / Q000145:classification / Q000235:genetics / Q000502:physiology*; D008928:Mitochondria / Q000502:physiology*; D010100:Oxygen / Q000378:metabolism; D010802:Phylogeny; D015800:Protozoan Proteins / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism; D016415:Sequence Alignment
D015800:Protozoan Proteins; D010100:Oxygen
ATP synthase; anaerobic; electron transport chain; evolution; hydrogenosome; mitochondria; protist; tricarboxylic acid cycle