The Biochemical Adaptations of Mitochondrion-Related Organelles of Parasitic and Free-Living Microbial Eukaryotes to Low Oxygen Environments

Abstract

While many multicellular anaerobes possess mitochondria that resemble those of aerobic eukaryotes, microbial eukaryotes that live exclusively in anoxic and low oxygen environments harbor mitochondrion-related organelles (MROs). Currently, these organelles are broadly classified as either hydrogenosomes (anaerobic ATP-producing organelles that produce molecular hydrogen) or mitosomes (organelles that do not generate ATP); however, ongoing studies of diverse microbial lineages are revealing a wider spectrum of functional types. In adaptation to low oxygen conditions, the MROs of anaerobic eukaryotes have acquired unique characteristics, some of which do not appear to derive from the $α$-proteobacterium that gave rise to the ancestral mitochondrion. These characteristics include alternative pathways for pyruvate metabolism as well as enzymes such as [FeFe]-hydrogenases that collectively function in anaerobic energy metabolism. In addition to these pathways, the mitochondrial protein import, metabolic exchange, and Fe--S cluster biosynthesis machineries are present in all MROs studied to date; these systems support the protein, solute, and energy requirements of both the organelles and the cells that harbor them. MROs represent a unique class of organelles that have successfully adapted by reduction or alteration of existing pathways as well as by acquisition of novel metabolic machineries that allowed their hosts to thrive in diverse environments without oxygen.