The Diversity and Origins of Mitochondrion-Related Organelles

Abstract

Multiple distantly-related eukaryotic lineages have adapted to low-oxygen environments, and possess modified mitochondria, known as mitochondrion-related organelles (MROs). Although relatively few MROs have been investigated in detail, they are known to vary in the types of ATP metabolism they possess, and in the nature of the ancestral mitochondrial functions that they have retained. Here, I expand our knowledge of this diversity, and provide insights into how characteristic anaerobic ATP generation enzymes became widespread among eukaryotes. MROs known as hydrogenosomes have lost the electron transport chain, and possess a distinctive anaerobic ATP generation pathway that produces hydrogen as an end-product. I describe this type of ATP generation pathway in Acanthamoeba castellanii, an amoebozoan previously believed to have typical aerobic mitochondria and I show that this pathway is located in the mitochondria using immunolocalization. This is the first known example of a mitochondrion that possesses both a complete electron transport chain and a complete hydrogenosomal-like ATP generation pathway. Bacterial cell division is initiated by a tubulin homolog, FtsZ, and three Min proteins that regulate its distribution. In mitochondria, this system has been supplanted by eukaryotic dynamin-related proteins. I show that mitochondrial homologs of FtsZ are widespread among eukaryotes, and that they were likely duplicated in the last eukaryotic common ancestor. I also provide the first evidence for the existence of Min proteins in mitochondria, and show that they are present in four out of six eukaryotic supergroups. The ancestral FtsZ-Min system is more representative of mitochondrial division in diverse eukaryotes than is the dynamin-based system of eukaryotic model organisms. Finally, I present an in silico reconstruction of the biochemical pathways present in the MRO of Andalucia incarcerata, a free-living, deep-branching excavate protist, and validate some of these predictions with immunolocalization. A. incarcerata’s MRO possesses a hydrogenosomal-like ATP generation pathway that presents a striking example of convergence with those of other, distantly anaerobic eukaryotes. However, it retains a greater complement of mitochondrial metabolic functions and import machinery than the well-described MROs of parasites. My work shows that this larger complement of ancestral mitochondrial functions is a common feature shared by MROs of free-living eukaryotes.