Highly divergent mitochondrion-related organelles in anaerobic parasitic protozoa

Abstract

The mitochondria have arisen as a consequence of endosymbiosis of an ancestral α-proteobacterium with a methane-producing archae. The main function of the canonical aerobic mitochondria include ATP generation via oxidative phosphorylation, heme and phospholipid synthesis, calcium homeostasis, programmed cell death, and the formation of iron-sulfur clusters. Under oxygen-restricted conditions, the mitochondrion has often undergone remarkable reductive alterations of its content and function, leading to the generation of mitochondrion-related organelles (MROs), such as mitosomes, hydrogenosomes, and mithochondrion-like organelles, which are found in a wide range of anaerobic/microaerophilic eukaryotes that include several medically important parasitic protists such as Entamoeba histolytica, Giardia intestinalis, Trichomonas vaginalis, Cryptosporidium parvum, Blastocystis hominis, and Encephalitozoon cuniculi, as well as free-living protists such as Sawyeria marylandensis, Neocallimastix patriciarum, and Mastigamoeba balamuthi. The transformation from canonical aerobic mitochondria to MROs apparently have occurred in independent lineages, and resulted in the diversity of their components and functions. Due to medical and veterinary importance of the MRO-possessing human- and animal-pathogenic protozoa, their genomic, transcriptomic, proteomic, and biochemical evidence has been accumulated. Detailed analyses of the constituents and functions of the MROs in such anaerobic pathogenic protozoa, which reside oxygen-deprived or oxygen-poor environments such as the mammalian intestine and the genital organs, should illuminate the current evolutionary status of the MROs in these organisms, and give insight to environmental constraints that drive the evolution of eukaryotes and their organelles. In this review, we summarize and discuss the diverse metabolic functions and protein transport systems of the MROs from anaerobic parasitic protozoa.

Peculiarities within peculiarities – dinoflagellates and their mitochondrial genomes

“…mitosomes (Liu et al 2016). But mitosomes, hydrogenosomes and other mitochondrion-related organelles (reviewed by Makiuchi & Nozaki 2014) have only evolved in parasitic lineages under anaerobic/hypoxic conditions, in which the energetic resources of the host are aplenty. In such environments, the abundance of host metabolites affects not only the mitochondrial genome but also the nuclear and plastid genomes as well.…”

Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis

“…Furthermore, MROs occasionally acquire novel functions from other organisms by lateral gene transfer (LGT) (1,3). Hence, MROs are not simply remnants of mitochondria but rather are organelles that display a variety of unique features (1)(2)(3)(4)(5).…”

“…Unique features have been demonstrated in different types of MRO (2)(3)(4). Some anaerobic lineages of eukaryotes possess MROs (hydrogenosomes or hydrogen-producing mitochondria) that have remodeled their mitochondria drastically to couple ATP generation with hydrogen production (2)(3)(4).…”

“…Some anaerobic lineages of eukaryotes possess MROs (hydrogenosomes or hydrogen-producing mitochondria) that have remodeled their mitochondria drastically to couple ATP generation with hydrogen production (2)(3)(4). Mitosomes, another type of MRO maintained in some organisms that inhabit anaerobic/microaerophilic environments, do not produce ATP or hydrogen and have lost typical mitochondrial functions, such as the tricarboxylic acid (TCA) cycle, electron transport, oxidative phosphorylation, and β-oxidation of fatty acids (1,2).…”

Iron–sulfur cluster biogenesis and trafficking in mitochondria

“…1 and 2) (2, 16). Mitochondria or the evolutionarily derived hydrogenosomes and mitosomes appear to be essential for biogenesis of all cellular Fe/S proteins (7,17,18). The only notable exception to this rule may be a newly characterized eukaryotic organism, which appears to be devoid of mitochondria (19).…”