The Trichomonas vaginalis hydrogenosome proteome is highly reduced relative to mitochondria, yet complex compared with mitosomes

Abstract

The human pathogen Trichomonas vaginalis lacks conventional mitochondria and instead contains divergent mitochondrial-related organelles. These double-membrane bound organelles, called hydrogenosomes, produce molecular hydrogen. Phylogenetic and biochemical analyses of hydrogenosomes indicate a common origin with mitochondria; however identification of hydrogenosomal proteins and studies on its metabolism have been limited. Here we provide a detailed proteomic analysis of the T. vaginalis hydrogenosome. The proteome of purified hydrogenosomes consists of 569 proteins, a number substantially lower than the 1,000 - 1,500 proteins reported for fungal and animal mitochondrial proteomes, yet considerably higher than proteins assigned to mitosomes. Pathways common to and distinct from both mitochondria and mitosomes were revealed by the hydrogenosome proteome. Proteins known to function in amino acid and energy metabolism, Fe-S cluster assembly, flavin-mediated catalysis, oxygen stress response, membrane translocation, chaperonin functions, proteolytic processing and ATP hydrolysis account for ∼30% of the hydrogenosome proteome. Of the 569 proteins in the hydrogenosome proteome, many appear to be associated with the external surface of hydrogenosomes, including large numbers of GTPases and ribosomal proteins. Glycolytic proteins were also found to be associated with the hydrogenosome proteome, similar to that previously observed for mitochondrial proteomes. Approximately 18% of the hydrogenosomal proteome is composed of hypothetical proteins of unknown function, predictive of multiple activities and properties yet to be uncovered for these highly adapted organelles.

N-Terminal Presequence-Independent Import of Phosphofructokinase into Hydrogenosomes of Trichomonas vaginalis

“…Through the HA-tagged TvATP-PFK1, products of four paralogous TvATP-PFK genes were immunoprecipitated from isolated hydrogenosomes and identified by mass spectrometry. Earlier proteomic studies suggested association of the glycolytic pathway, including TvATP-PFK, with the hydrogenosome (13,15), which raises the question of whether glycolytic enzymes form functional protein complexes on the hydrogenosomal outer membrane, as has been shown for mitochondria. For example, in Arabidopsis thaliana, 5 to 10% of each glycolytic enzyme is associated with the outer mitochondrial surface.…”

“…Therefore, it was surprising that genes for ATP-dependent phosphofructokinase (ATP-PFK) turned up in the Trichomonas genome (12). Furthermore, peptides of the expressed protein were found in the hydrogenosomal proteome (13-15), although the exact topology of hydrogenosome-associated T. vaginalis ATP-PFK (TvATP-PFK) remains unclear (13,15). PP i -PFK and ATP-PFK share an evolutionary origin (16,17).…”

The Genome of the Anaerobic Fungus Orpinomyces sp. Strain C1A Reveals the Unique Evolutionary History of a Remarkable Plant Biomass Degrader

“…For example, members of the Neocallimastigomycota have adapted a strict anaerobic lifestyle. Similar to other anaerobic eukaryotes (e.g., Trichomonas vaginalis [6,7]), their mitochondria have undergone a reductive evolution process to a hydrogenosome, an organelle whose main function is ATP production via substrate-level phosphorylation and hydrogen production (6,8,9). Anaerobic fungi also reproduce asexually via the release of motile flagellated zoospores from zoosporangia that develop during rhizoidal fungal growth (10,11).…”

Trichomonas vaginalis: Clinical relevance, pathogenicity and diagnosis

“…The cell also possesses an axostyl, a bundle of microtubules passing through the cell along its anterior-posterior axis into the extracellular environment , which has a function in cell attachment and mitosis (Ribeiro et al, 2000). The cytoplasm contains a single defined nucleus, and several hydrogenosomes; primitive redox organelles, evolved from mitochondria, which produce molecular hydrogen and ATP (Schneider et al, 2011).…”