Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex

Abstract

Trichomonas vaginalis is a unicellular microaerophilic eukaryote that lacks mitochondria yet contains an alternative organelle, the hydrogenosome, involved in pyruvate metabolism. Pathways between the two organelles differ substantially: in hydrogenosomes, pyruvate oxidation is catalysed by pyruvate:ferredoxin oxidoreductase (PFOR), with electrons donated to an [Fe]-hydrogenase which produces hydrogen. ATP is generated exclusively by substrate-level phosphorylation in hydrogenosomes, as opposed to oxidative phosphorylation in mitochondria. PFOR and hydrogenase are found in eubacteria and amitochondriate eukaryotes, but not in typical mitochondria. Analyses of mitochondrial genomes indicate that mitochondria have a single endosymbiotic origin from an alpha-proteobacterial-type progenitor. The absence of a genome in trichomonad hydrogenosomes precludes such comparisons, leaving the endosymbiotic history of this organelle unclear. Although phylogenetic reconstructions of a few proteins indicate that trichomonad hydrogenosomes share a common origin with mitochondria, others do not. Here we describe a novel NADH dehydrogenase module of respiratory complex I that is coupled to the central hydrogenosomal fermentative pathway to form a hydrogenosomal oxidoreductase complex that seems to function independently of quinones. Phylogenetic analyses of hydrogenosomal complex I-like proteins Ndh51 and Ndh24 reveal that neither has a common origin with mitochondrial homologues. These studies argue against a vertical origin of trichomonad hydrogenosomes from the proto-mitochondrial endosymbiont.

Multiple secondary origins of the anaerobic lifestyle in eukaryotes

“…They catalyse the enzymatic assembly and insertion of Fe-S centres into apoproteins, using the same enzymes, inherited from the mitochondrial endosymbiont, as do yeast mitochondria (Sutak et al 2004). Trichomonas hydrogenosomes also contain the NADH dehydrogenase module of complex I of the mitochondrial respiratory chain , although the reader should be aware that this last conclusion is controversial (see Gray 2005), because an alternative origin from another bacterium had previously been suggested for this module (Dyall et al 2004b). While these data are clearly difficult to analyse using conventional phylogenetic methods, it is important to appreciate that they cannot reject a common origin of Trichomonas and mitochondrial proteins using standard tests .…”

“…that all sequences evolve in the same way, so the aberrant behaviour of Archezoan sequences can make their phylogenetic position difficult to infer reliably (see Roger & Hug 2006). The difficulty experienced when trying to resolve the origins of the Trichomonas hydrogenosomal NADH dehydrogenase provides just one example of the kind of problems that can be encountered (Dyall et al 2004b;Hrdy et al 2004;Gray 2005). The case for a rethink is clear-cut for Microsporidia because most data and analyses now agree in placing them with fungi rather than as deep branching eukaryotes Keeling et al 2000;Inagaki et al 2004;Thomarat et al 2004).…”

Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts

“…A similar situation occurs in the termite gut spirochete T. azotonutricium . The observed hydrogen formation from unfavorable electron donors may be driven by reverse electron transport via a membrane-bound NADH:ferredoxin oxidoreductase (Boiangiu et al, 2005), or directly by a modified complex I, as proposed for hydrogenosomes of Trichomonas vaginalis (Dyall et al, 2004). Complex I is proposed to be related to energyconverting hydrogenases (Hedderich and Forzi, 2005).…”

Pyruvate Formate-lyase and a Novel Route of Eukaryotic ATP Synthesis in Chlamydomonas Mitochondria

“…The evolutionary origins of such enzymes for the anaerobic lifestyle in eukaryotes remains heavily debated. Either (i) the eukaryote common ancestor was a strict aerobe and anaerobic biochemistry in eukaryotes was acquired secondarily via lateral gene transfer (3,4) or (ii) it was a facultative anaerobe, with its descendant lineages having undergone specialization and differential loss (5)(6)(7)(8).…”