Organelles in Blastocystis that Blur the Distinction between Mitochondria and Hydrogenosomes

Abstract

SummaryBlastocystis is a unicellular stramenopile of controversial pathogenicity in humans [1, 2]. Although it is a strict anaerobe, Blastocystis has mitochondrion-like organelles with cristae, a transmembrane potential and DNA [2–4]. An apparent lack of several typical mitochondrial pathways has led some to suggest that these organelles might be hydrogenosomes, anaerobic organelles related to mitochondria [5, 6]. We generated 12,767 expressed sequence tags (ESTs) from Blastocystis and identified 115 clusters that encode putative mitochondrial and hydrogenosomal proteins. Among these is the canonical hydrogenosomal protein iron-only [FeFe] hydrogenase that we show localizes to the organelles. The organelles also have mitochondrial characteristics, including pathways for amino acid metabolism, iron-sulfur cluster biogenesis, and an incomplete tricarboxylic acid cycle as well as a mitochondrial genome. Although complexes I and II of the electron transport chain (ETC) are present, we found no evidence for complexes III and IV or F1Fo ATPases. The Blastocystis organelles have metabolic properties of aerobic and anaerobic mitochondria and of hydrogenosomes [7, 8]. They are convergently similar to organelles recently described in the unrelated ciliate Nyctotherus ovalis[9]. These findings blur the boundaries between mitochondria, hydrogenosomes, and mitosomes, as currently defined, underscoring the disparate selective forces that shape these organelles in eukaryotes.

Recent Developments in Blastocystis Research

“…Overall, the complete genome of Blastocystis (Denoeud et al, 2011) has confirmed many previous studies (Lantsman et al, 2008;Stechmann et al, 2008;Zierdt, 1986;Zierdt et al, 1988) with respect to the biochemical nature of the MLO but several questions still remain. Perhaps the most significant one relates to the anaerobic status of this organism (Zierdt, 1986), as its genome suggests that it most likely is not a strict anaerobe after all.…”

“…Two possible red algal genes might hint at a lost chromalveolate plastid while others might be involved in some aspects of anaerobic fermentation (Denoeud et al, 2011). The anaerobic nature of Blastocystis combined with the presence of MLOs with cristae that are capable of taking up active dyes such as Rhodamine 123 (Nasirudeen and Tan, 2004) has sparked an interest in the nature of these organelles (Denoeud et al, 2011;Lantsman et al, 2008;Stechmann et al, 2008). Unlike classic mitochondria, the Blastocystis organelles contain the enzymatic capability to convert pyruvate into CO2 and H2 using enzymes normally encountered in hydrogenosomes (van der Giezen, 2009).…”

“…Unlike classic mitochondria, the Blastocystis organelles contain the enzymatic capability to convert pyruvate into CO2 and H2 using enzymes normally encountered in hydrogenosomes (van der Giezen, 2009). Although hydrogen production has not been detected (Lantsman et al, 2008), the enzyme hydrogenase does localise to the organelle (Stechmann et al, 2008). Furthermore, the organelle contains the unusual acetate: succinateCoA transferase (ASCT) shuttle, which allows for the production of ATP via substrate-level phosphorylation.…”

“…The absence of cytochromes had been reported early on (Zierdt, 1986) so the lack of mitochondrial Complex III and IV components in the genome came as no surprise. Many genes encoding proteins that make up Complex I, possibly involved in proton pumping, have been detected, as has a complete Complex II (Denoeud et al, 2011;Stechmann et al, 2008). As no further downstream electron transport chain components have been found, the question whether Complex II functions as a succinate dehydrogenase, as in classical mitochondria, or as a fumarate reductase, is still open.…”

Evolution of Fe/S cluster biogenesis in the anaerobic parasite Blastocystis

“…To clarify the functions of these organelles, the first broad transcriptomic (12) and genomic (13) studies of Blastocystis were recently completed; these studies have identified 115 and 360 genes, respectively, encoding putative mitochondrial and hydrogenosomal proteins. Among these were mitochondrial ISC system proteins (12)(13)(14)(15), suggesting that Fe/S cluster biogenesis is a core function of Blastocystis MROs. Components of the CIA machinery have also been identified in the Blastocystis transcriptome.…”