J.H.P. Hackstein

Multiple origins of hydrogenosomes : functional and phylogenetic evidence from the ADP/ATP carrier of the anaerobic chytrid Neocallimastix sp.

A mitochondrial‐type ADP/ATP carrier (AAC) has been identified in the hydrogenosomes of the anaerobic chytridiomycete fungus Neocallimastix sp. L2. Biochemical and immunocytochemical studies revealed that this ADP/ATP carrier is an integral component of hydrogenosomal membranes. Expression of the corresponding cDNA in Escherichia coli confers the ability on the bacterial host to incorporate ADP at significantly higher rates than ATP – similar to isolated mitochondria of yeast and animals. Phylogenetic analysis of this AAC gene (hdgaac) confirmed with high statistical support that the hydrogenosomal ADP/ATP carrier of Neocallimastix sp. L2 belongs to the family of veritable mitochondrial‐type AACs. Hydrogenosome‐bearing anaerobic ciliates possess clearly distinct mitochondrial‐type AACs, whereas the potential hydrogenosomal carrier Hmp31 of the anaerobic flagellate Trichomonas vaginalis and its homologue from Trichomonas gallinae do not belong to this family of proteins. Also, phylogenetic analysis of genes encoding mitochondrial‐type chaperonin 60 proteins (HSP 60) supports the conclusion that the hydrogenosomes of anaerobic chytrids and anaerobic ciliates had independent origins, although both of them arose from mitochondria.

Hydrogenosomes: convergent adaptations of mitochondria to anaerobic environments

Hydrogenosomes are membrane-bound organelles that compartmentalise the final steps of energy metabolism in a number of anaerobic eukaryotes. They produce hydrogen and ATP. Here we will review the data, which are relevant for the questions: how did the hydrogenosomes originate, and what was their ancestor? Notably, there is strong evidence that hydrogenosomes evolved several times as adaptations to anaerobic environments. Most likely, hydrogenosomes and mitochondria share a common ancestor, but an unequivocal proof for this hypothesis is difficult because hydrogenosomes lack an organelle genome - with one remarkable exception (Nyctotherus ovalis). In particular, the diversity of extant hydrogenosomes hampers a straightforward analysis of their origins. Nevertheless, it is conceivable to postulate that the common ancestor of mitochondria and hydrogenosomes was a facultative anaerobic organelle that participated in the early radiation of unicellular eukaryotes. Consequently, it is reasonable to assume that both, hydrogenosomes and mitochondria are evolutionary adaptations to anaerobic or aerobic environments, respectively.

Voltage-Dependent Reversal of Anodic Galvanotaxis in Nyctotherus ovalis

Aerobic and anaerobic ciliates swim towards the cathode when they are exposed to a constant DC field. Nyctotherus ovalis from the intestinal tract of cockroaches exhibits a different galvanotactic response: at low strength of the DC field the ciliates orient towards the anode whereas DC fields above 2–4 V/cm cause cathodic swimming. This reversal of the galvanotactic response is not due to backward swimming. Rather the ciliates turn around and orient to the cathode with their anterior pole. Exposure to various cations, chelators, and Ca2‐‐channel inhibitors suggests that Ca2‐‐channels similar to the “long lasting” Ca2‐‐channels of vertebrates are involved in the voltage‐dependent anodic galvanotaxis. Evidence is presented that host‐dependent epigenetic factors can influence the voltage‐threshold for the switch from anodic to cathodic swimming.

Multiple origins of hydrogenosomes

A mitochondrial‐type ADP/ATP carrier (AAC) has been identified in the hydrogenosomes of the anaerobic chytridiomycete fungus Neocallimastix sp. L2. Biochemical and immunocytochemical studies revealed that this ADP/ATP carrier is an integral component of hydrogenosomal membranes. Expression of the corresponding cDNA in Escherichia coli confers the ability on the bacterial host to incorporate ADP at significantly higher rates than ATP – similar to isolated mitochondria of yeast and animals. Phylogenetic analysis of this AAC gene (hdgaac) confirmed with high statistical support that the hydrogenosomal ADP/ATP carrier of Neocallimastix sp. L2 belongs to the family of veritable mitochondrial‐type AACs. Hydrogenosome‐bearing anaerobic ciliates possess clearly distinct mitochondrial‐type AACs, whereas the potential hydrogenosomal carrier Hmp31 of the anaerobic flagellate Trichomonas vaginalis and its homologue from Trichomonas gallinae do not belong to this family of proteins. Also, phylogenetic analysis of genes encoding mitochondrial‐type chaperonin 60 proteins (HSP 60) supports the conclusion that the hydrogenosomes of anaerobic chytrids and anaerobic ciliates had independent origins, although both of them arose from mitochondria.

Symbiotic Associations Between Methanogenic Archaea, Protists and Metazoa: Evolutionary Implications

Long-lasting associations between organisms that belong to different taxa are described as “symbiosis”. They are very complex phenomena and, as we will emphasize in this essay, “symbiosis” can have a meaning beyond an exchange of nutrients and vitamins (Margulis 1976; Rennie 1992). Symbiosis requires a continuous cross-talk between organisms in the form of informational, physiological and behavioural interactions. Additionally, symbiotic associations have their peculiar evolutionary histories, involving co-evolution of host and symbiont (Douglas 1994; Moran and Baumann 1994; Page and Hafner 1996; Werren 1997; Hackstein 1997).

Biogenesis of hydrogenosomes in Psalteriomonas lanterna: no evidence for an exogenosomal ancestry

Hydrogenosomes are cellular organelles that occur exclusively in certain anaerobic, unicellular eukaryotes and some anaerobic fungi (reviewed in Muller 1993). The key enzymes of this organelle are a hydrogenase and a pyruvate: ferredoxin oxidoreductase (Lindmark and Muller 1973; Muller 1988). Hydrogenosomes are engaged with the anaerobic cellular energy metabolism, and they generate hydrogen and acetate if supplied with their characteristic substrates pyruvate or malate (Muller 1993). Hydrogenosomes in trichomonads have been studied extensively, but knowledge about such organelles in most of the other anaerobes is fragmentary. Frequently, identification as a hydrogenosome depends solely on a cyto-chemical hydrogenase assay and on ultrastructural similarities. Their occurrence in distantly related organisms, however, and substantial differences in shape and fine structure strongly suggest that the hydrogenosomes of the various protists and fungi are not the same (Fig. 1; cf. Coombs and Hackstein 1995).