Evolutionary Origin of Anaerobic Mitochondria

It is now generally accepted that the classical aerobic mitochondria evolved by a single endosymbiotic event between an anaerobic host and an a-proteobacterium. Endosymbiotic theories for the origin of cellular organelles had already been postulated at the end of the nineteenth and early in the twentieth century, but the publications of Margulis in the second half of the twentieth century renewed interest in the theory that mitochondria originate from an endosymbiotic event (Margulis 2005; see also Chap. 4 by Sapp in this volume). However, that theory needed refinement as various organelles were recently shown to exist that, although different, are clearly related to mitochondria (Martin and Müller 1998; Gray et al. 1999). Next to the classical aerobic mitochondria, which contain a respiratory chain and use oxygen as a final electron acceptor, anaerobically functioning mitochondria were identified that also contain a respiratory chain and perform oxidative phosphorylation, but do not use oxygen as a terminal electron acceptor (see before). In addition, several eukaryotes were identified that contained hydrogenosomes, double membrane bound, ATP-producing organelles that are related to mitochondria (Embley et al. 2003b; Dyall et al. 2004). Hydrogenosomes, however, differ from mitochondria as they lack a respiratory chain and produce hydrogen (see Chap. 6 by Tachezy and Dolezal, Chap. 7 by Hackstein et al. and Chap. 11 by Tovar for details). Several types of hydrogenosomes exist (Fig. 5.1) and they have evolved independently in unrelated lineages of eukaryotic microorganisms (Yarlett et al. 1984; Embley et al. 1995; Martin et al. 2001; Hackstein et al. 2001; Van der Giezen et al. 2005). Furthermore, several eukaryotes were shown to lack compartmentation of energy metabolism, but these organisms were nevertheless shown to contain organelles related to mitochondria (mitosomes) (see before and Chap. 10 by Barbera et al. for details). Although it is generally believed that all these organelles related to mitochondria share a common ancestor, the ancestral endosymbiont, evolution of the distinct types is hotly debated. It is conceivable that the distinct variants of anaerobically ATP-generating organelles all evolved directly from the ancestral endosymbiont. Alternatively, the different anaerobic types of organelles could have evolved from each other or from aerobic ones in a more dynamic fashion, where adaptations to the absence of oxygen turned aerobic mitochondria into anaerobically functioning ones (or where the energy-generating function of the organelle was even lost all together). It should be noted, however, that the distinct types of organelles related to mitochondria did not necessarily develope via the same evolutionary pathway.

Several observations indicate that anaerobically functioning mitochondria evolved from the classical aerobically functioning mitochondria, and did not originate directly (by adaptation to an anaerobic environment) from the facultative anaerobic ancestral cell that was the result of the endosymbiosis of an a-proteobacterial symbiont and the host cell. First, as discussed before, all sequence data available up to now on the fumarate-reducing enzymes (FRDs) of these organisms demonstrate that these enzymes are closely related to the SDHs of classical aerobic mitochondria. Second, the same argument holds true for the quinone used for this anaerobic fumarate reduction. All anaero-bically functioning, fumarate-reducing eukaryotes investigated so far use rhodoquinone for the transport of electrons from complex I to the fumarate-

reducing enzyme, while the more ancient prokaryotic systems use menaquinone. Again, the anaerobically functioning mitochondria use a molecule (rhodoquinone) which, as it is a benzoquinone, is structurally more related to the molecule of the classical mitochondria, ubiquinone (also a ben-zoquinone) than to the molecule used by the anaerobic prokaryotes, menaquinone (a naphthoquinone). As the synthesis of rhodoquinone probably differs only in one of the last steps from the synthesis of ubiquinone, this indicates that also the electron transporter was adapted to anaerobically functioning after the synthesis of the originally present transporter (menaquinone) had been lost by adaptation to an aerobic environment. Third, many organisms containing anaerobically functioning mitochondria evolved from aerobic ancestors, which argues for adaptation of classical aerobic mitochondria to an anaerobic environment instead of an earlier adaptation of the ancestral endosymbiont to an anaerobic environment. An example of such organisms is parasitic helminths, which are supposed to have evolved from free-living worms, which most likely functioned aerobically, like free-living worms nowadays. Fourth, in distinct lineages distinct mechanisms for mitochondrial reoxidation of reduced cofactors are used, such as fumarate reduction, wax-ester formation or synthesis of branched-chain fatty acids (see before). The existence of these different mechanisms in separate lineages can more easily be explained by the evolution of different adaptations rather than by differential loss. The extensive similarity observed between components involved in anaerobic and aerobic metabolism in mitochondria (see before) suggests that anaerobic mitochondria evolved by adaptation of classical aerobic mitochondria to hypoxic conditions (Tielens and Van Hellemond 1998; Tielens et al. 2002).

The recent characterization of the hydrogenosomes of the anaerobic cili-ate Nyctotherus ovalis, which thrives in the hindgut of cockroaches, supports the hypothesis that hydrogenosomes and anaerobic mitochondria can evolve from aerobic mitochondria (Boxma et al. 2005). The N. ovalis organelle was identified as a missing link between aerobic mitochondria and hydrogeno-somes, because it comprises hydrogen production together with the presence of a genome encoding active electron transport chain components (Boxma et al. 2005). In addition, phylogenetic analyses revealed that the proteins of this electron-transport chain, and all nuclear genes encoding mitochondrial proteins, cluster with their homologues from aerobic ciliates, which demonstrated that this organelle is closely related to aerobic mitochondria. Furthermore, this organelle contains biochemical features characteristic of anaerobic mitochondria, such as the presence of rhodoquinone and the ability to produce succinate. These results strongly suggest that this organelle evolved from a mitochondrion of aerobic ciliates, that adapted to anaerobic functioning. Subsequently, the mitochondrial hallmarks, electron transport chain complexes that are partially encoded by a mitochondrial genome, started to degenerate after the acquisition of alternative electron sinks, a hydrogenase and fumarate reduction.

The mitochondrion of the photosynthetic flagellate E. gracilis was also recently discovered as an intermediate between mitochondria and hydrogeno-somes that unites biochemical properties of hydrogenosomes and of both aerobic and anaerobic mitochondria. The mitochondrion of Euglena contains an electron-transport chain that uses ubiquinone, SDH and cytochrome-contain-ing complexes in the presence of oxygen, and rhodoquinone, FRD and endogenously produced fumarate during hypoxia. Furthermore, this mitochondrion comprises not only PDH, the mitochondrial enzyme for conversion of pyruvate to acetyl-CoA (Hoffmeister et al. 2004), but also a PNO, which consists of a C-terminal NADPH-cytochrome P450 reductase domain fused to an N-terminal PFO domain (Rotte et al. 2001). PFO has so far only been found in those eukaryotes that lack mitochondria and lack PDH; therefore, the mitochondrion of E. gracilis is an intermediate that unites biochemical properties of aerobic and anaerobic mitochondria and hydrogenosomes, as it comprises characteristic components of these organelles.

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