The Evolution of Oxygen-Independent Energy Metabolism in Eukaryotes with Hydrogenosomes and Mitosomes

Abstract

Hydrogenosomes and mitosomes are mitochondria in the evolutionary sense because they descend from one and the same bacterial endosymbiont. But the evolutionary significance of eukaryotic anaerobes that possess hydrogenosomes, mitosomes, and anaerobically functioning mitochondria is still an issue of some contention. This chapter serves to further revise the role of oxygen in eukaryote evolution in light of surprising findings about O2 and energetics and in light of what geologists have discovered regarding the timing of oxygen accumulation in Earth history. According to substantial newer findings that geologists have been reporting for about 20 years, the Proterozoic witnessed a protracted period of Earth ocean history, during which the oceans were mostly anoxic and often sulfidic. That period started about 2.3 billion years ago and only came to an end about 580 million years ago, perhaps as recently as 450 million years ago. That was the time during which eukaryotes arose and diversified into their major lineages. In light of that, anaerobic eukaryotes with mitochondria are not, in an evolutionary sense, strange, obscure, unexpected, or otherwise out of the ordinary; hence no special or unusual mechanisms are required to explain their origin. They are normal in every respect and so are their mitochondria. The surprise from energetics is not that O2 increases ATP yield from glucose but that the energetic costs for synthesis of cellular building blocks in oxic environments are 13 times greater than in anaerobic environments. Is oxygen overrated? The benefits of O2 are offset by its costs.