Energy metabolism among eukaryotic anaerobes in light of Proterozoic ocean chemistry

Abstract

Recent years have witnessed major upheavals in views about early eukaryotic evolution. One very significant finding was that mitochondria, including hydrogenosomes and the newly discovered mitosomes, are just as ubiquitous and defining among eukaryotes as the nucleus itself. A second important advance concerns the readjustment, still in progress, about phylogenetic relationships among eukaryotic groups and the roughly six new eukaryotic supergroups that are currently at the focus of much attention. From the standpoint of energy metabolism (the biochemical means through which eukaryotes gain their ATP, thereby enabling any and all evolution of other traits), understanding of mitochondria among eukaryotic anaerobes has improved. The mainstream formulations of endosymbiotic theory did not predict the ubiquity of mitochondria among anaerobic eukaryotes, while an alternative hypothesis that specifically addressed the evolutionary origin of energy metabolism among eukaryotic anaerobes did. Those developments in biology have been paralleled by a similar upheaval in the Earth sciences regarding views about the prevalence of oxygen in the oceans during the Proterozoic (the time from ca 2.5 to 0.6 Ga ago). The new model of Proterozoic ocean chemistry indicates that the oceans were anoxic and sulphidic during most of the Proterozoic. Its proponents suggest the underlying geochemical mechanism to entail the weathering of continental sulphides by atmospheric oxygen to sulphate, which was carried into the oceans as sulphate, fueling marine sulphate reducers (anaerobic, hydrogen sulphide-producing prokaryotes) on a global scale. Taken together, these two mutually compatible developments in biology and geology underscore the evolutionary significance of oxygen-independent ATP-generating pathways in mitochondria, including those of various metazoan groups, as a watermark of the environments within which eukaryotes arose and diversified into their major lineages.

Figure 1

(a) Schematic distribution of anaerobes among the six ‘supergroups’ currently considered in higher level eukaryotic phylogeny in relation to (b) current views about the timing of ocean oxygenation (redrawn with kind permission from Dietrich et al. 2006). Figure (a) embraces the classification of Adl et al. (2005) and avoids any statement about the position of the root or the possible branching order for those groups; for the purposes of this paper, the position of the root and the branching order are irrelevant because anaerobes occur in all of the supergroups. Energy metabolism for the examples shown are discussed in the text, with the exception of foraminiferans that inhabit anaerobic environments (Bernhard et al. 2006), where little information about energy metabolism is available. It schematically indicates the origin of mitochondria from a symbiosis of a eubacterium with an archaebacterial host (Pisani et al. 2007). For a discussion of whence the prokaryotes arose based on energy metabolic considerations, see Martin & Russell (2007). The age of eukaryotes indicated (ca 1.5 Ga ago) is based on Javaux et al. (2001). The dotted line linking (a) and (b) schematically links the evidence for the earliest eukaryotes and the diversification of major groups to the timing of oxygen accumulation in the oceans (see text). The specialization to aerobic and anaerobic lifestyles from a facultatively anaerobic ancestral state (Martin & Müller 1998) is indicated and schematically shown to temporally correspond with the end of anoxic and sulphidic Proterozoic oceans (see text).