Eukaryotic origins and the Proterozoic Earth system: A link between global scale glaciations and eukaryogenesis?

The Proterozoic Earth system is popularly viewed as having comprised prolonged periods of invariant conditions separating intervals of extreme change. Against this backdrop the earliest evidence of eukaryotic organisms is found, raising the (highly uncertain) possibility of an environmental impetus for this fundamental evolutionary transition. Here I review the eukaryotic fossil record and the theoretical issues surrounding eukaryogenesis, with the aim of relating these ideas to the broad context of the Proterozoic Earth system. In terms of fossils, either eukaryotes were present in Proterozoic oceans, (conceivably as early as 2.1Ga, but at the latest by 1.4 Ga), or the macroscopic fossils that are found from this period are prokaryotic colonies that converged on form very close to modern eukaryotes before going extinct (the first possibility is far more parsimonious). In terms of DNA, phylogenetic evidence indicates that eukaryotes derive from a symbiosis between an archaeon host cell and a eubacterial proto-mitochondrion. Bar a tiny number of isolated examples contemporary prokaryotic cells do not. simply end up inside the cells of other prokaryotes as a consequence of ecological interactions (however synergistic). Therefore the capacity for phagocytosis in the host cell is by far the most plausible way in which to explain the acquisition of the mitochondria' symbiont. But phagocytosis, and indeed the larger cell size of eukaryotes, is probably incompatible with use of the external cell membrane to sustain a proton gradient for ATP generation (as occurs in prokaryotes). By contrast, the multi-bacterial power of ATP generation in numerous mitochondria results in eukaryotes having considerably more free energy available per gene than prokaryotes. Importantly, this can be achieved whilst minimizing the (potentially extreme) free radical damage from misfiring electron transport chains, by a co-location for redox regulation involving transfer of most mitochondrial genes to the host nucleus, but transcription of key respiratory components near the site of their activity. Thus, debate persists about a catch-22 situation: Arguably, the host cell requires a cytoskeleton in order to acquire (proto) mitochondria, but cannot energetically sustain a cytoskeleton without ATP generation in multiple mitochondria. Explaining why an initially transient, facultative interaction progressed to full endosymbiosis amounts to aligning the fitness interests of the host and symbiont. I conclude by tentatively speculating that the Paleoproterozoic global-scale glaciations may have provided an impetus for eukaryogenesis by providing some form of extreme bottleneck, in which: (a) Ancestral host and symbiont organisms were physically forced into close proximity for an unprecedented length of evolutionary time, and (b) Restricted dispersal, small populations, and low resource availability rendered survival, rather than fecundity, the dominant component of fitness, permitting sequential fixation of multiple cooperative traits in host and symbiont genomes. Though admittedly speculative, a clear testable prediction is invoked by my suggestion: fossils with unequivocal proto-mitochondria (and perhaps nuclei), after, but not before, the Paleoproterozoic glaciations, should eventually be found.