Energetics and genetics across the prokaryote-eukaryote divide

Background

All complex life on Earth is eukaryotic. All eukaryotic cells share a common ancestor that arose justonce in four billion years of evolution. Prokaryotes show no tendency to evolve greater morphological complexity,despite their metabolic virtuosity. Here I argue that the eukaryotic cell originated in a unique prokaryoticendosymbiosis, a singular event that transformed the selection pressures acting on both host and endosymbiont.

Results

The reductive evolution and specialisation of endosymbionts to mitochondria resulted in an extremegenomic asymmetry, in which the residual mitochondrial genomes enabled the expansion of bioenergeticmembranes over several orders of magnitude, overcoming the energetic constraints on prokaryotic genome size,and permitting the host cell genome to expand (in principle) over 200,000-fold. This energetic transformation waspermissive, not prescriptive; I suggest that the actual increase in early eukaryotic genome size was driven by aheavy early bombardment of genes and introns from the endosymbiont to the host cell, producing a highmutation rate. Unlike prokaryotes, with lower mutation rates and heavy selection pressure to lose genes, earlyeukaryotes without genome-size limitations could mask mutations by cell fusion and genome duplication, as inallopolyploidy, giving rise to a proto-sexual cell cycle. The side effect was that a large number of shared eukaryoticbasal traits accumulated in the same population, a sexual eukaryotic common ancestor, radically different to anyknown prokaryote.

Conclusions

The combination of massive bioenergetic expansion, release from genome-size constraints, and highmutation rate favoured a protosexual cell cycle and the accumulation of eukaryotic traits. These factors explain theunique origin of eukaryotes, the absence of true evolutionary intermediates, and the evolution of sex in eukaryotesbut not prokaryotes.

The origin of the eukaryotic cell was a unique event

There is little doubt that all known eukaryotic cells share a common ancestor that arose only once in four billion years of evolution. Common traits range from the conserved position of many introns, to the structure of nuclear pore complexes,to complex traits such as syngamy and two-step meiosis. It is implausible that all of these shared properties arose by lateral gene transfer (which is inherently asymmetric in mechanism) or convergent evolution (which implies that traits like intron position are dictated by selective constraints, rather than historical contingency). Common ancestry is much the most parsimonious explanation.

However, a single ancestor is perfectly consistent with multiple origins if all ‘protoeukaryotic’ lines arising later were driven to extinction by fully-fledged eukaryotes already occupying every niche, and if all earlier protoeukaryotes were displaced by modern eukaryotes (or fell extinct for some other reason). This cannot be addressed phylogenetically, as any phylogenetic evidence for their existence is lost. Nor is the fossil record any help. It is hard to distinguish between eukaryotic and prokaryotic microfossils let alone prove the existence of extinct lines of protoeukaryotes. While asserting the unprovable existence of extinct lines of eukaryotes is unsatisfying, if not unscientific, extinction is commonplace, and the argument seems, on the face of it, irrefutable.

But there are several reasons to doubt that prokaryotes have repeatedly given rise to more complex ‘protoeukaryotes’, which were ultimately all driven to extinction by modern eukaryotes that came to occupy every niche. The periodic mass extinctions of plants and animals, followed by evolutionary radiations of hitherto suppressed groups, are not characteristic of microbial evolution-such radiations explore morphological, not metabolic, space. Moreover, large animals and plants generally have tiny populations in comparison with microbes, and cannot acquire life-saving genes by lateral gene transfer, making animals and plants much more vulnerable to extinction. The continuity of global geochemical cycles over three billion years shows that no major prokaryotic group has been driven to extinction, not even methanogens and acetogens, the most energetically tenuous forms of life. The abundance of apparently parallel niches suggests that extinction is not the rule. Archaea, once believed to be restricted to extreme environments such as hydrothermal vents and salt flats, are common in temperate oceans, whereas eukaryotes, long thought to be excluded from extreme environments by their delicate constitutions, are in fact abundant in anoxic conditions and in rivers contaminated with heavy metals. Picoeukaryotes compete directly with prokaryotes in many environments, yet neither group has fallen extinct. Extinction seems too facile an explanation to account for fact that all complex life on Earth shares a common ancestor that only arose once. If indeed many other independently arising lineages of protoeukaryotes all fell extinct, more persuasive reasons are needed than simple displacement by more competitive modern eukaryotes.

The existence of a diverse group of morphologically simple eukaryotes that occupy an intermediate niche between prokaryotes and more complex protists refines this point. Described as archezoa by Cavalier-Smith in the 1980s, the group was seen as primitively amitochondriate protoeukaryotes, living fossils of the prokaryotic-eukaryotic transition. Genetic and morphological studies, however, revealed that all known archezoa possessed mitochondria in the past, and lost them via reductive evolution to specialised organelles called hydrogenosomes and mitosomes. This is significant in terms of extinction. There are at least 1000 species of simple protist that lack mitochondria, yet all of them evolved by reductive evolution from more complex ancestors, rather than evolving ‘up’ from more simple prokaryotes.