Birth of the eukaryotes by a set of reactive innovations: New insights force us to relinquish gradual models

Abstract

Of two contending models for eukaryotic evolution the "archezoan" has an amitochondriate eukaryote take up an endosymbiont, while "symbiogenesis" states that an Archaeon became a eukaryote as the result of this uptake. If so, organelle formation resulting from new engulfments is simplified by the primordial symbiogenesis, and less informative regarding the bacterium-to-mitochondrion conversion. Gradualist archezoan visions still permeate evolutionary thinking, but are much less likely than symbiogenesis. Genuine amitochondriate eukaryotes have never been found and rapid, explosive adaptive periods characteristic of symbiogenetic models explain this. Mitochondrial proteomes, encoded by genes of "eukaryotic origin" not easily linked to host or endosymbiont, can be understood in light of rapid adjustments to new evolutionary pressures. Symbiogenesis allows "expensive" eukaryotic inventions via efficient ATP generation by nascent mitochondria. However, efficient ATP production equals enhanced toxic internal ROS formation. The synergistic combination of these two driving forces gave rise to the rapid evolution of eukaryotes. Also watch the Video Abstract.

Evolution of peroxisomes illustrates symbiogenesis

“…Indeed in [53] it is speculated that "...these findings may suggest the ability of simple phagocytic capabilities in the archaeal host...". I originally thought such phagocytic capabilities not unlikely [54], but actually there are many arguments against it, see e.g. [22,24].…”

What can we infer about the origin of sex in early eukaryotes?

“…Practically all the eukaryotic hallmarks (e.g. the nucleus, endoplasmatic reticulum, peroxisomes and meiotic sex systems) can be explained by evolutionary forces unleashed by the merger of the two founding cells [3]. In this context, it should be stressed that further organelle formation, even that of the chloroplast, and the, much later, eukaryotic uptake of eukaryotes by phagocytosis (for ongoing examples, see [43]) would develop along pathways set during the primordial bacterium to mitochondrion conversion (see below).…”

“…This set became available upon merging a lokiarchaeon-like host [12] with a bacterium related to present-day a-proteobacteria, at the basis of the eukaryotic lineage. I should also stress here that the eukaryotic meiotic sex machinery is a costly business and that its evolution thus depended on the ATP generated profusely by the endosymbiont [3]. So we can envisage the 'how' for the evolution of sex; what about the (combination of) 'why's'?…”

“…The processes involved are as follows: (i) Ploidy alterations: increases via cellular fusion processes and reductions via meiosis; (ii) cell -cell fusion regulation, which started out with the fusion of similar cell types (isogamous fusion) and later became anisogamous; (iii and iv) coupling mating-type allele regulation to (differential) organelle transmission and to (adaptive) spore formation [2]. In (archezoan) theories that postulated eukaryotic evolution prior to endosymbiont entry, organelle transmission was seen as a later addition to a fully operational meiotic mechanism, but nowadays meiotic sex is seen as one of the set of processes that probably arose in reaction to endosymbiont entry [3]. To be precise, in reaction to reactive oxygen species (ROS) stress (see [4][5][6][7] and references therein).…”

Inseparable tandem: evolution chooses ATP and Ca2+to control life, death and cellular signalling

“…Possible driving factors in eukaryote evolution may reflect the fact that ATP had been preset for energy conservation already in bacteria before Ca 2þ has been established as a signalling molecule; that Ca 2þ stimulates ATP synthesis by activating dehydrogenases of the tricarbonic acid (Krebs) cycle [7]; and that ATP prevails several fold over GTP, which is formed and used in only one step by transphosphorylation from ATP to GDP [8]. Acquisition of mitochondrial precursors is considered an early and critical step of eukaryote evolution [9,10]. Formation of an endomembrane system is attributed to the first eukaryotic common ancestor, which emerged in combination with formation of multiple paralogues of molecules dedicated to signalling and trafficking [11][12][13].…”