Eukaryogenesis, how special really?

Abstract

Eukaryogenesis is widely viewed as an improbable evolutionary transition uniquely affecting the evolution of life on this planet. However, scientific and popular rhetoric extolling this event as a singularity lacks rigorous evidential and statistical support. Here, we question several of the usual claims about the specialness of eukaryogenesis, focusing on both eukaryogenesis as a process and its outcome, the eukaryotic cell. We argue in favor of four ideas. First, the criteria by which we judge eukaryogenesis to have required a genuinely unlikely series of events 2 billion years in the making are being eroded by discoveries that fill in the gaps of the prokaryote:eukaryote "discontinuity." Second, eukaryogenesis confronts evolutionary theory in ways not different from other evolutionary transitions in individuality; parallel systems can be found at several hierarchical levels. Third, identifying which of several complex cellular features confer on eukaryotes a putative richer evolutionary potential remains an area of speculation: various keys to success have been proposed and rejected over the five-decade history of research in this area. Fourth, and perhaps most importantly, it is difficult and may be impossible to eliminate eukaryocentric bias from the measures by which eukaryotes as a whole are judged to have achieved greater success than prokaryotes as a whole. Overall, we question whether premises of existing theories about the uniqueness of eukaryogenesis and the greater evolutionary potential of eukaryotes have been objectively formulated and whether, despite widespread acceptance that eukaryogenesis was "special," any such notion has more than rhetorical value.eukaryogenesis | endosymbiosis | evolutionary theory | major transitionsThe eukaryotic cell originated by the most complex set of evolutionary changes since life began: eukaryogenesis. Their complexity and mechanistic difficulty explain why eukaryotes evolved two billion years or more after prokaryotes. To understand these changes, we must consider the cell biology of all five major kinds of cells; determine their correct phylogenetic relationships; and explain the causes, steps, and detailed mechanisms of the radical transitions between them. [Cavalier-Smith (1)]The acquisition of mitochondria was the pivotal moment in the history of life. [Lane (2)] Compared to prokaryotes, eukaryotic cells represent not only an alternative mode of cellular organization but one endowed with far richer evolutionary potential: only among Eukarya do we find integrated multicellular creatures that bear embryos, respond to music, and reflect on their own nature. Whatever meaning one assigns to the history of life, the advent of eukaryotic cells marked a radical and fateful transition. [Harold (3)]

Early Microbial Evolution: The Age of Anaerobes

“…Protein synthesis consumes 75% of a cell's energy budget, DNA replication only 3% (Stouthamer 1978). At the prokaryote eukaryote transition, people have long focused on the role of oxygen at eukaryote origin; for a recent example, see Booth and Doolittle (2015) and the reply by Lane and Martin (2015). Oxygen provides a roughly sixfold increase in the amount of ATP per glucose that eukaryotes with aerobic respiration in mitochondria-right at maximally 30 ATP per glucose in mammals (Rich 2013)-obtain relative to eukaryotic anaerobes, which glean 4 -5 ATP per glucose (Müller et al 2012).…”

Eukaryotes first: how could that be?

“…There is no reason to believe that complexity is always and of itself adaptive and destined to increase, and in fact, there are many well-documented examples of genomic reduction and streamlining [16,17,41,47]. Nor is it proven that the diversification and high level of differentiated cell types exhibited by eukaryotes was only possible because of the more complex nature of their cells [4].…”

“…First, it goes against what we think is the majority view about ESPs and CSSs, that their origins or acquisition of modern function represent advances achieved in Eukarya since its divergence from prokaryotes-that is, between the first eukaryotic common ancestor (FECA), all of whose descendants other than LECA are extinct, and LECA [3]. Even those who question that evolutionary complexification is intrinsically progressive overall often understand the history of the eukaryotic lineage in this way [4]. EF denies this view in whole or part, and puts at least some eukaryote-typical ESPs or CSSs in LUCA, generally as relics from an earlier 'progenote' stage or 'RNA world'.…”

Eukaryotes really are special, and mitochondria are why

“…They write "Second, an argument for why eukaryotes can, in principle, accomplish complex evolutionary feats that prokaryotes cannot should not rest on prokaryotic failures to do so in practice" (1). We made no such claim.…”

“…The inference that only aerobes could remain complex is theirs, not ours. Many animal mitochondria are anaerobic (1,4). Mitochondria lifted the energetic barrier to inventing the many protein-dependent traits that distinguish eukaryotes from prokaryotes (2).…”