Eukaryotes first: how could that be?

Abstract

In the half century since the formulation of the prokaryote : eukaryote dichotomy, many authors have proposed that the former evolved from something resembling the latter, in defiance of common (and possibly common sense) views. In such 'eukaryotes first' (EF) scenarios, the last universal common ancestor is imagined to have possessed significantly many of the complex characteristics of contemporary eukaryotes, as relics of an earlier 'progenotic' period or RNA world. Bacteria and Archaea thus must have lost these complex features secondarily, through 'streamlining'. If the canonical three-domain tree in which Archaea and Eukarya are sisters is accepted, EF entails that Bacteria and Archaea are convergently prokaryotic. We ask what this means and how it might be tested.

Keywords: LECA; LUCA; convergence; eukaryotes; streamlining.

Figure 1.

Four options for the evolution of eukaryote-like cellular complexity, represented by the dotted line. Where it exists, the last common ancestor exclusive to Archaea and Eukarya, LAECA, is shown as an open circle, and LUCA is shown as a starburst. In the first scenario, all three branches share a common ancestor in the form of a heterogeneous community of organisms [–9]. It is unclear that any form of comparative genomic analyses can test this. With the second, Bacteria and Archaea are sisters, and simplification from a eukaryote-like ancestral state began after their divergence from the eukaryotic lineage, which remains primitively complex [10]. With the third, which we take as having been the consensus or ‘received’ view for the last several decades, the tree is rooted on the line leading to Bacteria, and most complexification develops after Eukarya and Archaea diverge from each other (after LAECA). The fourth possibility differs from the third in that LAECA already possessed important complex, eukaryote-typical features which it inherited from LUCA. Thus, Bacteria and Archaea are independently ‘streamlined’ and the features that make them similar as prokaryotes are convergent. This interpretation unites the canonical three-domain phylogeny with EF thinking. How the likely possibility that Eukarya branch within–rather than as sister to–Archaea affects this interpretation is discussed in the text (§4). 1-2 and 1-4 are EF scenarios, as we define the concept.

Figure 2.

A continuum of specificity. Labelled are features common to Archaea and Bacteria that would be instances of convergent evolution if tree 1-4 is correct, though we stress these labels are early approximations. See §5 for a discussion of these features and their implications for the plausibility of EF views.