Eukaryotic origins: How and when was the mitochondrion acquired?

Abstract

Comparative genomics has revealed that the last eukaryotic common ancestor possessed the hallmark cellular architecture of modern eukaryotes. However, the remarkable success of such analyses has created a dilemma. If key eukaryotic features are ancestral to this group, then establishing the relative timing of their origins becomes difficult. In discussions of eukaryote origins, special significance has been placed on the timing of mitochondrial acquisition. In one view, mitochondrial acquisition was the trigger for eukaryogenesis. Others argue that development of phagocytosis was a prerequisite to acquisition. Results from comparative genomics and molecular phylogeny are often invoked to support one or the other scenario. We show here that the associations between specific cell biological models of eukaryogenesis and evolutionary genomic data are not as strong as many suppose. Disentangling these eliminates many of the arguments that polarize current debate.

Figure 1.

Timing of mitochondrial acquisition in eukaryogenesis. The relative timing of the acquisition of the mitochondrion during the process of eukaryogenesis from the FECA to the LECA (orange to blue shading) varies from scenarios in which this is the first step (“Mito-first”) to those in which it is the last step (“Mito-last”). Note that there is a difference between the mitochondrion-last and Archezoa models. When the mitochondrion is the final step, the host is a fully formed eukaryotic cell. In the Archezoa model, acquisition was proposed to have occurred subsequent to early diversification of a few eukaryote lineages (depicted schematically by a blue-to-green change). This model has been falsified so is in gray to reflect this. As discussed in the text, available data make it difficult to support either the Mito-first or Mito-last scenario. In particular, the absence of known premitochondrial lineages cannot be taken as an argument for Mito-first scenarios, as extinction of intermediate forms (dotted lines) is a natural process in evolution that has occurred before, during, and after eukaryogenesis. However, there may be considerable differences between “intermediate” scenarios, including with regard to the nature of the host (phylogenetically an archaeon or eukaryote). Major Eukaryotic groups are labeled and indicative relationships are presented.

Figure 2.

Alternative models for eukaryotic origins and different timing of mitochondrial acquisition are not incompatible. Contrary to what may be assumed, 2D hypotheses for eukaryotic origins (upper tree) do not necessarily imply mitochondria-first models and 3D models (lower tree) do not necessarily imply mitochondria-last models. Note that both 2D and 3D models require a stem from the FECA to the LECA along which eukaryogenesis occurred. If mitochondrial acquisition is the first step in eukaryogenesis, the host is, by definition, an archaeon. This is compatible with eukaryotes emerging from within archaea (2D), but also with 3D scenarios if they derive from a basal archaeal lineage. The mitochondrion-last model is agnostic as to the evolutionary relationship between eukaryotes and archaea because it only makes the statement that the final step in eukaryogenesis is mitochondrial acquisition, and the host can classically derive from the eukaryotic lineage (3D), but also from an archaeal lineage (2D) that would have developed eukaryotic features.

Figure 3.

Known endosymbiosis across Bacteria, Archaea, and Eukaryotes. Bacterial endosymbionts of other bacteria are well known, the most striking examples being that of M. endobia, a γ-proteobacterial endosymbiont of T. princeps, a β-proteobacterium that is, in turn, an endosymbiont of mealybugs (von Dohlen et al. 2001; Husnik et al. 2013), and Bdellovibrio bacteriovorus, which infiltrates prey bacteria as part of its life cycle (Rendulic et al. 2004). Eukaryotes are known to house bacterial, archaeal, and eukaryotic endosymbionts. For instance, ciliates in microoxic, sulfidic environments carry both archaeal and bacterial endosybionts (Edgcomb et al. 2011), and the persistence of nucleomorphs in cryptophytes and chlorarachniophytes show these lineages independently acquired photosynthesis through engulfment of eukaryote algae (Curtis et al. 2012). No instances of Archaea-carrying endosymbionts have been documented. This is a requirement for models of eukaryote origins in which the host is cell-biologically archaeal. Note that this is different from a phylogenetic origin of eukaryotes within Archaea in which phagocytosis predates mitochondrial acquisition (Jékely 2007a; Poole and Neumann 2011; Martijn and Ettema 2013).