Arguments based on cell energetics favour the view that a mitochondrion capable of oxidative phosphorylation was a prerequisite for the evolution of other features of the eukaryotic cell, including increased volume, genome size and, eventually, phagotrophy. Contrary to this we argue that: (i) extant amitochondriate eukaryotes possess voluminous phagotrophic cells with large genomes; (ii) picoeukaryotes demonstrate that phagotrophy is feasible at prokaryotic cell sizes; and (iii) the assumption that evolution of complex features requires extra ATP, often mentioned in this context, is unfounded and should not be used in such considerations. We claim that the diversity of cell organisations and functions observed today in eukaryotes gives no reason to postulate that a mitochondrion must have preceded phagocytosis in eukaryogenesis.
Eukaryotes and Mitochondria: A Chicken-and-Egg Dilemma?Exactly how the eukaryotic cell originated will probably always remain a matter of discussion. Evolutionary scenarios explaining this major evolutionary transition differ in the order of events, in the forces driving the process, and in the number and identity of partners involved [1][2][3][4][5][6]. One of the most contentious questions concerns the timing and role of mitochondrial acquisition in eukaryogenesis (see Glossary). Mitochondria are semiautonomous organelles that evolved from a single common ancestor, an endosymbiont related to Alphaproteobacteria [7][8][9]. Mapping the presence of mitochondria onto a reconstructed eukaryote phylogeny [10,11] indicates that the mitochondrion was present in the last eukaryotic common ancestor (LECA) (i.e., at the root node) and this holds true for all plausible root positions [12][13][14][15]. Analogous to mitochondria, the presence of other cellular features of LECA can be inferred, depicting it as a complex cell possessing not only the nucleus and mitochondrion, but also the cytoskeleton and flagellum, the endomembrane system and the capability for phagocytosis, linear chromosomes with telomeres, introns and the spliceosome, and mitotic and meiotic division, as well as many other traits [16]. Unfortunately, this comparative approach does not allow us to see prior to LECA. Hence, the relative order of structural innovations associated with modern eukaryotic cells is effectively unknown and highly controversial [17,18].Although we are confident that the mitochondrion had originated before LECA, and that its acquisition represents a very important eukaryote innovation, opinions sharply differ as to when this endosymbiosis occurred. One category of hypotheses proposes that this event occurred later in eukaryogenesis, when at least some eukaryotic features were already in place [2,3,5]. A common argument for these hypotheses is that the endosymbiosis event would become much more likely if the cell had already evolved an apparatus for engulfment of the endosymbiont. A later acquisition of the mitochondrion is supported by the finding that eukaryotic genes derived from Alphaproteobacteria have s...