A comparison of autogenous theories for the origin of eukaryotic cells

Eukaryotic cells have many unique features that all evolved on the stem lineage of living eukaryotes, making it difficult to reconstruct the order in which they accumulated. Nuclear endosymbiotic theories hold that three prokaryotes (nucleus, cytoplasm, and mitochondrion) came together to form a eukaryotic cell, whereas autogenous models hold that the nucleus and cytoplasm formed through evolutionary changes in a single prokaryotic lineage. Given several problems with nuclear endosymbiotic theories, this review focuses on autogenous models.

Until recently all autogenous models assumed an outside-in (OI) topology, proposing that the nuclear envelope was formed from membrane-bound vesicles within the original cell body. Buzz Baum and I recently proposed an inside-out (IO) alternative, suggesting that the nucleus corresponds to the original cell body, with the cytoplasmic compartment deriving from extracellular protrusions. In this review, I show that OI and IO models are compatible with both mitochondria early (ME) or mitochondria late (ML) formulations. Whereas ME models allow that the relationship between mitochondria and host was mutualistic from the outset, ML models imply that the association began with predation or parasitism, becoming mutualistic later. In either case, the mutualistic interaction that eventually formed was probably syntrophic.

Diverse features of eukaryotic cell biology align well with the IOME model, but it would be premature to rule out the OIME model. ML models require that phagocytosis, a complex and energy expensive process, evolved before mitochondria, which seems unlikely. Nonetheless, further research is needed, especially resolution of the phylogenetic affinities of mitochondria.