Breath-giving cooperation: critical review of origin of mitochondria hypotheses : Major unanswered questions point to the importance of early ecology

Abstract

The origin of mitochondria is a unique and hard evolutionary problem, embedded within the origin of eukaryotes. The puzzle is challenging due to the egalitarian nature of the transition where lower-level units took over energy metabolism. Contending theories widely disagree on ancestral partners, initial conditions and unfolding of events. There are many open questions but there is no comparative examination of hypotheses. We have specified twelve questions about the observable facts and hidden processes leading to the establishment of the endosymbiont that a valid hypothesis must address. We have objectively compared contending hypotheses under these questions to find the most plausible course of events and to draw insight on missing pieces of the puzzle. Since endosymbiosis borders evolution and ecology, and since a realistic theory has to comply with both domains' constraints, the conclusion is that the most important aspect to clarify is the initial ecological relationship of partners. Metabolic benefits are largely irrelevant at this initial phase, where ecological costs could be more disruptive. There is no single theory capable of answering all questions indicating a severe lack of ecological considerations. A new theory, compliant with recent phylogenomic results, should adhere to these criteria.

Reviewers: This article was reviewed by Michael W. Gray, William F. Martin and Purificación López-García.

Keywords: Ecology; Endosymbiosis; Eukaryogenesis; Evolution; Major transition; Metabolism; Mitochondria; Parasitism.

Fig. 1

Scenarios of the various mitochondrial origin models. Scenarios focus mostly on topological changes, after the works of Martin and others [12, 31, 57, 68, 109]. Archaea are depicted with red membrane, Bacteria with blue; purple indicates photosynthetic ability. Dashed curves stand for degrading membranes. If not indicated syntrophic “engulfment”, the inclusion involved phagocytosis (even if primitive) with at least a rudimentary cytoskeleton (indicated by the host forming phagosomal inclusions). If not indicated otherwise, mitochondria perform aerobic respiration. Ultimately, in all scenarios, mitochondria implement metabolic compartmentation and produce ATP. 1) Hydrogen hypothesis [12, 45, 67]. 2) Photosynthetic symbiont theory [36, 37, 74]. 3) Syntrophy hypothesis [48, 110]. 4) Phagocytosing archaeon theory [16]. 5) Pre-endosymbiont hypothesis [9, 41]. The origin of the endomembrane system (and nucleus) is not specified explicitly, but one must assume that it evolved endogenously, the pre-endosymbiont (brown organelle) being related to the internal membrane system. 6) Sulfur-cycling hypothesis [46, 57, 111]. 7) Origin-by-infection hypothesis [57]. 8) Oxygen-detoxification hypothesis [68, 69, 103]. The presence of a forming nucleus at the start is unknown [68]

Fig. 2

Energetic scenarios for the origin of eukaryotes. Filled arrows indicate FECA and the acquisition of mitochondria, empty arrows stand for LECA. Black lines roughly indicate averages in prokaryotes and eukaryotes. Prokaryotes cannot have genomes much larger than ~10 Mb (or ~10 K genes); smallest unicellular eukaryotes overlap with prokaryotes at this complexity. According to Lane and Martin [13, 50], there is an energetic barrier that prevents prokaryotes to maintain larger genomes (energy per cell values are from [13]). They claim that the early acquisition of mitochondria permit the transition of this barrier by temporarily increasing the gene count (blue curve; though the multiplier factor is only guessed by Lane, hence the dashed curves) to be able to experiment with new gene families. They maintain that amitochondriate eukaryotes cannot evolve directly from prokaryotes, only by losing the endosymbiont. Another possible scenario is to increase the area of internal respiratory membranes which provides extra energy with no additional genes (orange curve). This might just have been enough to power primitive phagocytosis. Mitochondria had to be acquired at a point where respiratory membranes could not be further exploited. Early mitochondria might induce gradual genome increase that progressively made inventions possible (green curve), though if this happened at low energetic levels, the archezoan niche (dashed oval) again could only be reached reductively. Theoretically, any trajectory between the orange and green curves is possible, either with early or late mitochondria. Ultimately, all scenarios lead to the same LECA, though starting from different FECAs. Present amitochondriate eukaryotes are secondarily derived (purple arrow), but some scenarios allow (orange and dark green) the existence of primarily amitochondriate “archezoan” eukaryotes