Endosymbiosis before eukaryotes: mitochondrial establishment in protoeukaryotes

Abstract

Endosymbiosis and organellogenesis are virtually unknown among prokaryotes. The single presumed example is the endosymbiogenetic origin of mitochondria, which is hidden behind the event horizon of the last eukaryotic common ancestor. While eukaryotes are monophyletic, it is unlikely that during billions of years, there were no other prokaryote-prokaryote endosymbioses as symbiosis is extremely common among prokaryotes, e.g., in biofilms. Therefore, it is even more precarious to draw conclusions about potentially existing (or once existing) prokaryotic endosymbioses based on a single example. It is yet unknown if the bacterial endosymbiont was captured by a prokaryote or by a (proto-)eukaryote, and if the process of internalization was parasitic infection, slow engulfment, or phagocytosis. In this review, we accordingly explore multiple mechanisms and processes that could drive the evolution of unicellular microbial symbioses with a special attention to prokaryote-prokaryote interactions and to the mitochondrion, possibly the single prokaryotic endosymbiosis that turned out to be a major evolutionary transition. We investigate the ecology and evolutionary stability of inter-species microbial interactions based on dependence, physical proximity, cost-benefit budget, and the types of benefits, investments, and controls. We identify challenges that had to be conquered for the mitochondrial host to establish a stable eukaryotic lineage. Any assumption about the initial interaction of the mitochondrial ancestor and its contemporary host based solely on their modern relationship is rather perilous. As a result, we warn against assuming an initial mutually beneficial interaction based on modern mitochondria-host cooperation. This assumption is twice fallacious: (i) endosymbioses are known to evolve from exploitative interactions and (ii) cooperativity does not necessarily lead to stable mutualism. We point out that the lack of evidence so far on the evolution of endosymbiosis from mutual syntrophy supports the idea that mitochondria emerged from an exploitative (parasitic or phagotrophic) interaction rather than from syntrophy.

Keywords: Endosymbiosis; Eukaryogenesis; Mitochondria; Mutualism; Prokaryotes.

Fig. 1

Prototypical ecological interactions of host and symbiont enabling endosymbiosis, along two orthogonal dimensions: symbiosis (physical contact) and net benefit of the interaction of populations (mutualism). All endobiotic partnerships are technically endosymbiosis. It is trivial that endosymbiosis requires a transition from ecto- to endobiosis, but it is not necessary that the interaction converges to (+|+) . Transition between states is always continuous, rather than stepwise, and boundary states are not separating (i.e., one can go from syntrophy to by-product symbiosis). Mutually beneficial syntrophy, if internalized, could naturally yield metabolic endosymbiosis. Similarly, farming becomes mutually beneficial when the farmed partner survives in an otherwise lethal environment thanks to the host. On the other hand, two steps are needed to turn phagocytosis into mutually beneficial endosymbiosis: first, a mechanism is needed to turn the host to farmer then another mechanism must ensure benefit for both parties. Green box indicates where phagocytosis seems indispensable. We exclude mutually disadvantageous cases (−|−) as those are unlikely to lead to association-level advantages

Fig. 2

Hypothetical evolutionary scenarios of prokaryotic endosymbiosis. The sign of the partner in the ecological interaction is indicated by the cell color: green is beneficial toward the partner, red is exploitative, and yellow is neutral. The blue cell indicates a fully integrated symbiont species within the host cell, a new evolutionary unit. The interaction either starts in a dense multi-species biofilm where there is a network of various interactions among species (gray arrows) or as a pairwise interaction of two free-living species (blue arrows). A, B: Initial interaction is exploitative as the host feeds on the partner species (this could happen by assuming phagotrophy or external digestion). If the symbiont can maintain its population internally against host culling, there is a chance for coevolution and endosymbiosis. If the original interaction is non-specific, host is expected to maintain a diverse internal population (A). Exploitation can also emerge as a specific pairwise interaction either in the biofilm or of free-living forms (B). Resulting symbionts could defect due to mutations (red symbionts). C: If symbiont is the exploitative partner (a parasite), its entry into the host does not depend on the host's ability to phagocytose. A prolonged interaction could lead to temperated parasite costs, and, ultimately, to a tamed parasite (green symbiont) that stays with the host. D, E: Initial interaction is mutually beneficial, e.g., syntrophy. Partners can be specific and strictly pairwise (D) or work together as a multi-species network to utilize resources (E). In case endosymbiosis emerges from a non-specific network of interactions of multiple species, one expects the resulting integrated pair has greater symbiont, organelle, or genetic diversity (especially in case of nucleated eukaryotes)

Fig. 3

Interaction benefits based on investment. Green arrows indicate evolutionary transitions. A: In by-product benefit, the recipient (purple cell) receives benefit that derives from the by-product of the donor (blue cell). The orange gradient and undulating arrows denote the release and diffusion of the by-product into the environment, which is then picked up by the recipient (black arrow). Both partners have genetic traits (blue and purple rectangles) that can only control their own actions (red arrows). As no costly investment is directed toward the partner [132], no mechanism is necessary to prevent the degradation of the interaction due to exploitative strategies. Since the donor has no interest in the interaction, the benefit for the recipient can only increase in a long-term association by accident or by pseudo-reciprocity (i.e., an investment to enhance by-product benefits [60]), leading ultimately to evolved dependence when the recipient tries to maintain close proximity to harness the by-product more efficiently and stably. In evolved dependence, the removal of the partner from the association causes immediate fitness decrease; however, since one or both of the parties are better off without the other, they can still regain their original fitnesses if separated [62]. B: In invested benefit, the benefit of the recipient (purple cell) derives from the product of the donor (blue cell) which depends on the adaptive trait of the donor (blue rectangle). The maintenance of costly cooperative investments, and ultimately coexistence, becomes an issue: non-investing defectors (cheaters) enjoy a fitness advantage and can outcompete cooperative types [64]. Benefits are expected to be stable or increase if the donor either (i) increases its investment and as a result receives more; or (ii) evolves partner control mechanisms to force adequate or even increasing returns. C: In purloined benefit, the benefit of the recipient (purple cell) depends on its own adaptive trait (purple rectangle) controlling the investment (red arrow). Dependence keeps parties together without quantifiable benefits for the exploited party (called addiction [12]). Different mechanisms may be combined to form pairwise interactions (e.g., A–A yields mutual commensalism, B–B reciprocity, C–B exploitation, and parasitism)

Fig. 4

Basic steps of endosymbiosis and organellogenesis. Geometric shapes represent various benefits (e.g., metabolites), solid black arrows represent the source and flow of the various benefits, dashed arrows indicate investments, and colored arrows indicate the option to leave the host. Note that the last step, if involves nuclear integration and protein import, is irreversible