Origin of phagotrophic eukaryotes as social cheaters in microbial biofilms

BACKGROUND: The origin of eukaryotic cells was one of the most dramatic evolutionary transitions in the history of life. It is generally assumed that eukaryotes evolved later then prokaryotes by the transformation or fusion of prokaryotic lineages. However, as yet there is no consensus regarding the nature of the prokaryotic group(s) ancestral to eukaryotes. Regardless of this, a hardly debatable fundamental novel characteristic of the last eukaryotic common ancestor was the ability to exploit prokaryotic biomass by the ingestion of entire cells, i.e. phagocytosis. The recent advances in our understanding of the social life of prokaryotes may help to explain the origin of this form of total exploitation. PRESENTATION OF THE HYPOTHESIS: Here I propose that eukaryotic cells originated in a social environment, a differentiated microbial mat or biofilm that was maintained by the cooperative action of its members. Cooperation was costly (e.g. the production of developmental signals or an extracellular matrix) but yielded benefits that increased the overall fitness of the social group. I propose that eukaryotes originated as selfish cheaters that enjoyed the benefits of social aggregation but did not contribute to it themselves. The cheaters later evolved into predators that lysed other cells and eventually became professional phagotrophs. During several cycles of social aggregation and dispersal the number of cheaters was contained by a chicken game situation, i.e. reproductive success of cheaters was high when they were in low abundance but was reduced when they were over-represented. Radical changes in cell structure, including the loss of the rigid prokaryotic cell wall and the development of endomembranes, allowed the protoeukaryotes to avoid cheater control and to exploit nutrients more efficiently. Cellular changes were buffered by both the social benefits and the protective physico-chemical milieu of the interior of biofilms. Symbiosis with the mitochondial ancestor evolved after phagotrophy as alphaproteobacterial prey developed post-ingestion defence mechanisms to circumvent digestion in the food vacuole. Mitochondrial symbiosis triggered the origin of the nucleus. Cilia evolved last and allowed eukaryotes to predate also on planktonic prey. I will discuss how this scenario may possibly fit into the contrasting phylogenetic frameworks that have been proposed. TESTING THE HYPOTHESIS: Some aspects of the hypothesis can be tested experimentally by studying the level of exploitation cheaters can reach in social microbes. It would be interesting to test whether absorption of nutrients from lysed fellow colony members can happen and if cheaters can evolve into predators that actively digest neighbouring cells. IMPLICATIONS OF THE HYPOTHESIS: The hypothesis highlights the importance of social exploitation in cell evolution and how a social environment can buffer drastic cellular transformations that would be lethal for planktonic forms. REVIEWERS: This article was reviewed by Eugene V Koonin, Purificación López-García, and Igor Zhulin.