Oxygen as a primary selective pressure for photo-endosymbiosis evolution

Photosymbiosis through eukaryotic or eukaryotic – prokaryotic associations provide energy and oxygen to the living world, however the mechanisms behind their evolution remain unknown. Here we develop a naïve system based on the predatory ciliate Tetrahymena thermophila , not known for hosting symbiont, to recapitulate early events leading to photosymbiosis evolution. T. thermophila was found to readily phagocyte eukaryotic algae ( Chlorella variabilis ) or cyanobacteria ( Synechoccocus elongatus ) that can reach high numbers within predatory cells. Feeding with either prey in a low carbon environment provide little or no growth advantage to T. thermophila . In contrast, in anoxic environment, both intracellular C. variabilis or S. elongatus can readily support growth of T. thermophila , in the light but not in the dark, demonstrating that oxygen in hospite supply can be an initial feature supporting further photo-endosymbiosis evolution. This suggests that it is unlikely that carbon metabolites produced by phototrophs could have represented a selective advantage for the evolution of photosymbionts. Although most extant photosymbiosis are based on carbon supply to the host cell, we therefore propose that it is a secondary event occurring from initial evolution in anoxic or hypoxic conditions, where O ₂ production was crucial for establishing the initial steps of photosymbiosis.