Oxygen as a primary selective pressure for photosymbiosis evolution

Photosymbioses provide carbon and oxygen to the biosphere, yet the mechanisms underlying their evolution remain poorly understood. We develop a naive system based on the predatory ciliate Tetrahymena thermophila, not known for hosting symbionts, to recapitulate early events of photosymbiosis evolution. Tetrahymena thermophila readily phagocytoses eukaryotic algae (Chlorella variabilis) or cyanobacteria (Synechococcus elongatus). Feeding on either prey in a low-carbon medium provided little or no growth advantage. By contrast, in a hypoxic environment, both intracellular C. variabilis and S. elongatus can support temporary survival of T. thermophila. These results suggest that oxygen supply within the host could represent a more plausible initial advantage supporting photosymbiosis evolution than carbon metabolites. While most extant photosymbioses are based on carbon supply to the host cell, we therefore propose that this would be a secondary event occurring from initial evolution in anoxic or hypoxic conditions, where O₂ production is crucial for establishing the initial steps of photosymbiosis.