Oxygen as a primary selective pressure for photo-endosymbiosis evolution

Abstract

Photosymbiosis through eukaryotic or eukaryotic - prokaryotic associations provide mainly carbon and oxygen to the living world, however the mechanisms behind their evolution remain unknown. Here we develop a naive 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 supply in hospite 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 O2 production was crucial for establishing the initial steps of photosymbiosis.