Photoacclimation strategies with depth involve alternative photosynthetic electron pathways in coral endosymbionts

Coral endosymbionts of the Symbiodiniaceae family can exhibit a wide range of physiological responses to environmental variations and stress, allowing their hosts to occupy a wide range of environmental niches but also significantly contributing to their persistence under global change. Among the external environmental conditions acting as the driving forces responsible for particular pairings between both partners, light is very likely the most important. In the natural environment, the holobiont have to cope with significant daily variations in light intensities that sometimes exceed endosymbiont photosynthetic capacity and promote the production of reactive species. This implies the existence of regulatory mechanisms in the symbiont that mitigate the excitation pressure. This can be done by dissipating excess light as heat (i.e. NPQ) or diverting electrons in excess through alternative electron flow (AEFs). Although, a growing number of studies indicated that some AEFs (Cyclic Electron Flow or Mehler reaction) could be important among the Symbiodiniaceae, especially under stress conditions, we have limited information on how these pathways operate in symbiosis.
This study aimed to improve our understanding of the photoacclimatory strategies employed by the reef-building coral Stylophora pistillata, by determining for the first time how AEFs were modulated with depth. Compared to colonies from shallow depth (10 m), colonies sampled at 40 m displayed a higher photosynthetic efficiency (Fv/Fm) but lower maximal electron transfer rates of photosystems I and II. In addition, maximum capacity for thermal dissipation at high light intensities was much lower in deep colonies. Our analyses of the AEFs also revealed: (1) a significantly lower CEF capacity in deep compared to shallow colonies and; (2) a high level of rerouting of photosynthetic electron toward O2 under high light intensities (about 40% of oxygenic photosynthesis), but similar between colonies from the two depths. In addition to these physiological measurements the composition of the Symbiodiniaceae community within the host was also found to differ with depth, with shallow and deep colonies harboring Symbiodiniaceae of the genus, Symbiodinium and Cladocopium, respectively. Overall this study shows a more complete picture of the coral photoacclimation strategies in which AEF and Symbiodiniaceae genotype play a significant role.