Photosystem regulation in coral-associated dinoflagellates (Symbiodiniaceae) is the primary mode for seasonal acclimation

The collapse of the coral-dinoflagellate relationship under stress, as, for example, induced by increasing sea surface temperatures due to climate change, leads to coral bleaching and coral mortality. While symbiont shuffling or community shifting has been put forth as a rapid adaptive mechanism in corals, reported instances of these phenomena typically focus on environmental extremes rather than natural seasonal increases in sea surface temperatures that may lead to thermal stress, requiring regulation and acclimation of endosymbiotic Symbiodiniaceae. Understanding the dynamic nature of Symbiodiniaceae endosymbiont community responses to seasonal environmental fluctuations is necessary to help predict the limits of acclimation and adaptation potential. We used a combination of flow cytometry, 3D scanning, and ITS2 DNA metabarcoding to quantify Acropora pulchra Symbiodiniaceae community assemblage composition and function in situ in Guam (Micronesia). Samples were collected during the onset of seasonal warming and the time of year during which corals experience the highest sea water temperatures. Flow cytometry allowed us to expediently generate physiological profiles for thousands of individual endosymbiont cells using their autofluorescent signatures. Under variable environmental conditions, Symbiodiniaceae assemblages displayed site and season-specific photophysiological acclimation signatures while community composition and cell densities in host tissues remained homogeneous across sites. Variable photoacclimation patterns during the early season was followed by an island-wide convergence of photophysiological acclimation signatures during the season that sees the highest water temperatures in Guam. Our results show that photoacclimation rather than symbiont community assemblage reorganization allows for acclimation of Acropora pulchra to seasonal extremes in water temperatures.