Photoreceptor complexity accompanies adaptation to challenging marine environments in Anthozoa

Light represents a key environmental factor, which shapes the physiology and evolution of most organisms. Notable illustrations of this are reef-building corals (Anthozoa), which adapted to shallow, oligotrophic, tropical oceans by exploiting light from the sun and the moon to regulate various aspects of physiology including sexual reproduction, phototaxis and photosymbiosis. Together with the Medusozoa, (including jellyfish), the Anthozoa constitute the ancestral metazoan phylum cnidaria. While light perception in Medusozoa has received attention, the mechanisms of light sensing in Anthozoa remain largely unknown. Cnidaria express two principle groups of light-sensing proteins: opsins and photolyases/cryptochromes. By inspecting the genomic loci encoding these photoreceptors in over 35 cnidarian species, we reveal that Anthozoa have substantially expanded and diversified their photoreceptor repertoire. We confirm that, in contrast to Medusozoa, which retained one opsin class, anthozoans possess all three urmetazoan opsin classes. We show that anthozoans also evolved an extra sub-group (actinarian ASO-IIs). Strikingly, we reveal that cryptochromes including CRY-IIs are absent in Medusozoa, while the Anthozoa retained these and evolved an additional, novel cryptochrome class (AnthoCRYs), which contain unique tandem duplications of up to 6 copies of the PHR region. We explored the functionality of these photoreceptor groups by structure-function and gene expression analysis in the anthozoan model species Exaiptasia pallida (Aiptasia), which recapitulates key photo-behaviors of corals. We identified an array of features that we speculate reflect adaptations to shallow aquatic environments, moonlight-induced spawning synchronization and photosymbiosis. We further propose that photoreceptor complexity and diversity in Anthozoa reflects adaptation to challenging habitats.