Photoreceptor complexity accompanies adaptation to challenging marine environments in Anthozoa

Abstract

12Light represents a key environmental factor, which shapes the physiology and evolution of 13 most organisms. Notable illustrations of this are reef-building corals (Anthozoa), which 14 adapted to shallow, oligotrophic, tropical oceans by exploiting light from the sun and the 15 moon to regulate various aspects of physiology including sexual reproduction, phototaxis and 16 photosymbiosis. Together with the Medusozoa, (including jellyfish), the Anthozoa constitute 17 the ancestral metazoan phylum cnidaria. While light perception in Medusozoa has received 18 attention, the mechanisms of light sensing in Anthozoa remain largely unknown. Cnidaria 19 express two principle groups of light-sensing proteins: opsins and photolyases/cryptochromes. 20By inspecting the genomic loci encoding these photoreceptors in over 35 cnidarian species, 21 we reveal that Anthozoa have substantially expanded and diversified their photoreceptor 22 repertoire. We confirm that, in contrast to Medusozoa, which retained one opsin class, 23 anthozoans possess all three urmetazoan opsin classes. We show that anthozoans also evolved 24 an extra sub-group (actinarian ASO-IIs). Strikingly, we reveal that cryptochromes including 25 CRY-IIs are absent in Medusozoa, while the Anthozoa retained these and evolved an 26 additional, novel cryptochrome class (AnthoCRYs), which contain unique tandem 27 duplications of up to 6 copies of the PHR region. We explored the functionality of these 28 photoreceptor groups by structure-function and gene expression analysis in the anthozoan 29 model species Exaiptasia pallida (Aiptasia), which recapitulates key photo-behaviors of 30 corals. We identified an array of features that we speculate reflect adaptations to shallow 31 aquatic environments, moonlight-induced spawning synchronization and photosymbiosis. We 32 further propose that photoreceptor complexity and diversity in Anthozoa reflects adaptation to 33 challenging habitats. 34 35 36 37Light from both the sun and moon dominates the life of many organisms and has had a 38 profound impact on their evolution. While the mechanisms underlying light sensing have 39 been studied in a comparatively small group of animal models, little is known about the 40 impact of light on the physiology and evolution of more ancestral metazoan groups such as 41 the cnidarians. These are basal, non-bilaterian, eumetazoan animals divided into two major 42 groups, the Anthozoa and the Medusozoa ( Figure 1A; [1], which both exploit a complexity of 43 sunlight and moonlight-based cues to regulate various aspects of their physiology and 44 behaviour ( Figure 1B). Notable examples of highly light-dependent cnidarians are reef-45 building corals and anemones (both Anthozoa; Figure 1A), many of which live in an 46 evolutionary ancient symbiotic relationship with eukaryotic, photosynthetic dinoflagellates of 47 the Symbiodiniaceae family [2, 3]. The symbionts use sunlight to provide essential 48 photosynthetically-fixed nutrients to their hosts to support host survival in otherwise 49 oligo...