Comparative transcriptomics revealed parallel evolution and innovation of photosymbiosis molecular mechanisms in a marine bivalve

Photosymbioses between heterotrophic hosts and autotrophic symbionts are evolutionarily prevalent and ecologically significant. However, molecular mechanisms behind such symbioses remain less elucidated, which hinders our understanding of their origin and adaptive evolution. This study compared gene expression patterns in a photosymbiotic bivalve (Fragum sueziense) and a closely related non-symbiotic species (Trigoniocardia granifera) under different light conditions to detect potential molecular pathways involved in mollusk photosymbiosis. We discovered that the presence of algal symbionts greatly impacted host gene expression in symbiont-containing tissues. We found that the host immune functions were suppressed under normal light compared to those in the dark. In addition, we found that cilia in the symbiont-containing tissues play important roles in symbiont regulation or photoreception. Interestingly, many potential photosymbiosis genes could not be annotated or do not exhibit orthologs in T. granifera transcriptomes, indicating unique molecular functions in photosymbiotic bivalves. Overall, we found both novel and known molecular mechanisms involved in animal-algal photosymbiosis within bivalves. Given that many of the molecular pathways are shared among distantly related host lineages, such as mollusks and cnidarians, it indicates that parallel and/or convergent evolution is instrumental in driving host-symbiont adaptations in diverse organisms.

Methods
Fragum sueziense were collected in Family Beach, Guam and Trigoniocardia granifera were collected near Isla Venado, Panama. 30 F. sueziense and 37 T. granifera were randomly assigned into 3 groups evenly and placed under different light intensities: 1. Under an ambient light-dark cycle, which the animals were exposed to in the natural habitats; 2. At reduced light during the day by blocking sunlight with black meshes; and 3. Under constant darkness by blocking sunlight with multiple layers of black meshes. Specimens were treated for 3 days then processed. See detailed collecting and processing information in electronic supplementary material text in Li et al. 2024.