Genome-wide characterization of chemosensory receptor genes in octopus and identification of key genes involved in paralarval benthic settlement

The high mortality rate during the benthic settlement process of Octopus sinensis paralarvae represents the primary technical bottleneck constraining the development of its aquaculture industry. The functional roles of chemical factors in this critical transitional phase are unknown. Considering the crucial role of chemosensory receptor genes in chemical factor perception, this study identified three classes of chemosensory receptor genes—Olfactory Receptors (ORs), Ionotropic Receptors (IRs), and Acetylcholine Receptors (ARs)—in both merobenthic species (O. sinensis, Octopus vulgaris) and holobenthic species (Octopus minor, Amphioctopus fangsiao). The results demonstrated that the number of chemosensory receptor genes identified in all species in this study was comparable. Tissue expression analysis revealed that IRs were widely expressed across multiple olfaction-related organs, while the cephalopod-specific ARs were predominantly expressed in suckers and sucker epithelium. From hatching to adulthood, merobenthic paralarvae exhibited downregulation of nearly half of their chemosensory receptor genes, whereas holobenthic paralarvae showed only about 10 % gene downregulation, reflecting distinct chemosensory receptor expression patterns driven by divergent ecological adaptations between the hatchlings of these two life-history strategies. Based on the analysis of chemosensory receptor gene expression levels at different developmental stages of merobenthic paralarvae, RYamide receptor, Cholecystokinin receptor A (CCKAR), and Free fatty acid receptor 4 (FFAR4) were identified as potential key chemosensory receptor genes involved in the benthic settlement process. All three genes were functionally linked to feeding regulation, suggesting that chemical factors may regulate paralarval physiological functions related to feeding, thereby helping paralarvae conserve energy while awaiting the maturation of their nervous system and arm functionality, which would facilitate a successful transition to benthic settlement. This study laid a solid foundation for identifying key chemical factors involved in the benthic settlement process, which will contribute to breakthroughs in artificial seedling breeding techniques for O. sinensis and promote the development of its aquaculture industry.