Exploration of chemosensory ionotropic receptors in cephalopods: the IR25 gene is expressed in the olfactory organs, suckers, and fins of Sepia officinalis

Abstract

While they are mostly renowned for their visual capacities, cephalopods are also good at olfaction for prey, predator, and conspecific detection. The olfactory organs and olfactory cells are well described but olfactory receptors—genes and proteins—are still undescribed in cephalopods. We conducted a broad phylogenetic analysis of the ionotropic glutamate receptor family in mollusks (iGluR), especially to identify IR members (Ionotropic Receptors), a variant subfamily whose involvement in chemosensory functions has been shown in most studied protostomes. A total of 312 iGluRs sequences (including 111 IRs) from gastropods, bivalves, and cephalopods were identified and annotated. One orthologue of the gene coding for the chemosensory IR25 co-receptor has been found in Sepia officinalis (Soff-IR25). We searched for Soff-IR25 expression at the cellular level by in situ hybridization in whole embryos at late stages before hatching. Expression was observed in the olfactory organs, which strongly validates the chemosensory function of this receptor in cephalopods. Soff-IR25 was also detected in the developing suckers, which suggests that the unique « taste by touch » behavior that cephalopods execute with their arms and suckers share features with olfaction. Finally, Soff-IR25 positive cells were unexpectedly found in fins, the two posterior appendages of cephalopods, mostly involved in locomotory functions. This result opens new avenues of investigation to confirm fins as additional chemosensory organs in cephalopods.

Evolutionary Dynamics of Lineage-Specific Class-A GPCR Subsets Reveal Widespread Chemosensory Roles and Adaptations in Lophotrochozoa

“…For example, species adapted to extreme environments like deep-sea hydrothermal vents and those with parasitic lifestyles, such as freshwater leeches and parasitic Platyhelminthes, consistently exhibit reduced numbers of Class-A GPCRs and LSEs across various phyla. Similarly, lineages with alternative chemosensory mechanisms, such as cephalopods (48,49,(88)(89)(90), and those emphasizing sessile behaviors like certain limpets (41), show decreased GPCR and LSE counts. Excluding deep-sea and species with specific lifestyle adaptations, taxa inhabiting various coastal, freshwater, and terrestrial habitats, as well as those with advanced sensory structures across different phyla, typically demonstrate large and divergent LSEs.…”