Structural basis of sensory receptor evolution in octopus.

Area of Science:

• Evolutionary biology
• Structural biology
• Neuroscience

Background:

• Chemotactile receptors (CRs) are unique to cephalopods, enabling 'taste by touch' for seafloor exploration.
• CRs evolved from nicotinic acetylcholine receptors to detect insoluble environmental molecules.
• Understanding CR structure is key to probing sensory receptor evolution and function.

Purpose of the Study:

• To investigate the structural basis of octopus CR evolution and function.
• To compare octopus CR structure with nicotinic receptors to differentiate environmental sensation from neurotransmission.
• To elucidate the atomic-level adaptations enabling new sensory capabilities and behaviors.

Main Methods:

• Cryo-electron microscopy (cryo-EM) to determine the structure of an octopus CR.
• Comparative structural analysis with nicotinic receptors.
• Evolutionary, structural, and biophysical analyses.

Main Results:

• The channel architecture for signal transduction is conserved between CRs and nicotinic receptors.
• The ligand-binding site of octopus CRs shows diversifying selection, allowing detection of new molecules.
• Octopus CRs possess an exceptionally hydrophobic binding pocket, facilitating sensation of greasy compounds.

Conclusions:

• Octopus CRs have evolved specialized structural features, particularly in their ligand-binding pocket, for environmental chemosensation.
• These adaptations allow octopuses to detect insoluble molecules, contributing to their unique exploratory behaviors.
• The study provides a structural framework for understanding the link between molecular evolution and organismal behavior.