How octopuses taste with their tentacles

The octopus has a signature move: this spineless mastermind sweeps its sucker-studded tentacles along a surface it is exploring, simultaneously probing and grasping it. Researchers have long thought that when the animal performs this action, its suckers act as chemotactile sense organs that combine touch and taste. But there have been few investigations of their molecular mechanisms.

Now, researchers studying the two-spot octopus (Octopus bimaculoides) have made this molecular link. They’ve identified receptors in the octopus’s suckers that get activated upon detecting chemicals emitted by its prey (Cell, 2020, DOI: 10.1016/j.cell.2020.09.008). The study is sure to launch a deep exploration of the enigmatic creature, which has a nervous system very different from our own, says Clifton Ragsdale, a neurobiologist studying cephalopods at the University of Chicago who was not involved in the research.

Anatomical studies from the 1960s suggested the suckers carried receptor cells similar to those in the nose and tongue of terrestrial animals. And the octopus genome, sequenced in 2015, held hints of a possible sensory receptor, though it was never investigated. “We have been waiting for this evidence,” says Jennifer Mather, a psychologist and cephalopod biologist at the University of Lethbridge, who was also not involved in the work.

Nicholas Bellono and his colleagues at Harvard University began their study by characterizing the cells in the suckers, first finding a typical-looking mechanoreceptor. Next, they homed in on ion channels whose genetic sequence was similar to those of neurotransmitter receptors. These were abundantly expressed in the sucker tissue. So the researchers expressed them in cells and tracked how they responded to chemical stimuli. But standard, water-soluble taste and odorant molecules—the kind that might make fish pay attention—had no effect.

Instead, Bellono’s team hit the jackpot when they stimulated the cells with a class of hydrophobic natural compounds called terpenoids. These molecules that are secreted by several marine invertebrates that octopuses eat. When an octopus touches surfaces infused with certain terpenoids, it responds with its characteristic fast-touch behavior, either retracting its arm or touching that surface rapidly, they found. Touch is key. “Having those molecules in the tank doesn’t change its behavior at all unless it makes contact with them,” Bellono says.

The newly identified receptors consist of multiple subunits that combine to form a variety of protein complexes, each of which can detect different molecules or have different sensitivities. That ability to form different combinations probably allows this sensory system to detect many different signals in different contexts relevant to the animal’s life, Bellono says.

The receptors undoubtedly detect much more than terpenoids, he adds. Octopuses may use this touch-taste sense to find prey, but they may also use it to engage with other aspects of their environment—“biofilms on surfaces or other features we really haven’t thought of yet,” he says. His team is testing the receptors’ response to some of the countless other chemicals it might encounter. They are also investigating whether this receptor system exists in other cephalopods, such as squid.

Mather calls the work a “wonderful, fascinating exploration of a chemosensing system that seems structurally different from those in other phyla.” The study, she says, shows how much we have to learn from the octopus.