A taste for microbes

The octopus is a creature with sensitive feelings.

Most of its 500 million neurons are in its arms, which explore the seafloor like eight muscular tongues. It navigates the deep with a “taste by touch” nervous system powered by 10,000 sensory cells in each individual suction cup.

Now, a new study by Harvard biologists reveals part of what the octopus is feeling — biochemical information from the microbial world. By tasting the biochemicals emitted by ever-changing bacterial communities, the animal gains information essential for survival, such as whether prey is safe to eat or whether unhealthy eggs should be ejected from the nest.

“Everything is coated by microbes, especially in these underwater worlds,” said Rebecka Sepela, a postdoctoral researcher and lead author of the new study. “These microbial communities are constantly restructuring in response to environmental conditions and will pump out different chemicals to reflect their surface-specific surroundings. The octopus senses the chemicals made by certain microbes, such as those growing on the surfaces of crabs or eggs, to distinguish the vitals of these surfaces.”

The sensory system of the octopus has been a topic of ongoing research at Harvard. In 2020, researchers in the lab of Nicholas Bellono, a professor of molecular and cellular biology, detailed how “chemotactile receptors” armed octopuses with their unique taste-by-touch capability. In 2023, the group described how these sensory organs had evolved from the acetylcholine receptors of their ancestors — but differently in octopuses than in their cephalopod relative the squid.

For the latest study, published Tuesday in the journal Cell, the Bellono team sought to better understand just what these organs were sensing. Octopuses forage by sweeping their arms over the seafloor and probing nooks and crannies for food. Even in the dark, they “blind feed” by relying only on the senses of their appendages. But it remained unclear just how they identified prey and other objects of interest.

To shed light on that question, the Harvard researchers simply let the animals show them what was important. The lab follows a “curiosity-based approach” of investigating biological novelties and trying to decipher the underlying mechanisms down to the level of molecules and proteins. It keeps California two-spot octopuses (a species native to the Pacific coast of the Americas) in saltwater tanks — with the lids fastened tight with Velcro straps and weighed by bricks. “We’ve had them open their tanks and get out,” explained Bellono.

In watching the octopuses, the researchers saw that two objects elicited strong reactions — the shells of fiddler crabs (a favorite food) and octopus eggs.

“It was very octopus-centric,” said Sepela. “By keeping the animal at the center of our study, we were able to find molecules in the environment that are actually meaningful to the animal.”

“By keeping the animal at the center of our study, we were able to find molecules in the environment that are actually meaningful to the animal.”

Rebecka Sepela

The researchers found that octopuses happily fed on live crabs, but rejected decayed ones. Octopus mothers avidly cleaned and groomed their clutches of eggs, but sometimes ejected infertile or dead eggs.

When the scientists examined these materials under an electron microscope, they found stark differences in microbial communities. Live crabs had only a few microbes on their shells, but decaying crabs were coated by many types of bacteria. Likewise, eggs rejected by octopus mothers were covered by spirillum-shaped bacteria while healthy eggs were not.

The scientists used RNA barcoding to reveal the taxonomic identities and abundances of these microbial communities before examining the molecules emitted by the microbes — and the responses these substances elicited in the octopus. The team cultivated nearly 300 strains of marine bacteria and tested their effects on octopus chemotactile receptors that had been cloned in the lab.

They discovered that certain microbes activated certain octopus receptors. In one dramatic finding, the scientists identified a molecule emitted by bacteria commonly found on eggs rejected by the mother octopus. Researchers made a fake egg, coated it with the substance, and dropped it into an octopus nest. After briefly grooming the egg, the mother ejected it from her brood.

Microbes — or single-celled organisms — are the most abundant creatures on Earth. The body of a single human hosts around 39 trillion microbes. Likewise, the Earth, waters, and even the air teem with microbial communities known as microbiomes.

Research on microbiomes focuses on the relationship between microbes and their hosts — how gut bacteria aid in digestion, for example — but the new paper explores a lesser-known realm: how animals interact with external microbes and adapt to an ever-changing world. Science has only a murky understanding of how multicellular animals read this outside microbiome.

“There is a lot more to be explored,” said Bellono. “Microbes are present on almost every surface. We had a nice system to look at this in the octopus, but that doesn’t mean it’s not happening across life.”

The Bellono Lab collaborated on the research with the teams of Jon Clardy, a professor of biological chemistry and molecular pharmacology at Harvard Medical School, and Ryan Hibbs, a professor of neurobiology at the University of California, San Diego.