A palate for microbes

The octopus is an organism with heightened sensitivities.

Most of its 500 million neurons reside in its limbs, which traverse the ocean floor like eight powerful tongues. It maneuvers through the depths with a “taste by touch” nervous system energized by 10,000 sensory cells within each suction cup.

Presently, a recent study by Harvard biologists uncovers some of what the octopus is discerning — biochemical signals from the microbial realm. By sampling the biochemicals released by fluctuating bacterial populations, the creature gathers crucial survival information, such as whether its prey is safe to consume or if unhealthy eggs should be expelled from the nest.

“Everything is covered with microbes, particularly in these underwater environments,” stated Rebecka Sepela, a postdoctoral researcher and primary author of the new study. “These microbial communities are in a constant state of flux in response to environmental changes and will emit distinct chemicals indicative of their surface-specific surroundings. The octopus detects the chemicals produced by specific microbes, including those thriving on crab or egg surfaces, to discern the particulars of those surfaces.”

The octopus’s sensory system has been an area of persistent inquiry at Harvard. In 2020, scholars in the laboratory of Nicholas Bellono, a professor of molecular and cellular biology, elaborated on how “chemotactile receptors” equipped octopuses with their distinct taste-by-touch aptitude. In 2023, the team described how these sensory structures had progressed from the acetylcholine receptors of their ancestors — but evolved differently in octopuses compared to their cephalopod cousin, the squid.

For the newest study, released Tuesday in the journal Cell, the Bellono group aimed to gain a deeper understanding of what sensations these organs were detecting. Octopuses search for food by sweeping their limbs over the ocean floor and investigating crevices for nourishment. Even in darkness, they “blind feed” by relying solely on their appendages’ sensory inputs. However, how they identify prey and other items of interest remained elusive.

To illuminate this inquiry, the Harvard researchers allowed the animals to reveal what was significant to them. The lab applies a “curiosity-driven approach” to explore biological curiosities and seeks to decipher the fundamental mechanisms at the molecular and protein level. It houses California two-spot octopuses (a species indigenous to the Pacific coast of the Americas) in saltwater tanks — securely fastened with Velcro straps and weighted with bricks. “We’ve observed them escape their tanks,” noted Bellono.

While observing the octopuses, the researchers noted that two items provoked strong responses — the shells of fiddler crabs (a preferred food source) and octopus eggs.

“It was very octopus-centric,” remarked Sepela. “By centering the animal in our research, we could identify molecules in the environment that hold actual significance for the animal.”

“By centering the animal in our research, we could identify molecules in the environment that hold actual significance for the animal.”

Rebecka Sepela

The researchers discovered that octopuses willingly fed on live crabs but avoided decomposed ones. Octopus mothers diligently cleansed and tended to their clutches of eggs but occasionally expelled infertile or dead eggs.

Upon scrutinizing these materials under an electron microscope, they observed stark variations in microbial populations. Live crabs had only a few microbes on their exteriors, whereas decaying crabs were enveloped by numerous bacterial types. Similarly, eggs rejected by octopus mothers exhibited spirillum-shaped bacteria, while healthy eggs did not.

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The researchers employed RNA barcoding to uncover the taxonomic classifications and quantities of these microbial groups prior to analyzing the compounds released by the microbes — along with the reactions these substances provoked in the octopus. The team cultivated nearly 300 strains of marine bacteria and evaluated their effects on cloned octopus chemotactile receptors in the laboratory.

They found that specific microbes activated particular receptors in octopuses. In an astonishing discovery, the scientists pinpointed a compound released by bacteria often found on eggs that were discarded by the mother octopus. The researchers created a synthetic egg, covered it with the compound, and placed it in an octopus nest. After briefly tending to the egg, the mother expelled it from her brood.

Microbes — or unicellular organisms — are the most prevalent entities on Earth. A single human’s body harbors approximately 39 trillion microbes. Similarly, the Earth, its waters, and even the atmosphere are abundant with microbial communities known as microbiomes.

Investigation into microbiomes centers on the interactions between microbes and their hosts — such as how gut bacteria facilitate digestion — yet the new article delves into a less-explored area: how creatures engage with external microbes and adjust to an ever-evolving environment. Science possesses only a vague comprehension of how multicellular animals interpret this external microbiome.

“There is vastly more to investigate,” stated Bellono. “Microbes exist on nearly every surface. We had an effective system to study this in the octopus, but that doesn’t imply it isn’t occurring throughout life.”

The Bellono Lab collaborated on this study 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.