Sensing the World
by Mechas
I recently travelled to my hometown of Cali, Colombia, where I was surprised by an announcement on the airport wall indicating that bacteria also travel everywhere. It seems microbiology is making a dent in society. But how can we sense these microbes? Perhaps we can get some clues from octopuses.
Fig. 1. Sign on airport wall in Cali, Colombia: Bacteria also travel everywhere. Image credit: Mechas Zambrano
We live in a microbe-rich world. And we are quickly accumulating data on our surrounding microbial communities, their composition, and their associations with our well-being and physiology. But we still lag in terms of understanding the detailed chemical conversations underlying these interactions. Uncovering the specific molecules within the rich array of signals that surround us can be daunting. This is where a system with clear connections between chemical signals and animal responses becomes important. One such model system is provided by the octopus Octopus bimaculoides.
Octopuses are both fascinating and surprising. These fearsome creatures are intelligent, they have nine brains, three hearts, and blue blood, and they are skilled in camouflage and escape. They also use their eight flexible arms, which have most of their neurons, to explore and taste their surroundings via chemotactile receptors (CRs) located in suction cups (suckers). By sensing surfaces, they can discriminate between live and decaying prey to avoid potentially toxic food sources, and, in the case of mothers, identify and eliminate nonviable embryos. But how are they able to do this?
Researchers at Harvard and UC San Diego exploited the O. bimaculoides model system to test the hypothesis that octopuses can identify microbial metabolites and interpret these signals. They first characterized the microbiomes found on surfaces associated with feeding and egg grooming responses: crab shells and egg casings. These crab and egg surface microbial communities differed depending on whether they were selected or rejected by octopuses, suggestingthat microbiomes influence octopus behaviors.
Fig. 2 (A) Octopus bimaculoides displays its sensory suckers (left) next to salient cues including crab prey (Leptuca pugilator, top right) and developing octopus eggs (bottom right). (B) Scanning electron micrographs reveal surface-adhered bacillus, coccus, and spirillum bacteria on crab shells and on octopus eggs; scale bar, 10 μm. © Distinct microbiome communities were present on different surfaces from the octopus's habitat, n = 10 for each surface. Source
The next step, therefore, involved culturing microbes and testing filtered supernatants for their capacity to activate cloned chemotactile sensory receptor genes. Further fractionation of supernatants that activated sensory receptors led to the isolation of molecules that elicit different responses despite interacting with a single octopus receptor. They do so by binding in different structural conformations. They were also sufficient to drive octopus behavior: the octopuses rejected crab mimics or false agarose eggs soaked in these molecules.
We can now add another remarkable ability to the already growing list of astonishing octopus feats: the detection of specific molecules from complex environmental microbiomes. Specifically, the detection of molecules that elicit behaviors involved in maternal care or predation, both of which are important for survival.
Although we fall short in comparison, we also have evolved strategies to keep harmful substances at bay. Think of the times you have been disgusted by certain food textures or put off by foul-smelling substances. These reactions may just be contributing to your survival by helping to tease apart what to ingest.
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