Three billion years after bacterial life originated, animals diverged from their protistan ancestors and began to evolve in a bacterial world. Microbes play vital roles in directing animal development, digestion, decision making, and disease, making them integral to studies of interoception and exteroception. Yet, the identity of the chemical effectors and molecular receptors that confer these interkingdom interactions are often unknown, resulting in uncertainty in exactly how microbes sculpt animal biology. In my postdoctoral work, I am developing a methodological framework that spans many tiers of biology to discover microbial chemical cues and elucidate the structural and physiological mechanisms by which they drive animal behavior.
Since bacteria accumulate on diverse surfaces, especially in underwater worlds, I will test the hypothesis that bacteria create perceptible surface- and state-dependent cues that inform how animals interact with their surrounding surfaces using the octopus as a model system. The octopus utilizes specialized chemotactile receptors (CRs) on its arms to explore surface-affixed molecules along the seafloor, but how they distinguish meaningful surfaces from the rocks and crevices they encounter is unknown. By surveying the microbial chemical ecology pertinent surfaces, I have defined natural chemical cues produced from prey- and egg-specific microbes that activate octopus CRs and drive predatory and parental behavior. By combining structural biology and molecular evolution with electrophysiology and animal behavior, I have been able to assess how the octopus chemosensory system is structured to function in direct opposition to a microbial world.
Future work will continue to exploit the shared history between animals and microbes to discover new evolutionarily-honed molecules that activate specific sensory receptors to influence signaling events across receptors, cells, organ systems, and organisms. Microbes are rapidly reproducing organisms that evolved within and adapted to their environmental conditions with metabolisms that reflect temperature, pH, sunlight, oxygen, and mineralized nutrient availability. They coat nearly every surface on our planet and are omnipresent ‘chemical factories’ that secrete metabolites reflecting this external world – a rich information source worth eavesdropping on. By looking across models across the tree of life, I hope to will uncover how the intertwined past of animals and microbes defines the sensory experience of animals and drives animal nervous system evolution. This work will illuminate how unidirectional cues transition into the bidirectional signals that orchestrate host-microbe symbioses and have sweeping implications for how we uncover and address host-microbe interactions in health and disease.