Bile acid chemosensation in mammals supports species and gut microbiome evaluation
The rodent vomeronasal system, also known as the accessory olfactory system (AOS), detects excreted chemosignals that guide social, reproductive, and defensive behaviors. Excretions sensed by the AOS contain blends of organic chemicals that reflect the biological identity of the emitter, but it remains unclear how the AOS extracts useful information from these complex natural cues. Vomeronasal sensory neurons (VSNs) sense bile acids, a diverse class of molecules excreted by vertebrates in feces. Using mass spectrometry, we found that patterns of bile acid excretion - not unique molecules - provide sufficient information to decode the emitters species, diet, and gut microbiome status. Using population calcium imaging, we found that VSN populations demonstrate an inverse relationship between natural bile acid abundance and population response magnitude and support efficient information encoding through stimulus "whitening." VSNs showed maximum sensitivity to taurine-conjugated bile acids, a novel class of vomeronasal ligands found at low natural abundance levels, that have high theoretical discriminatory value. VSN tuning patterns aligned strongly with theoretical axes for discriminating reptilian predators from vegetarians, and between mice with different gut microbiome states. These results reveal that the AOS extracts biological state from bile acid emission patterns through enhanced sensitivity to rare, information-rich ligands.