Experience-dependent C-elegans behavior by modulation of ambient oxygen

Background: Ambient oxygen (O-2) influences the behavior of organisms from bacteria to man. In C. elegans, an atypical O-2 binding soluble guanylate cyclase (sGC), GCY-35, regulates O-2 responses. However, how acute and chronic changes in O-2 modify behavior is poorly understood. Results: Aggregating C. elegans strains can respond to a reduction in ambient O-2 by a rapid, reversible, and graded inhibition of roaming behavior. This aerokinetic response is mediated by GCY-35 and GCY-36 sGCs, which appear to become activated as O-2 levels drop and to depolarize the AQR, PQR, and URX neurons. Coexpression of GCY-35 and GCY-36 is sufficient to transform olfactory neurons into O-2 sensors. Natural variation at the npr-1 neuropeptide receptor alters both food-sensing and O-2-sensing circuits to reconfigure the salient features of the C. elegans environment. When cultivated in 1% O-2 for a few hours, C. elegans reset their preferred ambient O-2, seeking instead of avoiding 0%-5% O-2. This plasticity involves reprogramming the AQR, PQR, and URX neurons. Conclusions: To navigate O-2 gradients, C. elegans can modulate turning rates and speed of movement. Aerotaxis can be reprogrammed by experience or engineered artificially. We propose a model in which prolonged activation of the AQR, PQR, and URX neurons by low O-2 switches on previously inactive O-2 sensors. This enables aerotaxis to low O-2 environments and may encode a memory of previous cultivation in low O-2.