Modulation of sensory information processing by a neuroglobin in Caenorhabditis elegans

Sensory receptor neurons match their dynamic range to ecologically relevant stimulus intensities. How this tuning is achieved is poorly understood in most receptors. The roundworm Caenorhabditis elegans avoids 21% O₂ and hypoxia and prefers intermediate O₂ concentrations. We show how this O₂ preference is sculpted by the antagonistic action of a neuroglobin and an O₂-binding soluble guanylate cyclase. These putative molecular O₂ sensors confer a sigmoidal O₂ response curve in the URX neurons that has highest slope between 15 and 19% O₂ and approaches saturation when O₂ reaches 21%. In the absence of the neuroglobin, the response curve is shifted to lower O₂ values and approaches saturation at 14% O₂ In behavioral terms, neuroglobin signaling broadens the O₂ preference of Caenorhabditis elegans while maintaining avoidance of 21% O₂ A computational model of aerotaxis suggests the relationship between GLB-5-modulated URX responses and reversal behavior is sufficient to broaden O₂ preference. In summary, we show that a neuroglobin can shift neural information coding leading to altered behavior. Antagonistically acting molecular sensors may represent a common mechanism to sharpen tuning of sensory neurons.