Modulation of sensory information processing by a neuroglobin in <i>Caenorhabditis elegans</i>.

Abstract

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 <i>Caenorhabditis elegans</i> 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 <i>Caenorhabditis elegans</i> 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.