Modulation of sensory information processing by a neuroglobin in C. elegans

TL;DR

This study reveals how a neuroglobin in C. elegans modulates sensory neuron responses to oxygen, affecting perception and behavior by shifting neural coding through antagonistic molecular interactions.

Contribution

It uncovers the role of a neuroglobin in tuning sensory neuron responses and behavior in C. elegans, demonstrating a novel mechanism of sensory information modulation.

Findings

GLB-5 neuroglobin inhibits O2-evoked Ca2+ responses in URX neurons.

Absence of GLB-5 shifts the O2 response saturation from 21% to 15%.

GLB-5 broadens O2 preference behaviorally in C. elegans.

Abstract

Sensory receptor neurons match their dynamic range to ecologically relevant stimulus intensities. How this tuning is achieved is poorly understood in most receptors. We show that in the C. elegans URX O2 sensing neurons two putative molecular O2 sensors, a neuroglobin and O2-binding soluble guanylate cyclases, work antagonistically to sculpt a slowly sigmoidal O2 response curve tuned to approach saturation when O2 reaches 21%. glb-5 imposes this sigmoidal function by inhibiting O2-evoked Ca2+ responses in URX when O2 levels fall. Without GLB-5, the URX response curve approaches saturation at 15% O2. Behaviorally, GLB-5 signaling broadens the O2 preference of C. elegans while maintaining strong avoidance of 21% O2. Our computational aerotaxis model suggests that the relationship between GLB-5-modulated URX responses and reversal behavior is sufficient to broaden O2-preference. Thus, a neuroglobin can shift neural information coding leading to a change in perception and altered behavior.