Avoiding Too Much Oxygen

Science Signaling  31 Mar 2009:
Vol. 2, Issue 64, pp. ec112
DOI: 10.1126/scisignal.264ec112

The nematode Caenorhabditis elegans is found in near-hypoxic environments as well as those with atmospheric (21%) O2 concentrations, but, given a choice, it moves toward intermediate O2 concentrations (5 to 10% O2). Noting that mutation of genes encoding soluble guanylate cyclases (sGCs, a class of proteins that bind gases) affects C. elegans aerotaxis, Zimmer et al. explored the properties of two classes of sensory neurons that express sGC and have been implicated in avoidance of high O2. By combining neuronal ablation with behavioral analyses, the authors determined that URX neurons were required for behavioral responses to increased O2, whereas BAG neurons were required for behavioral responses to decreased O2. Experiments using a genetically encoded calcium sensor targeted to either URX or BAG neurons revealed that URX responded to increasing O2 from 10% to 21% with an increase in calcium (indicative of membrane depolarization and neuronal activation); in contrast, BAG neurons were activated by decreasing O2 concentration. Behavioral analysis of mutant worms implicated the sGC genes gcy-35 and gcy-36 in the response to increased O2, gcy-31 in the response to decreased O2, and gcy-33 in both. gcy-35 and gcy-36 are known to be expressed in URX neurons, and analyses of fluorescent fusion proteins indicated that gcy-31 was expressed in BAG neurons, whereas gcy-33 was expressed in both URX and BAG. O2-evoked calcium signals in URX neurons depended on gcy-35 and gcy-36, whereas O2-evoked calcium signals in BAG depended on gcy-31 and gcy-33. Intriguingly, transgenic expression of gcy-35 and gcy-36 in BAG neurons of worms with mutant gcy-31 and gcy-35 (or triple mutant gcy-31, -33, and -35) conferred URX-like calcium responses on BAG neurons and enabled them to mediate behavioral responses to increased O2. Thus, nematode responses to changes in O2 appear to depend on the neuron-specific expression of distinct sGCs.

M. Zimmer, J. M. Gray, N. Pokala, A. J. Chang, D. S. Karow, M.. A. Marletta, M. L. Hudson, D. B. Morton, N. Chronis, C. I. Bargmann, Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases. Neuron 61, 865–879 (2009). [PubMed]