Behavioral motifs and neural pathways coordinating O2 responses and aggregation in C. elegans.

BACKGROUND: Simple stimuli can evoke complex behavioral responses coordinated by multiple neural circuits. O(2) is an important environmental variable for most animals. The nematode C. elegans avoids high O(2), and O(2) levels regulate its foraging and aggregation. RESULTS: Here, we dissect aggregation and responses to O(2) gradients into behavioral motifs and show how O(2) responses can promote aggregation. To remain in a group, C. elegans continually modify their movement. Animals whose heads emerge from a group will reverse or turn, thereby returning to the group. Re-entry inhibits further reversal, aiding retention in the group. If an animal's tail exits a group during a reversal, it switches to forward movement, returning to the group. Aggregating C. elegans locally deplete O(2). The rise in O(2) levels experienced by animals leaving a group induces both reversal and turning. Conversely, the fall in O(2) encountered when entering a clump suppresses reversal, turning, and high locomotory activity. The soluble guanylate cyclases GCY-35 and GCY-36, which are expressed in head and tail neurons, promote reversal and turning when O(2) rises. Avoidance of high O(2) is also promoted by the TRP-related channel subunits OCR-2 and OSM-9, and the transmembrane protein ODR-4, acting in the nociceptive neurons ASH and ADL. Both O(2) responsiveness and aggregation can be modified by starvation, but this is regulated by natural variation in the npr-1 neuropeptide receptor. CONCLUSIONS: Our work provides insights into how a complex behavior emerges from simpler behavioral motifs coordinated by a distributed circuit.

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

BACKGROUND: Ambient oxygen (O2) influences the behavior of organisms from bacteria to man. In C. elegans, an atypical O2 binding soluble guanylate cyclase (sGC), GCY-35, regulates O2 responses. However, how acute and chronic changes in O2 modify behavior is poorly understood. RESULTS: Aggregating C. elegans strains can respond to a reduction in ambient O2 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 O2 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 O2 sensors. Natural variation at the npr-1 neuropeptide receptor alters both food-sensing and O2-sensing circuits to reconfigure the salient features of the C. elegans environment. When cultivated in 1% O2 for a few hours, C. elegans reset their preferred ambient O2, seeking instead of avoiding 0%-5% O2. This plasticity involves reprogramming the AQR, PQR, and URX neurons. CONCLUSIONS: To navigate O2 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 O2 switches on previously inactive O2 sensors. This enables aerotaxis to low O2 environments and may encode a "memory" of previous cultivation in low O2.

Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1.

Social and solitary feeding in natural Caenorhabditis elegans isolates are associated with two alleles of the orphan G-protein-coupled receptor (GPCR) NPR-1: social feeders contain NPR-1 215F, whereas solitary feeders contain NPR-1 215V. Here we identify FMRFamide-related neuropeptides (FaRPs) encoded by the flp-18 and flp-21 genes as NPR-1 ligands and show that these peptides can differentially activate the NPR-1 215F and NPR-1 215V receptors. Multicopy overexpression of flp-21 transformed wild social animals into solitary feeders. Conversely, a flp-21 deletion partially phenocopied the npr-1(null) phenotype, which is consistent with NPR-1 activation by FLP-21 in vivo but also implicates other ligands for NPR-1. Phylogenetic studies indicate that the dominant npr-1 215V allele likely arose from an ancestral npr-1 215F gene in C. elegans. Our data suggest a model in which solitary feeding evolved in an ancestral social strain of C. elegans by a gain-of-function mutation that modified the response of NPR-1 to FLP-18 and FLP-21 ligands.