Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue.
Specialized oxygen-sensing cells in the nervous system generate rapid behavioural responses to oxygen. We show here that the nematode Caenorhabditis elegans exhibits a strong behavioural preference for 5-12% oxygen, avoiding higher and lower oxygen levels. 3',5'-cyclic guanosine monophosphate (cGMP) is a common second messenger in sensory transduction and is implicated in oxygen sensation. Avoidance of high oxygen levels by C. elegans requires the sensory cGMP-gated channel tax-2/tax-4 and a specific soluble guanylate cyclase homologue, gcy-35. The GCY-35 haem domain binds molecular oxygen, unlike the haem domains of classical nitric-oxide-regulated guanylate cyclases. GCY-35 and TAX-4 mediate oxygen sensation in four sensory neurons that control a naturally polymorphic social feeding behaviour in C. elegans. Social feeding and related behaviours occur only when oxygen exceeds C. elegans' preferred level, and require gcy-35 activity. Our results suggest that GCY-35 is regulated by molecular oxygen, and that social feeding can be a behavioural strategy for responding to hyperoxic environments.
Gray
Jesse M
JM
Howard Hughes Medical Institute and Department of Anatomy, The University of California, San Francisco, California 94143-0452, USA.
Karow
David S
DS
Lu
Hang
H
Chang
Andy J
AJ
Chang
Jennifer S
JS
Ellis
Ronald E
RE
Marletta
Michael A
MA
Bargmann
Cornelia I
CI
D000818:Animals; D001419:Bacteria / Q000235:genetics / Q000378:metabolism; D017173:Caenorhabditis elegans / Q000187:drug effects / Q000201:enzymology* / Q000235:genetics / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D002449:Cell Aggregation / Q000187:drug effects; D006152:Cyclic GMP / Q000378:metabolism; D005247:Feeding Behavior / Q000187:drug effects / Q000502:physiology*; D005502:Food; D005740:Gases / Q000378:metabolism; D006162:Guanylate Cyclase / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D006418:Heme / Q000378:metabolism; D018496:Hyperoxia / Q000201:enzymology / Q000235:genetics / Q000378:metabolism; D007473:Ion Channels / Q000378:metabolism; D009154:Mutation / Q000235:genetics; D009475:Neurons, Afferent / Q000378:metabolism; D009569:Nitric Oxide / Q000378:metabolism / Q000494:pharmacology; D010100:Oxygen / Q000378:metabolism* / Q000494:pharmacology; D011485:Protein Binding; D017434:Protein Structure, Tertiary; D012919:Social Behavior
D029742:Caenorhabditis elegans Proteins; D005740:Gases; D007473:Ion Channels; C102184:tax-4 protein, C elegans; D009569:Nitric Oxide; D006418:Heme; C488166:GCY-35 protein, C elegans; D006162:Guanylate Cyclase; D006152:Cyclic GMP; D010100:Oxygen