Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans.
All terrestrial animals must find a proper level of moisture to ensure their health and survival. The cellular-molecular basis for sensing humidity is unknown in most animals, however. We used the model nematode Caenorhabditis elegans to uncover a mechanism for sensing humidity. We found that whereas C. elegans showed no obvious preference for humidity levels under standard culture conditions, worms displayed a strong preference after pairing starvation with different humidity levels, orienting to gradients as shallow as 0.03% relative humidity per millimeter. Cell-specific ablation and rescue experiments demonstrate that orientation to humidity in C. elegans requires the obligatory combination of distinct mechanosensitive and thermosensitive pathways. The mechanosensitive pathway requires a conserved DEG/ENaC/ASIC mechanoreceptor complex in the FLP neuron pair. Because humidity levels influence the hydration of the worm's cuticle, our results suggest that FLP may convey humidity information by reporting the degree that subcuticular dendritic sensory branches of FLP neurons are stretched by hydration. The thermosensitive pathway requires cGMP-gated channels in the AFD neuron pair. Because humidity levels affect evaporative cooling, AFD may convey humidity information by reporting thermal flux. Thus, humidity sensation arises as a metamodality in C. elegans that requires the integration of parallel mechanosensory and thermosensory pathways. This hygrosensation strategy, first proposed by Thunberg more than 100 y ago, may be conserved because the underlying pathways have cellular and molecular equivalents across a wide range of species, including insects and humans.
Institute of Cell and Molecular Biology, Center for Brain, Behavior and Evolution, Center for Learning and Memory, Waggoner Center for Alcohol and Addiction Research, and Department of Neuroscience, The University of Texas at Austin, Austin, TX 78712.
Joshua
J
Russell
Institute of Cell and Molecular Biology, Center for Brain, Behavior and Evolution, Center for Learning and Memory, Waggoner Center for Alcohol and Addiction Research, and Department of Neuroscience, The University of Texas at Austin, Austin, TX 78712.
Andrés G
AG
Vidal-Gadea
Institute of Cell and Molecular Biology, Center for Brain, Behavior and Evolution, Center for Learning and Memory, Waggoner Center for Alcohol and Addiction Research, and Department of Neuroscience, The University of Texas at Austin, Austin, TX 78712.
Alex
A
Makay
Institute of Cell and Molecular Biology, Center for Brain, Behavior and Evolution, Center for Learning and Memory, Waggoner Center for Alcohol and Addiction Research, and Department of Neuroscience, The University of Texas at Austin, Austin, TX 78712.
Carolyn
C
Lanam
Institute of Cell and Molecular Biology, Center for Brain, Behavior and Evolution, Center for Learning and Memory, Waggoner Center for Alcohol and Addiction Research, and Department of Neuroscience, The University of Texas at Austin, Austin, TX 78712 jonps@austin.utexas.edu.
Jonathan T
JT
Pierce-Shimomura
D062565:Acid Sensing Ion Channels / Q000502:physiology; D000818:Animals; D001522:Behavior, Animal / Q000502:physiology; D017173:Caenorhabditis elegans / Q000166:cytology / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000502:physiology; D006152:Cyclic GMP / Q000502:physiology; D053503:Epithelial Sodium Channels / Q000502:physiology; D006801:Humans; D006813:Humidity; D015640:Ion Channel Gating / Q000502:physiology; D007473:Ion Channels / Q000502:physiology; D008465:Mechanoreceptors / Q000502:physiology*; D008565:Membrane Proteins / Q000502:physiology; D009043:Motor Activity / Q000502:physiology; D046912:Multiprotein Complexes / Q000502:physiology; D011984:Sensory Receptor Cells / Q000502:physiology*; D013217:Starvation / Q000503:physiopathology; D013697:Thermosensing / Q000502:physiology*
D062565:Acid Sensing Ion Channels; D029742:Caenorhabditis elegans Proteins; C094927:Deg-1 protein, C elegans; D053503:Epithelial Sodium Channels; D007473:Ion Channels; D008565:Membrane Proteins; D046912:Multiprotein Complexes; C102184:tax-4 protein, C elegans; D006152:Cyclic GMP
mechanosensation; thermosensation