Animals maintain the ability to survive and reproduce by acclimating to environmental temperatures. We showed here that
Caenorhabditis elegans
exhibited temperature acclimation plasticity, which was regulated by a head-tail-head neural circuitry coupled with gut fat storage. After experiencing cold,
C. elegans
individuals memorized the experience and were prepared against subsequent cold stimuli. The cyclic adenosine monophosphate (cAMP) response element-binding protein (CREB) regulated temperature acclimation in the ASJ thermosensory neurons and RMG head interneurons, where it modulated ASJ thermosensitivity in response to past cultivation temperature. The PVQ tail interneurons mediated the communication between ASJ and RMG via glutamatergic signaling. Temperature acclimation occurred via gut fat storage regulation by the triglyceride lipase ATGL-1, which was activated by a neuropeptide, FLP-7, downstream of CREB. Thus, a head-tail-head neural circuit coordinated with gut fat influenced experience-dependent temperature acclimation.
Many organisms can survive and proliferate in changing environmental temperatures. Here, we introduce a molecular physiological mechanism for cold tolerance and acclimation of the nematode Caenorhabditis elegans on the basis of previous reports and a new result. Three types of thermosensory neurons located in the head, ASJ, ASG, and ADL, regulate cold tolerance and acclimation. In ASJ, components of the light-signaling pathway are involved in thermosensation. In ASG, mechanoreceptor DEG-1 acts as thermoreceptor. In ADL, transient receptor potential channels are thermoreceptors; however, the presence of an additional unidentified thermoreceptor is also speculated. ADL thermoresponsivity is modulated by oxygen sensory signaling from URX oxygen sensory neurons via hub interneurons. ASJ releases insulin and steroid hormones that are received by the intestine, which results in lipid composition changing with cold tolerance. Additionally, the intestinal transcriptional alteration affects sperm functions, which in turn affects the thermosensitivity of ASJ; thus, the neuron-intestine-sperm-neuron tissue circuit is essential for cold tolerance.
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