Head-tail-head neural wiring underlies gut fat storage in Caenorhabditis elegans temperature acclimation

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.

Automated summary

This study revealed that Caenorhabditis elegans exhibited temperature acclimation plasticity, which was regulated by a head-tail-head neural circuitry and gut fat storage. The worms memorized the experience of cold and prepared against subsequent cold stimuli. The cyclic adenosine monophosphate response element-binding protein played a regulatory role in temperature acclimation. The communication between different neurons in the neural circuitry was mediated by glutamatergic signaling. Gut fat storage regulation, activated by a neuropeptide downstream of the cyclic adenosine monophosphate response element-binding protein, was responsible for temperature acclimation.