Molecules empowering animals to sense and respond to temperature in changing environments

Abstract

Adapting behavior to thermal cues is essential for animal growth and survival. Indeed, each and every biological and biochemical process is profoundly affected by temperature and its extremes can cause irreversible damage. Hence, animals have developed thermotransduction mechanisms to detect and encode thermal information in the nervous system and acclimation mechanisms to finely tune their response over different timescales. While temperature-gated TRP channels are the best described class of temperature sensors, recent studies highlight many new candidates, including ionotropic and metabotropic receptors. Here, we review recent findings in vertebrate and invertebrate models, which highlight and substantiate the role of new candidate molecular thermometers and reveal intracellular signaling mechanisms implicated in thermal acclimation at the behavioral and cellular levels. Variations in ambient temperature have dramatic effects on animal behavior, survival, and reproduction. One dramatic example is the response of a waddle of Emperor penguins to variations in ambient temperature: the colder the temperature, the more likely penguins are to huddle and to huddle more tightly [1]. The social behavior of huddling is essential for thermoregulation, energy conservation, and to complete the breeding cycle. Thus, animals have evolved behavioral and metabolic strategies for minimizing their exposure to rapid fluctuations and for adapting to slow seasonal variations. Such thermal acclimation behaviors depend on the animal's ability to link information provided by specialized thermosensory neurons to appropriate behaviors. Laboratory studies in animals that are amenable to genetic dissection such as fruit flies, nematodes, and mice, have revealed many relevant sensory neurons and thermoreceptor proteins. In this review, we consider candidate thermoreceptor proteins and signaling pathways as well as molecular mechanisms for responding to changing thermal environments, highlighting recent key results and emerging opportunities for discovery in this area. Molecular basis of thermosensingTo function as a thermoreceptor, a protein or signaling pathway should exhibit several properties. First, the protein(s) should localize to the presumptive site of temperature-sensing within sensory neurons embedded in tissues subjected to thermal fluctuations [2 ]. Second, the proteins(s) should be required for cellular and behavioral responses to thermal cues. Third, the protein(s) should confer extraordinary temperature sensitivity on heterologous cells and, fourth, protein function should itself be exquisitely temperature-sensitive. Distinguishing ordinary from extraordinary thermal sensitivity is not easy, however. One useful rule of thumb is to focus on proteins or signaling pathways with Q 10 values that exceed those typical of biochemical reactions such as active transport of ions (ca. 3) across biological membranes [3]. Though imperfect (see Ref.[2 ]), the Q 10 metric is frequently used to assess the effect of temperature on cell func...

A Critical Role for Thermosensation in Host Seeking by Skin-Penetrating Nematodes

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A system for the high-throughput analysis of acute thermal avoidance and adaptation in C. elegans

“…In order to demonstrate the utility of the ThermINATOR and IN-FERNO systems to dissect the molecular pathway controlling thermal sensitivity and plasticity, we used them to analyze the behavioral phenotype of mutant animals. We focus on three candidate genes, cmk-1, ckk-1, and crh-1, which are part of the same canonical pathway [37] and which had been previously implicated in behavioral plasticity evoked by constant temperature changes [27]. Nothing is known however on whether and how they could modulate behavioral response to repeated acute thermal stimuli.…”

“…Indeed, when pre-exposd to moderately noxious temperature for one hour, animals elevate their threshold for noxious heat avoidance. This plasticity involves the Ca 2+ signaling within thermosensory neurons and notably requires the Ca 2+ /calmodulin-dependent protein kinase-1 (CMK-1) and its upstream regulatory kinase Ca 2+ /calmodulin-dependent protein kinase kinase-1 (CKK-1) [27,28]. This pathway is also implicated in the response adaptation to other types of stimuli, such as adaptation in the innocuous range of temperature [29], salt learning [30], and habituation to repeated acute mechanical stimuli [31].…”

Ultrasound elicits behavioral responses through mechanical effects on neurons and ion channels in a simple nervous system

“…We used a genetic approach to distinguish among these possibilities, leveraging mutants deficient in thermosensation or mechanosensation. To test for thermal effects, we compared ultrasound-evoked behaviors in wild-type and gcy-23(nj37)gcy-8(oy44)gcy-18(nj38) that lack a trio of receptor guanylate cyclases expressed exclusively in the AFD thermoreceptor neurons and are defective in thermotaxis (Garrity et al, 2010;Glauser and Goodman, 2016). Although these mutants have an intact AFD thermoreceptor neuron, they lack the ability to sense tiny (<0.05 • C) thermal fluctuations in temperature Wasserman et al, 2011).…”