College of Wildlife and Protected Area, Northeast Forestry University 150040 Harbin, China.
Department of Biophysics and Kidney Disease Center of the First Affiliated Hospital, Zhejiang University School of Medicine 310058 Hangzhou, China.
Proc Natl Acad Sci U S A. 2023 Feb 21;120(8):e2218948120. doi: 10.1073/pnas.2218948120. Epub 2023 Feb 13.
Organisms from cyanobacteria to humans have evolved a wide array of photoreceptive strategies to detect light. Sunlight avoidance behavior is common in animals without vision or known photosensory genes. While indirect light perception via photothermal conversion is a possible scenario, there is no experimental evidence for this hypothesis. Here, we show a nonvisual and extraocular sunlight detection mechanism by identifying the broad-range thermal receptor 1 (BRTNaC1, temperature range = 33 to 48 °C) in centipede antennae. BRTNaC1, a heat-activated cation-permeable ion channel, is structurally related to members of the epithelial sodium channel family. At the molecular level, heat activation of BRTNaC1 exhibits strong pH dependence controlled by two protonatable sites. Physiologically, temperature-dependent activation of BRTNaC1 upon sunlight exposure comes from a striking photothermal effect on the antennae, where a slightly acidic environment (pH 6.1) of the body fluid leads to the protonation of BRTNaC1 and switches on its high thermal sensitivity. Furthermore, testosterone potently inhibits heat activation of BRTNaC1 and the sunlight avoidance behavior of centipedes. Taken together, our study suggests a sophisticated strategy for nonvisual sunlight detection in myriapods.
从蓝藻到人类，生物体已经进化出了各种各样的感光策略来探测光。在没有视觉或已知感光基因的动物中，避免阳光照射的行为很常见。虽然通过光热转换来感知间接光可能是一种情况，但目前还没有实验证据支持这一假说。在这里，我们通过鉴定蜈蚣触角中的广谱热受体 1（BRTNaC1，温度范围为 33 至 48°C），发现了一种非视觉和眼外的阳光探测机制。BRTNaC1 是一种热激活的阳离子渗透性离子通道，与上皮钠通道家族的成员在结构上相关。在分子水平上，BRTNaC1 的热激活表现出强烈的 pH 依赖性，由两个可质子化的位点控制。在生理上，阳光照射时，BRTNaC1 对温度的依赖性激活来自于触角上引人注目的光热效应，其中体液的微酸性环境（pH 6.1）导致 BRTNaC1 的质子化，并使其具有较高的热敏感性。此外，睾酮能有效地抑制 BRTNaC1 的热激活和蜈蚣对阳光的回避行为。总之，我们的研究表明，在多足类动物中存在一种复杂的非视觉阳光探测策略。
