Department of Integrative Biology, University of Texas at Austin, USA.
Genome Biol Evol. 2022 Feb 4;14(2). doi: 10.1093/gbe/evac009.
Animals rely on their sensory systems to inform them of ecologically relevant environmental variation. In the Southern Ocean, the thermal environment has remained between -1.9 and 5 °C for 15 Myr, yet we have no knowledge of how an Antarctic marine organism might sense their thermal habitat as we have yet to discover a thermosensitive ion channel that gates (opens/closes) below 10 °C. Here, we investigate the evolutionary dynamics of transient receptor potential (TRP) channels, which are the primary thermosensors in animals, within cryonotothenioid fishes-the dominant fish fauna of the Southern Ocean. We found cryonotothenioids have a similar complement of TRP channels as other teleosts (∼28 genes). Previous work has shown that thermosensitive gating in a given channel is species specific, and multiple channels act together to sense the thermal environment. Therefore, we combined evidence of changes in selective pressure, gene gain/loss dynamics, and the first sensory ganglion transcriptome in this clade to identify the best candidate TRP channels that might have a functional dynamic range relevant for frigid Antarctic temperatures. We concluded that TRPV1a, TRPA1b, and TRPM4 are the likeliest putative thermosensors, and found evidence of diversifying selection at sites across these proteins. We also put forward hypotheses for molecular mechanisms of other cryonotothenioid adaptations, such as reduced skeletal calcium deposition, sensing oxidative stress, and unusual magnesium homeostasis. By completing a comprehensive and unbiased survey of these genes, we lay the groundwork for functional characterization and answering long-standing thermodynamic questions of thermosensitive gating and protein adaptation to low temperatures.
动物依靠其感觉系统来感知与生态相关的环境变化。在南大洋，其热环境在 1500 万年里一直保持在-1.9 至 5°C 之间，但我们不知道南极海洋生物如何感知其热栖息地，因为我们尚未发现一种热敏离子通道，该通道在 10°C 以下开启/关闭。在这里，我们研究了瞬态受体电位（TRP）通道的进化动态，TRP 通道是动物的主要热感受器，存在于南极海洋的主要鱼类 cryonotothenioid 鱼类中。我们发现 cryonotothenioid 鱼类与其他硬骨鱼类具有相似的 TRP 通道组成（约 28 个基因）。先前的工作表明，给定通道中的热敏门控是物种特异性的，并且多个通道协同作用以感知热环境。因此，我们结合了该进化枝中选择性压力变化、基因获得/缺失动态以及第一感觉神经节转录组的证据，以确定最有可能具有与冰冷南极温度相关的功能动态范围的候选 TRP 通道。我们得出的结论是，TRPV1a、TRPA1b 和 TRPM4 是最有可能的假定热敏传感器，并在这些蛋白质的跨位点发现了多样化选择的证据。我们还提出了关于其他 cryonotothenioid 适应机制的分子机制的假设，例如减少骨骼钙沉积、感知氧化应激和异常镁稳态。通过对这些基因进行全面和无偏的调查，我们为功能特征描述和回答关于热敏门控和蛋白质对低温适应的长期热力学问题奠定了基础。
