Department of Anesthesiology and Perioperative Medicine, University of Rochester Medical Center, Rochester, NY, 14642, USA.
Department of Imaging Sciences, University of Rochester Medical Center, Rochester, NY, 14642, USA.
Redox Biol. 2023 Nov;67:102934. doi: 10.1016/j.redox.2023.102934. Epub 2023 Oct 13.
Environmental surveillance-mediated behavior integrates multiple cues through complex signaling mechanisms. In Caenorhabditis elegans, neurons coordinate perception and response through evolutionarily conserved molecular signaling cascades to mediate attraction and avoidance behaviors. However, despite lacking eyes, C. elegans was recently reported to perceive and react to the color blue. Here, we provide an explanation for this apparent color perception. We show that internally-generated reactive oxygen species (ROS) occurring in response to light are additive to exogenous sources of ROS, such as bacterial toxins or photosensitizers. Multiple sub-threshold sources of ROS are integrated to coordinate behavioral responses to the environment with internal physiologic cues, independent of color. We further demonstrate that avoidance behavior can be blocked by antioxidants, while ROS is both sufficient and scalable to phenocopy the avoidance response. Moreover, avoidance behavior in response to ROS is plastic and reversible, suggesting it may occur through a post-translation redox modification. Blue light affects C. elegans behavior through ROS generation by endogenous flavins in a process requiring the neuronal gustatory photoreceptor like protein, LITE-1. Our results demonstrate that LITE-1 is also required for ROS-mediated avoidance of pyocyanin and light-activated photosensitizers and this role is mediated through the modification of Cys44. Overall, these findings demonstrate that ROS and LITE-1 are central mediators of C. elegans foraging behavior through integration of multiple inputs, including light.
环境监测介导的行为通过复杂的信号机制整合多种线索。在秀丽隐杆线虫中，神经元通过进化保守的分子信号级联协调感知和反应，介导趋性和回避行为。然而，尽管线虫没有眼睛，最近有报道称它能够感知和反应蓝色。在这里，我们解释了这种明显的颜色感知现象。我们表明，内部产生的活性氧（ROS）对光的反应与外部 ROS 源（如细菌毒素或光敏剂）相加。多个亚阈值 ROS 源被整合，以协调对环境的行为反应与内部生理线索，而与颜色无关。我们进一步证明，抗氧化剂可以阻断回避行为，而 ROS 既是充分的又是可扩展的，可以模拟回避反应。此外，对 ROS 的回避行为是可塑和可逆的，这表明它可能通过翻译后氧化还原修饰发生。蓝光通过内源性黄素在一个过程中产生 ROS 来影响秀丽隐杆线虫的行为，该过程需要神经元味觉光感受器样蛋白 LITE-1。我们的结果表明，LITE-1 也需要 ROS 介导的对绿脓菌素和光激活光敏剂的回避，并且这种作用是通过 Cys44 的修饰来介导的。总之，这些发现表明 ROS 和 LITE-1 是秀丽隐杆线虫觅食行为的中枢调节剂，通过整合多种输入，包括光。
