Bai Shuai, Yao Zhichao, Cai Zhaohui, Ma Qiongke, Guo Qiongyu, Zhang Ping, Zhou Qi, Gu Jian, Liu Siying, Lemaitre Bruno, Li Xiaoxue, Zhang Hongyu
National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Hubei Hongshan Laboratory, Institute of Urban and Horticultural Entomology, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, People's Republic of China.
National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Hubei Hongshan Laboratory, Institute of Urban and Horticultural Entomology, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, People's Republic of China; Key Laboratory of Engineering Biology for Low-Carbon Manufacturing, Tianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences, Tianjin, People's Republic of China.
Cell Rep. 2025 Mar 25;44(3):115404. doi: 10.1016/j.celrep.2025.115404. Epub 2025 Mar 6.
The Duox-reactive oxygen species (ROS) system and the immune deficiency (Imd) pathway play a major role in insect gut immunity. However, their interaction to accomplish an effective immune response is still unclear. Here, we show that Duox regulates the peritrophic matrix (PM) and further affects the Imd immune response to pathogens in Bactrocera dorsalis. This regulation requires a nuanced ROS balance: low HO increases PM permeability, while higher HO damages the PM during infection. Importantly, we found that gut commensal bacteria ensured proper Duox-dependent ROS production and PM stability, thus preventing Imd pathway overactivation in response to pathogens. We conclude that gut commensal bacteria-induced Duox-ROS is crucial for maintaining PM structural homeostasis, and the PM, in turn, regulates Imd pathway activation and protects intestinal epithelial cells. Thus, our study reveals a crosstalk between the PM barrier and Imd-mediated antibacterial function to ensure host defense in the gut.
双氧化酶-活性氧（ROS）系统和免疫缺陷（Imd）途径在昆虫肠道免疫中起主要作用。然而，它们为实现有效免疫反应而进行的相互作用仍不清楚。在此，我们表明双氧化酶调节围食膜（PM），并进一步影响桔小实蝇对病原体的Imd免疫反应。这种调节需要微妙的ROS平衡：低水平的过氧化氢增加PM通透性，而较高水平的过氧化氢在感染期间会破坏PM。重要的是，我们发现肠道共生细菌确保了适当的双氧化酶依赖性ROS产生和PM稳定性，从而防止Imd途径因病原体而过度激活。我们得出结论，肠道共生细菌诱导的双氧化酶-ROS对于维持PM结构稳态至关重要，而PM反过来调节Imd途径激活并保护肠道上皮细胞。因此，我们的研究揭示了PM屏障与Imd介导的抗菌功能之间的相互作用，以确保肠道中的宿主防御。
