Department of Economic Zoology, Max Planck Partner Group, Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou 310058, China.
Analysis Center of Agrobiology and Environmental Sciences, Zhejiang University, Hangzhou 310058, China.
Proc Natl Acad Sci U S A. 2024 Oct 15;121(42):e2412165121. doi: 10.1073/pnas.2412165121. Epub 2024 Oct 11.
Lepidopterans commonly feed on plant material, being the most significant insect herbivores in nature. Despite plant resistance to herbivory, such as producing toxic secondary metabolites, herbivores have developed mechanisms encoded in their genomes to tolerate or detoxify plant defensive compounds. Recent studies also highlight the role of gut microbiota in mediating detoxification in herbivores; however, convincing evidence supporting the significant contribution of gut symbionts is rare in Lepidoptera. Here, we show that the growth of various lepidopteran species was inhibited by a mulberry-derived secondary metabolite, 1-deoxynojirimycin (DNJ); as expected, the specialist silkworm grew well, but interestingly, gut microbiota of early-instar silkworms was affected by the DNJ level, and several bacterial species responded positively to enriched DNJ. Among these, a bacterial strain isolated from the silkworm gut ( ZJU1) can degrade and utilize DNJ as the sole energy source, and after inoculation into nonspecialists (e.g., beet armyworm ), ZJU1 increased host resistance to DNJ and significantly promoted growth. We used genomic and transcriptomic analyses to identify genes potentially involved in DNJ degradation, and CRISPR-Cas9-mediated mutagenesis verified the function of , a key binding protein, in metabolizing DNJ. Furthermore, the deletion mutant, exhibiting normal bacterial growth, could no longer enhance nonspecialist performance, supporting a role in DNJ degradation in vivo. Therefore, our study demonstrated causality between the gut microbiome and detoxification of plant chemical defense in Lepidoptera, facilitating a mechanistic understanding of host-microbe relationships across this complex, abundant insect group.
鳞翅目昆虫通常以植物材料为食，是自然界中最重要的昆虫食草动物。尽管植物具有抵抗食草作用的能力，例如产生有毒的次生代谢物，但食草动物已经在其基因组中开发了耐受或解毒植物防御化合物的机制。最近的研究还强调了肠道微生物群在介导食草动物解毒中的作用；然而，在鳞翅目昆虫中，很少有令人信服的证据支持肠道共生体的重要贡献。在这里，我们表明，各种鳞翅目物种的生长受到桑衍生的次生代谢物 1-脱氧野尻霉素（DNJ）的抑制；正如预期的那样，专食性蚕生长良好，但有趣的是，早期蚕的肠道微生物群受到 DNJ 水平的影响，并且几种细菌物种对富含 DNJ 的反应呈阳性。在这些细菌中，从蚕肠道中分离出的一个细菌菌株（ZJU1）可以降解和利用 DNJ 作为唯一的能量来源，并且在接种非专食性昆虫（例如，甜菜夜蛾）后，ZJU1 增加了宿主对 DNJ 的抗性，并显著促进了生长。我们使用基因组和转录组分析来鉴定可能参与 DNJ 降解的基因，并通过 CRISPR-Cas9 介导的诱变验证了关键结合蛋白 在代谢 DNJ 中的功能。此外， 缺失突变体表现出正常的细菌生长，不再能够增强非专食性表现，支持其在体内降解 DNJ 的作用。因此，我们的研究证明了肠道微生物群与鳞翅目植物化学防御解毒之间的因果关系，促进了对宿主-微生物关系的机制理解在这个复杂的、丰富的昆虫群体中。
