Chu Bo, Ge Shishuai, He Wei, Sun Xiaoting, Ma Jiajie, Yang Xianming, Lv Chunyang, Xu Pengjun, Zhao Xincheng, Wu Kongming
Henan International Joint Laboratory of Green Pest Control, College of Plant Protection, Henan Agricultural University, Zhengzhou, 450002, China.
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China.
Microbiome. 2025 May 23;13(1):132. doi: 10.1186/s40168-025-02121-x.
The insect gut microbiota forms a complex, multifunctional system that significantly affects phenotypic traits linked to environmental adaptation. Strong reproductive potential underpins the migratory success, population growth and destructive impact of the fall armyworm, Spodoptera frugiperda (J.E. Smith). However, the precise role of gut bacteria in S. frugiperda reproductive processes, distribution and transmission dynamics remains unclear.
We examined the gut microbiota of S. frugiperda a major invasive agricultural pest, identifying Enterococcus, Enterobacter, and Klebsiella as core microorganisms present throughout its life cycle. These microbes showed heightened activity during the egg stage, early larval stages and pre-oviposition period in females. Using an axenic insect re-infection system, Enterococcus quebecensis FAW181, Klebsiella michiganensis FAW071 and Enterobacter hormaechei FAW049 were found to significantly enhance host fecundity, increasing egg production by 62.73%, 59.95%, and 56.71%, respectively. Metagenomic and haemolymph metabolomic analyses revealed a positive correlation between gut symbiotic bacteria and hormone metabolism in female S. frugiperda. Further analysis of metabolites in the insect hormone biosynthesis pathway, along with exogenous injection of juvenile hormone III and 20-hydroxyecdysone, revealed that gut microbes regulate these hormones, maintaining levels equivalent to those in control insects. This regulation supports improved fecundity in S. frugiperda, aiding rapid colonization and population expansion.
These findings emphasize the pivotal role of gut bacteria E. quebecensis FAW181, E. hormaechei FAW049, and K. michiganensis FAW071 in enhancing S. frugiperda reproduction by modulating JH III levels through JHAMT regulation and concurrently modulating the levels of 20E and its precursors via PHM. Our results provide novel insights into microbe-host symbiosis and pest management strategies for alien invasive species. Video Abstract.
昆虫肠道微生物群形成一个复杂的多功能系统，显著影响与环境适应相关的表型特征。强大的繁殖潜力是草地贪夜蛾（Spodoptera frugiperda，J.E. Smith）迁徙成功、种群增长和破坏性影响的基础。然而，肠道细菌在草地贪夜蛾生殖过程、分布和传播动态中的确切作用仍不清楚。
我们研究了主要入侵农业害虫草地贪夜蛾的肠道微生物群，确定肠球菌、肠杆菌和克雷伯菌是其整个生命周期中存在的核心微生物。这些微生物在卵期、幼虫早期和雌性产卵前期表现出较高的活性。使用无菌昆虫再感染系统，发现魁北克肠球菌FAW181、密歇根克雷伯菌FAW071和霍氏肠杆菌FAW049能显著提高宿主繁殖力，产卵量分别增加62.73%、59.95%和56.71%。宏基因组和血淋巴代谢组分析揭示了雌性草地贪夜蛾肠道共生细菌与激素代谢之间存在正相关。对昆虫激素生物合成途径中的代谢物进行进一步分析，以及外源注射保幼激素III和20-羟基蜕皮酮，结果表明肠道微生物调节这些激素，使其水平维持在与对照昆虫相当的水平。这种调节有助于提高草地贪夜蛾的繁殖力，促进其快速定殖和种群扩张。
这些发现强调了肠道细菌魁北克肠球菌FAW181、霍氏肠杆菌FAW049和密歇根克雷伯菌FAW071在通过JHAMT调节来调节保幼激素III水平，同时通过PHM调节20E及其前体水平，从而增强草地贪夜蛾繁殖方面的关键作用。我们的研究结果为微生物-宿主共生关系以及外来入侵物种的害虫管理策略提供了新的见解。视频摘要。
