Gut symbiotic bacteria enhance reproduction in Spodoptera frugiperda (J.E. Smith) by regulating juvenile hormone III and 20-hydroxyecdysone pathways.

IF 13.8 1区生物学 Q1 MICROBIOLOGY

Microbiome Pub Date : 2025-05-23 DOI:10.1186/s40168-025-02121-x

Bo Chu, Shishuai Ge, Wei He, Xiaoting Sun, Jiajie Ma, Xianming Yang, Chunyang Lv, Pengjun Xu, Xincheng Zhao, Kongming Wu

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引用次数: 0

Abstract

Background: 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.

Results: 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.

Conclusions: 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.

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肠道共生细菌通过调节幼体激素III和20-羟基蜕皮激素通路促进frugiperda （J.E. Smith）繁殖。

背景：昆虫肠道微生物群形成一个复杂的、多功能的系统，显著影响与环境适应相关的表型性状。强大的生殖潜力是秋粘虫（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frugiperda的繁殖过程、分布和传播动力学中的确切作用尚不清楚。结果：我们检查了主要的入侵农业害虫S. frugiperda的肠道微生物群，确定了肠球菌、肠杆菌和克雷伯氏菌是其整个生命周期中存在的核心微生物。这些微生物在雌虫的卵期、幼虫早期和产卵前表现出较高的活性。采用昆虫再感染系统，发现quebecenterococcus FAW181、Klebsiella michiganensis FAW071和Enterobacter hormaechei FAW049显著提高了宿主的繁殖力，分别提高了62.73%、59.95%和56.71%的产卵量。宏基因组学和血淋巴代谢组学分析显示，雌性frugiperda肠道共生菌群与激素代谢呈正相关。进一步分析昆虫激素生物合成途径的代谢物，以及外源性注射幼激素III和20-羟基蜕皮激素，发现肠道微生物调节这些激素，保持与对照昆虫相当的水平。这一调控有助于提高S. frugiperda的繁殖力，有助于快速定植和种群扩张。结论：这些发现强调了肠道细菌E. quebecensis FAW181、E. hormaechei FAW049和K. michiganensis FAW071通过JHAMT调节JH III水平，同时通过PHM调节20E及其前体水平，在促进S. frugiperda繁殖中的关键作用。我们的研究结果为外来入侵物种的微生物-宿主共生和害虫管理策略提供了新的见解。视频摘要。

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来源期刊

Microbiome MICROBIOLOGY-

CiteScore

21.90

自引率

2.60%

发文量

198

审稿时长

4 weeks

期刊介绍： Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.