Gut microbial community response to herbicide exposure in a ground beetle

The gut microbiota plays a key role in physiological processes of insects including nutritional metabolism, development, immunity and detoxification. Environmental stressors such as herbicides, used to optimize and improve crop yields, may interfere with the mutualistic relationships causing negative consequences for the host health. This study assessed the effect of a pendimethalin-based herbicide on the gut microbial community of the carabid beetle <em>Pterostichus melas</em><em> italicus </em>Dejean, 1828 (Coleoptera, Carabidae), a generalist predator in the soil food web of agroecosystems. The exposure effect was tested <em>in vivo</em> by using a recommended field rate and evaluating the variability of responses in 21 days, corresponding to the half-life of the pendimethalin. The 16S rRNA sequencing data showed that the gut lumen was dominated by Proteobacteria, Firmicutes, Fusobacteria, Tenericutes and Bacteroidetes. The herbicide exposure interfered with the bacterial community richness and diversity associated with the gut from 2 days after the treatment. The differential abundance analyses highlighted a shift involving families such as Lactobacillaceae, Streptomycetaceae, Neisseriaceae and Ruminococcaceae and genera belonging to Enterobacteriaceae. An increase of bacterial species such as <em>Enterobacter</em> sp., <em>Pseudomonas</em> sp., <em>Pantoea</em> sp and <em>Paracoccus </em>sp. involved in the herbicide degradation was also recorded after 21 days of exposure. Phylogenetic investigation of communities by reconstruction of unobserved states (PICRUSt) analysis indicated that the exposure have effects on the most predicted functional categories of gut microbiota related to metabolic function including carbohydrate, amino acid and lipid metabolism of<em> P.melas</em>. These results demonstrate that pendimethalin can impact microbial communities associated with generalist predators inhabiting croplands leading to severe implications for the species ecological role. Understanding the effects of herbicides such as pendimethalin on ground beetles may help to protect beneficial soil insects that have a crucial role in the ecosystem services.昆虫肠道微生物群（gut microbiota）在昆虫的营养代谢、生长发育、免疫防御及解毒生理等过程中发挥关键作用。为优化并提升作物产量而施用的除草剂等环境胁迫因子，可能干扰宿主与肠道微生物的互利共生关系，进而对宿主健康产生负面影响。本研究评估了基于二甲戊灵（pendimethalin）的除草剂对农田食物网内广食性土壤捕食者——意大利黑步甲（*Pterostichus melas italicus* Dejean, 1828，鞘翅目步甲科）肠道微生物群落的影响。研究采用田间推荐施用量开展体内（in vivo）暴露实验，于暴露后21天（对应二甲戊灵的半衰期）评估宿主响应的变异程度。16S rRNA测序结果显示，该步甲的肠道内腔以变形菌门(Proteobacteria)、厚壁菌门(Firmicutes)、梭杆菌门(Fusobacteria)、软壁菌门(Tenericutes)和拟杆菌门(Bacteroidetes)为优势类群。除草剂暴露可于处理后2天起，干扰肠道细菌群落的丰富度与多样性。差异丰度分析结果显示，乳杆菌科(Lactobacillaceae)、链霉菌科(Streptomycetaceae)、奈瑟菌科(Neisseriaceae)、瘤胃球菌科(Ruminococcaceae)以及肠杆菌科(Enterobacteriaceae)下属菌属的相对丰度均发生显著偏移。暴露21天后，研究还观测到参与除草剂降解的肠杆菌属(*Enterobacter* sp.)、假单胞菌属(*Pseudomonas* sp.)、泛菌属(*Pantoea* sp.)和副球菌属(*Paracoccus* sp.)等细菌类群的丰度显著上升。基于未观测状态重建的群落系统发育分析（PICRUSt）结果表明，二甲戊灵暴露可影响该步甲肠道微生物群的多数预测功能类别，这些功能与宿主代谢功能密切相关，涵盖碳水化合物代谢、氨基酸代谢与脂质代谢等途径。上述研究结果证实，二甲戊灵可对农田生境内广食性捕食者的肠道微生物群落产生影响，进而对该物种的生态功能造成严重影响。探明二甲戊灵等除草剂对步甲的影响，有助于保护在生态系统服务中发挥关键作用的有益土壤昆虫。