The effect of a partial anthelmintic clearance on microbial communities along the gastrointestinal tract in goats challenged with Haemonchus contortus

In this study, we examined the ability of a partial anthelmintic clearance in restoring the altered microbial composition and function in the gut of Haemonchus contortus-infected goats. Our results showed a single-dose treatment with the anthelmintic drug Cydectin restored abomasal pH to the baseline level and resulted in an 83.9% and 61.8% reduction in fecal egg counts (EPG) and worm burden, respectively (P < 0.01). The treatment significantly reduced microbial richness indices, but only in the proximal colon. The anthelmintic increased the abundance of Proteobacteria, particularly that of Campylobacter in the colon. The anthelmintic treatment significantly affected several basic pathways in the midgut and hindgut, including bacterial secretion, butyrate metabolism, and LPS biosynthesis. Several network modules displayed a strong correlation with EPG and worm burden. The Mantel test unraveled a strong correlation between treatment related network topologies of the OTUs belonging to Actinobacteria and Rikenellaceae and EPG and worm burden significance, respectively. The treatment seemingly reduced the cellulolytic capacity in the colon. Furthermore, microbial signatures that can better predict anthelmintic outcomes were identified using a balance-based algorithm. Our findings provided novel insights into intimate interactions between the microbiome and Haemonchus parasite within the caprine gut and potential negative consequence of a partial anthelmintic clearance on animal health and well-being.

本研究探究了部分驱虫疗法对捻转血矛线虫（Haemonchus contortus）感染山羊肠道菌群组成与功能异常的修复作用。结果显示，单次使用驱虫药Cydectin可将皱胃pH恢复至基线水平，并分别使粪便虫卵计数（EPG）与虫荷降低83.9%和61.8%（P < 0.01）。该治疗可显著降低菌群丰富度指数，但该效应仅见于近端结肠。驱虫治疗可提升变形菌门（Proteobacteria）的相对丰度，尤其是结肠内的弯曲杆菌属（Campylobacter）。该驱虫方案显著影响了中肠与后肠内的多条基础代谢通路，包括细菌分泌系统、丁酸代谢与脂多糖（LPS）生物合成。多个菌群网络模块与EPG及虫荷呈现显著相关性。曼特尔检验（Mantel test）结果显示，隶属于放线菌门（Actinobacteria）与理研菌科（Rikenellaceae）的操作分类单元（OTUs）的治疗相关网络拓扑结构，分别与EPG及虫荷的显著性水平呈现强相关性。该治疗似乎降低了结肠内的纤维素分解能力。此外，本研究通过基于平衡的算法筛选出了可更精准预测驱虫治疗效果的菌群标志物。本研究结果为山羊肠道内菌群与捻转血矛线虫的紧密互作关系提供了全新见解，同时揭示了部分驱虫疗法对动物健康与福祉的潜在负面影响。