The ectoparasites Dactylogyrus lamellatus usually infest fish gills and cause severe damage to the gill tissues of the host. However, whether the ectoparasites influence gut microbiota is still unknown. In this study, gut microbiota combined with histopathological characteristics, biochemical parameters, and relative expression of immune-related genes were analyzed in grass carp severely infected (SI), mildly infected (MI) and uninfected (UI) with D. lamellatus. Deep amplicon sequencing of the 16S rRNA gene of the gut microbiota revealed that the diversity of the SI group was significantly reduced than UI group (p < 0.05). In parallel with the increased loads of D. lamellatus, the relative abundance of Cetobacterium increased, and that of Bacteroides decreased. Antioxidant indices of the glutathione peroxidase (GPX) in the infected groups were significantly higher than those in the UI group (p < 0.05). The expression levels of several immune-related genes encoding toll-like receptor 3 (TLR3), myeloid differentiation factor 88 (MyD88), major histocompatibility complex II (MHCII), and immunoglobulin M (IgM) were relatively increased the degree of infection in grass carp tissues. Meanwhile, the histopathological characteristics show a large number of immune cells infiltrated in the mucosal and submucosal layers in intestine. It indicates that D. lamellatus infection stimulated both the innate and adaptive immune responses. Our data demonstrated that ectoparasites D. lamellatus infection on the gills resulted in a gut microbiota shift, histopathological changes, and immune responses in the grass carp. Furthermore, ectoparasite- microbiota- host interactions indicate that fish ectoparasites probably have remote “talk” mechanisms with host intestinal microbes. This is the first study of ectoparasites on fish gills affecting the gut microbiota in grass carp from far distance away, which is beneficial for understanding the relationships between parasites, gut microbiota, and host and for the control of parasitic diseases in fish.

外寄生虫Dactylogyrus lamellatus通常侵染鱼鳃并对宿主的鳃组织造成严重损害。然而，外寄生虫是否会影响肠道微生物群仍是未知数。在这项研究中，结合D. lamellatus严重感染 (SI)、轻度感染 (MI) 和未感染 (UI) 的草鱼，分析了肠道微生物群以及组织病理学特征、生化参数和免疫相关基因的相对表达。肠道菌群16S rRNA基因的深度扩增子测序显示，SI组的多样性显着低于UI组（p  < 0.05）。随着D. lamellatus负荷的增加， Cetobacterium的相对丰度增加，而拟杆菌减少。感染组谷胱甘肽过氧化物酶（GPX）抗氧化指数显着高于UI组（p  < 0.05）。编码toll样受体3（TLR3）、髓细胞分化因子88（MyD88）、主要组织相容性复合物II（MHCII）和免疫球蛋白M（IgM）的几种免疫相关基因的表达水平相对升高，草的感染程度鲤鱼组织。同时，组织病理学特征显示大量免疫细胞浸润于肠道黏膜和黏膜下层。这表明D. lamellatus感染刺激了先天性和适应性免疫反应。我们的数据表明，鳃上的外寄生虫D. lamellatus感染导致草鱼的肠道微生物群变化、组织病理学变化和免疫反应。此外，外寄生虫-微生物-宿主相互作用表明，鱼类外寄生虫可能与宿主肠道微生物具有远程“对话”机制。这是首次从远距离对鱼鳃外寄生虫影响草鱼肠道菌群的研究，有助于了解寄生虫、肠道菌群与宿主之间的关系，以及控制鱼类寄生虫病。