Do ectoparasites on fish gills “talk” with gut microbiota far away?

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.