Dactylogyrus intermedius parasitism enhances Flavobacterium columnare invasion and alters immune-related gene expression in Carassius auratus

The monogenean Dactylogyrus intermedius and the bacterium Flavobacterium columnare are 2 common pathogens in aquaculture. The objective of the present study was to examine the effect of prior parasitism by D. intermedius on the susceptibility of goldfish to F. columnare and to explore the potential immune mechanisms related to the parasite infection. A F. columnare challenge trial was conducted between D. intermedius-parasitized and non-parasitized goldfish. The F. columnare load in gill, kidney, spleen and liver were compared. The expression of immune-related genes (IL-1 beta 2, TNF-alpha 1, TGF-beta, iNOS-a, C3 and Lyz) in gill and kidney of D. intermedius-only infected and uninfected control fish were evaluated. D. intermedius- parasitized goldfish exhibited higher mortality and significantly higher loads (3051 to 537379 genome equivalents [GEs] mg(-1)) of F. columnare, which were 1.13 to 50.82-fold higher than non-parasitized fish (389 to 17829 GEs mg-1). Furthermore, the immune genes IL-1 beta 2, TNF alpha 1, iNOS-a and Lyz were up-regulated while the TGF-beta and C3 were down-regulated in the gill and kidney of parasite-infected fish compared to the non-parasitized controls. The down-regulation TGF-beta and C3 was especially noteworthy, as this might indicate the suppression of the host immune functions due to the parasitism by D. intermedius. Taken together, these data demonstrate that parasite infection can enhance bacterial invasion and presents a hypothesis, based on gene expression data, that modulation of host immune response could play a role.