Differential immune gene response in gills, skin, and spleen of rainbow trout Oncorhynchus mykiss infected by Ichthyophthirius multifiliis

Abstract

Infection of rainbow trout with the parasitic ciliate Ichthyopthirius multifiliis induces differential responses in gills, skin and spleen. A controlled experimental infection was performed and expression of immune-relevant genes in skin, gills, and spleen were recorded by qPCR at day 1 and 8 after parasite exposure. Infection induced a marked reaction involving regulation of innate and adaptive immune genes in rainbow trout at day 8 post-infection. The expression level of a total of 22 out of 24 investigated genes was significantly higher in gills compared to skin reflecting the more sensitive and delicate structure of gills. Especially pro-inflammatory cytokines IL-6, IL-17 C1, regulatory cytokines IL-4/13A, IL-10, TGFβ, complement factor C5, chemokines CK10, CK12, acute phase proteins (precerebellin, hepcidin) and immunoglobulins (IgM, IgT) displayed differential expression levels. The spleen, a central immune organ with no trace of the parasite, showed elevated expression of IgM, IgT, complement factor C5 and chemokine CK10 (compared to skin and gills directly exposed to the parasite), indicating an interaction between the infected surface sites and central immune organs. This communication could be mediated by chemokines CK10 and CK12 and cytokine IL-4/13A and may at least partly explain the establishment of a systemic response in rainbow trout against the parasite.

Integration of Transcriptome, Gross Morphology and Histopathology in the Gill of Sea Farmed Atlantic Salmon (Salmo salar): Lessons From Multi-Site Sampling

“…The proteins encoded by IL17 family genes have been shown to stimulate the production of several other cytokines, including IL6 and IL8 in splenocytes of rainbow trout using recombinant IL17A/F2a (Monte et al, 2013) as well as IL1β, IL6, IL8 and TNF-α in head kidney leukocytes of grass carp using recombinant IL17A/F1 (Du et al, 2015). Furthermore, the emerging role of IL17 cytokines in gill mucosal immunity is supported by reports showing differential expression of these genes following the exposure to Aeromonas hydrophila in common carp (Dong et al, 2019) and after challenge with Ichthyophthirius multifiliis in rainbow trout (Syahputra et al, 2019). According to our BLASTX results, CXCL9 represents salmon IL8, whose high expression in our data set (Log 2 FC = 3.4, Supplementary Table 7) is consistent with upregulation of IL17F (Zou and Secombes, 2016).…”

Antimicrobial Peptides of Salmonid Fish: From Form to Function

“…Infection of rainbow trout with the skin ciliate parasite, Ichthyophthirius multifiliis ( I. multifiliis ), resulted in a significant upregulation of hepc mRNA 8 days post-infection in the skin and gill, but was downregulated in the spleen [ 75 ]. Vaccination of rainbow trout against I. multifiliis , using DNA vaccines encoding plasmids for I. multifiliis antigens, resulted in increased expression of hepc mRNA in the liver of vaccinated fish; however, vaccination did not lead to significant protection against I. multifiliis [ 76 ].…”

Zebrafish as a Model for Fish Diseases in Aquaculture

“…From 2016, several studies have described the immune response of zebrafish against I. multifiliis and it was documented that zebrafish were susceptible towards the parasite and were able to acquire immunological immunity [51]. Subsequently, regulation of immune-relevant genes was investigated and the main findings included an upregulation of the Th2-associated genes il4/13 and ighm in immune fish and il4/13 and Saa in naïve fish [52,140], which similarly have been observed in fish species used in production [31,32,141,142]. The transgenic line of zebrafish expressing GFP in connection with neutrophils has also been exploited to investigate the cellular responses against the parasite as well as host/parasite dynamics [100].…”