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Investigation of the Initial Host Response of Naive Atlantic Salmon (Salmo salar) Inoculated with Paramoeba perurans.

ABSTRACT: Amoebic Gill Disease (AGD), caused by the ectoparasite Paramoeba perurans is characterised by hyperplasia of the gill epithelium and lamellar fusion. In this study, the initial host response of naïve Atlantic salmon (Salmo salar) inoculated with P. perurans was investigated. Using gel-free proteomic techniques and mass spectrometry gill and serum samples were analysed at 7 timepoints (2, 3, 4, 7, 9, 11 and 14 days) post-inoculation with P. perurans. Differential expression of immune related proteins was assessed by comparison of protein expression from each time point against naïve controls. Few host immune molecules associated with innate immunity showed increased expression in response to gill colonisation by amoebae. Furthermore, many proteins with roles in immune signalling, phagocytosis and T-cell proliferation were found to be inhibited upon disease progression. Initially, various immune factors demonstrated the anticipated increase in expression in response to infection in the serum while some immune inhibition became apparent at the later stages of disease progression. Taken together, the pro-immune trend observed in serum, the lack of a robust early immune response in the gill and the diversity of those proteins in the gill whose altered expression negatively impact the immune response, support the concept of a pathogen-derived suppression of the host response.

SUBMITTER: McCormack M

PROVIDER: S-EPMC8066739 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Marine farmed Atlantic salmon (Salmo salar) are susceptible to recurrent amoebic gill disease (AGD) caused by the ectoparasite Neoparamoeba perurans over the growout production cycle. The parasite elicits a highly localized response within the gill epithelium resulting in multifocal mucoid patches at the site of parasite attachment. This host-parasite response drives a complex immune reaction, which remains poorly understood. To generate a model for host-parasite interaction during pathogenesis of AGD in Atlantic salmon the local (gill) and systemic transcriptomic response in the host, and the parasite during AGD pathogenesis was explored. A dual RNA-seq approach together with differential gene expression and system-wide statistical analyses of gene and transcription factor networks was employed. A multi-tissue transcriptomic data set was generated from the gill (including both lesioned and non-lesioned tissue), head kidney and spleen tissues naïve and AGD-affected Atlantic salmon sourced from an in vivo AGD challenge trial. Differential gene expression of the salmon host indicates local and systemic upregulation of defense and immune responses. Two transcription factors, znfOZF-like and znf70-like, and their associated gene networks significantly altered with disease state. The majority of genes in these networks are candidates for mediators of the immune response, cellular proliferation and invasion. These include Aurora kinase B-like, rho guanine nucleotide exchange factor 25-like and protein NDNF-like inhibited. Analysis of the N. perurans transcriptome during AGD pathology compared to in vitro cultured N. perurans trophozoites, as a proxy for wild type trophozoites, identified multiple gene candidates for virulence and indicates a potential master regulatory gene system analogous to the two-component PhoP/Q system. Candidate genes identified are associated with invasion of host tissue, evasion of host defense mechanisms and formation of the mucoid lesion. We generated a novel model for host-parasite interaction during AGD pathogenesis through integration of host and parasite functional profiles. Collectively, this dual transcriptomic study provides novel molecular insights into the pathology of AGD and provides alternative theories for future research in a step towards improved management of AGD.

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Investigation of the Initial Host Response of Naive Atlantic Salmon (Salmo salar) Inoculated with Paramoeba perurans.

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