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. 2022 Nov 28;23(1):775.
doi: 10.1186/s12864-022-09007-4.

Transcriptomic response to ISAV infection in the gills, head kidney and spleen of resistant and susceptible Atlantic salmon

Ophélie Gervais  1 , Athina Papadopoulou  1 , Remi Gratacap  1 , Borghild Hillestad  2 , Alan E Tinch  3   4 , Samuel A M Martin  5 , Ross D Houston  6 , Diego Robledo  7
Affiliations

Transcriptomic response to ISAV infection in the gills, head kidney and spleen of resistant and susceptible Atlantic salmon

Ophélie Gervais et al. BMC Genomics. .

Abstract

Background: Infectious Salmon Anaemia virus (ISAV) is an orthomyxovirus responsible for large losses in Atlantic salmon (Salmo salar) aquaculture. Current available treatments and vaccines are not fully effective, and therefore selective breeding to produce ISAV-resistant strains of Atlantic salmon is a high priority for the industry. Genomic selection and potentially genome editing can be applied to enhance the disease resistance of aquaculture stocks, and both approaches can benefit from increased knowledge on the genomic mechanisms of resistance to ISAV. To improve our understanding of the mechanisms underlying resistance to ISAV in Atlantic salmon we performed a transcriptomic study in ISAV-infected salmon with contrasting levels of resistance to this virus.

Results: Three different tissues (gills, head kidney and spleen) were collected on 12 resistant and 12 susceptible fish at three timepoints (pre-challenge, 7 and 14 days post challenge) and RNA sequenced. The transcriptomes of infected and non-infected fish and of resistant and susceptible fish were compared at each timepoint. The results show that the responses to ISAV are organ-specific; an important response to the infection was observed in the head kidney, with up-regulation of immune processes such as interferon and NLR pathways, while in gills and spleen the response was more moderate. In addition to immune related genes, our results suggest that other processes such as ubiquitination and ribosomal processing are important during early infection with ISAV. Moreover, the comparison between resistant and susceptible fish has also highlighted some interesting genes related to ubiquitination, intracellular transport and the inflammasome.

Conclusions: Atlantic salmon infection by ISAV revealed an organ-specific response, implying differential function during the infection. An immune response was observed in the head kidney in these early timepoints, while gills and spleen showed modest responses in comparison. Comparison between resistance and susceptible samples have highlighted genes of interest for further studies, for instance those related to ubiquitination or the inflammasome.

Keywords: Aquaculture; Disease resistance; Fish; ISAV; RNA-seq; Salmo salar.

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Conflict of interest statement

A commercial organisation (Benchmark Holdings plc) was involved in the development of this study. BH and AET work for Benchmark at the time. The remaining authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Differential gene expression between ISAV-infected and control fish. A Principal Components Analysis showing the clustering of RNA-seq data; B Diverted stacked bar chart showing differentially expressed genes (padj < 0.05) between control and infected samples in gill, head kidney and spleen, with up-regulated genes in red and down-regulated genes in blue; C Venn diagram depicting the number of common and unique genes showing differential expression in each tissue at 7 dpc and D) 14 dpc compared to control
Fig. 2
Fig. 2
Gene expression patterns of common differentially expressed genes. Graph showing the number of normalised counts of common differentially expressed genes in gills, head kidney and spleen at 0, 7 and 14 dpc. Gene expression in each sample is represented with dots, and the distribution of the expression in each group is shown with a boxplot and a half-eye plot. A Peptidyl-prolyl cis-trans isomerase FKBP5-like, B Diencephalon/mesencephalon homeobox protein 1-B, C) Serine protease 23-like, D) Ankyrin repeat domain-containing protein SOWAHC-like
Fig. 3
Fig. 3
Common differentially expressed genes between 7 and 14 dpc in gills. A Venn diagram depicting the number of common and unique genes showing differential expression at 7 and 14 dpc compared to control in gills. B-C Bubblecharts showing enriched gene ontology in up-regulated (B) and down-regulated (C) genes at 7 and 14 days post challenge compared to controls in gills
Fig. 4
Fig. 4
Common differentially expressed genes between 7 and 14 dpc in spleen. A Venn diagram depicting the number of common and unique genes showing differential expression at 7 and 14 dpc compared to control in head kidney. B-C Bubblecharts showing enriched gene ontology in up-regulated (B) and down-regulated (C) genes at 7 and 14 days post challenge compared to controls in head kidney
Fig. 5
Fig. 5
Common differentially expressed genes between 7 and 14 dpc in spleen. A Venn diagram depicting the number of common and unique genes showing differential expression at 7 and 14 dpc compared to control in spleen. B-C Bubblecharts showing enriched gene ontology in up-regulated (B) and down-regulated (C) genes at 7 and 14 days post challenge compared to controls in spleen
Fig. 6
Fig. 6
Heatmap showing the expression patterns of genes differentially expressed between resistant and susceptible fish in the gills at all three timepoints
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