Investigation of the Transcriptomic Response in Atlantic Salmon (Salmo Salar) Gill Exposed to Paramoeba Perurans During Early Onset of Disease

Overview

Journal Sci Rep

Specialty Science

Date 2021 Oct 20

PMID 34667245

Citations 3

Authors

Anita Talbot

Laura Gargan

Grainne Moran

Louis Prudent

Ian OConnor

Luca Mirimin

Jens Carlsson

Eugene MacCarthy

Affiliations

Soon will be listed here.

Abstract

Amoebic Gill Disease (AGD), caused by the protozoan extracellular parasite Paramoeba perurans (P. perurans) is a disease affecting Atlantic salmon (Salmo salar). This study investigated the gill transcriptomic profile of pre-clinical AGD using RNA-sequencing (RNA-seq) technology. RNA-seq libraries generated at 0, 4, 7, 14 and 16 days post infection (dpi) identified 19,251 differentially expressed genes (DEGs) of which 56.2% were up-regulated. DEGs mapped to 224 Gene Ontology (GO) terms including 140 biological processes (BP), 45 cellular components (CC), and 39 molecular functions (MF). A total of 27 reference pathways in the Kyoto Encyclopedia of Genes and Genomes (KEGG) and 15 Reactome gene sets were identified. The RNA-seq data was validated using real-time, quantitative PCR (qPCR). A host immune response though the activation of complement and the acute phase genes was evident at 7 dpi, with a concurrent immune suppression involving cytokine signalling, notably in interleukins, interferon regulatory factors and tumour necrosis factor-alpha (tnf-α) genes. Down-regulated gene expression with involvement in receptor signalling pathways (NOD-like, Toll-like and RIG-1) were also identified. The results of this study support the theory that P. perurans can evade immune surveillance during the initial stages of gill colonisation through interference of signal transduction pathways.

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References

Young N, Cooper G, Nowak B, Koop B, Morrison R . Coordinated down-regulation of the antigen processing machinery in the gills of amoebic gill disease-affected Atlantic salmon (Salmo salar L.). Mol Immunol. 2008; 45(9):2581-97. DOI: 10.1016/j.molimm.2007.12.023. View

Liao Y, Smyth G, Shi W . featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013; 30(7):923-30. DOI: 10.1093/bioinformatics/btt656. View

Benedicenti O, Collins C, Wang T, McCarthy U, Secombes C . Which Th pathway is involved during late stage amoebic gill disease?. Fish Shellfish Immunol. 2015; 46(2):417-25. DOI: 10.1016/j.fsi.2015.07.002. View

Karnovsky A, Weymouth T, Hull T, Tarcea V, Scardoni G, Laudanna C . Metscape 2 bioinformatics tool for the analysis and visualization of metabolomics and gene expression data. Bioinformatics. 2011; 28(3):373-80. PMC: 3268237. DOI: 10.1093/bioinformatics/btr661. View

Goriely S, Neurath M, Goldman M . How microorganisms tip the balance between interleukin-12 family members. Nat Rev Immunol. 2007; 8(1):81-6. DOI: 10.1038/nri2225. View

Kim D, Langmead B, Salzberg S . HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015; 12(4):357-60. PMC: 4655817. DOI: 10.1038/nmeth.3317. View

LaMonte G, Orjuela-Sanchez P, Calla J, Wang L, Li S, Swann J . Dual RNA-seq identifies human mucosal immunity protein Mucin-13 as a hallmark of Plasmodium exoerythrocytic infection. Nat Commun. 2019; 10(1):488. PMC: 6353872. DOI: 10.1038/s41467-019-08349-0. View

Ishigame H, Kakuta S, Nagai T, Kadoki M, Nambu A, Komiyama Y . Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity. 2009; 30(1):108-19. DOI: 10.1016/j.immuni.2008.11.009. View

Pennacchi Y, Leef M, Crosbie P, Nowak B, Bridle A . Evidence of immune and inflammatory processes in the gills of AGD-affected Atlantic salmon, Salmo salar L. Fish Shellfish Immunol. 2014; 36(2):563-70. DOI: 10.1016/j.fsi.2013.12.013. View

10.

Boison S, Gjerde B, Hillestad B, Makvandi-Nejad S, Moghadam H . Genomic and Transcriptomic Analysis of Amoebic Gill Disease Resistance in Atlantic Salmon ( L.). Front Genet. 2019; 10:68. PMC: 6400892. DOI: 10.3389/fgene.2019.00068. View

11.

Yamamoto Y, Gaynor R . IkappaB kinases: key regulators of the NF-kappaB pathway. Trends Biochem Sci. 2004; 29(2):72-9. DOI: 10.1016/j.tibs.2003.12.003. View

12.

Bolger A, Lohse M, Usadel B . Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30(15):2114-20. PMC: 4103590. DOI: 10.1093/bioinformatics/btu170. View

13.

Love M, Huber W, Anders S . Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15(12):550. PMC: 4302049. DOI: 10.1186/s13059-014-0550-8. View

14.

Robledo D, Hamilton A, Gutierrez A, Bron J, Houston R . Characterising the mechanisms underlying genetic resistance to amoebic gill disease in Atlantic salmon using RNA sequencing. BMC Genomics. 2020; 21(1):271. PMC: 7106639. DOI: 10.1186/s12864-020-6694-x. View

15.

Tsai H, Velichko S, Hung L, Wu R . IL-17A and Th17 cells in lung inflammation: an update on the role of Th17 cell differentiation and IL-17R signaling in host defense against infection. Clin Dev Immunol. 2013; 2013:267971. PMC: 3730142. DOI: 10.1155/2013/267971. View

16.

Schurch N, Schofield P, Gierlinski M, Cole C, Sherstnev A, Singh V . How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use?. RNA. 2016; 22(6):839-51. PMC: 4878611. DOI: 10.1261/rna.053959.115. View

17.

Ashburner M, Ball C, Blake J, Botstein D, Butler H, Cherry J . Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000; 25(1):25-9. PMC: 3037419. DOI: 10.1038/75556. View

18.

Lien S, Koop B, Sandve S, Miller J, Kent M, Nome T . The Atlantic salmon genome provides insights into rediploidization. Nature. 2016; 533(7602):200-5. PMC: 8127823. DOI: 10.1038/nature17164. View

19.

Wynne J, OSullivan M, Cook M, Stone G, Nowak B, Lovell D . Transcriptome analyses of amoebic gill disease-affected Atlantic salmon (Salmo salar) tissues reveal localized host gene suppression. Mar Biotechnol (NY). 2008; 10(4):388-403. DOI: 10.1007/s10126-007-9075-4. View

20.

Bridle A, Morrison R, Cupit Cunningham P, Nowak B . Quantitation of immune response gene expression and cellular localisation of interleukin-1beta mRNA in Atlantic salmon, Salmo salar L., affected by amoebic gill disease (AGD). Vet Immunol Immunopathol. 2006; 114(1-2):121-34. DOI: 10.1016/j.vetimm.2006.08.002. View