Characterising the mechanisms underlying genetic resistance to amoebic gill disease in Atlantic salmon using RNA sequencing

Abstract

<jats:title>ABSTRACT</jats:title><jats:sec><jats:title>Background</jats:title><jats:p>Gill health is one of the main concerns for Atlantic salmon aquaculture, and Amoebic Gill Disease (AGD), attributable to infection by the amoeba <jats:italic>Neoparamoeba perurans</jats:italic>, is a frequent cause of morbidity. In the absence of preventive measures, increasing genetic resistance of salmon to AGD via selective breeding can reduce the incidence of the disease and mitigate gill damage. Understanding the mechanisms leading to AGD resistance and the underlying causative genomic features can aid in this effort, while also providing critical information for the development of other control strategies. AGD resistance is considered to be moderately heritable, and several putative QTL have been identified. The aim of the current study was to improve understanding of the mechanisms underlying AGD resistance, and to identify putative causative genomic factors underlying the QTL. To achieve this, RNA was extracted from the gill and head kidney of AGD resistant and susceptible animals following a challenge with <jats:italic>N</jats:italic>. <jats:italic>perurans</jats:italic>, and sequenced.</jats:p></jats:sec><jats:sec><jats:title>Results</jats:title><jats:p>Comparison between resistant and susceptible animals pointed to differences mainly in the local immune response in the gill, involving red blood cell genes and genes related to immune function and cell adhesion. Differentially expressed immune genes highlighted differences in the Th2 and Th17 responses, which are consistent with the increased heritability observed after successive challenges with the amoeba. Five QTL-region candidate genes showed differential expression, including a gene connected to interferon responses (<jats:italic>GVINP1</jats:italic>), a gene involved in systemic inflammation (<jats:italic>MAP4K4</jats:italic>), and a positive regulator of apoptosis (<jats:italic>TRIM39</jats:italic>). Analyses of allele-specific expression highlighted a gene in the QTL region on chromosome 17, cellular repressor of E1A-stimulated genes 1 (<jats:italic>CREG1</jats:italic>), showing allelic differential expression suggestive of a cis-acting regulatory variant.</jats:p></jats:sec><jats:sec><jats:title>Conclusions</jats:title><jats:p>In summary, this study provides new insights into the mechanisms of resistance to AGD in Atlantic salmon, and highlights candidate genes for further functional studies that can further elucidate the genomic mechanisms leading to resistance and contribute to enhancing salmon health via improved genomic selection.</jats:p></jats:sec>

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

“…Farming in net pens is typically associated with the multifactorial gill diseases (PGD, PGI or CGD) rather than the single-cause gill pathologies, such as AGD (Herrero et al, 2018;Gjessing et al, 2019;Laurin et al, 2019). So far, the extensive transcriptomic profiling of the gill tissue has been performed only in salmon exposed to the controlled environment of the closed-system tanks, following a single-pathogen challenge to induce either AGD (Morrison et al, 2006;Wynne et al, 2008a;Bloecher et al, 2018;Boison et al, 2019;Robledo et al, 2019) or infectious salmon anemia (Valenzuela-Miranda et al, 2015). In most cases, fish were subjected to a single-dose challenge of the infectious organisms, with only few studies evaluating the effects of re-infection (Bloecher et al, 2018;Boison et al, 2019) or co-exposure to other infectious agents, such as hydroids (Bloecher et al, 2018) and Yersinia ruckeri (Valdenegro-Vega et al, 2015).…”

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

“…Therefore, the significance of the complement cascade in the host response to AGD remains unclear. However, a recent genome mapping study implicated the C4 gene as one of three genes involved in disease resistance in AGD [ 49 ], and genetic screening of susceptible versus resistant fish also demonstrated an upregulation of plasma protease C1 inhibitor in resistant gill samples [ 50 ]. Kube et al also demonstrated that resistance after one P. perurans infection was attributable to an innate response, in contrast to resistance after multiple infections [ 8 ].…”

Genetic improvement technologies to support the sustainable growth of UK aquaculture

“…2019) and AGD (Robledo et al . 2020) have also successfully produced genome‐wide SNP chips suitable for research (Houston et al . 2014; Lien et al .…”

“…At the moment, genomic selection is the state of the art for salmon breeding (Table 3). Marker-assisted selection and genome-wide marker SNP array platforms have been used to improve salmon stock across several phenotypes (Zenger et al 2018) including disease resistance (Gonen et al 2015;Robledo et al 2016;Robledo et al 2019;Silva et al 2019;Rodr ıguez et al 2019;Robledo et al 2020), body size and weight (Reid et al 2005;Baranski et al 2010;Gutierrez et al 2012;Tsai et al 2015), but also delaying sexual maturation which can improve growth and meat quality (Pedersen et al 2013;Gutierrez et al 2014;Ayllon et al 2015;Barson et al 2015). As domestication of farmed Atlantic salmon progresses, genomic tools may also be used to assess impacts of the domestication process, examining the genetic basis for changes in growth, morphology, behaviour and physiology (Glover et al 2017;L opez et al 2019).…”

“…It is often the case that breeding research begins via such academic and industry collaborations, before being translated to widespread industry application when it becomes cost-effective. Research projects targeting resistance to the two biggest pathogenic threats to the UK salmon industry at present, sea lice (Tsai et al 2016;Robledo et al 2019) and AGD (Robledo et al 2020) have also successfully produced genome-wide SNP chips suitable for research (Houston et al 2014;Lien et al 2016). Subsequently, several SNP chips have also been developed and widely applied for industry implementation.…”