Functional Genomic Analysis of the Impact of Camelina (Camelina sativa) Meal on Atlantic Salmon (Salmo salar) Distal Intestine Gene Expression and Physiology

Abstract

The inclusion of plant meals in diets of farmed Atlantic salmon can elicit inflammatory responses in the distal intestine (DI). For the present work, fish were fed a standard fish meal (FM) diet or a diet with partial replacement of FM with solvent-extracted camelina meal (CM) (8, 16, or 24 % CM inclusion) during a 16-week feeding trial. A significant decrease in growth performance was seen in fish fed all CM inclusion diets (Hixson et al. in Aquacult Nutr 22:615–630, 2016). A 4x44K oligonucleotide microarray experiment was carried out and significance analysis of microarrays (SAM) and rank products (RP) methods were used to identify differentially expressed genes between the DIs of fish fed the 24 % CM diet and those fed the FM diet. Twelve features representing six known transcripts and two unknowns were identified as CM responsive by both SAM and RP. The six known transcripts (including thioredoxin and ependymin), in addition to tgfb, mmp13, and GILT, were studied using qPCR with RNA templates from all four experimental diet groups. All six microarray-identified genes were confirmed to be CM responsive, as was tgfb and mmp13. Histopathological analyses identified signs of inflammation in the DI of salmon fed CM-containing diets, including lamina propria and sub-epithelial mucosa thickening, infiltration of eosinophilic granule cells, increased goblet cells and decreased enterocyte vacuolization. All of these were significantly altered in 24 % CM compared to all other diets, with the latter two also altered in 16 % CM compared with 8 % CM and control diet groups. Significant correlation was seen between histological parameters as well as between five of the qPCR analyzed genes and histological parameters. These molecular biomarkers of inflammation arising from long-term dietary CM exposure will be useful in the development of CM-containing diets that do not have deleterious effects on salmon growth or physiology.Electronic supplementary materialThe online version of this article (doi:10.1007/s10126-016-9704-x) contains supplementary material, which is available to authorized users.

High‐oil residue camelina meal, a viable source of protein at low levels in diets for juvenile salmonids

“…At high levels from 80 to 240 g/kg SECM and HORM, these changes were pronounced in the gut, but in the present study, only the submucosal layer thickening was significant for salmon. Based on the results in the present study, we conclude that histopathology of the hindgut is generally unaffected by 60 g/kg HORM in rainbow trout and salmon; however, based on previous studies with salmon and SECM, >80 g/kg appears to be detrimental to salmon postsmolts (Brown et al, 2016).…”

“…In rainbow trout, there was a slight non‐significant increase in the number of goblet cells, which could have become biologically significant if the feeding period was longer than 12 weeks. The increased number of goblet cells (number of goblet cells per square millimetre) and thickening of the submucosa layer were also observed in salmon (postsmolts, ~230 g/fish initial weight) fed 160 and 240 g/kg SECM and HORM for 16 weeks, which was attributed to a protective response to a food antigen and to the inflammation in the gut (Brown et al, ). These histological parameters were also significantly correlated with qPCR analysed genes which were markers of inflammation (Brown et al, ).…”

“…The increased number of goblet cells (number of goblet cells per square millimetre) and thickening of the submucosa layer were also observed in salmon (postsmolts, ~230 g/fish initial weight) fed 160 and 240 g/kg SECM and HORM for 16 weeks, which was attributed to a protective response to a food antigen and to the inflammation in the gut (Brown et al, ). These histological parameters were also significantly correlated with qPCR analysed genes which were markers of inflammation (Brown et al, ). At high levels from 80 to 240 g/kg SECM and HORM, these changes were pronounced in the gut, but in the present study, only the submucosal layer thickening was significant for salmon.…”

De novo assembly of Sockeye salmon kidney transcriptomes reveal a limited early response to piscine reovirus with or without infectious hematopoietic necrosis virus superinfection

“…We also identified this gene to be the only qPCR-validated differentially expressed protein coding gene responsive to early PRV infection in head kidney tissues. Interestingly, Epd expression has also been shown to be upregulated in the liver of Atlantic salmon following exposure to the bacterial pathogen Aeromonas salmonicida [54], in the liver of medaka ( Oryzias latipes ) exposed to dioxin [55], and in the distal intestine of Atlantic salmon fed camelina-derived feeds [56]; suggesting the transcriptional regulation of Epn may be involved in immunological, inflammatory, or cellular repair responses. However, as neither immunological, inflammatory, cellular repair, nor indeed any other transcriptional pathway appeared to correspond to Epn expression in this study its biological role in response to PRV appears limited.…”

Assessing Diversity in theCamelinaGenus Provides Insights into the Genome Structure ofCamelina sativa

“…More recently it has shown potential to become a low-input high value oil crop for the food and feed industry (Faure and Tepfer 2016). Several advantages of this species have been reported (Brown et al 2016;Ye et al 2016) including the ability to yield well on dry and marginal lands and its unique seed quality traits (Gugel and Falk 2006), particularly its balanced omega fatty acids (Simopoulos 2002). However, improvements can be made to the crop such as increasing seed size for improved harvestability and reducing the glucosinolate content, which is an anti-nutritional in animal feed (Schuster and Friedt 1998;Amyot et al 2018).…”