Gut health and microbiota in post-smolt Atlantic salmon (Salmo salar) fed larvae meal from black soldier fly (Hermetia illucens)

Introduction \nIn salmon aquaculture, the limited availability of sustainable feed ingredients is a major obstacle. Insects, being part of the \nnatural diet of salmonids, may become a sustainable resource and expand the raw material repertoire. In the “AquaFly” \nproject, the potential of black soldier fly (Hermetia illucens) grown on low-quality organic matter as a source of sustainable \nfeed ingredients for Atlantic salmon (Salmo salar) was assessed in one freshwater and one seawater feeding trial. Herein, \nwe summarize data from the 16-week seawater feeding trial with salmon (initial body weight, 1.4kg) fed either a reference \ndiet (REF) with a combination of fish meal, soy protein concentrate, pea protein concentrate, corn gluten and wheat gluten \nas protein source, or a test diet (IM) wherein all the fish meal and most of the pea protein concentrate were replaced by \nblack soldier fly larvae meal \nMaterials and methods \nThe gut health of fish was evaluated using endpoints including organ and tissue indices, digestive enzyme activity, \nhistopathological parameters and gene expression. In total, 36 genes under different functional categories were profiled \nvia qPCR, including those indicative of lipid metabolism, immune responses, barrier functions and detoxification/stress \nresponses. Microbiota in the distal intestine, both gut contents and mucosa associated, was analyzed via 16S rRNA gene \nsequencing. \nResults \n1. Histology. Hypervacuolization of enterocytes, suggestive of lipid accumulation, was observed in the proximal and mid \nintestine in both diet groups. It was, however, less severe in the proximal intestine of fish fed the insect meal diet (p < 0.05). \nTypical signs of enteritis commonly observed in salmonid intestine fed soybean meal diets were present in all the intestinal \nsegments in both diet groups. A higher degree of submucosa cellularity was observed in the proximal intestine of fish fed \nthe insect meal diet (p < 0.05). \n2. Gene expression. Of the 36 genes profiled in the proximal and distal intestine, a few genes showed differential expressions. \nThe only genes showing differential expressions were mmp13 (matrix metalloproteinase 13) and chk (choline kinase), \nwhose expression level was significantly lower in the proximal and distal intestine, respectively, in fish fed the insect meal \ndiet (p < 0.05). \n3. Gut microbiota. Both diet and sample origin (gut contents vs mucosa) affected microbiota in the distal intestine. All the \nmeasured alpha-diversity indices, including observed OTUs, Shannon index, Pielou’s evenness and Faith’s phylogenetic \ndistance, showed higher values in samples exposed to insect meal diet or originated from gut contents (p < 0.05). For the \nbeta-diversity, samples formed 4 distinctive clusters in the PCoA plot separated by the diet and sample origin (Fig.1), \nconfirmed by permutational multivariate analysis of variance (PERMANOVA, p < 0.05). The diet showed a more profound \neffect on the samples originated from gut contents than those from mucosa. \nDiscussion and conclusion \nIn the present study, total replacement of fish meal with black soldier fly larvae meal showed no appreciable negative \neffects on the gut health and function of Atlantic salmon. In line with what we reported in the freshwater trial (Li et al., \n2019), insect meal inclusion was associated with a lower degree of enterocyte hypervacuolization in the proximal intestine, \nwhich is suggestive of lower lipid accumulation. In the context of frequent occurrence of steatosis found in the proximal \nintestine of farmed salmon in field surveys (Chikwati et al., 2018), the potential beneficial effect of insect meal inclusion \non reducing lipid deposition in the gut deserves further attention. In contrast to the previous finding in the freshwater trial \nthat insect meal diet increased the expression of foxp3 (Li et al., 2019), a transcription factor for the differentiation of naïve \nCD4 T-cells into regulatory T cells, no such effect was observed in the seawater trial. On the other hand, the present study \nshowed increased submucosa cellularity in the proximal intestine. The effect of insect meal inclusion on the gut immune \nresponse is also worth of attention in future studies. \nReference \nChikwati, E.M., Midtlyng, P.J., Krogdahl, Å., 2018. Gut health monitoring during the seawater phase of farmed Atlantic \nsalmon in different production regions of Norway – The Gutmatters Project, 8th International Symposium on Aquatic \nAnimal Health, Charlottetown, Prince Edward Island, Canada, pp. 400. \nLi, Y., Kortner, T.M., Chikwati, E.M., Munang’andu, H.M., Lock, E.-J., Krogdahl, Å., 2019. Gut health and vaccination \nresponse in pre-smolt Atlantic salmon (Salmo salar) fed black soldier fly (Hermetia illucens) larvae meal. Fish & \nShellfish Immunology, 86, 1106-1113.

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