Dietary Lipid:Protein Ratio and n-3 Long-Chain Polyunsaturated Fatty Acids Alters the Gut Microbiome of Atlantic Salmon Under Hypoxic and Normoxic Conditions

Abstract

Researchers have adjusted dietary lipid:protein ratios and n-3 long-chain polyunsaturated fatty acids (LC-PUFA) to optimize the growth performance of Atlantic salmon. However, dietary impacts on the gut microbiome are lacking, especially under varying environmental conditions. To examine this response, post-smolt salmon (184 ± 5 g) were fed diets with lipid:protein ratios considered low (180, 570 g/kg) and high (230, 460 g/kg) along with low and high levels of n-3 LC-PUFA (7 or 14 g/kg) while fish were reared under low and high levels of dissolved oxygen (6.7 or 8.0 mg/L). At day 0, 35 and 116, digesta in the distal intestine were collected and analyzed for viable counts and 16S ribosomal RNA (rRNA) genes (V4 region) using Illumina MiSeq. The reduction in oxygen had negligible effects, except on viable plate counts of total bacteria and an initial effect on beta-diversity. In contrast, the high lipid (HL) diets had an increased alpha-diversity (e.g., Shannon and Chao-1) at day 0 and day 35 whereas high n-3 diets suppressed these indices at day 116. Generally, a reduction in alpha-diversity was observed over time and an interaction between lipid:protein ratio x n-3 was found. Between diets, beta-diversity and phyla abundance were similar as both Proteobacteria (44%) and Firmicutes (21%) dominated. However, at the genus level Aliivibrio, Streptococcus, Weissella, and Lactobacillus, were associated with low lipid (LL) diets while the high lipid diets were associated with less abundant bacteria, e.g., Chromohalobacter. At day 116, the relative abundance of the Tenericutes phylum increased 10-fold (36%). Fish fed the high lipid diet with high n-3 had reduced alpha-diversity, lowest abundance of lactic acid bacteria, and highest abundance of Mycoplasma, which may indicate a less healthy gut microbiome. Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) analysis revealed that saturated and unsaturated fatty acid biosynthesis pathways were several folds higher in fish fed the high lipid diet, possibly to compensate for the lack of dietary n-3. In summary, our results show that the viable plate counts, alpha-diversity, beta-diversity, and predictive function of gut bacteria in Atlantic salmon post-smolts are influenced by dietary lipid:protein ratio and n-3 LC-PUFA over several time points with little effect by dissolved oxygen.

Modulation of Atlantic salmon (Salmo salar) gut microbiota composition and predicted metabolic capacity by feeding diets with processed black soldier fly (Hermetia illucens) larvae meals and fractions

“…The lipid fraction of BSF larvae was rich with medium chain lauric acid (40% of total FAs), and contained negligible level of long-chain polyunsaturated omega-3 FAs (Additional file 2 : Table S2). This FA composition of BSF can also be responsible partially for increased LAB abundance as shown by Rimoldi et al [ 80 ] and Huyben et al [ 88 ], although the insect oil diet did not enrich LAB in the present study. Fish fed de-chitinized meal showed the highest abundance of Corynebacterium in gut microbiota as observed in rainbow trout fed BSF larvae or pre-pupae meal [ 27 , 29 ].…”

“…The predicted enrichment of FA synthesis in fish fed BSF lipid-rich de-chitinized meal and oil can mostly be due to the lack of omega-3 FAs in lipid fraction of BSF larvae (Additional file 2 : Table S2). Gut microbiota can compensate for low levels of omega-3 FAs in the diet by increasing the abundance of FA producing bacteria [ 88 ]. In agreement with this, Huyben et al [ 88 ] showed that low omega-3 FAs in a diet containing 23% lipid led to a predicted increase in microbial FA synthesis in salmon.…”

“…Gut microbiota can compensate for low levels of omega-3 FAs in the diet by increasing the abundance of FA producing bacteria [ 88 ]. In agreement with this, Huyben et al [ 88 ] showed that low omega-3 FAs in a diet containing 23% lipid led to a predicted increase in microbial FA synthesis in salmon. In contrast, the full-fat meal diet did not give a predicted increase in microbial FA synthesis although this diet contained similar BSF lipid content as BSF oil diet.…”

Hypoxia does not change responses to dietary omega‐3 long‐chain polyunsaturated fatty acids, but rather reduces dietary energy demand by Atlantic salmon

“…Rainbow trout have been found to have an increased preference and intake of diets with higher n-3 LC-PUFA (Roy et al, 2020), which may have occurred in the present study due to tendency for higher intake when fed both high n-3 and lipid diets (Table 4). In a parallel study, hypoxia had only minor effects on the gut microbiome, while high lipid and high n-3 LC-PUFA diets significantly influenced bacterial diversity and composition (Huyben et al, 2020).…”

Effects of a Bioprocessed Soybean Meal Ingredient on the Intestinal Microbiota of Hybrid Striped Bass, Morone chrysops x M. saxatilis

“…Considering the importance of the hybrid striped bass in the aquaculture industry, the composition of its gut microbiome in healthy individuals has remained mostly unexplored. Indeed, in contrast to salmon [21][22][23][24][25], trout [26][27][28][29][30][31][32], and catfish [33][34][35][36][37][38], no published studies are currently available on hybrid striped bass or its parental strains using DNA sequencing-based methods; culture-independent approaches using high throughput Next-Generation sequencing platforms have been established as the gold standard for the analysis of microbiomes. Using a culturing approach, Aeromonas hydrophila was identified as a dominant species in the gut of striped bass [39][40][41][42] and hybrid striped bass [43].…”