Modulation of Gilthead Sea Bream Gut Microbiota by a Bioactive Egg White Hydrolysate: Interactions Between Bacteria and Host Lipid Metabolism

Abstract

This study aimed to highlight the relationship between diet, animal performance and mucosal adherent gut microbiota (anterior intestine) in fish fed plant-based diets supplemented with an egg white hydrolysate (EWH) with antioxidant and anti-obesogenic activity in obese rats. The feeding trial with juveniles of gilthead sea bream (Sparus aurata) lasted 8 weeks. Fish were fed near to visual satiety with a fish meal (FM)/fish oil (FO) based diet (CTRL) or a plant-based diet with/without EWH supplementation. Specific growth rate decreased gradually from 2.16% in CTRL fish to 1.88% in EWH fish due to a reduced feed intake, and a slight impairment of feed conversion ratio. Plant-based diets feeding triggered a hyperplasic inflammation of the anterior intestine regardless of EWH supplementation. However, EWH ameliorated the goblet cell depletion, and the hepatic and intestinal lipid accumulation induced by FM/FO replacement. Illumina sequencing of gut mucosal microbiota yielded a mean of 136,252 reads per sample assigned to 2,117 OTUs at 97% identity threshold. The bacterial diversity was similar in all groups, but a significantly lower richness was found in EWH fish. At the phylum level, Proteobacteria reached the highest proportion in CTRL and EWH fish, whereas Firmicutes were decreased and Actinobacteria increased with the FM/FO replacement. The proportion of Actinobacteria was restored by dietary EWH supplementation, which also triggered a highest amount of Bacteroidetes and Spirochaetes. At a closer look, a widespread presence of Lactobacillales among groups was found. Otherwise, polysaccharide hydrolases secretors represented by Corynebacterium and Nocardioides were increased by the FM/FO replacement, whereas the mucin-degrading Streptococcus was only raised in fish fed the plant-based diet without EWH. In addition, in EWH fish, a higher abundance of Propionibacterium was related to an increased concentration of intestinal propionate. The antagonism of gut health-promoting propionate with cholesterol could explain the inferred underrepresentation of primary bile acid biosynthesis and steroid degradation pathways in the EWH fish microbiota. Altogether, these results reinforce the central role of gut microbiota in the regulation of host metabolism and lipid metabolism in particular, suggesting a role of the bioactive EWH peptides as an anti-obesity and/or satiety factor in fish.

Alternative Proteins for Fish Diets: Implications beyond Growth

“…Gilthead seabream that were fed a diet with 5% hydrolysed fish protein for 92 days presented lower gut microbial diversity, with reduced abundances of Alteromonadales and Enterobacteriales, as well as Pseudoalteromonas and Vibrio [100]. In agreement, the same species, when fed a diet with 7.5% egg white hydrolysate in a low fishmeal and fish oil diet for eight weeks, presented reduced growth performance, and this was linked with an increase in Spirochaetes and Bacteroidetes abundance, as well as a reduction in Firmicutes [101]. On the other hand, including 18% tuna hydrolysate in barramundi diets for seven weeks improved survival and intestinal histomorphology, with a marked reduction of Vibrio members and increased abundance of Psychrobacter [102].…”

Diet and Host Genetics Drive the Bacterial and Fungal Intestinal Metatranscriptome of Gilthead Sea Bream

“…Archaeal transcripts were majorly assigned to the Euryarchaeota phylum (Supplementary Figure 1A), one of the most discussed in humans for positively impacting gut health (Horz and Conrads, 2010). In line with their highest abundance in bacterial gut microbiome studies using 16S rRNA (Piazzon et al, 2017(Piazzon et al, , 2019Naya-Català et al, 2021b;Solé-Jiménez et al, 2021), the phyla Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes were also the ones contributing with the most expressed bacterial transcripts when the axonomic assignment was possible (Supplementary Figure 1B). Ascomycota and Basidiomycota play a pivotal role in the expression of enzymes related to fish nutrition and intestinal maturation (Gatesoupe, 2007;Banerjee and Ghosh, 2014;Siriyappagouder et al, 2018), were the most abundant phyla among the fungal fraction (Supplementary Figure 1C).…”

Genetics and Nutrition Drive the Gut Microbiota Succession and Host-Transcriptome Interactions through the Gilthead Sea Bream (Sparus aurata) Production Cycle

“…In fact, only 11 out of 134 OTUs changed at both sampling times, as exemplified for the highly abundant Photobacterium, Reyranella, Brevinema and Streptococcus . In previous studies, these genera were triggered by low FM/FO diets in both gilthead sea bream and rainbow trout [ 2 , 87 ]. For gilthead sea bream in particular, the increase in Streptococcus and Brevinema can be linked to the use of DHA-algae oil as a main FO replacer [ 17 ], which suggests some association of gut bacteria with the source of dietary oil.…”

“…The shortage of traditional marine feedstuffs promotes the use of new aquafeeds based on plant ingredients, insect proteins, animal-by-products, seaweeds and fermented products among other alternative and sustainable feed ingredients [ 1 , 2 , 3 , 4 , 5 ]. Meanwhile, the contribution of aquaculture production to the global aquatic food production volume is continuously increasing [ 6 ], and selective breeding is a widely applied practice to improve the performance and profitability of a wide range of farmed fish to meet the increasing demand of animal proteins for human food consumption [ 7 , 8 ].…”

“…Indeed, both the transient and resident gut microbial communities produce a number of metabolites that impact the host functions not only at the local level, but also at a distant one [ 17 , 18 ]. As part of this complex puzzle, the modulatory effect of the diet on the intestinal microbiota has been extensively documented in some farmed fish, including gilthead sea bream ( Sparus aurata ) [ 2 , 19 ] and European sea bass ( Dicentrarchus labrax ) [ 20 , 21 , 22 ]. The same cannot be said for host genetics, whose influence on the composition and activity of gut microbiota remains less investigated.…”