Cross-Talk Between Intestinal Microbiota and Host Gene Expression in Gilthead Sea Bream (Sparus aurata) Juveniles: Insights in Fish Feeds for Increased Circularity and Resource Utilization

Abstract

New types of fish feed based on processed animal proteins (PAPs), insect meal, yeast, and microbial biomasses have been used with success in gilthead sea bream. However, some drawback effects on feed conversion and inflammatory systemic markers were reported in different degrees with PAP- and non-PAP-based feed formulations. Here, we focused on the effects of control and two experimental diets on gut mucosal-adherent microbiota, and how it correlated with host transcriptomics at the local (intestine) and systemic (liver and head kidney) levels. The use of tissue-specific PCR-arrays of 93 genes in total rendered 13, 12, and 9 differentially expressed (DE) genes in the intestine, liver, and head kidney, respectively. Illumina sequencing of gut microbiota yielded a mean of 125,350 reads per sample, assigned to 1,281 operational taxonomic unit (OTUs). Bacterial richness and alpha diversity were lower in fish fed with the PAP diet, and discriminant analysis displayed 135 OTUs driving the separation between groups with 43 taxa correlating with 27 DE genes. The highest expression of intestinal pcna and alpi was achieved in PAP fish with intermediate values in non-PAP, being the pro-inflammatory action of alpi associated with the presence of Psychrobacter piscatorii. The intestinal muc13 gene was down-regulated in non-PAP fish, with this gene being negatively correlated with anaerobic (Chloroflexi and Anoxybacillus) and metal-reducing (Pelosinus and Psychrosinus) bacteria. Other inflammatory markers (igm, il8, tnfα) were up-regulated in PAP fish, positively correlating the intestinal igm gene with the inflammasome activator Escherichia/Shigella, whereas the systemic expression of il8 and tnfα was negatively correlated with the Bacilli class in PAP fish and positively correlated with Paracoccus yeei in non-PAP fish. Overall changes in the expression pattern of il10, galectins (lgals1, lgals8), and toll-like receptors (tlr2, tlr5, tlr9) reinforced the anti-inflammatory profile of fish fed with the non-PAP diet, with these gene markers being associated with a wide range of OTUs. A gut microbiota-liver axis was also established, linking the microbial generation of short chain fatty acids with the fueling of scd1- and elovl6-mediated lipogenesis. In summary, by correlating the microbiome with host gene expression, we offer new insights in the evaluation of fish diets promoting gut and metabolism homeostasis, and ultimately, the health of farmed fish.

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

“…Like in other animals, the gut microbiome of fish contains thousands of microbial species that establish a complex network of relationships among each other and with the host [ 14 , 15 , 16 ]. 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 ].…”

Revising the Impact and Prospects of Activity and Ventilation Rate Bio-Loggers for Tracking Welfare and Fish-Environment Interactions in Salmonids and Mediterranean Farmed Fish

“…In that sense, behavior changes related to the acceptance of new feed formulations and changing environmental conditions can be mimicked and tested at laboratory scale for merging genetics, nutrition, health and environmental science into a single transdisciplinary and fundamental knowledge system, supporting the future and viable growth of aquaculture. All this will serve to ensure the use of behavior monitoring as a reliable and routine approach to evaluate new fish feed formulations, largely based on sustainability and circular economy principles (Aragão et al, 2020;Naya-Català et al, 2021a).…”

“…This feature would add a predictive value to AEFishBIT records, which becomes especially interesting for driving selective breeding toward tailored productive traits. Finally, major efforts for the integration of complex data informing of the host response to nutritional inputs and genetics and microbiota interactions have been accomplished recently in farmed fish and gilthead sea bream in particular (Piazzon et al, 2017(Piazzon et al, , 2019(Piazzon et al, , 2020Naya-Català et al, 2021a;Solé-Jiménez et al, 2021), but how this also affects to behavioral traits remains mostly unknown. Altogether, this opens new research opportunities for incorporating measurements of organism behavior as a routine procedure of academia researchers as well as fish farmers, and fish feed producers and breeders.…”

Effects of dietary plant and animal protein sources and replacement levels on growth and feed performance and nutritional status of market-sized turbot (Scophthalmus maximus) in RAS

“…Our approach within the GAIN2020 project (EU H2020 grant no. 773330) was to develop alternative feed formulation concepts for a range of European aquaculture species such as salmon, trout (Maiolo et al, 2021), sea bream (Naya-Català et al, 2021), sea bass (Petereit et al, 2022a) and turbot (Hoerterer et al, 2022b) based on various proteins sourced through circular economy tapping by-products and side-streams from food production sectors.…”