Reshaping of Gut Microbiota in Gilthead Sea Bream Fed Microbial and Processed Animal Proteins as the Main Dietary Protein Source

Paula Solé-Jiménez,Danny Van Mullem,Fernando Naya-Català,Jaume Pérez-Sánchez,M Carla Piazzon,Ariadna Sitjà-Bobadilla,Itziar Estensoro,Josep À Calduch-Giner

doi:10.3389/fmars.2021.705041

Paula Solé-Jiménez, Danny Van Mullem + Show 6 more

Open Access

https://doi.org/10.3389/fmars.2021.705041

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Abstract

The present study aimed to unravel the effects of partial (50%; 50LSAqua) and total (100%; 100LSAqua) replacement of fish meal (FM) by a commercial protein source (LSAqua SusPro) made of bacterial and processed animal proteins (PAP) in farmed juveniles of gilthead sea bream (Sparus aurata). The trial lasted 8 weeks, and the feasibility of replacement was assessed in terms of growth performance, histopathological scoring and composition of mucosal adherent microbiota from anterior intestine (AI). Specific growth rates (SGR) of 50LSAqua fish were undistinguishable from the CTRL group, whereas a slight but significant growth impairment was found with the total replacement. Histological signs of inflammation across the intestine were more evident at the highest level of FM replacement, and the total concentration of short chain fatty acids (SCFA) in stripped feces decreased in a dose dependent manner. Illumina sequencing of gut mucosal microbiota yielded a mean of 130,439 reads per sample assigned to 1,567 OTUs at 97% identity threshold. The bacterial richness was similar in all groups, but a significantly higher Simpson diversity index was found in 100LSAqua fish. At the phylum level, Proteobacteria were the most abundant in all groups, whereas Firmicutes decreased and Actinobacteria increased with the FM replacement. At a closer look, pro-inflammatory Gammaproteobacteria of the genus Psychrobacter, and Acinetobacter decreased with FM replacement, whereas the anti-inflammatory Paracoccus, Arthrobacter, and Actinomycetales increased, with a remarkable presence of the Propioniciclava genus in LSAqua groups. The inferred metagenome analysis suggested that these discriminant bacteria could be implicated in a counter-regulatory anti-inflammatory response. It also pointed to an over-representation of mucosal microbes that can potentially be involved in the natural production of antimicrobials in fish fed the experimental diets.

Highlights

Over the last two decades, the aquaculture industry is growing faster (∼7% annual growth rate) than any animal protein sector, with feed conversion ratios (FCR, dry feed intake/weight gain) (1.1–1.6) lower than in poultry (1.4–1.8), pork (2.6–4.4), and cattle (3.5–9) production (Clark and Tilman, 2017; Ritchie and Roser, 2019)
No statistically significant differences were found in hepatosomatic index (HSI), mesenteric fat index (MSI) and intestine weight (IWI), but overall the intestine of the LSAqua fish was shortened and the lowest ILI was observed in the 50LSAqua group
The results showed that 27 pathways could be significantly changing, taking into account the gene inventory of the discriminant operational taxonomic units (OTUs), in the comparison between fish fed 50/100LSAqua diets and fish fed CTRL diets

Summary

Introduction

Over the last two decades, the aquaculture industry is growing faster (∼7% annual growth rate) than any animal protein sector, with feed conversion ratios (FCR, dry feed intake/weight gain) (1.1–1.6) lower than in poultry (1.4–1.8), pork (2.6–4.4), and cattle (3.5–9) production (Clark and Tilman, 2017; Ritchie and Roser, 2019). Plant-based diets have been considered the most suitable alternative, and high levels of combined FM and fish oil (FO) replacement can be achieved in Atlantic salmon (Salmo salar) and in typically marine fish, such as European sea bass (Dicentrarchus labrax) and gilthead sea bream (Sparus aurata) (Espe et al, 2006; Torrecillas et al, 2017; Simó-Mirabet et al, 2018; Aas et al, 2019; Perera et al, 2019) These substitution diets need to be adequately supplemented with phosphorus, lysine, sulfur amino acids, protein hydrolysates, or nutraceuticals to meet the nutrient requirements for growth (Simó-Mirabet et al, 2018; Egerton et al, 2020), preventing pro-inflammatory processes and impaired intestinal barrier permeability (Estensoro et al, 2016; Piazzon et al, 2017). There is an urgent demand for suitable protein ingredients to maintain farmed fish performance, and stabilize the supply of feed ingredients during the expansion of aquaculture

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