Genetic selection for growth drives differences in intestinal microbiota composition and parasite disease resistance in gilthead sea bream

Abstract

Background The key effects of intestinal microbiota in animal health has led to an increasing interest in manipulating these bacterial populations to improve animal welfare. The aquaculture sector is no exception and in the last years many studies have described these populations in different fish species. However, this is not an easy task, as intestinal microbiota is composed of very dynamic populations that are influenced by different factors, such as diet, environment, host age and genetics. In the current study, we aimed to determine whether the genetic background of gilthead sea bream ( Sparus aurata ) influences the intestinal microbial composition, how these bacterial populations are modulated by dietary changes, and the effect of selection by growth on intestinal disease resistance. To that aim, three different groups of five families of gilthead sea bream that were selected during two generations for fast, intermediate or slow growth (F3 generation) were kept together in the same open-flow tanks and fed a control or a well-balanced plant-based diet during nine months. Six animals per family and dietary treatment were sacrificed and the adherent bacteria from the anterior intestinal portion were sequenced. In parallel, fish of the fast- and slow-growth groups were infected with the intestinal parasite Enteromyxum leei and the disease signs, prevalence, intensity and parasite abundance were evaluated. Results No differences were detected in alpha diversity indexes among families, and the core bacterial architecture was the prototypical composition of gilthead sea bream intestinal microbiota, indicating no dysbiosis in any of the groups. The plant-based diet significantly changed the microbiota in the intermediate- and slow-growth families, with a much lower effect on the fast-growth group. Interestingly, the smaller changes detected in the fast-growth families potentially accounted for more changes at the metabolic level when compared to the other families. Upon parasitic infection, the fast-growth group showed significantly lower disease signs and parasite intensity and abundance than the slow-growth animals. Conclusions These results show a clear genome-metagenome interaction indicating that the fast-growth families harbor a microbiota that is more flexible upon dietary changes. These animals also showed a better ability to cope with intestinal infections.

Fish microbiomics: Strengths and limitations of MinION sequencing of gilthead sea bream (Sparus aurata) intestinal microbiota

“…Microbiota research is a fast-growing field in aquaculture with important implications for fish nutrition, health, and welfare (Brugman et al, 2018). In particular, gilthead sea bream (Sparus aurata) is one of the main cultured fish in the Mediterranean (APROMAR, 2020), and recently, many studies have been conducted to unravel its intestinal microbial dynamics (Naya-Català et al, 2021a, 2022bPiazzon et al, 2020;Solé-Jiménez et al, 2021), as the gut microbiome plays a key role in maintaining the health status in fish, including the immune system response and digestion functions (Reda et al, 2022).…”

Use of accelerometer technology for individual tracking of activity patterns, metabolic rates and welfare in farmed gilthead sea bream (Sparus aurata) facing a wide range of stressors

“…The use of conventional and untargeted omic methodologies based on transcriptomics, proteomics or metabolomics has given insights at the cellular and tissue level on the adaptation of farmed gilthead sea bream to its challenging environment (Cordero et al, 2016;Martos-Sitcha et al, 2016;Mateus et al, 2017;Piazzon et al, 2017;Gil-Solsona et al, 2019). Other approaches have considered the use of integrative measurements of whole-organism traits, and recent studies in this and other fish species clearly evidenced a changing gut microbiome following variations in diet, season, age, sex, or genetic background (Hovda et al, 2012;Piazzon et al, 2017Piazzon et al, , 2019bPiazzon et al, , 2020Kokou et al, 2018). Observations of animal behaviour by video-recording are also an interesting indicator of fish health welfare, but individual determination and quantification of distress often becomes difficult (Martins et al, 2012;Castanheira et al, 2017).…”

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

“…Intestinal mucus was scrapped off using the blunt edge of a sterile scalpel and collected into sterile 1.5 mL tubes. Mucus samples were kept on ice and DNA extraction was performed immediately after the sampling exactly as previously described (Piazzon et al, 2020). The anterior intestine portion was selected due to its importance in fish nutrient absorption and metabolism.…”

“…A sequence identity cut-off of 97% was implemented, and the inferred metagenomic functions were assigned using the Kyoto Encyclopaedia of Genes and Genomes database (KEGG, October 2018 Release). Raw KEGG pathway output from Piphillin was analyzed with the R Bioconductor package DESeq2 using default parameters, after flooring fractional counts to the nearest integer (Love et al, 2014;Bledsoe et al, 2016;Piazzon et al, 2020).…”

“…In any case, the long-term suitability of high inclusion levels of alternative protein sources is often questioned in aquafeeds, because the potential use of new feed ingredients requires the use of conventional methodologies, but also cutting-edge tools for unraveling the interactions between diets, host metabolism and gut microbiota, which has co-evolved with the host to develop a mutualistic relationship (Zhang and Davies, 2016;Agus et al, 2018). Thus, in fish and gilthead sea bream in particular, this living ecosystem is affected not only by intrinsic factors such as sex, age, genetics, or developmental stage, but also by external agents like diet, trophic level, season or captive state (Estruch et al, 2015;Piazzon et al, 2017Piazzon et al, , 2019Piazzon et al, , 2020Egerton et al, 2018;Rimoldi et al, 2020).…”