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

SIMPLE SUMMARY: The AquaIMPACT H2020 EU project aims at the integration of selective breeding and nutrition for improving the competitiveness of European Aquaculture, promoting at the same time the production of robust and high-quality fish with a limited environmental impact. The gut microbiota is one of criteria chosen to assess the achievement of such goals, and we evaluated herein how the gut microbiota changes with the diet along the production cycle in reference (REF) fish and fish genetically improved (GS) for growth. To better underscore the association of the host with its gut microbiota, we also deconvoluted the correlation of gut bacteria with the host intestinal gene expression profile, which highlighted the physiological processes that are independent or potentially related to changes in gut microbiota composition. The physiological relevance of these findings is discussed in relation to the different growth potentiality of the two fish populations analysed. ABSTRACT: Fish genetically selected for growth (GS) and reference (REF) fish were fed with CTRL (15% FM, 5–7% FO) or FUTURE (7.5% FM, 10% poultry meal, 2.2% poultry oil + 2.5% DHA-algae oil) diets during a 12-months production cycle. Samples from initial (t(0); November 2019), intermediate (t(1); July 2020) and final (t(2); November 2020) sampling points were used for Illumina 16S rRNA gene amplicon sequencing of the adherent microbiota of anterior intestine (AI). Samples from the same individuals (t(1)) were also used for the gene expression profiling of AI by RNA-seq, and subsequent correlation analyses with microbiota abundances. Discriminant analyses indicated the gut bacterial succession along the production cycle with the proliferation of some valuable taxa for facing seasonality and different developmental stages. An effect of genetic background was evidenced along time, decreasing through the progression of the trial, namely the gut microbiota of GS fish was less influenced by changes in diet composition. At the same time, these fish showed wider transcriptomic landmarks in the AI to cope with these changes. Our results highlighted an enhanced intestinal sphingolipid and phospholipid metabolism, epithelial turnover and intestinal motility in GS fish, which would favour their improved performance despite the lack of association with changes in gut microbiota composition. Furthermore, in GS fish, correlation analyses supported the involvement of different taxa with the down-regulated expression of pro-inflammatory markers and the boosting of markers of extracellular remodelling and response to bacterium. Altogether, these findings support the combined action of the gut microbiome and host transcriptionally mediated effects to preserve and improve gut health and function in a scenario of different growth performance and potentiality.