Differential Reshaping of Skin and Intestinal Microbiota by Stocking Density and Oxygen Availability in Farmed Gilthead Sea Bream (Sparus aurata): A Behavioral and Network-Based Integrative Approach

Abstract

Fish were kept for six weeks at three different initial stocking densities and water O2 concentrations (low-LD, 8.5 kg/m3 and 95–70% O2 saturation; medium-MD, 17 kg/m3 and 55–75% O2 saturation; high-HD, 25 kg/m3 and 60–45% O2 saturation), with water temperature increasing from 19 °C to 26–27 °C. The improvement in growth performance with the decrease in stocking density was related to changes in skin and intestinal mucosal microbiomes. Changes in microbiome composition were higher in skin, with an increased abundance of Alteromonas and Massilia in HD fish. However, these bacteria genera were mutually exclusive, and Alteromonas abundance was related to a reactive behavior and systemic growth regulation via the liver Gh/Igf system, while Massilia was correlated to a proactive behavior and a growth regulatory transition towards muscle rather than liver. At the intestinal level, microbial abundance showed an opposite trend for two bacteria taxa, rendering in a low abundance of Reyranella and a high abundance of Prauserella in HD fish. This trend was correlated with up-regulated host gene expression, affecting the immune response, epithelial cell turnover, and abiotic stress response. Most of the observed responses are adaptive in nature, and they would serve to infer new welfare indicators for increased stress resilience.