Diet and seasonal dynamics shape microbiome structure across host and environmental compartments in gilthead seabream (Sparus aurata): a longitudinal multicompartment study

Host-associated microbiomes are shaped by ecological, environmental, and host-related factors. In farmed fish, diet has been widely studied as a driver of microbiome structure, whereas temporal dynamics remain comparatively underexplored. Integrating dietary effects with temporal trajectories is essential to understand microbiome dynamics under production conditions, particularly in ectothermic species reared in environmentally exposed systems subjected to seasonal variation and climate change–related effects. Accordingly, we conducted a longitudinal, multi-compartment analysis integrating host-associated (skin and gut) and environmental (inlet and rearing water) 16S rRNA time-series data across the production cycle of gilthead sea bream under distinct dietary regimes. Temporal progression emerged as the dominant factor structuring the microbiome, consistently explaining more compositional variance than diet in both gut and skin communities. Although dietary effects were detected in skin-associated communities, these responses were transient and season-dependent. By contrast, autochthonous gut mucosal populations showed strong resilience to dietary perturbation, retaining a persistent core microbiome fraction (20 taxa) independently of diet and time. Despite this stability in taxonomic prevalence, most core taxa exhibited pronounced temporal fluctuations, highlighting the coexistence of taxonomic persistence and temporal abundance dynamics within the intestinal microbiome. Environmental microbiomes showed reproducible seasonal rhythmicity in inlet seawater over two consecutive years, strongly associated with seawater temperature. Fish introduction restructured rearing water communities, enriching fish-associated and copiotrophic taxa commonly reported in aquaculture systems, including Vibrio , Tenacibaculum , Photobacterium and Alteromonas . Notably, skin and rearing water microbiomes displayed parallel temporal trajectories, with a subset of genera showing highly concordant seasonal dynamics across compartments, indicating ecological coupling at the host–water interface. Microbiome structure in gilthead sea bream under production conditions is driven primarily by seasonal environmental factors rather than diet. Seasonal filtering constrains microbiome responsiveness to diet, while simultaneously structuring both host-associated and surrounding water communities. These findings highlight the need for longitudinal study designs to correctly interpret dietary interventions under real production conditions. At the same time, the coupled microbial dynamics between host and environment highlight the potential of rearing-water microbiome analysis as a non-invasive proxy for tracking host-associated microbial changes within aquaculture systems.