New insights into the physiological effects of structural environmental enrichment on black sea bream (Acanthopagrus schlegelii) based on a combined analysis of transcriptomics and metabolomics

Abstract

Environmental enrichment (EE) has been generally accepted as an effective and promising way to enhance the performance and improve the welfare of animals kept in captivity. Evidence for the effects of EE on fish has accumulated rapidly, but little is known about its underlying mechanisms. In this study, black sea bream (Acanthopagrus schlegelii) were reared under enriched and enrichment-free conditions for 30 (post-larval) and 60 (juvenile) days. Physiological, transcriptome, and metabolome data were compared to investigate potential rearing improvements, physiological responses to acute stress, and the underlying mechanisms. The results showed that fish reared under enriched conditions had significantly better growth performance, a higher survival rate, and lower basal cortisol levels. Meanwhile, the cortisol, lactic acid, malondialdehyde (MDA), and total antioxidant capacity (T-AOC) levels in fish subjected to acute stress suggested that EE-reared individuals presented greater stress resistance. However, the effect of EE may decrease with the extension of treatment time for larger fish. The transcriptome analysis showed that energy-related pathways (including oxidative phosphorylation, the citrate cycle, and glycolysis/gluconeogenesis) as well as protein folding, sorting, and degradation-related pathways (protein processing in the endoplasmic reticulum and proteasome pathways); replication and repair related pathways (including pathways involved in nucleotide excision repair, base excision repair, mismatch repair, and homologous recombination); and immune-related pathways (complement and coagulation cascades pathway and the IL-17 signaling pathway) were significantly altered in the EE-reared individuals. In addition, integrated analysis of metabolome and transcriptome data revealed marked enrichment of transcription-associated metabolites involved in cortisol synthesis and secretion, taste transduction, olfactory transduction, and protein digestion and absorption pathways. Our results suggested that EE may influence the growth, fitness, and stress resistance of A. schlegelii by regulating a series of biological processes including energy metabolism, cortisol synthesis, antioxidant enzyme activities, protein folding, DNA replication and repair, and complement and coagulation cascades.