Integrated physio-biochemical and 16S rRNA analyses reveal the correlation of gut microbiota, meat quality and growth performance in red tilapia (Oreochromis spp.) under hyperosmotic stress

Abstract

Red tilapia (Oreochromis spp.), a euryhaline species, has emerged as a key species for brackish water culture due to its rapid growth and salt tolerance, making it a valuable resource in the face of declining land and freshwater resources. In this study, we investigated the impact of salinity levels on red tilapia growth performance, muscle quality, and gut microbiota. A total of 450 red tilapia (4.62 ± 0.04 g) were randomly assigned to 18 indoor recirculation tanks (500 L), with 25 fish per tank. Six salinity gradients (0, 4, 8, 12, 16, and 20 ‰; S0, S4, S8, S12, S16, and S20) were established, with three replicates for each group. The results showed significant differences in final body weight (FBW), final body length (FBL), weight gain rate (WGR), and specific growth rate (SGR) across salinity levels, with the highest values observed in the S12 group, while feed conversion ratio (FCR) had the lowest value in this group. After analyzing the growth performance data, the subsequent analysis of meat quality and intestinal microbiota specifically examined the three groups with salinity levels of 0, 12, and 20 ppt.

Muscle proximate composition, amino acid composition, and muscle texture remained unaffected by salinity (P > 0.05). Nucleotide composition showed significant differences among the groups (P < 0.05). Saturated fatty acids, polyunsaturated fatty acids, and ω-6 polyunsaturated fatty acids contents were not significantly different (P > 0.05). However, monounsaturated fatty acids (MUFA) and ω-3 polyunsaturated fatty acids (PUFA) were significantly different between the S0 and S20 groups, with the S20 group exhibiting significantly higher MUFA and ω-3 PUFA content compared to the S0 group (P < 0.05). Muscle structure was significantly different between S0 and S20 groups. Based on gut microbiota results, salinity significantly impacted microbial diversity, composition, and metabolic functions in red tilapia. Proteobacteria, Actinobacteria, Verrucomicrobia, Fusobacteria, Bacteroidetes, and Firmicutes were the dominant phyla, while the key differential genera were Mycobacterium, Acinetobacter, Rhodococcus, and Citrobacter in the S0 group, Cetobacterium and Photobacterium in the S12 group, and Vibrio and Shewanella in the S20 group. Significant positive correlations were observed between gut microbiota and growth performance parameters (FBW, WGR, and SGR), lipid content, adenosine monophosphate (AMP) and guanosine monophosphate (GMP), levels, myofibril density, and springiness. Conversely, inosine monophosphate (IMP) levels and myofibril diameter were negatively correlated with gut microbiota composition. Red tilapia exhibited optimal growth performance at 12 ‰, while muscle quality and gut microbiota were significantly influenced by salinity, particularly at the extremes of 0 and 20 ‰. Furthermore, gut microbiota had a significant influence on growth and meat quality. The findings of this study provide crucial insights for optimizing salinity levels in red tilapia aquaculture and contributing to more sustainable production practices.