Gut microbiome composition likely affects the growth of Trachinotus ovatus by influencing the host's metabolism

Abstract

Gut microbiota are essential in regulating host growth, development, and various pathophysiological processes, yet the exact mechanisms by which they operate remain largely unknown. T. ovatus is a key species in fishery trade, possessing a diverse gut microbiota, though the relationship between this microbial diversity and its growth is not well understood. To bridge this knowledge gap, we used 16S rRNA gene amplicon sequencing to compare the gut bacterial communities of cohabitating retarded, overgrown, and normal T. ovatus collected from similarly managed ponds. Significant differences were found between the gut bacterial communities of retarded, overgrown, and normal individuals, particularly in terms of the abundance of specific bacterial families and genera. For instance, overgrown T. ovatus showed a significantly higher proportion of Pseudomonadaceae, Lactobacillaceae, and Brevinemataceae families, as well as the Vibrio, Pseudomonas, and Brevinema genera. Normal T. ovatus were more enriched with Vibrionaceae and Vibrio, while retarded T. ovatus showed higher abundances of Mycoplasmataceae, Mycoplasma, and the Lachnospiraceae NK4A136 group. Overall, the Normal group had the highest species diversity and evenness, with the Retarded and Overgrown groups showing minimal differences. The PCA biplot visually highlighted distinct gut bacterial communities among retarded, normal, and overgrown T. ovatus, with ANOSIM confirming significant differences (P < 0.05) in microbial composition between each group, indicating a strong link between growth status and gut microbiome. The Pearson correlation coefficient showed that Pseudomonas and Brevinema were strongly positively correlated with the body height, body length, and body weight of Trachinotus ovatus; Vibrio was significantly positively correlated with the body length and body weight of T. ovatus; Mycoplasma was strongly negatively correlated with all physiological parameters, while Methyloversatilis and Lachnospiraceae NK4A136 group were significantly negatively correlated with the body length of T. ovatus. The module hubs in the normal group (ASV13 and ASV19) were classified as Rhodocyclaceae; Methyloversatilis and Vibrionaceae; Vibrio, respectively. The module hub in the retarded group (ASV32) was classified as Akkermansiaceae; Akkermansia; muciniphila. These findings suggest that the interspecies interaction network within the gut bacterial communities of T. ovatus is disrupted by significant changes in the topological roles of individual ASVs, potentially affecting overall community stability. Additionally, the metabolic pathways mediated by intestinal bacteria, such as those involved in amino acid, carbohydrate, energy, glycoside biosynthesis, and lipid metabolism, were significantly more active in retarded T. ovatus. Notably, overgrown T. ovatus showed significantly lower activities in the incomplete reductive TCA cycle and nucleotide degradation pathways compared to retarded and normal T. ovatus. Therefore, the retarded and normal growing T. ovatus might experience reduced energy efficiency or increased metabolic burden due to incomplete metabolic pathways or accumulation of non-native metabolites, thereby affecting normal cell growth. These findings suggest that changes in gut microbiota could play a critical role in influencing the growth status of T. ovatus, whether retarded or overgrown.