Coordinated remodeling of the mucosal microbiota and metabolome drives nonlinear growth transitions in leopard coral grouper (Plectropomus leopardus)

In this study, we characterized the growth dynamics of the leopard coral grouper (Plectropomus leopardus) from 1 to 18 months post-hatch (mph) by fitting four standard growth models. The von Bertalanffy model provided the best fit for body weight data, while the Logistic model was optimal for other growth parameters. Based on the optimal model, the key growth transition points GRI and RSI were identified at 4 and 14 mph, respectively. Morphological examination of mucosal tissues (e.g. skin, gill, and intestine) during these inflection points revealed significant tissue-specific restructuring underlying the growth trajectory. Specifically, we observed thickening of the skin and dermis, elongation and narrowing of gill filaments, and broadening/lengthening of intestinal villi from GRI to RSI. Analysis of microbial community indicated that temporal shifts outweighed tissue niche effects in shaping microbial composition. The abundance of Proteobacteria increased from GRI to RSI, coinciding with enhanced functional redundancy. Co-occurrence networks also displayed higher complexity and stability at RSI. Although stochastic processes predominantly governed microbial assembly, deterministic processes and the proportion of specialists became more pronounced at RSI. Metabolomic profiling further revealed stage-dependent metabolic reprogramming. GRI individuals were enriched with amino acid-related and nitrogenous metabolites, supporting accelerated growth, whereas RSI individuals were characterized by organic oxides, indicating a transition to metabolic homeostasis. Integrative analysis highlighted strong coherence between microbial functional potential and key metabolites (e.g. L-homoserine and taurodeoxycholic acid), suggesting a coordinated microbe-metabolite interaction during growth transitions.