Microbial drivers of high aquaculture productivity: decoupling of taxonomic and functional profiles enables efficient nitrogen cycling in greenhouse shrimp farming

As a global cornerstone of animal protein, farmed shrimp production in China has been revolutionized by the Greenhouse Shrimp Farming Model (GSFM). However, the microbial mechanisms underpinning the productivity and biosafety of this intensive paradigm remain poorly understood. Through a large-scale metagenomic survey of 90 standardized aquaculture units in the core GSFM production regions of China, spanning a 15-degree latitudinal gradient, we deciphered the functional architecture of the GSFM microbiome. Our results reveal a striking functional convergence despite geographic taxonomic variation: while microbial compositions shifted across regions, the core metabolic pathways—particularly those governing nutrient cycling—remained conserved. High-productivity systems, notably in southern provinces (Guangxi and Guangdong), were characterized by a specialized microbial repertoire that optimized water chemistry through efficient nitrogen processing. We identified a sophisticated spatial division of labor, where the gut microbiota acts as a specialized nitrite detoxification unit, while the water column microbiota serves as the primary engine for ammonia assimilation. Furthermore, we characterized a diverse antibiotic resistome and utilized host-tracking to evaluate the ecological costs of intensification. These findings shift the focus from microbial identity to functional niche partitioning, providing a mechanistic blueprint for the sustainable intensification of aquaculture through targeted microbiome management. Characterized the microbial diversity within GSFM and highlighted the multifaceted contributions and potential value of these communities to the overall aquaculture system. Mapped the distribution of antibiotic-resistance genes in GSFM, identifying aminoglycoside, macrolide, and tetracycline resistance genes as the most prevalent, primarily associated with Proteobacteria, Bacteroidetes, and Actinobacteria. Annotated nitrogen-cycle genes, showing that gut microbiota are enriched in nitrite-metabolizing genes, while water microbiota possess great ammonium-metabolizing capacity, highlighting a complementary metabolic division of labor that underpins GSFM’s adaptation to high nitrogen loads. The division of labour between aquatic and intestinal microbiota in nitrogen metabolism may be the key to promoting high GSFM production.