Hepatopancreatic Metabolomics Reveals Distinct Metabolic Reprogramming and Growth–Defense Trade-Offs in Pond- Versus Rice Paddy-Cultured Red Swamp Crayfish (Procambarus clarkii)

Abstract

The red swamp crayfish is cultivated in intensive ponds and integrated rice–crayfish systems, which drive distinct growth-oriented versus stress-resistance syndromes, yet their metabolic underpinnings are unclear. We applied untargeted LC-MS metabolomics to hepatopancreas from both systems. Among 2681 metabolites, 566 were differentially abundant. Pond-cultured crayfish exhibited a lipid-centric anabolic metabolome (enriched ceramides, lysophosphatidylcholines, and free fatty acids) that supports rapid growth but incurs oxidative stress. Conversely, rice-paddy crayfish showed enhanced purine metabolism, aminoacyl-tRNA biosynthesis, and D-amino acid metabolism, reflecting energy mobilization and protein turnover under limited resources. Targeted assays confirmed significantly higher GSH/GSSG ratios (11.29 vs. 5.07) and lower MDA (3.07 vs. 5.00 nmol/mL) in rice-paddy crayfish, validating transcriptomic upregulation of glutathione biosynthesis. Integration with transcriptomic and phenotypic data revealed coherent trait–metabolite modules. Our findings suggest a trade-off between biomass production and systemic stress resistance, mediated by differential activation of purine and glutathione pathways, consistent with a growth–defense trade-off framework. This provides a mechanistic framework for sustainable aquaculture: integrated systems enhance robustness, whereas ponds require strategies to mitigate physiological load.