Integrated Transcriptomic and Metabolomic Analysis Elucidates the Impact of Acute Ammonia Stress on Carbohydrate and Lipid Metabolic Pathways in Yellow Catfish (Pelteobagrus fulvidraco)

整合转录组学和代谢组学分析阐明急性氨胁迫对黄颡鱼(Pelteobagrus fulvidraco)碳水化合物和脂质代谢途径的影响

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Abstract

Ammonia stress (AS) constitutes a significant environmental challenge that impedes aquaculture development. In this investigation, histomorphology assessments, physiological, and biochemical parameter analyses, and multiomics approaches were employed to elucidate the impact of acute AS on yellow catfish (Pelteobagrus fulvidraco). Findings indicated that serum ammonia concentrations exhibited a dose-dependent increase, correlating with the intensity and duration of stress. As the primary detoxification organ, the liver facilitates ammonia clearance by upregulating genes involved in glutamine and ureagenesis (glutamine synthase [gs], carbamoyl-phosphate synthase [cps], ornithine transcarbamylase [otc], argininosuccinate lyase [asl], argininosuccinate synthase [ass], arginase [arg]), thereby promoting glutamine and ureagenesis while consuming glutamate, argininosuccinic acid, aspartic acid, arginine, and adenosine triphosphate (ATP). Physiological and biochemical data revealed that AS significantly elevated serum glucose, liver triglyceride (TG), and total cholesterol (TC) levels. Histological examination demonstrated a marked reduction in liver glycogen stores alongside a progressive accumulation of lipid droplets proportional to stress severity, suggesting activation of liver glycogenolysis coupled with suppression of lipolysis. Integrative transcriptomic and metabolomic analyses indicated a reprograming of liver energy metabolism characterized by enhanced glycogenolysis and suppressed lipogenesis: liver glycogen content decreased, key glycolytic gene expression (hk1, pdhx) was downregulated, and tricarboxylic acid (TCA) cycle flux was diminished due to decreased cs expression. Concurrently, transcription of fatty acid β-oxidation enzymes (acsbg1, cpt1) was suppressed, leading to palmitic acid accumulation and impaired lipid-derived energy production. Nonetheless, reorganization of carbon flux through upregulation of mdh2 and idh1 facilitated pyruvate utilization in the TCA cycle, promoting NADH generation and sustaining oxidative phosphorylation, as evidenced by increased ATP turnover and content. This study elucidates the metabolic response to AS via increased glycogenolysis. Optimizing liver glycogen reserves serves as a nutritional strategy to enhance ammonia tolerance. Targeted regulation of key genes (pygl, pk, mdh2, idh1) to promote glycogen-pyruvate metabolism may mitigate ammonia toxicity effects and improving aquaculture productivity.

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