Abstract
Background: As a globally significant aquaculture species, elucidating the molecular mechanisms underlying the regulation of the Pacific White Shrimp (Litopenaeus vannamei) growth holds substantial scientific and industrial value. This study systematically investigates the role of the LvChia2 gene in governing growth and development through a cross-tissue metabolic network approach. Methods: RNA knockdown (RNAi)-mediated knockdown of LvChia2 significantly impaired growth performance and triggered a tissue-specific metabolic compensation mechanism. Results: This mechanism was characterized by reduced crude lipid content in muscle and adaptive modulation of lipase (LPS) activities in hepatopancreatic and intestinal tissues, suggesting inter-tissue metabolic coordination. Transcriptomic profiling identified 610 differentially expressed genes (DEGs), forming a three-dimensional regulatory network encompassing "energy metabolism, molt regulation, and nutrient utilization." Key mechanistic insights revealed the following: (1) Enhanced mitochondrial energy transduction through the upregulation of ATP synthase subunits and NADH dehydrogenase (ND-SGDH). (2) The disruption of ecdysteroid signaling pathways via suppression of Krueppel homolog 1 (Kr-h1). (3) The coordinated regulation of nitrogen metabolism through the downregulation of glutamine synthetase and secretory phospholipase A2. These molecular adaptations, coupled with tissue-specific oxidative stress responses, reflect an integrated physiological strategy for environmental adaptation. Conclusions: Notably, this study provides the first evidence in crustaceans of chitinase-mediated growth regulation through cross-tissue metabolic interactions and identifies six core functional genes (ATP5L, ATP5G, ND-SGDH, Kr-h1, GS, sPLA2) as potential targets for molecular breeding. A novel "gut-hepatopancreas axis" energy compensation mechanism is proposed, offering insights into resource allocation during metabolic stress. These findings advance our understanding of crustacean growth regulation and establish a theoretical foundation for precision aquaculture strategies, including genome editing and multi-trait genomic selection.