Integrated application of transcriptomics and metabolomics provides insights into acute hepatopancreatic necrosis disease resistance of Pacific white shrimp Litopenaeus vannamei

Acute hepatopancreatic necrosis disease (AHPND) has caused a huge economic loss to shrimp aquaculture. Vibrio parahaemolyticus (Vp_AHPND) is regarded as a major causative agent of AHPND in the Pacific white shrimp Litopenaeus vannamei. However, knowledge about how shrimp resist to AHPND is very limited. In order to learn the molecular mechanisms underlying AHPND resistance of shrimp, comparison between disease-resistant family and susceptible family of L. vannamei were performed at transcriptional and metabolic levels. Integrated analysis of transcriptomics and metabolomics on hepatopancreas of shrimp, the target tissue of Vp_AHPND, showed that significant differences existed between resistant family and susceptible family of shrimp. The susceptible family showed higher level of glycolysis, serine-glycine metabolism, purine and pyrimidine metabolism, but lower level of betaine-homocysteine metabolism in the hepatopancreas in comparison with the resistant family without Vp_AHPND infection. Curiously, Vp_AHPND infection induced up-regulation of glycolysis, serine-glycine metabolism, purine metabolism, pyrimidine metabolism, and pentose phosphate pathway, and down-regulation of betaine-homocysteine metabolism in resistant family. In addition, arachidonic acid metabolism and some immune pathways, like NF-κB and cAMP pathways, were up-regulated in the resistant family after Vp_AHPND infection. In contrast, amino acid catabolism boosted via PEPCK-mediated TCA cycle flux was activated in the susceptible family after Vp_AHPND infection. These differences in transcriptome and metabolome between resistant family and susceptible family might contribute to the resistance of shrimp to bacteria. IMPORTANCE Vibrio parahaemolyticus (Vp_AHPND) is a major aquatic pathogen causing acute hepatopancreatic necrosis disease (AHPND) and leads to a huge economic loss to shrimp aquaculture. Despite the recent development of controlling culture environment, disease resistant broodstock breeding is still a sustainable approach for aquatic disease control. Metabolic changes occurred during Vp_AHPND infection, but knowledge about the metabolism in resistance to AHPND is very limited. Integrated analysis of transcriptome and metabolome revealed the basal metabolic differences exhibited between disease-resistant and susceptible shrimp. Amino acid catabolism might contribute to the pathogenesis of Vp_AHPND and arachidonic acid metabolism might be responsible for the resistance phenotype. This study will help to enlighten the metabolic and molecular mechanisms underlying shrimp resistance to AHPND. Also, the key genes and metabolites of amino acid and arachidonic acid pathway identified in this study will be applied for disease resistance improvement in the shrimp culture industry.