Lipidome and proteome analyses provide insights into Mariana Trench Snailfish (Pseudoliparis swirei) adaptation to the hadal zone

The hadal zone environment, characterized by extreme hydrostatic pressure, low temperatures, and limited food availability, presents substantial survival challenges for deep-sea fish species. In this study, we captured five deep-sea fish species (Bathysaurus mollis, Coryphaenoides rudis, Ilyophis sp., I. brunneus and Pseudoliparis swirei) from the Mariana Trench at depths ranging from 2027 to 7125 ​m, by employing China's “Exploration I and Exploration II”. By combining lipidomic and proteomic analyses, we aimed to explore the genetic basis of adaptive evolution to the hadal zone in fish. The results indicate several key findings: (1) P. swirei (Mariana hadal snailfish, MHS) may enhance energy storage and utilization during prolonged fasting periods by significantly increasing liver tissue levels of cholesterol ester (CE), ether-linked triacylglycerol (TG-O), coenzyme Q (CoQ), and ATPase content; (2) MHS could maintain membrane fluidity under high pressure by increasing the proportion of unsaturated fatty acids while reducing levels of cholesterol and phosphatidylethanolamine (PE) content. (3) The regulation of lipid types and ratios could increase the risk of lipid peroxidation. To counter oxidative stress, MHS likely elevates monounsaturated fatty acid content and enhances antioxidants such as transferrin and heat shock proteins. Overall, this study provides new insights into the adaptive mechanisms of MHS to deep-sea conditions through the lipidome and proteome analyses, thus broadening our understanding of its resilience in the hadal zone. •Lipidomic profiles of liver tissues from five deep-sea fish species (2027 to 7125 ​m) and the proteomic profile of MHS liver tissue have been reported.•MHS may enhance energy storage and utilization during prolonged fasting periods by significantly increasing liver tissue levels of cholesterol ester (CE), ether-linked triacylglycerol (TG-O), coenzyme Q (CoQ), and ATPase content.•MHS could maintain membrane fluidity under high pressure by increasing the proportion of unsaturated fatty acids while reducing levels of cholesterol and phosphatidyl-ethanolamine (PE) content.•The regulation of lipid types and ratios could increase the risk of lipid peroxidation. To counter oxidative stress, MHS likely elevates monounsaturated fatty acid content and enhances antioxidants such as transferrin and heat shock proteins.