Transcriptome analysis revealed that largemouth bass (Micropterus salmoides) may mobilize liver lipid metabolism to provide energy for adaptation to hypertonic stress

As the evaporation of water bodies increases globally, salts are accumulating in oceans, lakes, and rivers, and these increased salinity levels have a major effect on the survival, growth, and development of various organisms. Micropterus salmoides is a freshwater fish that can survive under different salinity levels, including brackish water culture in saline-alkali land; it thus provides an excellent model for studies of environmental salinity adaptation. In this study, culture experiments were conducted for 6 weeks at 4 salinity levels, 0 ‰ (C), 5 ‰ (E1), 10 ‰ (E2), and 15 ‰ (E3), to assess the salinity tolerance and the molecular response to salinity in M. salmoides. The histology of the liver tissues of M. salmoides under different levels of salinity stress was examined, and transcriptome sequencing was performed. As the salinity level increased, liver cells became increasingly deformed, the number of liver cells decreased, and the frequency of cavitation and other types of damage increased. We also examined the activity of antioxidant-related enzymes. As the salinity level increased, superoxide dismutase and catalase activities in the liver of largemouth bass decreased. The antioxidant oxidase activity was significantly lower in the high-salinity group (10 ‰, 15 ‰) than in the low-salinity group (0 ‰, 5 ‰), and the antioxidant oxidase activity was significantly lower in the experimental groups than in the control group. RNA sequencing analysis of liver tissues revealed 725, 1780, and 5669 differentially expressed genes (DEGs) in the high-salinity treatment groups (5 ‰, 10 ‰, and 15 ‰, respectively) compared with the control group (0 ‰). Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathway enrichment analysis showed that these DEGs were involved in material metabolism, energy metabolism, signal transduction, transcription and translation, and apoptosis of cells, especially lipid and energy metabolism. Further analysis showed that the PPAR and AMPK signaling pathways promoted fatty acid β-oxidation to release energy. DEGs involved in lipid metabolism were significantly up-regulated under high salinity stress, and these included genes encoding acetyl-CoA acyltransferase 2 (ACAA2), hydroxyacyl-CoA dehydrogenase alpha (HADHA), hydroxyacyl-CoA dehydrogenase beta (HADHB), and acyl-CoA dehydrogenase short chain (ACADs), which were associated with the β-oxidation pathway. In sum, largemouth bass adapts to high-salinity environments by regulating the fatty acid β-oxidation pathway and altering the activities of the PPAR and AMPK pathways and related hub genes to increase fat oxidation and release energy. Our results provide new insights into the response of M. salmoides to salinity challenges and enhance our understanding of the molecular basis of the metabolic regulatory mechanisms in this species.