Understanding the spleen response of Russian sturgeon (Acipenser gueldenstaedtii) dealing with chronic heat stress and Aeromonas hydrophila challenge

Sturgeon aquaculture has grown in recent years, driven by increasing global demand for its highly valued products. Russian sturgeon (Acipenser gueldenstaedtii), recognised as one of the most valuable species for caviar production, is farmed in several warm-temperate regions. However, the substantial temperature increase due to global warming represents a challenge for developing sturgeon aquaculture. Previously we demonstrated that Russian sturgeon under chronic heat stress (CHS) exhibited a liver metabolic reprogramming to meet energy demands, weakening their innate defences and leading to increased mortality and economic losses. Here, we used RNA-seq technology to analyse regulated genes in the spleen of Russian sturgeons exposed to CHS and challenged with Aeromonas hydrophila. The assembly gave 253,415 unigenes, with 13.7 % having at least one reliable functional annotation. We found that CHS caused mild splenitis and upregulated genes related to protein folding, heat shock response, apoptosis and autophagy while downregulated genes associated with the cell cycle. The cell cycle arrest was maintained upon A. hydrophila challenge in heat-stressed fish, potentially inducing cell senescence. Surprisingly, immunoglobulin heavy and light chains were upregulated in the spleen of stressed sturgeons but not in those maintained at tolerable temperatures; however, no changes in IgM serum levels were observed in any condition. Our findings indicate that long-term exposure to non-tolerable temperatures induced a heat shock response and activated apoptosis and autophagy processes in the spleen. These mechanisms may enable the control of tissue damage and facilitate the recycling of cell components in a condition where the nutrient supply by the liver might be insufficient. Stressed sturgeons challenged with A. hydrophila maintain these mechanisms, which could culminate in cellular senescence. [Display omitted] •A high-quality spleen transcriptome of the Russian sturgeon was de novo assembled•Spleen DEGs were identified under chronic heat stress (CHS) and bacterial challenge•CHS induced more transcriptomic changes than the bacterial challenge in the spleen•CHS caused a spleen heat-shock response, apoptosis, autophagy and cell cycle arrest•CHS-induced cell cycle arrest may lead to cell senescence after bacterial challenge