Transcriptome analysis reveals new insights into immune response to hypoxia challenge of large yellow croaker (Larimichthys crocea)

Fish live in direct contact with aquatic environment, which exhibits much wider temporal and spatial variations in oxygen content. The molecular mechanisms underlying fish response to hypoxia have become a subject of great concern in recent years. In the present study, we performed transcriptome analysis of spleen and head kidney tissues from large yellow croaker (Larimichthys crocea) at 6 h, 24 h and 48 h after hypoxia challenge. A total of 2,499 and 3,685 differentially expressed genes (DEGs) were obtained in spleen and head kidney, respectively. The expression changes of 10 selected genes in each tissue were further validated by quantitative real-time PCR. Gene ontology and Kyoto Encyclopedia of Genes and Genomes enrichments revealed that numerous DEGs were immune genes, involved in multiple immune-relevant pathways. In spleen, several pattern recognition receptors (PRRs), including Toll-like receptors (TLR1, TLR2.1, TLR2-2, TLR5 and TLR8), Fucolectins (FUCL1, FUCL4 and FUCL5) and macrophage mannose receptor (MRC1), were significantly down-regulated, suggesting that the immune processes mediated by these PRRs may be suppressed by hypoxia stress. However, some PRRs (FUCL4, FUCL5 and MRC1) and other innate immunity genes, such as C-type lectin domain gene family members, chemokines, chemokine receptors and complement components were up-regulated in head kidney, which may be due to the increases in phagocytosis and cytokine secretion by macrophages after hypoxic stimulus. The expression of genes involved in B cell receptor signaling pathway, Natural killer cell-mediated cytotoxicity and NF-kappa B signaling pathway decreased rapidly, but regained normal or increased over time, suggesting an early adjustment pattern of fish immune response to cope with hypoxia stress. Moreover, the anaerobic ATP-generating pathway was activated and energy consumption processes were repressed concurrently in both spleen and head kidney. These data provide valuable information for understanding the tissue-specific and temporal changes of immune gene expression in hypoxic large yellow croakers.