Immune Response of Silver Pomfret (Pampus argenteus) CC Chemokine Ligand Gene Family to Photobacterium damselae Subsp. Damselae and Nocardia seriolae Infections

Abstract

Chemokines play a crucial role in immune responses by facilitating the migration of cells expressing corresponding chemokine receptors along concentration gradients. Photobacterium damselae subsp. Damselae (PDD) and Nocardia seriolae (NS) are known to induce substantial mortality in silver pomfret populations, yet there exists a dearth of research regarding the immune response of CCLs in PDD‐ or NS‐infected silver pomfret. In our investigation, we identified 10 PaCCLs, which include one fish‐specific CCL (PaCCL44). Phylogenetic analysis revealed considerable diversity in CCL types and copy numbers among various teleost fishes. Notably, silver pomfret lacks specific CCL genes, with most PaCCLs exhibiting heightened expression levels in immune‐related organs such as the spleen and kidney, and some being expressed in mucosal immune‐related organs like the skin and gills. Transcriptome analysis conducted on silver pomfret infected with NS and PDD elucidated that the expression changes of PaCCLs primarily manifested in the spleen during the initial stages of NS infection, shifting to the kidney in later stages. Conversely, the expression changes of PaCCLs following PDD infection predominantly occurred in the kidney. In vitro studies using silver pomfret spleen cell lines demonstrated an early peak in PaCCLs expression during infection, followed by gradual decline with NS treatment and rapid diminishment with PDD treatment. These findings suggest that PaCCLs primarily support the innate immunity of silver pomfret, potentially exhibiting chemotactic effects in the early infection stages, such as the synergistic action of PaCCL4 and PaCCL25, and later serving as direct antibacterial agents. NS invasion is characterised by a chronic infection affecting multiple organs, whereas PDD primarily inflicts severe damage to the kidney. PaCCL19a and PaCCL19b are specific to PDD, and their expression levels may decrease in the later stages of infection due to PDD immune escape. These data offer initial insights into understanding the mechanism underlying the innate immune response of the CCL gene family in silver pomfret and provide theoretical underpinnings for fish culture practices.