Combined histopathological, immunoenzymatic and transcriptomic analyses reveal the immune response mechanisms of silver pomfret infected by Vibrio parahaemolyticus

Abstract

The silver pomfret (Pampus argenteus), a vital aquaculture species, is highly susceptible to Vibrio parahaemolyticus infections, yet the molecular mechanisms underlying its immune response remain poorly understood. This study investigated gill responses to V. parahaemolyticus infection via intraperitoneal injection, analyzing histopathological, transcriptomic, and enzymatic changes at 3, 6, 12, 24 and 48 h post-infection (hpi). Histological analysis revealed progressive gill damage, with significant architectural disruption from 6 hpi and severe lesions by 48 hpi. Transcriptome profiling of 18 cDNA libraries generated 40–67 million clean reads, yielding 4492–5231 differentially expressed genes (DEGs) across time points, with 1094–2174 unique DEGs per time point. Inflammatory cytokines (tnf-α, il-1β, il-8, il-12) showed robust upregulation, peaking at 6–24 hpi, indicative of an active immune response. Gene Ontology (GO) and KEGG analyses identified enriched pathways, including “oxidative phosphorylation” (3–48 hpi) and “tight junction” (24 hpi), with “oxidoreductase activity” and “aerobic respiration” as the dominant functional categories. Oxidative stress markers (MDA, SOD, CAT, POD) exhibited time-dependent increases, reflecting enhanced antioxidant defenses. Weighted Gene Co-expression Network Analysis (WGCNA) revealed the turquoise module as being strongly correlated with infection, identifying hub genes (gapdh, gapdhs, pgam2, g6pd, taldo1, pgam1a) critical to immune regulation. This study is the first to systematically investigate the temporal crosstalk between inflammatory responses, oxidative stress, and metabolic reprogramming in silver pomfret gills during V. parahaemolyticus infection, providing novel molecular targets for the control of vibriosis.