Effects of Aeromonas veronii and Its Vaccine on Immune-Related Gene, Liver Transcriptomics, and Gill Microbiota in Crucian Carp

Background: Aeromonas veronii is an important bacterial pathogen in crucian carp and can cause serious disease outbreaks and substantial economic losses in aquaculture. Objectives: To evaluate how A. veronii infection and its inactivated vaccine modulate immune responses in Carassius auratus. Methods: 270 juveniles were allocated into three groups: a saline-injected control group (Ctrl), a vaccination group receiving an inactivated A. veronii vaccine (Vac), and an artificial infection group (AIG) subjected to stimulation. Liver, spleen, head kidney, gill, and intestine samples were collected from fish after anesthesia. The relative transcript levels of IgM, IgD, BAFF, MHCII, CD4, BCL6, MyD88, and NF-κB were quantified. For liver transcriptome analysis, the effective library concentration was determined. And the 16S rRNA gene resulting reads of fish gill symbiotic microbiota were processed for downstream bioinformatic analysis. Results: The results showed that the Vac achieved an RPS of 73.33%, and vaccination significantly upregulated multiple immune-related genes in different fish organs. With BAFF transcription across organs emerging as a robust sentinel readout. The Pearson correlation coefficient (r) of BAFF between other genes were all ≥0.8. GO and KEGG enrichment analyses indicated that AIG had more DEGs than Vac (5885 vs. 4008) and Ctrl (6910 vs. 6178), respectively. Some genes in AIG revealed significant over-representation of immune pathways, such as BCL6, MyD88, and NF-κB. The fish gill microbiota comprised a diverse set of low-abundance taxa, the phylum level was dominated by Proteobacteria and Fusobacteriota across all groups; whereas, the Vac group remained broadly closer to the Ctrl group in overall composition. Conclusions: These results indicated marked post-challenge immune–metabolic coupling in the liver, and suggested coordinated immunophysiological interplay between the liver and the spleen. Gill microecology of symbiotic bacteria was affected by vaccination or challenge reactions, which in turn affects the health of the gills or the organism itself.