Research Article: Transcriptome Analysis Reveals Comprehensive Insights into the Early Immune Response of Large Yellow Croaker (Larimichthys crocea) Induced by Trivalent Bacterial Vaccine

Date Published: January 30, 2017

Publisher: Public Library of Science

Author(s): Xin Zhang, Yinnan Mu, Pengfei Mu, Jingqun Ao, Xinhua Chen, Tzong-Yueh Chen.


Vaccination is an effective and safe strategy for combating bacterial diseases in fish, but the mechanisms underlying the early immune response after vaccination remain to be elucidated. In the present study, we used RNA-seq technology to perform transcriptome analysis of spleens from large yellow croaker (Larimichthys crocea) induced by inactivated trivalent bacterial vaccine (Vibrio parahaemolyticus, Vibrio alginolyticus and Aeromonas hydrophila). A total of 2,789 or 1,511 differentially expressed genes (DEGs) were obtained at 24 or 72 h after vaccination, including 1,132 or 842 remarkably up-regulated genes and 1,657 or 669 remarkably down-regulated genes, respectively. Gene ontology and Kyoto Encyclopedia of Genes and Genomes enrichments revealed that numerous DEGs belong to immune-relevant genes, involved in many immune-relevant pathways. Most of the strongly up-regulated DEGs are innate defense molecules, such as antimicrobial peptides, complement components, lectins, and transferrins. Trivalent bacterial vaccine affected the expressions of many components associated with bacterial ligand–depending Toll-like receptor signaling pathways and inflammasome formation, indicating that multiple innate immune processes were activated at the early period of vaccination in large yellow croaker. Moreover, the expression levels of genes involved in antigen processing were also up-regulated by bacterial vaccine. However, the expression levels of several T cell receptors and related CD molecules and signal transducers were down-regulated, suggesting that the T cell receptor signaling pathway was rapidly suppressed after vaccination. These results provide the comprehensive insights into the early immune response of large yellow croaker to vaccination and valuable information for developing a highly immunogenic vaccine against bacterial infection in teleosts.

Partial Text

Large yellow croaker (Larimichthys crocea) is one of the most important aquaculture species in China, with the annual yield exceeding any other net-cage-farmed marine fish species [1]. However, the diseases caused by bacteria, such as Vibrio parahaemolyticus [2], Vibrio alginolyticus [3], and Aeromonas hydrophila [4], outbreak frequently and result in tremendous economic losses in large yellow croaker aquaculture industry. Chemotherapeutants and antibiotics are useful for preventing bacterial infection, but long term treatment often leads to resistance and environmental pollution [5]. Vaccination is an effective and safe strategy for combating bacterial diseases in fish [6]. A number of vaccines are commercially available for use in the aquaculture industry, such as formalin-inactivated Yersinia ruckeri [7], Aeromonas salmonicida [8], and Vibrio anguillarum [9]. The effects of vaccines were mainly evaluated by serum or mucus antibody titers and survival rate [10]. Recently, several studies on the gene expression changes have been performed to understand the immune response to bacterial vaccines in fish. In Atlantic salmon (Salmo salar), the increased expressions of antibacterial proteins and proteases were observed after vaccination with live Aeromonas salmonicida [11]. In zebrafish (Danio rerio), multiple pathways including acute phase response, complement activation, and antigen processing and presentation were remarkably affected during the early stage of vaccination [12]. The genes involved in inflammation and antioxidant defense were also up-regulated in Atlantic cod (Gadus morhua) following vaccination with heat-killed Vibrio anguillarum [13].

To date RNA-seq based transcriptome profiling has been widely used in fish for identifying host determinants of response to bacterial infection [22, 23, 31–33]. In previous study, we have demonstrated that A. hydrophila infection could activate Toll-like receptor, JAK-STAT, and MAPK pathways, while inhibit TCR signaling pathway at the early period in large yellow croaker [34]. In this study, we analyzed the spleen transcriptome profiles of large yellow croaker after vaccination and found abundant DEGs were involved in innate defense, ligand recognition, antigen processing, and TCR signaling processes.