Transcriptomic analysis using dual RNA sequencing revealed a Pathogen–Host interaction after Edwardsiella anguillarum infection in European eel (Anguilla anguilla)

• Published in: Fish & shellfish immunology 2022-01, Vol.120, p.745-757
• Main Authors: Xiao, Yiqun, Wu, Liqun, He, Le, Tang, Yijun, Guo, Songlin, Zhai, Shaowei
• Format: Article
• Language: English
• Subjects: Anguilla - genetics; Anguilla Anguilla; Animals; Differentially expressed gene; Dual RNA sequencing; Edwardsiella; Edwardsiella anguillarum; Enterobacteriaceae Infections - genetics; Enterobacteriaceae Infections - veterinary; Fish Diseases - genetics; Fish Diseases - microbiology; Gene Expression Profiling; Host-Pathogen Interactions; Pathogen-host; Pathological changes; Sequence Analysis, RNA; Transcriptome
• ISSN: 1050-4648; 1095-9947
• DOI: 10.1016/j.fsi.2021.12.051

Many studies have explored differentially expressed genes (DEGs) between some pathogens and hosts, but no study has focused on the interaction of DEGs between Edwardsiella anguillarum (Ea) and Anguilla anguilla (Aa). In this study, we examined the interactions of DEGs during Ea infection and Aa anti-infection processes by dual RNA sequencing. Total RNA from in vitro and in vivo (Aa liver) Ea culture was extracted. Using high-throughput transcriptomics, significant DEGs that were expressed between Ea cultured in vitro versus in vivo and those in the liver of the infected group versus control group were identified. Protein–protein interactions between the pathogen and host were explored using Cytoscape according to the HPIDB 3.0 interaction transcription database. The results showed that the liver in the infection group presented with severe bleeding and a large number of thrombi in the hepatic vessels. We found 490 upregulated and 398 downregulated DEGs of Ea in vivo versus Ea cultured in vitro, and 2177 upregulated and 970 downregulated genes in the liver of the infected eels. Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis of the pathogen DEGs revealed that the upregulated genes were mainly enriched in migration, colonization, biofilm formation, and significantly enriched in ABC transport and quorum sensing; the downregulated genes were mainly involved in metabolism, information transduction, organelle formation, enzyme catalysis, molecular transport, and binding. GO of the host DEGs showed that metabolic process, catalytic activity, single organism metabolic process, small molecule binding, nucleotide binding, nucleotide phosphate binding, and anion binding were markedly enriched. Finally, we found that 79 Ea and 148 Aa proteins encoded by these DEGs were involved in an interaction network, and some pathogen (DegP, gcvP, infC, carB, rpoC, trpD, sthA, and FhuB) and host proteins (MANBA, STAT1, ETS2, ZEP1, TKT1, NMI and RBPMS) appear to play crucial roles in infection. Thus, determining the interaction networks revealed crucial molecular mechanisms underlying the process of pathogenic infection and host anti-infection. •Interaction of DEGs between Edwardsiella anguillarum and European eels was first reported.•Eels infected by Edwardsiella anguillarum presented with severe pathological changes in the liver.•Seventy-nine Ea and 148 Aa proteins encoded by DEGs formed an interaction network.•Eight pathogen and 7 host proteins app