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Yellow River carp (Cyprinus carpio) is an economically-important freshwater fish. It is the common host of the epizootic bacterium Flavobacterium columnare, a common fish pathogen that causes columnaris disease resulting in aquacultural losses. However, information on the functions and mechanisms of the immune system of Yellow River carp infected with F. columnare is limited. Therefore, the aim of this study is to evaluate the genetic and histopathological effects of an experimentally-induced F. columnare infection in Yellow River carp. Sixty fish were divided into control (CT group) and challenged groups. The gills were collected for histological and transcriptome analysis to understand the host immune response after challenge with F. columnare. The infected fish of the IF group presented typical columnaris disease symptoms and higher mortality, as well as histological changes. However, some challenged fish showed asymptomatic infection (IC group). Additionally, there were 1776 significant differentially-expressed genes (DEGs) between the IC and CT groups, 1853 DEGs between the IF and CT groups, and 1836 DEGs between the IF and IC groups, All the DEGs were classified into three gene ontology categories, which were allocated to 158 KEGG pathways. Moreover, immune-related genes were confirmed by qRT-PCR. we quantified the level of IL-1, IL-6, TNF-α and IL-8 by ELISA. The results showed the highest expression levels of inflammatory cytokines as well as stress proteins and the adhesion molecules in the lF group, which may contribute to severe infection, and a higher case fatality rate, while the high expression of chemokines, costimulatory molecules and the up regulation of antigen presentation function could help the carp resist F. columnare infection. • The pathological changes of carp gills were caused by the infection of F. columnare. • Transcriptome can provide immune-related DEGs of carp infected with F. columnare. • Inflammatory cytokines may contribute to higher case fatality in the infected carp. [ABSTRACT FROM AUTHOR]