Characteristics of pathology and transcriptome profiling reveal features of immune response of acutely infected and asymptomatic infected of carp edema virus in Koi

Abstract

Koi sleepy disease (KSD) is a high mortality and infection viral disease caused by carp edema virus (CEV), which was a serious threat to aquaculture of common carp and export trade of Koi worldwide. Asymptomatic infection is an important cause of the difficulty in preventing KSD and its worldwide spread, because asymptomatic infection can be activated under appropriate condition. However, the understanding of the molecular correlates of these infections is still unknown. The purpose of this study was to compare the pathology change, enzyme activity, immunoglobulin activity, host and viral gene expression differences in acutely infected and cohabiting asymptomatic Koi infected with CEV. Healthy Koi were used as a control. The gross pathology, histopathology and ultrastructural pathology showed the difference and characteristics damage to the tissues of Koi under different infection conditions. Periodic Acid-Schiff stain (PAS), enzyme activity and immunoglobulin activity revealed changes in the immune response of gill tissue between acutely infected, asymptomatic infected and healthy Koi. A total of 111 and 2484 upregulated genes and 257 and 4940 downregulated genes were founded in healthy Koi vs asymptomatic infected Koi and healthy Koi vs acutely infected Koi, respectively. Additionally, 878 upregulated genes and 1089 downregulated genes were identified in asymptomatic vs. acutely infected Koi. Immune gene categories and their corresponding genes in different comparison groups were revealed. A total of 3, 59 and 28 immune-related genes were identified in the group of healthy Koi vs asymptomatic infected Koi, healthy Koi vs acutely infected Koi and asymptomatic infected Koi vs acutely infected Koi, respectively. Nineteen immune-related genes have the same expression manner both in healthy Koi vs acutely infected Koi and asymptomatic Koi vs acutely infected Koi, while 9 immune-related genes were differentially expressed only in asymptomatic Koi vs acutely infected Koi, which may play a role in viral reactivation. In addition, 8 differentially expressed genes (DEGs) were validated by quantitative reverse transcription PCR (RT-qPCR), and the results were consistent with the RNA-Seq results. In conclusion, the data obtained in this study provide new evidence for further elucidating CEV-host interactions and the CEV infection mechanism and will facilitate the implementation of integrated strategies for controlling CEV infection and spread.

Distribution of carp edema virus in organs of infected juvenile common carp

“…This contrasts with the finding of the study by Adamek et al . ( 2 ) concerning carp edema virus transmission, in which common carp gill tissue showed higher virus loads than intestine, kidney, skin or spleen tissue; the highest levels of viral nucleic acid were also found in the gills of infected koi in research by Ouyang et al ( 11 ).…”

Potential to grow carp oedema virus (genogroup I) in monolayers of carp‐derived primary cells with further implication in cell analysis

“…Employing cultivated CEV for in vivo testing could be efficient for studies focused on subclinical infection. In fact, host–pathogen interaction and immune‐derived markers might be used somewhat interchangeably depending upon the severity of CEV infection, which also controls the manifestation of symptoms (Ouyang et al., 2023). Although large doses of cultivated CEV were used (i.e., >10 7 –10 8 ) to experimentally challenge the fish variants, only carp strains from which the primary cultures were derived (R × T) or those ancestrally related to them (AS) showed sporadic positive cases, and then rather at a mid‐stage of infection (i.e.…”

“…The authors of the aforesaid study have found a positive relationship between the increasing size of a virus particle and a larger contact interface with the target cell that could facilitate Employing cultivated CEV for in vivo testing could be efficient for studies focused on subclinical infection. In fact, host-pathogen interaction and immune-derived markers might be used somewhat interchangeably depending upon the severity of CEV infection, which also controls the manifestation of symptoms (Ouyang et al, 2023).…”

“…Typical and unique characteristics of poxviruses that may influence their propagation in vitro are their strict host specificity and tendency to infect only certain tissues and/or cells within the host known as viral tropism (McFadden, 2005). In KSD, tissue of the gills is found to be the main entry route and the replicative site for CEV (Adamek et al., 2017; Ouyang et al., 2023). Thus, in the work reported here, gills epithelia and other carp‐derived primary cultures regarding which we previously reported a method for their obtaining were employed for the cultivation of CEV with subsequent cell‐based analysis of virus entry and infectivity.…”

Genetic characterization of alloherpesvirus (cyprinid herpesvirus-2 and koi herpesvirus) and poxvirus (carp edema virus) identified from domestic and imported cyprinids in Korea

“…Although different viruses can cause the disease, the clinical signs observed in infected fish are similar in terms of having gill necrosis and deposits of thick mucus under the gill covers being the most prominent (Bergmann et al, 2006;Granzow et al, 2014;Zhu et al, 2019). It is noteworthy that even though these viruses were identified decades ago, they continue to spread worldwide (Bergmann et al, 2020;Ouyang et al, 2023).…”