The Inactivated ISKNV-I Vaccine Confers Highly Effective Cross-Protection against Epidemic RSIV-I and RSIV-II from Cultured Spotted Sea Bass Lateolabrax maculatus

ABSTRACT The genus Megalocytivirus of the family Iridoviridae is composed of two distinct species, namely, infectious spleen and kidney necrosis virus (ISKNV) and scale drop disease virus (SDDV), and both are important causative agents in a variety of bony fish worldwide. Of them, the ISKNV species...

Full description

Bibliographic Details
Main Authors: Weixuan Fu, Yong Li, Yuting Fu, Wenfeng Zhang, Panpan Luo, Qianqian Sun, Fangzhao Yu, Shaoping Weng, Wangdong Li, Jianguo He, Chuanfu Dong
Format: Article
Language:English
Published: American Society for Microbiology 2023-06-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.04495-22
_version_ 1797803497052176384
author Weixuan Fu
Yong Li
Yuting Fu
Wenfeng Zhang
Panpan Luo
Qianqian Sun
Fangzhao Yu
Shaoping Weng
Wangdong Li
Jianguo He
Chuanfu Dong
author_facet Weixuan Fu
Yong Li
Yuting Fu
Wenfeng Zhang
Panpan Luo
Qianqian Sun
Fangzhao Yu
Shaoping Weng
Wangdong Li
Jianguo He
Chuanfu Dong
author_sort Weixuan Fu
collection DOAJ
description ABSTRACT The genus Megalocytivirus of the family Iridoviridae is composed of two distinct species, namely, infectious spleen and kidney necrosis virus (ISKNV) and scale drop disease virus (SDDV), and both are important causative agents in a variety of bony fish worldwide. Of them, the ISKNV species is subdivided into three genotypes, namely, red seabream iridovirus (RSIV), ISKNV, and turbot reddish body iridovirus (TRBIV), and a further six subgenotypes, RSIV-I, RSIV-II, ISKNV-I, ISKNV-II, TRBIV-I, and TRBIV-II. Commercial vaccines derived from RSIV-I , RSIV-II and ISKNV-I have been available to several fish species. However, studies regarding the cross-protection effect among different genotype or subgenotype isolates have not been fully elucidated. In this study, RSIV-I and RSIV-II were demonstrated as the causative agents in cultured spotted seabass, Lateolabrax maculatus, through serial robust evidence, including cell culture-based viral isolation, whole-genome determination and phylogeny analysis, artificial challenge, histopathology, immunohistochemistry, and immunofluorescence as well as transmission electron microscope observation. Thereafter, a formalin-killed cell (FKC) vaccine generated from an ISKNV-I isolate was prepared to evaluate the protective effects against two spotted seabass original RSIV-I and RSIV-II. The result showed that the ISKNV-I-based FKC vaccine conferred almost complete cross-protection against RSIV-I and RSIV-II as well as ISKNV-I itself. No serotype difference was observed among RSIV-I, RSIV-II, and ISKNV-I. Additionally, the mandarin fish Siniperca chuatsi is proposed as an ideal infection and vaccination fish species for the study of various megalocytiviral isolates. IMPORTANCE Red seabream iridovirus (RSIV) infects a wide mariculture bony fish and has resulted in significant annual economic loss worldwide. Previous studies showed that the phenotypic diversity of infectious RSIV isolates would lead to different virulence characteristics, viral antigenicity, and vaccine efficacy as well as host range. Importantly, it is still doubted whether a universal vaccine could confer the same highly protective effect against various genotypic isolates. Our study here presented enough experimental evidence that a water in oil (w/o) formation of inactivated ISKNV-I vaccine could confer almost complete protection against RSIV-I and RSIV-II as well as ISKNV-I itself. Our study provides valuable data for better understanding the differential infection and immunity among different genotypes of ISKNV and RSIV isolates in the genus Megalocytivirus.
first_indexed 2024-03-13T05:21:45Z
format Article
id doaj.art-df6dfef09a7243ebb53fa7de403c02ab
institution Directory Open Access Journal
issn 2165-0497
language English
last_indexed 2024-03-13T05:21:45Z
publishDate 2023-06-01
publisher American Society for Microbiology
record_format Article
series Microbiology Spectrum
spelling doaj.art-df6dfef09a7243ebb53fa7de403c02ab2023-06-15T13:18:30ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.04495-22The Inactivated ISKNV-I Vaccine Confers Highly Effective Cross-Protection against Epidemic RSIV-I and RSIV-II from Cultured Spotted Sea Bass Lateolabrax maculatusWeixuan Fu0Yong Li1Yuting Fu2Wenfeng Zhang3Panpan Luo4Qianqian Sun5Fangzhao Yu6Shaoping Weng7Wangdong Li8Jianguo He9Chuanfu Dong10State Key Laboratory of Biocontrol (Guangzhou, SYSU)/Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai, SMST-GDL), School of Life Sciences of Sun Yat-sen University, Guangzhou, ChinaZhuhai Modern Agriculture Development Center, Zhuhai, ChinaState Key Laboratory of Biocontrol (Guangzhou, SYSU)/Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai, SMST-GDL), School of Life Sciences of Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Biocontrol (Guangzhou, SYSU)/Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai, SMST-GDL), School of Life Sciences of Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Biocontrol (Guangzhou, SYSU)/Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai, SMST-GDL), School of Life Sciences of Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Biocontrol (Guangzhou, SYSU)/Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai, SMST-GDL), School of Life Sciences of Sun Yat-sen University, Guangzhou, ChinaZhuhai Modern Agriculture Development Center, Zhuhai, ChinaState Key Laboratory of Biocontrol (Guangzhou, SYSU)/Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai, SMST-GDL), School of Life Sciences of Sun Yat-sen University, Guangzhou, ChinaZhuhai Modern Agriculture Development Center, Zhuhai, ChinaState Key Laboratory of Biocontrol (Guangzhou, SYSU)/Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai, SMST-GDL), School of Life Sciences of Sun Yat-sen University, Guangzhou, ChinaState Key Laboratory of Biocontrol (Guangzhou, SYSU)/Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai, SMST-GDL), School of Life Sciences of Sun Yat-sen University, Guangzhou, ChinaABSTRACT The genus Megalocytivirus of the family Iridoviridae is composed of two distinct species, namely, infectious spleen and kidney necrosis virus (ISKNV) and scale drop disease virus (SDDV), and both are important causative agents in a variety of bony fish worldwide. Of them, the ISKNV species is subdivided into three genotypes, namely, red seabream iridovirus (RSIV), ISKNV, and turbot reddish body iridovirus (TRBIV), and a further six subgenotypes, RSIV-I, RSIV-II, ISKNV-I, ISKNV-II, TRBIV-I, and TRBIV-II. Commercial vaccines derived from RSIV-I , RSIV-II and ISKNV-I have been available to several fish species. However, studies regarding the cross-protection effect among different genotype or subgenotype isolates have not been fully elucidated. In this study, RSIV-I and RSIV-II were demonstrated as the causative agents in cultured spotted seabass, Lateolabrax maculatus, through serial robust evidence, including cell culture-based viral isolation, whole-genome determination and phylogeny analysis, artificial challenge, histopathology, immunohistochemistry, and immunofluorescence as well as transmission electron microscope observation. Thereafter, a formalin-killed cell (FKC) vaccine generated from an ISKNV-I isolate was prepared to evaluate the protective effects against two spotted seabass original RSIV-I and RSIV-II. The result showed that the ISKNV-I-based FKC vaccine conferred almost complete cross-protection against RSIV-I and RSIV-II as well as ISKNV-I itself. No serotype difference was observed among RSIV-I, RSIV-II, and ISKNV-I. Additionally, the mandarin fish Siniperca chuatsi is proposed as an ideal infection and vaccination fish species for the study of various megalocytiviral isolates. IMPORTANCE Red seabream iridovirus (RSIV) infects a wide mariculture bony fish and has resulted in significant annual economic loss worldwide. Previous studies showed that the phenotypic diversity of infectious RSIV isolates would lead to different virulence characteristics, viral antigenicity, and vaccine efficacy as well as host range. Importantly, it is still doubted whether a universal vaccine could confer the same highly protective effect against various genotypic isolates. Our study here presented enough experimental evidence that a water in oil (w/o) formation of inactivated ISKNV-I vaccine could confer almost complete protection against RSIV-I and RSIV-II as well as ISKNV-I itself. Our study provides valuable data for better understanding the differential infection and immunity among different genotypes of ISKNV and RSIV isolates in the genus Megalocytivirus.https://journals.asm.org/doi/10.1128/spectrum.04495-22MegalocytivirusRSIV genotypeISKNV genotypeinactivated vaccinecross-protectioninfectious spleen and kidney necrosis virus
spellingShingle Weixuan Fu
Yong Li
Yuting Fu
Wenfeng Zhang
Panpan Luo
Qianqian Sun
Fangzhao Yu
Shaoping Weng
Wangdong Li
Jianguo He
Chuanfu Dong
The Inactivated ISKNV-I Vaccine Confers Highly Effective Cross-Protection against Epidemic RSIV-I and RSIV-II from Cultured Spotted Sea Bass Lateolabrax maculatus
Microbiology Spectrum
Megalocytivirus
RSIV genotype
ISKNV genotype
inactivated vaccine
cross-protection
infectious spleen and kidney necrosis virus
title The Inactivated ISKNV-I Vaccine Confers Highly Effective Cross-Protection against Epidemic RSIV-I and RSIV-II from Cultured Spotted Sea Bass Lateolabrax maculatus
title_full The Inactivated ISKNV-I Vaccine Confers Highly Effective Cross-Protection against Epidemic RSIV-I and RSIV-II from Cultured Spotted Sea Bass Lateolabrax maculatus
title_fullStr The Inactivated ISKNV-I Vaccine Confers Highly Effective Cross-Protection against Epidemic RSIV-I and RSIV-II from Cultured Spotted Sea Bass Lateolabrax maculatus
title_full_unstemmed The Inactivated ISKNV-I Vaccine Confers Highly Effective Cross-Protection against Epidemic RSIV-I and RSIV-II from Cultured Spotted Sea Bass Lateolabrax maculatus
title_short The Inactivated ISKNV-I Vaccine Confers Highly Effective Cross-Protection against Epidemic RSIV-I and RSIV-II from Cultured Spotted Sea Bass Lateolabrax maculatus
title_sort inactivated isknv i vaccine confers highly effective cross protection against epidemic rsiv i and rsiv ii from cultured spotted sea bass lateolabrax maculatus
topic Megalocytivirus
RSIV genotype
ISKNV genotype
inactivated vaccine
cross-protection
infectious spleen and kidney necrosis virus
url https://journals.asm.org/doi/10.1128/spectrum.04495-22
work_keys_str_mv AT weixuanfu theinactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT yongli theinactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT yutingfu theinactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT wenfengzhang theinactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT panpanluo theinactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT qianqiansun theinactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT fangzhaoyu theinactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT shaopingweng theinactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT wangdongli theinactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT jianguohe theinactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT chuanfudong theinactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT weixuanfu inactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT yongli inactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT yutingfu inactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT wenfengzhang inactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT panpanluo inactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT qianqiansun inactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT fangzhaoyu inactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT shaopingweng inactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT wangdongli inactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT jianguohe inactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus
AT chuanfudong inactivatedisknvivaccineconfershighlyeffectivecrossprotectionagainstepidemicrsiviandrsiviifromculturedspottedseabasslateolabraxmaculatus