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Betanodavirus and VER Disease: a 30-Year Research Review

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pathogens Review Betanodavirus and VER Disease: A 30-year Research Review Isabel Bandín * and Sandra Souto Departamento de Microbioloxía e Parasitoloxía-Instituto de Acuicultura, Universidade de Santiago de Compostela, 15782 Santiago de Compostela, Spain; [email protected] * Correspondence: [email protected] Received: 20 December 2019; Accepted: 4 February 2020; Published: 9 February 2020 Abstract: The outbreaks of viral encephalopathy and retinopathy (VER), caused by nervous necrosis virus (NNV), represent one of the main infectious threats for marine aquaculture worldwide. Since the first description of the disease at the end of the 1980s, a considerable amount of research has gone into understanding the mechanisms involved in fish infection, developing reliable diagnostic methods, and control measures, and several comprehensive reviews have been published to date. This review focuses on host–virus interaction and epidemiological aspects, comprising viral distribution and transmission as well as the continuously increasing host range (177 susceptible marine species and epizootic outbreaks reported in 62 of them), with special emphasis on genotypes and the effect of global warming on NNV infection, but also including the latest findings in the NNV life cycle and virulence as well as diagnostic methods and VER disease control. Keywords: nervous necrosis virus (NNV); viral encephalopathy and retinopathy (VER); virus–host interaction; epizootiology; diagnostics; control 1. Introduction Nervous necrosis virus (NNV) is the causative agent of viral encephalopathy and retinopathy (VER), otherwise known as viral nervous necrosis (VNN). The disease was first described at the end of the 1980s in Australia and in the Caribbean [1–3], and has since caused a great deal of mortalities and serious economic losses in a variety of reared marine fish species, but also in freshwater species worldwide. The causative agent of VER was first described as a “picorna-like virus” [4,5], but after the characterization of a virus purified from diseased larval striped jack (Pseudocaranx dentex), it was considered a new member of the family Nodaviridae [6]. This first piscine nodavirus was designated as striped jack nervous necrosis virus (SJNNV). Afterwards, piscine nodaviruses were also identified as the causative agents of VER outbreaks in other fish species, such as European and Asian seabass (Dicenthrarchus labrax and Lates calcarifer, respectively) [7]. The International Committee on taxonomy of viruses (ICTV) included the piscine nodaviruses within the genus Betanodavirus of the family Nodaviridae in their seventh report [8], grouping seven species, that were later reduced to the four recognized at present: red-spotted grouper nervous necrosis virus (RGNNV), barfin flounder nervous necrosis virus (BFNNV), tiger puffer nervous necrosis virus (TPNNV) and SJNNV in the eighth report [9]. The first isolation of a betanodavirus was obtained from diseased sea bass using the SSN-1 cell line from whole fry tissue of striped snakehead Ophicephalus striatus [10]. Over the last 30 years, numerous research articles on betanodaviruses and VER have been published and a considerable amount of knowledge on the disease and causative viruses is available at present. However, further research is needed in terms of virus–host interaction, viral transmission (infection routes, differences in host range among genotypes, viral stability in different environmental Pathogens 2020, 9, 106; doi:10.3390/pathogens9020106 www.mdpi.com/journal/pathogens Pathogens 2020, 9, 106 2 of 46 conditionsSustainability::: ), 2019 disease, 11, x FOR epidemiology PEER REVIEW (i.e., reservoirs, impact of global warming on the development2 of 50 and spreadenvironmental of the disease conditions…),::: ) and disease infection epidemiology control in (i.e. fish, reservoirs, farms. In thisimpact review, of global we presentwarming the on latest findingsthe relateddevelopment to the and betanodavirus spread of the host disease…) range and and infection distribution, control with in fish special farms. emphasis In this review on genotypes,, we host–viruspresent interaction, the latest findings and VER rel epidemiology,ated to the betanodavirus as well as diagnosticshost range and and distribution, potential control with special measures for theemphasis disease. on genotypes, host–virus interaction, and VER epidemiology, as well as diagnostics and potential control measures for the disease. 2. The Virus 2. The Virus 2.1. Viral Structure 2.1. Viral Structure NNV is a small non-enveloped virus with a diameter of around 25–30 nm and a T = 3 icosahedral symmetryNNV (180 copiesis a small of anon single-enveloped protein) virus [6]. Thewith virala diameter genome of isaround composed 25–30 of nm two and single-stranded a T = 3 icosahedral symmetry (180 copies of a single protein) [6]. The viral genome is composed of two positive-sense RNA molecules known as RNA1 (1.01 106 Da) and RNA2 (0.49 106 Da), both co-packaged single-stranded positive-sense RNA molecules known× as RNA1 (1.01 × 106 Da)× and RNA2 (0.49 × 106 into a single virion (Figure1). The 5’-ends of these RNAs are capped but their 3’-ends are not polyadenylated. Da), both co-packaged into a single virion (Figure 1). The 5’-ends of these RNAs are capped but their The biggest3’-ends segment, are not RNApolyadenylated. 1, is composed The ofbiggest around segment, 3100 nucleotides RNA 1, is (nt) composed and contains of around an open 3100 reading framenucleotides (ORF) for the(nt) RNA-dependent and contains an RNA-polymerase open reading (RdRp),frame also(ORF) known for the as proteinRNA-dependent A. RNA2, the smallestRNA segment-polymerase (1410–1433 (RdRp), nt),also codes known for as the protein capsid A. proteinRNA2, the (CP) smallest [6,11]. segment In addition, (1410 a–1433 subgenomic nt), RNA,codes called for RNA3 the capsid (371–378 protein nt), (CP) which [6,11] is. notIn addition, packaged a subgenomic into virions, RNA, is synthetized called RNA3 from (371 the–378 3’-end nt), of RNA1which [12–14 is ]not and packaged codes for into two virions, non-structural is synthetized viral from proteins: the 3’- B1end and of RNA1 B2. [12–14] and codes for two non-structural viral proteins: B1 and B2. FigureFigure 1. Schematic 1. Schematic overview overview of the betanodavirusof the betanodavirus replication replication cycle: Aftercycle: entry,After theentry, viral the bisegmented viral singlebisegmented stranded (+ )single RNA stranded genome (+) is releasedRNA genome into the is cytoplasm.released into Subsequently, the cytoplasm host. Subsequently, ribosomes host translate the viralribosomes RNA1 translate into the the viral viral RNA-dependent RNA1 into the viral RNA RNA polymerase-dependent (RdRp) RNA polymerase (A). The RdRp (RdRp) is then(A). The used to copy theRdRp genomic is then used (+) RNA1, to copy synthetizing the genomic a(+) ( RNA1,) RNA synthetizing strand and a generating (−) RNA strand a dsRNA and generating (B). The dsRNA a − is nowdsRNA used for(B). replicationThe dsRNA/ transcriptionis now used for into replication/transcription new RNA1 molecules into (C), new all RNA1 this process molecules takes (C), placeall in this process takes place in association with outer mitochondrial membranes. Afterwards, a association with outer mitochondrial membranes. Afterwards, a sub-genomic RNA, namely RNA3, sub-genomic RNA, namely RNA3, is synthesized from the 3’ terminus of RNA1(D). RNA3 encodes is synthesized from the 3’ terminus of RNA1(D). RNA3 encodes -and is translated into- the two -and is translated into- the two small proteins B1 and B2 (E) which show nuclear localization. In smalladdition, proteins RNA3, B1 and presumably B2 (E) which like show in alfanodavirus, nuclear localization. also regulates In addition, RNA2 synthesis RNA3, presumably(F) and it is like in alfanodavirus,downregulated also at the regulates onset of RNA2RNA2 replication/transcription synthesis (F) and it is (dotted downregulated line). RNA2 at translation the onset yields of RNA2 replicationthe capsid/transcription protein (G) (dotted and, finally line)., nascent RNA2 (+) translation RNA1 and yields (+) RNA2 the capsidmolecules protein are packaged (G) and, into finally, nascent (+) RNA1 and (+) RNA2 molecules are packaged into progeny virions (H). Adapted from SMART (Servier Medical Art), licensed under a Creative Common Attribution 3.0 Generic License. http://smart.servier.com/. Pathogens 2020, 9, 106 3 of 46 Protein A, one of the three non-structural proteins of the virus, has a molecular weight of 110 kDa and a variable size depending on the viral genotype: 983 amino acids (aa) in SJNNV, 982 aa in RGNNV and 981 aa in BFNNV [12,14,15]. The capsid protein (338 aa, except the CP of SJNNV, which is 2 aa longer), has a molecular weight of 37 kDa [11,15–17]. In Alphanodavirus, upon genome encapsidation, the precursor of the capsid protein, protein α, is auto-catalytically cleaved into proteins β and γ [18], generating the mature capsid. This mechanism was not observed in betanodavirus [11]. Instead, the capsid protein undergoes conformational changes which are important for its structure and functions. Intramolecular disulfide bondings between cysteines 187 and 201 [19] or cysteines 115 and 201 [20] have been shown to play a role in the assembly and thermal stability of the viral particles. The structure of the Grouper nervous necrosis virus (GNNV) CP has been disclosed [21] and consists of three different domains and a flexible linker region. The N-terminal arm (N-arm)
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