- Open Access
Host range, host specificity and hypothesized host shift events among viruses of lower vertebrates
© Bandín and Dopazo; licensee BioMed Central Ltd. 2011
- Received: 19 July 2010
- Accepted: 18 May 2011
- Published: 18 May 2011
The successful replication of a viral agent in a host is a complex process that often leads to a species specificity of the virus and can make interspecies transmission difficult. Despite this difficulty, natural host switch seems to have been frequent among viruses of lower vertebrates, especially fish viruses, since there are several viruses known to be able to infect a wide range of species. In the present review we will focus on well documented reports of broad host range, variations in host specificity, and host shift events hypothesized for viruses within the genera Ranavirus, Novirhabdovirus, Betanodavirus, Isavirus, and some herpesvirus.
- Sockeye Salmon
- Infectious Salmon Anaemia Virus
- Infectious Pancreatic Necrosis Virus
- Interspecies Transmission
- Senegalese Sole
Ranaviruses - Interspecies and interclass transmission
Betanodaviruses - The role of mutation and reassortment in host specificity
Novirhabdoviruses - Infectious haematopoietic necrosis virus and viral haemorrhagic septicaemia virus, two different strategies within the same genus
Infectious salmon anaemia virus: Orthomyxoviruses "made for the change"
Herpesviruses: Very host specific viruses?
Aquabirnaviruses - Putative candidate for interspecies transmission but still not demonstrated
The successful replication of a viral agent in a host is a complex process which consists of a number of interactions, most of them related to the coevolution of pathogen and host. This coevolution often leads to a species specificity of the virus and can make interspecies transmission difficult. Therefore, natural host range switches by viruses are rare events. However, when they occur the results can become severe because the viruses may then spread widely through non previously adapted, and therefore immunologically naïve host populations.
Upon transmission to a new host species, viruses must usually adapt to a new genetic and immunologic environment in order to replicate and spread to other individuals within the species . The high rates of mutation and replication of RNA viruses, such as human immunodeficiency virus (HIV) and influenza, facilitate the occurrence and fixation of those mutations that become beneficial under certain conditions . Viral adaptations to new hosts primarily manifest as amino acid substitutions which can allow more efficient virus cell entry into the new host [3, 4], block interactions with detrimental host proteins [5, 6] or promote escape from both the new and the old host's immune responses [7, 8].
Influenza A is the paradigm of a virus capable of interspecies and interclass transmission. Those viruses are found in humans as well as in other animals, including swine, horses and birds, waterfowl being considered the natural reservoir . Subtypes of Influenza A are distinguished by the two surface glycoproteins: haemagglutinin (HA) and neuraminidase (NA). Periodically a subtype of influenza can make the shift from aquatic birds to humans, possibly through an intermediate host, resulting in a widespread pandemic in an immunologically naïve population. These antigenic shifts can occur either through the transfer of an entire virus from one host to another or through a reassortment process where genomic segments of the avian virus mix with genomic segments of a virus currently circulating in humans.
A number of proteins have been implicated in determining host specificity of the virus. Influenza haemagglutinin binds to sialic acid linked to galactose on the surface of the targeted cell, and the differing nature of the sialic acid-galactose linkages in birds and humans provides an important barrier to host shift events. In this sense, a number of amino acid substitutions have been produced in influenza haemagglutinin to adjust to the different receptors [10–14]. Neuraminidase, the protein responsible for cleaving the haemagglutinin from the receptor surface, also seems to be adapted to the particular sialic acid linkages . Proteins in the viral replication complex (PA, PB1, PB2 and NP) have also been implicated in limiting host range by restricting replication and intra-host spread in mammals (for a review see ). In particular, a specific substitution in the PB2 gene has been identified as crucial for replication and intra-host spread in mammals [17–19].
Severe acute respiratory syndrome coronavirus (SARS-CoV) is a recently identified human coronavirus. The extremely high homology of the viral genomic sequences between the viruses isolated from humans (huSARS-CoV) and those of palm civet origin (pcSARS-CoV) suggested possible palm civet-to-human transmission. Genetic analysis revealed that the spike (S) protein of pcSARS-CoV and huSARS-CoV was subjected to the strongest positive selection pressure during transmission, and there were six amino acid residues within the receptor binding domain of the S protein that were potentially important for SARS progression and tropism. It has been demonstrated that the double substitution of two amino acid residues of pcSARS-CoV for those of huSARS-CoV made pcSARS-CoV capable of infecting human cells , suggesting that these two residues are involved in the palm civet-human transmission.
Under certain circumstances, even a genetically stable DNA virus can gain the mutation required to adapt to a new host. That is the case of canine parvovirus (CPV) which emerged in 1978 as the cause of new enteric and myocardial diseases in dogs. The new virus spread globally in a pandemic and has since remained endemic in dogs throughout the world [20, 21]. Phylogenetic analysis showed that all CPV isolates obtained so far, termed CPV type 2, descended from a single ancestor closely related to the feline panleukopenia virus (FPV) which infects cats, mink and raccoons, but not dogs or cultured dog cells . FPV and CPV type 2 isolates differ by as little as 0.5% in DNA sequence and it is possible that changes of only two amino acid residues in the capsid protein could have introduced the canine host range [22, 23]. During 1979 a CPV variant (CPV type 2a) emerged, spread worldwide within 1 year and replaced the CPV type 2 strain. CPV type 2a contained five substitutions in the capsid sequence compared to CPV type 2 and also infected and caused disease in cats [24–26]. Therefore, the emergence of CPV seems to have been a multistep process, where a small number of mutations in the capsid protein gene allowed the virus to efficiently infect and spread within a new host order .
Viruses of lower vertebrates include a large number of viral agents, belonging to different viral families and genera, with RNA and DNA genomes, and displaying different host specificities. In fact, some viruses have a very narrow host range, whereas others are known to be able to infect a wide range of species. The wide host range suggests that, in any moment along the viral evolution, those viruses may have been involved in different host shift events. In the present review we will focus on well documented or hypothesized cases of host shift as well as variations in host range for the genera Ranavirus, Novirhabdovirus, Betanodavirus, Isavirus and several herpesvirus. However, the suspicion for interspecies transmission in other fish viruses remains.
Piscine nodaviruses belong to the genus Betanodavirus, within the family Nodaviridae. Betanodaviruses are the aetiological agents of the disease known as viral nervous necrosis (VNN) or viral encephalopathy and retinopathy (VER), a devastating neuropathological condition that affects marine fish worldwide . The affected fish developing clinical signs show abnormal swimming, neurological problems and buoyancy control loss.
Fish species affected -in natural infections- by viral nervous necrosis (VNN).
Taiwan, India, Singapore, Malaysia, Australia, Israel, Tahiti, Indonesia
Japanese sea bass
Atlantic Canada, Atlantic USA, Norway, UK
Atlantic Canada, Atlantic USA
Martinique, Italy, Greece, Spain, Malta, Portugal, Israel
Red spotted grouper
146, 147, 171]
Malaysia, Phillipines, Singapore
Spottet coral grouper
Caspian sea (Iran)
Gilthead sea bream
Israel, France, Italy, Iberian Peninsula
Betanodaviruses are small (25-30 nm), nonenveloped, icosahedral RNA viruses. The genome consists of two single stranded, positive-sense molecules. The larger genomic segment, RNA1 (3.1 kb), encodes the RNA dependent RNA polymerase (RdRp) of approximately 100 kDa, also named protein A [74, 75]. The smaller segment, RNA2 (1.4 kb), encodes the capsid protein of about 42 kDa [74, 76]. In addition, a subgenomic RNA3 is synthesised during RNA replication from the 3' terminus of RNA1.
Betanodaviruses have been classified into four genotypes, designated SJNNV (striped jack nervous necrosis virus), TPNNV (tiger puffer nervous necrosis virus), RGNNV (red grouper nervous necrosis virus) and BFNNV (barfin flounder nervous necrosis virus), using a partial sequence of RNA2, the T4 region, which is a highly variable region of around 400 nt [77, 78]. These types exhibit different capabilities for infecting fish species. Thus, RGNNV shows the broadest host range and causes disease in a variety of warm-water fish species, BFNNV is restricted to cold-water marine fish species and TPNNV infects only one species . With regards to the SJNNV type, although for several years it was considered to be restricted to a few species present in Japanese waters [72, 78], in recent years it has been found in Senegalese sole Solea senegalensis[79, 80] as well as gilthead sea bream Sparus aurata and sea bass cultured in the Iberian Peninsula . More recent studies  reported that most of the betanodavirus strains infecting Senegalese sole and gilthead sea bream, previously typed as SJNNV on the basis of the T4 region, were in fact RGNNV/SJNNV reassortants. Olveira et al.  observed that the reassortant strains exhibited a slightly modified SJNNV capsid, with three different amino acid positions in all strains (the differences increased to a maximum of six in some strains). One of these changes observed in residue 247 was encoded by the nucleotide triplet 737-739, which was included in the region between nucleotides 695 and 765, described previously by Ito et al.  as a host specificity determinant. Another change in the amino acid sequence at residue 270 was also observed on the C-terminal side of the capsid protein. These results confirmed that C-terminal protruding domains of the capsid protein are involved in host specificity, as reported previously by Iwamoto et al.  and Ito et al. . It is well known that even a small number of amino acid substitutions in the capsid proteins can have dramatic effects on the host specificity of different animal viruses . In this case, the changes observed in the SJNNV capsid seem to have allowed it to efficiently infect and spread within two new hosts, causing epizootic outbreaks in Senegalese sole and gilthead sea bream, which were not previously considered susceptible to SJNNV.
Other authors have also reported the existence of reassortants among betanodavirus isolates obtained from symptomatic sea bass harbouring an RNA1 segment of SJNNV type and an RNA2 of RGNNV type . These data indicated that both combinations of genomic segments of SJNNV and RGNNV genotypes are successful and allow the resultant reassortant strains to produce disease. Interestingly, a certain relationship between the type of reassortant and the susceptible host species seems to exist: SJ/RG affecting sea bass and RG/SJ affecting Senegalese sole and gilthead sea bream.
Souto et al.  experimentally demonstrated the pathogenicity of the reassortant RG/SJ strains for Senegalese sole and compared it to that of the parental strains (RGNNV and SJNNV). Mortality was recorded only in the fish infected with the RG/SJ strains and betanodavirus were re-isolated from dead fish, fulfilling the River's postulates. However, virus was detected by RT-PCR and isolated from all pools of fish inoculated with RGNNV and SJNNV strains. These results indicate that both genotypes can replicate in Senegalese sole with no evident pathological effects and that the changes produced after the reassortment account for the pathogenicity for Senegalese sole.
Infectious salmon anaemia virus (ISAV), the etiological agent of infectious salmon anaemia (ISA), is an RNA virus of the family Orthomyxoviridae, the only member of the genus Isavirus. The genome of ISAV consists of eight segments of linear negative-sense single- stranded RNA. Viral particles are enveloped, with a diameter of 90-140 nm, and show surface projections consisting of a combined haemagglutinin-esterase (HE) protein encoded on segment 6  and a separate fusion (F) protein encoded on segment 5 .
ISA is characterized by high mortality, and natural outbreaks have only been described in farmed Atlantic salmon. However, ISAV has been reported in both wild salmonid and non-salmonid fish [113–115], and the virus may, under experimental conditions, persist and replicate in other salmonid (Salvelinus alpinus, O. mykiss, O. keta, O. kisutch) [116–119] and non-salmonid fish (Clupea harengus, Gadus morhua) [120, 121].
The HE surface glycoprotein is the molecule with the highest sequence variability, and is assumed to be of importance in determining virulence. Most of the variation in this molecule is concentrated on a small highly polymorphic region (HPR). It is widely assumed that the source of the virulent ISAV isolates is an ISAV variant- designated HPR0- without any deletion in the HPR gene. The non-virulent nature of HPR0 viruses was indicated by the lack of disease in vivo and by their failure to replicate in cell culture [113, 122]. The widely held model suggests that virulent variants of the HPR0 archetype arise by deletion of several nucleotides in the HPR [113, 123, 124]. The driving forces behind the differential deletion patterns in the HPR could be analogous to a phenomenon described for Influenza A neuraminidase, where varying lengths of the stalk region have been reported, a property that was associated to host range adaptation [125, 126]. Following this theory and on the basis of a phylogenetic analysis of the HPR region, Mjaaland et al.  suggested that European ISA outbreaks may have been the result of several independent introductions of virus into farmed Atlantic salmon from wild fish, followed by adaptation to the new host through parallel but varied hemagglutinin gene deletions.
A recent study by Markussen et al.  has provided evidence for the role of recombination and reassortment in the evolution of ISAV. Those authors have demonstrated the existence of a new marker of virulence next to one of the two potential cleavage sites in the F protein and suggest that a single amino acid mutation may alter the recognition site, having a direct effect on the virulence of the virus. Markussen et al.  also suggested that the alterations at the cleavage site of the ISAV F protein together with deletions in the HPR region, most likely represent an adaptation of ISAV to Atlantic salmon from an unidentified reservoir, which leads to disease in densely populated fish farms.
However, Kibenge et al.  have postulated an alternative evolutionary model, which, in contrast to the widely accepted deletion theory, suggests that the original ancestral ISAV was virulent and that the insertion of specific motifs resulted in its attenuation. This last theory would not support a wild origin of ISAV because "wild" viruses are expected not to be as virulent as the farming-associated viruses. In natural conditions a balance between the virus and the host is expected to be maintained. However, this balance will be broken under intensive rearing conditions, conducive to an increase of virulence.
Herpesviruses (HVs) infect a wide variety of vertebrate hosts including mammals, birds, reptiles, amphibians and fish, and at least one invertebrate group, bivalve molluscs. HV share a characteristic virion structure, which consists of a large, linear, double-stranded DNA genome, an icosahedral capsid, a proteinaceous matrix (the tegument) and an envelope containing viral proteins .
Members of the family Alloherpesviridae and other fish herpesvirus isolated in cell culture.
Common name (abbreviation)
Cyprinid herpesvirus 1
Cyprinid herpesvirus 2
Cyprinid herpesvirus 3
Koi Herpesvirus (KHV)
Ictalurid herpesvirus 1
Channel cat fish virus (CCV)
Ictalurid herpesvirus 2
Ictalurus melas herpesvirus (ICmHV)
Acipenserid herpesvirus 2
White sturgeon HV2
Salmonid herpesvirus 1
HV salmonis (HPV)
Salmonid herpesvirus 2
Oncorhynchus masou virus (OMV)
Yamame tumor virus (YTV)
Oncorhynchus kisutch virus (OKV)
Coho salmon tumor virus (COTV)
Coho salmon herpes virus (CSH)
Ranid herpesvirus 1
Lucké tumor HV (LTHV)
Ranid herpesvirus 2
Frog virus 4 (FV-4)
Anguillid herpesvirus 1
Percid herpesvirus 1
HV vitreum, walleye HV
As a general rule, the natural host range of mammalian and avian HV is highly restricted, and most herpesviruses are thought to have evolved in association with single host species , but exceptions have been reported among mammals . On the basis of a comparative phylogenetic study of different hosts and fish herpesviruses, Waltzek et al.  indicate that some fish (salmonid, ictalurid and ciprinid) and ranid HV may have coevolved with their hosts, at least at the tips of the phylogenetic tree. However, the phylogenetic analysis revealed an overall discordance between HV and host lineages. One example of these discordances is provided by the family Acipenseridae (sturgeons), an ancient fish lineage and the sturgeon HV (AciHV1 and AciHV2) which are not sister taxa, with AciHV2 being the sister group of the ictalurid HV. Another example is provided by the eel HV (AngHV1), which grouped tightly with cyprinid HV. These authors suggested that the lack of cospeciation at deep nodes in the phylogenetic tree may indicate the existence of interspecies transmission.
There is clear evidence of interspecies transmission of OsHV-1 in marine bivalves [132, 133]. Although OsHV-1 was first isolated from the moribund larval Japanese oyster Crassostrea gigas, a variant of OsHV-1 (termed OsHV-1var) was detected in the Manila clam Ruditapes philipinarum and subsequently in French scallops Pecten maximus.
The wide host range shown by many viruses affecting lower vertebrates is well known. In fact, for some of them -those historically most extensively studied- the list of susceptible species is surprisingly extensive. The best example are aquabirnaviruses. However, some others are only virulent to one or to a very narrow number of species. This diversity of host specificity patterns has not been well studied, and it is therefore poorly understood at present. In this sense, the status of knowledge varies dramatically among the different viral groups. In fact, for many of them only characterisation of field isolates has been performed, focusing on natural hosts, transmission pathways, genetic variation, etc. In a few cases, however, experimental studies have been conducted to document variations in host specificity between viral species (as for betanodaviruses) or between strains within a viral species (IHNV and VHSV). For some viruses, there is field data to support interspecies and interclass transmissions (ranavirus), for others, interspecies and interclass transmission is hypothesised based on phylogenetic relationships (novirhabdovirus, herpesvirus). For some, the molecular basis of host-specific virulence and/or host specificity has been investigated (ISAV, betanodavirus).
Compared with the examples from mammalian viruses described in the introduction, there are no absolutely certain examples of host shifts in fish viruses, but there are some that have been hypothesised based on reasonable evidence. The viruses tackled in this review are the few for which some information has been documented and is available at present, and could be summarised as follows.
Ranaviruses constitute a group of viruses with a broad host range, for which the interspecies and interclass transmission has been well documented; in addition, evidence for host shifts based on phylogenies and genome analyses is also available; however, to our knowledge, the molecular determinants and/or mechanisms for host-specificity have not been investigated.
A variation in host-specificity among the four viral genotypes of betanodaviruses is well documented. In addition, molecular determinants for their host specificity patterns have been investigated using natural reassortants and chimeric recombinant viruses. From these studies, specific amino acid changes have been identified as putatively associated with differences in host specificity.
In the case of novirhabdoviruses, variations in host specificity have been demonstrated among viral strains within both species -IHNV and VHSV-, although to a higher extent within VHSV. Although not scientifically demonstrated from a molecular basis, host shift/adaptation events could be hypothesised based on phylogenetic analyses. Moreover, whole genome sequence comparisons and infectious clones of IHNV and VHSV are now available, which are being used to study, and more deeply understand, host specificity determination in these viruses.
Several studies on the molecular basis of virulence of ISA virus have indicated that changes located in the haemagglutinin (HPR) and in the fusion protein are associated with outbreaks in Atlantic salmon. Based on phylogenetic analysis, it has been hypothesised that these changes could have been involved in a change in host specificity.
Phylogenetic analysis comparing fish herpesvirus and host lineages have revealed discordances that may suggest the existence of interspecies transmission. In addition, in mollusk bivalves there is field evidence of interspecies transmission of herpesviruses.
Finally, regarding aquabirnaviruses little information other than broad host range and diversity of IPNV (and aquabirnavirus in general) genogroups, has been reported. Similarly, there is no demonstration of variations in host specificity among different viral strains, and no studies on host specificity are available; the recently demonstrated occurrence of natural reassortment among field isolates could have some implication in determining the host specificity and virulence of these viruses, and will probably be investigated in the future.
The authors want to thanks Gael Kurath for her very interesting suggestions that helped to improve the quality of this review.
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