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University of Bergen, Department of Biology, N-5020 Bergen, Norway
Correspondence
A. Nylund
are.nylund{at}bio.uib.no
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Rolland & Winton, 2003; Kibenge et al., 2005). It has a negative-stranded RNA genome consisting of eight segments of between 1.0 and 2.4 kb in length. The host range for ISAV includes most of the salmonid species in the genera Salmo and Oncorhynchus in the North Atlantic (Nylund et al., 1994, 1997; Nylund & Jakobsen, 1995; Devold et al., 2000; Snow et al., 2001). The species most likely to be the reservoir host in Norway is the trout, Salmo trutta (Nylund et al., 2003; Plarre et al., 2005).
Studies of sequences of the haemagglutinin–esterase (HE) gene have shown that ISAV can be divided into two subtypes, a North American subtype (NA-ISAV) and a European subtype (EU-ISAV) (Devold et al., 2001; Kibenge et al., 2001; Krossøy et al., 2001b; Nylund et al., 2003; A. Nylund, H. Plarre, M. Karlsen, F. Fridell, K. F. Ottem, A. Bratland & P. A. Sæther, unpublished data). EU-ISAV can be further divided into groups reflecting origin and time of collection (A. Nylund, H. Plarre, M. Karlsen, F. Fridell, K. F. Ottem, A. Bratland & P. A. Sæther, unpublished data). It has also been suggested that the highly polymorphic region (HPR) just outside the transmembrane region (TMR) of the HE protein may be an important virulence factor (Cunningham et al., 2002; Nylund et al., 2003; Plarre et al., 2005). Further studies of the HPR groups may explain the variation in virulence exhibited by ISAV isolates with different HPRs (Mjaaland et al., 2005). However, it is well known from studies of other members of the family Orthomyxoviridae that virulence is determined by multiple genes (Brown, 2000). Change in virulence may be a result of crosses between two different parental virus strains (reassortant viruses), mutations (substitutions, deletions or insertions) or recombination (Gorman et al., 1992; Webster et al., 1992; Brown, 2000; Suarez et al., 2004).
A critical feature of virulent avian strains of Influenza A virus is their ability to productively infect all tissues of the host (Suarez et al., 2004). This is due to the insertion of several basic amino acids into the cleavage site of HA (Zambon, 1999). The HA in Influenza A virus is the receptor-binding and membrane-fusion glycoprotein, and cleavage of the precursor HA0 primes the HA for subsequent activation of membrane fusion at endosomal pH (Skehel & Wiley, 2000). ISAV differs slightly from this arrangement of surface proteins, having one protein with haemagglutinin and esterase activity, HE (Falk et al., 2004; Hellebø et al., 2004). The fusion activity is on a separate surface protein coded on segment 5 of the ISAV genome (Falk et al., 2004; Aspehaug et al., 2005). Hence, segment 5 is an integral membrane protein and a major surface antigen and, as such, is probably one of the major targets for the host immune response. The substitution rate is shown to be highest for the surface proteins of members of the family Orthomyxoviridae (Webster et al., 1992). The fusion protein could also be an important virulence factor, as it is required for infectivity (Lamb & Krug, 2001), which makes segment 5 an interesting part of the ISAV genome with respect to genotyping and studies of virulence.
The present study presents the nucleotide sequence of 57 ISAV isolates from the North Atlantic. The majority of the isolates are from Norway. The putative amino acid sequences are analysed with respect to identifying TMRs, coiled-coil regions (F3 domain), possible cleavage sites for activation of the fusion activity and a possible N-terminal fusion peptide that is inserted into the host membrane (Skehel & Wiley, 2000). Recombination between strands of segment 5 and between segment 5 and segment 3 (the nucleoprotein) is documented and the possible importance is discussed.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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) (A. Nylund, H. Plarre, M. Karlsen, F. Fridell, K. F. Ottem, A. Bratland & P. A. Sæther, unpublished data).
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). Reverse transcription was performed using Moloney murine leukemia virus reverse transcriptase (Promega) with random hexamers as described previously (Devold et al., 2001). Subsequently, the transcribed single-stranded cDNA served as template in PCR using Taq DNA polymerase (Pharmacia) according to recommended conditions. The following primers were used as upstream and downstream primers: upstream (S5F1), 5'-AGTTAAAGATGGCTTTTCTAACAATT-3' and downstream (S5R3), 5'-TTCTAAATTATCCAATAAAGGTCCTG-3'. The reaction cycle consisted of 4 min incubation at 94 °C and 35 cycles of 94 °C for 30 s, 55 °C for 45 s and 72 °C for 1 min, followed by extension at 72 °C for 10 min. The PCR products were stored at 4 °C before sequencing.
Sequencing.
PCR products were purified on QIAquick PCR Purification columns (Qiagen) and sequenced by using a BigDye Terminator Sequencing kit (Applied Biosystems). Sequencing was done by using the amplification primers described above in addition to the following upstream and downstream primers: S5F2 (5'-GAATCTATCGACAACGTGAGT-3') and S5R4 (5'-ACTACTCTGAATGAAATTTCATTGC-3'). The products were run on an ABI 377 DNA analyser (PE Biosystems). Nearly the complete open reading frame (ORF) of all isolates was sequenced.
Phylogeny.
The sequence data were assembled with the help of Vector NTI software (InforMax, Inc.) and GenBank searches were done with BLAST (2.0). The Vector NTI Suite software package (InforMax, Inc.) was used for the multiple alignments of nucleotide and deduced amino acid sequences. To perform pairwise comparisons between the different sequences from the 54 ISAV isolates (excluding isolates CCBB and ME/01), the multiple sequence-alignment editor GeneDoc was used. Sequences already available in GenBank/EMBL were also included in the comparisons (Table 1
).
The phylogenetic trees obtained by analysis of the F protein gene (positions 17–1335 in the ORF) were compared with phylogenetic trees obtained by analyses of the 5' end of the HE gene (positions 13–1014 in the ORF) from the same isolates (A. Nylund, H. Plarre, M. Karlsen, F. Fridell, K. F. Ottem, A. Bratland & P. A. Sæther, unpublished data). These parallel trees were constructed by using PAUP v4.0 (Swofford, 1998) with maximum likelihood as optimality criterion and the heuristic-search option. For the PAUP analysis, MODELTEST 3.6 (Posada & Crandall, 1998) was used to identify the models best suited to the datasets. For both the F gene tree and the HE gene tree, models were employed with estimated base frequencies, six substitution types with six-parameter instantaneous rate (estimated), among-site rate variation with estimated gamma shape value (HE gene, 
=0.3536; F gene, =0.9988) and an estimated PInvar value. Trees identical to the PAUP trees were obtained by using TREE-PUZZLE 5.2 (available at http://www.tree-puzzle.de) with the HKY model of sequence evolution (Hasegawa et al., 1985) and with eight-category gamma distribution to describe substitution-rate heterogeneities. The maximum-likelihood trees were bootstrapped (25 000 puzzling steps) in TREE-PUZZLE and the support values were transferred to the PAUP trees. To test the robustness of the maximum-likelihood trees, additional trees were constructed using parsimony as optimality criterion and the heuristic-search option in PAUP. These parsimony trees were bootstrapped using 1000 replicates. Phylogenetic trees were drawn by using TreeView (Page, 1996).
Substitution rates.
Rates of nucleotide substitution with 0.95 confidence intervals were calculated for the F gene tree and the HE gene tree (n=54) based on all nucleotide substitutions in the surface tail (St) region of the HE gene (1002 nt, i.e. nt 13–1014) and 1319 nt (nt 17–1335) in the ORF of the F gene (Nylund et al., 2003), by BASEML in the PAML v3.14 package (Yang, 1997), using the single-rate dated-tips (SRDT) model (Rambaut, 2000). This model assumes that a single rate of substitution applies for every branch in a rooted phylogenetic tree (molecular clock) and optimizes the length of the branches so that relative tip positions correlate with sampling dates. The phylogenetic trees used for this calculation were prepared in PAUP v4.0 as described above and rooted by using the North American ISAV isolates CCBB and ME/01 (GenBank accession nos AF404342
[GenBank]
and AY059402
[GenBank]
, respectively) as outgroup. A molecular clock was tested by a likelihood-ratio test, comparing the likelihood of the SRDT model with the likelihood of a different rate (DR) model (also calculated by BASEML; PAML), in which the branches are allowed to evolve with independent rates.
Computer analysis of the isolates.
The origin of the three different short inserts (INs) present in a few isolates was identified by using BLASTX. TMRs and coiled-coil regions in the protein sequence were predicted by using the TMHMM program (v1.0; Center for Biological Sequence Analysis, The Technical University of Denmark; http://www.cbs.dtu.dk) and Coiled-Coils from Protein Sequences (Lupas et al., 1991), respectively. Possible proteinase cutting sites were identified by using the Vector NTI Suite software package (InforMax, Inc.).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sequence variation
Three different nucleotide INs have been found in the ORF of segment 5: IN1 (isolate MR60/01), IN2 (isolate MR46/99) and IN3 (isolates MR61/01, MR62/01, MR71/02, SF57/00 and SF70/02) (Fig. 1). The length of IN1, IN2 and IN3 is 24, 33 and 30 nt, respectively. The latter two are inserted at a cutting site for trypsin (amino acids R267A268). The identity or origin of the IN nucleotide sequences was found by using a BLASTX search. The 24 nt sequence of IN1 (isolate MR60/00) is identical to a sequence from segment 3, the nucleoprotein (NP), stretching from positions 1100 to 1123 in the ORF of the NP. The other two INs are identical to nucleotide sequences near the 5' end of segment 5. IN2 is identical to a sequence stretching from positions 123 to 155 in the ORF of segment 5, whilst the sequence of IN3 is identical to a stretch from nt 93 to 122. The last two INs split a codon for alanine (A268).
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Phylogeny
In the present study, segment 6 (HE gene) and segment 5 (F gene) of the same isolates (n=54) have been analysed with respect to phylogenetic relationship (Figs 2 and 3). Phylogenetic analysis of alignments of segment 6, the haemagglutinin gene (HE), have shown that the ISAV isolates can be divided into two major subtypes, North American (NA-ISAV) and European (EU-ISAV) (Devold et al., 2001; Krossøy et al., 2001b; Nylund et al., 2003). EU-ISAV can be further divided into three major groups, EU-G1, EU-G2 and EU-G3 (Fig. 2a, b; A. Nylund, H. Plarre, M. Karlsen, F. Fridell, K. F. Ottem, A. Bratland & P. A. Sæther, unpublished data). The relationships within the groups are not fully resolved. This analysis is based on 1002 nt in the 5' end of the HE gene, excluding the region encoding the HPR, TMR and the cytoplasmic tail.
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). In this phylogeny, the isolate from Nova Scotia (NS2003) is located in EU-H1, but it shows a sequence similarity of only 96 % to the other isolates in this subgroup. The sequence similarities between the other isolates in this subgroup are between 99 and 100 %. Isolate SF14/95 also moves around and is not a permanent member of EU-H1. The phylogeny resulting from analysis of the F protein gene (segment 5) is, to a certain degree, similar to that obtained after analysis of the HE gene. However, a few isolates change group and the relationships within the groups change. Isolate N75/03 moves from EU-G2 to EU-G3, whilst the subgroups EU-MN and EU-N and isolate H51/00 move from group EU-G3 to EU-G2. EU-NN groups together with isolates in subgroups EU-MN and EU-N and isolate SF14/95. This relationship is supported by bootstrap values of 80 (maximum likelihood) and 98 (parsimony), respectively.
A few isolates change subgroup within the EU groups in the F gene phylogeny compared with the HE gene phylogeny. In EU-G1, NT81/03 changes position with the two isolates MR52/00 and H93/04 in being related most closely to the other EU groups when changing from HE gene to F gene phylogenies.
The relationships between the subgroups in EU-G3 are poorly resolved in both the HE gene and F gene phylogenies. EU-H2 is highly supported in the HE gene phylogeny (maximum likelihood), but is only moderately supported by using parsimony analysis (support value=71). In the F gene phylogenies, this subgroup is split in two, EU-H21 and EU-H22, excluding some of the isolates (Figs 2a, b, 3a, b).
Substitution rate of the HE gene
Overall substitution rates for EU-ISAV were calculated based on 1002 and 1319 nt in the ORFs of the HE and F protein genes, respectively. The resulting substitution rate of the HE gene (n=54 isolates, EU-ISAV) was 6.1(±0.3)x10–6 nt per site per year, whilst the F gene (n=54) gave a substitution rate of 8.6(±5.0)x10–5 nt per site per year. The 54 isolates cover a period of 17 years, 1987–2005. A molecular clock was rejected in both cases.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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that segment 5 of ISAV encodes the F protein, which is synthesized as a precursor protein, F0. The F0 protein is cleaved proteolytically to F1 and F2, which are held together by disulfide bridges. This cleaved protein is in a metastable, fusion-activated state and fusion activity can be triggered by low pH, high temperature or a high concentration of urea. It was suggested that the proteolytic-cleavage site is after residue K276 in the protein sequence (Aspehaug et al., 2005). Computer analysis of segment 5 sequences from all isolates (n=54) included in this study recognizes the same three possible transmembrane helices, trypsin-cleavage sites and coiled-coil region as those described from the two isolates presented by Aspehaug et al. (2005). In addition, three different INs have been found in the area where the proteolytic-cleavage site is expected to be located, and two new putative trypsin-cleavage sites are introduced in this area by IN3. All isolates carrying IN3 are the only members of subgroup EU-NW, whilst the other two INs, IN1 and IN2, are found in EU-G3 in subgroups EU-H21 and EU-H22, respectively. However, a common feature for all isolates carrying an IN is substitution of nt T797 by A797 in the ORF, which leads to amino acid substitution in the putative protein. In all but one (MR61/01) of these isolates, L266 is substituted by Q266, whereas L266 is substituted by H266 in MR61/01. Amino acid 266 in the ORF of the F protein is just in front of a trypsin-cleavage site, R267, located in the area where the proteolytic cleavage is expected to occur and 10 aa away from cleavage site K276, suggested by Aspehaug et al. (2005). It is not known whether the cleavage site for the precursor protein F0 is located at residue K276 or at residue R267, only that F0 can be cleaved by trypsin in this area. Both of these sites are putative trypsin-cleavage sites close to a possible transmembrane helix (I274–L292), suggested to be the fusion peptide (C276–Y291) by Aspehaug et al. (2005), and a coiled-coil region (G298–I353). Hence, the possibility that the INs may influence the accessibility of these sites to trypsin by perturbing the structure of F0 cannot be excluded.
Recombination is an important evolutionary mechanism and is one of the key factors shaping the structure of genes and genomes. It also plays a major role in contributing to and maintaining genetic diversity. However, in cases where recombination between homologous strands occurs, it can be difficult to detect that this has happened. Still, it is important to detect recombination events, as phylogenetic analysis can be biased severely by the presence of recombination. Recombination usually occurs by a template-switching mechanism, where the viral RNA-dependent RNA polymerase switches templates during replication, leaving one template and continuing synthesis of the progeny strand on a second template. Both homologous and non-homologous recombinations have been documented from different RNA virus families. Recombination events have previously been suggested to be an important factor changing the HPR of segment 6 (HE gene) in ISAV (Devold et al., 2001) and, in phylogenetic analysis using this gene, only the 5' end, excluding the HPR and the 3' end, is used (A. Nylund, H. Plarre, M. Karlsen, F. Fridell, K. F. Ottem, A. Bratland & P. A. Sæther, unpublished data). However, it has been difficult to document that it is recombination and not just deletions that are shaping the HPR in the HE gene. The INs in the F gene presented in this study show, however, that recombination events are shaping the ISAV genome and could be an important mechanism in the evolution of ISAV. Two of the INs, IN2 and IN3, are results of recombination between strands of the F gene, whilst IN1 is a result of recombination between the F gene and segment 3, the nucleoprotein gene (NP gene). The fact that recombination events are a mechanism in the evolution of the F gene also lends support to the suggestion that the same mechanisms could be shaping other parts of the ISAV genome, such as the HE gene.
During an outbreak of influenza A in chickens in Chile, a highly pathogenic virus (HPAI) was isolated (Suarez et al., 2004). Sequence analysis of all genes showed only minor differences between this isolate and low-pathogenic isolates (LPAI) in the same area, with the exception of changes at the HA-cleavage site. The highly pathogenic isolate had a 30 nt IN, which probably occurred by recombination between the HA and nucleoprotein genes, resulting in a virulence shift (Suarez et al., 2004). The difference between LPAI and HPAI is that the former are limited to cleavage by host proteases, such as trypsin-like enzymes, and are thus restricted to replication at sites in the host where such enzymes are found, whereas the latter allow HA0 to be cleaved by ubiquitous host proteases. Phylogenetic analysis of HPAI viruses shows that they do not constitute separate phylogenetic lineages, but appear to arise from low-pathogenic strains (Röhm et al., 1995; Banks et al., 2000). The precursor F0 from ISAV is also cleaved by trypsin-like proteases (Aspehaug et al., 2005) and, in all isolates studied, there are two cleavage sites in the cleavage area. The present study also shows that F0 proteins from ISAV may have INs close to these cleavage sites. IN1 and IN3 introduce new basic amino acids into the cleavage area, whereas IN2 introduces no new basic amino acids into this area. As nearly all European ISAV isolates from salmonid aquaculture are pathogenic to the salmon and systems to check differences in pathogenicity are not readily available, it has not been possible so far to see whether the INs in the F protein do influence the virulence of ISAV. However, this should be addressed in future studies and these studies should also test whether the INs influence the range of proteases that may cleave the precursor F0. Such studies should also have a closer look at possible interactions between the HE and the F proteins, as surface proteins of infectious particles.
The present study of the F gene sequences confirms the finding from previous studies, based on the HE gene, separating ISAV into two subtypes: a North American (NA-ISAV) and a European (EU-ISAV) subtype (Devold et al., 2001; Krossøy et al., 2001a; A. Nylund, H. Plarre, M. Karlsen, F. Fridell, K. F. Ottem, A. Bratland & P. A. Sæther, unpublished data). A molecular clock was not supported, and, hence, the time of separation between NA-ISAV and EU-ISAV could not be calculated.
The rate of nucleotide substitution is a function of both the rate of mutation and the rate of replication, which means that fluctuations in population size will affect substitution rates and their constancy over time (Jenkins et al., 2002). Hence, it can be expected that the molecular evolution of the HE and F genes may have sped up since the introduction of ISAV into salmonid-culture systems. However, this need not be the case if most of the genetic variation that is generated during ISAV replication in marine salmon farms is lost when the fish are slaughtered at commercial size or culled after an outbreak of ISA. The low substitution rate of both segments encoding the HE and F proteins, compared with the substitution rate of these genes in other orthomyxoviruses, gives no reason to suspect increased evolution of ISAV due to increased availability of salmonid hosts. Limited horizontal transmission between marine farms means that the main transmission route for ISAV will be from broodfish via eggs and embryos to smolt, i.e. vertical transmission (Anonymous, 2005; A. Nylund, H. Plarre, M. Karlsen, F. Fridell, K. F. Ottem, A. Bratland & P. A. Sæther, unpublished data). It has been fairly well documented that vertically or sexually transmitted viruses will have reduced virulence and will lose much of the genetic variability present in the adult hosts (Bergstrom et al., 1999; Jenkins et al., 2002). If vertical transmission is dominating, the bottleneck effect on the ISAV population will be strong, reducing both variation and virulence.
The capacity for molecular-phylogenetic analysis to resolve complex epizootiological problems in fish aquaculture has been demonstrated for several viruses (Kurath et al., 2003; Einer-Jensen et al., 2004, 2005; Snow et al., 2004; Thiéry et al., 2004; Hodneland et al., 2005; A. Nylund, H. Plarre, M. Karlsen, F. Fridell, K. F. Ottem, A. Bratland & P. A. Sæther, unpublished data). Such sequence analysis can provide important information about the spreading of pathogens, information that can be used by fish-disease management as a tool in decision making. The present study shows that the basic structure of phylogenies based on the HE and F genes (Fig. 2a, b, 3a, b) is similar. Most of the subgroups are supported irrespective of method of analysis, but the relationships between these are not consistent. It should be pointed out that the relationships between the subgroups within EU-G2 and G3 are poorly resolved or unresolved. Hence, the most significant change is the movement of subgroups and isolates from EU-G2 to EU-G3 and vice versa. The most parsimonious explanation for this is that these cases represent examples of reassortment. A consequence of this is that a genotyping system meant to trace the origin and history of ISAV isolates should include sequences from more than one segment. Sequences of the St region of the HE gene and the whole ORF of the F gene are promising candidates as backbones of a genotyping system. These two ISAV segments are promising tools for the future management of ISAV in Norway.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 14 November 2005;
accepted 23 February 2006.
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