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Short Communication |
1 Laboratorio de Virología Molecular, Centro de Investigaciones Nucleares, Facultad de Ciencias, Iguá 4225, 11400 Montevideo, Uruguay
2 Department of Biochemistry and McGill Cancer Center, McGill University, Montreal, QC H3G 1Y6, Canada
3 Laboratorio de Organización y Evolución del Genoma, Instituto de Biología, Facultad de Ciencias, Iguá 4225, 11400 Montevideo, Uruguay
Correspondence
Juan Cristina
cristina{at}cin.edu.uy
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ABSTRACT |
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A table showing the origins of French genotype IA HAV strains is available with the online version of this paper.
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). The structure of HAV, its tissue tropism and genetic distance from other members of the family Picornaviridae, indicate that HAV is unique within this family (Costa-Mattioli et al., 2003; Ticehurst et al., 1989; Martin & Lemon, 2006). HAVs have been classified in three human (I, II, III) and three simian (IV, V, VI) genotypes (Costa-Mattioli et al., 2002, 2003). The first estimations of HAV mutation rate were done in cell culture by passage of plaque-purified reference strain HAV pHM175 43c in FRhK-4 cells. These studies determined a rate of 1x10–3–1x10–4 substitutions per site (Sanchez et al., 2003a). More recently, using partial VP1 gene sequences, the substitution rate of HAV was predicted to be 1.30x10–3 substitutions per site per year (Hanada et al., 2004).
In order to gain insight into the evolutionary rate and mode of evolution of HAV in natural populations, we have analysed full-length sequences of the highly variable gene, VP1, of genotype IA HAV strains isolated in France from 1984 to 2001 (for details on isolates, origin and sequences see Costa-Mattioli et al., 2003 and Supplementary Table S1, available with the online version of this paper).
Nucleotide sequences of the entire VP1-coding region were aligned using the CLUSTAL W program (Thompson et al., 1994).
We first tested whether a recombination event occurred on any of the sequences used in these studies. We used two approaches implemented in the SimPlot Program (Lole et al., 1999): (i) a sliding window analysis of distances and (ii) bootscanning (Salminen et al., 1995). No recombinant strains were found in the dataset (not shown).
To precisely estimate HAV substitution, we used a Bayesian Markov chain Monte Carlo (MCMC) approach as implemented in the BEAST package (Drummond & Rambaut, 2005; BEAST v1.0, available from http://beast.bio.ed.ac.uk/Main_Page).
The program MODELGENERATOR (Keane et al., 2006) was used to identify the optimal evolutionary model (Akaike information criteria and hierarchical likelihood ratio test indicated that the GTR+
model best fitted the sequence data). Different population dynamic models were used (constant population size, exponential population growth, logistic population growth and Bayesian skyline). All the analyses consistently revealed similar evolutionary rates. Statistical uncertainties in the data are reflected by the 95 % highest probability density (HPD) values.
The results shown in Table 1 are the outcome of the analysis for 20 million steps of the MCMC, using the GTR+ model partitioned by codon position, a relaxed clock (Drummond et al., 2006) and the Bayesian Skyline model for population growth (Drummond et al., 2005). Results were examined using the TRACER program from the BEAST package. Convergence was assessed with ESS (effective sample size) values, after a burning of 5 million steps.
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, when the GTR+ model is used, a mean rate of 9.76x10–4 nucleotide substitution per site per year was obtained. Since the majority of the reports on substitution rates of members of the family Picornaviridae relate to estimates of synonymous substitution rates, we have made a rough estimation of the synonymous substitution rate of HAV in order to make comparisons possible (see Table 2). We have found that the substitution rate at the 3rd codon position is 2.38x10–3 substitutions per site per year, and that approximately half of the 3rd codon positions are synonymous. This indicates that the estimation of synonymous substitution rate should be around 5x10–3 substitutions per site per year. In addition, following a method similar to method 1 of Hanada et al. (2004), we used PAML software (available at http://abacus.gene.ucl.ac.uk/software/paml.html) to estimate synonymous rates under different substitution models, and the results yielded a mean value of 4x10–3 substitutions per site per year. Thus, in spite of the approximate nature of the calculation, it is possible to conclude that HAV synonymous substitution rate is clearly lower than that observed for other representative members of the family Picornaviridae (Table 2). In this sense, this rate, obtained using complete VP1 sequences from isolates from natural HAV populations and a Bayesian MCMC approach, is in agreement with previous results (Hanada et al., 2004).
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have shown that variation in synonymous substitution rates is linked to differences in the transmission and infection modes of RNA viruses and ultimately to replication frequencies. This comparatively slow rate in HAV could be related to the slower replication cycle of the virus, its particular tropism and its transmission mode. Moreover, the results of this work confirm that negative selection is acting at the nonsynonymous sites (most of the first and all of the second codon positions, see Table 1) as an important force driving the evolution of HAV populations, in agreement with previous reports (Costa-Mattioli et al., 2003, 2006; Sanchez et al., 2003b).
Recent studies on the pattern of sequence divergence among different genera of the family Picornaviridae revealed a number of shared features of the evolution of this family. The relative frequencies of nonsynonymous (dN) and synonymous (dS) substitutions in different genomic regions of picornaviruses showed an important discrepancy in dN/dS ratios between structural and nonstructural regions, since higher ratios were found to coincide with a marked increase in amino acid sequence divergence in the structural capsid-encoding regions (Simmonds, 2006). Nevertheless, when comparisons of sequences of the same serotype (including genera without serologically defined groups like HAV) are performed, low (0.1 or less) dN/dS ratios are invariably obtained in the structural regions (Costa-Mattioli et al., 2002; Simmonds, 2006), which are comparable to those in the nonstructural regions (Simmonds, 2006). These results may reflect that the recent evolution within each picornavirus serotype operates under generally negative or purifying selection, and is consistent with the results found in this work (Sanchez et al., 2003b).
In order to reconstruct the population history of these genotype IA HAV strains isolated in France from 1983 to 2001, a Bayesian skyline plot (Drummond et al., 2005) was constructed using the BEAST package.
As can be seen in Fig. 1, an increase in effective population size is observed from approximately 1970 until 1996, when a sharp decline in population size is observed. This drop in population size coincides with the introduction of HAV vaccines in the mid-1990s (Wasley et al., 2006) and is consistent with major changes that occurred in the epidemiology of HAV in France at this time (Gendrel & Launay, 2005). Epidemiological surveillance studies performed in the French armed forces on HAV incidence are also consistent with these findings (Richard et al., 2006). The results of this work revealed that Bayesian coalescence analysis is a suitable and useful approach to study the evolution of HAV virus populations over time, in agreement with all previous epidemiological data available. These results suggest that improvement of sanitary conditions and HAV vaccination have been successful as an effective public health measure for HAV control.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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Costa-Mattioli, M., Cristina, J., Perez-Bercoff, R., Casane, D., Colina, R., Garcia, L., Vega, I., Glikman, G., Romanowsky, V. & other authors (2002). Molecular evolution of hepatitis A virus: a new classification based on the complete VP1 protein. J Virol 76, 9516–9525.
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Received 28 March 2007;
accepted 2 July 2007.
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