Phylogeographic characteristics of reassortant DS-1-like G3P[8]-strains of rotavirus type A isolated in Nizhny Novgorod (Russia).

doi:10.21203/rs.3.rs-2735115/v1

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Phylogeographic characteristics of reassortant DS-1-like G3P[8]-strains of rotavirus type A isolated in Nizhny Novgorod (Russia).

https://doi.org/10.21203/rs.3.rs-2735115/v1

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Since 2013, there has been an increase in reports of the spread of a double intergroup reassortant strain of rotavirus type A (RVA) with the genotype G3P[8] and other genes belonging to the second genogroup I2-R2-C2-M2-A2-N2-T2-E2-H2. Our study found an increase in the proportion of G3P[8] with a short migration profile of genome segments in RNA-PAGE from 15% (2020-2021) to 53% (2021-2022) in Nizhny Novgorod (Russia). The VP7, VP4 and VP6 genes were sequenced by the Sanger method. It was found that the studied strains belong to the genotype G3P[8]-I2, and are reassortants between Wa- and DS-1-like rotaviruses. Phylogenetic analysis revealed that VP7 sequences of studied strains are closely related to DS-1-like G3P[8] RVA, which have been isolated in other countries. The RVAs isolated in Nizhny Novgorod carried the allele P[8]-3.1 of the VP4 gene, as well as other worldwide spreading G3P[8] DS-1-like reassortants. None of the VP6 sequences of studied G3P[8] RVA were included in the group with equine-like strains isolated in other countries. Most VP6 alleles of Nizhny Novgorod G3P[8] DS-1-like RVAs clustered with G2P[4], which were studied earlier. This fact may indicate a local reassortment of the spread strains.

Rotavirus species A (family Sedoreoviridae, genus Rotavirus; RVA) remains one of the leading causes of acute gastroenteritis in children in their first years of life. The rotavirus virion is an unenveloped icosahedral three-layer particle containing genetic material represented by 11 segments of double-stranded RNA (dsRNA). The binary classification of RVA is based on two proteins of the rotavirion outer capsid – VP7 (G-genotype) and VP4 ([P]-genotype), which carry neutralising antigenic epitopes on their surface. To date, at least 41 G and 57 [P] RVA genotypes isolated from humans and animals are known [1]. However, in the world and in Russia in particular, six G/P combinations are the most common: G1P[8], G2P[4], G3P[8], G4P[8], G9P[8] and G12P[8] [2, 3].

The segmented genome and genetic diversity allow rotaviruses to generate a wide range of possible combinations, however, most human RVAs belong to the Wa-like (“long” RNA electrophoretype, genogroup 1) and DS-1-like (“short” RNA electrophoretype, genogroup 2) genogroups [4]. For the prototype strains of these genogroups, the genotypes of all 11 dsRNA segments were determined: Gx-P[x]-I1-R1-C1-M1-A1-N1-T1-E1-H1 for Wa-like strains and G2-P[4]-I2 -R2-C2-M2-A2-N2-T2-E2-H2 for DS-1-like strains [1]. Wa-like RVAs most commonly circulate in the following combinations: G1P[8], G3P[8], G4P[8], G9P[8], and G12P[8]. Although intergenogroup reassortants have been described, it was previously believed that such strains are evolutionarily less successful than parental variants [4, 5]. However, there is increasing evidence of the spread of double intergenogroup reassortants between Wa- and DS-1-like RVA strains. In such reassortants, the two surface proteins VP7 and VP4 belong to the first genogroup, and the remaining genes belong to the second genogroup. The circulation of DS-1-like G1P[8] RVAs was detected in Japan in 2012-2013, then in Thailand, Vietnam, Malawi, and other countries [6-9]. This variant was also identified in Nizhny Novgorod in 2013-14, but was not widely spread [10]. In 2013, based on a whole genome analysis, it was found that a DS-1-like G3P[8] RVA strains became dominant in children with severe rotavirus gastroenteritis in Australia [11].

In Nizhny Novgorod, the proportion of G3P[8] RVA and a short migration segments profile in RNA-PAGE was first detected in 2017 [12]. The aim of this work was the molecular and phylogeography characterisation of DS-1-like strains of G3P[8] RVA.

Samples and identification of RVA. The present study used the residual amounts of fecal samples of children hospitalised in the infectious diseases hospital of Nizhny Novgorod from July 2020 to June 2022 with acute intestinal infection. The study protocol was approved by the Local Ethics Committee of the I.N. Blokhina Nizhny Novgorod Research Institute of Epidemiology and Microbiology. The study was conducted in the format of a random sample and anonymous testing.

Isolation of total RNA from clinical material was carried out using the AmpliSens® RIBO-prep isolation kit manufactured by the Central Research Institute of Epidemiology (CRIE) (Moscow, Russia), according to the instructions. RVA detection was performed using the test system AmpliSens® Rotavirus/Norovirus/Astrovirus-FL (CRIE, Russia), according to the instructions.

Genotyping and sequencing. RVA genotyping was performed by multiplex PCR to identify 12 VP7 and VP4 genotypes: G1-G4, G6, G8, G9, G12, P[4], P[8], P[6] and P[9] [13-17]. RVA electrophoretyping was performed by RNA-PAGE as described previously [18, 19].

Fragment VP8* of the VP4 gene, 877 bp in size, was synthesised with primers con2/con3mod proposed earlier [13, 17]. Full-length VP7 and VP6 genes were amplified with primers VP7F/VP7R and GEN_VP6F/GEN_VP6R, respectively [20]. The obtained sequences were deposited in the international GenBank database under the numbers: OQ446695-OQ446794.

The nucleotide sequences of the obtained cDNA fragments were determined using the Nanophor-05 genetic analyser (Russia) and a set of reagents for sequencing by Sanger BigDye® Terminator v3.1 (Applied Biosystems, USA).

Philodynamic analysis. In total 1,668 sequences of VP7 gene G3 genotype, with an open reading frame of more than 80%, available date and place of isolation of the strain (as of 06/01/2022) were downloaded from the GenBank database. Sequences that contained unknown bases, premature stop codons, mutations leading to a shift in the reading frame were removed from alignment. In addition, sequences with high homology, one time and a place of RVA isolation were removed from the alignment. We tried to diversify the temporal and spatial information in the dataset as much as possible. As a result, 544 sequences were selected.

To assess the G3 RVA clustering in the study sample, using the MEGA X program, a model was selected: GTR + G (General Time Reversible model with discrete Gamma distribution with 5 rate categories). Further analysis was carried out using the BEAST v 1.10.4 software package, using the Constant population size, strict clock, and long Markov chain (MCMC) 500 mln steps model. The Bayes factor (BF) was calculated using the SPREAD 3D program [21]. The Maximum Clade Credibility (MCC) tree was summarised from the posterior distribution of trees using the TreeAnnotator included in the BEAST package, and visualised and annotated using FigTree v1.4.4 (http://tree.bio.ed.ac.uk/software/ figtree /).

For phylogenetic analysis of the VP4 and VP6 genes, sequences with the highest homology with the studied strains and G3P[8] DS-1-like strains isolated in other countries and deposited in the GenBank database were used.

RVA detection. From July 2020 to June 2022, in total 4,125 samples of faeces of children hospitalised in an infectious hospital in Nizhny Novgorod with acute intestinal infection were examined.

Rotavirus RNA was detected in 30.4% of cases (n=1253), of which the G[P] type was determined in 81.6% (n=1022). RT-PCR typing revealed the presence of the following combinations of G/P types in the studied period: G1P[8], G2P[4], G4P[8], G3P[8], G9P[8], G3P[6], G3P[9], G2P[8], G8P[8], G12P[6], G6P[9], G9P[4], G3P[4]; as well as partially typed strains with genotypes: G2P[x], G3P[x], G8P[x], G9P[x], GxP[4], GxP[6], GxP[8], GxP[9]. Figure 1 shows that the proportion of G3P[8] RVA increased from 15% in the period 2020-2021 to 53% in the season 2021-2022.

The G3P[8] rotaviruses identified in this work, in addition to typing by RT-PCR, were analysed by RNA-PAGE. Combination of RT-PCR and RNA-PAGE made it possible to establish the presence of G3P[8] RVA with short, DS-1-like profile of segment migration in polyacrylamide gel (PAGE), which clearly indicated intergroup reassortment (Fig. 2).

Phylogenetic analysis of the VP7 gene. Phylogenetic analysis of the VP7 gene of G3P[8] RVAs was performed based on 42 sequences obtained in this study and sequences available in the GenBank database (n=544). On the formed MCC (Maximum Clade Credibility) tree, two large clusters I and II are identified (Fig. 3). A complete phylogenetic tree with the names of sequences and their numbers in the GenBank database is provided in additional materials (Suppl Fig.1).

In cluster I, 3 lines can be reliably distinguished. The I-1 line includes G3P[8] RVA isolated in different regions of the world in 1998-2017. The I-2 and I-3 lines include RVAs with genotypes G3P[6] and G3P[9] isolated in 1997-2016 and 1996-2014, respectively. In addition, cluster I includes a number of G3 rotaviruses isolated from pigs in Europe, Africa and Asia in 2009-2017 in combination with genotypes P[6], P[7], P[13], P[22], P[23], P[32] of the VP4 gene (in Figure 2 marked as Porcine G3).

Four lines are allocated in cluster II. The II-1 line is mainly represented by G3P[8] DS-1-like rotaviruses which have spread widely around the world since 2013. It should be noted that the same line includes RVA with the G3 genotype, which was isolated in India from horses in 2004, as well as G3P[45] rotaviruses isolated in China from rats in 2013. Apparently, the formation of DS-1-like G3P[8] RVA occurred in Asia with the participation of local animal populations. Lines II-2 to II-4 are represented by animal rotaviruses (bat, bovine, rodents (Mouse, Rat), horse, rabbit, simian etc.), which were isolated in different years (Fig. 3).

Philodynamic analysis of the VP7 gene. In this paper, a discrete phylogeographic analysis of the RVA strains belonging to line II-1, shown in Figure 3, was carried out. The estimated mutation rate was 2.14*10-3 substitutions per site per year [95% HPD: 1.38x10-4; 3.18x10-3]. Data of spatio-temporal reconstruction suggest that the spread of the G3 line originated around 2002 [95% HPD: 2000-2007]. Based on the analysis of all relevant sequences available in GenBank, the closest ancestor of the G3 lineage considered and the RVA strain isolated from a horse in India in 2004 was circulating in 1980 [95% HPD: 1974-1989]. The obtained phylogenetic tree with sufficient probability suggests that the origin of DS-1-like G3P[8] rotavirus originated from animals (including horses, rats, bats, cattle) and the source of its distribution is East Asia (India, China) (Fig. 4). The formed variant with the genotype G3P[8] quickly spread around the world. Table 1 shows the values of BF>3 obtained using the SPREAD 3D software. If the value of this factor exceeds 3, this confirms a strong epidemiological connection between the regions being compared. However, since the spread of the DS-1-like variant of G3P[8] occurred in a short time and widely, it is not possible to establish a reliable source of drift for each region (Fig. 3 Plot map).

Phylogenetic analysis of the VP4 gene. According to the classification of da Silva et al., DS-1-like G3P[8] rotaviruses isolated in Nizhny Novgorod by the VP4 gene belong to the line P[8]-3.1 [22]. The nucleotide sequences obtained in this study were clustered together with strains isolated in other countries of Europe, East and Southeast Asia, and Russia in combination with the G3 genotype. Some isolates (a smaller group) were clustered with rotaviruses of G8, G9 and G3 genotypes isolated in Russia, East and Southeast Asia and Europe (Fig. 5).

Phylogenetic analysis of the VP6 gene. During the study, we obtained 25 nucleotide sequences of the VP6 gene of G3 DS-1-like rotaviruses. All of them belonged to genotype I2. In the resulting tree, we identified three lines: I2-I to I2-III (Fig. 6). Interestingly, 23 of the 25 sequenced sequences formed an I2-1 cluster together with G2P[4] RVA strains, which were isolated in Russia and other countries (Fig. 4). G3P[8] RVA isolated in Novosibirsk in 2018 belongs to the same cluster.

The I2-II cluster was formed by RVAs with genotypes G1P[8], G2P[4], G3P[8], G8P[8] and G9P[8], it also included one sequence of the VP6 rotavirus gene with genotype G3P[8] isolated in Nizhny Novgorod in 2021. Cluster I2-III included a single sequence of RVA with the genotype G3P[4], which was isolated by us in 2022. It is noteworthy that the third cluster includes the majority of DS-1-like G3P[8] RVAs described in the literature, including strains isolated in Moscow in 2020. In addition, the third group also included intergroup reassortants with genotype G1P[8] isolated in Nizhny Novgorod in 2014 [10].

Rotavirus gastroenteritis is a serious health problem worldwide. Despite the genotypic diversity, the largest number of RVAs belongs to six ubiquitously circulating G/P-types: G1P[8], G2P[4], G3P[8], G4P[8], G9P[8] and G12P[8] belonging to Wa- and DS-1-like genogroups. Earlier in the literature there was evidence demonstrating that intergroup reassortants are rare and it was believed that they are less competitive [5]. Since 2013, there have been increasing reports of intergroup reassortants of Wa- and DS-1-like genogroups that occur singly, lead to outbreaks or occupy a dominant position in the genotype structure of the RVA in different regions of the world [6, 11].

Animal rotaviruses play an important role in the formation of epidemiologically significant human RVAs. Previously, based on the analysis of the complete genome, it was shown that DS-1-like G2P[8] and G3P[8] intergroup reassortants in their composition carry the genes of equine and bovine rotavirus [23]. Animal rotaviruses in humans have been repeatedly detected, which apparently leads to the formation of new epidemiologically significant variants [24-28]. In addition to pigs and cattle, there is evidence in the literature that rodents and insectivores may represent an important reservoir of rotaviruses, including their potential transmission to humans [29, 30].

The circulation of reassortant DS-1-like G1P[8] rotaviruses in Nizhny Novgorod was established in 2014, but they were not widely distributed [10]. G3P[8] rotaviruses with a "short" profile of RNA segments migration in PAGE were first identified in Nizhny Novgorod and Novosibirsk in 2017. In the period 2019-2020, the proportion of DS-1-like reassortants with genotypes G1P[8]-I2-E2, G3P[8]-I2-E2, G8P[8]-I2-E2, G9P[8]-I2-E2 was 11.8% [12]. Analysis of the complete genotypes of double intergroup reassortants in 2017-2018 allowed us to establish their common clustering with DS-1-like G3P[8] rotaviruses isolated in other countries, for all 11 genes [31]. In the sample given in this study, which included reassortant G3P[8] RVAs isolated in 2020-2022, the nucleotide sequences of the VP6 gene were clustered with G2P[4] rotaviruses that were studied earlier [32].

In our work, for phylogenetic analysis, all the nucleotide sequences of the VP7 gene with the G3 genotype available in the GenBank database (as of 06/01/2022), and the known date of isolation of the sample and a length of at least 80% of the open reading frame were used. As established earlier, and confirmed in this work, RVAs with the G3 genotype are divided into two large groups [29]. Both clusters I and II included animal RVAs. Cluster I is formed by three lines of rotaviruses with genotypes G3P[8], G3P[6] and G3P[9], as well as RVA isolated from pigs that did not form a clear group. The second cluster formed by the nucleotide sequences of the VP7 gene can be divided into four lines II-1 to II-4. Group II-1 includes intergroup reassortants isolated in Nizhny Novgorod in 2020-2022 and described in the present work. In addition, the second cluster includes G3P[8] DS-1-like RVA isolated around the world. According to the literature data, double intergroup G3P[8] reassortants, which in a number of articles are also called "equine-like" RVAs, dominated in Thailand (2014-16), Indonesia (2013-16), Malaysia (2018-19), Japan (2017-18), Brazil (2018-19), Russia (2019) [33-38]. In addition, G3P[8] reassortants were found in the territories of European countries: Spain (2014-15), Italy (2017-19), Slovakia (2019), Germany (2016), Hungary (2015), Turkey (2016-17), as well as China (2017-18) and Kenya (2018) [39-46].

In the VP4 phylogenetic tree, most Russian strains clustered with other DS-1-like G3P[8] nucleotide sequences isolated worldwide. However, some of the strains belonged to another cluster. In the VP6 phylogenetic tree the isolates considered in our work were related to typical G2P[4] rotaviruses, as well as DS-1-like G1P[8], which were discovered in Nizhny Novgorod in 2014 [10]. The cluster formed by DS-1-like G3P[8] strains identified in other countries included only one sequence of the VP6 RVA gene isolated in Nizhny Novgorod. These facts may indicate episodes of reassortment that occurred in Russia.

Intergenogroup reassortants (G1[8] and G3P[8] DS-1-like RVAs) appeared in 2012 in East Asia and Australia and have spread widely around the world. Such intergroup reassortants can be widely distributed, without attracting due attention, when monitoring RVAs based only on the RT-PCR typing of VP7 and VP4 genes. To track the spread of intergroup reassortants, it is necessary to conduct additional studies such as electrophoretyping of RNA-PAAG, sequencing or PCR typing of other genome segments.

In the presented work, the growth and then the dominance of G3P[8] DS-1-like RVA strains in Nizhny Novgorod (Russia) was established. The phylogenetic relationship of these reassortants with strains spread all over the world has been revealed. Analysis of the sequences available in the GenBank database allowed us to establish that the ubiquitous double intergroup reassortant of RVA has the closest common ancestor with horse rotavirus, which was isolated in India in 2004. It was found that in 2020-2022, the VP6 gene was changed in the G3P[8] RVA circulating in Nizhny Novgorod. Such findings may indicate that intergenegroup reassortment is actively taking place in the rotavirus population and leads to the emergence of new, epidemiologically significant variants.

Author Contributions OM conceived and designed the experiments. OM, TS, NE and EV performed the experiments. OM, TS analysed the data. OM, NN wrote the manuscript. TS and NE participated in revising the manuscript. All authors read and approved the final manuscript.

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Table 1. Epidemic connections between geographical regions at BF>3, calculated using SPREAD 3D software.

Сountry	BF	Сountry	BF
India-Indonesia	68826.7	Spain-Thailand	27.4
India-Japan	13759.2	Hungary-Indonesia	10.6
China-Japan	454.3	Germany-India	10.2
Belgium-Italy	290.3	Australia-India	7.6
India-Thailand	210.2	Dominican Republic-Indonesia	6.5
Brazil-Germany	127.1	Italy-Japan	5.6
Japan-Russia	54.5	Japan-Turkey	5.5
Japan-Kenya	53.2	Germany-Thailand	4.5
Brazil-Japan	38.1	Australia-Thailand	4.2
Russia-Thailand	34.4	Dominican Republic-Thailand	3.8
India-Malaysia	30.2

No competing interests reported.

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Phylogeographic characteristics of reassortant DS-1-like G3P[8]-strains of rotavirus type A isolated in Nizhny Novgorod (Russia).

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