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New Simian Enterovirus 19 (EV-A122) Strains in China Reveal Large- Scale Inter-Serotype Recombination Between Simian EV-As

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New Simian Enterovirus 19 (EV-A122) Strains in China Reveal Large- Scale Inter-Serotype Recombination Between Simian EV-As Virologica Sinica www.virosin.org https://doi.org/10.1007/s12250-021-00412-9 www.springer.com/12250 (0123456789().,-volV)(0123456789().,-volV) LETTER New Simian Enterovirus 19 (EV-A122) Strains in China Reveal Large- Scale Inter-Serotype Recombination between Simian EV-As 1 1 1 1 1 1 Zhenzhi Han • Jinbo Xiao • Yang Song • Shuangli Zhu • Dongyan Wang • Huanhuan Lu • 1 1 1,2 1,2 Tianjiao Ji • Dongmei Yan • Wenbo Xu • Yong Zhang Received: 6 December 2020 / Accepted: 13 April 2021 Ó Wuhan Institute of Virology, CAS 2021 Dear Editor, humans have also been detected in NHPs, suggesting the possibility of cross-species transmission (Sadeuh-Mba The genus Enterovirus (EV), belonging to the family et al. 2014; Mombo et al. 2015). Enteroviruses identified Picornaviridae, order Picornavirales, comprises 15 spe- in NHPs are significant among the emerging enteroviruses cies: Enterovirus A–L and rhinovirus A–C (Zell et al. that infect humans (Oberste et al. 2013b). Therefore, 2017). Enterovirus A (EV-A) has 25 serotypes, including investigating pathogenic NHP enteroviruses is essential. several pathogens, such as EV-A71, coxsackievirus A16 In this study, 60 specimens were collected from 30 (CV-A16), and CV-A6 that infect humans, as well as four monkeys, including throat swabs (n = 30, 50%) and rectal serotypes (EV-A122, 123, 124, and 125) isolated from swabs (n = 30, 50%). The specimens were collected from simians (Zell et al. 2017). EV genomes share a similar several species of monkeys, including Rhesus macaque or structure with a length of 7.5 kb, and two open reading Macaca mulatta (n = 16, 53.3%), Macaca thibetana frames (ORFs) flanked by 50- and 30-untranslated regions (n = 5, 16.7%), Macaca nemestrina (n = 5, 16.7%), and (UTRs) in some EVs (Oberste et al. 2013b; Zell et al. Macaca assamensis (n = 4, 13.3%), located in two coun- 2017; Guo et al. 2019; Lulla et al. 2019). ties of Yunnan Province, China (Supplementary Table S1). Although EV-A71, CV-A16, and CV-A6 have been well We constructed two libraries following the Illumina Tru- investigated, the genomic data, epidemiological charac- Seq DNA Preparation Protocol, which were pooled and teristics of several other enterovirus serotypes remain to be subjected to 150 bp paired-end sequencing using the identified (Puenpa et al. 2018; Han et al. 2020a). Other Novaseq 6000 platform (Illumina, San Diego, CA, USA). than humans, novel enterovirus serotypes have been iden- We obtained 172,681,140 and 176,787,228 raw reads from tified in non-human primates (NHPs), rodents, dromedary these two libraries (Supplementary Table S1). camels, pigs, and bovines (Oberste et al. 2007; Zell et al. The order Caudovirales, which includes viral species 2017;Li et al. 2020). EV-A122 [previously known as infecting bacteria, showed the highest proportion between the Simian enterovirus 19 (SV19)], detected in Macaca fasci- two pools, followed bythe known eukaryotic viral assignment, cularis, showed distant phylogenetic characteristics com- Riboviria (Fig. 1A), with 56,547 and 34,969 assembled con- pared with other EV-A serotypes (Oberste et al. 2007). tigs (Trinity version 2.8.4) longer than 300 bp, respectively. Surprisingly, certain enterovirus serotypes that circulate in Based on annotation against the nucleotide database, we identified 8475 and 1457 contigs in the viral kingdom. Manual Supplementary Information The online version contains analysis resulted in a total of 4 contigs, a nearly complete supplementary material available at https://doi.org/10.1007/s12250- 021-00412-9. genome, showing 77% nucleotide identity with the M19s (P2) strain (GenBank accession number AF326754). The clean & Yong Zhang reads were mapped to the M19s (P2) genome and the [email protected] sequencing depth was calculated, resulting in two consensus 1 WHO WPRO Regional Polio Reference Laboratory, NHC sequences from two pools (Fig. 1B). Based on the full-length Key Laboratory for Biosafety, NHC Key Laboratory for genome, both consensus sequences clustered with the RJG7 Medical Virology, National Institute for Viral Disease strain (GenBank accession number EF667344) of the EV-A92 Control and Prevention, Chinese Center for Disease Control prototype, and also clustered with EV-A species along with the and Prevention, Beijing 102206, China EV-A122 prototype (GenBank accession number AF326754) 2 Center for Biosafety Mega-Science, Chinese Academy of based on the P1 coding region. (Supplementary Fig. S1A-1B). Sciences, Wuhan 430071, China 123 Virologica Sinica A 100% B Pool 1 90% Pool 2 60 80% 70% Unclassified viruses 40 60% Ortervirales 50% Herpesvirales e sequencing depth Riboviria v 40% 20 Caudovirales Relati 30% 20% 0 10% 0 1000 2000 3000 4000 5000 6000 7000 Genome position 0% Pool1 Pool2 C D JX538013_1_SV19_strain 0.9 Query: EV-A122(SV19)−AF326754 0.807 JX538014_1_SV19_strain JX538015_1_SV19_strain Bangladesh JX538016_1_SV19_strain China JX538012_1_SV19_strain Lineage 2 JX538018_1_SV19_strain America 0.797 JX538010_1_SV19_strain 0.8 JX538011_1_SV19_strain 0.988 JX538017_1_SV19_strain JX538006_1_SV19_strain 0.992 JX538007_1_SV19_strain JX538008_1_SV19_strain 0.7 AKM8−YN−2020−CHN 0.952 AKM5_YN_2020_CHN AKM9−YN−2020−CHN AKM8_YN_2020_CHN Similarity (%) OKM5_YN_2020_CHN JH04−YN−2020−CHN 1 AKM9_YN_2020_CHN JH05−YN−2020−CHN 0.985 JH04_YN_2020_CHN JH06−YN−2020−CHN 0.811 Lineage 3 JH05_YN_2020_CHN 0.6 OKM5−YN−2020−CHN 0.04 1 JH06_YN_2020_CHN AKM5−YN−2020−CHN 0.997 EU194538_1_SV19 0.884 EU194539_1_SV19 0.78 7 EU194537_1_SV19 EU194517_1_SV19 0.5 KT961648_1_19 KT961654_1_190 0 500 1000 1500 2000 2500 3000 3500 4000 4500 5000 5500 6000 6500 7000 0.814 1 Lineage 1 KT961653_1_19 AF326754_2_SV19_strain 5‘-UTR 3’-UTR 0.876 KT961647_1_19 VP2 VP3 VP1 2A 2B 2C 3C 3D AF326761_SV43_strain_OM11 VPg VP4 3A 3B Nucleotide Position Fig. 1 A The taxonomy of viral reads identified in each pool. The variants and the query strain. D Bayesian phylogenetic tree based on y-axis represents the proportion of different viruses. B The sequenc- the partial VP1 coding region of EV-A122 strains. Different colours ing depth and coverage of two pools along with the reference genome. indicate the information of countries. The EV-A123 prototype (Gen- C Similarity plot of novel EV-A122 variants and EV-A122 bank no. AF326761) was used as an outgroup. The number at each prototypes. The x-axis shows the nucleotide position, whereas the node represents the posterior probability, and scale bars represent the y-axis represents the genomic similarity between novel EV-A122 substitutions per site. Real-time RT-PCR assays were used to distinguish the were deposited in the GenBank database under accession positive specimens in the two libraries, with specific pri- numbers MT649085–MT649091. The metagenomic data mers and probes targeting the assembled genomic were submitted to NCBI Sequence Read Archive (SRA) sequences (Supplementary Table S2). Finally, we identified under accession number SRP270853. nine positive samples with different cycle threshold values All EV-A122 variant genomes were 7316–7341 in the two pools (Table 1). Among the positive specimens, nucleotides long, with a long poly(A) tail. We did not two throat swabs showed a positive reaction for EV-A122, identify the second small ORF (ORF2) in the EV-A122 even though simian enteroviruses are typically detected in strains, despite the typical genomic characteristic of several stool specimens (Oberste et al. 2007, 2013a). We imple- EVs harbouring two ORFs (Supplementary Fig. S2A). mented the ‘‘primer-walking’’ strategy to obtain the full- Several conserved sites were found in ORF2 of EV-A length genomes (Oberste et al. 2007; Han et al. (Supplementary Fig. S2B). Although ORF2 was not 2018, 2020b), seven of nine were successfully obtained and detected in these EV-A122 strains, the conserved domains 123 Z. Han et al.: New Enterovirus A122 Recombinants Table 1 The overall information of positive strains identified in this study. GenBank accession number Strain Host Sample source Region Ct value NA JH03 Rhesus macaque Rectal swab Xishuangbanna Dai Autonomous Prefecture 24 MT649087 JH04 Rhesus macaque Rectal swab Xishuangbanna Dai Autonomous Prefecture 19 MT649088 JH05 Macaca nemestrina Rectal swab Xishuangbanna Dai Autonomous Prefecture 22 MT649089 JH06 Macaca nemestrina Rectal swab Xishuangbanna Dai Autonomous Prefecture 20 NA OKM4 Rhesus macaque Throat swab Kunming city 28 MT649091 AKM5 Rhesus macaque Rectal swab Kunming city 18 MT649090 OKM5 Rhesus macaque Throat swab Kunming city 28 MT649085 AKM8 Rhesus macaque Rectal swab Kunming city 24 MT649086 AKM9 Macaca assamensis Rectal swab Kunming city 22 The cycle threshold value shows the threshold results of qRT-PCR assay for positive specimens. All samples were collected from different counties of Yunnan province of China. NA represents that no genome sequences were available. might play an important role in receptor binding, which Thus, geographic obstruction may play important roles in determines viral intestinal infection (Guo et al. 2019), the the evolutionary trajectories of the simian enteroviruses. highly conserved WIGHPV domain is required for EV-A71 Based on the bootscanning plots of the prototypes and particle release (Guo et al. 2019; Lulla et al. 2019). variants (Supplementary Fig. S2 and S3), the P1 coding The seven variants showed approximately 79% and 80% region corresponded to the EV-A122 prototype, whereas nucleotide similarity with the EV-A122 prototype in terms the P2 and P3 coding regions showed large-scale recom- of the VP1 and P1 coding regions, respectively, higher than bination activity with EV-A92-like strains. We screened that of other serotypes (Supplementary Table S3). The the possible EV-A122-like and EV-A92-like sequences in seven variants showed the highest nucleotide similarity GenBank with P2 and P3 coding regions. The P1 genomic with the EV-A122 prototype in the P1 coding region and region of strain cg4006 (EV-A122-like strain), which was partial 50-UTR, whereas the similarity between the 30-UTR identified in the faeces of Rhesus macaque in 2014, showed and P2 and P3 coding regions was low (Fig.
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