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Characterization of the Bujaru, Frijoles and Tapara Antigenic Complexes Into the Sandfly Fever Group and Two Unclassified Phleboviruses from Brazil

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Characterization of the Bujaru, Frijoles and Tapara Antigenic Complexes Into the Sandfly Fever Group and Two Unclassified Phleboviruses from Brazil RESEARCH ARTICLE Nunes-Neto et al., Journal of General Virology 2017;98:585–594 DOI 10.1099/jgv.0.000724 Characterization of the Bujaru, frijoles and Tapara antigenic complexes into the sandfly fever group and two unclassified phleboviruses from Brazil Joaquim Pinto Nunes-Neto,1† William Marciel de Souza,2,3† Gustavo Olszanski Acrani,4 Marilia Farignoli Romeiro,2 MarcílioJorge Fumagalli,2 Luiz Carlos Vieira,2 Daniele Barbosa de Almeida Medeiros,1 Juliana Abreu Lima,1 Clayton Pereira Silva de Lima,5 Jedson Ferreira Cardoso,5 Luiz Tadeu Moraes Figueiredo,2 Sandro Patroca da Silva,5 Robert Tesh,6 Marcio Roberto Teixeira Nunes1,5,6 and Pedro Fernando da Costa Vasconcelos1,7,* Abstract The genus Phlebovirus includes the sandfly fever viruses and tick-transmitted uukuviruses. Sandfly fever group viruses have been isolated from various vertebrate species and from phlebotomines and occasionally alternative arthropods, e.g. mosquitoes, or ceratopogonids of the genus Culicoides. Uukuniemi serogroup viruses have been isolated from various vertebrate species and from ticks. Despite the public health importance of some viruses of the genus, the genomic diversity of phleboviruses that could be incriminated as causative of human or veterinary diseases remains underestimated. Here we describe the nearly complete sequences and genomic characterization of two phleboviruses belonging to the Bujaru antigenic complex: the prototype species and the Munguba virus. Furthermore, six previously unclassified phleboviruses isolated in Brazil were also sequenced and characterized: Ambe, Anhanga, Joa, Uriurana, Urucuri and Tapara viruses. The results of the phylogenetic analysis indicated that these viruses group with viruses of three antigenic complexes (Bujaru, Tapara and frijoles clades), with two unclassified phleboviruses. We also performed genomic reassortment analysis and confirmed that there were no events for the viruses described in this study, but we found a new potential reassortment in Medjerda Valley virus, which contains S and L segments of Arbia virus, and probably a unique M segment, both viruses circulate in the same geographic region, indicating these two isolates represent two distinct viruses. This study provides insights into the genetic diversity, classification and evolution of phleboviruses. INTRODUCTION large segment (LRNA), which encodes the viral RNA- dependent RNA polymerase (RdRp); medium segment At present, more than 350 named bunyaviruses are subdi- (MRNA), which encodes two envelope glycoproteins (Gn vided into order Bunyavirales based on serological, morpho- and Gc) and a non-structural protein (NSm); and small seg- logical and genomic features [1]. Of these, the genus ment (SRNA), with an ambisense coding strategy, which Phlebovirus is composed of approximately 70 named encodes the viral nucleocapsid (N) protein in the negative- viruses, which, based on serological methods, are classified sense orientation and a non-structural protein (NSs) that is into two antigenic groups: the phlebotomus fever (or sand- encoded in the positive sense [2, 3]. fly fever) group and the Uukuniemi group [2]. The genus Phlebovirus includes the sandfly fever viruses and Phleboviruses possesses a genome organization typical of tick-transmitted uukuviruses. Sandfly fever group viruses other members of the order Bunyavirales, with a tripartite have been isolated from various vertebrate species and from negative-sense RNA genome with components named as phlebotomines and occasionally alternative arthropods, e.g. Received 11 October 2016; Accepted 26 January 2017 Author affiliations: 1Departamento de Arbovirologia e Febres Hemorragicas, Instituto Evandro Chagas, Ananindeua, Para, Brazil; 2Virology Research Center, School of Medicine of Ribeirao Preto of University of Sao~ Paulo, Ribeirao Preto, Sao~ Paulo, Brazil; 3MRC-University of Glasgow Centre for Virus Research, Glasgow, Scotland, UK; 4Universidade Federal da Fronteira Sul, Passo Fundo, Rio Grande do Sul, Brazil; 5Center for Technological Innovation, Instituto Evandro Chagas, Ananindeua, Para, Brazil; 6Department of Pathology, University of Texas Medical Branch, Galveston Texas, USA; 7Department of Pathology, Para State University, Belem, Para, Brazil. *Correspondence: Pedro Fernando da Costa Vasconcelos, [email protected] Keywords: phleboviruses; genetic characterization; sandfly fever group; ungrouped phlebovirus; Brazilian Amazon. Abbreviations: CF, complement fixation; ML, maximum likelihood; RdRp, RNA-dependent RNA polymerase. †These authors contributed equally to this work. Three supplementary figures and three supplementary tables are available with the online Supplementary Material. 000724 ã 2017 The Authors Downloaded from www.microbiologyresearch.org by IP: 200.139.9.66585 On: Tue, 03 Jul 2018 19:08:24 Nunes-Neto et al., Journal of General Virology 2017;98:585–594 mosquitoes, or ceratopogonids of the genus Culicoides [3– NSm with its sequence upstream from the Gn protein, a 5]. On the other hand, viral members of Uukuniemi sero- typical organization of some phleboviruses. The glycopro- complex have been isolated from various vertebrate species teins are predicted to contain transmembrane domains and from ticks and include three phleboviruses of public (TMDs) that are typical of the genus, which is a single TMD health importance: severe fever with thrombocytopenia syn- in Gn, close to the C-terminus of this protein and two drome (SFTS) virus, Heartland and Bhanja viruses [6–9]. TMDs in Gc, one in the N-terminal region and the other one close to the C-terminal region (Figs 2 and S2). Both Despite the public health importance of some viruses of the TMDs in Gn and Gc are responsible for anchoring the gly- genus Phlebovirus, and the recent number of discoveries coproteins on the viral envelope [15]. The asparagine sites and sequencing data of phleboviruses that had been only that are predicted to be N-glycosylated in the M polyprotein previously described through classical virological methods, were also observed, and neither the number of sites nor the genomic diversity of phleboviruses associated with their positions seem to be conserved in these viruses, as can human or veterinary diseases remains underestimated [9– be observed in Fig. 1. These N-glycosylation sites of the pre- 14]. Therefore, it is important to clarify the genetic diversity, dicted protein topologies are located in the polyprotein por- distribution and evolutionary aspects of these viruses. Here, tion, which faces the lumen of the endoplasmic reticulum we describe the nearly complete sequences and characteriza- and of the Golgi apparatus, which could indicate that they tion of the two viruses of the Bujaru antigenic complex, as could be glycosylated during viral replication. However, fur- well as six unassigned phleboviruses isolated in Brazil. ther investigation focusing on biological processes of repli- cation is needed in order to address whether they are RESULTS actually being glycosylated in vivo. Genomic characterization of phlebovirus The SRNA segments of these viruses display the same The genomes of Bujaru, Ambe, Anhanga, Joa, Munguba, encoding strategies, with two ORFs in different directions: Uriurana, Urucuri and Tapara viruses (Table 1) comprise a negative-sense N protein and a positive-sense non- three negative-sense RNA molecules with sizes ranging structural protein (NSs). The sizes of the NP range from from 1628 (SRNA) to 6510 (LRNA) nucleotides with 244 to 250 aa, and those of the NSs between 249 and 289 aa. deduced amino acid lengths similar to those of other phle- boviruses (Fig. 1). The L segment of these viruses encodes Phylogenetic and serological relationship of an RdRp of about 2090 aa, with a predicted molecular phleboviruses weight of 238 kDa. Tapara virus contains the largest putative The maximum-likelihood (ML) trees based on nucleotide RdRp, comprising 2120 aa with a predicted molecular or amino acid sequences produced the same clustering pat- weight of 24 165 kDa, and the conserved polymerase activity tern of groups, but with different topologies (Figs 2 and domains consisting of pre-motif A and motifs A through E S3). This fact indicates that the saturation site has not (amino acids 915–922 to 1182–1189), which is conserved adversely affected the phylogenetic inference. The 85 full- in negative sense RNA viral polymerases [Figs 1 and length phlebovirus ORFs were clustered into 18 well- S1 (available in the online Supplementary Material)]. The M supported monophyletic groups; however, many of the polyprotein encoded by the MRNA segment ranges from deeper nodes were unresolved throughout the phylogeny. 1302 to 1429 aa in length, with differences distributed across Eleven of the well-supported clades corresponded to viral the polyprotein sequences. Furthermore, the M polyprotein species that have already been established by the ICTV: contains the characteristic N-terminal signal peptide that is Bujaru, Chagres, candiru, frijoles, Icoaraci, Punta Toro, common to all members of the genus (Fig. 1). The M poly- Rift Valley, Salehabad, sandfly fever Naples, severe fever protein is cleaved into three structural proteins, NSm, Gn with thrombocytopenia syndrome (SFTS) and Uukuniemi. and Gc. All phleboviruses examined in this study possess an Additionally, we found groups that had been previously Table 1. Names, abbreviations, strain numbers, dates, sources, localities of isolation and accession numbers of the viruses used in this study Virus name Abbreviation Strain Date of Source
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