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Molecular genomic characterization of tick- and human-derived severe fever with thrombocytopenia syndrome virus isolates from South Korea

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      Abstract

      BackgroundSevere fever with thrombocytopenia syndrome (SFTS) is an emerging tick-borne viral disease caused by the SFTS virus (SFTSV) from Bunyaviridae that is endemic in East Asia. However, the genetic and evolutionary characteristics shared between tick- and human-derived Korean SFTSV strains are still limited.Methodology/Principal findingsIn this study we identify, for the first time, the genome sequence of a tick (Haemaphysalis longicornis)-derived Korean SFTSV strain (designated as KAGWT) and compare this virus with recent human SFTSV isolates to identify the genetic variations and relationships among SFTSV strains. The genome of the KAGWT strain is consistent with the described genome of other members of the genus Phlebovirus with 6,368 nucleotides (nt), 3,378 nt, and 1,746 nt in the Large (L), Medium (M) and Small (S) segments, respectively. Compared with other completely sequenced human-derived Korean SFTSV strains, the KAGWT strain had highest sequence identities at the nucleotide and deduced amino acid level in each segment with the KAGWH3 strain which was isolated from SFTS patient within the same region, although there is one unique amino acid substitution in the Gn protein (A66S). Phylogenetic analyses of complete genome sequences revealed that at least four different genotypes of SFTSV are co-circulating in South Korea, and that the tick- and human-derived Korean SFTSV strains (genotype B) are closely related to one another. Although we could not detect reassortant, which are commonly observed in segmented viruses, further large-scale surveillance and detailed genomic analysis studies are needed to better understand the molecular epidemiology, genetic diversity, and evolution of SFTSV.Conclusions/SignificanceFull-length sequence analysis revealed a clear association between the genetic origins of tick- and human-derived SFTSV strains. While the most prevalent Korean SFTSV is genotype B, at least four different genotypes of SFTSV strains are co-circulating in South Korea. These findings provide information regarding the molecular epidemiology, genetic diversity, and evolution of SFTSV in East Asia.

      Author summary

      Severe fever with thrombocytopenia syndrome (SFTS) is an emerging tick-borne viral disease caused by the SFTS virus (SFTSV). During entomological surveillance of SFTSV infection in Korean ticks collected from SFTS outbreak areas, we isolated a single SFTSV strain which we designated KAGWT. In addition, we isolated three SFTSVs from human patients with typical SFTS symptoms. In this study, we report the genomic sequences of each of these isolates and compare the genetic and evolutionary characteristics between tick- and human-derived Korean SFTSV isolates. Genetic and phylogenetic analyses of these sequences revealed that the tick-derived Korean SFTSV strain is clustered into genotype B, the most prevalent genotype in South Korea, and was closely related to other SFTSV in the same group. Furthermore, our results show that at least four different genotypes of SFTSV strains are co-circulating in South Korea.

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      Most cited references 37

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      MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.

      We announce the release of an advanced version of the Molecular Evolutionary Genetics Analysis (MEGA) software, which currently contains facilities for building sequence alignments, inferring phylogenetic histories, and conducting molecular evolutionary analysis. In version 6.0, MEGA now enables the inference of timetrees, as it implements the RelTime method for estimating divergence times for all branching points in a phylogeny. A new Timetree Wizard in MEGA6 facilitates this timetree inference by providing a graphical user interface (GUI) to specify the phylogeny and calibration constraints step-by-step. This version also contains enhanced algorithms to search for the optimal trees under evolutionary criteria and implements a more advanced memory management that can double the size of sequence data sets to which MEGA can be applied. Both GUI and command-line versions of MEGA6 can be downloaded from www.megasoftware.net free of charge.
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        Fever with thrombocytopenia associated with a novel bunyavirus in China.

        Heightened surveillance of acute febrile illness in China since 2009 has led to the identification of a severe fever with thrombocytopenia syndrome (SFTS) with an unknown cause. Infection with Anaplasma phagocytophilum has been suggested as a cause, but the pathogen has not been detected in most patients on laboratory testing. We obtained blood samples from patients with the case definition of SFTS in six provinces in China. The blood samples were used to isolate the causal pathogen by inoculation of cell culture and for detection of viral RNA on polymerase-chain-reaction assay. The pathogen was characterized on electron microscopy and nucleic acid sequencing. We used enzyme-linked immunosorbent assay, indirect immunofluorescence assay, and neutralization testing to analyze the level of virus-specific antibody in patients' serum samples. We isolated a novel virus, designated SFTS bunyavirus, from patients who presented with fever, thrombocytopenia, leukocytopenia, and multiorgan dysfunction. RNA sequence analysis revealed that the virus was a newly identified member of the genus phlebovirus in the Bunyaviridae family. Electron-microscopical examination revealed virions with the morphologic characteristics of a bunyavirus. The presence of the virus was confirmed in 171 patients with SFTS from six provinces by detection of viral RNA, specific antibodies to the virus in blood, or both. Serologic assays showed a virus-specific immune response in all 35 pairs of serum samples collected from patients during the acute and convalescent phases of the illness. A novel phlebovirus was identified in patients with a life-threatening illness associated with fever and thrombocytopenia in China. (Funded by the China Mega-Project for Infectious Diseases and others.).
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          A new phlebovirus associated with severe febrile illness in Missouri.

          Two men from northwestern Missouri independently presented to a medical facility with fever, fatigue, diarrhea, thrombocytopenia, and leukopenia, and both had been bitten by ticks 5 to 7 days before the onset of illness. Ehrlichia chaffeensis was suspected as the causal agent but was not found on serologic analysis, polymerase-chain-reaction (PCR) assay, or cell culture. Electron microscopy revealed viruses consistent with members of the Bunyaviridae family. Next-generation sequencing and phylogenetic analysis identified the viruses as novel members of the phlebovirus genus. Although Koch's postulates have not been completely fulfilled, we believe that this phlebovirus, which is novel in the Americas, is the cause of this clinical syndrome.
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            Author and article information

            Affiliations
            [1 ] Division of Arboviruses, National Research Institute of Health, Korea Centers for Disease Control and Prevention, Cheongju-si, Republic of Korea
            [2 ] College of Medicine and Medical Research Institute, Chungbuk National University, Cheongju-si, Republic of Korea
            National Institute of Infectious Disease, JAPAN
            Author notes

            The authors have declared that no competing interests exist.

            [¤a]

            Current address: Division of Emerging Infectious Disease and Vector Research, Center for Infectious Diseases Research, National Institute of Health, Korea Centers for Disease Control and Prevention, Cheongju-si, Republic of Korea

            [¤b]

            Current address: Division of Viral Diseases, Center for Laboratory Control of Infectious Diseases, Korea Centers for Disease Control and Prevention, Cheongju-si, Republic of Korea

            Contributors
            Role: Conceptualization, Role: Data curation, Role: Formal analysis, Role: Investigation, Role: Methodology, Role: Resources, Role: Validation, Role: Visualization, Role: Writing – original draft, Role: Writing – review & editing
            Role: Conceptualization, Role: Data curation, Role: Formal analysis, Role: Investigation, Role: Methodology, Role: Resources, Role: Validation, Role: Writing – original draft, Role: Writing – review & editing
            Role: Methodology, Role: Resources, Role: Writing – review & editing
            Role: Resources, Role: Writing – review & editing
            Role: Resources, Role: Writing – review & editing
            Role: Conceptualization, Role: Data curation, Role: Funding acquisition, Role: Project administration, Role: Supervision, Role: Validation, Role: Writing – original draft, Role: Writing – review & editing
            ORCID: http://orcid.org/0000-0002-9519-0219, Role: Conceptualization, Role: Data curation, Role: Funding acquisition, Role: Project administration, Role: Supervision, Role: Validation, Role: Writing – review & editing
            Role: Editor
            Journal
            PLoS Negl Trop Dis
            PLoS Negl Trop Dis
            plos
            plosntds
            PLoS Neglected Tropical Diseases
            Public Library of Science (San Francisco, CA USA )
            1935-2727
            1935-2735
            22 September 2017
            September 2017
            : 11
            : 9
            28937979
            5627960
            10.1371/journal.pntd.0005893
            PNTD-D-17-00706
            (Editor)
            © 2017 Yun et al

            This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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            Figures: 4, Tables: 3, Pages: 15
            Product
            Funding
            This research was funded by intramural grants of the Korea National Research Institute of Health (grant numbers: 2014-ND53001 and 2017-NI53002-00) and a grant of the Korea Health Industry Development Institute (grant number: HI15C2817). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
            Categories
            Research Article
            Research and analysis methods
            Database and informatics methods
            Bioinformatics
            Sequence analysis
            DNA sequence analysis
            Research and Analysis Methods
            Database and Informatics Methods
            Bioinformatics
            Sequence Analysis
            Biology and Life Sciences
            Evolutionary Biology
            Evolutionary Genetics
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            Molecular Biology
            Molecular Biology Techniques
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            Nucleotide Sequencing
            Research and Analysis Methods
            Molecular Biology Techniques
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            Evolutionary Biology
            Evolutionary Systematics
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            Computer and Information Sciences
            Data Management
            Taxonomy
            Evolutionary Systematics
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            Research and Analysis Methods
            Database and Informatics Methods
            Bioinformatics
            Sequence Analysis
            Sequence Alignment
            Biology and Life Sciences
            Genetics
            Human Genetics
            Research and Analysis Methods
            Database and Informatics Methods
            Bioinformatics
            Sequence Analysis
            Amino Acid Sequence Analysis
            Custom metadata
            vor-update-to-uncorrected-proof
            2017-10-04
            All relevant data are within the paper and its Supporting Information files, and deposited in the GenBank database with accession numbers KY273136-KY273138 and KY789433-KY789441.

            Infectious disease & Microbiology

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