Comprehensive molecular detection of tick-borne phleboviruses leads to the retrospective identification of taxonomically unassigned bunyaviruses and the discovery of a novel member of the genus Phlebovirus

Keita Matsuno, Carla Weisend, Masahiro Kajihara, Colette Matysiak, Brandi N. Williamson, Martin Simuunza, Aaron S. Mweene, Ayato Takada, Robert B. Tesh, Hideki Ebihara

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

Until the recent emergence of two human-pathogenic tick-borne phleboviruses (TBPVs) (severe fever with thrombocytopenia syndrome virus [SFTSV] and Heartland virus), TBPVs have been neglected as causative agents of human disease. In particular, no studies have addressed the global distribution of TBPVs, and consequently, our understanding of the mechanism(s) underlying their evolution and emergence remains poor. In order to provide a useful tool for the ecological and epidemiological study of TBPVs, we have established a simple system that can detect all known TBPVs, based on conventional reverse transcription-PCR (RT-PCR) with degenerate primer sets targeting conserved regions of the viral L genome segment. Using this system, we have determined that several viruses that had been isolated from ticks decades ago but had not been taxonomically identified are novel TBPVs. Full-genome sequencing of these viruses revealed a novel fourth TBPV cluster distinct from the three known TBPV clusters (i.e., the SFTS, Bhanja, and Uukuniemi groups) and from the mosquito/sandfly-borne phleboviruses. Furthermore, by using tick samples collected in Zambia, we confirmed that our system had enough sensitivity to detect a new TBPV in a single tick homogenate. This virus, tentatively designated Shibuyunji virus after the region of tick collection, grouped into a novel fourth TBPV cluster. These results indicate that our system can be used as a first-line screening approach for TBPVs and that this kind of work will undoubtedly lead to the discovery of additional novel tick viruses and will expand our knowledge of the evolution and epidemiology of TBPVs.

Original languageEnglish (US)
Pages (from-to)594-604
Number of pages11
JournalJournal of Virology
Volume89
Issue number1
DOIs
StatePublished - 2015

Fingerprint

Phlebovirus
Orthobunyavirus
Ticks
ticks
Viruses
viruses
eclosion

ASJC Scopus subject areas

  • Immunology
  • Virology

Cite this

Comprehensive molecular detection of tick-borne phleboviruses leads to the retrospective identification of taxonomically unassigned bunyaviruses and the discovery of a novel member of the genus Phlebovirus. / Matsuno, Keita; Weisend, Carla; Kajihara, Masahiro; Matysiak, Colette; Williamson, Brandi N.; Simuunza, Martin; Mweene, Aaron S.; Takada, Ayato; Tesh, Robert B.; Ebihara, Hideki.

In: Journal of Virology, Vol. 89, No. 1, 2015, p. 594-604.

Research output: Contribution to journalArticle

Matsuno, Keita ; Weisend, Carla ; Kajihara, Masahiro ; Matysiak, Colette ; Williamson, Brandi N. ; Simuunza, Martin ; Mweene, Aaron S. ; Takada, Ayato ; Tesh, Robert B. ; Ebihara, Hideki. / Comprehensive molecular detection of tick-borne phleboviruses leads to the retrospective identification of taxonomically unassigned bunyaviruses and the discovery of a novel member of the genus Phlebovirus. In: Journal of Virology. 2015 ; Vol. 89, No. 1. pp. 594-604.
@article{fb6e71f11eed402dbf63a9c9f2755a1c,
title = "Comprehensive molecular detection of tick-borne phleboviruses leads to the retrospective identification of taxonomically unassigned bunyaviruses and the discovery of a novel member of the genus Phlebovirus",
abstract = "Until the recent emergence of two human-pathogenic tick-borne phleboviruses (TBPVs) (severe fever with thrombocytopenia syndrome virus [SFTSV] and Heartland virus), TBPVs have been neglected as causative agents of human disease. In particular, no studies have addressed the global distribution of TBPVs, and consequently, our understanding of the mechanism(s) underlying their evolution and emergence remains poor. In order to provide a useful tool for the ecological and epidemiological study of TBPVs, we have established a simple system that can detect all known TBPVs, based on conventional reverse transcription-PCR (RT-PCR) with degenerate primer sets targeting conserved regions of the viral L genome segment. Using this system, we have determined that several viruses that had been isolated from ticks decades ago but had not been taxonomically identified are novel TBPVs. Full-genome sequencing of these viruses revealed a novel fourth TBPV cluster distinct from the three known TBPV clusters (i.e., the SFTS, Bhanja, and Uukuniemi groups) and from the mosquito/sandfly-borne phleboviruses. Furthermore, by using tick samples collected in Zambia, we confirmed that our system had enough sensitivity to detect a new TBPV in a single tick homogenate. This virus, tentatively designated Shibuyunji virus after the region of tick collection, grouped into a novel fourth TBPV cluster. These results indicate that our system can be used as a first-line screening approach for TBPVs and that this kind of work will undoubtedly lead to the discovery of additional novel tick viruses and will expand our knowledge of the evolution and epidemiology of TBPVs.",
author = "Keita Matsuno and Carla Weisend and Masahiro Kajihara and Colette Matysiak and Williamson, {Brandi N.} and Martin Simuunza and Mweene, {Aaron S.} and Ayato Takada and Tesh, {Robert B.} and Hideki Ebihara",
year = "2015",
doi = "10.1128/JVI.02704-14",
language = "English (US)",
volume = "89",
pages = "594--604",
journal = "Journal of Virology",
issn = "0022-538X",
publisher = "American Society for Microbiology",
number = "1",

}

TY - JOUR

T1 - Comprehensive molecular detection of tick-borne phleboviruses leads to the retrospective identification of taxonomically unassigned bunyaviruses and the discovery of a novel member of the genus Phlebovirus

AU - Matsuno, Keita

AU - Weisend, Carla

AU - Kajihara, Masahiro

AU - Matysiak, Colette

AU - Williamson, Brandi N.

AU - Simuunza, Martin

AU - Mweene, Aaron S.

AU - Takada, Ayato

AU - Tesh, Robert B.

AU - Ebihara, Hideki

PY - 2015

Y1 - 2015

N2 - Until the recent emergence of two human-pathogenic tick-borne phleboviruses (TBPVs) (severe fever with thrombocytopenia syndrome virus [SFTSV] and Heartland virus), TBPVs have been neglected as causative agents of human disease. In particular, no studies have addressed the global distribution of TBPVs, and consequently, our understanding of the mechanism(s) underlying their evolution and emergence remains poor. In order to provide a useful tool for the ecological and epidemiological study of TBPVs, we have established a simple system that can detect all known TBPVs, based on conventional reverse transcription-PCR (RT-PCR) with degenerate primer sets targeting conserved regions of the viral L genome segment. Using this system, we have determined that several viruses that had been isolated from ticks decades ago but had not been taxonomically identified are novel TBPVs. Full-genome sequencing of these viruses revealed a novel fourth TBPV cluster distinct from the three known TBPV clusters (i.e., the SFTS, Bhanja, and Uukuniemi groups) and from the mosquito/sandfly-borne phleboviruses. Furthermore, by using tick samples collected in Zambia, we confirmed that our system had enough sensitivity to detect a new TBPV in a single tick homogenate. This virus, tentatively designated Shibuyunji virus after the region of tick collection, grouped into a novel fourth TBPV cluster. These results indicate that our system can be used as a first-line screening approach for TBPVs and that this kind of work will undoubtedly lead to the discovery of additional novel tick viruses and will expand our knowledge of the evolution and epidemiology of TBPVs.

AB - Until the recent emergence of two human-pathogenic tick-borne phleboviruses (TBPVs) (severe fever with thrombocytopenia syndrome virus [SFTSV] and Heartland virus), TBPVs have been neglected as causative agents of human disease. In particular, no studies have addressed the global distribution of TBPVs, and consequently, our understanding of the mechanism(s) underlying their evolution and emergence remains poor. In order to provide a useful tool for the ecological and epidemiological study of TBPVs, we have established a simple system that can detect all known TBPVs, based on conventional reverse transcription-PCR (RT-PCR) with degenerate primer sets targeting conserved regions of the viral L genome segment. Using this system, we have determined that several viruses that had been isolated from ticks decades ago but had not been taxonomically identified are novel TBPVs. Full-genome sequencing of these viruses revealed a novel fourth TBPV cluster distinct from the three known TBPV clusters (i.e., the SFTS, Bhanja, and Uukuniemi groups) and from the mosquito/sandfly-borne phleboviruses. Furthermore, by using tick samples collected in Zambia, we confirmed that our system had enough sensitivity to detect a new TBPV in a single tick homogenate. This virus, tentatively designated Shibuyunji virus after the region of tick collection, grouped into a novel fourth TBPV cluster. These results indicate that our system can be used as a first-line screening approach for TBPVs and that this kind of work will undoubtedly lead to the discovery of additional novel tick viruses and will expand our knowledge of the evolution and epidemiology of TBPVs.

UR - http://www.scopus.com/inward/record.url?scp=84919458576&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84919458576&partnerID=8YFLogxK

U2 - 10.1128/JVI.02704-14

DO - 10.1128/JVI.02704-14

M3 - Article

C2 - 25339769

AN - SCOPUS:84919458576

VL - 89

SP - 594

EP - 604

JO - Journal of Virology

JF - Journal of Virology

SN - 0022-538X

IS - 1

ER -