The high genetic variation of viruses of the genus Nairovirus reflects the diversity of their predominant tick hosts

The genus Nairovirus (family Bunyaviridae) contains seven serogroups consisting of 34 predominantly tick-borne viruses, including several associated with severe human and livestock diseases [e.g., Crimean Congo hemorrhagic fever (CCHF) and Nairobi sheep disease (NSD), respectively]. Before this repo...

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Published in:Virology (New York, N.Y.) Vol. 318; no. 1; pp. 10 - 16
Main Authors: Honig, Jessica E, Osborne, Jane C, Nichol, Stuart T
Format: Journal Article
Language:English
Published: United States 05-01-2004
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Abstract The genus Nairovirus (family Bunyaviridae) contains seven serogroups consisting of 34 predominantly tick-borne viruses, including several associated with severe human and livestock diseases [e.g., Crimean Congo hemorrhagic fever (CCHF) and Nairobi sheep disease (NSD), respectively]. Before this report, no comparative genetic studies or molecular detection assays had been developed for this virus genus. To characterize at least one representative from each of the seven serogroups, reverse transcriptase-polymerase chain reaction (RT-PCR) primers targeting the L polymerase-encoding region of the RNA genome of these viruses were successfully designed based on conserved amino acid motifs present in the predicted catalytic core region. Sequence analysis showed the nairoviruses to be a highly diverse group, exhibiting up to 39.4% and 46.0% nucleotide and amino acid identity differences, respectively. Virus genetic relationships correlated well with serologic groupings and with tick host associations. Hosts of these viruses include both the hard (family Ixodidae) and soft (family Argasidae) ticks. Virus phylogenetic analysis reveals two major monophyletic groups: hard tick and soft tick-vectored viruses. In addition, viruses vectored by Ornithodoros, Carios, and Argas genera ticks also form three separate monophyletic lineages. The striking similarities between tick and nairovirus phylogenies are consistent with possible coevolution of the viruses and their tick hosts. Fossil and phylogenetic data placing the hard tick-soft tick divergence between 120 and 92 million years ago suggest an ancient origin for viruses of the genus Nairovirus.
AbstractList The genus Nairovirus (family Bunyaviridae) contains seven serogroups consisting of 34 predominantly tick-borne viruses, including several associated with severe human and livestock diseases [e.g., Crimean Congo hemorrhagic fever (CCHF) and Nairobi sheep disease (NSD), respectively]. Before this report, no comparative genetic studies or molecular detection assays had been developed for this virus genus. To characterize at least one representative from each of the seven serogroups, reverse transcriptase-polymerase chain reaction (RT-PCR) primers targeting the L polymerase-encoding region of the RNA genome of these viruses were successfully designed based on conserved amino acid motifs present in the predicted catalytic core region. Sequence analysis showed the nairoviruses to be a highly diverse group, exhibiting up to 39.4% and 46.0% nucleotide and amino acid identity differences, respectively. Virus genetic relationships correlated well with serologic groupings and with tick host associations. Hosts of these viruses include both the hard (family Ixodidae) and soft (family Argasidae) ticks. Virus phylogenetic analysis reveals two major monophyletic groups: hard tick and soft tick-vectored viruses. In addition, viruses vectored by Ornithodoros, Carios, and Argas genera ticks also form three separate monophyletic lineages. The striking similarities between tick and nairovirus phylogenies are consistent with possible coevolution of the viruses and their tick hosts. Fossil and phylogenetic data placing the hard tick-soft tick divergence between 120 and 92 million years ago suggest an ancient origin for viruses of the genus Nairovirus.
Author Honig, Jessica E
Osborne, Jane C
Nichol, Stuart T
Author_xml – sequence: 1
  givenname: Jessica E
  surname: Honig
  fullname: Honig, Jessica E
  organization: Special Pathogens Branch, Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, Atlanta, GA 30333, USA
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  givenname: Jane C
  surname: Osborne
  fullname: Osborne, Jane C
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  givenname: Stuart T
  surname: Nichol
  fullname: Nichol, Stuart T
BackLink https://www.ncbi.nlm.nih.gov/pubmed/14972529$$D View this record in MEDLINE/PubMed
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Cites_doi 10.1006/viro.2002.1514
10.1007/s00705-002-0913-4
10.1093/oxfordjournals.molbev.a003992
10.1111/j.1365-3113.1993.tb00669.x
10.1603/0013-8746(2001)094[0010:FMROAP]2.0.CO;2
10.1099/0022-1317-77-8-1775
10.1099/0022-1317-66-11-2513
10.1099/0022-1317-75-6-1345
10.1016/0042-6822(92)90609-S
10.1146/annurev.es.20.110189.002145
10.1128/JVI.76.14.7263-7275.2002
10.1093/emboj/17.19.5844
10.1016/0021-9975(78)90005-1
10.1006/mpev.1996.0382
10.1093/jmedent/15.4.307
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References Klompen (10.1016/j.virol.2003.09.021_BIB8) 2001; 94
Mans (10.1016/j.virol.2003.09.021_BIB11) 2002; 19
Oliver (10.1016/j.virol.2003.09.021_BIB17) 1989; 20
Terpstra (10.1016/j.virol.2003.09.021_BIB20) 1994
Nichol (10.1016/j.virol.2003.09.021_BIB16) 2001; vol. 2
Watret (10.1016/j.virol.2003.09.021_BIB21) 1985; 66
Hoogstraal (10.1016/j.virol.2003.09.021_BIB6) 1985
Muller (10.1016/j.virol.2003.09.021_BIB15) 1994; 75
Marriott (10.1016/j.virol.2003.09.021_BIB13) 1992; 189
Swanepoel (10.1016/j.virol.2003.09.021_BIB19) 1994
Black (10.1016/j.virol.2003.09.021_BIB2) 1997; 7
Elliott (10.1016/j.virol.2003.09.021_BIB4) 2000
Hoogstraal (10.1016/j.virol.2003.09.021_BIB5) 1979; 15
Aquino (10.1016/j.virol.2003.09.021_BIB1) 2003; 148
Marriott (10.1016/j.virol.2003.09.021_BIB14) 1996; 77
Sanchez (10.1016/j.virol.2003.09.021_BIB18) 2002; 76
Karabatsos (10.1016/j.virol.2003.09.021_BIB7) 1985
Li (10.1016/j.virol.2003.09.021_BIB10) 1998; 17
Davies (10.1016/j.virol.2003.09.021_BIB3) 1978; 88
Marczinke (10.1016/j.virol.2003.09.021_BIB12) 2002; 303
Klompen (10.1016/j.virol.2003.09.021_BIB9) 1993; 18
References_xml – volume: 303
  start-page: 146
  year: 2002
  ident: 10.1016/j.virol.2003.09.021_BIB12
  article-title: Nairobi sheep disease virus, an important tick-borne pathogen of sheep and goats in Africa, is also present in Asia
  publication-title: Virology
  doi: 10.1006/viro.2002.1514
  contributor:
    fullname: Marczinke
– volume: 148
  start-page: 19
  year: 2003
  ident: 10.1016/j.virol.2003.09.021_BIB1
  article-title: Analysis of Oropouche virus L protein amino acid sequence showed the presence of an additional conserved region that could harbour an important role for the polymerase activity
  publication-title: Arch. Virol.
  doi: 10.1007/s00705-002-0913-4
  contributor:
    fullname: Aquino
– volume: 19
  start-page: 1695
  year: 2002
  ident: 10.1016/j.virol.2003.09.021_BIB11
  article-title: Evolution of hematophagy in ticks: common origins for blood coagulation and platelet aggregation inhibitors for soft ticks of the genus Ornithodoros
  publication-title: Mol. Biol. Evol.
  doi: 10.1093/oxfordjournals.molbev.a003992
  contributor:
    fullname: Mans
– volume: 18
  start-page: 313
  year: 1993
  ident: 10.1016/j.virol.2003.09.021_BIB9
  article-title: Systematic relationships in the soft ticks (Acari: Ixodida: Argasidae)
  publication-title: Syst. Entomol.
  doi: 10.1111/j.1365-3113.1993.tb00669.x
  contributor:
    fullname: Klompen
– volume: 94
  start-page: 10
  year: 2001
  ident: 10.1016/j.virol.2003.09.021_BIB8
  article-title: First mesozoic record of a parasitiform mite: a larval argasid tick in Cretaceous amber (Acari: Ixodida: Argasidae)
  publication-title: Ann. Entomol. Soc. Am.
  doi: 10.1603/0013-8746(2001)094[0010:FMROAP]2.0.CO;2
  contributor:
    fullname: Klompen
– volume: 77
  start-page: 1775
  year: 1996
  ident: 10.1016/j.virol.2003.09.021_BIB14
  article-title: Large RNA segment of Dugbe nairovirus encodes the putative RNA polymerase
  publication-title: J. Gen. Virol.
  doi: 10.1099/0022-1317-77-8-1775
  contributor:
    fullname: Marriott
– volume: 66
  start-page: 2513
  year: 1985
  ident: 10.1016/j.virol.2003.09.021_BIB21
  article-title: The proteins and RNAs specified by Clo Mor virus, a Scottish nairovirus
  publication-title: J. Gen. Virol.
  doi: 10.1099/0022-1317-66-11-2513
  contributor:
    fullname: Watret
– start-page: 599
  year: 2000
  ident: 10.1016/j.virol.2003.09.021_BIB4
  article-title: Family Bunyaviridae
  contributor:
    fullname: Elliott
– volume: 75
  start-page: 1345
  year: 1994
  ident: 10.1016/j.virol.2003.09.021_BIB15
  article-title: Rift Valley fever virus L segment: correction of the sequence and possible functional role of newly identified regions conserved in RNA-dependent polymerases
  publication-title: J. Gen. Virol.
  doi: 10.1099/0022-1317-75-6-1345
  contributor:
    fullname: Muller
– volume: 189
  start-page: 795
  year: 1992
  ident: 10.1016/j.virol.2003.09.021_BIB13
  article-title: Comparison of the S RNA segments and nucleoprotein sequences of Crimean-Congo hemorrhagic fever, Hazara, and Dugbe viruses
  publication-title: Virology
  doi: 10.1016/0042-6822(92)90609-S
  contributor:
    fullname: Marriott
– volume: 20
  start-page: 397
  year: 1989
  ident: 10.1016/j.virol.2003.09.021_BIB17
  article-title: Biology and systematics of ticks (Acari: Ixodida)
  publication-title: Annu. Rev. Ecol. Syst.
  doi: 10.1146/annurev.es.20.110189.002145
  contributor:
    fullname: Oliver
– volume: 76
  start-page: 7263
  year: 2002
  ident: 10.1016/j.virol.2003.09.021_BIB18
  article-title: Characterization of the glycoproteins of Crimean-Congo hemorrhagic fever virus
  publication-title: J. Virol.
  doi: 10.1128/JVI.76.14.7263-7275.2002
  contributor:
    fullname: Sanchez
– start-page: 718
  year: 1994
  ident: 10.1016/j.virol.2003.09.021_BIB20
  article-title: Nairobi sheep disease
  contributor:
    fullname: Terpstra
– volume: 17
  start-page: 5844
  year: 1998
  ident: 10.1016/j.virol.2003.09.021_BIB10
  article-title: RNA-dependent activation of primer RNA production by influenza virus polymerase: different regions of the same protein subunit constitute the two required RNA-binding sites
  publication-title: EMBO J.
  doi: 10.1093/emboj/17.19.5844
  contributor:
    fullname: Li
– volume: vol. 2
  start-page: 1603
  year: 2001
  ident: 10.1016/j.virol.2003.09.021_BIB16
  article-title: Bunyaviruses
  contributor:
    fullname: Nichol
– start-page: 505
  year: 1985
  ident: 10.1016/j.virol.2003.09.021_BIB6
  article-title: Tick and mammal coevolution, with emphasis on Haemaphysalis
  contributor:
    fullname: Hoogstraal
– year: 1985
  ident: 10.1016/j.virol.2003.09.021_BIB7
  contributor:
    fullname: Karabatsos
– start-page: 723
  year: 1994
  ident: 10.1016/j.virol.2003.09.021_BIB19
  article-title: Crimean-Congo haemorrhagic fever
  contributor:
    fullname: Swanepoel
– volume: 88
  start-page: 519
  year: 1978
  ident: 10.1016/j.virol.2003.09.021_BIB3
  article-title: The serological relationships of Nairobi sheep disease virus
  publication-title: J. Comp. Pathol.
  doi: 10.1016/0021-9975(78)90005-1
  contributor:
    fullname: Davies
– volume: 7
  start-page: 129
  year: 1997
  ident: 10.1016/j.virol.2003.09.021_BIB2
  article-title: Phylogenetic relationships among tick subfamilies (Ixodida: Ixodidae: Argasidae) based on the 18S nuclear rDNA gene
  publication-title: Mol. Phylogenet. Evol.
  doi: 10.1006/mpev.1996.0382
  contributor:
    fullname: Black
– volume: 15
  start-page: 407
  year: 1979
  ident: 10.1016/j.virol.2003.09.021_BIB5
  article-title: The epidemiology of tick borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa
  publication-title: J. Med. Entomol.
  doi: 10.1093/jmedent/15.4.307
  contributor:
    fullname: Hoogstraal
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Snippet The genus Nairovirus (family Bunyaviridae) contains seven serogroups consisting of 34 predominantly tick-borne viruses, including several associated with...
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SubjectTerms Amino Acid Sequence
Animals
Argasidae
Argasidae - classification
Argasidae - virology
Carios
DNA Primers
Genetic Variation
Hemorrhagic Fever, Crimean - virology
Humans
Ixodidae
Ixodidae - classification
Ixodidae - virology
Molecular Sequence Data
Nairobi Sheep Disease - virology
Nairovirus
Nairovirus - classification
Nairovirus - genetics
Nairovirus - physiology
Ornithodoros
Phylogeny
Reverse Transcriptase Polymerase Chain Reaction
Sequence Analysis, DNA
Serotyping
Tick-Borne Diseases - virology
Title The high genetic variation of viruses of the genus Nairovirus reflects the diversity of their predominant tick hosts
URI https://www.ncbi.nlm.nih.gov/pubmed/14972529
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