A New Clade of Insect-Specific Flaviviruses from Australian <italic toggle="yes">Anopheles</italic> Mosquitoes Displays Species-Specific Host Restriction

ABSTRACT Flaviviruses are arthropod-borne viruses found worldwide and are responsible for significant human and veterinary diseases, including dengue, Zika, and West Nile fever. Some flaviviruses are insect specific and replicate only in mosquitoes. We report a genetically divergent group of insect-...

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Autores principales: Agathe M. G. Colmant, Jody Hobson-Peters, Helle Bielefeldt-Ohmann, Andrew F. van den Hurk, Sonja Hall-Mendelin, Weng Kong Chow, Cheryl A. Johansen, Jelke Fros, Peter Simmonds, Daniel Watterson, Chris Cazier, Kayvan Etebari, Sassan Asgari, Benjamin L. Schulz, Nigel Beebe, Laura J. Vet, Thisun B. H. Piyasena, Hong-Duyen Nguyen, Ross T. Barnard, Roy A. Hall
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:8ec632591db04dedb9b88059f1d0663e2021-11-15T15:22:04ZA New Clade of Insect-Specific Flaviviruses from Australian <italic toggle="yes">Anopheles</italic> Mosquitoes Displays Species-Specific Host Restriction10.1128/mSphere.00262-172379-5042https://doaj.org/article/8ec632591db04dedb9b88059f1d0663e2017-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00262-17https://doaj.org/toc/2379-5042ABSTRACT Flaviviruses are arthropod-borne viruses found worldwide and are responsible for significant human and veterinary diseases, including dengue, Zika, and West Nile fever. Some flaviviruses are insect specific and replicate only in mosquitoes. We report a genetically divergent group of insect-specific flaviviruses from Anopheles mosquitoes that do not replicate in arthropod cell lines or heterologous Anopheles species, exhibiting unprecedented specialization for their host species. Determination of the complete sequences of the RNA genomes of three of these viruses, Karumba virus (KRBV), Haslams Creek virus, and Mac Peak virus (McPV), that are found in high prevalence in some Anopheles mosquito populations and detection of virus-specific proteins, replicative double-stranded RNA, and small interfering RNA responses in the host mosquito species provided strong evidence of a functional replicating virus in the mosquito midgut. Analysis of nucleotide composition in the KRBV and McPV sequences also revealed a pattern consistent with the virus evolving to replicate only in insects. These findings represent a significant advance in our knowledge of mosquito-borne flavivirus ecology, host restriction, and evolution. IMPORTANCE Flaviviruses like dengue, Zika, or West Nile virus infect millions of people each year and are transmitted to humans via infected-mosquito bites. A subset of flaviviruses can only replicate in the mosquito host, and recent studies have shown that some can interfere with pathogenic flaviviruses in mosquitoes and limit the replication and transmission of the latter. The insect-specific flaviviruses (ISFs) reported here form a new Anopheles mosquito-associated clade separate from the Aedes- and Culex-associated ISF clades. The identification of distinct clades for each mosquito genus provides new insights into the evolution and ecology of flaviviruses. One of these viruses was shown to replicate in the midgut of the mosquito host and exhibit the most specialized host restriction reported to date for ISFs. Understanding this unprecedented host restriction in ISFs could help identify the mechanisms involved in the evolution of flaviviruses and their emergence as mosquito-borne pathogens.Agathe M. G. ColmantJody Hobson-PetersHelle Bielefeldt-OhmannAndrew F. van den HurkSonja Hall-MendelinWeng Kong ChowCheryl A. JohansenJelke FrosPeter SimmondsDaniel WattersonChris CazierKayvan EtebariSassan AsgariBenjamin L. SchulzNigel BeebeLaura J. VetThisun B. H. PiyasenaHong-Duyen NguyenRoss T. BarnardRoy A. HallAmerican Society for MicrobiologyarticleAnophelesinsect-specific flaviviruscoevolutiondinucleotide analysishost restrictionimmunohistochemistryMicrobiologyQR1-502ENmSphere, Vol 2, Iss 4 (2017)
institution DOAJ
collection DOAJ
language EN
topic Anopheles
insect-specific flavivirus
coevolution
dinucleotide analysis
host restriction
immunohistochemistry
Microbiology
QR1-502
spellingShingle Anopheles
insect-specific flavivirus
coevolution
dinucleotide analysis
host restriction
immunohistochemistry
Microbiology
QR1-502
Agathe M. G. Colmant
Jody Hobson-Peters
Helle Bielefeldt-Ohmann
Andrew F. van den Hurk
Sonja Hall-Mendelin
Weng Kong Chow
Cheryl A. Johansen
Jelke Fros
Peter Simmonds
Daniel Watterson
Chris Cazier
Kayvan Etebari
Sassan Asgari
Benjamin L. Schulz
Nigel Beebe
Laura J. Vet
Thisun B. H. Piyasena
Hong-Duyen Nguyen
Ross T. Barnard
Roy A. Hall
A New Clade of Insect-Specific Flaviviruses from Australian <italic toggle="yes">Anopheles</italic> Mosquitoes Displays Species-Specific Host Restriction
description ABSTRACT Flaviviruses are arthropod-borne viruses found worldwide and are responsible for significant human and veterinary diseases, including dengue, Zika, and West Nile fever. Some flaviviruses are insect specific and replicate only in mosquitoes. We report a genetically divergent group of insect-specific flaviviruses from Anopheles mosquitoes that do not replicate in arthropod cell lines or heterologous Anopheles species, exhibiting unprecedented specialization for their host species. Determination of the complete sequences of the RNA genomes of three of these viruses, Karumba virus (KRBV), Haslams Creek virus, and Mac Peak virus (McPV), that are found in high prevalence in some Anopheles mosquito populations and detection of virus-specific proteins, replicative double-stranded RNA, and small interfering RNA responses in the host mosquito species provided strong evidence of a functional replicating virus in the mosquito midgut. Analysis of nucleotide composition in the KRBV and McPV sequences also revealed a pattern consistent with the virus evolving to replicate only in insects. These findings represent a significant advance in our knowledge of mosquito-borne flavivirus ecology, host restriction, and evolution. IMPORTANCE Flaviviruses like dengue, Zika, or West Nile virus infect millions of people each year and are transmitted to humans via infected-mosquito bites. A subset of flaviviruses can only replicate in the mosquito host, and recent studies have shown that some can interfere with pathogenic flaviviruses in mosquitoes and limit the replication and transmission of the latter. The insect-specific flaviviruses (ISFs) reported here form a new Anopheles mosquito-associated clade separate from the Aedes- and Culex-associated ISF clades. The identification of distinct clades for each mosquito genus provides new insights into the evolution and ecology of flaviviruses. One of these viruses was shown to replicate in the midgut of the mosquito host and exhibit the most specialized host restriction reported to date for ISFs. Understanding this unprecedented host restriction in ISFs could help identify the mechanisms involved in the evolution of flaviviruses and their emergence as mosquito-borne pathogens.
format article
author Agathe M. G. Colmant
Jody Hobson-Peters
Helle Bielefeldt-Ohmann
Andrew F. van den Hurk
Sonja Hall-Mendelin
Weng Kong Chow
Cheryl A. Johansen
Jelke Fros
Peter Simmonds
Daniel Watterson
Chris Cazier
Kayvan Etebari
Sassan Asgari
Benjamin L. Schulz
Nigel Beebe
Laura J. Vet
Thisun B. H. Piyasena
Hong-Duyen Nguyen
Ross T. Barnard
Roy A. Hall
author_facet Agathe M. G. Colmant
Jody Hobson-Peters
Helle Bielefeldt-Ohmann
Andrew F. van den Hurk
Sonja Hall-Mendelin
Weng Kong Chow
Cheryl A. Johansen
Jelke Fros
Peter Simmonds
Daniel Watterson
Chris Cazier
Kayvan Etebari
Sassan Asgari
Benjamin L. Schulz
Nigel Beebe
Laura J. Vet
Thisun B. H. Piyasena
Hong-Duyen Nguyen
Ross T. Barnard
Roy A. Hall
author_sort Agathe M. G. Colmant
title A New Clade of Insect-Specific Flaviviruses from Australian <italic toggle="yes">Anopheles</italic> Mosquitoes Displays Species-Specific Host Restriction
title_short A New Clade of Insect-Specific Flaviviruses from Australian <italic toggle="yes">Anopheles</italic> Mosquitoes Displays Species-Specific Host Restriction
title_full A New Clade of Insect-Specific Flaviviruses from Australian <italic toggle="yes">Anopheles</italic> Mosquitoes Displays Species-Specific Host Restriction
title_fullStr A New Clade of Insect-Specific Flaviviruses from Australian <italic toggle="yes">Anopheles</italic> Mosquitoes Displays Species-Specific Host Restriction
title_full_unstemmed A New Clade of Insect-Specific Flaviviruses from Australian <italic toggle="yes">Anopheles</italic> Mosquitoes Displays Species-Specific Host Restriction
title_sort new clade of insect-specific flaviviruses from australian <italic toggle="yes">anopheles</italic> mosquitoes displays species-specific host restriction
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/8ec632591db04dedb9b88059f1d0663e
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