A new clade of insect-specific flaviviruses from Australian Anopheles mosquitoes displays species-specific host-restriction

Colmant, Agathe M. G., Hobson-Peters, Jody, Bielefeldt-Ohmann, Helle, van den Hurk, Andrew F., Hall-Mendelin, Sonja, Chow, Weng Kong, Johansen, Cheryl A., Fros, Jelke, Simmonds, Peter, Watterson, Daniel, Cazier, Chris, Etebari, Kayvan, Asgari, Sassan, Schulz, Benjamin L., Beebe, Nigel, Vet, Laura J., Piyasena, Thisun B. H., Nguyen, Hong-Duyen, Barnard, Ross T. and Hall, Roy A. (2017) A new clade of insect-specific flaviviruses from Australian Anopheles mosquitoes displays species-specific host-restriction. mSphere, 2 4: e00262-17.1-e00262-17.19. doi:10.1128/mSphere.00262-17

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Author Colmant, Agathe M. G.
Hobson-Peters, Jody
Bielefeldt-Ohmann, Helle
van den Hurk, Andrew F.
Hall-Mendelin, Sonja
Chow, Weng Kong
Johansen, Cheryl A.
Fros, Jelke
Simmonds, Peter
Watterson, Daniel
Cazier, Chris
Etebari, Kayvan
Asgari, Sassan
Schulz, Benjamin L.
Beebe, Nigel
Vet, Laura J.
Piyasena, Thisun B. H.
Nguyen, Hong-Duyen
Barnard, Ross T.
Hall, Roy A.
Title A new clade of insect-specific flaviviruses from Australian Anopheles mosquitoes displays species-specific host-restriction
Formatted title
A new clade of insect-specific flaviviruses from Australian Anopheles mosquitoes displays species-specific host-restriction
Journal name mSphere   Check publisher's open access policy
ISSN 2379-5042
Publication date 2017-07-12
Year available 2017
Sub-type Article (original research)
DOI 10.1128/mSphere.00262-17
Open Access Status DOI
Volume 2
Issue 4
Start page e00262-17.1
End page e00262-17.19
Total pages 19
Place of publication Washington, DC, United States
Publisher American Society for Microbiology
Language eng
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.
Formatted 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.
Keyword Anopheles
Insect-specific flavivirus
Coevolution
Dinucleotide analysis
Host restriction
Immunohistochemistry
Monoclonal antibodies
Mosquito midgut
Recombinant NS1
siRNA
Q-Index Code C1
Q-Index Status Provisional Code
Grant ID DP120103994
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: HERDC Pre-Audit
School of Biological Sciences Publications
School of Chemistry and Molecular Biosciences
 
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Created: Thu, 13 Jul 2017, 15:50:28 EST by Prof Sassan Asgari on behalf of School of Biological Sciences