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Commensal Viruses of Mosquitoes: Host Restriction, Transmission, and Interaction with Arboviral Pathogens Roy A. Hall1, Helle Bielefeldt-Ohmann1, Breeanna J. McLean1, Caitlin A. O’Brien1, Agathe M.G. Colmant1, Thisun B.H. Piyasena1, Jessica J. Harrison1, Natalee D. Newton1, Ross T. Barnard1, Natalie A. Prow1,2, Joshua M. Deerain1, Marcus G.K.Y. Mah1,2 and Jody Hobson-Peters1 1Australian Infectious Diseases Research Centre, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, Australia. 2QIMR Berghofer Medical Research Institute, Herston, QLD, Australia. Supplementary Issue: Evolution of the Insect Virome ABSTR ACT: Recent advances in virus detection strategies and deep sequencing technologies have enabled the identification of a multitude of new viruses that persistently infect mosquitoes but do not infect vertebrates. These are usually referred to as insect-specific viruses (ISVs). These novel viruses have generated considerable interest in their modes of transmission, persistence in mosquito populations, the mechanisms that restrict their host range to mosquitoes, and their interactions with pathogens transmissible by the same mosquito. In this article, we discuss studies in our laboratory and others that demonstrate that many ISVs are efficiently transmitted directly from the female mosquito to their progeny via infected eggs, and, moreover, that persistent infection of mosquito cell cultures or whole mosquitoes with ISVs can restrict subsequent infection, replication, and transmission of some mosquito-borne viral pathogens. This suggests that some ISVs may act as natural regulators of arboviral transmission. We also discuss viral and host factors that may be responsible for their host restriction. KEYWORDS: mosquito-borne viruses, insect-specific viruses, flaviviruses, bunyaviruses, mesoniviruses, negeviruses SUPPLEMENT: Evolution of the Insect Virome COrrespONDence: [email protected] CITATION: Hall et al. Commensal Viruses of Mosquitoes: Host Restriction, Transmission, COpyriGht: © the authors, publisher and licensee Libertas Academica Limited. This is and Interaction with Arboviral Pathogens. Evolutionary Bioinformatics 2016:12(S2) 35–44 an open-access article distributed under the terms of the Creative Commons CC-BY-NC doi: 10.4137/EBO.S40740. 3.0 License. TYPE: Review Paper subject to independent expert blind peer review. All editorial decisions made ReceiveD: October 04, 2016. RESUBmitteD: November 21, 2016. AccepteD FOR by independent academic editor. Upon submission manuscript was subject to anti- PUBlicatiON: November 23, 2016. plagiarism scanning. Prior to publication all authors have given signed confirmation of agreement to article publication and compliance with all applicable ethical and legal AcaDemic EDitOR: Liuyang Wang, Associate Editor requirements, including the accuracy of author and contributor information, disclosure of competing interests and funding sources, compliance with ethical requirements relating Peer RevieW: Four peer reviewers contributed to the peer review report. Reviewers’ to human and animal study participants, and compliance with any copyright requirements reports totaled 711 words, excluding any confidential comments to the academic editor. of third parties. This journal is a member of the Committee on Publication Ethics (COPE). FunDinG: This study was funded by the Australian Research Council (ARC Published by Libertas Academica. Learn more about this journal. DP120103994). The authors confirm that the funder had no influence over the study design, content of the article, or selection of this journal. COmpetinG Interests: Authors disclose no potential conflicts of interest. Introduction avenue for developing vector control strategies. Furthermore, Mosquito-borne viruses are objects of intense research due to the potential to genetically manipulate ISVs to develop new their complex biology, ecology, and evolution and their poten- platforms for the production of safe diagnostic antigens and tial to produce large and unpredictable outbreaks of disease.1 vaccines for mosquito-borne pathogens is now recognized as Indeed, explosive outbreaks of disease in many regions of the an innovative and a viable strategy.8 world have been caused by mosquito-borne viruses such as In this article, we review the key research conducted dengue virus (DENV), Zika virus (ZIKV), chikungunya virus on mosquito-borne ISVs with a focus on the recent isola- (CHIKV), yellow fever virus (YFV), Japanese encephalitis tion and characterization of several new ISVs that group virus (JEV), Ross River virus (RRV), and Rift Valley fever within a range of virus families including flaviviruses, virus. In the absence of safe and effective vaccines and anti- alphaviruses, bunyaviruses, mesoniviruses, negeviruses, and virals against many of these viruses, new approaches are being reoviruses. We also discuss mechanistic and evolutionary explored to control these diseases and their transmissions. features that are likely to be associated with the adaption of Currently, there is a strong research focus on a novel ISVs to a mosquito-only transmission cycle and the poten- group of “insect-specific” viruses (ISVs) that persistently infect tial applications of these viruses as novel model systems for mosquitoes, but do not infect vertebrates.2,3 Importantly, research, recombinant technology platforms, and agents of persistent infection of mosquitoes with some ISVs appears biological control. to interfere with the replication and transmission of medi- cally significant viruses, such as West Nile virus (WNV).4–7 Flaviviruses These findings suggest that ISVs may act as natural regulators The genus Flavivirus (family Flaviviridae) includes many of transmission of some arboviruses and may provide a new important mosquito-borne human pathogens such as DENV, EVOLUTIONARY BIOINFORMATICS 2016:12(S2) 35 Hall et al WNV, YFV, and ZIKV.9 These viruses cycle between inoculation of the samples onto C6/36 cells prior to the mosquitoes and human or animal hosts with replication in detection by reverse transcription polymerase chain reac- both the arthropod and the vertebrate required to maintain tion and/or the presence of cytopathic effect (CPE) in the transmission and persistence of the virus. In contrast, insect- cells.5 Subsequently, we enhanced the speed and sensitivity specific flaviviruses (ISFs) replicate only in mosquitoes and of the ISF isolation protocol by the detection of viral replica- form an interesting subgroup within the Flavivirus genus.2 tive dsRNA in inoculated mosquito cell culture by the use of The first recognized ISF, cell-fusing agent virus (CFAV), anti-dsRNA mAbs in enzyme-linked immunosorbent assay – was identified as an endogenous virus in a cell line derived referred to as “MAVRIC” (monoclonal antibodies against from Aedes aegypti mosquito larvae.10 However, it was not until viral RNA intermediates in cells).16 This approach allowed the almost 30 years later that ISFs, including CFAV and a related detection of novel and genetically diverse ISFs (as well as other virus “Kamiti River virus”, were first isolated from mosquitoes novel RNA viruses, which are given in the following sections) in the wild and characterized.11–13 Since then, many ISFs have in a sequence-independent manner and provided a relatively been isolated or genetically detected in several mosquito species simple, cost-effective, and high-throughput protocol for the from different regions of the world.2 Studies by Saiyasombat detection of infected cultures prior to sequencing and charac- et al.14 and Bolling et al.6 indicate that ISFs are maintained in terization of the isolates. mosquito populations by vertical transmission – a process by Several ISFs were subsequently isolated from Australian which the progeny of infected female mosquitoes is infected mosquitoes including Palm Creek virus (PCV) from Coquillet- via the egg.15 tidia xanthogaster in northern Australia5,17; Parramatta River In 2010, our laboratory initiated a project to assess the virus (PaRV) from Aedes vigilax from Sydney, Newcastle, biodiversity of ISFs in Australian mosquitoes. This was ini- and Brisbane17; and local isolates of CFAV from Ae. aegypti tially performed by the detection of flavivirus RNA directly from Cairns (Harrison et al, unpublished data). Figure 1 in archival samples of homogenized mosquito pools or by illustrates the geographical distribution of these viruses Palm Creek virus (PCV) Bamaga virus Cq. xanthogaster (BgV) Cx. annulirostris Cell Fusing Agent Virus (CFAV) Ae. aegypti Nothern Territory Queensland Western Australia South Australia Parramatta river Virus (PaRV) New Ae. vigilax South Wales Victoria Tasmania Figure 1. Map of Australia showing general locations of insect-specific flavivirus isolations. 36 EVOLUTIONARY BIOINFORMATICS 2016:12(S2) Commensal viruses of mosquitoes MODV NC_003635.1 TBEV NC_001672 1 CxFV NC_008604 1 CTFV HE574574 1 QBV NC_012671 Lineage I ISF 1 NIEV NC_024299 1 PCV KC505248 1 NAKV GQ165809 1 AEFV NC_012932 1 KRV NC_005064 1 CFAV NC_001564 1 HANKV JQ268258 PaRV KT192549 1 1 YFV NC_002031 1 BgV KU308380 EHV DQ859060 1 DENV_3 NC_001475 1 ZIKV NC_012532 1 KOKV NC_009029 0.94 1 WNV NC_009942 1 1 JEV NC_001437 MVEV NC_000943 1 NOUV EU159426 Lineage II ISF 1 1 NHUV NC_024017 BJV KC496020 1 LAMV NC_024806 1 CHAOV NC_017086 1 DONV NC_016997 ILOV NC_024805 0.5 Figure 2. Bayesian phylogenies of flaviviruses over the whole open reading frame nucleotide sequence. The tree was constructed in Geneious using
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