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      Viral metagenomics reveals the presence of highly divergent quaranjavirus in Rhipicephalus ticks from Mozambique

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          ABSTRACT

          Background: Ticks are primary vectors for many well-known disease-causing agents that affect human and animal populations globally such as tick-borne encephalitis, Crimean-Congo hemorrhagic fever and African swine fever. In this study, viral metagenomics was used to identify what viruses are present in Rhipicephalus spp. ticks collected in the Zambezi Valley of Mozambique.

          Methods: The RNA was amplified with sequence-independent single primer amplification (SISPA) and high-throughput sequencing was performed on the Ion Torrent platform. The generated sequences were subjected to quality check and classfied by BLAST. CodonCode aligner and SeqMan were used to assemble the sequences.

          Results: The majority of viral sequences showed closest sequence identity to the Orthomyxoviridae family, although viruses similar to the Parvoviridae and Coronaviridae were also identified. Nearly complete sequences of five orthomyxoviral segments (HA, NP, PB1, PB2, and PA) were obtained and these showed an amino acid identity of 32–52% to known quaranjaviruses. The sequences were most closely related to the Wellfleet Bay virus, detected and isolated from common eider during a mortality event in the USA.

          Conclusions: In summary, this study has identified a highly divergent virus with in the Orthomyxoviridae family associated with Rhipicephalus ticks from Mozambique. Further genetic and biological studies are needed in order to investigate potential pathogenesis of the identified orthomyxovirus.

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          Most cited references21

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          Pathogen-mediated manipulation of arthropod microbiota to promote infection.

          Arthropods transmit diverse infectious agents; however, the ways microbes influence their vector to enhance colonization are poorly understood. Ixodes scapularis ticks harbor numerous human pathogens, including Anaplasma phagocytophilum, the agent of human granulocytic anaplasmosis. We now demonstrate that A. phagocytophilum modifies the I. scapularis microbiota to more efficiently infect the tick. A. phagocytophilum induces ticks to express Ixodes scapularis antifreeze glycoprotein (iafgp), which encodes a protein with several properties, including the ability to alter bacterial biofilm formation. IAFGP thereby perturbs the tick gut microbiota, which influences the integrity of the peritrophic matrix and gut barrier-critical obstacles for Anaplasma colonization. Mechanistically, IAFGP binds the terminal d-alanine residue of the pentapeptide chain of bacterial peptidoglycan, resulting in altered permeability and the capacity of bacteria to form biofilms. These data elucidate the molecular mechanisms by which a human pathogen appropriates an arthropod antibacterial protein to alter the gut microbiota and more effectively colonize the vector.
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            Secreted Vago restricts West Nile virus infection in Culex mosquito cells by activating the Jak-STAT pathway.

            Although West Nile virus (WNV) and other arthropod-borne viruses are a major public health problem, the mechanisms of antiviral immunity in mosquitoes are poorly understood. Dicer-2, responsible for the RNAi-mediated response through the C-terminal RNase-III domain, also contains an N-terminal DExD/H-box helicase domain similar to mammalian RIG-I/MDA5 which, in Drosophila, was found to be required for activation of an antiviral gene, Vago. Here we show that the Culex orthologue of Vago (CxVago) is up-regulated in response to WNV infection in a Dicer-2-dependent manner. Further, our data show that CxVago is a secreted peptide that restricts WNV infection by activation of the Jak-STAT pathway. Thus, Vago appears to function as an IFN-like antiviral cytokine in mosquitoes.
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              Virome analysis of Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis ticks reveals novel highly divergent vertebrate and invertebrate viruses.

              A wide range of bacterial pathogens have been identified in ticks, yet the diversity of viruses in ticks is largely unexplored. In the United States, Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis are among the principal tick species associated with pathogen transmission. We used high-throughput sequencing to characterize the viromes of these tick species and identified the presence of Powassan virus and eight novel viruses. These included the most divergent nairovirus described to date, two new clades of tick-borne phleboviruses, a mononegavirus, and viruses with similarity to plant and insect viruses. Our analysis revealed that ticks are reservoirs for a wide range of viruses and suggests that discovery and characterization of tick-borne viruses will have implications for viral taxonomy and may provide insight into tick-transmitted diseases. Ticks are implicated as vectors of a wide array of human and animal pathogens. To better understand the extent of tick-borne diseases, it is crucial to uncover the full range of microbial agents associated with ticks. Our current knowledge of the diversity of tick-associated viruses is limited, in part due to the lack of investigation of tick viromes. In this study, we examined the viromes of three tick species from the United States. We found that ticks are hosts to highly divergent viruses across several taxa, including ones previously associated with human disease. Our data underscore the diversity of tick-associated viruses and provide the foundation for further studies into viral etiology of tick-borne diseases. Copyright © 2014, American Society for Microbiology. All Rights Reserved.
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                Author and article information

                Journal
                Infect Ecol Epidemiol
                Infect Ecol Epidemiol
                ZIEE
                ziee20
                Infection Ecology & Epidemiology
                Taylor & Francis
                2000-8686
                2018
                28 May 2018
                : 8
                : 1
                : 1478585
                Affiliations
                [a ] Section of Virology, Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences (SLU) , Uppsala, Sweden
                [b ] SLU Global Bioinformatics Centre, Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences , Uppsala, Sweden
                [c ] Division of Molecular Diagnostics and Epidemiology, Biotechnology Center, Eduardo Mondlane University , Maputo, Mozambique
                [d ] Department of Microbiology, Tumor and Cell Biology (MTC), Karolinska Institute , Stockholm, Sweden
                Author notes
                CONTACT Harindranath Cholleti harindranath.cholleti@ 123456slu.se Section of Virology, Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences (SLU) , PO Box 7028 SE-750 07, Uppsala, Sweden
                Author information
                http://orcid.org/0000-0003-4899-9637
                Article
                1478585
                10.1080/20008686.2018.1478585
                5974704
                29868166
                a07fb535-9844-452a-94b5-92d162c76128
                © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 19 February 2018
                : 14 May 2018
                Page count
                Figures: 3, Tables: 3, References: 35, Pages: 1
                Funding
                Funded by: Svenska Forskningsrådet Formas 10.13039/501100001862
                Award ID: 2012-586
                Funded by: Vetenskapsrådet 10.13039/501100004359
                Award ID: 2012-138
                This study was funded by Svenska Forskingrådet Formas (2012-586) and Vetenskaprådet (2012-138).
                Categories
                Research Article

                Infectious disease & Microbiology
                ticks,arthropods,rhipicephalus,quaranjavirus,viral metagenomics,mozambique

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