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      Metagenomic sequencing reveals viral abundance and diversity in mosquitoes from the Shaanxi-Gansu-Ningxia region, China

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          Abstract

          Background

          Mosquitoes host and transmit numerous arthropod-borne viruses (arboviruses) that cause disease in both humans and animals. Effective surveillance of virome profiles in mosquitoes is vital to the prevention and control of mosquito-borne diseases in northwestern China, where epidemics occur frequently.

          Methods

          Mosquitoes were collected in the Shaanxi-Gansu-Ningxia region (Shaanxi Province, Gansu Province, and Ningxia Hui Autonomous Region) of China from June to August 2019. Morphological methods were used for taxonomic identification of mosquito species. High-throughput sequencing and metagenomic analysis were used to characterize mosquito viromes.

          Results

          A total of 22,959 mosquitoes were collected, including Culex pipiens (45.7%), Culex tritaeniorhynchus (40.6%), Anopheles sinensis (8.4%), Aedes (5.2%), and Armigeres subalbatus (0.1%). In total, 3,014,183 (0.95% of clean reads) viral sequences were identified and assigned to 116 viral species (including pathogens such as Japanese encephalitis virus and Getah virus) in 31 viral families, including Flaviviridae, Togaviridae, Phasmaviridae, Phenuiviridae, and some unclassified viruses. Mosquitoes collected in July (86 species in 26 families) showed greater viral diversity than those from June and August. Culex pipiens (69 species in 25 families) and Culex tritaeniorhynchus (73 species in 24 families) carried more viral species than Anopheles sinensis (50 species in 19 families) or Aedes (38 species in 20 families) mosquitoes.

          Conclusion

          Viral diversity and abundance were affected by mosquito species and collection time. The present study elucidates the virome compositions of various mosquito species in northwestern China, improving the understanding of virus transmission dynamics for comparison with those of disease outbreaks.

          Author summary

          Most traditional viral research methods are limited to screening for a few types of viruses with low throughput. Here, we relied on metagenomic sequencing, which is a broadly non-specific screen for any virus, for monitoring of mosquito-borne viruses in the Shaanxi-Gansu-Ningxia region of China in 2019. The baseline of viral abundance and diversity in local Culex pipiens, Culex tritaeniorhynchus, Anopheles sinensis, and Aedes mosquitoes were investigated, with 116 viral species identified in 31 viral families, including Flaviviridae, Togaviridae, Phasmaviridae, Phenuiviridae, and some unclassified viruses. This study provides a baseline survey of the viromes of mosquitoes in the study area, highlighting the necessity of strengthened monitoring of mosquito-borne pathogens.

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          Most cited references48

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          TBtools - an integrative toolkit developed for interactive analyses of big biological data

          The rapid development of high-throughput sequencing techniques has led biology into the big-data era. Data analyses using various bioinformatics tools rely on programming and command-line environments, which are challenging and time-consuming for most wet-lab biologists. Here, we present TBtools (a Toolkit for Biologists integrating various biological data-handling tools), a stand-alone software with a user-friendly interface. The toolkit incorporates over 130 functions, which are designed to meet the increasing demand for big-data analyses, ranging from bulk sequence processing to interactive data visualization. A wide variety of graphs can be prepared in TBtools using a new plotting engine ("JIGplot") developed to maximize their interactive ability; this engine allows quick point-and-click modification of almost every graphic feature. TBtools is platform-independent software that can be run under all operating systems with Java Runtime Environment 1.6 or newer. It is freely available to non-commercial users at https://github.com/CJ-Chen/TBtools/releases.
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            Redefining the invertebrate RNA virosphere

            Current knowledge of RNA virus biodiversity is both biased and fragmentary, reflecting a focus on culturable or disease-causing agents. Here we profile the transcriptomes of over 220 invertebrate species sampled across nine animal phyla and report the discovery of 1,445 RNA viruses, including some that are sufficiently divergent to comprise new families. The identified viruses fill major gaps in the RNA virus phylogeny and reveal an evolutionary history that is characterized by both host switching and co-divergence. The invertebrate virome also reveals remarkable genomic flexibility that includes frequent recombination, lateral gene transfer among viruses and hosts, gene gain and loss, and complex genomic rearrangements. Together, these data present a view of the RNA virosphere that is more phylogenetically and genomically diverse than that depicted in current classification schemes and provide a more solid foundation for studies in virus ecology and evolution.
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              Early life dynamics of the human gut virome and bacterial microbiome in infants.

              The early years of life are important for immune development and influence health in adulthood. Although it has been established that the gut bacterial microbiome is rapidly acquired after birth, less is known about the viral microbiome (or 'virome'), consisting of bacteriophages and eukaryotic RNA and DNA viruses, during the first years of life. Here, we characterized the gut virome and bacterial microbiome in a longitudinal cohort of healthy infant twins. The virome and bacterial microbiome were more similar between co-twins than between unrelated infants. From birth to 2 years of age, the eukaryotic virome and the bacterial microbiome expanded, but this was accompanied by a contraction of and shift in the bacteriophage virome composition. The bacteriophage-bacteria relationship begins from birth with a high predator-low prey dynamic, consistent with the Lotka-Volterra prey model. Thus, in contrast to the stable microbiome observed in adults, the infant microbiome is highly dynamic and associated with early life changes in the composition of bacteria, viruses and bacteriophages with age.
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                Author and article information

                Contributors
                Role: Data curationRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: ValidationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Resources
                Role: Data curationRole: Resources
                Role: Data curationRole: Resources
                Role: Formal analysisRole: Funding acquisitionRole: MethodologyRole: ValidationRole: Writing – review & editing
                Role: SoftwareRole: Validation
                Role: Data curationRole: Resources
                Role: InvestigationRole: Resources
                Role: InvestigationRole: Resources
                Role: Resources
                Role: SoftwareRole: Validation
                Role: Writing – review & editing
                Role: Methodology
                Role: Formal analysis
                Role: InvestigationRole: Resources
                Role: Formal analysisRole: Validation
                Role: Data curationRole: Resources
                Role: Validation
                Role: ConceptualizationRole: Supervision
                Role: Funding acquisitionRole: MethodologyRole: Project administrationRole: Writing – review & editing
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                26 April 2021
                April 2021
                : 15
                : 4
                : e0009381
                Affiliations
                [1 ] NHC Key Laboratory of Medical Virology and Viral Diseases, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People’s Republic of China
                [2 ] Chinese Center for Disease Control and Prevention -Wuhan Institute of Virology, Chinese Academy of Sciences Joint Research Center for Emerging Infectious Diseases and Biosafety, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, People’s Republic of China
                [3 ] Department of Arboviruses, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, State Key Laboratory for Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, Beijing, People’s Republic of China
                [4 ] Ningxia Hui Autonomous Region Center for Disease Control and Prevention, Yinchuan, People’s Republic of China
                [5 ] Gansu Provincial Center for Disease Control and Prevention, Lanzhou, People’s Republic of China
                [6 ] Shaanxi Provincial Center for Disease Control and Prevention, Xi’an, People’s Republic of China
                Universita degli Studi di Pavia, ITALY
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0001-9292-5788
                https://orcid.org/0000-0001-8771-7044
                Article
                PNTD-D-20-01517
                10.1371/journal.pntd.0009381
                8101993
                33901182
                c97e18ee-6325-41a2-a8c5-77b88a84ff9b
                © 2021 He et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 24 August 2020
                : 13 April 2021
                Page count
                Figures: 3, Tables: 2, Pages: 13
                Funding
                Funded by: the National Natural Science Foundation of China
                Award ID: 31900156
                Award Recipient :
                Funded by: Study on etiology, pathogenic mechanism and prevention and control of epidemic Japanese encephalitis in ningxia region, Key research project of ningxia science and technology in 2019
                Award ID: 2019BCG01003
                Award Recipient :
                Funded by: National Science and Technology Major Project of China
                Award ID: 2018ZX10711001
                Award Recipient :
                Funded by: National Science and Technology Major Project of China
                Award ID: 2017ZX10104001
                Award Recipient :
                Funded by: National Science and Technology Major Project of China
                Award ID: 2018ZX10713-002
                Award Recipient :
                Funded by: the Development Grant of State Key Laboratory of Infectious Disease Prevention and Control
                Award ID: 2015SKLID505
                Award Recipient :
                This work was supported by the National Natural Science Foundation of China (31900156)(FL); Key Research Project of Ningxia Science and Technology in 2019 (2019BCG01003)(HW); National Science and Technology Major Project (2018ZX10711001)(HW, XM), (2017ZX10104001)(FL, XM) and (2018ZX10713-002)(XM), the Development Grant of State Key Laboratory of Infectious Disease Prevention and Control (2015SKLID505)(HW). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Species Interactions
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                Insect Vectors
                Mosquitoes
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                Custom metadata
                vor-update-to-uncorrected-proof
                2021-05-06
                The data that support the findings of this study have been deposited into CNGB Sequence Archive (CNSA: https://db.cngb.org/cnsa; accession number CNP0001261). Other data that support the findings of this study are available within the paper and its Supplementary Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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