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      Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses

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          Abstract

          Although arthropods are important viral vectors, the biodiversity of arthropod viruses, as well as the role that arthropods have played in viral origins and evolution, is unclear. Through RNA sequencing of 70 arthropod species we discovered 112 novel viruses that appear to be ancestral to much of the documented genetic diversity of negative-sense RNA viruses, a number of which are also present as endogenous genomic copies. With this greatly enriched diversity we revealed that arthropods contain viruses that fall basal to major virus groups, including the vertebrate-specific arenaviruses, filoviruses, hantaviruses, influenza viruses, lyssaviruses, and paramyxoviruses. We similarly documented a remarkable diversity of genome structures in arthropod viruses, including a putative circular form, that sheds new light on the evolution of genome organization. Hence, arthropods are a major reservoir of viral genetic diversity and have likely been central to viral evolution.

          DOI: http://dx.doi.org/10.7554/eLife.05378.001

          eLife digest

          Many illnesses, including influenza, hemorrhagic fever, and rabies, are caused by a group of viruses called negative-sense RNA viruses. The genetic information—or genome—of these viruses is encoded in strands of RNA that must be copied before they can be translated into the proteins needed to build new viruses. It is currently known that there are at least eight different families of these viruses, which have a wide range of shapes and sizes and arrange their RNA in different ways.

          Insects, spiders, and other arthropods carry many different RNA viruses. Many of these viruses have not previously been studied, and those that have been studied so far are mainly those that cause diseases in humans and other vertebrates. Researchers therefore only know a limited amount about the diversity of the negative-sense RNA viruses that arthropods harbor and how these viruses evolved. Studying how viruses evolve helps scientists to understand what makes some viruses deadly and others harmless and can also help develop treatments or vaccines for the diseases caused by the viruses.

          Li, Shi, Tian, Lin, Kang et al. collected 70 species of insects, spiders, centipedes, and other arthropods in China and sequenced all the negative-sense RNA viruses in the creatures. This revealed an enormous number of negative-sense RNA viruses, including 112 new viruses. Many of the newly discovered arthropod viruses appear to be the ancestors of disease-causing viruses, including influenza viruses and the filoviruses—the group that includes the Ebola virus. Indeed, it appears that arthropods host many—if not all—of the negative-sense RNA viruses that cause disease in vertebrates and plants.

          While documenting the new RNA viruses and how they are related to each other, Li et al. found many different genome structures. Some genomes were segmented, which may play an important role in evolution as segments can be easily swapped to create new genetic combinations. Non-segmented and circular genomes were also found. This genetic diversity suggests that arthropods are likely to have played a key role in the evolution of new viruses by acting as a site where many different viruses can interact and exchange genetic information.

          DOI: http://dx.doi.org/10.7554/eLife.05378.002

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          Most cited references25

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          Fast gapped-read alignment with Bowtie 2.

          As the rate of sequencing increases, greater throughput is demanded from read aligners. The full-text minute index is often used to make alignment very fast and memory-efficient, but the approach is ill-suited to finding longer, gapped alignments. Bowtie 2 combines the strengths of the full-text minute index with the flexibility and speed of hardware-accelerated dynamic programming algorithms to achieve a combination of high speed, sensitivity and accuracy.
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            MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

            We report a major update of the MAFFT multiple sequence alignment program. This version has several new features, including options for adding unaligned sequences into an existing alignment, adjustment of direction in nucleotide alignment, constrained alignment and parallel processing, which were implemented after the previous major update. This report shows actual examples to explain how these features work, alone and in combination. Some examples incorrectly aligned by MAFFT are also shown to clarify its limitations. We discuss how to avoid misalignments, and our ongoing efforts to overcome such limitations.
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              The SILVA ribosomal RNA gene database project: improved data processing and web-based tools

              SILVA (from Latin silva, forest, http://www.arb-silva.de) is a comprehensive web resource for up to date, quality-controlled databases of aligned ribosomal RNA (rRNA) gene sequences from the Bacteria, Archaea and Eukaryota domains and supplementary online services. The referred database release 111 (July 2012) contains 3 194 778 small subunit and 288 717 large subunit rRNA gene sequences. Since the initial description of the project, substantial new features have been introduced, including advanced quality control procedures, an improved rRNA gene aligner, online tools for probe and primer evaluation and optimized browsing, searching and downloading on the website. Furthermore, the extensively curated SILVA taxonomy and the new non-redundant SILVA datasets provide an ideal reference for high-throughput classification of data from next-generation sequencing approaches.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                2050-084X
                29 January 2015
                2015
                : 4
                : e05378
                Affiliations
                [1 ]deptState Key Laboratory for Infectious Disease Prevention and Control , National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention , Beijing, China
                [2 ]Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases , Hangzhou, China
                [3 ]deptMarie Bashir Institute for Infectious Diseases and Biosecurity , Charles Perkins Centre, School of Biological Sciences and Sydney Medical School, The University of Sydney , Sydney, Australia
                [4 ]Wuhan Center for Disease Control and Prevention , Wuhan, China
                [5 ]Wenzhou Center for Disease Control and Prevention , Wenzhou, China
                Howard Hughes Medical Institute, Columbia University , United States
                Howard Hughes Medical Institute, Columbia University , United States
                Author notes
                [* ]For correspondence: zhangyongzhen@ 123456icdc.cn
                [†]

                These authors contributed equally to this work.

                Article
                05378
                10.7554/eLife.05378
                4384744
                25633976
                890331bb-2e30-4596-8419-2dea70b2c5a2
                © 2015, Li et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 29 October 2014
                : 27 January 2015
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China (NSFC);
                Award ID: 81290343, 81273014
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100002855, Ministry of Science and Technology of the People's Republic of China;
                Award ID: 2014ZX10004001-005
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council (NHMRC);
                Award ID: AF30
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Microbiology and Infectious Disease
                Custom metadata
                2.0
                Extensive genetic diversity and novel genome structures in RNA viruses from arthropods shed important new light on the ancestry and evolutionary history of major classes of vertebrate and plant viruses.

                Life sciences
                rna virus,evolution,arthropods,segmentation,negative-sense,phylogeny,viruses
                Life sciences
                rna virus, evolution, arthropods, segmentation, negative-sense, phylogeny, viruses

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