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Guidelines for public database submission of uncultivated virus genome sequences for taxonomic classification

Nature Biotechnology volume 41, pages 898–902 (2023)Cite this article

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An Author Correction to this article was published on 22 August 2023

This article has been updated

Mining data derived from high-throughput DNA or RNA sequencing approaches, including metagenomics, has led to the discovery of a multitude of uncultivated virus genome sequences1,2,3,4,5,6,7,8,9,10,11,12. These sequences improve our knowledge about the representation of the global virosphere and fuel the expansion and refinement of virus taxonomy. Incorporation of these newly discovered viral sequences into high-quality reference databases adds a bottleneck to virology. For formal taxonomic classification, International Committee on Taxonomy of Viruses (ICTV) guidelines stipulate that genome sequences must be available from a public database. However, the correct use of nomenclature and the inclusion of standardized metadata fields are just as important as the availability of sequence data to enable the use and reuse of the data by the global research community. Here, we present standards and recommendations for the submission of virus genome sequence data to public databases for the purpose of taxonomic classification. These represent a conceptual and practical extension to the Minimum Information about an Uncultivated Virus Genome (MIUViG) standards that include guidelines for reporting the virus origin, genome quality, genome annotation, taxonomic classification, biogeographic distribution and host prediction13. Aspects of these standards have been reiterated in a recently published consensus viewpoint statement indicating that viruses inferred from metagenomic sequences require strict quality control before they can be used for taxonomic assignments14. The guidelines presented here focus on the MIUViG standards on genome quality and expand on the naming of sequences and their submission to public databases.

We note that many complete, coding-complete and incomplete virus genome sequences and genomic fragments are available in public repositories other than INSDC (for example, IMG/VR12, BV-BRC23, RAST24, iVirus25 or GISAID26), whereas other databases such as the Sequence Read Archive (SRA) and Whole Genome Shotgun (WGS) contain unassembled sequencing reads and unannotated or draft genomes, respectively (example guidance from the NCBI: https://www.ncbi.nlm.nih.gov/sra/docs/submit/ and https://www.ncbi.nlm.nih.gov/genbank/wgs/). Such repositories provide a resource for data mining of virus genome sequences if these genomes are further assembled and annotated27,28. By mandating the deposition of annotated sequences into the INSDC databases, the ICTV limits the scattering of exemplar genome sequences across databases and promotes the accessibility of the taxonomically classified exemplar viruses. Furthermore, the close links between the ICTV and INSDC through the NCBI enable better database organization and updating because taxonomy identifiers are persistent and the identifiers are updated routinely with each new ICTV taxonomy release.

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Fig. 1: Growth in ICTV-ratified species numbers since the 7th ICTV Report in 1999.
Fig. 2: GenBank example of record BK035346.

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Acknowledgements

The authors thank Anya Crane (Integrated Research Facility at Fort Detrick/National Institute of Allergy and Infectious Diseases (NIAID)/National Institutes of Health (NIH), Fort Detrick, Frederick, MD, USA) for critically editing the manuscript. The views and conclusions contained in this document are those of the authors and should not be interpreted as necessarily representing the official policies, either expressed or implied, of the US Department of Health and Human Services or of the institutions and companies affiliated with the authors, nor does mention of trade names, commercial products or organizations imply endorsement by the US Government. E.M.A. gratefully acknowledges the support of the Biotechnology and Biological Sciences Research Council (BBSRC); this research was funded by the BBSRC Institute Strategic Program Gut Microbes and Health BB/R012490/1 and its constituent projects BBS/E/F/000PR10353 and BBS/E/F/000PR10356. The work conducted by the US Department of Energy (DOE) Joint Genome Institute (S.R.) was supported by the Office of Science of the DOE under contract no. DE-AC02-05CH11231. Work by J.R.B. and I.K.M. was supported by the National Center for Biotechnology Information of the National Library of Medicine (NLM), NIH. This work was supported in part through Laulima Government Solutions, LLC, prime contract with the NIAID under contract no. HHSN272201800013C. J.H.K. performed this work as an employee of Tunnell Government Services (TGS), a subcontractor of Laulima Government Solutions, LLC, under Contract No. HHSN272201800013C. M.B.S. was supported by the US National Science Foundation Award #1759874. R.A.E. was supported by the National Institute of Diabetes and Digestive and Kidney Diseases of the NIH under award no. RC2DK116713 and by the Australian Research Council under award no. DP220102915. C.L. was supported by a Postdoctoral Mandate from KU Leuven (PDMt2/21/038) and the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy – EXC 2051 – Project-ID 390713860. E.J.L. was supported by the NIAID, NIH, under award no. U24AI162625. P.S. was supported by a Wellcome Trust Biomedical Resource grant (WT108418AIA). S.S. acknowledges support from the Mississippi Agricultural and Forestry Experiment Station (MAFES), US Department of Agriculture (USDA)–Agricultural Research Service project 58-6066-9-033, and the National Institute of Food and Agriculture, USDA, Hatch Project, under accession USDA 1021494. B.E.D. was supported by the European Research Council (ERC) Consolidator Grant 865694: DiversiPHI, the DFG under Germany’s Excellence Strategy – EXC 2051 – Project-ID 390713860, the Alexander von Humboldt Foundation in the context of an Alexander von Humboldt Professorship founded by German Federal Ministry of Education and Research, and the European Union’s Horizon 2020 research and innovation program, under Marie Skłodowska-Curie Actions Innovative Training Networks grant agreement no. 955974 (VIROINF).

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Authors and Affiliations

  1. Quadram Institute Bioscience, Norwich Research Park, Rosalind Franklin Road, Norwich, UK

    Evelien M. Adriaenssens

  2. United States Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    Simon Roux

  3. National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, USA

    J. Rodney Brister & Ilene Karsch-Mizrachi

  4. Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort Detrick, Frederick, MD, USA

    Jens H. Kuhn

  5. The Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ, USA

    Arvind Varsani

  6. Structural Biology Research Unit, Department of Clinical Laboratory Sciences, University of Cape Town, Cape Town, South Africa

    Arvind Varsani

  7. Beijing Advanced Innovation Center for Soft Matter Science and Engineering, College of Life Science and Technology, Beijing University of Chemical Technology, Beijing, China

    Tong Yigang

  8. Max Planck Tandem Group in Computational Biology, Department of Biological Sciences, Universidad de los Andes, Bogotá, Colombia

    Alejandro Reyes

  9. Centre of Microbial and Plant Genetics, Department of Microbial and Molecular Systems, KU Leuven, Leuven, Belgium

    Cédric Lood

  10. Laboratory of Gene Technology, Department of Biosystems, KU Leuven, Leuven, Belgium

    Cédric Lood

  11. Institute of Biodiversity, Faculty of Biological Sciences, Cluster of Excellence Balance of the Microverse, Friedrich Schiller University Jena, Jena, Germany

    Cédric Lood & Bas E. Dutilh

  12. Department of Microbiology, University of Alabama at Birmingham, Birmingham, AL, USA

    Elliot J. Lefkowitz

  13. Department of Microbiology, The Ohio State University, Columbus, OH, USA

    Matthew B. Sullivan

  14. Department of Civil, Environmental and Geodetic Engineering, The Ohio State University, Columbus, OH, USA

    Matthew B. Sullivan

  15. Center of Microbiome Science, The Ohio State University, Columbus, OH, USA

    Matthew B. Sullivan

  16. College of Science and Engineering, Flinders University, Bedford Park, South Australia, Australia

    Robert A. Edwards

  17. Nuffield Department of Medicine, University of Oxford, South Parks Road, Oxford, UK

    Peter Simmonds

  18. Consiglio Nazionale delle Ricerche, Istituto per la Protezione Sostenibile delle Piante, Bari, Italy

    Luisa Rubino

  19. Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS, USA

    Sead Sabanadzovic

  20. Institut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit, Paris, France

    Mart Krupovic

  21. Theoretical Biology and Bioinformatics, Department of Biology, Science for Life, Utrecht University, Utrecht, CH, the Netherlands

    Bas E. Dutilh

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  1. Evelien M. Adriaenssens
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Correspondence to Evelien M. Adriaenssens.

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Nature Biotechnology thanks Alice McHardy, Hayden Metsky and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Adriaenssens, E.M., Roux, S., Brister, J.R. et al. Guidelines for public database submission of uncultivated virus genome sequences for taxonomic classification. Nat Biotechnol 41, 898–902 (2023). https://doi.org/10.1038/s41587-023-01844-2

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