Minimum Information about an Uncultivated Virus Genome (MIUViG)

Simon Roux¹, Evelien M Adriaenssens², Bas E Dutilh^{3

4}, Eugene V Koonin⁵, Andrew M Kropinski⁶, Mart Krupovic⁷, Jens H Kuhn⁸, Rob Lavigne⁹, J Rodney Brister⁵, Arvind Varsani^{10

11}, Clara Amid¹², Ramy K Aziz¹³, Seth R Bordenstein¹⁴, Peer Bork¹⁵, Mya Breitbart¹⁶, Guy R Cochrane¹², Rebecca A Daly¹⁷, Christelle Desnues¹⁸, Melissa B Duhaime¹⁹, Joanne B Emerson²⁰, François Enault²¹, Jed A Fuhrman²², Pascal Hingamp²³, Philip Hugenholtz²⁴, Bonnie L Hurwitz^{25

26}, Natalia N Ivanova¹, Jessica M Labonté²⁷, Kyung-Bum Lee²⁸, Rex R Malmstrom¹, Manuel Martinez-Garcia²⁹, Ilene Karsch Mizrachi⁵, Hiroyuki Ogata³⁰, David Páez-Espino¹, Marie-Agnès Petit³¹, Catherine Putonti^{32

33

34}, Thomas Rattei³⁵, Alejandro Reyes³⁶, Francisco Rodriguez-Valera³⁷, Karyna Rosario¹⁶, Lynn Schriml³⁸, Frederik Schulz¹, Grieg F Steward³⁹, Matthew B Sullivan^{40

41}, Shinichi Sunagawa⁴², Curtis A Suttle^{43

44

45

46}, Ben Temperton⁴⁷, Susannah G Tringe¹, Rebecca Vega Thurber⁴⁸, Nicole S Webster^{24

49}, Katrine L Whiteson⁵⁰, Steven W Wilhelm⁵¹, K Eric Wommack⁵², Tanja Woyke¹, Kelly C Wrighton¹⁷, Pelin Yilmaz⁵³, Takashi Yoshida⁵⁴, Mark J Young⁵⁵, Natalya Yutin⁵, Lisa Zeigler Allen^{56

57}, Nikos C Kyrpides¹, Emiley A Eloe-Fadrosh¹

Affiliations

¹ US Department of Energy Joint Genome Institute, Walnut Creek, California, USA.
² Institute of Integrative Biology, University of Liverpool, Liverpool, UK.
³ Theoretical Biology and Bioinformatics, Utrecht University, Utrecht, the Netherlands.
⁴ Centre for Molecular and Biomolecular Informatics, Radboud University Medical Centre, Nijmegen, the Netherlands.
⁵ National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA.
⁶ Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada.
⁷ Institut Pasteur, Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Paris, France.
⁸ Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort Detrick, Frederick, Maryland, USA.
⁹ KU Leuven, Laboratory of Gene Technology, Heverlee, Belgium.
¹⁰ Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, Arizona, USA.
¹¹ Structural Biology Research Unit, Department of Integrative Biomedical Sciences, University of Cape Town, Observatory, Cape Town, South Africa.
¹² European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Wellcome Genome Campus, Hinxton, UK.
¹³ Department of Microbiology and Immunology, Faculty of Pharmacy, Cairo University, Cairo, Egypt.
¹⁴ Departments of Biological Sciences and Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt Genetics Institute, Vanderbilt University, Nashville, Tennessee, USA.
¹⁵ European Molecular Biology Laboratory, Heidelberg, Germany.
¹⁶ College of Marine Science, University of South Florida, Saint Petersburg, Florida, USA.
¹⁷ Soil and Crop Sciences Department, Colorado State University, Fort Collins, Colorado, USA.
¹⁸ Aix-Marseille Université, CNRS, MEPHI, IHU Méditerranée Infection, Marseille, France.
¹⁹ Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA.
²⁰ University of California, Davis, Department of Plant Pathology, Davis, California, USA.
²¹ LMGE,UMR 6023 CNRS, Université Clermont Auvergne, Aubiére, France.
²² University of Southern California, Los Angeles, Los Angeles, California, USA.
²³ Aix Marseille Université, Université de Toulon, CNRS, IRD, MIO UM 110, Marseille, France.
²⁴ Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St. Lucia, Queensland, Australia.
²⁵ Department of Agricultural and Biosystems Engineering, University of Arizona, Tucson, Arizona, USA.
²⁶ BIO5 Research Institute, University of Arizona, Tucson, Arizona, USA.
²⁷ Department of Marine Biology, Texas A&M University at Galveston, Galveston, Texas, USA.
²⁸ DDBJ Center, National Institute of Genetics, Mishima, Shizuoka, Japan.
²⁹ Department of Physiology, Genetics and Microbiology, University of Alicante, Alicante, Spain.
³⁰ Institute for Chemical Research, Kyoto University, Uji, Japan.
³¹ Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France.
³² Department of Biology, Loyola University Chicago, Chicago, Illinois, USA.
³³ Bioinformatics Program, Loyola University Chicago, Chicago, Illinois, USA.
³⁴ Department of Computer Science, Loyola University Chicago, Chicago, Illinois, USA.
³⁵ Division of Computational Systems Biology, Department of Microbiology and Ecosystem Science, Research Network "Chemistry Meets Microbiology," University of Vienna, Vienna, Austria.
³⁶ Max Planck Tandem Group in Computational Biology, Department of Biological Sciences, Universidad de los Andes, Bogotá, Colombia.
³⁷ Evolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel Hernández, Alicante, Spain.
³⁸ University of Maryland School of Medicine, Baltimore, Maryland, USA.
³⁹ Center for Microbial Oceanography: Research and Education, Department of Oceanography, University of Hawai'i at Manoa, Honolulu, Hawai'i, USA.
⁴⁰ Department of Microbiology, The Ohio State University, Columbus, Ohio, USA.
⁴¹ Department of Civil, Environmental and Geodetic Engineering, The Ohio State University, Columbus, Ohio, USA.
⁴² ETH Zurich, Department of Biology, Zurich, Switzerland.
⁴³ Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, British Columbia, Canada.
⁴⁴ Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada.
⁴⁵ Department of Microbiology and Immunology, University of British Columbia, Vancouver, British Columbia, Canada.
⁴⁶ Institute of Oceans and Fisheries, University of British Columbia, Vancouver, British Columbia, Canada.
⁴⁷ School of Biosciences, University of Exeter, Exeter, UK.
⁴⁸ Department of Microbiology, Oregon State University, Oregon, USA.
⁴⁹ Australian Institute of Marine Science, Townsville, Queensland, Australia.
⁵⁰ Department of Molecular Biology and Biochemistry, University of California, Irvine, California, USA.
⁵¹ Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA.
⁵² University of Delaware, Delaware Biotechnology Institute, Newark, Delaware, USA.
⁵³ Microbial Physiology Group, Max Planck Institute for Marine Microbiology, Bremen, Germany.
⁵⁴ Graduate School of Agriculture, Kyoto University, Kitashirakawa-Oiwake, Kyoto, Japan.
⁵⁵ Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, Montana, USA.
⁵⁶ J Craig Venter Institute, La Jolla, California, USA.
⁵⁷ Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California, USA.

PMID: 30556814
PMCID: PMC6871006
DOI: 10.1038/nbt.4306

Minimum Information about an Uncultivated Virus Genome (MIUViG)

Simon Roux et al. Nat Biotechnol. 2019 Jan.

. 2019 Jan;37(1):29-37.

doi: 10.1038/nbt.4306. Epub 2018 Dec 17.

Authors

Affiliations

¹ US Department of Energy Joint Genome Institute, Walnut Creek, California, USA.
² Institute of Integrative Biology, University of Liverpool, Liverpool, UK.
³ Theoretical Biology and Bioinformatics, Utrecht University, Utrecht, the Netherlands.
⁴ Centre for Molecular and Biomolecular Informatics, Radboud University Medical Centre, Nijmegen, the Netherlands.
⁵ National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA.
⁶ Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada.
⁷ Institut Pasteur, Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Paris, France.
⁸ Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort Detrick, Frederick, Maryland, USA.
⁹ KU Leuven, Laboratory of Gene Technology, Heverlee, Belgium.
¹⁰ Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, Arizona, USA.
¹¹ Structural Biology Research Unit, Department of Integrative Biomedical Sciences, University of Cape Town, Observatory, Cape Town, South Africa.
¹² European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Wellcome Genome Campus, Hinxton, UK.
¹³ Department of Microbiology and Immunology, Faculty of Pharmacy, Cairo University, Cairo, Egypt.
¹⁴ Departments of Biological Sciences and Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt Genetics Institute, Vanderbilt University, Nashville, Tennessee, USA.
¹⁵ European Molecular Biology Laboratory, Heidelberg, Germany.
¹⁶ College of Marine Science, University of South Florida, Saint Petersburg, Florida, USA.
¹⁷ Soil and Crop Sciences Department, Colorado State University, Fort Collins, Colorado, USA.
¹⁸ Aix-Marseille Université, CNRS, MEPHI, IHU Méditerranée Infection, Marseille, France.
¹⁹ Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA.
²⁰ University of California, Davis, Department of Plant Pathology, Davis, California, USA.
²¹ LMGE,UMR 6023 CNRS, Université Clermont Auvergne, Aubiére, France.
²² University of Southern California, Los Angeles, Los Angeles, California, USA.
²³ Aix Marseille Université, Université de Toulon, CNRS, IRD, MIO UM 110, Marseille, France.
²⁴ Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St. Lucia, Queensland, Australia.
²⁵ Department of Agricultural and Biosystems Engineering, University of Arizona, Tucson, Arizona, USA.
²⁶ BIO5 Research Institute, University of Arizona, Tucson, Arizona, USA.
²⁷ Department of Marine Biology, Texas A&M University at Galveston, Galveston, Texas, USA.
²⁸ DDBJ Center, National Institute of Genetics, Mishima, Shizuoka, Japan.
²⁹ Department of Physiology, Genetics and Microbiology, University of Alicante, Alicante, Spain.
³⁰ Institute for Chemical Research, Kyoto University, Uji, Japan.
³¹ Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France.
³² Department of Biology, Loyola University Chicago, Chicago, Illinois, USA.
³³ Bioinformatics Program, Loyola University Chicago, Chicago, Illinois, USA.
³⁴ Department of Computer Science, Loyola University Chicago, Chicago, Illinois, USA.
³⁵ Division of Computational Systems Biology, Department of Microbiology and Ecosystem Science, Research Network "Chemistry Meets Microbiology," University of Vienna, Vienna, Austria.
³⁶ Max Planck Tandem Group in Computational Biology, Department of Biological Sciences, Universidad de los Andes, Bogotá, Colombia.
³⁷ Evolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel Hernández, Alicante, Spain.
³⁸ University of Maryland School of Medicine, Baltimore, Maryland, USA.
³⁹ Center for Microbial Oceanography: Research and Education, Department of Oceanography, University of Hawai'i at Manoa, Honolulu, Hawai'i, USA.
⁴⁰ Department of Microbiology, The Ohio State University, Columbus, Ohio, USA.
⁴¹ Department of Civil, Environmental and Geodetic Engineering, The Ohio State University, Columbus, Ohio, USA.
⁴² ETH Zurich, Department of Biology, Zurich, Switzerland.
⁴³ Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, British Columbia, Canada.
⁴⁴ Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada.
⁴⁵ Department of Microbiology and Immunology, University of British Columbia, Vancouver, British Columbia, Canada.
⁴⁶ Institute of Oceans and Fisheries, University of British Columbia, Vancouver, British Columbia, Canada.
⁴⁷ School of Biosciences, University of Exeter, Exeter, UK.
⁴⁸ Department of Microbiology, Oregon State University, Oregon, USA.
⁴⁹ Australian Institute of Marine Science, Townsville, Queensland, Australia.
⁵⁰ Department of Molecular Biology and Biochemistry, University of California, Irvine, California, USA.
⁵¹ Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA.
⁵² University of Delaware, Delaware Biotechnology Institute, Newark, Delaware, USA.
⁵³ Microbial Physiology Group, Max Planck Institute for Marine Microbiology, Bremen, Germany.
⁵⁴ Graduate School of Agriculture, Kyoto University, Kitashirakawa-Oiwake, Kyoto, Japan.
⁵⁵ Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, Montana, USA.
⁵⁶ J Craig Venter Institute, La Jolla, California, USA.
⁵⁷ Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California, USA.

PMID: 30556814
PMCID: PMC6871006
DOI: 10.1038/nbt.4306

Abstract

We present an extension of the Minimum Information about any (x) Sequence (MIxS) standard for reporting sequences of uncultivated virus genomes. Minimum Information about an Uncultivated Virus Genome (MIUViG) standards were developed within the Genomic Standards Consortium framework and include virus origin, genome quality, genome annotation, taxonomic classification, biogeographic distribution and in silico host prediction. Community-wide adoption of MIUViG standards, which complement the Minimum Information about a Single Amplified Genome (MISAG) and Metagenome-Assembled Genome (MIMAG) standards for uncultivated bacteria and archaea, will improve the reporting of uncultivated virus genomes in public databases. In turn, this should enable more robust comparative studies and a systematic exploration of the global virosphere.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures

**Figure 1. Size of virus genome databases over time^,,,,,,,,,,.**
Genome sequences from isolates (blue and green) or from UViGs (yellow) are shown. For genomes from isolates, the total number of genomes (blue) and the number of 'reference' genomes (green) are shown. Data were downloaded using the queries “Viruses[Organism] AND srcdb_refseq[PROP] NOT wgs[PROP] NOT cellular organisms[ORGN] NOT AC_000001:AC_999999[PACC]” for reference genomes and “Viruses[Organism] NOT cellular organisms[ORGN] NOT wgs[PROP] NOT AC_000001:AC_999999[pacc] NOT gbdiv syn[prop] AND nuccore genome samespecies[Filter]” for total number of virus genomes, on the NCBI nucleotide database portal (https://www.ncbi.nlm.nih.gov/nuccore) in January 2018. Genomes from the influenza virus database (https://www.ncbi.nlm.nih.gov/genomes/FLU/Database/nph-select.cgi?go=genomeset) were also added to the total number of virus genomes. UViGs can be assembled from metagenomes, from proviruses identified in microbial genomes, or from single-virus genomes, and estimated total UViG numbers were obtained by compiling data from the literature and from the total number of sequences in the IMG/VR database in January 2017, January 2018 and July 2018 (https://img.jgi.doe.gov/vr/). UpViG, uncultivated provirus.

**Figure 2. Identification of UViGs.**
Schematic of methods used to obtain UViGs. Steps that have been adapted from those used to assemble MAGs and SAGs or added for UViG are shown for sample preparation (orange) and bioinformatics analysis (blue). Steps specifically required for virus targeting and identification are highlighted in bold. *For viruses with short genomes, long-read technologies can provide complete genomes from shotgun sequencing in a single read, bypassing the assembly step. **Targeted sequence capture can be used to recover viral genomes from a known virus group. These genomes can be recovered from samples in which they represent a small fraction of the templates (for example, clinical samples).

**Figure 3. UViG classification and associated sequence analyses.**
“Functional potential” is functional annotation used in gene content analysis. “Host prediction” is the application of different *in silico* host prediction tools. “Taxonomic classification” is classification of the contig to established groups using marker genes or gene content comparison. “Diversity and distribution” includes vOTU clustering and relative abundance estimation through metagenome read mapping, at the geographical scale or across anatomical sites for host-associated datasets. “New taxonomic groups” concerns the delineation of new proposed groups (for example, families or genera) based exclusively on UViG sequences. “New reference species” refers to the proposal of a new entry in ICTV (https://talk.ictvonline.org/files/taxonomy-proposal-templates/). *Some of these approaches require a minimum contig size—for example, contigs ≥10 kb for taxonomic classification based on gene content or diversity estimation—and will not be applicable to every genome fragment.

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References

1. Breitbart M, Bonnain C, Malki K, Sawaya NA. Phage puppet masters of the marine microbial realm. Nat. Microbiol. 2018;3:754–766. - PubMed
1. Youle, M., Haynes, M. & Rohwer, F. in Viruses: Essential Agents of Life (ed. Witzany, G.) 61–81 (Springer Netherlands, 2012).
1. Brum JR, Sullivan MB. Rising to the challenge: accelerated pace of discovery transforms marine virology. Nat. Rev. Microbiol. 2015;13:147–159. - PubMed
1. Páez-Espino D, et al. Uncovering Earth's virome. Nature. 2016;536:425–430. - PubMed
1. Shi M, et al. Redefining the invertebrate RNA virosphere. Nature. 2016;540:539–543. - PubMed

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Minimum Information about an Uncultivated Virus Genome (MIUViG)

Affiliations

Minimum Information about an Uncultivated Virus Genome (MIUViG)

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources