Consensus statement: Virus taxonomy in the age of metagenomics

Nature Reviews Microbiology

Volumn 15, Issue 3, 2017, Pages 161-168

  Simmonds, Peter ^a   Adams, Mike J ^b   Benk, Mária ^c   Breitbart, Mya ^d   Brister, J Rodney ^e   Carstens, Eric B ^f   Davison, Andrew J ^g   Delwart, Eric ^h,i   Gorbalenya, Alexander E ^j,k   Harrach, Balázs ^c   Hull, Roger ^b   King, Andrew M Q ^l   Koonin, Eugene V ^e   Krupovic, Mart ^m   Kuhn, Jens H ⁿ   Lefkowitz, Elliot J ^o   Nibert, Max L ^p   Orton, Richard ^g   Roossinck, Marilyn J ^q   Sabanadzovic, Sead ^r   Sullivan, Matthew B ^s   Suttle, Curtis A ^t,u   Tesh, Robert B ^v   Van Der Vlugt, René A ^w   Varsani, Arvind ^x   Zerbini, F Murilo ^y   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Hungarian Academy of Sciences ^*  (United Kingdom)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

^e NATIONAL INSTITUTES OF HEALTH   (United States)

^f QUEEN S UNIVERSITY   (Canada)

^g MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

^h BLOOD SYSTEMS RESEARCH INSTITUTE   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^k MOSCOW STATE UNIVERSITY   (Russian Federation)

^l INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^m INSTITUT PASTEUR   (France)

ⁿ NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^o University of Alabama at Birmingham   (United States)

^p HARVARD MEDICAL SCHOOL   (United States)

^q PENNSYLVANIA STATE UNIVERSITY   (United States)

^r MISSISSIPPI STATE UNIVERSITY   (United States)

^s OHIO STATE UNIVERSITY   (United States)

^t UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^u CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

^v University of Texas Medical Branch School of Medicine   (United States)

^w WAGENINGEN UNIVERSITY   (Netherlands)

^x ARIZONA STATE UNIVERSITY   (United States)

^y FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; DNA VIRUS; GENETIC VARIABILITY; METAGENOMICS; NEW SPECIES; NOMENCLATURE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUALITY CONTROL; SEQUENCE ANALYSIS; TAXONOMY; VIRUS CLASSIFICATION; CLASSIFICATION; CONSENSUS DEVELOPMENT; GENETICS; HIGH THROUGHPUT SEQUENCING; NUCLEOTIDE SEQUENCE; VIRUS;

BASE SEQUENCE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; METAGENOMICS; VIRUSES;

EID: 85008394347     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro.2016.177     Document Type: Article

References (71)

1. Edwards, R. A. & Rohwer, F. Viral metagenomics. Nat. Rev. Microbiol. 3, 504-510 (2005).
2. Mokili, J. L., Rohwer, F. & Dutilh, B. E. Metagenomics and future perspectives in virus discovery. Curr. Opin. Virol. 2, 63-77 (2012).
3. Rosario, K. & Breitbart, M. Exploring the viral world through metagenomics. Curr. Opin. Virol. 1, 289-297 (2011).
4. Chow, C. E. & Suttle, C. A. Biogeography of viruses in the sea. Annu. Rev. Virol. 2, 41-66 (2015).
5. Wigington, C. H. et al. Re?e xamination of the relationship between marine virus and microbial cell abundances. Nat. Microbiol. 1, 15024 (2016).
6. Suttle, C. A. Viruses: unlocking the greatest biodiversity on Earth. Genome 56, 542-544 (2013).
7. Roossinck, M. J. Move over, bacteria! Viruses make their mark as mutualistic microbial symbionts. J. Virol. 89, 6532-6535 (2015).
8. Steward, G. F. et al. Are we missing half of the viruses in the ocean? ISME J. 7, 672-679 (2013).
9. Simmonds, P. Methods for virus classification and the challenge of incorporating metagenomic sequence data. J. Gen. Virol. 96, 1193-1206 (2015).
10. Krupovic, M., Ghabrial, S. A., Jiang, D. & Varsani, A. Genomoviridae: a new family of widespread singlestranded DNA viruses. Arch. Virol. 161, 2633-2643 (2016).
11. Labonte, J. M. & Suttle, C. A. Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J. 7, 2169-2177 (2013).
12. Dayaram, A. et al. Diverse small circular DNA viruses circulating amongst estuarine molluscs. Infect. Genet. Evol. 31, 284-295 (2015).
13. Dayaram, A. et al. Diverse circular replicationassociated protein encoding viruses circulating in invertebrates within a lake ecosystem. Infect. Genet. Evol. 39, 304-316 (2016).
14. Rosario, K., Schenck, R. O., Harbeitner, R. C., Lawler, S. N. & Breitbart, M. Novel circular singlestranded DNA viruses identified in marine invertebrates reveal high sequence diversity and consistent predicted intrinsic disorder patterns within putative structural proteins. Front. Microbiol. 6, 696 (2015).
15. Yutin, N., Shevchenko, S., Kapitonov, V., Krupovic, M. & Koonin, E. V. A novel group of diverse Polinton-like viruses discovered by metagenome analysis. BMC Biol. 13, 95 (2015).
16. Zhou, J. et al. Diversity of virophages in metagenomic data sets. J. Virol. 87, 4225-4236 (2013).
17. Dutilh, B. E. et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat. Commun. 5, 4498 (2014).
18. Yutin, N., Kapitonov, V. V. & Koonin, E. V. A new family of hybrid virophages from an animal gut metagenome. Biol. Direct 10, 19 (2015).
19. Zhang, W. et al. Four novel algal virus genomes discovered from Yellowstone Lake metagenomes. Sci. Rep. 5, 15131 (2015).
20. Yau, S. et al. Virophage control of antarctic algal host-virus dynamics. Proc. Natl Acad. Sci. USA 108, 6163-6168 (2011).
21. Brum, J. R. et al. Ocean plankton. Patterns and ecological drivers of ocean viral communities. Science 348, 1261498 (2015).
22. Angly, F. E. et al. The marine viromes of four oceanic regions. PLoS Biol. 4, e368 (2006).
23. Breitbart, M. et al. Diversity and population structure of a near-shore marine-sediment viral community. Proc. Biol. Sci. 271, 565-574 (2004).
24. Paez-Espino, D. et al. Uncovering Earth's virome. Nature 536, 425-430 (2016).
25. Culley, A. I. et al. The characterization of RNA viruses in tropical seawater using targeted PCR and metagenomics. mBio 5, e0121014 (2014).
26. Kraberger, S. et al. Characterisation of a diverse range of circular replication-associated protein encoding DNA viruses recovered from a sewage treatment oxidation pond. Infect. Genet. Evol. 31, 73-86 (2015).
27. Roossinck, M. J. Plants, viruses and the environment: ecology and mutualism. Virology 479-480, 271-277 (2015).
28. Labonte, J. M., Hallam, S. J. & Suttle, C. A. Previously unknown evolutionary groups dominate the ssDNA gokushoviruses in oxic and anoxic waters of a coastal marine environment. Front. Microbiol. 6, 315 (2015).
29. Szekely, A. J. & Breitbart, M. Single-stranded DNA phages: from early molecular biology tools to recent revolutions in environmental microbiology. FEMS Microbiol. Lett. 363, fnw027 (2016).
30. Hopkins, M. et al. Diversity of environmental singlestranded DNA phages revealed by PCR amplification of the partial major capsid protein. ISME J. 8, 2093-2103 (2014).
31. Roux, S., Krupovic, M., Poulet, A., Debroas, D. & Enault, F. Evolution and diversity of the Microviridae viral family through a collection of 81 new complete genomes assembled from virome reads. PLoS ONE 7, e40418 (2012).
32. Rosario, K., Duffy, S. & Breitbart, M. A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch. Virol. 157, 1851-1871 (2012).
33. Roossinck, M. J. Plant virus metagenomics: biodiversity and ecology. Annu. Rev. Genet. 46, 359-369 (2012).
34. Li, C. X. et al. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 4, e05378 (2015).
35. Shi, M. et al. Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J. Virol. 90, 659-669 (2015).
36. Zablocki, O. et al. High-level diversity of tailed phages, eukaryote-associated viruses, and virophage-like elements in the metaviromes of antarctic soils. Appl. Environ. Microbiol. 80, 6888-6897 (2014).
37. Roux, S., Hallam, S. J., Woyke, T. & Sullivan, M. B. Viral dark matter and virus-host interactions resolved from publicly available microbial genomes. eLife 4, e08490 (2015).
38. Bolduc, B., Youens-Clark, K., Roux, S., Hurwitz, B. L. & Sullivan, M. B. iVirus: facilitating new insights in viral ecology with software and community data sets imbedded in a cyberinfrastructure. ISME J. http:// dx.doi.org/10.1038/ismej.2016.89 (2016).
39. Koonin, E. V., Senkevich, T. G. & Dolja, V. V. The ancient Virus World and evolution of cells. Biol. Direct 1, 29 (2006).
40. Holmes, E. C. What does virus evolution tell us about virus origins? J. Virol. 85, 5247-5251 (2011).
41. Koonin, E. V. & Dolja, V. V. A virocentric perspective on the evolution of life. Curr. Opin. Virol. 3, 546-557 (2013).
42. Rohwer, F. & Edwards, R. The Phage Proteomic Tree: a genome-based taxonomy for phage. J. Bacteriol. 184, 4529-4535 (2002).
43. Woese, C. R. Bacterial evolution. Microbiol. Rev. 51, 221-271 (1987).
44. O'Malley, M. A. & Koonin, E. V. How stands the Tree of Life a century and a half after The Origin? Biol. Direct 6, 32 (2011).
45. Pace, N. R., Sapp, J. & Goldenfeld, N. Phylogeny and beyond: scientific, historical, and conceptual significance of the first tree of life. Proc. Natl Acad. Sci. USA 109, 1011-1018 (2012).
46. Adams, M. J. et al. Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2016). Arch. Virol. 161, 2921-2949 (2016).
47. King, A. M. Q., Adams, M. J., Carstens, E. B. & Lefkowitz, E. J. (eds) Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses (Elsevier, 2011).
48. Colson, P. et al. Megavirales, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses. Arch. Virol. 158, 2517-2521 (2013).
49. Van Regenmortel, M. H. V. Classes, taxa and categories in hierarchical virus classification: a review of current debates on definitions and names of virus species. Bionomina 10, 1-21 (2016).
50. Cai, Y. et al. Nonhuman transferrin receptor 1 is an efficient cell entry receptor for Ocozocoautla de Espinosa virus. J. Virol. 87, 13930-13935 (2013).
51. Kapoor, A., Simmonds, P., Lipkin, W. I., Zaidi, S. & Delwart, E. Use of nucleotide composition analysis to infer hosts for three novel picorna-like viruses. J. Virol. 84, 10322-10328 (2010).
52. Choo, Q. L. et al. Isolation of a cDNA clone derived from a blood-borne non?A, non?B viral hepatitis genome. Science 244, 359-362 (1989).
53. Kuo, G. et al. An assay for circulating antibodies to a major etiologic virus of human non?A, non?B hepatitis. Science 244, 362-364 (1989).
54. Acevedo, A. & Andino, R. Library preparation for highly accurate population sequencing of RNA viruses. Nat. Protoc. 9, 1760-1769 (2014).
55. Hurwitz, B. L. & Sullivan, M. B. The Pacific Ocean virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS ONE 8, e57355 (2013).
56. Lima-Mendez, G., Van Helden, J., Toussaint, A. & Leplae, R. Reticulate representation of evolutionary and functional relationships between phage genomes. Mol. Biol. Evol. 25, 762-777 (2008).
57. Lauber, C. & Gorbalenya, A. E. Partitioning the genetic diversity of a virus family: approach and evaluation through a case study of picornaviruses. J. Virol. 86, 3890-3904 (2012).
58. Hatfull, G. F. & Hendrix, R. W. Bacteriophages and their genomes. Curr. Opin. Virol. 1, 298-303 (2011).
59. Koonin, E. V., Wolf, Y. I., Nagasaki, K. & Dolja, V. V. The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat. Rev. Microbiol. 6, 925-939 (2008).
60. Li, L. et al. Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J. Virol. 84, 1674-1682 (2010).
61. Steel, O. et al. Circular replication-associated protein encoding DNA viruses identified in the faecal matter of various animals in New Zealand. Infect. Genet. Evol. 43, 151-164 (2016).
62. Parker, C. T., Tindall, B. J. & Garrity, G. M. International Code of Nomenclature of Prokaryotes. Int. J. Syst. Evol. Microbiol. http://dx.doi. org/10.1099/ijsem.0.000778 (2015).
63. Konstantinidis, K. T. & Rossello-Mora, R. Classifying the uncultivated microbial majority: a place for metagenomic data in the Candidatus proposal. Syst. Appl. Microbiol. 38, 223-230 (2015).
64. Hedlund, B. P., Dodsworth, J. A. & Staley, J. T. The changing landscape of microbial biodiversity exploration and its implications for systematics. Syst. Appl. Microbiol. 38, 231-236 (2015).
65. Murray, R. G. & Stackebrandt, E. Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int. J. Syst. Bacteriol. 45, 186-187 (1995).
66. Hawksworth, D. L. et al. The Amsterdam declaration on fungal nomenclature. IMA Fungus 2, 105-112 (2011).
67. Schoch, C. L. et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc. Natl Acad. Sci. USA 109, 6241-6246 (2012).
68. Hibbett, D. S. & Taylor, J. W. Fungal systematics: is a new age of enlightenment at hand? Nat. Rev. Microbiol. 11, 129-133 (2013).
69. Roux, S. et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689-693 (2016).
70. Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066 (2002).
71. Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).