Global Organization and Proposed Megataxonomy of the Virus World

Viruses and mobile genetic elements are molecular parasites or symbionts that coevolve with nearly all forms of cellular life. The route of virus replication and protein expression is determined by the viral genome type. Comparison of these routes led to the classification of viruses into seven &quo...

Celý popis

Uložené v:
Podrobná bibliografia
Vydané v:Microbiology and molecular biology reviews Ročník 84; číslo 2
Hlavní autori: Koonin, Eugene V, Dolja, Valerian V, Krupovic, Mart, Varsani, Arvind, Wolf, Yuri I, Yutin, Natalya, Zerbini, F Murilo, Kuhn, Jens H
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States 20.05.2020
Predmet:
DNA Replication
DNA Viruses - genetics
Evolution, Molecular
Genes, Viral
Genome, Viral
Phylogeny
RNA Viruses - genetics
Virus Physiological Phenomena
Viruses - classification
virosphere
megataxonomy
virus nomenclature
phylogeny
realm
evolution
virus classification
virus taxonomy
ICTV
phylogenomics
ISSN:1098-5557, 1098-5557
On-line prístup:Zistit podrobnosti o prístupe
Tagy: Pridať tag
Žiadne tagy, Buďte prvý, kto otaguje tento záznam!
Abstract Viruses and mobile genetic elements are molecular parasites or symbionts that coevolve with nearly all forms of cellular life. The route of virus replication and protein expression is determined by the viral genome type. Comparison of these routes led to the classification of viruses into seven "Baltimore classes" (BCs) that define the major features of virus reproduction. However, recent phylogenomic studies identified multiple evolutionary connections among viruses within each of the BCs as well as between different classes. Due to the modular organization of virus genomes, these relationships defy simple representation as lines of descent but rather form complex networks. Phylogenetic analyses of virus hallmark genes combined with analyses of gene-sharing networks show that replication modules of five BCs (three classes of RNA viruses and two classes of reverse-transcribing viruses) evolved from a common ancestor that encoded an RNA-directed RNA polymerase or a reverse transcriptase. Bona fide viruses evolved from this ancestor on multiple, independent occasions via the recruitment of distinct cellular proteins as capsid subunits and other structural components of virions. The single-stranded DNA (ssDNA) viruses are a polyphyletic class, with different groups evolving by recombination between rolling-circle-replicating plasmids, which contributed the replication protein, and positive-sense RNA viruses, which contributed the capsid protein. The double-stranded DNA (dsDNA) viruses are distributed among several large monophyletic groups and arose via the combination of distinct structural modules with equally diverse replication modules. Phylogenomic analyses reveal the finer structure of evolutionary connections among RNA viruses and reverse-transcribing viruses, ssDNA viruses, and large subsets of dsDNA viruses. Taken together, these analyses allow us to outline the global organization of the virus world. Here, we describe the key aspects of this organization and propose a comprehensive hierarchical taxonomy of viruses.
AbstractList Viruses and mobile genetic elements are molecular parasites or symbionts that coevolve with nearly all forms of cellular life. The route of virus replication and protein expression is determined by the viral genome type. Comparison of these routes led to the classification of viruses into seven "Baltimore classes" (BCs) that define the major features of virus reproduction. However, recent phylogenomic studies identified multiple evolutionary connections among viruses within each of the BCs as well as between different classes. Due to the modular organization of virus genomes, these relationships defy simple representation as lines of descent but rather form complex networks. Phylogenetic analyses of virus hallmark genes combined with analyses of gene-sharing networks show that replication modules of five BCs (three classes of RNA viruses and two classes of reverse-transcribing viruses) evolved from a common ancestor that encoded an RNA-directed RNA polymerase or a reverse transcriptase. Bona fide viruses evolved from this ancestor on multiple, independent occasions via the recruitment of distinct cellular proteins as capsid subunits and other structural components of virions. The single-stranded DNA (ssDNA) viruses are a polyphyletic class, with different groups evolving by recombination between rolling-circle-replicating plasmids, which contributed the replication protein, and positive-sense RNA viruses, which contributed the capsid protein. The double-stranded DNA (dsDNA) viruses are distributed among several large monophyletic groups and arose via the combination of distinct structural modules with equally diverse replication modules. Phylogenomic analyses reveal the finer structure of evolutionary connections among RNA viruses and reverse-transcribing viruses, ssDNA viruses, and large subsets of dsDNA viruses. Taken together, these analyses allow us to outline the global organization of the virus world. Here, we describe the key aspects of this organization and propose a comprehensive hierarchical taxonomy of viruses.Viruses and mobile genetic elements are molecular parasites or symbionts that coevolve with nearly all forms of cellular life. The route of virus replication and protein expression is determined by the viral genome type. Comparison of these routes led to the classification of viruses into seven "Baltimore classes" (BCs) that define the major features of virus reproduction. However, recent phylogenomic studies identified multiple evolutionary connections among viruses within each of the BCs as well as between different classes. Due to the modular organization of virus genomes, these relationships defy simple representation as lines of descent but rather form complex networks. Phylogenetic analyses of virus hallmark genes combined with analyses of gene-sharing networks show that replication modules of five BCs (three classes of RNA viruses and two classes of reverse-transcribing viruses) evolved from a common ancestor that encoded an RNA-directed RNA polymerase or a reverse transcriptase. Bona fide viruses evolved from this ancestor on multiple, independent occasions via the recruitment of distinct cellular proteins as capsid subunits and other structural components of virions. The single-stranded DNA (ssDNA) viruses are a polyphyletic class, with different groups evolving by recombination between rolling-circle-replicating plasmids, which contributed the replication protein, and positive-sense RNA viruses, which contributed the capsid protein. The double-stranded DNA (dsDNA) viruses are distributed among several large monophyletic groups and arose via the combination of distinct structural modules with equally diverse replication modules. Phylogenomic analyses reveal the finer structure of evolutionary connections among RNA viruses and reverse-transcribing viruses, ssDNA viruses, and large subsets of dsDNA viruses. Taken together, these analyses allow us to outline the global organization of the virus world. Here, we describe the key aspects of this organization and propose a comprehensive hierarchical taxonomy of viruses.
Viruses and mobile genetic elements are molecular parasites or symbionts that coevolve with nearly all forms of cellular life. The route of virus replication and protein expression is determined by the viral genome type. Comparison of these routes led to the classification of viruses into seven "Baltimore classes" (BCs) that define the major features of virus reproduction. However, recent phylogenomic studies identified multiple evolutionary connections among viruses within each of the BCs as well as between different classes. Due to the modular organization of virus genomes, these relationships defy simple representation as lines of descent but rather form complex networks. Phylogenetic analyses of virus hallmark genes combined with analyses of gene-sharing networks show that replication modules of five BCs (three classes of RNA viruses and two classes of reverse-transcribing viruses) evolved from a common ancestor that encoded an RNA-directed RNA polymerase or a reverse transcriptase. Bona fide viruses evolved from this ancestor on multiple, independent occasions via the recruitment of distinct cellular proteins as capsid subunits and other structural components of virions. The single-stranded DNA (ssDNA) viruses are a polyphyletic class, with different groups evolving by recombination between rolling-circle-replicating plasmids, which contributed the replication protein, and positive-sense RNA viruses, which contributed the capsid protein. The double-stranded DNA (dsDNA) viruses are distributed among several large monophyletic groups and arose via the combination of distinct structural modules with equally diverse replication modules. Phylogenomic analyses reveal the finer structure of evolutionary connections among RNA viruses and reverse-transcribing viruses, ssDNA viruses, and large subsets of dsDNA viruses. Taken together, these analyses allow us to outline the global organization of the virus world. Here, we describe the key aspects of this organization and propose a comprehensive hierarchical taxonomy of viruses.
Author Koonin, Eugene V
Krupovic, Mart
Zerbini, F Murilo
Wolf, Yuri I
Dolja, Valerian V
Varsani, Arvind
Yutin, Natalya
Kuhn, Jens H
Author_xml – sequence: 1
  givenname: Eugene V
  orcidid: 0000-0003-3943-8299
  surname: Koonin
  fullname: Koonin, Eugene V
  email: koonin@ncbi.nlm.nih.gov, kuhnjens@mail.nih.gov
  organization: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA koonin@ncbi.nlm.nih.gov kuhnjens@mail.nih.gov
– sequence: 2
  givenname: Valerian V
  orcidid: 0000-0002-8148-4670
  surname: Dolja
  fullname: Dolja, Valerian V
  organization: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA
– sequence: 3
  givenname: Mart
  orcidid: 0000-0001-5486-0098
  surname: Krupovic
  fullname: Krupovic, Mart
  organization: Institut Pasteur, Archaeal Virology Unit, Department of Microbiology, Paris, France
– sequence: 4
  givenname: Arvind
  orcidid: 0000-0003-4111-2415
  surname: Varsani
  fullname: Varsani, Arvind
  organization: Structural Biology Research Unit, Department of Clinical Laboratory Sciences, University of Cape Town, Observatory, Cape Town, South Africa
– sequence: 5
  givenname: Yuri I
  orcidid: 0000-0002-0247-8708
  surname: Wolf
  fullname: Wolf, Yuri I
  organization: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA
– sequence: 6
  givenname: Natalya
  orcidid: 0000-0002-3633-5123
  surname: Yutin
  fullname: Yutin, Natalya
  organization: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA
– sequence: 7
  givenname: F Murilo
  orcidid: 0000-0001-8617-0200
  surname: Zerbini
  fullname: Zerbini, F Murilo
  organization: Departamento de Fitopatologia/Bioagro, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil
– sequence: 8
  givenname: Jens H
  orcidid: 0000-0002-7800-6045
  surname: Kuhn
  fullname: Kuhn, Jens H
  email: koonin@ncbi.nlm.nih.gov, kuhnjens@mail.nih.gov
  organization: Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Frederick, Maryland, USA koonin@ncbi.nlm.nih.gov kuhnjens@mail.nih.gov
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32132243$$D View this record in MEDLINE/PubMed
BookMark eNpNz0tLw0AUBeBBKvahS7cySzepc-eRZnZq0Sq0VMTHMsxkbmskydSZBKy_3oAKrs5ZfBw4YzJofIOEnAKbAvDsYrW6fpwyxlJIQB-QETCdJUqp2eBfH5JxjO-9kkrrIzIUHATnUozI5aLy1lR0HbamKb9MW_qGmsbRh-B3PqKjK9ya1nz6xtd76je0fUP6UoYu0lcfKndMDjeminjymxPyfHvzNL9LluvF_fxqmRQKdJs4CSkUXItUpcoJRLWxiMxxZ7XR0gJymMm0yLTimeHMSl5wUCiF7YlifELOf3Z3wX90GNu8LmOBVWUa9F3MuZhB1n9V0NOzX9rZGl2-C2Vtwj7_e82_Ab-ZWac
CitedBy_id crossref_primary_10_3389_fmicb_2023_1290062
ContentType Journal Article
Copyright Copyright © 2020 American Society for Microbiology.
Copyright_xml – notice: Copyright © 2020 American Society for Microbiology.
DBID CGR
CUY
CVF
ECM
EIF
NPM
7X8
DOI 10.1128/MMBR.00061-19
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic
MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: 7X8
  name: MEDLINE - Academic
  url: https://search.proquest.com/medline
  sourceTypes: Aggregation Database
DeliveryMethod no_fulltext_linktorsrc
Discipline Biology
EISSN 1098-5557
ExternalDocumentID 32132243
Genre Research Support, N.I.H., Intramural
Review
Research Support, Non-U.S. Gov't
Journal Article
Research Support, N.I.H., Extramural
GrantInformation_xml – fundername: NIAID NIH HHS
  grantid: HHSN272200700016I
GroupedDBID ---
-DZ
-~X
.55
0R~
123
18M
29M
2KS
2WC
39C
4.4
5RE
5VS
85S
AAGFI
AAIKC
AAMNW
ABPPZ
ACGFO
ACGOD
ACIWK
ACNCT
ACPRK
ADBBV
AENEX
AFRAH
AGHSJ
AGVNZ
ALMA_UNASSIGNED_HOLDINGS
AOIJS
BAWUL
BKOMP
BTFSW
CGR
CJ0
CS3
CUY
CVF
D0L
DIK
DU5
E3Z
EBS
ECM
EIF
F5P
GX1
H13
HF~
HYE
HZ~
KQ8
L7B
NPM
O9-
OMK
P2P
PQQKQ
RHI
RNS
RPM
RSF
RXW
TAE
TR2
W8F
WH7
WOQ
X7M
YNT
YQT
~02
7X8
ID FETCH-LOGICAL-c519t-d4161c2936565d3ee5fbee0d2db9a94b1e21746c89528a20b42c215e43b2db502
IEDL.DBID 7X8
ISICitedReferencesCount 407
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000540853300001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 1098-5557
IngestDate Fri Sep 05 08:56:07 EDT 2025
Mon Jul 21 05:14:13 EDT 2025
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 2
Keywords virosphere
megataxonomy
virus nomenclature
phylogeny
realm
evolution
virus classification
virus taxonomy
ICTV
phylogenomics
Language English
License Copyright © 2020 American Society for Microbiology.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c519t-d4161c2936565d3ee5fbee0d2db9a94b1e21746c89528a20b42c215e43b2db502
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
ObjectType-Review-3
content type line 23
ORCID 0000-0002-3633-5123
0000-0002-8148-4670
0000-0003-3943-8299
0000-0003-4111-2415
0000-0001-5486-0098
0000-0001-8617-0200
0000-0002-0247-8708
0000-0002-7800-6045
OpenAccessLink https://mmbr.asm.org/content/mmbr/84/2/e00061-19.full.pdf
PMID 32132243
PQID 2371855551
PQPubID 23479
ParticipantIDs proquest_miscellaneous_2371855551
pubmed_primary_32132243
PublicationCentury 2000
PublicationDate 2020-05-20
PublicationDateYYYYMMDD 2020-05-20
PublicationDate_xml – month: 05
  year: 2020
  text: 2020-05-20
  day: 20
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Microbiology and molecular biology reviews
PublicationTitleAlternate Microbiol Mol Biol Rev
PublicationYear 2020
SSID ssj0004599
Score 2.7081006
SecondaryResourceType review_article
Snippet Viruses and mobile genetic elements are molecular parasites or symbionts that coevolve with nearly all forms of cellular life. The route of virus replication...
SourceID proquest
pubmed
SourceType Aggregation Database
Index Database
SubjectTerms DNA Replication
DNA Viruses - genetics
Evolution, Molecular
Genes, Viral
Genome, Viral
Phylogeny
RNA Viruses - genetics
Virus Physiological Phenomena
Viruses - classification
Title Global Organization and Proposed Megataxonomy of the Virus World
URI https://www.ncbi.nlm.nih.gov/pubmed/32132243
https://www.proquest.com/docview/2371855551
Volume 84
WOSCitedRecordID wos000540853300001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV3JTsMwELWAgsSFfSmbjMTVkHhp4xObqLikqhCg3iJvQb0kpWkR_D1jJxU9ISRyyCW2FI3HM-95mYfQRWxi-OA44ZDeCM9lhygpGIk0ZEtlEmZ1LTbR7feT4VAOmgW3qjlWOY-JIVDb0vg18ivKIIoKeOLr8TvxqlF-d7WR0FhGLQZQxnt1d7hYLTzoR8a-Zib07M5rbNLkKk3vni5DAifxL-gyZJne5n__bwttNPgS39YOsY2WXLGD1mrFya9ddFPX-MeLVzCxKiweeLWEylmcujc1VZ_hrgMucwwAEb-OJrMKh3M3e-il9_B8_0gaEQViAJxNifUMxkBSB-AmLHNO5Nq5yFKrpZJcx86Tko5JpKCJopHm1AAMcJxpaCIiuo9WirJwhwhTZnMrLZBpJ7hVQlIgcCzWFCgXg7Fuo_O5aTJwUr_zoApXzqrsxzhtdFDbNxvX1TQyRj0h5uzoD72P0Tr1fDcSMLtPUCuHKepO0ar5mI6qyVkYfXj3B-k3P_63sQ
linkProvider ProQuest
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Global+Organization+and+Proposed+Megataxonomy+of+the+Virus+World&rft.jtitle=Microbiology+and+molecular+biology+reviews&rft.au=Koonin%2C+Eugene+V&rft.au=Dolja%2C+Valerian+V&rft.au=Krupovic%2C+Mart&rft.au=Varsani%2C+Arvind&rft.date=2020-05-20&rft.eissn=1098-5557&rft.volume=84&rft.issue=2&rft_id=info:doi/10.1128%2FMMBR.00061-19&rft_id=info%3Apmid%2F32132243&rft_id=info%3Apmid%2F32132243&rft.externalDocID=32132243
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1098-5557&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1098-5557&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1098-5557&client=summon