100-My history of bornavirus infections hidden in vertebrate genomes
Although viruses have threatened our ancestors for millions of years, prehistoric epidemics of viruses are largely unknown. Endogenous bornavirus-like elements (EBLs) are ancient bornavirus sequences derived from the viral messenger RNAs that were reverse transcribed and inserted into animal genomes...
Saved in:
Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 118; no. 20; pp. 1 - 9 |
---|---|
Main Authors | , , , , |
Format | Journal Article |
Language | English |
Published |
United States
National Academy of Sciences
18.05.2021
|
Subjects | |
Online Access | Get full text |
Cover
Loading…
Abstract | Although viruses have threatened our ancestors for millions of years, prehistoric epidemics of viruses are largely unknown. Endogenous bornavirus-like elements (EBLs) are ancient bornavirus sequences derived from the viral messenger RNAs that were reverse transcribed and inserted into animal genomes, most likely by retrotransposons. These elements can be used as molecular fossil records to trace past bornaviral infections. In this study, we systematically identified EBLs in vertebrate genomes and revealed the history of bornavirus infections over nearly 100 My. We confirmed that ancient bornaviral infections have occurred in diverse vertebrate lineages, especially in primate ancestors. Phylogenetic analyses indicated that primate ancestors were infected with various bornaviral lineages during evolution. EBLs in primate genomes formed clades according to their integration ages, suggesting that bornavirus lineages infected with primate ancestors had changed chronologically. However, some bornaviral lineages may have coexisted with primate ancestors and underwent repeated endogenizations for tens of millions of years. Moreover, a bornaviral lineage that coexisted with primate ancestors also endogenized in the genomes of some ancestral bats. The habitats of these bat ancestors have been reported to overlap with the migration route of primate ancestors. These results suggest that long-term virus–host coexistence expanded the geographic distributions of the bornaviral lineage along with primate migration and may have spread their infections to these bat ancestors. Our findings provide insight into the history of bornavirus infections over geological timescales that cannot be deduced from research using extant viruses alone, thus broadening our perspective on virus–host coevolution. |
---|---|
AbstractList | Although viruses have threatened our ancestors for millions of years, prehistoric epidemics of viruses are largely unknown. Endogenous bornavirus-like elements (EBLs) are ancient bornavirus sequences derived from the viral messenger RNAs that were reverse transcribed and inserted into animal genomes, most likely by retrotransposons. These elements can be used as molecular fossil records to trace past bornaviral infections. In this study, we systematically identified EBLs in vertebrate genomes and revealed the history of bornavirus infections over nearly 100 My. We confirmed that ancient bornaviral infections have occurred in diverse vertebrate lineages, especially in primate ancestors. Phylogenetic analyses indicated that primate ancestors were infected with various bornaviral lineages during evolution. EBLs in primate genomes formed clades according to their integration ages, suggesting that bornavirus lineages infected with primate ancestors had changed chronologically. However, some bornaviral lineages may have coexisted with primate ancestors and underwent repeated endogenizations for tens of millions of years. Moreover, a bornaviral lineage that coexisted with primate ancestors also endogenized in the genomes of some ancestral bats. The habitats of these bat ancestors have been reported to overlap with the migration route of primate ancestors. These results suggest that long-term virus–host coexistence expanded the geographic distributions of the bornaviral lineage along with primate migration and may have spread their infections to these bat ancestors. Our findings provide insight into the history of bornavirus infections over geological timescales that cannot be deduced from research using extant viruses alone, thus broadening our perspective on virus–host coevolution. Many viral diseases have emerged in recent decades, but prehistoric viral infections remain poorly understood. In some cases, nucleotide sequences of ancient viruses, which infected ancestral animals, have been integrated into their genomes during evolution. Such “molecular fossil records” of viruses help researchers trace past viral infections. Here, we reconstructed the infection history of an RNA virus, the bornavirus, for approximately 100 My in vertebrate evolution, using molecular fossils of ancient bornaviruses. Our analyses using ancient bornaviral sequences from over 100 vertebrate species genomes indicated that bornaviruses infected a broader range of host lineages during their long-term evolution than expected from extant bornaviral host ranges. Our findings highlighted the hidden history of this RNA viral infection over geological timescales. Although viruses have threatened our ancestors for millions of years, prehistoric epidemics of viruses are largely unknown. Endogenous bornavirus-like elements (EBLs) are ancient bornavirus sequences derived from the viral messenger RNAs that were reverse transcribed and inserted into animal genomes, most likely by retrotransposons. These elements can be used as molecular fossil records to trace past bornaviral infections. In this study, we systematically identified EBLs in vertebrate genomes and revealed the history of bornavirus infections over nearly 100 My. We confirmed that ancient bornaviral infections have occurred in diverse vertebrate lineages, especially in primate ancestors. Phylogenetic analyses indicated that primate ancestors were infected with various bornaviral lineages during evolution. EBLs in primate genomes formed clades according to their integration ages, suggesting that bornavirus lineages infected with primate ancestors had changed chronologically. However, some bornaviral lineages may have coexisted with primate ancestors and underwent repeated endogenizations for tens of millions of years. Moreover, a bornaviral lineage that coexisted with primate ancestors also endogenized in the genomes of some ancestral bats. The habitats of these bat ancestors have been reported to overlap with the migration route of primate ancestors. These results suggest that long-term virus–host coexistence expanded the geographic distributions of the bornaviral lineage along with primate migration and may have spread their infections to these bat ancestors. Our findings provide insight into the history of bornavirus infections over geological timescales that cannot be deduced from research using extant viruses alone, thus broadening our perspective on virus–host coevolution. Although viruses have threatened our ancestors for millions of years, prehistoric epidemics of viruses are largely unknown. Endogenous bornavirus-like elements (EBLs) are ancient bornavirus sequences derived from the viral messenger RNAs that were reverse transcribed and inserted into animal genomes, most likely by retrotransposons. These elements can be used as molecular fossil records to trace past bornaviral infections. In this study, we systematically identified EBLs in vertebrate genomes and revealed the history of bornavirus infections over nearly 100 My. We confirmed that ancient bornaviral infections have occurred in diverse vertebrate lineages, especially in primate ancestors. Phylogenetic analyses indicated that primate ancestors were infected with various bornaviral lineages during evolution. EBLs in primate genomes formed clades according to their integration ages, suggesting that bornavirus lineages infected with primate ancestors had changed chronologically. However, some bornaviral lineages may have coexisted with primate ancestors and underwent repeated endogenizations for tens of millions of years. Moreover, a bornaviral lineage that coexisted with primate ancestors also endogenized in the genomes of some ancestral bats. The habitats of these bat ancestors have been reported to overlap with the migration route of primate ancestors. These results suggest that long-term virus-host coexistence expanded the geographic distributions of the bornaviral lineage along with primate migration and may have spread their infections to these bat ancestors. Our findings provide insight into the history of bornavirus infections over geological timescales that cannot be deduced from research using extant viruses alone, thus broadening our perspective on virus-host coevolution.Although viruses have threatened our ancestors for millions of years, prehistoric epidemics of viruses are largely unknown. Endogenous bornavirus-like elements (EBLs) are ancient bornavirus sequences derived from the viral messenger RNAs that were reverse transcribed and inserted into animal genomes, most likely by retrotransposons. These elements can be used as molecular fossil records to trace past bornaviral infections. In this study, we systematically identified EBLs in vertebrate genomes and revealed the history of bornavirus infections over nearly 100 My. We confirmed that ancient bornaviral infections have occurred in diverse vertebrate lineages, especially in primate ancestors. Phylogenetic analyses indicated that primate ancestors were infected with various bornaviral lineages during evolution. EBLs in primate genomes formed clades according to their integration ages, suggesting that bornavirus lineages infected with primate ancestors had changed chronologically. However, some bornaviral lineages may have coexisted with primate ancestors and underwent repeated endogenizations for tens of millions of years. Moreover, a bornaviral lineage that coexisted with primate ancestors also endogenized in the genomes of some ancestral bats. The habitats of these bat ancestors have been reported to overlap with the migration route of primate ancestors. These results suggest that long-term virus-host coexistence expanded the geographic distributions of the bornaviral lineage along with primate migration and may have spread their infections to these bat ancestors. Our findings provide insight into the history of bornavirus infections over geological timescales that cannot be deduced from research using extant viruses alone, thus broadening our perspective on virus-host coevolution. |
Author | Kawasaki, Junna Mukai, Yahiro Tomonaga, Keizo Horie, Masayuki Kojima, Shohei |
Author_xml | – sequence: 1 givenname: Junna surname: Kawasaki fullname: Kawasaki, Junna – sequence: 2 givenname: Shohei surname: Kojima fullname: Kojima, Shohei – sequence: 3 givenname: Yahiro surname: Mukai fullname: Mukai, Yahiro – sequence: 4 givenname: Keizo surname: Tomonaga fullname: Tomonaga, Keizo – sequence: 5 givenname: Masayuki surname: Horie fullname: Horie, Masayuki |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33990470$$D View this record in MEDLINE/PubMed |
BookMark | eNp1kctr3DAYxEVJaDZJzz21GHrpxcmnly1dCiV9QkIuuQtZj0SLV9pK9sL-95XZJG0DvUgg_WYYZk7RUUzRIfQWwwWGnl5uoy4XBEhHKMdYvEIrDBK3HZNwhFYApG8FI-wEnZayBgDJBbxGJ5RKCayHFfqCAdqbffMQypTyvkm-GVKOehfyXJoQvTNTSLFUwFoX60uzc3lyQ9aTa-5dTBtXztGx12Nxbx7vM3T37evd1Y_2-vb7z6vP163hIKe2Ho53jNlBMqJrYKut8MZIY6n3XkLfG9d1lDEtzWClsL4XRoC3zAvK6Bn6dLDdzsPGWePilPWotjlsdN6rpIP69yeGB3Wfdkpg3kvOq8HHR4Ocfs2uTGoTinHjqKNLc1GEE4EFBU4r-uEFuk5z7WVcqEpgxvrF8P3fiZ6jPPVbAX4ATE6lZOeVCZNeGq0Bw6gwqGVHteyo_uxYdZcvdE_W_1e8OyjWy5DPOOmBAaOU_garvKoC |
CitedBy_id | crossref_primary_10_1016_j_bbrc_2023_03_069 crossref_primary_10_1016_j_celrep_2021_109530 crossref_primary_10_1371_journal_ppat_1011864 crossref_primary_10_1128_jvi_00997_24 crossref_primary_10_1002_1873_3468_14290 crossref_primary_10_1093_ve_veac085 crossref_primary_10_3390_epidemiologia3040034 crossref_primary_10_1186_s13059_024_03258_y crossref_primary_10_2222_jsv_72_47 crossref_primary_10_3390_v16081210 crossref_primary_10_1071_MA21036 crossref_primary_10_1146_annurev_phyto_021621_122122 crossref_primary_10_1002_2211_5463_13626 crossref_primary_10_1073_pnas_2108123118 crossref_primary_10_3390_ani14010047 crossref_primary_10_1038_s41579_021_00590_z crossref_primary_10_1093_molbev_msac190 crossref_primary_10_1016_j_cois_2021_11_007 crossref_primary_10_1038_s42003_023_04917_9 crossref_primary_10_1038_s41564_024_01825_4 |
Cites_doi | 10.1007/s00705-014-2276-z 10.1093/molbev/msu300 10.1073/pnas.0807873105 10.1292/jvms.18-0211 10.1038/s41586-020-2873-9 10.1126/science.aba9411 10.1098/rspb.2014.1122 10.1038/nmeth.4285 10.1038/ncomms13954 10.3390/v3101836 10.1093/nar/gky1095 10.1371/journal.ppat.1005785 10.1101/gr.361602 10.1016/j.virusres.2018.02.002 10.1038/nature12323 10.1073/pnas.1414980112 10.1093/molbev/msw046 10.1111/2041-210X.12628 10.1371/journal.pbio.1000436 10.7717/peerj-cs.116 10.1371/journal.ppat.1001030 10.1016/j.virusres.2018.04.006 10.1093/molbev/msx281 10.1038/s41579-019-0189-2 10.1093/molbev/mst010 10.1016/j.cub.2016.10.061 10.1080/10635150500234534 10.1371/journal.ppat.1006881 10.1186/1471-2105-10-421 10.1016/j.virol.2015.02.011 10.1038/nature14120 10.1038/s41586-021-03224-9 10.1073/pnas.91.10.4362 10.1093/nar/gkv1189 10.1186/s13100-015-0041-9 10.1126/science.1105113 10.1126/science.275.5307.1793 10.1038/nature08695 10.1126/science.1118124 10.1016/j.cub.2018.05.032 10.1186/s13059-014-0539-3 10.1038/s41564-018-0296-2 10.1098/rstb.2012.0499 10.3201/eid1204.051418 10.1038/s41586-018-0097-z 10.1186/s12977-018-0442-1 10.1007/s00705-019-04247-4 10.1038/s41586-018-0012-7 10.1371/journal.pone.0049521 10.1093/molbev/msx116 10.1073/pnas.0809297106 10.1038/s41586-020-2876-6 10.1093/jmammal/gyz018 10.1098/rstb.2011.0023 10.1073/pnas.1804921115 10.1371/journal.pgen.1001191 10.1073/pnas.0610579104 |
ContentType | Journal Article |
Copyright | Copyright National Academy of Sciences May 18, 2021 2021 |
Copyright_xml | – notice: Copyright National Academy of Sciences May 18, 2021 – notice: 2021 |
DBID | AAYXX CITATION NPM 7QG 7QL 7QP 7QR 7SN 7SS 7T5 7TK 7TM 7TO 7U9 8FD C1K FR3 H94 M7N P64 RC3 7X8 5PM |
DOI | 10.1073/pnas.2026235118 |
DatabaseName | CrossRef PubMed Animal Behavior Abstracts Bacteriology Abstracts (Microbiology B) Calcium & Calcified Tissue Abstracts Chemoreception Abstracts Ecology Abstracts Entomology Abstracts (Full archive) Immunology Abstracts Neurosciences Abstracts Nucleic Acids Abstracts Oncogenes and Growth Factors Abstracts Virology and AIDS Abstracts Technology Research Database Environmental Sciences and Pollution Management Engineering Research Database AIDS and Cancer Research Abstracts Algology Mycology and Protozoology Abstracts (Microbiology C) Biotechnology and BioEngineering Abstracts Genetics Abstracts MEDLINE - Academic PubMed Central (Full Participant titles) |
DatabaseTitle | CrossRef PubMed Virology and AIDS Abstracts Oncogenes and Growth Factors Abstracts Technology Research Database Nucleic Acids Abstracts Ecology Abstracts Neurosciences Abstracts Biotechnology and BioEngineering Abstracts Environmental Sciences and Pollution Management Entomology Abstracts Genetics Abstracts Animal Behavior Abstracts Bacteriology Abstracts (Microbiology B) Algology Mycology and Protozoology Abstracts (Microbiology C) AIDS and Cancer Research Abstracts Chemoreception Abstracts Immunology Abstracts Engineering Research Database Calcium & Calcified Tissue Abstracts MEDLINE - Academic |
DatabaseTitleList | Virology and AIDS Abstracts CrossRef MEDLINE - Academic PubMed |
Database_xml | – sequence: 1 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Sciences (General) |
EISSN | 1091-6490 |
EndPage | 9 |
ExternalDocumentID | PMC8157955 33990470 10_1073_pnas_2026235118 27040433 |
Genre | Journal Article |
GrantInformation_xml | – fundername: Japan Society for the Promotion of Science London (JSPS London) grantid: JP19J22241 – fundername: Ministry of Education, Culture, Sports, Science and Technology (MEXT) grantid: JP17H05821 – fundername: Japan Society for the Promotion of Science London (JSPS London) grantid: JP20H05682 – fundername: Ministry of Education, Culture, Sports, Science and Technology (MEXT) grantid: JP16H0643 – fundername: Japan Society for the Promotion of Science London (JSPS London) grantid: JP18K19443 – fundername: Ministry of Education, Culture, Sports, Science and Technology (MEXT) grantid: JP16H06429 – fundername: Ministry of Education, Culture, Sports, Science and Technology (MEXT) grantid: JP16K21723 – fundername: Ministry of Education, Culture, Sports, Science and Technology (MEXT) grantid: JP19H04833 |
GroupedDBID | --- -DZ -~X .55 0R~ 123 29P 2AX 2FS 2WC 4.4 53G 5RE 5VS 85S AACGO AAFWJ AANCE ABBHK ABOCM ABPLY ABPPZ ABTLG ABXSQ ABZEH ACGOD ACIWK ACNCT ACPRK AENEX AEUPB AEXZC AFFNX AFOSN AFRAH ALMA_UNASSIGNED_HOLDINGS BKOMP CS3 D0L DCCCD DIK DU5 E3Z EBS F5P FRP GX1 H13 HH5 HYE IPSME JAAYA JBMMH JENOY JHFFW JKQEH JLS JLXEF JPM JSG JST KQ8 L7B LU7 N9A N~3 O9- OK1 PNE PQQKQ R.V RHI RNA RNS RPM RXW SA0 SJN TAE TN5 UKR W8F WH7 WOQ WOW X7M XSW Y6R YBH YKV YSK ZCA ~02 ~KM AAYXX CITATION NPM 7QG 7QL 7QP 7QR 7SN 7SS 7T5 7TK 7TM 7TO 7U9 8FD C1K FR3 H94 M7N P64 RC3 7X8 5PM |
ID | FETCH-LOGICAL-c509t-509e5644db942a351dad8fcc9cd3fff9077ce66344a9cbd98df78c80fd4f8343 |
ISSN | 0027-8424 1091-6490 |
IngestDate | Thu Aug 21 14:14:36 EDT 2025 Fri Jul 11 08:18:12 EDT 2025 Mon Jun 30 09:48:36 EDT 2025 Thu Apr 03 06:59:27 EDT 2025 Tue Jul 01 01:02:56 EDT 2025 Thu Apr 24 23:09:18 EDT 2025 Thu May 29 08:53:14 EDT 2025 |
IsDoiOpenAccess | false |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
Issue | 20 |
Keywords | vertebrate evolution endogenous bornavirus-like element virus–host coevolutionary history ancient viral infection paleovirology |
Language | English |
License | Published under the PNAS license. |
LinkModel | OpenURL |
MergedId | FETCHMERGED-LOGICAL-c509t-509e5644db942a351dad8fcc9cd3fff9077ce66344a9cbd98df78c80fd4f8343 |
Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author contributions: J.K. and M.H. designed research; J.K., S.K., Y.M., and M.H. performed research; J.K. contributed new reagents/analytic tools; J.K., S.K., K.T., and M.H. analyzed data; and J.K. and M.H. wrote the paper. Edited by Stephen P. Goff, Columbia University Medical Center, New York, NY, and approved March 31, 2021 (received for review December 29, 2020) 3Present address: Division of Veterinary Science, Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Izumisano 598-8531, Japan. 1Present address: Genome Immunology RIKEN Hakubi Research Team, RIKEN Cluster for Pioneering Research, Yokohama 230-0045, Japan. |
ORCID | 0000-0003-0405-7103 0000-0001-9351-5238 0000-0002-6609-5300 0000-0003-4682-7698 |
OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/8157955 |
PMID | 33990470 |
PQID | 2530514475 |
PQPubID | 42026 |
PageCount | 9 |
ParticipantIDs | pubmedcentral_primary_oai_pubmedcentral_nih_gov_8157955 proquest_miscellaneous_2528183053 proquest_journals_2530514475 pubmed_primary_33990470 crossref_citationtrail_10_1073_pnas_2026235118 crossref_primary_10_1073_pnas_2026235118 jstor_primary_27040433 |
ProviderPackageCode | CITATION AAYXX |
PublicationCentury | 2000 |
PublicationDate | 2021-05-18 |
PublicationDateYYYYMMDD | 2021-05-18 |
PublicationDate_xml | – month: 05 year: 2021 text: 2021-05-18 day: 18 |
PublicationDecade | 2020 |
PublicationPlace | United States |
PublicationPlace_xml | – name: United States – name: Washington |
PublicationTitle | Proceedings of the National Academy of Sciences - PNAS |
PublicationTitleAlternate | Proc Natl Acad Sci U S A |
PublicationYear | 2021 |
Publisher | National Academy of Sciences |
Publisher_xml | – name: National Academy of Sciences |
References | e_1_3_4_3_2 e_1_3_4_1_2 e_1_3_4_9_2 e_1_3_4_7_2 e_1_3_4_40_2 e_1_3_4_5_2 e_1_3_4_23_2 e_1_3_4_44_2 e_1_3_4_21_2 e_1_3_4_42_2 e_1_3_4_27_2 e_1_3_4_48_2 Hagberg A. A. (e_1_3_4_49_2) 2008 e_1_3_4_25_2 e_1_3_4_46_2 e_1_3_4_29_2 e_1_3_4_30_2 e_1_3_4_11_2 e_1_3_4_34_2 e_1_3_4_57_2 e_1_3_4_55_2 e_1_3_4_32_2 e_1_3_4_59_2 e_1_3_4_53_2 e_1_3_4_15_2 e_1_3_4_38_2 e_1_3_4_13_2 e_1_3_4_36_2 e_1_3_4_19_2 Harris R. S. (e_1_3_4_51_2) 2007 e_1_3_4_17_2 e_1_3_4_2_2 e_1_3_4_60_2 e_1_3_4_8_2 e_1_3_4_41_2 e_1_3_4_6_2 e_1_3_4_4_2 e_1_3_4_22_2 e_1_3_4_45_2 e_1_3_4_20_2 e_1_3_4_43_2 e_1_3_4_26_2 e_1_3_4_24_2 e_1_3_4_47_2 e_1_3_4_28_2 e_1_3_4_52_2 e_1_3_4_50_2 e_1_3_4_12_2 e_1_3_4_33_2 e_1_3_4_58_2 e_1_3_4_54_2 e_1_3_4_10_2 e_1_3_4_31_2 e_1_3_4_16_2 e_1_3_4_37_2 e_1_3_4_14_2 e_1_3_4_35_2 e_1_3_4_56_2 e_1_3_4_18_2 e_1_3_4_39_2 |
References_xml | – ident: e_1_3_4_17_2 doi: 10.1007/s00705-014-2276-z – ident: e_1_3_4_56_2 doi: 10.1093/molbev/msu300 – ident: e_1_3_4_12_2 doi: 10.1073/pnas.0807873105 – ident: e_1_3_4_22_2 doi: 10.1292/jvms.18-0211 – ident: e_1_3_4_27_2 doi: 10.1038/s41586-020-2873-9 – ident: e_1_3_4_20_2 – ident: e_1_3_4_2_2 doi: 10.1126/science.aba9411 – ident: e_1_3_4_25_2 doi: 10.1098/rspb.2014.1122 – ident: e_1_3_4_57_2 doi: 10.1038/nmeth.4285 – ident: e_1_3_4_11_2 doi: 10.1038/ncomms13954 – ident: e_1_3_4_43_2 doi: 10.3390/v3101836 – ident: e_1_3_4_55_2 doi: 10.1093/nar/gky1095 – ident: e_1_3_4_23_2 doi: 10.1371/journal.ppat.1005785 – volume-title: Improved Pairwise Alignment of Genomic Dna year: 2007 ident: e_1_3_4_51_2 – ident: e_1_3_4_52_2 doi: 10.1101/gr.361602 – ident: e_1_3_4_8_2 doi: 10.1016/j.virusres.2018.02.002 – ident: e_1_3_4_42_2 doi: 10.1038/nature12323 – ident: e_1_3_4_9_2 doi: 10.1073/pnas.1414980112 – ident: e_1_3_4_60_2 doi: 10.1093/molbev/msw046 – ident: e_1_3_4_59_2 doi: 10.1111/2041-210X.12628 – ident: e_1_3_4_35_2 doi: 10.1371/journal.pbio.1000436 – start-page: 11 volume-title: Proceedings of the 7th Python in Science Conference (SciPy2008) year: 2008 ident: e_1_3_4_49_2 – ident: e_1_3_4_50_2 doi: 10.7717/peerj-cs.116 – ident: e_1_3_4_21_2 doi: 10.1371/journal.ppat.1001030 – ident: e_1_3_4_26_2 doi: 10.1016/j.virusres.2018.04.006 – ident: e_1_3_4_58_2 doi: 10.1093/molbev/msx281 – ident: e_1_3_4_44_2 doi: 10.1038/s41579-019-0189-2 – ident: e_1_3_4_47_2 doi: 10.1093/molbev/mst010 – ident: e_1_3_4_5_2 doi: 10.1016/j.cub.2016.10.061 – ident: e_1_3_4_37_2 doi: 10.1080/10635150500234534 – ident: e_1_3_4_18_2 doi: 10.1371/journal.ppat.1006881 – ident: e_1_3_4_46_2 doi: 10.1186/1471-2105-10-421 – ident: e_1_3_4_7_2 doi: 10.1016/j.virol.2015.02.011 – ident: e_1_3_4_39_2 doi: 10.1038/nature14120 – ident: e_1_3_4_41_2 doi: 10.1038/s41586-021-03224-9 – ident: e_1_3_4_15_2 doi: 10.1073/pnas.91.10.4362 – ident: e_1_3_4_45_2 doi: 10.1093/nar/gkv1189 – ident: e_1_3_4_48_2 doi: 10.1186/s13100-015-0041-9 – ident: e_1_3_4_40_2 doi: 10.1126/science.1105113 – ident: e_1_3_4_3_2 doi: 10.1126/science.275.5307.1793 – ident: e_1_3_4_13_2 doi: 10.1038/nature08695 – ident: e_1_3_4_38_2 doi: 10.1126/science.1118124 – ident: e_1_3_4_34_2 doi: 10.1016/j.cub.2018.05.032 – ident: e_1_3_4_24_2 doi: 10.1186/s13059-014-0539-3 – ident: e_1_3_4_1_2 doi: 10.1038/s41564-018-0296-2 – ident: e_1_3_4_14_2 doi: 10.1098/rstb.2012.0499 – ident: e_1_3_4_29_2 doi: 10.3201/eid1204.051418 – ident: e_1_3_4_6_2 doi: 10.1038/s41586-018-0097-z – ident: e_1_3_4_54_2 doi: 10.1186/s12977-018-0442-1 – ident: e_1_3_4_16_2 doi: 10.1007/s00705-019-04247-4 – ident: e_1_3_4_19_2 doi: 10.1038/s41586-018-0012-7 – ident: e_1_3_4_32_2 doi: 10.1371/journal.pone.0049521 – ident: e_1_3_4_53_2 doi: 10.1093/molbev/msx116 – ident: e_1_3_4_31_2 doi: 10.1073/pnas.0809297106 – ident: e_1_3_4_28_2 doi: 10.1038/s41586-020-2876-6 – ident: e_1_3_4_36_2 doi: 10.1093/jmammal/gyz018 – ident: e_1_3_4_30_2 doi: 10.1098/rstb.2011.0023 – ident: e_1_3_4_4_2 doi: 10.1073/pnas.1804921115 – ident: e_1_3_4_10_2 doi: 10.1371/journal.pgen.1001191 – ident: e_1_3_4_33_2 doi: 10.1073/pnas.0610579104 |
SSID | ssj0009580 |
Score | 2.478456 |
Snippet | Although viruses have threatened our ancestors for millions of years, prehistoric epidemics of viruses are largely unknown. Endogenous bornavirus-like elements... Many viral diseases have emerged in recent decades, but prehistoric viral infections remain poorly understood. In some cases, nucleotide sequences of ancient... |
SourceID | pubmedcentral proquest pubmed crossref jstor |
SourceType | Open Access Repository Aggregation Database Index Database Enrichment Source Publisher |
StartPage | 1 |
SubjectTerms | Biological Sciences Coevolution Coexistence Genomes Geographical distribution Infections Phylogeny Vertebrates Viruses |
Title | 100-My history of bornavirus infections hidden in vertebrate genomes |
URI | https://www.jstor.org/stable/27040433 https://www.ncbi.nlm.nih.gov/pubmed/33990470 https://www.proquest.com/docview/2530514475 https://www.proquest.com/docview/2528183053 https://pubmed.ncbi.nlm.nih.gov/PMC8157955 |
Volume | 118 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3db9MwELfKeOEFMWBQGChIPAxNKWns1MnjBJumdSuT6KTyFNmJrYaPBPUDxP4A_m7uYidOp4KAF6tyHMv1nS-_O9u_I-TlUGukFY_9gGnpM8W5L5ga-VImjCcy1pnG0MDFZHR6xc5m0azX-9k5tbReyUF2vfVeyf9IFepArnhL9h8k23YKFfAb5AslSBjKv5LxMAj8ix-WM7jeKpeYcPhbsVi7Y1blEhqgecHQBmZfxq3ilcLcyVVz_cOi08v2a7Zszg5MmmDhkbt6Yu3B8tA_vJy4RMZj8V0shUmDfQa4uDX44-pj8aUGqe_n1VwVTsifTDLsD2JeLCoX8IYJFCbgO1bFddWNTIRD3FS3xrRD7L11gF2THMJnkpmL1ANlrDCAGH_ETB7R1kw7O43uctCxusOt3wIwXpjAuBTIyh4CzIuaLjZYtyfv0pOr8_N0ejyb3iK3Q3A3wibq05I3x-Yqkx1qQxHF6esb3W-gG3PAdZvrcvMEbgfSTO-Ru9YX8Y6MYu2Snirvk91m8rwDS0n-6gF5azTNs5rmVdpzmuY5TfOMpkGN5zTNs5r2kExPjqdvTn2bf8PPAEaufChUBHg5h3UbCvh_uchh8WZJllOtdRJwnilArIyJJJN5Eueax1kc6JzpmDK6R3bKqlSPiQc-N5VcCPB1M7AHSlKZ5DSnidI54GHdJ4Nm2tLMctNjipTPaX1GgtMU5zl189wnB-0LXw0ty--b7tVyaNuFPEBKKdon-41gUruo4b2IYkYAxqM-edE-BpOL-2iiVNUa2yCFGrSDLh4ZObadUwD8AeNBn_ANCbcNkM5980lZzGta93gY8SSKnvx5WE_JHbfW9snOarFWzwAXr-TzWml_AUtqu60 |
linkProvider | National Library of Medicine |
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=100-My+history+of+bornavirus+infections+hidden+in+vertebrate+genomes&rft.jtitle=Proceedings+of+the+National+Academy+of+Sciences+-+PNAS&rft.au=Kawasaki%2C+Junna&rft.au=Kojima%2C+Shohei&rft.au=Mukai%2C+Yahiro&rft.au=Tomonaga%2C+Keizo&rft.date=2021-05-18&rft.pub=National+Academy+of+Sciences&rft.issn=0027-8424&rft.eissn=1091-6490&rft.volume=118&rft.issue=20&rft.spage=1&rft_id=info:doi/10.1073%2Fpnas.2026235118&rft.externalDBID=NO_FULL_TEXT |
thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0027-8424&client=summon |
thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0027-8424&client=summon |
thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0027-8424&client=summon |