Systematic estimation of insertion dates of endogenous bornavirus-like elements in vesper bats
Endogenous bornavirus-like elements (EBLs) are sequences derived from bornaviruses (the family Bornaviridae) that are integrated into animal genomes. They are formed through germline insertions of segments of bornaviral transcripts into animal genomes. Because EBLs are molecular fossils of bornaviru...
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| Published in | Journal of Veterinary Medical Science Vol. 80; no. 8; pp. 1356 - 1363 |
|---|---|
| Main Authors | , , |
| Format | Journal Article |
| Language | English |
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Japan
JAPANESE SOCIETY OF VETERINARY SCIENCE
01.08.2018
Japan Science and Technology Agency The Japanese Society of Veterinary Science |
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| Abstract | Endogenous bornavirus-like elements (EBLs) are sequences derived from bornaviruses (the family Bornaviridae) that are integrated into animal genomes. They are formed through germline insertions of segments of bornaviral transcripts into animal genomes. Because EBLs are molecular fossils of bornaviruses, they serve as precious sources of information to understand the evolutionary history of bornaviruses. Previous studies revealed the presence of many EBLs in bat genomes, especially in vesper bats, and suggested the long-term association between bats and bornaviruses. However, insertion dates of EBLs are largely unknown because of the limitations of available bat genome sequences in the public database. In this study, through a combination of database searches, PCR, and sequencing approaches, we systematically determined the gene orthologies of 13 lineages of EBLs in bats of the genus Myotis and Eptesicus and family Vespertilionidae. Using the above data, we estimated their insertion dates: the EBLs in vesper bats were inserted approximately 14.2 to 53 million years ago. These results suggest that vesper bats have been repeatedly infected by bornaviruses at different points in time during evolution. This study provides novel insights into the evolutionary history of bornaviruses and demonstrates the robustness of combining database searches, PCR, and sequencing approaches to estimate insertion dates of bornaviruses. |
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| AbstractList | Endogenous bornavirus-like elements (EBLs) are sequences derived from bornaviruses (the
family
Bornaviridae
) that are integrated into animal genomes. They are
formed through germline insertions of segments of bornaviral transcripts into animal
genomes. Because EBLs are molecular fossils of bornaviruses, they serve as precious
sources of information to understand the evolutionary history of bornaviruses. Previous
studies revealed the presence of many EBLs in bat genomes, especially in vesper bats, and
suggested the long-term association between bats and bornaviruses. However, insertion
dates of EBLs are largely unknown because of the limitations of available bat genome
sequences in the public database. In this study, through a combination of database
searches, PCR, and sequencing approaches, we systematically determined the gene
orthologies of 13 lineages of EBLs in bats of the genus
Myotis
and
Eptesicus
and family Vespertilionidae. Using the above data, we
estimated their insertion dates: the EBLs in vesper bats were inserted approximately 14.2
to 53 million years ago. These results suggest that vesper bats have been repeatedly
infected by bornaviruses at different points in time during evolution. This study provides
novel insights into the evolutionary history of bornaviruses and demonstrates the
robustness of combining database searches, PCR, and sequencing approaches to estimate
insertion dates of bornaviruses. Endogenous bornavirus-like elements (EBLs) are sequences derived from bornaviruses (the family Bornaviridae) that are integrated into animal genomes. They are formed through germline insertions of segments of bornaviral transcripts into animal genomes. Because EBLs are molecular fossils of bornaviruses, they serve as precious sources of information to understand the evolutionary history of bornaviruses. Previous studies revealed the presence of many EBLs in bat genomes, especially in vesper bats, and suggested the long-term association between bats and bornaviruses. However, insertion dates of EBLs are largely unknown because of the limitations of available bat genome sequences in the public database. In this study, through a combination of database searches, PCR, and sequencing approaches, we systematically determined the gene orthologies of 13 lineages of EBLs in bats of the genus Myotis and Eptesicus and family Vespertilionidae. Using the above data, we estimated their insertion dates: the EBLs in vesper bats were inserted approximately 14.2 to 53 million years ago. These results suggest that vesper bats have been repeatedly infected by bornaviruses at different points in time during evolution. This study provides novel insights into the evolutionary history of bornaviruses and demonstrates the robustness of combining database searches, PCR, and sequencing approaches to estimate insertion dates of bornaviruses. Endogenous bornavirus-like elements (EBLs) are sequences derived from bornaviruses (the family Bornaviridae) that are integrated into animal genomes. They are formed through germline insertions of segments of bornaviral transcripts into animal genomes. Because EBLs are molecular fossils of bornaviruses, they serve as precious sources of information to understand the evolutionary history of bornaviruses. Previous studies revealed the presence of many EBLs in bat genomes, especially in vesper bats, and suggested the long-term association between bats and bornaviruses. However, insertion dates of EBLs are largely unknown because of the limitations of available bat genome sequences in the public database. In this study, through a combination of database searches, PCR, and sequencing approaches, we systematically determined the gene orthologies of 13 lineages of EBLs in bats of the genus Myotis and Eptesicus and family Vespertilionidae. Using the above data, we estimated their insertion dates: the EBLs in vesper bats were inserted approximately 14.2 to 53 million years ago. These results suggest that vesper bats have been repeatedly infected by bornaviruses at different points in time during evolution. This study provides novel insights into the evolutionary history of bornaviruses and demonstrates the robustness of combining database searches, PCR, and sequencing approaches to estimate insertion dates of bornaviruses.Endogenous bornavirus-like elements (EBLs) are sequences derived from bornaviruses (the family Bornaviridae) that are integrated into animal genomes. They are formed through germline insertions of segments of bornaviral transcripts into animal genomes. Because EBLs are molecular fossils of bornaviruses, they serve as precious sources of information to understand the evolutionary history of bornaviruses. Previous studies revealed the presence of many EBLs in bat genomes, especially in vesper bats, and suggested the long-term association between bats and bornaviruses. However, insertion dates of EBLs are largely unknown because of the limitations of available bat genome sequences in the public database. In this study, through a combination of database searches, PCR, and sequencing approaches, we systematically determined the gene orthologies of 13 lineages of EBLs in bats of the genus Myotis and Eptesicus and family Vespertilionidae. Using the above data, we estimated their insertion dates: the EBLs in vesper bats were inserted approximately 14.2 to 53 million years ago. These results suggest that vesper bats have been repeatedly infected by bornaviruses at different points in time during evolution. This study provides novel insights into the evolutionary history of bornaviruses and demonstrates the robustness of combining database searches, PCR, and sequencing approaches to estimate insertion dates of bornaviruses. |
| Author | MUKAI, Yahiro TOMONAGA, Keizo HORIE, Masayuki |
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| Keywords | vesper bat endogenous bornavirus-like element paleovirology |
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Horie, M., Kobayashi, Y., Honda, T., Fujino, K., Akasaka, T., Kohl, C., Wibbelt, G., Mühldorfer, K., Kurth, A., Müller, M. A., Corman, V. M., Gillich, N., Suzuki, Y., Schwemmle, M. and Tomonaga, K. 2016. An RNA-dependent RNA polymerase gene in bat genomes derived from an ancient negative-strand RNA virus. Sci. Rep. 6: 25873. 19. Katzourakis, A. and Gifford, R. J. 2010. Endogenous viral elements in animal genomes. PLoS Genet. 6: e1001191. 30. Zhuo, X. and Feschotte, C. 2015. Cross-species transmission and differential fate of an endogenous retrovirus in three mammal lineages. PLoS Pathog. 11: e1005279. 6. Fujino, K., Horie, M., Honda, T., Merriman, D. K. and Tomonaga, K. 2014. Inhibition of Borna disease virus replication by an endogenous bornavirus-like element in the ground squirrel genome. Proc. Natl. Acad. Sci. U.S.A. 111: 13175–13180. 9. Horie, M. and Tomonaga, K. 2011. Non-retroviral fossils in vertebrate genomes. Viruses 3: 1836–1848. 18. Katoh, K. and Standley, D. M. 2013. 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Comprehensive analysis of endogenous bornavirus-like elements in eukaryote genomes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368: 20120499. 28. Tomonaga, K., Kobayashi, T. and Ikuta, K. 2002. Molecular and cellular biology of Borna disease virus infection. Microbes Infect. 4: 491–500. 25. Simmons, N. B. 2005. Order chiroptera. pp. 312–529 In: Mammal Species of the World. A Taxonomic and Geographic Reference (Wilson, D. E. and Reeder, D. M. E. eds.), Johns Hopkins University Press, Washington, D.C. 27. Sofuku, K., Parrish, N. F., Honda, T. and Tomonaga, K. 2015. Transcription Profiling Demonstrates Epigenetic Control of Non-retroviral RNA Virus-Derived Elements in the Human Genome. Cell Reports 12: 1548–1554. 29. Weiss, R. A. 2006. The discovery of endogenous retroviruses. Retrovirology 3: 67. 12. Horie, M., Honda, T., Suzuki, Y., Kobayashi, Y., Daito, T., Oshida, T., Ikuta, K., Jern, P., Gojobori, T., Coffin, J. M. and Tomonaga, K. 2010. 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| References_xml | – reference: 15. Hyndman, T. H., Shilton, C. M., Stenglein, M. D. and Wellehan, J. F. X. Jr 2018. Divergent bornaviruses from Australian carpet pythons with neurological disease date the origin of extant Bornaviridae prior to the end-Cretaceous extinction. PLoS Pathog. 14: e1006881. – reference: 22. Kumar, S., Stecher, G. and Tamura, K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870–1874. – reference: 16. Imakawa, K., Nakagawa, S. and Miyazawa, T. 2015. Baton pass hypothesis: successive incorporation of unconserved endogenous retroviral genes for placentation during mammalian evolution. Genes Cells 20: 771–788. – reference: 19. Katzourakis, A. and Gifford, R. J. 2010. Endogenous viral elements in animal genomes. PLoS Genet. 6: e1001191. – reference: 13. Horie, M., Kobayashi, Y., Honda, T., Fujino, K., Akasaka, T., Kohl, C., Wibbelt, G., Mühldorfer, K., Kurth, A., Müller, M. A., Corman, V. M., Gillich, N., Suzuki, Y., Schwemmle, M. and Tomonaga, K. 2016. An RNA-dependent RNA polymerase gene in bat genomes derived from an ancient negative-strand RNA virus. Sci. Rep. 6: 25873. – reference: 26. Smith, R. H., Hallwirth, C. V., Westerman, M., Hetherington, N. A., Tseng, Y. S., Cecchini, S., Virag, T., Ziegler, M. L., Rogozin, I. B., Koonin, E. V., Agbandje-McKenna, M., Kotin, R. M. and Alexander, I. E. 2016. Germline viral “fossils” guide in silico reconstruction of a mid-Cenozoic era marsupial adeno-associated virus. Sci. Rep. 6: 28965. – reference: 5. Cui, J. and Wang, L. F. 2015. Genomic Mining Reveals Deep Evolutionary Relationships between Bornaviruses and Bats. Viruses 7: 5792–5800. – reference: 10. Horie, M. and Tomonaga, K. 2018. Paleovirology of bornaviruses: What can be learned from molecular fossils of bornaviruses. Virus Res. – reference: 4. Cantrell, M. A., Scott, L., Brown, C. J., Martinez, A. R. and Wichman, H. A. 2008. Loss of LINE-1 activity in the megabats. Genetics 178: 393–404. – reference: 9. Horie, M. and Tomonaga, K. 2011. Non-retroviral fossils in vertebrate genomes. Viruses 3: 1836–1848. – reference: 14. Horie, M., Kobayashi, Y., Suzuki, Y. and Tomonaga, K. 2013. Comprehensive analysis of endogenous bornavirus-like elements in eukaryote genomes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368: 20120499. – reference: 23. Mi, S., Lee, X., Li, X., Veldman, G. M., Finnerty, H., Racie, L., LaVallie, E., Tang, X. Y., Edouard, P., Howes, S., Keith, J. C. Jr. and McCoy, J. M. 2000. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403: 785–789. – reference: 27. Sofuku, K., Parrish, N. F., Honda, T. and Tomonaga, K. 2015. Transcription Profiling Demonstrates Epigenetic Control of Non-retroviral RNA Virus-Derived Elements in the Human Genome. Cell Reports 12: 1548–1554. – reference: 17. Jern, P. and Coffin, J. M. 2008. Effects of retroviruses on host genome function. Annu. Rev. 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| Snippet | Endogenous bornavirus-like elements (EBLs) are sequences derived from bornaviruses (the family Bornaviridae) that are integrated into animal genomes. They are... Endogenous bornavirus-like elements (EBLs) are sequences derived from bornaviruses (the family Bornaviridae ) that are integrated into animal genomes. They are... |
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| SubjectTerms | Animals Bornaviridae - genetics Chiroptera Chiroptera - virology endogenous bornavirus-like element Evolution Evolutionary genetics Genome Genomes paleovirology Phylogeny vesper bat Virology |
| Title | Systematic estimation of insertion dates of endogenous bornavirus-like elements in vesper bats |
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