Diverse variola virus (smallpox) strains were widespread in northern Europe in the Viking Age

Barbara Mühlemann; Lasse Vinner; Ashot Margaryan; Helene Wilhelmson; Constanza de la Fuente Castro; Morten E Allentoft; Peter de Barros Damgaard; Anders Johannes Hansen; Sofie Holtsmark Nielsen; Lisa Mariann Strand; Jan Bill; Alexandra Buzhilova; Tamara Pushkina; Ceri Falys; Valeri Khartanovich; Vyacheslav Moiseyev; Marie Louise Schjellerup Jørkov; Palle Østergaard Sørensen; Yvonne Magnusson; Ingrid Gustin; Hannes Schroeder; Gerd Sutter; Geoffrey L Smith; Christian Drosten; Ron A M Fouchier; Derek J Smith; Eske Willerslev; Terry C Jones; Martin Sikora

doi:10.1126/science.aaw8977

Diverse variola virus (smallpox) strains were widespread in northern Europe in the Viking Age

Barbara Mühlemann, Lasse Vinner, Ashot Margaryan, Helene Wilhelmson, Constanza de la Fuente Castro, Morten E Allentoft, Peter de Barros Damgaard, Anders Johannes Hansen, Sofie Holtsmark Nielsen, Lisa Mariann Strand, Jan Bill, Alexandra Buzhilova, Tamara Pushkina, Ceri Falys, Valeri Khartanovich, Vyacheslav Moiseyev, Marie Louise Schjellerup Jørkov, Palle Østergaard Sørensen, Yvonne Magnusson, Ingrid GustinHannes Schroeder, Gerd Sutter, Geoffrey L Smith, Christian Drosten, Ron A M Fouchier, Derek J Smith, Eske Willerslev^*, Terry C Jones, Martin Sikora^*

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › Research › peer-review

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Abstract

Smallpox, one of the most devastating human diseases, killed between 300 million and 500 million people in the 20th century alone. We recovered viral sequences from 13 northern European individuals, including 11 dated to ~600-1050 CE, overlapping the Viking Age, and reconstructed near-complete variola virus genomes for four of them. The samples predate the earliest confirmed smallpox cases by ~1000 years, and the sequences reveal a now-extinct sister clade of the modern variola viruses that were in circulation before the eradication of smallpox. We date the most recent common ancestor of variola virus to ~1700 years ago. Distinct patterns of gene inactivation in the four near-complete sequences show that different evolutionary paths of genotypic host adaptation resulted in variola viruses that circulated widely among humans.

Original language	English
Journal	Science (New York, N.Y.)
Volume	369
Issue number	6502
Pages (from-to)	1-12
ISSN	0036-8075
DOIs	https://doi.org/10.1126/science.aaw8977
Publication status	Published - 2020

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Diverse variola virus (smallpox) strains were widespread in northern Europe in the Viking Age_(early_version)Submitted manuscript, 503 KBLicence: Unspecified

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Mühlemann, B., Vinner, L., Margaryan, A., Wilhelmson, H., de la Fuente Castro, C., Allentoft, M. E., de Barros Damgaard, P., Hansen, A. J., Holtsmark Nielsen, S., Strand, L. M., Bill, J., Buzhilova, A., Pushkina, T., Falys, C., Khartanovich, V., Moiseyev, V., Jørkov, M. L. S., Østergaard Sørensen, P., Magnusson, Y., ... Sikora, M. (2020). Diverse variola virus (smallpox) strains were widespread in northern Europe in the Viking Age. Science (New York, N.Y.), 369(6502), 1-12. https://doi.org/10.1126/science.aaw8977

Diverse variola virus (smallpox) strains were widespread in northern Europe in the Viking Age. / Mühlemann, Barbara; Vinner, Lasse ; Margaryan, Ashot; Wilhelmson, Helene; de la Fuente Castro, Constanza; Allentoft, Morten E; de Barros Damgaard, Peter; Hansen, Anders Johannes; Holtsmark Nielsen, Sofie; Strand, Lisa Mariann; Bill, Jan; Buzhilova, Alexandra; Pushkina, Tamara; Falys, Ceri; Khartanovich, Valeri; Moiseyev, Vyacheslav; Jørkov, Marie Louise Schjellerup; Østergaard Sørensen, Palle; Magnusson, Yvonne; Gustin, Ingrid; Schroeder, Hannes; Sutter, Gerd; Smith, Geoffrey L; Drosten, Christian; Fouchier, Ron A M; Smith, Derek J; Willerslev, Eske; Jones, Terry C; Sikora, Martin.

In: Science (New York, N.Y.), Vol. 369, No. 6502, 2020, p. 1-12.

Research output: Contribution to journal › Journal article › Research › peer-review

Mühlemann, B, Vinner, L , Margaryan, A, Wilhelmson, H, de la Fuente Castro, C, Allentoft, ME, de Barros Damgaard, P, Hansen, AJ, Holtsmark Nielsen, S, Strand, LM, Bill, J, Buzhilova, A, Pushkina, T, Falys, C, Khartanovich, V, Moiseyev, V, Jørkov, MLS, Østergaard Sørensen, P, Magnusson, Y, Gustin, I, Schroeder, H, Sutter, G, Smith, GL, Drosten, C, Fouchier, RAM, Smith, DJ, Willerslev, E, Jones, TC & Sikora, M 2020, 'Diverse variola virus (smallpox) strains were widespread in northern Europe in the Viking Age', Science (New York, N.Y.), vol. 369, no. 6502, pp. 1-12. https://doi.org/10.1126/science.aaw8977

Mühlemann, Barbara ; Vinner, Lasse ; Margaryan, Ashot ; Wilhelmson, Helene ; de la Fuente Castro, Constanza ; Allentoft, Morten E ; de Barros Damgaard, Peter ; Hansen, Anders Johannes ; Holtsmark Nielsen, Sofie ; Strand, Lisa Mariann ; Bill, Jan ; Buzhilova, Alexandra ; Pushkina, Tamara ; Falys, Ceri ; Khartanovich, Valeri ; Moiseyev, Vyacheslav ; Jørkov, Marie Louise Schjellerup ; Østergaard Sørensen, Palle ; Magnusson, Yvonne ; Gustin, Ingrid ; Schroeder, Hannes ; Sutter, Gerd ; Smith, Geoffrey L ; Drosten, Christian ; Fouchier, Ron A M ; Smith, Derek J ; Willerslev, Eske ; Jones, Terry C ; Sikora, Martin. / Diverse variola virus (smallpox) strains were widespread in northern Europe in the Viking Age. In: Science (New York, N.Y.). 2020 ; Vol. 369, No. 6502. pp. 1-12.

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title = "Diverse variola virus (smallpox) strains were widespread in northern Europe in the Viking Age",

abstract = "Smallpox, one of the most devastating human diseases, killed between 300 million and 500 million people in the 20th century alone. We recovered viral sequences from 13 northern European individuals, including 11 dated to ~600-1050 CE, overlapping the Viking Age, and reconstructed near-complete variola virus genomes for four of them. The samples predate the earliest confirmed smallpox cases by ~1000 years, and the sequences reveal a now-extinct sister clade of the modern variola viruses that were in circulation before the eradication of smallpox. We date the most recent common ancestor of variola virus to ~1700 years ago. Distinct patterns of gene inactivation in the four near-complete sequences show that different evolutionary paths of genotypic host adaptation resulted in variola viruses that circulated widely among humans.",

author = "Barbara M{\"u}hlemann and Lasse Vinner and Ashot Margaryan and Helene Wilhelmson and {de la Fuente Castro}, Constanza and Allentoft, {Morten E} and {de Barros Damgaard}, Peter and Hansen, {Anders Johannes} and {Holtsmark Nielsen}, Sofie and Strand, {Lisa Mariann} and Jan Bill and Alexandra Buzhilova and Tamara Pushkina and Ceri Falys and Valeri Khartanovich and Vyacheslav Moiseyev and J{\o}rkov, {Marie Louise Schjellerup} and {{\O}stergaard S{\o}rensen}, Palle and Yvonne Magnusson and Ingrid Gustin and Hannes Schroeder and Gerd Sutter and Smith, {Geoffrey L} and Christian Drosten and Fouchier, {Ron A M} and Smith, {Derek J} and Eske Willerslev and Jones, {Terry C} and Martin Sikora",

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AU - de la Fuente Castro, Constanza

AU - Allentoft, Morten E

AU - de Barros Damgaard, Peter

AU - Hansen, Anders Johannes

AU - Holtsmark Nielsen, Sofie

AU - Strand, Lisa Mariann

AU - Bill, Jan

AU - Buzhilova, Alexandra

AU - Pushkina, Tamara

AU - Falys, Ceri

AU - Khartanovich, Valeri

AU - Moiseyev, Vyacheslav

AU - Jørkov, Marie Louise Schjellerup

AU - Østergaard Sørensen, Palle

AU - Magnusson, Yvonne

AU - Gustin, Ingrid

AU - Schroeder, Hannes

AU - Sutter, Gerd

AU - Smith, Geoffrey L

AU - Drosten, Christian

AU - Fouchier, Ron A M

AU - Smith, Derek J

AU - Willerslev, Eske

AU - Jones, Terry C

AU - Sikora, Martin

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N2 - Smallpox, one of the most devastating human diseases, killed between 300 million and 500 million people in the 20th century alone. We recovered viral sequences from 13 northern European individuals, including 11 dated to ~600-1050 CE, overlapping the Viking Age, and reconstructed near-complete variola virus genomes for four of them. The samples predate the earliest confirmed smallpox cases by ~1000 years, and the sequences reveal a now-extinct sister clade of the modern variola viruses that were in circulation before the eradication of smallpox. We date the most recent common ancestor of variola virus to ~1700 years ago. Distinct patterns of gene inactivation in the four near-complete sequences show that different evolutionary paths of genotypic host adaptation resulted in variola viruses that circulated widely among humans.

AB - Smallpox, one of the most devastating human diseases, killed between 300 million and 500 million people in the 20th century alone. We recovered viral sequences from 13 northern European individuals, including 11 dated to ~600-1050 CE, overlapping the Viking Age, and reconstructed near-complete variola virus genomes for four of them. The samples predate the earliest confirmed smallpox cases by ~1000 years, and the sequences reveal a now-extinct sister clade of the modern variola viruses that were in circulation before the eradication of smallpox. We date the most recent common ancestor of variola virus to ~1700 years ago. Distinct patterns of gene inactivation in the four near-complete sequences show that different evolutionary paths of genotypic host adaptation resulted in variola viruses that circulated widely among humans.

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