Genome-scale sequencing and analysis of human, wolf, and bison DNA from 25,000-year-old sediment

Pere Gelabert; Susanna Sawyer; Anders Bergström; Ashot Margaryan; Thomas C. Collin; Tengiz Meshveliani; Anna Belfer-Cohen; David Lordkipanidze; Nino Jakeli; Zinovi Matskevich; Guy Bar-Oz; Daniel M. Fernandes; Olivia Cheronet; Kadir T. Özdoğan; Victoria Oberreiter; Robin N.M. Feeney; Mareike C. Stahlschmidt; Pontus Skoglund; Ron Pinhasi

doi:10.1016/j.cub.2021.06.023

Genome-scale sequencing and analysis of human, wolf, and bison DNA from 25,000-year-old sediment

Pere Gelabert, Susanna Sawyer, Anders Bergström, Ashot Margaryan, Thomas C. Collin, Tengiz Meshveliani, Anna Belfer-Cohen, David Lordkipanidze, Nino Jakeli, Zinovi Matskevich, Guy Bar-Oz, Daniel M. Fernandes, Olivia Cheronet, Kadir T. Özdoğan, Victoria Oberreiter, Robin N.M. Feeney, Mareike C. Stahlschmidt, Pontus Skoglund, Ron Pinhasi

Department of Archaeology

Research output: Contribution to journal › Article › peer-review

Abstract

Cave sediments have been shown to preserve ancient DNA but so far have not yielded the genome-scale information of skeletal remains. We retrieved and analyzed human and mammalian nuclear and mitochondrial environmental “shotgun” genomes from a single 25,000-year-old Upper Paleolithic sediment sample from Satsurblia cave, western Georgia:first, a human environmental genome with substantial basal Eurasian ancestry, which was an ancestral component of the majority of post-Ice Age people in the Near East, North Africa, and parts of Europe; second, a wolf environmental genome that is basal to extant Eurasian wolves and dogs and represents a previously unknown, likely extinct, Caucasian lineage; and third, a European bison environmental genome that is basal to present-day populations, suggesting that population structure has been substantially reshaped since the Last Glacial Maximum. Our results provide new insights into the Late Pleistocene genetic histories of these three species and demonstrate that direct shotgun sequencing of sediment DNA, without target enrichment methods, can yield genome-wide data informative of ancestry and phylogenetic relationships.

Original language	English
Pages (from-to)	3564-3574.e9
Journal	Current Biology
Volume	31
Issue number	16
DOIs	https://doi.org/10.1016/j.cub.2021.06.023
State	Published - 23 Aug 2021

Bibliographical note

Funding Information:
This study makes use of data generated by the NextGen Consortium. We acknowledge Gabriel Renaud for advice on Schmutzi and on the analysis of the mitochondrial genome. We acknowledge Spencer Sawyer, Manuela Alscher, and Odin for modern DNA. We acknowledge David Reich and Iosif Lazaridis for sharing the data of the Dzudzuana2 genome and helping us with its analysis. This work has been supported by the ?Mineralogical Preservation of the Human Biome from the Depth of Time? (MINERVA) research platform, code AGB326800, from the University of Vienna. P.S. was supported by the European Research Council (852558), a Wellcome Trust Investigator award (217223/Z/19/Z), and the Vallee Foundation. P.S. and A.B. were supported by Francis Crick Institute core funding (FC001595) from Cancer Research UK, the UK Medical Research Council, and the Wellcome Trust. This research was funded in whole, or in part, by the Wellcome Trust (FC001595). For the purpose of open access, the author has applied a CC BY public copyright license to any author accepted manuscript version arising from this submission T.C.C. was supported by the Medical Trainee PhD Scholarship, UCD. R.P. S.S. and P.G. conceived the study. A.B.-C. D.L. T.M. N.J. Z.M. and G.B.-O. provided samples. M.C.S. collected the samples. S.S. O.C. D.F. T.C.C. V.O. K.T.?. and R.N.M.F. performed the experimental work. P.G. S.S. A.B. A.M. and T.C.C. analyzed the data. P.G. S.S. A.B. R.P. and P.S. wrote the manuscript with inputs from all coauthors. The authors declare no competing interests.

Funding Information:
This study makes use of data generated by the NextGen Consortium. We acknowledge Gabriel Renaud for advice on Schmutzi and on the analysis of the mitochondrial genome. We acknowledge Spencer Sawyer, Manuela Alscher, and Odin for modern DNA. We acknowledge David Reich and Iosif Lazaridis for sharing the data of the Dzudzuana2 genome and helping us with its analysis. This work has been supported by the “Mineralogical Preservation of the Human Biome from the Depth of Time” (MINERVA) research platform, code AGB326800, from the University of Vienna. P.S. was supported by the European Research Council ( 852558 ), a Wellcome Trust Investigator award ( 217223/Z/19/Z ), and the Vallee Foundation . P.S. and A.B. were supported by Francis Crick Institute core funding ( FC001595 ) from Cancer Research UK , the UK Medical Research Council , and the Wellcome Trust . This research was funded in whole, or in part, by the Wellcome Trust ( FC001595 ). For the purpose of open access, the author has applied a CC BY public copyright license to any author accepted manuscript version arising from this submission T.C.C. was supported by the Medical Trainee PhD Scholarship, UCD .

Publisher Copyright:
© 2021 The Authors

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Keywords

Canis
Caucasus
Upper Paleolithic
bison
enviromental DNA
human
shotgun
soil sequencing

ASJC Scopus subject areas

Neuroscience (all)
Biochemistry, Genetics and Molecular Biology (all)
Agricultural and Biological Sciences (all)

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10.1016/j.cub.2021.06.023

Cite this

Gelabert, P., Sawyer, S., Bergström, A., Margaryan, A., Collin, T. C., Meshveliani, T., Belfer-Cohen, A., Lordkipanidze, D., Jakeli, N., Matskevich, Z., Bar-Oz, G., Fernandes, D. M., Cheronet, O., Özdoğan, K. T., Oberreiter, V., Feeney, R. N. M., Stahlschmidt, M. C., Skoglund, P., & Pinhasi, R. (2021). Genome-scale sequencing and analysis of human, wolf, and bison DNA from 25,000-year-old sediment. Current Biology, 31(16), 3564-3574.e9. https://doi.org/10.1016/j.cub.2021.06.023

@article{657a6db9b8bd4438bc12124e4943df50,

title = "Genome-scale sequencing and analysis of human, wolf, and bison DNA from 25,000-year-old sediment",

abstract = "Cave sediments have been shown to preserve ancient DNA but so far have not yielded the genome-scale information of skeletal remains. We retrieved and analyzed human and mammalian nuclear and mitochondrial environmental “shotgun” genomes from a single 25,000-year-old Upper Paleolithic sediment sample from Satsurblia cave, western Georgia:first, a human environmental genome with substantial basal Eurasian ancestry, which was an ancestral component of the majority of post-Ice Age people in the Near East, North Africa, and parts of Europe; second, a wolf environmental genome that is basal to extant Eurasian wolves and dogs and represents a previously unknown, likely extinct, Caucasian lineage; and third, a European bison environmental genome that is basal to present-day populations, suggesting that population structure has been substantially reshaped since the Last Glacial Maximum. Our results provide new insights into the Late Pleistocene genetic histories of these three species and demonstrate that direct shotgun sequencing of sediment DNA, without target enrichment methods, can yield genome-wide data informative of ancestry and phylogenetic relationships.",

keywords = "Canis, Caucasus, Upper Paleolithic, bison, enviromental DNA, human, shotgun, soil sequencing",

author = "Pere Gelabert and Susanna Sawyer and Anders Bergstr{\"o}m and Ashot Margaryan and Collin, {Thomas C.} and Tengiz Meshveliani and Anna Belfer-Cohen and David Lordkipanidze and Nino Jakeli and Zinovi Matskevich and Guy Bar-Oz and Fernandes, {Daniel M.} and Olivia Cheronet and {\"O}zdoğan, {Kadir T.} and Victoria Oberreiter and Feeney, {Robin N.M.} and Stahlschmidt, {Mareike C.} and Pontus Skoglund and Ron Pinhasi",

note = "Funding Information: This study makes use of data generated by the NextGen Consortium. We acknowledge Gabriel Renaud for advice on Schmutzi and on the analysis of the mitochondrial genome. We acknowledge Spencer Sawyer, Manuela Alscher, and Odin for modern DNA. We acknowledge David Reich and Iosif Lazaridis for sharing the data of the Dzudzuana2 genome and helping us with its analysis. This work has been supported by the ?Mineralogical Preservation of the Human Biome from the Depth of Time? (MINERVA) research platform, code AGB326800, from the University of Vienna. P.S. was supported by the European Research Council (852558), a Wellcome Trust Investigator award (217223/Z/19/Z), and the Vallee Foundation. P.S. and A.B. were supported by Francis Crick Institute core funding (FC001595) from Cancer Research UK, the UK Medical Research Council, and the Wellcome Trust. This research was funded in whole, or in part, by the Wellcome Trust (FC001595). For the purpose of open access, the author has applied a CC BY public copyright license to any author accepted manuscript version arising from this submission T.C.C. was supported by the Medical Trainee PhD Scholarship, UCD. R.P. S.S. and P.G. conceived the study. A.B.-C. D.L. T.M. N.J. Z.M. and G.B.-O. provided samples. M.C.S. collected the samples. S.S. O.C. D.F. T.C.C. V.O. K.T.?. and R.N.M.F. performed the experimental work. P.G. S.S. A.B. A.M. and T.C.C. analyzed the data. P.G. S.S. A.B. R.P. and P.S. wrote the manuscript with inputs from all coauthors. The authors declare no competing interests. Funding Information: This study makes use of data generated by the NextGen Consortium. We acknowledge Gabriel Renaud for advice on Schmutzi and on the analysis of the mitochondrial genome. We acknowledge Spencer Sawyer, Manuela Alscher, and Odin for modern DNA. We acknowledge David Reich and Iosif Lazaridis for sharing the data of the Dzudzuana2 genome and helping us with its analysis. This work has been supported by the “Mineralogical Preservation of the Human Biome from the Depth of Time” (MINERVA) research platform, code AGB326800, from the University of Vienna. P.S. was supported by the European Research Council ( 852558 ), a Wellcome Trust Investigator award ( 217223/Z/19/Z ), and the Vallee Foundation . P.S. and A.B. were supported by Francis Crick Institute core funding ( FC001595 ) from Cancer Research UK , the UK Medical Research Council , and the Wellcome Trust . This research was funded in whole, or in part, by the Wellcome Trust ( FC001595 ). For the purpose of open access, the author has applied a CC BY public copyright license to any author accepted manuscript version arising from this submission T.C.C. was supported by the Medical Trainee PhD Scholarship, UCD . Publisher Copyright: {\textcopyright} 2021 The Authors Copyright {\textcopyright} 2021 The Authors. Published by Elsevier Inc. All rights reserved.",

year = "2021",

month = aug,

day = "23",

doi = "10.1016/j.cub.2021.06.023",

language = "English",

volume = "31",

pages = "3564--3574.e9",

journal = "Current Biology",

issn = "0960-9822",

publisher = "Cell Press",

number = "16",

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Gelabert, P, Sawyer, S, Bergström, A, Margaryan, A, Collin, TC, Meshveliani, T, Belfer-Cohen, A, Lordkipanidze, D, Jakeli, N, Matskevich, Z, Bar-Oz, G, Fernandes, DM, Cheronet, O, Özdoğan, KT, Oberreiter, V, Feeney, RNM, Stahlschmidt, MC, Skoglund, P & Pinhasi, R 2021, 'Genome-scale sequencing and analysis of human, wolf, and bison DNA from 25,000-year-old sediment', Current Biology, vol. 31, no. 16, pp. 3564-3574.e9. https://doi.org/10.1016/j.cub.2021.06.023

TY - JOUR

T1 - Genome-scale sequencing and analysis of human, wolf, and bison DNA from 25,000-year-old sediment

AU - Gelabert, Pere

AU - Sawyer, Susanna

AU - Bergström, Anders

AU - Margaryan, Ashot

AU - Collin, Thomas C.

AU - Meshveliani, Tengiz

AU - Belfer-Cohen, Anna

AU - Lordkipanidze, David

AU - Jakeli, Nino

AU - Matskevich, Zinovi

AU - Bar-Oz, Guy

AU - Fernandes, Daniel M.

AU - Cheronet, Olivia

AU - Özdoğan, Kadir T.

AU - Oberreiter, Victoria

AU - Feeney, Robin N.M.

AU - Stahlschmidt, Mareike C.

AU - Skoglund, Pontus

AU - Pinhasi, Ron

N1 - Funding Information: This study makes use of data generated by the NextGen Consortium. We acknowledge Gabriel Renaud for advice on Schmutzi and on the analysis of the mitochondrial genome. We acknowledge Spencer Sawyer, Manuela Alscher, and Odin for modern DNA. We acknowledge David Reich and Iosif Lazaridis for sharing the data of the Dzudzuana2 genome and helping us with its analysis. This work has been supported by the ?Mineralogical Preservation of the Human Biome from the Depth of Time? (MINERVA) research platform, code AGB326800, from the University of Vienna. P.S. was supported by the European Research Council (852558), a Wellcome Trust Investigator award (217223/Z/19/Z), and the Vallee Foundation. P.S. and A.B. were supported by Francis Crick Institute core funding (FC001595) from Cancer Research UK, the UK Medical Research Council, and the Wellcome Trust. This research was funded in whole, or in part, by the Wellcome Trust (FC001595). For the purpose of open access, the author has applied a CC BY public copyright license to any author accepted manuscript version arising from this submission T.C.C. was supported by the Medical Trainee PhD Scholarship, UCD. R.P. S.S. and P.G. conceived the study. A.B.-C. D.L. T.M. N.J. Z.M. and G.B.-O. provided samples. M.C.S. collected the samples. S.S. O.C. D.F. T.C.C. V.O. K.T.?. and R.N.M.F. performed the experimental work. P.G. S.S. A.B. A.M. and T.C.C. analyzed the data. P.G. S.S. A.B. R.P. and P.S. wrote the manuscript with inputs from all coauthors. The authors declare no competing interests. Funding Information: This study makes use of data generated by the NextGen Consortium. We acknowledge Gabriel Renaud for advice on Schmutzi and on the analysis of the mitochondrial genome. We acknowledge Spencer Sawyer, Manuela Alscher, and Odin for modern DNA. We acknowledge David Reich and Iosif Lazaridis for sharing the data of the Dzudzuana2 genome and helping us with its analysis. This work has been supported by the “Mineralogical Preservation of the Human Biome from the Depth of Time” (MINERVA) research platform, code AGB326800, from the University of Vienna. P.S. was supported by the European Research Council ( 852558 ), a Wellcome Trust Investigator award ( 217223/Z/19/Z ), and the Vallee Foundation . P.S. and A.B. were supported by Francis Crick Institute core funding ( FC001595 ) from Cancer Research UK , the UK Medical Research Council , and the Wellcome Trust . This research was funded in whole, or in part, by the Wellcome Trust ( FC001595 ). For the purpose of open access, the author has applied a CC BY public copyright license to any author accepted manuscript version arising from this submission T.C.C. was supported by the Medical Trainee PhD Scholarship, UCD . Publisher Copyright: © 2021 The Authors Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

PY - 2021/8/23

Y1 - 2021/8/23

N2 - Cave sediments have been shown to preserve ancient DNA but so far have not yielded the genome-scale information of skeletal remains. We retrieved and analyzed human and mammalian nuclear and mitochondrial environmental “shotgun” genomes from a single 25,000-year-old Upper Paleolithic sediment sample from Satsurblia cave, western Georgia:first, a human environmental genome with substantial basal Eurasian ancestry, which was an ancestral component of the majority of post-Ice Age people in the Near East, North Africa, and parts of Europe; second, a wolf environmental genome that is basal to extant Eurasian wolves and dogs and represents a previously unknown, likely extinct, Caucasian lineage; and third, a European bison environmental genome that is basal to present-day populations, suggesting that population structure has been substantially reshaped since the Last Glacial Maximum. Our results provide new insights into the Late Pleistocene genetic histories of these three species and demonstrate that direct shotgun sequencing of sediment DNA, without target enrichment methods, can yield genome-wide data informative of ancestry and phylogenetic relationships.

AB - Cave sediments have been shown to preserve ancient DNA but so far have not yielded the genome-scale information of skeletal remains. We retrieved and analyzed human and mammalian nuclear and mitochondrial environmental “shotgun” genomes from a single 25,000-year-old Upper Paleolithic sediment sample from Satsurblia cave, western Georgia:first, a human environmental genome with substantial basal Eurasian ancestry, which was an ancestral component of the majority of post-Ice Age people in the Near East, North Africa, and parts of Europe; second, a wolf environmental genome that is basal to extant Eurasian wolves and dogs and represents a previously unknown, likely extinct, Caucasian lineage; and third, a European bison environmental genome that is basal to present-day populations, suggesting that population structure has been substantially reshaped since the Last Glacial Maximum. Our results provide new insights into the Late Pleistocene genetic histories of these three species and demonstrate that direct shotgun sequencing of sediment DNA, without target enrichment methods, can yield genome-wide data informative of ancestry and phylogenetic relationships.

KW - Canis

KW - Caucasus

KW - Upper Paleolithic

KW - bison

KW - enviromental DNA

KW - human

KW - shotgun

KW - soil sequencing

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U2 - 10.1016/j.cub.2021.06.023

DO - 10.1016/j.cub.2021.06.023

M3 - Article

C2 - 34256019

AN - SCOPUS:85111696181

SN - 0960-9822

VL - 31

SP - 3564-3574.e9

JO - Current Biology

JF - Current Biology

IS - 16

ER -

Genome-scale sequencing and analysis of human, wolf, and bison DNA from 25,000-year-old sediment

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Bibliographical note

Keywords

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