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Research Article

Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis

Yujun Cui, Chang Yu, Yanfeng Yan, Dongfang Li, Yanjun Li, Thibaut Jombart, Lucy A. Weinert, Zuyun Wang, Zhaobiao Guo, Lizhi Xu, Yujiang Zhang, Hancheng Zheng, Nan Qin, Xiao Xiao, Mingshou Wu, Xiaoyi Wang, Dongsheng Zhou, Zhizhen Qi, Zongmin Du, Honglong Wu, Xianwei Yang, Hongzhi Cao, Hu Wang, Jing Wang, Shusen Yao, Alexander Rakin, Yingrui Li, Daniel Falush, Francois Balloux, Mark Achtman, Yajun Song, Jun Wang, and Ruifu Yang
  1. aState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China;
  2. bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
  3. cMedical Research Council Centre for Outbreak Analysis and Modelling, Department of Infectious Disease Epidemiology, Imperial College, London W2 1PG, United Kingdom;
  4. dUniversity College London Genetics Institute, Department of Genetics Evolution and Environment, University College London, London WC1E 6BT, United Kingdom;
  5. eQinghai Institute for Endemic Diseases Prevention and Control, Xining 811602, Qinghai Province, China;
  6. fXinjiang Center for Disease Control and Prevention, Urumiqi 830002, Xijiang province, China;
  7. gYunnan Institute for Epidemic Diseases Control and Research, Dali 671000, Yunnan Province, China;
  8. hInstitute of Health Quarantine, Chinese Academy of Inspection and Quarantine, Beijing 100025, China;
  9. iMilitary Center for Disease Control and Prevention, Beijing 100850, China;
  10. jMax von Pettenkofer Institute, Ludwig-Maximilians-University, Munich 80336, Germany; and
  11. kEnvironmental Research Institute, University College Cork, Cork, Ireland

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PNAS January 8, 2013 110 (2) 577-582; https://doi.org/10.1073/pnas.1205750110
Yujun Cui
aState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China;
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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Chang Yu
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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Yanfeng Yan
aState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China;
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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Dongfang Li
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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Yanjun Li
aState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China;
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Thibaut Jombart
cMedical Research Council Centre for Outbreak Analysis and Modelling, Department of Infectious Disease Epidemiology, Imperial College, London W2 1PG, United Kingdom;
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Lucy A. Weinert
dUniversity College London Genetics Institute, Department of Genetics Evolution and Environment, University College London, London WC1E 6BT, United Kingdom;
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Zuyun Wang
eQinghai Institute for Endemic Diseases Prevention and Control, Xining 811602, Qinghai Province, China;
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Zhaobiao Guo
aState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China;
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Lizhi Xu
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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Yujiang Zhang
fXinjiang Center for Disease Control and Prevention, Urumiqi 830002, Xijiang province, China;
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Hancheng Zheng
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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Nan Qin
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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Xiao Xiao
aState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China;
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Mingshou Wu
gYunnan Institute for Epidemic Diseases Control and Research, Dali 671000, Yunnan Province, China;
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Xiaoyi Wang
aState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China;
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Dongsheng Zhou
aState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China;
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Zhizhen Qi
eQinghai Institute for Endemic Diseases Prevention and Control, Xining 811602, Qinghai Province, China;
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Zongmin Du
aState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China;
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Honglong Wu
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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Xianwei Yang
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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Hongzhi Cao
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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Hu Wang
eQinghai Institute for Endemic Diseases Prevention and Control, Xining 811602, Qinghai Province, China;
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Jing Wang
hInstitute of Health Quarantine, Chinese Academy of Inspection and Quarantine, Beijing 100025, China;
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Shusen Yao
iMilitary Center for Disease Control and Prevention, Beijing 100850, China;
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Alexander Rakin
jMax von Pettenkofer Institute, Ludwig-Maximilians-University, Munich 80336, Germany; and
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Yingrui Li
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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Daniel Falush
kEnvironmental Research Institute, University College Cork, Cork, Ireland
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Francois Balloux
dUniversity College London Genetics Institute, Department of Genetics Evolution and Environment, University College London, London WC1E 6BT, United Kingdom;
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  • For correspondence: f.balloux@ucl.ac.uk m.achtman@ucc.ie songyajun88@gmail.com wangj@genomics.org.cn ruifuyang@gmail.com
Mark Achtman
kEnvironmental Research Institute, University College Cork, Cork, Ireland
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  • For correspondence: f.balloux@ucl.ac.uk m.achtman@ucc.ie songyajun88@gmail.com wangj@genomics.org.cn ruifuyang@gmail.com
Yajun Song
aState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China;
kEnvironmental Research Institute, University College Cork, Cork, Ireland
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  • For correspondence: f.balloux@ucl.ac.uk m.achtman@ucc.ie songyajun88@gmail.com wangj@genomics.org.cn ruifuyang@gmail.com
Jun Wang
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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  • For correspondence: f.balloux@ucl.ac.uk m.achtman@ucc.ie songyajun88@gmail.com wangj@genomics.org.cn ruifuyang@gmail.com
Ruifu Yang
aState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China;
bBeijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
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  • For correspondence: f.balloux@ucl.ac.uk m.achtman@ucc.ie songyajun88@gmail.com wangj@genomics.org.cn ruifuyang@gmail.com
  1. Edited* by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved November 29, 2012 (received for review April 10, 2012)

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Abstract

The genetic diversity of Yersinia pestis, the etiologic agent of plague, is extremely limited because of its recent origin coupled with a slow clock rate. Here we identified 2,326 SNPs from 133 genomes of Y. pestis strains that were isolated in China and elsewhere. These SNPs define the genealogy of Y. pestis since its most recent common ancestor. All but 28 of these SNPs represented mutations that happened only once within the genealogy, and they were distributed essentially at random among individual genes. Only seven genes contained a significant excess of nonsynonymous SNP, suggesting that the fixation of SNPs mainly arises via neutral processes, such as genetic drift, rather than Darwinian selection. However, the rate of fixation varies dramatically over the genealogy: the number of SNPs accumulated by different lineages was highly variable and the genealogy contains multiple polytomies, one of which resulted in four branches near the time of the Black Death. We suggest that demographic changes can affect the speed of evolution in epidemic pathogens even in the absence of natural selection, and hypothesize that neutral SNPs are fixed rapidly during intermittent epidemics and outbreaks.

  • infectious disease
  • molecular clock
  • phylogenomics
  • NGS
  • molecular epidemiology

Footnotes

  • ↵1Y.C., C.Y., Y.Y., D.L., Yanjun Li, T.J., and L.A.W. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. E-mail: f.balloux{at}ucl.ac.uk, m.achtman{at}ucc.ie, songyajun88{at}gmail.com, wangj{at}genomics.org.cn, or ruifuyang{at}gmail.com.
  • Author contributions: Y.C., Y.S., Jun Wang, and R.Y. designed research; Y.C., Yanjun Li, Z.G., X.X., X.W., D.Z., and Z.D. performed research; T.J., Z.W., Y.Z., N.Q., M.W., Z.Q., H. Wang, Jing Wang, S.Y., and A.R. contributed new reagents/analytic tools; Y.C., C.Y., Y.Y., D.L., T.J., L.A.W., L.X., H.Z., H. Wu, X.Y., H.C., Yingrui Li, D.F., F.B., M.A., Y.S., and R.Y. analyzed data; and Y.C., T.J., L.A.W., D.F., F.B., M.A., Y.S., and R.Y. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • Data deposition: Raw genome data have been deposited in the National Center for Biotechnology Information/Short Read archive database, www.ncbi.nlm.nih.gov/sra (accession no SRA010790; individual genome assemblies have been deposited under accession nos. ADOV00000000 47685–ADTI00000000 47685). The accession numbers for each strain are listed in Dataset S1.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1205750110/-/DCSupplemental.

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Phylogenomic analysis of Y. pestis
Yujun Cui, Chang Yu, Yanfeng Yan, Dongfang Li, Yanjun Li, Thibaut Jombart, Lucy A. Weinert, Zuyun Wang, Zhaobiao Guo, Lizhi Xu, Yujiang Zhang, Hancheng Zheng, Nan Qin, Xiao Xiao, Mingshou Wu, Xiaoyi Wang, Dongsheng Zhou, Zhizhen Qi, Zongmin Du, Honglong Wu, Xianwei Yang, Hongzhi Cao, Hu Wang, Jing Wang, Shusen Yao, Alexander Rakin, Yingrui Li, Daniel Falush, Francois Balloux, Mark Achtman, Yajun Song, Jun Wang, Ruifu Yang
Proceedings of the National Academy of Sciences Jan 2013, 110 (2) 577-582; DOI: 10.1073/pnas.1205750110

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Phylogenomic analysis of Y. pestis
Yujun Cui, Chang Yu, Yanfeng Yan, Dongfang Li, Yanjun Li, Thibaut Jombart, Lucy A. Weinert, Zuyun Wang, Zhaobiao Guo, Lizhi Xu, Yujiang Zhang, Hancheng Zheng, Nan Qin, Xiao Xiao, Mingshou Wu, Xiaoyi Wang, Dongsheng Zhou, Zhizhen Qi, Zongmin Du, Honglong Wu, Xianwei Yang, Hongzhi Cao, Hu Wang, Jing Wang, Shusen Yao, Alexander Rakin, Yingrui Li, Daniel Falush, Francois Balloux, Mark Achtman, Yajun Song, Jun Wang, Ruifu Yang
Proceedings of the National Academy of Sciences Jan 2013, 110 (2) 577-582; DOI: 10.1073/pnas.1205750110
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