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Research Article

Ancient bacteria show evidence of DNA repair

Sarah Stewart Johnson, Martin B. Hebsgaard, Torben R. Christensen, Mikhail Mastepanov, Rasmus Nielsen, Kasper Munch, Tina Brand, M. Thomas P. Gilbert, Maria T. Zuber, Michael Bunce, Regin Rønn, David Gilichinsky, Duane Froese, and Eske Willerslev
  1. *Department of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, 77 Massachusetts Avenue, 54-810, Cambridge, MA 02139;
  2. †Centre for Ancient Genetics and Centre for Comparative Genomics, Institute of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark;
  3. ‡GeoBiosphere Science Centre, Lund University, Sölvegatan 12, Lund, 22362 Sweden;
  4. §Ancient DNA Research Laboratory, Murdoch University, Perth, WA 6150, Australia;
  5. ¶Soil Cryology Laboratory, Institute of Physicochemical and Biological Problems in Soil Science, Russian Academy of Sciences, Pushchino, Russia; and
  6. ‖Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB, Canada T6G283

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PNAS September 4, 2007 104 (36) 14401-14405; https://doi.org/10.1073/pnas.0706787104
Sarah Stewart Johnson
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Martin B. Hebsgaard
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Torben R. Christensen
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Mikhail Mastepanov
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Rasmus Nielsen
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Kasper Munch
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Tina Brand
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M. Thomas P. Gilbert
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Maria T. Zuber
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Michael Bunce
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Regin Rønn
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David Gilichinsky
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Duane Froese
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Eske Willerslev
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  • For correspondence: ewillerslev@bi.ku.dk
  1. Communicated by P. Buford Price, University of California, Berkeley, CA, July 25, 2007 (received for review June 14, 2007)

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Abstract

Recent claims of cultivable ancient bacteria within sealed environments highlight our limited understanding of the mechanisms behind long-term cell survival. It remains unclear how dormancy, a favored explanation for extended cellular persistence, can cope with spontaneous genomic decay over geological timescales. There has been no direct evidence in ancient microbes for the most likely mechanism, active DNA repair, or for the metabolic activity necessary to sustain it. In this paper, we couple PCR and enzymatic treatment of DNA with direct respiration measurements to investigate long-term survival of bacteria sealed in frozen conditions for up to one million years. Our results show evidence of bacterial survival in samples up to half a million years in age, making this the oldest independently authenticated DNA to date obtained from viable cells. Additionally, we find strong evidence that this long-term survival is closely tied to cellular metabolic activity and DNA repair that over time proves to be superior to dormancy as a mechanism in sustaining bacteria viability.

  • DNA damage
  • long-term microbial survival
  • metabolic activity

Footnotes

  • **To whom correspondence should be addressed. E-mail: ewillerslev{at}bi.ku.dk
  • Author contributions: S.S.J., T.R.C., R.R., and E.W. designed research; S.S.J., M.B.H., T.R.C., M.M., T.B., M.T.P.G., and M.B. performed research; S.S.J., M.B.H., M.M., R.N., and K.M. analyzed data; and S.S.J., M.T.Z., R.R., D.G., D.F., and E.W. wrote the paper.

  • The authors declare no conflict of interest.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. EV083531–EV083798).

  • ↵ †† Stone, J., Sletten, R. S., Hallet, B., Caffee, M. (2000) EOS Trans Am Geophys Union, Fall 2000 meeting supplement.

  • Abbreviations:
    Kyr,
    thousand years;
    UNG,
    uracil-N-glycosylase.
  • Freely available online through the PNAS open access option.

  • © 2007 by The National Academy of Sciences of the USA
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Ancient bacteria show evidence of DNA repair
Sarah Stewart Johnson, Martin B. Hebsgaard, Torben R. Christensen, Mikhail Mastepanov, Rasmus Nielsen, Kasper Munch, Tina Brand, M. Thomas P. Gilbert, Maria T. Zuber, Michael Bunce, Regin Rønn, David Gilichinsky, Duane Froese, Eske Willerslev
Proceedings of the National Academy of Sciences Sep 2007, 104 (36) 14401-14405; DOI: 10.1073/pnas.0706787104

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Ancient bacteria show evidence of DNA repair
Sarah Stewart Johnson, Martin B. Hebsgaard, Torben R. Christensen, Mikhail Mastepanov, Rasmus Nielsen, Kasper Munch, Tina Brand, M. Thomas P. Gilbert, Maria T. Zuber, Michael Bunce, Regin Rønn, David Gilichinsky, Duane Froese, Eske Willerslev
Proceedings of the National Academy of Sciences Sep 2007, 104 (36) 14401-14405; DOI: 10.1073/pnas.0706787104
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Proceedings of the National Academy of Sciences: 104 (36)
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