Ancient bacteria show evidence of DNA repair
Open accessAbstract
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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Research into mechanisms bacteria use for self-preservation during sub-optimal environmental conditions provides supporting evidence for long-term preservation and stability of DNA in bacterial pathogens.
“however research into the mechanisms bacteria use for self preservation during periods of sub-optimal environmental conditions has provided supporting evidence for the long term preservation [26] and stability of DNA in bacterial pathogens.”
From Molecular Exploration of the First-Century Tomb of the Shroud in Akeldama, Jerusalem (2009) · cites this paper as [26]
Cites
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.22.4673 · Cited by 64,617 · see citing works
MRBAYES: Bayesian inference of phylogenetic trees.
Huelsenbeck, J. P., & Ronquist, F. (2001) · Bioinformatics · doi:10.1093/bioinformatics/17.8.754 · Cited by 21,937 · see citing works
Instability and decay of the primary structure of DNA
Lindahl, T. (1993) · Nature · doi:10.1038/362709a0 · Cited by 5,679 · see citing works
Resistance ofBacillusEndospores to Extreme Terrestrial and Extraterrestrial Environments
Nicholson, W. L., Munakata, N., Horneck, G., Melosh, H. J., & Setlow, P. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.3.548-572.2000 · Cited by 2,041 · see citing works
Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification.
Pääbo, S. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.6.1939 · Cited by 1,011 · see citing works
Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal
Vreeland, R. H., Rosenzweig, W. D., & Powers, D. W. (2000) · Nature · doi:10.1038/35038060 · Cited by 828 · see citing works
Temperature dependence of metabolic rates for microbial growth, maintenance, and survival
Price, P. B., & Sowers, T. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400522101 · Cited by 819 · see citing works
Willerslev, E., & Cooper, A. (2005) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2004.2813 · Cited by 712 · see citing works
Self-citationDiverse Plant and Animal Genetic Records from Holocene and Pleistocene Sediments
Willerslev, E., Hansen, A. J., Binladen, J., Brand, T. B., Gilbert, M. T. P., Shapiro, B., Bunce, M., Wiuf, C., Gilichinsky, D. A., & Cooper, A. (2003) · Science · doi:10.1126/science.1084114 · Cited by 687 · see citing works
Self-citationHofreiter, M. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.23.4793 · Cited by 684 · see citing works
Revival and identification of bacterial spores in 25- to 40-million-year-old Dominican amber
Cano, R. J., & Borucki, M. K. (1995) · Science · doi:10.1126/science.7538699 · Cited by 641 · see citing works
Metabolic Activity of Permafrost Bacteria below the Freezing Point
Rivkina, E., Friedmann, E. I., McKay, C. P., & Gilichinsky, D. A. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.8.3230-3233.2000 · Cited by 585 · see citing works
Self-citationTotal bacterial diversity in soil and sediment communities—A review
Torsvik, V. L., Sørheim, R., & Goksøyr, J. (1996) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/bf01574690 · Cited by 513 · see citing works
DNA Damage and DNA Sequence Retrieval from Ancient Tissues
Höss, M., Jaruga, P., Zastawny, T. H., Dizdaroğlu, M., & Pääbo, S. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.7.1304 · Cited by 403 · see citing works
Amino Acid Racemization and the Preservation of Ancient DNA
Poinar, H. N., Höss, M., Bada, J. L., & Pääbo, S. (1996) · Science · doi:10.1126/science.272.5263.864 · Cited by 392 · see citing works
Isolation of nucleic acids and cultures from fossil ice and permafrost
Willerslev, E., Hansen, A. J., & Poinar, H. N. (2003) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2003.11.010 · Cited by 279 · see citing works
Self-citationRates of Evolution in Ancient DNA from Adelie Penguins
Lambert, D. M., Ritchie, P. A., Millar, C. D., Holland, B. R., Drummond, A. J., & Baroni, C. D. (2002) · Science · doi:10.1126/science.1068105 · Cited by 276 · see citing works
Preservation of Miocene glacier ice in East Antarctica
Sugden, D. E., Marchant, D. R., Potter, N. L., Souchez, R. A., Denton, G. H., Swisher, C. C., & Tison, J. (1995) · Nature · doi:10.1038/376412a0 · Cited by 261 · see citing works
Gilichinsky, D. A., Wilson, G. S., Friedmann, E. I., McKay, C. P., Sletten, R. S., Rivkina, E., Vishnivetskaya, T. A., Erokhina, L. G., Ivanushkina, N. E., Kochkina, G. A., et al. (2007) · Astrobiology · doi:10.1089/ast.2006.0012 · Cited by 260 · see citing works
Self-citationMicrobial activity in soils frozen to below −39 °C
Panikov, N. S., Flanagan, P. W., Oechel, W. C., Mastepanov, M., & Christensen, T. R. (2005) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2005.07.004 · Cited by 259 · see citing works
Self-citationThe deep cold biosphere: facts and hypothesis
Vorobyova, E. A., Soina, V. S., Mv, G., Minkovskaya, N., Zalinova, N., Mamukelashvili, A. G., Gilichinsky, D. A., Rivkina, E., & Vishnivetskaya, T. A. (1997) · FEMS Microbiology Reviews · doi:10.1016/s0168-6445(97)00047-8 · Cited by 254 · see citing works
Self-citationCharacterization of Genetic Miscoding Lesions Caused by Postmortem Damage
Gilbert, M. T. P., Hansen, A. J., Willerslev, E., Rudbeck, L., Barnes, I., Lynnerup, N., & Cooper, A. (2003) · The American Journal of Human Genetics · doi:10.1086/345379 · Cited by 248 · see citing works
Self-citationLong-term persistence of bacterial DNA
Willerslev, E., Hansen, A. J., Rønn, R., Brand, T. B., Barnes, I., Wiuf, C., Gilichinsky, D., Mitchell, D., & Cooper, A. (2004) · Current Biology · doi:10.1016/j.cub.2003.12.012 · Cited by 232 · see citing works
Self-citationReproduction and metabolism at − 10°C of bacteria isolated from Siberian permafrost
Bakermans, C., Tsapin, A. I., Souza‐Egipsy, V., Gilichinsky, D. A., & Nealson, K. H. (2003) · Environmental Microbiology · doi:10.1046/j.1462-2920.2003.00419.x · Cited by 217 · see citing works
Self-citationPreservation records of micro-organisms: evidence of the tenacity of life
Kennedy, M., Reader, S. L., & Swierczynski, L. M. (1994) · Microbiology · doi:10.1099/00221287-140-10-2513 · Cited by 211 · see citing works
Statistical Evidence for Miscoding Lesions in Ancient DNA Templates
Hansen, A. J., Willerslev, E., Wiuf, C., Mourier, T., & Arctander, P. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003800 · Cited by 180 · see citing works
Self-citationVishnivetskaya, T. A., Ma, P., Urbance, J. W., Ponder, M. A., Moyer, C. L., Gilichinsky, D. A., & Tiedje, J. M. (2006) · Astrobiology · doi:10.1089/ast.2006.6.400 · Cited by 167 · see citing works
Self-citationNot just old but old and cold?
Smith, C. I., Chamberlain, A. T., Riley, M. S., Cooper, A., Stringer, C. B., & Collins, M. J. (2001) · Nature · doi:10.1038/35071177 · Cited by 160 · see citing works
Geologically ancient DNA: fact or artefact?
Hebsgaard, M. B., Phillips, M. J., & Willerslev, E. (2005) · Trends in Microbiology · doi:10.1016/j.tim.2005.03.010 · Cited by 160 · see citing works
Self-citationRivkina, E., Laurinavichius, K. S., McGrath, J., Tiedje, J. M., Shcherbakova, V. A., & Gilichinsky, D. A. (2004) · Advances in Space Research · doi:10.1016/j.asr.2003.06.024 · Cited by 157 · see citing works
Self-citationMicrobial origin of excess methane in glacial ice and implications for life on Mars
Tung, H. C., Bramall, N. E., & Price, P. B. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507601102 · Cited by 150 · see citing works
Recovery of 16S ribosomal RNA gene fragments from ancient halite
Fish, S., Shepherd, T. J., McGenity, T. J., & Grant, W. D. (2002) · Nature · doi:10.1038/417432a · Cited by 139 · see citing works
Crosslinks Rather Than Strand Breaks Determine Access to Ancient DNA Sequences From Frozen Sediments
Hansen, A. J., Mitchell, D. L., Wiuf, C., Paniker, L., Brand, T. B., Binladen, J., Gilichinsky, D. A., Rønn, R., & Willerslev, E. (2006) · Genetics · doi:10.1534/genetics.106.057349 · Cited by 129 · see citing works
Self-citationAssessing the Fidelity of Ancient DNA Sequences Amplified From Nuclear Genes
Binladen, J., Wiuf, C., Gilbert, M. T. P., Bunce, M., Barnett, R., Larson, G., Greenwood, A. D., Haile, J., Ho, S. Y. W., Hansen, A. J., et al. (2005) · Genetics · doi:10.1534/genetics.105.049718 · Cited by 119 · see citing works
Self-citationDiversity of Holocene life forms in fossil glacier ice
Willerslev, E., Hansen, A. J., Christensen, B. T., Steffensen, J. P., & Arctander, P. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.14.8017 · Cited by 116 · see citing works
Self-citationSuperselective clay for radium uptake
Komarneni, S., Kozai, N., & Paulus, W. J. (2001) · Nature · doi:10.1038/35071173 · Cited by 111 · see citing works
The oldest ice on Earth in Beacon Valley, Antarctica: new evidence from surface exposure dating
Schäfer, J. M., Heinrich Baur, A., Denton, G. H., Ivy-Ochs, S. D., Marchant, D. R., Schlüchter, C., & WIELER, R. (2000) · Earth and Planetary Science Letters · doi:10.1016/s0012-821x(00)00095-9 · Cited by 101 · see citing works
Eschbach, M., Möbitz, H., Rompf, A., & Jahn, D. (2003) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(03)00383-5 · Cited by 82 · see citing works
Fast-growing till over ancient ice in Beacon Valley, Antarctica
Ng, F., Hallet, B., Sletten, R. S., & Stone, J. O. H. (2005) · Geology · doi:10.1130/g21064.1 · Cited by 59 · see citing works
Preparation of a Methylated DNA Standard, and Its Stability on Storage
Osborne, M. R., & Phillips, D. H. (2000) · Chemical Research in Toxicology · doi:10.1021/tx990182e · Cited by 37 · see citing works
Rowley (2002) · doi:10.1130/0016-7606(2002)114
Flagged first, then by citations
1 of the 42 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Environmental DNA – An emerging tool in conservation for monitoring past and present biodiversity
Thomsen, P. F., & Willerslev, E. (2015) · Biological Conservation · doi:10.1016/j.biocon.2014.11.019 · Cited by 2,082 · see citing works
Self-citationMicrobial seed banks: the ecological and evolutionary implications of dormancy
Lennon, J. T., & Jones, S. E. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2504 · Cited by 1,872 · see citing works
Bacteria and archaea on Earth and their abundance in biofilms
Flemming, H.-C., & Wuertz, S. (2019) · Nature Reviews Microbiology · doi:10.1038/s41579-019-0158-9 · Cited by 1,729 · see citing works
Microbial life under extreme energy limitation
Hoehler, T. M., & Jørgensen, B. B. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro2939 · Cited by 784 · see citing works
Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw
Mackelprang, R., Waldrop, M. P., DeAngelis, K. M., David, M. M., Chavarría, K. L., Blazewicz, S. J., Rubin, E. M., & Jansson, J. K. (2011) · Nature · doi:10.1038/nature10576 · Cited by 713 · see citing works
Some like it cold: understanding the survival strategies of psychrophiles
Maayer, P. D., Anderson, D. E., Cary, S. C., & Cowan, D. A. (2014) · EMBO Reports · doi:10.1002/embr.201338170 · Cited by 572 · see citing works
Permafrost carbon emissions in a changing Arctic
Miner, K. R., Turetsky, M. R., Malina, E., Bartsch, A., Tamminen, J., McGUIRE, A. D., Fix, A. R., Sweeney, C., Elder, C. D., & Miller, C. E. (2022) · Nature Reviews Earth & Environment · doi:10.1038/s43017-021-00230-3 · Cited by 544 · see citing works
Diversity and ecology of psychrophilic microorganisms
Margesin, R., & Miteva, V. (2011) · Research in Microbiology · doi:10.1016/j.resmic.2010.12.004 · Cited by 518 · see citing works
The microbial ecology of permafrost
Jansson, J. K., & Taş, N. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3262 · Cited by 485 · see citing works
Life under extreme energy limitation: a synthesis of laboratory- and field-based investigations
Lever, M. A., Rogers, K. L., Lloyd, K. G., Overmann, J., Schink, B., Thauer, R. K., Hoehler, T. M., & Jørgensen, B. B. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv020 · Cited by 378 · see citing works
Protein stability and enzyme activity at extreme biological temperatures
Feller, G. (2010) · Journal of Physics Condensed Matter · doi:10.1088/0953-8984/22/32/323101 · Cited by 338 · see citing works
Ancient DNA reveals late survival of mammoth and horse in interior Alaska
Haile, J., FROESE, D. G., MacPhee, R. D. E., Roberts, R. G., Arnold, L. J., Reyes, A. V., Rasmussen, M. A., Nielsen, R., Brook, B. W., Robinson, S., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912510106 · Cited by 313 · see citing works
Self-citationYergeau, É., Hogues, H., Whyte, L. G., & Greer, C. W. (2010) · The ISME Journal · doi:10.1038/ismej.2010.41 · Cited by 306 · see citing works
The generation and maintenance of diversity in microbial communities
Fierer, N., & Lennon, J. T. (2011) · American Journal of Botany · doi:10.3732/ajb.1000498 · Cited by 290 · see citing works
Zhou, H., Zhang, D., Jiang, Z., Sun, P., Xiao, H., Wu, Y., & Chen, J. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.09.336 · Cited by 258 · see citing works
Warinner, C., Speller, C., & Collins, M. J. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0376 · Cited by 256 · see citing works
Protein oxidation: key to bacterial desiccation resistance?
Fredrickson, J. K., Li, S.-M. W., Gaidamakova, E. K., Matrosova, V. Y., Zhai, M., Sulloway, H. M., Scholten, J. C. M., Brown, M. G., Balkwill, D. L., & Daly, M. J. (2008) · The ISME Journal · doi:10.1038/ismej.2007.116 · Cited by 248 · see citing works
Emergent biogeochemical risks from Arctic permafrost degradation
Miner, K. R., D’Andrilli, J., Mackelprang, R., Edwards, A., Malaska, M. J., Waldrop, M. P., & Miller, C. E. (2021) · Nature Climate Change · doi:10.1038/s41558-021-01162-y · Cited by 212 · see citing works
Corinaldesi, C., Beolchini, F., & Dell’Anno, A. (2008) · Molecular Ecology · doi:10.1111/j.1365-294x.2008.03880.x · Cited by 210 · see citing works
Jørgensen, T., Haile, J., Möller, P., ANDREEV, A. A., Boessenkool, S., Rasmussen, M. A., Kienast, F., Coissac, É., Taberlet, P., Brochmann, C., et al. (2011) · Molecular Ecology · doi:10.1111/j.1365-294x.2011.05287.x · Cited by 205 · see citing works
Self-citationSlow Microbial Life in the Seabed
Jørgensen, B. B., & Marshall, I. P. G. (2015) · Annual Review of Marine Science · doi:10.1146/annurev-marine-010814-015535 · Cited by 189 · see citing works
Evolution of the plankton paleome in the Black Sea from the Deglacial to Anthropocene
Coolen, M. J. L., Orsi, W. D., Balkema, C., Quince, C., Harris, K. J., Sylva, S. P., Filipova-Marinova, M. V., & Giosan, L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219283110 · Cited by 183 · see citing works
Microbial communities in fluid inclusions and long-term survival in halite
Lowenstein, T. K., Schubert, B. A., & Timofeeff, M. N. (2010) · GSA Today · doi:10.1130/gsatg81a.1 · Cited by 180 · see citing works
Wilhelm, R. C., Niederberger, T. D., Greer, C. W., & Whyte, L. G. (2011) · Canadian Journal of Microbiology · doi:10.1139/w11-004 · Cited by 173 · see citing works
Aüllo, T., Ranchou‐Peyruse, A., Ollivier, B., & Magot, M. (2013) · Frontiers in Microbiology · doi:10.3389/fmicb.2013.00362 · Cited by 164 · see citing works
Energy use efficiency of soil microorganisms: Driven by carbon recycling and reduction
Wang, C., & Kuzyakov, Y. V. (2023) · Global Change Biology · doi:10.1111/gcb.16925 · Cited by 161 · see citing works
Distinct microbial communities associated with buried soils in the Siberian tundra
Gittel, A., Bárta, J., Kohoutová, I., Mikutta, R., Owens, S. M., Gilbert, J. A., Schnecker, J., Wild, B., Hannisdal, B., Maerz, J., et al. (2013) · The ISME Journal · doi:10.1038/ismej.2013.219 · Cited by 152 · see citing works
The Geobacillus paradox: why is a thermophilic bacterial genus so prevalent on a mesophilic planet?
Zeigler, D. R. (2013) · Microbiology · doi:10.1099/mic.0.071696-0 · Cited by 143 · see citing works
Deep subseafloor microbial cells on physiological standby
Jørgensen, B. B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1115421108 · Cited by 141 · see citing works
Shifts of tundra bacterial and archaeal communities along a permafrost thaw gradient in A laska
Deng, J., Gu, Y., Zhang, J., Xue, K., Qin, Y., Yuan, M., Yin, H., He, Z., Wu, L., Schuur, E. A. G., et al. (2014) · Molecular Ecology · doi:10.1111/mec.13015 · Cited by 130 · see citing works
Wang, X., Zhang, Z., Yu, Z., Shen, G., Cheng, H., & Tao, S. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.141358 · Cited by 128 · see citing works
The Icebreaker Life Mission to Mars: A Search for Biomolecular Evidence for Life
McKay, C. P., Stoker, C. R., Glass, B., Dave, A. I., Dávila, A. F., Heldmann, J. L., Marinova, M. M., Fairén, A. G., Quinn, R. C., Zacny, K. A., et al. (2013) · Astrobiology · doi:10.1089/ast.2012.0878 · Cited by 122 · see citing works
Burkert, A., Douglas, T. A., Waldrop, M. P., & Mackelprang, R. (2019) · Applied and Environmental Microbiology · doi:10.1128/aem.02646-18 · Cited by 121 · see citing works
Bacterial genome replication at subzero temperatures in permafrost
Tuorto, S. J., Darias, P., McGuinness, L. R., Panikov, N. S., Zhang, T., Häggblom, M. M., & Kerkhof, L. J. (2013) · The ISME Journal · doi:10.1038/ismej.2013.140 · Cited by 117 · see citing works
Using palaeoenvironmental DNA to reconstruct past environments: progress and prospects
Rawlence, N. J., Lowe, D. J., Wood, J. R., Young, J. M., Churchman, G. J., Huang, D. Y., & Cooper, A. (2014) · Journal of Quaternary Science · doi:10.1002/jqs.2740 · Cited by 116 · see citing works
Schostag, M. D., Stibal, M., Jacobsen, C. S., Bælum, J., Taş, N., Elberling, B., Jansson, J. K., Semenchuk, P. R., & Priemé, A. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00399 · Cited by 116 · see citing works
Miteva, V. I., Teacher, C. E., Sowers, T., & Brenchley, J. E. (2008) · Environmental Microbiology · doi:10.1111/j.1462-2920.2008.01835.x · Cited by 110 · see citing works
Buried Alive: Microbes from Ancient Halite
Jaakkola, S., Ravantti, J., Oksanen, H. M., & Bamford, D. H. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2015.12.002 · Cited by 109 · see citing works
Evolution with a seed bank: The population genetic consequences of microbial dormancy
Shoemaker, W. R., & Lennon, J. T. (2017) · Evolutionary Applications · doi:10.1111/eva.12557 · Cited by 110 · see citing works
Collapse of the mammoth-steppe in central Yukon as revealed by ancient environmental DNA
Murchie, T. J., Monteath, A., Mahony, M. E., Long, G. S., Cocker, S. L., Sadoway, T. R., Karpinski, E., Zazula, G. D., MacPhee, R. D. E., FROESE, D. G., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-27439-6 · Cited by 104 · see citing works
Self-citationBergholz, P. W., Bakermans, C., & Tiedje, J. M. (2009) · Journal of Bacteriology · doi:10.1128/jb.01377-08 · Cited by 105 · see citing works
Actinobacteria of the Extremobiosphere
Bull, A. T. (2010) · Springer eBooks · doi:10.1007/978-4-431-53898-1_58 · Cited by 106 · see citing works
Stroes-Gascoyne, S., Hamon, C. J., Maak, P., & Russell, S. B. (2008) · Applied Clay Science · doi:10.1016/j.clay.2008.06.010 · Cited by 104 · see citing works
Microbial communities associated with Antarctic snow pack and their biogeochemical implications
Antony, R., Sanyal, A., Kapse, N. G., Dhakephalkar, P. K., Thamban, M., & Nair, S. (2016) · Microbiological Research · doi:10.1016/j.micres.2016.07.004 · Cited by 99 · see citing works
Zhang, H., & Fu, G. (2020) · Land Degradation and Development · doi:10.1002/ldr.3835 · Cited by 99 · see citing works
New developments in ancient genomics
Millar, C. D., Huynen, L., Subramanian, S., Mohandesan, E., & Lambert, D. M. (2008) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2008.04.002 · Cited by 95 · see citing works
Vuillemin, A., Horn, F., Alawi, M., Henny, C., Wagner, D., Crowe, S. A., & Kallmeyer, J. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01440 · Cited by 96 · see citing works
Stomeo, F., Makhalanyane, T. P., Valverde, Á., Pointing, S. B., Stevens, M. I., Cary, S. C., Tuffin, M. I., & Cowan, D. A. (2012) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2012.01360.x · Cited by 88 · see citing works
de Rezende, J. R., Kjeldsen, K. U., Hubert, C. R. J., Finster, K. W., Loy, A., & Jørgensen, B. B. (2012) · The ISME Journal · doi:10.1038/ismej.2012.83 · Cited by 89 · see citing works
Piette, F., D’Amico, S., Mazzucchelli, G., Danchin, A., Leprince, P., & Feller, G. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.02757-10 · Cited by 89 · see citing works
‘The Farm Beneath the Sand’ – an archaeological case study on ancient ‘dirt’ DNA
Hebsgaard, M. B., Gilbert, M. T. P., Arneborg, J., Heyn, P. C., Allentoft, M. E., Bunce, M., Munch, K., Schweger, C. E., & Willerslev, E. (2009) · Antiquity · doi:10.1017/s0003598x00098537 · Cited by 76 · see citing works
Self-citationFast phylogenetic DNA barcoding
Munch, K., Boomsma, W., Willerslev, E., & Nielsen, R. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0169 · Cited by 72 · see citing works
Self-citationLerm, S., Westphal, A., Miethling-Graff, R., Alawi, M., Seibt, A., Wolfgramm, M., & Würdemann, H. (2013) · Extremophiles · doi:10.1007/s00792-013-0518-8 · Cited by 71 · see citing works
Arnold, L. J., Roberts, R. G., MacPhee, R. D. E., Haile, J., Brock, F., Möller, P., FROESE, D. G., Tikhonov, A., Chivas, A. R., Gilbert, M. T. P., et al. (2010) · Boreas · doi:10.1111/j.1502-3885.2010.00181.x · Cited by 69 · see citing works
Self-citationMolecular Exploration of the First-Century Tomb of the Shroud in Akeldama, Jerusalem
Matheson, C. D., Vernon, K. K., Lahti, A., Fratpietro, R., Spigelman, M., Gibson, S., Greenblatt, C. L., & Donoghue, H. D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008319 · Cited by 68 · see citing works
Isolation and Characterization of Bacteria from Ancient Siberian Permafrost Sediment
Zhang, D.-C., Brouchkov, A. V., Грива, Г. И., Schinner, F., & Margesin, R. (2013) · Biology · doi:10.3390/biology2010085 · Cited by 68 · see citing works
The Effect of Ancient DNA Damage on Inferences of Demographic Histories
Axelsson, E., Willerslev, E., Gilbert, M. T. P., & Nielsen, R. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn163 · Cited by 67 · see citing works
Self-citationAn Update on Eukaryotic Viruses Revived from Ancient Permafrost
Alempic, J.-M., Lartigue, A., Goncharov, A. Е., Grosse, G., Strauß, J., Tikhonov, A. N., Fedorov, A. N., Poirot, O., Legendre, M., Santini, S., et al. (2023) · Viruses · doi:10.3390/v15020564 · Cited by 66 · see citing works
Glaciers and Ice Sheets As Analog Environments of Potentially Habitable Icy Worlds
García‐López, E., & Cid, C. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01407 · Cited by 64 · see citing works
Boere, A. C., Damsté, J. S. S., Rijpstra, W. I. C., Volkman, J. K., & Coolen, M. J. L. (2011) · Organic Geochemistry · doi:10.1016/j.orggeochem.2011.08.005 · Cited by 63 · see citing works
Diversity and physiology of culturable bacteria associated with a coastal Antarctic ice core
Antony, R., Krishnan, K. P., Laluraj, C. M., Thamban, M., Dhakephalkar, P. K., Engineer, A. S., & Shivaji, S. (2012) · Microbiological Research · doi:10.1016/j.micres.2012.03.003 · Cited by 62 · see citing works
Low Energy Subsurface Environments as Extraterrestrial Analogs
Jones, R. M., Goordial, J., & Orcutt, B. N. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01605 · Cited by 63 · see citing works
Microbial ageing and longevity
Moger-Reischer, R. Z., & Lennon, J. T. (2019) · Nature Reviews Microbiology · doi:10.1038/s41579-019-0253-y · Cited by 59 · see citing works
Microbial diversity and functional capacity in polar soils
Makhalanyane, T. P., Goethem, M. W. V., & Cowan, D. A. (2016) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2016.01.011 · Cited by 59 · see citing works
Bioprospecting for microbial products that affect ice crystal formation and growth
Christner, B. C. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-009-2291-2 · Cited by 55 · see citing works
Survival of the fewest: Microbial dormancy and maintenance in marine sediments through deep time
Bradley, J. A., Amend, J. P., & LaRowe, D. E. (2018) · Geobiology · doi:10.1111/gbi.12313 · Cited by 56 · see citing works
In situ microbial metabolism as a cause of gas anomalies in ice
Rohde, R. A., Price, P. B., Bay, R., & Bramall, N. E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803763105 · Cited by 54 · see citing works
Active and dormant microorganisms on glacier surfaces
Bradley, J. A., Trivedi, C. B., Winkel, M., Mourot, R., Lutz, S., Larose, C., Keuschnig, C., Doting, E. L., Halbach, L., Zervas, A., et al. (2022) · Geobiology · doi:10.1111/gbi.12535 · Cited by 53 · see citing works
How do prokaryotes survive in fluid inclusions in halite for 30 k.y.?
Schubert, B. A., Lowenstein, T. K., Timofeeff, M. N., & Parker, M. A. (2009) · Geology · doi:10.1130/g30448a.1 · Cited by 52 · see citing works
Time‐shift experiments and patterns of adaptation across time and space
Blanquart, F., & Gandon, S. (2012) · Ecology Letters · doi:10.1111/ele.12007 · Cited by 49 · see citing works
Lewin, A. S., Johansen, J. A., Wentzel, A., Kotlar, H. K., Drabløs, F., & Valla, S. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12181 · Cited by 51 · see citing works
Leupin, O. X., Bernier‐Latmani, R., Bagnoud, A., Moors, H., Leys, N., Wouters, K., & Stroes-Gascoyne, S. (2017) · Swiss Journal of Geosciences · doi:10.1007/s00015-016-0255-y · Cited by 51 · see citing works
Cryosphere and Psychrophiles: Insights into a Cold Origin of Life?
Feller, G. (2017) · Life · doi:10.3390/life7020025 · Cited by 51 · see citing works
Halophilic Archaea Cultivated from Surface Sterilized Middle-Late Eocene Rock Salt Are Polyploid
Jaakkola, S., Zerulla, K., Guo, Q., Liu, Y., Ma, H., Yang, C., Bamford, D. H., Chen, X., Soppa, J., & Oksanen, H. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110533 · Cited by 50 · see citing works
Liang, R., Lau, M. C. Y., Vishnivetskaya, T. A., Lloyd, K. G., Wang, W., Wiggins, J. B., Miller, J. M., Pfiffner, S. M., Rivkina, E., & Onstott, T. C. (2019) · Applied and Environmental Microbiology · doi:10.1128/aem.00560-19 · Cited by 50 · see citing works
Survival and rapid resuscitation permit limited productivity in desert microbial communities
Imminger, S., Meier, D. V., Schintlmeister, A., Legin, A. A., Schnecker, J., Richter, A. A., Gillor, O., Eichorst, S. A., & Woebken, D. (2024) · Nature Communications · doi:10.1038/s41467-024-46920-6 · Cited by 49 · see citing works
Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost
Liang, R., Li, Z., Lau, M. C. Y., Vishnivetskaya, T. A., Zanina, O. G., Lloyd, K. G., Pfiffner, S. M., Rivkina, E., Wang, W., Wiggins, J. B., et al. (2021) · Microbiome · doi:10.1186/s40168-021-01057-2 · Cited by 48 · see citing works
Nunn, B. L., Slattery, K., Cameron, K. A., Timmins‐Schiffman, E., & Junge, K. (2014) · Environmental Microbiology · doi:10.1111/1462-2920.12691 · Cited by 48 · see citing works
Macromolecular synthesis by yeasts under frozen conditions
Amato, P., Doyle, S. M., & Christner, B. C. (2008) · Environmental Microbiology · doi:10.1111/j.1462-2920.2008.01829.x · Cited by 48 · see citing works
Ernakovich, J. G., & Wallenstein, M. D. (2015) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2015.04.009 · Cited by 48 · see citing works
Amato, P., Doyle, S. M., Battista, J. R., & Christner, B. C. (2010) · Astrobiology · doi:10.1089/ast.2010.0477 · Cited by 45 · see citing works
Foundations of Paleoparasitology
Ferreira, L. F., Reinhard, K. J., & Araújo, A. (2014) · Editora FIOCRUZ eBooks · doi:10.7476/9788575415986 · Cited by 49 · see citing works
Psychrophiles: Ecological significance and potential industrial application
Hamdan, A. M. (2018) · South African Journal of Science · doi:10.17159/sajs.2018/20170254 · Cited by 47 · see citing works
Price, P. B. (2009) · Canadian Journal of Microbiology · doi:10.1139/w08-117 · Cited by 47 · see citing works
St‐Jean, M., Lauriol, B. M., Clark, I. D., Lacelle, D., & Zdanowicz, C. M. (2010) · Permafrost and Periglacial Processes · doi:10.1002/ppp.680 · Cited by 45 · see citing works
Stroes-Gascoyne, S., Hamon, C. J., & Maak, P. (2011) · Physics and Chemistry of the Earth Parts A/B/C · doi:10.1016/j.pce.2011.07.085 · Cited by 45 · see citing works
Are permafrost microorganisms as old as permafrost?
Abramov, A., Vishnivetskaya, T. A., & Rivkina, E. (2020) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiaa260 · Cited by 45 · see citing works
Antarctic Relic Microbial Mat Community Revealed by Metagenomics and Metatranscriptomics
Zaikova, E., Goerlitz, D. S., Tighe, S. W., Wagner, N. Y., Bai, Y., Hall, B. L., Bevilacqua, J. G., Weng, M. M., Samuels-Fair, M. D., & Johnson, S. S. (2019) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2019.00001 · Cited by 45 · see citing works
Self-citation830-million-year-old microorganisms in primary fluid inclusions in halite
Schreder-Gomes, S. I., Benison, K. C., & Bernau, J. A. (2022) · Geology · doi:10.1130/g49957.1 · Cited by 43 · see citing works
DunaliellaCells in Fluid Inclusions in Halite: Significance for Long-term Survival of Prokaryotes
Schubert, B. A., Timofeeff, M. N., Lowenstein, T. K., & Polle, J. E. W. (2010) · Geomicrobiology Journal · doi:10.1080/01490450903232207 · Cited by 42 · see citing works
The effects of warming and soil chemistry on bacterial community structure in Arctic tundra soils
Ricketts, M. P., Matamala, R., JASTROW, J. D., Antonopoulos, D. A., Koval, J., Ping, C., Liang, C. C., & Gonzàlez‐Meler, M. A. (2020) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2020.107882 · Cited by 41 · see citing works
Antarctic ice core samples: culturable bacterial diversity
Shivaji, S., Begum, Z., Rao, S. S. S. N., Reddy, P. V. V. V., Manasa, P., Sailaja, B., Prathiba, M. S., Thamban, M., Krishnan, K. P., Singh, S. M., et al. (2012) · Research in Microbiology · doi:10.1016/j.resmic.2012.09.001 · Cited by 41 · see citing works
JinJin, S., Wang, P.-B., Wang, H., & Yu, X. (2021) · Global Ecology and Conservation · doi:10.1016/j.gecco.2021.e01621 · Cited by 40 · see citing works
The complete genome of a viable archaeum isolated from 123‐million‐year‐old rock salt
Jaakkola, S., Pfeiffer, F., Ravantti, J., Guo, Q., Liu, Y., Chen, X., Ma, H., Yang, C., Oksanen, H. M., & Bamford, D. H. (2015) · Environmental Microbiology · doi:10.1111/1462-2920.13130 · Cited by 40 · see citing works
Hu, W., Zhang, Q., Tian, T., Li, D., Cheng, G., Mu, J., Wu, Q., Niu, F., Stegen, J., An, L., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0145747 · Cited by 40 · see citing works
Wake me when it’s over – Bacterial toxin–antitoxin proteins and induced dormancy
Coussens, N. P., & Daines, D. A. (2016) · Experimental Biology and Medicine · doi:10.1177/1535370216651938 · Cited by 40 · see citing works
Glombitza, C., Adhikari, R. R., Riedinger, N., Gilhooly, W., Hinrichs, K., & Inagaki, F. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01576 · Cited by 39 · see citing works
Baker, L. J., Freed, L. L., Easson, C., Lopez, J. V., Fenolio, D. B., Sutton, T., Nyholm, S. V., & Hendry, T. A. (2019) · eLife · doi:10.7554/elife.47606 · Cited by 39 · see citing works
Ancient Microbes from Halite Fluid Inclusions: Optimized Surface Sterilization and DNA Extraction
Sankaranarayanan, K., Timofeeff, M. N., Spathis, R., Lowenstein, T. K., & Lum, J. K. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020683 · Cited by 38 · see citing works
Gutt, J., & Dieckmann, G. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108683319 · Cited by 36 · see citing works
- Authors
- Johnson, S. S., Hebsgaard, M. B., Christensen, T. R., Mastepanov, M., Nielsen, R., Munch, K., Brand, T., Gilbert, M. T. P., Zuber, M. T., Bunce, M., Rønn, R., Gilichinsky, D., Froese, D., & Willerslev, E.
- Affiliations
- University of Copenhagen (DK)
- Lund University (SE)
- Massachusetts Institute of Technology (US)
- Murdoch University (AU)
- Russian Academy of Sciences (RU)
- University of Alberta (CA)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2007-09-04
- Volume
- 104
- Issue
- 36
- Pages
- 14401-14405
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1958816
- OpenAlex
- W2147486201
- Cited by
- 292
- References
- 42
- Citations by year
- 2026: 10 · 2025: 5 · 2024: 12 · 2023: 12 · 2022: 17 · 2021: 24 · 2020: 35 · 2019: 14 · 2018: 9 · 2017: 14 · 2016: 12 · 2015: 12 · 2014: 20 · 2013: 16 · 2012: 12
- FWCI
- 14.16
- Type
- journal article
- Language
- en
- Update notices
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Murdoch University Research Portal (submittedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- Wellcome Trust
- Topics
- Physical Sciences › Environmental Science › Ecology › Polar Research and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- ancient bacteria, DNA repair, bacterial dormancy, metabolic activity
- MeSH terms
- Bacteria, Base Sequence, DNA Repair, DNA, Bacterial, Gene Amplification, Molecular Sequence Data, Soil Microbiology
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review