1887

Abstract

Groundbreaking studies conducted in the mid-1980s demonstrated the possibility of sequencing ancient DNA (aDNA), which has allowed us to answer fundamental questions about the human past. Microbiologists were thus given a powerful tool to glimpse directly into inscrutable bacterial history, hitherto inaccessible due to a poor fossil record. Initially plagued by concerns regarding contamination, the field has grown alongside technical progress, with the advent of high-throughput sequencing being a breakthrough in sequence output and authentication. Albeit burdened with challenges unique to the analysis of bacteria, a growing number of viable sources for aDNA has opened multiple avenues of microbial research. Ancient pathogens have been extracted from bones, dental pulp, mummies and historical medical specimens and have answered focal historical questions such as identifying the aetiological agent of the black death as . Furthermore, ancient human microbiomes from fossilized faeces, mummies and dental plaque have shown shifts in human commensals through the Neolithic demographic transition and industrial revolution, whereas environmental isolates stemming from permafrost samples have revealed signs of ancient antimicrobial resistance. Culminating in an ever-growing repertoire of ancient genomes, the quickly expanding body of bacterial aDNA studies has also enabled comparisons of ancient genomes to their extant counterparts, illuminating the evolutionary history of bacteria. In this review we summarize the present avenues of research and contextualize them in the past of the field whilst also pointing towards questions still to be answered.

Funding
This study was supported by the:
  • Wellcome Trust (Award 101237/Z/13/B)
    • Principle Award Recipient: Daniel J. Wilson
  • Biotechnology and Biological Sciences Research Council (Award BB/M011224/1)
    • Principle Award Recipient: Nicolas Arning
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000384
2020-06-29
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/7/mgen000384.html?itemId=/content/journal/mgen/10.1099/mgen.0.000384&mimeType=html&fmt=ahah

References

  1. Jutras BL, Jacobs-Wagner C. Bacterial evolution: what goes around comes around. Current Biology 2015; 25:R496–R498
    [Google Scholar]
  2. Woese CR. Bacterial evolution. Microbiol Rev 1987; 51:221–271
    [Google Scholar]
  3. Louca S, Shih PM, Pennell MW, Fischer WW, Parfrey LW et al. Bacterial diversification through geological time. Nature Ecology & Evolution 2018; 2:1458–1467
    [Google Scholar]
  4. Spyrou MA, Keller M, Tukhbatova RI, Scheib CL, Nelson EA et al. Phylogeography of the second plague pandemic revealed through analysis of historical Yersinia pestis genomes. Nature Communications 2019; 10:1–13
    [Google Scholar]
  5. Slatkin M, Racimo F. Ancient DNA and human history. Proceedings of the National Academy of Sciences 2016; 113:6380–6387
    [Google Scholar]
  6. Higuchi R, Bowman B, Freiberger M, Ryder OA, Wilson AC. Dna sequences from the quagga, an extinct member of the horse family. Nature 1984; 312:282
    [Google Scholar]
  7. Mullis KB, Faloona FA. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Meth Enzymol 1987; 155:335–350
    [Google Scholar]
  8. Spigelman M, Lemma E. The use of the polymerase chain reaction (PCR) to detect Mycobacterium tuberculosis in ancient skeletons. International Journal of Osteoarchaeology 1993; 3:137–143
    [Google Scholar]
  9. Rafi A, Spigelman M, Stanford J, Lemma E, Donoghue H et al. Mycobacterium leprae DNA from ancient bone detected by PCR. Lancet 1994; 343:1360–1361
    [Google Scholar]
  10. Müller R, Roberts CA, Brown TA. Complications in the study of ancient tuberculosis: presence of environmental bacteria in human archaeological remains. Journal of Archaeological Science 2016; 68:5–11
    [Google Scholar]
  11. Shapiro B, Hofreiter M. A paleogenomic perspective on evolution and gene function: new insights from ancient DNA. Science 2014; 343:1236573
    [Google Scholar]
  12. Warinner C, Herbig A, Mann A, Fellows Yates JA, Weiß CL et al. A robust framework for microbial archaeology. Annu Rev Genomics Hum Genet 2017; 18:321–356
    [Google Scholar]
  13. Hagelberg E, Hofreiter M, Keyser C. Ancient DNA: the first three decades. Philosophical Transactions of the Royal Society B: Biological Sciences 2015; 370:20130371 [View Article]
    [Google Scholar]
  14. Willerslev E, Cooper A, Ancient DNA. Proc Biol Sci 2005; 272:3–16
    [Google Scholar]
  15. Yang DY, Eng B, Saunders SR. Hypersensitive PCR, ancient human mtDNA, and contamination. Human Biology 2003; 75:355–364
    [Google Scholar]
  16. Der Sarkissian C, Allentoft ME, Ávila-Arcos MC, Barnett R, Campos PF et al. Ancient genomics. Philos Trans R Soc Lond B Biol Sci 2015; 370:
    [Google Scholar]
  17. Green RE, Briggs AW, Krause J, Prüfer K, Burbano HA et al. The Neandertal genome and ancient DNA authenticity. Embo J 2009; 28:2494–2502
    [Google Scholar]
  18. Mouttham N, Klunk J, Kuch M, Fourney R, Poinar H. Surveying the repair of ancient DNA from bones via high-throughput sequencing. BioTechniques 2015; 59:19–25
    [Google Scholar]
  19. Dabney J, Meyer M, Pääbo S. Ancient DNA damage. cold Spring harbor perspectives in biology.; 2013; 5
  20. Briggs AW, Stenzel U, Johnson PLF, Green RE, Kelso J et al. Patterns of damage in genomic DNA sequences from a Neandertal. Proc Natl Acad Sci USA 2007; 104:14616–14621
    [Google Scholar]
  21. Sawyer S, Krause J, Guschanski K, Savolainen V, Pääbo S. Temporal patterns of nucleotide misincorporations and DNA fragmentation in ancient DNA. PLoS ONE 2012; 7:e34131
    [Google Scholar]
  22. Kistler L, Ware R, Smith O, Collins M, Allaby RG. A new model for ancient DNA decay based on paleogenomic meta-analysis. Nucleic Acids Res 2017; 45:6310–6320
    [Google Scholar]
  23. Skoglund P, Northoff BH, Shunkov MV, Derevianko AP, Pääbo S et al. Separating endogenous ancient DNA from modern day contamination in a Siberian Neandertal. PNAS 2014; 111:2229–2234
    [Google Scholar]
  24. Okou DT, Steinberg KM, Middle C, Cutler DJ, Albert TJ et al. Microarray-Based genomic selection for high-throughput resequencing. Nature Methods 2007; 4:907–909
    [Google Scholar]
  25. Carpenter ML, Buenrostro JD, Valdiosera C, Schroeder H, Allentoft ME et al. Pulling out the 1%: Whole-Genome Capture for the Targeted Enrichment of Ancient DNA Sequencing Libraries. The American Journal of Human Genetics 2013; 93:852–864
    [Google Scholar]
  26. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005; 437:376–380 [View Article]
    [Google Scholar]
  27. Bos KI, Schuenemann VJ, Golding GB, Burbano HA, Waglechner N et al. A draft genome of Yersinia pestis from victims of the black death. Nature 2011; 478:506–510
    [Google Scholar]
  28. Drancourt M, Aboudharam G, Signoli M, Dutour O, Raoult D. Detection of 400-year-old Yersinia pestis DNA in human dental pulp: an approach to the diagnosis of ancient septicemia. PNAS 1998; 95:12637–12640
    [Google Scholar]
  29. Drancourt M, Raoult D. Yersinia pestis and the three plague pandemics. The Lancet Infectious Diseases 2014; 14:918–919
    [Google Scholar]
  30. Ochman H, Elwyn S, Moran NA. Calibrating bacterial evolution. PNAS 1999; 96:12638–12643
    [Google Scholar]
  31. Wilson DJ, Gabriel E, Leatherbarrow AJH, Cheesbrough J, Gee S et al. Rapid evolution and the importance of recombination to the gastroenteric pathogen Campylobacter jejuni. Mol Biol Evol. 2009;Feb; 26:(2):385–397. David Penny. Relativity for molecular clocks. Nature, 436(7048):183, July 2005.
    [Google Scholar]
  32. Penny D. Relativity for molecular clocks. Nature 2005; 436:183
    [Google Scholar]
  33. SYW H, Phillips MJ, Cooper A, Drummond AJ. Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 2005; 22:1561–1568
    [Google Scholar]
  34. Pérez-Losada M, Crandall KA, Bash MC, Dan M, Zenilman J et al. Distinguishing importation from diversification of quinolone-resistant Neisseria gonorrhoeae by molecular evolutionary analysis. BMC Evolutionary Biology 2007; 7:84
    [Google Scholar]
  35. Comas I, Coscolla M, Luo T, Borrell S, Holt KE et al. Out-Of-Africa migration and Neolithic co-expansion of Mycobacterium tuberculosis with modern humans. Nat Genet 2013; 45:1176–1182
    [Google Scholar]
  36. Bos KI, Kühnert D, Herbig A, Esquivel-Gomez LR, Andrades Valtueña A et al. Paleomicrobiology: diagnosis and evolution of ancient pathogens. Annual Review of Microbiology 2019; 73:639–666
    [Google Scholar]
  37. Duchêne S, Geoghegan JL, Holmes EC, SYW H. Estimating evolutionary rates using time-structured data: a general comparison of phylogenetic methods. Bioinformatics 2016; 32:3375–3379
    [Google Scholar]
  38. Schuenemann VJ, Singh P, Mendum TA, Krause-Kyora B, Jäger G et al. Genome-Wide comparison of medieval and modern Mycobacterium leprae. Science 2013; 341:179–183
    [Google Scholar]
  39. Bos KI, Harkins KM, Herbig A, Coscolla M, Weber N et al. Pre-Columbian mycobacterial genomes reveal seals as a source of new world human tuberculosis. Nature 2014; 514:494–497
    [Google Scholar]
  40. Wagner DM, Klunk J, Harbeck M, Devault A, Waglechner N et al. Yersinia pestis and the plague of Justinian 541-543 AD: a genomic analysis. Lancet Infect Dis 2014; 14:319–326
    [Google Scholar]
  41. Krings M, Stone A, Schmitz RW, Krainitzki H, Stoneking M et al. Neandertal DNA sequences and the origin of modern humans. Cell 1997; 90:19–30 [View Article]
    [Google Scholar]
  42. Miller W, Drautz DI, Ratan A, Pusey B, Qi J et al. Sequencing the nuclear genome of the extinct woolly mammoth. Nature 2008; 456:387–390 [View Article]
    [Google Scholar]
  43. Zink AR, Molnár E, Motamedi N, Pálfy G, Marcsik A et al. Molecular history of tuberculosis from ancient mummies and skeletons. International Journal of Osteoarchaeology 2007; 17:380–391
    [Google Scholar]
  44. Donoghue HD, Marcsik A, Matheson C, Vernon K, Nuorala E et al. Co-Infection of Mycobacterium tuberculosis and Mycobacterium leprae in human archaeological samples: a possible explanation for the historical decline of leprosy. Proc Biol Sci 2005; 272:389–394
    [Google Scholar]
  45. Ubaldi M, Luciani S, Marota I, Fornaciari G, Cano RJ et al. Sequence analysis of bacterial DNA in the colon of an Andean mummy. Am J Phys Anthropol 1998; 107:285–295
    [Google Scholar]
  46. Salo WL, Aufderheide AC, Buikstra J, Holcomb TA. Identification of Mycobacterium tuberculosis DNA in a pre-Columbian Peruvian mummy. PNAS 1994; 91:2091–2094
    [Google Scholar]
  47. Cano RJ, Tiefenbrunner F, Ubaldi M, Del Cueto C, Luciani S et al. Sequence analysis of bacterial DNA in the colon and stomach of the Tyrolean Iceman. Am J Phys Anthropol 2000; 112:297–309
    [Google Scholar]
  48. Donoghue HD, Spigelman M, Zias J, Gernaey-Child AM, Minnikin DE. Mycobacterium tuberculosis complex DNA in calcified pleura from remains 1400 years old. Lett Appl Microbiol 1998; 27:265–269
    [Google Scholar]
  49. Jackson PJ, Hugh-Jones ME, Adair DM, Green G, Hill KK et al. Pcr analysis of tissue samples from the 1979 Sverdlovsk anthrax victims: the presence of multiple Bacillus anthracis strains in different victims. Proc Natl Acad Sci U S A 1998; 95:1224–1229
    [Google Scholar]
  50. Devault AM, Golding GB, Waglechner N, Enk JM, Kuch M et al. Second-Pandemic strain of Vibrio cholerae from the Philadelphia cholera outbreak of 1849. New England Journal of Medicine 2014; 370:334–340
    [Google Scholar]
  51. Nelson-Sathi S, Martin WF. The origin of a killer revealed by bronze age Yersinia genomes. Cell Host & Microbe 2015; 18:513–514
    [Google Scholar]
  52. Gorgé O, Bennett EA, Massilani D, Daligault J, Pruvost M et al. Analysis of ancient DNA in microbial ecology. Methods Mol Biol 2016; 1399:289–315
    [Google Scholar]
  53. Priscu JC, Adams EE, Lyons WB, Voytek MA, Mogk DW et al. Geomicrobiology of Subglacial ice above lake Vostok, Antarctica. Science 1999; 286:2141–2144
    [Google Scholar]
  54. Christner BC, Mosley‐Thompson E, Thompson LG, Reeve JN. Isolation of bacteria and 16S rDNAs from lake Vostok accretion ice. Environmental Microbiology 2001; 3:570–577
    [Google Scholar]
  55. Willerslev E, Hansen AJ, Poinar HN. Isolation of nucleic acids and cultures from fossil ice and permafrost. Trends Ecol Evol 2004; 19:141–147
    [Google Scholar]
  56. Bulat SA, Alekhina IA, VYa L, Leitchenkov GL, Raynaud D et al. Limitations for life in lake Vostok, Antarctica; 2003; 3288
  57. Willerslev E, Hansen AJ, Rønn R, Brand TB, Barnes I et al. Long-Term persistence of bacterial DNA. Curr Biol 2004; 14:R9–10
    [Google Scholar]
  58. Warinner C, Speller C, Collins MJ, Lewis CM. Ancient human microbiomes. Journal of Human Evolution 2015; 79:125–136
    [Google Scholar]
  59. Cano RJ, Rivera-Perez J, Toranzos GA, Santiago-Rodriguez TM, Narganes-Storde YM et al. Paleomicrobiology: revealing fecal Microbiomes of ancient Indigenous cultures. Plos One 2014; 9:e106833
    [Google Scholar]
  60. Poinar H, Kuch M, McDonald G, Martin P, Pääbo S. Nuclear gene sequences from a late Pleistocene Sloth Coprolite. Current Biology 2003; 13:1150–1152
    [Google Scholar]
  61. Santiago-Rodriguez TM, Narganes-Storde YM, Chanlatte L, Crespo-Torres E, Toranzos GA et al. Microbial communities in Pre-Columbian Coprolites. Plos One 2013; 8:e65191
    [Google Scholar]
  62. Reinhard K, Bryant V. Pathoecology and the Future of Coprolite Studies in Bioarchaeology Karl Reinhard Papers/Publications; 2008 Jan
    [Google Scholar]
  63. Tito RY, Macmil S, Wiley G, Najar F, Cleeland L et al. Phylotyping and functional analysis of two ancient human Microbiomes. Plos One 2008; 3:e3703
    [Google Scholar]
  64. Bryant VM. Prehistoric diet in Southwest Texas: the Coprolite evidence. American Antiquity 1974; 39:407–420
    [Google Scholar]
  65. Rivera-Perez JI, Santiago-Rodriguez TM, Toranzos GA. Paleomicrobiology: a snapshot of ancient microbes and approaches to forensic microbiology. Microbiol Spectr. 2016; 4:
    [Google Scholar]
  66. Tito RY, Knights D, Metcalf J, Obregon-Tito AJ, Cleeland L et al. Insights from characterizing extinct human gut Microbiomes. Plos One 2012; 7:e51146
    [Google Scholar]
  67. Warinner C, Rodrigues JFM, Vyas R, Trachsel C, Shved N et al. Pathogens and host immunity in the ancient human oral cavity. Nature Genetics 2014; 46:336–344
    [Google Scholar]
  68. Davenport ER, Sanders JG, Song SJ, Amato KR, Clark AG et al. The human microbiome in evolution. BMC Biology 2017; 15:127
    [Google Scholar]
  69. Dobney K, Brothwell D. A scanning electron microscope study of archaeological dental calculus. Scanning Electron Microscopy in Archaeology BAR International Series 1988; 452:372–385
    [Google Scholar]
  70. Preus HR, Marvik OJ, Selvig KA, Bennike P. Ancient bacterial DNA (aDNA) in dental calculus from archaeological human remains. Journal of Archaeological Science 2011; 38:1827–1831
    [Google Scholar]
  71. Fuente CDL, Flores S, Moraga M. Dna from human ancient bacteria: a novel source of genetic evidence from archaeological dental calculus. Archaeometry 2013; 55:767–778
    [Google Scholar]
  72. Adler CJ, Dobney K, Weyrich LS, Kaidonis J, Walker AW et al. Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and industrial revolutions. Nature Genetics 2013; 45:450–455
    [Google Scholar]
  73. Velsko IM, Fellows Yates JA, Aron F, Hagan RW, Frantz LAF et al. Microbial differences between dental plaque and historic dental calculus are related to oral biofilm maturation stage. Microbiome 2019; 7:102
    [Google Scholar]
  74. Bidle KD, Lee S, Marchant DR, Falkowski PG. Fossil genes and microbes in the oldest ice on earth. Proceedings of the National Academy of Sciences 2007; 104:13455–13460
    [Google Scholar]
  75. Campana MG, Robles García N, Rühli FJ, Tuross N. False positives complicate ancient pathogen identifications using high-throughput shotgun sequencing. BMC Research Notes 2014; 7:111
    [Google Scholar]
  76. Weiß CL, Gansauge M-T, Aximu-Petri A, Meyer M, Burbano HA. Mining ancient microbiomes using selective enrichment of damaged DNA molecules. bioRxiv 2018; 397927:
    [Google Scholar]
  77. Ginolhac A, Rasmussen M, Gilbert MTP, Willerslev E, Orlando L. mapDamage: testing for damage patterns in ancient DNA sequences. Bioinformatics 2011; 27:2153–2155
    [Google Scholar]
  78. Rollo F, Luciani S, Marota I, Olivieri C, Ermini L. Persistence and decay of the intestinal microbiota’s DNA in glacier mummies from the Alps. Journal of Archaeological Science 2007; 34:1294–1305
    [Google Scholar]
  79. Donoghue HD, Spigelman M, Greenblatt CL, Lev-Maor G, Bar-Gal GK et al. Tuberculosis: from prehistory to Robert koch, as revealed by ancient DNA. Lancet Infect Dis 2004; 4:584–592
    [Google Scholar]
  80. Ziesemer KA, Mann AE, Sankaranarayanan K, Schroeder H, Ozga AT et al. Intrinsic challenges in ancient microbiome reconstruction using 16S rRNA gene amplification. Scientific Reports 2015; 5:16498
    [Google Scholar]
  81. Schouten S, Middelburg JJ, Hopmans EC, Sinninghe Damsté JS. Fossilization and degradation of intact polar lipids in deep subsurface sediments: a theoretical approach. Geochimica et Cosmochimica Acta 2010; 74:3806–3814
    [Google Scholar]
  82. Harper KN, Genomics AGJ. The origins of agriculture, and our changing microbe-scape: time to revisit some old tales and tell some new ones. Am J Phys Anthropol 2013; 152:135–152
    [Google Scholar]
  83. Harkins KM, Stone AC. Ancient pathogen genomics: insights into timing and adaptation. J Hum Evol 2015; 79:137–149
    [Google Scholar]
  84. Pearce-Duvet JMC. The origin of human pathogens: evaluating the role of agriculture and domestic animals in the evolution of human disease. Biol Rev Camb Philos Soc 2006; 81:369–382
    [Google Scholar]
  85. Rasmussen S, Allentoft ME, Nielsen K, Orlando L, Sikora M et al. Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell 2015; 163:571–582
    [Google Scholar]
  86. Feldman M, Harbeck M, Keller M, Spyrou MA, Rott A et al. A high-coverage Yersinia pestis genome from a Sixth-Century Justinianic plague victim. Mol Biol Evol 2016; 33:2911–2923
    [Google Scholar]
  87. Andrades Valtueña A, Mittnik A, Key FM, Haak W, Allmäe R et al. The stone age plague and its persistence in Eurasia. Curr Biol 2017; 27:3683–3691
    [Google Scholar]
  88. Damgaard P de B, Marchi N, Rasmussen S, Peyrot M, Renaud G et al. 137 ancient human genomes from across the Eurasian steppes. Nature 2018; 557:369
    [Google Scholar]
  89. Spyrou MA, Tukhbatova RI, Wang C-C, Valtueña AA, Lankapalli AK et al. Analysis of 3800-year-old Yersinia pestis genomes suggests bronze age origin for bubonic plague. Nature Communications 2018; 9:2234
    [Google Scholar]
  90. Keller M, Spyrou MA, Scheib CL, Neumann GU, Kröpelin A et al. Ancient Yersinia pestis genomes from across Western Europe reveal early diversification during the first pandemic (541–750). Proceedings of the National Academy of Sciences 2019; 116:12363–12372
    [Google Scholar]
  91. Spyrou MA, Tukhbatova RI, Feldman M, Drath J, Kacki S et al. Historical Y. pestis genomes reveal the European black death as the source of ancient and modern plague pandemics. Cell Host Microbe 2016; 19:874–881
    [Google Scholar]
  92. Benedictow OJ. The black death, 1346–1353: the complete history. Woodbridge, Suffolk, United Kingdom, Boydell press, 2004. XVI, 433 pp., illus. (NO price given). Journal of the History of Medicine and Allied Sciences 2005; 60:514–516
    [Google Scholar]
  93. Bos KI, Herbig A, Sahl J, Waglechner N, Fourment M et al. Eighteenth century Yersinia pestis genomes reveal the long-term persistence of an historical plague focus. Neher RA, editor. eLife 2016; 5:e12994
    [Google Scholar]
  94. Spyrou MA, Bos KI, Herbig A, Krause J. Ancient pathogen genomics as an emerging tool for infectious disease research. Nature Reviews Genetics 2019; 1:
    [Google Scholar]
  95. Cui Y, Yu C, Yan Y, Li D, Li Y et al. Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proc Natl Acad Sci USA 2013; 110:577–582
    [Google Scholar]
  96. Haensch S, Bianucci R, Signoli M, Rajerison M, Schultz M et al. Distinct clones of Yersinia pestis caused the black death. PLoS Pathog 2010; 6:
    [Google Scholar]
  97. Harbeck M, Seifert L, Hänsch S, Wagner DM, Birdsell D et al. Yersinia pestis DNA from skeletal remains from the 6th century AD reveals insights into Justinianic plague. PLOS Pathogens 2013; 9:e1003349
    [Google Scholar]
  98. Leonardi M, Librado P, Der Sarkissian C, Schubert M, Alfarhan AH et al. Evolutionary patterns and processes: lessons from ancient DNA. Syst Biol 2017; 66:e1–e29
    [Google Scholar]
  99. CRyPTIC Consortium Prediction of susceptibility to first-line tuberculosis drugs by DNA sequencing. New England Journal of Medicine 2018; 379:1403–1415
    [Google Scholar]
  100. Kay GL, Sergeant MJ, Zhou Z, Chan JZ-M, Millard A et al. Eighteenth-Century genomes show that mixed infections were common at time of peak tuberculosis in Europe. Nature Communications 2015; 6:6717
    [Google Scholar]
  101. Koch R. Die Ätiologie der Tuberkulose. In Gradmann C, Koch Robert. (editors) Zentrale Texte Berlin, Heidelberg: Springer Berlin Heidelberg; 2018 pp 113–131
    [Google Scholar]
  102. Hershkovitz I, Donoghue HD, Minnikin DE, Besra GS, OY-C L et al. Detection and molecular characterization of 9000-Year-Old Mycobacterium tuberculosis from a Neolithic settlement in the eastern Mediterranean. Plos One 2008; 3:e3426
    [Google Scholar]
  103. Holloway KL, Henneberg RJ, de Barros Lopes M, Henneberg M. Evolution of human tuberculosis: a systematic review and meta-analysis of paleopathological evidence. HOMO 2011; 62:402–458
    [Google Scholar]
  104. Masson M, Molnár E, Donoghue HD, Besra GS, Minnikin DE et al. Osteological and biomolecular evidence of a 7000-Year-Old case of hypertrophic pulmonary osteopathy secondary to tuberculosis from Neolithic Hungary. PLoS One 2013; 8:e78252 [View Article]
    [Google Scholar]
  105. Zink A, Haas CJ, Reischl UDO, Szeimies U, Nerlich AG. Molecular analysis of skeletal tuberculosis in an ancient Egyptian population. J Med Microbiol 2001; 50:355–366 [View Article]
    [Google Scholar]
  106. Götherström NEA, Ahlström T, Donoghue H, Spigelman M, Lidén K. Mtb complex DNA in a Scandinavian Neolithic passage Grave. paper I, molecular Palaeopathology. ancient DNA analyses of the bacterial diseases tuberculosis and leprosy. in: theses and papers in scientific archaeology 6. archaeological research laboratory, Stockholm University, Stockholm. theses and papers in scientific archaeology; 2004; 6
  107. Rothschild BM, Martin LD, Lev G, Bercovier H, Bar-Gal GK et al. Mycobacterium tuberculosis complex DNA from an extinct Bison dated 17,000 years before the present. Clin Infect Dis 2001; 33:305–311 [View Article][PubMed]
    [Google Scholar]
  108. Hershberg R, Lipatov M, Small PM, Sheffer H, Niemann S et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol 2008; 6:e311 [View Article]
    [Google Scholar]
  109. Fletcher HA, Donoghue HD, Holton J, Pap I, Spigelman M. Widespread occurrence of Mycobacterium tuberculosis DNA from 18th-19th century Hungarians. Am J Phys Anthropol 2003; 120:144–152 [View Article][PubMed]
    [Google Scholar]
  110. Chan JZ-M, Sergeant MJ, Lee OY-C, Minnikin DE, Besra GS et al. Metagenomic analysis of tuberculosis in a mummy. N Engl J Med 2013; 369:289–290 [View Article]
    [Google Scholar]
  111. Hansen GA. On the etiology of leprosy. The British and Foreign Medico-Chirurgical Review 1875; 55:459–489
    [Google Scholar]
  112. Taylor GM, Blau S, Mays S, Monot M, Lee OY-C et al. Mycobacterium leprae genotype amplified from an archaeological case of lepromatous leprosy in central Asia. J Archaeol Sci 2009; 36:2408–2414 [View Article]
    [Google Scholar]
  113. Britton WJ, Lockwood DNJ, Leprosy LDN. Leprosy. The Lancet 2004; 363:1209–1219 [View Article]
    [Google Scholar]
  114. Schuenemann VJ, Avanzi C, Krause-Kyora B, Seitz A, Herbig A et al. Ancient genomes reveal a high diversity of Mycobacterium leprae in medieval Europe. PLoS Pathog 2018; 14:e1006997 [View Article]
    [Google Scholar]
  115. Monot M, Honor N, Garnier T, Zidane N, Sherafi D et al. Comparative genomic and phylogeographic analysis of Mycobacterium leprae. Nat Genet 2009; 41:1282–1289 [View Article]
    [Google Scholar]
  116. Monot M et al. On the origin of leprosy. Science 2005; 308:1040–1042 [View Article]
    [Google Scholar]
  117. Trautman JR. A brief history of Hansen’s disease. Bulletin of the New York Academy of Medicine 1984; 60:689–695
    [Google Scholar]
  118. Mendum TA, Schuenemann VJ, Roffey S, Taylor G, Wu H et al. Mycobacterium leprae genomes from a British medieval leprosy Hospital: towards understanding an ancient epidemic. BMC Genomics 2014; 15:270 [View Article]
    [Google Scholar]
  119. Krause-Kyora B, Nutsua M, Boehme L, Pierini F, Pedersen DD et al. Ancient DNA study reveals HLA susceptibility locus for leprosy in medieval Europeans. Nat Commun 2018; 9:1569 [View Article]
    [Google Scholar]
  120. Benjak A, Avanzi C, Singh P, Loiseau Chlo, Girma S et al. Phylogenomics and antimicrobial resistance of the leprosy Bacillus Mycobacterium leprae. Nat Commun 2018; 9:352 [View Article]
    [Google Scholar]
  121. Papagrigorakis MJ, Synodinos PN, Yapijakis C. Ancient typhoid epidemic reveals possible ancestral strain of Salmonella enterica serovar typhi. Infection, Genetics and Evolution 2007; 7:126–127 [View Article]
    [Google Scholar]
  122. Papagrigorakis MJ, Yapijakis C, Synodinos PN, Baziotopoulou-Valavani E. Dna examination of ancient dental pulp incriminates typhoid fever as a probable cause of the plague of Athens. International Journal of Infectious Diseases 2006; 10:206–214 [View Article]
    [Google Scholar]
  123. Shapiro B, Rambaut A, Gilbert MTP. No proof that typhoid caused the plague of Athens (a reply to Papagrigorakis et al.). International Journal of Infectious Diseases 2006; 10:334–335 [View Article]
    [Google Scholar]
  124. ÅJ V, Herbig A, Campana MG, García NMR, Warinner C et al. Salmonella enterica genomes from victims of a major sixteenth-century epidemic in Mexico. Nature Ecology & Evolution 2018; 2:520–528
    [Google Scholar]
  125. Zhou Z, Lundstrøm I, Tran-Dien A, Duchêne S, Alikhan N-F et al. Pan-Genome analysis of ancient and modern Salmonella enterica demonstrates genomic stability of the invasive para C lineage for millennia. Curr Biol 2018; 28:2420–2428 [View Article][PubMed]
    [Google Scholar]
  126. Schuenemann VJ, Kumar Lankapalli A, Barquera R, Nelson EA, Iraíz Hernández D et al. Historic Treponema pallidum genomes from colonial Mexico retrieved from archaeological remains. PLoS Negl Trop Dis 2018; 12:e0006447 [View Article][PubMed]
    [Google Scholar]
  127. Guedes L, Dias O, Neto J. Ribeiro dA Silva L dA P, Mendonça de Souza SMF, Iñiguez am. first Paleogenetic evidence of probable syphilis and Treponematoses cases in the Brazilian colonial period. BioMed Research International 2018
    [Google Scholar]
  128. Baker BJ, Armelagos GJ, Becker MJ, Brothwell D, Drusini A et al. The origin and antiquity of syphilis: paleopathological diagnosis and interpretation [and comments and reply]. Curr Anthropol 1988; 29:703–737 [View Article]
    [Google Scholar]
  129. Bloch I. Der Ursprung Der syphilis. G. Fischer 1911
    [Google Scholar]
  130. Luger A. The origin of syphilis. Clinical and epidemiologic considerations on the Columbian theory. Sexually Transmitted Diseases 1993; 20:110–117
    [Google Scholar]
  131. Rothschild BM, Turnbull W. Treponemal infection in a Pleistocene bear. Nature 1987; 329:61–62 [View Article]
    [Google Scholar]
  132. Harper KN, Zuckerman MK, Harper ML, Kingston JD, Armelagos GJ. The origin and antiquity of syphilis revisited: an appraisal of old world pre-Columbian evidence for treponemal infection. Am J Phys Anthropol 2011; 146:99–133 [View Article]
    [Google Scholar]
  133. Kolman CJ, Centurion-Lara A, Lukehart SA, Owsley DW, Tuross N. Identification of Treponema pallidum Subspecies pallidum in a 200-year-old Skeletal Specimen. J Infect Dis 1999; 180:2060–2063 [View Article]
    [Google Scholar]
  134. Montiel R, Solórzano E, Díaz N, Álvarez-Sandoval BA, González-Ruiz M et al. Neonate human remains: a window of opportunity to the molecular study of ancient syphilis. PLoS One 2012; 7:e36371 [View Article]
    [Google Scholar]
  135. von Hunnius TE, Yang D, Eng B, Waye JS, Saunders SR. Digging deeper into the limits of ancient DNA research on syphilis. J Archaeol Sci 2007; 34:2091–2100 [View Article]
    [Google Scholar]
  136. Bouwman AS, Brown TA. The limits of biomolecular palaeopathology: ancient DNA cannot be used to study venereal syphilis. J Archaeol Sci 2005; 32:703–713 [View Article]
    [Google Scholar]
  137. Barnes I, Thomas MG. Evaluating bacterial pathogen DNA preservation in museum osteological collections. Proc. R. Soc. B 2006; 273:645–653 [View Article]
    [Google Scholar]
  138. Feng L, Reeves PR, Lan R, Ren Y, Gao C et al. A Recalibrated molecular clock and independent origins for the cholera pandemic clones. PLoS One 2008; 3:e4053 [View Article]
    [Google Scholar]
  139. Andam CP, Worby CJ, Chang Q, Campana MG. Microbial genomics of ancient plagues and outbreaks. Trends Microbiol 2016; 24:978–990 [View Article]
    [Google Scholar]
  140. Hu D, Liu B, Feng L, Ding P, Guo X et al. Origins of the current seventh cholera pandemic. Proc Natl Acad Sci U S A 2016; 113:E7730–E7739 [View Article]
    [Google Scholar]
  141. Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 2011; 477:462–465 [View Article]
    [Google Scholar]
  142. Atherton JC. The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Annu Rev Pathol 2006; 1:63–96 [View Article]
    [Google Scholar]
  143. Swanston T, Haakensen M, Deneer H, Walker EG. The characterization of Helicobacter pylori DNA associated with ancient human remains recovered from a Canadian glacier. PLoS One 2011; 6:e16864 [View Article]
    [Google Scholar]
  144. Falush D et al. Traces of human migrations in Helicobacter pylori populations. Science 2003; 299:1582–1585 [View Article]
    [Google Scholar]
  145. Linz B, Balloux Franois, Moodley Y, Manica A, Liu H et al. An African origin for the intimate association between humans and Helicobacter pylori. Nature 2007; 445:915–918 [View Article]
    [Google Scholar]
  146. Allison MJ, Bergman T, Gerszten E. Further studies on fecal parasites in antiquity. Am J Clin Pathol 1999; 112:605–609 [View Article]
    [Google Scholar]
  147. Castillo-Rojas G, Cerbón MA, López-Vidal Y. Presence of Helicobacter pylori in a Mexican Pre-Columbian mummy. BMC Microbiol 2008; 8:119 [View Article][PubMed]
    [Google Scholar]
  148. Maixner F, Krause-Kyora B, Turaev D, Herbig A, Hoopmann MR et al. The 5300-year-old Helicobacter pylori genome of the Iceman. Science 2016; 351:162–165 [View Article]
    [Google Scholar]
  149. Kay GL, Sergeant MJ, Giuffra V, Bandiera P, Milanese M et al. Recovery of a medieval Brucella melitensis genome using shotgun Metagenomics. MBio 2014; 5:e01337–14 [View Article]
    [Google Scholar]
  150. D'anastasio R, Staniscia T, Milia ML, Manzoli L, Capasso L. Origin, evolution and paleoepidemiology of brucellosis. Epidemiol Infect 2011; 139:149–156 [View Article]
    [Google Scholar]
  151. D'Anastasio R, Zipfel B, Moggi-Cecchi J, Stanyon R, Capasso L. Possible brucellosis in an early hominin skeleton from sterkfontein, South Africa. PLoS One 2009; 4:e6439 [View Article]
    [Google Scholar]
  152. Devault AM, Mortimer TD, Kitchen A, Kiesewetter H, Enk JM et al. A molecular portrait of maternal sepsis from Byzantine Troy. eLife 2017; 6:e20983 [View Article]
    [Google Scholar]
  153. Guellil M, Kersten O, Namouchi A, Bauer EL, Derrick M et al. Genomic blueprint of a relapsing fever pathogen in 15th century Scandinavia. Proc Natl Acad Sci U S A 2018; 115:10422–10427 [View Article]
    [Google Scholar]
  154. Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 1977; 31:107–133 [View Article]
    [Google Scholar]
  155. Schnorr SL, Sankaranarayanan K, Lewis CM, Warinner C. Insights into human evolution from ancient and contemporary microbiome studies. Curr Opin Genet Dev 2016; 41:14–26 [View Article]
    [Google Scholar]
  156. Hofreiter M, Paijmans JLA, Goodchild H, Speller CF, Barlow A et al. The future of ancient DNA: technical advances and conceptual shifts. BioEssays 2015; 37:284–293 [View Article]
    [Google Scholar]
  157. Suzuki N, Yoneda M, Hirofuji T. Mixed red-complex bacterial infection in periodontitis. Int J Dent 2013; 2013:1–6 [View Article][PubMed]
    [Google Scholar]
  158. Weyrich LS, Duchene S, Soubrier J, Arriola L, Llamas B et al. Neanderthal behaviour, diet, and disease inferred from ancient DNA in dental calculus. Nature 2017; 544:357–361 [View Article]
    [Google Scholar]
  159. Luciani S, Fornaciari G, Rickards O, Labarga Cristina Martínez, Rollo F. Molecular characterization of a pre-Columbian mummy and in situ coprolite. Am J Phys Anthropol 2006; 129:620–629 [View Article]
    [Google Scholar]
  160. Santiago-Rodriguez TM, Fornaciari G, Luciani S, Dowd SE, Toranzos GA et al. Gut microbiome of an 11th century A.D. Pre-Columbian Andean mummy. PLoS One 2015; 10:e0138135 [View Article]
    [Google Scholar]
  161. Lugli GA, Milani C, Mancabelli L, Turroni F, Ferrario C et al. Ancient bacteria of the Ötzi’s microbiome: a genomic tale from the Copper Age.. Microbiome 2017; 5:
    [Google Scholar]
  162. Smith LD. The occurrence of Clostridium botulinum and Clostridium tetani in the soil of the United States. Health laboratory science 1978; 15:74–80
    [Google Scholar]
  163. D’Costa VM, King CE, Kalan L, Morar M, Sung WWL et al. Antibiotic resistance is ancient. Nature 2011; 477:457–461 [View Article]
    [Google Scholar]
  164. Segawa T, Takeuchi N, Fujita K, Aizen VB, Willerslev E et al. Demographic analysis of cyanobacteria based on the mutation rates estimated from an ancient ice core. Heredity 2018; 120:562–573 [View Article]
    [Google Scholar]
  165. McAdam PR, Templeton KE, Edwards GF, Holden MTG, Feil EJ et al. Molecular tracing of the emergence, adaptation, and transmission of hospital-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 2012; 109:9107–9112 [View Article]
    [Google Scholar]
  166. Sheppard AE, Stoesser N, Wilson DJ, Sebra R, Kasarskis A et al. Nested Russian Doll-Like Genetic Mobility Drives Rapid Dissemination of the Carbapenem Resistance Gene blaKPC. Antimicrob Agents Chemother 2016; 60:3767–3778 [View Article]
    [Google Scholar]
  167. Brunson K, Reich D. The promise of Paleogenomics beyond our own species. Trends in Genetics 2019; 35:319–329 [View Article]
    [Google Scholar]
  168. Namouchi A, Guellil M, Kersten O, Hänsch S, Ottoni C et al. Integrative approach using Yersinia pestis genomes to revisit the historical landscape of plague during the Medieval Period. Proc Natl Acad Sci USA 2018; 115:E11790–E11797 [View Article]
    [Google Scholar]
  169. Rascovan N, Sjögren K-G, Kristiansen K, Nielsen R, Willerslev E et al. Emergence and Spread of Basal Lineages of Yersinia pestis during the Neolithic Decline. Cell 2019; 176:295–305 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000384
Loading
/content/journal/mgen/10.1099/mgen.0.000384
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error