Medical paleomicrobiology: problems and prospects
Abstract
The study of microbial DNA from paleontological and archaeological samples is a powerful tool for estimating the molecular evolution of human pathogens.
The paper is a retrospective of the most significant achievements in medical paleomicrobiology. The subject of discussion is the genetic diversity of ancient microbiomes including pathogenicity and antibiotic resistance genes. Paleomicrobiological studies of permafrost as a repository of pathogenic microbiota are highly promising.
About the Authors
Artemiy E GoncharovRussian Federation
Artemiy E. Goncharov - Ph.D., Dr. Med. Sci, Head of laboratory of functional genomics and proteomics of microorganisms, Institute of experimental medicine, Russian Federation, 197376, Saint-Petersburg, Academic Pavlov st., 12; Professor at the Department of Epidemiology, Parasitology and Disinfectology of North-Western State Medical University named after I.I. Mechnikov, Russian Federation, 191015, Saint-Petersburg, Kirochnaya str., 41, Saint-Petersburg State University, associate professor at the Department of of fundamental problems of medicine and medical technologies, tel. (812) 303-50-00. E-mail: phage1@yandex.ru
Viktoria V Kolodzhieva
Russian Federation
Viktoria V. Kolodzhieva - Ph.D., Associate Professor at the Department of Epidemiology, Parasitology and Disinfectology of North- Western State Medical University named after I.I. Mechnikov, Saint-Petersburg, Russian Federation
References
1. 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. Proc Natl Acad Sci USA. 1998;95:12637–40
2. Tran-Hung, L., Tran-Thi, N., Aboudharam, G., Raoult, D., & Drancourt, M. (2007). A new method to extract dental pulp DNA: application to universal detection of bacteria. PLoS One, 2(10), e1062.
3. Spyrou, M. A., Bos, K. I., Herbig, A., & Krause, J. (2019). Ancient pathogen genomics as an emerging tool for infectious disease research. Nature Reviews Genetics, 20(6), 323-340.
4. Warinner, C., Herbig, A., Mann, A., Fellows Yates, J. A., Weiß, C. L., Burbano, H. A., ... & Krause, J. (2017). A robust framework for microbial archaeology. Annual review of genomics and human genetics, 18, 321-356.
5. Hebsgaard, M. B., Phillips, M. J., & Willerslev, E. (2005). Geologically ancient DNA: fact or artefact?. Trends in microbiology, 13(5), 212-220.
6. Key, F. M., Posth, C., Krause, J., Herbig, A., & Bos, K. I. (2017). Mining metagenomic data sets for ancient DNA: recommended protocols for authentication. Trends in Genetics, 33(8), 508-520.
7. Guellil, M., Kersten, O., Namouchi, A., Bauer, E. L., Derrick, M., Jensen, A. Ø., ... & Bramanti, B. (2018). Genomic blueprint of a relapsing fever pathogen in 15th century Scandinavia. Proceedings of the National Academy of Sciences, 115(41), 10422-10427.
8. Drancourt, M., Tran-Hung, L., Courtin, J., Lumley, H. D., & Raoult, D. (2005). Bartonella quintana in a 4000-year-old human tooth. The Journal of infectious diseases, 191(4), 607-611.
9. Kay, G. L., Sergeant, M. J., Giuffra, V., Bandiera, P., Milanese, M., Bramanti, B., ... & Pallen, M. J. (2014). Recovery of a medieval Brucella melitensis genome using shotgun metagenomics. MBio, 5(4).
10. Maixner, F., Krause-Kyora, B., Turaev, D., Herbig, A., Hoopmann, M. R., Hallows, J. L., ... & O’Sullivan, N. (2016). The 5300-year-old Helicobacter pylori genome of the Iceman. Science, 351(6269), 162-165.
11. Rafi, A., Spigelman, M., Stanford, J., Lemma, E., Donoghue, H., & Zias, J. (1994). Mycobacterium leprae DNA from ancient bone detected by PCR. The Lancet, 343(8909), 1360-1361.
12. Hershkovitz I, Donoghue HD, Minnikin DE, Besra GS, Lee O-Y, Gernaey AM, Galili E, Eshed V, Greenblatt CL, Lemma E, Bar-Gal GK, Spigelman M. 2008. Detection and molecular characterization of 9,000-year-old Mycobacterium tuberculosis from a Neolithic settlement in the Eastern Mediterranean. PLoS One 3:e3426. http://dx.doi.org/10.1371/journal.pone.0003426.
13. Zhou Z, Lundstrøm I, Tran-Dien A, 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(15):2420-2428.e10. doi:10.1016/j.cub.2018.05.058
14. Schuenemann, V. J., Kumar Lankapalli, A., Barquera, R., Nelson, E. A., Iraíz Hernández, D., Acuña Alonzo, V., ... & Krause, J. (2018). Historic Treponema pallidum genomes from Colonial Mexico retrieved from archaeological remains. PLoS neglected tropical diseases, 12(6), e0006447.
15. Devault AM, et al. Second-pandemic strain of Vibrio cholerae from the Philadelphia cholera outbreak of 1849. N. Engl. J. Med. 2014;370:334–340. doi: 10.1056/NEJMoa1308663
16. Spyrou, M.A., Tukhbatova, R.I., Wang, C. et al. Analysis of 3800-year-old Yersinia pestis genomes suggests Bronze Age origin for bubonic plague. Nat Commun 9, 2234 (2018). https://doi.org/10.1038/s41467-018-04550-9
17. Mühlemann, B., Jones, T.C., Damgaard, P. et al. Ancient hepatitis B viruses from the Bronze Age to the Medieval period. Nature 557, 418–423 (2018). https://doi.org/10.1038/s41586-018-0097-z
18. Taubenberger J, Reid A, Lourens R, Wang R, Jin G, Fanning T. Characterization of the 1918 influenza virus polymerase genes. Nature. 2005;437(7060):889-893. doi:10.1038/nature04230
19. Mühlemann, B., Vinner, L., Margaryan, A., Wilhelmson, H., de la Fuente Castro, C., Allentoft, M. E., ... & Bill, J. (2020). Diverse variola virus (smallpox) strains were widespread in northern Europe in the Viking Age. Science, 369(6502).
20. Aufderheide, A. C., Salo, W., Madden, M., Streitz, J., Buikstra, J., Guhl, F., Arriaza, B., Renier, C., Wittmers, L. E., Jr., Fornaciari, G.and Allison, M. (2004). A 9,000-year record of Chagas’ disease. Proceedings of the National Academy of Sciences of the United States of America 101, 2034–2039
21. Nerlich, A. G., Schraut, B., Dittrich, S., Jelinek, T. and Zink, A. R. (2008). Plasmodium falciparum in Ancient Egypt. Emerging Infectious Diseases 14, 1317–1319
22. Petrigh, R. S., Martínez, J. G., Mondini, M., & Fugassa, M. H. (2019). Ancient parasitic DNA reveals Toxascaris leonina presence in Final Pleistocene of South America. Parasitology, 146(10), 1284-1288.
23. Taylor GM, Crossey M, Saldanha J, Waldron T (1996) Mycobacterium tuberculosis identified in mediaeval human skeletal remains using polymerase chain reaction. J Archaeol Sci 23: 789–798.
24. Rothschild BM, Martin LD, Lev G, Bercovier H, Bar-Gal GK, et al. (2001) Mycobacterium tuberculosis complex DNA from an extinct bison dated 17,000 years before the present. Clin Infect Dis 33: 305–311
25. Schuenemann, V. J., Avanzi, C., Krause-Kyora, B., Seitz, A., Herbig, A., Inskip, S., ... & Taylor, G. M. (2018). Ancient genomes reveal a high diversity of Mycobacterium leprae in medieval Europe. PLoS pathogens, 14(5), e1006997
26. Kolman, C. J., Centurion-Lara, A., Lukehart, S. A., Owsley, D. W., & Tuross, N. (1999). Identification of Treponema pallidum subspecies pallidum in a 200-year-old skeletal specimen. Journal of Infectious Diseases, 180(6), 2060-2063
27. Simón, M., Montiel, R., Smerling, A., Solórzano, E., Díaz, N., Álvarez-Sandoval, B. A., ... & Malgosa, A. (2014). Molecular analysis of ancient caries. Proceedings of the Royal Society B: Biological Sciences, 281(1790), 20140586.
28. Bos, K. I., Schuenemann, V. J., Golding, G. B., Burbano, H. A., Waglechner, N., Coombes, B. K., Wood, J. (2011). A draft genome of Yersinia pestis from victims of the Black Death. Nature, 478(7370), 506-510
29. Haensch, S., Bianucci, R., Signoli, M., Rajerison, M., Schultz, M., Kacki, S., Carniel, E. (2010). Distinct clones of Yersinia pestis caused the black death. PLoS Pathog, 6(10), e1001134
30. Namouchi, A., Guellil, M., Kersten, O., Hänsch, S., Ottoni, C., Schmid, B. V., ... & Derrick, M. (2018). Integrative approach using Yersinia pestis genomes to revisit the historical landscape of plague during the Medieval Period. Proceedings of the National Academy of Sciences, 115(50), E11790-E11797. https://doi.org/10.1073/pnas.1812865115
31. Harbeck, M., Seifert, L., Hänsch, S., Wagner, D. M., Birdsell, D., Parise, K. L., ... & Zöller, L. (2013). Yersinia pestis DNA from skeletal remains from the 6th century AD reveals insights into Justinianic Plague. PLoS Pathogens, 9(5), e1003349
32. Feldman, M., Harbeck, M., Keller, M., Spyrou, M. A., Rott, A., Trautmann, B., ... & Bos, K. (2016). A high-coverage Yersinia pestis genome from a sixth-century Justinianic plague victim. Molecular biology and evolution, 33(11), 2911-2923.
33. Rasmussen, S., Allentoft, M., Nielsen, K., Orlando, L., Sikora, M., Pedersen, A., ... & Epimakhov, A. (2015). Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell, 163(3), 571-582.
34. Alcamí, A. (2020). Was smallpox a widespread mild disease? Science, 369(6502), 376-377. DOI: 10.1126/science.abd1214
35. Morono, Y., Ito, M., Hoshino, T. et al. Aerobic microbial life persists in oxic marine sediment as old as 101.5 million years. Nat Commun 11, 3626 (2020). https://doi.org/10.1038/s41467-020-17330-1
36. Gilichinsky, D. A., Wilson, G. S., Friedmann, E. I., McKay, C. P., Sletten, R. S., Rivkina, E. M., ... & Shcherbakova, V. A. (2007). Microbial populations in Antarctic permafrost: biodiversity, state, age, and implication for astrobiology. Astrobiology, 7(2), 275-311.
37. Vishnivetskaya, T. A., & Kathariou, S. (2005). Putative transposases conserved in Exiguobacterium isolates from ancient Siberian permafrost and from contemporary surface habitats. Applied and Environmental Microbiology, 71(11), 6954-6962.
38. Hueffer K, Drown D, Romanovsky V, Hennessy T. Factors Contributing to Anthrax Outbreaks in the Circumpolar North. Ecohealth. 2020;17(1):174-180. doi:10.1007/s10393-020-01474-z
39. Grigoriev SE, Fisher DC, Obadă T, ShirleyEA, Rountrey AN, Savvinov GN, Garmaeva DK, Novgorodov GP, Cheprasov MY, Vasilev SE, Goncharov AE, Masharskiy A., Egorova VE, Petrova PP, Egorova EE, Akhremenko YaA, van der Plicht J, Galanin AA, Fedorov SE, Ivanov EV& Tikhonov AN. A woolly mammoth (Mammuthus primigenius) carcass from Maly Lyakhovsky Island (New Siberian Islands, Russian Federation). Quaternary Int. 2017; 445: 89-103.
40. Goncharov A, Grigorjev S, Karaseva A, et al. Draft Genome Sequence of Enterococcus faecium Strain 58m, Isolated from Intestinal Tract Content of a Woolly Mammoth, Mammuthus primigenius. Genome Announc. 2016;4(1):e01706-15. Published 2016 Feb 11. doi:10.1128/genomeA.01706-15
41. Timofeev V, Bahtejeva I, Mironova R, et al. Insights from Bacillus anthracis strains isolated from permafrost in the tundra zone of Russia. PLoS One. 2019;14(5):e0209140. Published 2019 May 22. doi:10.1371/journal.pone.0209140
42. Dabernat H, Thèves C, Bouakaze C, Nikolaeva D, Keyser C, Mokrousov I, Géraut A, Duchesne S, Gérard P, Alexeev AN, Crubézy E, Ludes B. & Crubézy E. Tuberculosis epidemiology and selection in an autochthonous Siberian population from the 16th-19th century. PloS One. 2014; 9(2): e89877. doi: 10.1371/journal.pone.0089877
43. Biagini P, Thèves C, Balaresque P, et al. Variola virus in a 300-year-old Siberian mummy. N Engl J Med. 2012;367(21):2057-2059. doi:10.1056/NEJMc1208124
44. Sajjad W, Rafiq M, Din G, et al. Resurrection of inactive microbes and resistome present in the natural frozen world: Reality or myth? [published correction appears in Sci Total Environ. 2020 Jun 23;:140107]. Sci Total Environ. 2020;735:139275. doi:10.1016/j.scitotenv.2020.139275
45. D’Costa, V. M., King, C. E., Kalan, L., Morar, M., Sung, W. W., Schwarz, C., ... & Golding, G. B. (2011). Antibiotic resistance is ancient. Nature, 477(7365), 457-461.
46. Petrova M, Gorlenko Z, Mindlin S. 2011. Tn5045, a novel integron-containing antibiotic and chromate resistance transposon isolated from a permafrost bacterium. Res Microbiol 162: 337–345.
47. Petrova M., Kurakov A., Shcherbatova N., Mindlin S. Genetic structure and biological properties of the first ancient multiresistance plasmid isolated from a permafrost bacterium // Microbiology.— 2014.— Vol. 160, ¹ 10.— P. 2253–2263. doi: 10.1099/mic.0.079335–0.
48. Kerfahi, D., Tripathi, B. M., Dong, K., Kim, M., Kim, H., Slik, J. F., ... & Adams, J. M. (2019). From the high Arctic to the equator: do soil metagenomes differ according to our expectations? Microbial ecology, 77(1), 168-185
Review
For citations:
Goncharov A.E., Kolodzhieva V.V. Medical paleomicrobiology: problems and prospects. Antibiot Khimioter = Antibiotics and Chemotherapy. 2021;66(5-6).
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