Log in

Giant virus-related sequences in the 5300-year-old Ötzi mummy metagenome

  • Short Report
  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

Giant viruses have brought new perspectives on the virosphere. They have been increasingly described in humans, including in several metagenomic studies. Here, we searched into the metagenome of the 5300-year-old Ötzi mummy for the presence of giant virus-related sequences using MG-Digger pipeline. We found 19 reads (0.00006% of the total read number) that best matched (mean ± standard deviation (range) for e-values of 5.0E-6 ± 1.4E-6 (6.0E-5–4.0E-10) and for amino acid identity of 69.9 ± 8.7% (46.4–84.9%) and most significantly with sequences from various giant viruses, including mostly mimiviruses. This expands current knowledge on the ubiquity and relationship with humans of giant viruses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1

References

  1. La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, Birtles R, Claverie JM, Raoult D (2003) A giant virus in amoebae. Science 299:2033

    Article  Google Scholar 

  2. Raoult D, Forterre P (2008) Redefining viruses: lessons from mimivirus. Nat Rev Microbiol 6:315–319

    Article  CAS  Google Scholar 

  3. Colson P, La Scola B, Levasseur A, Caetano-Anolles G, Raoult D (2017) Mimivirus: leading the way in the discovery of giant viruses of amoebae. Nat Rev Microbiol 15:243–254

    Article  CAS  Google Scholar 

  4. Saadi H, Pagnier I, Colson P, Cherif JK, Beji M, Boughalmi M, Azza S, Armstrong N, Robert C, Fournous G, La Scola B, Raoult D (2013) First isolation of mimivirus in a patient with pneumonia. Clin Infect Dis 57:e127–e134

    Article  Google Scholar 

  5. La Scola B, Marrie TJ, Auffray JP, Raoult D (2005) Mimivirus in pneumonia patients. Emerg Infect Dis 11:449–452

    Article  Google Scholar 

  6. Popgeorgiev N, Boyer M, Fancello L, Monteil S, Robert C, Rivet R, Nappez C, Azza S, Chiaroni J, Raoult D, Desnues C (2013) Marseillevirus-like virus recovered from blood donated by asymptomatic humans. J Infect Dis 208:1042–1050

    Article  CAS  Google Scholar 

  7. Popgeorgiev N, Michel G, Lepidi H, Raoult D, Desnues C (2013) Marseillevirus adenitis in an 11-month-old child. J Clin Microbiol 51:4102–4105

    Article  Google Scholar 

  8. Rampelli S, Soverini M, Turroni S, Quercia S, Biagi E, Brigidi P, Candela M (2016) ViromeScan: a new tool for metagenomic viral community profiling. BMC Genomics 17:165–2446

    Article  Google Scholar 

  9. Verneau J, Levasseur A, Raoult D, La Scola B, Colson P (2016) MG-digger: an automated pipeline to search for giant virus-related sequences in metagenomes. Front Microbiol 7:428

    Article  Google Scholar 

  10. Moustafa A, **e C, Kirkness E, Biggs W, Wong E, Turpaz Y, Bloom K, Delwart E, Nelson KE, Venter JC, Telenti A (2017) The blood DNA virome in 8,000 humans. PLoS Pathog 13:e1006292

    Article  Google Scholar 

  11. Ghose C, Ly M, Schwanemann LK, Shin JH, Atab K, Barr JJ, Little M, Schooley RT, Chopyk J, Pride DT (2019) The virome of cerebrospinal fluid: viruses where we once thought there were none. Front Microbiol 10:2061

    Article  Google Scholar 

  12. Levasseur A, Andreani J, Delerce J, Bou Khalil J, Robert C, La Scola B, Raoult D (2016) Comparison of a modern and fossil pithovirus reveals its genetic conservation and evolution. Genome Biol Evol 8:2333–2339

    Article  Google Scholar 

  13. Keller A, Graefen A, Ball M, Matzas M, Boisguerin V, Maixner F, Leidinger P, Backes C, Khairat R, Forster M, Stade B, Franke A, Mayer J, Spangler J, McLaughlin S, Shah M, Lee C, Harkins TT, Sartori A, Moreno-Estrada A, Henn B, Sikora M, Semino O, Chiaroni J, Rootsi S, Myres NM, Cabrera VM, Underhill PA, Bustamante CD, Vigl EE, Samadelli M, Cipollini G, Haas J, Katus H, O’Connor BD, Carlson MR, Meder B, Blin N, Meese E, Pusch CM, Zink A (2012) New insights into the Tyrolean Iceman’s origin and phenotype as inferred by whole-genome sequencing. Nat Commun 3:698

    Article  Google Scholar 

  14. Maixner F, Krause-Kyora B, Turaev D, Herbig A, Hoopmann MR, Hallows JL, Kusebauch U, Vigl EE, Malfertheiner P, Megraud F, O’Sullivan N, Cipollini G, Coia V, Samadelli M, Engstrand L, Linz B, Moritz RL, Grimm R, Krause J, Nebel A, Moodley Y, Rattei T, Zink A (2016) The 5300-year-old Helicobacter pylori genome of the Iceman. Science 351:162–165

    Article  CAS  Google Scholar 

  15. Lugli GA, Milani C, Mancabelli L, Turroni F, Ferrario C, Duranti S, van Sinderen D, Ventura M (2017) Ancient bacteria of the Ötzi’s microbiome: a genomic tale from the copper age. Microbiome 5:5

    Article  Google Scholar 

  16. Abrahao J, Silva L, Silva LS, Khalil JYB, Rodrigues R, Arantes T, Assis F, Boratto P, Andrade M, Kroon EG, Ribeiro B, Bergier I, Seligmann H, Ghigo E, Colson P, Levasseur A, Kroemer G, Raoult D, La Scola B (2018) Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat Commun 9:749–03168

    Article  Google Scholar 

  17. Andreani J, Khalil JYB, Sevvana M, Benamar S, Di Pinto F, Bitam I, Colson P, Klose T, Rossmann MG, Raoult D, La Scola B (2017) Pacmanvirus, a new giant icosahedral virus at the crossroads between asfarviridae and faustoviruses. J Virol 91:e00212–e00217

    Article  Google Scholar 

  18. Bajrai LH, de Assis FL, Azhar EI, Jardot P, Robert C, Abrahao J, Raoult D, La Scola B (2016) Saudi moumouvirus, the first group b mimivirus isolated from Asia. Front Microbiol 7:2029

    Article  Google Scholar 

  19. Colson P, de Lamballerie X, Fournous G, Raoult D (2012) Reclassification of giant viruses composing a fourth domain of life in the new order Megavirales. Intervirology 55:321–332

    Article  Google Scholar 

  20. Boughalmi M, Pagnier I, Aherfi S, Colson P, Raoult D, La Scola B (2013) First isolation of a giant virus from wild hirudo medicinalis leech: mimiviridae isolation in hirudo medicinalis. Viruses 5:2920–2930

    Article  Google Scholar 

  21. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinf 5:113

    Article  Google Scholar 

  22. Price MN, Dehal PS, Arkin AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490

    Article  Google Scholar 

  23. Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242–W245

    Article  CAS  Google Scholar 

  24. Ames SK, Hysom DA, Gardner SN, Lloyd GS, Gokhale MB, Allen JE (2013) Scalable metagenomic taxonomy classification using a reference genome database. Bioinformatics 29:2253–2260

    Article  CAS  Google Scholar 

  25. Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA, Hedlund BP, Tsiamis G, Sievert SM, Liu WT, Eisen JA, Hallam SJ, Kyrpides NC, Stepanauskas R, Rubin EM, Hugenholtz P, Woyke T (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499:431–437

    Article  CAS  Google Scholar 

  26. Rolland C, Andreani J, Louazani AC, Aherfi S, Francis R, Rodrigues R, Silva LS, Sahmi D, Mougari S, Chelkha N, Bekliz M, Silva L, Assis F, Dornas F, Khalil JYB, Pagnier I, Desnues C, Levasseur A, Colson P, Abrahao J, La Scola B (2019) Discovery and further studies on giant viruses at the IHU mediterranee infection that modified the perception of the virosphere. Viruses 11(4):312

    Article  CAS  Google Scholar 

  27. Schulz F, Alteio L, Goudeau D, Ryan EM, Yu FB, Malmstrom RR, Blanchard J, Woyke T (2018) Hidden diversity of soil giant viruses. Nat Commun 9:4881–07335

    Article  Google Scholar 

  28. Boughalmi M, Saadi H, Pagnier I, Colson P, Fournous G, Raoult D, La Scola B (2012) High-throughput isolation of giant viruses of the Mimiviridae and Marseilleviridae families in the Tunisian environment. Environ Microbiol 15(7):2000–2007

    Article  Google Scholar 

  29. Schulz F, Yutin N, Ivanova NN, Ortega DR, Kwonee T, Vierheilig J, Daims H, Horn M, Wagner M, Jensen GJ, Kyrpides NC, Koonin EV, Woyke T (2017) Giant viruses with an expanded complement of translation system components. Science 356:82–85

    Article  CAS  Google Scholar 

  30. Colson P, Aherfi S, La Scola B (2017) Evidence of giant viruses of amoebae in the human gut. Humic 5–6:14–19

    Google Scholar 

  31. Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY, Keller BC, Kambal A, Monaco CL, Zhao G, Fleshner P, Stappenbeck TS, McGovern DP, Keshavarzian A, Mutlu EA, Sauk J, Gevers D, Xavier RJ, Wang D, Parkes M, Virgin HW (2015) Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160:447–460

    Article  CAS  Google Scholar 

  32. Colson P, Fancello L, Gimenez G, Armougom F, Desnues C, Fournous G, Yoosuf N, Million M, La Scola B, Raoult D (2013) Evidence of the megavirome in humans. J Clin Virol 57:191–200

    Article  CAS  Google Scholar 

  33. Saadi H, Reteno DG, Colson P, Aherfi S, Minodier P, Pagnier I, Raoult D, La Scola B (2013) Shan virus: a new mimivirus isolated from the stool of a Tunisian patient with pneumonia. Intervirology 56:424–429

    Article  Google Scholar 

  34. Appelt S, Fancello L, Le Bailly M, Raoult D, Drancourt M, Desnues C (2014) Viruses in a 14th-century coprolite. Appl Environ Microbiol 80:2648–2655

    Article  Google Scholar 

Download references

Funding

Funding

This work was supported by the French Government under the “Investments for the Future” program managed by the National Agency for Research (ANR), Méditerranée-Infection 10-IAHU-03 and was also supported by Région Provence Alpes Côte d’Azur and European funding FEDER PRIMMI (Fonds Européen de Développement Régional - Plateformes de Recherche et d'Innovation Mutualisées Méditerranée Infection).

Author information

Authors and Affiliations

Authors

Contributions

Authors contribution

Conceived and designed the experiments: PC and BLS. Contributed materials/analysis tools: GAPS, CR, BN and PC. Analyzed the data: GAPS, CR, BN, BLS and PC Wrote the paper: GAPS and PC.

Corresponding author

Correspondence to Philippe Colson.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare. Funding sources had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the manuscript.

Additional information

Edited by Hartmut Hengel.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pires de Souza, G.A., Rolland, C., Nafeh, B. et al. Giant virus-related sequences in the 5300-year-old Ötzi mummy metagenome. Virus Genes 57, 222–227 (2021). https://doi.org/10.1007/s11262-021-01823-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-021-01823-2

Keywords

Navigation