Identification of microbial pathogens in Neolithic Scandinavian humans.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
07 Mar 2024
Historique:
received: 01 06 2023
accepted: 01 03 2024
medline: 8 3 2024
pubmed: 8 3 2024
entrez: 7 3 2024
Statut: epublish

Résumé

With the Neolithic transition, human lifestyle shifted from hunting and gathering to farming. This change altered subsistence patterns, cultural expression, and population structures as shown by the archaeological/zooarchaeological record, as well as by stable isotope and ancient DNA data. Here, we used metagenomic data to analyse if the transitions also impacted the microbiome composition in 25 Mesolithic and Neolithic hunter-gatherers and 13 Neolithic farmers from several Scandinavian Stone Age cultural contexts. Salmonella enterica, a bacterium that may have been the cause of death for the infected individuals, was found in two Neolithic samples from Battle Axe culture contexts. Several species of the bacterial genus Yersinia were found in Neolithic individuals from Funnel Beaker culture contexts as well as from later Neolithic context. Transmission of e.g. Y. enterocolitica may have been facilitated by the denser populations in agricultural contexts.

Identifiants

pubmed: 38453993
doi: 10.1038/s41598-024-56096-0
pii: 10.1038/s41598-024-56096-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

5630

Subventions

Organisme : Vetenskapsrådet
ID : 2017-02503
Organisme : Vetenskapsrådet
ID : 2019-00849
Organisme : Riksbankens Jubileumsfond
ID : P21-0266
Organisme : Riksbankens Jubileumsfond
ID : P19.0740:1

Informations de copyright

© 2024. The Author(s).

Références

Skoglund, P. et al. Origins and genetic legacy of neolithic farmers and hunter-gatherers in Europe. Science 336, 466–469 (2012).
doi: 10.1126/science.1216304
Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409–413 (2014).
doi: 10.1038/nature13673
Gron, K. J. & Sørensen, L. Cultural and economic negotiation: A new perspective on the neolithic transition of southern Scandinavia. Antiquity 92, 958–974 (2018).
doi: 10.15184/aqy.2018.71
Larsson, M. & Rzepecki, S. Pottery, houses and graves: The early Funnel Beaker culture in southern Sweden and central Poland. Lund Archaeol. Rev. 8–9, 1–21 (2005).
Skoglund, P. et al. Genomic diversity and admixture differs for stone-age Scandinavian foragers and farmers. Science 344, 747–750 (2014).
doi: 10.1126/science.1253448
Günther, T. et al. Population genomics of Mesolithic Scandinavia: Investigating early postglacial migration routes and high-latitude adaptation. PLoS Biol. 16, 1–22 (2018).
doi: 10.1371/journal.pbio.2003703
Sánchez-Quinto, F. et al. Megalithic tombs in western and northern Neolithic Europe were linked to a kindred society. Proc. Natl. Acad. Sci. U. S. A. 116, 9469–9474 (2019).
doi: 10.1073/pnas.1818037116
Larsson, Å. M. Taking out the trash: On excavating settlements in general, and houses of the battle axe culture in particular. Curr. Swedish Archaeol. 16, 111–136 (2008).
doi: 10.37718/CSA.2008.07
Wehlin, J. Arkeologisk undersökning vid Orsandbaden av en mesolitisk slagplats inom stenåldersboplatsen Leksand 2001, Noret 62: 64, Leksands kommun, Dalarna. Dalarnas Museum. Arkeol. Rapp. 12 (2015).
Malmström, H. et al. Ancient mitochondrial DNA from the northern fringe of the Neolithic farming expansion in Europe sheds light on the dispersion process. Philos. Trans. R. Soc. B Biol. Sci. 370, 20130373 (2015).
doi: 10.1098/rstb.2013.0373
Malmström, H. et al. The genomic ancestry of the Scandinavian Battle axe culture people and their relation to the broader Corded Ware horizon. Proc. R. Soc. B Biol. Sci. 286, 20191528 (2019).
doi: 10.1098/rspb.2019.1528
Coutinho, A. et al. The Neolithic Pitted Ware culture foragers were culturally but not genetically influenced by the Battle Axe culture herders. Am. J. Phys. Anthropol. 172, 638–649 (2020).
doi: 10.1002/ajpa.24079
Weisdorf, J. L. From foraging to farming: The So-called ‘Neolithic revolution’. J. Econ. Surv. 19, 561–586 (2005).
doi: 10.1111/j.0950-0804.2005.00259.x
Armelagos, G. J. & Dewey, J. R. Evolutionary response to human infectious diseases. Bioscience 20, 271–275 (1970).
doi: 10.2307/1295204
Fournié, G., Pfeiffer, D. U. & Bendrey, R. Early animal farming and zoonotic disease dynamics: Modelling brucellosis transmission in Neolithic goat populations. R. Soc. Open Sci. 4, 160943 (2017).
doi: 10.1098/rsos.160943
Bos, K. I. et al. A draft genome of Yersinia pestis from victims of the Black Death. Nature 478, 506–510 (2011).
doi: 10.1038/nature10549
Haller, M. et al. Mass burial genomics reveals outbreak of enteric paratyphoid fever in the Late Medieval trade city Lübeck. iScience 24, 102419 (2021).
doi: 10.1016/j.isci.2021.102419
Spyrou, M. A. et al. The source of the Black Death in fourteenth-century central Eurasia. Nature https://doi.org/10.1038/s41586-022-04800-3 (2022).
doi: 10.1038/s41586-022-04800-3
Rascovan, N. et al. Emergence and spread of basal lineages of Yersinia pestis during the Neolithic Decline. Cell 176, 295-305.e10 (2019).
doi: 10.1016/j.cell.2018.11.005
Adler, C. J. et al. Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions. Nat. Genet. 45, 450–455 (2013).
doi: 10.1038/ng.2536
Wibowo, M. C. et al. Reconstruction of ancient microbial genomes from the human gut. Nature 594, 234–239 (2021).
doi: 10.1038/s41586-021-03532-0
Fraser, M. et al. New insights on cultural dualism and population structure in the Middle Neolithic Funnel Beaker culture on the island of Gotland. J. Archaeol. Sci. Rep. 17, 325–334 (2018).
Margaryan, A. et al. Ancient pathogen DNA in human teeth and petrous bones. Ecol. Evol. 8, 3534–3542 (2018).
doi: 10.1002/ece3.3924
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10–12 (2011).
doi: 10.14806/ej.17.1.200
Pochon, Z. et al. aMeta: An accurate and memory-efficient ancient metagenomic profiling workflow. Genome Biol. 24, 242 (2023).
doi: 10.1186/s13059-023-03083-9
Breitwieser, F. P., Baker, D. N. & Salzberg, S. L. KrakenUniq: Confident and fast metagenomics classification using unique k-mer counts. Genome Biol. 19, 1–10 (2018).
doi: 10.1186/s13059-018-1568-0
Herbig, A. et al. MALT: Fast alignment and analysis of metagenomic DNA sequence data applied to the Tyrolean Iceman. biorXiv https://doi.org/10.1101/050559 (2016).
doi: 10.1101/050559
Hübler, R. et al. HOPS: Automated detection and authentication of pathogen DNA in archaeological remains. bioRxiv https://doi.org/10.1101/534198 (2019).
doi: 10.1101/534198
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
doi: 10.1093/bioinformatics/btp352
Skoglund, P. et al. Separating endogenous ancient DNA from modern day contamination in a Siberian Neandertal. Proc. Natl. Acad. Sci. U. S. A. 111, 2229–2234 (2014).
doi: 10.1073/pnas.1318934111
Huson, D. H. et al. MEGAN community edition - Interactive exploration and analysis of large-scale microbiome sequencing data. PLOS Comput. Biol. 12, e1004957 (2016).
doi: 10.1371/journal.pcbi.1004957
Nielsen, S. H. et al. Common childhood infections (2021).
Moore, G., Tessler, M., Cunningham, S. W., Betancourt, J. & Harbert, R. Paleo-metagenomics of north American fossil packrat middens: Past biodiversity revealed by ancient DNA. Ecol. Evol. 10, 2530–2544 (2020).
doi: 10.1002/ece3.6082
Warinner, C. et al. Pathogens and host immunity in the ancient human oral cavity. Nat. Genet. 46, 336–344 (2014).
doi: 10.1038/ng.2906
Eerkens, J. W. et al. A probable prehistoric case of meningococcal disease from San Francisco Bay: Next generation sequencing of Neisseria meningitidis from dental calculus and osteological evidence. Int. J. Paleopathol. 22, 173–180 (2018).
doi: 10.1016/j.ijpp.2018.05.001
Rasmussen, S. et al. Early divergent strains of yersinia pestis in Eurasia 5,000 Years Ago. Cell 163, 571–582 (2015).
doi: 10.1016/j.cell.2015.10.009
Sabina, Y., Rahman, A., Ray, R. C. & Montet, D. Yersinia enterocolitica: Mode of transmission, molecular insights of virulence, and pathogenesis of infection. J. Pathog. 2011, 1–10 (2011).
doi: 10.4061/2011/429069
Key, F. M. et al. Emergence of human-adapted Salmonella enterica is linked to the Neolithization process. Nat. Ecol. Evol. 4, 324–333 (2020).
doi: 10.1038/s41559-020-1106-9
Gal-Mor, O., Boyle, E. C. & Grassl, G. A. Same species, different diseases: How and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front. Microbiol. 5, 391 (2014).
doi: 10.3389/fmicb.2014.00391
Warinner, C., Speller, C., Collins, M. J. & Lewis, C. M. Ancient human microbiomes. J. Hum. Evol. 79, 125–136 (2015).
doi: 10.1016/j.jhevol.2014.10.016

Auteurs

Nora Bergfeldt (N)

Centre for Palaeogenetics, Stockholm University, Stockholm, Sweden. nora.bergfeldt@zoologi.su.se.
Department of Zoology, Stockholm University, Stockholm, Sweden. nora.bergfeldt@zoologi.su.se.
Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden. nora.bergfeldt@zoologi.su.se.

Emrah Kırdök (E)

Department of Biotechnology, Faculty of Science, Mersin University, Mersin, Turkey.

Nikolay Oskolkov (N)

Science for Life Laboratory, Department of Biology, National Bioinformatics Infrastructure Sweden, Lund University, Lund, Sweden.

Claudio Mirabello (C)

Science for Life Laboratory, Department of Physics, Chemistry and Biology, National Bioinformatics Infrastructure Sweden, Linköping University, Linköping, Sweden.

Per Unneberg (P)

Science for Life Laboratory, Department of Cell and Molecular Biology, National Bioinformatics Infrastructure Sweden, Uppsala University, Uppsala, Sweden.

Helena Malmström (H)

Human Evolution, Department of Organism Biology, Uppsala University, Uppsala, Sweden.

Magdalena Fraser (M)

Human Evolution, Department of Organism Biology, Uppsala University, Uppsala, Sweden.

Federico Sanchez-Quinto (F)

Human Evolution, Department of Organism Biology, Uppsala University, Uppsala, Sweden.

Roger Jorgensen (R)

Tromsø University Museum, University of Tromsø-The Arctic University of Norway, Tromsø, Norway.

Birgitte Skar (B)

Department of Archaeology and Cultural History, NTNU University Museum, Trondheim, Norway.

Kerstin Lidén (K)

Department of Archaeology and Classical Studies, Stockholm University, Stockholm, Sweden.

Mattias Jakobsson (M)

Human Evolution, Department of Organism Biology, Uppsala University, Uppsala, Sweden.

Jan Storå (J)

Department of Archaeology and Classical Studies, Stockholm University, Stockholm, Sweden.

Anders Götherström (A)

Centre for Palaeogenetics, Stockholm University, Stockholm, Sweden.
Department of Archaeology and Classical Studies, Stockholm University, Stockholm, Sweden.

Classifications MeSH