Pan-genome Analysis of Ancient and Modern Salmonella enterica Demonstrates Genomic Stability of the Invasive Para C Lineage for Millennia

Zhemin Zhou*, Inge Lundstrøm, Alicia Tran-Dien, Sebastián Duchêne, Nabil Fareed Alikhan, Martin J. Sergeant, Gemma Langridge, Anna K. Fotakis, Satheesh Nair, Hans K. Stenøien, Stian S. Hamre, Sherwood Casjens, Axel Christophersen, Christopher Quince, Nicholas R. Thomson, François Xavier Weill, Simon Y.W. Ho, M. Thomas P. Gilbert, Mark Achtman

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

38 Citations (Scopus)

Abstract

Salmonella enterica serovar Paratyphi C causes enteric (paratyphoid) fever in humans. Its presentation can range from asymptomatic infections of the blood stream to gastrointestinal or urinary tract infection or even a fatal septicemia [1]. Paratyphi C is very rare in Europe and North America except for occasional travelers from South and East Asia or Africa, where the disease is more common [2, 3]. However, early 20 th -century observations in Eastern Europe [3, 4] suggest that Paratyphi C enteric fever may once have had a wide-ranging impact on human societies. Here, we describe a draft Paratyphi C genome (Ragna) recovered from the 800-year-old skeleton (SK152) of a young woman in Trondheim, Norway. Paratyphi C sequences were recovered from her teeth and bones, suggesting that she died of enteric fever and demonstrating that these bacteria have long caused invasive salmonellosis in Europeans. Comparative analyses against modern Salmonella genome sequences revealed that Paratyphi C is a clade within the Para C lineage, which also includes serovars Choleraesuis, Typhisuis, and Lomita. Although Paratyphi C only infects humans, Choleraesuis causes septicemia in pigs and boar [5] (and occasionally humans), and Typhisuis causes epidemic swine salmonellosis (chronic paratyphoid) in domestic pigs [2, 3]. These different host specificities likely evolved in Europe over the last ∼4,000 years since the time of their most recent common ancestor (tMRCA) and are possibly associated with the differential acquisitions of two genomic islands, SPI-6 and SPI-7. The tMRCAs of these bacterial clades coincide with the timing of pig domestication in Europe [6]. Zhou et al. reshape our understandings of the origins of an invasive bacterial pathogen, Salmonella enterica Paratyphi C, by combining a reconstructed pan-genome from an 800-year-old skeleton in Norway with 221 genomes from modern bacteria.

Original languageEnglish
Pages (from-to)2420-2428.e10
JournalCurrent Biology
Volume28
Issue number15
DOIs
Publication statusPublished - 6 Aug 2018

Bibliographical note

Funding Information:
EnteroBase ( BBSRC BB/L020319/1 ) was developed by N.-F.A., M.J.S., and Z.Z. (equal contributions) under guidance by M.A. Additional grant support was from the Wellcome Trust ( 202792/Z/16/Z ), Medical Research Council ( MR/M50161X/1 ), Grundforksningfonden ( DNRF 94 ) and Lundbeckfonden ( R52-5062 ), the French government ( ANR-10-LABX-62-IBEID ), the Institut Pasteur , Santé Publique France , and Fondation Le Roch-Les Mousquertaires . We thank A. Murat Eren for assistance with implementation of Anvi’o in EnteroBase, and we thank Siavash Mirarab and Tandy Warnow for advice on Astrid and running Astral-II. We thank Birgitte Skar for permission to sample the skeletal material and the Danish National High-Throughput DNA Sequencing Centre for technical assistance with data generation. We thank Monica H. Green, Timothy P. Newfield, and Francois Balloux for helpful comments on the manuscript.

Funding Information:
EnteroBase (BBSRC BB/L020319/1) was developed by N.-F.A., M.J.S., and Z.Z. (equal contributions) under guidance by M.A. Additional grant support was from the Wellcome Trust (202792/Z/16/Z), Medical Research Council (MR/M50161X/1), Grundforksningfonden (DNRF 94) and Lundbeckfonden (R52-5062), the French government (ANR-10-LABX-62-IBEID), the Institut Pasteur, Sant? Publique France, and Fondation Le Roch-Les Mousquertaires. We thank A. Murat Eren for assistance with implementation of Anvi'o in EnteroBase, and we thank Siavash Mirarab and Tandy Warnow for advice on Astrid and running Astral-II. We thank Birgitte Skar for permission to sample the skeletal material and the Danish National High-Throughput DNA Sequencing Centre for technical assistance with data generation. We thank Monica H. Green, Timothy P. Newfield, and Francois Balloux for helpful comments on the manuscript.

Publisher Copyright:
© 2018 The Authors

Keywords

  • Ancient DNA
  • Salmonella enterica
  • enteric fever
  • genomic stability
  • historical infections
  • host jump
  • pan-genome
  • paratyphoid fever
  • population genomics
  • tMRCA of bacterial pathogens

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