Genomic perspective on the bacillus causing paratyphoid B fever

Jane Hawkey; Lise Frézal; Alicia Tran Dien; Anna Zhukova; Derek Brown; Marie Anne Chattaway; Sandra Simon; Hidemasa Izumiya; Patricia I. Fields; Niall De Lappe; Lidia Kaftyreva; Xuebin Xu; Junko Isobe; Dominique Clermont; Elisabeth Njamkepo; Yukihiro Akeda; Sylvie Issenhuth-Jeanjean; Mariia Makarova; Yanan Wang; Martin Hunt; Brent M. Jenkins; Magali Ravel; Véronique Guibert; Estelle Serre; Zoya Matveeva; Laëtitia Fabre; Martin Cormican; Min Yue; Baoli Zhu; Masatomo Morita; Zamin Iqbal; Carolina Silva Nodari; Maria Pardos de la Gandara; François Xavier Weill

doi:10.1038/s41467-024-54418-4

Genomic perspective on the bacillus causing paratyphoid B fever

Jane Hawkey, Lise Frézal, Alicia Tran Dien, Anna Zhukova, Derek Brown, Marie Anne Chattaway, Sandra Simon, Hidemasa Izumiya, Patricia I. Fields, Niall De Lappe, Lidia Kaftyreva, Xuebin Xu, Junko Isobe, Dominique Clermont, Elisabeth Njamkepo, Yukihiro Akeda, Sylvie Issenhuth-Jeanjean, Mariia Makarova, Yanan Wang, Martin HuntBrent M. Jenkins, Magali Ravel, Véronique Guibert, Estelle Serre, Zoya Matveeva, Laëtitia Fabre, Martin Cormican, Min Yue, Baoli Zhu, Masatomo Morita, Zamin Iqbal, Carolina Silva Nodari, Maria Pardos de la Gandara, François Xavier Weill

Research output: Contribution to journal › Article › peer-review

Abstract

Paratyphoid B fever (PTB) is caused by an invasive lineage (phylogroup 1, PG1) of Salmonella enterica serotype Paratyphi B (SPB). However, little was known about the global population structure, geographic distribution, and evolution of this pathogen. Here, we report a whole-genome analysis of 568 historical and contemporary SPB PG1 isolates, obtained globally, between 1898 and 2021. We show that this pathogen existed in the 13th century, subsequently diversifying into 11 lineages and 38 genotypes with strong phylogeographic patterns. Following its discovery in 1896, it circulated across Europe until the 1970s, after which it was mostly reimported into Europe from South America, the Middle East, South Asia, and North Africa. Antimicrobial resistance recently emerged in various genotypes of SPB PG1, mostly through mutations of the quinolone-resistance-determining regions of gyrA and gyrB. This study provides an unprecedented insight into SPB PG1 and essential genomic tools for identifying and tracking this pathogen, thereby facilitating the global genomic surveillance of PTB.

Original language	English
Article number	10143
Journal	Nature Communications
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41467-024-54418-4
Publication status	Published - 10 Dec 2024

Data Availability Statement

The publicly available sequences used in this study are available from GenBank (https://www.ncbi.nlm.nih.gov/genbank/) under accession numbers NC_028699, NC_026014, NC_010102.1, CP074225.1, L78932, NZ_CP065185, NZ_CP065186.1, NZ_CP065187.1, NZ_CP065188.1, and JWQX00000000.1.

The long-read sequence data generated in this study are available from GenBank under accession numbers CP147895, CP147896, CP147897, CP147898, CP147899, CP147900, CP147901, CP147902, CP147903, CP147904, CP147905, CP147906, and CP147907. The short-read sequence data generated in this study were submitted to EnteroBase (https://enterobase.warwick.ac.uk/) and to the European Nucleotide Archive (ENA, https://www.ebi.ac.uk/ena/) under study numbers PRJDB11608, PRJEB18998, PRJEB28356, PRJEB30317, PRJEB67705, PRJNA248792, PRJEB68323, PRJEB49424, PRJEB71958. All the accession numbers of the short-read sequences produced and/or used in this study are listed in Supplementary Data 1 and Supplementary Data 6.

The list of genomes studied (and their assembled short-read data) can be obtained from EnteroBase at: https://enterobase.warwick.ac.uk/species/senterica/search_strains?query=workspace:86468 (diversity dataset, Supplementary Data 1) and: https://enterobase.warwick.ac.uk/species/senterica/search_strains?query=workspace:91222 (surveillance data set, Supplementary Data 6).

The list of 166 genomes (and their assembled short-read data) published by Connor et al.27 and present in EnteroBase can be obtained from https://enterobase.warwick.ac.uk/species/senterica/search_strains?query=workspace:86472 (Supplementary Data 7).

The cgMLST GrapeTrees shown in Supplementary Figs. 1 and 6 can be visualised with EnteroBase at: https://enterobase.warwick.ac.uk/ms_tree?tree_id=92077 and https://enterobase.warwick.ac.uk/ms_tree?tree_id=92095, respectively. Source data are provided with this paper.

Acknowledgements

We thank Prof. Jacques Ravel, Prof. David A. Rasko, Luke Tallon, Kranthi Vavikolanu, and Michael Pietsch for submitting archived or new short reads to a public repository, Susan Van Duyne for ensuring the safe shipping of strains, Anthony M. Smith and Chien-Shun Chiou for reviewing their data, Paul O’Dette for his support, and the sequencing team at the Institut Pasteur (PF1 & P2M-Plateforme de Microbiologie Mutualisée) for sequencing the samples. We also thank all the corresponding laboratories of the French National Reference Centre for Escherichia coli, Shigella, and Salmonella.

Funding

This research was funded by the Fondation Le Roch-Les Mousquetaires (to F.-X.W); Institut Pasteur (to F.-X.W); Santé publique France (to F.-X.W); and by the French Government’s Investissement d’Avenir programme, Laboratoire d’Excellence ‘Integrative Biology of Emerging Infectious Diseases’ (grant no. ANR-10-LABX-62-IBEID to F.-X.W). M.H. was funded by the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Healthcare Associated Infections and Antimicrobial Resistance at Oxford University in partnership with the UK Health Security Agency (NIHR200915), and the NIHR Biomedical Research Centre, Oxford. M.A.C. is affiliated to the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) (NIHR200892) in Genomics and Enabling Data at University of Warwick in partnership with the UK Health Security Agency (UKHSA), in collaboration with Universities of Cambridge and Oxford. M.A.C. is based at UKHSA. The views expressed are those of the authors and not necessarily those of the Centers for Disease Control and Prevention, the NIHR, the Department of Health and Social Care or the UK Health Security Agency. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

ASJC Scopus subject areas

General Chemistry
General Biochemistry,Genetics and Molecular Biology
General Physics and Astronomy

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Cite this

Hawkey, J., Frézal, L., Tran Dien, A., Zhukova, A., Brown, D., Chattaway, M. A., Simon, S., Izumiya, H., Fields, P. I., De Lappe, N., Kaftyreva, L., Xu, X., Isobe, J., Clermont, D., Njamkepo, E., Akeda, Y., Issenhuth-Jeanjean, S., Makarova, M., Wang, Y., ... Weill, F. X. (2024). Genomic perspective on the bacillus causing paratyphoid B fever. Nature Communications, 15(1), Article 10143. https://doi.org/10.1038/s41467-024-54418-4

Hawkey, J, Frézal, L, Tran Dien, A, Zhukova, A, Brown, D, Chattaway, MA, Simon, S, Izumiya, H, Fields, PI, De Lappe, N, Kaftyreva, L, Xu, X, Isobe, J, Clermont, D, Njamkepo, E, Akeda, Y, Issenhuth-Jeanjean, S, Makarova, M, Wang, Y, Hunt, M, Jenkins, BM, Ravel, M, Guibert, V, Serre, E, Matveeva, Z, Fabre, L, Cormican, M, Yue, M, Zhu, B, Morita, M, Iqbal, Z, Silva Nodari, C, Pardos de la Gandara, M & Weill, FX 2024, 'Genomic perspective on the bacillus causing paratyphoid B fever', Nature Communications, vol. 15, no. 1, 10143. https://doi.org/10.1038/s41467-024-54418-4

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Genomic perspective on the bacillus causing paratyphoid B fever

Abstract

Data Availability Statement

Acknowledgements

Funding

ASJC Scopus subject areas

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