Global population structure and genotyping framework for genomic surveillance of the major dysentery pathogen, Shigella sonnei

Jane Hawkey; Kalani Paranagama; Kate S. Baker; Rebecca J. Bengtsson; François Xavier Weill; Nicholas R. Thomson; Stephen Baker; Louise Cerdeira; Zamin Iqbal; Martin Hunt; Danielle J. Ingle; Timothy J. Dallman; Claire Jenkins; Deborah A. Williamson; Kathryn E. Holt

doi:10.1038/s41467-021-22700-4

Global population structure and genotyping framework for genomic surveillance of the major dysentery pathogen, Shigella sonnei

Jane Hawkey^*, Kalani Paranagama, Kate S. Baker, Rebecca J. Bengtsson, François Xavier Weill, Nicholas R. Thomson, Stephen Baker, Louise Cerdeira, Zamin Iqbal, Martin Hunt, Danielle J. Ingle, Timothy J. Dallman, Claire Jenkins, Deborah A. Williamson, Kathryn E. Holt

^*Corresponding author for this work

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Abstract

Shigella sonnei is the most common agent of shigellosis in high-income countries, and causes a significant disease burden in low- and middle-income countries. Antimicrobial resistance is increasingly common in all settings. Whole genome sequencing (WGS) is increasingly utilised for S. sonnei outbreak investigation and surveillance, but comparison of data between studies and labs is challenging. Here, we present a genomic framework and genotyping scheme for S. sonnei to efficiently identify genotype and resistance determinants from WGS data. The scheme is implemented in the software package Mykrobe and tested on thousands of genomes. Applying this approach to analyse >4,000 S. sonnei isolates sequenced in public health labs in three countries identified several common genotypes associated with increased rates of ciprofloxacin resistance and azithromycin resistance, confirming intercontinental spread of highly-resistant S. sonnei clones and demonstrating the genomic framework can facilitate monitoring the spread of resistant clones, including those that have recently emerged, at local and global scales.

Original language	English
Article number	2684
Journal	Nature Communications
Volume	12
DOIs	https://doi.org/10.1038/s41467-021-22700-4
Publication status	Published - 11 May 2021

Bibliographical note

Funding Information:
K.E.H. is supported by a Senior Medical Research Fellowship from the Viertel Foundation of Australia, and Bill and Melinda Gates Foundation, Seattle (grant #OPP1175797). K.S.B. is supported by a Wellcome Trust Clinical Research Career Development Fellowship (A/106690/A/14/Z) and RJB through a UKRI MRC New Investigator Research Grant (held by KSB, MR/R020787/1). K.S.B., T.J.D. and C.J. are affiliated to the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Gastrointestinal Infections at University of Liverpool in partnership with Public Health England (PHE), in collaboration with University of Warwick. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health and Social Care or Public Health England. D.A.W. is supported by an Investigator Grant from the National Health and Medical Research Council (NHMRC) of Australia (APP1174555).

Open Access: This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

Publisher Copyright: © 2021, The Author(s).

Citation: Hawkey, J., Paranagama, K., Baker, K.S. et al. Global population structure and genotyping framework for genomic surveillance of the major dysentery pathogen, Shigella sonnei. Nat Commun 12, 2684 (2021).

DOI: https://doi.org/10.1038/s41467-021-22700-4

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Hawkey, J., Paranagama, K., Baker, K. S., Bengtsson, R. J., Weill, F. X., Thomson, N. R., Baker, S., Cerdeira, L., Iqbal, Z., Hunt, M., Ingle, D. J., Dallman, T. J., Jenkins, C., Williamson, D. A., & Holt, K. E. (2021). Global population structure and genotyping framework for genomic surveillance of the major dysentery pathogen, Shigella sonnei. Nature Communications, 12, [2684]. https://doi.org/10.1038/s41467-021-22700-4

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title = "Global population structure and genotyping framework for genomic surveillance of the major dysentery pathogen, Shigella sonnei",

abstract = "Shigella sonnei is the most common agent of shigellosis in high-income countries, and causes a significant disease burden in low- and middle-income countries. Antimicrobial resistance is increasingly common in all settings. Whole genome sequencing (WGS) is increasingly utilised for S. sonnei outbreak investigation and surveillance, but comparison of data between studies and labs is challenging. Here, we present a genomic framework and genotyping scheme for S. sonnei to efficiently identify genotype and resistance determinants from WGS data. The scheme is implemented in the software package Mykrobe and tested on thousands of genomes. Applying this approach to analyse >4,000 S. sonnei isolates sequenced in public health labs in three countries identified several common genotypes associated with increased rates of ciprofloxacin resistance and azithromycin resistance, confirming intercontinental spread of highly-resistant S. sonnei clones and demonstrating the genomic framework can facilitate monitoring the spread of resistant clones, including those that have recently emerged, at local and global scales.",

author = "Jane Hawkey and Kalani Paranagama and Baker, {Kate S.} and Bengtsson, {Rebecca J.} and Weill, {Fran{\c c}ois Xavier} and Thomson, {Nicholas R.} and Stephen Baker and Louise Cerdeira and Zamin Iqbal and Martin Hunt and Ingle, {Danielle J.} and Dallman, {Timothy J.} and Claire Jenkins and Williamson, {Deborah A.} and Holt, {Kathryn E.}",

note = "Funding Information: K.E.H. is supported by a Senior Medical Research Fellowship from the Viertel Foundation of Australia, and Bill and Melinda Gates Foundation, Seattle (grant #OPP1175797). K.S.B. is supported by a Wellcome Trust Clinical Research Career Development Fellowship (A/106690/A/14/Z) and RJB through a UKRI MRC New Investigator Research Grant (held by KSB, MR/R020787/1). K.S.B., T.J.D. and C.J. are affiliated to the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Gastrointestinal Infections at University of Liverpool in partnership with Public Health England (PHE), in collaboration with University of Warwick. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health and Social Care or Public Health England. D.A.W. is supported by an Investigator Grant from the National Health and Medical Research Council (NHMRC) of Australia (APP1174555). Open Access: This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article{\textquoteright}s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article{\textquoteright}s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Publisher Copyright: {\textcopyright} 2021, The Author(s). Citation: Hawkey, J., Paranagama, K., Baker, K.S. et al. Global population structure and genotyping framework for genomic surveillance of the major dysentery pathogen, Shigella sonnei. Nat Commun 12, 2684 (2021). DOI: https://doi.org/10.1038/s41467-021-22700-4",

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Hawkey, J, Paranagama, K, Baker, KS, Bengtsson, RJ, Weill, FX, Thomson, NR, Baker, S, Cerdeira, L, Iqbal, Z, Hunt, M, Ingle, DJ, Dallman, TJ, Jenkins, C, Williamson, DA & Holt, KE 2021, 'Global population structure and genotyping framework for genomic surveillance of the major dysentery pathogen, Shigella sonnei', Nature Communications, vol. 12, 2684. https://doi.org/10.1038/s41467-021-22700-4

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AU - Weill, François Xavier

AU - Thomson, Nicholas R.

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AU - Cerdeira, Louise

AU - Iqbal, Zamin

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Global population structure and genotyping framework for genomic surveillance of the major dysentery pathogen, Shigella sonnei

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