A global genomic analysis of Salmonella Concord reveals lineages with high antimicrobial resistance in Ethiopia

Wim L. Cuypers*, Pieter Meysman, François Xavier Weill, Rene S. Hendriksen, Getenet Beyene, John Wain, Satheesh Nair, Marie A. Chattaway, Blanca M. Perez-Sepulveda, Pieter Jan Ceyssens, Tessa de Block, Winnie W.Y. Lee, Maria Pardos de la Gandara, Christian Kornschober, Jacob Moran-Gilad, Kees T. Veldman, Martin Cormican, Mia Torpdahl, Patricia I. Fields, Tomáš ČernýLiselotte Hardy, Bieke Tack, Kate C. Mellor, Nicholas Thomson, Gordon Dougan, Stijn Deborggraeve, Jan Jacobs, Kris Laukens, Sandra Van Puyvelde*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

3 Citations (Scopus)

Abstract

Antimicrobial resistant Salmonella enterica serovar Concord (S. Concord) is known to cause severe gastrointestinal and bloodstream infections in patients from Ethiopia and Ethiopian adoptees, and occasional records exist of S. Concord linked to other countries. The evolution and geographical distribution of S. Concord remained unclear. Here, we provide a genomic overview of the population structure and antimicrobial resistance (AMR) of S. Concord by analysing genomes from 284 historical and contemporary isolates obtained between 1944 and 2022 across the globe. We demonstrate that S. Concord is a polyphyletic serovar distributed among three Salmonella super-lineages. Super-lineage A is composed of eight S. Concord lineages, of which four are associated with multiple countries and low levels of AMR. Other lineages are restricted to Ethiopia and horizontally acquired resistance to most antimicrobials used for treating invasive Salmonella infections in low- and middle-income countries. By reconstructing complete genomes for 10 representative strains, we demonstrate the presence of AMR markers integrated in structurally diverse IncHI2 and IncA/C2 plasmids, and/or the chromosome. Molecular surveillance of pathogens such as S. Concord supports the understanding of AMR and the multi-sector response to the global AMR threat. This study provides a comprehensive baseline data set essential for future molecular surveillance.

Original languageEnglish
Article number3517
JournalNature Communications
Volume14
Issue number1
DOIs
Publication statusPublished - Dec 2023

Bibliographical note

Funding Information:
This work was financially supported by the Research Foundation - Flanders (FWO: SB Ph.D. fellowship 1S40018N to W. L. C.). The computational resources and services used in this work were provided by the HPC core facility CalcUA of the University of Antwerp, and the VSC (Flemish Supercomputer Center), funded by the Research Foundation - Flanders (FWO) and the Flemish Government. We acknowledge the support of BIOMINA (Biomedical Informatics Network Antwerpen). The work by S.V.P. and G.D. is funded in part by a grant from the Bill & Melinda Gates Foundation (OPP1151153). This research was funded by the National Institute for Health Research [Cambridge Biomedical Research Centre at the Cambridge University Hospitals NHS Foundation Trust]. K.M. and N.R.T. were supported by Wellcome Trust (grant number 206194). For the purpose of Open Access, the author has applied a CC-BY public copyright license to any Author Accepted Manuscript version arising from this submission. M.A.C. is affiliated to the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Genomics and Enabling Data at University of Warwick in partnership with the UK Health Security Agency (UKHSA), in collaboration with University or Cambridge and Oxford. M.A.C. is based at UKHSA and the views expressed are those of the authors and not necessarily those of the NHS, UKHSA, the NIHR or the Department of Health and Social Care. The laboratory of F.X.W. belongs to the “Integrative Biology of Emerging Infectious Diseases” Laboratory of Excellence funded by the French Government “Investissement d’Avenir” programme (grant no. ANR-10-LABX-62-IBEID). The French National Reference Center for Escherichia coli , Shigella and Salmonella is co-funded by Santé Publique France and the Institut Pasteur. Genome sequencing performed at the Earlham Institute as part of the 10KSG consortium was supported by the Global Challenges Research Fund data and resources grant (BBS/OS/GC/000009D), and the BBSRC National Capability in Genomics and Single Cell (BB/CCG1720/1) grant via members of the Genomics Pipelines Group. J.W. acknowledges the support of the Biotechnology and Biological Sciences Research Council through the Institute Strategic Programme Microbes in the Food Chain BB/R012504/1 and its constituent project BBS/E/F/000PR10349. We thank Ellen Corsmit, Tine Vermoesen, Véronique Guibert, Magali Ravel, and Estelle Serre for their assistance and/or advice concerning the cultivation of isolates and antimicrobial susceptibility testing, and Philippe Selhorst and Bart Cuypers for their advice on Nanopore sequencing.

Funding Information:
This work was financially supported by the Research Foundation - Flanders (FWO: SB Ph.D. fellowship 1S40018N to W. L. C.). The computational resources and services used in this work were provided by the HPC core facility CalcUA of the University of Antwerp, and the VSC (Flemish Supercomputer Center), funded by the Research Foundation - Flanders (FWO) and the Flemish Government. We acknowledge the support of BIOMINA (Biomedical Informatics Network Antwerpen). The work by S.V.P. and G.D. is funded in part by a grant from the Bill & Melinda Gates Foundation (OPP1151153). This research was funded by the National Institute for Health Research [Cambridge Biomedical Research Centre at the Cambridge University Hospitals NHS Foundation Trust]. K.M. and N.R.T. were supported by Wellcome Trust (grant number 206194). For the purpose of Open Access, the author has applied a CC-BY public copyright license to any Author Accepted Manuscript version arising from this submission. M.A.C. is affiliated to the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Genomics and Enabling Data at University of Warwick in partnership with the UK Health Security Agency (UKHSA), in collaboration with University or Cambridge and Oxford. M.A.C. is based at UKHSA and the views expressed are those of the authors and not necessarily those of the NHS, UKHSA, the NIHR or the Department of Health and Social Care. The laboratory of F.X.W. belongs to the “Integrative Biology of Emerging Infectious Diseases” Laboratory of Excellence funded by the French Government “Investissement d’Avenir” programme (grant no. ANR-10-LABX-62-IBEID). The French National Reference Center for Escherichia coli, Shigella and Salmonella is co-funded by Santé Publique France and the Institut Pasteur. Genome sequencing performed at the Earlham Institute as part of the 10KSG consortium was supported by the Global Challenges Research Fund data and resources grant (BBS/OS/GC/000009D), and the BBSRC National Capability in Genomics and Single Cell (BB/CCG1720/1) grant via members of the Genomics Pipelines Group. J.W. acknowledges the support of the Biotechnology and Biological Sciences Research Council through the Institute Strategic Programme Microbes in the Food Chain BB/R012504/1 and its constituent project BBS/E/F/000PR10349. We thank Ellen Corsmit, Tine Vermoesen, Véronique Guibert, Magali Ravel, and Estelle Serre for their assistance and/or advice concerning the cultivation of isolates and antimicrobial susceptibility testing, and Philippe Selhorst and Bart Cuypers for their advice on Nanopore sequencing.

Publisher Copyright:
© 2023, The Author(s).

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