Cited by 710Salmonella and Campylobacter epidemiologyEscherichia coli research studiesGenetic diversity and population structure

Multilocus sequence typing as a replacement for serotyping in Salmonella enterica

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Achtman, Mark, Wain, John, Weill, François-Xavier, Nair, Satheesh, Zhou, Zhemin, Sangal, Vartul, Krauland, Mary G., Hale, James L. +6 more·2012·PLoS Pathogens

Abstract

Salmonella enterica subspecies enterica is traditionally subdivided into serovars by serological and nutritional characteristics. We used Multilocus Sequence Typing (MLST) to assign 4,257 isolates from 554 serovars to 1092 sequence types (STs). The majority of the isolates and many STs were grouped into 138 genetically closely related clusters called eBurstGroups (eBGs). Many eBGs correspond to a serovar, for example most Typhimurium are in eBG1 and most Enteritidis are in eBG4, but many eBGs contained more than one serovar. Furthermore, most serovars were polyphyletic and are distributed across multiple unrelated eBGs. Thus, serovar designations confounded genetically unrelated isolates and failed to recognize natural evolutionary groupings. An inability of serotyping to correctly group isolates was most apparent for Paratyphi B and its variant Java. Most Paratyphi B were included within a sub-cluster of STs belonging to eBG5, which also encompasses a separate sub-cluster of Java STs. However, diphasic Java variants were also found in two other eBGs and monophasic Java variants were in four other eBGs or STs, one of which is in subspecies salamae and a second of which includes isolates assigned to Enteritidis, Dublin and monophasic Paratyphi B. Similarly, Choleraesuis was found in eBG6 and is closely related to Paratyphi C, which is in eBG20. However, Choleraesuis var. Decatur consists of isolates from seven other, unrelated eBGs or STs. The serological assignment of these Decatur isolates to Choleraesuis likely reflects lateral gene transfer of flagellar genes between unrelated bacteria plus purifying selection. By confounding multiple evolutionary groups, serotyping can be misleading about the disease potential of S. enterica. Unlike serotyping, MLST recognizes evolutionary groupings and we recommend that Salmonella classification by serotyping should be replaced by MLST or its equivalents.

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  • Most Salmonella serotypes are polyphyletic.

    “Most Salmonella serotypes are polyphyletic (i.e., formed by at least two unrelated lineages that convergently acquired the genetic basis for a similar O and H antigenic formula) [25].”

    From Contamination of street food with multidrug-resistant Salmonella, in Ouagadougou, Burkina Faso (2021) · cites this paper as [25]

    The 'Variable association between eBG and serovar' section reports that 25 of 42 serovars with at least 15 sampled isolates were associated with multiple genetic groups and/or sequence types. The 'Serovars and their problems' section describes polyphyletic serovars as common, including some found in distantly related groups. Those findings support the concern, but they do not establish that most Salmonella serotypes overall are polyphyletic; multiple sequence types alone also do not establish unrelated lineages. (LLM, conf=0.86)

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  1. [2]2. Grimont PA, Weill F-X (2007) Antigenic formulae of the Salmonella serovars. 9 th Edition. Paris, France: WHO Collaborating Centre for Reference and Research on Salmonella. http://www.pasteur.fr/sante/clre/cadrecnr/salmoms/WKLM_ 2007.pdf

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Authors
Achtman, M., Wain, J., Weill, F.-X., Nair, S., Zhou, Z., Sangal, V., Krauland, M. G., Hale, J. L., Harbottle, H., Uesbeck, A., Dougan, G., Harrison, L. H., Brisse, S., & the S. enterica MLST study group
Affiliations
  • University College Cork (IE)
  • Wellcome Sanger Institute (GB)
  • Institut Pasteur (FR)
  • Max Planck Institute for Infection Biology (DE)
  • University of Pittsburgh (US)
  • Center for Veterinary Medicine (US)
  • University of Cologne (DE)
Corresponding author
Achtman, Mark
Venue
PLoS Pathogens
Published
2012-06-21
Volume
8
Issue
6
Pages
e1002776
ISSN
  • 1553-7366 (ISSN-L)
  • 1553-7374
OpenAlex
W2128352784
Cited by
710
References
105
Citations by year
2026: 36 · 2025: 48 · 2024: 47 · 2023: 52 · 2022: 54 · 2021: 64 · 2020: 57 · 2019: 69 · 2018: 49 · 2017: 49 · 2016: 54 · 2015: 41 · 2014: 47 · 2013: 30 · 2012: 12
FWCI
63.94
Type
journal article
Language
en
Open access
Locations
  • PLoS Pathogens (publishedVersion, public-domain)
  • PubMed Central (publishedVersion, public-domain)
  • PubMed (publishedVersion)
  • Northumbria Research Link (Northumbria University) (acceptedVersion)
  • Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
  • D-Scholarship@Pitt (University of Pittsburgh) (acceptedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
  • OpenAgrar (submittedVersion)
  • HAL (submittedVersion, public-domain)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Max Planck Institute for Plasma Physics (submittedVersion, other-oa)
  • Figshare (submittedVersion, cc-by)
  • Minerva Access (University of Melbourne) (submittedVersion)
Funders
  • National University of Ireland
  • Wellcome Trust
  • Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology
  • Imperial College London
  • University of Galway
  • University College Cork
  • Bundesministerium für Bildung und Forschung
  • Institut de Veille Sanitaire
  • Robert Koch Institut
  • National Institutes of Health (UL1TR000005)
  • Directorate for Biological Sciences
  • Bundesinstitut für Risikobewertung
  • National Center for Advancing Translational Sciences
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
Keywords
Salmonella enterica, multilocus sequence typing, serotyping, serotypes, sequence types, genetic clustering, purifying selection
MeSH terms
Phylogeny, Serotyping, Bacterial Typing Techniques, Salmonella enterica

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