{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,27]],"date-time":"2026-10-27T22:53:08Z","timestamp":1793141588478,"version":"4.5.0"},"reference-count":40,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,9,8]],"date-time":"2022-09-08T00:00:00Z","timestamp":1662595200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Public Health"],"abstract":"<jats:p><jats:italic>Salmonella<\/jats:italic> is the most common cause of gastroenteritis in the world. Over the past 5 years, whole-genome analysis has led to the high-resolution characterization of clinical and foodborne <jats:italic>Salmonella<\/jats:italic> responsible for typhoid fever, foodborne illness or contamination of the agro-food chain. Whole-genome analyses are simplified by the availability of high-quality, complete genomes for mapping analysis and for calculating the pairwise distance between genomes, but unfortunately some difficulties may still remain. For some serovars, the complete genome is not available, or some serovars are polyphyletic and knowing the serovar alone is not sufficient for choosing the most appropriate reference genome. For these serovars, it is essential to identify the genetically closest complete genome to be able to carry out precise genome analyses. In this study, we explored the genomic proximity of 650 genomes of the 58 <jats:italic>Salmonella enterica<\/jats:italic> subsp. <jats:italic>enterica<\/jats:italic> serovars most frequently isolated in humans and from the food chain in the United States (US) and in Europe (EU), with a special focus on France. For each serovar, to take into account their genomic diversity, we included all the multilocus sequence type (MLST) profiles represented in EnteroBase with 10 or more genomes (on 19 July 2021). A phylogenetic analysis using both core- and pan-genome approaches was carried out to identify the genomic proximity of all the <jats:italic>Salmonella<\/jats:italic> studied and 20 polyphyletic serovars that have not yet been described in the literature. This study determined the genetic proximity between all 58 serovars studied and revealed polyphyletic serovars, their genomic lineages and MLST profiles. Finally, we enhanced the open-access databases with 73 new genomes and produced a list of high-quality complete reference genomes for 48 <jats:italic>S. enterica<\/jats:italic> subsp. <jats:italic>enterica<\/jats:italic> serovars among the most isolated in the US, EU, and France.<\/jats:p>","DOI":"10.3389\/fpubh.2022.963188","type":"journal-article","created":{"date-parts":[[2022,9,8]],"date-time":"2022-09-08T10:28:33Z","timestamp":1662632913000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":11,"title":["Polyphyly in widespread Salmonella enterica serovars and using genomic proximity to choose the best reference genome for bioinformatics analyses"],"prefix":"10.3389","volume":"10","author":[{"given":"Emeline","family":"Cherchame","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guy","family":"Ilango","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"V\u00e9ronique","family":"No\u00ebl","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sabrina","family":"Cadel-Six","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,9,8]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"e1007261","DOI":"10.1371\/journal.pgen.1007261","article-title":"A genomic overview of the population structure of Salmonella","volume":"14","author":"Alikhan","year":"2018"},{"key":"B2","doi-asserted-by":"publisher","first-page":"2578","DOI":"10.3389\/fmicb.2019.02578","article-title":"Critical Orientation in the Jungle of Currently Available Methods and Types of Data for Source Attribution of Foodborne Diseases","volume":"10","author":"Mughini-Gras","year":"2019","journal-title":"Front Microbiol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"30544","DOI":"10.2807\/1560-7917.ES.2017.22.23.30544","article-title":"PulseNet International: vision for the implementation of whole genome sequencing (WGS) for global food-borne disease surveillance","volume":"22","author":"Nadon","year":"2017","journal-title":"Euro Surveill"},{"key":"B4","doi-asserted-by":"publisher","first-page":"889","DOI":"10.3389\/fmicb.2020.00889","article-title":"Source attribution study of sporadic Salmonella derby cases in France","volume":"11","author":"Sevellec","year":"2020","journal-title":"Front Microbiol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1186\/s12864-022-08439-2","article-title":"Salmonella enterica subsp. enterica Welikade: guideline for phylogenetic analysis of serovars rarely involved in foodborne outbreaks","volume":"23","author":"Cherchame","year":"2022","journal-title":"BMC Genomics."},{"key":"B6","doi-asserted-by":"publisher","first-page":"11779322221080264","DOI":"10.1177\/11779322221080264","article-title":"Retrieving good-quality Salmonella genomes from the genbank database using a python tool, SalmoDEST","volume":"16","author":"Cherchame","year":"2022","journal-title":"Bioinform Biol Insights."},{"key":"B7","doi-asserted-by":"publisher","first-page":"giaa007","DOI":"10.1093\/gigascience\/giaa007","article-title":"Genomic diversity affects the accuracy of bacterial single-nucleotide polymorphism-calling pipelines","volume":"9","author":"Bush","year":"2020","journal-title":"Gigascience."},{"key":"B8","doi-asserted-by":"publisher","first-page":"223","DOI":"10.12688\/wellcomeopenres.16291.1","article-title":"Genomic diversity of Salmonella enterica-The UoWUCC 10K genomes project","volume":"5","author":"Achtman","year":"2020","journal-title":"Wellcome Open Res."},{"key":"B9","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1101\/gr.251678.119","article-title":"The EnteroBase user's guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity","volume":"30","author":"Zhou","year":"2020","journal-title":"Genome Res."},{"key":"B10","unstructured":"Inventaire des Salmonella d'origine non humaine"},{"key":"B11","unstructured":"National Surveillance of Bacterial Foodborne Illnesses (Enteric Diseases)"},{"key":"B12","volume-title":"Antigenic Formulae of the Salmonella serovars","author":"Grimont","year":"2007"},{"key":"B13","doi-asserted-by":"publisher","first-page":"891","DOI":"10.3389\/fmicb.2018.00891","article-title":"Polyphyletic nature of Salmonella enterica serotype derby and lineage-specific host-association revealed by genome-wide analysis","volume":"9","author":"Sevellec","year":"2018","journal-title":"Front Microbiol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"2109","DOI":"10.1093\/gbe\/evt159","article-title":"Phylogenetic diversity of the enteric pathogen Salmonella enterica subsp. enterica inferred from genome-wide reference-free SNP characters","volume":"5","author":"Timme","year":"2013","journal-title":"Genome Biol Evol."},{"key":"B15","unstructured":"European Centre for Disease Prevention and Control"},{"key":"B16","unstructured":"Tables, Figures and Country Datasets complementing the European Union Summary Report on Zoonoses and Food-borne Outbreaks 2016"},{"key":"B17","unstructured":"Serotypes Profile of Salmonella Isolates from Meat and Poultry Products January 1998 through December 2014"},{"key":"B18","unstructured":"Quarterly Sampling Reports on Salmonella and Campylobacter"},{"key":"B19","unstructured":"Rapport d'activit\u00e9 annuel 2017 - Ann\u00e9e d'exercice 2016Centre National de R\u00e9f\u00e9rence des Escherichia coli Shigella et Salmonella, Unit\u00e9 de Recherche et d'Expertise des Bact\u00e9ries Pathog\u00e8nes Ent\u00e9riques, Laboratoire associ\u00e9 Service de Microbiologie H\u00f4pital Robert Debr\u00e9 - Paris"},{"key":"B20","doi-asserted-by":"publisher","first-page":"R80","DOI":"10.1186\/gb-2004-5-10-r80","article-title":"Bioconductor: open software development for computational biology and bioinformatics","volume":"5","author":"Gentleman","year":"2004","journal-title":"Genome Biol."},{"key":"B21","doi-asserted-by":"crossref","DOI":"10.1128\/AEM.01746-19","article-title":"SeqSero2: rapid and improved Salmonella serotype determination using whole-genome sequencing data","volume-title":"Appl Environ Microbiol","author":"Zhang","year":"2019"},{"key":"B22","doi-asserted-by":"publisher","first-page":"651124","DOI":"10.3389\/fmicb.2021.651124","article-title":"The spatiotemporal dynamics and microevolution events that favored the success of the highly clonal multidrug-resistant monophasic Salmonella Typhimurium circulating in Europe","volume":"12","author":"Cadel-Six","year":"2021","journal-title":"Front Microbiol."},{"key":"B23","unstructured":"ARtWORK\n            FeltenA\n            DurimelK"},{"key":"B24","unstructured":"SeemannT"},{"key":"B25","doi-asserted-by":"publisher","first-page":"e1002776","DOI":"10.1371\/journal.ppat.1002776","article-title":"Multilocus sequence typing as a replacement for serotyping in Salmonella enterica","volume":"8","author":"Achtman","year":"2012"},{"key":"B26","doi-asserted-by":"publisher","first-page":"2413","DOI":"10.3389\/fmicb.2019.02413","article-title":"A simple and robust statistical method to define genetic relatedness of samples related to outbreaks at the genomic scale - application to retrospective Salmonella foodborne outbreak investigations","volume":"10","author":"Radomski","year":"2019","journal-title":"Front Microbiol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"132","DOI":"10.1186\/s13059-016-0997-x","article-title":"Mash: fast genome and metagenome distance estimation using MinHash","volume":"17","author":"Ondov","year":"2016","journal-title":"Genome Biol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1569","DOI":"10.1093\/bioinformatics\/btq228","article-title":"DendroPy: a Python library for phylogenetic computing","volume":"26","author":"Sukumaran","year":"2010","journal-title":"Bioinformatics."},{"key":"B29","doi-asserted-by":"publisher","first-page":"3041","DOI":"10.1093\/molbev\/msy194","article-title":"Two methods for mapping and visualizing associated data on phylogeny using Ggtree","volume":"35","author":"Yu","year":"2018","journal-title":"Mol Biol Evol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1111\/2041-210X.12628","article-title":"GGTREE: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data","volume":"8","author":"Yu","year":"2016","journal-title":"Method Ecol Evol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"e000284","DOI":"10.1099\/mgen.0.000284","article-title":"The speciation and hybridization history of the genus Salmonella","volume":"5","author":"Criscuolo","year":"2019"},{"key":"B32","doi-asserted-by":"publisher","first-page":"589","DOI":"10.1016\/j.gde.2005.09.006","article-title":"The microbial pan-genome","volume":"15","author":"Medini","year":"2005","journal-title":"Curr Opin Genet Dev."},{"key":"B33","doi-asserted-by":"publisher","first-page":"3691","DOI":"10.1093\/bioinformatics\/btv421","article-title":"Roary: rapid large-scale prokaryote pan genome analysis","volume":"31","author":"Page","year":"2015","journal-title":"Bioinformatics."},{"key":"B34","doi-asserted-by":"publisher","first-page":"6465","DOI":"10.1128\/JB.00969-10","article-title":"Evolution and population structure of Salmonella enterica serovar Newport","volume":"192","author":"Sangal","year":"2010","journal-title":"J Bacteriol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1047","DOI":"10.1093\/gbe\/evx065","article-title":"Whole-genome comparative analysis of Salmonella enterica Serovar newport strains reveals lineage-specific divergence","volume":"9","author":"Zheng","year":"2017","journal-title":"Genome Biol Evol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"e0166162","DOI":"10.1371\/journal.pone.0166162","article-title":"Real-time pathogen detection in the era of whole-genome sequencing and big data: comparison of k-mer and site-based methods for inferring the genetic distances among tens of thousands of Salmonella samples","volume":"11","author":"Pettengill","year":"2016","journal-title":"PLoS ONE."},{"key":"B37","doi-asserted-by":"crossref","DOI":"10.1128\/MRA.01027-18","article-title":"Complete Genome Sequence of Salmonella enterica subsp. enterica Serotype Derby, Associated with the Pork Sector in France","volume-title":"Microbiol Resour Announc","author":"Sevellec","year":"2018"},{"key":"B38","doi-asserted-by":"publisher","first-page":"7494","DOI":"10.1038\/s41598-021-86243-w","article-title":"Salmonella nomenclature in the genomic era: a time for change","volume":"11","author":"Chattaway","year":"2021","journal-title":"Sci Rep."},{"key":"B39","doi-asserted-by":"publisher","first-page":"1355","DOI":"10.1128\/JCM.06094-11","article-title":"Multilocus sequence typing of total-genome-sequenced bacteria","volume":"50","author":"Larsen","year":"2012","journal-title":"J Clin Microbiol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"1074","DOI":"10.1099\/jmm.0.000325","article-title":"Characterization of new Salmonella serovars by whole-genome sequencing and traditional typing techniques","volume":"65","author":"Bale","year":"2016","journal-title":"J Med Microbiol."}],"container-title":["Frontiers in Public Health"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpubh.2022.963188\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,8]],"date-time":"2022-09-08T10:28:46Z","timestamp":1662632926000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpubh.2022.963188\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,8]]},"references-count":40,"alternative-id":["10.3389\/fpubh.2022.963188"],"URL":"https:\/\/doi.org\/10.3389\/fpubh.2022.963188","relation":{},"ISSN":["2296-2565"],"issn-type":[{"value":"2296-2565","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,8]]},"article-number":"963188"}}