Phylogenomic Analysis of Salmonella enterica subsp. enterica Serovar Bovismorbificans from Clinical and Food Samples Using Whole Genome Wide Core Genes and kmer Binning Methods to Identify Two Distinct Polyphyletic Genome Pathotypes

Gopal R. Gopinath; Hyein Jang; Junia Jean-Gilles Beaubrun; Jayanthi Gangiredla; Mark K. Mammel; Andrea Müller; Sandeep Tamber; Isha R. Patel; Laura Ewing; Leah M. Weinstein; Caroline Z. Wang; Samantha Finkelstein; Flavia Negrete; Tim Muruvanda; Marc Allard; Donald C. Sockett; Franco Pagotto; Ben D. Tall; Roger Stephan

doi:10.3390/microorganisms10061199

Microorganisms (Jun 2022)

Phylogenomic Analysis of Salmonella enterica subsp. enterica Serovar Bovismorbificans from Clinical and Food Samples Using Whole Genome Wide Core Genes and kmer Binning Methods to Identify Two Distinct Polyphyletic Genome Pathotypes

Gopal R. Gopinath,
Hyein Jang,
Junia Jean-Gilles Beaubrun,
Jayanthi Gangiredla,
Mark K. Mammel,
Andrea Müller,
Sandeep Tamber,
Isha R. Patel,
Laura Ewing,
Leah M. Weinstein,
Caroline Z. Wang,
Samantha Finkelstein,
Flavia Negrete,
Tim Muruvanda,
Marc Allard,
Donald C. Sockett,
Franco Pagotto,
Ben D. Tall,
Roger Stephan

Affiliations

Gopal R. Gopinath: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Hyein Jang: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Junia Jean-Gilles Beaubrun: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Jayanthi Gangiredla: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Mark K. Mammel: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Andrea Müller: Institute for Food Safety and Hygiene, University of Zurich, CH-8057 Zurich, Switzerland
Sandeep Tamber: Food Directorate, Bureau of Microbial Hazards/Health Canada, Ottawa, ON K1A 0K9, Canada
Isha R. Patel: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Laura Ewing: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Leah M. Weinstein: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Caroline Z. Wang: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Samantha Finkelstein: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Flavia Negrete: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Tim Muruvanda: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, College Park, MD 20740, USA
Marc Allard: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, College Park, MD 20740, USA
Donald C. Sockett: Wisconsin Veterinary Diagnostic Laboratory, University of Wisconsin-Madison, Madison, WI 53706, USA
Franco Pagotto: Food Directorate, Bureau of Microbial Hazards/Health Canada, Ottawa, ON K1A 0K9, Canada
Ben D. Tall: Center of Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708, USA
Roger Stephan: Institute for Food Safety and Hygiene, University of Zurich, CH-8057 Zurich, Switzerland

DOI: https://doi.org/10.3390/microorganisms10061199
Journal volume & issue: Vol. 10, no. 6
p. 1199

Abstract

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Salmonella enterica subsp. enterica serovar Bovismorbificans has caused multiple outbreaks involving the consumption of produce, hummus, and processed meat products worldwide. To elucidate the intra-serovar genomic structure of S. Bovismorbificans, a core-genome analysis with 2690 loci (based on 150 complete genomes representing Salmonella enterica serovars developed as part of this study) and a k-mer-binning based strategy were carried out on 95 whole genome sequencing (WGS) assemblies from Swiss, Canadian, and USA collections of S. Bovismorbificans strains from foodborne infections. Data mining of a digital DNA tiling array of legacy SARA and SARB strains was conducted to identify near-neighbors of S. Bovismorbificans. The core genome analysis and the k-mer-binning methods identified two polyphyletic clusters, each with emerging evolutionary properties. Four STs (2640, 142, 1499, and 377), which constituted the majority of the publicly available WGS datasets from >260 strains analyzed by k-mer-binning based strategy, contained a conserved core genome backbone with a different evolutionary lineage as compared to strains comprising the other cluster (ST150). In addition, the assortment of genotypic features contributing to pathogenesis and persistence, such as antimicrobial resistance, prophage, plasmid, and virulence factor genes, were assessed to understand the emerging characteristics of this serovar that are relevant clinically and for food safety concerns. The phylogenomic profiling of polyphyletic S. Bovismorbificans in this study corresponds to intra-serovar variations observed in S. Napoli and S. Newport serovars using similar high-resolution genomic profiling approaches and contributes to the understanding of the evolution and sequence divergence of foodborne Salmonellae. These intra-serovar differences may have to be thoroughly understood for the accurate classification of foodborne Salmonella strains needed for the uniform development of future food safety mitigation strategies.

Published in Microorganisms

ISSN: 2076-2607 (Online)
Publisher: MDPI AG
Country of publisher: Switzerland
LCC subjects: Science: Biology (General)
Website: https://www.mdpi.com/journal/microorganisms

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