A pan-genome perspective on the evolutionary dynamics of polyphyly, virulence, and antibiotic resistance in Salmonella enterica serovar Mbandaka highlights emerging threats to public health and food safety posed by cloud gene families

Salmonella enterica serovar Mbandaka, a prevalent foodborne pathogen, poses a threat to public health but remains poorly understood. We have determined the phylogenomic tree, genetic diversity, virulence, and antimicrobial resistance (AMR) profiles on a large genomic scale to elucidate the evolution...

Full description

Saved in:
Bibliographic Details
Main Authors: Nai-peng Kan, Zhiqiu Yin, Yu-feng Qiu, Enhui Zheng, Jianhui Chen, Jianzhong Huang, Yuhui Du
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Current Research in Food Science
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2665927124002843
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849694595486580736
author Nai-peng Kan
Zhiqiu Yin
Yu-feng Qiu
Enhui Zheng
Jianhui Chen
Jianzhong Huang
Yuhui Du
author_facet Nai-peng Kan
Zhiqiu Yin
Yu-feng Qiu
Enhui Zheng
Jianhui Chen
Jianzhong Huang
Yuhui Du
author_sort Nai-peng Kan
collection DOAJ
description Salmonella enterica serovar Mbandaka, a prevalent foodborne pathogen, poses a threat to public health but remains poorly understood. We have determined the phylogenomic tree, genetic diversity, virulence, and antimicrobial resistance (AMR) profiles on a large genomic scale to elucidate the evolutionary dynamics within the Mbandaka pan-genome. The polyphyletic nature of this serovar is characterized by two distinct phylogenetic groups and inter-serovar recombination boundaries, that potentially arising from recombination events at the H2-antigen loci. The open pan-genome exhibited a flexible gene repertoire, with numerous cloud gene families involved in virulence and AMR. Extensive gene gain and loss observed at the terminal nodes of the phylogenetic tree indicate that Mbandaka individuals have undergone frequent gene turnover. The resulting changes in virulence and AMR genes potentially pose emerging threats to public health. We explored serovar conversion due to recombination of H-antigen loci, inter-serovar divergences in gene gain and loss, prophage-mediated acquisition of virulence factors, and the role of incompatibility group plasmids in acquiring resistance determinants as key molecular mechanisms driving the pathogenicity and antibiotic resistance of Mbandaka. Our work contributes to a comprehensive understanding of the complex mechanisms of pathogenesis and the ongoing evolutionary arms race with current therapeutic approaches in serovar Mbandaka.
format Article
id doaj-art-1cb76906db76495f96ea2041d41efe7f
institution DOAJ
issn 2665-9271
language English
publishDate 2025-01-01
publisher Elsevier
record_format Article
series Current Research in Food Science
spelling doaj-art-1cb76906db76495f96ea2041d41efe7f2025-08-20T03:20:01ZengElsevierCurrent Research in Food Science2665-92712025-01-011010095710.1016/j.crfs.2024.100957A pan-genome perspective on the evolutionary dynamics of polyphyly, virulence, and antibiotic resistance in Salmonella enterica serovar Mbandaka highlights emerging threats to public health and food safety posed by cloud gene familiesNai-peng Kan0Zhiqiu Yin1Yu-feng Qiu2Enhui Zheng3Jianhui Chen4Jianzhong Huang5Yuhui Du6National Engineering Research Center of Industrial Microbiology and Fermentation Technology, College of Life Sciences, Fujian Normal University, Fuzhou, 350117, PR China; Fujian Provincial Center for Disease Control and Prevention, Fuzhou, 350012, PR ChinaDepartment of Clinical Laboratory, The Fifth Affiliated Hospital of Guangzhou Medical University, Guangzhou, 510700, Guangdong, PR China; Corresponding author.Fujian Provincial Center for Disease Control and Prevention, Fuzhou, 350012, PR ChinaFujian Provincial Center for Disease Control and Prevention, Fuzhou, 350012, PR ChinaFujian Provincial Center for Disease Control and Prevention, Fuzhou, 350012, PR ChinaNational Engineering Research Center of Industrial Microbiology and Fermentation Technology, College of Life Sciences, Fujian Normal University, Fuzhou, 350117, PR China; Corresponding author.MOE International Joint Research Laboratory on Synthetic Biology and Medicines, School of Biology and Biological Engineering, South China University of Technology, Guangzhou, 510006, PR China; Corresponding author.Salmonella enterica serovar Mbandaka, a prevalent foodborne pathogen, poses a threat to public health but remains poorly understood. We have determined the phylogenomic tree, genetic diversity, virulence, and antimicrobial resistance (AMR) profiles on a large genomic scale to elucidate the evolutionary dynamics within the Mbandaka pan-genome. The polyphyletic nature of this serovar is characterized by two distinct phylogenetic groups and inter-serovar recombination boundaries, that potentially arising from recombination events at the H2-antigen loci. The open pan-genome exhibited a flexible gene repertoire, with numerous cloud gene families involved in virulence and AMR. Extensive gene gain and loss observed at the terminal nodes of the phylogenetic tree indicate that Mbandaka individuals have undergone frequent gene turnover. The resulting changes in virulence and AMR genes potentially pose emerging threats to public health. We explored serovar conversion due to recombination of H-antigen loci, inter-serovar divergences in gene gain and loss, prophage-mediated acquisition of virulence factors, and the role of incompatibility group plasmids in acquiring resistance determinants as key molecular mechanisms driving the pathogenicity and antibiotic resistance of Mbandaka. Our work contributes to a comprehensive understanding of the complex mechanisms of pathogenesis and the ongoing evolutionary arms race with current therapeutic approaches in serovar Mbandaka.http://www.sciencedirect.com/science/article/pii/S2665927124002843MbandakaFoodborne pathogenEvolutionary dynamicPolyphyleticVirulenceAntimicrobial resistance
spellingShingle Nai-peng Kan
Zhiqiu Yin
Yu-feng Qiu
Enhui Zheng
Jianhui Chen
Jianzhong Huang
Yuhui Du
A pan-genome perspective on the evolutionary dynamics of polyphyly, virulence, and antibiotic resistance in Salmonella enterica serovar Mbandaka highlights emerging threats to public health and food safety posed by cloud gene families
Current Research in Food Science
Mbandaka
Foodborne pathogen
Evolutionary dynamic
Polyphyletic
Virulence
Antimicrobial resistance
title A pan-genome perspective on the evolutionary dynamics of polyphyly, virulence, and antibiotic resistance in Salmonella enterica serovar Mbandaka highlights emerging threats to public health and food safety posed by cloud gene families
title_full A pan-genome perspective on the evolutionary dynamics of polyphyly, virulence, and antibiotic resistance in Salmonella enterica serovar Mbandaka highlights emerging threats to public health and food safety posed by cloud gene families
title_fullStr A pan-genome perspective on the evolutionary dynamics of polyphyly, virulence, and antibiotic resistance in Salmonella enterica serovar Mbandaka highlights emerging threats to public health and food safety posed by cloud gene families
title_full_unstemmed A pan-genome perspective on the evolutionary dynamics of polyphyly, virulence, and antibiotic resistance in Salmonella enterica serovar Mbandaka highlights emerging threats to public health and food safety posed by cloud gene families
title_short A pan-genome perspective on the evolutionary dynamics of polyphyly, virulence, and antibiotic resistance in Salmonella enterica serovar Mbandaka highlights emerging threats to public health and food safety posed by cloud gene families
title_sort pan genome perspective on the evolutionary dynamics of polyphyly virulence and antibiotic resistance in salmonella enterica serovar mbandaka highlights emerging threats to public health and food safety posed by cloud gene families
topic Mbandaka
Foodborne pathogen
Evolutionary dynamic
Polyphyletic
Virulence
Antimicrobial resistance
url http://www.sciencedirect.com/science/article/pii/S2665927124002843
work_keys_str_mv AT naipengkan apangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT zhiqiuyin apangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT yufengqiu apangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT enhuizheng apangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT jianhuichen apangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT jianzhonghuang apangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT yuhuidu apangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT naipengkan pangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT zhiqiuyin pangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT yufengqiu pangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT enhuizheng pangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT jianhuichen pangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT jianzhonghuang pangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies
AT yuhuidu pangenomeperspectiveontheevolutionarydynamicsofpolyphylyvirulenceandantibioticresistanceinsalmonellaentericaserovarmbandakahighlightsemergingthreatstopublichealthandfoodsafetyposedbycloudgenefamilies