Characterization of a Salmonella enterica serovar Typhimurium lineage with rough colony morphology and multidrug resistance

Ying Xiang, Kunpeng Zhu, Kaiyuan Min, Yaowen Zhang, Jiangfeng Liu, Kangkang Liu, Yiran Han, Xinge Li, Xinying Du, Xin Wang, Ying Huang, Xinping Li, Yuqian Peng, Chaojie Yang, Hongbo Liu, Liu Hongbo, Xiaoying Li, Hui Wang, Chao Wang, Qi Wang, Huiqun Jia, Mingjuan Yang, Ligui Wang, Yarong Wu, Yujun Cui, Fei Chen, Haiyan Yang, Stephen Baker, Xuebin Xu (), Juntao Yang (), Hongbin Song () and Shaofu Qiu ()
Additional contact information
Ying Xiang: Center for Disease Control and Prevention of Chinese PLA
Kunpeng Zhu: Center for Disease Control and Prevention of Chinese PLA
Kaiyuan Min: School of Basic Medicine Peking Union Medical College
Yaowen Zhang: Center for Disease Control and Prevention of Chinese PLA
Jiangfeng Liu: School of Basic Medicine Peking Union Medical College
Kangkang Liu: Center for Disease Control and Prevention of Chinese PLA
Yiran Han: Center for Disease Control and Prevention of Chinese PLA
Xinge Li: Center for Disease Control and Prevention of Chinese PLA
Xinying Du: Center for Disease Control and Prevention of Chinese PLA
Xin Wang: Center for Disease Control and Prevention of Chinese PLA
Ying Huang: Center for Disease Control and Prevention of Chinese PLA
Xinping Li: Center for Disease Control and Prevention of Chinese PLA
Yuqian Peng: Center for Disease Control and Prevention of Chinese PLA
Chaojie Yang: Center for Disease Control and Prevention of Chinese PLA
Hongbo Liu: Center for Disease Control and Prevention of Chinese PLA
Liu Hongbo: Center for Disease Control and Prevention of Chinese PLA
Xiaoying Li: Center for Disease Control and Prevention of Chinese PLA
Hui Wang: Center for Disease Control and Prevention of Chinese PLA
Chao Wang: Center for Disease Control and Prevention of Chinese PLA
Qi Wang: Center for Disease Control and Prevention of Chinese PLA
Huiqun Jia: Center for Disease Control and Prevention of Chinese PLA
Mingjuan Yang: Center for Disease Control and Prevention of Chinese PLA
Ligui Wang: Center for Disease Control and Prevention of Chinese PLA
Yarong Wu: Beijing Institute of Microbiology and Epidemiology
Yujun Cui: Beijing Institute of Microbiology and Epidemiology
Fei Chen: China National Center for Bioinformation
Haiyan Yang: Zhengzhou University
Stephen Baker: Cambridge Biomedical Campus
Xuebin Xu: Shanghai Municipal Center for Disease Control and Prevention
Juntao Yang: School of Basic Medicine Peking Union Medical College
Hongbin Song: Center for Disease Control and Prevention of Chinese PLA
Shaofu Qiu: Center for Disease Control and Prevention of Chinese PLA

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract Salmonella enterica serovar Typhimurium (S. Typhimurium) is a major cause of salmonellosis, and the emergence of multidrug-resistant pathovariants has become a growing concern. Here, we investigate a distinct rough colony variant exhibiting a strong biofilm-forming ability isolated in China. Whole-genome sequencing on 2,212 Chinese isolates and 1,739 publicly available genomes reveals the population structure and evolutionary history of the rough colony variants. Characterized by macro, red, dry, and rough (mrdar) colonies, these variants demonstrate enhanced biofilm formation at 28 °C and 37 °C compared to typical rdar colonies. The mrdar variants exhibit extensive multidrug resistance, with significantly higher resistance to at least five classes of antimicrobial agents compared to non-mrdar variants. This resistance is primarily conferred by an IncHI2 plasmid harboring 19 antimicrobial resistance genes. Phylogenomic analysis divides the global collections into six lineages. The majority of mrdar variants belong to sublineage L6.5, which originated from Chinese smooth colony strains and possibly emerged circa 1977. Among the mrdar variants, upregulation of the csgDEFG operons is observed, probably due to a distinct point mutation (−44G > T) in the csgD gene promoter. Pangenome and genome-wide association analyses identify 87 specific accessory genes and 72 distinct single nucleotide polymorphisms associated with the mrdar morphotype.

Date: 2024
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DOI: 10.1038/s41467-024-50331-y

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