IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50331-y.html
   My bibliography  Save this article

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

Author

Listed:
  • Ying Xiang

    (Center for Disease Control and Prevention of Chinese PLA)

  • Kunpeng Zhu

    (Center for Disease Control and Prevention of Chinese PLA
    Kaifeng Center for Disease Control and Prevention)

  • Kaiyuan Min

    (School of Basic Medicine Peking Union Medical College)

  • Yaowen Zhang

    (Center for Disease Control and Prevention of Chinese PLA
    Daxing Center for Disease Control and Prevention)

  • 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)

  • HONGBO Liu

    (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)

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.

Suggested Citation

  • 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 , 2024. "Characterization of a Salmonella enterica serovar Typhimurium lineage with rough colony morphology and multidrug resistance," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50331-y
    DOI: 10.1038/s41467-024-50331-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50331-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-50331-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Ilana Kaspy & Eitan Rotem & Noga Weiss & Irine Ronin & Nathalie Q. Balaban & Gad Glaser, 2013. "HipA-mediated antibiotic persistence via phosphorylation of the glutamyl-tRNA-synthetase," Nature Communications, Nature, vol. 4(1), pages 1-7, December.
    2. Kate S. Baker & Timothy J. Dallman & Nigel Field & Tristan Childs & Holly Mitchell & Martin Day & François-Xavier Weill & Sophie Lefèvre & Mathieu Tourdjman & Gwenda Hughes & Claire Jenkins & Nicholas, 2018. "Horizontal antimicrobial resistance transfer drives epidemics of multiple Shigella species," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    3. Danielle J. Ingle & Rebecca L. Ambrose & Sarah L. Baines & Sebastian Duchene & Anders Gonçalves da Silva & Darren Y. J. Lee & Miriam Jones & Mary Valcanis & George Taiaroa & Susan A. Ballard & Martyn , 2021. "Evolutionary dynamics of multidrug resistant Salmonella enterica serovar 4,[5],12:i:- in Australia," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    4. Michael McClelland & Kenneth E. Sanderson & John Spieth & Sandra W. Clifton & Phil Latreille & Laura Courtney & Steffen Porwollik & Johar Ali & Mike Dante & Feiyu Du & Shunfang Hou & Dan Layman & Shaw, 2001. "Complete genome sequence of Salmonella enterica serovar Typhimurium LT2," Nature, Nature, vol. 413(6858), pages 852-856, October.
    5. Sandra Van Puyvelde & Derek Pickard & Koen Vandelannoote & Eva Heinz & Barbara Barbé & Tessa de Block & Simon Clare & Eve L. Coomber & Katherine Harcourt & Sushmita Sridhar & Emily A. Lees & Nicole E., 2019. "An African Salmonella Typhimurium ST313 sublineage with extensive drug-resistance and signatures of host adaptation," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Xiangkai Zhen & Yongyu Wu & Jinli Ge & Jiaqi Fu & Le Ye & Niannian Lin & Zhijie Huang & Zihe Liu & Zhao-qing Luo & Jiazhang Qiu & Songying Ouyang, 2022. "Molecular mechanism of toxin neutralization in the HipBST toxin-antitoxin system of Legionella pneumophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Tuan-Anh Tran & Sushmita Sridhar & Stephen T. Reece & Octavie Lunguya & Jan Jacobs & Sandra Puyvelde & Florian Marks & Gordon Dougan & Nicholas R. Thomson & Binh T. Nguyen & Pham The Bao & Stephen Bak, 2024. "Combining machine learning with high-content imaging to infer ciprofloxacin susceptibility in isolates of Salmonella Typhimurium," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Vincenzo Torraca & Myrsini Kaforou & Jayne Watson & Gina M Duggan & Hazel Guerrero-Gutierrez & Sina Krokowski & Michael Hollinshead & Thomas B Clarke & Rafal J Mostowy & Gillian S Tomlinson & Vanessa , 2019. "Shigella sonnei infection of zebrafish reveals that O-antigen mediates neutrophil tolerance and dysentery incidence," PLOS Pathogens, Public Library of Science, vol. 15(12), pages 1-26, December.
    4. Wim L. Cuypers & Pieter Meysman & François-Xavier Weill & Rene S. Hendriksen & Getenet Beyene & John Wain & Satheesh Nair & Marie A. Chattaway & Blanca M. Perez-Sepulveda & Pieter-Jan Ceyssens & Tessa, 2023. "A global genomic analysis of Salmonella Concord reveals lineages with high antimicrobial resistance in Ethiopia," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    5. Sophie Lefèvre & Elisabeth Njamkepo & Sarah Feldman & Corinne Ruckly & Isabelle Carle & Monique Lejay-Collin & Laëtitia Fabre & Iman Yassine & Lise Frézal & Maria Pardos de la Gandara & Arnaud Fontane, 2023. "Rapid emergence of extensively drug-resistant Shigella sonnei in France," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    6. George E. Stenhouse & Karen H. Keddy & Rebecca J. Bengtsson & Neil Hall & Anthony M. Smith & Juno Thomas & Miren Iturriza-Gómara & Kate S. Baker, 2023. "The genomic epidemiology of shigellosis in South Africa," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Lena Krone & Srujita Mahankali & Tobias Geiger, 2024. "Cytolysin A is an intracellularly induced and secreted cytotoxin of typhoidal Salmonella," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. Lewis C. E. Mason & David R. Greig & Lauren A. Cowley & Sally R. Partridge & Elena Martinez & Grace A. Blackwell & Charlotte E. Chong & P. Malaka Silva & Rebecca J. Bengtsson & Jenny L. Draper & Andre, 2023. "The evolution and international spread of extensively drug resistant Shigella sonnei," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    9. Iman Yassine & Sophie Lefèvre & Elisabeth E. Hansen & Corinne Ruckly & Isabelle Carle & Monique Lejay-Collin & Laëtitia Fabre & Rayane Rafei & Dominique Clermont & Maria Pardos Gandara & Fouad Dabbous, 2022. "Population structure analysis and laboratory monitoring of Shigella by core-genome multilocus sequence typing," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    10. Yu-Yu Cheng & Zhengyi Chen & Xinyun Cao & Tyler D. Ross & Tanya G. Falbel & Briana M. Burton & Ophelia S. Venturelli, 2023. "Programming bacteria for multiplexed DNA detection," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    11. Nanna Munck & Patrick Murigu Kamau Njage & Pimlapas Leekitcharoenphon & Eva Litrup & Tine Hald, 2020. "Application of Whole‐Genome Sequences and Machine Learning in Source Attribution of Salmonella Typhimurium," Risk Analysis, John Wiley & Sons, vol. 40(9), pages 1693-1705, September.
    12. Shaofu Qiu & Kangkang Liu & Chaojie Yang & Ying Xiang & Kaiyuan Min & Kunpeng Zhu & Hongbo Liu & Xinying Du & Mingjuan Yang & Ligui Wang & Yong Sun & Haijian Zhou & Muti Mahe & Jiayong Zhao & Shijun L, 2022. "A Shigella sonnei clone with extensive drug resistance associated with waterborne outbreaks in China," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50331-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.