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Evolution of the murine gut resistome following broad-spectrum antibiotic treatment

Author

Listed:
  • Laura Nies

    (University of Luxembourg)

  • Susheel Bhanu Busi

    (University of Luxembourg)

  • Mina Tsenkova

    (University of Luxembourg)

  • Rashi Halder

    (University of Luxembourg)

  • Elisabeth Letellier

    (University of Luxembourg)

  • Paul Wilmes

    (University of Luxembourg
    University of Luxembourg)

Abstract

The emergence and spread of antimicrobial resistance (AMR) represent an ever-growing healthcare challenge worldwide. Nevertheless, the mechanisms and timescales shaping this resistome remain elusive. Using an antibiotic cocktail administered to a murine model along with a longitudinal sampling strategy, we identify the mechanisms by which gut commensals acquire antimicrobial resistance genes (ARGs) after a single antibiotic course. While most of the resident bacterial populations are depleted due to the treatment, Akkermansia muciniphila and members of the Enterobacteriaceae, Enterococcaceae, and Lactobacillaceae families acquire resistance and remain recalcitrant. We identify specific genes conferring resistance against the antibiotics in the corresponding metagenome-assembled genomes (MAGs) and trace their origins within each genome. Here we show that, while mobile genetic elements (MGEs), including bacteriophages and plasmids, contribute to the spread of ARGs, integrons represent key factors mediating AMR in the antibiotic-treated mice. Our findings suggest that a single course of antibiotics alone may act as the selective sweep driving ARG acquisition and incidence in gut commensals over a single mammalian lifespan.

Suggested Citation

  • Laura Nies & Susheel Bhanu Busi & Mina Tsenkova & Rashi Halder & Elisabeth Letellier & Paul Wilmes, 2022. "Evolution of the murine gut resistome following broad-spectrum antibiotic treatment," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29919-9
    DOI: 10.1038/s41467-022-29919-9
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    1. Alessio Milanese & Daniel R Mende & Lucas Paoli & Guillem Salazar & Hans-Joachim Ruscheweyh & Miguelangel Cuenca & Pascal Hingamp & Renato Alves & Paul I Costea & Luis Pedro Coelho & Thomas S. B. Schm, 2019. "Microbial abundance, activity and population genomic profiling with mOTUs2," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    2. Linda Wampach & Anna Heintz-Buschart & Joëlle V. Fritz & Javier Ramiro-Garcia & Janine Habier & Malte Herold & Shaman Narayanasamy & Anne Kaysen & Angela H. Hogan & Lutz Bindl & Jean Bottu & Rashi Hal, 2018. "Birth mode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    3. Yongfei Hu & Xi Yang & Junjie Qin & Na Lu & Gong Cheng & Na Wu & Yuanlong Pan & Jing Li & Liying Zhu & Xin Wang & Zhiqi Meng & Fangqing Zhao & Di Liu & Juncai Ma & Nan Qin & Chunsheng Xiang & Yonghong, 2013. "Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota," Nature Communications, Nature, vol. 4(1), pages 1-7, October.
    4. Elizabeth J. Culp & Nicholas Waglechner & Wenliang Wang & Aline A. Fiebig-Comyn & Yen-Pang Hsu & Kalinka Koteva & David Sychantha & Brian K. Coombes & Michael S. Nieuwenhze & Yves V. Brun & Gerard D. , 2020. "Evolution-guided discovery of antibiotics that inhibit peptidoglycan remodelling," Nature, Nature, vol. 578(7796), pages 582-587, February.
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