Rapid and Integrated Bacterial Evolution Analysis unveils gene mutations and clinical risk of Klebsiella pneumoniae

Kojiro Uemura, Toyotaka Sato (), Soh Yamamoto, Noriko Ogasawara, Jirachaya Toyting, Kotaro Aoki, Akira Takasawa, Masayuki Koyama, Atsushi Saito, Takayuki Wada, Kaho Okada, Yurie Yoshida, Koji Kuronuma, Chie Nakajima, Yasuhiko Suzuki, Motohiro Horiuchi, Kenichi Takano, Satoshi Takahashi, Hirofumi Chiba and Shin-ichi Yokota
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Kojiro Uemura: Sapporo Medical University School of Medicine
Toyotaka Sato: Sapporo Medical University School of Medicine
Soh Yamamoto: Sapporo Medical University School of Medicine
Noriko Ogasawara: Sapporo Medical University School of Medicine
Jirachaya Toyting: Hokkaido University
Kotaro Aoki: 5-21-16 Omori-nishi
Akira Takasawa: Asahikawa Medical University
Masayuki Koyama: Sapporo Medical University School of Medicine
Atsushi Saito: Sapporo Medical University School of Medicine
Takayuki Wada: Sugimoto
Kaho Okada: Hokkaido University
Yurie Yoshida: Sapporo Medical University School of Medicine
Koji Kuronuma: Sapporo Medical University School of Medicine
Chie Nakajima: N20
Yasuhiko Suzuki: N20
Motohiro Horiuchi: Hokkaido University
Kenichi Takano: University
Satoshi Takahashi: Sapporo Medical University School of Medicine
Hirofumi Chiba: Sapporo Medical University School of Medicine
Shin-ichi Yokota: Sapporo Medical University School of Medicine

Nature Communications, 2025, vol. 16, issue 1, 1-17

Abstract: Abstract Bacteria continually evolve. Previous studies have evaluated bacterial evolution in retrospect, but this approach is based on only speculation. Cohort studies are reliable but require a long duration. Additionally, identifying which genetic mutations that have emerged during bacterial evolution possess functions of interest to researchers is an exceptionally challenging task. Here, we establish a Rapid and Integrated Bacterial Evolution Analysis (RIBEA) based on serial passaging experiments using hypermutable strains, whole-genome and transposon-directed sequencing, and in vivo evaluations to monitor bacterial evolution in a cohort for one month. RIBEA reveals bacterial factors contributing to serum and antimicrobial resistance by identifying gene mutations that occurred during evolution in the major respiratory pathogen Klebsiella pneumoniae. RIBEA also enables the evaluation of the risk for the progression and the development of invasive ability from the lung to blood and antimicrobial resistance. Our results demonstrate that RIBEA enables the observation of bacterial evolution and the prediction and identification of clinically relevant high-risk bacterial strains, clarifying the associated pathogenicity and the development of antimicrobial resistance at genetic mutation level.

Date: 2025
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DOI: 10.1038/s41467-025-58049-1

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