Altered genomic methylation promotes Staphylococcus aureus persistence in hospital environment

Yuriko Yamazaki, Tomoka Ito, Seitaro Nakagawa, Takashi Sugihira, Chinami Kurita-Tachibana, Amer E. Villaruz, Kensuke Ishiguro, Barbora Salcman, Shuo Li, Sanami Takada, Naohiro Inohara, Yoko Kusuya, Aki Shibata, Masakazu Tamai, Reika Aoyama, Kanako Inoue, Shota Murata, Kazuyuki Matsushita, Akiko Miyabe, Toshibumi Taniguchi, Hidetoshi Igari, Naruhiko Ishiwada, Masateru Taniguchi, Taka-Aki Nakada, Hiroyuki Matsue, Manabu Fujimoto, Haruka Hishiki, Yoshiteru Osone, Hiromichi Hamada, Naoki Shimojo, Tsutomu Suzuki, Michael Otto, Gabriel Núñez, Hiroki Takahashi, Akiko Takaya and Yuumi Nakamura ()
Additional contact information
Yuriko Yamazaki: Chiba University Graduate School of Medicine
Tomoka Ito: Osaka University Graduate School of Medicine
Seitaro Nakagawa: Chiba University Graduate School of Medicine
Takashi Sugihira: Osaka University Graduate School of Medicine
Chinami Kurita-Tachibana: Osaka University
Amer E. Villaruz: Bethesda
Kensuke Ishiguro: The University of Tokyo
Barbora Salcman: Osaka University
Shuo Li: Osaka University
Sanami Takada: Chiba University Graduate School of Medicine
Naohiro Inohara: University of Michigan Medical School
Yoko Kusuya: Chiba University
Aki Shibata: Chiba University
Masakazu Tamai: Osaka University Graduate School of Medicine
Reika Aoyama: Osaka University Graduate School of Medicine
Kanako Inoue: Osaka University
Shota Murata: Chiba University Hospital
Kazuyuki Matsushita: Chiba University Hospital
Akiko Miyabe: Chiba University Hospital
Toshibumi Taniguchi: Chiba University Hospital
Hidetoshi Igari: Chiba University Hospital
Naruhiko Ishiwada: Chiba University
Masateru Taniguchi: Osaka University
Taka-Aki Nakada: Chiba University Graduate School of Medicine
Hiroyuki Matsue: Chiba University Graduate School of Medicine
Manabu Fujimoto: Osaka University Graduate School of Medicine
Haruka Hishiki: Chiba University Graduate School of Medicine
Yoshiteru Osone: Chiba University Graduate School of Medicine
Hiromichi Hamada: Chiba University Graduate School of Medicine
Naoki Shimojo: Chiba University Graduate School of Medicine
Tsutomu Suzuki: The University of Tokyo
Michael Otto: Bethesda
Gabriel Núñez: University of Michigan Medical School
Hiroki Takahashi: Chiba University
Akiko Takaya: Chiba University
Yuumi Nakamura: Osaka University

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

Abstract: Abstract Staphylococcus aureus can cause outbreaks and becomes multi-drug resistant through gene mutations and acquiring resistance genes. However, why S. aureus easily adapts to hospital environments, promoting resistance and recurrent infections, remains unknown. Here we show that a specific S. aureus lineage evolved from a clone that expresses the accessory gene regulator (Agr) system to subclones that reversibly suppressed Agr and caused an outbreak in the hospital setting. S. aureus with flexible Agr regulation shows increased ability to acquire antibiotic-resistant plasmids, escape host immunity, and colonize mice. Bacteria with flexible Agr regulation shows altered cytosine genomic methylation, including the decreased 5mC methylation in transcriptional regulator genes (pcrA and rpsD), compared to strains with normal Agr expression patterns. In this work, we discover how altered genomic methylation promotes flexible Agr regulation which is associated with persistent pathogen colonization in the hospital environment.

Date: 2024
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DOI: 10.1038/s41467-024-54033-3

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