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Peer-reviewedCC BYScience Advances

Phage-ICE tandems facilitate bacterial adaptation and antimicrobial resistance spread

  • Jinhu Huang1,2
  • Jiaqi Zhao2,3
  • Pengchao Zhan3
  • Xingyang Dai2
  • Xinming Pan4
  • Zhenmiao Li5
  • Wenbin Zhao1,2
  • Xiaoli Shi6
  • Xiaoming Wang2
  • Shengyong Mao3
  • Jiale Ma4
  • Liping Wang2
1 more authors
  • Jinxin Liu1,3
6 affiliations
  1. 1Sanya Institute of Nanjing Agricultural University, Sanya 572025, China.
  2. 2MOE Joint International Research Laboratory of Animal Health and Food Safety, Risk Assessment Center of Veterinary Drug Residue and Antimicrobial Resistance, Center for Veterinary Drug Research and Evaluation, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, China.
  3. 3Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, National Center for International Research on Animal Gut Nutrition, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China.
  4. 4WOAH Reference Lab for Swine Streptococcosis, Nanjing 210095, China.
  5. 5The Air Force Hospital of Eastern Theater of PLA, Nanjing 210002, China.
  6. 6National Experimental Teaching Demonstration Center for Animal Science, Nanjing 210095, China.
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Abstract

Phages and integrative and conjugative elements (ICEs) drive bacterial evolution, but how their interplay shapes bacterial adaptation and antimicrobial resistance (AMR) dissemination remains unclear. Here, we characterize phage-ICE tandems formed by site-specific accretion of phages and ICEs into cotransferable units. In Streptococcus , phage-encoded integrases (IntIE Phage ) drive stress-inducible excision and circularization, after which ICE machinery mediates conduction of the tandem. When excision is impaired, phage and phage-ICE fragments disseminate by transformation and integrate via RecA-dependent homologous recombination (HR), providing a fail-safe route. This pathway enables cotransfer of flanking chromosomal DNA, generating length-variable integrations that remodel transcriptional programs and increase oxidative stress tolerance. A global screen identified 612 phage-ICE tandems across seven phyla and 135 species, including multidrug-resistant pathogens, with lineage-specific repertoires of AMR, virulence, and metabolic genes. Rather than a hybrid element, these structures represent functional interplay where prophages exploit ICE conjugation while facilitating mobilization of the composite region. By coupling excision, transfer, and recombination, phage-ICEs shape adaptation and accelerate AMR spread.

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Cite

BibTeXRIS
BibTeX
@article{huang2026phageice,
  title = {{Phage-ICE tandems facilitate bacterial adaptation and antimicrobial resistance spread}},
  author = {Jinhu Huang and Jiaqi Zhao and Pengchao Zhan and Xingyang Dai and Xinming Pan and Zhenmiao Li and Wenbin Zhao and Xiaoli Shi and Xiaoming Wang and Shengyong Mao and Jiale Ma and Liping Wang and Jinxin Liu},
  journal = {Science Advances},
  year = {2026},
  month = oct,
  doi = {10.1126/sciadv.aed3416},
  url = {https://www.science.org/doi/10.1126/sciadv.aed3416},
  note = {CC BY},
}
RIS
TY  - JOUR
TI  - Phage-ICE tandems facilitate bacterial adaptation and antimicrobial resistance spread
AU  - Jinhu Huang
AU  - Jiaqi Zhao
AU  - Pengchao Zhan
AU  - Xingyang Dai
AU  - Xinming Pan
AU  - Zhenmiao Li
AU  - Wenbin Zhao
AU  - Xiaoli Shi
AU  - Xiaoming Wang
AU  - Shengyong Mao
AU  - Jiale Ma
AU  - Liping Wang
AU  - Jinxin Liu
PY  - 2026
DA  - 2026/10/09
JO  - Science Advances
DO  - 10.1126/sciadv.aed3416
UR  - https://www.science.org/doi/10.1126/sciadv.aed3416
AB  - Phages and integrative and conjugative elements (ICEs) drive bacterial evolution, but how their interplay shapes bacterial adaptation and antimicrobial resistance (AMR) dissemination remains unclear. Here, we characterize phage-ICE tandems formed by site-specific accretion of phages and ICEs into cotransferable units. In Streptococcus , phage-encoded integrases (IntIE Phage ) drive stress-inducible excision and circularization, after which ICE machinery mediates conduction of the tandem. When excision is impaired, phage and phage-ICE fragments disseminate by transformation and integrate via RecA-dependent homologous recombination (HR), providing a fail-safe route. This pathway enables cotransfer of flanking chromosomal DNA, generating length-variable integrations that remodel transcriptional programs and increase oxidative stress tolerance. A global screen identified 612 phage-ICE tandems across seven phyla and 135 species, including multidrug-resistant pathogens, with lineage-specific repertoires of AMR, virulence, and metabolic genes. Rather than a hybrid element, these structures represent functional interplay where prophages exploit ICE conjugation while facilitating mobilization of the composite region. By coupling excision, transfer, and recombination, phage-ICEs shape adaptation and accelerate AMR spread.
SN  - 2375-2548
ER  -