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Prophage-encoded antibiotic resistance genes are enriched in human-impacted environments

Author

Listed:
  • Hanpeng Liao

    (Fujian Agriculture and Forestry University)

  • Chen Liu

    (Fujian Agriculture and Forestry University)

  • Shungui Zhou

    (Fujian Agriculture and Forestry University)

  • Chunqin Liu

    (Fujian Agriculture and Forestry University)

  • David J. Eldridge

    (University of New South Wales)

  • Chaofan Ai

    (Fujian Agriculture and Forestry University)

  • Steven W. Wilhelm

    (The University of Tennessee)

  • Brajesh K. Singh

    (Western Sydney University)

  • Xiaolong Liang

    (Chinese Academy of Sciences)

  • Mark Radosevich

    (The University of Tennessee)

  • Qiu-e Yang

    (Fujian Agriculture and Forestry University)

  • Xiang Tang

    (Fujian Agriculture and Forestry University)

  • Zhong Wei

    (Nanjing Agricultural University)

  • Ville-Petri Friman

    (University of Helsinki)

  • Michael Gillings

    (Macquarie University)

  • Manuel Delgado-Baquerizo

    (Consejo Superior de Investigaciones Científicas)

  • Yong-guan Zhu

    (Chinese Academy of Sciences)

Abstract

The spread of antibiotic resistance genes (ARGs) poses a substantial threat to human health. Phage-mediated transduction could exacerbate ARG transmission. While several case studies exist, it is yet unclear to what extent phages encode and mobilize ARGs at the global scale and whether human impacts play a role in this across different habitats. Here, we combine 38,605 bacterial genomes, 1432 metagenomes, and 1186 metatranscriptomes across 12 contrasting habitats to explore the distribution of prophages and their cargo ARGs in natural and human-impacted environments. Worldwide, we observe a significant increase in the abundance, diversity, and activity of prophage-encoded ARGs in human-impacted habitats linked with relatively higher risk of past antibiotic exposure. This effect was driven by phage-encoded cargo ARGs that could be mobilized to provide increased resistance in heterologous E. coli host for a subset of analyzed strains. Our findings suggest that human activities have altered bacteria-phage interactions, enriching ARGs in prophages and making ARGs more mobile across habitats globally.

Suggested Citation

  • Hanpeng Liao & Chen Liu & Shungui Zhou & Chunqin Liu & David J. Eldridge & Chaofan Ai & Steven W. Wilhelm & Brajesh K. Singh & Xiaolong Liang & Mark Radosevich & Qiu-e Yang & Xiang Tang & Zhong Wei & , 2024. "Prophage-encoded antibiotic resistance genes are enriched in human-impacted environments," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52450-y
    DOI: 10.1038/s41467-024-52450-y
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    References listed on IDEAS

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    1. Santiago Redondo-Salvo & Raúl Fernández-López & Raúl Ruiz & Luis Vielva & María de Toro & Eduardo P. C. Rocha & M. Pilar Garcillán-Barcia & Fernando de la Cruz, 2020. "Pathways for horizontal gene transfer in bacteria revealed by a global map of their plasmids," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    2. Xiyang Dong & Chuwen Zhang & Yongyi Peng & Hong-Xi Zhang & Ling-Dong Shi & Guangshan Wei & Casey R. J. Hubert & Yong Wang & Chris Greening, 2022. "Phylogenetically and catabolically diverse diazotrophs reside in deep-sea cold seep sediments," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Hannah G. Hampton & Bridget N. J. Watson & Peter C. Fineran, 2020. "The arms race between bacteria and their phage foes," Nature, Nature, vol. 577(7790), pages 327-336, January.
    4. Yi Yi & Shunzhang Liu & Yali Hao & Qingyang Sun & Xinjuan Lei & Yecheng Wang & Jiahua Wang & Mujie Zhang & Shan Tang & Qingxue Tang & Yue Zhang & Xipeng Liu & Yinzhao Wang & Xiang Xiao & Huahua Jian, 2023. "A systematic analysis of marine lysogens and proviruses," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Mohammad Moniruzzaman & Louie L. Wurch & Harriet Alexander & Sonya T. Dyhrman & Christopher J. Gobler & Steven W. Wilhelm, 2017. "Virus-host relationships of marine single-celled eukaryotes resolved from metatranscriptomics," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    6. Frederik Schulz & Simon Roux & David Paez-Espino & Sean Jungbluth & David A. Walsh & Vincent J. Denef & Katherine D. McMahon & Konstantinos T. Konstantinidis & Emiley A. Eloe-Fadrosh & Nikos C. Kyrpid, 2020. "Giant virus diversity and host interactions through global metagenomics," Nature, Nature, vol. 578(7795), pages 432-436, February.
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