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Giant viruses as reservoirs of antibiotic resistance genes

Author

Listed:
  • Xinzhu Yi

    (South China Normal University)

  • Jie-Liang Liang

    (South China Normal University)

  • Ping Wen

    (South China Normal University)

  • Pu Jia

    (South China Normal University)

  • Shi-wei Feng

    (South China Normal University)

  • Shen-yan Liu

    (South China Normal University)

  • Yuan-yue Zhuang

    (South China Normal University)

  • Yu-qian Guo

    (South China Normal University)

  • Jing-li Lu

    (South China Normal University)

  • Sheng-ji Zhong

    (South China Normal University)

  • Bin Liao

    (Sun Yat-sen University)

  • Zhang Wang

    (South China Normal University)

  • Wen-sheng Shu

    (South China Normal University)

  • Jin-tian Li

    (South China Normal University)

Abstract

Nucleocytoplasmic large DNA viruses (NCLDVs; also called giant viruses), constituting the phylum Nucleocytoviricota, can infect a wide range of eukaryotes and exchange genetic material with not only their hosts but also prokaryotes and phages. A few NCLDVs were reported to encode genes conferring resistance to beta‑lactam, trimethoprim, or pyrimethamine, suggesting that they are potential vehicles for the transmission of antibiotic resistance genes (ARGs) in the biome. However, the incidence of ARGs across the phylum Nucleocytoviricota, their evolutionary characteristics, their dissemination potential, and their association with virulence factors remain unexplored. Here, we systematically investigated ARGs of 1416 NCLDV genomes including those of almost all currently available cultured isolates and high-quality metagenome-assembled genomes from diverse habitats across the globe. We reveal that 39.5% of them carry ARGs, which is approximately 37 times higher than that for phage genomes. A total of 12 ARG types are encoded by NCLDVs. Phylogenies of the three most abundant NCLDV-encoded ARGs hint that NCLDVs acquire ARGs from not only eukaryotes but also prokaryotes and phages. Two NCLDV-encoded trimethoprim resistance genes are demonstrated to confer trimethoprim resistance in Escherichia coli. The presence of ARGs in NCLDV genomes is significantly correlated with mobile genetic elements and virulence factors.

Suggested Citation

  • Xinzhu Yi & Jie-Liang Liang & Ping Wen & Pu Jia & Shi-wei Feng & Shen-yan Liu & Yuan-yue Zhuang & Yu-qian Guo & Jing-li Lu & Sheng-ji Zhong & Bin Liao & Zhang Wang & Wen-sheng Shu & Jin-tian Li, 2024. "Giant viruses as reservoirs of antibiotic resistance genes," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51936-z
    DOI: 10.1038/s41467-024-51936-z
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    References listed on IDEAS

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    1. Sofia Rigou & Sébastien Santini & Chantal Abergel & Jean-Michel Claverie & Matthieu Legendre, 2022. "Past and present giant viruses diversity explored through permafrost metagenomics," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. 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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