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

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, Ville-Petri Friman, Michael Gillings, Manuel Delgado-Baquerizo () and Yong-guan Zhu ()
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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

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-52450-y

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