Organic fertilization co-selects genetically linked antibiotic and metal(loid) resistance genes in global soil microbiome

Zi-Teng Liu, Rui-Ao Ma, Dong Zhu, Konstantinos T. Konstantinidis, Yong-Guan Zhu and Si-Yu Zhang ()
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Zi-Teng Liu: East China Normal University
Rui-Ao Ma: East China Normal University
Dong Zhu: Chinese Academy of Sciences
Konstantinos T. Konstantinidis: Georgia Institute of Technology
Yong-Guan Zhu: Chinese Academy of Sciences
Si-Yu Zhang: East China Normal University

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

Abstract: Abstract Antibiotic resistance genes (ARGs) and metal(loid) resistance genes (MRGs) coexist in organic fertilized agroecosystems based on their correlations in abundance, yet evidence for the genetic linkage of ARG-MRGs co-selected by organic fertilization remains elusive. Here, an analysis of 511 global agricultural soil metagenomes reveals that organic fertilization correlates with a threefold increase in the number of diverse types of ARG-MRG-carrying contigs (AMCCs) in the microbiome (63 types) compared to non-organic fertilized soils (22 types). Metatranscriptomic data indicates increased expression of AMCCs under higher arsenic stress, with co-regulation of the ARG-MRG pairs. Organic fertilization heightens the coexistence of ARG-MRG in genomic elements through impacting soil properties and ARG and MRG abundances. Accordingly, a comprehensive global map was constructed to delineate the distribution of coexistent ARG-MRGs with virulence factors and mobile genes in metagenome-assembled genomes from agricultural lands. The map unveils a heightened relative abundance and potential pathogenicity risks (range of 4-6) for the spread of coexistent ARG-MRGs in Central North America, Eastern Europe, Western Asia, and Northeast China compared to other regions, which acquire a risk range of 1-3. Our findings highlight that organic fertilization co-selects genetically linked ARGs and MRGs in the global soil microbiome, and underscore the need to mitigate the spread of these co-resistant genes to safeguard public health.

Date: 2024
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DOI: 10.1038/s41467-024-49165-5

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