Tackling Soil ARG-Carrying Pathogens with Global-Scale Metagenomics

Antibiotic overuse and the subsequent environmental contamination of residual antibiotics poses a public health crisis via an acceleration in the spread of antibiotic resistance genes (ARGs) through horizontal gene transfer. Although the occurrence, distribution, and driving factors of ARGs in soils have been widely investigated, little is known about the antibiotic resistance of soilborne pathogens at a global scale. To explore this gap, contigs from 1643 globally sourced metagnomes are assembled, yielding 407 ARG-carrying pathogens (APs) with at least one ARG; APs are detected in 1443 samples (sample detection rate of 87.8%). The richness of APs is greater in agricultural soils (with a median of 20) than in non-agricultural ecosystems. Agricultural soils possess a high prevalence of clinical APs affiliated with Escherichia, Enterobacter, Streptococcus, and Enterococcus. The APs detected in agricultural soils tend to coexist with multidrug resistance genes and bacA. A global map of soil AP richness is generated, where anthropogenic and climatic factors explained AP hot spots in East Asia, South Asia, and the eastern United States. The results herein advance this understanding of the global distribution of soil APs and determine regions prioritized to control soilborne APs worldwide.

Automated summary

Antibiotic overuse and environmental contamination of residual antibiotics contribute to the global spread of antibiotic resistance genes (ARGs) through horizontal gene transfer. This study investigated the antibiotic resistance of soilborne pathogens at a global scale, identifying 407 ARG-carrying pathogens (APs) in 1443 samples. Agricultural soils exhibited a higher richness of APs compared to non-agricultural ecosystems, with a prevalence of clinical APs affiliated with Escherichia, Enterobacter, Streptococcus, and Enterococcus. A global map of soil AP richness was generated, highlighting hot spots in East Asia, South Asia, and the eastern United States, which can guide efforts to control soilborne APs worldwide.