4.8 Article

Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes

Journal

MOLECULAR BIOLOGY AND EVOLUTION
Volume 38, Issue 6, Pages 2337-2350

Publisher

OXFORD UNIV PRESS
DOI: 10.1093/molbev/msab029

Keywords

agrochemicals; antibiotic resistance; experimental evolution; herbicide tolerance; soil microbiomes; mobile genetic elements

Funding

  1. National Natural Science Foundation of China [31972521, 42090060]
  2. National Key Technologies R&D Program of China [2017YFD0800203]
  3. Fujian Agriculture and Forestry University Program for Distinguished Young Scholar [XJQ2017001]
  4. Natural Science Foundation of Fujian [2018J01709]
  5. Royal Society [RSG\R1\180213, CHL\R1\180031]
  6. UKRI under the Strategic Priorities Fund Plant Bacterial Diseases programme at the University of York [BB/T010606/1]
  7. Defra under the Strategic Priorities Fund Plant Bacterial Diseases programme at the University of York [BB/T010606/1]
  8. Scottish Government, under the Strategic Priorities Fund Plant Bacterial Diseases programme at the University of York [BB/T010606/1]

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This study found that three widely used herbicides can increase the prevalence of antibiotic resistance genes and mobile genetic elements in soil microbiomes without significantly altering the abundance, diversity, and composition of bacterial communities. This could be due to positive selection for more tolerant genotypes and mutations in herbicide and antibiotic resistance genes. Additionally, herbicide exposure was shown to increase cell membrane permeability and the frequency of multidrug resistance plasmid transfer, facilitating the movement of antibiotic resistance genes between bacteria.
Herbicides are one of the most widely used chemicals in agriculture. While they are known to be harmful to nontarget organisms, the effects of herbicides on the composition and functioning of soil microbial communities remain unclear. Here we show that application of three widely used herbicides-glyphosate, glufosinate, and dicamba-increase the prevalence of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) in soil microbiomes without clear changes in the abundance, diversity and composition of bacterial communities. Mechanistically, these results could be explained by a positive selection for more tolerant genotypes that acquired several mutations in previously wellcharacterized herbicide and ARGs. Moreover, herbicide exposure increased cell membrane permeability and conjugation frequency of multidrug resistance plasmids, promoting ARG movement between bacteria. A similar pattern was found in agricultural soils across 11 provinces in China, where herbicide application, and the levels of glyphosate residues in soils, were associated with increased ARG and MGE abundances relative to herbicide-free control sites. Together, our results show that herbicide application can enrich ARGs and MGEs by changing the genetic composition of soil microbiomes, potentially contributing to the global antimicrobial resistance problem in agricultural environments.

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