Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes

Abstract

Herbicides are one of the most widely used chemicals in agriculture. While they are known to be harmful to non-target 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 well-characterized herbicide and antibiotic resistance genes. 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 eleven 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.

A glyphosate-based herbicide cross-selects for antibiotic resistance genes in bacterioplankton communities

“…For example, the surfactant polyethoxylenamine (POEA) has produced negative effects on Vibrio fischeri at lower doses than glyphosate acid [29]. However, given that our results are in general agreement with previous soil experiments using pure glyphosate [23], we believe that our findings are at least in part attributable to an effect of glyphosate itself. Furthermore, regardless of whether it is glyphosate or other constituents of GBH that drive cross-selection of ARGs, assessing the risks associated with commercial formulations is more ecologically realistically, as these formulations are used in agriculture fields and lawns [30].…”

“…An association between glyphosate and increases in ARGs and mobile genetic elements has been previously found in soil microbiomes, as demonstrated in a recent study combining experimental microcosms and environmental data from agricultural field sites in China [23]. Through laboratory assays in three bacterial strains, the authors quantified the conjugation frequency of a multidrug resistance plasmid induced by glyphosate and further investigated changes in cell membrane permeability.…”

“…Most studies of cross-resistance induced by herbicides focused on bacterial isolates in laboratory experiments [13][14][15][16]22]. A recent study has shown that herbicide selection increases the prevalence of ARGs in soil bacterial communities, using observational and experimental field data [23]. However, we still lack evidence for aquatic communities, which are of particular interest because herbicides often reach waterbodies through leaching, runoff, and spray drift from agricultural fields [4,24].…”

History and perspective of herbicide use in Australia and New Zealand

“…Bacterial composition in soil changes over time with herbicide exposure, with the type of herbicide also affecting composition (Moretto et al, 2017). Glyphosate, glufosinate, and dicamba have increased the occurrence of antibiotic resistance genes and mobile genetic elements in soil microbial communities (Liao et al, 2021). Transfer of these genes between bacteria was also found, whereby herbicides increased conjugation of multidrug resistance plasmids (Liao et al, 2021).…”

Molecular mechanisms underlying glyphosate resistance in bacteria

“…Recently, it has been observed that the application of glyphosate increases the prevalence of antibiotic resistance genes in soil microbiomes (Liao et al, 2021). However, this phenomenon seems to be due to an enrichment of antibiotic resistance genes and not caused by a genome-wide glyphosate-induced increase in the mutation rate (Tincher et al, 2017;Liao et al, 2021). Although glyphosate is considered toxicologically safe for animals and humans (Li and Long, 1988), the scientific debate about the toxicity of the weedkiller glyphosate is still ongoing (Arj o et al, 2013;Klingelhöfer et al, 2020).…”