Dissemination of antibiotic resistance through soil-plant-earthworm continuum in the food production environment

Authors: BHATTACHARJEE, ANANDA - University Of California, Riverside; PHAN, D - University Of California, Riverside; ZHENG, CHUJING - University Of California, Riverside; Ashworth, Daniel; Schmidt, Michael - Mike; MEN, YUJI - University Of California, Riverside; Ferreira, Jorge; MUIR, GABRIELLE - Ezbiome; HASAN, NUR - Ezbiome; Ibekwe, Abasiofiok - Mark

Submitted to: Environment International
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/5/2023
Publication Date: 12/10/2023
Citation: Bhattacharjee, A.S., Phan, D., Zheng, C., Ashworth, D.J., Schmidt, M.P., Men, Y., Ferreira, J.F., Muir, G., Hasan, N.A., Ibekwe, A.M. 2023. Dissemination of antibiotic resistance through soil-plant-earthworm continuum in the food production environment. Environment International. 183. Article 108374. https://doi.org/10.1016/j.envint.2023.108374.
DOI: https://doi.org/10.1016/j.envint.2023.108374

Interpretive Summary: The increasing demand for food production and the expansion of irrigated agriculture have put significant pressure on water resources, particularly in arid and semi-arid regions. Recycling wastewater for irrigation is one potential avenue to increasing water availability. However, there are major concerns regarding chemicals of emerging concern such as antibiotics and antibiotic resistance genes in treated municipal wastewater. In this study spinach and radish were irrigated with treated municipal wastewater grown in a greenhouse experiment. Our results show that microbial diversity in spinach and radish phyllosphere were lower than those from the bulk soil, rhizosphere soil, and earthworm feces. However, the number of antibiotic resistance genes and antibiotic-resistant bacteria enriched in spinach was higher than that of radish. The results of this research will be used by researchers and agencies that are involved in wastewater management.

Technical Abstract: Treated municipal wastewater (TMW) can provide a reliable source of irrigation water for crops, which is especially important in arid areas where water resources are limited or prone to drought. Nonetheless, TMW may contain residual antibiotics, potentially exposing the crops to these substances. In this study, we investigated the dissemination of antimicrobial resistance (AMR) in the soil–plant–earthworm continuum impacted by irrigation with TMW containing trimethoprim, sulfamethoxazole, and sulfapyridine antibiotics under greenhouse experiment using shotgun sequencing. Our results show that microbial diversity in spinach and radish phyllosphere were significantly (P<0.001) lower than those from the bulk soil, rhizosphere soil, and earthworm feces. However, the number of ARGs and antibiotic-resistant bacteria (ARB) enriched in spinach was significantly higher (P = 0.001) compared to radish. Moreover, a strong correlation was observed between ARG and microbial diversities in spinach and radish. Thus, changes in the abundance of ARG may exert selective pressure on the microbial community, influencing its composition and diversity. The abundance of ARG decreased from bulk soil to rhizosphere to phyllospheres and endospheres. Similarly, zero ARB genomes were recovered from the rhizosphere, phyllosphere, and endosphere of spinach and radish. However, this did not impede the enrichment of ARGs and ARBs in earthworms fed with plant materials grown on TMW and TMW spiked with higher concentrations of antibiotics. Our study highlights that irrigation with TMW, and TMW spiked with higher concentrations of antibiotics are drivers of the enrichment of ARGs and ARBs in the soil–plant–earthworm continuum.