Soil microbial and plant responses to increasing antibiotic concentration: a case study of five antibiotics

Abstract

Antibiotic contamination from biogenic waste in agricultural soils poses a significant threat to soil health and crop productivity. We investigated the effect of antibiotics on the soil microbial community, antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) and plant productivity in a six week greenhouse trial. Here, Spinacia oleracea (spinach) and Raphanus sativus (radish) were grown from seed and a mix of five antibiotics, namely sulfamethoxazole, trimethoprim, enrofloxacin, clarithromycin and chlortetracycline, were added to the soil at concentrations 0, 0.1, 1 and 10 mg kg-1 soil dry weight (c0, c0.1, c1 and c10, respectively). Overall, we found that the antibiotic treatments significantly impacted prokaryotic -diversity and prokaryotic and fungal {beta}-diversity. Human and plant pathogen abundance did not increase under antibiotic exposure, but there was a significant reduction of plant growth-promoting bacteria. Moreover, the c10 treatment significantly increased the abundance of MGE intI1 indicative of horizontal gene transfer and ARG sul1 antibiotic resistance and significantly lowered radish biomass and nitrogen uptake, while spinach biomass and nitrogen uptake were unaffected. In summary, our study showed that antibiotic exposure significantly changed prokaryotic community diversity and taxonomy, while fungi remained largely unaffected. The reduction of plant growth-promoting bacteria may have a significant impact on soil nutrient cycling and crop productivity, but more research is needed to understand the long-term impact of these co-applied antibiotics on food production. Additionally, more studies are needed to understand the effect of antibiotics on realistic, field scale, conditions to fully understand the impact on environmental and human health. ImportanceAgricultural soils are increasingly contaminated with complex mixtures of antibiotics from various biogenic sources, yet we lack a clear understanding of their specific ecological impact. While many studies investigate antibiotics, they often are studied in pollution sources like manure which contain confounding factors like heavy metals. To provide clear mechanistic insight, we investigated the effects of a complex, five-antibiotic mixture on the soil-plant system, independent of other contaminants. This revealed that the effect of antibiotics extends beyond selecting for antibiotic resistance. Specifically, the reduction of prokaryotic diversity and plant growth-promoting bacteria under antibiotic exposure can have potential detrimental effects on plant and soil health. Moreover, we found that antibiotic exposure can reduce plant biomass and nitrogen uptake, but this is highly plant dependent. This research highlights the critical need to monitor antibiotic pollution due to its potential detrimental effect on plant health and alterations to the soil microbiome.