Antibiotic Resistance in Agricultural Soil and Crops Associated to the Application of Cow Manure-Derived Amendments From Conventional and Organic Livestock Farms

Abstract

The application of organic amendments to agricultural soil can enhance crop yield, while improving the physicochemical and biological properties of the recipient soils. However, the use of manure-derived amendments as fertilizers entails environmental risks, such as the contamination of soil and crops with antibiotic residues, antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs). In order to delve into these risks, we applied dairy cow manure-derived amendments (slurry, fresh manure, aged manure), obtained from a conventional and an organic farm, to soil. Subsequently, lettuce and wheat plants were grown in the amended soils. After harvest, the abundance of 95 ARGs and MGE-genes from the amended soils and plants were determined by high-throughput qPCR. The structure of soil prokaryotic communities was determined by 16S rRNA amplicon sequencing and qPCR. The absolute abundance of ARGs and MGE-genes differed between treatments (amended vs. unamended), origins of amendment (conventional vs. organic), and types of amendment (slurry vs. fresh manure vs. aged manure). Regarding ARG-absolute abundances in the amendments themselves, higher values were usually found in slurry vs. fresh or aged manure. These abundances were generally higher in soil than in plant samples, and higher in wheat grain than in lettuce plants. Lettuce plants fertilized with conventional amendments showed higher absolute abundances of tetracycline resistance genes, compared to those amended with organic amendments. No single treatment could be identified as the best or worst treatment regarding the risk of antibiotic resistance in soil and plant samples. Within the same treatment, the resistome risk differed between the amendment, the amended soil and, finally, the crop. In other words, according to our data, the resistome risk in manure-amended crops cannot be directly inferred from the analysis of the amendments themselves. We concluded that, depending on the specific question under study, the analysis of the resistome risk should specifically focus on the amendment, the amended soil or the crop.

Reduction of the resistome risk from cow slurry and manure microbiomes to soil and vegetable microbiomes

“…It is well‐known fact that cow slurry and manure can be reservoirs of antibiotic resistance (Fahrenfeld et al ., 2014; Udikovic‐Kolic et al ., 2014; Jauregi et al ., 2021). In our study, in both exposure pathways (i.e.…”

“…The Chao1 index has been recommended, based on studies on large metagenomic datasets from multiple environments, for estimating ARG diversity (Lal Gupta et al ., 2020). We found higher resistome diversity in animal dejections compared to soils and vegetables, as previously reported (Li et al ., 2015a; Jauregi et al ., 2021; Macedo et al ., 2021). Prior to faecal excretion, ARGs can be horizontally transfer between different bacterial species within the animal gut.…”

Insights into the impact of manure on the environmental antibiotic residues and resistance pool

“…The abundance of 95 ARGs and MGEs from soils fertilized with dairy cow manure-derived amendments (slurry, fresh manure, aged manure), and plants (wheat grain and lettuce) was analyzed by high-throughput qPCR. The structure of soil prokaryotic communities was determined by 16S rRNA amplicon sequencing and qPCR (Jauregi et al, 2021). A higher ARGs abundance was found in slurry vs. fresh or aged manure, in soil vs. plant samples, and in wheat grain vs. lettuce (Jauregi et al, 2021;Zalewska et al, 2021).…”

“…The structure of soil prokaryotic communities was determined by 16S rRNA amplicon sequencing and qPCR (Jauregi et al, 2021). A higher ARGs abundance was found in slurry vs. fresh or aged manure, in soil vs. plant samples, and in wheat grain vs. lettuce (Jauregi et al, 2021;Zalewska et al, 2021). The available manure processing technologies are currently not taking into consideration, in terms of treatment performance, the removal of antibiotics, ARG and ARB, although evidence exists that ARB and ARG are not completely eliminated during manure treatments, contributing to the environmental resistome (Hou et al, 2017; Figure 5).…”

Biochar, Ochre, and Manure Maturation in an Acidic Technosol Helps Stabilize As and Pb in Soil and Allows Its Vegetation by Salix triandra

“…Impacts of amendments on soil properties and plant productivity in metal(loid)contaminated lands vary not only with soil characteristics, plant species, amendment properties, and application rates, but also with aging time [34][35][36]. Among all, the soil conditioner aging time is one of the factors that influence the efficacy of phytoremediation and on which much clarity still needs to be given [37].…”