Long-Term Nickel Contamination Increases the Occurrence of Antibiotic Resistance Genes in Agricultural Soils

Abstract

Heavy metal contamination is assumed to be a selection pressure on antibiotic resistance, but to our knowledge, evidence of the heavy metal-induced changes of antibiotic resistance is lacking on a long-term basis. Using quantitative PCR array and Illumina sequencing, we investigated the changes of a wide spectrum of soil antibiotic resistance genes (ARGs) following 4-5 year nickel exposure (0-800 mg kg) in two long-term experimental sites. A total of 149 unique ARGs were detected, with multidrug and β-lactam resistance as the most prevailing ARG types. The frequencies and abundance of ARGs tended to increase along the gradient of increasing nickel concentrations, with the highest values recorded in the treatments amended with 400 mg nickel kg soil. The abundance of mobile genetic elements (MGEs) was significantly associated with ARGs, suggesting that nickel exposure might enhance the potential for horizontal transfer of ARGs. Network analysis demonstrated significant associations between ARGs and MGEs, with the integrase intI1 gene having the most frequent interactions with other co-occurring ARGs. The changes of ARGs were mainly driven by nickel bioavailability and MGEs as revealed by structural equation models. Taken together, long-term nickel exposure significantly increased the diversity, abundance, and horizontal transfer potential of soil ARGs.

Diversity of herbaceous plants and bacterial communities regulates soil resistome across forest biomes

“…Our findings contribute to the growing body of evidence that ARGs are widespread in relatively pristine habitats with less contact with commercial sources of antibiotics (Chen et al ., ; Segawa et al ., ; Pawlowski et al ., ), and highlight that the natural forest ecosystem is a significant reservoir of ARGs and needs to be considered in the risk assessment frameworks of antibiotic resistance. Comparison of the background ARG profiles between the forest ecosystems and some human‐impacted soils by using the same HT‐qPCR array suggested that the diversity and relative abundance of ARGs in copper‐contaminated soils (Hu et al ., ), nickel‐contaminated soils (Hu et al ., ), animal manure‐amended soils (Zhang et al ., ) and antibiotics‐treated soils (Zhang et al ., ) are significantly higher than those in forest biomes (Supporting Information Fig. S10).…”

“…and Supporting Information Table S5), suggestive of a low rate of HGT in forests. However, ARGs are not linked to the phylogenetic composition in animal agriculture (Johnson et al ., ) and heavy metal‐contaminated soils (Hu et al ., ), indicating that genetic potential for HGT might be enhanced when natural soils are subjected to anthropogenic activities.…”

“…Soil is one of the largest environmental reservoir comprising approximately 30% of known ARGs in public repositories (Forsberg et al ., ; Nesme et al ., ), and is one of the most complex ecosystems in terms of ecological niches and biodiversity (Nesme and Simonet, ). To date, a large body of studies have documented the prevalence of ARGs in environments under anthropogenic perturbations, such as soils with manure amendments (Zhu et al ., ; Zhang et al ., ), contaminated with pharmaceutical residues (Zhu et al ., ) or heavy metals (Hu et al ., ) and irrigated with reclaimed water (Wang et al ., ; Han et al ., ). We have, however, limited knowledge of the background levels of antibiotic resistance and the distribution of ARGs in natural settings with little or no human disturbance.…”

“…S10. Comparison of the diversity and relative abundance of ARGs in the forest ecosystems in this study and some human‐impacted soils including 85 copper‐contaminated soils (Hu et al ., 2016), 85 nickel‐contaminated soils (Hu et al ., ), 30 animal manure‐amended soils (Zhang et al ., ) and 50 antibiotics‐treated soils (Zhang et al ., ) by using the same HT‐qPCR array. Fig.…”

Co‐selection for antibiotic resistance genes is induced in a soil amended with zinc

“…Unlike most easily biodegradable antibiotics, heavy metals in soil cannot be degraded, but can only be transformed into different forms; the fate and behaviour of heavy metals strongly depends on soil conditions because these influence their form and bioavailability. There are known links between heavy metals and antibiotic resistance maintenance and spread in multiple environments, including freshwater microcosms (Ramunas et al., ), activated sludge bioreactor (Peltier, Vincent, Finn, & Graham, ), soils amended with Cu (Hu, Wang, Li, Li, et al., ) and soil amended with nickel (Ni) (Hu, Wang, Li, Shi, et al., ). Thus, it is possible that opportunities for co‐selection are widespread across soils, resistant bacteria and different heavy metals.…”