Abstract
Bacterial genes responsible for resistance to antibiotic agents (ARG) are spread from livestock to soil through application of manure, threatening environmental and human health. We investigated the mechanisms of ARG dissemination and persistence to disentangle i) the influence of nutrients and microorganisms on the soil tetracycline (TET) resistome, and ii) the role of indigenous soil microbiota in preventing ARG spread. We analysed short-term (7 days) and persistent (84 days) effects of manure on the resistome of three antibiotic-free pasture soils. Four microcosm treatments were evaluated: control, mineral nutrient fertilization, and deposition of a layer of fresh manure onto soil or γ-irradiated soil. We quantified five TET-resistance genes, isolated 135 TET-resistant bacteria and sequenced both culturable TET-resistant and whole bacterial communities. Manure amendments, but not nutrient addition, increased the abundance of TET-r genes such as tet(Y). Such changes persisted with time, in contrast with the TET-resistant bacterial composition, which partially recovered after manure amendments. Manured γ-irradiated soils showed significantly lower nutrient content and higher TET-r gene abundance than non-irradiated soils, suggesting that native soil bacteria are essential for the fertilization effect of manure on soil as well as control the dissemination of potentially risky TET-r genes.
Highlights
The increasing prevalence of antibiotic resistance among bacteria is a global clinical problem[1] that has an important ecological dimension
Native soil bacteria seem to play a relevant role in survival and persistence of manure bacteria, as they prevent the establishment of invaders in the soil[11,12,13]
A recent study has shown that the interaction between manure and indigenous soil bacteria might be key in determining the outcome of antibiotic resistance genes (ARG) in soils[12]
Summary
The increasing prevalence of antibiotic resistance among bacteria is a global clinical problem[1] that has an important ecological dimension. The massive and widespread use of antimicrobial agents in humans and animals (e.g. livestock) selects for resistant microorganisms[2] that enter the environment and the food chain Organic wastes such as municipal sewage sludge and animal manure, containing high levels of antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARG), are commonly used for agricultural fertilization. As the survival of TET-r gene hosts in the environment can be limited, it has been suggested that horizontal gene transfer into native soil bacteria could be involved in the long-term persistence of TET-r genes in soil[2,16,23,24]. We comparatively assessed the effects of manure, soil abiotic properties, and soil microbiome on the outcoming TET resistome and soil nutrient status in pasture soils receiving fresh cattle manure
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