From gut to mud: dissemination of antimicrobial resistance between animal and agricultural niches

Abstract

With increasing reports on antimicrobial resistance (AMR) in humans, animals and the environment, we are at risk of returning to a pre-antibiotic era. Therefore, AMR is recognized as one of the major global health threats of this century. Antibiotics are used extensively in farming systems to treat and prevent infections in food animals or to increase their growth. Besides the risk of a transfer of AMR between the human and the animal sector, there is another yet largely overlooked sector in the One Health triad. Human-dominated ecosystems such as agricultural soils are a major sink for antibiotics and AMR originating from livestock farming. This review summarizes current knowledge on the prevalence of AMR at the interface of animal and agricultural production and discusses the potential implications for human health. Soil resistomes are augmented by the application of manure from treated livestock. Subsequent transfer of AMR into plant microbiomes may likely play a critical role in human exposure to antibiotic resistance in the environment. Based on the knowledge that is currently available we advocate that more attention should be paid to the role of environmental resistomes in the AMR crisis.

Deterministic Effect of pH on Shaping Soil Resistome Revealed by Metagenomic Analysis

“…Although ARGs developed in clinical and natural environments with different driving forces, the rapid evolution and spread of ARGs in the past decades were undoubtedly related to the utilization and excretion of antibiotics. In particular, antibiotics exert extensive selective pressures on microbes, which promote the amplification, inter/intracellular transfer, and mutation-based generation of ARGs in scenarios such as hospitals, farmlands, and sewage treatment plants . For instance, manure fertilizer and wastewater irrigation were considered to be the main anthropogenic sources of ARGs, while they are often associated with high antibiotic concentrations in agricultural systems. , However, such selective pressures are indeed uncommon for most natural environments in which antibiotic concentrations are generally lower than their estimated (or known) minimum selective concentrations in the laboratory, i.e., at ppb or even lower levels. , Instead, the physicochemical properties of the environmental interfaces and mixing effects of coexisting compounds have more profound impacts on the diversity and abundances of ARGs. − Chen et al recently reported the shaping effects of soil aging on the development of the resistome.…”

“…In particular, antibiotics exert extensive selective pressures on microbes, which promote the amplification, inter/intracellular transfer, and mutation-based generation of ARGs in scenarios such as hospitals, farmlands, and sewage treatment plants. 12 For instance, manure fertilizer and wastewater irrigation were considered to be the main anthropogenic sources of ARGs, while they are often associated with high antibiotic concentrations in agricultural systems. 13,14 However, such selective pressures are indeed uncommon for most natural environments in which antibiotic concentrations are generally lower than their estimated (or known) minimum selective concentrations in the laboratory, i.e., at ppb or even lower levels.…”

Identification of diverse antibiotic resistant bacteria in agricultural soil with H218O stable isotope probing and metagenomics

“…Alternatively, antibiotic resistant bacteria or ARGs could have been introduced to the soil from external sources. This is common in soils exposed to livestock manure or sludge [9,18]. Moreover, the dispersal through unconventional sources such as birds can provide the initial seed for the microbial communities to spread AMR.…”

“…This is essential to achieve climate-change goals and concomitantly meet the dietary demands of 9 billion people by 2050. However, the build-up of antibiotic concentrations and ARG abundance in environmentally sustainable organic fertilisers, such as livestock manure and sewage sludge, permeates agricultural soils to spread AMR by altering the microbiome [1,9,13,18].…”

Deterministic effects of pH on shaping soil resistome revealed by metagenomic analysis

“…Although ARGs developed in clinical and natural environments with different driving forces, the rapid evolution and spread of ARGs in past decades were undoubtedly related to the utilization and excretion of antibiotics. In particular, antibiotics exert extensive selective pressures on microbes, so that signi cant ARG mobilization, horizontal transfer and mutation-based generation occur in scenarios such as hospitals, farmlands and sewage treatment plants (Jadeja and Worrich 2022). However, such selective pressures are indeed uncommon for most natural environments in which antibiotic concentrations were generally lower than their estimated (or known) minimum selective concentrations in the laboratory, i.e.…”