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Advances in antibiotic resistance genes in soil ecosystems

Article 1:Antibiotic resistance in the soil ecosystem: A One Health perspective

Author: Fang Wang*, Yuhao Fu, Hongjie Sheng, Edward Topp, Xin Jiang, Yongguan Zhu, James M. Tiedje

Cite this: Current Opinion in Environmental Science & Health, 20: 100230

Link: https://doi.org/10.1016/j.coesh.2021.100230

Abstract

Rapid emergence of antibiotic resistance genes (ARGs) is a global problem. Soil is a major reservoir of ARGs. The extensive use and/or abuse of antibiotics has increased ARGs proliferation in the soil. The dynamics and transfer of ARGs amongst microorganisms associated with plants and fauna are being investigated. Exogenous coselective agents further exacerbate the problem. Integrated approaches reducing selection pressure and disrupting ARGs transmission routes are essential in the One Health perspective, which appreciates the interconnectivity between humans, animals, and the environment. In particular, we propose that the following are needed: (1) to distinguish clinically relevant ARGs in soil and on soil-grown vegetables from those ARGs that do not confer resistance; (2) to develop a framework for assessing risks associated with the coexistence of ARGs and other contaminants; (3) to understand the extent and conditions for the emergence of ARGs with co-occurring contaminants, and their transfer processes in soil and to water, plants and fauna; and (4) to develop green technologies to mitigate the introduction of ARGs into soil and the transmission of ARGs to humans through the food chain.

 

Article 2: Removal of extracellular antibiotic resistance genes using magnetic biochar/quaternary phosphonium salt in aquatic environments: A mechanistic study

Author: Yuhao Fu, Fang Wang*, Hongjie Sheng, Fang Hu, Ziquan Wang, Min Xu, Yongrong Bian, Xin Jiang, James M. Tiedje

Cite this: Journal of Hazardous Materials, 411: 125048

Link: https://doi.org/10.1016/j.jhazmat.2021.125048

Abstract

The proliferation and spread of antibiotic resistance genes (ARGs) is becoming a worldwide crisis. Extracellular DNA encoding ARGs (eARGs) in aquatic environment plays a critical role in the dispersion of antimicrobial resistance genes. Strategies to control the dissemination of eARGs are urgently required for ecological safety and human health. Towards this goal, magnetic biochar/quaternary phosphonium salt (MBQ), was used to investigate the efficiency and removal mechanism for eARGs. Magnetic biochar modified by quaternary phosphonium salt enhanced the adsorption capacity of extracellular DNA to approximately 9 folds, compared to that of the unmodified. DNA adsorption by MBQ was mainly dominated by chemisorption in heterogeneous systems and was promoted in acidic and low-salt environment. The generation of •OH and MBQ colloid jointly cleaved DNA into fragments, facilitating the adsorption of the phosphate backbone of DNA onto MBQ through electrostatic force as well as the conformational transition of DNA. Furthermore, quantification of extracellular DNA after MBQ was applied in water demonstrated that over 92.7% of resistance genes were removed, indicating a significantly reduced risk of propagation of antimicrobial resistance in aquatic environments. These findings have a practical significance in the application of MBQ in mitigating the spread of ARGs in aquatic environment.

 

Article 3: Does anaerobic soil condition play a more positive role in dissipation of antibiotic resistance genes in soil?

Author: Min Xu, Fang Wang*, Hongjie Sheng, Robert D. Stedtfeld, Zhongpei Li, Syed A. Hashsham, Xin Jiang, James M. Tiedje

Cite this: Science of the Total Environment, 757: 143737

Link: https://doi.org/10.1016/j.scitotenv.2020.143737

Abstract

The persistence of antibiotic resistance genes (ARGs) under the aerobic vs. anaerobic conditions is unknown, especially under different fertilization. Towards this goal, a microcosm experiment was carried out with chemical fertilized and manured soil under aerobic and anaerobic conditions. High throughput qPCR was used to analyze ARGs with 144 primer sets and sequencing for microorganisms. Completely different dynamics of ARGs were observed in soil under aerobic and anaerobic conditions, regardless of the fertilization type. ARGs had different half-lives, even though they confer resistance to the same type of antibiotics. Aminoglycoside, chloramphenicol, macrolide - lincosamide - streptogramin B (MLSB) and tetracycline resistance genes were significantly accumulated in the aerobic soils. Anaerobic soil possessed a higher harboring capacity for exogenous microorganisms and ARGs than aerobic soil. The interaction between ARGs and mobile genetic elements (MGEs) in manured soil under aerobic condition was more pronounced than the anaerobic condition. These findings unveil that anaerobic soil could play a more positive role in reducing potential risk of ARGs in the farmland environment.

 

Article 4: Enhanced antibacterial activity of magnetic biochar conjugated quaternary phosphonium salt

Author: Yuhao Fu, Fang Wang*, Hongjie Sheng, Min Xu, Ying Liang, Yongrong Bian, Syed A. Hashsham, Xin Jiang, James M. Tiedje

Cite this: Carbon, 163: 360-369

Link: https://doi.org/10.1016/j.carbon.2020.03.010

Abstract

Microbial contamination in water remains a global issue in threatening human health. Although current disinfection methods can effectively control microbial contamination, the formation of harmful disinfection byproducts is increasingly questioned. Towards this goal, a facile, green and low-priced bacteriocide - magnetic biochar/quaternary phosphonium salt (MBQ) - was developed using precipitation of iron oxide on biochar followed by ion exchange with quaternary phosphonium salt (QPS). Gram-negative bacteria Escherichia coli and Gram-positive bacteria Staphylococcus aureus - were used as model pathogens to quantify the antibacterial activity and to elucidate the antibacterial mechanism. MBQ was an effective antimicrobial agent against both pathogenic bacteria. The controllable release of QPS and magnetic recovery of MBQ favored antibacterial reuse. Significant disruption of membrane led to the inactivation of bacteria, resulting from the loss of cell membrane integrity and permeability. The induced oxidative damage inhibited the essential cell metabolism. Penetration of MBQ nanoparticles through the cell wall and membrane into the cytoplasm enhanced the biocide effect. Taken together, MBQ, presenting effective, recyclable and long-acting antibacterial properties, has a promising application in bacterial decontamination.

 

Article 5: Antibiotic resistance genes in the human impacted environment: A one health perspective

Author: James M. Tiedje, Fang Wang*, Célia Manaia, Marko Virta, Hongjie Sheng, Liping Ma, Tong Zhang, Edward Topp

Cite this: Pedosphere, 29(3): 273-282

Link: https://doi.org/10.1016/S1002-0160(18)60062-1

Abstract

Antibiotic resistance and its environmental component are gaining more attention as part of combating the growing healthcare crisis. The One Health framework, promulgated by many global health agencies, recognizes that antimicrobial resistance is a truly inter-domain problem in which human health, animal agriculture, and the environment are the core and interrelated components. This prospectus presents the status and issues relevant to the environmental component of antibiotic resistance, namely, the needs for advancing surveillance methodology: the environmental reservoirs and sources of resistance, namely, urban wastewater treatment plants, aquaculture production systems, soil receiving manure and biosolid, and the atmosphere which includes longer range dispersal. Recently, much work has been done describing antibiotic resistance genes in various environments; now quantitative, mechanistic, and hypothesis-driven studies are needed to identify practices that reduce real risks and maintain the effectiveness of our current antibiotics as long as possible. Advanced deployable detection methods for antibiotic resistance in diverse environmental samples are needed in order to provide the surveillance information to identify risks and define barriers that can reduce risks. Also needed are practices that reduce antibiotic use and thereby reduce selection for resistance, as well as practices that limit the dispersal of or destroy antibiotic-resistant bacteria or their resistance genes that are feasible for these varied environmental domains.

 

Article 6: Composting increased persistence of manure-borne antibiotic resistance genes in soils with different fertilization history

Author: Min Xu, Robert D. Stedtfeld, Fang Wang*, Syed A. Hashsham, Yang Song, Yahui Chuang, Jianbo Fan, Hui Li, Xin Jiang, James M. Tiedje

Cite this: Science of the Total Environment, 689, 1172-1180

Link: https://doi.org/10.1016/j.scitotenv.2019.06.376

Abstract

Different long-term fertilization regimes may change indigenous microorganism diversity in the arable soil and thus might influence the persistence and transmission of manure-born antibiotic resistance genes (ARGs). Different manure origins and composting techniques might affect the fate of introduced ARGs in farmland. A four-month microcosm experiment was performed using two soils, which originated from the same field and applied with the same chemical fertilizer or swine manure for 26 years, to investigate the dynamics of ARGs in soil amended with manure or compost from the farm and an agro-technology company. High throughput qPCR and sequencing were applied to quantify ARGs using 144 primer sets and microorganism in soil. Fertilization history had little effect on dynamics of manure-borne ARGs in soil regardless of manure origin or composting. Very different half-lives of ARGs and mobile genetic elements from farm manure and commercial manure were observed in both soils. Composting decreased abundance of most ARGs in manure, but increased the persistence of manure-introduced ARGs in soil irrespective of fertilization history, especially for those from farm manure. These findings help understanding the fate of ARGs in manured soil and may inform techniques to mitigate ARGs transmission.

 

Article 7: Long-term effect of different fertilization and cropping systems on the soil antibiotic resistome

Author: Fang Wang*, Min Xu, Robert D. Stedtfeld, Hongjie Sheng, Jianbo Fan, Ming Liu, Benli Chai, Teotonio Soares de Carvalho, Hui Li, Zhongpei Li, Syed A. Hashsham, James M. Tiedje*

Cite this: Environmental Science & Technology, 52(22): 13037-13046

Link: https://doi.org/10.1021/acs.est.8b04330

Abstract

Different fertilization and cropping systems may influence short- and long-term residues of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) in soil. Soils from dryland (peanut) and paddy (rice) fields, which originated from the same nonagricultural land (forested), were treated with either chemical fertilizer, composted manure, or no fertilizer for 26 years before sampling, which occurred one year after the last applications. ARGs and MGEs were investigated using highly parallel qPCR and high-throughput sequencing. Six of the 11 antibiotics measured by LC–MS/MS were detected in the manure applied soil, but not in the nonmanured soils, indicating their source was from previous manure applications. Compared to the unfertilized control, manure application did not show a large accumulation of ARGs in either cropping system but there were some minor effects of soil management on indigenous ARGs. Paddy soil showed higher accumulation of these ARGs, which corresponded to higher microbial biomass than the dryland soil. Chemical fertilizer increased relative abundance of these ARGs in dryland soil but decreased their relative abundance in paddy soil. These results show how long-term common soil management practices affect the abundance and type of ARGs and MGEs in two very different soil environments, one aerobic and the other primarily anaerobic.

 

Article 8: Influence of soil characteristics and proximity to Antarctic research stations on abundance of antibiotic resistance genes in soils

Author: Fang Wang, Robert D. Stedtfeld1, Ok-Sun Kim, Benli Chai, Luxi Yang, Tiffany M. Stedtfeld, Soon Gyu Hong, Dockyu Kim, Hyoun Soo Lim, Syed A. Hashsham, James M. Tiedje, Woo Jun Sul*

Cite this: Environmental Science & Technology, 50 (23): 12621-12629

Link: https://doi.org/10.1021/acs.est.6b02863

Abstract

Soil is an important environmental reservoir of antibiotic resistance genes (ARGs), which are increasingly recognized as environmental contaminants. Methods to assess the risks associated with the acquisition or transfer of resistance mechanisms are still underdeveloped. Quantification of background levels of antibiotic resistance genes and what alters those is a first step in understanding our environmental resistome. Toward this goal, 62 samples were collected over 3 years from soils near the 30-year old Gondwana Research Station and for 4 years before and during development of the new Jang Bogo Research Station, both at Terra Nova Bay in Antarctica. These sites reflect limited and more extensive human impact, respectively. A qPCR array with 384 primer sets targeting antibiotic resistance genes and mobile genetic elements (MGEs) was used to detect and quantify these genes. A total of 73 ARGs and MGEs encompassing eight major antibiotic resistance gene categories were detected, but most at very low levels. Antarctic soil appeared to be a common reservoir for seven ARGs since they were present in most samples (42%–88%). If the seven widespread genes were removed, there was a correlation between the relative abundance of MGEs and ARGs, more typical of contaminated sites. There was a relationship between ARG content and distance from both research stations, with a significant effect at the Jang Bogo Station especially when excluding the seven widespread genes; however, the relative abundance of ARGs did not increase over the 4 year period. Silt, clay, total organic carbon, and SiO2 were the top edaphic factors that correlated with ARG abundance. Overall, this study identifies that human activity and certain soil characteristics correlate with antibiotic resistance genes in these oligotrophic Antarctic soils and provides a baseline of ARGs and MGEs for future comparisons.