Changes in tetracycline partitioning and bacteria/phage-comediated ARGs in microplastic-contaminated greenhouse soil facilitated by sophorolipid. - Related Documents




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692201.0000Changes in tetracycline partitioning and bacteria/phage-comediated ARGs in microplastic-contaminated greenhouse soil facilitated by sophorolipid. The emerging mixed contamination of antibiotics and microplastics in greenhouse soil has made the control of antibiotic resistant gene (ARG) transmission a novel challenge. In this work, surfactant sophorolipid was applied to enhance the dissipation of tetracycline (TC) and tet genes in the presence of microplastics in greenhouse soil. During 49days of incubation, soil bacteria and phages were both found to be the crucial reservoirs of ARGs. Meanwhile, microplastic's presence significantly inhibited the dissipation of TC and ARGs in the soil. However, sophorolipid application was proved to outweigh the negative impact caused by microplastic existence, and lead to the highest dissipation of soil TC and ARGs. Significant positive correlation was detected between the dissipation rate of water-soluble and exchangeable TC content and bacteria/phage co-mediated ARG levels. This also held true between the two fractions of soil TC and the ratio of ARG level in the bacteria to that in the phages (B(ARGs)/P(ARGs)). The opposite impacts of microplastic presence and sophorolipid amendment on the TC/ARG dissipation found in this work provides new information for understanding ARG transmission between bacteria and phages in the mixed contaminated greenhouse soil.201829175125
703910.9998Profiles and key drivers of bacteria/phage co-mediated antibiotic resistance genes during swine manure composting amended with humic acid. Phages can promote the spread of antibiotic resistance genes (ARGs) in agricultural environments through transduction. However, studies on phage-mediated ARG profiles during composting have not been performed. This study investigated the effects of adding humic acid (HA) on the abundances of bacteria/phage co-mediated ARGs (b/pARGs) during swine manure composting and the key factors that affected the transmission of b/pARGs. The results showed that the addition of 5 % HA during composting could effectively reduce the absolute abundances of b/pARGs, inhibit the proliferation of pathogenic microorganisms (e.g., Corynebacterium and Streptococcus) that carried ARGs, and ultimately affect the fate of b/pARGs in the composting process by regulating key environmental factors to change the abundance of co-host bacteria. Overall, the findings of this study provided new information for understanding the main driving factors affecting the b/pARGs profile and provided a reference for the prevention and control of ARGs pollution during composting.202336774987
704020.9998The maturity period is the main stage of antibiotic resistance genes reduction in aerobic composting process of swine manure in sub-scale farms. This study was focused on the changes of antibiotic resistance genes (ARGs) and their potential host bacteria during the swine manure composting on sub-scale farms. Eight target ARGs increased 427% on average, with a trend of increase at early stage and decrease at later stage, and the main reduction stage appeared in maturity stage. The abundance of ARGs was mainly affected by the community succession of potential host bacteria. Composting could reduce the abundance of potential host bacteria of ARGs as well as pathogens such as Pseudomonas, and reduce the environmental risks of swine manure. N/C and S levels had a positive effect on the potential host of most ARGs. Prolonging the maturity period would inhibit the growth of potential host bacteria of ARGs during composting, therefore inhibiting the transmission of ARGs.202132971337
704230.9997Response of antibiotic resistance genes abundance by graphene oxide during the anaerobic digestion of swine manure with copper pollution. The pollution of various environments with antibiotic resistance genes (ARGs) is an urgent problem that needs to be addressed, especially in heavy metal-polluted environments. This study investigated the responses of ARGs and mobile genetic elements (MGEs) to the addition of graphene oxide (GO) to swine manure containing a high concentration copper during anaerobic digestion. The total copy numbers of ARGs and MGEs were significantly enhanced by the pressure due to Cu. GO significantly decreased the ARG and MGE copy numbers, where the low GO concentration performed better than the high GO concentration. Network analysis showed that most of the ARGs and MGEs co-occurred and they shared the same major potential host bacteria. The contributions of different factors to ARG abundances were assessed by redundancy analysis and MGEs had the most important effect on the fate of ARGs. Thus, GO may reduce the abundance of ARGs mainly by removing MGEs.201930445329
807640.9997Effects of chlortetracycline and copper on tetracyclines and copper resistance genes and microbial community during swine manure anaerobic digestion. As antibiotic and heavy metals are over used in the livestock industry, animal manure is a reservoir of antibiotic resistance genes (ARGs). Anaerobic digestion has been reported to have the potential to reduce ARGs. However, few studies investigated whether reduction of ARGs would be affected by different external pressures including antibiotics and heavy metals during anaerobic digestion. The purpose of this study was thus to investigate effects of both chlortetracycline (CTC) and Cu on reduction of ARGs, heavy metal resistance genes (HMRGs) and mobile genetic elements (MGEs) during the swine manure anaerobic digestion. The results showed that the predominant ARGs (tetO, tetW, tetX, tetL) could be effectively reduced (approximately 1.00 log copies/g TS) through mesophilic anaerobic digestion. Microbial community evolution was the main driver. It was interesting that Treponema might indicate the termination of anaerobic digestion and compete with ARGs host bacteria. Addition of CTC, Cu and CTC+Cu affected microbial community change and hindered removal of ARGs, especially, CTC+Cu seriously affected Treponema and ARGs during anaerobic digestion.201728432950
704150.9997Antibiotic and heavy metal resistance genes in sewage sludge survive during aerobic composting. Municipal sewage sludge has been generated in increasing amounts with the acceleration of urbanization and economic development. The nutrient rich sewage sludge can be recycled by composting that has a great potential to produce stabilized organic fertilizer and substrate for plant cultivation. However, little is known about the metals, pathogens and antibiotic resistance transfer risks involved in applying the composted sludge in agriculture. We studied changes in and relationships between heavy metal contents, microbial communities, and antibiotic resistance genes (ARGs), heavy metal resistance genes (HMRGs) and mobile genetic elements (MGEs) in aerobic composting of sewage sludge. The contents of most of the analyzed heavy metals were not lower after composting. The bacterial α-diversity was lower, and the community composition was different after composting. Firmicutes were enriched, and Proteobacteria and potential pathogens in the genera Arcobacter and Acinetobacter were depleted in the composted sludge. The differences in bacteria were possibly due to the high temperature phase during the composting which was likely to affect temperature-sensitive bacteria. The number of detected ARGs, HMRGs and MGEs was lower, and the relative abundances of several resistance genes were lower after composting. However, the abundance of seven ARGs and six HMRGs remained on the same level after composting. Co-occurrence analysis of bacterial taxa and the genes suggested that the ARGs may spread via horizontal gene transfer during composting. In summary, even though aerobic composting is effective for managing sewage sludge and to decrease the relative abundance of potential pathogens, ARGs and HMRGs, it might include a potential risk for the dissemination of ARGs in the environment.202336608829
702560.9997Aerobic composting as an effective cow manure management strategy for reducing the dissemination of antibiotic resistance genes: An integrated meta-omics study. Livestock manure is considered as an important source for spreading antibiotic resistance genes (ARGs) into the environment, and therefore poses a direct threat to public health. Whereas the effects of reused manure on soil microbial communities and ARGs have been studied extensively, comprehensive characterizations of microbial communities and ARGs of manure produced by different management methods are not well understood. Here, we analyzed the fate of microbial communities and ARGs of cow manure treated by three conventional management strategies: aerobic composting, mechanical drying and precipitation, applying an integrated-omics approach combining metagenomics and metaproteomics. Integrated-omics demonstrated that composted manure contained the lowest diversity of microbial community and ARGs compared with manure treated by other two strategies. Quantitative PCR methods revealed that the abundances of ARGs were reduced by over 83 % after composting for 14 days, regardless of the season. Besides, the potential ARG hosts Acinetobacter and Pseudomonas dominating mechanical drying process were sharply decreased in abundances after composting. The significant co-occurrence networks among bacteria, ARGs and transposase gene tnpA-01 in composting samples indicated the important role of these bacteria in the dissemination of ARGs. These findings offer insight into potential strategies to control the spread of ARGs during livestock manure reuse.202031884359
807770.9997Effects of coexistence of tetracycline, copper and microplastics on the fate of antibiotic resistance genes in manured soil. The coexistence of antibiotics, heavy metals and microplastics is becoming commonplace and may affect antibiotic resistance in manured soil. The current understanding of the role of microplastics in soil with combined pollution of antibiotics, heavy metals and antibiotic resistance genes (ARGs) is limited. Here, the effects of the coexistence of tetracycline (TC), Cu and environmental microplastics (EM) on the fate of nine ARGs and three heavy metal resistance genes in agricultural soil were investigated by batch and microcosm experiments. EM were obtained by exposing virgin microplastics to soil environments for 80 days, which exhibited higher adsorption affinity for Cu and TC than soil particles and virgin microplastics. 1% EM in soil increased bioavailable concentrations of TC and Cu by 79-138% and 88-135%, respectively, and decreased TC dissipation from 11.79 mg kg(-1) to 3.08 mg kg(-1). Correspondingly, the total relative abundances of target ARGs increased by 219-348%. The significant correlations of tetG, tetB, tetQ, sul2, sul1 and intl1 with bioavailable fractions of TC and Cu in soil environments were revealed by network analysis. Moreover, scanning electron micrographs showed the special plastisphere around EM. Attributed to the biofilm generation and higher pollutant accumulation in the plastisphere, EM could be the source of antibiotic-resistant bacteria and ARGs in soil environments. Structure equation models further identified that indirect effects of EM acted a major role in the propagation of ARGs by altering soil properties, soil microbial diversity and intl1 abundance. This study revealed that EM could increase the stimulative effects of Cu and TC on antibiotic resistance and magnify the environmental risk of manure application in soil environments.202134091329
695580.9997Soil antibiotic resistance genes accumulate at different rates over four decades of manure application. Manure can be a source of antibiotic resistance genes (ARGs) that enter the soil. However, previous studies assessing ARG persistence in soil have generally lacked continuity over sampling times, consistency of location, and assessing the impact of discontinuing manure application. We evaluated both short- and long-term ARG accumulation dynamics in soil with a 40-year known history of manure use. Manure application caused a greater abundance of tetracycline, macrolide, and sulfonamide ARGs in the soil. There was an initial spike in ARG abundance resulting from manure bacteria harboring ARGs being introduced to soil, followed by resident soil bacteria out-competing them, which led to ARG dissipation within a year. However, over four decades, annual manure application caused linear or exponential ARG accumulation, and bacteria associated with ARGs differed compared to those in the short term. Eleven years after discontinuing manure application, most soil ARG levels declined but remained elevated. We systematically explored the historical accumulation of ARGs in manured soil, and provide insight into factors that affect their persistence.202336444046
808390.9997Alteration of the migration trajectory of antibiotic resistance genes by microplastics in a leachate activated sludge system. The environmental behavior of emerging contaminants of microplastics (MPs), antibiotics and antibiotic resistance genes (ARGs) in the leachate activated sludge system has been monitored and analyzed comprehensively. The results suggested that MPs could effectively alter the migration trajectory of tetracycline resistance genes (tet genes) in the leachate activated sludge system under intermittent and continuous influent conditions. After adding MPs, the total average abundance of tet genes in leachate increased from 0.74 ± 0.07 to 0.78 ± 0.07 (log(10)tet genes/log(10) 16S rRNA) and that in sludge increased from 0.65 ± 0.08 to 0.70 ± 0.06 (log(10)tet genes/log(10) 16S rRNA). Except for tetA, the abundance of tetB, tetO, tetM and tetQ on MPs increased with increasing TC concentration under both aerobic and anaerobic conditions. MPs not only significantly affect the abundance level and migration trajectory of ARGs in the leachate activated sludge system, but also remarkably improve the level of heavy metals in the ambient environment, indirectly promoting the selective effect of antibiotic-resistant bacteria (ARB) and promoting the development of antibiotic resistance (AR). In addition, MPs changed their physicochemical properties and released hazardous substances with aging to force tet genes to migrate from the leachate activated sludge system to the MPs, making AR more difficult to eliminate and persisted in wastewater treatment plants. Meanwhile, microorganisms played a driving role, making MPs serve as a niche for ARGs and ARB colonization. The co-occurrence network analysis indicated the specific distribution pattern of tet genes and microorganisms in different media, and the potential host was speculated. This study improves the understanding of the environmental behavior of emerging contaminants in leachate activated sludge system and lays a theoretical for protecting the ecological environment.202337321316
7548100.9997Maturity phase is crucial for removing antibiotic resistance genes during composting: novel insights into dissolved organic matter-microbial symbiosis system. Composting is widely regarded as an effective method for reducing antibiotic resistance genes (ARGs) in livestock and poultry manure. However, the critical mechanisms of ARGs in different composting phase are still unclear. In this study, normal composting and two types of rapid composting (without mature phase) were used to analyze the removal of ARGs and the succession of dissolved organic matter (DOM). Compared to normal composting, rapid composting reactivated tetracyclines, sulfonamide, and quinolones resistance genes during the maturation phase and reduced the total ARGs removal rates by 45.58 %-57.87 %. Humus-like components could inhibit the proliferation of ARGs, and the enrichment of protein-like components increased abundances of Pusillimonas, Persicitalea, and Pseudomonas, indirectly reducing the removal. This study is the first to demonstrate the contribution of DOM and microbial community to ARGs removal, emphasizing the importance of the maturation phase for ARGs elimination. This research provides guidance for producing safe compost products.202540311709
6999110.9997Different impacts of manure and chemical fertilizers on bacterial community structure and antibiotic resistance genes in arable soils. Both manure and chemical fertilizers are widely used in modern agriculture. However, the impacts of different fertilizers on bacterial community structure and antibiotic resistance genes (ARGs) in arable soils still remain unclear. In this study, high-throughput sequencing and quantitative PCR were employed to investigate the bacterial community structure, ARGs and mobile genetic elements (MGEs) influenced by the application of different fertilizers, including chemical fertilizers, piggery manure and straw ash. The results showed that the application of fertilizers could significantly change the soil bacterial community and the abundance of Gaiella under phylum Actinobacteria was significantly reduced from 12.9% in unfertilized soil to 4.1%-7.4% in fertilized soil (P < 0.05). It was also found that the application of manure could cause a transient effect on soil resistome composition and the relative abundance of ARGs increased from 7.37 ppm to 32.10 ppm. The abundance of aminoglycoside, sulfonamide and tetracycline resistance genes greatly increased after manure fertilization and then gradually returned to normal levels with the decay of some intestinal bacteria carrying ARGs. In contrast, the application of chemical fertilizers and straw ash significantly changed the bacterial community structure but exerted little effect on soil resistome. Overall, the results of this study illustrated the different effects of different fertilizers on the soil resistome and revealed that the changes of soil resistome induced by manure application mainly resulted from alteration of bacteria community rather than the horizontal gene transfer.201728898777
8578120.9997Impact of earthworms on suppressing dissemination of antibiotic resistance genes during vermicomposting treatment of excess sludge. Earthworms play a crucial role in suppressing the dissemination of antibiotic resistance genes (ARGs) during vermicomposting. However, there is still a lack of how earthworms influence the spread of ARGs. To address this gap, a microcosm experiment was conducted, incorporating earthworms and utilizing metagenomics and quantitative PCR to assess the impact of earthworms on microbial interactions and the removal of plasmid-induced ARGs. The findings revealed that vermicomposting led to a reduction in the relative abundance of ARGs by altering microbial communities and interactions. Significantly, vermicomposting demonstrated an impressive capability, reducing 92% of ARGs donor bacteria and impeding the transmission of 94% of the RP4 plasmid. Furthermore, through structural equation model analysis, it was determined that mobile genetic elements and environmental variables were the primary influencers of ARG reduction. Overall, this study offers a fresh perspective on the effects of vermicomposting and its potential to mitigate the spread of ARGs.202438885722
7931130.9997The stress response of tetracycline resistance genes and bacterial communities under the existence of microplastics in typical leachate biological treatment system. Landfill leachate is an important source of microplastics (MPs) and antibiotic-resistance genes (ARGs). Here, in the presence of polystyrene MPs (PS-MPs) and polyethylene MPs (PE-MPs), the nitrogen and phosphorus removal effect and sludge structure performance were affected in an anaerobic-anoxic-aerobic system, a typical biological leachate treatment process. The abundance of tetracycline-resistance genes (tet genes) in biofilms on the two types of MP was significantly higher than that in the leachate and sludge, and the load on PE-MPs was higher than that on PS-MPs because of the porous structure of PE-MPs. Aging of the MPs increased their surface roughness and abundance of oxygen-containing functional groups and shaped the profile of ARGs in the MP biofilms. The biofilm biomass and growth rate on the two types of MP increased with the incubation time in the first 30 days, and was affected by environmental factors. Structural equation models and co-occurrence network analysis demonstrated that the MPs indirectly affected the spectrum of ARGs by affecting biofilm formation, and, to a lesser extent, had a direct impact on the selective enrichment of ARGs. We discuss the mechanisms of the relationships between MPs and ARGs in the leachate treatment system, which will have guiding significance for future research. Our data on the colonization of microorganisms and tet genes in MPs biofilms provide new evidence concerning the accumulation and transmission of these ARGs, and are important for understanding the mechanisms of MPs in spreading pollution.202439018858
7033140.9997Environmental drivers and interaction mechanisms of heavy metal and antibiotic resistome exposed to amoxicillin during aerobic composting. The environmental accumulation and spread of antibiotic resistance pose a major threat to global health. Aerobic composting has become an important hotspot of combined pollution [e.g., antibiotic resistance genes (ARGs) and heavy metals (HMs)] in the process of centralized treatment and resource utilization of manure. However, the interaction mechanisms and environmental drivers of HMs resistome (MRGs), antibiotic resistance (genotype and phenotype), and microbiome during aerobic composting under the widely used amoxicillin (AMX) selection pressure are still poorly understood. Here, we investigated the dynamics of HMs bioavailability and their MRGs, AMX-resistant bacteria (ARB) and antibiotic resistome (ARGs and intI1), and bacterial community to decipher the impact mechanism of AMX by conducting aerobic composting experiments. We detected higher exchangeable HMs and MRGs in the AMX group than the control group, especially for the czrC gene, indicating that AMX exposure may inhibit HMs passivation and promote some MRGs. The presence of AMX significantly altered bacterial community composition and AMX-resistant and -sensitive bacterial structures, elevating antibiotic resistome and its potential transmission risks, in which the proportions of ARB and intI1 were greatly increased to 148- and 11.6-fold compared to the control group. Proteobacteria and Actinobacteria were significant biomarkers of AMX exposure and may be critical in promoting bacterial resistance development. S0134_terrestrial_group was significantly negatively correlated with bla(TEM) and czrC genes, which might play a role in the elimination of some ARGs and MRGs. Except for the basic physicochemical (MC, C/N, and pH) and nutritional indicators (NO(3) (-)-N, NH(4) (+)-N), Bio-Cu may be an important environmental driver regulating bacterial resistance during composting. These findings suggested the importance of the interaction mechanism of combined pollution and its synergistic treatment during aerobic composting need to be emphasized.202236687604
8576150.9997Biochar can mitigate co-selection and control antibiotic resistant genes (ARGs) in compost and soil. Heavy metals (HMs) contamination raises the expression of antibiotic resistance (AR) in bacteria through co-selection. Biochar application in composting improves the effectiveness of composting and the quality of compost. This improvement includes the elimination and reduction of antibiotic resistant genes (ARGs). The use of biochar in contaminated soils reduces the bioaccessibility and bioavailability of the contaminants hence reducing the biological and environmental toxicity. This decrease in contaminant bioavailability reduces contaminants induced co-selection pressure. Conditions which favour reduction in HMs bioavailable fraction (BF) appear to favour reduction in ARGs in compost and soil. Biochar can prevent horizontal gene transfer (HGT) and can eliminate ARGs carried by mobile genetic elements (MGEs). This effect reduces maintenance and propagation of ARGs. Firmicutes, Proteobacteria, and Actinobacteria are the major bacteria phyla identified to be responsible for dissipation, maintenance, and propagation of ARGs. Biochar application rate at 2-10% is the best for the elimination of ARGs. This review provides insight into the usefulness of biochar in the prevention of co-selection and reduction of AR, including challenges of biochar application and future research prospects.202235663734
6916160.9997Mobile genetic elements in potential host microorganisms are the key hindrance for the removal of antibiotic resistance genes in industrial-scale composting with municipal solid waste. During the municipal solid waste (MSW) composting, antibiotic resistance genes (ARGs) could be one of the concerns to hinder the application of MSW composting. However, the understanding of enrichment and dissemination of ARGs during the industrial-scale composting is still not clear. Hence, this study aimed to investigate the ARG distributions at different stages in an industrial-scale MSW composting plant. Seven target ARGs and four target mobile genetic elements (MGEs) and bacterial communities were investigated. The abundances of ARGs and MGEs increased during two aerobic thermophilic stages, but they decreased in most ARGs and MGEs after composting. Network analysis showed that potential host bacteria of ARGs were mainly Firmicutes and Actinobacteria. The reduction of potential host bacteria was important to remove ARGs. MGEs were an important factor hindering ARG removal. Water-extractable S and pH were two main physicochemical factors in the changes of microbial community and the abundance of ARGs.202031962245
6927170.9997Manure application: A trigger for vertical accumulation of antibiotic resistance genes in cropland soils. The application of livestock manure increases the dissemination risk of antibiotic resistance genes (ARGs) in farmland soil environment. However, the vertical migration behavior and driving factor of ARGs in manured soil under swine manure application remains undefined. Here, the dynamics of ARGs, mobile genetic elements (MGEs) and bacterial communities in different soil depths (0 - 80 cm) with long-term swine manure application were tracked and conducted using real-time qPCR. Results showed that long-term application of swine manure remarkably facilitated the vertical accumulation of ARGs and MGEs, in particular that the relative abundance of bla(ampC) showed significant enrichment with increasing depth. ARGs abundance was similar in the three fields with long-term application of swine manure. (p＞0.05). Procrustes analysis indicated that microbial communities were the dominant drivers of ARGs variation in topsoil, and the changes of environmental factors played a vital role in vertical migration ARGs in cropland soils. Additionally, the variation patterns of high-risk ARGs (i.e., bla(ampC), bla(TEM-1)) were influenced by the dominant bacteria (Actinomycetes) and pH. This study illustrated that the swine manure application promoted the vertical migration of ARGs, including multidrug resistance determinants, highlighting the ecological risk caused by long-term manure application.202235483148
7507180.9997Impact of different organic matters on the occurrence of antibiotic resistance genes in activated sludge. The occurrence of antibiotic resistance genes (ARGs) in various environments has drawn worldwide attention due to their potential risks. Previous studies have reported that a variety of substances can enhance the occurrence and dissemination of ARGs. However, few studies have compared the response of ARGs under the stress of different organic matters in biological wastewater treatment systems. In this study, seven organic pollutants were added into wastewater treatment bioreactors to investigate their impacts on the ARG occurrence in activated sludge. Based on high-throughput sequencing, it was found that the microbial communities and ARG patterns were significantly changed in the activated sludge exposed to these organic pollutants. Compared with the non-antibiotic refractory organic matters, antibiotics not only increased the abundance of ARGs but also significantly changed the ARG compositions. The increase of Gram-negative bacteria (e.g., Archangium, Prosthecobacter and Dokdonella) carrying ARGs could be the main cause of ARG proliferation. In addition, significant co-occurrence relationships between ARGs and mobile genetic elements were also observed in the sludge samples, which may also affect the ARG diversity and abundance during the organic matter treatment in the bioreactors. Overall, these findings provide new information for better understanding the ARG occurrence and dissemination caused by organic pollutants in wastewater treatment systems.202336522059
6953190.9997Long-term biogas slurry application increased antibiotics accumulation and antibiotic resistance genes (ARGs) spread in agricultural soils with different properties. Animal manures are commonly applied to soil which possibly promote the spread of antibiotic resistance from soil to human beings via food chains. Biogas slurry is an end product of anaerobic digestion of animal manures, which has been widely applied as fertilizers in the agricultural soil. However, effect of long-term biogas slurry application on the soil antibiotic resistance and the associated mechanism still remains unclear. The present study characterized antibiotics, antibiotic resistance genes (ARGs), mobile genetic elements (MGEs) and bacterial community, in different agricultural soils unamended (BS-) and amended (BS+) with biogas slurry (8-18 years) in five field experiments. Our results indicated that long-term application of biogas slurry largely increased the concentrations of tetracyclines in soils, and greatly increased the abundances of ARGs, transposase gene (Tn916/1545) and ARGs-associated bacteria. Long-term application of biogas slurry led to tetracyclines accumulation and ARGs enrichment in agricultural soil, and the selection pressure from tetracyclines and the increase of Tn916/1545 abundace become potential contributors for the increase of soil antibiotic resistance via promoting the enrichment of ARG-associated bacteria. The results of the present study should be taken into consideration to develop policy and practice for mitigating the enrichment and spread of antibiotic resistance during the recycling of biogas slurry into agricultural soil.202133203566