School of Agriculture, Food and Ecosystem Sciences - Research Publications

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    Aerobic composting reduces antibiotic resistance genes in cattle manure and the resistome dissemination in agricultural soils
    Gou, M ; Hu, H-W ; Zhang, Y-J ; Wang, J-T ; Hayden, H ; Tang, Y-Q ; He, J-Z (ELSEVIER, 2018-01-15)
    Composting has been suggested as a potential strategy to eliminate antibiotic residues and pathogens in livestock manure before its application as an organic fertilizer in agro-ecosystems. However, the impacts of composting on antibiotic resistance genes (ARGs) in livestock manure and their temporal succession following the application of compost to land are not well understood. We examined how aerobic composting affected the resistome profiles of cattle manure, and by constructing laboratory microcosms we compared the effects of manure and compost application to agricultural soils on the temporal succession of a wide spectrum of ARGs. The high-throughput quantitative PCR array detected a total of 144 ARGs across all the soil, manure and compost samples, with Macrolide-Lincosamide-Streptogramin B, aminoglycoside, multidrug, tetracycline, and β-lactam resistance as the most dominant types. Composting significantly reduced the diversity and relative abundance of ARGs and mobile genetic elements (MGEs) in the cattle manure. In the 120-day microcosm incubation, the diversity and abundance of ARGs in manure-treated soils were significantly higher than those in compost-treated soils at the beginning of the experiment. The level of antibiotic resistance rapidly declined over time in all manure- and compost-treated soils, coupled with similar temporal patterns of manure- and compost-derived bacterial communities as revealed by SourceTracker analysis. The network analysis revealed more intensive interactions/associations among ARGs and MGEs in manure-treated soils than in compost-treated soils, suggesting that mobility potential of ARGs was lower in soils amended with compost. Our results provide evidence that aerobic composting of cattle manure may be an effective approach to mitigate the risk of antibiotic resistance propagation associated with land application of organic wastes.
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    Salinity as a predominant factor modulating the distribution patterns of antibiotic resistance genes in ocean and river beach soils
    Zhang, Y-J ; Hu, H-W ; Yan, H ; Wang, J-T ; Lam, SK ; Chen, Q-L ; Chen, D ; He, J-Z (Elsevier, 2019-06-10)
    Growing evidence points to the pivotal role of the environmental factors in influencing the transmission of antibiotic resistance genes (ARGs) and the propagation of resistant human pathogens. However, our understanding of the ecological and evolutionary environmental factors that contribute to development and dissemination of antibiotic resistance is lacking. Here, we profiled a wide variety of ARGs using the high-throughput quantitative PCR analysis in 61 soil samples collected from ocean and river beaches, which are hotspots for human activities and platforms for potential transmission of environmental ARGs to human pathogens. We identified the dominant abiotic and biotic factors influencing the diversity, abundance and composition of ARGs in these ecosystems. A total of 110 ARGs conferring resistance to eight major categories of antibiotics were detected. The core resistome was mainly affiliated into β-lactam and multidrug resistance, accounting for 66.9% of the total abundance of ARGs. The oprJ gene conferring resistance to multidrug was the most widespread ARG subtype detected in all the samples. The relative abundances of total ARGs and core resistome were significantly correlated with salinity-related properties including electrical conductivity and concentrations of sodium and chloride. Random forest analysis and structural equation modelling revealed that salinity was the most important factor modulating the distribution patterns of beach soil ARGs after accounting for multiple drivers. These findings suggest that beach soil is a rich reservoir of ARGs and that salinity is a predominant factor shaping the distribution patterns of soil resistome.
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    Antibiotic resistance in urban green spaces mirrors the pattern of industrial distribution
    Yan, Z-Z ; Chen, Q-L ; Zhang, Y-J ; He, J-Z ; Hu, H-W (Elsevier Ltd, 2019-11-01)
    Urban green spaces are closely related to the activities and health of urban residents. Turf grass and soil are two major interfaces between the environmental and human microbiome, which represent potential pathways for the spread of antibiotic resistance genes (ARGs) from environmental to human microbiome through skin-surface contact. However, the information regarding the prevalence of ARGs in urban green spaces and drivers in shaping their distribution patterns remain unclear. Here, we profiled a wide spectrum of ARGs in grass phyllosphere and soils from 40 urban parks across Greater Melbourne, Australia, using high throughput quantitative PCR. A total of 217 and 218 unique ARGs and MGEs were detected in grass phyllosphere and soils, respectively, conferring resistance to almost all major classes of antibiotics commonly used in human and animals. The plant microbiome contained a core resistome, which occupied >84% of the total abundance of ARGs. In contrast, no core resistome was identified in the soil microbiome. The difference between plant and soil resistome composition was attributed to the difference in bacterial community structure and intensity of environmental and anthropogenic influence. Most importantly, the abundance of ARGs in urban green spaces was significantly positively related to industrial factors including total number of business, number of manufacturing, and number of electricity, gas, water and waste services in the region. Structural equation models further revealed that industrial distribution was a major factor shaping the ARG profiles in urban green spaces after accounting for multiple drivers. These findings have important implications for mitigation of the potential risks posed by ARGs to urban residents.
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    Transfer of antibiotic resistance from manure-amended soils to vegetable microbiomes
    Zhang, Y-J ; Hu, H-W ; Chen, Q-L ; Singh, BK ; Yan, H ; Chen, D ; He, J-Z (PERGAMON-ELSEVIER SCIENCE LTD, 2019-09)
    The increasing antimicrobial resistance in manure-amended soil can potentially enter food chain, representing an important vehicle for antibiotic resistance genes (ARGs) transmission into human microbiome. However, the pathways for transmission of ARGs from soil to plant remain unclear. Here, we explored the impacts of poultry and cattle manure application on the patterns of resistome in soil and lettuce microbiome including rhizosphere, root endosphere, leaf endosphere and phyllosphere, to identify the potential transmission routes of ARGs in the soil-plant system. After 90 days of cultivation, a total of 144 ARGs were detected in all samples using high-throughput quantitative PCR. Rhizosphere soil samples harbored the most diverse ARGs compared with other components of lettuce. Cattle manure application increased the abundance of ARGs in root endophyte, while poultry manure application increased ARGs in rhizosphere, root endophyte and phyllosphere, suggesting that poultry manure may have a stronger impact on lettuce resistomes. The ARG profiles were significantly correlated with the bacterial community, and the enrichment of soil and plant resistomes was strongly affected by the bacterial taxa including Solibacteres, Chloroflexi, Acidobacteria, Gemm-1 and Gemmatimonadetes, as revealed by the network analyses. Moreover, the overlaps of ARGs between lettuce tissues and soil were identified, which indicated that plant and environmental resistomes are interconnected. Our findings provide insights into the transmission routes of ARGs from manured soil to vegetables, and highlight the potential risks of plant resistome migration to the human food chain.
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    Diversity of herbaceous plants and bacterial communities regulates soil resistome across forest biomes
    Hu, H-W ; Wang, J-T ; Singh, BK ; Liu, Y-R ; Chen, Y-L ; Zhang, Y-J ; He, J-Z (WILEY, 2018-09)
    Antibiotic resistance is ancient and prevalent in natural ecosystems and evolved long before the utilization of synthetic antibiotics started, but factors influencing the large-scale distribution patterns of natural antibiotic resistance genes (ARGs) remain largely unknown. Here, a large-scale investigation over 4000 km was performed to profile soil ARGs, plant communities and bacterial communities from 300 quadrats across five forest biomes with minimal human impact. We detected diverse and abundant ARGs in forests, including over 160 genes conferring resistance to eight major categories of antibiotics. The diversity of ARGs was strongly and positively correlated with the diversity of bacteria, herbaceous plants and mobile genetic elements (MGEs). The ARG composition was strongly correlated with the taxonomic structure of bacteria and herbs. Consistent with this strong correlation, structural equation modelling demonstrated that the positive effects of bacterial and herb communities on ARG patterns were maintained even when simultaneously accounting for multiple drivers (climate, spatial predictors and edaphic factors). These findings suggest a paradigm that the interactions between aboveground and belowground communities shape the large-scale distribution of soil resistomes, providing new knowledge for tackling the emerging environmental antibiotic resistance.
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    Short-term copper exposure as a selection pressure for antibiotic resistance and metal resistance in an agricultural soil
    Kang, W ; Zhang, Y-J ; Shi, X ; He, J-Z ; Hu, H-W (SPRINGER HEIDELBERG, 2018-10)
    Owing to the similar mechanisms of antibiotic and metal resistance, there is a growing concern that metal contamination may select for antibiotic resistance genes (ARGs) in the environment. Here, we constructed short-term laboratory microcosms to investigate the dynamics of a wide range of ARGs and two copper (Cu) resistance genes in an agricultural soil amended with a gradient of Cu concentrations (0~1000 mg kg-1). Mobile genetic elements (MGEs) were also quantified as a proxy for the horizontal gene transfer potential of ARGs. We detected 126 unique ARGs across all the soil samples using the high-capacity quantitative PCR array, and multidrug and β-lactam resistance were the most abundant ARG categories. The copper amendments significantly enhanced the absolute and relative abundances of ARGs and MGEs, which gradually increased along the gradient of increasing Cu concentrations. The two Cu resistance genes (copA and pcoR) were highly enriched in low-level Cu treatment (50 and 100 mg kg-1), and their abundances decreased with the increasing Cu concentrations. The level of metal and antibiotic resistance gradually declined over time in all Cu-amended treatments but was still considerably higher in contaminated soils than untreated soils after 56 days' incubation. Significant associations among ARGs and MGEs were revealed by the network analysis, suggesting the mobility potential of antibiotic resistance in Cu-amended soils. No significant positive correlations were found between ARGs and copper resistance genes, suggesting that these genes are not located in the same bacterial hosts. Taken together, our results provide empirical evidence that short-term copper stress can cause evolution of high-level antibiotic and metal resistance and significantly change the diversity, abundance, and horizontal transfer potential of soil ARGs.
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    Temporal succession of soil antibiotic resistance genes following application of swine, cattle and poultry manures spiked with or without antibiotics
    Zhang, Y-J ; Hu, H-W ; Gou, M ; Wang, J-T ; Chen, D ; He, J-Z (ELSEVIER SCI LTD, 2017-12)
    Land application of animal manure is a common agricultural practice potentially leading to dispersal and propagation of antibiotic resistance genes (ARGs) in environmental settings. However, the fate of resistome in agro-ecosystems over time following application of different manure sources has never been compared systematically. Here, soil microcosm incubation was conducted to compare effects of poultry, cattle and swine manures spiked with or without the antibiotic tylosin on the temporal changes of soil ARGs. The high-throughput quantitative PCR detected a total of 185 unique ARGs, with Macrolide-Lincosamide-Streptogramin B resistance as the most frequently encountered ARG type. The diversity and abundance of ARGs significantly increased following application of manure and manure spiked with tylosin, with more pronounced effects observed in the swine and poultry manure treatments than in the cattle manure treatment. The level of antibiotic resistance gradually decreased over time in all manured soils but was still significantly higher in the soils treated with swine and poultry manures than in the untreated soils after 130 days' incubation. Tylosin-amended soils consistently showed higher abundances of ARGs than soils treated with manure only, suggesting a strong selection pressure of antibiotic-spiked manure on soil ARGs. The relative abundance of ARGs had significantly positive correlations with integrase and transposase genes, indicative of horizontal transfer potential of ARGs in manure and tylosin treated soils. Our findings provide evidence that application of swine and poultry manures might enrich more soil ARGs than cattle manure, which necessitates the appropriate treatment of raw animal manures prior to land application to minimise the spread of environmental ARGs.