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Chicken Manure and Mushroom Residues Affect Soil Bacterial Community Structure but Not the Bacterial Resistome When Applied at the Same Rate of Nitrogen for 3 Years.

ABSTRACT: Animal manure is a reservoir of antibiotic resistance genes (ARGs), and direct application of the manure will lead to spread of ARGs in farmland. Here, we explored the impacts of chicken manure and heat-treated chicken manure on the patterns of soil resistome after 3 years' application, with mushroom residues set as the plant-derived organic manure treatment. A total of 262 ARG subtypes were detected in chicken manure using high-throughput qPCR, and heat treatment can effectively remove 50 types of ARGs. Although ARG subtypes and abundance were both higher in chicken manure, there was no significant difference in the ARG profiles and total ARG abundance among three manure-treated soils. Soil bacteria community compositions were significantly different among manure-treated soils, but they were not significantly correlated with soil ARG profiles. Fast expectation-maximization microbial source tracking (FEAST) was used for quantifying the contributions of the potential sources to microbial taxa and ARGs in manure-fertilized soil. Results revealed that only 0.2% of the chicken manure-derived bacterial communities survived in soil, and intrinsic ARGs were the largest contributor of soil ARGs (95.8-99.7%); ARGs from chicken manure only contributed 0.4%. The total ARG abundance in the heat-treated chicken manure-amended soils was similar to that in the mushroom residue-treated soils, while it was 1.41 times higher in chicken manure-treated soils. Thus, heat treatment of chicken manure may efficiently reduce ARGs introduced into soil and decrease the risk of dissemination of ARGs.

SUBMITTER: Peng S

PROVIDER: S-EPMC8177108 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Manure application to agricultural soil introduces antibiotic residues and increases the abundance of antibiotic-resistant bacteria (ARB) carrying antibiotic resistance genes (ARGs), often located on mobile genetic elements (MGEs). The rhizosphere is regarded as a hotspot of microbial activity and gene transfer, which can alter and prolong the effects of organic fertilizers containing antibiotics. However, not much is known about the influence of plants on the effects of doxycycline applied to soil via manure. In this study, the effects of manure spiked with or without doxycycline on the prokaryotic community composition as well as on the relative abundance of ARGs and MGEs in lettuce rhizosphere and bulk soil were investigated by means of a polyphasic cultivation-independent approach. Samples were taken 42 days after manure application, and total community DNA was extracted. Besides a pronounced manure effect, doxycycline spiking caused an additional enrichment of ARGs and MGEs. High-throughput quantitative PCR revealed an increase in tetracycline, aminoglycoside, and macrolide-lincosamide-streptogramin B (MLSB) resistance genes associated with the application of manure spiked with doxycycline. This effect was unexpectedly lower in the rhizosphere than in bulk soil, suggesting a faster dissipation of the antibiotic and a more resilient prokaryotic community in the rhizosphere. Interestingly, the tetracycline resistance gene tetA(P) was highly enriched in manure-treated bulk soil and rhizosphere, with highest values observed in doxycycline-treated bulk soil, concurring with an enrichment of Clostridia. Thus, the gene tetA(P) might be a suitable marker of soil contamination by ARB, ARGs, and antibiotics of manure origin. These findings illustrate that the effects of manure and doxycycline on ARGs and MGEs differ between rhizosphere and bulk soil, which needs to be considered when assessing risks for human health connected to the spread of ARGs in the environment.

Project description:Transcriptomic evidence is needed to determine whether composting is more effective than conventional stockpiling in mitigating the risk of resistome in livestock manure. The objective of this study is to compare composting and stockpiling for their effectiveness in reducing the risk of antibiotic resistance in beef cattle manure. Samples collected from the center and the surface of full-size manure stockpiling and composting piles were subject to metagenomic and metatranscriptomic analyses. While the distinctions in resistome between stockpiled and composted manure were not evident at the DNA level, the advantages of composting over stockpiling were evident at the transcriptomic level in terms of the abundance of antibiotic resistance genes (ARGs), the number of ARG subtypes, and the prevalence of high-risk ARGs (i.e., mobile ARGs associated with zoonotic pathogens). DNA and transcript contigs show that the pathogen hosts of high-risk ARGs included Escherichia coli O157:H7 and O25b:H4, Klebsiella pneumoniae, and Salmonella enterica. Although the average daily temperatures for the entire composting pile exceeded 55°C throughout the field study, more ARG and ARG transcripts were removed at the center of the composting pile than at the surface. This work demonstrates the advantage of composting over stockpiling in reducing ARG risk in active populations in beef cattle manure.IMPORTANCEProper treatment of manure before land application is essential to mitigate the spread of antibiotic resistance in the environment. Stockpiling and composting are two commonly used methods for manure treatment. However, the effectiveness of composting in reducing antibiotic resistance in manure has been debated. This work compared the ability of these two methods to reduce the risk of antibiotic resistance in beef cattle manure. Our results demonstrate that composting reduced more high-risk resistance genes at the transcriptomic level in cattle manure than conventional stockpiling. This finding not only underscores the effectiveness of composting in reducing antibiotic resistance in manure but also highlights the importance of employing RNA analyses alongside DNA analyses.

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Chicken Manure and Mushroom Residues Affect Soil Bacterial Community Structure but Not the Bacterial Resistome When Applied at the Same Rate of Nitrogen for 3 Years.

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