Microbial phylogeny determines transcriptional response of resistome to dynamic composting processes
Abstract Background Animal manure is a reservoir of antibiotic resistance genes (ARGs) that pose a potential health risk globally, especially for resistance to the antibiotics commonly used in livestock production (such as tetracycline, sulfonamide, and fluoroquinolone). Currently, the effects of bi...
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BMC
2017-08-01
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Series: | Microbiome |
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Online Access: | http://link.springer.com/article/10.1186/s40168-017-0324-0 |
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author | Cheng Wang Da Dong P. J. Strong Weijing Zhu Zhuang Ma Yong Qin Weixiang Wu |
author_facet | Cheng Wang Da Dong P. J. Strong Weijing Zhu Zhuang Ma Yong Qin Weixiang Wu |
author_sort | Cheng Wang |
collection | DOAJ |
description | Abstract Background Animal manure is a reservoir of antibiotic resistance genes (ARGs) that pose a potential health risk globally, especially for resistance to the antibiotics commonly used in livestock production (such as tetracycline, sulfonamide, and fluoroquinolone). Currently, the effects of biological treatment (composting) on the transcriptional response of manure ARGs and their microbial hosts are not well characterized. Composting is a dynamic process that consists of four distinct phases that are distinguished by the temperature resulting from microbial activity, namely the mesophilic, thermophilic, cooling, and maturing phases. In this study, changes of resistome expression were determined and related to active microbiome profiles during the dynamic composting process. This was achieved by integrating metagenomic and time series metatranscriptomic data for the evolving microbial community during composting. Results Composting noticeably reduced the aggregated expression level of the manure resistome, which primarily consisted of genes encoding for tetracycline, vancomycin, fluoroquinolone, beta-lactam, and aminoglycoside resistance, as well as efflux pumps. Furthermore, a varied transcriptional response of resistome to composting at the ARG levels was highlighted. The expression of tetracycline resistance genes (tetM-tetW-tetO-tetS) decreased during composting, where distinctive shifts in the four phases of composting were related to variations in antibiotic concentration. Composting had no effect on the expression of sulfonamide and fluoroquinolone resistance genes, which increased slightly during the thermophilic phase and then decreased to initial levels. As indigenous populations switched greatly throughout the dynamic composting, the core resistome persisted and their reservoir hosts’ composition was significantly correlated with dynamic active microbial phylogenetic structure. Hosts for sulfonamide and fuoroquinolone resistance genes changed notably in phylognetic structure and underwent an initial increase and then a decrease in abundance. By contrast, hosts for tetracycline resistance genes (tetM-tetW-tetO-tetS) exhibited a constant decline through time. Conclusions The transcriptional patterns of a core resistome over the course of composting were identified, and microbial phylogeny was the key determinant in defining the varied transcriptional response of resistome to this dynamic biological process. This research demonstrated the benefits of composting for manure treatment. It reduced the risk of emerging environmental contaminants such as tetracyclines, tetracycline resistance genes, and clinically relevant pathogens carrying ARGs, as well as RNA viruses and bacteriophages. |
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spelling | doaj.art-b1d18c6d4ccc444bbb01c1145d6ea90f2022-12-22T03:03:27ZengBMCMicrobiome2049-26182017-08-015111510.1186/s40168-017-0324-0Microbial phylogeny determines transcriptional response of resistome to dynamic composting processesCheng Wang0Da Dong1P. J. Strong2Weijing Zhu3Zhuang Ma4Yong Qin5Weixiang Wu6Zhejiang Province Key Laboratory for Water Pollution Control and Environmental Safety Technology, Institute of Environmental Science and Technology, Zhejiang UniversityZhejiang Province Key Laboratory for Water Pollution Control and Environmental Safety Technology, Institute of Environmental Science and Technology, Zhejiang UniversityQueensland University of TechnologyZhejiang Province Key Laboratory for Water Pollution Control and Environmental Safety Technology, Institute of Environmental Science and Technology, Zhejiang UniversityZhejiang Province Key Laboratory for Water Pollution Control and Environmental Safety Technology, Institute of Environmental Science and Technology, Zhejiang UniversityZhejiang Province Key Laboratory for Water Pollution Control and Environmental Safety Technology, Institute of Environmental Science and Technology, Zhejiang UniversityZhejiang Province Key Laboratory for Water Pollution Control and Environmental Safety Technology, Institute of Environmental Science and Technology, Zhejiang UniversityAbstract Background Animal manure is a reservoir of antibiotic resistance genes (ARGs) that pose a potential health risk globally, especially for resistance to the antibiotics commonly used in livestock production (such as tetracycline, sulfonamide, and fluoroquinolone). Currently, the effects of biological treatment (composting) on the transcriptional response of manure ARGs and their microbial hosts are not well characterized. Composting is a dynamic process that consists of four distinct phases that are distinguished by the temperature resulting from microbial activity, namely the mesophilic, thermophilic, cooling, and maturing phases. In this study, changes of resistome expression were determined and related to active microbiome profiles during the dynamic composting process. This was achieved by integrating metagenomic and time series metatranscriptomic data for the evolving microbial community during composting. Results Composting noticeably reduced the aggregated expression level of the manure resistome, which primarily consisted of genes encoding for tetracycline, vancomycin, fluoroquinolone, beta-lactam, and aminoglycoside resistance, as well as efflux pumps. Furthermore, a varied transcriptional response of resistome to composting at the ARG levels was highlighted. The expression of tetracycline resistance genes (tetM-tetW-tetO-tetS) decreased during composting, where distinctive shifts in the four phases of composting were related to variations in antibiotic concentration. Composting had no effect on the expression of sulfonamide and fluoroquinolone resistance genes, which increased slightly during the thermophilic phase and then decreased to initial levels. As indigenous populations switched greatly throughout the dynamic composting, the core resistome persisted and their reservoir hosts’ composition was significantly correlated with dynamic active microbial phylogenetic structure. Hosts for sulfonamide and fuoroquinolone resistance genes changed notably in phylognetic structure and underwent an initial increase and then a decrease in abundance. By contrast, hosts for tetracycline resistance genes (tetM-tetW-tetO-tetS) exhibited a constant decline through time. Conclusions The transcriptional patterns of a core resistome over the course of composting were identified, and microbial phylogeny was the key determinant in defining the varied transcriptional response of resistome to this dynamic biological process. This research demonstrated the benefits of composting for manure treatment. It reduced the risk of emerging environmental contaminants such as tetracyclines, tetracycline resistance genes, and clinically relevant pathogens carrying ARGs, as well as RNA viruses and bacteriophages.http://link.springer.com/article/10.1186/s40168-017-0324-0Resistome responseMetatranscriptomicsMetagenomicsCompostingARGsMGEs |
spellingShingle | Cheng Wang Da Dong P. J. Strong Weijing Zhu Zhuang Ma Yong Qin Weixiang Wu Microbial phylogeny determines transcriptional response of resistome to dynamic composting processes Microbiome Resistome response Metatranscriptomics Metagenomics Composting ARGs MGEs |
title | Microbial phylogeny determines transcriptional response of resistome to dynamic composting processes |
title_full | Microbial phylogeny determines transcriptional response of resistome to dynamic composting processes |
title_fullStr | Microbial phylogeny determines transcriptional response of resistome to dynamic composting processes |
title_full_unstemmed | Microbial phylogeny determines transcriptional response of resistome to dynamic composting processes |
title_short | Microbial phylogeny determines transcriptional response of resistome to dynamic composting processes |
title_sort | microbial phylogeny determines transcriptional response of resistome to dynamic composting processes |
topic | Resistome response Metatranscriptomics Metagenomics Composting ARGs MGEs |
url | http://link.springer.com/article/10.1186/s40168-017-0324-0 |
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