Growth of microbes in competitive lifestyles promotes increased ARGs in soil microbiota: insights based on genetic traits
Abstract Background The widespread selective pressure of antibiotics in the environment has led to the propagation of antibiotic resistance genes (ARGs). However, the mechanisms by which microbes balance population growth with the enrichment of ARGs remain poorly understood. To address this, we empl...
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2025-01-01
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| Online Access: | https://doi.org/10.1186/s40168-024-02005-6 |
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| author | Zishu Liu Xiangwu Yao Chengyi Chen Yuxiang Zhao Chifei Dong Lingtao Sun Junxian Zhao Baofeng Zhang Zhendi Yu Dongqing Cheng Lizhong Zhu Baolan Hu |
| author_facet | Zishu Liu Xiangwu Yao Chengyi Chen Yuxiang Zhao Chifei Dong Lingtao Sun Junxian Zhao Baofeng Zhang Zhendi Yu Dongqing Cheng Lizhong Zhu Baolan Hu |
| author_sort | Zishu Liu |
| collection | DOAJ |
| description | Abstract Background The widespread selective pressure of antibiotics in the environment has led to the propagation of antibiotic resistance genes (ARGs). However, the mechanisms by which microbes balance population growth with the enrichment of ARGs remain poorly understood. To address this, we employed microcosm cultivation at different antibiotic (i.e., Oxytetracycline, OTC) stresses across the concentrations from the environmental to the clinical. Paired with shot-gun metagenomics analysis and quantification of bacterial growth, trait-based assessment of soil microbiota was applied to reveal the association between key ARG subtypes, representative bacterial taxa, and functional-gene features that drive the growth of ARGs. Results Our results illuminate that resistome variation is closely associated with bacterial growth. A non-monotonic change in ARG abundance and richness was observed over a concentration gradient from none to 10 mg/l. Soil microbiota exposed to intermediate OTC concentrations (i.e., 0.1 and 0.5 mg/l) showed greater increases in the total abundance of ARGs. Community compositionally, the growth of representative taxa, i.e., Pseudomonadaceae was considered to boost the increase of ARGs. It has chromosomally carried kinds of multidrug resistance genes such as mexAB-oprM and mexCD-oprJ could mediate the intrinsic resistance to OTC. Streptomycetaceae has shown a better adaptive ability than other microbes at the clinical OTC concentrations. However, it contributed less to the ARGs growth as it represents a stress-tolerant lifestyle that grows slowly and carries fewer ARGs. In terms of community genetic features, the community aggregated traits analysis further indicates the enhancement in traits of resource acquisition and growth yield is driving the increase of ARGs abundance. Moreover, optimizations in energy production and conversion, alongside a streamlining of bypass metabolic pathways, further boost the growth of ARGs in sub-inhibitory antibiotic conditions. Conclusion The results of this study suggest that microbes with competitive lifestyles are selected under the stress of environmental sub-inhibitory concentrations of antibiotics and nutrient scarcity. They possess greater substrate utilization capacity and carry more ARGs, due to this they were faster growing and leading to a greater increase in the abundance of ARGs. This study has expanded the application of trait-based assessments in understanding the ecology of ARGs propagation. And the finding illustrated changes in soil resistome are accompanied by the lifestyle switching of the microbiome, which theoretically supports the ARGs control approach based on the principle of species competitive exclusion. Video Abstract |
| format | Article |
| id | doaj-art-c6deb961bd3740318f2dc9fd51561a06 |
| institution | Kabale University |
| issn | 2049-2618 |
| language | English |
| publishDate | 2025-01-01 |
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| series | Microbiome |
| spelling | doaj-art-c6deb961bd3740318f2dc9fd51561a062025-01-19T12:32:31ZengBMCMicrobiome2049-26182025-01-0113111710.1186/s40168-024-02005-6Growth of microbes in competitive lifestyles promotes increased ARGs in soil microbiota: insights based on genetic traitsZishu Liu0Xiangwu Yao1Chengyi Chen2Yuxiang Zhao3Chifei Dong4Lingtao Sun5Junxian Zhao6Baofeng Zhang7Zhendi Yu8Dongqing Cheng9Lizhong Zhu10Baolan Hu11Key Laboratory of Environment Remediation and Ecological Health, Ministry of Education, College of Environmental and Resource Sciences, Zhejiang UniversityCollege of Environmental and Resource Sciences, Zhejiang UniversityCollege of Environmental and Resource Sciences, Zhejiang UniversityCollege of Environmental and Resource Sciences, Zhejiang UniversityCollege of Environmental and Resource Sciences, Zhejiang UniversityCollege of Environmental and Resource Sciences, Zhejiang UniversityCollege of Environmental and Resource Sciences, Zhejiang UniversityHangzhou Ecological and Environmental Monitoring CenterSchool of Medical Technology and Information Engineering, Zhejiang Chinese Medical UniversitySchool of Medical Technology and Information Engineering, Zhejiang Chinese Medical UniversityKey Laboratory of Environment Remediation and Ecological Health, Ministry of Education, College of Environmental and Resource Sciences, Zhejiang UniversityKey Laboratory of Environment Remediation and Ecological Health, Ministry of Education, College of Environmental and Resource Sciences, Zhejiang UniversityAbstract Background The widespread selective pressure of antibiotics in the environment has led to the propagation of antibiotic resistance genes (ARGs). However, the mechanisms by which microbes balance population growth with the enrichment of ARGs remain poorly understood. To address this, we employed microcosm cultivation at different antibiotic (i.e., Oxytetracycline, OTC) stresses across the concentrations from the environmental to the clinical. Paired with shot-gun metagenomics analysis and quantification of bacterial growth, trait-based assessment of soil microbiota was applied to reveal the association between key ARG subtypes, representative bacterial taxa, and functional-gene features that drive the growth of ARGs. Results Our results illuminate that resistome variation is closely associated with bacterial growth. A non-monotonic change in ARG abundance and richness was observed over a concentration gradient from none to 10 mg/l. Soil microbiota exposed to intermediate OTC concentrations (i.e., 0.1 and 0.5 mg/l) showed greater increases in the total abundance of ARGs. Community compositionally, the growth of representative taxa, i.e., Pseudomonadaceae was considered to boost the increase of ARGs. It has chromosomally carried kinds of multidrug resistance genes such as mexAB-oprM and mexCD-oprJ could mediate the intrinsic resistance to OTC. Streptomycetaceae has shown a better adaptive ability than other microbes at the clinical OTC concentrations. However, it contributed less to the ARGs growth as it represents a stress-tolerant lifestyle that grows slowly and carries fewer ARGs. In terms of community genetic features, the community aggregated traits analysis further indicates the enhancement in traits of resource acquisition and growth yield is driving the increase of ARGs abundance. Moreover, optimizations in energy production and conversion, alongside a streamlining of bypass metabolic pathways, further boost the growth of ARGs in sub-inhibitory antibiotic conditions. Conclusion The results of this study suggest that microbes with competitive lifestyles are selected under the stress of environmental sub-inhibitory concentrations of antibiotics and nutrient scarcity. They possess greater substrate utilization capacity and carry more ARGs, due to this they were faster growing and leading to a greater increase in the abundance of ARGs. This study has expanded the application of trait-based assessments in understanding the ecology of ARGs propagation. And the finding illustrated changes in soil resistome are accompanied by the lifestyle switching of the microbiome, which theoretically supports the ARGs control approach based on the principle of species competitive exclusion. Video Abstracthttps://doi.org/10.1186/s40168-024-02005-6Antibiotic resistanceResistomeSoil microbiomeLife history strategyGrowth yieldAntibiotic stress |
| spellingShingle | Zishu Liu Xiangwu Yao Chengyi Chen Yuxiang Zhao Chifei Dong Lingtao Sun Junxian Zhao Baofeng Zhang Zhendi Yu Dongqing Cheng Lizhong Zhu Baolan Hu Growth of microbes in competitive lifestyles promotes increased ARGs in soil microbiota: insights based on genetic traits Microbiome Antibiotic resistance Resistome Soil microbiome Life history strategy Growth yield Antibiotic stress |
| title | Growth of microbes in competitive lifestyles promotes increased ARGs in soil microbiota: insights based on genetic traits |
| title_full | Growth of microbes in competitive lifestyles promotes increased ARGs in soil microbiota: insights based on genetic traits |
| title_fullStr | Growth of microbes in competitive lifestyles promotes increased ARGs in soil microbiota: insights based on genetic traits |
| title_full_unstemmed | Growth of microbes in competitive lifestyles promotes increased ARGs in soil microbiota: insights based on genetic traits |
| title_short | Growth of microbes in competitive lifestyles promotes increased ARGs in soil microbiota: insights based on genetic traits |
| title_sort | growth of microbes in competitive lifestyles promotes increased args in soil microbiota insights based on genetic traits |
| topic | Antibiotic resistance Resistome Soil microbiome Life history strategy Growth yield Antibiotic stress |
| url | https://doi.org/10.1186/s40168-024-02005-6 |
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