Tianyi Luo, Xiaohu Dai, Yuting Zhang, Wei Wei, Bing-Jie Ni
{"title":"高铁酸盐(Fe(VI))对抗生素耐药基因的双途径抑制:厌氧消化污泥的氧化失活和遗传迁移障碍","authors":"Tianyi Luo, Xiaohu Dai, Yuting Zhang, Wei Wei, Bing-Jie Ni","doi":"10.1016/j.watres.2025.124648","DOIUrl":null,"url":null,"abstract":"Antibiotic resistance genes (ARGs) and antibiotic resistant bacteria (ARB) are emerging environmental contaminants that threaten public health, highlighting the urgent need for effective control strategies. Ferrate (Fe(VI)), a strong and eco-friendly oxidant, shows great potential for this purpose. This study systematically evaluated the efficacy of Fe(VI) in mitigating ARGs and ARB in anaerobically digested sludge, with a particular focus on elucidating the underlying mechanisms by which Fe(VI) effects ARGs dissemination through both vertical gene transfer (VGT) and horizontal gene transfer (HGT). Result shows that Fe(VI) doses of 20 and 60 mg/g-TS reduce ARGs by 9.75% and 19.12%, respectively, while inactivating up to 24.7% of ARB at the higher dose. Pathogenic ARB, such as <em>Escherichia coli</em> and <em>Shigella sonnei,</em> are preferentially removed, with abundances decrease by 63.7% and 28.0%. Mechanistically, the structural disruption of bacterial cells caused by Fe(VI) in anaerobically digested sludge, as indicated by a 29% reduction in extracellular polymeric substances and a 23.7% increase in cell membrane permeability. Subsequently, a marked release of intracellular ARGs into the extracellular environment is also observed, where they are likely subjected to degradation by Fe(VI). This oxidative killing accounts for the observed ARB decrease, thereby limiting the VGT of ARGs. In addition, Fe(VI) impairs the HGT of ARGs by diminishing their mobility potential, reflected in the reduced co-occurence with mobile genetic elements. Meanwhile, sludge bacterial competence for DNA uptake and recombination is markedly reduced, as evidenced by a 9.8% decline in the abundance of related functional genes. These findings demonstrate that Fe(VI) effectively inhibits the dissemination of ARGs by targeting both primary transmission pathways. It suppresses VGT, thereby reducing the inheritance of ARB within populations, and limits HGT, curbing the spread of mobile ARGs among competent species. By disrupting these two critical routes, Fe(VI) shows strong potential as an effective strategy for mitigating ARGs propagation in sludge systems.","PeriodicalId":443,"journal":{"name":"Water Research","volume":"53 1","pages":""},"PeriodicalIF":12.4000,"publicationDate":"2025-09-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Dual-Pathway Inhibition of Antibiotic Resistance Genes by Ferrate (Fe(VI)): Oxidative Inactivation and Genetic Mobility Impairment in Anaerobically Digested Sludge\",\"authors\":\"Tianyi Luo, Xiaohu Dai, Yuting Zhang, Wei Wei, Bing-Jie Ni\",\"doi\":\"10.1016/j.watres.2025.124648\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"Antibiotic resistance genes (ARGs) and antibiotic resistant bacteria (ARB) are emerging environmental contaminants that threaten public health, highlighting the urgent need for effective control strategies. Ferrate (Fe(VI)), a strong and eco-friendly oxidant, shows great potential for this purpose. This study systematically evaluated the efficacy of Fe(VI) in mitigating ARGs and ARB in anaerobically digested sludge, with a particular focus on elucidating the underlying mechanisms by which Fe(VI) effects ARGs dissemination through both vertical gene transfer (VGT) and horizontal gene transfer (HGT). Result shows that Fe(VI) doses of 20 and 60 mg/g-TS reduce ARGs by 9.75% and 19.12%, respectively, while inactivating up to 24.7% of ARB at the higher dose. Pathogenic ARB, such as <em>Escherichia coli</em> and <em>Shigella sonnei,</em> are preferentially removed, with abundances decrease by 63.7% and 28.0%. Mechanistically, the structural disruption of bacterial cells caused by Fe(VI) in anaerobically digested sludge, as indicated by a 29% reduction in extracellular polymeric substances and a 23.7% increase in cell membrane permeability. Subsequently, a marked release of intracellular ARGs into the extracellular environment is also observed, where they are likely subjected to degradation by Fe(VI). This oxidative killing accounts for the observed ARB decrease, thereby limiting the VGT of ARGs. In addition, Fe(VI) impairs the HGT of ARGs by diminishing their mobility potential, reflected in the reduced co-occurence with mobile genetic elements. Meanwhile, sludge bacterial competence for DNA uptake and recombination is markedly reduced, as evidenced by a 9.8% decline in the abundance of related functional genes. These findings demonstrate that Fe(VI) effectively inhibits the dissemination of ARGs by targeting both primary transmission pathways. It suppresses VGT, thereby reducing the inheritance of ARB within populations, and limits HGT, curbing the spread of mobile ARGs among competent species. By disrupting these two critical routes, Fe(VI) shows strong potential as an effective strategy for mitigating ARGs propagation in sludge systems.\",\"PeriodicalId\":443,\"journal\":{\"name\":\"Water Research\",\"volume\":\"53 1\",\"pages\":\"\"},\"PeriodicalIF\":12.4000,\"publicationDate\":\"2025-09-20\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Water Research\",\"FirstCategoryId\":\"93\",\"ListUrlMain\":\"https://doi.org/10.1016/j.watres.2025.124648\",\"RegionNum\":1,\"RegionCategory\":\"环境科学与生态学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"ENGINEERING, ENVIRONMENTAL\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Water Research","FirstCategoryId":"93","ListUrlMain":"https://doi.org/10.1016/j.watres.2025.124648","RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"ENGINEERING, ENVIRONMENTAL","Score":null,"Total":0}
Dual-Pathway Inhibition of Antibiotic Resistance Genes by Ferrate (Fe(VI)): Oxidative Inactivation and Genetic Mobility Impairment in Anaerobically Digested Sludge
Antibiotic resistance genes (ARGs) and antibiotic resistant bacteria (ARB) are emerging environmental contaminants that threaten public health, highlighting the urgent need for effective control strategies. Ferrate (Fe(VI)), a strong and eco-friendly oxidant, shows great potential for this purpose. This study systematically evaluated the efficacy of Fe(VI) in mitigating ARGs and ARB in anaerobically digested sludge, with a particular focus on elucidating the underlying mechanisms by which Fe(VI) effects ARGs dissemination through both vertical gene transfer (VGT) and horizontal gene transfer (HGT). Result shows that Fe(VI) doses of 20 and 60 mg/g-TS reduce ARGs by 9.75% and 19.12%, respectively, while inactivating up to 24.7% of ARB at the higher dose. Pathogenic ARB, such as Escherichia coli and Shigella sonnei, are preferentially removed, with abundances decrease by 63.7% and 28.0%. Mechanistically, the structural disruption of bacterial cells caused by Fe(VI) in anaerobically digested sludge, as indicated by a 29% reduction in extracellular polymeric substances and a 23.7% increase in cell membrane permeability. Subsequently, a marked release of intracellular ARGs into the extracellular environment is also observed, where they are likely subjected to degradation by Fe(VI). This oxidative killing accounts for the observed ARB decrease, thereby limiting the VGT of ARGs. In addition, Fe(VI) impairs the HGT of ARGs by diminishing their mobility potential, reflected in the reduced co-occurence with mobile genetic elements. Meanwhile, sludge bacterial competence for DNA uptake and recombination is markedly reduced, as evidenced by a 9.8% decline in the abundance of related functional genes. These findings demonstrate that Fe(VI) effectively inhibits the dissemination of ARGs by targeting both primary transmission pathways. It suppresses VGT, thereby reducing the inheritance of ARB within populations, and limits HGT, curbing the spread of mobile ARGs among competent species. By disrupting these two critical routes, Fe(VI) shows strong potential as an effective strategy for mitigating ARGs propagation in sludge systems.
期刊介绍:
Water Research, along with its open access companion journal Water Research X, serves as a platform for publishing original research papers covering various aspects of the science and technology related to the anthropogenic water cycle, water quality, and its management worldwide. The audience targeted by the journal comprises biologists, chemical engineers, chemists, civil engineers, environmental engineers, limnologists, and microbiologists. The scope of the journal include:
•Treatment processes for water and wastewaters (municipal, agricultural, industrial, and on-site treatment), including resource recovery and residuals management;
•Urban hydrology including sewer systems, stormwater management, and green infrastructure;
•Drinking water treatment and distribution;
•Potable and non-potable water reuse;
•Sanitation, public health, and risk assessment;
•Anaerobic digestion, solid and hazardous waste management, including source characterization and the effects and control of leachates and gaseous emissions;
•Contaminants (chemical, microbial, anthropogenic particles such as nanoparticles or microplastics) and related water quality sensing, monitoring, fate, and assessment;
•Anthropogenic impacts on inland, tidal, coastal and urban waters, focusing on surface and ground waters, and point and non-point sources of pollution;
•Environmental restoration, linked to surface water, groundwater and groundwater remediation;
•Analysis of the interfaces between sediments and water, and between water and atmosphere, focusing specifically on anthropogenic impacts;
•Mathematical modelling, systems analysis, machine learning, and beneficial use of big data related to the anthropogenic water cycle;
•Socio-economic, policy, and regulations studies.