Hormetic Effect of Pyroligneous Acids on Conjugative Transfer of Plasmid-mediated Multi-antibiotic Resistance Genes within Bacterial Genus

IF 6.7 Q1 ENGINEERING, ENVIRONMENTAL ACS Environmental Au Pub Date : 2022-12-22 DOI:10.1021/acsenvironau.2c00056
Mengying Shao, Liuqingqing Liu, Bingjie Liu, Hao Zheng*, Wei Meng, Yifan Liu, Xiao Zhang, Xiaohan Ma, Cuizhu Sun, Xianxiang Luo, Fengmin Li and Baoshan Xing*, 
{"title":"Hormetic Effect of Pyroligneous Acids on Conjugative Transfer of Plasmid-mediated Multi-antibiotic Resistance Genes within Bacterial Genus","authors":"Mengying Shao,&nbsp;Liuqingqing Liu,&nbsp;Bingjie Liu,&nbsp;Hao Zheng*,&nbsp;Wei Meng,&nbsp;Yifan Liu,&nbsp;Xiao Zhang,&nbsp;Xiaohan Ma,&nbsp;Cuizhu Sun,&nbsp;Xianxiang Luo,&nbsp;Fengmin Li and Baoshan Xing*,&nbsp;","doi":"10.1021/acsenvironau.2c00056","DOIUrl":null,"url":null,"abstract":"<p >Spread of antibiotic resistance genes (ARGs) by conjugation poses great challenges to public health. Application of pyroligneous acids (PA) as soil amendments has been evidenced as a practical strategy to remediate pollution of ARGs in soils. However, little is known about PA effects on horizontal gene transfer (HGT) of ARGs by conjugation. This study investigated the effects of a woody waste-derived PA prepared at 450°C and its three distillation components (F1, F2, and F3) at different temperatures (98, 130, and 220°C) on conjugative transfer of plasmid RP4 within <i>Escherichia coli</i>. PA at relatively high amount (40–100 μL) in a 30-mL mating system inhibited conjugation by 74–85%, following an order of PA &gt; F3 ≈ F2 ≈ F1, proving the hypothesis that PA amendments may mitigate soil ARG pollution by inhibiting HGT. The bacteriostasis caused by antibacterial components of PA, including acids, phenols, and alcohols, as well as its acidity (pH 2.81) contributed to the inhibited conjugation. However, a relatively low amount (10–20 μL) of PA in the same mating system enhanced ARG transfer by 26–47%, following an order of PA &gt; F3 ≈ F2 &gt; F1. The opposite effect at low amount is mainly attributed to the increased intracellular reactive oxygen species production, enhanced cell membrane permeability, increased extracellular polymeric substance contents, and reduced cell surface charge. Our findings highlight the hormesis (low-amount promotion and high-amount inhibition) of PA amendments on ARG conjugation and provide evidence for selecting an appropriate amount of PA amendment to control the dissemination of soil ARGs. Moreover, the promoted conjugation also triggers questions regarding the potential risks of soil amendments (e.g., PA) in the spread of ARGs via HGT.</p>","PeriodicalId":29801,"journal":{"name":"ACS Environmental Au","volume":"3 2","pages":"105–120"},"PeriodicalIF":6.7000,"publicationDate":"2022-12-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://pubs.acs.org/doi/epdf/10.1021/acsenvironau.2c00056","citationCount":"3","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"ACS Environmental Au","FirstCategoryId":"1085","ListUrlMain":"https://pubs.acs.org/doi/10.1021/acsenvironau.2c00056","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"ENGINEERING, ENVIRONMENTAL","Score":null,"Total":0}
引用次数: 3

Abstract

Spread of antibiotic resistance genes (ARGs) by conjugation poses great challenges to public health. Application of pyroligneous acids (PA) as soil amendments has been evidenced as a practical strategy to remediate pollution of ARGs in soils. However, little is known about PA effects on horizontal gene transfer (HGT) of ARGs by conjugation. This study investigated the effects of a woody waste-derived PA prepared at 450°C and its three distillation components (F1, F2, and F3) at different temperatures (98, 130, and 220°C) on conjugative transfer of plasmid RP4 within Escherichia coli. PA at relatively high amount (40–100 μL) in a 30-mL mating system inhibited conjugation by 74–85%, following an order of PA > F3 ≈ F2 ≈ F1, proving the hypothesis that PA amendments may mitigate soil ARG pollution by inhibiting HGT. The bacteriostasis caused by antibacterial components of PA, including acids, phenols, and alcohols, as well as its acidity (pH 2.81) contributed to the inhibited conjugation. However, a relatively low amount (10–20 μL) of PA in the same mating system enhanced ARG transfer by 26–47%, following an order of PA > F3 ≈ F2 > F1. The opposite effect at low amount is mainly attributed to the increased intracellular reactive oxygen species production, enhanced cell membrane permeability, increased extracellular polymeric substance contents, and reduced cell surface charge. Our findings highlight the hormesis (low-amount promotion and high-amount inhibition) of PA amendments on ARG conjugation and provide evidence for selecting an appropriate amount of PA amendment to control the dissemination of soil ARGs. Moreover, the promoted conjugation also triggers questions regarding the potential risks of soil amendments (e.g., PA) in the spread of ARGs via HGT.

Abstract Image

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
热解酸对细菌属内质粒介导的多重耐药基因共轭转移的激效作用
抗生素抗性基因(ARGs)的结合传播给公众健康带来了巨大挑战。焦木酸(PA)作为土壤改良剂的应用已被证明是修复土壤中ARGs污染的一种实用策略。然而,人们对PA通过偶联对ARGs水平基因转移(HGT)的影响知之甚少。本研究研究了在450°C下制备的木质废弃物衍生PA及其三种蒸馏组分(F1、F2和F3)在不同温度(98、130和220°C)下对质粒RP4在大肠杆菌内偶联转移的影响。在30 mL交配系统中,相对较高量(40–100μL)的PA抑制接合74–85%,遵循PA>;F3≈F2≈F1,证明了PA改良剂可以通过抑制HGT来减轻土壤ARG污染的假说。PA的抗菌成分,包括酸、酚和醇,以及其酸度(pH 2.81)引起的抑菌作用有助于抑制结合。然而,在同一交配系统中,相对较低量(10–20μL)的PA使ARG转移增强了26–47%,遵循PA>;F3≈F2>;F1.在低量下的相反作用主要归因于细胞内活性氧产生的增加、细胞膜通透性的增强、细胞外聚合物含量的增加和细胞表面电荷的减少。我们的研究结果强调了PA改良剂对ARG结合的刺激作用(低量促进和高量抑制),并为选择适量的PA改良剂来控制土壤ARG的传播提供了证据。此外,促进的结合还引发了关于土壤改良剂(如PA)通过HGT传播ARGs的潜在风险的问题。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
ACS Environmental Au
ACS Environmental Au 环境科学-
CiteScore
7.10
自引率
0.00%
发文量
0
期刊介绍: ACS Environmental Au is an open access journal which publishes experimental research and theoretical results in all aspects of environmental science and technology both pure and applied. Short letters comprehensive articles reviews and perspectives are welcome in the following areas:Alternative EnergyAnthropogenic Impacts on Atmosphere Soil or WaterBiogeochemical CyclingBiomass or Wastes as ResourcesContaminants in Aquatic and Terrestrial EnvironmentsEnvironmental Data ScienceEcotoxicology and Public HealthEnergy and ClimateEnvironmental Modeling Processes and Measurement Methods and TechnologiesEnvironmental Nanotechnology and BiotechnologyGreen ChemistryGreen Manufacturing and EngineeringRisk assessment Regulatory Frameworks and Life-Cycle AssessmentsTreatment and Resource Recovery and Waste Management
期刊最新文献
Issue Publication Information Issue Editorial Masthead Biogeochemistry of Actinides: Recent Progress and Perspective Biogeochemistry of Actinides: Recent Progress and Perspective. Advancing Microbial Electrochemical H2O2 Synthesis by Tailoring the Surface Chemistry of Stereolithography-Derived 3D Pyrolytic Carbon Electrodes
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1