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全氟辛烷磺酸促进细菌抗生素耐药基因接合转移的未被识别风险。

Unrecognized risk of perfluorooctane sulfonate in promoting conjugative transfers of bacterial antibiotic resistance genes.

机构信息

Ministry of Education Key Laboratory of Pollution Processes and Environmental Criteria, College of Environmental Science and Engineering, Nankai University , Tianjin, China.

出版信息

Appl Environ Microbiol. 2023 Sep 28;89(9):e0053323. doi: 10.1128/aem.00533-23. Epub 2023 Aug 11.

Abstract

Antibiotic resistance is a major global health crisis facing humanity, with horizontal gene transfer (HGT) as a principal dissemination mechanism in the natural and clinical environments. Perfluoroalkyl substances (PFASs) are emerging contaminants of global concern due to their high persistence in the environment and adverse effects on humans. However, it is unknown whether PFASs affect the HGT of bacterial antibiotic resistance. Using a genetically engineered MG1655 as the donor of plasmid-encoded antibiotic resistance genes (ARGs), J53 and soil bacterial community as two different recipients, this study demonstrated that the conjugation frequency of ARGs between two strains was (1.45 ± 0.17) × 10 and perfluorooctane sulfonate (PFOS) at environmentally relevant concentrations (2-50 μg L) increased conjugation transfer between strains by up to 3.25-fold. Increases in reactive oxygen species production, cell membrane permeability, biofilm formation capacity, and cell contact in two strains were proposed as major promotion mechanisms from PFOS exposure. Weighted gene co-expression network analysis of transcriptome data identified a series of candidate genes whose expression changes could contribute to the increase in conjugation transfer induced by PFOS. Furthermore, PFOS also generally increased the ARG transfer into the studied soil bacterial community, although the uptake ability of different community members of the plasmid either increased or decreased upon PFOS exposure depending on specific bacterial taxa. Overall, this study reveals an unrecognized risk of PFOS in accelerating the dissemination of antibiotic resistance. IMPORTANCE Perfluoroalkyl substances (PFASs) are emerging contaminants of global concern due to their high persistence in the environment and adverse health effects. Although the influence of environmental pollutants on the spread of antibiotic resistance, one of the biggest threats to global health, has attracted increasing attention in recent years, it is unknown whether environmental residues of PFASs affect the dissemination of bacterial antibiotic resistance. Considering PFASs, often called "forever" compounds, have significantly higher environmental persistence than most emerging organic contaminants, exploring the effect of PFASs on the spread of antibiotic resistance is more environmentally relevant and has essential ecological and health significance. By systematically examining the influence of perfluorooctane sulfonate on the antibiotic resistance gene conjugative transfer, not only at the single-strain level but also at the community level, this study has uncovered an unrecognized risk of PFASs in promoting conjugative transfers of bacterial antibiotic resistance genes, which could be incorporated into the risk assessment framework of PFASs.

摘要

抗生素耐药性是人类面临的主要全球健康危机,水平基因转移(HGT)是自然和临床环境中主要的传播机制。全氟烷基物质(PFASs)由于其在环境中的高持久性和对人类的不良影响,是一种受到全球关注的新兴污染物。然而,目前尚不清楚 PFASs 是否会影响细菌抗生素耐药性的 HGT。本研究使用基因工程 MG1655 作为质粒编码抗生素耐药基因(ARGs)的供体,J53 和土壤细菌群落作为两种不同的受体,证明了在环境相关浓度(2-50μg/L)下,两种 菌株之间 ARGs 的接合频率增加了 3.25 倍。PFOS 暴露会导致两种 菌株中活性氧物质产生、细胞膜通透性、生物膜形成能力和细胞接触增加,这被认为是促进 HGT 的主要机制。基于转录组数据的加权基因共表达网络分析,确定了一系列候选基因,这些基因的表达变化可能有助于增加 PFOS 诱导的接合转移。此外,PFOS 通常也会增加研究中土壤细菌群落中 ARG 的转移,尽管由于特定细菌类群的不同,质粒的不同群落成员对 PFOS 的摄取能力增加或减少。总的来说,这项研究揭示了 PFOS 在加速抗生素耐药性传播方面的一个未被认识到的风险。

重要性

全氟烷基物质(PFASs)由于其在环境中的高持久性和对健康的不良影响,是一种受到全球关注的新兴污染物。尽管近年来,环境污染物对抗生素耐药性(一种对全球健康最大的威胁之一)传播的影响引起了越来越多的关注,但尚不清楚环境中 PFASs 的残留是否会影响细菌抗生素耐药性的传播。考虑到 PFASs 通常被称为“永久”化合物,其环境持久性明显高于大多数新兴有机污染物,因此研究 PFASs 对抗生素耐药性传播的影响在环境方面更具相关性,具有重要的生态和健康意义。通过系统研究全氟辛烷磺酸对抗生素耐药基因接合转移的影响,不仅在单菌株水平,而且在群落水平,本研究揭示了 PFASs 在促进细菌抗生素耐药基因接合转移方面的一个未被认识到的风险,这可能被纳入 PFASs 的风险评估框架中。

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