Microplastic biofilm: An important microniche that may accelerate the spread of antibiotic resistance genes via natural transformation

Huixiang Wang; Kaiwen Xu; Jing Wang; Chong Feng; Yihan Chen; Jianghong Shi; Yan Ding; Chengxun Deng; Xiaowei Liu

doi:10.1016/j.jhazmat.2023.132085

Microplastic biofilm: An important microniche that may accelerate the spread of antibiotic resistance genes via natural transformation

J Hazard Mater. 2023 Oct 5:459:132085. doi: 10.1016/j.jhazmat.2023.132085. Epub 2023 Jul 18.

Authors

Huixiang Wang¹, Kaiwen Xu², Jing Wang³, Chong Feng⁴, Yihan Chen⁵, Jianghong Shi⁶, Yan Ding⁵, Chengxun Deng², Xiaowei Liu⁷

Affiliations

¹ School of Biology, Food, and Environment, Hefei University, Hefei 230601, China; School of Environment, Nanjing Normal University, Nanjing 210023, China; School of Resources and Environmental Engineering, Hefei University of Technology, Hefei 230009, China.
² School of Biology, Food, and Environment, Hefei University, Hefei 230601, China; International (Sino-German) Joint Research Center for Biomass of Anhui Province, Hefei 230601, China.
³ School of Biology, Food, and Environment, Hefei University, Hefei 230601, China; School of Resources and Environmental Engineering, Hefei University of Technology, Hefei 230009, China.
⁴ School of Biology, Food, and Environment, Hefei University, Hefei 230601, China.
⁵ School of Resources and Environmental Engineering, Hefei University of Technology, Hefei 230009, China.
⁶ State Environmental Protection Key Laboratory of Integrated Surface Water-Groundwater Pollution Control, School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen 518055, China.
⁷ School of Biology, Food, and Environment, Hefei University, Hefei 230601, China; International (Sino-German) Joint Research Center for Biomass of Anhui Province, Hefei 230601, China. Electronic address: liuxw@hfuu.edu.cn.

PMID: 37494793
DOI: 10.1016/j.jhazmat.2023.132085

Abstract

Microplastic (MP) biofilms provide a specific microniche for microbial life and are a potential hotspot for the horizontal gene transfer (HGT) of antibiotic resistance genes (ARGs). Nevertheless, the acquisition of ARGs in MP biofilms via natural transformation mediated by extracellular DNA (eDNA) has been rarely explored. This study demonstrated that MP biofilms promoted the natural transformation of extracellular ARGs at the single-cell and multi-species levels, compared to natural substrate (NS) biofilms and bacterioplankton. The transformation frequency on MP biofilms was up to 1000-fold compare to that on NS. The small MPs and aged MPs enhanced the ARG transformation frequencies up to 77.16-fold and 32.05-fold, respectively, compared with the large MPs and pristine MPs. The transformation frequencies on MP biofilms were significantly positively correlated with the bacterial density and extracellular polymeric substance (EPS) content (P < 0.05). Furthermore, MPs significantly increased the expression of the biofilm formation related genes (motA and pgaA) and DNA uptake related genes (pilX and comA) compared to NS and bacterioplankton. The more transformants colonized on MPs contributed to the enhanced transformation frequencies at the community-wide level. Overall, eDNA-mediated transformation in MP biofilms may be an important path of ARG spread, which was promoted by heterogeneous biofilm.

Keywords: ARG; Extracellular DNA; Extracellular polymeric substance; HGT; Microbial community.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Anti-Bacterial Agents* / pharmacology
Biofilms
Drug Resistance, Microbial / genetics
Extracellular Polymeric Substance Matrix*
Genes, Bacterial
Microplastics
Plastics

Substances

Anti-Bacterial Agents
Plastics
Microplastics