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Distinct lipid membrane interaction and uptake of differentially charged nanoplastics in bacteria

BACKGROUND: Nanoplastics have been recently found widely distributed in our natural environment where ubiquitously bacteria are major participants in various material cycles. Understanding how nanoplastics interact with bacterial cell membrane is critical to grasp their uptake processes as well as t...

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Autores principales: Dai, Shang, Ye, Rui, Huang, Jianxiang, Wang, Binqiang, Xie, Zhenming, Ou, Xinwen, Yu, Ning, Huang, Cheng, Hua, Yuejin, Zhou, Ruhong, Tian, Bing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9011954/
https://www.ncbi.nlm.nih.gov/pubmed/35428303
http://dx.doi.org/10.1186/s12951-022-01321-z
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author Dai, Shang
Ye, Rui
Huang, Jianxiang
Wang, Binqiang
Xie, Zhenming
Ou, Xinwen
Yu, Ning
Huang, Cheng
Hua, Yuejin
Zhou, Ruhong
Tian, Bing
author_facet Dai, Shang
Ye, Rui
Huang, Jianxiang
Wang, Binqiang
Xie, Zhenming
Ou, Xinwen
Yu, Ning
Huang, Cheng
Hua, Yuejin
Zhou, Ruhong
Tian, Bing
author_sort Dai, Shang
collection PubMed
description BACKGROUND: Nanoplastics have been recently found widely distributed in our natural environment where ubiquitously bacteria are major participants in various material cycles. Understanding how nanoplastics interact with bacterial cell membrane is critical to grasp their uptake processes as well as to analyze their associated risks in ecosystems and human microflora. However, little is known about the detailed interaction of differentially charged nanoplastics with bacteria. The present work experimentally and theoretically demonstrated that nanoplastics enter into bacteria depending on the surface charges and cell envelope structural features, and proved the shielding role of membrane lipids against nanoplastics. RESULTS: Positively charged polystyrene nanoplastics (PS-NH(2), 80 nm) can efficiently translocate across cell membranes, while negatively charged PS (PS-COOH) and neutral PS show almost no or much less efficacy in translocation. Molecular dynamics simulations revealed that the PS-NH(2) displayed more favourable electrostatic interactions with bacterial membranes and was subjected to internalisation through membrane penetration. The positively charged nanoplastics destroy cell envelope of Gram-positive B. subtilis by forming membrane pore, while enter into the Gram-negative E. coli with a relatively intact envelope. The accumulated positively charged nanoplastics conveyed more cell stress by inducing a higher level of reactive oxygen species (ROS). However, the subsequently released membrane lipid-coated nanoplastics were nearly nontoxic to cells, and like wise, stealthy bacteria wrapped up with artifical lipid layers became less sensitive to the positively charged nanoplastics, thereby illustrating that the membrane lipid can shield the strong interaction between the positively charged nanoplastics and cells. CONCLUSIONS: Our findings elucidated the molecular mechanism of nanoplastics’ interaction and accumulation within bacteria, and implied the shielding and internalization effect of membrane lipid on toxic nanoplastics could promote bacteria for potential plastic bioremediation. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12951-022-01321-z.
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spelling pubmed-90119542022-04-16 Distinct lipid membrane interaction and uptake of differentially charged nanoplastics in bacteria Dai, Shang Ye, Rui Huang, Jianxiang Wang, Binqiang Xie, Zhenming Ou, Xinwen Yu, Ning Huang, Cheng Hua, Yuejin Zhou, Ruhong Tian, Bing J Nanobiotechnology Research BACKGROUND: Nanoplastics have been recently found widely distributed in our natural environment where ubiquitously bacteria are major participants in various material cycles. Understanding how nanoplastics interact with bacterial cell membrane is critical to grasp their uptake processes as well as to analyze their associated risks in ecosystems and human microflora. However, little is known about the detailed interaction of differentially charged nanoplastics with bacteria. The present work experimentally and theoretically demonstrated that nanoplastics enter into bacteria depending on the surface charges and cell envelope structural features, and proved the shielding role of membrane lipids against nanoplastics. RESULTS: Positively charged polystyrene nanoplastics (PS-NH(2), 80 nm) can efficiently translocate across cell membranes, while negatively charged PS (PS-COOH) and neutral PS show almost no or much less efficacy in translocation. Molecular dynamics simulations revealed that the PS-NH(2) displayed more favourable electrostatic interactions with bacterial membranes and was subjected to internalisation through membrane penetration. The positively charged nanoplastics destroy cell envelope of Gram-positive B. subtilis by forming membrane pore, while enter into the Gram-negative E. coli with a relatively intact envelope. The accumulated positively charged nanoplastics conveyed more cell stress by inducing a higher level of reactive oxygen species (ROS). However, the subsequently released membrane lipid-coated nanoplastics were nearly nontoxic to cells, and like wise, stealthy bacteria wrapped up with artifical lipid layers became less sensitive to the positively charged nanoplastics, thereby illustrating that the membrane lipid can shield the strong interaction between the positively charged nanoplastics and cells. CONCLUSIONS: Our findings elucidated the molecular mechanism of nanoplastics’ interaction and accumulation within bacteria, and implied the shielding and internalization effect of membrane lipid on toxic nanoplastics could promote bacteria for potential plastic bioremediation. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12951-022-01321-z. BioMed Central 2022-04-15 /pmc/articles/PMC9011954/ /pubmed/35428303 http://dx.doi.org/10.1186/s12951-022-01321-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Dai, Shang
Ye, Rui
Huang, Jianxiang
Wang, Binqiang
Xie, Zhenming
Ou, Xinwen
Yu, Ning
Huang, Cheng
Hua, Yuejin
Zhou, Ruhong
Tian, Bing
Distinct lipid membrane interaction and uptake of differentially charged nanoplastics in bacteria
title Distinct lipid membrane interaction and uptake of differentially charged nanoplastics in bacteria
title_full Distinct lipid membrane interaction and uptake of differentially charged nanoplastics in bacteria
title_fullStr Distinct lipid membrane interaction and uptake of differentially charged nanoplastics in bacteria
title_full_unstemmed Distinct lipid membrane interaction and uptake of differentially charged nanoplastics in bacteria
title_short Distinct lipid membrane interaction and uptake of differentially charged nanoplastics in bacteria
title_sort distinct lipid membrane interaction and uptake of differentially charged nanoplastics in bacteria
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9011954/
https://www.ncbi.nlm.nih.gov/pubmed/35428303
http://dx.doi.org/10.1186/s12951-022-01321-z
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