Regulatory roles of extracellular polymeric substances in uranium reduction via extracellular electron transfer by Desulfovibrio vulgaris UR1

Guangming Xu; Haotian Yang; Juncheng Han; Xinyao Liu; Kexin Shao; Xindai Li; Guanying Wang; Weifeng Yue; Junfeng Dou

doi:10.1016/j.envres.2024.119862

Regulatory roles of extracellular polymeric substances in uranium reduction via extracellular electron transfer by Desulfovibrio vulgaris UR1

Environ Res. 2024 Aug 28;262(Pt 1):119862. doi: 10.1016/j.envres.2024.119862. Online ahead of print.

Authors

Guangming Xu¹, Haotian Yang¹, Juncheng Han¹, Xinyao Liu¹, Kexin Shao¹, Xindai Li¹, Guanying Wang², Weifeng Yue³, Junfeng Dou⁴

Affiliations

¹ Engineering Research Center of Ministry of Education on Groundwater Pollution Control and Remediation, College of Water Sciences, Beijing Normal University, Beijing 100875, PR China.
² Engineering Research Center of Ministry of Education on Groundwater Pollution Control and Remediation, College of Water Sciences, Beijing Normal University, Beijing 100875, PR China; Beijing Boqi Electric Power Science and Technology Co., Ltd, Beijing 100012, PR China.
³ Engineering Research Center of Ministry of Education on Groundwater Pollution Control and Remediation, College of Water Sciences, Beijing Normal University, Beijing 100875, PR China. Electronic address: yuewf@bnu.edu.cn.
⁴ Engineering Research Center of Ministry of Education on Groundwater Pollution Control and Remediation, College of Water Sciences, Beijing Normal University, Beijing 100875, PR China. Electronic address: doujf@bnu.edu.cn.

PMID: 39208974
DOI: 10.1016/j.envres.2024.119862

Abstract

The pathway of reducing U(VI) to insoluble U(IV) using electroactive bacteria has become an effective and promising approach to address uranium-contaminated water caused by human activities. However, knowledge regarding the roles of extracellular polymeric substances (EPS) in the uranium reduction process involving in extracellular electron transfer (EET) mechanisms is limited. Here, this study isolated a novel U(VI)-reducing strain, Desulfovibrio vulgaris UR1, with a high uranium removal capacity of 2.75 mM/(g dry cell). Based on a reliable EPS extraction method (45 °C heating), manipulation of EPS in D. vulgaris UR1 suspensions (removal or addition of EPS) highlighted its critical role in facilitating uranium reduction efficiency. On the second day, U(VI) removal rates varied significantly across systems with different EPS contents: 60.8% in the EPS-added system, 48.5% in the pristine system, and 22.2% in the EPS-removed system. Characterization of biogenic solids confirmed the reduction of U(VI) by D. vulgaris UR1, and the main products were uraninite and UO₂ (2.88-4.32 nm in diameter). As EPS formed a permeable barrier, these nanoparticles were primarily immobilized within the EPS in EPS-retained/EPS-added cells, and within the periplasm in EPS-removed cells. Multiple electroactive substances, such as tyrosine/tryptophan aromatic compounds, flavins, and quinone-like substances, were identified in EPS, which might be the reason for enhancement of uranium reduction via providing more electron shuttles. Furthermore, proteomics revealed that a large number of proteins in EPS were enriched in the subcategories of catalytic activity and electron transfer activity. Among these, iron-sulfur proteins, such as hydroxylamine reductase (P31101), pyruvate: ferredoxin oxidoreductase (A0A0H3A501), and sulfite reductase (P45574), played the most critical role in regulating EET in D. vulgaris UR1. This work highlighted the importance of EPS in the uranium reduction by D. vulgaris UR1, indicating that EPS functioned as both a reducing agent and a permeation barrier for access to heavy metal uranium.

Keywords: Electrical transfer; Extracellular polymetric substance; Redox active protein; Uraninite; Uranium reduction.