Surface biomineralization of uranium onto Shewanella putrefaciens with or without extracellular polymeric substances

Xiaoqin Nie; Qiaoya Lin; Faqin Dong; Wencai Cheng; Congcong Ding; Junling Wang; Mingxue Liu; Guozheng Chen; Yan Zhou; Xiaoan Li; Maxim I Boyanov; Kenneth M Kemner

doi:10.1016/j.ecoenv.2022.113719

Surface biomineralization of uranium onto Shewanella putrefaciens with or without extracellular polymeric substances

Ecotoxicol Environ Saf. 2022 Aug:241:113719. doi: 10.1016/j.ecoenv.2022.113719. Epub 2022 Jun 9.

Authors

Xiaoqin Nie¹, Qiaoya Lin², Faqin Dong³, Wencai Cheng⁴, Congcong Ding⁵, Junling Wang⁵, Mingxue Liu⁴, Guozheng Chen⁶, Yan Zhou⁶, Xiaoan Li⁷, Maxim I Boyanov⁸, Kenneth M Kemner⁹

Affiliations

¹ National Collaborative Innovation Center for Nuclear Waste and Environmental Safety, Southwest University of Science and Technology, Mianyang 621010, China; Fundamental Science on Nuclear Wastes and Environmental Safety Laboratory, Southwest University of Science and Technology, Mianyang 621010, China; Mianyang Central Hospital, NHC Key Laboratory of Nuclear Technology Medical Transformation，Mianyang 621000, China. Electronic address: xiaoqin_nie@163.com.
² National Collaborative Innovation Center for Nuclear Waste and Environmental Safety, Southwest University of Science and Technology, Mianyang 621010, China; Sino-French Institute of Nuclear Engineering and Technology, Sun Yat-sen University, Zhuhai 519082, China.
³ National Collaborative Innovation Center for Nuclear Waste and Environmental Safety, Southwest University of Science and Technology, Mianyang 621010, China; Key Laboratory of Solid Waste Treatment and Resource Recycle, Ministry of Education, Southwest University of Science and Technology, Mianyang 621010, China.
⁴ National Collaborative Innovation Center for Nuclear Waste and Environmental Safety, Southwest University of Science and Technology, Mianyang 621010, China.
⁵ Fundamental Science on Nuclear Wastes and Environmental Safety Laboratory, Southwest University of Science and Technology, Mianyang 621010, China.
⁶ Mianyang Central Hospital, NHC Key Laboratory of Nuclear Technology Medical Transformation，Mianyang 621000, China.
⁷ Mianyang Central Hospital, NHC Key Laboratory of Nuclear Technology Medical Transformation，Mianyang 621000, China. Electronic address: 435445611@qq.com.
⁸ Biosciences Division, Argonne National Laboratory, Argonne, IL 60439, USA; Bulgarian Academy of Sciences, Institute of Chemical Engineering, Sofia 1113, Bulgaria.
⁹ Biosciences Division, Argonne National Laboratory, Argonne, IL 60439, USA.

PMID: 35691198
DOI: 10.1016/j.ecoenv.2022.113719

Abstract

The influence of extracellular polymeric substances (EPS) on the interaction between uranium [U(VI)] and Shewanella putrefaciens (S. putrefaciens), especially the U(VI) biomineralization process occurring on whole cells and cell components of S. putrefaciens was investigated in this study. The removal efficiency of U(VI) by S. putrefaciens was decreased by 22% after extraction of EPS. Proteins were identified as the main components of EPS by EEM analysis and were determined to play a major role in the biosorption of uranium. SEM-EDS results showed that U(VI) was distributed around the whole cell as 500-nanometer schistose structures, which consisted primarily of U and P. However, similar uranium lamellar crystal were wrapped only on the surface of EPS-free S. putrefaciens cells. FTIR and XPS analysis indicated that phosphorus- and nitrogen-containing groups played important roles in complexing U (VI). XRD and U L_III-edge EXAFS analyses demonstrated that the schistose structure consisted of hydrogen uranyl phosphate [H₂(UO₂)₂(PO₄)₂•8H₂O]. Our study provides new insight into the mechanisms of induced uranium crystallization by EPS and cell wall membranes of living bacterial cells under aerobic conditions.

Keywords: Biomineralization; EPS; Shewanella putrefaciens; Uranium.

MeSH terms

Biomineralization
Extracellular Polymeric Substance Matrix / metabolism
Phosphorus
Shewanella putrefaciens* / metabolism
Uranium* / metabolism

Substances

Phosphorus
Uranium