Microbial-driven ectopic uranium extraction with net electrical energy production

doi:10.1007/s11783-024-1764-y

Front. Environ. Sci. Eng.

2024, Vol. 18

Issue (1) : 4 https://doi.org/10.1007/s11783-024-1764-y

RESEARCH ARTICLE

Microbial-driven ectopic uranium extraction with net electrical energy production

Xin Tang¹, Yin Ye¹, Chunlin Wang¹, Bingqian Wang², Zemin Qin¹, Cui Li¹, Yanlong Chen¹, Yuheng Wang¹(

), Zhiling Li³, Miao Lv⁴, Aijie Wang³, Fan Chen¹(

)

¹. School of Ecology and Environment, Northwestern Polytechnical University, Xi’an 710129, China
². School of Materials Science and Engineering, Xi’an University of Architecture and Technology, Xi’an 710055, China
³. State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of Technology, Harbin 150090, China
⁴. Faculty of Geosciences and Environmental Engineering, Southwest Jiaotong University, Chengdu 611756, China

Download: PDF(3623 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

● Stable and efficient U extraction with electrical energy production was achieved.

● The U(VI) removal proceeded via a diffusion-controlled U(VI)-to-U(IV) reduction.

● Electro-microbiome was constructed for microbial-driven ectopic U extraction.

● Metabolic pathways of anode biofilm were deciphered by metagenomics.

The extraction of uranium (U) from U-bearing wastewater is of paramount importance for mitigating negative environmental impacts and recovering U resources. Microbial reduction of soluble hexavalent uranium (U(VI)) to insoluble tetravalent uranium (U(IV)) holds immense potential for this purpose, but its practical application has been impeded by the challenges associated with managing U-bacterial mixtures and the biotoxicity of U. To address these challenges, we present a novel spontaneous microbial electrochemical (SMEC) method that spatially decoupled the microbial oxidation reaction and the U(VI) reduction reaction. Our results demonstrated stable and efficient U extraction with net electrical energy production, which was achieved with both synthetic and real wastewater. U(VI) removal occurred via diffusion-controlled U(VI)-to-U(IV) reduction-precipitation at the cathode, and the U^IVO₂ deposited on the surface of the cathode contributed to the stability and durability of the abiotic U(VI) reduction. Metagenomic sequencing revealed the formation of efficient electroactive communities on the anodic biofilm and enrichment of the key functional genes and metabolic pathways involved in electron transfer, energy metabolism, the TCA cycle, and acetate metabolism, which indicated the ectopic reduction of U(VI) at the cathode. Our study represents a significant advancement in the cost-effective recovery of U from U(VI)-bearing wastewater and may open a new avenue for sustainable uranium extraction.

Keywords U(VI) bioreduction Electricity production Reaction decoupling Uranium-bearing wastewater Biofilm microbiome

Corresponding Author(s): Yuheng Wang,Fan Chen

Issue Date: 09 August 2023

Cite this article:

Xin Tang,Yin Ye,Chunlin Wang, et al. Microbial-driven ectopic uranium extraction with net electrical energy production[J]. Front. Environ. Sci. Eng., 2024, 18(1): 4.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-024-1764-y
https://academic.hep.com.cn/fese/EN/Y2024/V18/I1/4

Fig.1 (a) Performance in U extraction from synthetic wastewater under different operating conditions; (b) long-term U extraction performance for the SMEC method during cycled runs with synthetic U-mining wastewater; (c) U extraction from real U-mining wastewater with 50 mmol/L acetate in the anolyte; (d) output power of the SMEC system during the treatment of synthetic and real U-mining wastewater.

Fig.2 (a) SEM image, (b, c) elemental mappings, and (d) EDS spectrum of the electrode after uranium extraction via the SMEC method.

Fig.3 Characterizations of the extracted uranium and electrode. (a) XPS survey scan, (b) U 4f scan, and (c) XRD pattern for the cathode deposits; (d) CV curves for the electrode with and without U(VI) at a scan rate of 150 mV/s; (e) CV curves of the electrode with varying scan rates; (f) reduction peak currents as a function of the square root of the scan rate.

Fig.4 Bacterial community structures of the anodic biofilm at the (a) phylum, (b) class, and (c) genus levels (relative abundance > 1%).

Fig.5 Relative abundance of the KEGG Orthology (KO) involved in the metabolism of the bioanode driving U(VI) reduction.

Fig.6 Conceptual model for microbial-driven ectopic uranium extraction with net electrical energy production.

1	A P Borole , C Y Hamilton , T Vishnivetskaya , D Leak , C Andras . (2009). Improving power production in acetate-fed microbial fuel cells via enrichment of exoelectrogenic organisms in flow-through systems. Biochemical Engineering Journal, 48(1): 71–80 https://doi.org/10.1016/j.bej.2009.08.008
2	A P Borole , H O’Neill , C Tsouris , S Cesar . (2008). A microbial fuel cell operating at low pH using the acidophile Acidiphilium cryptum. Biotechnology Letters, 30(8): 1367–1372 https://doi.org/10.1007/s10529-008-9700-y
3	T Cai , Y Zhang , N Wang , Z Zhang , X Lu , G Zhen . (2022). Electrochemically active microorganisms sense charge transfer resistance for regulating biofilm electroactivity, spatio-temporal distribution, and catabolic pathway. Chemical Engineering Journal, 442: 136248 https://doi.org/10.1016/j.cej.2022.136248
4	F Chen , B Fan , C Wang , J Qian , B Wang , X Tang , Z Qin , Y Chen , L Bin , W Liu . et al.. (2022a). Weak electro-stimulation promotes microbial uranium removal: efficacy and mechanisms. Journal of Hazardous Materials, 439: 129622 https://doi.org/10.1016/j.jhazmat.2022.129622
5	F Chen , Z Li , Y Ye , M Lv , B Liang , Y Yuan , H Y Cheng , Y Liu , Z He , H Wang . et al.. (2022b). Coupled sulfur and electrode-driven autotrophic denitrification for significantly enhanced nitrate removal. Water Research, 220: 118675 https://doi.org/10.1016/j.watres.2022.118675
6	N Gao , Z Huang , H Liu , J Hou , X Liu . (2019). Advances on the toxicity of uranium to different organisms. Chemosphere, 237: 124548 https://doi.org/10.1016/j.chemosphere.2019.124548
7	A Kouzuma , S I Ishii , K Watanabe . (2018). Metagenomic insights into the ecology and physiology of microbes in bioelectrochemical systems. Bioresource Technology, 255: 302–307 https://doi.org/10.1016/j.biortech.2018.01.125
8	H Li , B Wang , S Deng , J Dai , S Shao . (2019). Oxygen-containing functional groups on bioelectrode surface enhance expression of c-type cytochromes in biofilm and boost extracellular electron transfer. Bioresource Technology, 292: 121995 https://doi.org/10.1016/j.biortech.2019.121995
9	P Li , J Wang , Y Wang , L Dong , W Wang , R Geng , Z Ding , D Luo , D Pan , J Liang . et al.. (2021). Ultrafast recovery of aqueous uranium: photocatalytic U(VI) reduction over cds/g-C3N4. Chemical Engineering Journal, 425: 131552 https://doi.org/10.1016/j.cej.2021.131552
10	J Liu , Y Qiao , Z S Lu , H Song , C M Li . (2012). Enhance electron transfer and performance of microbial fuel cells by perforating the cell membrane. Electrochemistry Communications, 15(1): 50–53 https://doi.org/10.1016/j.elecom.2011.11.018
11	T Liu , J Yuan , B Zhang , W Liu , L Lin , Y Meng , S Yin , C Liu , F Luan . (2019). Removal and recovery of uranium from groundwater using direct electrochemical reduction method: performance and implications. Environmental Science & Technology, 53(24): 14612–14619 https://doi.org/10.1021/acs.est.9b06790
12	D R Lovley . (2017). Electrically conductive pili: biological function and potential applications in electronics. Current Opinion in Electrochemistry, 4(1): 190–198 https://doi.org/10.1016/j.coelec.2017.08.015
13	M Ma , R Wang , L Xu , M Xu , S Liu . (2020). Emerging health risks and underlying toxicological mechanisms of uranium contamination: lessons from the past two decades. Environment International, 145: 106107 https://doi.org/10.1016/j.envint.2020.106107
14	Y Mo , L Sun , L Zhang , J Li , J Li , X Chu , L Wang . (2022). Electrocatalytic biofilm reactor for effective and energy-efficient azo dye degradation: the synergistic effect of MnOx/Ti flow-through anode and biofilm on the cathode. Frontiers of Environmental Science & Engineering, 17(4): 49 https://doi.org/10.1007/s11783-023-1649-5
15	A Paitier , A Godain , D Lyon , N Haddour , T M Vogel , J M Monier . (2017). Microbial fuel cell anodic microbial population dynamics during MFC start-up. Biosensors & Bioelectronics, 92: 357–363 https://doi.org/10.1016/j.bios.2016.10.096
16	R Rhodes . (2017). More nuclear power can speed CO2 cuts. Nature, 548(7667): 281–281 https://doi.org/10.1038/548281d
17	D Sasaki , K Sasaki , Y Tsuge , A Kondo . (2019). Less biomass and intracellular glutamate in anodic biofilms lead to efficient electricity generation by microbial fuel cells. Biotechnology for Biofuels, 12(1): 72 https://doi.org/10.1186/s13068-019-1414-y
18	U Schröder , F Harnisch . (2017). Life electric—nature as a blueprint for the development of microbial electrochemical technologies. Joule, 1(2): 244–252 https://doi.org/10.1016/j.joule.2017.07.010
19	K Tahir , W Miran , J Jang , N Maile , A Shahzad , M Moztahida , A A Ghani , B Kim , D S Lee . (2021). MnCo2O4 coated carbon felt anode for enhanced microbial fuel cell performance. Chemosphere, 265: 129098 https://doi.org/10.1016/j.chemosphere.2020.129098
20	C I Torres , A Kato Marcus , B E Rittmann . (2008). Proton transport inside the biofilm limits electrical current generation by anode-respiring bacteria. Biotechnology and Bioengineering, 100(5): 872–881 https://doi.org/10.1002/bit.21821
21	B Wang , W Zeng , N Li , Y Guo , Q Meng , S Chang , Y Peng . (2020). Insights into the effects of acetate on the community structure of Candidatus Accumulibacter in biological phosphorus removal system using DNA stable-isotope probing (DNA-SIP). Enzyme and Microbial Technology, 139: 109567 https://doi.org/10.1016/j.enzmictec.2020.109567
22	J Wang , S Zhuang . (2019). Extraction and adsorption of U(VI) from aqueous solution using affinity ligand-based technologies: an overview. Reviews in Environmental Science and Biotechnology, 18(3): 437–452 https://doi.org/10.1007/s11157-019-09507-y
23	Y H Wang , B S Wang , Y P Liu , Q Y Chen . (2013). Electricity and hydrogen co-production from a bio-electrochemical cell with acetate substrate. International Journal of Hydrogen Energy, 38(16): 6600–6606 https://doi.org/10.1016/j.ijhydene.2013.03.043
24	Y Yan , X Wang . (2021). Integrated energy view of wastewater treatment: a potential of electrochemical biodegradation. Frontiers of Environmental Science & Engineering, 16(4): 52 https://doi.org/10.1007/s11783-021-1486-3
25	G Yang , L Huang , Z Yu , X Liu , S Chen , J Zeng , S Zhou , L Zhuang . (2019). Anode potentials regulate Geobacter biofilms: new insights from the composition and spatial structure of extracellular polymeric substances. Water Research, 159: 294–301 https://doi.org/10.1016/j.watres.2019.05.027
26	K Yang , Y Zhao , X Zhou , Q Wang , T H Pedersen , Z Jia , J Cabrera , M Ji . (2021). “Self-degradation” of 2-chlorophenol in a sequential cathode-anode cascade mode bioelectrochemical system. Water Research, 206: 117740 https://doi.org/10.1016/j.watres.2021.117740
27	Y YangJ WangJ ZhuT (2015) Zhang. Electricity generation by urban black smelly river sediment-MFC and the effect on sediment remediation. Acta Ecologica Sinica, 24(3): 463−468 (in Chinese)
28	Y Ye , B Fan , Z Qin , X Tang , Y Feng , M Lv , S Miao , H Li , Y Chen , F Chen . et al.. (2022). Electrochemical removal and recovery of uranium: effects of operation conditions, mechanisms, and implications. Journal of Hazardous Materials, 432: 128723 https://doi.org/10.1016/j.jhazmat.2022.128723
29	Y Ye , J Jin , Y Liang , Z Qin , X Tang , Y Feng , M Lv , S Miao , C Li , Y Chen . et al.. (2021). Efficient and durable uranium extraction from uranium mine tailings seepage water via a photoelectrochemical method. iScience, 24(11): 103230 https://doi.org/10.1016/j.isci.2021.103230
30	K Yuan , E S Ilton , M R Antonio , Z Li , P J Cook , U Becker . (2015). Electrochemical and spectroscopic evidence on the one-electron reduction of U(VI) to U(V) on magnetite. Environmental Science & Technology, 49(10): 6206–6213 https://doi.org/10.1021/acs.est.5b00025
31	Y Yuan , W Yin , Y Huang , A Feng , T Chen , L Qiao , H Cheng , W Liu , Z Li , C Ding . et al.. (2023). Intermittent electric field stimulated reduction-oxidation coupled process for enhanced azo dye biodegradation. Chemical Engineering Journal, 451: 138732 https://doi.org/10.1016/j.cej.2022.138732
32	Y Yuan , Q Yu , M Cao , L Feng , S Feng , T Liu , T Feng , B Yan , Z Guo , N Wang . (2021). Selective extraction of uranium from seawater with biofouling-resistant polymeric peptide. Nature Sustainability, 4(8): 708–714 https://doi.org/10.1038/s41893-021-00709-3
33	B S Zakaria , L Lin , B R Dhar . (2019). Shift of biofilm and suspended bacterial communities with changes in anode potential in a microbial electrolysis cell treating primary sludge. Science of the Total Environment, 689: 691–699 https://doi.org/10.1016/j.scitotenv.2019.06.519
34	S Zhang , H L Song , X L Yang , X Z Long , X Liu , T Q Chen . (2017). Behavior of tetracycline and sulfamethoxazole and their corresponding resistance genes in three-dimensional biofilm-electrode reactors with low current. Journal of Environmental Science and Health. Part A, Toxic/Hazardous Substances & Environmental Engineering, 52(4): 333–340 https://doi.org/10.1080/10934529.2016.1258870
35	C Zhao , Y Wang , M Cheng , H Zhang , Y Yang , N Liu , J Liao . (2022). Performance and mechanism of anaerobic granular sludge enhancing uranium immobilization via extracellular polymeric substances in column reactors and batch experiments. Journal of Cleaner Production, 363: 132517 https://doi.org/10.1016/j.jclepro.2022.132517
36	H Zhao , C H Kong . (2018). Enhanced removal of p-nitrophenol in a microbial fuel cell after long-term operation and the catabolic versatility of its microbial community. Chemical Engineering Journal, 339: 424–431 https://doi.org/10.1016/j.cej.2018.01.158
37	J Zhao , F Li , Y Cao , X Zhang , T Chen , H Song , Z Wang . (2021). Microbial extracellular electron transfer and strategies for engineering electroactive microorganisms. Biotechnology Advances, 53: 107682 https://doi.org/10.1016/j.biotechadv.2020.107682

[1]

FSE-23057-OF-TX_suppl_1

Download

Viewed

Full text

Abstract

Cited

Shared

Discussed