In-situ bioremediation of acidic uranium-contaminated groundwater: Development and challenges

doi:10.13745/j.esf.sf.2025.10.36

Abstract

Abstract:

Acidic uranium-contaminated groundwater represents a significant and urgent environmental issue worldwide. Due to its cost-effectiveness and sustainability, in situ bioremediation has emerged as a promising mitigation strategy. This review systematically analyzes the technical principles, existing challenges, and future directions for in situ bioremediation of this environmental challenge. We begin by tracing the genesis of acidic uranium-contaminated water from uranium mining and milling activities, elucidating microbial reduction mechanisms, and outlining the evolution of in situ remediation technologies. Key uranium immobilization mechanisms - including bioreduction (the core pathway), biomineralization (for stable sequestration), biosorption (enabling rapid retention), and bioaccumulation (with resource recovery potential - are critically examined. This review also analyzes critical constraints such as extreme acidity (pH<4.0), the presence of competitive electron acceptors (e.g., nitrate), oligotrophic conditions, dynamic microbial community succession, and the stability risks of U(IV), proposing targeted countermeasures for each. Future research should prioritize: (1) developing self-adaptive microbial consortia, (2) enhancing long-term stability through the promotion of crystalline U(IV) phases, and (3) establishing synergistic systems that integrate multiple mechanisms (e.g., bio-chemical coupling and smart electron donor delivery). These innovations are crucial for advancing the efficacy and longevity of in situ bioremediation in complex acidic environments.

Key words: uranium contamination, acid groundwater, in situ bioremediation, uranium immobilization mechanisms, challenges

CLC Number:

X523

LIU Yajie, LI Jiang, WANG Xuegang, KE Pingchao, SUN Zhanxue. In-situ bioremediation of acidic uranium-contaminated groundwater: Development and challenges[J]. Earth Science Frontiers, 2026, 33(1): 250-268.

Figures/Tables 7

References 164

[1]	ILAKNOON I M S K, TANG Y, GHORBANI Y, et al. The current state and future directions of percolation leaching in the Chinese mining industry: challenges and opportunities[J]. Minerals Engineering, 2018, 125: 206-222. DOI URL
[2]	HAGUE N, NORGATE T. The greenhouse gas footprint of in-situ leaching of uranium, gold and copper in Australia[J]. Journal of Cleaner Production, 2014, 84: 382-390. DOI URL
[3]	WORLD NUCLEAR ASSOCIATION. World uranium mining report[R]. Viena, OECD-NEA & IAEA, Uranium 2024: Resources, Production and Demand (‘Red Book’)
[4]	ZHOU Y P, LI G R, XU L L, et al. Uranium recovery from sandstone-type uranium deposit by acid in-situ leaching: an example from the Kujieertai[J]. Hydrometallurgy, 2020, 191: 105215. DOI URL
[5]	CHENG Y Z, HU X Y, KONG Y L, et al. Imaging acidic contaminants in a confined aquifer using electromagnetic geophysical method constrained by hydrochemical data[J]. Journal of Hydrology, 2022, 609: 127867.
[6]	ZHU F F, ZHAO B, MIN W W, et al. Characteristics of groundwater microbial communities and the correlation with the environmental factors in a decommissioned acid in-situ uranium mine[J]. Frontiers in Microbiology, 2023, 13: 1125421.
[7]	CORAL T, PLACKO A, BEAUFORT D, et al. Biostimulation as a sustainable solution for acid neutralization and uranium immobilization post acidic in-situ recovery[J]. Science of the Total Environment, 2022, 822: 153597. DOI URL
[8]	PEREIRA R, ANTUNES S C, MARQUES S M, et al. Contribution for tier 1 of the ecological risk assessment of Cunha Baixa uranium mine (Central Portugal): I soil chemical characterization[J]. Science of the Total Environment, 2008, 390: 377-386. PMID
[9]	CORAL T, DESCOSTES M, DE BOISSEZON H, et al. Microbial communities associated with uranium in-situ recovery mining process are related to acid mine drainage assemblages[J]. Science of the Total Environment, 2018, 628-629: 26-35.
[10]	MAGALHÃES S M C, FERREIRA JORGE R M, CASTRO P M L. Investigations into the application of a combination of bioventing and biotrickling filter technologies for soil decontamination processes: a transition regime between bioventing and soil vapour extraction[J]. Journal of Hazardous Materials, 2009, 170(2/3): 711-715. DOI URL
[11]	LUO Q S, WANG H, ZHANG X H, et al. In situ bioelectrokinetic remediation of phenol-contaminated soil by use of an electrode matrix and a rotational operation mode[J]. Chemosphere, 2006, 24: 415-422.
[12]	WU W M, CARLEY J, GENTRY T, et al. Pilot-Scale in situ bioremediation of uranium in a highly contaminated aquifer. 1. Conditioning of a treatment zone[J]. Environmental Science & Technology, 2006, 40: 3978-3985. DOI URL
[13]	WU W M, CARLEY J, LUO J, et al. In situ bioreduction of uranium (VI) to submicromolar levels and reoxidation by dissolved oxygen[J]. Environmental Science & Technology, 2007, 41(16): 5716-5723. DOI URL
[14]	HWANG C, WU W M, GENTRY T J, et al. Bacterial community succession during in situ uranium bioremediation: spatial similarities along controlled flow paths[J]. The ISME Journal, 2009, 3: 47-64. DOI URL
[15]	GANDHI T P, SAMPATH P V, MALIYEKKA S M. A critical review of uranium contamination in groundwater: treatment and sludge disposal[J]. Science of the Total Environment, 2022, 825: 153947. DOI URL
[16]	HERRERO M, STUCKEY D C. Bioaugmentation and its application in wastewater treatment: a review[J]. Chemosphere, 2015, 140: 119-128. DOI PMID
[17]	FERNANDO W A M, ILANKOON I, SYED T H, et al. Challenges and opportunities in the removal of sulphate ions in contaminated mine water: a review[J]. Minerals Engineering, 2018, 117: 74-90. DOI URL
[18]	孙占学, 马文洁, 刘亚洁, 等. 地浸采铀矿山地下水环境修复研究进展[J]. 地学前缘, 2021, 28(5): 215-225. DOI
[19]	THAKUR A, KUMAR A. Emerging paradigms into bioremediation approaches for nuclear contaminant removal: from challenge to solution[J]. Chemosphere, 2024, 352: 141369. DOI URL
[20]	SANCHEZ-CASTRO I, MARTINEZ-RODRIGUEZ P, JROUNDI F, et al. High-efficient microbial immobilization of solved U(VI) by the Stenotrophomonas strain Br8[J]. Water Research, 2020, 183: 116110. DOI URL
[21]	MACGREGOR A A. Recovery of U by underground leaching[J]. CIM Bulletin, 1966, 59(654): 583-587.
[22]	MCCREADY R G L, GOULD W D. Bioleaching of uranium[M]. New York: McGraw-Hill, 1990: 107-125.
[23]	CAMERON J. Discussion on natural leaching of uranium ores[J]. Transactions of the Institution of Mining and Metallurgy, 1963, 72: 52-56.
[24]	SHEWAN D M. Pseudomonas putrefaciens in fish spoilage[J]. Journal of Bacteriology, 1931, 22(2): 89-97.
[25]	MACDONELL M T, COLWELL R R. Proposal to recognize Shewanella gen. nov. for Alteromonas putrefaciens and related species[J]. International Journal of Systematic Bacteriology, 1983, 35(1): 223-224. DOI URL
[26]	SHEWAN J M. The bacteriology of fresh and spoiling fish and the biochemical changes induced by bacterial action[C]// Proceedings of the Conference on Handling, Processing and Marketing of Tropical Fish. London: Tropical Products Institute, 1977: 51-66.
[27]	JORGENSEN B R, HUB H H. Growth and activity of Shewanella putrefaciens isolated from spoiling fish[J]. International Journal of Food Microbiology, 1989, 9: 51-62. DOI URL
[28]	PETROVSKIS E A, VOGEL T M, ADRIAENS P. Effects of electron acceptors and donors on transformation of tetrachloromethane by Shewanella putrefaciens MR-1[J]. FEMS Microbiology Letters, 1994, 121(3): 57-63.
[29]	POSTGATE J R, CAMPBELL L L. Identified coleman’s sulfate-reducing bacterium as a mesophilic relative of Clostridium nigrificans[J]. Journal of Bacteriology, 1963, 86(2): 274-279. DOI URL
[30]	KARNACHUK O V, KURGANSKAYA I A, AVAKYAN M R, et al. An acidophilic Desulfosporosinus isolated from the oxidized mining wastes in the Transbaikal area[J]. Microbiology, 2015, 84: 677-686. DOI URL
[31]	WIDDEL F, PFENNIG N. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. I. Isolation of new sulfate-reducing bacteria enriched with acetate from saline environments. Description of Desulfobacter postgatei gen. nov., sp. nov.[J]. Archives of Microbiology, 1981, 129(5): 395-400. DOI URL
[32]	LOVLEY D R, GIOVANNONI S J, WHITE D C, et al. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals[J]. Archives of Microbiology, 1993, 159(4): 336-344. DOI URL
[33]	MUYZER G, STAMS A J M. The ecology and biotechnology of sulphate-reducing bacteria[J]. Nature Reviews Microbiology, 2008, 6(6): 441-454. DOI PMID
[34]	BADZIONG W, THAUER R K. Growth yields and growth rates of Desulfovibrio vulgaris (Marburg) growing on hydrogen plus sulfate and hydrogen plus thiosulfate as the sole energy sources[J]. Archives of Microbiology, 1978, 117(2): 209-214. DOI URL
[35]	CACCAVO F J R, LONERGAN D J, LOVLEY D R, et al. Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism[J]. Applied and Environmental Microbiology, 1994, 60(10): 3752-3759. DOI URL
[36]	LOVLEY D R, PHILLIPS E J P. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese[J]. Applied and Environmental Microbiology, 1988, 54(6): 1472-1480. DOI PMID
[37]	LOVLEY D R, PHILLIPS E J P. Requirement for a microbial consortium to completely oxidize glucose in Fe(Ⅲ)-reducing sediments[J]. Applied and Environmental Microbiology, 1989, 55(12): 3234-3236. DOI URL
[38]	FREDRICKSON J K, ZACHARA J M, KENNEDY D W, et al. Influence of Mn oxides on the reduction of uranium(VI) by the metal-reducing bacterium Shewanella putrefaciens[J]. Geochimica et Cosmochimica Acta, 2002, 66(18): 3247-3262. DOI URL
[39]	CACCAVO F Jr, BLAKEMORE R P, LOVLEY D R. A hydrogen-oxidizing, Fe(Ⅲ)-reducing microorganism from the Great Bay Estuary, New Hampshire[J]. Applied and Environmental Microbiology, 1992, 58(10): 3211-3216. DOI URL
[40]	BACKHUS D A, PICARDAL F W, JOHNSON S, et al. Soil and surfactant-enhanced reductive dechlorination of carbon tetrachloride in the presence of Shewanella putrefaciens 200[J]. Journal of Contaminant Hydrology, 1997, 28: 337-361. DOI URL
[41]	BLUM J S, BINDI A B, BUZZELLI J, et al. Bacillus arsenicoselenatis, sp. nov., and Bacillus selenitireducens, sp. nov.: two haloalkaliphiles from Mono Lake, California that respire oxyanions of selenium and arsenic[J]. Archives of Microbiology, 1998, 171(1): 19-30. DOI URL
[42]	FRANCIS A J, DODGE C, CHENDRAYAN K, et al. Microbial recovery of uranium from solutions[P]. US Patent US4758345A, 1988-07-19.
[43]	HUBER R, KRISTJANSSON J K, STETTER K O. Pyrobaculum gen. nov., a new genus of neutrophilic, rod-shaped archaebacteria from continental solfataras growing optimally at 100℃[J]. International Journal of Systematic Bacteriology, 1987, 37: 197.
[44]	KIEFT T L, FREDRICKSON J K, ONSTOTT T C, et al. Dissimilatory reduction of Fe(Ⅲ) and other electron acceptors by a Thermus Isolate[J]. Applied and Environmental Microbiology, 1999, 65: 1214-1221. DOI URL
[45]	SLOBODKIN A, REYSENBACH A L, STRUTZ N, et al. Thermoterrabacterium ferrireducens gen. nov., sp. nov., a thermophilic anaerobic dissimilatory Fe(Ⅲ)-reducing bacterium from a continental hot spring[J]. International Journal of Systematic Bacteriology, 1997, 47: 541-547. DOI URL
[46]	LOVLEY D R, STOLZ J F, NORD G L, et al. Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism[J]. Nature, 1987, 330: 252-254. DOI
[47]	LOVLEY D R, PHILLIPS E J P, LONERGAN D J. Hydrogen and formate oxidation coupled to dissimilatory reduction of iron or manganese by Alteromonas putrefaciens[J]. Applied and Environmental Microbiology, 1989, 55: 700-706. DOI URL
[48]	石文静, 刘轶哲, 徐浩然, 等. 乌梁素海铁还原微生物对砷-磷迁移转化的影响[J]. 环境科学, 2025, 45(3): 1612-1622.
[49]	LOVLEY D R, CHAPELLE F H, PHILLIPS E J P, et al. Fe(Ⅲ)-reducing bacteria in deeply buried sediments of the Atlantic Coastal Plain[J]. Geology, 1990, 18: 954-957. DOI URL
[50]	LOVLEY D R, PHILLIPS E J P, GORBY Y A, et al. Microbial reduction of uranium[J]. Nature, 1991, 350: 413-416. DOI
[51]	LLOYD J R, RIDLEY J, KHIZNIAK T, et al. Reduction of technetium by Desulfovibrio desulfuricans: biocatalyst characterization and use in a flowthrough bioreactor[J]. Applied and Environmental Microbiology, 1999, 65: 2691-2696. DOI URL
[52]	KASHEFI K, LOVLEY D R. Reduction of Fe(Ⅲ) and toxic and radioactive metals by Pyrobaculum species[J]. Applied and Environmental Microbiology, 2000, 66: 1050-1056. DOI URL
[53]	LOVLEY D R, HOLMES D E, NEVIN K P. Dissimilatory Fe(Ⅲ) and Mn(IV) reduction[J]. Advances in Microbial Physiology, 2004, 49: 219-286.
[54]	GORBY Y A, LOVLEY D R. Enzymatic uranium precipitation[J]. Environmental Science & Technology, 1992, 26: 205-207. DOI URL
[55]	LOVLEY D R, CHAPELLE F H. Deep subsurface microbial processes[J]. Reviews of Geophysics, 1995, 33: 365-381.
[56]	FINNERAN K T, HOUSEWRIGHT M E, LOVLEY D R. Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments[J]. Environmental Microbiology, 2002, 4(9): 510-516. PMID
[57]	BOND D R, HOLMES D E, TENDER L M, et al. Electrode-reducing microorganisms that harvest energy from marine sediments[J]. Science, 2002, 295(5554): 483-485. DOI PMID
[58]	SUZUKI Y, KELLY S D, KEMNER K M, et al. Nanometre-size products of uranium bioreduction[J]. Nature, 2002, 419: 134-137. DOI
[59]	OHNUKI T, AOYAGI H, KITATSUJI Y, et al. Plutonium(VI) accumulation and reduction by lichen biomass: correlation with U(VI)[J]. Journal of Environmental Radioactivity, 2004, 77(3): 339-353. PMID
[60]	KAKSONEN A H, PLUMB J J, FRANZMANN P D, et al. Simple organic electron donors support diverse sulfate-reducing communities in fluidized-bed reactors treating acidic metal- and sulfate-containing wastewater[J]. FEMS Microbiology Ecology, 2004, 47(3): 279-289. DOI PMID
[61]	ANDERSON R T, VRIONIS H A, ORTIZ-BERNAD I, et al. Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer[J]. Applied and Environmental Microbiology, 2003, 69: 5884-5891. DOI URL
[62]	ISTOK J D, SENKO J M, KRUMHOLZ L R, et al. In situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer[J]. Environmental Science & Technology, 2004, 38(2): 468-475. DOI URL
[63]	YABUSAKI S B, FANG Y, LONG P E, et al. Uranium removal from groundwater via in situ biostimulation: field-scale modeling of transport and biological processes[J]. Journal of Contaminant Hydrology, 2007, 93(1/2/3/4): 216-235. DOI URL
[64]	VRIONIS H A, ANDERSON R T, ORTIZ-BERNAD I, et al. Microbiological and geochemical heterogeneity in an in situ uranium bioremediation field site[J]. Applied and Environmental Microbiology, 2005, 71(10): 6308-6318. PMID
[65]	FANG Y, YABUSAKI S B, YEH G T. A general simulator for reaction-based biogeochemical processes[J]. Computers & Geosciences, 2006, 32(1): 64-72. DOI URL
[66]	DEVLIN J F, KATIC D, BARKER J F. In situ sequenced bioremediation of mixed contaminants in groundwater[J]. Journal of Contaminant Hydrology, 2004, 69(3-4): 233-261. PMID
[67]	RAY A E, BARGAR J R, SIVASWAMY V, et al. Evidence for multiple modes of uranium immobilization by an anaerobic bacterium[J]. Geochimica et Cosmochimica Acta, 2011, 75(10): 2684-2695. DOI URL
[68]	SPRING S, ROSENZWEIG F. The genera Desulfitobacterium and Desulfosporosinus: taxonomy[J]. The Prokaryotes, 2006: 771-786.
[69]	LLOYD J R, KLESSA D A, PARRY D L, et al. Stimulation of microbial sulphate reduction in a constructed wetland: microbiological and geochemical analysis[J]. Water Research, 2004, 38(7): 1822-1830. PMID
[70]	LLOYD J R. Bioremediation of metals: application of micro-organisms that make and break minerals[J]. Microbiology Today, 2002, 29: 67-69.
[71]	WANG G H, SONG J, ZHANG Z Y, et al. Enhanced indigenous consortia for the remediation of uranium-contaminated groundwater by bioaugmentation: reducing and phosphate-solubilizing consortia[J]. Science of the Total Environment, 2022, 912: 168954. DOI URL
[72]	LIAN G X, AN Y F, SUN J, et al. Effects and driving mechanisms of bioremediation on groundwater after the neutral in situ leaching of uranium[J]. Science of the Total Environment, 2024, 946: 174406. DOI URL
[73]	WANG Y D, YI H T, LI G Y, et al. Influence of enriched nitrate reducing bacteria communities on bacterial community structure and groundwater condition during in situ bioremediation of nitrate in acidic uranium-contaminated groundwater[J]. Science of the Total Environment, 2025, 958: 177896. DOI URL
[74]	FRANCIS A J, DODGE C J, LU F, et al. XPS and XANES studies of uranium reduction by Clostridium sp.[J]. Environmental Science & Technology, 1994, 28(4): 636-639. DOI URL
[75]	BADER M, MÜLLER K, FOERSTENDORF H, et al. Multistage bioassociation of uranium onto an extremely halophilic archaeon revealed by a unique combination of spectroscopic and microscopic techniques[J]. Journal of Hazardous Materials, 2017, 327: 225-232. DOI PMID
[76]	董海良, 曾强, 刘邓, 等. 黏土矿物微生物相互作用机理以及在环境领域中的应用[J]. 地学前缘, 2024, 31(1): 467-485. DOI
[77]	YU Q H, YUAN Y H, FENG L J, et al. Highly efficient immobilization of environmental uranium contamination with Pseudomonas stutzeri by biosorption, biomineralization, and bioreduction[J]. Journal of Hazardous Materials, 2022, 424: 127758. DOI URL
[78]	YOU W B, PENG W T, TIAN Z C, et al. Uranium bioremediation with U(VI)-reducing bacteria[J]. Science of the Total Environment, 2021, 798: 149107. DOI URL
[79]	CORAL T, PLACKO A L, BEAUFORT D, et al. Biostimulation as a sustainable solution for acid neutralization and uranium immobilization post acidic in-situ recovery[J]. Science of the Total Environment, 2022, 822: 153597. DOI URL
[80]	ZHOU L, HOU S Y, DUAN X Q, et al. New insights into uranium biomineralization mediated by Pseudomonas sp. WG2-6 in the presence of organic phosphorus: promoting effect of extracellular polymeric substance and formation of U-P nanominerals[J]. Journal of Hazardous Materials, 2024, 480: 136123. DOI URL
[81]	CHOUDHARY S, SAR P. Uranium biomineralization by a metal resistant Pseudomonas aeruginosa strain isolated from contaminated mine waste[J]. Journal of Hazardous Materials, 2011, 186: 336-343. DOI URL
[82]	ZHANG K Y, CAI C L, TANG C, et al. Surface adsorption and bioreduction of uranium in low-concentration uranium-containing wastewater induced by Jonesia quinghaiensis ZFSY-01[J]. Journal of Water Process Engineering, 2025, 70: 107062. DOI URL
[83]	DALLA VECCHIA E, VEERAMANI H, SUVOROVA E I, et al. U(VI) reduction by spores of Clostridium acetobutylicum[J]. Research in Microbiology, 2010, 161(9): 765-771. DOI URL
[84]	JIMENEZ-LOPEZ A, NEAL A L, PEREZ-GONZALEZ T, et al. Magnetite biomineralization induced by Shewanella oneidensis[J]. Geochimica et Cosmochimica Acta, 2010, 74(3): 967-979. DOI URL
[85]	BEAZLEY M J, MARTINEZ R J, SOBECKY P A, et al. Uranium biomineralization as a result of bacterial phosphatase activity: insights from bacterial isolates from a contaminated subsurface[J]. Environmental Science & Technology, 2007, 41(16): 5701-5707. DOI URL
[86]	GERBER U, ZIRNSTEIN I, KRAWCZYK-BÄRSCH E, et al. Combined use of flow cytometry and microscopy to study the interactions between the gram-negative beta-proteobacterium Acidovorax facilis and uranium(VI)[J]. Journal of Hazardous Materials, 2016, 317: 127-134. DOI URL
[87]	WANG T S, ZHENG X Y, WANG X Y, et al. Different biosorption mechanisms of Uranium(VI) by live and heat-killed Saccharomyces cerevisiae under environmentally relevant conditions[J]. Journal of Environmental Radioactivity, 2017, 167: 92-99. DOI URL
[88]	DING L, TAN W F, XIE S B, et al. Uranium adsorption and subsequent re-oxidation under aerobic conditions by Leifsonia sp.-Coated biochar as green trapping agent[J]. Environmental Pollution, 2018, 242: 778-787. DOI URL
[89]	GERBER U, HÜBNER R, ROSSBERG A, et al. Metabolism-dependent bioaccumulation of uranium by Rhodosporidium toruloides isolated from the flooding water of a former uranium mine[J]. PLoS ONE, 2018, 13(8): e0201903. DOI URL
[90]	WILLIAMS K H, BARGAR J R, LLOYD J R, et al. Bioremediation of uranium-contaminated groundwater: a systems approach to subsurface biogeochemistry[J]. Current Opinion in Biotechnology, 2013, 24(3): 489-497. DOI PMID
[91]	BANALA U K, DAS N P I, TOLETI S R. Microbial interactions with uranium: towards an effective bioremediation approach[J]. Environmental Technology & Innovation, 2021, 21: 101254.
[92]	MOLINAS M, MEIBOM K L, FAIZOVA R, et al. Mechanism of reduction of aqueous U(V)-dpaea and solid-phase U(VI)-dpaea complexes: the role of multiheme c type cytochromes[J]. Environmental Science & Technology, 2023, 57(19): 7537-7546. DOI URL
[93]	CHEN S Z, GONG J Y, CHENG Y X, et al. The biochemical behavior and mechanism of uranium (VI) bioreduction induced by natural Bacillus thuringiensis[J]. Journal of Environmental Sciences, 2024, 136: 372-381. DOI URL
[94]	LOVLEY D R, PHILLIPS E J P. Reduction of uranium by Desulfovibrio desulfuricans[J]. Applied and Environmental Microbiology, 1992, 58(1): 85-88. DOI URL
[95]	BADZIONG W, THAUER R K. Growth yields and growth rates of Desulfovibrio vulgaris (Marburg) growing on hydrogen plus sulfate and hydrogen plus thiosulfate as the sole energy sources[J]. Archives of Microbiology, 1978, 117(2): 209-214. DOI URL
[96]	SENKO J M, ISTOK J D, SUFLITA J M, et al. In-situ evidence for uranium immobilization and remobilization[J]. Environmental Science & Technology, 2002, 36(7): 1491-1496. DOI URL
[97]	ZENG Q, ZHU T, WEN Y F, et al. The dynamic behavior and mechanism of uranium (VI) biomineralization in Enterobacter sp. X57[J]. Chemosphere, 2022, 298: 134196. DOI URL
[98]	KORIBANICS N M, TUORTO S J, LOPEZ-CHIAFFARELLI N, et al. Spatial distribution of an uranium-respiring beta-proteobacterium at the Rifle, CO field research site[J]. PLoS ONE, 2015, 10(4): e0123378. DOI URL
[99]	LOVLEY D R. Dissimilatory Fe(Ⅲ) and Mn(IV) reduction[J]. Microbiological Reviews, 1991, 55(2): 259-287. DOI URL
[100]	WILLIAMS K H, LONG P E, DAVIS J A, et al. Acetate availability and its influence on sustainable bioremediation of uranium-contaminated groundwater[J]. Geomicrobiology Journal, 2011, 28(5/6): 519-539. DOI URL
[101]	SPEAR J R, FIGUEROA L A, HONEYMAN B D. Modeling reduction of uranium U(VI) under variable sulfate concentrations by sulfate-reducing bacteria[J]. Applied and Environmental Microbiology, 2000, 66(9): 3711-3721. DOI PMID
[102]	FOX J A, WILLIAMS P M, LONG K H, et al. Speciation and reactivity of uranium products formed during in situ bioremediation in a shallow alluvial aquifer[J]. Environmental Science & Technology, 2014, 48(21): 12842-12850. DOI URL
[103]	LOVLEY D R, COATES J D, BLUNT-HARRIS E L, et al. Humic substances as electron acceptors for microbial respiration[J]. Nature, 1996, 382(6590): 446-448.
[104]	LLOYD J R, LEANG C, MYERSON A L H, et al. Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens[J]. Biochemical Journal, 2003, 369(1): 153-161. DOI URL
[105]	张琳琳, 刘亚洁, 陈诗怡, 等. 果皮发酵液为碳源的硫酸盐还原性与酸性含铀废水处理效果[J]. 有色金属(冶炼部分), 2022(6): 74-82.
[106]	赵瑜婷, 陈宏亮, 陈新, 等. 一株硫酸盐还原菌脱硫性能及复合菌强化研究[J]. 有色金属(冶炼部分), 2025, 5: 145-153.
[107]	MORRISON K D, ZAVARIN M, KERSTING A B, et al. Influence of Uranium Concentration and pH on U-Phosphate Biomineralization by Caulobacter OR37[J]. Environmental Science & Technology, 2021, 55(3): 1626-1636. DOI URL
[108]	DEO R, SONGKASIRI W, RITTMANN B, et al. Surface complexation of neptunium(V) onto whole cells and cell components of Shewanella alga: modeling and experimental study[J]. Environmental Science & Technology, 2010, 44(13): 4930-4935. DOI URL
[109]	HUANG W, NIE X, DONG F, et al. Kinetics and pH-dependent uranium bioprecipitation by Shewanella putrefaciens under aerobic conditions[J]. Journal of Radioanalytical and Nuclear Chemistry, 2017, 312(3): 531-541. DOI URL
[110]	ZHAO X, DO H, ZHOU Y, et al. Rahnella sp. LRP3 induces phosphate precipitation of Cu(II) and its role in copper-contaminated soil remediation[J]. Journal of Hazardous Materials, 2019, 368: 133-140. DOI URL
[111]	NIE X Q, LIN Q Y, DONG F Q, et al. Surface biomineralization of uranium onto Shewanella putrefaciens with or without extracellular polymeric substances[J]. Ecotoxicology and Environmental Safety, 2022, 241: 113719. DOI URL
[112]	KHARE D, ACHARYA C. Uranium biomineralization by immobilized Chryseobacterium sp. strain PMSZPI cells for efficient uranium removal[J]. Journal of Hazardous Materials, 2024, 465: 133503. DOI URL
[113]	HE J, HONG Y B, XIAO Q Q, et al. Fate and behavior of uranium biomineralization by the native Burkholderia sp. S1 isolated from tailing areas[J]. Journal of Environmental Chemical Engineering, 2025, 13(3): 116602. DOI URL
[114]	寸金芝, 彭雷, 庞超, 等. 含磷化合物生物矿化铀的形态转化与机理[J]. 南华大学(自然科学版), 2023, 37(5): 9-14.
[115]	YUNG M C, JIAO Y Q. Biomineralization of uranium by PhoY phosphatase activity aids cell survival in Caulobacter crescentus[J]. Applied and Environmental Microbiology, 2014, 80(16): 4795-4804. DOI URL
[116]	LI Z L, LI S F, WANG A J, et al. Extracellular electron transfer-dependent bioremediation of uranium-contaminated groundwater: advancements and challenges[J]. Water Research, 2025, 272: 122957. DOI URL
[117]	LONG P E, WILLIAMS K H, DAVIS J A, et al. Bicarbonate impact on U(VI) bioreduction in a shallow alluvial aquifer[J]. Geochimica et Cosmochimica Acta, 2015, 150: 106-124. DOI URL
[118]	DUAN Y T, XU X, NIU L, et al. Study on the mechanism and stability of microbially induced struvite precipitation (MISP) for enhanced immobilization of uranium[J]. Journal of Cleaner Production, 2024, 449: 141536. DOI URL
[119]	SUN J, LI Q, LI T, et al. Insights into formation and dissolution mechanism of bio-ore pellets in the one-step uranium leaching process by Aspergillus niger[J]. Minerals Engineering, 2022, 184: 107672. DOI URL
[120]	BEYENAL H, SANI R K, PEYTON B M, et al. Uranium immobilization by sulfate-reducing biofilms[J]. Environmental Science & Technology, 2004, 38(7): 2067-2074. DOI URL
[121]	WANG X L, LI F X, ZHANG Y K, et al. Mechanism of direct treatment of high concentration uranium using sulfate reducing bacteria[J]. Chemical Engineering Journal, 2025, 520: 166265. DOI URL
[122]	HYUN S P, DAVIS J A, SUN K, et al. Uranium(VI) reduction by iron(II) monosulfide mackinawite[J]. Environmental Science & Technology, 2012, 46(6): 3369-3376. DOI URL
[123]	NEWSOME L, MORRIS K, TRIVEDI D, et al. Biostimulation by glycerol phosphate to precipitate recalcitrant uranium(IV) phosphate[J]. Environmental Science & Technology, 2015, 49(18): 11070-11078. DOI URL
[124]	REITZ T, ROSSBERG A, BARKLEIT A, et al. Decrease of U(VI) immobilization capability of the facultative anaerobic strain Paenibacillus sp. JG-TB8 under anoxic conditions due to strongly reduced phosphatase activity[J]. PLOS ONE, 2014, 9(8): e102447. DOI URL
[125]	HAAS J R, DICHRISTINA T J, JR R W. Thermodynamics of U(VI) sorption onto Shewanella putrefaciens[J]. Chemical Geology, 2001, 180(1/2/3/4): 33-54. DOI URL
[126]	MORCILLO F, GONZALEZ-MUNOZ M T, REITZ T, et al. Biosorption and biomineralization of U(VI) by the marine bacterium Idiomarina loihiensis MAH1: effect of background electrolyte and pH[J]. PLoS ONE, 2014, 9(3): e91305. DOI URL
[127]	BADER M, MUELLER K, FOERSTENDORF H, et al. Comparative analysis of uranium bioassociation with halophilic bacteria and archaea[J]. PLoS ONE, 2018, 13(1): e0190953. DOI URL
[128]	POVEDANO-PRIEGO C, JROUNDI F, LOPEZ-FERNANDEZ M, et al. Shifts in bentonite bacterial community and mineralogy in response to uranium and glycerol-2-phosphate exposure[J]. Science of the Total Environment, 2019, 692: 219-232. DOI URL
[129]	ABOSTATEM A, SALAH Y, HAMED M, et al. Characterization, kinetics and thermodynamics of biosynthesized uranium nanoparticles (UNPs)[J]. Artificial Cells, Nanomedicine, and Biotechnology, 2018, 46(1): 147-159.
[130]	HUSSAIN A, REHMAN F, RAFEEQ H, et al. In-situ, Ex-situ, and nano-remediation strategies to treat polluted soil, water, and air: a review[J]. Chemosphere, 2022, 289: 133252. DOI URL
[131]	ANEKWE I M S, ISA Y M. Comparative evaluation of wastewater and bioventing system for the treatment of acid mine drainage contaminated soils[J]. Water-Energy Nexus, 2021, 4: 134-140. DOI URL
[132]	BOOPATHY R. Factors limiting bioremediation technologies[J]. Bioresource Technology, 2000, 74(1): 63-67. DOI URL
[133]	YANG Z, LIU Z, DABROWSKA M, et al. Biostimulation of sulfate-reducing bacteria used for treatment of hydrometallurgical waste by secondary metabolites of urea decomposition by Ochrobactrum sp. POC9: from genome to microbiome analysis[J]. Chemosphere, 2021, 282: 131064. DOI URL
[134]	LOVLEY D R, CHAPELLE F H, WOODWARD J C. Use of dissolved H₂ concentrations to determine distribution of microbially catalyzed redox reactions in anoxic groundwater[J]. Environmental Science & Technology, 1994, 28(7): 1205-1210. DOI URL
[135]	VETROVA A A, TROFIMOV S Y, KINZHAEV R R, et al. Development of microbial consortium for bioremediation of oil-contaminated soils in the middle Ob region[J]. Eurasian Soil Science, 2022, 55(5): 651-662. DOI
[136]	WANG L, XIE J, CHEN J, et al. Study on the migration pattern of uranium in soil by Deino-ure, a genetically engineered bacterium of Deinococcus radiodurans[J]. Journal of Radioanalytical and Nuclear Chemistry, 2024, 333(8): 4015-4026. DOI
[137]	LI S, ZHU Q, LUO J, et al. Application progress of Deinococcus radiodurans in biological treatment of radioactive uranium-containing wastewater[J]. Indian Journal of Microbiology, 2021, 61(4): 417-426. DOI
[138]	LANGLEY S, GAULT A G, IBRAHIM A, et al. Strontium desorption from bacteriogenic iron oxides (BIOS) subjected to microbial Fe(Ⅲ) reduction[J]. Chemical Geology, 2009, 262(3/4): 217-228. DOI URL
[139]	JOHNSON D B. Extremophiles: acidic environments[M]//Encyclopedia of microbiology. Third Edition. Cambridge, USA: Academic Press, 2009: 107-126.
[140]	KUSHKEVYCH I, DORDEVIĆ D, VÍTĚZOVÁ M. Toxicity of hydrogen sulfide toward sulfate-reducing bacteria Desulfovibrio piger Vib-7[J]. Archives of Microbiology, 2019, 201(3): 389-397.
[141]	JOHNSON D B, JAMESON E, ROWE O, et al. Sulfidogenesis at low pH by acidophilic bacteria and its potential for the selective recovery of transition metals from mine waters[J]. Advanced Materials Research, 2009, 71-73: 693-696. DOI URL
[142]	NANCUCHEO I, BITENCOURT J A, SAHOO P K, et al. Recent developments for remediating acidic mine waters using sulfidogenic bacteria[J]. BioMed Research International, 2017, 2017(1): 7256582.
[143]	ZHOU L, BAI N, XIAO R, et al. Unlocking the bioremediation potential of adapted Desulfovibrio desulfuricans in acidic low-temperature U-contaminated groundwater[J]. Journal of Environmental Sciences, 2025, 155: 303-315. DOI URL
[144]	LIANG Y R, WANG L L, GAO P P, et al. Uranium immobilization by Brevundimonas vesicularis LWG1: a synergistic approach via biomineralization, biosorption, and bioreduction[J]. Journal of Hazardous Materials, 2025, 496: 139236. DOI URL
[145]	HUANG W, NIE X, DONG F, et al. Kinetics and pH-dependent uranium bioprecipitation by Shewanella putrefaciens under aerobic conditions[J]. Journal of Radioanalytical and Nuclear Chemistry, 2017, 312(3): 531-541. DOI URL
[146]	李琛. 尾矿铀及重金属胁迫微生物标识物演替与共生协同分子机制[D]. 绵阳: 西南科技大学, 2024.
[147]	MACASKIE L E, JEONG B C, TOLLEY M R. Enzymically accelerated biomineralization of heavy metals: application to the removal of americium and plutonium from aqueous flows[J]. FEMS Microbiology Reviews, 1994, 14(4): 351-367. PMID
[148]	CHEN A W, SHANG C, SHAO J H, et al. The application of iron-based technologies in uranium remediation: a review[J]. Science of the Total Environment, 2017, 575: 1291-1306. DOI URL
[149]	王继勇, 肖挺, 何伟. 一株耐酸SRB的分离及其脱硫除镉性能[J]. 中国环境科学, 2018, 38(11): 4255-4260.
[150]	YAN L J, KÜSEL K, HERMANS S M, et al. Groundwater bacterial communities evolve over time in response to recharge[J]. Water Research, 2021, 201: 117290. DOI URL
[151]	LIU S F, CHEN Q, LI J R, et al. Different spatiotemporal dynamics, ecological drivers and assembly processes of bacterial, archaeal and fungal communities in brackish-saline groundwater[J]. Water Research, 2022, 214: 118193. DOI URL
[152]	HE Z L, ZHANG P, WU L W, et al. Microbial functional gene diversity predicts groundwater contamination and ecosystem functioning[J]. Microbiology, 2018, 9(1): e02435-17.
[153]	SLABE M O, DANEVCIC T, HUG K, et al. Key drivers of microbial abundance, activity, and diversity in karst spring waters across an altitudinal gradient in Slovenia[J]. Aquatic Microbial Ecology, 2021, 86: 99-114. DOI URL
[154]	JROUNDI F, DESCOSTES M, POVEDANO-PRIEGO C, et al. Profiling native aquifer bacteria in a uranium roll-front deposit and their role in biogeochemical cycle dynamics: insights regarding in situ recovery mining[J]. Science of the Total Environment, 2020, 721: 137758. DOI URL
[155]	JROUNDI F, POVEDANO-PRIEGO C, PINEL-CABELLO M, et al. Evidence of microbial activity in a uranium roll-front deposit: unlocking their potential role as bioenhancers of the ore genesis[J]. Science of the Total Environment, 2023, 861: 160636. DOI URL
[156]	SUZUKI Y, SUKO T. Geomicrobiological factors that control uranium mobility in the environment: update on recent advances in the bioremediation of uranium-contaminated sites[J]. Journal of Mineralogical and Petrological Sciences, 2007, 101(6): 299-307. DOI URL
[157]	WU W M, CARLEY J, GREEN S J, et al. Effects of nitrate on the stability of uranium in a bioreduced region of the subsurface[J]. Environmental Science & Technology, 2010, 44(13): 5104-5111. DOI URL
[158]	CHANDLER D P, KUKHTIN A, MOKHIBER R, et al. Monitoring microbial community structure and dynamics during in situ U(VI) bioremediation with a field-portable microarray analysis system[J]. Environmental Science and Technology, 2010, 44(14): 5516-5522. DOI PMID
[159]	DONG W, BROOKS S C. Determination of the formation constants of ternary complexes of uranyl and carbonate with alkaline earth metals (Mg²⁺, Ca²⁺, Sr²⁺, and Ba²⁺) using anion exchange method[J]. Environmental Science & Technology, 2006, 40(15): 4689-4695. DOI URL
[160]	HYUN S P, FOX P M, DAVIS J A, et al. Surface complexation modeling of U(VI) adsorption on granite at ambient/elevated temperatures[J]. Applied Geochemistry, 2009, 24(7): 1231-1240.
[161]	CURTIS G P, FOX P, KOHLER M, et al. Comparison of in situ uranium KD values with a laboratory determined surface complexation model[J]. Environmental Science & Technology, 2004, 38(14): 3679-3686.
[162]	DAVIS J A, MEECE D E, KOHLER M, et al. Approaches to surface complexation modeling of uranium(VI) adsorption on aquifer sediments[J]. Geochimica et Cosmochimica Acta, 2004, 68(18): 3621-3641. DOI URL
[163]	KOMLOS J, PEACOCK A, KUKKADAPU R K, et al. Long-term dynamics of uranium reduction/reoxidation under low sulfate conditions[J]. Geochimica et Cosmochimica Acta, 2008, 72(15): 3603-3615. DOI URL
[164]	WATSON D B, WU W M, MEHLHORN T, et al. In situ bioremediation of uranium with emulsified vegetable oil as the electron donor[J]. Environmental Science & Technology, 2013, 47(12): 6440-6448. DOI URL

细菌株型	富集分离环境	最适生长条件	代谢特点	参考文献
Desulfosporosinus orientis	发酵液	厌氧,35 ℃,pH 6.5	硫酸盐还原与酸性环境适应性	★[29] ▲[30]
Desulfovibrio baarsii DSM 2075	淡水沉积物	厌氧,37 ℃,pH 7.5	代谢多样性	★[31]
Desulfovibrio desulfuricans ATCC 29577	土壤	厌氧,37 ℃,pH 7.2	铀还原能力	▲[32]
Desulfovibrio sulfodismutans DSM 3696	淡水湖沉积物	厌氧,30 ℃,pH 7.2	硫歧化代谢途径	▲[33]
Desulfovibrio vulgaris Hildenborough ATCC 29579	活性污泥	厌氧,35 ℃,pH 6.8	铀还原能力	★[34]
Geobacter sulfurreducens PCA	海水沉积物	严格厌氧,30 ℃,pH 6.8	直接电子传递	★[35]
Geobacter metallireducens, strain GS-15(ATCC 53774)	美国马里兰州波托马克河沉积物	严格厌氧,30~35 ℃, pH 6.7~7.0	直接电子传递	★[36] ▲[37]
Shewanella putrefaciens (原名:Pseudomonas putrefaciens)	鱼内脏	兼性厌氧,30 ℃,pH 7.0	金属还原+硫代谢	★[24]
Shewanella oneidensis MR-1	奥奈达湖沉积物	好氧/微好氧,30 ℃,pH 7.0		▲[28] *[38]
Shewanella alga BrY	海湾沉积物	兼性厌氧,25 ℃,pH 7.5		★[39]
Shewanella putrefaciens 200	淡水环境	兼性厌氧,30 ℃,pH 7.0		*[40]
Bacillus arsenicoselenatis, E1H	加利福尼亚州莫诺湖淤泥-碱性、高盐度、富含砷的水体	严格厌氧,20 ℃,pH 8.5~10	As还原	*[41]
Bacillus selenitireducens MLS10	加利福尼亚州莫诺湖淤泥-碱性、高盐度、富含砷的水体	微好氧,20 ℃,pH 8.5~10	Se和As还原	*[41]
Clostridium sp. ATCC 53464	土壤样	厌氧,30 ℃,pH 6.8	U还原	*[42]
Pyrobaculum islandicum DSM 4184	地热区	厌氧,100 ℃,pH 7.0	铁还原	▲[43]
Thermus scotoductus SA-01	金矿地下水	兼性厌氧,65 ℃,pH 7.0	铁还原	▲[44]
Thermoterrabacterium ferrireducens DSM 11255	美怀俄明州黄石公园方解石热泉	厌氧,65 ℃,pH 6.0~6.2	铁还原	★[45]

细菌株型	富集分离环境	最适生长条件	代谢特点	参考文献
Desulfosporosinus orientis	发酵液	厌氧,35 ℃,pH 6.5	硫酸盐还原与酸性环境适应性	★[29] ▲[30]
Desulfovibrio baarsii DSM 2075	淡水沉积物	厌氧,37 ℃,pH 7.5	代谢多样性	★[31]
Desulfovibrio desulfuricans ATCC 29577	土壤	厌氧,37 ℃,pH 7.2	铀还原能力	▲[32]
Desulfovibrio sulfodismutans DSM 3696	淡水湖沉积物	厌氧,30 ℃,pH 7.2	硫歧化代谢途径	▲[33]
Desulfovibrio vulgaris Hildenborough ATCC 29579	活性污泥	厌氧,35 ℃,pH 6.8	铀还原能力	★[34]
Geobacter sulfurreducens PCA	海水沉积物	严格厌氧,30 ℃,pH 6.8	直接电子传递	★[35]
Geobacter metallireducens, strain GS-15(ATCC 53774)	美国马里兰州波托马克河沉积物	严格厌氧,30~35 ℃, pH 6.7~7.0	直接电子传递	★[36] ▲[37]
Shewanella putrefaciens (原名:Pseudomonas putrefaciens)	鱼内脏	兼性厌氧,30 ℃,pH 7.0	金属还原+硫代谢	★[24]
Shewanella oneidensis MR-1	奥奈达湖沉积物	好氧/微好氧,30 ℃,pH 7.0		▲[28] *[38]
Shewanella alga BrY	海湾沉积物	兼性厌氧,25 ℃,pH 7.5		★[39]
Shewanella putrefaciens 200	淡水环境	兼性厌氧,30 ℃,pH 7.0		*[40]
Bacillus arsenicoselenatis, E1H	加利福尼亚州莫诺湖淤泥-碱性、高盐度、富含砷的水体	严格厌氧,20 ℃,pH 8.5~10	As还原	*[41]
Bacillus selenitireducens MLS10	加利福尼亚州莫诺湖淤泥-碱性、高盐度、富含砷的水体	微好氧,20 ℃,pH 8.5~10	Se和As还原	*[41]
Clostridium sp. ATCC 53464	土壤样	厌氧,30 ℃,pH 6.8	U还原	*[42]
Pyrobaculum islandicum DSM 4184	地热区	厌氧,100 ℃,pH 7.0	铁还原	▲[43]
Thermus scotoductus SA-01	金矿地下水	兼性厌氧,65 ℃,pH 7.0	铁还原	▲[44]
Thermoterrabacterium ferrireducens DSM 11255	美怀俄明州黄石公园方解石热泉	厌氧,65 ℃,pH 6.0~6.2	铁还原	★[45]

电子供体类型	适用pH范围	铀去除率	优势	限制	数据来源
乳酸钠	4.0~8.0	70%~85%	易生物降解,SRB偏好	酸性条件效率下降	[95]
腐殖酸	3.0~5.5	可变	电子穿梭作用	高浓度抑制(>50 mg/L)	[103]
氢气(MBfR)	2.5~7.0	>90%	无碳添加,抑制杂菌	设备投资高	[104]
苹果皮发酵液	3.5~6.0	88.6%	废物利用,低成本	需预发酵处理	[105]
玉米芯发酵液	3.0~6.0	>99%(低于检测限)	废物利用,低成本	预发酵时间较长	[106]

电子供体类型	适用pH范围	铀去除率	优势	限制	数据来源
乳酸钠	4.0~8.0	70%~85%	易生物降解,SRB偏好	酸性条件效率下降	[95]
腐殖酸	3.0~5.5	可变	电子穿梭作用	高浓度抑制(>50 mg/L)	[103]
氢气(MBfR)	2.5~7.0	>90%	无碳添加,抑制杂菌	设备投资高	[104]
苹果皮发酵液	3.5~6.0	88.6%	废物利用,低成本	需预发酵处理	[105]
玉米芯发酵液	3.0~6.0	>99%(低于检测限)	废物利用,低成本	预发酵时间较长	[106]

细菌种属	沉积物	U固定的pH	参考文献
Brevundimonas vesicularis LWG1	CaU(PO₄)₂	9.4	[139]
Shewanella putrefaciens	H₂-(UO₂)₂(PO₄)₂·8H₂O	5.0	[140]
Clostridium sp.	醋酸铀酰脱水复杂产物	7.2	[141]
Citrobacter sp.	铀酰磷酸化合物	6.9	[142]
Bacillus spp.	钙铀酰碳酸盐	5.0	[91]
Jonesia quinghaiensis ZFSY-01	无机和有机铀酰磷酸化合物(吸附态)	5.0	[143]
Caulobacter crescentus	CaU(PO₄)₂	4.5	[144]
Desulfovibrio desulfuricans	未分析	4.0	[145]
Desulfosporosinus desulfolous	铀酰磷酸化合物	3.5(模拟含矿含水层水平管试验, 生物强化)	作者研究成果, 尚未发表