Phosphorus additives driving the bacterial community succession during Bacillus spp. remediation of the uranium tailings

Abstract

Uranium tailings discharged into uranium tailings ponds could generate environmental pollution issues. Microbial-induced phosphate mineralization could reduce the release of uranium, in turn effectively managing pollution. However, it is unclear that how the phosphorus additives affect the microbial structure of uranium tailings under biomineralization. Herein, we evaluate the microbial community succession during Bacillus spp. remediation of uranium tailings, when adding hydroxyapatite (HS) and β-glycerol phosphate pentahydrate (GP). The results show that phosphorus additives effectively changed pH and uranium leaching concentration, significantly increased bacterial richness, and promoted microbial community succession, whilst promoting actinobacteria to Firmicutes and Proteobacteria populations. The two additives influenced the bacterial community succession patterns differently, with GP eliciting the greater enhancement. Additionally, GP enhanced the growth of core species and recognized the phylum firmicutes as a crucial taxon. The abundance of Bacillus, Pseudomonas, Desulfotomaculum, and Clostridium_sensu_stricto_12 was higher in GP treatments, indicating the substantial roles played by these genera in the microbial community. The results provide evidence of the involvement of the two phosphorus additives in bioremediation and bacterial community perturbations and thus provide new insights into the biomineralization technologies for uranium tailings.

Keywords

biomineralization / hydroxyapatite / microbial community / uranium / β-glycerol phosphate pentahydrate

References

[1] ChenA, ShangC, ShaoJ, et al. . The application of iron-based technologies in uranium remediation: A review [J]. The Science of the Total Environment, 2017, 575: 1291-1306

[2] LakaniemiA M, DouglasG B, KaksonenA H. Engineering and kinetic aspects of bacterial uranium reduction for the remediation of uranium contaminated environments [J]. Journal of Hazardous Materials, 2019, 371: 198-212

[3] XieY, ChenC, RenX, et al. . Emerging natural and tailored materials for uranium-contaminated water treatment and environmental remediation [J]. Progress in Materials Science, 2019, 103: 180-234

[4] WellmanD M, PierceE M, ValentaM M. Efficacy of soluble sodium tripolyphosphate amendments for the in situ immobilisation of uranium [J]. Environmental Chemistry, 2007, 4(5): 293

[5] MehtaV S, MaillotF, WangZ, et al. . Effect of reaction pathway on the extent and mechanism of uranium(VI) immobilization with calcium and phosphate [J]. Environmental Science & Technology, 2016, 5063128-3136

[6] AkashS, SivaprakashB, RajaV C V, et al. . Remediation techniques for uranium removal from polluted environment—Review on methods, mechanism and toxicology [J]. Environmental Pollution, 2022, 302: 119068

[7] HanT, ChenW, CaiY, et al. . Immobilization of uranium during the deposition of carbonated hydroxyapatite [J]. Journal of the Taiwan Institute of Chemical Engineers, 2022, 134104331

[8] TangC, ZhongJ, LyuY, et al. . Research progress of uranium contaminated soil remediation technology [J]. Chemical Industry and Engineering Progress, 2021, 40(8): 4587-4599(in Chinese)

[9] SelvakumarR, RamadossG, MenonM P, et al. . Challenges and complexities in remediation of uranium contaminated soils: A review [J]. Journal of Environmental Radioactivity, 2018, 192592-603

[10] ChengC, ChenL, GuoK, et al. . Progress of uranium-contaminated soil bioremediation technology [J]. Journal of Environmental Radioactivity, 2022, 241: 106773

[11] HuZ, ZhouZ, ZhouY, et al. . Synergy of surface adsorption and intracellular accumulation for removal of uranium with Stenotrophomonas sp: Performance and mechanisms [J]. Environmental Research, 2023, 220115093

[12] BanalaU K, DasN P I, ToletiS R. Microbial interactions with uranium: Towards an effective bioremediation approach [J]. Environmental Technology & Innovation, 2021, 21101254

[13] MkandawireM. Biogeochemical behaviour and bioremediation of uranium in waters of abandoned mines [J]. Environmental Science and Pollution Research, 2013, 20(11): 7740-7767

[14] YouW, PengW, TianZ, et al. . Uranium bioremediation with U(VI) -reducing bacteria [J]. The Science of the Total Environment, 2021, 798149107

[15] HuN, ChenX, ZhangH, et al. . Experimental study on the remediation of low concentration uranium wastewater by Sporosarcina pasteurii induced carbonate-uranium co-precipitation [J]. CIESC Journal, 2021, 72(10): 5354-5361(in Chinese)

[16] TanW, WangY, DingL, et al. . Effects of phosphorus modified bio-char on metals in uranium-containing soil [J]. Water, Air, & Soil Pollution, 2019, 230(2): 35

[17] RaicevicS, WrightJ, VeljkovicV, et al. . Theoretical stability assessment of uranyl phosphates and apatites: Selection of amendments for in situ remediation of uranium [J]. The Science of the Total Environment, 2006, 3551–313-24

[18] ChandwadkarP, MisraH S, AcharyaC. Uranium biomineralization induced by a metal tolerant serratia strain under acid, alkaline and irradiated conditions [J]. Metallomics, 2018, 10(8): 1078-1088

[19] LammersL N, RasmussenH, AdilmanD, et al. . Groundwater uranium stabilization by a metastable hydroxyapatite [J]. Applied Geochemistry, 2017, 84105-113

[20] ChenH, MinF, HuX, et al. . Biochar assists phosphate solubilizing bacteria to resist combined Pb and Cd stress by promoting acid secretion and extracellular electron transfer [J]. Journal of Hazardous Materials, 2023, 452: 131176

[21] TengZ, ZhaoX, YuanJ, et al. . Phosphate functionalized iron based nanomaterials coupled with phosphate solubilizing bacteria as an efficient remediation system to enhance lead passivation in soil [J]. Journal of Hazardous Materials, 2021, 419126433

[22] LiX, DingC, LiaoJ, et al. . Biosorption of uranium on Bacillus sp. dwc-2: Preliminary investigation on mechanism [J]. Journal of Environmental Radioactivity, 2014, 1356-12

[23] MartinezR J, BeazleyM J, TaillefertM, et al. . Aerobic uranium(VI) bioprecipitation by metal-resistant bacteria isolated from radionuclide- and metal-contaminated subsurface soils [J]. Environmental Microbiology, 2007, 9(12): 3122-3133

[24] YongP, MacaskieL E. Enhancement of uranium bioaccumulation by a Citrobacter sp. via enzymically-mediated growth of polycrystalline NH₄UO₂PO₄ [J]. Journal of Chemical Technology & Biotechnology, 1995, 63(2): 101-108

[25] SowmyaS, RekhaP D, ArunA B. Uranium(VI) bioprecipitation mediated by a phosphate solubilizing Acinetobacter sp. YU-SS-SB-29 isolated from a high natural background radiation site [J]. International Biodeterioration & Biodegradation, 2014, 94: 134-140

[26] YuQ, YuanY, FengL, et al. . Highly efficient immobilization of environmental uranium contamination with Pseudomonas stutzeri by biosorption, biomineralization, and bioreduction [J]. Journal of Hazardous Materials D, 2022, 424: 127758

[27] ZengT, MoG, HuQ, et al. . Microbial characteristic and bacterial community assessment of sediment sludge upon uranium exposure [J]. Environmental Pollution, 2020, 261114176

[28] MumtazS, StretenC, ParryD L, et al. . Soil uranium concentration at ranger uranium mine land application areas drives changes in the bacterial community [J]. Journal of Environmental Radioactivity, 2018, 18914-23

[29] MartinezR J, WuC H, BeazleyM J, et al. . Microbial community responses to organophosphate substrate additions in contaminated subsurface sediments [J]. PLoS One, 2014, 9(6): e100383

[30] NewsomeL, MorrisK, TrivediD, et al. . Biostimulation by glycerol phosphate to precipitate recalcitrant uranium(IV) phosphate [J]. Environmental Science & Technology, 2015, 491811070-11078

[31] CrisitinaP, FadwaJ, MargaritaL, et al. . Impact of anoxic conditions, uranium(VI) and organic phosphate substrate on the biogeochemical potential of the indigenous bacterial community of bentonite [J]. Applied Clay Science, 2022, 216: 106331

[32] ZhengL, RenM, XieE, et al. . Roles of phosphorus sources in microbial community assembly for the removal of organic matters and ammonia in activated sludge [J]. Frontiers in Microbiology, 2019, 101023

[33] TangC, ZhongJ, LvY, et al. . Response and dynamic change of microbial community during bioremediation of uranium tailings by bacillus sp. [J]. Minerals, 2021, 11(9): 967

[34] ZhongJ, HuX, LiuX, et al. . Isolation and identification of uranium tolerant phosphate-solubilizing Bacillus spp. and their synergistic strategies to U(VI) immobilization [J]. Frontiers in Microbiology, 2021, 12676391

[35] JinL, JinN, WangS, et al. . Changes in the microbial structure of the root soil and the yield of Chinese baby cabbage by chemical fertilizer reduction with bio-organic fertilizer application [J]. Microbiology Spectrum, 2022, 106e0121522

[36] LiaoR, ShiZ, ChenY, et al. . Characteristics of uranium sorption on illite in a ternary system: Effect of phosphate on adsorption [J]. Journal of Radioanalytical and Nuclear Chemistry, 2020, 3231159-168

[37] KongL, ZhangH, JiW, et al. . Recovery of phosphorus rich krill shell biowaste for uranium immobilization: A study of sorption behavior, surface reaction, and phase transformation [J]. Environmental Pollution A, 2018, 243630-636

[38] VEKATARAMAPPA R, MAHADEV N K, VENKATESH S, et al. Isolation, characterization and identification of multifaceted halotolerant bacillus licheniformis and bacillus wudalianchiensis from rhizospheric soils of Bangalore [J]. Journal of Microbiology, Biotechnology and Food Sciences, 2022: e3553. DOI: https://doi.org/10.55251/jmbfs.3553.

[39] ChenD, LiH, ZhangB, et al. . Phosphate solubilization activities and action mechanisms of two phosphate-solubilizing bacteria [J]. Chinese Journal of Eco-Agriculture, 2017, 25(3): 410-418(in Chinese)

[40] BeazleyM J, MartinezR J, SobeckyP A, et al. . Nonreductive biomineralization of uranium(VI) phosphate via microbial phosphatase activity in anaerobic conditions [J]. Geomicrobiology Journal, 2009, 26(7): 431-441

[41] AmarasingheT, MadhushaC, MunaweeraI, et al. . Review on mechanisms of phosphate solubilization in rock phosphate fertilizer [J]. Communications in Soil Science and Plant Analysis, 2022, 53(8): 944-960

[42] VenkatramananR, PrakashO, WoykeT, et al. . Genome sequences for three denitrifying bacterial strains isolated from a uranium- and nitrate-contaminated subsurface environment [J]. Genome Announcements, 2013, 1(4): e00449-e00413

[43] WanW, HaoX, XingY, et al. . Spatial differences in soil microbial diversity caused by pH-driven organic phosphorus mineralization [J]. Land Degradation & Development, 2021, 32(2): 766-776

[44] ZhangW, SunR, XuL, et al. . Assessment of bacterial communities in Cu-contaminated soil immobilized by a one-time application of micro-/ nano-hydroxyapatite and phytoremediation for 3 years [J]. Chemosphere, 2019, 223: 240-249

[45] WeiL, WangS, ZuoQ, et al. . Nano-hydroxyapatite alleviates the detrimental effects of heavy metals on plant growth and soil microbes in e-waste-contaminated soil [J]. Environmental Science Processes & Impacts, 2016, 18(6): 760-767

[46] LiuS, LiuY, TanX, et al. . The effect of several activated biochars on Cd immobilization and microbial community composition during in situ remediation of heavy metal contaminated sediment [J]. Chemosphere, 2018, 208: 655-664

[47] SharmaP, PandeyA K, KimS H, et al. . Critical review on microbial community during in situ bioremediation of heavy metals from industrial wastewater [J]. Environmental Technology & Innovation, 2021, 24: 101826

[48] SantiniT C, KerrJ L, WarrenL A. Microbially-driven strategies for bioremediation of bauxite residue [J]. Journal of Hazardous Materials, 2015, 293131-157

[49] ShenJ, XuZ, HeJ-zheng. Frontiers in the microbial processes of ammonia oxidation in soils and sediments [J]. Journal of Soils and Sediments, 2014, 14(6): 1023-1029

[50] YangY, LiG, MinK, et al. . The potential role of fertilizer-derived exogenous bacteria on soil bacterial community assemblage and network formation [J]. Chemosphere, 2022, 287(3): 132338

[51] YangH, ZhangY, ChuangS, et al. . Bioaugmentation of acetamiprid-contaminated soil with Pigmentiphaga sp. strain D-2 and its effect on the soil microbial community [J]. Ecotoxicology, 2021, 3081559-1571

[52] CristinaP, FadwaJ, MarM, et al. . Unveiling fungal diversity in uranium and glycerol-2-phosphate-amended bentonite microcosms: Implications for radionuclide immobilization within the Deep Geological Repository system [J]. Science of the Total Environment, 2024, 908: 168284

[53] CristinaP, FadwaJ, MargaritaL, et al. . Shifts in bentonite bacterial community and mineralogy in response to uranium and glycerol-2-phosphate exposure [J]. The Science of the Total Environment, 2019, 692219-232

[54] WangG, LiuY, WangJ, et al. . The remediation of uranium-contaminated groundwater via bioreduction coupled to biomineralization with different pH and electron donors [J]. Environmental Science and Pollution Research International, 2023, 30(9): 23096-23109

[55] LvY, TangC, LiuX, et al. . Optimization of environmental conditions for microbial stabilization of uranium tailings, and the microbial community response [J]. Frontiers in Microbiology, 2021, 12: 770206

[56] LiuH, ChenS, LuJ, et al. . Pentavalent vanadium and hexavalent uranium removal from groundwater by woodchip-sulfur based mixotrophic biotechnology [J]. Chemical Engineering Journal, 2022, 437135313

[57] SuriyaJ, Chandra ShekarM, NathaniN M, et al. . Assessment of bacterial community composition in response to uranium levels in sediment samples of sacred Cauvery River [J]. Applied Microbiology and Biotechnology, 2017, 101(2): 831-841

[58] AnY, SunJ, GaoY, et al. . Variation of microbial community diversity with long-term exposure of radionuclides in dry uranium tailings pond [J]. China Environmental Science, 2021, 41(2): 923-929(in Chinese)

[59] IslamE, DhalP K, KazyS K, et al. . Molecular analysis of bacterial communities in uranium ores and surrounding soils from Banduhurang open cast uranium mine, India: A comparative study [J]. Journal of Environmental Science and Health Part A, 2011, 46(3): 271-280

[60] WilliamsonA J, MorrisK, LawG T W, et al. . Microbial reduction of U(VI) under alkaline conditions: Implications for radioactive waste geodisposal [J]. Environmental Science & Technology, 2014, 48(22): 13549-13556

[61] LvY, TangC, LiuX, et al. . Stabilization and mechanism of uranium sequestration by a mixed culture consortia of sulfate-reducing and phosphate-solubilizing bacteria [J]. The Science of the Total Environment, 2022, 827154216

[62] VishnivetskayaT A, BrandtC C, MaddenA S, et al. . Microbial community changes in response to ethanol or methanol amendments for U(VI) reduction [J]. Applied and Environmental Microbiology, 2010, 76(17): 5728-5735

[63] LiuH, HongZ, LinJ, et al. . Bacterial coculture enhanced Cd sorption and As bioreduction in co-contaminated systems [J]. Journal of Hazardous Materials A, 2023, 444130376

[64] LiY, WangH, WuP, et al. . Bioreduction of hexavalent chromium on goethite in the presence of Pseudomonas aeruginosa [J]. Environmental Pollution, 2020, 265114765

[65] StoryS, BrigmonR L. Influence of triethyl phosphate on phosphatase activity in shooting range soil: Isolation of a zinc-resistant bacterium with an acid phosphatase [J]. Ecotoxicology and Environmental Safety, 2017, 137165-171

[66] MartinsM, FaleiroM L, ChavesS, et al. . Effect of uranium(VI) on two sulphate-reducing bacteria cultures from a uranium mine site [J]. The Science of the Total Environment, 2010, 408(12): 2621-2628

[67] CecchiG, CeciA, MarescottiP, et al. . Interactions among microfungi and pyrite-chalcopyrite mineralizations: Tolerance, mineral bioleaching, and metal bioaccumulation [J]. Mycological Progress, 2019, 18(3): 415-423

[68] GazitúaM C, MorganteV, PoupinM J, et al. . The microbial community from the early-plant colonizer (Baccharis linearis) is required for plant establishment on copper mine tailings [J]. Scientific Reports, 2021, 11: 10448

[69] XueS, ZhuF, KongX, et al. . A review of the characterization and revegetation of bauxite residues (Red mud) [J]. Environmental Science and Pollution Research, 2016, 23(2): 1120-1132

[70] LiH, YaoJ, MinN, et al. . Microbial metabolic activity in metal(loid)s contaminated sites impacted by different non-ferrous metal activities [J]. Journal of Hazardous Materials, 2023, 459132005

[71] KeW, ZhangX, ZhuF, et al. . Appropriate human intervention stimulates the development of microbial communities and soil formation at a long-term weathered bauxite residue disposal area [J]. Journal of Hazardous Materials, 2021, 405124689

[72] CardonaC, WeisenhornP, HenryC, et al. . Network-based metabolic analysis and microbial community modeling [J]. Current Opinion in Microbiology, 2016, 31124-131

[73] LiL, WangS, LiX, et al. . Effects of Pseudomonas chenduensis and biochar on cadmium availability and microbial community in the paddy soil [J]. The Science of the Total Environment, 2018, 640–641: 1034-1043

[74] ShiA, HuY, ZhangX, et al. . Biochar loaded with bacteria enhanced Cd/Zn phytoextraction by facilitating plant growth and shaping rhizospheric microbial community [J]. Environmental Pollution, 2023, 327121559

[75] SantoliniM, BarabásiA L. Predicting perturbation patterns from the topology of biological networks [J]. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(27): E6375-E6383

[76] LiuS, YuH, YuY, et al. . Ecological stability of microbial communities in Lake Donghu regulated by keystone taxa [J]. Ecological Indicators, 2022, 136108695

[77] LiuB, YaoJ, MaB, et al. . Metal(loid)s diffusion pathway triggers distinct microbiota responses in key regions of typical Karst non-ferrous smelting assembly [J]. Journal of Hazardous Materials B, 2022, 423127164

[78] LiuX, LiuH, ZhangY, et al. . Organic amendments alter microbiota assembly to stimulate soil metabolism for improving soil quality in wheat-maize rotation system [J]. Journal of Environmental Management, 2023, 339117927

[79] KeW, LiC, ZhuF, et al. . Effect of potentially toxic elements on soil multifunctionality at a lead smelting site [J]. Journal of Hazardous Materials, 2023, 454131525

[80] YaoY, ZhangX, HuangZ, et al. . A field study on the composition, structure, and function of endophytic bacterial community of Robinia pseudoacacia at a composite heavy metals tailing [J]. The Science of the Total Environment, 2022, 850157874

[81] ZhangL, YiM, LuP-li. Effects of pyrene on the structure and metabolic function of soil microbial communities [J]. Environmental Pollution, 2022, 305119301

[82] FuX, SongQ, LiS, et al. . Dynamic changes in bacterial community structure are associated with distinct priming effect patterns [J]. Soil Biology and Biochemistry, 2022, 169108671

[83] XiaY, WenX, ZhangB, et al. . Diversity and assembly patterns of activated sludge microbial communities: A review [J]. Biotechnology Advances, 2018, 36(4): 1038-1047

[84] CarusoT, ChanY, LacapD C, et al. . Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale [J]. The ISME Journal, 2011, 5(9): 1406-1413

[85] MendesL W, KuramaeE E, NavarreteA A, et al. . Taxonomical and functional microbial community selection in soybean rhizosphere [J]. The ISME Journal, 2014, 8(8): 1577-1587