Contributions of adsorption, bioreduction and desorption to uranium immobilization by extracellular polymeric substances

Abstract

● EPS immobilizes U(VI) via adsorption, bioreduction and desorption.

● This work provides a framework to quantify the three immobilization processes.

● The non-equilibrium adsorption of U follows pseudo-second-order kinetics.

● The equilibrium adsorption of U followed Langmuir and Freundlich isotherms.

Hexavalent uranium (U(VI)) can be immobilized by various microbes. The role of extracellular polymeric substances (EPS) in U(VI) immobilization has not been quantified. This work provides a model framework to quantify the contributions of three processes involved in EPS-mediated U(VI) immobilization: adsorption, bioreduction and desorption. Loosely associated EPS was extracted from a pure bacterial strain, Klebsiella sp. J1, and then exposed to H₂ and O₂ (no bioreduction control) to immobilize U(VI) in batch experiments. U(VI) immobilization was faster when exposed to H₂ than O₂ and stabilized at 94% for H₂ and 85% for O₂, respectively. The non-equilibrium data from the H₂ experiments were best simulated by a kinetic model consisting of pseudo-second-order adsorption (k_a = 2.87 × 10⁻³ g EPS·(mg U)⁻¹·min⁻¹), first-order bioreduction (k_b = 0.112 min⁻¹) and first-order desorption (k_d = 7.00 × 10⁻³ min⁻¹) and fitted the experimental data with R² of 0.999. While adsorption was dominant in the first minute of the experiments with H₂, bioreduction was dominant from the second minute to the 50^th min. After 50 min, adsorption was negligible, and bioreduction was balanced by desorption. This work also provides the first set of equilibrium data for U(VI) adsorption by EPS alone. The equilibrium experiments with O₂ were well simulated by both the Langmuir isotherm and the Freundlich isotherm, suggesting multiple mechanisms involved in the interactions between U(VI) and EPS. The thermodynamic study indicated that the adsorption of U(VI) onto EPS was endothermic, spontaneous and favorable at higher temperatures.

Graphical abstract

Keywords

Adsorption / Bioreduction / Desorption / Kinetics / Isotherm / Uranium

References

[1] Al-Ghouti M A, Da’ana D A. (2020). Guidelines for the use and interpretation of adsorption isotherm models: a review. Journal of Hazardous Materials, 393: 122383

[2] ATSDR (2013). Toxicological profile for uranium. Agency for Toxic Substances and Disease Registry, U.S. Department of Health and Human Services, Public Health Services: 1−526

[3] BairdR B, Eaton A D, RiceE W (2017). Standard methods for the examination of water and wastewater. American Public Health Association, American Water Works Association, and Water Environment Federation. 23rd ed: 1−1545

[4] Bayramoglu G, Arica M Y. (2017). Polyethylenimine and tris(2-aminoethyl)amine modified p(GA–EGMA) microbeads for sorption of uranium ions: equilibrium, kinetic and thermodynamic studies. Journal of Radioanalytical and Nuclear Chemistry, 312(2): 293–303

[5] Cao B, Ahmed B, Kennedy D W, Wang Z, Shi L, Marshall M J, Fredrickson J K, Isern N G, Majors P D, Beyenal H. (2011). Contribution of extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms to U(VI) immobilization. Environmental Science & Technology, 45(13): 5483–5490

[6] Cecal A, Humelnicu D, Rudic V, Cepoi L, Ganju D, Cojocari A. (2012). Uptake of uranyl ions from uranium ores and sludges by means of Spirulina platensis, Porphyridium cruentum and Nostok linckia alga. Bioresource Technology, 118: 19–23

[7] Chen F, Guo S, Wang Y, Ma L, Li B, Song Z, Huang L, Zhang W. (2022). Concurrent adsorption and reduction of chromium(VI) to chromium(III) using nitrogen-doped porous carbon adsorbent derived from loofah sponge. Frontiers of Environmental Science & Engineering, 16(5): 57

[8] Cologgi D L, Speers A M, Bullard B A, Kelly S D, Reguera G. (2014). Enhanced uranium immobilization and reduction by Geobacter sulfurreducens biofilms. Applied and Environmental Microbiology, 80(21): 6638–6646

[9] Erkaya I A, Arica M Y, Akbulut A, Bayramoglu G. (2014). Biosorption of uranium(VI) by free and entrapped Chlamydomonas reinhardtii: kinetic, equilibrium and thermodynamic studies. Journal of Radioanalytical and Nuclear Chemistry, 299(3): 1993–2003

[10] FebriantoJ, Kosasih A N, SunarsoJ, JuY H, Indraswati N, IsmadjiS (2009). Equilibrium and kinetic studies in adsorption of heavy metals using biosorbent: a summary of recent studies. Journal of Hazardous Materials, 162(2–3): 616–645

[11] Foo K Y, Hameed B H. (2010). Insights into the modeling of adsorption isotherm systems. Chemical Engineering Journal, 156(1): 2–10

[12] Kausar A, Bhatti H N, MacKinnon G. (2013). Equilibrium, kinetic and thermodynamic studies on the removal of U(VI) by low cost agricultural waste. Colloids and Surfaces. B, Biointerfaces, 111: 124–133

[13] Khani M H. (2011). Statistical analysis and isotherm study of uranium biosorption by Padina sp. algae biomass. Environmental Science and Pollution Research International, 18(5): 790–799

[14] Lakaniemi A M, Douglas G B, Kaksonen A H. (2019). Engineering and kinetic aspects of bacterial uranium reduction for the remediation of uranium contaminated environments. Journal of Hazardous Materials, 371: 198–212

[15] Leigh M B, Wu W-M, Cardenas E, Uhlik O, Carroll S, Gentry T, Marsh T L, Zhou J, Jardine P, Criddle C S, Tiedje J M. (2015). Microbial communities biostimulated by ethanol during uranium (VI) bioremediation in contaminated sediment as shown by stable isotope probing. Frontiers of Environmental Science & Engineering, 9(3): 453–464

[16] Li A, Zhou C, Liu Z, Xu X, Zhou Y, Zhou D, Tang Y, Ma F, Rittmann B E. (2018). Direct solid-state evidence of H₂-induced partial U(VI) reduction concomitant with adsorption by extracellular polymeric substances (EPS). Biotechnology and Bioengineering, 115(7): 1685–1693

[17] Liu Y, Liu Y, Cao X, Hua R, Wang Y, Pang C, Hua M, Li X. (2011). Biosorption studies of uranium (VI) on cross-linked chitosan: isotherm, kinetic and thermodynamic aspects. Journal of Radioanalytical and Nuclear Chemistry, 290(2): 231–239

[18] Liu Y, Liu Y J. (2008). Biosorption isotherms, kinetics and thermodynamics. Separation and Purification Technology, 61(3): 229–242

[19] Liu Y, Shen L. (2008). From Langmuir kinetics to first- and second-order rate equations for adsorption. Langmuir, 24(20): 11625–11630

[20] Liu Y H, Wang Y Q, Zhang Z B, Cao X H, Nie W B, Li Q, Hua R. (2013). Removal of uranium from aqueous solution by a low cost and high-efficient adsorbent. Applied Surface Science, 273: 68–74

[21] MajumderE L W, WallJ D (2017). Uranium bio-transformations: chemical or biological processes? Open Journal of Inorganic Chemistry, 7(2): 28–60

[22] Nuhanović M, Grebo M, Draganović S, Memić M, Smječanin N. (2019). Uranium(VI) biosorption by sugar beet pulp equilibrium, kinetic and thermodynamic studies. Journal of Radioanalytical and Nuclear Chemistry, 322(3): 2065–2078

[23] Pan X, Liu J, Song W, Zhang D. (2012). Biosorption of Cu(II) to extracellular polymeric substances (EPS) from Synechoeystis sp.: a fluorescence quenching study. Frontiers of Environmental Science & Engineering, 6(4): 493–497

[24] Pi S, Li A, Qiu J, Feng L, Zhou L, Zhao H P, Ma F. (2021). Enhanced recovery of hexavalent chromium by remodeling extracellular polymeric substances through engineering Agrobacterium tumefaciens F2. Journal of Cleaner Production, 279: 123829

[25] Renslow R S, Ahmed B, Nuñez J R, Cao B, Majors P D, Fredrickson J K, Beyenal H. (2017). Modeling substrate utilization, metabolite production, and uranium immobilization in Shewanella Oneidensis biofilms. Frontiers in Environmental Science, 5: 30

[26] Šabanović E, Muhić-Šarac T, Nuhanović M, Memić M. (2019). Biosorption of uranium(VI) from aqueous solution by Citrus limon peels kinetics, equlibrium and batch studies. Journal of Radioanalytical and Nuclear Chemistry, 319(1): 425–435

[27] Sheng G P, Yu H Q, Li X Y. (2010). Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnology Advances, 28(6): 882–894

[28] Spear J R, Figueroa L A, Honeyman B D. (1999). Modeling the removal of uranium U(VI) from aqueous solutions in the presence of sulfate reducing bacteria. Environmental Science & Technology, 33(15): 2667–2675

[29] Tan K L, Hameed B H. (2017). Insight into the adsorption kinetics models for the removal of contaminants from aqueous solutions. Journal of the Taiwan Institute of Chemical Engineers, 74: 25–48

[30] Wang F, Tan L, Liu Q, Li R, Li Z, Zhang H, Hu S, Liu L, Wang J. (2015). Biosorption characteristics of Uranium (VI) from aqueous solution by pollen pini. Journal of Environmental Radioactivity, 150: 93–98

[31] Wang K, Wang Y, Zhang S, Chen Y, Wang R, Ho S. (2022). Tailoring a novel hierarchical cheese-like porous biochar from algae residue to boost sulfathiazole removal. Environmental Science and Ecotechnology, 10: 100168

[32] Wei W, Li A, Ma F, Pi S, Yang J, Wang Q, Ni B J. (2018). Simultaneous sorption and reduction of Cr(VI) in aquatic system by microbial extracellular polymeric substances from Klebsiella sp. J1. Journal of Chemical Technology and Biotechnology (Oxford, Oxfordshire), 93(11): 3152–3159

[33] Wei W, Wang Q, Li A, Yang J, Ma F, Pi S, Wu D. (2016). Biosorption of Pb(II) from aqueous solution by extracellular polymeric substances extracted from Klebsiella sp. J1: adsorption behavior and mechanism assessment. Scientific Reports, 6(1): 31575

[34] Xie S, Yang J, Chen C, Zhang X, Wang Q, Zhang C. (2008). Study on biosorption kinetics and thermodynamics of uranium by Citrobacter freudii. Journal of Environmental Radioactivity, 99(1): 126–133

[35] Zhang H L, Cheng M X, Li S C, Huang H X, Liu W D, Lyu X J, Chu J, Ding H, Zhao D, Wang Y, Huang F. (2019). Roles of extracellular polymeric substances in uranium immobilization by anaerobic sludge. AMB Express, 9(1): 199

[36] Zhao C, Wang Y, Cheng M, Zhang H, Yang Y, Liu N, Liao J. (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

[37] Zhou L, Li A, Ma F, Yang J, Pi S, Tang A. (2019). Sb(V) reduced to Sb(III) and more easily adsorbed in the form of Sb(OH)₃ by microbial extracellular polymeric substances and core–shell magnetic nanocomposites. ACS Sustainable Chemistry & Engineering, 7(11): 10075–10083

[38] Zhou L, Li A, Ma F, Zhao H, Deng F, Pi S, Tang A, Yang J. (2020). Combining high electron transfer efficiency and oxidation resistance in nZVI with coatings of microbial extracellular polymeric substances to enhance Sb(V) reduction and adsorption. Chemical Engineering Journal, 395: 125168

RIGHTS & PERMISSIONS

Higher Education Press