Abstract
Heavy metal contaminations in acid mine drainage (AMD) have posed a serious health and environmental risk. Biosorption is a promising in situ remediation technique to remove heavy metals from AMD. In this study, the potential of thermophilic acidophilus Sulfobacillus thermosulfidooxidans was used as biosorbent to remove heavy metal ions (Cd2+, Cu2+, Zn2+ and Ni2+) from acidic solution. The results indicated that the maximum adsorption capabilities of S. thermosulfidooxidans in the order of Ni2+ > Cd2+ > Zn2+ > Cu2+ at initial heavy metal concentrations range from 0.5 to 6 mM in single-metal system while showed an extremely high affinity toward Cu2+ in quaternary metal coexisting system. pH was positively related to adsorption capacity, and isothermal models also indicated monolayer adsorption played a major role in the biosorption process. Additionally, the deprotonation of carboxyl and phosphoryl contributed to the adsorption of heavy metal ions which were identified by ProtoFit analysis. Fourier transform infrared spectroscopy (FTIR) further proved these two kinds of functional groups as well as amino groups participated in the biosorption process. This study provided a new strategy for in situ bioremediation of heavy metal ions in AMD.
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Alkan H, Gul-Guven R, Guven K, Erdogan S, Dogru M (2015) Biosorption of Cd2+, Cu2+, and Ni2+ ions by a thermophilic haloalkalitolerant bacterial strain (KG9) immobilized on amberlite XAD-4. Pol J Environ Stud 24:1903–1910. https://doi.org/10.15244/pjoes/36359
Allen SJ, Mckay G, Porter JF (2004) Adsorption isotherm models for basic dye adsorption by peat in single and binary component systems. J Colloid Interface Sci 280:322–333. https://doi.org/10.1016/j.jcis.2004.08.078
Aneja RK, Chaudhary G, Ahluwalia SS, Goyal D (2010) Biosorption of Pb2+ and Zn2+ by non-living biomass of Spirulina sp. Indian J Microbiol 50:438–442. https://doi.org/10.1007/s12088-011-0091-8
Bozorgi M, Abbasizadeh S, Samani F, Mousavi SE (2018) Performance of synthesized cast and electrospun PVA/chitosan/ZnO-NH2 nano-adsorbents in single and simultaneous adsorption of cadmium and nickel ions from wastewater. Environ Sci Pollut Res 25:17457–17472. https://doi.org/10.1007/s11356-018-1936-z
Burnett PG, Heinrich H, Peak D, Bremer PJ, McQuillan AJ, Daughney CJ (2006) The effect of pH and ionic strength on proton adsorption by the thermophilic bacterium Anoxybacillus flavithermus. Geochim Cosmochim Acta 70:1914–1927. https://doi.org/10.1016/j.gca.2006.01.009
Burnett PGG, Handley K, Peak D, Daughney CJ (2007) Divalent metal adsorption by the thermophile Anoxybacillus flavithermus in single and multi-metal systems. Chem Geol 244:493–506. https://doi.org/10.1016/j.chemgeo.2007.07.006
Chang J-S, Chen C-C (1998) Quantitative analysis and equilibrium models of selective adsorption in multimetal systems using a bacterial biosorbent. Sep Sci 33:611–632
Chen C, Wang J (2007a) Correlating metal ionic characteristics with biosorption capacity using QSAR model. Chemosphere 69:1610–1616. https://doi.org/10.1016/j.chemosphere.2007.05.043
Chen C, Wang J (2007b) Influence of metal ionic characteristics on their biosorption capacity by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 74:911–917. https://doi.org/10.1007/s00253-006-0739-1
Chen XC, Wang YP, Lin Q, Shi JY, Wu WX, Chen YX (2005) Biosorption of copper(II) and zinc(II) from aqueous solution by Pseudomonas putida CZ1. Colloids Surf B Biointerfaces 46:101–107. https://doi.org/10.1016/j.colsurfb.2005.10.003
Chen XC, Shi JY, Chen YX, Xu XH, Xu SY, Wang YP (2006) Tolerance and biosorption of copper and zinc by Pseudomonas putida CZ1 isolated from metal-polluted soil. Can J Microbiol 52:308–316. https://doi.org/10.1139/w05-157
Chen LX, Huang LN, Mendez-Garcia C, Kuang JL, Hua ZS, Liu J, Shu WS (2016) Microbial communities, processes and functions in acid mine drainage ecosystems. Curr Opin Biotechnol 38:150–158. https://doi.org/10.1016/j.copbio.2016.01.013
Choi H-J (2015) Biosorption of heavy metals from acid mine drainage by modified sericite and microalgae hybrid system. Water Air Soil Pollut 226:1–8. https://doi.org/10.1007/s11270-015-2433-3
Choi H-J, Lee S-M (2015) Heavy metal removal from acid mine drainage by calcined eggshell and microalgae hybrid system. Environ Sci Pollut Res 22:13404–13411. https://doi.org/10.1007/s11356-015-4623-3
Choudhary S, Sar P (2009) Characterization of a metal resistant Pseudomonas sp. isolated from uranium mine for its potential in heavy metal (Ni2+, Co2+, Cu2+, and Cd2+) sequestration. Bioresour Technol 100:2482–2492. https://doi.org/10.1016/j.biortech.2008.12.015
Daughney et al (2004) Adsorption and precipitation of iron from seawater on a marine bacteriophage (PWH3A-P1). Mar Chem 91:101–115. https://doi.org/10.1016/j.marchem.2004.06.003
Daughney CJ et al (2010) Proton and cadmium adsorption by the archaeon Thermococcus zilligii: generalising the contrast between thermophiles and mesophiles as sorbents. Chem Geol 273:82–90. https://doi.org/10.1016/j.chemgeo.2010.02.014
Donmez GÇ, Aksu Z, Öztürk A, Kutsal T (1999) A comparative study on heavy metal biosorption characteristics of some algae. Process Biochem 34:885–892
Dopson M, Holmes DS (2014) Metal resistance in acidophilic microorganisms and its significance for biotechnologies. Appl Microbiol Biotechnol 98:8133–8144. https://doi.org/10.1007/s00253-014-5982-2
Du H, Chen W, Cai P, Rong X, Feng X, Huang Q (2016) Competitive adsorption of Pb and Cd on bacteria-montmorillonite composite. Environ Pollut 218:168–175. https://doi.org/10.1016/j.envpol.2016.08.022
Frutos I, Garcia-Delgado C, Garate A, Eymar E (2016) Biosorption of heavy metals by organic carbon from spent mushroom substrates and their raw materials. Int J Environ Sci Technol 13:2713–2720. https://doi.org/10.1007/s13762-016-1100-6
Fu FL, Wang Q (2011) Removal of heavy metal ions from wastewaters: a review. J Environ Manage 92:407–418. https://doi.org/10.1016/j.jenvman.2010.11.011
Giese EC, Dekker RFH, Barbosa-Dekker AM (2019) Biosorption of lanthanum and samarium by viable and autoclaved mycelium of Botryosphaeria rhodina MAMB-05. Biotechnol Prog 35:e2783–e2783. https://doi.org/10.1002/btpr.2783
González AG et al (2010) Adsorption of copper on Pseudomonas aureofaciens: protective role of surface exopolysaccharides. J Colloid Interface Sci 350:305–314. https://doi.org/10.1016/j.jcis.2010.06.020
Gorgievski M, Bozic D, Stankovic V, Bogdanovic G (2009) Copper electrowinning from acid mine drainage: a case study from the closed mine “Cerovo”. J Hazard Mater 170:716–721. https://doi.org/10.1016/j.jhazmat.2009.04.135
Gunatilake SK, Chandrajith R (2017) Removal of Pb(II) from contaminated water using low-temperature pyrolyzed agricultural and forest waste biochars: a comparative study. Desalin Water Treat 62:316–324. https://doi.org/10.5004/dwt.2017.1813
Guo-Hua GU, Xian-xue XIONG, Ke-Ting HU, Shuang-Ke LI, Zhang X (2013) Bioleaching of marmatite with mixed cultures of S. Thermosulfidooxidans and A. Caldus. Min Metall Eng 33(5):91–94
Haq F, Butt M, Ali H, Chaudhary HJ (2015) Biosorption of cadmium and chromium from water by endophytic Kocuria rhizophila: equilibrium and kinetic studies. Desalin Water Treat. https://doi.org/10.1080/19443994.2015.1109561
He Z, Yang Y, Zhou S, Zhong H, Sun W (2013) The effect of culture condition and ionic strength on proton adsorption at the surface of the extreme thermophile Acidianus manzaensis. Colloids Surf B 102:667–673. https://doi.org/10.1016/j.colsurfb.2012.09.028
Hetzer A, Daughney C, Morgan H (2006) Cadmium ion biosorption by the thermophilic bacteria Geobacillus stearothermophilus and G. thermocatenulatus. Appl Environ Microbiol 72:4020–4027. https://doi.org/10.1128/AEM.00295-06
Hurtado C, Viedma P, Cotoras D (2018) Design of a bioprocess for metal and sulfate removal from acid mine drainage. Hydrometallurgy 180:72–77. https://doi.org/10.1016/j.hydromet.2018.07.006
Johnson DB, Hallberg KB (2005) Acid mine drainage remediation options: a review. Sci Total Environ 338:3–14. https://doi.org/10.1016/j.scitotenv.2004.09.002
Kefeni KK, Msagati TAM, Mamba BB (2017) Acid mine drainage: prevention, treatment options, and resource recovery: a review. J Clean Prod 151:475–493. https://doi.org/10.1016/j.jclepro.2017.03.082
Kleinubing SJ, da Silva EA, da Silva MGC, Guibal E (2011) Equilibrium of Cu(II) and Ni(II) biosorption by marine alga Sargassum filipendula in a dynamic system: competitiveness and selectivity. Bioresour Technol 102:4610–4617. https://doi.org/10.1016/j.biortech.2010.12.049
Li JJ, Hitch M (2015) Carbon dioxide sorption isotherm study on pristine and acid-treated olivine and its application in the vacuum swing adsorption process. Minerals 5:259–275. https://doi.org/10.3390/min5020259
Liang Y, Chen JQ, Mei J, Chang JJ, Wang QY, Wan GS, Yin BY (2019) Characterization of Cu and Cd biosorption by Pseudomonas sp. strain DC-B3 isolated from metal mine soil. Int J Environ Sci Technol 16:4035–4046. https://doi.org/10.1007/s13762-018-2011-5
Limcharoensuk T, Sooksawat N, Sumarnrote A, Awutpet T, Kruatrachue M, Pokethitiyook P, Auesukaree C (2015) Bioaccumulation and biosorption of Cd2+ and Zn2+ by bacteria isolated from a zinc mine in Thailand. Ecotox Environ Safe 122:322–330. https://doi.org/10.1016/j.ecoenv.2015.08.013
Liu HL, Chen BY, Lan YW, Cheng YC (2004) Biosorption of Zn(II) and Cu(II) by the indigenous Thiobacillus thiooxidans. Chem Eng J 97:195–201. https://doi.org/10.1016/S1385-8947(03)00210-9
Liu HC et al (2015) Investigation of copper, iron and sulfur speciation during bioleaching of chalcopyrite by moderate thermophile Sulfobacillus thermosulfidooxidans. Int J Miner Process 137:1–8. https://doi.org/10.1016/j.minpro.2015.02.008
Mashitah MD, Azila YY, Bhatia S (2008) Biosorption of cadmium(II) ions by immobilized cells of Pycnoporus sanguineus from aqueous solution. Bioresour Technol 99:4742–4748. https://doi.org/10.1016/j.biortech.2007.09.062
Moodley I, Sheridan CM, Kappelmeyer U, Akcil A (2018) Environmentally sustainable acid mine drainage remediation: research developments with a focus on waste/by-products. Miner Eng 126:207–220. https://doi.org/10.1016/j.mineng.2017.08.008
Narayanan SL, Venkatesan G, Potheher IV (2018) Equilibrium studies on removal of lead (II) ions from aqueous solution by adsorption using modified red mud. Int J Environ Sci Technol 15:1687–1698. https://doi.org/10.1007/s13762-017-1513-x
Orell A, Navarro CA, Arancibia R, Mobarec JC, Jerez CA (2010) Life in blue: copper resistance mechanisms of bacteria and Archaea used in industrial biomining of minerals. Biotechnol Adv 28:839–848. https://doi.org/10.1016/j.biotechadv.2010.07.003
Ozcan AS, Ozcan A, Ay CO, Erdoğan Y (2012) Characterization of Punica granatum L. peels and quantitatively determination of its biosorption behavior towards lead(II) ions and Acid Blue 40. Colloids Surf B 100:197–204. https://doi.org/10.1016/j.colsurfb.2012.05.013
Park I, Tabelin CB, Jeon S, Li XL, Seno K, Ito M, Hiroyoshi N (2019) A review of recent strategies for acid mine drainage prevention and mine tailings recycling. Chemosphere 219:588–606. https://doi.org/10.1016/j.chemosphere.2018.11.053
Pokrovsky OS, Martinez RE, Kompantseva EI, Shirokova LS (2013) Interaction of metals and protons with anoxygenic phototrophic bacteria Rhodobacter blasticus. Chem Geol 335:75–86. https://doi.org/10.1016/j.chemgeo.2012.10.052
Puyen ZM, Villagrasa E, Maldonado J, Diestra E, Esteve I, Sole A (2012) Biosorption of lead and copper by heavy-metal tolerant Micrococcus luteus DE2008. Bioresour Technol 126:233–237. https://doi.org/10.1016/j.biortech.2012.09.036
Rahman Z, Thomas L, Singh VP (2019) Biosorption of heavy metals by a lead (Pb) resistant bacterium, Staphylococcus hominis strain AMB-2. J Basic Microbiol 59:477–486. https://doi.org/10.1002/jobm.201900024
Schooling SR, Beveridge TJ (2006) Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188:5945. https://doi.org/10.1128/JB.00257-06
Sethuraman P, Kumar MD (2011) Bacillus subtilis on Pb2+ ions removal from aqueous solution by biosorption. Res J Pharm Biol Chem Sci 2:247–257
Shabalala AN, Ekolu SO, Diop S, Solomon F (2017) Pervious concrete reactive barrier for removal of heavy metals from acid mine drainage—column study. J Hazard Mater 323:641–653. https://doi.org/10.1016/j.jhazmat.2016.10.027
Shafiee M, Abedi MA, Abbasizadeh S, Sheshdeh RK, Mousavi SE, Shohani S (2019) Effect of zeolite hydroxyl active site distribution on adsorption of Pb(II) and Ni(II) pollutants from water system by polymeric nanofibers. Sep Sci Technol. https://doi.org/10.1080/01496395.2019.1624572
Sheng PX, Ting YP, Chen JP, Hong L (2004) Sorption of lead, copper, cadmium, zinc, and nickel by marine algal biomass: characterization of biosorptive capacity and investigation of mechanisms. J Colloid Interface Sci 275:131–141. https://doi.org/10.1016/j.jcis.2004.01.036
Sheoran AS, Sheoran V (2006) Heavy metal removal mechanism of acid mine drainage in wetlands: a critical review. Miner Eng 19:105–116. https://doi.org/10.1016/j.mineng.2005.08.006
Skousen JG, Ziemkiewicz PF, McDonald LM (2019) Acid mine drainage formation, control and treatment: approaches and strategies. Extract Ind Soc Int J 6:241–249. https://doi.org/10.1016/j.exis.2018.09.008
Srivastava SK, Tyagi R (1995) Competitive adsorption of substituted phenols by activated carbon developed from the fertilizer waste slurry. Water Res 29:483–488
Su YK, Mi RJ, Chang HC, Yun YS, Jahng KY, Yu KY (2015) Biosorption of cationic basic dye and cadmium by the novel biosorbent Bacillus catenulatus JB-022 strain. J Biosci Bioeng 119:433–439. https://doi.org/10.1016/j.jbiosc.2014.09.022
Turner BF, Fein JB (2006) Protofit: a program for determining surface protonation constants from titration data. Comput Geosci 32:1344–1356. https://doi.org/10.1016/j.cageo.2005.12.005
Ueshima M, Ginn BR, Haack EA, Szymanowski JES, Fein JB (2008) Cd adsorption onto Pseudomonas putida in the presence and absence of extracellular polymeric substances. Geochim Cosmochim Acta 72:5885–5895. https://doi.org/10.1016/j.gca.2008.09.014
van der Merwe JA, Deane SM, Rawlingse DE (2010) The chromosomal arsenic resistance genes of Sulfobacillus thermosulfidooxidans. Hydrometallurgy 104:477–482. https://doi.org/10.1016/j.hydromet.2010.01.017
Wightman PG, Fein JB, Wesolowski DJ, Phelps TJ, Bénézeth P, Palmer DA (2001) Measurement of bacterial surface protonation constants for two species at elevated temperatures. Geochim Cosmochim Acta 65:3657–3669. https://doi.org/10.1016/S0016-7037(01)00763-3
Xing SC, Chen JY, Lv N, Mi JD, Chen WL, Liang JB, Liao XD (2018) Biosorption of lead (Pb2+) by the vegetative and decay cells and spores of Bacillus coagulans R11 isolated from lead mine soil. Chemosphere 211:804–816. https://doi.org/10.1016/j.chemosphere.2018.08.005
Xu SZ, Xing YH, Liu S, Hao XL, Chen WL, Huang QY (2020) Characterization of Cd2+ biosorption by Pseudomonas sp. strain 375, a novel biosorbent isolated from soil polluted with heavy metals in Southern China. Chemosphere 240:7. https://doi.org/10.1016/j.chemosphere.2019.124893
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This work was financially supported by the National Natural Science Foundation of China (No. 51774339), Co-Innovation Center for Clean and Efficient Utilization of Strategic Metal Mineral Resources.
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Huang, Y., Li, M., Yang, Y. et al. Sulfobacillus thermosulfidooxidans: an acidophile isolated from acid hot spring for the biosorption of heavy metal ions. Int. J. Environ. Sci. Technol. 17, 2655–2666 (2020). https://doi.org/10.1007/s13762-020-02669-1
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DOI: https://doi.org/10.1007/s13762-020-02669-1