Sulfobacillus thermosulfidooxidans: an acidophile isolated from acid hot spring for the biosorption of heavy metal ions

  • Y. Huang
  • M. Li
  • Y. Yang
  • Q. Zeng
  • P. Loganathan
  • L. Hu
  • H. Zhong
  • Z. HeEmail author
Original Paper


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.


Acid mine drainage Carboxyl Phosphoryl Heavy metal ion adsorption Sulfobacillus thermosulfidooxidans 



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.


  1. 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. CrossRefGoogle Scholar
  2. 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. CrossRefGoogle Scholar
  3. 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. CrossRefGoogle Scholar
  4. 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. CrossRefGoogle Scholar
  5. 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. CrossRefGoogle Scholar
  6. 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. CrossRefGoogle Scholar
  7. Chang J-S, Chen C-C (1998) Quantitative analysis and equilibrium models of selective adsorption in multimetal systems using a bacterial biosorbent. Sep Sci 33:611–632CrossRefGoogle Scholar
  8. Chen C, Wang J (2007a) Correlating metal ionic characteristics with biosorption capacity using QSAR model. Chemosphere 69:1610–1616. CrossRefGoogle Scholar
  9. Chen C, Wang J (2007b) Influence of metal ionic characteristics on their biosorption capacity by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 74:911–917. CrossRefGoogle Scholar
  10. 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. CrossRefGoogle Scholar
  11. 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. CrossRefGoogle Scholar
  12. 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. CrossRefGoogle Scholar
  13. 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. CrossRefGoogle Scholar
  14. 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. CrossRefGoogle Scholar
  15. 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. CrossRefGoogle Scholar
  16. Daughney et al (2004) Adsorption and precipitation of iron from seawater on a marine bacteriophage (PWH3A-P1). Mar Chem 91:101–115. CrossRefGoogle Scholar
  17. 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. CrossRefGoogle Scholar
  18. Donmez GÇ, Aksu Z, Öztürk A, Kutsal T (1999) A comparative study on heavy metal biosorption characteristics of some algae. Process Biochem 34:885–892CrossRefGoogle Scholar
  19. Dopson M, Holmes DS (2014) Metal resistance in acidophilic microorganisms and its significance for biotechnologies. Appl Microbiol Biotechnol 98:8133–8144. CrossRefGoogle Scholar
  20. 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. CrossRefGoogle Scholar
  21. 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. CrossRefGoogle Scholar
  22. Fu FL, Wang Q (2011) Removal of heavy metal ions from wastewaters: a review. J Environ Manage 92:407–418. CrossRefGoogle Scholar
  23. 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. CrossRefGoogle Scholar
  24. González AG et al (2010) Adsorption of copper on Pseudomonas aureofaciens: protective role of surface exopolysaccharides. J Colloid Interface Sci 350:305–314. CrossRefGoogle Scholar
  25. 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. CrossRefGoogle Scholar
  26. 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. CrossRefGoogle Scholar
  27. 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):91–94Google Scholar
  28. 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. CrossRefGoogle Scholar
  29. 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. CrossRefGoogle Scholar
  30. 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. CrossRefGoogle Scholar
  31. Hurtado C, Viedma P, Cotoras D (2018) Design of a bioprocess for metal and sulfate removal from acid mine drainage. Hydrometallurgy 180:72–77. CrossRefGoogle Scholar
  32. Johnson DB, Hallberg KB (2005) Acid mine drainage remediation options: a review. Sci Total Environ 338:3–14. CrossRefGoogle Scholar
  33. Kefeni KK, Msagati TAM, Mamba BB (2017) Acid mine drainage: prevention, treatment options, and resource recovery: a review. J Clean Prod 151:475–493. CrossRefGoogle Scholar
  34. 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. CrossRefGoogle Scholar
  35. 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. CrossRefGoogle Scholar
  36. 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. CrossRefGoogle Scholar
  37. 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. CrossRefGoogle Scholar
  38. 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. CrossRefGoogle Scholar
  39. 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. CrossRefGoogle Scholar
  40. 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. CrossRefGoogle Scholar
  41. 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. CrossRefGoogle Scholar
  42. 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. CrossRefGoogle Scholar
  43. 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. CrossRefGoogle Scholar
  44. 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. CrossRefGoogle Scholar
  45. 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. CrossRefGoogle Scholar
  46. 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. CrossRefGoogle Scholar
  47. 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. CrossRefGoogle Scholar
  48. 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. CrossRefGoogle Scholar
  49. Schooling SR, Beveridge TJ (2006) Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188:5945. CrossRefGoogle Scholar
  50. Sethuraman P, Kumar MD (2011) Bacillus subtilis on Pb2+ ions removal from aqueous solution by biosorption. Res J Pharm Biol Chem Sci 2:247–257Google Scholar
  51. 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. CrossRefGoogle Scholar
  52. 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. CrossRefGoogle Scholar
  53. 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. CrossRefGoogle Scholar
  54. Sheoran AS, Sheoran V (2006) Heavy metal removal mechanism of acid mine drainage in wetlands: a critical review. Miner Eng 19:105–116. CrossRefGoogle Scholar
  55. 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. CrossRefGoogle Scholar
  56. Srivastava SK, Tyagi R (1995) Competitive adsorption of substituted phenols by activated carbon developed from the fertilizer waste slurry. Water Res 29:483–488CrossRefGoogle Scholar
  57. 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. CrossRefGoogle Scholar
  58. Turner BF, Fein JB (2006) Protofit: a program for determining surface protonation constants from titration data. Comput Geosci 32:1344–1356. CrossRefGoogle Scholar
  59. 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. CrossRefGoogle Scholar
  60. van der Merwe JA, Deane SM, Rawlingse DE (2010) The chromosomal arsenic resistance genes of Sulfobacillus thermosulfidooxidans. Hydrometallurgy 104:477–482. CrossRefGoogle Scholar
  61. 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. CrossRefGoogle Scholar
  62. 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. CrossRefGoogle Scholar
  63. 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. CrossRefGoogle Scholar

Copyright information

© Islamic Azad University (IAU) 2020

Authors and Affiliations

  1. 1.School of Minerals Processing and Bioengineering, Key Laboratory of Biohydrometallurgy of Ministry of EducationCentral South UniversityChangshaChina
  2. 2.School of Life ScienceCentral South UniversityChangshaChina

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