Abstract
Chemical precipitation, oxidation/reduction, filtration, ion-exchange, reverse osmosis, membrane technology, evaporation and electrochemical treatment as remediation technologies have various shortcomings which have fueled the search for more environmentally friendly and cost-effective methods of remediating heavy metal contaminated environments. Indigenous bacteria in heavy metal contaminated sites present a possible solution to this concern. This study assessed the potential of indigenous heavy metal resistant bacteria as immobilization agents of Pb, Ni and Zn in Au mine tailings. Tailings from three abandoned Au mining environments; mine tailings A (MA), mine tailings B (MB), and Tudor shaft (TS) were collected and indigenous heavy metal resistant bacteria present in the tailings isolated. The isolated bacteria OMF 532 (E. asburiae) and OMF 003 (B. cereus) were used in bioaugmenting Ni-, Pb- and Zn-spiked tailings to determine the potential of the isolates to immobilize these metals. The immobilization potential of the isolates as determined by the difference in metal mobility in the tailings samples before and after bioaugmentation was used to assess the immobilization potential of the bacterial isolates. Mobility factor (MF) of Ni in the samples was reduced from 16.4 to 6.2, and 17.6 to 7.4 in MB and MA, respectively, reflecting a 35% decrease in Ni mobility. Lead and Zn mobility in the samples also showed a decrease of 90% and 60%, respectively, after bioaugmentation. Though MF values for Ni, Pb and Zn in the TS samples indicated low level of mobility of these elements at the site, bioaugmentation further reduced their mobility by 25–35% for Ni, 95% for Pb, and 10–30% for Zn. The results of this study show that indigenous bacteria in the tailings have the potential to reduce the bioavailable fractions of the three metals studied in the mine tailing and could be further exploited in heavy metal remediation of the sites.
Article Highlights
The study investigated the potential of indigenous bacteria to immobilize selected heavy metals in tailings samples. The highlights of the manuscript include the following:
The study identified Bacillus cereus OMF 003 and Enterobacter asburiae OMF 532 as heavy metal resistant bacteria in Au mine tailings.
Bioaugmenting tailings with the bacterial isolates reduced the mobility Factor of Ni in the samples by up to 35% for Ni, 90% for Pb and 60% for Zn.
Indigenous Bacillus cereus OMF 003 and Enterobacter asburiae OMF 532 presents significant opportunities for heavy metal immobilization in tailings contaminated environments.
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References
Achal V, Pan X, Fu Q, Zhang D (2012) Biomineralization based remediation of As(III) contaminated soil by Sporosarcina ginsengisoli. J Hazard Mater 201–202:178–184. https://doi.org/10.1016/j.jhazmat.2011.11.067
Adhikari T, Rattan RK (2007) Distribution of zinc fractions in some major soils of India and the impact on nutrition of rice. Commun Soil Sci Plant Anal 38:2779–2798. https://doi.org/10.1080/00103620701663032
Ahmad Z, Rehman AU, Anees M (2013) Microcosmic study of nickel stress towards soil bacteria and their biochemical characterization. J BioMol Sci (JBMS) 1:37–44
Ahmadipour F, Bahramifar N, Mahmood Ghasempouri S (2014) Fractionation and mobility of cadmium and lead in soils of Amol area in Iran, using the modified BCR sequential extraction method. Chem Speciat Bioavailab 26:31–36. https://doi.org/10.3184/095422914x13884321932037
Akcil A, Karahan AG, Ciftci H, Sagdic O (2003) Biological treatment of cyanide by natural isolated bacteria (Pseudomonas sp.). Miner Eng 16:643–649. https://doi.org/10.1016/S0892-6875(03)00101-8
Akhtar MS, Chali B, Azam T (2013) Bioremediation of arsenic and lead by plants and microbes from contaminated soil. Res Plant Sci 1:68–73. https://doi.org/10.12691/plant-1-3-4
Alloway BJ (2013) Heavy metals in soils. Springer, Dordrecht
Anderson CR, Cook GM (2004) Isolation and characterization of arsenate-reducing bacteria from arsenic-contaminated sites in New Zealand. Curr Microbiol 45:341–347
Arenas-Lago D, Vega FA, Silva LFO, Lago-Vila M, Andrade L (2014) Lead distribution between soil geochemical phases and its fractionation in Pb-treated soils. Fresenius Environ Bull 23:1025–1035
Ayangbenro A, Babalola O (2018) Metal(loid) bioremediation: strategies employed by microbial polymers. Sustainability 10:3028. https://doi.org/10.3390/su10093028
Azubuike CC, Chikere CB, Okpokwasili GC (2016) Bioremediation techniques–classification based on site of application: principles, advantages, limitations and prospects. World J Microbiol Biotechnol 32:180. https://doi.org/10.1007/s11274-016-2137-x
Badaway SH, El-Motaium RA (2000) Fate of some heavy metals in sandy soil amended with sewage sludge and their accumulation in plants. In: Paper presented at the ICEHM2000, Cairo University, Egypt
Barrow G, Feltham R (1993) Cowan and Steel’s manual for the identification of medical bacteria, 3rd edn. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511527104
Bredenkamp G (2002) The Savanna ecoregion. In: The biodiversity of South Africa, indicators, trends and human impacts. Struik Publishers, Cape Town
Brown S, Chaney RL, Hallfrisch JG, Xue Q (2003) Effect of biosolids processing on lead bioavailability in an urban soil. J Environ Qual 32:100–108. https://doi.org/10.2134/jeq2003.1000
Bruemmer GW, Gerth J, Tiller KG (1988) Reaction kinetics of the adsorption and desorption of nickel, zinc and cadmium by goethite. I. Adsorption and diffusion of metals. J Soil Sci 39:37–52. https://doi.org/10.1111/j.1365-2389.1988.tb01192.x
Cairncross E, Kisting S, Liefferink MA, van Wyk D (2013) Case study on extractive industries prepared for the Lancet Commission on Global Governance. South Africa
Colin VL, Villegas LB, Abate CM (2012) Indigenous microorganisms as potential bioremediators for environments contaminated with heavy metals. Int Biodeterior Biodegrad 69:28–37. https://doi.org/10.1016/j.ibiod.2011.12.001
Council for Geosciences (2011) Guide to the Services of the CGS Analytical Laboratory 2016 [cited 18 March 2011]. http://196.33.85.14/cgs_inter/images/stories/Lab_Guide/Services_of_the_CGS_Analytical_Laboratory.pdf. Accessed Sept 2017
Dadrasnia A, Chuan Wei KS, Shahsavari N, Azirun MS, Ismail S (2015) Biosorption potential of Bacillus salmalaya strain 139SI for removal of Cr(VI) from aqueous solution. Int J Environ Res Public Health 12:15321–15338. https://doi.org/10.3390/ijerph121214985
Das P, Sinha S, Mukherjee SK (2014) Nickel bioremediation potential of Bacillus thuringiensis KUNi1 and some environmental factors in nickel removal. Bioremediat J 18:169–177. https://doi.org/10.1080/10889868.2014.889071
Davutluoglu OI, Seckin G, Ersu CB, Yilmaz T, Sari B (2011) Heavy metal content and distribution in surface sediments of the Seyhan River. Turkey J Environ Manag 92:2250–2259. https://doi.org/10.1016/j.jenvman.2011.04.013
Fashola MO, Ngole-Jeme VM, Babalola OO (2015) Diversity of acidophilic bacteria and Archaea and their roles in bioremediation of acid mine drainage. Br Microbiol Res J 8:443–456
Fashola MO, Ngole-Jeme VM, Babalola OO (2016) Heavy metal pollution from gold mines: environmental effects and bacterial strategies for resistance. Int J Environ Res Public Health 13:1047. https://doi.org/10.3390/ijerph13111047
Flemming CA, Ferris FG, Beveridge TJ, Bailey GW (1990) Remobilization of toxic heavy metals adsorbed to bacterial wall-clay composites. Appl Environ Microbiol 56:3191–3203
Fonti V, Beolchini F, Rocchetti L, Dell’Anno A (2015) Bioremediation of contaminated marine sediments can enhance metal mobility due to changes of bacterial diversity. Water Res 68:637–650. https://doi.org/10.1016/j.watres.2014.10.035
Guo X, Huang Q, Chen W (2002) Effect of microbial activities on the mobility of heavy metals in soil environments. Chin J Appl Environ Biol 8:12–18
Hyun S, Lee LS, Rao PSC (2003) Significance of anion exchange in pentachlorophenol sorption by variable-charge soils. J Environ Qual 32:966–976
Islam MS, Ahmed MK, Habibullah-Al-Mamun M, Raknuzzaman M (2015) The concentration, source and potential human health risk of heavy metals in the commonly consumed foods in Bangladesh. Ecotoxicol Environ Saf 122:462–469. https://doi.org/10.1016/j.ecoenv.2015.09.022
Issazadeh K, Majid MR, Pahlaviani K, Massiha A (2011) Bioremediation of toxic heavy metals pollutants by Bacillus spp. isolated from Guilan Bay Sediments, North of Iran. In: International conference on biotechnology and environment management IPCBEE, Singapore, vol 18. IACSIT Press, pp 67–71
Joonu J, Averal HI (2016) Heavy metal resistant CZC genes identification in Bacillus cereus, Enterobacter asburiae and Pseudomonas aeruginosa isolated from BHEL industry, Tamilnadu research and reviews. J Microbiol Biotechnol 5:27–31
Khan S, El-Latif Hesham A, Qiao M, Rehman S, He J-Z (2010) Effects of Cd and Pb on soil microbial community structure and activities. Environ Sci Pollut Res 17:288–296. https://doi.org/10.1007/s11356-009-0134-4
Kim I, Lee M, Wang S (2014) Heavy metal removal in groundwater originating from acid mine drainage using dead Bacillus drentensis sp. immobilized in polysulfone polymer. J Environ Manag 146:568–574. https://doi.org/10.1016/j.jenvman.2014.05.042
Ledin M (2000) Accumulation of metals by microorganisms—processes and importance for soil systems. Earth Sci Rev 51:1–31. https://doi.org/10.1016/S0012-8252(00)00008-8
Ma LQ, Rao GN (1997) Chemical fractionation of cadmium, copper, nickel, and zinc in contaminated soils. J Environ Qual 26:259–264. https://doi.org/10.2134/jeq1997.00472425002600010036x
Morais S, Garcia e Costa F, Pereira ML (2012) Heavy metals and human health, environmental health. In: Oosthuizen J (ed) Emerging issues and practice. IntechOpen, London. https://doi.org/10.5772/29869
Mudgal V, Madaan N, Mudgal A, Singh R, Mishra S (2010) Effect of toxic metals on human health. Open Nutraceuticals J 3:94–99. https://doi.org/10.2174/18763960010030100094
Murthy S, Bali G, Sarangi SK (2014) Effect of lead on growth, protein and biosorption capacity of Bacillus cereus isolated from industrial effluent. J Environ Biol 35:407–411
Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216. https://doi.org/10.1007/s10311-010-0297-8
Nemati K, Bakar NKA, Abas MR, Sobhanzadeh E (2011) Speciation of heavy metals by modified BCR sequential extraction procedure in different depths of sediments from Sungai Buloh, Selangor, Malaysia. J Hazard Mater 192:402–410. https://doi.org/10.1016/j.jhazmat.2011.05.039
Ngole VM (2011) Using soil heavy metal enrichment and mobility factors to determine potential uptake by vegetables Plant. Soil Environ 57:75–80
Ngole-Jeme VM (2017) Changes in the Mineralogy and Geochemistry of mine tailings contaminated soil as a result of fire events and the Implications on soil sorption properties. In: Paper presented at the 2017 international conference on environmental pollution control, 8–12 October 2017, Vancouver
Ngole-Jeme VM, Fantke P (2017) Ecological and human health risks associated with abandoned gold mine tailings contaminated soil. PLoS One 12:e0172517. https://doi.org/10.1371/journal.pone.0172517
Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750. https://doi.org/10.1007/s002530051457
Njinga RL, Tshivhase VM (2016) Lifetime cancer risk due to gamma radioactivity in soils from Tudor Shaft mine environs, South Africa. J Radiat Res Appl Sci 9:310–315. https://doi.org/10.1016/j.jrras.2016.02.003
Pan J-H, Liu R-X, Tang H-X (2007) Surface reaction of Bacillus cereus biomass and its biosorption for lead and copper ions. J Environ Sci 19:403–408. https://doi.org/10.1016/s1001-0742(07)60067-9
Parkpian P, Klankrong K, DeLaune R, Jugsujinda A (2002) Metal leachability from sewage sludge-amended Thai soils. J Environ Sci Health Part A 37:765–791. https://doi.org/10.1081/ESE-120003588
Pazos M, Plaza A, Martín M, Lobo MC (2012) The impact of electrokinetic treatment on a loamy-sand soil properties. Chem Eng J 183:231–237. https://doi.org/10.1016/j.cej.2011.12.067
Percival JB, White HP, Goodwin TA, Smith PK, Parsons MB (2014) Mineralogy and spectral reflectance of soils and tailings from historical gold mines, Nova Scotia. Geochem Explor Environ Anal 14:3–16. https://doi.org/10.1144/geochem2011-071
Ptistišek N, Milačič R, Veber M (2001) Use of the BCR three-step sequential extraction procedure for the study of the partitioning of Cd, Pb and Zn in various soil samples. J Soils Sediments 1:25–29. https://doi.org/10.1007/BF02986466
Rauret G, López-Sánchez JF, Sahuquillo A, Rubio R, Davidson C, Ure A, Quevauviller P (1999) Improvement of the BCR three step sequential extraction procedure prior to the certification of new sediment and soil reference materials. J Environ Monit 1:57–61. https://doi.org/10.1039/a807854h
Rosas JM, Vicente F, Santos A, Romero A (2013) Soil remediation using soil washing followed by Fenton oxidation. Chem Eng J 220:125–132. https://doi.org/10.1016/j.cej.2012.11.137
Salam LB, Ilori MO, Amund OO (2015) Carbazole degradation in the soil microcosm by tropical bacterial strains. Braz J Microbiol 46:1037–1044. https://doi.org/10.1590/s1517-838246420140610
Sánchez-Andrea I, Sanz JL, Bijmans MFM, Stams AJM (2014) Sulfate reduction at low pH to remediate acid mine drainage. J Hazard Mater 269:98–109. https://doi.org/10.1016/j.jhazmat.2013.12.032
Ščančar J, Milačič R, Stražar M, Burica O, Bukovec P (2001) Environmentally safe sewage sludge disposal: the impact of liming on the behaviour of Cd, Cr, Cu, Fe, Mn, Ni, Pb, and Zn. J Environ Monit 3:226–231. https://doi.org/10.1039/B008948F
Singh SK, Tripathi VR, Jain RK, Vikram S, Garg SK (2010) An antibiotic, heavy metal resistant and halotolerant Bacillus cereus SIU1 and its thermoalkaline protease. Microbial Cell Factories 9:59. https://doi.org/10.1186/1475-2859-9-59
Subida MD, Berihuete A, Drake P, Blasco J (2013) Multivariate methods and artificial neural networks in the assessment of the response of infaunal assemblages to sediment metal contamination and organic enrichment. Sci Total Environ 450–451:289–300. https://doi.org/10.1016/j.scitotenv.2013.02.009
Svete P, Milačič R, Pihlar B (2001) Partitioning of Zn, Pb and Cd in river sediments from a lead and zinc mining area using the BCR three-step sequential extraction procedure. J Environ Monit 3:586–590. https://doi.org/10.1039/B106311C
Tewari G, Tewari L, Srivastava PC, Ram B (2010) Nickel chemical transformation in polluted soils as affected by metal source and moisture regime. Chem Speciat Bioavailab 22:141–155. https://doi.org/10.3184/095422910X12826770835261
Tsang DCW, Lo Irene MC, Surampalli Rao Y (2012) Design, implementation, and economic/societal considerations of chelant-enhanced soil washing. Chelating agents for land decontamination technologies. American Society of Civil Engineers, Reston. https://doi.org/10.1061/9780784412183.ch01
Tu C (1996) Distribution and transformation of native and added Ni fraction in puple soils from Sichuan Province (China). Pedosphere 6:183–192
van Bussel CGJ, Schroeder JP, Mahlmann L, Schulz C (2014) Aquatic accumulation of dietary metals (Fe, Zn, Cu Co, Mn) in recirculating aquaculture systems (RAS) changes body composition but not performance and health of juvenile turbot (Psetta maxima). Aquac Eng 61:35–42. https://doi.org/10.1016/j.aquaeng.2014.05.003
Vashishth A, Khanna S (2018) Toxic heavy metals tolerance in bacterial isolates based on their inducible mechanism. Int J Novel Res Life Sci. 2:34–41
Viljoen MJ (1999) An introduction to South Africa’s geological and mining heritage, Randburg, South Africa
Vulkan R, Mingelgrin U, Ben-Asher J, Frenkel H (2002) Copper and zinc speciation in the solution of a soil-sludge mixture. J Environ Qual 31:193–203
Wei G, Fan L, Zhu W, Fu Y, Yu J, Tang M (2009) Isolation and characterization of the heavy metal resistant bacteria CCNWRS33-2 isolated from root nodule of Lespedeza cuneata in gold mine tailings in China. J Hazard Mater 162:50–56. https://doi.org/10.1016/j.jhazmat.2008.05.040
Wu SC, Luo YM, Cheung KC, Wong MH (2006) Influence of bacteria on Pb and Zn speciation, mobility and bioavailability in soil: a laboratory study. Environ Pollut 144:765–773. https://doi.org/10.1016/j.envpol.2006.02.022
Xie X, Zhu W, Liu N, Liu J (2013) Bacterial community composition in reclaimed and unreclaimed tailings of Dexing copper mine, China. Afr J Biotechnol 12:4841–4849
Xie Y, Fan J, Zhu W, Amombo E, Lou Y, Chen L, Fu J (2016) Effect of heavy metals pollution on soil microbial diversity and bermudagrass genetic variation frontiers in plant. Science 7:755
Yu X et al (2014) Culturable heavy metal-resistant and plant growth promoting bacteria in V–Ti magnetite mine tailing soil from Panzhihua, China. PLoS One 9:e106618. https://doi.org/10.1371/journal.pone.0106618
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Fashola, M.O., Ngole-Jeme, V.M. & Babalola, O.O. Heavy Metal Immobilization Potential of Indigenous Bacteria Isolated from Gold Mine Tailings. Int J Environ Res 14, 71–86 (2020). https://doi.org/10.1007/s41742-019-00240-6
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DOI: https://doi.org/10.1007/s41742-019-00240-6