Microbial bioremediation of heavy metals Review
Article Sidebar
Main Article Content
Abstract
Heavy metal pollution is one of the most serious environmental problems, due to metal ions persistence, bioavailability, and toxicity. There are many conventional physical and chemical techniques traditionally used for environmental clean-up. Due to several drawbacks regarding these methods, the use of living organisms, or bioremediation, is becoming more prevalent. Biotechnological application of microorganisms is already successfully implemented and is in constant development, with many microbial strains successfully removing heavy metals. This paper provides an overview of the main heavy metal characteristics and describes the interactions with microorganisms. Key heavy metal resistance mechanisms in microorganisms are described, as well as the main principles and types of heavy metal bioremediation methods, with details on successful pilot scale bioreactor studies. Special attention should be given to indigenous bacteria isolated from the polluted environments since such species are already adapted to contamination and possess resistance mechanisms. Utilization of bacterial biofilms or consortia could be advantageous due to higher resistance and a combination of several metabolic pathways, and thus, the possibility to remove several heavy metals simultaneously. Novel technologies covered in this review, such as nanotechnology, genetic engineering, and metagenomics, are being introduced to the field of bioremediation in order to improve the process. To conclude, bioremediation is a potentially powerful solution for cleaning the environment.
Downloads
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Authors who publish with this journal agree to the following terms:Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
Authors grant to the Publisher the following rights to the manuscript, including any supplemental material, and any parts, extracts or elements thereof:
- the right to reproduce and distribute the Manuscript in printed form, including print-on-demand;
- the right to produce prepublications, reprints, and special editions of the Manuscript;
- the right to translate the Manuscript into other languages;
- the right to reproduce the Manuscript using photomechanical or similar means including, but not limited to photocopy, and the right to distribute these reproductions;
- the right to reproduce and distribute the Manuscript electronically or optically on any and all data carriers or storage media – especially in machine readable/digitalized form on data carriers such as hard drive, CD-Rom, DVD, Blu-ray Disc (BD), Mini-Disk, data tape – and the right to reproduce and distribute the Article via these data carriers;
- the right to store the Manuscript in databases, including online databases, and the right of transmission of the Manuscript in all technical systems and modes;
- the right to make the Manuscript available to the public or to closed user groups on individual demand, for use on monitors or other readers (including e-books), and in printable form for the user, either via the internet, other online services, or via internal or external networks.
References
Čučak DI, Spasojević JM, Babić OB, Maletić SP, Simeunović JB, Rončević SD, Dalmacija BD, Tamaš I, Radnović D V. A chemical and microbiological characterization and toxicity assessment of the Pančevo industrial complex wastewater canal sediments, Serbia. Environ Sci Pollut Res. 2017;24(9):8458-8468.
Isakovski MK, Maletić S, Tamindžija D, Apostolović T, Petrović J, Tričković J, Agbaba J. Impact of hydrochar and biochar amendments on sorption and biodegradation of organophosphorus pesticides during transport through Danube alluvial sediment. J Environ Manage. 2020;274.
Dhankhar R, Hooda A. Fungal biosorption-an alternative to meet the challenges of heavy metal pollution in aqueous solutions. Environ Technol. 2011;32(5):467-491.
Fashola MO, Ngole-Jeme VM, Babalola OO. Heavy metal pollution from gold mines: Environmental effects and bacterial strategies for resistance. Int J Environ Res Public Health. 2016;13.
USEPA. Recent Developments for In Situ Treatment of Metal Contaminated Soils.; 1997.
Wuana RA, Okieimen FE. Heavy Metals in Contaminated Soils: A Review of Sources, Chemistry, Risks and Best Available Strategies for Remediation. ISRN Ecol. 2011;2011.
Gupta A, Joia J. Microbes as Potential Tool for Remediation of Heavy Metals: A Review. J Microb Biochem Technol. 2016;8(4):364-372.
Volarić A, Čučak D, Radnović D. Rezistentnost i sposobnost redukcije šestovalentnog hroma od strane bakterija izolovanih iz različitih sredina. In: Zivic M, Petkovic B, eds. Drugi Kongresa Biologa Srbije Knjiga Sažetaka. Beograd: Srpsko biološko društvo; 2018:241-242. (In Serbian)
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ. Heavy metal toxicity and the Environment. In: Luch A, ed. Molecular, Clinical and Environmental Toxicology. Vol 101. Basel: Springer; 2012:133-164.
Kastori R, Vukmirović Z, Polić P, Blagojević S, Bogdanović D, Ubavić M, Vapa L, Hadžić V, Govedarica M, Milošević N, Jarak M, Petrović N, Arsenijević-Maksimović I, Vapa M. Teški Metali u Životnoj Sredini: Heavy Metals in the Environment. Novi Sad: Naučni institut za ratarstvo i povrtarstvo; 1997.
Spasojević JM, Maletić SP, Rončević SD, Radnović D V., Čučak DI, Tričković JS, Dalmacija BD. Using chemical desorption of PAHs from sediment to model biodegradation during bioavailability assessment. J Hazard Mater. 2015;283:60-69.
John DA, Leventhal JS. Bioavailability of metals. In: du Bray EA, ed. Preliminary Compilation of Descriptive Geoenvironmental Mineral Deposit Models. ; 1995:10-18.
Ludwig B. Cytochrome c Oxidase in Prokaryotes. Vol 16.; 1987.
Nies DH. Microbial heavy-metal resistance. Appl Microbiol Biotechnol. 1999;51:730-750.
Hassen A, Saidi N, Cherif M, Boudabous A. Resistance of environmental bacteria to heavy metals. Bioresour Technol. 1998;64:7-15.
Oliveira A, Pampulha ME. Effects of long-term heavy metal contamination on soil microbial characteristics. J Biosci Bioeng. 2006;102(3):157-161.
Tamindžija D, Chromikova Z, Spaić A, Barak I, Bernier-Latmani R, Radnović D. Chromate tolerance and removal of bacterial strains isolated from uncontaminated and chromium-polluted environments. World J Microbiol Biotechnol. 2019;35(4):56.
Čučak DI, Pavlović A, Chromikova Z, Bernier-Latmani R, Barak I, Radnović D. Chromium impact on a cultivable soil bacterial community. In: Abstract Book of the 19th International Conference on Bacilli & Gram-Positive Bacteria. Berlin; 2017:267-268.
Xie Y, Fan J, Zhu W, Amombo E, Lou Y, Chen L, Fu J. Effect of heavy metals pollution on soil microbial diversity and bermudagrass genetic variation. Front Plant Sci. 2016;7(755).
Andronov EE, Petrova SN, Pinaev AG, Pershina E V., Rakhimgaliyeva S, Akhmedenov KM, Gorobets A V., Sergaliev NK. Analysis of the structure of microbial community in soils with different degrees of salinization using T-RFLP and real-time PCR techniques. Eurasian Soil Sci. 2012;45(2):147-156.
Tipayno S, Kim CG, Sa T. T-RFLP analysis of structural changes in soil bacterial communities in response to metal and metalloid contamination and initial phytoremediation. Appl Soil Ecol. 2012;61:137-146.
Yao X feng, Zhang J ming, Tian L, Guo J hua. The effect of heavy metal contamination on the bacterial community structure at Jiaozhou Bay, China. Brazilian J Microbiol. 2017;48:71-78.
Čučak D, Pavlović A, Chromikova Z, Barak I, Bernier Latmani R, Radnović D. Comparison of chromate resistance of environmental and reference strains of Bacillus genus. In: Obradović D, Ranin L, eds. Abstract Book of the XI Microbiology Congress- MIKROMED. Belgrade: Serbian microbiology society; 2017.
Cervantes C, Campos-García J. Reduction and Efflux of Chromate by Bacteria. In: Nies DH, Silve S, eds. Microbiol Monogr. Berlin: Springer; 2007.
Nanda M, Kumar V, Sharma DK. Multimetal tolerance mechanisms in bacteria: The resistance strategies acquired by bacteria that can be exploited to clean-up heavy metal contaminants from water. Aquat Toxicol. 2019;212:1-10.
Choudhury R, Srivastava S. Zinc resistance mechanisms in bacteria. Curr Sci. 2001;81(7):768-775.
Ianieva OD. Mechanisms of bacteria resistance to heavy metals. Mikrobiol Zh. 2009;71(6):54-65.
El-Helow ER, Sabry SA, Amer RM. Cadmium biosorption by a cadmium resistant strain of Bacillus thuringiensis: Regulation and optimization of cell surface affinity for metal cations. BioMetals. 2000;13:273-280.
Ramírez-Díaz MI, Díaz-Pérez C, Vargas E, Riveros-Rosas H, Campos-García J, Cervantes C. Mechanisms of bacterial resistance to chromium compounds. BioMetals. 2008;21:321-332.
Pinto E, Sigaud-Kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P. Heavy metal-induced oxidative stress in algae. J Phycol. 2003;39:1008-1018.
Roane TM, Pepper IL, Miller RM. Microbial remediation of metals. In: Lynch J, ed. Bioremediation: Principles and Applications. 2nd ed. New York: Cambridge University Press; 1996:312-340.
Gupta P, Diwan B. Bacterial Exopolysaccharide mediated heavy metal removal: A Review on biosynthesis, mechanism and remediation strategies. Biotechnol Reports. 2017;13:58-71.
Lovley DR. Dissimilatory Metal Reduction. Annu Rev Microbiol. 1993;47:263-290.
Ishibashi Y, Cervantes C, Silver S. Chromium Reduction in Pseudomonas putida. Appl Environ Microbiol. 1990;56(7):2268-2270.
Bopp LH, Ehrlich HL. Chromate resistance and reduction in Pseudomonas fluorescens strain LB300. Arch Microbiol. 1988;150:426-431.
Dey S, Paul AK. Hexavalent Chromate Reduction During Growth and by Immobilized Cells of Arthrobacter sp . SUK 1205. Sci Technol Dev. 2015;34(3):158-168.
Ackerley DF, Gonzalez CF, Keyhan M, Blake R, Matin A. Mechanism of chromate reduction by the Escherichia coli protein, NfsA, and the role of different chromate reductases in minimizing oxidative stress during chromate reduction. Environ Microbiol. 2004;6(8):851-860.
Čučak DI, Chromikova Z, Pavlović A, Radnović D, Bernier-Latmani R, Barak I. Chromate tolerance and reduction of environmental Bacillus species isolates. In: Abstract Book of the 19th International Conference on Bacilli & Gram-Positive Bacteria. Berlin; 2017:266-267.
Gupta A, Phung LT, Chakravarty L, Silver S. Mercury resistance in Bacillus cereus RC607: Transcriptional organization and two new open reading frames. J Bacteriol. 1999;181(22):7080-7086.
Nevin KP, Lovley DR. Lack of production of electron-shuttling compounds or solubilization of Fe(III) during reduction of insoluble Fe(III) oxide by Geobacter metallireducens. Appl Environ Microbiol. 2000;66(5):2248-2251.
Ji G, Silver S. Reduction of arsenate to arsenite by the ArsC protein of the arsenic resistance operon of Staphylococcus aureus plasmid pI258. Proc Natl Acad Sci U S A. 1992;89:9474-9478.
Khijniak T V., Slobodkin AI, Coker V, Renshaw JC, Livens FR, Bonch-Osmolovskaya EA, Birkeland NK, Medvedeva-Lyalikova NN, Lloyd JR. Reduction of uranium(VI) phosphate during growth of the thermophilic bacterium Thermoterrabacterium ferrireducens. Appl Environ Microbiol. 2005;71(10):6423-6426.
Myers CR, Nealson KH. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science (80- ). 1988;240(4857):1319-1321.
Sugio T, Tsujita Y, Hirayama K, Inagaki K, Tano T. Reduction of Mo6+ with Elemental Sulfur by Thiobacillus ferrooxidans. J Bacteriol. 1988;170(12):5956-5959.
Escudero L V., Casamayor EO, Chong G, Pedrós-Alió C, Demergasso C. Distribution of Microbial Arsenic Reduction, Oxidation and Extrusion Genes along a Wide Range of Environmental Arsenic Concentrations. Vos M, ed. PLoS One. 2013;8(10).
Ghosh D, Bhadury P, Routh J. Diversity of arsenite oxidizing bacterial communities in arsenic-rich deltaic aquifers in West Bengal, India. Front Microbiol. 2014;5.
Rulkens WH, Tichy R, Grotenhuis JTC. Remediation of Polluted Soil and Sediment: Perspectives and Failures. Wat Sci Tech. 1998;37(8):27-35.
Vidali M. Bioremediation. An overview. Pure Appl Chem. 2001;73(7):1163-1172.
Garbisu C, Alkorta I. Basic concepts on heavy metal soil bioremediation. Eur J Miner Process Environ Prot. 2003;3(1):58-66.
Chibuike GU, Obiora SC. Heavy metal polluted soils: Effect on plants and bioremediation methods. Appl Environ Soil Sci. 2014;2014.
Svirčev Z, Krstić S, Važić T. THE PHILOSOPHY AND APPLICABILITY OF ECOREMEDIATIONS FOR THE PROTECTION OF WATER ECOSYSTEMS. Acta Geogr Slov. 2014;54(1):179-188.
Schmoger MEV, Oven M, Grill E. Detoxification of arsenic by phytochelatins in plants. Plant Physiol. 2000;122:793-801.
Kumar A, Bisht B., Joshi V., Dhewa T. Review on Bioremediation of Polluted Environment : A Management Tool. Int J Environ Sci. 2011;1(6):1079-1093.
Gupta R, Mittal A. Bioremediation: an inexpensive yet effective strategy for remediation of heavy metal contaminated sites. Int J Adv Res. 2016;4(4):519-530.
Spasojević JM, Maletić SP, Rončević SD, Radnović D V., Čučak DI, Tričković JS, Dalmacija BD. Using chemical desorption of PAHs from sediment to model biodegradation during bioavailability assessment. J Hazard Mater. 2015;283:60-69.
Bertrand J-C, Doumenq P, Guyoneaud R, Marrot B, Martin-Laurent F, Matheron R, Moulin P, Soulas G. Applied Microbial Ecology and Bioremediation. In: Bertrand JC, Caumette P, Lebaron P, Matheron R, Normand P, Sime-Ngando T, eds. Environmental Microbiology: Fundamentals and Applications. Springer; 2011.
Joshi N. Bioremediation of heavy metals and organic pollutants through green technology. Int J Adv Sci Res. 2018;3(2):1-4.
Panneerselvam P, Choppala G, Kunhikrishnan A, Bolan N. Potential of novel bacterial consortium for the remediation of chromium contamination. Water Air Soil Pollut. 2013;224(12).
Volarić A, Tamindžija D, Radnović D. Hexavalent chromium reduction of individual bacterial strains and consortia. In: Šerbula S, ed. 27th International Conference Ecological Truth and Environmental Research - EcoTER19. Bor: University of Belgrade, Technical Faculty in Bor; 2019:240-246.
Chen Y, Gu G. Preliminary studies on continuous chromium(VI) biological removal from wastewater by anaerobic-aerobic activated sludge process. Bioresour Technol. 2005;96:1713-1721.
Quintelas C, Fonseca B, Silva B, Figueiredo H, Tavares T. Treatment of chromium(VI) solutions in a pilot-scale bioreactor through a biofilm of Arthrobacter viscosus supported on GAC. Bioresour Technol. 2009;100:220-226.
Tamindžija D, Volarić A, Radnović D. Characterization of chromate resistant and reducing bacterial strains. In: Šerbula S, ed. Proceedings 27th International Conference Ecological Truth and Environmental Research. Bor: University of Belgrade, Technical Faculty in Bor; 2019:255 – 261.
Lameiras S, Quintelas C, Tavares T. Biosorption of Cr (VI) using a bacterial biofilm supported on granular activated carbon and on zeolite. Bioresour Technol. 2008;99:801-806.
Cabrera G, Viera M, Gómez JM, Cantero D, Donati E. Bacterial removal of chromium (VI) and (III) in a continuous system. Biodegradation. 2007;18:505-513.
Altun M, Sahinkaya E, Durukan I, Bektas S, Komnitsas K. Arsenic removal in a sulfidogenic fixed-bed column bioreactor. J Hazard Mater. 2014;269:31-37.
Wagner-Döbler I. Pilot plant for bioremediation of mercury-containing industrial wastewater. Appl Microbiol Biotechnol. 2003;62:124-133.
Yan R, Yang F, Wu Y, Hu Z, Nath B, Yang L, Fang Y. Cadmium and mercury removal from non-point source wastewater by a hybrid bioreactor. Bioresour Technol. 2011;102:9927-9932.
Cerruti C, Curutchet G, Donati E. Bio-dissolution of spent nickel-cadmium batteries using Thiobacillus ferrooxidans. J Biotechnol. 1998;62:209-219.
Bayrakdar A, Sahinkaya E, Gungor M, Uyanik S, Atasoy AD. Performance of sulfidogenic anaerobic baffled reactor (ABR) treating acidic and zinc-containing wastewater. Bioresour Technol. 2009;100:4354-4360.
Chen GQ, Jiang XR. Next generation industrial biotechnology based on extremophilic bacteria. Curr Opin Biotechnol. 2018;50:94-100.
Krzmarzick MJ, Taylor DK, Fu X, McCutchan AL. Diversity and niche of archaea in bioremediation. Archaea. 2018;2018.
Sehlin HM, Lindstrom EB. Oxidation and reduction of arsenic by Sulfolobus acidocaldarius strain BC. FEMS Microbiol Lett. 1992;93:87-92.
Schelert J, Dixit V, Hoang V, Simbahan J, Drozda M, Blum P. Occurrence and Characterization of Mercury Resistance in the Hyperthermophilic Archaeon Sulfolobus solfataricus by Use of Gene Disruption. J Bacteriol. 2004;186(2):427-437.
Singh JS, Abhilash PC, Singh HB, Singh RP, Singh DP. Genetically engineered bacteria: An emerging tool for environmental remediation and future research perspectives. Gene. 2011;480:1-9.
Chromiková Z, Čučak D, Kučerová K, B. B, Radnović D, Bernier-Latmani R, Barak I. Microbial tolerance to heavy metal stress. In: Mandic-Mulec I, Danevcic T, Stefanic P, eds. Abstract Book Bacell 2019. Ljubljana: University of Ljubljana Biotechnical Faculty; 2019.
Valls M, Atrian S, De Lorenzo V, Fernández LA. Engineering a mouse metallothionein on the cell surface of Ralstonia eutropha CH34 for immobilization of heavy metals in soil. Nat Biotechnol. 2000;18:661-665.
Kostal J, Yang R, Wu CH, Mulchandani A, Chen W. Enhanced Arsenic Accumulation in Engineered Bacterial Cells Expressing ArsR. Appl Environ Microbiol. 2004;70(8):4582-4587.
Zhao XW, Zhou MH, Li QB, Lu YH, He N, Sun DH, Deng X. Simultaneous mercury bioaccumulation and cell propagation by genetically engineered Escherichia coli. Process Biochem. 2005;40:1611-1616.
Bondarenko O, Rõlova T, Kahru A, Ivask A. Bioavailability of Cd, Zn and Hg in soil to nine recombinant luminescent metal sensor bacteria. Sensors. 2008;8:6899-6923.
Dixit R, Wasiullah, Malaviya D, Pandiyan K, Singh UB, Sahu A, Shukla R, Singh BP, Rai JP, Sharma PK, Lade H, Paul D. Bioremediation of heavy metals from soil and aquatic environment: An overview of principles and criteria of fundamental processes. Sustainability. 2015;7:2189-2212.
Pandey S, Kumari M, Singh SP, Bhattacharya A, Mishra S, Chauhan PS, Mishra A. Bioremediation via nanoparticles: An innovative microbial approach. In: Handbook of Research on Uncovering New Methods for Ecosystem Management Through Bioremediation. IGI Global; 2015:491-515.
Ahmad A, Senapati S, Khan MI, Kumar R, Ramani R, Srinivas V, Sastry M. Intracellular synthesis of gold nanoparticles by a novel alkalotolerant actinomycete, Rhodococcus species. Nanotechnology. 2003;14:824-828.
Ganesh Babu MM, Gunasekaran P. Production and structural characterization of crystalline silver nanoparticles from Bacillus cereus isolate. Colloids Surfaces B Biointerfaces. 2009;74:191-195.
Perez-Gonzalez T, Jimenez-Lopez C, Neal AL, Rull-Perez F, Rodriguez-Navarro A, Fernandez-Vivas A, Iañez-Pareja E. Magnetite biomineralization induced by Shewanella oneidensis. Geochim Cosmochim Acta. 2010;74:967-979.
Němeček J, Lhotský O, Cajthaml T. Nanoscale zero-valent iron application for in situ reduction of hexavalent chromium and its effects on indigenous microorganism populations. Sci Total Environ. 2014;485-486(1):739-747.
Ash A, Revati K, Pandey BD. Microbial synthesis of iron-based nanomaterials - A review. Bull Mater Sci. 2011;34(2):191-198.
Abdeen M, Sabry S, Ghozlan H, El-Gendy AA, Carpenter EE. Microbial-Physical Synthesis of Fe and Fe3O4 Magnetic Nanoparticles Using Aspergillus Niger YESM1 and Supercritical Condition of Ethanol. J Nanomater. 2016;2016.
Zhang S, Niu H, Cai Y, Zhao X, Shi Y. Arsenite and arsenate adsorption on coprecipitated bimetal oxide magnetic nanomaterials: MnFe2O4 and CoFe2O4. Chem Eng J. 2010;158:599-607.
Cheng Z, Tan ALK, Tao Y, Shan D, Ting KE, Yin XJ. Synthesis and characterization of iron oxide nanoparticles and applications in the removal of heavy metals from industrial wastewater. Int J Photoenergy. 2012;2012.
Kaeberlein T, Lewis K, Epstein SS. Isolating "Uncultivable" Microorganisms in Pure Culture in a Simulated Natural Environment. Science (80- ). 2002;296:1127-1130.
Daniel R. The metagenomics of soil. Nat Rev Microbiol. 2005;3:470-478.
Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM. Molecular biological access to the chemistry of unknown soil microbes: A new frontier for natural products. Chem Biol. 1998;5(10):245-249.
Rondon MR, Goodman RM, Handelsman J. The Earths bounty: Assessing and accessing soil microbial diversity. Trends Biotechnol. 1999;17:403-409.
Kumar Awasthi M, Ravindran B, Sarsaiya S, Chen H, Wainaina S, Singh E, Liu T, Kumar S, Pandey A, Singh L, Zhang Z. Metagenomics for taxonomy profiling: tools and approaches. Bioengineered. 2020;11(1):356-374.
Drewniak L, Krawczyk PS, Mielnicki S, Adamska D, Sobczak A, Lipinski L, Burec-Drewniak W, Sklodowska A. Physiological and metagenomic analyses of microbial mats involved in self-purification of mine waters contaminated with heavy metals. Front Microbiol. 2016;7.
Salam LB. Unravelling the antibiotic and heavy metal resistome of a chronically polluted soil. 3 Biotech. 2020;10(238).
Feng G, Xie T, Wang X, Bai J, Tang L, Zhao H, Wei W, Wang M, Zhao Y. Metagenomic analysis of microbial community and function involved in cd-contaminated soil. BMC Microbiol. 2018;18(11):1-13.