Nashrieh Shimi va Mohandesi Shimi Iran

Nashrieh Shimi va Mohandesi Shimi Iran

A Review of Mechanisms of Resistance to Heavy Metals in Microorganisms and Their Applications in Bioremediation

Document Type : Review Article

Authors
Nazanin Bahaloo Horeh 1
Seyyed Mohammad Mousavi 1
Ahmad Khodadadi Darban 2
1 Iran, Tehran, Tarbiat Modarres University, Department of Chemical Engineering, Biotechnology Group
2 Department of Mineral Processing Engineering, Tarbiat Modares University (TMU), P.O. Box 111-14115 Tehran, I.R. IRAN
Abstract
One of the most important issues in the world is the environmental pollution caused by toxic metals. Human activities such as the extraction of metals from mines, industrial wastes production led to the heavy metals accumulation in the environment that cause toxic effects on living organisms. On the other hand, the only way of environmental cleanup is metal removing, recycling and reusing, due to lack of metals biodegradability. For this purpose, the use of biological processes and microorganisms is one of the adopted solutions. Biological processes are based on interactions between microorganisms and metals. The identification of microorganisms resistant to metals plays an important role in the removal of environmental pollution. In order to survive, microorganisms can be resistant to heavy metals by different mechanisms as they contacted with metals. In this paper, the effects of toxic metals on microorganisms, resistance mechanisms, and applications of resistance mechanisms to metals such as bioaccumulation, biosorption, biotransformation, biomineralization and bioleaching of metals have been studied. The results illustrate that the use of microorganisms is a natural, sustainable and economical solution to recycle wastes and clean up the environment from heavy metals and could have a high percentage of valuable and toxic metals recovery and/or detoxification.
Keywords
Heavy metals
Toxicity
Mechanisms of resistance
Bioremediation

Subjects

[1] Motaghed M., Mousavi SM., Rastegar SO., Shojaosadati SA., Platinum And Rhenium Extraction From A Spent Refinery Catalyst Using Bacillus megaterium As A Cyanogenic Bacterium: Statistical Modeling And Process Optimization, Bioresour Technol, 171: 401–09 (2014).
[2] Li L., Ge J., Chen R., Wu F., Chen S., Zhang X., Environmental Friendly Leaching Reagent For Cobalt and Lithium Recovery from Spent Lithium-ion Batteries., Waste Manag, 30(12): 2615–21 (2010).
[3] حسنی، ع؛ اعتمادی فر، ز؛ نحوی، ا؛ بررسی تحمل و جذب فلزات مس و سرب توسط سه سویه استاندارد مخمر، مجله پژوهش‌های سلولی و مولکولی (مجله زیست‌شناسی ایران)، (2)27: 91 تا 179 (1393).
[4] Arshadi M., Mousavi S.M., Simultaneous Recovery Of Ni and Cu from Computer-Printed Circuit Boards Using Bioleaching: Statistical Evaluation and Optimization, Bioresour Technol, 174: 233–42 (2014).
[5] Kalkan E., Nadaroglu H., Dikbas N., Tasgin E., Celebi N., Bacteria-Modified Red Mud for Adsorption of Cadmium Ions from Aqueous Solutions, Pol. J. Env. Stud., 22: 105–17 (2013).
[6] Ahmed M.J.K., Ahmaruzzaman M., A Review on Potential Usage of Industrial Waste Materials for Binding Heavy Metal Ions from Aqueous Solutions, J Water Process Eng, 10: 39-47 (2016).
[7] طیبان، س؛ ترابی، ا، نجف پور، ع؛ علیدادی، ح؛ ززولی، م؛ بررسی روش‌های بیوجذب فلزات سنگین کروم و کادمیوم از پساب‌های صنعتی با استفاده از زائدات کشاورزی ( مطالعه مروری)، نوید نو، (58)۱۶، (13۹۱).
[8]    Gadd G.M., Metals, Minerals, and Microbes: Geomicrobiology and Bioremediation, Microbiology Society, 156(3): 609–43 (2010).
[9] Bruins M.R., Kapil S., Oehme F.W., Microbial Resistance to Metals in the Environment, Ecotoxicol. Environ. Saf., 45(3): 198-207 (2000).
[10] Harrison J.J., Ceri H., Turner R.J., Multimetal Resistance and Tolerance in Microbial Biofilms, Nat Rev Microbiol, 5(12): 928-38 (2007).
11[] مرادی پور، ه؛ آبنوسی، م؛ امیرجانی، م؛ مهدیه، م، تأثیر فلز کادمیم بر توانائی زیستی و فعالیت برخی آنزیم‌های پاداکسندگی در پینه گیاه پریوش (Catharanthus Roseus)، علوم باغبانی ایران، (1)47: 21 تا 31 (1395).
[12] Huang K., Li J., Xu Z., Characterization and Recycling of Cadmium from Waste Nickel–Cadmium Batteries, Waste Manag, 30(11): 2292-98 (2010).
[13] Zeng G., Luo S., Deng X., Li L., Au C., Influence Of Silver Ions On Bioleaching Of Cobalt From Spent Lithium Batteries, Miner Eng, 49:40–44 (2013).
[14] Jadhav U.U., Hocheng H., A Review of Recovery of Metals from Industrial Waste, J. Achiev. Mater. Manuf. Eng., 54(2): 159-67 (2012).
[15] خردمند، ف؛ موسوی، ع؛ نورمحمدی، ع؛ سینایی، ب، عنصر روی و مکانیسم­های مولکولی دخیل در هموستاز آن، مجله دانشکده پیراپزشکی ارتش جمهوری اسلامی ایران، (1)4: 33 تا 38 (1388).
[16] Markowicz A., Płociniczak T., Piotrowska-Seget Z., Response of Bacteria to Heavy Metals Measured as Changes in FAME Profiles, Polish J Environ Stud, 19(5): 957-65 (2010).
[17] Amiri F., Yaghmaei S., Mousavi S.M., Bioleaching of Tungsten-Rich Spent Hydrocracking Catalyst Using Penicillium simplicissimum, Bioresour Technol, 102(2):1567–73 (2011).
[18] Fashola M.O., Ngole-Jeme V.M., Babalola O.O., Heavy Metal Pollution from Gold Mines: Environmental Effects and Bacterial Strategies for Resistance, Int J Environ Res Public Health, 13(11): 1-20 (2016).
[19] حسینی، س؛ اوستان، ش؛ اصغرزاد، ن؛ نجفی ن، عوامل مؤثر بر اکسایشCr(III)  به Cr(VI) در تعدادی از خاک‌های شمال و شمال غرب ایران, نشریه دانش آب و خاک, (4)22: 31 تا 49 (1391).
[20] منصوری، ط؛ گلچین، ا؛ نیستانی، م؛ کوهستانی، ح، بررسی تأثیر جاذب‌های نانوذرات هماتیت و کوپلیمر اکریلیکی بر توزیع اجزاء آرسنیک در خاک، نشریه پژوهش‌های خاک (علوم خاک و آب)، (1)31: 89 تا 102 (1396).
[21] Santhiya D., Ting Y-P., Use of Adapted Aspergillus niger in the Bioleaching of Spent Refinery Processing Catalyst., J Biotechnol, 121(1):62–74 (2006).
[22] Yang J., Wang Q., Wang Q., Wu T., Heavy Metals Extraction from Municipal Solid Waste Incineration Fly Ash Using Adapted Metal Tolerant Aspergillus niger., Bioresour Technol, 100(1):254–60 (2009).
[23] Kelly C.J., Tumsaroj N., Lajoie C.A., Assessing Wastewater Metal Toxicity With Bacterial Bioluminescence in a Bench-Scale Wastewater Treatment System, Water Res, 38(2):423–31 (2004).
[24] کفیل زاده، ف؛ چیت تایی، م، بررسی میزان رشد، مقاومت و توانایی حذف فلز روی در باکتری­های مقاوم جداشده از آب و رسوبات رودخانه کارون، مجله سلامت و بهداشت، (2)5: 14 تا 103 (1393).
[25] لکزیان، ا، تعیین آستانه سمیت فلزات مس و روی در باکتری E. Coli (حسگر زیستی), مجله آب و خاک (علوم و صنایع کشاورزی), (1)23: 1 تا 7 (1388).
]26[ محسنی، م؛ معقول، ش، سنجش سمیت فلزات سنگین سرب، کادمیوم و مس توسط باکتری نورافشان 
جدا شده از دریای مازندران، مجله پژوهش‌های سلولی و مولکولی (مجله زیست شناسی ایران)، (4)28: 
588 تا 598 (139۴).
[27] Gikas P., Single and Combined Effects of Nickel (Ni (II)) and Cobalt (Co (II)) Ions on Activated Sludge and on other Aerobic Microorganisms: A Review, J. Hazard. Mater., 159(2):187–203 (2008).
[28] Sandrin T.R., Maier R.M., Effect of pH on Cadmium Toxicity, Speciation, and Accumulation During Naphthalene Biodegradation, Environ. Toxicol. Chem., 21(10): 2075–79 (2002).
[29] Hunter M.T., Painter J.C., Eckenfelder Jr WW., The Effects of Sludge Age and Metal Concentration on Copper Equilibrium in the Activated Sludge Process, Environ. Technol., 4(11): 475–484 (1983).
[30] Dupont C.L., Grass G., Rensing C., Copper Toxicity and the Origin Of Bacterial Resistance—New Insights and Applications, Metallomics, Metallomics, 3(11):1109–18 (2011).
[31] Murthy S., Bali G., Sarangi SK., Lead Biosorption by a Bacterium Isolated From Industrial Effluents, Int J Microbiol Res, 4(3):192 (2012).
[32] مشکینی، م؛ ایران نژاد، م؛ آزادمهر، ا؛ سمیعی بیرق، ع، بررسی امکان استخراج روی از کانی‌های کم عیار اکسیدی با استفاده از باکتری هتروتروف Pseudomonas aeruginosa و تطبیق باکتری به غلظت بالای یون روی، نشریه شیمی و مهندسی شیمی ایران، (1)32: 93 تا 100 (2013).
[33] Kang C-H., So J-S., Heavy Metal and Antibiotic Resistance of Ureolytic Bacteria and Their Immobilization of Heavy Metals, Ecol. Eng., 97: 304-312 (2016).
[34] Ahalya N., Ramachandra T.V., Kanamadi R.D., Biosorption of Heavy Metals, Res. J. Chem. Env., 7(4): 71–79 (2003).
[35] Deng X., Chai L., Yang Z., Tang C., Tong H., Yuan P., Bioleaching of Heavy Metals from a Contaminated Soil Using Indigenous Penicillium chrysogenum Strain F1., J. Hazard. Mater., 233–234:25–32 (2012).
[36] Park J.H., Chon H-T., Characterization of Cadmium Biosorption by Exiguobacterium Sp. Isolated From Farmland Soil Near Cu-Pb-Zn Mine, Environ. Sci. Pollut. Res., 23(12): 11814–22 (2016).
[37] Prabhakaran P., Ashraf M.A., Aqma W.S., Microbial Stress Response to Heavy Metals in the Environment, RSC Adv., 6(111): 109862-77 (2016).
[38] Bautista-Hernández D.A., Ramírez-Burgos L.I., Duran-Páramo E., Fernández-Linares L., Zinc and Lead Biosorption by Delftia Tsuruhatensis: A Bacterial Strain Resistant to Metals Isolated from Mine Tailings, J. Water Resour. Prot,. 4(4): 207-  (2012).
[39] Wei G., Fan L., Zhu W., Fu Y., Yu J., Tang M., 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(1): 50-56 (2009).
[40] Monachese M., Burton J.P., Reid G., Bioremediation and Tolerance of Humans to Heavy Metals Through Microbial Processes: A Potential Role for Probiotics?, Appl Environ Microbiol, 78(18): 6397-404 (2012).
[41] Konhauser KO.,"Introduction to Geomicrobiology", John Wiley & Sons (2009).
[42] محمدزاده کرکرق، ر؛ چرم، م؛ معتمدی، ح؛ محبت، ع، جذب زیستی و تجمع زیستی کادمیم و نیکل در محلول رقابتی توسط سه جدایه باکتری از خاک آلوده به لجن فاضلاب، مجله دنیای میکروب­ها، (3)7: 241 تا 251 (1393).
[43] Gourdon R., Bhende S., Rus E., Sofer S.S., Comparison of Cadmium Biosorption by Gram-positive and Gram-negative Bacteria from Activated Sludge, Biotechnol. Lett., 12(11): 839–42 (1990).
[44] Dopson M., Baker-Austin C., Koppineedi P.R., Bond PL., Growth in Sulfidic Mineral Environments: Metal Resistance Mechanisms in Acidophilic Micro-organisms, Microbiology Society, 149(8):1959–70 (2003).
[45] Choudhury R., Srivastava S., Zinc Resistance Mechanisms in Bacteria, Curr. Sci., 81(7):768–75 (2001).
[46] Chojnacka K., Biosorption and Bioaccumulation–the Prospects for Practical Applications, Environ. Int., 36(3): 299-307 (2010).
[47] Botello-Morte L., Gonzalez A., Bes M.T., Peleato M.L., Fillat M.F., Functional Genomics of Metalloregulators in Cyanobacteria, Genom Cyanobact, 65: 107-156 (2013).
[48] Bahaloo-Horeh N., Mousavi S.M., Enhanced Recovery of Valuable Metals from Spent Lithium-ion Batteries Through Optimization of Organic Acids Produced By Aspergillus niger, Waste. Manag., 60: 666-679 (2017).
[49] اسلامی، ا؛ نعمتی، ر، بررسی حذف فلزات سنگین از محیط­های آبی با استفاده از فناوری زیست پالایی (مطالعه مروری), فصلنامه بهداشت در عرصه، (2)3: 43 تا 51 (1394).
[50] Singh S., Barla A., Shrivastava A., Bose S., Interplay of Arsenic Alteration in Plant Soil and Water: Distribution, Contamination and Remediation, Glob J Multidiscip Stud Available online www gjms co, 3(11) (2014).
[51] Gadd G.M., Microbial Influence on Metal Mobility and Application for Bioremediation, Geoderma, 122(2): 109–119 (2004).
[52] Chang J-S., Kim Y-H., Kim K-W., The Ars Genotype Characterization of Arsenic-resistant Bacteria from Arsenic-Contaminated Gold–silver Mines in the Republic of Korea, Appl. Microbiol. Biotechnol., 80(1): 155-165 (2008).
[53] Kazemi S., Faezi-Ghasemi M., Effect of Heavy Metals Stresses on Growth, Surface Structure and Biochemical Features of Listeria monocytogenes PTCC 1297: An in Vitro Study, Avicenna. J. Clin. Microbiol. Infect., 2(4): 15-19 (2015).
[54] Asghari I., Mousavi S.M., Amiri F., Tavassoli S., Bioleaching of Spent Refinery Catalysts: A Review, J. Ind. Eng. Chem., 19(4): 1069-1081 (2013).
[55] Hoque M.E., Philip O.J., Biotechnological Recovery of Heavy Metals from Secondary Sources—An Overview, Mater. Sci. Eng. C, 31(2): 57-66 (2011).
[56] Panwichian S., Kantachote D., Wittayaweerasak B., Mallavarapu M., Removal of Heavy Metals by Exopolymeric Substances Produced by Resistant Purple Nonsulfur Bacteria Isolated from Contaminated Shrimp Ponds, Electron. J. Biotechnol., 14(4): 1-13 (2011).
[57] احمدی اسبچین، س؛ پوربابایی، ا؛ آندره، ا، بررسی فرایند جذب زیستی همزمان دو فلز روی/ نیکل به وسیله جلبک قهوه‌ای فوکوس سراتوس، نشریه شیمی و مهندسی شیمی ایران، (1)32: 85 تا 91 (2013).
[58] Sana S., Roostaazad R., Yaghmaei S., Biosorption of Uranium (VI) from Aqueous Solution 
by Pretreated Aspergillus niger Using Sodium Hydroxide, Iran. J. Chem. Chem. Eng. (IJCCE), 34(1): 65–74 (2015).
[59] Das S., Biosorption of Chromium and Nickel by Dried Biomass of Cyanobacterium Oscillatoria Laetevirens, Int. J Environ. Sci., 3(1): 341-352 (2012).
[60] آسمان، ا؛ سیاف، ح، حذف کروم شش ظرفیتی با استفاده پودر جلبک سبز اسپیروژیرا پرتیکالیس از محلول­های آبی، مجله علمی پژوهشی دانشگاه علوم پزشکی سبزوار، (3)۲۴: ۱۶۵ تا ۱۷۱ (۱۳۹۶).
[61] Kim S.U., Cheong Y.H., Seo D.C., Hur J.S., Heo J.S., Cho J.S., Characterisation of Heavy Metal Tolerance and Biosorption Capacity of Bacterium Strain CPB4 (Bacillus Spp.), Water. Sci. Technol., 55(1–2): 105-111 (2007).
[62] Abd-Elnaby H., Abou-Elela G.M., El-Sersy N.A., Cadmium Resisting Bacteria in Alexandria Eastern Harbor (Egypt) and Optimization of Cadmium Bioaccumulation by Vibrio harveyi, African. J. Biotechnol., 10(17): 3412-3423 (2011).
[63] گلبابایی، ف؛ قهری، ا؛ صعودی، م؛ رحیمی فروشانی، ع؛ تیرگر، آ؛ مطالعه‌های تعادل و سینتیک جذب زیستی کروم شش ظرفیتی از محلول‌های آبی با استفاده از دانه‌های پلیمر زانتان B82، نشریه شیمی و مهندسی شیمی ایران، (2)30: 11 تا 24 (2011).
[64] Lefebvre D.D., Kelly D., Budd K., Biotransformation of Hg (II) By Cyanobacteria, Appl. Environ. Microbiol., 73(1): 243-249 (2007).
[65] Francis A.J., Biotransformation of Uranium and Other Actinides in Radioactive Wastes, 
J. Alloy.s Compd., 271: 78–84 (1998).
[66] Stasinakis A.S., Thomaidis N.S., Fate and Biotransformation of Metal And Metalloid Species 
in Biological Wastewater Treatment Processes, Crit. Rev. Environ. Sci. Technol., 40(4): 307-364 (2010).
[67] Kaewdoung B., Sutjaritvorakul T., Gadd G.M., Whalley A.J.S., Sihanonth P., Heavy Metal Tolerance and Biotransformation of Toxic Metal Compounds by New Isolates of Wood-rotting Fungi from Thailand, Geomicrobiol. J., 33(3–4): 283-288 (2016).
[68] Dixit R., Malaviya D., Pandiyan K., Singh U.B., Sahu A., Shukla R., Singh B.P., Rai J.P., Lade H., Bioremediation of Heavy Metals from Soil and Aquatic Environment: an Overview of Principles and Criteria of Fundamental Processes, Sustainability, 7(2): 2189–2212 (2015).
[69] Govarthanan M., Lee K-J., Cho M., Kim J.S., Kamala-Kannan S., Oh B-T., Significance of Autochthonous Bacillus Sp. KK1 on Biomineralization of Lead in Mine Tailings, Chemosphere, 90(8): 2267–2272 (2013).
[70] Bai H-J., Zhang Z-M., Microbial Synthesis of Semiconductor Lead Sulfide Nanoparticles Using Immobilized Rhodobacter sphaeroides, Mater. Lett., 63(9):764–66 (2009).
[71] Salome K.R., Beazley M.J., Webb S.M., Sobecky P.A., Taillefert M., Biomineralization of 
U(VI) Phosphate Promoted by Microbially-mediated Phytate Hydrolysis in Contaminated Soils, Geochim. Cosmochim. Acta., 197: 27–42 (2017).
[72] Li M., Cheng X., Guo H., Heavy Metal Removal by Biomineralization of Urease Producing Bacteria Isolated from Soil, Int Biodeterior Biodegradation, 76: 81–85 (2013).
[73] Horeh N.B., Mousavi S.M., Shojaosadati S.A., Bioleaching of Valuable Metals from Spent Lithium-ion Mobile Phone Batteries Using Aspergillus niger, J. Power. Sources., 320: 257–266 (2016).
[74] Amiri F., Mousavi S.M., Yaghmaei S., Barati M., Bioleaching Kinetics of A Spent Refinery Catalyst Using Aspergillus niger at Optimal Conditions, Biochem. Eng. J., 67: 208-217 (2012).
[75] Arshadi M., Mousavi SM., Multi-objective Optimization of Heavy Metals Bioleaching from Discarded Mobile Phone PCBs: Simultaneous Cu and Ni Recovery Using Acidithiobacillus ferrooxidans, Sep. Purif. Technol., 147: 210–219 (2015).
[76] Ilyas S., Ruan C., Bhatti H.N., Ghauri M.A., Anwar M.A., Column Bioleaching of Metals from Electronic Scrap, Hydrometallurgy, 101(3): 135-140 (2010).
[77] Qu Y., Lian B., Mo B., Liu C., Bioleaching of Heavy Metals from Red Mud Using Aspergillus niger, Hydrometallurgy, 136: 71–77 (2013).
[78] Ijadi Bajestani M., Mousavi S.M., Shojaosadati S.A., Bioleaching of Heavy Metals from Spent Household Batteries Using Acidithiobacillus ferrooxidans: Statistical Evaluation and Optimization, Sep. Purif. Technol., 132: 309-316 (2014).
[79] Jang H-C., Valix M., Overcoming The Bacteriostatic Effects of Heavy Metals on Acidithiobacillus thiooxidans for Direct Bioleaching of Saprolitic Ni Laterite Ores, Hydrometallurgy, 168: 21-25 (2017).
[80] Amiri F., Yaghmaei S., Mousavi S.M., Sheibani S., Recovery of Metals from Spent Refinery Hydrocracking Catalyst Using Adapted Aspergillus niger, Hydrometallurgy, 109(1): 65–71 (2011).
[81] Rastegar S.O., Mousavi S.M., Shojaosadati S.A., Mamoory R.S., Bioleaching of V, Ni, and Cu From Residual Produced in Oil Fired Furnaces Using Acidithiobacillus ferrooxidans, Hydrometallurgy, 157:50–59 (2015).
[82] Rasoulnia P., Mousavi S.M., Rastegar S.O., Azargoshasb H., Fungal Leaching of Valuable Metals from A Power Plant Residual Ash Using Penicillium simplicissimum: Evaluation of Thermal Pretreatment and Different Bioleaching Methods, Waste. Manag., 52:309-317 (2016).
[83] Arshadi M., Mousavi S.M., Rasoulnia P., Enhancement of Simultaneous Gold and Copper Recovery from Discarded Mobile Phone PCBs Using Bacillus megaterium: RSM Based Optimization of Effective Factors and Evaluation of Their Interactions, Waste. Manag., (2016).
[84] نجف آبادی، ع؛ عبدالهی، م؛ خدادادی دربان، ا؛ موسوی، س، پیش‌فرآوری زیستی کانه‌ی مقاوم طلا با استفاده از قارچ فانروکیت کرایسوسپوریوم، نشریه شیمی و مهندسی شیمی ایران، (3)34: 49 تا 59 (2015).
[85] Ghorbani Y., Oliazadeh M., Shahverdi A.R., Microbiological Leaching of Al from the Waste of Bayer Process by Some Selective Fungi, Iran. J. Chem. Chem. Eng. (IJCCE), 28(1):109–15 (2009).
[86] Vakilchap F., Mousavi S.M., Shojaosadati S.A., Role of Aspergillus niger in Recovery Enhancement of Valuable Metals from Produced Red Mud in Bayer Process, Bioresour. Technol., 218:991-998 (2016).
[87] Simsek O., Arısoy M., A New Approach for Evaluating Wastes: Bioleaching, Hacettepe J. Biol. Chem., 35: 17–24 (2007).
[88] Mishra D., Rhee Y.H., Microbial Leaching of Metals from Solid Industrial Wastes, J. icrobiol., 52(1):1–7 (2014).