Int. J. Biosci.18( 3), 74-88, March 2021
Nickel (Ni) is an essential element which is required in low, controlled amounts for various cellular process in both the human body and in microorganisms, respectively, where it also serves its function as a cofactor for the regulation of many different enzymes, including hydrogenases and ureases. In the environment, its presence owing to anthropogenic activities over many decades has resulted in its accumulation at potentially high levels, which has since given rise to different resistance mechanisms in microbial species having adapted themselves for their survival in environmentally high Ni concentrations. In the wake of high metal concentration inside the cell, many Gram-positive and Gram-negative bacterial species have resistance mechanisms that degrade, precipitate, or pump out the toxic heavy metal ions out from the cell. In this review, we summarize the various mechanisms that enable the entry of Ni ions into bacterial cells when it is needed for biological processes, its resistance and efflux systems, as well as the various studies which have reported its bioremediation by both Gram-positive and negative bacteria, respectively, thus presenting these Ni-resistant bacterial species as potential candidates for the efficient removal of Ni from Ni-polluted environments.
Adriano DC, Wenzel WW, Vangronsveld J, Bolan NS. 2004. Role of assisted natural remediation in environmental cleanup. Geoderma 122(2-4), 121-142. https://dx.doi.org/10.1016/j.geoderma.2004.01.003
Afzal AM, Rasool MH, Waseem M, Aslam B. 2017. Assessment of heavy metal tolerance and biosorptive potential of Klebsiella variicola isolated from industrial effluents. AMB Express 7, 184-193. https://dx.doi.org/10.1186/s13568-017-0482-2
Agency for Toxic Substances and Disease Registry (ATSDR). 2005. Toxicological profile for nickel. Public Health Service. US Department of Health and Human Services.
Ahemad M, Malik A. 2012. Bioaccumulation of heavy metals by zinc resistant bacteria isolated from agricultural soils irrigated with wastewater. Bacteriology Journal 2(1), 12-21. https://dx.doi.org/10.3923/bj.2012.12.21
Akhtar MW, Sengupta D, Chowdhury A. 2009. Impact of pesticides use in agriculture: Their benefits and hazards. Interdisciplinary Toxicology 2(1), 1-12. https://dx.doi.org/10.2478/v10102-009-0001-7
Akudo S, Obuah A, Emodi G. 2018. A study of heavy metal tolerant bacteria and their potential for bioremediation. Journal of Biochemistry and Biotechnology 7(2), 791-799.
Alam M, Nadeem R, Jilani MI. 2012. Pb (II) removal from wastewater using pomegranate waste biomass. International Journal of Chemical and Biochemical Sciences 1, 24-29.
Alboghobeish H, Tahmourespour A, Doudi M. 2014. The study of nickel resistant bacteria (NiRB) isolated from wastewaters polluted with different industrial sources. Journal of Environmental Health Science and Engineering 12(1), 44-50. https://dx.doi.org/10.1186/2052-336X-12-44
Alzahrani OM, Ahamad NT. 2015. Isolation and characterization of heavy metal resistant Bacillus subtilis spp. collected from water sources of Taif Province of Saudi Arabia. International Journal of Current Microbiology and Applied Sciences 4(6), 350-357.
Ansari MI, Malik A. 2007. Biosorption of nickel and cadmium by metal resistant bacterial isolates from agricultural soil irrigated with industrial wastewater. Bioresource Technology 98(16), 3149-3153. https://dx.doi.org/10.1016/j.biortech.2006.10.008
Antić-Mladenović S, Frohne T, Kresović M, Frohne T, Kresović M, Stärk H-J, Tomić Z, Ličina V, Rinklebe J. 2017. Biogeochemistry of Ni and Pb in a periodically flooded arable soil: Fractionation and redox-induced (im)mobilization. Journal of Environmental Management 186, 141-150. https://dx.doi.org/10.1016/j.jenvman.2016.06.005
Ayangbenro AS, Babalola OO. 2017. A new strategy for heavy metal polluted environments: A review of microbial biosorbents. International Journal of Environmental Research and Public Health 14(1), 94-110. https://dx.doi.org/10.3390/ijerph14010094
Barceloux, DG. 1999. Nickel. Journal of Toxicology: Clinical Toxicology 37(2), 239-258. https://dx.doi.org/10.1081/CLT-100102423
Cempel M, Nikel G. 2006. Nickel: A review of its sources and environmental toxicology. Polish Journal of Environmental Studies 15(3), 375-382.
Chen X, Kumari D, Cao CJ, Plazac G, Achal V. 2019. A review on remediation technologies for nickel-contaminated soil. Human and Ecological Risk Assessment 26(1), 571-585. https://dx.doi.org/10.1080/10807039.2018.1539639
Cherrier MV, Cavazza C, Bochot C, Lemaire D, Fontecilla-Camps JC. 2008. Structural characterization of a putative endogenous metal chelator in the periplasmic nickel transporter NikA. Biochemistry 47(38), 9937-9943. https://dx.doi.org/10.1021/bi801051y
Chihomvu P, Stegmann P, Pillay M. 2014. Identification and characterization of heavy metal resistant bacteria from the Klip River. International Journal of Biological, Food, Veterinary and Agricultural Engineering 8(11), 1107-1117.
Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393(6685), 537-544. https://dx.doi.org/10.1038/31159
Congeevaram S, Dhanarani S, Park J, Dexilin M, Thamaraiselvi K. 2007. Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates. Journal of Hazardous Materials 146(1-2), 270-277. https://dx/doi.org/10.1016/j.jhazmat.2006.12.017
Das KK, Das SN, Dhundasi SA. 2008. Nickel, its adverse health effects and oxidative stress. Indian Journal of Medical Research 128(4), 412-425.
Davis GS, Flannery EL, Mobley HL. 2006. Helicobacter pylori HP1512 is a nickel-responsive NikR-regulated outer membrane protein. Infection and Immunity 74(12), 6811-6820. https://dx.doi.org/10.1128/IAI.01188-06
De Pina K, Desjardin V, Mandrand-Berthelot MA, Giordano G, Wu LF. 1999. Isolation and characterization of the nikR gene encoding a nickel-responsive regulator in Escherichia coli. Journal of Bacteriology, 181(2), 670-674. https://dx.doi.org/10.1128/JB.181.2.670-674.1999
Degen O, Kobayashi M, Shimizu S, Eitinger T. 1999. Selective transport of divalent cations by transition metal permeases: the Alcaligenes eutrophus HoxN and the Rhodococcus rhodochrous NhlF. Archives of Microbiology 171(3), 139-145. https://dx.doi.org/10.1007/s002030050691
Eitinger T, Suhr J, Moore L, Smith JA. 2005. Secondary transporters for nickel and cobalt ions: theme and variations. Biometals 18(4), 399-405. https://dx.doi.org/10.1007/s10534-005-3714-x
Fierros-Romero G, Gómez-Ramirez M, Arenas-Isaac GE, Pless RC, Rojas-Avelizapa NG. 2016. Identification of Bacillus megaterium and Microbacterium liquefaciens genes involved in metal resistance and metal removal. Canadian Journal of Microbiology 62(6), 505-513. https://dx.doi.org/10.1139/cjm-2015-0507
Fu C, Javedan S, Moshiri F, Maier RJ. 1994. Bacterial genes involved in incorporation of nickel into a hydrogenase enzyme. Proceedings of the National Academy of Sciences of the United States of America 91(11), 5099-5103. https://dx.doi.org/10.1073/pnas.91.11.5099
Gabr RM, Hassan SHA, Shoreit AAM. 2008. Biosorption of lead and nickel by living and non-living cells of Pseudomonas aeruginosa ASU 6a. International Biodeterioration and Biodegradation 62(2), 195-203. https://dx.doi.org/10.1016/j.ibiod.2008.01.008
Gadd GM. 1990. Heavy metal accumulation by bacterial and the microorganisms. Experientia 46, 834-840. https://dx.doi.org/10.1007/BF01935534
Gupta N, Kumar V. 2012. Identification and isolation of heavy metal (copper) resistant bacteria. Archives of Applied Science Research 4(1), 577-583.
Haq MU, Khattak RA, Puno HK, Saif MS, Memon KS. 2005. Surface and ground water contamination in NWFP and Sindh provinces with respect to trace elements. International Journal of Agriculture and Biology 7(2), 214-217.
Hiron A, Posterara B, Carrière M, Remy L, Delporte C, La Sorda M, Sanguinetti M, Juillard V, Brorezée-Durant E. 2010. A nickel ABC-transporter of Staphylococcus aureus is involved in urinary tract infection. Molecular Microbiology 77(5), 1246-1260. https://dx.doi.org/10.1111/j.1365-2958.2010.07287.x
Hong J, Wang Y, McDermott S, Cai B, Aelion CM, Lead J. 2016. The use of a physiologically-based extraction test to assess relationships between bioaccessible metals in urban soil and neurodevelopmental conditions in children. Environmental Pollution 212, 9-17. https://dx.doi.org/10.1016/j.envpol.2016.01.001
Hookoom M, Puchooa D. 2013. Isolation and identification of heavy metals tolerant bacteria from industrial and agricultural areas in Mauritius. Current Research in Microbiology and Biotechnology 1, 119-123.
Issazadeh K, Savaheli H, Momeni N. 2014. Isolation and identification of heavy metal tolerant bacteria from industrial wastewaters in Guilan Province. International Journal of Advanced Biological and Biomedical Research 2(6), 2066-2071.
Iwig JS, Rowe JL, Chivers PT. 2006. Nickel homeostasis in Escherichia coli – the rcnR-rcnA efflux pathway and its linkage to NikR function. Molecular Microbiology 62(1), 252-262. https://dx.doi.org/10.1111/j.1365-2958.2006.05369.x
Kavamura VN, Esposito E. 2010. Biotechnological strategies applied to the decontamination of soils polluted with heavy metals. Biotechnology Advances 28, 61-69. https://dx.doi.org/10.1016/j.biotechadv.2009.09.002
Kelepertzis E. 2014. Accumulation of heavy metals in agricultural soils of Mediterranean: Insights from Argolida basin, Peloponnese, Greece. Geoderma 221-222, 82-90. https://dx.doi.org/10.1016/j.geoderma.2014.01.007
Khajavian M, Wood DA, Hallajsani A, Majidian N. 2019. Simultaneous biosorption of nickel and cadmium by the brown algae Cystoseria indica characterized by isotherm and kinetic models. Applied Biological Chemistry 62, 69-81. https://dx.doi.org/10.1186/s13765-019-0477-6
Khan HM, Chaudhry ZS, Ismail M, Khan K. 2010. Assessment of radionuclides, trace metals and radionuclide transfer from soil to food of Jhangar Valley (Pakistan) using gamma-ray spectrometry. Water, Air, and Soil Pollution 213(1), 353-362. https://dx.doi.org/10.1007/s11270-010-0390-4
Lone MI, Saleem S, Mahmood T, Saifullah K, Hussain G. 2003. Heavy metal contents of vegetables irrigated by sewage/tube-well water. International Journal of Agricultural Biology 5(4), 533-535.
Ma Y, Prasad MNV, Rajkumar M, Freitas H. 2011. Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnology Advances 29(2), 248-258. https://dx.doi.org10.1016/j.biotechadv.2010.12.001
Macomber L, Hausinger RP. 2011. Mechanisms of nickel toxicity in microorganisms. Metallomics 3(11), 1153-1162. https://dx.doi.org/10.1039/c1mt00063b
Mahmood A, Malik RN. 2014. Human health risk assessment of heavy metals via consumption of contaminated vegetables collected from different irrigation sources in Lahore, Pakistan. Arabian Journal of Chemistry 7(1), 91-99. https://dx.doi.org/10.1016/j.arabjc.2013.07.002
Margaryan AA, Panosyan HH, Birkeland NK, Trchounian AH. 2013. Heavy metal accumulation and the expression of the copA and nikA genes in Bacillus subtilis AG4 isolated from the Sotk gold mine in Armenia. Biological Journal of Armenia 3(65), 51-57.
Mobley HL, Garner RM, Bauerfeind P. 1995. Helicobacter pylori nickel-transport gene nixA: Synthesis of catalytically active urease in Escherichia coli independent of growth conditions. Molecular Microbiology 16(1), 97-109. https://dx.doi.org/10.1111/j.13652958.1995.tb02395.x
Moore CM, Helmann JD. 2005. Metal ion homeostasis in Bacillus subtilis. Current Opinion in Microbiology 8(2), 188-195. https://dx.doi.org/10.1016/j.mib.2005.02.007
Naidu R, Bolan NS. 2008. Contaminant chemistry in soils: Key concepts and bioavailability, In: Chemical bioavailability in terrestrial environment. (Ed. R Naidu). Elsevier, Amsterdam, The Netherlands, p 9-38.
Navarro C, Wu LF, Mandrand-Berthelot MA. 1993. The nik operon of Escherichia coli encodes a periplasmic binding-protein-dependent transport system for nickel. Molecular Microbiology 9(6), 1181-1191. https://dx.doi.org/10.1111/j.13652958.1993.tb01247.x
Niegowski D, Eshaghi S. 2007. The CorA family: Structure and function revisited. Cellular and Molecular Life Sciences 64(19-20), 2564-2574. https://dx.doi.org/10.1007/s00018-007-7174-z
Pakistan Environmental Protection Agency. 2008. Ministry of Environment, National Standards for Drinking Water Quality (NSDWQ).
Patel PJ, Patel CP, Kalla K. 2006. Isolation and characterization of nickel uptake by nickel resistant bacterial isolate (NiRBI). Biomedical and Environmental Sciences 19(4), 297-301.
Radić S, Babic M, Skobic D, Roje V, Kozlina BP. 2009. Ecotoxicological effects of aluminum and zinc on growth and antioxidants in Lemna minor L. Ecotoxicology and Environmental Safety 73(3), 336-342. https://dx.doi.org/10.1016/j.ecoenv.2009.10.014
Ramya D, Thatheyus AJ. 2018. Microscopic investigation on the biosorption of heavy metals by bacterial cells: A review. Science International 6(1), 11-17. https://dx.doi.org/10.17311/sciintl.2018.11.17
Reis ARD, deQueiroz Barcelos JP, deSouza Osorio CRW, Santos EF, Lisboa LAM, Santini JMK, dos Santos MJD, Junior EF, Campos M, Figueiredo PAM, Lavres J, Gratão PL. 2017. A glimpse into the physiological, biochemical and nutritional status of soybean plants under Ni-stress conditions. Environmental and Experimental Botany 144, 76-87. https://dx.doi.org/10.1016/j.envexpbot.2017.10.006
Rodionov DA, Hebbeln P, Gelfand MS, Eitinger T. 2006. Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters. Journal of Bacteriology 188(1), 317-327. https://dx.doi.org/10.1128/JB.188.1.317-327.2006
Rowe JL, Starnes GL, Chivers PT. 2005. Complex transcriptional control links NikABCDE‐dependent nickel transport with hydrogenase expression in Escherichia coli. Journal of Bacteriology 187(18), 6317-6323. https://dx.doi.org/10.1128/JB.187.18.6317-6323.2005
Salvador M, Carolina G, Jose E. 2007. Novel nickel resistance genes from the rhizosphere metagenome of plants adapted to acid mine drainage. Applied Environmental Microbiology 73(19), 6001-601. https://dx.doi.org/10.1128/AEM.00048-07
Schauer K, Gouget B, Carriere M, Labigne A, de Reuse H. 2007. Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Molecular Microbiology 63(4), 1054-1068. https://dx.doi.org/10.1111/j.1365-2958.2006.05578.x
Schauer K, Rodionov DA, de Reuse H. 2008. New substrates for TonB-dependent transport: do we only see the ‘tip of the iceberg’? Trends in Biochemical Sciences 33(7), 330-338. https://dx.doi.org/10.1016/j.tibs.2008.04.012
Shah MH, Shaheen N. 2007. Statistical analysis of atmospheric trace metals and particulate fractions in Islamabad, Pakistan. Journal of Hazardous Materials 147(3), 759-767. https://dx.doi.org/10.1016/j.jhazmat.2007.01.075
Shamim S. 2014. Comparative analysis of metal resistance, accumulation and antioxidant enzymes in Cupriavidus metallidurans CH34 and Pseudomonas putida mt2 during cadmium stress. Ph. D. thesis. Department of Microbiology and Molecular Genetics, University of the Punjab, Pakistan.
Shamim S. 2018. Biosorption of heavy metals. In: Biosorption. (Eds. Derco J, and B Vrana). IntechOpen, London, United Kingdom, p 23-49. https://dx.doi.org/10.5772/intechopen.72099
Sharma S, Tiwari S, Hasan A, Saxena V, Pandey LM. 2018. Recent advances in conventional and contemporary methods for remediation of heavy metal contaminated soils. 3 Biotech 8(4), 216-234. https://dx.doi.org/10.1007/s13205-018-1237-8
Siddique A, Mumtaz M, Zaigham NA, Mallick KA, Saied S, Zahir E, Khwaja HA. 2009. Heavy metal toxicity levels in the coastal sediments of the Arabian Sea along the urban Karachi (Pakistan) region. Marine Pollution Bulletin 58(9), 1406-1414. https://dx.doi.org/10.1016/j.marpolbul.2009.06.010
Solecka J, Zajko J, Postek M, Rajnisz A. 2012. Biologically active secondary metabolites from Actinomycetes. Central European Journal of Biology 7(3), 373-390. https://dx.doi.org/10.2478/s11535-012-0036-1
Stojic N, Pucarevic M, Stojic G. 2017. Railway transportation as a source of soil pollution. Transportation Research Part D: Transport and Environment 57, 124-129. https://dx.doi.org/10.1016/j.trd.2017.09.024
Syed S, Chinthala P. 2015. Heavy metal detoxification by different Bacillus species isolated from solar salterns. Scientifica 2015, 1-8. https://dx.doi.org/10.1155/2015/319760
Toor IA, Tahir SNA. 2009. Study of arsenic concentration levels in Pakistani drinking water. Polish Journal of Environmental Studies 18(5), 907-912.
Uslu G, Tanyol M. 2006. Equilibrium and thermodynamic parameters of single and binary mixture biosorption of lead and copper ions onto Pseudomonas putida: Effect of temperature. Journal of Hazardous Materials 135(1-3), 87-93. https://dx.doi.org/10.1016/j.jhazmat.2005.11.029
Waseem A, Arshad J, Iqbal F, Sajjad A, Mehmood Z, Murtaza G. 2014. Pollution status of Pakistan: A retrospective review on heavy metal contamination of water, soil, and vegetables. BioMed Research International 2014, 1-29. https://dx.doi.org/10.1155/2014/813206
West AL, St John F, Lopes PE, MacKerell AD Jr, Pozharski E, Michel SL. 2010. Holo-Ni(II)HpNikR is an asymmetric tetramer containing two different nickel-binding sites. Journal of the American Chemical Society 132(41), 14447-14456. https://dx.doi.org/10.1021/ja104118r
Wierzba S. 2015. Biosorption of lead (II), zinc (II) and nickel (II) from industrial wastewater by Stenotrophomonas maltophilia and Bacillus subtilis. Polish Journal of Chemical Technology 17(1), 79-87.
Wu LF, Navarro C, de Pina K, Quénard M, Mandrand MA. 1994. Antagonistic effect of nickel on the fermentative growth of Escherichia coli K-12 and comparison of nickel and cobalt toxicity on the aerobic and anaerobic growth. Environmental Health Perspectives 102, 297-300. https://dx.doi.org/10.1289/ehp.94102s3297
Yilmaz EI. 2003. Metal tolerance and biosorption capacity of Bacillus circulans strain EB1. Research in Microbiology 154(6), 409-415. https://dx.doi.org/10.1016/S0923-2508(03)00116-5
Yilmaz M, Soran H, Beyatli Y. 2005. Antimicrobial activities of some Bacillus spp. strains isolated from the soil. Microbiological Research 161(2), 127-131. https://dx.doi.org/10.1016/j.micres.2005.07.001
Ziarati P, Alaedini S. 2014. The phytoremediation technique for cleaning up contaminated soil by Amaranthus sp. Journal of Environmental and Analytical Toxicology 4(2), 1-4. http://dx.doi.org/10.4172/2161-0525.1000208
Zhong M-S, Jiang L. 2017. Refining health risk assessment by incorporating site-specific background concentration and bioaccessibility data of nickel in soil. Science of the Total Environment 581-582, 866-873. https://dx.doi.org/10.1016/j.scitotenv.2017.01.036