Abstract
Bacteria exhibit a number of metabolism-dependent and metabolism-independent processes for the uptake and accumulation of toxic metals. The removal of these metals from environmental sources such as soil, sludge, and wastewaters using microbe-based technologies provide an alternative for their recovery and remediation. Lead (Pb) is a pervasive metal in the environment that adversely affects all living organisms. Many aspects of metal-microbe interactions remain unexploited in biotechnology and further development and application is necessary, particularly to the problem of Pb release into the environment. Thus, this review provides a synopsis of the most important bacterial phenotypes and biochemical attributes that are instrumental in lead bioremediation, along with what is known of their genetic background that can be exploited or improved through genetic engineering. This review also highlights the potential of Pb-resistant bacteria in bringing about detoxification of Pb-contaminated terrestrial and aquatic systems in a highly sustainable and environmental friendly manner, and the existing challenges that still lie in the path to in situ and large-scale bioremediation.
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References
Aiking H, Govers H, van’t Riet J (1985) Detoxification of mercury, cadmium, and lead in Klebsiella aerogenes NCTC 418 growing in continuous culture. Appl Environ Microbiol 50:1262–1267
Akmal M, Jianming X (2009) Microbial biomass and bacterial community changes by Pb contamination in acidic soil. J Agric Biol Sci 1:30–37
Al-Aoukaty A, Appanna VD, Huang J (1991) Exocellular and intracellular accumulation of lead in Pseudomonas fluorescens ATCC13525 is mediated by the phosphate content of the growth medium. FEMS Microbiol Lett 83:283–290
Almaguer-Cantú V, Morales-Ramos LH, Balderas-Rentería I (2011) Biosorption of lead (II) and cadmium (II) using Escherichia coli genetically engineered with mice metallothionein I. Water Sci Technol 63:1607–1613
Amoozegar MA, Ghazanfari N, Didari M (2012) Lead and cadmium bioremoval by Halomonas sp., an exopolysaccharide producing halophilic bacterium. Prog Biol Sci 2:1–11
Bhaskar PV, Bhosle NB (2006) Bacterial extracellular polymeric substances (EPS) a carrier of heavy metals in the marine food-chain. Environ Int 32:192–198
Blindauer CA, Harrison MD, Robinson AK, Parkinson JA, Bowness PW, Sadler PJ, Robinson NJ (2002) Multiple bacteria encode metallothione in sand SmtA-like fingers. Mol Microbiol 45:1421–1432
Boeckx RL (1986) Lead poisoning in children. Anal Chem 58:274A–288A
Bowman N, Patel D, Sanchez A, Xu W, Alsaffar A, Tiquia-Arashiro SM (2018) Lead-resistant bacteria from Saint Clair River sediments and Pb removal in aqueous solutions. Appl Microbiol Biotechnol 102:2391–2398
Braud A, Geoffroy V, Hoegy F, Mislin GLA, Schalk IJ (2010) Presence of the siderophores pyoverdine and pyochelin in the extracellular medium reduces toxic metal accumulation in Pseudomonas aeruginosa and increases bacterial metal tolerance. Environ Microbiol Rep 2:419–425
Burd GI, Dixon DG, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46:237–245
Chen S, Wilson DB (1997) Construction and characterization of Escherichia coli genetically engineered for bioremediation of Hg2+-contaminated environments. Appl Environ Microbiol 63:2442–2445
Chen Z, Pan X, Chen H, Lin Z, Guan X (2015) Investigation of lead(II) uptake by Bacillus thuringiensis 016. World J Microbiol Biotechnol 31:1729–1736
Cleveland LM, Minter ML, Cobb KA, Scott AA, German VF (2008) Lead hazards for pregnant women and children. Am J Nurs 108:40–49.
Das S, Dash HR, Chakraborty J (2016) Genetic basis and importance of metal resistant genes in bacteria for bioremediation of contaminated environments with toxic metal pollutants. Appl Microbiol Biotechnol 100:2967–2984
De J, Ramaiah N, Vardanyan L (2008) Detoxification of toxic heavy metals by marine bacteria highly resistant to mercury. Mar Biotechnol 10:471–477
Elliott HA, Liberati MR, Huang CP (1986) Competitive adsorption of heavy metals by soils. J Environ Qual 15:214–219
Enger ED, Smith BF (1992) Hazardous and toxic wastes. In: Enger ED, Smith BF (eds) Environmental science: a study of interrelationships, 4th ed. WC C Brown publishers, pp 444–464
Fomina M, Gadd GM (2014) Biosorption: current perspectives on concept, definition and application. Bioresour Technol 160:3–14
Gabr RM, Hassan SHA, Shoreit AAM (2008) Biosorption of lead and nickel by living and non-living cells of Pseudomonas aeruginosa ASU 6a. Int Biodeterior Biodegrad 62:195–203
Gadd GM (1990) Heavy metal accumulation by bacteria and other microorganisms. Experientia 46:834–840
Gadd GM (2009) Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. J Chem Technol Biotechnol 84:13–28
Grant LD (2009) Lead and compounds. In: Lippmann M (ed) Environmental toxicants: human exposures and their health effects. 3rd edition. Wiley-Interscience, pp 758–809
Gupta P, Diwan B (2017) Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnol Rep 13:58–71
Hamer DH (1986) Metallothioneins. Annu Rev Biochem 55:913–951
Hawari AH, Mulligan CN (2006) Biosorption of lead(II), cadmium(II), copper(II) and nickel(II) by anaerobic granular biomass. Bioresour Technol 97:692–700
Higham DP, Sadler PJ, Scawen MO (1984) Cadmium resistant Pseudomas putida synthesizes novel cadmium binding proteins. Science 225:1043–1046
Huckle JW, Morby AP, Turner JS, Robinson NJ (1993) Isolation of a prokaryotic metallothionein locus and analysis of transcriptional control by trace metal ions. Mol Microbiol 7:177–187
Jafarian V, Ghaffari F (2017) A unique metallothionein-engineered in Escherichia coli for biosorption of lead, zinc, and cadmium; absorption or adsorption? Microbiology 86:73–81
Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7:60–72
Jarosławiecka A, Piotrowska-Seget Z (2014) Lead resistance in micro-organisms. Microbiology 160:12–25
Joutey NT, Sayel H, Bahafid W, El Ghachtouli N (2015) Mechanisms of hexavalent chromium resistance and removal by microorganisms. Rev Environ Contam Toxicol 233:45–69.
Kalita D, Joshi SR (2017) Study on bioremediation of lead by exopolysaccharide producing metallophilic bacterium isolated from extreme habitat. Biotechnol Rep 16:48–57
Kumar M, Upreti RK (2000) Impact of lead stress and adaptation in Escherichia coli. Ecotoxicol Environ Saf 47:246–252
Kundu D, Mondal S, Dutta D, Haque S, Ghosh AR (2016) Accumulation and contamination of lead in different trophic levels of food chain in sewage-fed East Kolkata Wetland, West Bengal, India. Int J Environ Tech Sci 2:61–68
Kuroda K, Ueda M (2010) Engineering of microorganisms towards recovery of rare metal ions. Appl Microbiol Biotechnol 87:53−60
Leung WC, Wong MF, Chua H, Lo W, Yu PHF, Leung CK (2000) Removal and recovery of heavy metals by bacteria isolated from activated sludge treating industrial effluents and municipal wastewater. Water Sci Technol 41:233–240
Levinson HS, Mahler I, Blackwelder P, Hood T (1996) Lead resistance and sensitivity in Staphylococcus aureus. FEMS Microbiol Lett 145:421–425
Li M, Cheng X, Guo H, Yang Z (2015) Biomineralization of carbonate by Terrabacter tumescens for heavy metal removal and biogrouting applications. J Environ Eng https://doi.org/10.1061/(ASCE)EE.1943-7870.0000970. C4015005-C4015005
Li X, Peng W, Jia Y, Lu L, Fan W (2016) Bioremediation of lead contaminated soil with Rhodobacter sphaeroides. Chemosphere 156:228–235
Liu T, Nakashima S, Hirose K, Uemura Y, Shibasaka M, Katsuhara M, Kasamo K (2003) A metallothionein and CPx-ATPase handle heavy-metal tolerance in the filamentous cyanobacteria Oscillatoriabrevis. FEBS Lett 542:159–163
Lombardi PE, Peri SI, Verrengia NR (2010) ALA-D and ALA-Dreactivated as biomarkers of lead contamination in the fish Prochilodus lineatus. Ecotoxicol Environ Saf 73:1704–1711
Mejare M, Ljung S, Bulow L (1998) Selection of cadmium specificc hexapeptides and their expression as OmpA fusion proteins in Escherichia coli. Protein Eng 11:489–494
Mire CE, Tourjee JA, O’Brien WF, Ramanujachary KV, Hecht GB (2004) Lead precipitation by Vibrio harveyi: evidence for novel quorum-sensing interactions. Appl Environ Microbiol 70:855–864
Moncrieff AA, Koumides OP, Clayton BE, Patrick AD, Renwick AGC, Roberts GE (1964) Lead poisoning in children. Arch Dis Child 39:1–13.
Mugwar AJ, Harbottle MJ (2016) Toxicity effects on metal sequestration by microbially- induced carbonate precipitation. J Hazard Mater 314:237–248
Murthy S, Geetha B, Sarangi SK (2011) Effect of lead on metallothionein concentration in lead-resistant bacteria Bacillus cereus isolated from industrial effluent. Afr J Biotechnol 10:15966–15972
Mwandira W, Nakashima K, Kawasaki S (2017) Bioremediation of lead-contaminated mine waste by Pararhodobacter sp. based on the microbially induced calcium carbonate precipitation technique and its effects on strength of coarse and fine-grained sand. Ecol Eng 109:57–64
Naik MM, Dubey SK (2011) Lead-enhanced siderophore production and alteration in cell morphology in a Pb-resistant Pseudomonas aeruginosa strain 4EA. Curr Microbiol 62:409–414
Naik MM, Pandey A, Dubey SK (2012a) Biological characterization of lead-enhanced exopolysaccharide produced by a lead resistant Enterobacter cloacae strain P2B. Biodegradation 23:775–783
Naik MM, Pandey A, Dubey SK (2012b) Pseudomonas aeruginosa strain WI-1 from Mandovi estuary possesses metallothionein to alleviate lead toxicity and promotes plant growth. Ecotoxicol Environ Saf 79:129–133
Naik MM, Shamim K, Dubey SK (2012c) Biological characterization of lead resistant bacteria to explore role of bacterial metallothionein in lead resistance. Curr Sci 103:1–3
Naik MM, Khanolkar DS, Dubey SK (2013) Lead resistant Providentia alcalifaciens strain 2EA bioprecipitates Pb2+ as lead phosphate. Lett Appl Microbiol 56:99–104
Nian R, Kim DS, Nguyen T, Tan L, Kim CW, Yoo IK, Choe WS (2010) Chromatographic biopanning for the selection of peptides with high specificity to Pb2+ from phage displayed peptide library. J Chromatogr A 1217:5940–5949
Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750
Pagnanelli F, Papini MP, Toro L, Trifoni M, Veglio` F (2000) Biosorption of metal ions on Arthrobacter sp.: biomass characterization and biosorption modeling. Environ Sci Technol 34:2773–2778
Pal A, Paul AK (2008) Microbial extracellular polymeric substances: central elements in heavy metal bioremediation. Indian J Microbiol 48:49–64
Park JH, Bolan N, Meghraj M, Naidu N (2011) Concomitant rock phosphate dissolution and lead immobilization by phosphate solubilizing bacteria (Enterobacter sp.). J Environ Manag 92:1115–1120
Perez MPJA, Garcıa-Ribera R, Quesada T, Aguilera M, Ramos-Cormenzana A, Monteoliva-Sanchez M (2008) Biosorption of heavy metals by the exopolysaccharide produced by Paenibacillus jamilae. World J Microbiol Biotechnol 24:2699–2704
Raungsomboon S, Chidthaisong A, Bunnag B, Inthorn D, Harvey NW (2006) Production: composition and Pb2+ adsorption characteristics of capsular polysaccharides extracted from a cyanobacterium Gloeocapsa gelatinosa. Water Res 40:3759–3766
Raungsomboon S, Chidthaisong A, Bunnag B, Inthorn D, Harvey NW (2007) Lead (Pb2+) adsorption characteristics and sugar composition of capsular polysaccharides of cyanobacterium Calothrix marchica. Songklanakarin, Songklanakarin. J Sci Technol 29:529–541
Rifaat HM, Mahrous KF, Khalil WKB (2009) Effect of heavy metals upon metallothioneins in some Streptomyces species isolated from Egyptian soil. J Appl Sci Environ Sanit 4:197–206
Roanne TM (1999) Lead resistance in two bacterial isolates from heavy metal-contaminated soils. Microb Ecol 37:218–224
Sag Y, Tarar B, Kutsal T (2003) Biosorption of Pb(II) and Cu(II) by activated sludge in batch and continuous flow stirred reactors. Bioresour Technol 87:27–33
Saha M, Sarkar S, Sarkar B, Kumar B, Bhattacharjee S, Tribedi P (2016) Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res 23:3984–3999
Salehizadeh H, Shojaosadati SA (2003) Removal of metal ions from aqueous solution by polysaccharide produced from Bacillus firmus. Water Res 37:4231–4235
Santillan-Medrano J, Jurinak JJ (1975) The chemistry of lead and cadmium in soil: solid phase formation. Soil Sci Soc Am Proc 39:851–856
Sharma J, Shamim K, Dubeya SK, Meena RM (2017) Metallothionein assisted periplasmic lead sequestration as lead sulfite by Providencia vermicola strain SJ2A. Sci Tot Environ 579:359–365
Schwab AP, He YH, Banks MK (2005) The influence of organic ligands on the retention of lead in soil. Chemosphere 61:856–866
Shen L, Xia JL, He H, Nie ZY (2008) Comparative study on biosorption of Pb(II) and Cr(VI) by Synechococcus sp. Trans Nonferrous Metals Soc 18:1336–1342
Taghavi S, Lesaulnier C, Monchy S, Wattiez R, Mergeay M, vander Lelie D (2009) Lead(II) resistance in Cupriavidus metallidurans CH34: interplay between plasmid and chromosomally-located functions. Antonievan Leeuwenhoek 96:171–182
Templeton AS, Trainor TP, Spormann AM, Newville M, Sutton SR, Dohnalkova A, Gorby Y, Brown GE (2003) Sorption versus biomineralization of Pb(II) within Burkholderia cepacia biofilms. Environ Sci Technol 37:300–307
Tong S, von Schirnding YE, Prapamontol T (2000) Environmental lead exposure: a public health problem of global dimensions. Bull World Health Org 78:1068–1077
Tripathi M, Munot HP, Shouche Y, Meyer JM, Goel R (2005) Isolation and functional characterization of siderophore-producing lead- and cadmium-resistant Pseudomonas putida KNP9. Curr Microbiol 50:233–237
Turner JS, Glands PD, Samson ACR, Robinson NJ (1996) Zn2+-sensing by the cyanobacterial metallothione in repressor SmtB: different motifs mediate metal-induced protein-DNA dissociation. Nucl Acid Res 24:3714–3721
Varenyam A, Pan X, Zhang D, Fu Q (2012) Bioremediation of Pb-contaminated soil based on microbially induced calcite precipitation. J Microbiol Biotechnol 22:244–247
Veglio F, Beolchini F, Gasbarro A (1997) Biosorption of toxic metals: an equilibrium study using free cells of Arthrobacter sp. Process Biochem 32:99–105
Velásquez L, Dussan J (2009) Biosorption and bioaccumulation of heavy metals on dead and living biomass of Bacillus sphaericus. J Hazard Mater 167:713−716
Wei W, Zhu T, Wang Y, Yang H, Hao Z, Chen PR, Zhao J (2012) Engineering a gold-specific regulon for cell-based visual detection and recovery of gold. Chem Sci 3:1780–1784
Wei W, Liu X, Sun P, Wang X, Zhu H, Hong M, Mao ZW, Zhao J (2014) Simple whole-cell biodetection and bioremediation of heavy metals based on an engineered lead-specific operon. Environ Sci Technol 48:3363−3371
Xie B, Gu JD, Li XY (2006) Protein profiles of extracellular polymeric substances and activated sludge in a membrane biological reactor by 2-dimensional gel electrophoresis. Water Sci Technol 6:27–33
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Work in author’s laboratory is funded by the Office of Research and Sponsored Programs at the University of Michigan-Dearborn.
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Tiquia-Arashiro, S.M. Lead absorption mechanisms in bacteria as strategies for lead bioremediation. Appl Microbiol Biotechnol 102, 5437–5444 (2018). https://doi.org/10.1007/s00253-018-8969-6
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DOI: https://doi.org/10.1007/s00253-018-8969-6