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Investigation of lead(II) uptake by Bacillus thuringiensis 016

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Abstract

In this work, we investigated the lead(II) biosorption mechanism of Bacillus thuringiensis (Bt) 016 through batch and microscopic experiments. We found that the maximum lead(II) biosorption capacity of Bt 016 was 164.77 mg/g (dry weight). The pH value could affect the biosorption of lead(II) in a large extent. Fourier transform infrared analyses and selective passivation experiments suggested that the carboxyl, amide and phosphate functional groups of Bt 016 played an important role in lead(II) biosorption. Scanning electron microscopy observation showed that noticeable lead(II) precipitates were accumulated on bacterial surfaces. Further transmission electron microscopy thin section analysis coupled with energy dispersive X-ray spectroscopy as well as selected area electron diffraction indicated that lead(II) immobilized on the bacteria could be transformated into random-shaped crystalline lead-containing minerals eventually. This work provided a new insight into lead(II) uptake of Bt, highlighting the potential of Bt in the restoration of lead(II) contaminated repositories.

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References

  • Aiking H, Govers H, Vantriet J (1985) Detoxification of mercury, cadmium, and lead in Klebsiella aerogenes NCTC 418 growing in continuous culture. Appl Environ Microbiol 50:1262–1267

    CAS  Google Scholar 

  • Akar T, Tunali S (2006) Biosorption characteristics of Aspergillus flavus biomass for removal of Pb(II) and Cu(II) ions from an aqueous solution. Bioresour Technol 97:1780–1787. doi:10.1016/j.biortech.2005.09.009

    Article  CAS  Google Scholar 

  • Akar ST, Gorgulu A, Anilan B, Kaynak Z, Akar T (2009) Investigation of the biosorption characteristics of lead(II) ions onto Symphoricarpus albus: Batch and dynamic flow studies. J Hazard Mater 165:126–133. doi:10.1016/j.jhazmat.2008.09.089

    Article  CAS  Google Scholar 

  • Al-Qadiri HM, Al-Alami NI, Al-Holy MA, Rasco BA (2008) Using Fourier transform infrared (FT-IR) absorbance spectroscopy and multivariate analysis to study the effect of chlorine-induced bacterial injury in water. J Agric Food Chem 56:8992–8997. doi:10.1021/jf801604p

    Article  CAS  Google Scholar 

  • Brar SK, Verma M, Tyagi RD, Valero JR, Surampalli RY (2009) Concurrent degradation of dimethyl phthalate (DMP) during production of Bacillus thuringiensis based biopesticides. J Hazard Mater 171:1016–1023. doi:10.1016/j.jhazmat.2009.06.108

    Article  CAS  Google Scholar 

  • Bravo A, Gill SS, Soberon M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49:423–435. doi:10.1016/j.toxicon.2006.11.022

    Article  CAS  Google Scholar 

  • Bueno B, Torem ML, Molina F, de Mesquita L (2008) Biosorption of lead(II), chromium(III) and copper(II) by R. opacus: Equilibrium and kinetic studies. Miner Eng 21:65–75. doi:10.1016/j.mineng.2007.08.013

    Article  CAS  Google Scholar 

  • Cheng YJ, Yan FB, Huang F, Chu WS, Pan DM, Chen Z, Zheng JS, Yu MJ, Lin Z, Wu ZY (2010) Bioremediation of Cr(VI) and Immobilization as Cr(III) by Ochrobactrum anthropi. Environ Sci Technol 44:6357–6363. doi:10.1021/es100198v

    Article  CAS  Google Scholar 

  • Cho DH, Kim EY (2003) Characterization of Pb2+ biosorption from aqueous solution by Rhodotorula glutinis. Bioprocess Biosyst Eng 25:271–277. doi:10.1007/s00449-002-0315-8

    Article  CAS  Google Scholar 

  • Dave SR, Dave RH (2009) Isolation and characterization of Bacillus thuringiensis for Acid red 119 dye decolourisation. Bioresour Technol 100:249–253. doi:10.1016/j.biortech.2008.05.019

    Article  CAS  Google Scholar 

  • De J, Ramaiah N, Vardanyan L (2008) Detoxification of toxic heavy metals by marine bacteria highly resistant to mercury. Mar Biotechnol 10:471–477. doi:10.1007/s10126-008-9083-z

    Article  CAS  Google Scholar 

  • Edris G, Alhamed Y, Alzahrani A (2014) Biosorption of cadmium and lead from aqueous solutions by Chlorella vulgaris biomass: equilibrium and kinetic study. Arab J Sci Eng 39:87–93. doi:10.1007/s13369-013-0820-x

    Article  CAS  Google Scholar 

  • Fowler BA (1998) Roles of lead-binding proteins in mediating lead bioavailability. Environ Health Perspect 1066:1585–1587. doi:10.1289/ehp.98106s61585

    Article  Google Scholar 

  • Gordon JN, Taylor A, Bennett PN (2002) Lead poisoning: case studies. Br J Clin Pharmacol 53:451–458. doi:10.1046/j.1365-2125.2002.01580.x

    Article  CAS  Google Scholar 

  • Huang TP, Xiao Y, Pan JR, Chen Z, Li LF, Xu L, Zhang LL, Guan X (2014) Aerobic Cr(VI) reduction by an indigenous soil isolate Bacillus thuringiensis BRC-ZYR2. Pedosphere 5:652–661. doi:10.1016/S1002-0160(14)60051-5

    Article  Google Scholar 

  • Kapoor A, Viraraghavan T (1997) Heavy metal biosorption sites in Aspergillus niger. Bioresour Technol 61:221–227. doi:10.1016/S0960-8524(97)00055-2

    Article  CAS  Google Scholar 

  • Karaduman AB, Yamac M, Pat Z, Amoroso MJ, Cuozzo SA (2011) Lead(II) biosorption by a metal tolerant Streptomyces strain. Environ Eng Manag J 10:1761–1771

    CAS  Google Scholar 

  • Kebria DY, Khodadadi A, Ganjidoust H, Badkoubi A, Amoozegar MA (2009) Isolation and characterization of a novel native Bacillus strain capable of degrading diesel fuel. Int J Environ Sci Technol 6:435–442. doi:10.1007/BF03326082

    Article  CAS  Google Scholar 

  • 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. doi:10.1128/AEM.70.2.855-864.2004

    Article  CAS  Google Scholar 

  • Muneer B, Rehman A, Shakoori F, Shakoori A (2009) Evaluation of consortia of microorganisms for efficient removal of hexavalent chromium from Industrial wastewater. Bull Environ Contam Toxicol 82:597–600. doi:10.1007/s00128-009-9662-3

    Article  CAS  Google Scholar 

  • Murugesan A, Ravikumar L, SathyaSelvaBala V, SenthilKumar P, Vidhyadevi T, Kirupha SD, Kalaivani SS, Krithiga S, Sivanesan S (2011) Removal of Pb(II), Cu(II) and Cd(II) ions from aqueous solution using polyazomethineamides: equilibrium and kinetic approach. Desalination 271:199–208. doi:10.1016/j.desal.2010.12.029

    Article  CAS  Google Scholar 

  • Naik MM, Dubey SK (2013) Lead resistant bacteria: lead resistance mechanisms, their applications in lead bioremediation and biomonitoring. Ecotoxicol Environ Saf 98:1–7. doi:10.1016/j.ecoenv.2013.09.039

    Article  CAS  Google Scholar 

  • Naik MM, Khanolkar D, Dubey SK (2013) Lead-resistant Providencia alcalifaciens strain 2EA bioprecipitates Pb+2 as lead phosphate. Lett Appl Microbiol 56:99–104. doi:10.1111/lam.12026

    Article  CAS  Google Scholar 

  • Pan JH, Ge XP, Liu RX, Tang HX (2006) Characteristic features of Bacillus cereus cell surfaces with biosorption of Pb(II) ions by AFM and FT-IR. Colloid Surf B 52:89–95. doi:10.1016/j.colsurfb.2006.05.016

    Article  CAS  Google Scholar 

  • Park D, Yun YS, Park JM (2005) Studies on hexavalent chromium biosorption by chemically treated biomass of Ecklonia sp. Chemosphere 60:1356–1364. doi:10.1016/j.chemosphere.2005.02.020

    Article  CAS  Google Scholar 

  • Park JH, Bolan N, Megharaj M, Naidu R (2011) Concomitant rock phosphate dissolution and lead immobilization by phosphate solubilizing bacteria (Enterobacter sp.). J Environ Manage 92:1115–1120. doi:10.1016/j.jenvman.2010.11.031

    Article  CAS  Google Scholar 

  • Rhee YJ, Hillier S, Pendlowski H, Gadd GM (2014) Pyromorphite formation in a fungal biofilm community growing on lead metal. Environ Microbiol 16:1441–1451. doi:10.1111/1462-2920.12416

    Article  CAS  Google Scholar 

  • Sahin I, Keskin SY, Keskin CS (2013) Biosorption of cadmium, manganese, nickel, lead, and zinc ions by Aspergillus tamarii. Desalin Water Treat 51:4524–4529. doi:10.1080/19443994.2012.752332

    Article  CAS  Google Scholar 

  • Sari A, Tuzen M (2009) Kinetic and equilibrium studies of biosorption of Pb(II) and Cd(II) from aqueous solution by macrofungus (Amanita rubescens) biomass. J Hazard Mater 164:1004–1011. doi:10.1016/j.jhazmat.2008.09.002

    Article  CAS  Google Scholar 

  • Sellami S, Zghal T, Cherif M, Zalila-Kolsi I, Jaoua S, Jamoussi K (2013) Screening and identification of a Bacillus thuringiensis strain S1/4 with large and efficient insecticidal activities. J Basic Microbiol 53:539–548. doi:10.1002/jobm.201100653

    Article  CAS  Google Scholar 

  • Shamala TR, Divyashree MS, Davis R, Kumari K, Vijayendra S, Raj B (2009) Production and characterization of bacterial polyhydroxyalkanoate copolymers and evaluation of their blends by fourier transform infrared spectroscopy and scanning electron microscopy. Indian J Microbiol 49:251–258. doi:10.1007/s12088-009-0031-z

    Article  CAS  Google Scholar 

  • Soberon M, Gill SS, Bravo A (2009) Signaling versus punching hole: how do Bacillus thuringiensis toxins kill insect midgut cells? Cell Mol Life Sci 66:1337–1349. doi:10.1007/s00018-008-8330-9

    Article  CAS  Google Scholar 

  • Subhashini SS, Velan M, Kaliappan S (2013) Biosorption of lead by Kluyveromyces marxianus immobilized in alginate beads. J Environ Biol 34:831–835

    Google Scholar 

  • Tong S, von Schirnding YE, Prapamontol T (2000) Environmental lead exposure: a public health problem of global dimensions. Bull World Health Organ 78:1068–1077

    CAS  Google Scholar 

  • Tuzun I, Bayramoglu G, Yalcin E, Basaran G, Celik G, Arica MY (2005) Equilibrium and kinetic studies on biosorption of Hg(II), Cd(II) and Pb(II) ions onto microalgae Chlamydomonas reinhardtii. J Environ Manage 77:85–92. doi:10.1016/j.jenvman.2005.01.028

    Article  CAS  Google Scholar 

  • Watt G, Britton A, Gilmour HG, Moore MR, Murray GD, Robertson SJ (2000) Public health implications of new guidelines for lead in drinking water: a case study in an area with historically high water lead levels. Food Chem Toxicol 381:S73–S79. doi:10.1016/S0278-6915(99)00137-4

    Article  Google Scholar 

  • Zhang BG, Fan RM, Bai ZH, Wang S, Wang L, Shi JP (2013) Biosorption characteristics of Bacillus gibsonii S-2 waste biomass for removal of lead (II) from aqueous solution. Environ Sci Pollut Res Int 20:1367–1373. doi:10.1007/s11356-012-1146-z

    Article  CAS  Google Scholar 

  • Zhuang L, Zhou SG, Wang YQ, Liu Z, Xu RX (2011) Cost-effective production of Bacillus thuringiensis biopesticides by solid-state fermentation using wastewater sludge: effects of heavy metals. Bioresour Technol 102:4820–4826. doi:10.1016/j.biortech.2010.12.098

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work is supported by the National High Technology Research and Development Program 863 (Grant No. 2011AA10A203), the National Basic Research Program of China (973 Program) (Nos. 2010CB933501, 2013CB934302), National Natural Science Foundation of China (21477129), the Outstanding Youth Fund (21125730), the Leading Talents of Fujian Province College (k8012012a) and the Technology Key Project of Fujian Province (2013H0058).

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Authors and Affiliations

  1. Key Lab of Biopesticide and Chemical Biology, Ministry of Education, Fujian Agriculture and Forestry University, and Fujian-Taiwan Joint Center for Ecological Control of Crop Pests, Fuzhou, 350002, People’s Republic of China

    Zhi Chen, Xiaohong Pan & Xiong Guan

  2. Key Laboratory of Design and Assembly of Functional Nanostructures, Fujian Institute of Research on the Structure of Matter, Chinese Academy of Sciences, Fuzhou, 350002, People’s Republic of China

    Zhi Chen, Xiaohong Pan, Hui Chen & Zhang Lin

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  1. Zhi Chen
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Correspondence to Xiong Guan.

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Chen, Z., Pan, X., Chen, H. et al. Investigation of lead(II) uptake by Bacillus thuringiensis 016. World J Microbiol Biotechnol 31, 1729–1736 (2015). https://doi.org/10.1007/s11274-015-1923-1

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