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The role of electron shuttle enhances Fe(III)-mediated reduction of Cr(VI) by Shewanella oneidensis MR-1

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Abstract

Chromate is one of the hazardous toxic pollutants. Reduction of Cr(VI) to Cr(III) has shown to reduce the toxicity of chromate. This work examined the reduction of Cr(VI) using an anaerobic batch cultures of Shewanella oneidensis MR-1 containing Fe(III). To do so, 10 mg/L Cr(VI) was reduced to Cr(III) within 3 days along with the oxidization of Fe(II) to Fe(III). The removal rate of Cr(VI) increased with increasing the concentration of Fe(III). In the absence of Cr(VI), the Fe(II) concentration of the batch culture increased with the growth of S. oneidensis MR-1. These data showed that S. oneidensis MR-1 could reduce Fe(III) into Fe(II), resulting in reduction of Cr(VI) to Cr(III). During this process, the anthraquinone-2,6-disulfonate (AQDS) acted as an electron shuttle. Microscopic analysis showed that Cr(VI) had toxic effects on S. oneidensis MR-1 due to the appearance of Cr species on the bacterial surface. Cr2O3 or Cr(OH)3 precipitates formed during Cr(VI) reduction was identified using X-ray photoelectron spectroscopy. The AQDS as an electron shuttle enhanced the Cr(VI) reduction by S. oneidensis MR-1. Microbial reduction of Cr(VI) can be a useful technique for Cr detoxification.

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References

  • Ahmad T, Mustafa S, Naeem A, Anwar F, Shah KH, Mehmood T (2014) Selective sorption of chromium from tannery wastes by hybrid cation exchange resin. Asian J Chem 26(14):4351–4355

    Article  CAS  Google Scholar 

  • Ai Z, Cheng Y, Zhang L, Qiu J (2008) Efficient removal of Cr(VI) from aqueous solution with Fe@Fe2O3 core-shell nanowires. Environ Sci Technol 42(18):6955–6960

    Article  CAS  Google Scholar 

  • Belchik SM, Kennedy DW, Dohnalkova AC, Wang Y, Sevinc PC, Wu H, Lin Y, Lu HP, Fredrickson JK, Shi L (2011) Extracellular reduction of hexavalent chromium by cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Appl Environ Microbiol 77(12):4035–4041

    Article  CAS  Google Scholar 

  • Carvalho AAC, Silvestre DM, Leme FO, Naozuka J, Intima DP, Nomura CS (2019) Feasibility of measuring Cr(III) and Cr(VI) in water by laser-induced breakdown spectroscopy using ceramics as the solid support. Microchem J 144:33–38

    Article  CAS  Google Scholar 

  • Chardin B, Giudici-Orticoni MT, De Luca G, Guigliarelli B, Bruschi M (2003) Hydrogenases in sulfate-reducing bacteria function as chromium reductase’. Appl Microbiol Biotechnol 63(3):315–321

    Article  CAS  Google Scholar 

  • Chourey K, Thompson MR, Shah M, Zhang B, VerBerkmoes NC, Thompson DK, Hettich RL (2009) Comparative temporal proteomics of a response regulator (SO2426)-deficient strain and wild-type Shewanella oneidensis MR-1 during chromate transformation. J Proteome Res 8(1):59–71

    Article  CAS  Google Scholar 

  • Cummings DE, Fendorf S, Singh N, Sani RK, Peyton BM, Magnuson TS (2007) Reduction of Cr(VI) under acidic conditions by the facultative Fe(III)-reducing bacterium Acidiphilium cryptum. Environ Sci Technol 41(1):146–152

    Article  CAS  Google Scholar 

  • Daulton TL, Little BJ, Lowe K, Jones-Meehan J (2002) Electron energy loss spectroscopy techniques for the study of microbial chromium(VI) reduction’. J Microbiol Methods 50(1):39–54

    Article  CAS  Google Scholar 

  • Ding SL, Xie LH, Dong LX, Liu J, Zhao LG (2016) Development of a reagent kit for rapid determination of chromium (VI). J Soc Leather Technol Chem 100(4):175–181

    CAS  Google Scholar 

  • Du Y, Liu X, Li J, Li L, Si Y (2018) Reduction of Cr(VI) by Shewanella oneidensis MR-1 and its influencing factors. China Environ Sci 38(7):2740–2745

    Google Scholar 

  • Field EK, Gerlach R, Viamajala S, Jennings LK, Peyton BM, Apel WA (2013) Hexavalent chromium reduction by Cellulomonas sp. strain ES6: the influence of carbon source, iron minerals, and electron shuttling compounds. Biodegradation 24(3):437–450

    Article  CAS  Google Scholar 

  • Fredrickson JK, Kostandarithes HM, Li SW, Plymale AE, Daly MJ (2000) Reduction of Fe(III), Cr(VI), U(VI), and Tc(VII) by deinococcus radiodurans R1. Appl Environ Microbiol 66(5):2006–2011

    Article  CAS  Google Scholar 

  • Fu F, Min H, Bing T, Han W, Cheng Z (2015) Removal of Cr(VI) from wastewater using acid-washed zero-valent iron catalyzed by polyoxometalate under acid conditions: efficacy, reaction mechanism and influencing factors. J Taiwan Inst Chem Eng 47:177–181

    Article  CAS  Google Scholar 

  • Geelhoed JS, Meeussen JCL, Roe MJ, Hillier S, Thomas RP, Farmer JG, Paterson E (2003) Chromium remediation or release? Effect of iron(II) sulfate addition on chromium(VI) leaching from columns of chromite ore processing residue. Environ Sci Technol 37(14):3206–3213

    Article  CAS  Google Scholar 

  • Hong Y, Wu P, Li W, Gu J, Duan S (2012) Humic analog AQDS and AQS as an electron mediator can enhance chromate reduction by Bacillus sp. strain 3C(3). Appl Microbiol Biotechnol 93(6):2661–2668

    Article  CAS  Google Scholar 

  • Jiang B, Gong YF, Gao JN, Sun T, Liu YJ, Oturan N, Oturan MA (2019) The reduction of Cr(VI) to Cr(III) mediated by environmentally relevant carboxylic acids: state-of-the-art and perspectives. J Hazard Mater 365:205–226

    Article  CAS  Google Scholar 

  • Kantar C, Cetin Z, Demiray H (2008) In situ stabilization of chromium(VI) in polluted soils using organic ligands: the role of galacturonic, glucuronic and alginic acids. J Hazard Mater 159(2–3):287–293

    Article  CAS  Google Scholar 

  • Li YY, Liang JL, Yang ZH, Wang H, Liu YS (2019) Reduction and immobilization of hexavalent chromium in chromite ore processing residue using amorphous FeS2. Sci Total Environ 658:315–323

    Article  CAS  Google Scholar 

  • Liu CX, Gorby YA, Zachara JM, Fredrickson JK, Brown CF (2002) ‘Reduction kinetics of Fe(III), Co(III), U(VI) Cr(VI) and Tc(VII) in cultures of dissimilatory metal-reducing bacteria’. Biotechnol Bioeng 80(6):637–649

    Article  CAS  Google Scholar 

  • Liu T, Li H, Li Z, Xiao X, Chen L, Deng L (2007) Removal of hexavalent chromium by fungal biomass of Mucor racemosus: influencing factors and removal mechanism. World J Microbiol Biotechnol 23(12):1685–1693

    Article  CAS  Google Scholar 

  • Liu R, Guo Y, Wang Z, Liu J (2014) Iron species in layered clay: efficient electron shuttles for simultaneous conversion of dyes and Cr(VI). Chemosphere 95(1):643–646

    Article  CAS  Google Scholar 

  • Liu TX, Li XM, Li FB, Han R, Wu YD, Yuan X, Wang Y (2016) In situ spectral kinetics of Cr(VI) reduction by c-type cytochromes in a suspension of living Shewanella putrefaciens 200. Sci Rep 6:11

    Article  Google Scholar 

  • Lloyd JR, Sole VA, Van Praagh CVG, Lovley DR (2000) Direct and Fe(II)-mediated reduction of technetium by Fe(III)-reducing bacteria. Appl Environ Microbiol 66(9):3743–3749

    Article  CAS  Google Scholar 

  • Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. In: Poole RK (ed) Advances in microbial physiology, vol. 49. Academic Press Ltd-Elsevier Science Ltd, London, pp 219–286

    Google Scholar 

  • Mandal B, Halder A, Sinha PK, Sen R, Mandal AK (2016) Investigation of iron redox ratio in zinc borate glass prepared in microwave heating and comparison with conventional glass. J Non-Cryst Solids 450:12–17

    Article  CAS  Google Scholar 

  • Middleton SS, Bencheikh-Latmani R, Mackey MR, Ellisman MH, Tebo BM, Criddle CS (2003) Cometabolism of Cr(VI) by Shewanella oneidensis MR-1 produces cell-associated reduced chromium and inhibits growth’. Biotechnol Bioeng 83(6):627–637

    Article  CAS  Google Scholar 

  • Mishra RR, Dhal B, Dutta SK, Dangar TK, Das NN, Thatoi HN (2012) Optimization and characterization of chromium(VI) reduction in saline condition by moderately halophilic Vigribacillus sp. isolated from mangrove soil of Bhitarkanika, India. J Hazard Mater 227:219–226

    Article  Google Scholar 

  • Myers CR, Carstens BP, Antholine WE, Myers JM (2000) Chromium(VI) reductase activity is associated with the cytoplasmic membrane of anaerobically grown Shewanella putrefaciens MR-1. J Appl Microbiol 88(1):98–106

    Article  CAS  Google Scholar 

  • Parker DL, Borer P, Bernier-Latmani R (2011) The response of Shewanella oneidensis MR-1 to Cr(III) toxicity differs from that to Cr(VI). Front Microbiol. https://doi.org/10.3389/fmicb.2011.00223

    Article  PubMed  PubMed Central  Google Scholar 

  • Rebhi AEM, Lounici H, Lahrech MB, Morel JL (2019), Response of Artemisia herba alba to hexavalent chromium pollution under arid and semi-arid conditions. Int J Phytoremediat. https://doi.org/10.1080/15226514.2018.1524841

    Article  Google Scholar 

  • Saha B, Orvig C (2010) Biosorbents for hexavalent chromium elimination from industrial and municipal effluents. Coord Chem Rev 254(23):2959–2972

    Article  CAS  Google Scholar 

  • Schaefer JK, Rocks SS, Zheng W, Liang L, Gu B, Morel FMM (2011) Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria. Proc Natl Acad Sci USA 108(21):8714–8719

    Article  CAS  Google Scholar 

  • Tang YJ, Laidlaw D, Gani K, Keasling JD (2006) Evaluation of the effects of various culture conditions on Cr(VI) reduction by Shewanella oneidensis MR-1 in a novel high-throughput mini-bioreactor. Biotechnol Bioeng 95(1):176–184

    Article  CAS  Google Scholar 

  • Tian X, Wang W, Tian N, Zhou C, Yang C, Komarneni S (2016) Cr(VI) reduction and immobilization by novel carbonaceous modified magnetic Fe3O4/halloysite nanohybrid. J Hazard Mater 309:151–156

    Article  CAS  Google Scholar 

  • Vaiopoulou E, Gikas P (2012) Effects of chromium on activated sludge and on the performance of wastewater treatment plants: a review. Water Res 46(3):549–570

    Article  CAS  Google Scholar 

  • VanEngelen MR, Peyton BM, Mormile MR, Pinkart HC (2008) Fe(III), Cr(VI), and Fe(III) mediated Cr(VI) reduction in alkaline media using a Halomonas isolate from Soap Lake,Washington. Biodegradation 19(6):841–850

    Article  CAS  Google Scholar 

  • Wang J, Wu M, Lu G, Si Y (2016) Biotransformation and biomethylation of arsenic by Shewanella oneidensis MR-1. Chemosphere 145:329–335

    Article  CAS  Google Scholar 

  • Wang L, Xu S, Pan B, Yang Y (2017) Emerging investigator series: dual role of organic matter in the anaerobic degradation of triclosan. Environ Sci-Processes Impacts 19(4):499–506

    Article  CAS  Google Scholar 

  • Wielinga B, Mizuba MM, Hansel CM, Fendorf S (2001) Iron promoted reduction of chromate by dissimilatory iron-deducing bacteria. Environ Sci Technol 35(3):522–527

    Article  CAS  Google Scholar 

  • Xia S, Zhou L, Zhang Z, Hermanowicz SW (2015) Removal mechanism of low-concentration Cr (VI) in a submerged membrane bioreactor activated sludge system. Appl Microbiol Biotechnol 99(12):5351–5360

    Article  CAS  Google Scholar 

  • Yang L, Chen JP (2008) Biosorption of hexavalent chromium onto raw and chemically modified Sargassum sp. Bioresour Technol 99(2):297–307

    Article  CAS  Google Scholar 

  • Yuan Z, Li J, Cui L, Xu B, Zhang H, Yu C-P (2013) Interaction of silver nanoparticles with pure nitrifying bacteria. Chemosphere 90(4):1404–1411

    Article  CAS  Google Scholar 

  • Zhang YM, Chen J, Shi WL, Zhang DD, Zhu TT, Li XY (2017) Establishing a human health risk assessment methodology for metal species and its application of Cr6+ in groundwater environments. Chemosphere 189:525–537

    Article  CAS  Google Scholar 

  • Zhang L, Wu LL, Si YB, Shu KH (2018), Size-dependent cytotoxicity of silver nanoparticles to Azotobacter vinelandii: growth inhibition, cell injury, oxidative stress and internalization. PLoS ONE. https://doi.org/10.1371/journal.pone.0209020

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao W, Zheng YM, Zou SW, Ting YP, Chen JP (2009) Effect of hexavalent chromium on performance of membrane bioreactor in wastewater treatment. J Environ Eng 135(9):796–805

    Article  CAS  Google Scholar 

  • Zhu WH, Yu D, Shi MR, Zhang YT, Huang TL (2017) Quinone-mediated microbial goethite reduction and transformation of redox mediator, anthraquinone-2,6-disulfonate (AQDS). Geomicrobiol J 34(1):27–36

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Key Technology R & D Program of China (Grant No. 2015BAD05B04), the Fund of Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences and Key Project of Anhui Provincial Department of Education (Grant No. KJ2016A228).

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Correspondence to Youbin Si.

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Liu, X., Chu, G., Du, Y. et al. The role of electron shuttle enhances Fe(III)-mediated reduction of Cr(VI) by Shewanella oneidensis MR-1. World J Microbiol Biotechnol 35, 64 (2019). https://doi.org/10.1007/s11274-019-2634-9

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