Advertisement

Selective metal removal from chromium-containing synthetic effluents using Shewanella xiamenensis biofilm supported on zeolite

  • Inga ZinicovscaiaEmail author
  • Alexey Safonov
  • Kirill Boldyrev
  • Svetlana Gundorina
  • Nikita Yushin
  • Oleg Petuhov
  • Nadejda Popova
Research Article
  • 20 Downloads

Abstract

A scheme of selective removal of metal ions from chromium-containing synthetic solutions with the following chemical composition, Cr (VI)-Fe (III), Cr (VI)-Fe (III)-Ni (II), Cr (VI)-Fe (III)-Ni (II)-Zn (II), and Cr (VI)-Fe (III)-Ni (II)-Zn (II)-Cu (II)) by Shewanella xiamenensis biofilm immobilized on a zeolite support, was proposed. Three biological processes, biosorption, bioaccumulation, and longtime bioreduction, were applied for metal removal. The process of Zn (II), Ni (II), and Cu (II) showed to be pH dependent. The maximum removal of Ni (II) was achieved during a 1-hour biosorption process at pH 5.0–6.0, of Zn (II) at pH 5.0, and of Cu (II) at pH 3.0. Chromium (VI) and Fe (III) ions were more efficiently removed by bioaccumulation. Chromium (VI) removal in the studied systems varied from 16.4% to 34.8 and of iron from 55.8 to 94.6%. In a long-term bioreduction experiment, it was possible to achieve complete reduction of Cr (VI) to Cr (III) ions by Shewanella xiamenensis in 42 days and by Shewanella xiamenensis biofilm on zeolite in 35 days. Shewanella oneidensis can be effectively used to remove metal ions from chemically complex effluents.

Keywords

Shewanella xiamenensis Biosorption Bioaccumulation Bioreduction Neutron activation analysis Selective removal 

Notes

Funding information

This work was supported by the Russian Foundation for Basic Research (RFBR) [grant numbers 18-29-25023-мк].

References

  1. 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 7:184–189.  https://doi.org/10.1186/s13568-017-0482-2 CrossRefGoogle Scholar
  2. Andrade FJ, Tudino MB, Troccoli OE (1996) Flow dissolution of 1, 5-diphenylcarbazide for the determination of chromium (VI). Analyst 121(5):613–616.  https://doi.org/10.1039/AN9962100613 CrossRefGoogle Scholar
  3. Basak G, Lakshmi V, Chandran P, Das N (2014) Removal of Zn(II) from electroplating effluent using yeast biofilm formed on gravels: batch and column studies. J Environ Health Sci Eng 12:8.  https://doi.org/10.1186/2052-336X-12-8 CrossRefGoogle Scholar
  4. Beers MH, Berkow R (1999) The Merck manual of diagnosis and therapy. Merck & Co. Inc, West PointGoogle Scholar
  5. 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.  https://doi.org/10.1128/AEM.02463-10 CrossRefGoogle Scholar
  6. Bhargava P, Mishra Y, Srivastava AK, Narayan OP, Rai LC (2008) Excess copper induces anoxygenic photosynthesis in Anabaena doliolum: a homology based proteomic assessment of its survival strategy. Photosynth Res 96:61–74.  https://doi.org/10.1007/s11120-007-9285-7 CrossRefGoogle Scholar
  7. Boldyrev KA, Kruchkov DV, Martynov KV, Nuzhyi AS, Suskin VV (2017) Development of the methods of assessment of the radionuclides migration beyond IBB taking into the account their evolution. Preprint № IBRAE-2017-11, Moscow, p. 23. (in Russian)Google Scholar
  8. Bozal N, Montes MJ, Tudela E, Jiménez F, Guinea J (2002) Shewanella frigidimarina and Shewanella livingstonensis sp. nov. isolated from antarctic coastal areas. Int J Syst Evol Microbiol 52:195–205.  https://doi.org/10.1099/00207713-52-1-195 CrossRefGoogle Scholar
  9. Brady D, Stoll A, Duncan JR (2008) Biosorption of heavy metal cations by non-viable yeast biomass. Environ Technol 15(5):429-438.  https://doi.org/10.1080/09593339409385447 CrossRefGoogle Scholar
  10. Çetin D, Dönmez S, Dönmez G (2008) The treatment of textile wastewater including chromium (VI) and reactive dye by sulfate-reducing bacterial enrichment. J Environ Manag 88(1):76–82.  https://doi.org/10.1016/j.jenvman.2007.01.019 CrossRefGoogle Scholar
  11. Das KK, Reddy RC, Bagoji IB, Das S, Bagali S, Mullur L, Khodnapur JP, Biradar MS (2018) Primary concept of nickel toxicity: an overview. J Basic Clin Physiol Pharmacol 30(2):141–152.  https://doi.org/10.1515/jbcpp-2017-0171 CrossRefGoogle Scholar
  12. Deborah S, Sebastin Raj J (2016) Bioremediation of heavy metals from distilleries effluent using microbes. J Appl Adv Res 1(2):23–28.  https://doi.org/10.21839/jaar.2016.v1i2.21 CrossRefGoogle Scholar
  13. Figueiredo H, Neves IC, Quintelas C, Tavares T, Taralunga M, Mijoin J, Magnoux P (2006) Oxidation catalysts prepared from biosorbents supported on zeolites. Appl Catal B 66:274–280.  https://doi.org/10.1016/j.apcatb.2006.04.002 CrossRefGoogle Scholar
  14. Frontasyeva M (2011) Neutron activation analysis for the life sciences. Rev Phys Part Nuclei 42(2011):322–378.  https://doi.org/10.1134/S1063779611020043 CrossRefGoogle Scholar
  15. Ghorbanzadeh N, Kumar R, Lee SH, Park HS, Jeon BH (2018) Impact of Shewanella oneidensis on heavy metals remobilization under reductive conditions in soil of Guilan Province, Iran. Geosci J 22:423–432.  https://doi.org/10.1007/s12303-017-0067-8 CrossRefGoogle Scholar
  16. Grouzdev DS, Safonov AV, Babich TL, Tourova TP, Krutkina MS, Nazina TN (2018) Draft genome sequence of a dissimilatory U (VI)-reducing bacterium, Shewanella xiamenensis strain DCB2-1, isolated from nitrate-and radionuclide-contaminated groundwater in Russia. Genome Announc 6(25):e00555–e00518.  https://doi.org/10.1128/genomeA.00555-18 CrossRefGoogle Scholar
  17. Guler UA, Sarioglu M (2014) Mono and binary component biosorption of cu(II), Ni(II), and methylene blue onto raw and pretreated S. cerevisiae: equilibrium and kinetics. Desalin Water Treat 52:4871–4888.  https://doi.org/10.1080/19443994.2013.810359 CrossRefGoogle Scholar
  18. Ha J, Gélabert A, Spormann AM, Brown GE Jr (2010) Role of extracellular polymeric substances in metal ion complexation on Shewanella oneidensis: batch uptake, thermodynamic modeling, ATR-FTIR, and EXAFS study. Geochim Cosmochim Acta 74:1–15.  https://doi.org/10.1016/j.gca.2009.06.031 CrossRefGoogle Scholar
  19. Huertas M, López-Maury L, Giner-Lamia J, Sánchez-Riego A, Florencio F (2014) Metals in cyanobacteria: analysis of the copper, nickel, cobalt and arsenic homeostasis mechanisms. Life 4(4):865–886.  https://doi.org/10.3390/life4040865 CrossRefGoogle Scholar
  20. Kimber RL, Lewis EA, Parmeggiani F et al (2018) Biosynthesis and characterization of copper nanoparticles using Shewanella oneidensis: application for click chemistry. Small 14(10):1703145.  https://doi.org/10.1002/smll.201703145 CrossRefGoogle Scholar
  21. Kitayama M, Koga R, Kasai T, Kouzuma A, Watanabe K (2017) Structures, compositions, and activities of live Shewanella biofilms formed on graphite electrodes in electrochemical flow cells. Appl Environ Microbiol 83(17):e00903–e00917.  https://doi.org/10.1128/AEM.00903-17 CrossRefGoogle Scholar
  22. Kučić D, Simonič M, Furač L (2017) Batch adsorption of Cr(VI) ions on zeolite and agroindustrial waste. Chem Biochem Eng Q 31(4):497–507.  https://doi.org/10.15255/CABEQ.2017.1100 CrossRefGoogle Scholar
  23. Lameiras S, Quintelas C, Tavares T (2008) Biosorption of Cr (VI) using a bacterial biofilm supported on granular activated carbon and on zeolite. Bioresour Technol 99:801–806.  https://doi.org/10.1016/j.biortech.2007.01.040 CrossRefGoogle Scholar
  24. Lawrence JR, Korber DR, Hoyle BD, Costerton JW, Caldwell DE (1991) Optical sectioning of microbial biofilms. J Bacteriol 173(20):6558–6567.  https://doi.org/10.1128/jb.173.20.6558-6567.1991 CrossRefGoogle Scholar
  25. Machado MD, Soares HM, Soares EV (2010) Removal of chromium, copper, and nickel from an electroplating effluent using a flocculent brewer’s yeast strain of Saccharomyces cerevisiae. Water Air Soil Poll 212:199–204.  https://doi.org/10.1007/s11270-010-0332-1 CrossRefGoogle Scholar
  26. Mamba BB, Dlamini NP, Mulaba-Bafubiandi AF (2009) Biosorptive removal of copper and cobalt from aqueous solutions: Shewanella spp. put to the test. Phys Chem Earth 34:841–849.  https://doi.org/10.1016/j.pce.2009.07.009 CrossRefGoogle Scholar
  27. Moghaddam E, Amirebrahim S, Harun R, Mokhtar MN, Zakaria R (2018) Potential of zeolite and algae in biomass immobilization. Biomed Res Int.  https://doi.org/10.1155/2018/6563196 CrossRefGoogle Scholar
  28. Muyssen BT, De Schamphelaere KA, Janssen CR (2006) Mechanisms of chronic waterborne Zn toxicity in Daphnia magna. Aquat Toxicol 77(4):393–401.  https://doi.org/10.1016/j.aquatox.2006.01.006 CrossRefGoogle Scholar
  29. Ng IS, Ndive CI, Zhou Y, Wu X (2015) Cultural optimization and metal effects of Shewanella xiamenensis BC01 growth and swarming motility. Bioresour Bioprocess 2(1):28–10.  https://doi.org/10.1186/s40643-015-0055-7 CrossRefGoogle Scholar
  30. Phaniendra A, Babu Jestadi D, Periyasamy L (2015) Free radicals: properties, sources, targets, and their implication in various diseases. Indian J Clin Biochem 30(1):11–26.  https://doi.org/10.1007/s12291-014-0446-0 CrossRefGoogle Scholar
  31. Plum LM, Rink L, Haase H (2010) The essential toxin: impact of zinc on human health. International journal of environmental research and public health. Int J Environ Res Public Health 7(4):1342–1365.  https://doi.org/10.3390/ijerph7041342 CrossRefGoogle Scholar
  32. Qian H, Yu S, Sun Z, Xie X, Liu W, Fu Z (2010) Effects of copper sulfate, hydrogen peroxide and N-phenyl-2-naphthylamine on oxidative stress and the expression of genes involved photosynthesis and microcystin disposition in Microcystis aeruginosa. Aquat Toxicol 99(3):405–412.  https://doi.org/10.1016/j.aquatox.2010.05.018 CrossRefGoogle Scholar
  33. Quintelas C, Rocha Z, Silva B, Fonseca B, Figueiredo H, Tavares T (2009) Biosorptive performance of an Escherichia coli biofilm supported on zeolite NaY for the removal of Cr(VI), cd(II), Fe(III) and Ni(II). Chem Eng J 152(1):110–115.  https://doi.org/10.1016/j.cej.2009.03.039 CrossRefGoogle Scholar
  34. Quiton KG, Doma B Jr, Futalan CM, Wan MW (2018) Removal of chromium(VI) and zinc(II) from aqueous solution using kaolin-supported bacterial biofilms of Gram-negative E. coli and gram-positive Staphylococcus epidermidis. Sustain Environ Res 28(5):206–213.  https://doi.org/10.1016/j.serj.2018.04.002 CrossRefGoogle Scholar
  35. Ramesh K, Sammi Reddy K, Rashmi I, Biswas AK (2014) Nanostructured natural zeolite: surface area, meso-pore and volume distribution, and morphology. Commun Soil Sci Plant Anal 45(25):2878–2897.  https://doi.org/10.1080/00103624.2014.956934 CrossRefGoogle Scholar
  36. Rey-Mellano ME, Senoro DB, Tayo LL, Wan MW (2016) Adsorption of Cu (II) and Ni(II) in aqueous solution using biofilm supported with kaolinite clay. 6th International Conference on Biological, Chemical & Environmental Sciences (BCES-2016) August 8–9, 2016 Pattaya (Thailand)  https://doi.org/10.15242/IICBE.C0816210
  37. Roh Y, Gao H, Vali H, Kennedy DW, Yang ZK, Gao W, Dohnalkova AC, Stapleton RD, Moon JW, Phelps TJ, Fredrickson JK, Zhou J (2006) Metal reduction and iron biomineralization by a psychrotolerant Fe(III)-reducing bacterium, Shewanella sp. strain PV-4. Appl Environ Microb 72(5):3236–3244.  https://doi.org/10.1128/AEM.72.5.3236-3244.2006 CrossRefGoogle Scholar
  38. Rout GR, Das P (2009) Effect of metal toxicity on plant growth and metabolism: I. zinc. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C (eds) Sustainable Agriculture. Springer, Dordrecht.  https://doi.org/10.1007/978-90-481-2666-8_53 CrossRefGoogle Scholar
  39. Salnikow K, Zhitkovich A (2007) Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: nickel, arsenic, and chromium. Chem Res Toxicol 21(1):28–44.  https://doi.org/10.1021/tx700198a CrossRefGoogle Scholar
  40. Sheng PX, Ting YP, Chen JP (2007) Biosorption of heavy metal ions (Pb, cu, and cd) from aqueous solutions by the marine alga Sargassum sp. in single- and multiple-metal systems. Ind Eng Chem Res 46(8):2438–2444.  https://doi.org/10.1021/ie0615786 CrossRefGoogle Scholar
  41. Silva B, Figueiredo H, Quintelas C, Neves IC, Tavares T (2008) Iron and chromium removal from binary solutions of Fe (III)/Cr (III) and Fe (III)/Cr (VI) by biosorbents supported on zeolites. In: materials science forum, vol 587. Trans tech publications, pp 463–467.  https://doi.org/10.4028/www.scientific.net/MSF.587-588.463 CrossRefGoogle Scholar
  42. Sommerfeld Ross S, Han Tu M, Falsetta ML, Ketterer MR, Kiedrowski MR, Horswill AR, Apicella MA, Reinhardt JM, Fiegel J (2014) Quantification of confocal images of biofilms grown on irregular surfaces. J Microbiol Methods 100:111–120.  https://doi.org/10.1016/j.mimet.2014.02.020 CrossRefGoogle Scholar
  43. Viamajala S, Peyton BM, Sani RK, Apel WA, Petersen JN (2004) Toxic effects of chromium (VI) on anaerobic and aerobic growth of Shewanella oneidensis MR-1. Biotechnol Prog 20:87–95.  https://doi.org/10.1021/bp034131q CrossRefGoogle Scholar
  44. Wildung RE, Gorby YA, Krupka KM, Hess NJ, Li SW, Plymale AE (2000) Effect of electron donor and solution chemistry on products of dissimilatory reduction of technetium by Shewanella putrefaciens. Appl Environ Microbiol 66(6):2451–2460.  https://doi.org/10.1128/AEM.66.6.2451-2460.2000 CrossRefGoogle Scholar
  45. Wu H, Wu Q, Zhang J, Gu Q, Wei L, Guo W, He M (2019) Chromium ion removal from raw water by magnetic iron composites and Shewanella oneidensis MR-1. Sci Rep 9(1):3687.  https://doi.org/10.1038/s41598-018-37470-1 CrossRefGoogle Scholar
  46. Zinicovscaia I, Cepoi L, Chiriac T, Yushin N, Vergel K (2018a) Study of selected metals biosorption by Arthrospira platensis using neutron activation analysis. Desalin Water Treat 108:119–124.  https://doi.org/10.5004/dwt.2018.21940 CrossRefGoogle Scholar
  47. Zinicovscaia I, Cepoi L, Povar I, Chiriac T, Rodlovskaya E, Culicov OA (2018b) Study of metal uptake from complex industrial effluents by Spirulina platensis using neutron activation analysis. Water Air Soil Pollut 229:220–210.  https://doi.org/10.1007/s11270-018-3873-3 CrossRefGoogle Scholar
  48. Zinicovscaia I, Safonov A, Ostalkevich S, Gundorina S, Nekhoroshkov P, Grozdov D (2019) Metal ions removal from different type of industrial effluents using Spirulina platensis biomass. Int J Phytoremediat 21(14):1442–1448.  https://doi.org/10.1080/15226514.2019.1633264 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Joint Institute for Nuclear ResearchMoscowRussia
  2. 2.Horia Holubei National Institute for R&D in Physics and Nuclear Engineering (IFIN-HH)MagureleRomania
  3. 3.The Institute of ChemistryKishinevMoldova
  4. 4.Frumkin Institute of Physical Chemistry and Electrochemistry, Russian Academy of SciencesMoscowRussia
  5. 5.Nuclear Safety Institute of the Russian Academy of SciencesMoscowRussia

Personalised recommendations