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Environmental Chemistry Letters

, Volume 17, Issue 3, pp 1413–1420 | Cite as

Microbial fuel cell-induced production of fungal laccase to degrade the anthraquinone dye Remazol Brilliant Blue R

  • Marta Filipa Simões
  • Alfredo Eduardo Maiorano
  • Jonas Gomes dos Santos
  • Luciana Peixoto
  • Rodrigo Fernando Brambilla de Souza
  • Almir Oliveira Neto
  • António Guerreiro Brito
  • Cristiane Angélica OttoniEmail author
Original Paper
  • 189 Downloads

Abstract

The anthraquinone dye Remazol Brilliant Blue R is largely used in the textile industry. However, its removal from wastewaters is costly and complex. Many methods have been tested to solve this ecological problem, but there is still a need for efficient methods. We propose here an alternative use of a two-chambered microbial fuel cell (MFC), fuelled with domestic wastewater in the anodic chamber, to degrade a simulated textile dye effluent made of Remazol Brilliant Blue R inoculated with an immobilised fungal strain, Pleurotus ostreatus URM 4809, as a laccase producer, in the cathodic chamber. The MFC showed continuous synthesis of laccase in the cathodic chamber, which, in turn, promoted the rapid decolourisation, of more than 86% of the textile dye effluent. The yield was further increased by the addition of glycerol. Electrochemical monitoring also indicated an increase in power density and current density. After 20 days of MFC operation, 62.1% of organic matter was removed in the anodic compartment, thus leaving the effluent with a much lower toxicity.

Keywords

Microbial fuel cell Pleurotus ostreatus Laccase Remazol Brilliant Blue R Vigna radiata 

Notes

Acknowledgements

Authors would like to acknowledge the technician and financial support of Programa Novos Talentos provided by the Instituto de Pesquisa Tecnológica do Estado de São Paulo (IPT) and Instituto de Estudos Avançados do Mar (IEAMar).

Compliance with ethical standards

Conflicts of interest

There are no conflicts to declare.

Supplementary material

10311_2019_876_MOESM1_ESM.docx (25 kb)
Supplementary material 1 (DOCX 25 kb)
10311_2019_876_MOESM2_ESM.docx (49 kb)
Supplementary material 2 (DOCX 49 kb)

References

  1. Afreen S, Bano F, Ahmad N, Fatma T (2017) Screening and optimization of laccase from cyanobacteria with its potential in decolorization of anthraquinonic dye Remazol Brilliant Blue R. Biocatal Agric Biotechnol 10:403–410.  https://doi.org/10.1016/j.bcab.2017.05.004 Google Scholar
  2. Aravind P, Selvaraj H, Ferro S, Sundaram M (2016) An integrated (electro-and bio-oxidation) approach for remediation of industrial wastewater containing azo-dyes: understanding the degradation mechanism and toxicity assessment. J Hazard Mater 318:203–215.  https://doi.org/10.1016/j.jhazmat.2016.07.028 Google Scholar
  3. Bakhshian S, Kariminia H-R, Roshandel R (2011) Bioelectricity generation enhancement in a dual chamber microbial fuel cell under cathodic enzyme catalyzed dye decolorization. Bioresour Technol 102:6761–6765.  https://doi.org/10.1016/j.biortech.2011.03.060 Google Scholar
  4. Bouabidi ZB, El-Naas MH, Zhang Z (2018) Immobilization of microbial cells for the biotreatment of wastewater: a review. Environ Chem Lett.  https://doi.org/10.1007/s10311-018-0795-7 Google Scholar
  5. Campo AG, Cañizares P, Rodrigo MA, Fernández FJ, Lobato J (2013) Microbial fuel cell with an algae-assisted cathode: a preliminary assessment. J Power Sources 242:638–645.  https://doi.org/10.1016/j.jpowsour.2013.05.110 Google Scholar
  6. Chaijak P, Sukkasem C, Lertworapreecha M, Boonsawang P, Wijasika S, Sato C (2018) Enhancing electricity generation using a laccase-based microbial fuel cell with yeast Galactomyces reessii on the cathode. J Microbiol Biotechnol 28:1360–1366.  https://doi.org/10.4014/jmb.1803.03015 Google Scholar
  7. Fernández de Dios MÁ, del Campo AG, Fernández FJ, Rodrigo M, Pazos M, Sanromán MÁ (2013) Bacterial-fungal interactions enhance power generation in microbial fuel cells and drive dye decolorisation by an ex situ and in situ electro Fenton process. Bioresour Technol 148:39–46.  https://doi.org/10.1016/j.biortech.2013.08.084 Google Scholar
  8. Fogelman S, Zhao H, Blumenstein M (2006) A rapid analytical method for predicting the oxygen demand of wastewater. Anal Bioanal Chem 386:1773–1779.  https://doi.org/10.1007/s00216-006-0817-3 Google Scholar
  9. Franks AE, Nevin KP (2010) Microbial fuel cells, a current review. Energies 3:899–919.  https://doi.org/10.3390/en3050899 Google Scholar
  10. Hajilary N, Rezakazemi M, Shirazian S (2018) Biofuel types and membrane separation. Environ Chem Lett.  https://doi.org/10.1007/s10311-018-0777-9 Google Scholar
  11. Hashmat AJ, Islam E, Haq MA, Khan QM (2014) Integrated treatment technology for textile effluent and its phytotoxic evaluation. Desalin Water Treat 57:4146–4156.  https://doi.org/10.1080/19443994.2014.989270 Google Scholar
  12. Hou H, Zhou J, Wang J, Du C, Yan B (2004) Enhancement of laccase production by Pleurotus ostreatus and its use for the decolorization of anthraquinone dye. Process Biochem 39(11):1415–1419.  https://doi.org/10.1016/S0032-9592(03)00267-X Google Scholar
  13. Hou J, Dong G, Ye Y, Chen V (2014) Laccase immobilization on titania nanoparticles and titania-functionalized membranes. J Membr Sci 452:229–240.  https://doi.org/10.1016/j.memsci.2013.10.019 Google Scholar
  14. Ilamathi R, Jayapriya J (2018) Microbial fuel cells for dye decolorization. Environ Chem Lett 16:239–250.  https://doi.org/10.1007/s1031 Google Scholar
  15. Izadi P, Rahimnejad M (2014) Simultaneous electricity generation and sulfide removal via a dual chamber microbial fuel cell. Biofuel Res J 1:34–38.  https://doi.org/10.18331/brj2015.1.1.8 Google Scholar
  16. Jadhav DA, Ghadge AN, Ghangrekar MM (2014) Simultaneous organic matter removal and disinfection of wastewater with enhanced power generation in microbial fuel cell. Bioresour Technol 163:328–334.  https://doi.org/10.1016/j.biortech.2014.04.055 Google Scholar
  17. Kacem SH, Galai S, Ríos AP, Fernández FJH, Smaali I (2017) New efficient laccase immobilization strategy using ionic liquids for biocatalysis and microbial fuel cells applications. J Chem Technol Biotechnol 93:174–183.  https://doi.org/10.1002/jctb.5337 Google Scholar
  18. Karthikeyan V, Kumar MA, Mohanapriya P, Amudha T, Thiruselvi D, Karthik P, Sivanesan S (2017) Biodegradation of Remazol Brilliant Blue R using isolated bacterial culture (Staphylococcus sp. K2204). Environ Technol 39:2900–2907.  https://doi.org/10.1080/09593330.2017.1369579 Google Scholar
  19. Kolangare IM, Isloor AM, Karim ZA, Kulal A, Ismail AF, Inamuddin Asiri AM (2018) Antibiofouling hollow-fiber membranes for dye rejection by embedding chitosan and silver-loaded chitosan nanoparticles. Environ Chem Lett.  https://doi.org/10.1007/s10311-018-0799-3 Google Scholar
  20. Lai C-Y, Wu G-P, Meng C-T, Lin C-W (2017a) Decolorization of azo dye and generation of electricity by microbial fuel cell with laccase-producing white-rot fungus on cathode. Appl Energy 188:392–398.  https://doi.org/10.1016/j.apenergy.2016.12.044 Google Scholar
  21. Lai C-Y, Liu S-H, Wu G-P, Lin C-W (2017b) Enhanced bio-decolorization of acid orange 7 and electricity generation in microbial fuel cells with superabsorbent-containing membrane and laccase-based bio-cathode. J Clean Prod 166:381–386.  https://doi.org/10.1016/j.jclepro.2017.08.047 Google Scholar
  22. Lin CW, Wu C-H, LinY-Y Liu S-H, Chang S-H (2018) Enhancing the performance of microbial fuel cell using a carbon-fiber-brush air cathode with low-cost mushroom Ganoderma laccase enzyme. J Taiwan Inst Chem E.  https://doi.org/10.1016/j.jtice.2017.12.025 Google Scholar
  23. Liu G, Yates MD, Cheng S, Call DF, Sun D, Logan BE (2011) Examination of microbial fuel cell start-up times with domestic wastewater and additional amendments. Bioresour Technol 102:7301–7306.  https://doi.org/10.1016/j.biortech.2011.04.087 Google Scholar
  24. Lu N, S-g Zhou, Zhuang L, Zhang J-T, Ni J-R (2009) Electricity generation from starch processing wastewater using microbial fuel cell technology. Biochem Eng J 43:246–251.  https://doi.org/10.1016/j.bej.2008.10.005 Google Scholar
  25. Lu R, Ma L, He F, Yu D, Fan R, Zhang Y, Long Z, Zhang X, Yang Y (2016) White-rot fungus Ganoderma sp. En3 had a strong ability to decolorize and tolerate the anthraquinone, indigo and triphenylmethane dye with high concentrations. Bioprocess Biosyst Eng 39:381–390.  https://doi.org/10.1007/s00449-015-1521-5 Google Scholar
  26. Luo H, Jin S, Fallgren PH, Park HJ, Johnson PA (2010) A novel laccase-catalyzed cathode for microbial fuel cells. Chem Eng J 165:524–528.  https://doi.org/10.1016/j.cej.2010.09.061 Google Scholar
  27. Mani P, Keshavarz T, Chandra TS, Kyazze G (2017) Decolourisation of Acid orange 7 in a microbial fuel cell with a laccase-based biocathode: influence of mitigating pH changes in the cathode chamber. Enzyme Microb Technol 96:170–176.  https://doi.org/10.1016/j.enzmictec.2016.10.012 Google Scholar
  28. Martins MAM, Lima N, Silvestre AJD, Queiroz MJ (2003) Comparative studies of fungal degradation of single or mixed bioaccessible reactive azo dyes. Chemosphere 52:967–973.  https://doi.org/10.1016/S0045-6535(03)00286-8 Google Scholar
  29. Morant KV, Silva PH, Campos-Takaki GM, Hernández CER (2014) Isolation and bioelectrochemical characterization of novel fungal sources with oxidasic activity applied in situ for the cathodic oxygen reduction in microbial fuel cells. Enzyme Microb Technol 66:20–27.  https://doi.org/10.1016/j.enzmictec.2014.07.007 Google Scholar
  30. Mudhoo A, Gautam RK, Ncibi MC, Zhao F, Garg VK, Sillanpää M (2018) Green synthesis, activation and functionalization of adsorbents for dye sequestration. Environ Chem Lett.  https://doi.org/10.1007/s1031 Google Scholar
  31. Nouren S, Bhatti HN (2015) Mechanistic study of degradation of basic violet 3 by citrus limon peroxidase and phytotoxicity assessment of its degradation products. Biochem Eng J 95:9–19.  https://doi.org/10.1016/j.bej.2014.11.021 Google Scholar
  32. Oon Y-S, Ong S-A, Ho L-N, Wong Y-S, Oon Y-L, Lehl HK, Thung W-E, Nordin N (2017) Microbial fuel cell operation using monoazo and diazo dyes asterminal electron acceptor for simultaneous decolourisation and bioelectricity generation. J Hazard Mater 325:170–177.  https://doi.org/10.1016/j.jhazmat.2016.11.074 Google Scholar
  33. Oon Y-S, Ong SA, Ho L-N, Wong Y-S, Oon Y-L, Lehl HK, Thung W-E, Nordin N (2018a) Disclosing the synergistic mechanisms of azo dye degradation and bioelectricity generation in a microbial fuel cell. Chem Eng J 344:236–245.  https://doi.org/10.1016/j.cej.2018.03.060 Google Scholar
  34. Oon Y-L, Ong S-A, Ho L-N, Wong Y-S, Dahalan FA, Oon Y-S, Lehl HK, Thung W-E, Nordin N (2018b) Up-flow constructed wetland-microbial fuel cell for azo dye, saline and nitrate remediation and bioelectricity generation: from waste to energy approach. Bioresour Technol 266:97–108.  https://doi.org/10.1016/j.biortech.2018.06.035 Google Scholar
  35. Orlikowska M, Rostro-Alanis MJ, Bujacz A, Hernández-Luna C, Rubio R, Parra R, Bujacz G (2018) Structural studies of two thermostable laccases from the white-rot fungus Pycnoporus sanguineus. Int J Biol Macromol 107:1629–1640.  https://doi.org/10.1016/j.ijbiomac.2017.10.024 Google Scholar
  36. Ottoni C, Lima L, Santos C, Lima N (2014) Effect of different carbon sources on decolourisation of an industrial textile dye under alkaline-saline conditions. Curr Microbiol 68:53–58.  https://doi.org/10.1007/s00284-013-0441-3 Google Scholar
  37. Ottoni CA, Simões MF, Santos JG, Peixoto L, Martins CR, Silva BP, Neto AO, Brito AG, Maiorano AE (2019) Application of microbial fuel cell technology for vinasse treatment and bioelectricity generation. Biotechnol Lett 41:107–114.  https://doi.org/10.1007/s10529-018-2624-2 Google Scholar
  38. Patel AM, Patel VM, Pandya J, Trivedi UB, Patel KC (2017) Evaluation of catalytic efficiency of Coriolopsis caperata DN laccase to decolorize and detoxify RBBR dye. Water Conserv Sci Eng 2:85–98.  https://doi.org/10.1007/s4110 Google Scholar
  39. Peixoto L, Rodrigues AL, Martins G, Nicolau A, Brito AG, Silva MM, Parpot P, Nogueira R (2013) A flat microbial fuel cell for decentralized wastewater valorization: process performance and optimization potential. Environ Technol 34:1947–1956.  https://doi.org/10.1080/09593330.2013.827223 Google Scholar
  40. Rezakazemi M, Khajeh A, Mesbah M (2018a) Membrane filtration of wastewater from gas and oil production. Environ Chem Lett 16:367–388.  https://doi.org/10.1007/s10311-017-0693-4 Google Scholar
  41. Rezakazemi M, Dashti A, Harami HR, Hajilari N, Inamuddin (2018b) Fouling-resistant membranes for water reuse. Environ Chem Lett 16:715–763.  https://doi.org/10.1007/s10311-018-0717-8 Google Scholar
  42. Rodríguez-Couto S, Sanromán MA, Hofer D, Gübitz GM (2004) Stainless steel sponge: a novel carrier for the immobilization of the white-rot fungus Trametes hirsuta for decolourization of textile dyes. Bioresour Technol 95:67–72.  https://doi.org/10.1016/j.biortech.2003.05.002 Google Scholar
  43. Saeed M, Ahmad A, Boddula R, Inamuddin, ul Haq A, Azhar A (2018) Ag@MnxOy: an effective catalyst for photo-degradation of rhodamine B dye. Environ Chem Lett 16:287–294.  https://doi.org/10.1007/s10311-017-0661-z Google Scholar
  44. Salazar-López M, Rostro-Alanis MJ, Castillo-Zacarías C, Parra-Guardado AL, Hernández-Luna C, Iqbal HMN, Parra-Saldivar R (2017) Induced degradation of anthraquinone-based dye by laccase produced from Pycnoporus sanguineus (CS43). Water Air Soil Pollut 228:469.  https://doi.org/10.1007/s11270-017-3644-6 Google Scholar
  45. Sané S, Jolivalt C, Mittler G, Nielsen PJ, Rubenwolf S, Zengerle R, Kerzenmacher S (2013) Overcoming bottlenecks of enzymatic biofuel cell cathodes: crude fungal culture supernatant can help to extend lifetime and reduce cost. Chemsuschem 6:1209–1215.  https://doi.org/10.1002/cssc.20130020 Google Scholar
  46. Sané S, Richter K, Rubenwolf S, Matschke NJ, Jolivalt C, Madzak C, Zengerle R, Gescher J, Kerzenmacher S (2014) Using planktonic microorganisms to supply the unpurified multi-copper oxidases laccase and copper efflux oxidases at a biofuel cell cathode. Bioresour Technol 158:23–238.  https://doi.org/10.1016/j.biortech.2014.02.038 Google Scholar
  47. Savizi ISP, Kariminia H-R, Bakhshian S (2012) Simultaneous decolorization and bioelectricity generation in a dual chamber microbial fuel cell using electropolymerized-enzymatic cathode. Environ Sci Technol 46:6584–6593.  https://doi.org/10.1021/es300367h Google Scholar
  48. Schaetzle O, Barrière F, Schröder U (2009) An improved microbial fuel cell with laccase as the oxygen reduction catalyst. Energy Environ Sci 2:96–99.  https://doi.org/10.1039/b815331k Google Scholar
  49. Sharma V, Kundu PP (2010) Biocatalysts in microbial fuel cells. Enzyme Microb Technol 47:179–188.  https://doi.org/10.1016/j.enzmictec.2010.07.001 Google Scholar
  50. Shukla S, Oturan MA (2015) Dye removal using electrochemistry and semiconductor oxide nanotubes. Environ Chem Lett 13(2):157–172.  https://doi.org/10.1007/s10311-015-0501-y Google Scholar
  51. Sonawane JP, Marsili E, Ghosh PC (2014) Treatment of domestic and distillery wastewater in high surface microbial fuel cells. Int J Hydrog Energy 39:21819–21827.  https://doi.org/10.1016/j.ijhydene.2014.07.085 Google Scholar
  52. Strack G, Luckarift HR, Sizemore SR, Nichols RK, Farrington KE, Wu PK, Atanassov P, Biffinger JC, Johnson GR (2013) Power generation from a hybrid biological fuel cell in seawater. Bioresour Technol 128:222–228.  https://doi.org/10.1016/j.biortech.2012.10.104 Google Scholar
  53. Sultan M (2017) Polyurethane for removal of organic dyes from textile wastewater. Environ Chem Lett 15:347–366.  https://doi.org/10.1007/s10311-016-0597-8 Google Scholar
  54. Sun J, Bi Z, Hou B, Cao Y-Q, Hu Y-Y (2011) Further treatment of decolorization liquid of azo dye coupled with increased power production using microbial fuel cell equipped with an aerobic biocathode. Water Res 45:283–291.  https://doi.org/10.1016/j.watres.2010.07.059 Google Scholar
  55. Tarkwa J-B, Oturan N, Acayanka E, Laminsi S, Oturan MA (2018) Photo-Fenton oxidation of Orange G azo dye: process optimization and mineralization mechanism. Environ Chem Lett.  https://doi.org/10.1007/s10311-018-0773-0 Google Scholar
  56. Téllez-Téllez M, Fernández FJ, Montiel-González AM, Sánchez C, Díaz-Godínez G (2008) Growth and laccase production by Pleurotus ostreatus in submerged and solid-state fermentation. Appl Microbiol Biotechnol 81(4):675.  https://doi.org/10.1007/s00253-008-1628-6 Google Scholar
  57. Varghese AG, Paul SA, Latha MS (2018) Remediation of heavy metals and dyes from wastewater using cellulose-based adsorbents. Environ Chem Lett 9:1–11.  https://doi.org/10.1007/s10311-018-00843-z Google Scholar
  58. Vats A, Mishra S (2018) Identification and evaluation of bioremediation potential of laccase isoforms produced by Cyathus bulleri on wheat bran. J Hazard Mater 344:466–479.  https://doi.org/10.1016/j.jhazmat.2017.10.043 Google Scholar
  59. Wang N, Chu Y, Wu F, Zhao Z, Xu X (2017) Decolorization and degradation of Congo red by a newly isolated white rot fungus, Ceriporia lacerata, from decayed mulberry branches. Int Biodeterior Biodegrad 117:236–244.  https://doi.org/10.1016/j.ibiod.2016.12.015 Google Scholar
  60. Wang Y, Chen Y, Wen Q (2018) Microbial fuel cells: enhancement with a polyaniline/carbon felt capacitive bioanode and reduction of Cr(VI) using the intermittent operation. Environ Chem Lett 16:319–326.  https://doi.org/10.1007/s10311-017-0678-3 Google Scholar
  61. Watson VJ, Delgado CD, Logan BE (2013) Influence of chemical and physical properties of activated carbon powders on oxygen reduction and microbial fuel cell performance. Environ Sci Technol 47:6704–6710.  https://doi.org/10.1021/es401722j Google Scholar
  62. Wu C, Liu X-W, Li W-W, Sheng G-P, Zang G-L, Cheng Y-Y, Shen N, Yang Y-P, Yu H-Q (2012) A white-rot fungus is used as a biocathode to improve electricity production of a microbial fuel cell. Appl Energy 98:594–596.  https://doi.org/10.1016/j.apenergy.2012.02.058 Google Scholar
  63. Yang J, Lin Q, Ng TB, Ye X, Lin J (2014) Purification and characterization of a novel laccase from Cerrena sp. HYB07 with dye decolorizing ability. PLoS ONE 9(10):e110834.  https://doi.org/10.1371/journal.pone.0110834 Google Scholar
  64. Zhang F, Merrill MD, Tokash JC, Saito T, Cheng S, Hickner MA, Logan BE (2011) Mesh optimization for microbial fuel cell cathodes constructed around stainless steel mesh current collectors. J Power Sources 196:1097–1102.  https://doi.org/10.1016/j.jpowsour.2010.08.011 Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Marta Filipa Simões
    • 1
  • Alfredo Eduardo Maiorano
    • 2
  • Jonas Gomes dos Santos
    • 2
  • Luciana Peixoto
    • 3
  • Rodrigo Fernando Brambilla de Souza
    • 4
  • Almir Oliveira Neto
    • 4
  • António Guerreiro Brito
    • 5
  • Cristiane Angélica Ottoni
    • 2
    • 6
    • 7
    • 8
    Email author
  1. 1.Biology DepartmentEdge Hill UniversityLancashireUK
  2. 2.Laboratório de Biotecnologia IndustrialInstituto de Pesquisas Tecnológicas do Estado de São PauloSão PauloBrazil
  3. 3.Centre of Biological EngineeringUniversity of MinhoBragaPortugal
  4. 4.Centro de Célula a Combustível e HidrogênioInstituto de Pesquisas Energéticas e NuclearesSão PauloBrazil
  5. 5.Department of Biosystems Sciences and Engineering, Institute of AgronomyUniversity of LisbonLisbonPortugal
  6. 6.São Paulo State University (UNESP)São VicenteBrazil
  7. 7.Instituto de Estudos Avançados do Mar (IEAMar/UNESP)São VicenteBrazil
  8. 8.Bioscience InstituteSão Paulo State UniversitySão VicenteBrazil

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