Sustainable technologies for energy production and storage are currently in great demand. Bioelectrochemical systems (BESs) offer promising solutions for both. Several attempts have been made to improve carbon felt electrode characteristics with various pretreatments in order to enhance performance. This study was motivated by gaps in current knowledge of the impact of pretreatments on the enrichment and microbial composition of bioelectrochemical systems. Therefore, electrodes were treated with poly(neutral red), chitosan, or isopropanol in a first step and then fixed in microbial electrolysis cells (MECs). Four MECs consisting of organic substance-degrading bioanodes and methane-producing biocathodes were set up and operated in batch mode by controlling the bioanode at 400 mV vs. Ag/AgCl (3M NaCl). After 1 month of operation, Enterococcus species were dominant microorganisms attached to all bioanodes and independent of electrode pretreatment. However, electrode pretreatments led to a decrease in microbial diversity and the enrichment of specific electroactive genera, according to the type of modification used. The MEC containing isopropanol-treated electrodes achieved the highest performance due to presence of both Enterococcus and Geobacter. The obtained results might help to select suitable electrode pretreatments and support growth conditions for desired electroactive microorganisms, whereby performance of BESs and related applications, such as BES-based biosensors, could be enhanced.

ACIB GmbH Krenngasse 37 2 8010 Graz Austria

Department of Agrobiotechnology Institute of Environmental Biotechnology University of Natural Resources and Life Sciences Vienna Konrad Lorenz Strasse 20 3430 Tulln an der Donau Austria

Department of Biochemistry Faculty of Science Masaryk University Kamenice 753 5 62500 Brno Czech Republic

K1 MET GmbH Stahlstrasse 14 4020 Linz Austria

Linz Institute for Organic Solar Cells Institute of Physical Chemistry Johannes Kepler University Linz Altenberger Strasse 69 4040 Linz Austria

Zobrazit více v PubMed

Houghton J.T., Ding Y., Griggs D.J., Noguer M., van der Linden P.J., Dai X., Maskell K., Johnson C.A. IPCC, 2001: Climate Change 2001: The Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press; Cambridge, UK: New York, NY, USA: 2001.

Kumar S.S., Kumar V., Kumar R., Malyan S.K., Pugazhendhi A. Microbial fuel cells as a sustainable platform technology for bioenergy, biosensing, environmental monitoring, and other low power device applications. Fuel. 2019;255:115682. doi: 10.1016/j.fuel.2019.115682. DOI

Logan B.E., Hamelers B., Rozendal R., Schröder U., Keller J., Freguia S., Aelterman P., Verstraete W., Rabaey K. Microbial fuel cells: Methodology and technology. Environ. Sci. Technol. 2006;40:5181–5192. doi: 10.1021/es0605016. PubMed DOI

Kadier A., Kalil M.S., Abdeshahian P., Chandrasekhar K., Mohamed A., Azman N.F., Logroño W., Simayi Y., Hamid A.A. Recent advances and emerging challenges in microbial electrolysis cells (MECs) for microbial production of hydrogen and value-added chemicals. Renew. Sustain. Energy Rev. 2016;61:501–525. doi: 10.1016/j.rser.2016.04.017. DOI

Bajracharya S., Sharma M., Mohanakrishna G., Dominguez Benneton X., Strik D.P.B.T.B., Sarma P.M., Pant D. An overview on emerging bioelectrochemical systems (BESs): Technology for sustainable electricity, waste remediation, resource recovery, chemical production and beyond. Renew. Energy. 2016;98:153–170. doi: 10.1016/j.renene.2016.03.002. DOI

Rabaey K., Rozendal R.A. Microbial electrosynthesis-Revisiting the electrical route for microbial production. Nat. Rev. Microbiol. 2010;8:706–716. doi: 10.1038/nrmicro2422. PubMed DOI

Cheng S., Xing D., Call D.F., Logan B.E. Direct biological conversion of electrical current into methane by electromethanogenesis. Environ. Sci. Technol. 2009;43:3953–3958. doi: 10.1021/es803531g. PubMed DOI

Potter M.C. Electrical Effects Accompanying the Decomposition of Organic Compounds. Proc. R. Soc. B Biol. Sci. 1911;84:260–276. doi: 10.1098/rspb.1911.0073. DOI

Kumar R., Singh L., Zularisam A.W. Exoelectrogens: Recent advances in molecular drivers involved in extracellular electron transfer and strategies used to improve it for microbial fuel cell applications. Renew. Sustain. Energy Rev. 2016;56:1322–1336. doi: 10.1016/j.rser.2015.12.029. DOI

Do M.H., Ngo H.H., Guo W., Chang S.W., Nguyen D.D., Liu Y., Varjani S., Kumar M. Microbial fuel cell-based biosensor for online monitoring wastewater quality: A critical review. Sci. Total Environ. 2020;712:135612. doi: 10.1016/j.scitotenv.2019.135612. PubMed DOI

Abrevaya X.C., Sacco N.J., Bonetto M.C., Hilding-Ohlsson A., Cortón E. Analytical applications of microbial fuel cells. Part II: Toxicity, microbial activity and quantification, single analyte detection and other uses. Biosens. Bioelectron. 2015;63:591–601. doi: 10.1016/j.bios.2014.04.053. PubMed DOI

Pham T.H., Aelterman P., Verstraete W. Bioanode performance in bioelectrochemical systems: Recent improvements and prospects. Trends Biotechnol. 2009;27:168–178. doi: 10.1016/j.tibtech.2008.11.005. PubMed DOI

Jafary T., Daud W.R.W., Ghasemi M., Kim B.H., Md Jahim J., Ismail M., Lim S.S. Biocathode in microbial electrolysis cell; Present status and future prospects. Renew. Sustain. Energy Rev. 2015;47:23–33. doi: 10.1016/j.rser.2015.03.003. DOI

Zhao H.Z., Zhang Y., Chang Y.Y., Li Z.S. Conversion of a substrate carbon source to formic acid for carbon dioxide emission reduction utilizing series-stacked microbial fuel cells. J. Power Sources. 2012;217:59–64. doi: 10.1016/j.jpowsour.2012.06.014. DOI

Steinbusch K.J.J., Hamelers H.V.M., Schaap J.D., Kampman C., Buisman C.J.N. Bioelectrochemical ethanol production through mediated acetate reduction by mixed cultures. Environ. Sci. Technol. 2010;44:513–517. doi: 10.1021/es902371e. PubMed DOI

Clauwaert P., Tolêdo R., van der Ha D., Crab R., Verstraete W., Hu H., Udert K.M., Rabaey K. Combining biocatalyzed electrolysis with anaerobic digestion. Water Sci. Technol. 2008;57:575–579. doi: 10.2166/wst.2008.084. PubMed DOI

Villano M., Aulenta F., Ciucci C., Ferri T., Giuliano A., Majone M. Bioelectrochemical reduction of CO2 to CH4 via direct and indirect extracellular electron transfer by a hydrogenophilic methanogenic culture. Bioresour. Technol. 2010;101:3085–3090. doi: 10.1016/j.biortech.2009.12.077. PubMed DOI

Villano M., Monaco G., Aulenta F., Majone M. Electrochemically assisted methane production in a biofilm reactor. J. Power Sources. 2011;196:9467–9472. doi: 10.1016/j.jpowsour.2011.07.016. DOI

Villano M., Ralo C., Zeppilli M., Aulenta F., Majone M. Influence of the set anode potential on the performance and internal energy losses of a methane-producing microbial electrolysis cell. Bioelectrochemistry. 2016;107:1–6. doi: 10.1016/j.bioelechem.2015.07.008. PubMed DOI

Jiang Y., Su M., Li D. Removal of sulfide and production of methane from carbon dioxide in microbial fuel cells-microbial electrolysis cell (MFCs-MEC) coupled system. Appl. Biochem. Biotechnol. 2014;172:2720–2731. doi: 10.1007/s12010-013-0718-9. PubMed DOI

Clauwaert P., Van Der Ha D., Boon N., Verbeken K., Verhaege M., Rabaey K., Verstraete W. Open air biocathode enables effective electricity generation with microbial fuel cells. Environ. Sci. Technol. 2007;41:7564–7569. doi: 10.1021/es0709831. PubMed DOI

Clauwaert P., Rabaey K., Aelterman P., De Schamphelaire L., Pham T.H., Boeckx P., Boon N., Verstraete W. Biological denitrification in microbial fuel cells. Environ. Sci. Technol. 2007;41:3354–3360. doi: 10.1021/es062580r. PubMed DOI

Zeppilli M., Paiano P., Villano M., Majone M. Anodic vs cathodic potentiostatic control of a methane producing microbial electrolysis cell aimed at biogas upgrading. Biochem. Eng. J. 2019;152:107393. doi: 10.1016/j.bej.2019.107393. DOI

Zeppilli M., Villano M., Aulenta F., Lampis S., Vallini G., Majone M. Effect of the anode feeding composition on the performance of a continuous-flow methane-producing microbial electrolysis cell. Environ. Sci. Pollut. Res. 2015;22:7349–7360. doi: 10.1007/s11356-014-3158-3. PubMed DOI

Villano M., Scardala S., Aulenta F., Majone M. Carbon and nitrogen removal and enhanced methane production in a microbial electrolysis cell. Bioresour. Technol. 2013;130:366–371. doi: 10.1016/j.biortech.2012.11.080. PubMed DOI

Penteado E.D., Fernandez-Marchante C.M., Zaiat M., Gonzalez E.R., Rodrigo M.A. Influence of carbon electrode material on energy recovery from winery wastewater using a dual-chamber microbial fuel cell. Environ. Technol. 2017;38:1333–1341. doi: 10.1080/09593330.2016.1226961. PubMed DOI

Santoro C., Guilizzoni M., Correa Baena J.P., Pasaogullari U., Casalegno A., Li B., Babanova S., Artyushkova K., Atanassov P. The effects of carbon electrode surface properties on bacteria attachment and start up time of microbial fuel cells. Carbon N. Y. 2014;67:128–139. doi: 10.1016/j.carbon.2013.09.071. DOI

Kaur R., Marwaha A., Chhabra V.A., Kim K.H., Tripathi S.K. Recent developments on functional nanomaterial-based electrodes for microbial fuel cells. Renew. Sustain. Energy Rev. 2020;119:109551. doi: 10.1016/j.rser.2019.109551. DOI

Palanisamy G., Jung H.Y., Sadhasivam T., Kurkuri M.D., Kim S.C., Roh S.H. A comprehensive review on microbial fuel cell technologies: Processes, utilization, and advanced developments in electrodes and membranes. J. Clean. Prod. 2019;221:598–621. doi: 10.1016/j.jclepro.2019.02.172. DOI

Li S., Cheng C., Thomas A. Carbon-Based Microbial-Fuel-Cell Electrodes: From Conductive Supports to Active Catalysts. Adv. Mater. 2017;29 doi: 10.1002/adma.201602547. PubMed DOI

Sonawane J.M., Yadav A., Ghosh P.C., Adeloju S.B. Recent advances in the development and utilization of modern anode materials for high performance microbial fuel cells. Biosens. Bioelectron. 2017;90:558–576. doi: 10.1016/j.bios.2016.10.014. PubMed DOI

Srinophakun P., Thanapimmetha A., Plangsri S., Vetchayakunchai S., Saisriyoot M. Application of modified chitosan membrane for microbial fuel cell: Roles of proton carrier site and positive charge. J. Clean. Prod. 2017;142:1274–1282. doi: 10.1016/j.jclepro.2016.06.153. DOI

Harewood A.J.T., Popuri S.R., Cadogan E.I., Lee C.H., Wang C.C. Bioelectricity generation from brewery wastewater in a microbial fuel cell using chitosan/biodegradable copolymer membrane. Int. J. Environ. Sci. Technol. 2017;14:1535–1550. doi: 10.1007/s13762-017-1258-6. DOI

Zhang T., Nie H., Bain T.S., Lu H., Cui M., Snoeyenbos-West O.L., Franks A.E., Nevin K.P., Russell T.P., Lovley D.R. Improved cathode materials for microbial electrosynthesis. Energy Environ. Sci. 2013;6:217–224. doi: 10.1039/C2EE23350A. DOI

Pauliukaite R., Ghica M.E., Barsan M., Brett C.M.A. Characterisation of poly(neutral red) modified carbon film electrodes; Application as a redox mediator for biosensors. J. Solid State Electrochem. 2007;11:899–908. doi: 10.1007/s10008-007-0281-9. DOI

Park D.H., Zeikus J.G. Electricity generation in microbial fuel cells using neutral red as an electronophore. Appl. Environ. Microbiol. 2000;66:1292–1297. doi: 10.1128/AEM.66.4.1292-1297.2000. PubMed DOI PMC

Seelajaroen H., Haberbauer M., Hemmelmair C., Aljabour A., Dumitru L.M., Hassel A.W., Sariciftci N.S. Enhanced Bio-Electrochemical Reduction of Carbon Dioxide by Using Neutral Red as a Redox Mediator. ChemBioChem. 2019;20:1196–1205. doi: 10.1002/cbic.201800784. PubMed DOI PMC

Cheng S., Liu W., Sun D., Huang H. Enhanced power production of microbial fuel cells by reducing the oxygen and nitrogen functional groups of carbon cloth anode. Surf. Interface Anal. 2017;49:410–418. doi: 10.1002/sia.6173. DOI

Kondaveeti S., Min B. Nitrate reduction with biotic and abiotic cathodes at various cell voltages in bioelectrochemical denitrification system. Bioprocess. Biosyst. Eng. 2013;36:231–238. doi: 10.1007/s00449-012-0779-0. PubMed DOI

Seelajaroen H., Spiess S., Haberbauer M., Hassel M.M., Aljabour A., Thallner S., Guebitz G., Sariciftci N.S. Enhanced methane producing microbial electrolysis cells for wastewater treatment using poly(neutral red) and chitosan modified electrodes. Sustain. Energy Fuels. 2020 doi: 10.1039/D0SE00770F. DOI

Pichler M., Coskun Ö.K., Ortega-Arbulú A.S., Conci N., Wörheide G., Vargas S., Orsi W.D. A 16S rRNA gene sequencing and analysis protocol for the Illumina MiniSeq platform. Microbiologyopen. 2018;7:1–10. doi: 10.1002/mbo3.611. PubMed DOI PMC

Callahan B.J., McMurdie P.J., Rosen M.J., Han A.W., Johnson A.J.A., Holmes S.P. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods. 2016;13:581–583. doi: 10.1038/nmeth.3869. PubMed DOI PMC

Vítěz T., Novák D., Lochman J., Vítězová M. Methanogens diversity during anaerobic sewage sludge stabilization and the effect of temperature. Processes. 2020;8:822. doi: 10.3390/pr8070822. DOI

Geppert F., Liu D., van Eerten-Jansen M., Weidner E., Buisman C., ter Heijne A. Bioelectrochemical Power-to-Gas: State of the Art and Future Perspectives. Trends Biotechnol. 2016;34:879–894. doi: 10.1016/j.tibtech.2016.08.010. PubMed DOI

Feng Y., Yang Q., Wang X., Logan B.E. Treatment of carbon fiber brush anodes for improving power generation in air-cathode microbial fuel cells. J. Power Sources. 2010;195:1841–1844. doi: 10.1016/j.jpowsour.2009.10.030. DOI

Cai H., Wang J., Bu Y., Zhong Q. Treatment of carbon cloth anodes for improving power generation in a dual-chamber microbial fuel cell. J. Chem. Technol. Biotechnol. 2013;88:623–628. doi: 10.1002/jctb.3875. DOI

Pankratova G., Leech D., Gorton L., Hederstedt L. Extracellular Electron Transfer by the Gram-Positive Bacterium Enterococcus faecalis. Biochemistry. 2018;57:4597–4603. doi: 10.1021/acs.biochem.8b00600. PubMed DOI

Pillai S.K., Sakoulas G., Eliopoulos G.M., Moellering R.C., Murray B.E., Inouye R.T. Effects of glucose on fsr-mediated biofilm formation in Enterococcus faecalis. J. Infect. Dis. 2004;190:967–970. doi: 10.1086/423139. PubMed DOI

Freguia S., Masuda M., Tsujimura S., Kano K. Lactococcus lactis catalyses electricity generation at microbial fuel cell anodes via excretion of a soluble quinone. Bioelectrochemistry. 2009;76:14–18. doi: 10.1016/j.bioelechem.2009.04.001. PubMed DOI

Bohn J., Yüksel-Dadak A., Dröge S., König H. Isolation of lactic acid-forming bacteria from biogas plants. J. Biotechnol. 2017;244:4–15. doi: 10.1016/j.jbiotec.2016.12.015. PubMed DOI

Grabowski A., Tindall B.J., Bardin V., Blanchet D., Jeanthon C. Petrimonas sulfuriphila gen. nov., sp. nov., a mesophilic fermentative bacterium isolated from a biodegraded oil reservoir. Int. J. Syst. Evol. Microbiol. 2005;55:1113–1121. doi: 10.1099/ijs.0.63426-0. PubMed DOI

Khan F., Pham D.T.N., Oloketuyi S.F., Manivasagan P., Oh J., Kim Y.M. Chitosan and their derivatives: Antibiofilm drugs against pathogenic bacteria. Colloids Surfaces B Biointerfaces. 2020;185:110627. doi: 10.1016/j.colsurfb.2019.110627. PubMed DOI

Joicy A., Song Y.C., Li J., Oh S.E., Jang S.H., Ahn Y. Effect of electrostatic field strength on bioelectrochemical nitrogen removal from nitrogen-rich wastewater. Energies. 2020;13:3218. doi: 10.3390/en13123218. DOI

Xu H., Wang L., Wen Q., Chen Y., Qi L., Huang J., Tang Z. A 3D porous NCNT sponge anode modified with chitosan and Polyaniline for high-performance microbial fuel cell. Bioelectrochemistry. 2019;129:144–153. doi: 10.1016/j.bioelechem.2019.05.008. PubMed DOI

Logan B.E., Rossi R., Ragab A., Saikaly P.E. Electroactive microorganisms in bioelectrochemical systems. Nat. Rev. Microbiol. 2019;17:307–319. doi: 10.1038/s41579-019-0173-x. PubMed DOI

Gregory K.B., Bond D.R., Lovley D.R. Graphite electrodes as electron donors for anaerobic respiration. Environ. Microbiol. 2004;6:596–604. doi: 10.1111/j.1462-2920.2004.00593.x. PubMed DOI

Bond D.R., Lovley D.R. Electricity production by Geobacter sulfurreducens attached to electrodes. Appl. Environ. Microbiol. 2003;69:1548–1555. doi: 10.1128/AEM.69.3.1548-1555.2003. PubMed DOI PMC

Reguera G., Nevin K.P., Nicoll J.S., Covalla S.F., Woodard T.L., Lovley D.R. Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl. Environ. Microbiol. 2006;72:7345–7348. doi: 10.1128/AEM.01444-06. PubMed DOI PMC

White G.F., Edwards M.J., Gomez-Perez L., Richardson D.J., Butt J.N., Clarke T.A. Mechanisms of Bacterial Extracellular Electron. Exchange. 1st ed. Volume 68 Elsevier Ltd.; Amsterdam, The Netherlands: 2016. PubMed

Dennis P.G., Virdis B., Vanwonterghem I., Hassan A., Hugenholtz P., Tyson G.W., Rabaey K. Anode potential influences the structure and function of anodic electrode and electrolyte-associated microbiomes. Sci. Rep. 2016;6:1–11. doi: 10.1038/srep39114. PubMed DOI PMC

Zhang Y., Min B., Huang L., Angelidaki I. Electricity generation and microbial community response to substrate changes in microbial fuel cell. Bioresour. Technol. 2011;102:1166–1173. doi: 10.1016/j.biortech.2010.09.044. PubMed DOI

Baldwin S.A., Khoshnoodi M., Rezadehbashi M., Taupp M., Hallam S., Mattes A., Sanei H. The microbial community of a passive biochemical reactor treating arsenic, zinc, and sulfate-rich seepage. Front. Bioeng. Biotechnol. 2015;3:1–13. doi: 10.3389/fbioe.2015.00027. PubMed DOI PMC

Pelletier E., Kreimeyer A., Bocs S., Rouy Z., Gyapay G., Chouari R., Rivière D., Ganesan A., Daegelen P., Sghir A., et al. “Candidatus Cloacamonas acidaminovorans”: Genome sequence reconstruction provides a first glimpse of a new bacterial division. J. Bacteriol. 2008;190:2572–2579. doi: 10.1128/JB.01248-07. PubMed DOI PMC

Dahle H., Birkeland N.K. Thermovirga lienii gen. nov., sp. nov., a novel moderately thermophilic, anaerobic, amino-acid-degrading bacterium isolated from a North Sea oil well. Int. J. Syst. Evol. Microbiol. 2006;56:1539–1545. doi: 10.1099/ijs.0.63894-0. PubMed DOI

Commault A.S., Barrière F., Lapinsonnière L., Lear G., Bouvier S., Weld R.J. Influence of inoculum and anode surface properties on the selection of Geobacter-dominated biofilms. Bioresour. Technol. 2015;195:265–272. doi: 10.1016/j.biortech.2015.06.141. PubMed DOI

Guo K., Freguia S., Dennis P.G., Chen X., Donose B.C., Keller J., Gooding J.J., Rabaey K. Effects of surface charge and hydrophobicity on anodic biofilm formation, community composition, and current generation in bioelectrochemical systems. Environ. Sci. Technol. 2013;47:7563–7570. doi: 10.1021/es400901u. PubMed DOI

Stöckl M., Teubner N.C., Holtmann D., Mangold K.M., Sand W. Extracellular Polymeric Substances from Geobacter sulfurreducens Biofilms in Microbial Fuel Cells. ACS Appl. Mater. Interfaces. 2019;11:8961–8968. doi: 10.1021/acsami.8b14340. PubMed DOI

Yang G., Huang L., Yu Z., Liu X., Chen S., Zeng J., Zhou S., Zhuang L. Anode potentials regulate Geobacter biofilms: New insights from the composition and spatial structure of extracellular polymeric substances. Water Res. 2019;159:294–301. doi: 10.1016/j.watres.2019.05.027. PubMed DOI

Rezaei F., Xing D., Wagner R., Regan J.M., Richard T.L., Logan B.E. Simultaneous cellulose degradation and electricity production by Enterobacter cloacae in a microbial fuel cell. Appl. Environ. Microbiol. 2009;75:3673–3678. doi: 10.1128/AEM.02600-08. PubMed DOI PMC

Fedorovich V., Knighton M.C., Pagaling E., Ward F.B., Free A., Goryanin I. Novel electrochemically active bacterium phylogenetically related to Arcobacter butzleri, isolated from a microbial fuel cell. Appl. Environ. Microbiol. 2009;75:7326–7334. doi: 10.1128/AEM.01345-09. PubMed DOI PMC

Ha P.T., Tae B., Chang I.S. Performance and bacterial consortium of microbial fuel cell fed with formate. Energy Fuels. 2008;22:164–168. doi: 10.1021/ef700294x. DOI

Zhang T., Cui C., Chen S., Yang H., Shen P. The direct electrocatalysis of Escherichia coli through electroactivated excretion in microbial fuel cell. Electrochem. Commun. 2008;10:293–297. doi: 10.1016/j.elecom.2007.12.009. DOI

Bourdakos N., Marsili E., Mahadevan R. A defined co-culture of Geobacter sulfurreducens and Escherichia coli in a membrane-less microbial fuel cell. Biotechnol. Bioeng. 2014;111:709–718. doi: 10.1002/bit.25137. PubMed DOI

Aulenta F., Catapano L., Snip L., Villano M., Majone M. Linking bacterial metabolism to graphite cathodes: Electrochemical insights into the H2-producing capability of desulfovibrio sp. ChemSusChem. 2012;5:1080–1085. doi: 10.1002/cssc.201100720. PubMed DOI

Metal recovery from spent lithium-ion batteries via two-step bioleaching using adapted chemolithotrophs from an acidic mine pit lake

Zinc recovery from bioleachate using a microbial electrolysis cell and comparison with selective precipitation

Bioelectrochemical methanation by utilization of steel mill off-gas in a two-chamber microbial electrolysis cell