Enrichment of electrogenic consortiums for the degradation of vinasses and molasses in MFC

Abstract

Energy production in Microbial Fuel Cell can be affected by microorganisms developed during organic matter degradation in wastewater from sugar cane, such as tequila and mezcal industry. Efficiencies of energy conversion remain insufficient for large-scale implementation of this technology. Geobacter sulfurreduscens and Shewanella oneidensis have been exhaustively studied; however, there are few reports about the capabilities of mixed consortiums for the degradation of organic matter and bioelectricity production. In this study, the most abundant bacterial genera were Bacteroides, Lactobacillus, Gluconobacter, Pseudomonas, and Rikenellaceae in Dual Chamber-Microbial Fuel Cell, whose consortia generated a maximum voltage of 160 mV from a chemical oxygen demand of 4200 mg/L. Furthermore, we evaluate performance by equivalent circuit modeling; results suggest that internal resistances affect performance, and high-power density is observed when ohmic resistance decreases. In addition, capacitive and ion transport elements and load transfer resistance can be influenced by the consortiums developed, which determines that the bioelectrochemical performance depends to a greater extent on the microbial community. Scanning electronic microscopy analysis showed differences in the apparent density of anodic biofilm. We found that the substrate directly affects the development of electrogenic microbial consortiums, their organic matter degradation, and bioelectricity production capacities.

Keywords

Electrogenic microbial consortium / Microbial fuel cell / Molasse / Vinasse / Bioelectricity production

References

[1] AdachiT, KitazumiY, ShiraiO, KanoK. Direct electron transfer-type bioelectrocatalysis by membrane-bound aldehyde dehydrogenase from Gluconobacter oxydans and cyanide effects on its bioelectrocatalytic properties. Electrochem Commun, 2021, 123106911.

[2] Arellano-GarcíaL, Velázquez-FernándezJB, Macías-MuroM, Marino-MarmolejoEN. Continuous hydrogen production and microbial community profile in the dark fermentation of tequila Vinasse: response to increasing loading rates and immobilization of biomass. Biochem Eng J, 2021, 172108049.

[3] BhattiZA, SyedM, MaqboolF, ZhaoYG, YingX, SiddiquiMF, MahmoodQ. Potential of molasses substrate for bioelectricity production in microbial fuel cell with the help of active microbial community. Int J Energy Res, 2022, 46(8): 11185-11199.

[4] BianB, ShiD, CaiX, HuM, GuoQ, ZhangC, YangJ. 3D printed porous carbon anode for enhanced power generation in microbial fuel cell. Nano Energy, 2018, 44: 174-180.

[5] CallahanBJ, McMurdiePJ, HolmesSP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J, 2017, 11(12): 2639-2643.

[6] ChenL, WangM, FengY, XuX, LuoX, ZhangZ. Production of bioelectricity May play an important role for the survival of Xanthomonas campestris Pv. campestris (Xcc) under anaerobic conditions. Sci Total Environ, 2021, 768144335.

[7] ChenYY, YangFQ, XuN, WangXQ, XiePC, WangYZ, YongYC. Engineered cytochrome fused extracellular matrix enabled efficient extracellular electron transfer and improved performance of microbial fuel cell. Sci Total Environ, 2022, 830154806.

[8] ChoudhuryP, RayRN, BandyopadhyayTK, BasakB, MuthurajM, BhuniaB. Process engineering for stable power recovery from dairy wastewater using microbial fuel cell. Int J Hydrogen Energy, 2021, 46(4): 3171-3182.

[9] DingQ, HuangJ, ZhangH. Time-frequency spillovers among carbon, fossil energy and clean energy markets: the effects of attention to climate change. IRFA, 2022, 83102222.

[10] García-DepraectO, MuñozR, RodríguezE, ReneER, Leon-BecerrilE. Microbial ecology of a lactate-driven dark fermentation process producing hydrogen under carbohydrate-limiting conditions. Int J Hydrogen Energy, 2021, 46(20): 11284-11296.

[11] Guadarrama-PérezO, Guevara-PérezAC, Guadarrama-PérezVH, Bustos-TerronesV, Hernández-RomanoJ, Guillén-GarcésRA, Moeller-ChávezGE. Bioelectricity production from the anodic inoculation of Geobacter sulfurreducens DL-1 bacteria in constructed wetlands-microbial fuel cells. Bioelectrochemistry, 2023, 154108537.

[12] Guadarrama-PérezVH, Mijaylova-NachevaP, Moeller-ChávezGE, Guadarrama-PérezO. Equivalent circuits studied by means of electrochemical tests employing different inoculum and simultaneous treatment during bioelectricity production in a single chamber-microbial fuel cell. Biofuels, 2024, 15(1): 17-24.

[13] GuanCY, YuCP. Evaluation of plant microbial fuel cells for urban green roofs in a subtropical metropolis. Sci Total Environ, 2021, 765142786.

[14] HabeH, SatoY, TaniH, MatsutaniM, TaniokaK, TheeragoolG, YakushiT. Heterologous expression of membrane-bound alcohol dehydrogenase–encoding genes for glyceric acid production using Gluconobacter Sp CHM43 and its derivatives. Appl Microbiol Biotechnol, 2021, 105(18): 6749-6758.

[15] Hall M, Beiko RG (2018) 16S rRNA gene analysis with QIIME2 Microbiome analysis: methods and protocols. Humana Press 113–129. https://cir.nii.ac.jp/crid/1131412883668638861

[16] HemdanBA, El-TaweelGE, NahaS, GoswamiP. Bacterial community structure of electrogenic biofilm developed on modified graphite anode in microbial fuel cell. Sci Rep, 2023, 1311255.

[17] Huo W, Fu X, Bao M, Ye R, Shao Y, Liu Y, Lu W (2022) Manipulating and effect of electron acceptors on caproate production based on food waste two-phase chain elongation fermentation system. Available at SSRN 4033370. https://papers.ssrn.com/sol3/papers.cfm?abstract_id=4033370

[18] IEA, International energy agency (2023) https://www.iea.org/ (accessed 13 March 2024)

[19] KandpalR, NaraS, ShahadatM, AnsariMO, AlshahrieA, AliSW, MalhotraBD. Impedance spectroscopic study of biofilm formation on pencil lead graphite anode in microbial fuel cell. J Taiwan Inst Chem Eng, 2021, 128: 114-123.

[20] KataokaN, HirataK, MatsutaniM, AnoY, NguyenTM, AdachiO, YakushiT. Three ATP-dependent phosphorylating enzymes in the first committed step of dihydroxyacetone metabolism in Gluconobacter thailandicus NBRC3255. Appl Microbiol Biotechnol, 2021, 105(3): 1227-1236.

[21] KozichJJ, WestcottSL, BaxterNT, HighlanderSK, SchlossPD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq illumina sequencing platform. Appl Environ Microbiol, 2013, 79(17): 5112-5120.

[22] Krishnaraj RN, Berchmans S, Pal P (2015) The three-compartment microbial fuel cell: a new sustainable approach to bioelectricity generation from lignocellulosic biomass. Cellulose 22 (1), 655–662. https://link.springer.com/article/10.1007/s10570-014-0463-4

[23] LiM, ZhouS. Efficacy of Cu (II) as an electron-shuttle mediator for improved bioelectricity generation and cr (VI) reduction in microbial fuel cells. Bioresour Technol, 2019, 273: 122-129.

[24] LiXM, ChengKY, SelvamA, WongJW. Bioelectricity production from acidic food waste leachate using microbial fuel cells: effect of microbial inocula. Process Biochem, 2013, 48(2): 283-288.

[25] LiS, ChengC, ThomasA. Carbon-based microbial-fuel-cell electrodes: from conductive supports to active catalysts. Adv Mater, 2017, 2981602547.

[26] LiP, YuanW, HuangY, ZhangC, NiC, LinQ, WangJ. Complete genome sequence of Pseudomonas stutzeri S116 owning bifunctional catalysis provides insights into affecting performance of microbial fuel cells. BMC Microbiol, 2022, 221137.

[27] LiuQ, YangY, MeiX, LiuB, ChenC, XingD. Response of the microbial community structure of biofilms to ferric iron in microbial fuel cells. Sci Total Environ, 2018, 631: 695-701.

[28] LoganBE, ZikmundE, YangW, RossiR, KimKY, SaikalyPE, ZhangF. Impact of ohmic resistance on measured electrode potentials and maximum power production in microbial fuel cells. Environ Sci Technol, 2018, 52(15): 8977-8985.

[29] LuoJ, LiX, ZhangJ, FengA, XiaM, ZhouM. Global regulator engineering enhances bioelectricity generation in Pseudomonas aeruginosa-inoculated MFCs. Biosens Bioelectron, 2020, 163112269.

[30] MäkinenAE, LayCH, NissiläME, PuhakkaJA. Bioelectricity production on xylose with a compost enrichment culture. Int J Hydrogen Energy, 2013, 38(35): 15606-15612.

[31] MalikS, KishoreS, DhasmanaA, KumariP, MitraT, ChaudharyV, RajputVD. A perspective review on microbial fuel cells in treatment and product recovery from wastewater. Water, 2023, 152316.

[32] MartinsF, FelgueirasC, SmitkovaM, CaetanoN. Analysis of fossil fuel energy consumption and environmental impacts in European countries. Energies, 2019, 126964.

[33] Moran-SalazarRG, Sanchez-LizarragaAL, Rodriguez-CamposJ, Davila-VazquezG, Marino-MarmolejoEN, DendoovenL, Contreras-RamosSM. Utilization of Vinasses as soil amendment: consequences and perspectives. SpringerPlus, 2016, 511007.

[34] NegassaLW, MohiuddinM, TiruyeGA. Treatment of brewery industrial wastewater and generation of sustainable bioelectricity by microbial fuel cell inoculated with locally isolated microorganisms. J Water Process Eng, 2021, 41102018.

[35] PirbadianS, BarchingerSE, LeungKM, ByunHS, JangirY, BouhenniRA, GorbyYA. Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. PNAS, 2014, 111(35): 12883-12888.

[36] PlekhanovaY, TarasovS, BykovA, PrisyazhnayaN, KolesovV, SigaevV, ReshetilovA. Multiwalled carbon nanotubes and the electrocatalytic activity of Gluconobacter oxydans as the basis of a biosensor. Biosensors, 2019, 94137.

[37] RenH, LeeHS, ZhangJ, GardnerCL, ChaeJ. A quantitative extracellular electron transfer (EET) kinetics study of Geobacter sulfurreducens enriched microbial community reveals the transition of EET limiting step during biofilm growth. Int J Hydrogen Energy, 2021, 46(4): 3124-3134.

[38] RivallandC, RadouaniF, Gonzalez-RizzoS, RobertF, SalvinP. Enrichment of Clostridia enhances Geobacter population and electron harvesting in a complex electroactive biofilm. Bioelectrochemistry, 2022, 143107954.

[39] Robles-GonzálezV, Galíndez-MayerJ, Rinderknecht-SeijasN, Poggi-VaraldoHM. Treatment of Mezcal vinasses: A review. J Biotechnol, 2012, 157(4): 524-546.

[40] Rojas-FloresS, Pérez-DelgadoO, Nazario-NavedaR, Rojales-AlfaroH, BenitesSM, La Cruz-NoriegaD, OtinianoNM. Potential use of Papaya Aaste as a fuel for bioelectricity generation. Processes, 2021, 9101799.

[41] SarataleGD, SarataleRG, ShahidMK, ZhenG, KumarG, ShinHS, KimSH. A comprehensive overview on electro-active biofilms, role of exo-electrogens and their microbial niches in microbial fuel cells (MFCs). Chemosphere, 2017, 178: 534-547.

[42] Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O, Huttenhower C (2012) Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods 8811. https://doi.org/10.1038/nmeth.2066

[43] SindhujaM, KumarNS, SudhaV, HarinipriyaS. Equivalent circuit modeling of microbial fuel cells using impedance spectroscopy. J Energy Storage, 2016, 7: 136-146.

[44] Singh A, Kaushik A (2025) Suitability of wetland microbial consortium for enhanced and sustained power generation from distillery effluent in microbial fuel cell. Energy sources part A or ES part A. 47(1):4095–4111. https://doi.org/10.1080/15567036.2020.1864515

[45] WangA, LiuL, SunD, RenN, LeeDJ. Isolation of Fe (III)-reducing fermentative bacterium Bacteroides Sp W7 in the anode suspension of a microbial electrolysis cell (MEC). Int J Hydrogen Energy, 2010, 35(7): 3178-3182.

[46] WangVB, ChuaSL, CaoB, SeviourT, NesatyyVJ, MarsiliE, YangL. Engineering PQS biosynthesis pathway for enhancement of bioelectricity production in Pseudomonas aeruginosa microbial fuel cells. PLoS ONE, 2013, 85e63129.

[47] WangH, ChenP, ZhangS, JiangJ, HuaT, LiF. Degradation of pyrene using single-chamber air-cathode microbial fuel cells: electrochemical parameters and bacterial community changes. Sci Total Environ, 2022, 804150153.

[48] YangX, ChenS. Microorganisms in sediment microbial fuel cells: ecological niche, microbial response, and environmental function. Sci Total Environ, 2021, 756144145.

[49] YongYC, YuYY, LiCM, ZhongJJ, SongH. Bioelectricity enhancement via overexpression of quorum sensing system in Pseudomonas aeruginosa-inoculated microbial fuel cells. Biosens Bioelectron, 2011, 30(1): 87-92.

[50] ZaniACB, de AlmeidaÉJR, FurlanJPR, PedrinoM, GuazzaroniME, StehlingEG, ReginattoV. Electrobiochemical skills of Pseudomonas aeruginosa species that produce pyocyanin or Pyoverdine for glycerol oxidation in a microbial fuel cell. Chemosphere, 2023, 335139073.

[51] ZhaoYG, ZhangY, SheZ, ShiY, WangM, GaoM, GuoL. Effect of substrate conversion on performance of microbial fuel cells and anodic microbial communities. Environ Eng Sci, 2017, 34(9): 666-674.

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