Abstract
This study describes the effects of graphene oxide (GO) and reduced graphene oxide (rGO) on the acetoclastic, hydrogenotrophic and methylotrophic pathways of methanogenesis by an anaerobic consortium. The results showed that GO negatively affected the hydrogenotrophic and acetoclastic pathways at a concentration of 300 mg/L, causing a decrease of ~ 38% on the maximum specific methanogenic activity (MMA) with respect to the controls lacking GO. However, the presence of rGO (300 mg/L) promoted an improvement of the MMA (> 45%) achieved with all substrates, except for the hydrogenotrophic pathway, which was relatively insensitive to rGO. The presence of either rGO or GO enhanced the methylotrophic pathway and resulted in an increase of the MMA of up to 55%. X-ray photoelectron spectroscopy (XPS) analysis revealed that GO underwent microbial reduction during the incubation period. Electrons derived from substrates oxidation were deviated from methanogenesis towards the reduction of GO, which may explain the MMA decreased observed in the presence of GO. Furthermore, XPS evidence indicated that the extent of GO reduction depended on the metabolic pathway triggered by a given substrate.
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References
Akhavan O, Ghaderi E (2012) Escherichia coli bacteria reduce graphene oxide to bactericidal graphene in a self-limiting manner. Carbon 50:1853–1860. https://doi.org/10.1016/j.carbon.2011.12.035
Bagri A, Mattevi C, Acik M et al (2010) Structural evolution during the reduction of chemically derived graphene oxide. Nat Chem 2:581–587. https://doi.org/10.1038/nchem.686
Barua S, Dhar BR (2017) Advances towards understanding and engineering direct interspecies electron transfer in anaerobic digestion. Bioresour Technol 244:698–707. https://doi.org/10.1016/j.biortech.2017.08.023
Biniak S, Szymański G, Siedlewski J, Świątkowski A (1997) The characterization of activated carbons with oxygen and nitrogen surface groups. Carbon 35:1799–1810. https://doi.org/10.1016/S0008-6223(97)00096-1
Bueno-López JI, Rangel-Mendez JR, Alatriste-Mondragón F et al (2018) Graphene oxide triggers mass transfer limitations on the methanogenic activity of an anaerobic consortium with a particulate substrate. Chemosphere 211:709–716. https://doi.org/10.1016/j.chemosphere.2018.08.001
Capson-Tojo G, Moscoviz R, Ruiz D et al (2018) Addition of granular activated carbon and trace elements to favor volatile fatty acid consumption during anaerobic digestion of food waste. Bioresour Technol 260:157–168. https://doi.org/10.1016/J.BIORTECH.2018.03.097
Caruana DJ, Olsen AE (eds) (2016) Anaerobic digestion: processes, products, and applications. Nova Science Publishers, New York
Cervantes FJ, Dos Santos AB (2011) Reduction of azo dyes by anaerobic bacteria: microbiological and biochemical aspects. Rev Environ Sci Biotechnol 10:125–137. https://doi.org/10.1007/s11157-011-9228-9
Cervantes FJ, De Bok FAM, Duong-Dac T et al (2002) Reduction of humic substances by halorespiring, sulphate-reducing and methanogenic microorganisms. Environ Microbiol 4:51–57. https://doi.org/10.1046/j.1462-2920.2002.00258.x
Chen Y, Niu Y, Tian T et al (2017) Microbial reduction of graphene oxide by Azotobacter chroococcum. Chem Phys Lett 677:143–147. https://doi.org/10.1016/j.cplett.2017.04.002
Colunga A, Rangel-Mendez JR, Celis LB, Cervantes FJ (2015) Graphene oxide as electron shuttle for increased redox conversion of contaminants under methanogenic and sulfate-reducing conditions. Bioresour Technol 175:309–314. https://doi.org/10.1016/j.biortech.2014.10.101
Costa KC, Leigh JA (2014) Metabolic versatility in methanogens. Curr Opin Biotechnol 29:70–75. https://doi.org/10.1016/j.copbio.2014.02.012
De Silva KKH, Huang H-H, Joshi RK, Yoshimura M (2017) Chemical reduction of graphene oxide using green reductants. Carbon 119:190–199. https://doi.org/10.1016/j.carbon.2017.04.025
De Velasco-Maldonado PS, Pat-Espadas AM, Cházaro-Ruíz LF, Cervantes FJ, Hernández-Montoya V (2019) Cold oxygen plasma induces changes on the surface of carbon materials enhancing methanogenesis and N2O reduction in anaerobic sludge incubations. J Chem Technol Biotechnol 94:3367–3374. https://doi.org/10.1002/jctb.6149
Deppenmeier U (2002) Redox-driven proton translocation in methanogenic Archaea. Cell Mol Life Sci 59:1513–1533. https://doi.org/10.1007/s00018-002-8526-3
Dong B, Xia Z, Sun J et al (2019) The inhibitory impacts of nano-graphene oxide on methane production from waste activated sludge in anaerobic digestion. Sci Tot Environ 646:1376–1384. https://doi.org/10.1016/j.scitotenv.2018.07.424
Dreyer DR, Park S, Bielawski CW, Ruoff RS (2010) The chemistry of graphene oxide. Chem Soc Rev 39:228–240. https://doi.org/10.1039/b917103g
Edyvean RGJ, Banwart SA, Ojeda JJ et al (2008) Characterization of the cell surface and cell wall chemistry of drinking water bacteria by combining XPS, FTIR spectroscopy, modeling, and potentiometric titrations. Langmuir 24:4032–4040. https://doi.org/10.1021/la702284b
Guo Z, Xie C, Zhang P et al (2017) Toxicity and transformation of graphene oxide and reduced graphene oxide in bacteria biofilm. Sci Tot Environ 580:1300–1308. https://doi.org/10.1016/j.scitotenv.2016.12.093
Gurunathan S, Woong Han J, Eppakayala V, Kim J-H (2013) Microbial reduction of graphene oxide by Escherichia coli: a green chemistry approach. Colloid Surf B Biointerfaces 102:772–777. https://doi.org/10.1016/j.colsurfb.2012.09.011
Jastrzębska AM, Olszyna AR (2015) The ecotoxicity of graphene family materials: current status, knowledge gaps and future needs. J Nanopart Res 17:40. https://doi.org/10.1007/s11051-014-2817-0
Jung I, Vaupel M, Pelton M et al (2008) Characterization of thermally reduced graphene oxide by imaging ellipsometry. J Phys Chem C 112:8499–8506. https://doi.org/10.1021/jp802173m
Leone L, Loring J, Sjöberg S et al (2006) Surface characterization of the Gram-positive bacteria Bacillus subtilis—an XPS study. Surf Interface Anal 38:202–205. https://doi.org/10.1002/sia.2184
Lin R, Cheng J, Zhang J et al (2017) Boosting biomethane yield and production rate with graphene: the potential of direct interspecies electron transfer in anaerobic digestion. Bioresour Technol 239:345–352. https://doi.org/10.1016/j.biortech.2017.05.017
Liu S, Hu M, Zeng TH et al (2012) Lateral dimension dependent antibacterial activity of graphene oxide sheets. Langmuir. https://doi.org/10.1021/la3023908
Lovley DR (2011) Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination. Energy Environ Sci 4:4896. https://doi.org/10.1039/c1ee02229f
Martins G, Salvador AF, Pereira L, Alves MM (2018) Methane production and conductive materials: a critical review. Environ Sci Technol 52:10241–10253. https://doi.org/10.1021/acs.est.8b01913
Park J-H, Kang H-J, Park K-H, Park H-D (2018) Direct interspecies electron transfer via conductive materials: a perspective for anaerobic digestion applications. Bioresour Technol 254:300–311. https://doi.org/10.1016/j.biortech.2018.01.095
Pei S, Cheng H-M (2012) The reduction of graphene oxide. Carbon 50:3210–3228. https://doi.org/10.1016/j.carbon.2011.11.010
Pereira L, Pereira R, Pereira MFR, Alves MM (2016) Effect of different carbon materials as electron shuttles in the anaerobic biotransformation of nitroanilines. Biotechnol Bioeng 113:1194–1202. https://doi.org/10.1002/bit.25896
Raveendran S, Chauhan N, Nakajima Y et al (2013) Ecofriendly route for the synthesis of highly conductive graphene using extremophiles for green electronics and bioscience. Part Syst Charact 30:573–578. https://doi.org/10.1002/ppsc.201200126
Raza H (ed) (2012) Graphene nanoelectronic. Springer, Berlin. https://doi.org/10.1007/978-3-642-22984-8
Rivière D, Desvignes V, Pelletier E, Chaussonnerie S, Guermazi S, Weissenbach J, Li T, Camacho P, Sghir A (2009) Towards the definition of a core of microorganisms involved in anaerobic digestion of sludge. ISME J 3:700–714
Salas EC, Sun Z, Lüttge A, Tour JM (2010) Reduction of graphene oxide via bacterial respiration. ACS Nano 4:4852–4856. https://doi.org/10.1021/nn101081t
Salvador AF, Martins G, Melle-Franco M, Serpa R, Stams AJM, Cavaleiro AJ, Pereira MA, Alves MM (2017) Carbon nanotubes accelerate methane production in pure cultures of methanogens and in syntrophic coculture. Environ Microbiol 19:2727–2739. https://doi.org/10.1111/1462-2920.13774
Shen L, Jin Z, Wang D et al (2018) Enhance wastewater biological treatment through the bacteria induced graphene oxide hydrogel. Chemosphere 190:201–210. https://doi.org/10.1016/j.chemosphere.2017.09.105
Simon-Pascal A, Sierra-Alvarez R, Field JA (2019) Platinum(II) reduction to platinum nanoparticles in anaerobic sludge. J Chem Technol Biotechnol 94:468–474. https://doi.org/10.1002/jctb.5791
Thakur S, Karak N (2015) Alternative methods and nature-based reagents for the reduction of graphene oxide: a review. Carbon 94:224–242. https://doi.org/10.1016/j.carbon.2015.06.030
Tian T, Qiao S, Li X et al (2017) Nano-graphene induced positive effects on methanogenesis in anaerobic digestion. Bioresour Technol 224:41–47. https://doi.org/10.1016/j.biortech.2016.10.058
Toral-Sánchez E, Ascacio Valdés JA, Aguilar CN et al (2016) Role of the intrinsic properties of partially reduced graphene oxides on the chemical transformation of iopromide. Carbon 99:456–465. https://doi.org/10.1016/j.carbon.2015.12.067
Toral-Sánchez E, Ascacio Valdés JA, Aguilar CN, Rangel-Méndez JR, Cervantes FJ (2017) Tailoring partially reduced graphene oxide as redox mediator for enhanced biotransformation of iopromide under methanogenic and sulfate-reducing conditions. Bioresour Technol 227:269–276. https://doi.org/10.1016/j.biortech.2016.10.062
Toral-Sánchez E, Rangel-Méndez JR, Hurt RH, Ascacio-Valdés JA, Aguilar CN, Cervantes FJ (2018) Novel application of magnetic nano-carbon composite as redox mediator in the reductive biodegradation of iopromide in anaerobic continuous systems. Appl Microbiol Biotechnol 102:8951–8961. https://doi.org/10.1007/s00253-018-9250-8
van der Zee FP, Bisschops IAE, Lettinga G, Field JA (2003) Activated carbon as an electron acceptor and redox mediator during the anaerobic biotransformation of azo dyes. Environ Sci Technol 37:402–408. https://doi.org/10.1021/es025885o
Wang G, Qian F, Saltikov CW, Jiao Y, Li Y (2011) Microbial reduction of graphane oxide by Shewanella. Nano Res 4:563–570. https://doi.org/10.1007/s12274-011-0112-2
Weiland P (2010) Biogas production: current state and perspectives. Appl Microbiol Biotechnol 85:849–860. https://doi.org/10.1007/s00253-009-2246-7
Xu S, He C, Luo L et al (2015) Comparing activated carbon of different particle sizes on enhancing methane generation in upflow anaerobic digester. Bioresour Technol 196:606–612. https://doi.org/10.1016/j.biortech.2015.08.018
Yoshida N, Miyata Y, Doi K et al (2016) Graphene oxide-dependent growth and self-aggregation into a hydrogel complex of exoelectrogenic bacteria. Sci Rep 6:21867. https://doi.org/10.1038/srep21867
Zhang H, Da Z, Feng Y et al (2018) Enhancing the electricity generation and sludge reduction of sludge microbial fuel cell with graphene oxide and reduced graphene oxide. J Clean Prod 186:104–112. https://doi.org/10.1016/j.jclepro.2018.02.159
Acknowledgements
J.I. Bueno-López thanks for the scholarship received from Tecnológico Nacional de México. Additionally, authors acknowledge the technical support provided by K. Jog at The University of Arizona. This research was financially supported by the Council of Science and Technology of Mexico (CONACYT, Grant 1289 from the program Frontiers in Science) and by the National Science Foundation (NSF award # 1507446).
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Bueno-López, J.I., Nguyen, C.H., Rangel-Mendez, J.R. et al. Effects of graphene oxide and reduced graphene oxide on acetoclastic, hydrogenotrophic and methylotrophic methanogenesis. Biodegradation 31, 35–45 (2020). https://doi.org/10.1007/s10532-020-09892-0
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DOI: https://doi.org/10.1007/s10532-020-09892-0