Microbial reduction of graphene oxide and its application in microbial fuel cells and biophotovoltaics

Abstract

Despite more than a decade of study, there are still significant obstacles to overcome before graphene can be successfully produced on a large scale for commercial use. Chemical oxidation of graphite to produce graphene oxide (GO), followed by a subsequent reduction process to synthesize reduced graphene oxide (rGO), is considered the most practical method for mass production. Microorganisms, which are abundant in nature and inexpensive, are one of the potential green reductants for rGO synthesis. However, there is no recent review discussing the reported microbial reduction of GO in detail. To address this, we present a comprehensive review on the reduction of GO by a range of microorganisms and compared their efficacies and reaction conditions. Also, presented were the mechanisms by which microorganisms reduce GO. We also reviewed the recent advancements in using microbially reduced GO as the anode and cathode material in the microbial fuel cell (MFC) and algal biophotovoltaics (BPV), as well as the challenges and future directions in microbial fuel cell research.

Graphical abstract

Keywords

reduced graphene oxide / microbial reduction / microbial fuel cell / algal biophotovoltaics / green chemistry

References

[1] Meyer J C, Geim A K, Katsnelson M I, . The structure of suspended graphene sheets.Nature, 2007, 446(7131): 60–63

[2] Novoselov K S, Geim A K, Morozov S V, . Electric field effect in atomically thin carbon films.Science, 2004, 306(5696): 666–669

[3] Kumar R, Sahoo S, Joanni E, . Recent progress in the synthesis of graphene and derived materials for next generation electrodes of high performance lithium ion batteries.Progress in Energy and Combustion Science, 2019, 75: 100786

[4] Peña-Bahamonde J, Nguyen H N, Fanourakis S K, . Recent advances in graphene-based biosensor technology with applications in life sciences.Journal of Nanobiotechnology, 2018, 16(1): 75

[5] Radsar T, Khalesi H, Ghods V . Graphene properties and applications in nanoelectronic.Optical and Quantum Electronics, 2021, 53(4): 178

[6] Reina G, González-Domínguez J M, Criado A, . Promises, facts and challenges for graphene in biomedical applications.Chemical Society Reviews, 2017, 46(15): 4400–4416

[7] Hernandez Y, Nicolosi V, Lotya M, . High-yield production of graphene by liquid-phase exfoliation of graphite.Nature Nanotechnology, 2008, 3(9): 563–568

[8] Parvez K, Wu Z S, Li R, . Exfoliation of graphite into graphene in aqueous solutions of inorganic salts.Journal of the American Chemical Society, 2014, 136(16): 6083–6091

[9] Kim K S, Zhao Y, Jang H, . Large-scale pattern growth of graphene films for stretchable transparent electrodes.Nature, 2009, 457(7230): 706–710

[10] Emtsev K V, Bostwick A, Horn K, . Towards wafer-size graphene layers by atmospheric pressure graphitization of silicon carbide.Nature Materials, 2009, 8(3): 203–207

[11] Cossutta M, McKechnie J, Pickering S J . A comparative LCA of different graphene production routes.Green Chemistry, 2017, 19(24): 5874–5884

[12] Compton O C, Nguyen S T . Graphene oxide, highly reduced graphene oxide, and graphene: versatile building blocks for carbon-based materials.Small, 2010, 6(6): 711–723

[13] Ray S C. Application and uses of graphene oxide and reduced graphene oxide. In: Ray S C, ed. Applications of Graphene and Graphene-Oxide based Nanomaterials. Oxford: William Andrew Publishing, 2015, 39–55

[14] Hummers W S, Offeman R E . Preparation of graphitic oxide.Journal of the American Chemical Society, 1958, 80(6): 1339

[15] Stankovich S, Dikin D A, Piner R D, . Synthesis of graphene-based nanosheets via chemical reduction of exfoliated graphite oxide.Carbon, 2007, 45(7): 1558–1565

[16] Chua C K, Pumera M . Chemical reduction of graphene oxide: a synthetic chemistry viewpoint.Chemical Society Reviews, 2014, 43(1): 291–312

[17] Agharkar M, Kochrekar S, Hidouri S, . Trends in green reduction of graphene oxides, issues and challenges: a review.Materials Research Bulletin, 2014, 59: 323–328

[18] Novoselov K S, Fal’ko V I, Colombo L, . A roadmap for graphene.Nature, 2012, 490(7419): 192–200

[19] Agarwal V, Zetterlund P B . Strategies for reduction of graphene oxide ― a comprehensive review.Chemical Engineering Journal, 2021, 405: 127018

[20] Lehner B A E, Janssen V A E C, Spiesz E M, . Creation of conductive graphene materials by bacterial reduction using Shewanella Oneidensis.ChemistryOpen, 2019, 8(7): 888–895

[21] Salas E C, Sun Z, Lüttge A, . Reduction of graphene oxide via bacterial respiration.ACS Nano, 2010, 4(8): 4852–4856

[22] Wang G, Qian F, Saltikov C W, . Microbial reduction of graphene oxide by Shewanella.Nano Research, 2011, 4(6): 563–570

[23] Shen L, Jin Z, Wang D, . Enhance wastewater biological treatment through the bacteria induced graphene oxide hydrogel.Chemosphere, 2018, 190: 201–210

[24] Song T S, Tan W M, Xie J . Bio-reduction of graphene oxide using sulfate-reducing bacteria and its implication on anti-biocorrosion.Journal of Nanoscience and Nanotechnology, 2018, 18(8): 5770–5776

[25] Guo P, Xiao F, Liu Q, . One-pot microbial method to synthesize dual-doped graphene and its use as high-performance electrocatalyst.Scientific Reports, 2013, 3(1): 3499

[26] Yan J, Ye W, Jian Z, . Enhanced sulfate and metal removal by reduced graphene oxide self-assembled Enterococcus avium sulfate-reducing bacteria particles.Bioresource Technology, 2018, 266: 447–453

[27] Kalathil S, Katuri K P, Alazmi A S, . Bioinspired synthesis of reduced graphene oxide-wrapped Geobacter sulfurreducens as a hybrid electrocatalyst for efficient oxygen evolution reaction.Chemistry of Materials, 2019, 31(10): 3686–3693

[28] Lu Y, Zhong L, Tang L, . Extracellular electron transfer leading to the biological mediated production of reduced graphene oxide.Chemosphere, 2020, 256: 127141

[29] Akhavan O, Ghaderi E . Escherichia coli bacteria reduce graphene oxide to bactericidal graphene in a self-limiting manner.Carbon, 2012, 50(5): 1853–1860

[30] Zhao H, Zhang C, Wang Y, . Self-damaging aerobic reduction of graphene oxide by Escherichia coli: role of GO-mediated extracellular superoxide formation.Environmental Science & Technology, 2018, 52(21): 12783–12791

[31] Gurunathan S, Han J W, Eppakayala V, . Microbial reduction of graphene oxide by Escherichia coli: a green chemistry approach.Colloids and Surfaces B: Biointerfaces, 2013, 102: 772–777

[32] Gurunathan S, Han J W, Eppakayala V, . An environmentally friendly approach to the reduction of graphene oxide by Escherichia fergusoni.Journal of Nanoscience and Nanotechnology, 2013, 13(3): 2091–2098

[33] Vargas C, Simarro R, Reina J A, . New approach for biological synthesis of reduced graphene oxide.Biochemical Engineering Journal, 2019, 151: 107331

[34] Chouhan R S, Pandey A, Qureshi A, . Nanomaterial resistant microorganism mediated reduction of graphene oxide.Colloids and Surfaces B: Biointerfaces, 2016, 146: 39–46

[35] Boutchich M, Jaffré A, Alamarguy D, . Characterization of graphene oxide reduced through chemical and biological processes.Journal of Physics: Conference Series, 2013, 433: 012001

[36] Utkan G, Ozturk T, Duygulu O, . Microbial reduction of graphene oxide by‎ Lactobacillus plantarum.International Journal of Nanoscience and Nanotechnology, 2019, 15(2): 127–136

[37] Fan M, Zhu C, Feng Z Q, . Preparation of N-doped graphene by reduction of graphene oxide with mixed microbial system and its haemocompatibility.Nanoscale, 2014, 6(9): 4882–4888

[38] Chen Y, Niu Y, Tian T, . Microbial reduction of graphene oxide by Azotobacter chroococcum.Chemical Physics Letters, 2017, 677: 143–147

[39] Akhavan O . Bacteriorhodopsin as a superior substitute for hydrazine in chemical reduction of single-layer graphene oxide sheets.Carbon, 2015, 81: 158–166

[40] Jiao Y, Qian F, Li Y, . Deciphering the electron transport pathway for graphene oxide reduction by Shewanella oneidensis MR-1.Journal of Bacteriology, 2011, 193(14): 3662–3665

[41] Liu T, Jiang L L, He M F, . Green synthesis of reduced graphene oxide by a GRAS strain Bacillus subtilis 168 with high biocompatibility to zebrafish embryos.RSC Advances, 2015, 5(74): 60024–60032

[42] Khanra P, Kuila T, Kim N H, . Simultaneous bio-functionalization and reduction of graphene oxide by baker’s yeast.Chemical Engineering Journal, 2012, 183: 526–533

[43] Nandgaonkar A G, Wang Q, Fu K, . A one-pot biosynthesis of reduced graphene oxide (RGO)/bacterial cellulose (BC) nanocomposites.Green Chemistry, 2014, 16(6): 3195–3201

[44] Choudhary P, Das S K . Bio-reduced graphene oxide as a nanoscale antimicrobial coating for medical devices.ACS Omega, 2019, 4(1): 387–397

[45] Muthoosamy K, Bai R G, Abubakar I B, . Exceedingly biocompatible and thin-layered reduced graphene oxide nanosheets using an eco-friendly mushroom extract strategy.International Journal of Nanomedicine, 2015, 10: 1505–1519

[46] Gurunathan S, Han J, Park J H, . An in vitro evaluation of graphene oxide reduced by Ganoderma spp.in human breast cancer cells (MDA-MB-231). International Journal of Nanomedicine, 2014, 9: 1783–1797

[47] Ahmad S, Ahmad A, Khan S, . Algal extracts based biogenic synthesis of reduced graphene oxides (rGO) with enhanced heavy metals adsorption capability.Journal of Industrial and Engineering Chemistry, 2019, 72: 117–124

[48] Han M, Xu B, Zhang M, . Preparation of biologically reduced graphene oxide-based aerogel and its application in dye adsorption.Science of the Total Environment, 2021, 783: 147028

[49] Xu B, Cheng S, Han M, . The characteristic and performance of reduced graphene oxide by marine bacterium Pseudoalteromonas sp.CF10-13. Ceramics International, 2020, 46(13): 21699–21706

[50] Wang W, Mi J L, Shen Q C, . Shewanella oneidensis assisted biosynthesis of Pd/reductive-graphene-oxide nanocomposites for oxygen reduction reaction.ChemistrySelect, 2020, 5(11): 3179–3186

[51] Raveendran S, Chauhan N, Nakajima Y, . Ecofriendly route for the synthesis of highly conductive graphene using extremophiles for green electronics and bioscience.Particle & Particle Systems Characterization, 2013, 30(7): 573–578

[52] Gurunathan S, Han J W, Eppakayala V, . Biocompatibility of microbially reduced graphene oxide in primary mouse embryonic fibroblast cells.Colloids and Surfaces B: Biointerfaces, 2013, 105: 58–66

[53] Gurunathan S, Han J W, Eppakayala V, . Green synthesis of graphene and its cytotoxic effects in human breast cancer cells.International Journal of Nanomedicine, 2013, 8(1): 1015–1027

[54] Rathinam N K, Berchmans S, Sani R K, . Rewiring the microbe–electrode interfaces with biologically reduced graphene oxide for improved bioelectrocatalysis.Bioresource Technology, 2018, 256: 195–200

[55] Gao W. Chapter 3: The chemistry of graphene oxide. In: Gao W, ed. Graphene Oxide: Reduction Recipes, Spectroscopy, and Applications. Switzerland: Springer, 2015, 61–95

[56] Tanizawa Y, Okamoto Y, Tsuzuki K, . Microorganism mediated synthesis of reduced graphene oxide films.Journal of Physics: Conference Series, 2012, 352: 012011

[57] Khanna P, Kaur A, Goyal D . Algae-based metallic nanoparticles: synthesis, characterization and applications.Journal of Microbiological Methods, 2019, 163: 105656

[58] Liu S, Wang L, Tian J, . Aniline as a dispersing and stabilizing agent for reduced graphene oxide and its subsequent decoration with Ag nanoparticles for enzymeless hydrogen peroxide detection.Journal of Colloid and Interface Science, 2011, 363(2): 615–619

[59] Logan B E, Hamelers B, Rozendal R, . Microbial fuel cells: methodology and technology.Environmental Science & Technology, 2006, 40(17): 5181–5192

[60] Tay Z H Y, Ng F L, Ling T C, . The use of marine microalgae in microbial fuel cells, photosynthetic microbial fuel cells and biophotovoltaic platforms for bioelectricity generation.3 Biotech, 2022, 12(7): 148

[61] Gajda I, Greenman J, Melhuish C, . Self-sustainable electricity production from algae grown in a microbial fuel cell system.Biomass and Bioenergy, 2015, 82: 87–93

[62] Ng F L, Phang S M, Thong C H, . Integration of bioelectricity generation from algal biophotovoltaic (BPV) devices with remediation of palm oil mill effluent (POME) as substrate for algal growth.Environmental Technology & Innovation, 2021, 21: 101280

[63] Sonawane J M, Yadav A, Ghosh P C, . Recent advances in the development and utilization of modern anode materials for high performance microbial fuel cells.Biosensors & Bioelectronics, 2017, 90: 558–576

[64] Wey L T, Bombelli P, Chen X, . The development of biophotovoltaic systems for power generation and biological analysis.ChemElectroChem, 2019, 6(21): 5375–5386

[65] Li S, Cheng C, Thomas A . Carbon-based microbial-fuel-cell electrodes: from conductive supports to active catalysts.Advanced Materials, 2017, 29(8): 1602547

[66] Periasamy V, Jaafar M M, Chandrasekaran K, . Langmuir–Blodgett graphene-based films for algal biophotovoltaic fuel cells.Nanomaterials, 2022, 12(5): 840

[67] Habte A T, Ayele D W . Synthesis and characterization of reduced graphene oxide (rGO) started from graphene oxide (GO) using the tour method with different parameters.Advances in Materials Science and Engineering, 2019, 2019: 5058163

[68] Yuan Y, Zhou S, Zhao B, . Microbially-reduced graphene scaffolds to facilitate extracellular electron transfer in microbial fuel cells.Bioresource Technology, 2012, 116: 453–458

[69] Zhu W H, Gao H X, Li P, . The interaction between microbes and electrodes decorated with bio-reduced graphene oxide — from an electrochemical point of view.Journal of Chemical Technology and Biotechnology, 2021, 96(1): 172–179

[70] Goto Y, Yoshida N, Umeyama Y, . Enhancement of electricity production by graphene oxide in soil microbial fuel cells and plant microbial fuel cells.Frontiers in Bioengineering and Biotechnology, 2015, 3(42): 42

[71] Paul D, Noori M T, Rajesh P P, . Modification of carbon felt anode with graphene oxide–zeolite composite for enhancing the performance of microbial fuel cell.Sustainable Energy Technologies and Assessments, 2018, 26: 77–82

[72] Ng F L, Jaafar M M, Phang S M, . Reduced graphene oxide anodes for potential application in algae biophotovoltaic platforms.Scientific Reports, 2014, 4(1): 7562

[73] Zhuang L, Yuan Y, Yang G, . In situ formation of graphene/biofilm composites for enhanced oxygen reduction in biocathode microbial fuel cells.Electrochemistry Communications, 2012, 21: 69–72

[74] Chen J, Hu Y, Huang W, . Enhanced electricity generation for biocathode microbial fuel cell by in situ microbial-induced reduction of graphene oxide and polarity reversion.International Journal of Hydrogen Energy, 2017, 42(17): 12574–12582

[75] Chen J, Hu Y, Tan X, . Enhanced performance of microbial fuel cell with in situ preparing dual graphene modified bioelectrode.Bioresource Technology, 2017, 241: 735–742

[76] Song T S, Jin Y, Bao J, . Graphene/biofilm composites for enhancement of hexavalent chromium reduction and electricity production in a biocathode microbial fuel cell.Journal of Hazardous Materials, 2016, 317: 73–80

[77] Yoshida N, Miyata Y, Doi K, . Graphene oxide-dependent growth and self-aggregation into a hydrogel complex of exoelectrogenic bacteria.Scientific Reports, 2016, 6(1): 21867

[78] Yoshida N, Goto Y, Miyata Y . Selective growth of and electricity production by marine exoelectrogenic bacteria in self-aggregated hydrogel of microbially reduced graphene oxide.C ― Journal of Carbon Research, 2016, 2(2): 15

[79] Yoshida N, Miyata Y, Mugita A, . Electricity recovery from municipal sewage wastewater using a hydrogel complex composed of microbially reduced graphene oxide and sludge.Materials, 2016, 9(9): 742

[80] Goto Y, Yoshida N . Microbially reduced graphene oxide shows efficient electricity ecovery from artificial dialysis wastewater.The Journal of General and Applied Microbiology, 2017, 63(3): 165–171

[81] Ng F L, Phang S M, Periasamy V, . Algal biophotovoltaic (BPV) device for generation of bioelectricity using Synechococcus elongatus (Cyanophyta).Journal of Applied Phycology, 2018, 30(6): 2981–2988

[82] Yong Y C, Yu Y Y, Zhang X, . Highly active bidirectional electron transfer by a self-assembled electroactive reduced-graphene-oxide-hybridized biofilm.Angewandte Chemie International Edition in English, 2014, 53(17): 4480–4483

[83] Huang L, Regan J M, Quan X . Electron transfer mechanisms, new applications, and performance of biocathode microbial fuel cells.Bioresource Technology, 2011, 102(1): 316–323

[84] Chen J, Hu Y, Huang W, . Biodegradation of oxytetracycline and electricity generation in microbial fuel cell with in situ dual graphene modified bioelectrode.Bioresource Technology, 2018, 270: 482–488

[85] Gnana kumar G, Awan Z, Suk Nahm K, . Nanotubular MnO₂/graphene oxide composites for the application of open air-breathing cathode microbial fuel cells.Biosensors and Bioelectronics, 2014, 53: 528–534

[86] Yu J, Huang H, Bian F, . Supercritical CO₂-fluid-assisted synthesis of TiO₂ quantum dots/reduced graphene oxide composites for outstanding sodium storage capability.ACS Applied Energy Materials, 2018, 1(12): 7213–7219

[87] Yu J, Huang H, Gan Y, . A new strategy for the construction of 3D TiO₂ nanowires/reduced graphene oxide for high-performance lithium/sodium batteries.Journal of Materials Chemistry A: Materials for Energy and Sustainability, 2018, 6(47): 24256–24266

[88] Zhong Y, Xia X, Deng S, . Popcorn inspired porous macrocellular carbon: rapid puffing fabrication from rice and its applications in lithium–sulfur batteries.Advanced Energy Materials, 2018, 8(1): 1701110

[89] Zhu W, Huang H, Gan Y, . Mesoporous cobalt monoxide nanorods grown on reduced graphene oxide nanosheets with high lithium storage performance.Electrochimica Acta, 2014, 138: 376–382

[90] Kumar R, Singh R K, Vaz A R, . Self-assembled and one-step synthesis of interconnected 3D network of Fe₃O₄/reduced graphene oxide nanosheets hybrid for high-performance supercapacitor electrode.ACS Applied Materials & Interfaces, 2017, 9(10): 8880–8890

[91] Bian F, Yu J, Song W, . A new magnesium hydride route to synthesize morphology-controlled Si/rGO nanocomposite towards high-performance lithium storage.Electrochimica Acta, 2020, 330: 135248

Disclosure of potential conflicts of interest

There is no conflict of interest.

Acknowledgements

This work was supported by the Ministry of Higher Education Malaysia via Fundamental Research Grant Scheme (FRGS) [FRGS/1/2022/STG01/UM/03/2][FP064-2022], Ministry of Higher Education Malaysia under the Higher Institution Centre of Excellence (HICoE) Programme [IOES-2014F], UM Innovate Fund [PPSI-2020-HICOE-03] and the Research University Grant, Universiti Malaya [RU003-2022].

RIGHTS & PERMISSIONS

2023 Higher Education Press