Algal biomass derived biochar anode for efficient extracellular electron uptake from Shewanella oneidensis MR-1

Highlights

Algal biochar anode produced higher biocurrent compared with graphite plate anode.

Algal biochar exhibited stronger electrochemical response to redox mediators.

Algal biochar showed excellent adsorption to redox mediators.

Abstract

The development of cost-effective and highly efficient anode materials for extracellular electron uptake is important to improve the electricity generation of bioelectrochemical systems. An effective approach to mitigate harmful algal bloom (HAB) is mechanical harvesting of algal biomass, thus subsequent processing for the collected algal biomass is desired. In this study, a low-cost biochar derived from algal biomass via pyrolysis was utilized as an anode material for efficient electron uptake. Electrochemical properties of the algal biochar and graphite plate electrodes were characterized in a bioelectrochemical system (BES). Compared with graphite plate electrode, the algal biochar electrode could effectively utilize both indirect and direct electron transfer pathways for current production, and showed stronger electrochemical response and better adsorption of redox mediators. The maximum current density of algal biochar anode was about 4.1 times higher than graphite plate anode in BES. This work provides an application potential for collected HAB to develop a cost-effective anode material for efficient extracellular electron uptake in BES and to achieve waste resource utilization.

Graphical abstract

Keywords

Algal biochar / Anode material / Electrochemical activity / Extracellular electron transport / Waste resource utilization

References

[1] Alshehri A N Z (2017). Formation of electrically conductive bacterial nanowires by Desulfuromonas acetoxidans in microbial fuel cell reactor. International Journal of Current Microbiology and Applied Sciences, 6(8): 1197–1211

[2] Avila A, Gregory B W, Niki K, Cotton T M (2000). An electrochemical approach to investigate gated electron transfer using a physiological model system: Cytochrome c immobilized on carboxylic acid-terminated alkanethiol self-assembled monolayers on gold electrodes. Journal of Physical Chemistry B, 104(12): 2759–2766

[3] Bertaux J, Froehlich F, Ildefonse P (1998). Multicomponent analysis of FTIR spectra: Quantification of amorphous and crystallized mineral phases in synthetic and natural sediments. Journal of Sedimentary Research, 68(3): 440–447

[4] Bian B, Shi D, Cai X B, Hu M J, Guo Q Q, Zhang C H, Wang Q, Sun A X L, Yang J (2018). 3D printed porous carbon anode for enhanced power generation in microbial fuel cell. Nano Energy, 44: 174–180

[5] Chan K Y, Van Zwieten L, Meszaros I, Downie A, Joseph S (2008). Agronomic values of greenwaste biochar as a soil amendment. Soil Research (Collingwood, Vic.), 45(8): 629–634

[6] Chen Q, Pu W, Hou H, Hu J, Liu B, Li J, Cheng K, Huang L, Yuan X, Yang C, Yang J (2018a). Activated microporous-mesoporous carbon derived from chestnut shell as a sustainable anode material for high performance microbial fuel cells. Bioresource Technology, 249: 567–573

[7] Chen S, Rotaru A E, Shrestha P M, Malvankar N S, Liu F, Fan W, Nevin K P, Lovley D R (2014). Promoting interspecies electron transfer with biochar. Scientific Reports, 4: 5019

[8] Chen W W, Liu Z L, Hou J X, Zhou Y, Lou X G, Li Y X (2018b). Enhancing performance of microbial fuel cells by using novel double-layer-capacitor-materials modified anodes. International Journal of Hydrogen Energy, 43(3): 1816–1823

[9] Creamer A E, Gao B, Zhang M (2014). Carbon dioxide capture using biochar produced from sugarcane bagasse and hickory wood. Chemical Engineering Journal, 249: 174–179

[10] El Kasmi A, Wallace J M, Bowden E F, Binet S M, Linderman R J (1998). Controlling interfacial electron-transfer kinetics of cytochrome c with mixed self-assembled monolayers. Journal of the American Chemical Society, 120(1): 225–226

[11] Fan Y, Xu S, Schaller R, Jiao J, Chaplen F, Liu H (2011). Nanoparticle decorated anodes for enhanced current generation in microbial electrochemical cells. Biosensors & Bioelectronics, 26(5): 1908–1912

[12] Ferrari A C, Robertson J (2000). Interpretation of Raman spectra of disordered and amorphous carbon. Physical Review B: Condensed Matter and Materials Physics, 61(20): 14095–14107

[13] Guo L (2007). Doing battle with the green monster of Taihu Lake. Science, 317(5842): 1166

[14] Kashyap D, Dwivedi P K, Pandey J K, Kim Y H, Kim G M, Sharma A, Goel S (2014). Application of electrochemical impedance spectroscopy in bio-fuel cell characterization: A review. International Journal of Hydrogen Energy, 39(35): 20159–20170

[15] Kim J R, Min B, Logan B E (2005). Evaluation of procedures to acclimate a microbial fuel cell for electricity production. Applied Microbiology and Biotechnology, 68(1): 23–30

[16] Koposova E, Liu X, Kisner A, Ermolenko Y, Shumilova G, Offenhäusser A, Mourzina Y (2014). Bioelectrochemical systems with oleylamine-stabilized gold nanostructures and horseradish peroxidase for hydrogen peroxide sensor. Biosensors & Bioelectronics, 57: 54–58

[17] Kotloski N J, Gralnick J A (2013). Flavin electron shuttles dominate extracellular electron transfer by Shewanella oneidensis. mBio, 4(1): e00553–12PMID:23322638

[18] Li S W, Zeng R J, Sheng G P (2017). An excellent anaerobic respiration mode for chitin degradation by Shewanella oneidensis MR-1 in microbial fuel cells. Biochemical Engineering Journal, 118: 20–24

[19] Liu H, Matsuda S, Kato S, Hashimoto K, Nakanishi S (2010). Redox-responsive switching in bacterial respiratory pathways involving extracellular electron transfer. ChemSusChem, 3(11): 1253–1256

[20] Liu N, Sun Z T, Wu Z C, Zhan X M, Zhang K, Zhao E F, Han X R (2013). Adsorption characteristics of ammonium nitrogen by biochar from diverse origins in water. Advanced Materials Research, 664: 305–312

[21] Luo C H, Lü F, Shao L M, He P J (2015). Application of eco-compatible biochar in anaerobic digestion to relieve acid stress and promote the selective colonization of functional microbes. Water Research, 68: 710–718

[22] Lv Q, Cao C B, Li C, Zhang J T, Zhu H X, Kong X, Duan X F (2003). Formation of crystalline carbon nitride powder by a mild solvothermal method. Journal of Materials Chemistry, 13(6): 1241–1243

[23] Ma X X, Feng C H, Zhou W J, Yu H (2016). Municipal sludge-derived carbon anode with nitrogen-and oxygen-containing functional groups for high-performance microbial fuel cells. Journal of Power Sources, 307: 105–111

[24] MacKintosh C, Beattie K A, Klumpp S, Cohen P, Codd G A (1990). Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Letters, 264(2): 187–192

[25] Meng X, Savage P E, Deng D (2015). Trash to treasure: From harmful algal blooms to high-performance electrodes for sodium-ion batteries. Environmental Science & Technology, 49(20): 12543–12550

[26] Mohanakrishna G, Abu-Reesh I M, Al-Raoush R I, He Z (2018). Cylindrical graphite based microbial fuel cell for the treatment of industrial wastewaters and bioenergy generation. Bioresource Technology, 247: 753–758

[27] Okamoto A, Hashimoto K, Nealson K H, Nakamura R (2013). Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones. Proceedings of the National Academy of Sciences of the United States of America, 110(19): 7856–7861

[28] Roberts D A, Paul N A, Cole A J, de Nys R (2015). From waste water treatment to land management: Conversion of aquatic biomass to biochar for soil amelioration and the fortification of crops with essential trace elements. Journal of Environmental Management, 157: 60–68

[29] Sacco N J, Bonetto M C, Cortón E (2017). Isolation and characterization of a novel electrogenic bacterium, Dietzia sp. RNV-4. PLoS One, 12(2): e0169955

[30] Su Y, Li L, Hou J, Wu N, Lin W, Li G (2016). Life-cycle exposure to microcystin-LR interferes with the reproductive endocrine system of male zebrafish. Aquatic Toxicology (Amsterdam, Netherlands), 175: 205–212

[31] Suguihiro T M, de Oliveira P R, de Rezende E I P, Mangrich A S, Marcolino Junior L H, Bergamini M F (2013). An electroanalytical approach for evaluation of biochar adsorption characteristics and its application for lead and cadmium determination. Bioresource Technology, 143: 40–45

[32] Tan I A W, Ahmad A L, Hameed B H (2008). Adsorption of basic dye on high-surface-area activated carbon prepared from coconut husk: equilibrium, kinetic and thermodynamic studies. Journal of Hazardous Materials, 154(1–3): 337–346

[33] ter Heijne A, Hamelers H V M, Saakes M, Buisman C J N (2008). Performance of non-porous graphite and titanium-based anodes in microbial fuel cells. Electrochimica Acta, 53(18): 5697–5703

[34] Wang Q Q, Wu X Y, Yu Y Y, Sun D Z, Jia H H, Yong Y C (2017). Facile in-situ fabrication of graphene/riboflavin electrode for microbial fuel cells. Electrochimica Acta, 232: 439–444

[35] Wu S, Fang G, Wang Y, Zheng Y, Wang C, Zhao F, Jaisi D P, Zhou D (2017). Redox-active oxygen-containing functional groups in activated carbon facilitate microbial reduction of ferrihydrite. Environmental Science & Technology, 51(17): 9709–9717

[36] Xiao Y, Zheng Y, Wu S, Yang Z H, Zhao F (2016). Nitrogen recovery from wastewater using microbial fuel cells. Frontiers of Environmental Science & Engineering, 10(1): 185–191

[37] Xing D, Cheng S, Logan B E, Regan J M (2010). Isolation of the exoelectrogenic denitrifying bacterium Comamonas denitrificans based on dilution to extinction. Applied Microbiology and Biotechnology, 85(5): 1575–1587

[38] Xiong L, Chen J J, Huang Y X, Li W W, Xie J F, Yu H Q (2015). An oxygen reduction catalyst derived from a robust Pd-reducing bacterium. Nano Energy, 12: 33–42

[39] Zhang F, Yuan S J, Li W W, Chen J J, Ko C C, Yu H Q (2015). WO₃ nanorods-modified carbon electrode for sustained electron uptake from Shewanella oneidensis MR-1 with suppressed biofilm formation. Electrochimica Acta, 152: 1–5

[40] Zhang F, Yu S S, Li J, Li W W, Yu H Q (2016). Mechanisms behind the accelerated extracellular electron transfer in Geobacter sulfurreducens DL-1 by modifying gold electrode with self-assembled monolayers. Frontiers of Environmental Science & Engineering, 10(3): 531–538

[41] Zhang Y, Angelidaki I (2014). Microbial electrolysis cells turning to be versatile technology: Recent advances and future challenges. Water Research, 56: 11–25

[42] Zhang Y Z, Mo G Q, Li X W, Zhang W D, Zhang J Q, Ye J S, Huang X D, Yu C Z (2011). A graphene modified anode to improve the performance of microbial fuel cells. Journal of Power Sources, 196(13): 5402–5407

[43] Zheng H, Guo W, Li S, Chen Y, Wu Q, Feng X, Yin R, Ho S H, Ren N, Chang J S (2017). Adsorption of p-nitrophenols (PNP) on microalgal biochar: Analysis of high adsorption capacity and mechanism. Bioresource Technology, 244(Pt 2): 1456–1464

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Nos. 21477121 and 51538012) and the Fundamental Research Funds for the Central Universities.

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