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Self-sustained photocatalytic power generation using eco-electrogenic engineered systems
Accepted Manuscript Self-Sustained Photocatalytic Power Generation using Eco-Electrogenic Engineered Systems Dileep Kumar Yeruva, P. Chiranjeevi, Sai Kishore Butti, S. Venkata Mohan PII: DOI: Reference:
S0960-8524(18)30411-5 https://doi.org/10.1016/j.biortech.2018.03.063 BITE 19702
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Bioresource Technology
Received Date: Revised Date: Accepted Date:
27 November 2017 8 March 2018 9 March 2018
Please cite this article as: Yeruva, D.K., Chiranjeevi, P., Butti, S.K., Mohan, S.V., Self-Sustained Photocatalytic Power Generation using Eco-Electrogenic Engineered Systems, Bioresource Technology (2018), doi: https:// doi.org/10.1016/j.biortech.2018.03.063
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Self-Sustained Photocatalytic Power Generation using Eco-Electrogenic Engineered Systems Dileep Kumar Yeruva1,2, P.Chiranjeevi1,2, Sai Kishore Butti1,2, S.Venkata Mohan1* 1
Bioengineering and Environmental Sciences Lab, EEFF Centre, CSIR-Indian Institute of Chemical Technology (CSIR-IICT), Hyderabad- 500 007, India. 2 Academy of Scientific and Innovative Research (AcSIR), Hyderabad, India. *E-mail: [email protected]; [email protected]; Tel: +9140-27191765
Abstract An eco-electrogenic engineered system (EES) was designed to mimic the functional role of natural aquatic ecosystems and evaluated their response to bio-electrogenic activity by cascadically interlinking three tanks with functionally diverse biota viz., floating macrophytes (Tank 1), submerged plants (Tank 2) and filter feeders (fish and snails) (Tank 3). Tank-1 showed efficient power generation (voltage (series): 0.86 V; current density (parallel): 37 mA/m2) than Tank-2 (voltage (series): 0.76 V; current density (Parallel): 34 mA/m2) and Tank-3 (voltage (series):0.65 V; current density (parallel): 22 mA/m2). Integrating all three tanks enabled maximum power generation in parallel-series (P-S) connection (9.5 mW/m2) than individual series and parallel connections (6.5/5 mW/m2). Interaction of microbes and plant studied at the interface of electrochemical and engineering aspects illustrated the feasibility of EES as a selfsustainable system with innate diverse functional aquatic biota and rhizo-microbiome to produce bioelectricity. Keywords: Aquatic Macrophytes; Bioelectricity; Water Ecosystem; Electric Circuit. 1. Introduction Ecological water bodies are inhabited by numerous aquatic living forms functioning symbiotically to balance the ecological status of aquatic ecosystem and fulfilling their characteristic roles (Baron et al., 2003; Aoki, 2006; Venkata Mohan et al., 2010). The congregations of diversified biota ranging from exo-electrogenic bacteria to CO2 assimilating phototrophic macrophytes make the ecological water bodies a natural source to harness energy (Venkata Mohan et al., 2009). The core sustenance of ecological water bodies depends on primary phototrophic producers which are phytoplankton and hydrophytes (Pennak, 1971; Wiley et al., 1984). The ecosystem balance is dependent on both abiotic factors including light, temperature, nutrients, and sediment composition and biotic factors which includes mainly the plant-microbial interactions (rhizosphere) to sustain the nutrient cycles (Bond et al., 2002). Plants actively recruit and sustain microorganisms in the rhizosphere by translocation of organic compounds from leaves to the roots that serves as growth substrate for rhizospheric microbes by the translocation of organic compounds from the leaves to the roots and into the rhizosphere that serves as growth substrates (Nitisoravut and Regmi, 2017). Rhizosphere bacterial community is dependent on root exudates which serve as a wide range of complex organic compounds ranging from border cells and root debris i.e., soluble and insoluble organic compounds. However, exudation of low weight molecules (organic acids, amino acids, and sugars) is a continuous process that is driven by passive diffusion and migration (Deng et al., 2012; Timmer et al., 2011). Root exudates which are produced during the photosynthetic process are uptaken by root 1
sediment microbes via microbial mineralization processes, which further restore nutrients (for aquatic plants) (Barko et al., 1986; Violante et al., 2010; Venkata Mohan et al., 2011; Chiranjeevi et al., 2013). Sediment microbes have a specific role in nutrient regeneration by releasing inorganic forms of carbon, nitrogen, phosphorus, and sulfur which serve as macro or micronutrients to aquatic plants and microorganisms (Colombo et al., 2017; Naiman and Turner, 2000). Plant-microbe symbiotic relationship and the nutrient cycle of microbial community in the rhizosphere is influenced by the variation of adaptation process due to diverse physiological and environmental stress according to geographical locations (Durako and Moffler, 1987; Venkata Mohan et al., 2009). Interactions among the biotic component along with nutrients and organic matter stored in the sediment sub-surface of aquatic ecosystems as an integral part stores a large and potential source of energy (He et al., 2007; Rezaei et al., 2007; Venkata Mohan et al., 2009). The anaerobicity of the sediments and the organic rhizodeposits enrich specific rhizosphere microorganisms that are well adapted to utilization of specific compounds (Reimers et al., 2001) Rhizobial microflora exhibited signaling mechanism between plants and microbes present in the sediment (Duineveld et al., 2001). Among them, some of the rhizodeposits are oxidized by electrochemically active bacteria (EAB) specific for plant species (Venkata Mohan et al.,2009; Chiranjeevi et al., 2012; Rosenbaum and Angenent, 2010; Strik et al., 2008). The possibility of utilizing these EAB for energy generation in the natural ecological water bodies has been evaluated by incorporating an electrode setup into the sediment acting as anode and air exposed electrode as cathode (Venkata Mohan et al., 2011; Babu and Venkata Mohan, 2012). The electrogenic capability of aquatic plants and associated rhizomicrobiome was not explored earlier for the production of electricity. The fundamental mechanism that will be employed for power generation in natural aquatic bodies is the photosynthetic activity that results in production of organic compounds through utilization of solar energy. These organic compounds serve as substrate for microbiome which further generates bioelectricity in the presence of a fuel cell setup, functioning in a self-sustainable mode without the addition of any external carbon source. Considering the advantage of natural ecosystems and microbial fuel cell for power generation, study is designed to focus on self -sustainability of aquatic environment for the production of electricity from aquatic plants by converting light energy to electrical energy by the photosynthetic process. An attempt was made in this study to assess the hidden potential of natural water bodies for self-sustained power production using embedded fuel cell assemblies. Natural lake ecosystems were simulated in aquatic tanks (150 l capacity) which were designed and fabricated as eco-electrogenic engineered systems (EES) containing different types of plants species related to floating, submerged and emergent hydrophytes placed in a defined sequence. The systems were operated in self-sustained mode without the addition of external carbon or nutrients, and the carbon source was obtained from the atmospheric CO2 for the plants and root excretes for the microbial community. 2. Experimental methodology 2.1. EES An eco-electrogenic engineered system (EES) was designed with three rectangular tanks having dimensions 55 X 30 X 30 cm length, width and height. Each tank was fabricated using perplex sheets with total/ working volume of 50/35 L with a free board of 5 cm. The rectangular design provides an advantage of effective space utility and ease of operation with an even distribution of the water flow. The three tank EES was placed on a customized stand with natural height 2
gradient of 15 cm allowing the flow with gravity, the feed tank/water source is kept at the highest point followed by the series of other tanks with specific plant types. The tanks were labeled from the top to bottom as Tank 1, Tank 2 and Tank 3 respectively. The tanks were provided with baffles to prevent cross discharge by reducing solids discharge and also to equalize the flow. Vents were provided at a distance of 5 cm from the top of the tank, these were used to hydrological connection each tank. The system was operated in continuous mode with a constant flow rate of 2 l/h. Bottom of Tank 1 and Tank 2 was filled with sediment obtained from Nacharam lake up to a height of 5 cm and the Tank 3 was filled with fine sand. 2.2. Operation Contents of tanks were designed to simulate the natural condition in water bodies with variations based on different hydroponic macrophytes in each tank. Tank1 was designed to contain freefloating macrophytes having plants like Eichhornia crassipes (water hyacinth) which is vascular and has rapid growth. It covers the water surface of the tank and helps to maintain anoxic microenvironment in Tank1. Moreover, Eichhornia crassipes develops a fibrous root system which is favorable for the growth of different microbial communities in the rhizosphere. Tank2 contains slender, submerged, perennial aquatic herbs like Hydrilla verticillata, which helps in maintaining aerobic condition in the tank by respiring underwater. The growth of these plants is rapid and they contain a tuberous root system anchored in the sediment. Tank3 was designed for filter-feeding action with fish and snails along with Pistiastratiotes, which enables final water polishing by the filter-feeding action of snails and fish and consume the bacteria and planktons. 2.3. Fuel Cell Assembly Each tank was embedded with 4 electrode assembly setups (without membrane). Non-catalyzed graphite electrodes with a surface area of 0.105 m2 were used as cathode and anode. Anodes were placed on the sediment at the depth of 1 cm and cathodes were placed on the sub-surface of water, where the upper portion of the electrode was exposed to air and bottom surface was in contact with the water. The inter-electrode distance was 20 cm. The circuit connections to electrodes were made with copper wire sealed by epoxy sealant. The stacked electrode setups were placed in each tank with the support of inert non-conductive material suspended from the top. The power output was analyzed with electrodes connections in different circuitries. The electrical circuitries were evaluated in three variations, the first setup was with series operation were anode was connected to the subsequent cathode, the second was a parallel setup were all the anodes are connected and all the cathodes are connected and the third setup was a combination of series and parallel operation were electrodes in each tank were connected in parallel and the tanks were connected in series. The bio-electrochemical data was obtained in open circuit mode by connecting the free terminal electrodes. 2.4. Bioelectrogenic Analysis Bioelectrogenic profiles based on open circuit voltage (OCV) and current (I; with 100 Ω resistance) were recorded using a digital multi-meter. The bioelectrogenic measurements were recorded in three circuitry modes viz., series, parallel and parallel-series (P-S) connection in individual tanks. Polarization profiles were recorded by changing external (30-0.05 kΩ) resistances in each individual tank with three circuited modes. Power was derived from P=VI equation, power density (PD) (mW/m2) and current density (CD) (mA/m2) were calculated with the function of anodic surface area (m2). Cell potentials of anode and cathode were measured at various external resistances against saturated Ag/AgCl (S) as reference electrode. All the 3
electrogenic measurements were performed separately for each tank in all circuit mode of operations. Bio-electrochemical and redox behavior was studied for each individual tank employing a potentiostat-galvanostat system (Bio-logic, VMP3, France). A potential ramp from +1.0 to -1.0 V was applied at scan rates of 50, 30, 20, 10 and 1 mV/s to record the voltammograms. All the electrochemical assays were performed using anode as working electrode and cathode as a counter electrode against Ag/AgCl (3.5M KCl) as reference electrode. 3. Results and Discussion 3.1. Photo-eco-electrogenic activity vs circuitry mode Feasibility of self-sustained power generation with the symbiotic association of microbes and plant root metabolites was studied by introducing electrodes in the rhizosphere of all the three tanks. Bioelectrogenic activity was measured in three electrical circuit modes such as series, parallel and parallel-series (P-S) for electrically stacked tanks. EES showed power generation in the order with Tank 1 > Tank 2 > Tank 3 and open circuit voltages (OCV) were observed to be 0.8, 0.7 and 0.65 V, respectively in series connection. When these three systems were stacked together in series, maximum OCV output recorded was 2.2 V, which is cumulative of the three individual tanks (Fig 1). Maximum current density of stacked-series circuit was 4.15 mA/m2, and the corresponding current densities of individual tanks were recorded as 2.7 mA/m2 (Tank 1), 2.5 mA/m2 (Tank 2) and 2.4 mA/m2 (Tank 3) (Fig 2). EES showed consistent power production without any voltage reversal in series circuit, as each tank performance was stable in terms of electrogenic activity. The power production in parallel stacked EES operation was 0.6 V and the OCV of individual tanks were recorded as 0.65, 0.63 and 0.60 V respectively. Maximum current of the parallel stacked circuit was 103 mA/m2 and the corresponding current generation for each tank was recorded as 37 (Tank 1), 33 (Tank 2) and 20 mA/m2 (Tank 3) which was much higher than the performance of single tank in series connection. The power output obtained in series and parallel circuits was less as the series circuitry yields low current (cumulates only voltage) and parallel circuitry yields low voltage (cumulates only current). Therefore, a hybrid circuitry was developed and evaluated by interconnecting tanks partially in parallel and series (P-S) circuits. A circuit was arranged in such way that the individual tanks consisting of electrode setups were connected in parallel to obtain maximum current and the three parallel circuited tanks were stacked in series circuit to obtain the maximum power output and to cumulatively enhance the bioelectrogenesis of EES. P-S circuit yielded maximum voltage and current (1.6 V; 50 mA/m2) in stacked conditions (Fig 1) with corresponding individual tanks depicting maximum voltage and currents in Tank 1 (0.75 V; 37 mA/m2) followed by Tank 2 (0.6 V; 33 mA/m2) and Tank 3 (0.3 V; 22 mA/m2) (Fig 2). Figure 1 Rhizosphere a rich source of carbonaceous root exudates (carbohydrates, fatty acids, amino acids, hormones and other phenolic organic compounds) are synthesized by plants via converting solar (light) energy into chemical energy (Pierret et al., 2007; De Schamphelaire et al., 2008; Kaku et al., 2008; Chiranjeevi et al., 2012). The photosynthetic process depends on its capability to exploit everlasting reservoirs of sunlight, water, and carbon dioxide to transform photonic energy into chemical energy (Janssen et al. 2014). The hydrophytes, floating and rooted macrophytes play an important role in aquatic ecosystems as food providers that enable the maintenance of ecological diversity (Pennak, 1971; Wiley et al., 1984). In Tank 1, the floating plant Eichhornia facilitates an anoxic microenvironment by spreading on the water surface allowing low air exchange to the water. The conditions enrich mostly anaerobic and facultative 4
consortia which enable power generation by metabolizing the rhizo deposits. Sponge and marsh based root system of Eichhornia also helps in creating the suitable environment for the root associated bacterial communities which also increases the availability of organic matters (Chandra et al., 2017, 2018). Tank 2 facilitates aerobic microenvironment by means of submerged Hydrilla which has the capability of releasing O2 through their photosynthetic action. This evolved oxygen can facilitate aerobic conditions in cathode zone, which improves electric output (Shanthi Sravan et al., 2017). The observed power output relatively lower than Tank 1, might be attribited to the absence of heavy root system (lesser availability of root excreates) and the presence of dissolved oxygen that neutralizes the produced electrons. Apart from the carbon source, root exudates also stimulate chemotaxis to promote soil microbes to the rhizosphere (Nitisoravut and Regmi, 2017; Babu and Venkata Mohan, 2012). Figure 2 3.2. Polarization Profiles Internal resistance and electrochemical losses can be determined by the polarization profiles along with the cell design point which indicates the maximum operational load (Venkata Mohan et al., 2008). The polarization profiles were plotted as the voltage vs power density (PD) in response to varying external loads from 30 kΩ to 50 Ω on the system (Fig 3). The maximum power density (9 mW/m2) and a current density (28 mA/m2) were observed in Tank 1 with corresponding resistance (100 Ω) (Fig 4). In the stacked-series circuit, higher PD (5 mW/m2) with a maximum voltage of 1.9 V was obtained at an external resistance of 200 Ω. In parallel circuit mode, maximum PD was observed in individual tanks (Tank 1, 15 mW/m2) corresponding to CD (35 mA/m2). Subsequently, a stacked-parallel circuit obtained maximum PD of 6.8 mW/m2 with the corresponding CD (15 mA/m2). In the combinatory P-S circuits showed the maximum power density of 9.5 mW/m2 at resistance (100 Ω) and current density (18 mA/m2) which is comparatively higher than series and parallel circuits. The stacked circuit modes showed lower PD than individual tanks as the surface area of anodes cumulates lowering the charge present per unit area. Similar results were reported, were the increase in surface area of anode decreases the PD (Liu et al., 2013).The individual tanks showed ohmic and activation losses irrespective of circuit modes connections which are primarily due to the non-catalytic electrode material and the inter-electrode distance between anode and cathode. Figure 3 & 4 3.3. Cell Potentials Cell potential/EMF (E0) determines the performance of the fuel cell and is dependent on the anode (Ea) and cathode (Ec) potentials, which are also termed as half-cell potentials. These halfcell potentials were recorded at various external resistances against Ag/AgCl reference electrode (Fig 5). Stacked P-S circuit conditions showed higher Ea (-850 mV) than individually stacked series and parallel circuits and were also higher than the individual tanks. In the stacked-series circuit the maximum Ea of -295 mV was observed greater than the individual tanks. Ea profile in the stacked parallel circuit was observed to be more or less similar with a maximum of -118mV among each individual tank values. In all circuit conditions, Ea drops at lower resistance owing to its rapid electron discharge from the anode to the counter electrode in the circuit. Cathode potential (Ec) were observed to show the similar trends like anode potential (Ea) with the varying external resistance. The rate of drop in Ec of parallel connection was high compared to series and P-S circuit connection. The Ec of stacked series, parallel and P-S circuit connections were between 0.90 to 1.22, 0.335 to 0.001 and 0.487 to 0.002 V, respectively. The higher Ec can 5
be due to the innate capabilities of plant root system to evolve oxygen in allelectric configurations (Doherty et al., 2015). It indicates that the total cell potential and current generation were limited by both anode and cathode potentials with the function of varying external resistance. Figure 5 3.4. Bio-electrochemical behavior Cyclic voltammetry (CV) was employed to analyze the bio-electrochemical redox behavior. The voltammetric analysis was performed individually for each tank during the daytime with a scan rate of 1 mV/s in a range of -1.0 to 1.0 V. Voltammograms depicted variation in redox catalytic currents for each tank respectively (Fig 6).Tank 1 showed more reductive current-3.8 mA and 2.5 mA oxidative current. Tank 2 showed -4.2 mA and 1.5 mA reductive current and oxidative currents respectively. Tank 3 showed lower oxidation and reductive currents with 1 mA and -2.9 mA. Obtained voltammograms illustrated the difference in catalytic currents as well as the capacitance for each of the tank. Higher redox catalytic currents without any noticeable capacitance were observed with Tank1 with Eichhornia crassipes (water hyacinth). The fibrous root system of Eichhornia provides nesting habitat for much bacterial sp. prevalence of anaerobic conditions in the system might have contributed to low capacitance and high reductive currents. The root excretes flavonoids which might involve the electron carries and favors to develop the higher catalytic currents (as observed in voltammograms). The electrochemical profile of flavonoids, akin to their redox behavior is mainly driven by the stability of electrogenerated phenoxyl radicals which determines the overall electrode reactions (Gil and Couto, 2013). Figure 6 Following higher redox currents were noticed in the Tank 2 which might be due to the anoxic conditions prevailing due to the presence of Hydrilla verticilata. Oxygen generation by Hydrilla in the system may increase in capacitive current generation. While in the case of Tank 3, redox catalytic currents were comparatively less than tank 2. This might be due to the availability of organic matter/root exudates in less quantity (than at Tank 2). The variations observed at all the tanks were majorly due to the presence of root system and the efficiency of plant system to perform photosynthesis which was the only source to derive energy for the growth of plant systems. Cyclic voltammograms showed the activity of different redox mediators observed in the three tank systems (Fig 6). Tank 1 showed the redox peek at -345, +05, +105 mV, Tank 2 at -45,+155 mV and Tank 3 at -95, +155 mV with against Ag/AgCl (3.5 M KCl). The observed redox potentials correspond to NAD+/ NADH+H+, Ubiquinone OX/RED, FAD/FADH2 and cytochrome c activity. These redox compounds participate in the electron transport across the bacterial cell membrane. Comparatively the control system (without plant) showed high capacitive currents, this may be due to the effect of electrode distances. High reductive currents observed in the plant components represented bacterial activity with rhizoexudates metabolisms. Cyclic voltammograms were also performed at different scan rates from 1, 10, 20, 30 and 50 mV/s which illustrate the relationship between individual plants towards power production. 4. Conclusions Study illustrated the feasibility of harnessing power in EES system through symbiotic association of water ecosystems via photosynthetic machinery. Synergetic interaction was observed between 6
aquatic plant-microbes (rhizosphere) and sediment microbiome which converts light energy into electric energy by catalytic function of organic/inorganic (root excretes) compounds. The designed EES is a self-sustainable complex biome imitating the natural aquatic ecosystems which has operational feasibility and is inexpensive to harness light energy into electrical energy. Power generation attained through natural eco-systems depicts the self-sustenance towards real field applications. Acknowledgements The authors thank Director, CSIR-IICT for support and encouragement in carrying out this work. The authors would like to acknowledge Department of Biotechnology (DBT) for proving research grant (BT/PR18965/BCE/8/1401/2016). PC duly acknowledges CSIR for providing research fellowship. SKB duly acknowledges UGC for providing research fellowship. References 1. Aoki, I., 2006. Ecological pyramid of dissipation function and entropy production inaquatic ecosystems. Ecol. Complex. 3,104–108. 2. Babu, M.L., Venkata Mohan, S., 2012. Influence of graphite flake addition to sediment on electrogenesis in a sediment-type fuel cell. Bioresour. Technol. 110, 206-213 3. Barko, J.W., Adams, M.S., Clesceri, N.L., 1986. Environmental factors and their consideration in the management of submersed aquatic vegetation: A review. J Aquat Plant Manag. 24,1−10. 4. Bond, D.R., Holmes, D.E., Tender, L.M.,Lovley, D.R., 2002. Electrode-reducing microorganisms that harvest energy from marine sediments. Science. 295,483–485. 5. Chandra, R., Sravan, J.S., Hemalatha, M., Kishore Butti, S., 2017. Photosynthetic synergism for sustained power production with microalgae and photobacteria in a biophotovoltaic cell. Energy Fuels 31, 7635-7644 6. Chandra, R., Venkata Mohan, S., Roberto, P, S., Ritmann, B.E., Cornejo, R.A.S., (2018) Biophotovoltaics: Conversion of Light Energy to Bioelectricity Through Photosynthetic Microbial Fuel Cell Technology. Microbial Fuel Cell, Springer, 373-387 7. Chiranjeevi, P., Mohanakrishna, G., Venkata Mohan, S., 2012. Rhizosphere mediated electrogenesis with the function of anode placement for harnessing bioenergy through CO2 sequestration. Bioresour Technol. 124,364–370. 8. Chiranjeevi, P., Rashmi, C., Venkata Mohan,S., 2013. Ecologically engineered submerged and emergent macrophyte based system: An integrated eco-electrogenic design for harnessing power with simultaneous wastewater treatment,Ecological Engineering. 51,181– 190. 9. Colombo, A., Marzorati, S., Lucchini, G., Cristiani, P., Pant, D., Schievano, A., 2017. Assisting cultivation of photosynthetic microorganisms by microbial fuel cells to enhance nutrients recovery from wastewater. Bioresour Technol. 237,240-248. 10. De Schamphelaire, L., Bossche, L. V., Dang, H.S., Hofte, M., Boon, N., Rabaey, K.,Verstraete, W., 2008. Microbial fuel cells generating electricity from rhizodeposits of rice plants. Environ. Sci. Technol. 42,3053–3058. 11. Dakora, F.D., Phillips, D.A. 2002. Root exudates as mediators of mineral acquisition in lownutrient environments. Plant Soil. 245, 35-47 12. Deng, H., Chen, Z., Zhao, F., 2012. Energy from plants and microorganisms: progress in plant-microbial fuel cells. ChemSus Chem. 5,1006–1011. 7
13. Doherty, L., Zhao, Y., Zhao, X., Hu, Y., Hao, X., Xu, L., Liu, R., 2015. A review of a recently emerged technology: Constructed wetland e Microbial fuel cells, Water Research. 85,38-45 14. Durako, M.J., Moffler, M.D., 1987. Nutritional studies of the submergedmarine angiosperm Thalassiatestudinum. I. Growth responses of axenicseedlings to nitrogen enrichment. American Journal of Botany. 74,234-240. 15. Duineveld, B. M., Kowalchuk, G. A., Keijzer, A., van Elsas, J. D., van Veen, J. A., 2001. Analysis of bacterial communities in the rhizosphere of chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA. Appl. Environ. Microbiol. 67,172-178. 16. Gil, E.S., Couto, R.O., 2013. Flavonoid electrochemistry: a review on the electroanalytical applications. Rev. Bras. Farmacogn. Braz. J. Pharmacogn. 23, 542-558. 17. He, Z., Shao, H.,Angenent, L.T., 2007. Increased power production from asediment microbial fuel cell with a rotating cathode. Biosens. Bioelectron.22, 3252–3255. 18. Janssen, P.J.D., Lambreva, M.D., Plumeré, N., Bartolucci, C., Antonacci, A., Buonasera, K., Frese, R.N., Scognamiglio, V., Rea, G. 2014. Photosynthesis at the forefront of a sustainable life. Front. Chem. 2,36.1-22 19. Kaku,N., Yonezawa, N., Kodama, Y., Watanabe, K., 2008. Plant/microbe cooperation for electricity generation in a rice paddy field. Appl. Microbiol. Biotechnol. 79,43–49. 20. Liu, S., Hailiang, S., Li, X., Yang, F., 2013. Power Generation Enhancement by Utilizing Plant Photosynthate in Microbial Fuel Cell Coupled Constructed Wetland System, International Journal of Photoenergy, 2013, 1-10. 21. Naiman, R.J., Turner, M.G., 2000. A future perspective on North America’s freshwater ecosystems. Ecological Applications. 10,958–970. 22. Nitisoravut, R., Regmi, R., 2017. Plant microbial fuel cells: A promising biosystems engineering. Renewable and Renew sust energ rev. 76 81–89 23. Pennak, R.W., 1971. Toward a classification of lotic habitats. Hydrobiologia.38,321-334. 24. Pierret, A., Doussan, C., Capowiez, Y.,Bastardie, F., 2007. Root functional architecture: a framework for modeling the interplay between roots and soil. Vadose Zone J. 6,269–81. 25. Reimers, C.E., Tender, L.M., Fertig, S.,Wang, W., 2001. Harvesting energy from the marine sediment–water interface. Environ. Sci. Technol. 35,192–195. 26. Rezaei, F., Richard, T., Brennan, R., Logan, B.E., 2007. Substrate-enhanced microbial fuel cells for improved remote power generation from sediment-based systems. Environ. Sci. Technol. 41,4053–4058. 27. Rosenbaum, M., He, Z., Angenent, L.T., 2010. Light energy to bioelectricity photosynthetic microbial fuel cells. Curr. Opin. Biotechnol. 21,1–6. 28. Strik, D.P.B.T.B., Hamelers, H.V.M., Snel, J.F.H., Buisman, C.J.N., 2008. Green electricity production with living plants and bacteria in a fuel cell. Int. J. Energy Res. 32,870–876. 29. Shanthi Sravan, J., Sai Kishore, B., Verma, A., Venkata Mohan, S., 2017. Phasic availability of terminal electron acceptor on oxygen reduction reaction in microbial fuel cell. Bioresour. Technol. 242, 101-108 30. Venkata Mohan, S., Mohanakrishna, G., Chiranjeevi, P., 2011. Sustainable power generation from floating macrophytes based ecological microenvironment through embedded fuel cells along with simultaneous wastewater treatment, Bioresour. Technol. 102,7036–7042. 31. Venkata Mohan, S., Mohanakrishna, G., Chiranjeevi, P., Dinakar, P., Sarma, P.N., 2010. Ecologically engineered system (EES) designed to integrate floating, emergent and 8
submerged macrophytes for the treatment of domestic sewage and acid rich fermenteddistillery wastewater: Evaluation of long term performance. Bioresource Technology. 101,3363–3370. 32. Venkata Mohan, S., Srikanth, S., Raghavulu, S.V., Mohanakrishna, G., Kiran Kumar, A.,Sarma, P.N., 2009. Evaluation of the potential of various aquatic eco-systems in harnessing bioelectricity through benthic fuel cell: effect of electrode assembly and water characteristics. Bioresour. Technol. 100, 2240–2246. 33. Venkata Mohan, S., Veer Raghuvulu, S., Sarma, P.N., 2008. Biochemical evaluation of bioelectricity production process from anaerobic wastewater treatment in a single chambered microbial fuel cell (MFC) employing glass wool membrane.Biosens. Bioelectron. 23,1326– 1332. 34. Violante, A., Cozzolino, V., Perelomov, L., Caporale, A.G.,Pigna, M, J., 2010. Mobility and bioavailability of heavy metals and metalloids in soil environments. Soil Sci Plant Nutr.10,268–92 35. Wiley, M,J., Gordon, R.W., Waite, S.W.,Powless, T., 1984. The relationship between aquatic macrophytes and sport fish production in Illinois ponds: A sample model. North American Journal of Fishery Management. 4,111-119.
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Figure captions Figure 1: Bioelectrogenic profiles in three circuited modes in stacking condition a) OCV and b) Current density profile Figure 2: OCV and Current density profiles of individual tanks in series circuit, Parallel circuit and P-S circuit connections Figure 3: Polarization profiles in stacked circuits a) series circuit b) Parallel circuit c) P-S circuit connection Figure 4: Polarization profiles of individual tanks in various circuit connections Figure 5: Anode and Cathode potentials in three circuited modes in stacking condition and respective individual tanks a) Series circuit b) parallel circuit c) Series-parallel circuit Figure 6: Cyclic Voltammograms profiles for each individual Tanks at scan rate of 1 mV/s
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Highlights
Eco-electrogenic engineered system mimics the natural functional role of aquatic ecosystem. Designed EES has complex imitating aquatic ecology with high operational feasibility and low cost. EES focusing self -sustainability of aquatic environment by converting light energy to electrical energy by the photosynthetic process
17
Graphical Abstract
18
S0960-8524(18)30411-5 https://doi.org/10.1016/j.biortech.2018.03.063 BITE 19702
To appear in:
Bioresource Technology
Received Date: Revised Date: Accepted Date:
27 November 2017 8 March 2018 9 March 2018
Please cite this article as: Yeruva, D.K., Chiranjeevi, P., Butti, S.K., Mohan, S.V., Self-Sustained Photocatalytic Power Generation using Eco-Electrogenic Engineered Systems, Bioresource Technology (2018), doi: https:// doi.org/10.1016/j.biortech.2018.03.063
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Self-Sustained Photocatalytic Power Generation using Eco-Electrogenic Engineered Systems Dileep Kumar Yeruva1,2, P.Chiranjeevi1,2, Sai Kishore Butti1,2, S.Venkata Mohan1* 1
Bioengineering and Environmental Sciences Lab, EEFF Centre, CSIR-Indian Institute of Chemical Technology (CSIR-IICT), Hyderabad- 500 007, India. 2 Academy of Scientific and Innovative Research (AcSIR), Hyderabad, India. *E-mail: [email protected]; [email protected]; Tel: +9140-27191765
Abstract An eco-electrogenic engineered system (EES) was designed to mimic the functional role of natural aquatic ecosystems and evaluated their response to bio-electrogenic activity by cascadically interlinking three tanks with functionally diverse biota viz., floating macrophytes (Tank 1), submerged plants (Tank 2) and filter feeders (fish and snails) (Tank 3). Tank-1 showed efficient power generation (voltage (series): 0.86 V; current density (parallel): 37 mA/m2) than Tank-2 (voltage (series): 0.76 V; current density (Parallel): 34 mA/m2) and Tank-3 (voltage (series):0.65 V; current density (parallel): 22 mA/m2). Integrating all three tanks enabled maximum power generation in parallel-series (P-S) connection (9.5 mW/m2) than individual series and parallel connections (6.5/5 mW/m2). Interaction of microbes and plant studied at the interface of electrochemical and engineering aspects illustrated the feasibility of EES as a selfsustainable system with innate diverse functional aquatic biota and rhizo-microbiome to produce bioelectricity. Keywords: Aquatic Macrophytes; Bioelectricity; Water Ecosystem; Electric Circuit. 1. Introduction Ecological water bodies are inhabited by numerous aquatic living forms functioning symbiotically to balance the ecological status of aquatic ecosystem and fulfilling their characteristic roles (Baron et al., 2003; Aoki, 2006; Venkata Mohan et al., 2010). The congregations of diversified biota ranging from exo-electrogenic bacteria to CO2 assimilating phototrophic macrophytes make the ecological water bodies a natural source to harness energy (Venkata Mohan et al., 2009). The core sustenance of ecological water bodies depends on primary phototrophic producers which are phytoplankton and hydrophytes (Pennak, 1971; Wiley et al., 1984). The ecosystem balance is dependent on both abiotic factors including light, temperature, nutrients, and sediment composition and biotic factors which includes mainly the plant-microbial interactions (rhizosphere) to sustain the nutrient cycles (Bond et al., 2002). Plants actively recruit and sustain microorganisms in the rhizosphere by translocation of organic compounds from leaves to the roots that serves as growth substrate for rhizospheric microbes by the translocation of organic compounds from the leaves to the roots and into the rhizosphere that serves as growth substrates (Nitisoravut and Regmi, 2017). Rhizosphere bacterial community is dependent on root exudates which serve as a wide range of complex organic compounds ranging from border cells and root debris i.e., soluble and insoluble organic compounds. However, exudation of low weight molecules (organic acids, amino acids, and sugars) is a continuous process that is driven by passive diffusion and migration (Deng et al., 2012; Timmer et al., 2011). Root exudates which are produced during the photosynthetic process are uptaken by root 1
sediment microbes via microbial mineralization processes, which further restore nutrients (for aquatic plants) (Barko et al., 1986; Violante et al., 2010; Venkata Mohan et al., 2011; Chiranjeevi et al., 2013). Sediment microbes have a specific role in nutrient regeneration by releasing inorganic forms of carbon, nitrogen, phosphorus, and sulfur which serve as macro or micronutrients to aquatic plants and microorganisms (Colombo et al., 2017; Naiman and Turner, 2000). Plant-microbe symbiotic relationship and the nutrient cycle of microbial community in the rhizosphere is influenced by the variation of adaptation process due to diverse physiological and environmental stress according to geographical locations (Durako and Moffler, 1987; Venkata Mohan et al., 2009). Interactions among the biotic component along with nutrients and organic matter stored in the sediment sub-surface of aquatic ecosystems as an integral part stores a large and potential source of energy (He et al., 2007; Rezaei et al., 2007; Venkata Mohan et al., 2009). The anaerobicity of the sediments and the organic rhizodeposits enrich specific rhizosphere microorganisms that are well adapted to utilization of specific compounds (Reimers et al., 2001) Rhizobial microflora exhibited signaling mechanism between plants and microbes present in the sediment (Duineveld et al., 2001). Among them, some of the rhizodeposits are oxidized by electrochemically active bacteria (EAB) specific for plant species (Venkata Mohan et al.,2009; Chiranjeevi et al., 2012; Rosenbaum and Angenent, 2010; Strik et al., 2008). The possibility of utilizing these EAB for energy generation in the natural ecological water bodies has been evaluated by incorporating an electrode setup into the sediment acting as anode and air exposed electrode as cathode (Venkata Mohan et al., 2011; Babu and Venkata Mohan, 2012). The electrogenic capability of aquatic plants and associated rhizomicrobiome was not explored earlier for the production of electricity. The fundamental mechanism that will be employed for power generation in natural aquatic bodies is the photosynthetic activity that results in production of organic compounds through utilization of solar energy. These organic compounds serve as substrate for microbiome which further generates bioelectricity in the presence of a fuel cell setup, functioning in a self-sustainable mode without the addition of any external carbon source. Considering the advantage of natural ecosystems and microbial fuel cell for power generation, study is designed to focus on self -sustainability of aquatic environment for the production of electricity from aquatic plants by converting light energy to electrical energy by the photosynthetic process. An attempt was made in this study to assess the hidden potential of natural water bodies for self-sustained power production using embedded fuel cell assemblies. Natural lake ecosystems were simulated in aquatic tanks (150 l capacity) which were designed and fabricated as eco-electrogenic engineered systems (EES) containing different types of plants species related to floating, submerged and emergent hydrophytes placed in a defined sequence. The systems were operated in self-sustained mode without the addition of external carbon or nutrients, and the carbon source was obtained from the atmospheric CO2 for the plants and root excretes for the microbial community. 2. Experimental methodology 2.1. EES An eco-electrogenic engineered system (EES) was designed with three rectangular tanks having dimensions 55 X 30 X 30 cm length, width and height. Each tank was fabricated using perplex sheets with total/ working volume of 50/35 L with a free board of 5 cm. The rectangular design provides an advantage of effective space utility and ease of operation with an even distribution of the water flow. The three tank EES was placed on a customized stand with natural height 2
gradient of 15 cm allowing the flow with gravity, the feed tank/water source is kept at the highest point followed by the series of other tanks with specific plant types. The tanks were labeled from the top to bottom as Tank 1, Tank 2 and Tank 3 respectively. The tanks were provided with baffles to prevent cross discharge by reducing solids discharge and also to equalize the flow. Vents were provided at a distance of 5 cm from the top of the tank, these were used to hydrological connection each tank. The system was operated in continuous mode with a constant flow rate of 2 l/h. Bottom of Tank 1 and Tank 2 was filled with sediment obtained from Nacharam lake up to a height of 5 cm and the Tank 3 was filled with fine sand. 2.2. Operation Contents of tanks were designed to simulate the natural condition in water bodies with variations based on different hydroponic macrophytes in each tank. Tank1 was designed to contain freefloating macrophytes having plants like Eichhornia crassipes (water hyacinth) which is vascular and has rapid growth. It covers the water surface of the tank and helps to maintain anoxic microenvironment in Tank1. Moreover, Eichhornia crassipes develops a fibrous root system which is favorable for the growth of different microbial communities in the rhizosphere. Tank2 contains slender, submerged, perennial aquatic herbs like Hydrilla verticillata, which helps in maintaining aerobic condition in the tank by respiring underwater. The growth of these plants is rapid and they contain a tuberous root system anchored in the sediment. Tank3 was designed for filter-feeding action with fish and snails along with Pistiastratiotes, which enables final water polishing by the filter-feeding action of snails and fish and consume the bacteria and planktons. 2.3. Fuel Cell Assembly Each tank was embedded with 4 electrode assembly setups (without membrane). Non-catalyzed graphite electrodes with a surface area of 0.105 m2 were used as cathode and anode. Anodes were placed on the sediment at the depth of 1 cm and cathodes were placed on the sub-surface of water, where the upper portion of the electrode was exposed to air and bottom surface was in contact with the water. The inter-electrode distance was 20 cm. The circuit connections to electrodes were made with copper wire sealed by epoxy sealant. The stacked electrode setups were placed in each tank with the support of inert non-conductive material suspended from the top. The power output was analyzed with electrodes connections in different circuitries. The electrical circuitries were evaluated in three variations, the first setup was with series operation were anode was connected to the subsequent cathode, the second was a parallel setup were all the anodes are connected and all the cathodes are connected and the third setup was a combination of series and parallel operation were electrodes in each tank were connected in parallel and the tanks were connected in series. The bio-electrochemical data was obtained in open circuit mode by connecting the free terminal electrodes. 2.4. Bioelectrogenic Analysis Bioelectrogenic profiles based on open circuit voltage (OCV) and current (I; with 100 Ω resistance) were recorded using a digital multi-meter. The bioelectrogenic measurements were recorded in three circuitry modes viz., series, parallel and parallel-series (P-S) connection in individual tanks. Polarization profiles were recorded by changing external (30-0.05 kΩ) resistances in each individual tank with three circuited modes. Power was derived from P=VI equation, power density (PD) (mW/m2) and current density (CD) (mA/m2) were calculated with the function of anodic surface area (m2). Cell potentials of anode and cathode were measured at various external resistances against saturated Ag/AgCl (S) as reference electrode. All the 3
electrogenic measurements were performed separately for each tank in all circuit mode of operations. Bio-electrochemical and redox behavior was studied for each individual tank employing a potentiostat-galvanostat system (Bio-logic, VMP3, France). A potential ramp from +1.0 to -1.0 V was applied at scan rates of 50, 30, 20, 10 and 1 mV/s to record the voltammograms. All the electrochemical assays were performed using anode as working electrode and cathode as a counter electrode against Ag/AgCl (3.5M KCl) as reference electrode. 3. Results and Discussion 3.1. Photo-eco-electrogenic activity vs circuitry mode Feasibility of self-sustained power generation with the symbiotic association of microbes and plant root metabolites was studied by introducing electrodes in the rhizosphere of all the three tanks. Bioelectrogenic activity was measured in three electrical circuit modes such as series, parallel and parallel-series (P-S) for electrically stacked tanks. EES showed power generation in the order with Tank 1 > Tank 2 > Tank 3 and open circuit voltages (OCV) were observed to be 0.8, 0.7 and 0.65 V, respectively in series connection. When these three systems were stacked together in series, maximum OCV output recorded was 2.2 V, which is cumulative of the three individual tanks (Fig 1). Maximum current density of stacked-series circuit was 4.15 mA/m2, and the corresponding current densities of individual tanks were recorded as 2.7 mA/m2 (Tank 1), 2.5 mA/m2 (Tank 2) and 2.4 mA/m2 (Tank 3) (Fig 2). EES showed consistent power production without any voltage reversal in series circuit, as each tank performance was stable in terms of electrogenic activity. The power production in parallel stacked EES operation was 0.6 V and the OCV of individual tanks were recorded as 0.65, 0.63 and 0.60 V respectively. Maximum current of the parallel stacked circuit was 103 mA/m2 and the corresponding current generation for each tank was recorded as 37 (Tank 1), 33 (Tank 2) and 20 mA/m2 (Tank 3) which was much higher than the performance of single tank in series connection. The power output obtained in series and parallel circuits was less as the series circuitry yields low current (cumulates only voltage) and parallel circuitry yields low voltage (cumulates only current). Therefore, a hybrid circuitry was developed and evaluated by interconnecting tanks partially in parallel and series (P-S) circuits. A circuit was arranged in such way that the individual tanks consisting of electrode setups were connected in parallel to obtain maximum current and the three parallel circuited tanks were stacked in series circuit to obtain the maximum power output and to cumulatively enhance the bioelectrogenesis of EES. P-S circuit yielded maximum voltage and current (1.6 V; 50 mA/m2) in stacked conditions (Fig 1) with corresponding individual tanks depicting maximum voltage and currents in Tank 1 (0.75 V; 37 mA/m2) followed by Tank 2 (0.6 V; 33 mA/m2) and Tank 3 (0.3 V; 22 mA/m2) (Fig 2). Figure 1 Rhizosphere a rich source of carbonaceous root exudates (carbohydrates, fatty acids, amino acids, hormones and other phenolic organic compounds) are synthesized by plants via converting solar (light) energy into chemical energy (Pierret et al., 2007; De Schamphelaire et al., 2008; Kaku et al., 2008; Chiranjeevi et al., 2012). The photosynthetic process depends on its capability to exploit everlasting reservoirs of sunlight, water, and carbon dioxide to transform photonic energy into chemical energy (Janssen et al. 2014). The hydrophytes, floating and rooted macrophytes play an important role in aquatic ecosystems as food providers that enable the maintenance of ecological diversity (Pennak, 1971; Wiley et al., 1984). In Tank 1, the floating plant Eichhornia facilitates an anoxic microenvironment by spreading on the water surface allowing low air exchange to the water. The conditions enrich mostly anaerobic and facultative 4
consortia which enable power generation by metabolizing the rhizo deposits. Sponge and marsh based root system of Eichhornia also helps in creating the suitable environment for the root associated bacterial communities which also increases the availability of organic matters (Chandra et al., 2017, 2018). Tank 2 facilitates aerobic microenvironment by means of submerged Hydrilla which has the capability of releasing O2 through their photosynthetic action. This evolved oxygen can facilitate aerobic conditions in cathode zone, which improves electric output (Shanthi Sravan et al., 2017). The observed power output relatively lower than Tank 1, might be attribited to the absence of heavy root system (lesser availability of root excreates) and the presence of dissolved oxygen that neutralizes the produced electrons. Apart from the carbon source, root exudates also stimulate chemotaxis to promote soil microbes to the rhizosphere (Nitisoravut and Regmi, 2017; Babu and Venkata Mohan, 2012). Figure 2 3.2. Polarization Profiles Internal resistance and electrochemical losses can be determined by the polarization profiles along with the cell design point which indicates the maximum operational load (Venkata Mohan et al., 2008). The polarization profiles were plotted as the voltage vs power density (PD) in response to varying external loads from 30 kΩ to 50 Ω on the system (Fig 3). The maximum power density (9 mW/m2) and a current density (28 mA/m2) were observed in Tank 1 with corresponding resistance (100 Ω) (Fig 4). In the stacked-series circuit, higher PD (5 mW/m2) with a maximum voltage of 1.9 V was obtained at an external resistance of 200 Ω. In parallel circuit mode, maximum PD was observed in individual tanks (Tank 1, 15 mW/m2) corresponding to CD (35 mA/m2). Subsequently, a stacked-parallel circuit obtained maximum PD of 6.8 mW/m2 with the corresponding CD (15 mA/m2). In the combinatory P-S circuits showed the maximum power density of 9.5 mW/m2 at resistance (100 Ω) and current density (18 mA/m2) which is comparatively higher than series and parallel circuits. The stacked circuit modes showed lower PD than individual tanks as the surface area of anodes cumulates lowering the charge present per unit area. Similar results were reported, were the increase in surface area of anode decreases the PD (Liu et al., 2013).The individual tanks showed ohmic and activation losses irrespective of circuit modes connections which are primarily due to the non-catalytic electrode material and the inter-electrode distance between anode and cathode. Figure 3 & 4 3.3. Cell Potentials Cell potential/EMF (E0) determines the performance of the fuel cell and is dependent on the anode (Ea) and cathode (Ec) potentials, which are also termed as half-cell potentials. These halfcell potentials were recorded at various external resistances against Ag/AgCl reference electrode (Fig 5). Stacked P-S circuit conditions showed higher Ea (-850 mV) than individually stacked series and parallel circuits and were also higher than the individual tanks. In the stacked-series circuit the maximum Ea of -295 mV was observed greater than the individual tanks. Ea profile in the stacked parallel circuit was observed to be more or less similar with a maximum of -118mV among each individual tank values. In all circuit conditions, Ea drops at lower resistance owing to its rapid electron discharge from the anode to the counter electrode in the circuit. Cathode potential (Ec) were observed to show the similar trends like anode potential (Ea) with the varying external resistance. The rate of drop in Ec of parallel connection was high compared to series and P-S circuit connection. The Ec of stacked series, parallel and P-S circuit connections were between 0.90 to 1.22, 0.335 to 0.001 and 0.487 to 0.002 V, respectively. The higher Ec can 5
be due to the innate capabilities of plant root system to evolve oxygen in allelectric configurations (Doherty et al., 2015). It indicates that the total cell potential and current generation were limited by both anode and cathode potentials with the function of varying external resistance. Figure 5 3.4. Bio-electrochemical behavior Cyclic voltammetry (CV) was employed to analyze the bio-electrochemical redox behavior. The voltammetric analysis was performed individually for each tank during the daytime with a scan rate of 1 mV/s in a range of -1.0 to 1.0 V. Voltammograms depicted variation in redox catalytic currents for each tank respectively (Fig 6).Tank 1 showed more reductive current-3.8 mA and 2.5 mA oxidative current. Tank 2 showed -4.2 mA and 1.5 mA reductive current and oxidative currents respectively. Tank 3 showed lower oxidation and reductive currents with 1 mA and -2.9 mA. Obtained voltammograms illustrated the difference in catalytic currents as well as the capacitance for each of the tank. Higher redox catalytic currents without any noticeable capacitance were observed with Tank1 with Eichhornia crassipes (water hyacinth). The fibrous root system of Eichhornia provides nesting habitat for much bacterial sp. prevalence of anaerobic conditions in the system might have contributed to low capacitance and high reductive currents. The root excretes flavonoids which might involve the electron carries and favors to develop the higher catalytic currents (as observed in voltammograms). The electrochemical profile of flavonoids, akin to their redox behavior is mainly driven by the stability of electrogenerated phenoxyl radicals which determines the overall electrode reactions (Gil and Couto, 2013). Figure 6 Following higher redox currents were noticed in the Tank 2 which might be due to the anoxic conditions prevailing due to the presence of Hydrilla verticilata. Oxygen generation by Hydrilla in the system may increase in capacitive current generation. While in the case of Tank 3, redox catalytic currents were comparatively less than tank 2. This might be due to the availability of organic matter/root exudates in less quantity (than at Tank 2). The variations observed at all the tanks were majorly due to the presence of root system and the efficiency of plant system to perform photosynthesis which was the only source to derive energy for the growth of plant systems. Cyclic voltammograms showed the activity of different redox mediators observed in the three tank systems (Fig 6). Tank 1 showed the redox peek at -345, +05, +105 mV, Tank 2 at -45,+155 mV and Tank 3 at -95, +155 mV with against Ag/AgCl (3.5 M KCl). The observed redox potentials correspond to NAD+/ NADH+H+, Ubiquinone OX/RED, FAD/FADH2 and cytochrome c activity. These redox compounds participate in the electron transport across the bacterial cell membrane. Comparatively the control system (without plant) showed high capacitive currents, this may be due to the effect of electrode distances. High reductive currents observed in the plant components represented bacterial activity with rhizoexudates metabolisms. Cyclic voltammograms were also performed at different scan rates from 1, 10, 20, 30 and 50 mV/s which illustrate the relationship between individual plants towards power production. 4. Conclusions Study illustrated the feasibility of harnessing power in EES system through symbiotic association of water ecosystems via photosynthetic machinery. Synergetic interaction was observed between 6
aquatic plant-microbes (rhizosphere) and sediment microbiome which converts light energy into electric energy by catalytic function of organic/inorganic (root excretes) compounds. The designed EES is a self-sustainable complex biome imitating the natural aquatic ecosystems which has operational feasibility and is inexpensive to harness light energy into electrical energy. Power generation attained through natural eco-systems depicts the self-sustenance towards real field applications. Acknowledgements The authors thank Director, CSIR-IICT for support and encouragement in carrying out this work. The authors would like to acknowledge Department of Biotechnology (DBT) for proving research grant (BT/PR18965/BCE/8/1401/2016). PC duly acknowledges CSIR for providing research fellowship. SKB duly acknowledges UGC for providing research fellowship. References 1. Aoki, I., 2006. Ecological pyramid of dissipation function and entropy production inaquatic ecosystems. Ecol. Complex. 3,104–108. 2. Babu, M.L., Venkata Mohan, S., 2012. Influence of graphite flake addition to sediment on electrogenesis in a sediment-type fuel cell. Bioresour. Technol. 110, 206-213 3. Barko, J.W., Adams, M.S., Clesceri, N.L., 1986. Environmental factors and their consideration in the management of submersed aquatic vegetation: A review. J Aquat Plant Manag. 24,1−10. 4. Bond, D.R., Holmes, D.E., Tender, L.M.,Lovley, D.R., 2002. Electrode-reducing microorganisms that harvest energy from marine sediments. Science. 295,483–485. 5. Chandra, R., Sravan, J.S., Hemalatha, M., Kishore Butti, S., 2017. Photosynthetic synergism for sustained power production with microalgae and photobacteria in a biophotovoltaic cell. Energy Fuels 31, 7635-7644 6. Chandra, R., Venkata Mohan, S., Roberto, P, S., Ritmann, B.E., Cornejo, R.A.S., (2018) Biophotovoltaics: Conversion of Light Energy to Bioelectricity Through Photosynthetic Microbial Fuel Cell Technology. Microbial Fuel Cell, Springer, 373-387 7. Chiranjeevi, P., Mohanakrishna, G., Venkata Mohan, S., 2012. Rhizosphere mediated electrogenesis with the function of anode placement for harnessing bioenergy through CO2 sequestration. Bioresour Technol. 124,364–370. 8. Chiranjeevi, P., Rashmi, C., Venkata Mohan,S., 2013. Ecologically engineered submerged and emergent macrophyte based system: An integrated eco-electrogenic design for harnessing power with simultaneous wastewater treatment,Ecological Engineering. 51,181– 190. 9. Colombo, A., Marzorati, S., Lucchini, G., Cristiani, P., Pant, D., Schievano, A., 2017. Assisting cultivation of photosynthetic microorganisms by microbial fuel cells to enhance nutrients recovery from wastewater. Bioresour Technol. 237,240-248. 10. De Schamphelaire, L., Bossche, L. V., Dang, H.S., Hofte, M., Boon, N., Rabaey, K.,Verstraete, W., 2008. Microbial fuel cells generating electricity from rhizodeposits of rice plants. Environ. Sci. Technol. 42,3053–3058. 11. Dakora, F.D., Phillips, D.A. 2002. Root exudates as mediators of mineral acquisition in lownutrient environments. Plant Soil. 245, 35-47 12. Deng, H., Chen, Z., Zhao, F., 2012. Energy from plants and microorganisms: progress in plant-microbial fuel cells. ChemSus Chem. 5,1006–1011. 7
13. Doherty, L., Zhao, Y., Zhao, X., Hu, Y., Hao, X., Xu, L., Liu, R., 2015. A review of a recently emerged technology: Constructed wetland e Microbial fuel cells, Water Research. 85,38-45 14. Durako, M.J., Moffler, M.D., 1987. Nutritional studies of the submergedmarine angiosperm Thalassiatestudinum. I. Growth responses of axenicseedlings to nitrogen enrichment. American Journal of Botany. 74,234-240. 15. Duineveld, B. M., Kowalchuk, G. A., Keijzer, A., van Elsas, J. D., van Veen, J. A., 2001. Analysis of bacterial communities in the rhizosphere of chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA. Appl. Environ. Microbiol. 67,172-178. 16. Gil, E.S., Couto, R.O., 2013. Flavonoid electrochemistry: a review on the electroanalytical applications. Rev. Bras. Farmacogn. Braz. J. Pharmacogn. 23, 542-558. 17. He, Z., Shao, H.,Angenent, L.T., 2007. Increased power production from asediment microbial fuel cell with a rotating cathode. Biosens. Bioelectron.22, 3252–3255. 18. Janssen, P.J.D., Lambreva, M.D., Plumeré, N., Bartolucci, C., Antonacci, A., Buonasera, K., Frese, R.N., Scognamiglio, V., Rea, G. 2014. Photosynthesis at the forefront of a sustainable life. Front. Chem. 2,36.1-22 19. Kaku,N., Yonezawa, N., Kodama, Y., Watanabe, K., 2008. Plant/microbe cooperation for electricity generation in a rice paddy field. Appl. Microbiol. Biotechnol. 79,43–49. 20. Liu, S., Hailiang, S., Li, X., Yang, F., 2013. Power Generation Enhancement by Utilizing Plant Photosynthate in Microbial Fuel Cell Coupled Constructed Wetland System, International Journal of Photoenergy, 2013, 1-10. 21. Naiman, R.J., Turner, M.G., 2000. A future perspective on North America’s freshwater ecosystems. Ecological Applications. 10,958–970. 22. Nitisoravut, R., Regmi, R., 2017. Plant microbial fuel cells: A promising biosystems engineering. Renewable and Renew sust energ rev. 76 81–89 23. Pennak, R.W., 1971. Toward a classification of lotic habitats. Hydrobiologia.38,321-334. 24. Pierret, A., Doussan, C., Capowiez, Y.,Bastardie, F., 2007. Root functional architecture: a framework for modeling the interplay between roots and soil. Vadose Zone J. 6,269–81. 25. Reimers, C.E., Tender, L.M., Fertig, S.,Wang, W., 2001. Harvesting energy from the marine sediment–water interface. Environ. Sci. Technol. 35,192–195. 26. Rezaei, F., Richard, T., Brennan, R., Logan, B.E., 2007. Substrate-enhanced microbial fuel cells for improved remote power generation from sediment-based systems. Environ. Sci. Technol. 41,4053–4058. 27. Rosenbaum, M., He, Z., Angenent, L.T., 2010. Light energy to bioelectricity photosynthetic microbial fuel cells. Curr. Opin. Biotechnol. 21,1–6. 28. Strik, D.P.B.T.B., Hamelers, H.V.M., Snel, J.F.H., Buisman, C.J.N., 2008. Green electricity production with living plants and bacteria in a fuel cell. Int. J. Energy Res. 32,870–876. 29. Shanthi Sravan, J., Sai Kishore, B., Verma, A., Venkata Mohan, S., 2017. Phasic availability of terminal electron acceptor on oxygen reduction reaction in microbial fuel cell. Bioresour. Technol. 242, 101-108 30. Venkata Mohan, S., Mohanakrishna, G., Chiranjeevi, P., 2011. Sustainable power generation from floating macrophytes based ecological microenvironment through embedded fuel cells along with simultaneous wastewater treatment, Bioresour. Technol. 102,7036–7042. 31. Venkata Mohan, S., Mohanakrishna, G., Chiranjeevi, P., Dinakar, P., Sarma, P.N., 2010. Ecologically engineered system (EES) designed to integrate floating, emergent and 8
submerged macrophytes for the treatment of domestic sewage and acid rich fermenteddistillery wastewater: Evaluation of long term performance. Bioresource Technology. 101,3363–3370. 32. Venkata Mohan, S., Srikanth, S., Raghavulu, S.V., Mohanakrishna, G., Kiran Kumar, A.,Sarma, P.N., 2009. Evaluation of the potential of various aquatic eco-systems in harnessing bioelectricity through benthic fuel cell: effect of electrode assembly and water characteristics. Bioresour. Technol. 100, 2240–2246. 33. Venkata Mohan, S., Veer Raghuvulu, S., Sarma, P.N., 2008. Biochemical evaluation of bioelectricity production process from anaerobic wastewater treatment in a single chambered microbial fuel cell (MFC) employing glass wool membrane.Biosens. Bioelectron. 23,1326– 1332. 34. Violante, A., Cozzolino, V., Perelomov, L., Caporale, A.G.,Pigna, M, J., 2010. Mobility and bioavailability of heavy metals and metalloids in soil environments. Soil Sci Plant Nutr.10,268–92 35. Wiley, M,J., Gordon, R.W., Waite, S.W.,Powless, T., 1984. The relationship between aquatic macrophytes and sport fish production in Illinois ponds: A sample model. North American Journal of Fishery Management. 4,111-119.
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Figure captions Figure 1: Bioelectrogenic profiles in three circuited modes in stacking condition a) OCV and b) Current density profile Figure 2: OCV and Current density profiles of individual tanks in series circuit, Parallel circuit and P-S circuit connections Figure 3: Polarization profiles in stacked circuits a) series circuit b) Parallel circuit c) P-S circuit connection Figure 4: Polarization profiles of individual tanks in various circuit connections Figure 5: Anode and Cathode potentials in three circuited modes in stacking condition and respective individual tanks a) Series circuit b) parallel circuit c) Series-parallel circuit Figure 6: Cyclic Voltammograms profiles for each individual Tanks at scan rate of 1 mV/s
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a)
b) 2.5 Series circuit Parall circuit P-S circuit
Current Density (mA/m 2)
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Series Circuit 1.0
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65
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b) 2.0
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Current Density (mA/m2)
15
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PD
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Fig: 4
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PD
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V
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Current Density (mA/m )
Voltage (V)
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Voltage (V)
5
2
2
2
0.20
2
0.55
Voltage (V)
V PD
3.0
0.35
2
Voltage (V)
0.45
5
Current Density (mA/m )
P-S circuit
0.50
7
0.20
0
Series circuit
8
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2
Parallel circuit
Voltage (V)
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V PD
Power Density (mW/m )
12
Tank 3
Power Density (mW/m )
0.55
Power Density (mW/m )
14
Voltage (V)
0.55
Tank 2
Voltage (V)
Tank 1
a)
b)
0.6 Stacked
Tank 1
Tank 2
0.35
Tank 3 Anode/Cathode potential (V)
1.2 1.0 0.8 0.6 0.4 0.2 0.0 -0.2
stacked
Tank 1
Tank 2
stacked
Tank 3
Tank 1
Tank 2
Tank 3
0.4
0.30
Anode/Cathode Potential (V)
1.4
Anode/cathode potential (V)
c)
0.25 0.20 0.15 0.10 0.05 0.00 -0.05 -0.10
0.2 0.0 -0.2 -0.4 -0.6 -0.8
-0.4 0
5
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25
30
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Resistance (k)
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Resistance (k)
Fig: 5
15
3
Tank 1 Tank 2
2
Tank 3
1
I/mA
0 -1 -2 -3 -4 -1.0
-0.5
0.0
0.5
1.0
Ewe/V vs Ag/AgCl
Fig: 6
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Highlights
Eco-electrogenic engineered system mimics the natural functional role of aquatic ecosystem. Designed EES has complex imitating aquatic ecology with high operational feasibility and low cost. EES focusing self -sustainability of aquatic environment by converting light energy to electrical energy by the photosynthetic process
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Graphical Abstract
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