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Chlorophytum microbial fuel cell characterization

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Chlorophytum

microbial fuel cell characterization

I. Tou, Y. M. Azri, M. Sadi, H. Lounici & S. kebbouche-Gana

To cite this article: I. Tou, Y. M. Azri, M. Sadi, H. Lounici & S. kebbouche-Gana (2019): Chlorophytum microbial fuel cell characterization, International Journal of Green Energy, DOI: 10.1080/15435075.2019.1650049

To link to this article: https://doi.org/10.1080/15435075.2019.1650049

Published online: 04 Aug 2019.

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Chlorophytum

microbial fuel cell characterization

I. Toua,b, Y. M. Azria, M. Sadia, H. Lounicic, and S. kebbouche-Ganab

aDivision Bioénergie et Environnement- Algérie, Centre de Développement des Energies Renouvelables, Alger;bDépartement de Biologie, Université

M´hamed Bougara, Boumerdes, Algérie;cMD2lab, Université Akli Mohand Oulhadj, Bouira, Algérie

ABSTRACT

In the present work, solar energy conversion into electricity was evidenced by the Chlorophytum comosum-Microbial Fuel Cell (Chlorophytum-MFC). Our Chlorophytum-MFC had produced an Open Circuit Voltage (OCV) up to 1211 mV, without adding any nutrient or membrane. Plant biomass heigh and anodic bacterial number were proportional to OCV, current Icmax, and power Pmax, and were

inversely proportional to the internal resistance Rint thus: 42 cm, 110.103 U/ml, 900 mV, 0.037 mA, 744 µW/m2 and 17 KΩ, respectively, at the 191th day of experiment. We had also highlighted that Chlorophytum-MFC had behaved like a typical fuel cell via polarization and power curves. Also, we had studied the photosynthesis effect on electrical energy production by measuring voltage fluctuation during three successive days and nights. The solar and temperatures influences were also highlighted by comparing weather software data to the measured Open Voltage. The electrogenous activity was clearly proportional to soil and climate temperature as well as to sunlight intensity. The obtained results showed that developingChlorophytum-MFC could provide significant prospects for p-MFC and bioe-nergy recovery. ARTICLE HISTORY Received 27 September 2018 Accepted 26 July 2019 KEYWORDS Bioelectricity; Chlorophytum microbial fuel cell; electroactive biofilm; electrogenous activity; plant microbial fuel cell; rhizospheric bacteria; green electricity

1. Introduction

Fossil fuels are supplying about 85% of the world’s energy resources. Fossil fuels are non-renewable, are limited in sup-ply and will be depleted soon, since they are consumed faster than they are produced. In contrast, renewable energies (solar-energy, wind-energy, energy from biomass or bioe-nergy…), that are the sources whose formation rate is higher than their consumption rate could be a credible alternative. Furthermore, renewable energy is defined as clean since it generates electricity with little or no pollution (Salvin, Roos, and Robert2012).

A microbial fuel cell (MFC) is a bio-electrochemical system for converting chemical energy into electricity using the bio-catalyst. It is a new technology that can potentially provide renewable and sustainable energy. Plant-Microbial Fuel Cell (p-MFC) is a promising MFC modified that exercises the rhizosphere – microbe relationship to convert solar energy into bioelectricity using living plants and an MFC system. It constitutes a future way for agro-energy chains in context of sustainable development (Timmer et al.2012).

Living plants release a wide range of organic matters through roots into rhizosphere via photosynthesis (Goto et al. 2015; Nitisoravut and Regmi 2017; Rovira 1959). The plants may exude more than 20% of the assimilated carbon into the rhizo-sphere (Guckert et al.1992). The exudates contain water-soluble, water-insoluble and volatile compounds including sugars, amino acids, organic acids, nucleotides, flavanones, phenolic compounds and enzymes (Hoagland and Williams 1985). Rhizodeposits modify the soil pH as well as the water flow and

the oxygen availability around the roots (Preece and Peñuelas

2016). The rhizodeposits are readily used as a direct energy source to stimulate the rhizospheric microorganisms’ growth (Paterson2003) and represent therefore a vast chemical energy flow into the soil matrix (Dakora and Phillips2002).

P-MFCs considered as self-sustaining systems with long-term stability can use this chemical energy flow. Indeed, the electro-chemically active bacteria (EAB) forming the electroactive bio-film on the p-MFC anode, conserve a part of chemical substrate energy for their own metabolism (to support growth) and simul-taneously deliver electrons to the p-MFC anode by oxidizing organic compounds (Lovley 2006). The anode-cathode redox gradient facilitates the electrons transfer through an external circuit to reduce an electron acceptor (O2) at the cathode (Bennetto 1990; Chiranjeevi, Mohanakrishna, and Mohan

2012; Strik, Snel, and Buisman2008). Thus, understanding and controlling electroactive biofilm metabolism have a primordial impact on p-MFCs development.

Rhizodeposition via photosynthetic pathway is probably one of the most important parameters in p-MFC efficiency (Helder et al.

2010). Plants are devised into three pathways according to the photosynthetic activity C3, C4, and CAM. C4 plants have the highest photosynthesis efficiency for converting solar energy into bioelectricity (Wang et al.2012a). However, there are some C3 plants species that exhibit higher efficiency than C4 plants (Helder et al.2010). Therefore, in order to compare p-MFC performances, the bioelectricity yield of C3, C4, and CAM plants must be studied in an identical system under the same operating conditions (Nitisoravut and Regmi2017).

CONTACTI. Tou [email protected];[email protected] Centre de Développement des Energies Renouvelables, Alger

Color versions of one or more of the figures in the article can be found online atwww.tandfonline.com/ljge.

INTERNATIONAL JOURNAL OF GREEN ENERGY https://doi.org/10.1080/15435075.2019.1650049

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Several previous works have been carried out in the p-MFC field using different plants for bioelectricity generation. Most plants used in p-MFC systems are belonging to aquatic environ-ments where rice paddy fields are frequently studied (Kaku et al.

2008; Moqsud et al.2015; Takanezawa et al. 2010), O. sativa (Schamphelaire et al.2008). Other aquatic or sub-aquatic plants are also studied to producing bioelectricity via p-MFC: G. maxima (Strik, Snel, and Buisman2008; Timmer et al.2012,

2013), A. anomala and S. anglica (Helder et al. 2010), E. glabrescens (Bombelli et al. 2013), I. aquatica (Liu et al.

2013), L. minuta and V. ducweed (Hubenova and Mitov2012,

2015), A. calamus (Yan et al. 2015), C. involucratus (Klaisongkram and Holasut 2015), S. arabicus and C. dactylonspecies (Gilani et al. 2016), B. juncea, T. foenum-graecum and C. stuttgart (Sophia and Sreeja 2017) and Alkaligrass plants (Khudzari et al. 2018). However, very few works have used ornamental plants such as C. indica (Lu, Xing, and Ren2015) and L. perenne (Habibul et al.2016). The first objective of the present work is to investigate a new plant specie in p-MFC to optimize renewable bioelectricity produc-tion. Using ornamental plants in p-MFC system which can have environmental phytoremediation impact could be the subject of green roofs or panels installed in gardens, schools, public places offering at the same time bioelectricity for public lighting, depol-luting the environment and embellishing the grounds.

Chlorophytum comosum (C. comosum) is a small herb, which appears from tuberous rhizome, with fleshy thickened and fusiform primary roots. Despite C. comosum is a C3 plant, it has an important O2 production rate and electrical conductivity significantly correlated to its high tolerance and high accumulation of cadmium (Wang et al. 2012b). It has a unique ability to grow in a wide variety of light and tem-perature conditions and it grows particularly well in the increased daylight regions. It has a greater ability for tempera-ture acclimation of photosynthesis across a broad temperatempera-ture range (10–35°C) (Yamori, Hikosaka, and Way 2014). It has been suggested that C. comosum had a better survival poten-tial at 0°C (Gupta et al. 2016). It can grow in high water conditions as imposed in the p-MFC system and it is not attributed to the photorespiration phenomenon in hot and dry conditions (Wang, Tao, and Dai2011).

C. comosum is an evergreen plant, having a high ornamental value native from southern Africa and widespread in Algeria. It is a popular plant belonging to the monocotyledon Liliacea family. It is characterized by high biomass, easy cultivation, intense competitive ability, high pollutants stress tolerance and remove gaseous waste (formaldehyde, nitrogen dioxide, carbon

oxide, ozone, benzene, toluene, cigarette smoke, and ammonia) (Gawrońska and Bakera2015; Giese et al.1994; Tao, Wang, and Dai2011). In addition, it has a wide geographic distribution (Bai et al.2010; Jia-ying2013). Consequently, for all the above rea-sons C. comosum can have practical applications in renewable energy following and control.

However, C. comosum had not been systematically studied in p-MFC system, except briefly in our previous work (Azri et al.

2018). It has been though studied for its ability to reduce heavy metals in phytoremediation (Hernández-Apaolaza et al.2005; Tao, Wang, and Dai2011). In the present work, it has been firstly investigated the Chlorophytum capacity to produce energy through the p-MFC system and characterize therefore the Chlororophytum-MFC by the polarization study, then the effect of climatic and soil temperatures, sunlight and day-night cycle on the bioelectricity production had been studied.

2. Material and methods 2.1. Chlorophytum-MFC setup

The Chlorophytum-MFC was designed in Bioenergy and Environment laboratory of the CDER (Centre de Développement des Energies Renouvlables) using a PVC (polyvinyl chloride) pot, filled with CDER garden soil, without adding any organic fertilizer. A second pot was prepared in the same way with the same conditions without a plant, to determine if current generation was due to oxidation of organic compounds. We use two electrodes (anode a and cathode c) of rectangular shape (3 cm x 2.5 cm) with plane surfaces of S= Sanode = Scathode = 7.5 cm2, made from graphite which is an eco-friendly material, cheap and a good current conductor. To close the electrical circuit, the electrodes were connected through epoxy-capsuled wires to an external resistance of 66 KΩ. The anode was set vertically at the plant roots, approxi-mately 4 cm below the soil surface, while the cathode was placed horizontally on the soil surface and no cations exchange membrane was used (Figure 1).

The Chlorophytum was planted at the biological growth beginning with eighteen (18) leaves, eight (08) roots and 9 cm height. Chlorophytum-MFC performances was evaluated from December 2014 to July 2016 (5 days a week). The plant was exposed to natural sunlight and watered daily at 09:00 AM with 100 ml of CDER water tap (Table1) during all the experiment, which was gradually increased with plants growth.

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2.2. Chlorophytum-MFC monitoring and system voltammetry study

From December 2014 to August 2015, the Chlorophytum-MFC electrochemical performance was studied by measuring the potential difference Uacbetween the electrodes in the case of open circuit (external resistance disconnected, i.e., current cell Ic= 0) and recording the OCV (OCV = Uacfor Ic = 0) every hour using a multimeter (Fluke).

To illustrate Chlorophytum-MFC electrochemical system behavior, polarization curves were established at four dif-ferent days (day 106, day 114, day 122 and day 191) from what many performance parameters were extracted includ-ing OCV, maximum of current cell (max(Ic) = Icmax), max-imum of output power (max(P) = Pmax) and internal resistance (Rint). Polarization curve represents the cell potential as a linear function of the current Uac(Ic) which is a useful tool for the MFC performance measurement (Salvin, Roos, and Robert 2012). Polarization curve is the MFC characteristic curve called also voltage-current curve, used to characterize voltage as a current function and shows how well the MFC maintains voltage as a current function. Furthermore, electroactive biofilm maturity can be demonstrated through the polarization curves study measurement (Moqsud et al. 2015; Salvin, Roos, and Robert2012).

When establishing the curves, the external resistance was first not connected for 30 min, allowing the measure-ment of OCV, which is the maximum cell potential. After the external resistance was connected and decreased every 10 min from 1 MΩ to 10 KΩ, to obtain at least 15 different Ic measurements. The voltage Uac and the cur-rent cell Ic were measured for each value of the external resistance. The resulting current–voltage values Uac(Ic) were used to construct the polarization curve. The power curve is deducing from the previous curve with P(Ic) = Uac(Ic). Ic. Internal resistance Rint of the Chlorophytum-MFC is determined as the slope of the polarization curve (Fan et al. 2008). Indeed, at each

measurement Uac= OCV- Rint Ic which lead to Rin= dUac /dIc t. Internal resistance Rint is constant for the linear zone of the polarization curve. Internal resistance can also be obtained from the power curve from the notion that at maximum power the internal resistance is equal to the external resistance which leads to Rint = P/Ic2.

From September 2015 to July 2016 the circuit was closed using an external resistance with value R equal to the internal resistance (R = Rint) of the Chlorophytum-MFC and so the current Ic was measured as a time function. In addition, the power P was computed to evaluate and characterize the Chlorophytum-MFC performance. In our study, the current Ic was expressed as current density Ic/2S (as current per anode geometric surface area) and the power was computed as power density R Ic2/2S (as power per anode geometric surface area).

The plant development as well as the electrical output of the rhizospheric anodic Chlorophytum-MFC biofilm were co-monitored over time.

Nutrient agar was used for the total flora enumeration, and all dishes were incubated at 30°C for 24–48 h (Prescott, Harley, and Klein2010). The approximate number of bacteria per suspension volume was obtained by counting the isolated colonies on agar medium per dilution, which corresponded to 30–300 colonies, and was calculated using the formula UFC¼N

V F; (where V is the dilution volume, N is the

number of colonies and F is the dilution factor). All experi-ments were performed in triplicate and only the mean values were reported.

2.3. The photosynthesis and temperature effect on energy production

Photosynthesis and temperature effects on electrical energy production was highlighted by studying the day-night cycle, sunlight and temperature effects on the OCV produced. 2.3.1. Day-night cycle effect

Photosynthesis activity influence was carried out by record-ing the 24 hr data of three successive days and nights usrecord-ing a multimeter (Fluke) with an interface to measure Chlorophytum-MFC voltage during day and night circadian cycle.

2.3.2. Sunlight and outside temperature effect

Sunlight and outside temperature effect on the plant’s electro-generating activity was carried out by comparing METEONORM software data to the measured OCV from December 2014 to September 2015. METEONORM software is a climate database combined with a weather generator.

2.3.3. Soil temperature effect

To study the anodic temperature effect on the voltage pro-duced, a thermocouple had planted at the rhizosphere near the anode. OCV variations and soil temperatures were recorded as time functions during the 15th, 30th, 50th and 80th day starting December 2014.

Table 1.CDER potable water analysis.

Parameter Value Conductivity 863 µS/cm pH 7.8 Turbidity 1.9 NTU Nitrates <2 mg/L Sulfates 60 mg/L Bicarbonates 110 mg/L Chlorides 200 mg/L Calcium 42 mg/L Magnesium 13 mg/L Potassium 4 mg/L Sodium 102 mg/L Oxidizable materials 0.6 mg/L

Sulphite reducing 0UFC

E.coli 0UFC

Enterococci 0UFC

Coliform bacteria 0UFC

Al 0.1 mg/L

Cu <0.05 mg/L

Mn <0.05 mg/L

Fe 0.11 mg/L

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3. Results and discussion

3.1. OCV study with Chlorophytum-MFC

OCV is the maximum p-MFC potential found when no cur-rent flows. So the OCV does not measure the flow of electrical current produced by the plant, nevertheless, it can estimate the anodic and cathodic reagents activity on the electrodes surfaces (Salvin, Roos, and Robert2012).Figure 2shows the OCV evolution produced by the Chlorophytum-MFC from December 2014 to August 2015. The reliability study of our p-MFC was carried out by a comparison with the pot without plant. The OCVs are collected between 11 AM and 2 PM corresponding to maximum sunlight intensity time.

From the above graph, three-time areas were defined. The first area of 20 days revealed low OCV fluctuations due to the time required for the initial electroactive biofilm formation on the anode surface. Indeed, in p-MFCs, bacteria need time to colonize the electrodes. A phase during which bacteria should release hydrolytic enzymes used to increase the nutrients amount available and necessary for the plant growth (Logan

2008). This area gives a positive tension values up to 173 mV correlated with the beginning of first conventional stage of biofilm formation (Initial attachment). This stage concerns cells products adsorption (polysaccharides, phospholipids, pro-teins, and nucleic acids) on the anode surface, for the adhesion of the first electroactive planktonic bacteria layers during the bio-film formation (O’Toole, Kaplan, and Kolter 2000; Toutain, Caiazza, and O’Toole2004).

During second area: from day 20 to day 52, the recorded voltage increased up to 292 mV. This period corresponds to the consolidation stage and Extra-cellular Polymer Substances pro-duction for the biofilm maturation (Logan2008). After 52 days of activity, the voltage intensity dropped sharply and tended towards negative values, which may be due to a first bacterial detachment and allowed another planktonic bacteria species co-adhesion to the anode (Svensäter and Bergenholtz2004). The OCV increased After 70 days rapidly and reached a value of 351 mV, which was primarily due to the biofilm maturation and colonization of new

bacterial communities that catalyze the anode reactions (Rafrafi

2012; Svensäter and Bergenholtz2004).

After 120 days (third area), the values increased and reached maximum values of 1211 mV at August 2015 due to the main following reasons. First, sunlight intensity that favors photosynth-esis and roots development, which had led to higher organic material content released at the rhizosphere. Roots exudates are oxidized by rhizospheric bacteria and released thereby electrons operable by the Chlorophytum-MFC system to produce green electricity. Therefore, more organic material would have been available for electricity production and consequently a faster build-up of cell voltage (Helder et al.2012,2013).

The second reason could involve the electroactive biofilm formation, containing a great diversity of microorganisms responsible for the organic matter degradation and thus to electron transfer between anode and cathode and use the anode as electrons acceptor (Moqsud et al.2015; Sophia and Sreeja2017). In several studies, it has been demonstrated that the anode placement at different rhizospheric regions had influence on the electro-genesis where the maximum of the power output was observed with the anode placed near the root zone (Chiranjeevi, Mohanakrishna, and Mohan2012).

The rhizospheric microorganisms using root exudates are the key factor of mediating plant-microbe dialogues, form thereby the main basis for the bioelectricity genera-tion in an adequate system. It has been demonstrated in other studies that more the biofilm reaches maturity, the organic matter is rapidly oxidized and a large current amount is produced (Deng, Chen, and Zhao 2012; Moqsud et al.2014; Pierret et al.2007). However, because of the rhizosphere complexity and dynamism, understand-ing its ecology and evolution is difficult and thus requires additional and extensive research to support it (Moqsud et al.2015; Sophia and Sreeja 2017).

For the pot without a plant, a low voltage was recorded at the experiment beginning, due to the potential differ-ence between electrodes probably caused by the decom-position phenomenon of the organic matter remains existing in the soil (Deng, Chen, and Zhao 2012; Helder et al. 2013). A gradual voltage drop was noted over time for the cell without a plant and negative values were observed, which would due to the depletion of soil organic matter. The comparative study between p-MFC with and without plant makes possible to conclude that the Chlorophytum plant may represent a green fuel allowing a green electricity generation.

In our study, the maximum OCV of 1211 mV produced by Chlorophytum-MFC, was higher than one reported with sediment microbial fuel cell (Schamphelaire et al. 2008) where the maximum recorded was 700 mV, which was the highest result obtained so far in p-MFCs and MFCs research. Voltage produced with Glyceria maxima (Strik, Snel, and Buisman2008) had achieved peak of around 250 mV. Maximum voltage of 300 mV was produced using paddy-MFC (Kaku et al.2008). Around 350 mv from food industries wastewater (Khare and Bundela 2014) and 650 mV was obtained with Ipompoea aquatic p-MFC coupled at MFC using wastewater (Liu et al. 2013).

-600 -400 -200 0 200 400 600 800 1000 1200 1400 0 20 40 60 80 100 120 140 160 180 OCV (mV) Time (day) with Chlorophytum Without Chlorophytum

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3.2. System voltammetry study and Chlorophytum-MFC characterization

Polarization curves (respectively, power curves) depicted in

Figure 3a (respectively, Figure 3b) are very similar to those reported for other MFCs (Goto et al.2015; Logan et al.2006; Moqsud et al.2014,2013).

As depicted in the Figure 3a OCV increased with time from 45.41 mV to 900 mV, which reflects the anodic surface state time evolution (Goto et al.2015; Hubenova and Mitov

2012; Lu, Xing, and Ren2015). Indeed, at high voltages MFC system operation facilitated the activation of the anode-respiring bacteria and thereby stimulate the electrons trans-port from anode to cathode (Salvin, Roos, and Robert2012; Takanezawa et al.2010).

Also, in Figure 3a, a voltage drop was observed (voltage losses), starting from the OCV value, the potential Uac dropped rapidly when current Icincreased due to activation over-potentials (Azri et al.2018; Logan2008). It was followed by a slow and near-linear drop region characterized by a current dependent voltage loss. The remaining region pre-sent a nonlinear voltage loss related to mass transport limita-tion and concentralimita-tion polarizalimita-tion (Logan et al.2006, Logan, Microbial fuel cells2008). From the near linear region of the polarization curves, the internal resistances were computed as in 2.2, we get 173 KΩ, 102 KΩ, 62 KΩ, and 17 KΩ.

For each polarization curve inFigure 3athe maximums of current Icmaxwas measured and summarized inTable 2. The result showed increasing trend with a predictable resistance decrease which is consistent with the literature (Jang et al.

2004; Mohan et al.2008). Furthermore, based on the results of

Figure 3aandTable 2. We conclude that our reactor behaved like a typical fuel cell.

As highlighted in the power curveFigure 3b and for the first three curves (day 106, day 114 and day 122), despite the Chlorophytum-MFC powers increased over time during this period, it showed relatively low values (Table 2), which may be explained by a low electrolyte content in the fuel cell because of the initial acclimatization period and the insuffi-cient maturity of the anode electroactive biofilm. With the biofilm progressive maturation, the anolyte content increased, and the electrochemical

exchanges become more important (Hubenova and Mitov

2012), which has resulted in an increased power after 191 days reached a maximum value of 744 µW/m2.

Plant biomass heigh and anodic bacterial number were recorded over time (Table 2), which were proportional to OCV, current Icmaxand power Pmax, and were inversely pro-portional to the internal resistance Rint. This relationship is strongly due to increase of the root exudates availability for the electroactive anodic biofilm maturity, following the plant development (Hoagland and Williams 1985), which has resulted an electrolyte content increase in the Chlorophytum-MFC and had stimulated electrogenus activity and increased bio-current production (Hubenova and Mitov 2012, 2015; Paterson2003).

Microbiological analysis of Chlorophytum-MFC anodic biofilm in our previous work (Azri et al.2018) had shown microbial diversity, which had revealed the presence of Pseudomonas, Enterobacter and Bacillus genera and two fungi species (Table2). As demonstrated in several studies, the above-mentioned genus were isolated from several electroactive biofilm and have been studied for their bioelectroactivity. Therefore, they are becoming a reel tools in MFCs (Cournet et al. 2010; Liu et al. 2017;

Figure 3.Polarization (a) and power (b) curves of Chlorophytum-MFC at days: 106, 114, 122 and 191.

Table 2.Chlorophytum-MFC parameters.

Day OCV (mV) Icmax(mA) Pmax(µW/m2) Rint(KΩ) Plant biomass (Height cm) Anodic bacterial number (U/ml) Microbial anodic C-MFC (Y. Azri et al.2018)

106 45.41 0.000349 0.527 173 21 69.103 Pseudomonas putida

Pseudomonas spp1 Pseudomonas spp2 Aeromonas hydrophila

Enterobacter cloacae Bacillus tequilensis Aspergillus. sp

Penicillium. sp

114 64.78 0.0008 2.53 102 25 75.103

122 120.1 0.00115 4.62 62 30 88.103

191 900 0.037 744.98 17 42 110.103

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Lovley 2006; Lu, Xing, and Ren 2015; Rabaey and Verstraete 2005; Sheng et al. 2012). Indeed, it was shown that the complex and enriched microbial consortia are more effective and can produce 22% more power than pure culture (Ishii et al. 2008; Logan 2008; Schaetzle, Barrière, and Baronian 2008).

In p-MFC, the anodic biofilm composed of syntrophic consortium of cellulolytic, fermentative and electroactive bac-teria expand in order to degrade complex rhizodeposits which released at the plant roots via the photosynthesis during its development (Lu, Xing, and Ren 2015). The electricity gen-eration in the p-MFC is based on the oxidation of these organic compounds (rhizodeposits) by electrochemically active bacteria (EAB) used like carbon sources (Pinton, Varanini, and Nannipieri2007; Potter1911). Lipids, proteins, and carbohydrates can be also processed to supply organisms with carbon and energy. These organic substrates serve as electron donors for a redox reactions that result in the pro-duction of an energy carrier molecule (ATP) (Schaetzle, Barrière, and Baronian 2008).

3.3. Power and current densities generation of Chlorophytum-MFC at 66 KΩ

The current and power densities were calculated to evaluate the Chlorophytum-MFC performance. their variations were measured between terminal electrodes as time function for 120 days and represented in Figure 4a,b. The internal resis-tance was approximately 66 kΩ calculated from the relation-ship between the voltage and the current output.

The power and current densities kinetics registered in

Figure 4a,b, respectively, had shown two phases: first (1–64

days), where both of power and current waves were relatively low and waved around its mean. This phase corresponded to the autumn-winter period (September–February) where the temperature and lighting decreased, that had decreased the photosynthesis rate and thus affect rhizodeposits availability which reduced rhizospheric microbial activity and may had

caused electrogenicity decline at this phase (Helder et al.2013; Moqsud et al. 2015). At the second phase (64–100 days), previous power and current cycles were amplified to reach a maximum of 7.87 μW/m2 and 5.25 mA/m2 respectively. This phase corresponded to the spring-summer seasons (April–August) which represent an optimal photosynthesis rate with maximum lighting and temperature and thereby rhizodeposits availability that stimulate the rhizospheric microbial activity around the anode (Helder et al. 2013; Moqsud et al. 2015; Strik, Snel, and Buisman 2008; Timmer et al.2010).

The maximum values obtained were relatively low com-pared to the previous works results, where a power density of 67 mW/m2 had produced with G.maxima (Strik, Snel, and Buisman2008), rice paddy filed had produced 14,44 mW/m2 with current density up to 162 mA/m2 (Takanezawa et al.

2010), S. anglica had produced different powers in several studies where:100 mW/m2 (Timmer et al. 2010), 222 mW/ m2(Helder et al. 2010), 88 mW/m2in outside and 440 mW/ m2in lab-conditions (Helder et al.2013), E.crassieps (Mohan, Mohanakrishna, and Chiranjeevi 2011), which produced a bio-power of 222.93 mW/m2, C. indica giving a maximum current density of 105 mA/m2 (Lu, Xing, and Ren 2015), L. valdiviana reaching current output of 226 mA/m2(Hubenova and Mitov2015), L. perenne with a production equal to 55 mW/m2(Oon et al.2015), C. stuttgart showing power densitie of 222 mW/m2 (Sophia and Sreeja 2017) and weeping Alkaligrass plant Pucinellia distans (Khudzari et al. 2018) giving average power of 12.78 mW/m2 and maximum of 83.7 mW/m2.

The high power and current densities obtained in previous works were often due to the electrochemical use of catalysts and cation exchange membranes for optimizing electrochemi-cal exchanges within the p-MFC which increase thus bioelec-tricity efficiency (Helder et al.2010; Sophia and Sreeja2017). Therefore, the low densities obtained in the present work may due to the high soil resistance used as a support for p-MFC, that may limits electron transfer between anode and cathode.

0 1 2 3 4 5 6 7 8 9 0 15 30 45 60 75 90 105 120 135 m/ W µ( yti s ne d re w o P 2) Time (days) 0 1 2 3 4 5 6 0 15 30 45 60 75 90 105 120 135 Curr ent density (mA/m 2) Time (days) (b) (a)

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Indeed, the internal resistance in the present work was much greater than that reported in previous works using graphite felt and graphite granules as a p-MFC support (Helder et al.

2010; Timmer et al. 2013) that are electrochemically active, having a lower resistance and are therefore current conduc-tive, comparing to soil which is electrochemically inactive. So that, if the support strength was less important as in the graphite granules and felt cases, the p-MFC would have greater densities (Goto et al. 2015; Jang et al. 2004; Kaku et al. 2008; Liu et al. 2013; Mohan et al. 2008; Takanezawa et al.2010).

Furthermore, the photosynthetic pathway can be decisive in power production. Chlorophytum comosom is classified in the C3 pathway, which can explain the densities values obtained in the present work. In general, the C4 pathway has highest photosynthesis efficiency than the C3 pathway to convert solar energy into bioelectricity because of their rhizodeposition importance (Helder et al.2010, Wang et al.

2012a). However, some research has shown that some C3 species had exhibit higher efficiency than C4 plants (Helder et al. 2010)

In the literature, there are not enough available reports on the photosynthetic role for p-MFC system performances. In addition, the system performances are often affected by several parameters including the p-MFC design, the rich-ness and nature of the electroactive biofilm composition, electrode materials, and plant growth supports, operating conditions. These parameters can differ from one system to another. Therefore, to compare p-MFC performances, the bioelectricity yield, they must be studied in identical system under the same operating conditions and at the same time. (Deng, Chen, and Zhao 2012; Helder et al. 2012, 2010; Klaisongkram and Holasut 2015; Nitisoravut and Regmi

2017; Timmer et al. 2012).

3.4. Photosynthesis influence on the OCV 3.4.1. Day-night cycle effect on OCV fluctuation

Most of the living plants set CO2and release a wide range of organic matters through roots into rhizosphere via photo-synthesis process (Paterson2003). In p-MFC, electrochemical active bacteria catalyze the rhizodeposits anaerobic oxidation, releasing electrons at the anode, which migrate to the cathode where oxygen is preferably reduced to give water. This process leads to generate electrical energy do not need to plant har-vesting. Root exudation appears to be currently the energy production-limiting factor in p-MFCs (Timmer et al.2013)

To study the photosynthetic effect on the potential fluctua-tions, the Chlorophytum-MFC 24 h OCV data were recorded for three consecutive days and nights. The obtained measure-ments reflect the day-night cycle influence on electrogenic activity (Figure 5).

OCV kinetics depicted in Figure 5 showed that: at the daylighting start (sunrise), a marked electrogenous activity increased was recorded with a maximum voltage between 14 and 15 h, that exceeded 328 mV and had fallen to 192 mV during the night for the three studied nights. In the diurnal cycle, OCV fluctuations were caused by light and temperature variations (Moqsud et al.2015).

Indeed, electrogenic activity decreased in the evening and the fall continued until the morning, when the light and temperature decreased (between 18 h and 7 h) and consequently at the photosynthetic activity decrease (Chiranjeevi, Mohanakrishna, and Mohan2012; Helder et al.2013). Inversely, the photosyn-thetic process begin with relatively important temperature and light intensity affected the Chlorophytum-MFC electrogenous activity via the root exudates releasing and the rhizospheric microbial metabolism activation (Husain and McKeen 1963; Rovira1959; Vančura1967).

Figure 5.OCV fluctuations according to the day/night cycle of three successive days.

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Low OCV was recorded over the three nights, suggesting that the voltage generation depended highly on direct sun-light. However, low OCV production continues overnight where the Chlorophytum-MFC uses the illuminated-phase products of the photosynthesis (root exudations) for the dark phase process (Neumann and Römheld 2007). It also can means that the Chlorophytum-MFC has a battery equiva-lent built into its system (bio-battery) (Helder et al. 2010). Tension fluctuation during the night may be due to the oxy-gen concentration, which would be too low with the plant reactions in the dark phase. Swift decline of voltage was observed but it was gradually increased as the photosynthesis and oxygen rates increased during day times. Oxygen served as electron acceptor on cathode side in this mechanism (Helder et al. 2010, 2013). The oxygen concentration increased had tremendously increased the voltage outputs. Low concentration of oxygen during dark reactions would adversely be affected OCV generation (Gilani et al.2016). In addition, OCV decrease may be owed to an oxygen reduction at the cathode surface (Sheng et al. 2012) due to the algae development at the cathode surface. The algae produce oxy-gen during the day and consume it during the night, thus causing tensions fluctuations between day and night (Helder et al.2013; Strik, Snel, and Buisman2008).

3.4.2. Sunlight and outside temperature effect on OCV production

Temperature is one of the most abiotic factors that can limit the photosynthetic performance (Ashraf and Harris 2013; Oliveira and Peñuelas 2005). Photosynthesis rate increases with outside temperature, which implies plant growth and rhizospheric biomass increase (Gupta et al. 2016). Average solar radiation available in north Algeria is 4.6 KWh/m2/day (Yaiche et al.2014), allows the photosynthesis rate increase, which facilitates rhizodeposition for microorganisms and bioelectricity production.

The average global cumulative horizontal radiation and exter-nal temperature data obtained with METEONORM software for each month from December 2014 to September 2015 were exploited to made comparison between meteorological para-meters and OCV measurements (Figure 6), allowed studying sunlight and outside temperature effect on the Chlorophytum-MFC‘s electro-generating activity as presented.

Results of Figure 6highlight that OCV variation was pro-portional to solar radiation and outside temperature and all histograms had the same trend line. From December 2014 to June 2015, voltage released increased with temperature and radiation increasing. In July, when a temperature peak of 35°C and a maximum radiation about 302.4 KWh/m2 were

0 5 10 15 20 25 30 35 40

dec 14 jan 15 feb 15 mars-15 apr 15 may 15 june 15 jul 015 aug 15 sept-15

Maximum average temperatur

e

(C°) (a)

dec 14 jan 15 feb 15 mars-15 apr 15 may 15 june 15 jul 015 aug 15 sept-15

Solar radiation (kWh/m²) (b) -100 100 300 500 700 900 1100 1300

dec 14 jan 15 feb 15 mars-15 apr 15 may 15 june 15 jul 015 aug 15 sept-15

OCV

(mV)

(c)

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recorded, OCV reached the maximum value of 960 mV com-pared to the previous month with a voltage of about 335 mV. OCV proportionality to solar radiation and temperature would strongly due to the rhizospheric medium enrichment by the photosynthesis organic compounds (Kaku et al. 2008), which stimulated the selective rhizospheric biofilm development that degrade as the roots exudates for electrons donation and thus improved the cathode and anode catalytic activity (Helder et al.

2013; Liu et al.2013; Timmer et al.2012).

However, during the winter period (December–March), when the temperature doesn’t exceed 15°C and low radiation was recorded about maximum of 128 KWh/m2, OCV was relatively low [−70 mV, 280 mV]. At the rest-winter period, the solar radiations and the temperatures fall, and the plant enters in its rest-winter period, where plant growth and meta-bolic activities are slowed down because the meristem stops dividing during this period. During this season, most plants do not need a lot of water and thus minimize their vegetation to store and conserve the maximum energy in the roots, thus decreased the rhizospheric microbial activity which strongly depends on the rhizodeposits availability (Havranek and Tranquillini 1995; Paul and Kumar 2011). Consequently, that may had caused the electrogenicity decline (Moqsud et al.2015).

During active growing months, the plant completed its winter dormancy period and resumed its root and leaf growth (spring). Each plant uses the photosynthesis process to change carbon dioxide, water, and some inorganic salts into carbohy-drates and thereby exchange electrons between its aerial part and the rhizosphere. This may explain the increase in the current voltage recorded during this period (March– August). Implying that electrogenic activity would depend on the seasons and so on the photosynthesis and rhizodepo-sits availability that stimulate the rhizospheric microbial activ-ity around the anode (Paul and Kumar 2011; Moqsud et al.

2015; Wang et al. 2012a).

Proportional relationship between voltage and solar radia-tion indicates that solar radiaradia-tion can be considered as a significant for Chlorophytum-MFC since it influenced directly the photosynthesis rate. Furthermore, during the photosynthesis process, the plant continuously produces organic matter through root during its life cycle (Strik et al.

2011). Root exudates are highly degradable to rhizospheric microorganisms which are the most responsible for electron releasing and produce electricity in Chlorophytum -MFC (Deng, Chen, and Zhao 2012; Gilani et al. 2016; Helder et al.2013; Liu et al.2013).

3.4.3. Soil temperature effect on OCV

Several factors determine the bacterial community of a soil, its structure (Wakelin et al. 2008), its texture (Sessitsch et al.

2001), its pH (Lauber et al. 2009) as well as the nitrogen availability (Frey et al. 2004). Soil undergoes continuous redox reactions (Vepraskas and Faulkner 2001) and apart from organic decomposition, the inorganic material present in the soil can affect the redox potential (Patrick1981). Soil can produce electrons by chemical decomposition of sulfur species, humic acid and iron (II) (De Schamphelaire et al.

2008; Meek and Chesworth 2008). In the p-MFCs, the soil

naturally with its microbial world, plays an important role in the electricity production. Therefore, developing the best p-MFC system requires a good understanding of soil role in bioelectricity production.

To study soil temperature effect on OCV production, a thermocouple had planted at the rhizosphere near the anode. OCV and soil temperature were recorded as time function, at the 15th-30th-50th and 80th day starting December 2014.

As highlighted in Figure 7, temperature increased during the day and decreased after 14 h, the same OCV profile was recorded. When the temperatures were approximately 13°C for the 15th and 50th day, OCV did not exceed 80 and 65 mV, respectively, unlike the 30th and 80th day, the OCV reached, respectively, 280 and 370 mV for a temperature of 18°C. The bioelectric potential increased when the temperature increase, this is mainly due to the anodic microbial activity stimulation, which is highly sensitive to the environment temperature. So the temperature influences significantly their reproduction as well as their metabolism by intervening in the catalysis of many enzymes (Mezrioui and Baleux 1992; Moqsud et al.

2015). Consequently, temperature influence electron transfer which is taking place from reduced mediators towards the anode and migrate to the cathode (Helder et al.2013; Strik, Snel, and Buisman 2008). When temperature dropped, the OCV decreased because ions and electrons were hardly trans-ported towards anode and cathode (Hayhoe and De Jong

1988; Kaku et al. 2008; Lu, Xing, and Ren 2015; Lundin and Johnsson1994; Nitisoravut and Regmi2017).

Electroactive biofilm performance as well as its formation time on the electrode surface are processes that strongly depend on incubation and operating temperatures, thus influ-enced voltage which considered as an activity electrocatalytic measure (Aelterman et al.2006; Patil et al.2010).

It was shown by (Patil et al.2010) that biofilms are active in a temperature range of 5°C to 45°C. Biofilms grown at high incubation temperatures are electrochemically more active than those cultured at lower temperatures but with higher (50°C) and lower (0°C) temperature limits defining the opera-tional limits of a microbial fuel cell or microbial biosensor and similar electrochemical transfer characteristics.

4. Conclusion

In the present work, Chlorophytum-MFC fed with CDER garden soil had presented specificities justifying its study choice and may own a rich and interesting microbial rhizospheric flora for the electrochemically active biofilm formation.

Chlorophytum-MFC had an electrogenous activity clearly proportional to the soil and climate temperatures as well as to sunlight intensity and it had behaved like a typical fuel cell via the polarization and power curves studies.

Chlorophytum-MFC system study with natural light inten-sity indicates that the Chlorophytum ornamental plant photo-autotrophically developed can generate electricity but the values are still low compared to other researches. However, in order to optimize the bioelectricity production yields via Chlorophytum-MFC further studies and researches are

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required to better understand the electrochemical process responsible for electronic exchanges.

Chlorophytum-MFC can be optimized by replacing or modifying the battery support (soil), using a soil richer in organic matter (compost, for example), airier, having a lower system resistance and ensuring control of climatic conditions which proves to have a major impact on the production of bioelectricity, and also by increasing the electrode work sur-face and optimizing the electroactive microbial system.

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Figure

Figure 1. Experimental plan.
Table 1. CDER potable water analysis.
Figure 2. OCV evolution with Chlorophytum-MFC during 160 days.
Figure 3. Polarization (a) and power (b) curves of Chlorophytum-MFC at days: 106, 114, 122 and 191.
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