Abstract

Sediment microbial fuel cells (SMFCs) are bio-electrochemical devices generating electricity from redox gradients occurring across the sediment–water interface. Sediment microbial carbon-capture cell (SMCC), a modified SMFC, uses algae grown in the overlying water of sediment and is considered as a promising system for power generation along with algal cultivation. In this study, the performance of SMCC and SMFC was evaluated in terms of power generation, dissolved oxygen variations, sediment organic matter removal and algal growth. SMCC gave a maximum power density of 22.19 mW/m2, which was 3.65 times higher than the SMFC operated under similar conditions. Sediment organic matter removal efficiencies of 77.6 ± 2.1% and 61.0 ± 1.3% were obtained in SMCC and SMFC, respectively. With presence of algae at the cathode, a maximum chemical oxygen demand and total nitrogen removal efficiencies of 63.3 ± 2.3% (8th day) and 81.6 ± 1.2% (10th day), respectively, were observed. The system appears to be favorable from a resources utilization perspective as it does not depend on external aeration or membranes and utilizes algae and organic matter present in sediment for power generation. Thus, SMCC has proven its applicability for installation in an existing oxidation pond for sediment remediation, algae growth, carbon conversion and power generation, simultaneously.

INTRODUCTION

Sediment in aquatic environments resembles soil in terrestrial environments as both serve as a source of nutrition to the fauna and flora thriving in that ecosystem. Even though they play a key role in the environmental food cycle, they are the primary catalyst responsible for the dynamics of water quality of the overlying water. The sediment surface layer contains a significant amount of nutrients, such as organic matter, nitrogen, and phosphorus, which threatens the integrity of an ecosystem (Beg et al. 2001). The United States Environmental Protection Agency (USEPA 2017) lists sediment as the most common pollutant in rivers, streams, lakes, and reservoirs. As already mentioned, sediment in stream beds can destroy the habitat of organisms and affect the fish population, which in turn disrupts the natural food chain. Also, algal bloom as a result of nutrient transport cannot be ignored. Hence, these examples emphasize the need for the development of a cost effective technology for sediment remediation.

A microbial fuel cell (MFC) can generate electricity by using bacteria as catalyst to oxidize organic and inorganic matter at the anodic side (Logan et al. 2006). A sediment microbial fuel cell (SMFC) is a modification of MFC where oxygen is available in the overlying water and, at the cathode, oxygen reduction occurs to complete the circuit by reducing it to water (Wang et al. 2014). Thus, oxygen availability is one of the major factors that govern the performance of SMFC. Unlike most MFCs, which contain a membrane to separate the compartments of the anode (where oxidation takes place) and the cathode (where reduction takes place), SMFCs can function without membranes. SMFC can have better application in natural water bodies, if it could power small autonomous devices, but here the low power generation has become a major challenge. Several researchers have paid attention to overcome this challenge. Yuan et al. (2010) came out with the concept of tubular air cathode MFC, which gave a maximum power density of 107 mW/m2; however, Chen et al. (2017) reported a maximum power density of 562.7 mW/m2 using MnO2/polypyrrole catalyzed cathode. Challenges, including high internal resistance of the sediment, question its application as a feasible and cost effective power source. Hence, there is a need for exploiting various other possibilities to make it an energy efficient system. Sediment remediation, mitigation of the aquatic water pollution, algal cultivation, etc., are some of these possibilities.

In a sediment microbial carbon-capture cell (SMCC), requirement of oxygen supply is fulfilled by utilizing the oxygen production potential of algae through photosynthesis. The reactions are as follows:

At anode:  
formula
(1)

At cathode:

Photosynthetic reaction:  
formula
(2)
Reduction reaction:  
formula
(3)

In SMCC, the external aeration system is replaced by algae, a low-cost oxygen producer, which in turn helps in reducing operating cost and contributes to enhancing performance. A previous study on SMCC has reported a maximum power density of 16 mW/m2 using graphite felt electrode and 38 mW/m2 using graphite felt-multi-walled carbon nanotubes (GF-MWNT) (Wang et al. 2014). Whereas a study performed using a rotating cathode for increasing oxygen availability gave a higher power density of 49 mW/m2 (He et al. 2007).

Even though nitrogen contaminated water released into the water bodies can cause serious the problem of eutrophication, deterioration of water quality, etc. (Sumino et al. 2006), such contaminated water can be wisely utilized to cultivate algae. In the aquaculture pond, removal of nitrogen, which exists in the inorganic form as ammonium nitrogen , nitrite nitrogen , nitrate nitrogen , as well as organic nitrogen, is an important aspect. Algae have the ability to take up nitrogen in inorganic form as , , NO or and also organic form like urea (Markou et al. 2014). The role of sediment and its overlying water as nutrient source has thrown light on the advantage of using pond sediments rather than culture media for algal cultivation in a pond system, thereby further making it less expensive than a photo-bioreactor.

In this study, SMFC was modified by culturing algae in the overlying water on the cathode side and it was operated without using any expensive electrode catalyst, membrane or aerator system. A comparative evaluation was carried out in this study with algae and without algae at the cathode side with emphasis laid on sediment remediation and pond water pollution mitigation. Further, efficiency of SMCC in generating electricity was evaluated. In addition, the influence of algal growth on organic matter removal in terms of chemical oxygen demand (COD) reduction and nitrogen removal efficiency was analyzed. The effect of concentration of dissolved oxygen (DO) on voltage generation was evaluated, taking into account the light and dark cycle.

MATERIALS AND METHODS

Construction of SMCC and SMFC

Two identical configuration SMFCs, made from a poly-acrylic column with 9 cm inner diameter and 120 cm height making a total volume of 7.6 L, were used in this study. Each SMFC was filled with sediment collected from a working aquaculture pond up to a height of 40 cm from bottom and further 65 cm height was filled with effluent of the pond. Pre-cultured algae were added in overlying water to one of the SMFC to make it SMCC and the other one was operated without algae as control. Anodic and cathodic zones had a working volume of 2.54 L and 4.1 L, respectively. Figure 1(a) and 1(b) show the experimental set-up and photograph of the SMCC used in this study, respectively. Graphite plates, having length of 10 cm and width of 5 cm (total projected surface area of 100 cm2), was used as anode material, considering its material strength, inertness and commercial availability (Girguis et al. 2010). Non-catalyzed carbon felt (Panex_35 Zolex Corporation), with a length of 10 cm and width of 9 cm (total projected surface area of 180 cm2), was used as cathode material considering its larger specific surface area, that assists in a better algal cell attachment (Wu et al. 2013). The anode and the cathode were connected with concealed copper wire through an external load of 1,000 Ω in both SMFC and SMCC. A three-layered axial stirrer (80 rpm) was provided in the cathodic zone for the uniform mixing of the three phases, namely algae (solid), culture media represented here by the pond overlying water (liquid), and the gas formed as a result of sediment degradation and that was produced by algae (gas). The cathode was placed vertically in the overlying water and the anode was immersed in the sediment at a distance of 50 cm and 15 cm, respectively, from the sediment–water interface. A free board of 15 cm was provided above the cathodic zone of both SMCC and SMFC. In addition, the anodic side of SMCC was painted black to prevent the growth of microalgae.

Figure 1

(a) Experimental setup of SMCC and (b) photograph of SMCC used in this study.

Figure 1

(a) Experimental setup of SMCC and (b) photograph of SMCC used in this study.

Microbial strain, media, and growth conditions

The mixed microalgae culture used in this experiment was collected from an irrigation canal near Indian Institute of Technology, Kharagpur, India, and pre-cultured in an illuminated autoclaved Erlenmeyer flask containing BG11 media on a 12:12 h light:dark cycle, using 2000 Lux fluorescent light. The concentrations of nutrients (BG11) were (per liter of deionized water): 1.5 g NaNO3, 0.04 g K2HPO4, 0.075 g MgSO4.7H2O, 0.036 g CaCl2.2H2O, 0.006 g citric acid, 0.006 g ferric ammonium citrate, 0.001 g EDTANa2, 0.02 g Na2CO3 and 1 mL trace metal solution. The trace metal solution consisted of (per liter of deionized water): 2.86 mg H3BO3, 1.86 mg MnCl2.4H2O, 0.22 mg ZnSO4.7H2O, 0.39 mg Na2MoO4.2H2O, 0.08 mg CuSO4.5H2O, and 0.05 mg Co (NO3)2.6H2O (Zhou et al. 2012).

SMCC inoculation: sediment, algae and overlying water

Pond sediment sample was collected from a working aquaculture pond in IIT Kharagpur, cultivating fish: Rohu, Catla and Mrigal with stocking density of three fish per m2 and it was found to have an organic matter content of 5.8%. The study relied on the natural bacterial inoculum present in the sediment and therefore no external inoculation was done. This sediment was filled at the bottom of the SMCC and represented the anodic side. The column above sediment zone was filled with water taken from the working aquaculture pond and the performance of SMCC was also monitored on the basis of change in water quality parameters such as DO, pH, , and COD. Algae, pre-cultured in BG11 media, were transferred in the cathodic zone of SMCC; however, no algae were added to the control SMFC.

SMCC operation

At the anodic side, microbial activities in sediment produce electrons by oxidation of organic matter and then the electron captured by anode flow through external circuit to the cathode. Further, degradation of organic matter results in the release of certain gases such as NO2, H2S, NH3, CH4, and CO2 (Chau et al. 1977), which diffuses into the cathodic zone. At the cathodic side, the electrons combine with the protons and the oxygen (electron acceptor) to form water. The oxygen helping in this process is produced by the algae through the process of photosynthesis. Also, CO2 from the anode reaches the cathodic side and acts as carbon source for algal growth. The control SMFC was operated without microalgae in the cathodic side, keeping all other conditions the same. The experiments were conducted in four cycles of 15 days each and the algae cells were replaced after each cycle.

Analytical measurements and calculations

Electrochemical analysis

The SMFC and SMCC were continuously monitored for voltage produced using a data acquisition unit (Agilent Technologies, Malaysia) across a fixed external resistance (Rext) of 1,000 Ω (unless stated otherwise) and current (I) in amperes (A) was calculated from Ohm's law (I = Ecell/Rext), where Ecell is the potential drop in volts (V) across external load resistance (R, Ohms). The overall performance of the SMCC and SMFC was evaluated through power output (P, Watts) according to Equation (4).  
formula
(4)
The maximum power density was obtained from polarization curve plotted by varying the external resistances from 10,000 to 100 Ω using resistance box (GEC05R Decade Resistance Box, Bangaluru, India) over a fixed time interval until a stable voltage was achieved. Because in the present study, the cathodic reaction is thought to limit the overall power generation, the power density (Pcat, mW/m2) was therefore normalized to cathodic surface area (Acat) as per Equation (5).  
formula
(5)

The internal resistance was calculated from the slope of linear portion of voltage vs. current curve (Logan et al. 2006).

Measurement of sediment organic matter

The percent weight of organic matter in sediments was determined by loss on ignition (LOI) method, which is based on sequential heating of the samples in a muffle furnace (Heiri et al. 2001). LOI was calculated using Equation (6).  
formula
(6)
where W105 represents dry weight of the sample before combustion and W550 represents the residual weight of the sample after heating at 550 °C.

Measurement of algal growth

Algal dry weight was determined by centrifuging 20 mL of algae solution and drying the pellet at 70 °C in hot air oven until getting a constant weight. The biomass productivity (P, mg/L·d) was calculated by Equation (7) (Ho et al. 2012).  
formula
(7)
where, ΔX is the variation of biomass concentration (mg/L) within a cultivation time ΔT (day).

Surface morphology of the cathode containing attached algal biofilms was studied by scanning electron microscopy (SEM, Zeiss Merlin Gemini II, Germany). The samples were fixed in 2.5% paraformaldehyde solution for 3 h at 4 °C and then washed three times in a phosphate buffer solution. The samples were then washed by stepwise dehydration in a gradient series (50%, 70%, 80%, 90%, and 100%) of water/ethanol solutions (v/v) and dried. The samples were finally coated with Au/Pt coating before SEM observation (Wang et al. 2014).

Water quality analysis

The DO, pH, and conductivity were measured using digital water quality bench meter (Thermo Scientific Inc., USA) at a temperature around 25 °C. The collected samples of overlying water from the cathodic side were centrifuged at 5,000 rpm for 15 min and the supernatants were collected for COD analyses. The COD was determined by closed reflux colorimetric method at a calibrated standard wavelength of 600 nm using a spectrophotometer (T80 UV/VIS Spectrophotometer, PG Instruments Ltd, Leicestershire, UK). The titrimetric method was followed to determine the ammonium nitrogen concentration using Kjeldahl apparatus (APHA 2012).

RESULTS AND DISCUSSION

Electricity generation and polarization behavior

A SMFC can produce energy in the form of readily usable electrical power and this can be considered as one of its direct applications for powering onsite devices (De Schamphelaire et al. 2008). The electricity generation in both SMFCs was observed from the starting of each cycle by measuring the operating voltage (OV) and open circuit voltage (OCV). Maximum OV of 172 mV and 74 mV and average OCV of 687 ± 4 mV and 427 ± 2 mV were observed in the SMCC and control SMFC, respectively. After observing a stable performance, the polarization behavior was examined by changing applied external resistances ranging from 10 kΩ to 100 Ω. The SMCC showed a better performance compared to control SMFC (Figure 2). A maximum power density, with respect to cathode surface area, of 22.19 mW/m2 was achieved with an external resistance of 1,000 Ω. This power density observed was higher than an earlier study with sediment containing less LOI giving a power density of 2 mW/m2 (Rezaei et al. 2007). A better power of 38 mW/m2 was obtained using carbon nano-tube coated cathode by Wang et al. (2014) and 48 mW/m2 using rotating cathode by He et al. (2007), which was mainly due to the cathode modifications. In the present study, control SMFC exhibited power density of 6.03 mW/m2 at an external resistance of 1,000 Ω. For a linear portion of the polarization curve, the value of the internal resistance (Rint) was obtained and the internal resistance of SMCC was estimated as 1,150 Ω; whereas the internal resistance of SMFC was 1,821 Ω.

Figure 2

(a) Power density and (b) polarization curves of SMCC and SMFC.

Figure 2

(a) Power density and (b) polarization curves of SMCC and SMFC.

For cathode performance, oxygen availability is a major limiting factor. The performance of SMCC can be explained by the difference in cathode performance observed as a result of photosynthetic oxygen production from algae. The organic matter content of sediment is another limiting factor for performance of SMCC and higher organic matter content in sediment can be considered as a major cause for an increase in power when compared to studies using sediment with lower organic matter. Hence a maximum sustainable power output of 22.19 mW/m2 could be attributed to both the algae and sediment for better oxygen production and higher organic content, respectively. Whereas the lower performance in terms of power generation compared to some other studies can be attributed to factors including the size of SMCC, its higher internal resistance, greater electrode spacing, and at the later stage, the algal growth inhibition due to limited bacterial metabolism because of depletion of organic matter.

Water quality remediation

Organic matter removal

The overlying water in the beginning of each cycle had a COD in the range of 103–107 mg/L. It decreased by about 63.3 ± 3.2% on 8th day after which it was observed to increase (Figure 3). Microalgae can grow under phototrophic condition in which they use CO2 as carbon source; however, microalgae can also grow under heterotrophic condition by utilizing the dissolved organic carbon like acetate, sugar, and organic acids (Borowitzka 1998). This could be the reason for a more or less similar pattern observed in both COD removal efficiency and algal growth curve (Figure 3). A sharp increase in the COD removal efficiency was observed after the algal lag growth phase was over and a decreasing pattern was observed later on when the stationary growth phase was reached. Comparatively less removal during initial days might have been caused by initial slow growth, observed due to the requirement of acclimation of algae to the new environment and also because of carbon limitation due to slow rate of organic matter degradation from sediment. The reason for decrease in COD removal later on is likely due to the die-off of some fraction of algae, which was evident from the color change (green to pale yellow) observed in the cathodic side. A decrease in removal efficiency and an increase in oxygen demand can be justified by considering the COD contributed due to the dead algal cells and its oxygen demand which was evident in the DO variation studies (discussed later).

Figure 3

Effect of algal growth on COD and removal efficiency.

Figure 3

Effect of algal growth on COD and removal efficiency.

Ammonium nitrogen conversion

Ammonium nitrogen in the overlying water was measured daily during each cycle. Initial concentration was in the range 1.1–2.3 mg/L. Highest conversion efficiency of 81.6 ± 1.2% was observed on 10th day of the cycle. Figure 3 illustrates the observed trend of ammonium nitrogen conversion and its similarity with the algal growth curve. is the main fraction of nitrogen (N) in the sediment and is released to the overlying water via molecular diffusion, convection and re-suspension (He et al. 2015). Normally there are three mechanisms for removal: microalgae uptake, conversion to nitrate and ammonia volatilization due to elevated pH, among which direct assimilation by algae is the main mechanism (Delgadillo-Mirquez et al. 2016). In a study by Dalrymple et al. (2013) on nutrient uptake by algae, it was reported that the removal of ammonium nitrogen was above 70%, while total nitrogen removal was less than 50%. Hence, this study was concentrated mainly on removal of ammonia nitrogen rather than total nitrogen. For the first few days, the nitrogen removal was probably lower due to the adaption phase of algae to the new environment. A previous study has reported that the nitrate uptake rate of algal cells decline as the culture becomes dense and approaches the stationary phase (Hu et al. 2000). As algae are mainly responsible for the removal of the released from the sediment in the overlying water, hence slow growth of algae can affect the removal of released from the sediment over time.

Organic matter removal from sediment

The initial LOI of 5.8% got reduced to 1.3% and 2.1% after 45 days of operation in SMCC and SMFC, respectively. Thus, an organic matter removal from sediment of 77.6% and 64.2% was observed in SMCC and SMFC, respectively. Availability of high DO near cathode for supporting reduction reaction at higher rate can be the reason for a better removal of organic matter in SMCC. As such, SMFC can maintain an oxidized layer at the bottom of the pond that can prevent diffusion of toxic compounds into overlying water, favoring algal growth (Sajana et al. 2013). Improved cathodic reactions in SMCC support higher oxidation rates in sediments and helped in maintaining improved oxidized layer at the bottom sediment.

Algal growth

In SMCC, 0.2 g/L of pre-cultured algae was added to the catholyte. As seen in Figure 3, an initial lag phase was observed due to time required for algae to adapt to the new environment. It was followed by an exponential growth phase. At the end of the exponential growth phase, a maximum dry weight of 0.8 g/L was achieved. Later on, the growth was observed to decline after stationary phase. This change can be linked to the increase in oxygen content in the catholyte, i.e. overlying water. Gas exchange is one of the important factors that affect the productivity of algal culture. Supply of carbon source, CO2, is an important issue in algae production and equally important is the removal of oxygen generated to prevent it from inhibiting algal growth (Lee & Palsson 1994). This will not be a problem for the field SMCC as it will not be a closed system. However, the sudden transition to the stationary phase and then to death phase could also be the result of limited availability of carbon due to reduction in the rate of organic matter oxidation from bacterial metabolism.

DO variations

Monitoring the DO concentration variation has led to a conclusion that voltage and DO exhibited a similar trend (Figure 4). Algae, the oxygen producer, has contributed to a highest DO of 14.2 mg/L in the catholyte of SMCC and remained more or less same throughout the exponential phase of algal growth curve. A slight decrease in DO was observed later on while going through the stationary phase. On the contrary, DO level of SMFC followed a constantly decreasing trend throughout the cycle and the voltage change reflected more or less the same pattern (Figure 4). It is evident from the study that voltage has a positive correlation with DO.

Figure 4

Variation of voltage with DO: (a) SMCC and (b) SMFC.

Figure 4

Variation of voltage with DO: (a) SMCC and (b) SMFC.

During the light phase of the study oxygen concentration increased due to photosynthesis and during the dark phase respiration started resulting in decreasing oxygen concentration. This variation in DO concentration was studied for 200 h and showed an up and down pattern (Figure 5) of DO concentration. Correlating this fluctuation with the above voltage-DO relationship, a chance for voltage fluctuation cannot be neglected. This can be one of the major limitations for power production during practical application of SMCC.

Figure 5

Variation in DO during the light and dark phase of SMCC.

Figure 5

Variation in DO during the light and dark phase of SMCC.

Electrode characterization

Surface morphology image of the carbon felt (cathode, SMCC) was developed by scanning electron microscope. Figure 6 shows the typical SEM images, which revealed the presence of dense algal biofilm on the electrode surface. As the thickness of the biofilm increases with time, limitation of oxygen diffusion occurs (Behera et al. 2010) and results in a decrease in voltage towards the end of the cycle. Rough texture and high surface area of graphite felt gave way to an increased attachment of algal cells on electrode.

Figure 6

SEM images: carbon felt with attached algal cells at different magnification: (a) 300 nm, (b) 2 μm, (c) 20 μm, and (d) 200 μm.

Figure 6

SEM images: carbon felt with attached algal cells at different magnification: (a) 300 nm, (b) 2 μm, (c) 20 μm, and (d) 200 μm.

CONCLUSIONS

Availability of a high concentration of DO near the cathode enhanced oxygen reduction reaction, thus resulted in 77.6% removal of organic matter from sediment in SMCC, which was superior to that observed in SMFC without algae in overlying water. When algae were added to the catholyte of SMFC, the maximum power density observed was 3.6 times higher than that produced without it. Along with sediment remediation, a COD removal efficiency of 63.3% and ammonium-nitrogen removal of 81.6% was observed from the overlying water. As microalgae are proved to be a good raw material for biodiesel production, further studies can be done on harvesting and lipid extraction from microalgae. These results gave way to the conclusion that SMCC can come out as a cost-effective system with multiple advantages of energy production and reclamation of pond water. The major problem observed with SMCC was the decreased algal life time, which was mainly due to limited nutrient supply. In field scale application of the system, this effect will not be a problem as there will be nutrients in abundance. To verify this situation and other effects mentioned, studies on scaled up systems would be useful.

ACKNOWLEDGEMENT

The research project was supported by the Department of Biotechnology, Government of India (BT/EB/PAN IIT/2012) providing the financial assistance.

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