Download Production of Electricity from Proteins Using a Microbial Fuel Cell

Production of Electricity from Proteins
Using a Microbial Fuel Cell
Jenna Heilmann, Bruce E. Logan
ABSTRACT: Electricity generation was examined from proteins and a
protein-rich wastewater using a single chamber microbial fuel cell (MFC).
The maximum power densities achieved were 354 6 10 mW/m2 using
bovine serum albumin (BSA) and 269 6 14 mW/m2 using peptone (1100
mg/L BSA and 300 mg/L peptone). The recovery of organic matter as
electricity, defined as the Coulombic efficiency (CE), was comparable to that
obtained with other substrates with CE 5 20.6% for BSA and CE 5 6.0%
for peptone. A meat packing wastewater (MPW), diluted to 1420 mg/L
chemical oxygen demand, produced 80 6 1 mW/m2, and power was
increased by 33% by adding salt (300 mg/L sodium chloride) to increase
solution conductivity. A wastewater inoculum generated 33% less power
than the MPW inoculum. The MFC was an effective method of wastewater
treatment, demonstrated by .86% of biochemical oxygen demand and total
organic carbon removal from wastewater. Water Environ. Res., 78, 531
(2006).
KEYWORDS: microbial fuel cell, bovine serum albumin, peptone, meat
processing wastewater.
doi:10.2175/106143005X73046
Introduction
Microbial fuel cells (MFCs) are being developed as a new
method for both renewable energy production and as a method of
wastewater treatment. Electrically active bacteria at the anode of an
MFC oxidize substrates under anaerobic conditions. This oxidation
by the bacteria releases protons and electrons. The electrons are
transferred to the anode and travel through a circuit to the cathode.
The protons move to the cathode directly through solution. At the
cathode, oxygen, protons, and electrons react at a catalyst surface to
create water. Some oxygen can be transferred through the cathode
(and through a proton exchange membrane, if it is present) and be
used by bacteria in the anode section also, although this substrate
degradation does not lead to current generation (Liu, Cheng, and
Logan, 2005a; Liu et al., 2004; Min et al., 2005).
The MFCs can be used to produce electricity using a variety of
different materials (Chaudhuri and Lovley, 2003; Liu, Cheng, and
Logan, 2005b; Niessen et al., 2004). A single chamber MFC has
previously been shown to produce 494 mW/m2 with glucose as
a substrate and 146 mW/m2 with domestic wastewater (Liu and
Logan, 2004). Electricity has been produced by carbohydrates and
amino acids present in wastewater, but not by proteins. Although
proteins have been shown to be biodegradable (McLoughlin and
Crombie-Quilty, 1983) and solutions such as domestic wastewater
that contain proteins have been used in MFCs, electricity generation
has not previously shown to be directly linked to protein degradation.
To examine the potential for power generation in MFCs using
proteins, three different substrates were examined. Bovine serum albumin (BSA) was selected as a model compound with a known
molecular weight and structure. The BSA is also highly water soluble
and has been previously used as a model protein in wastewater studies
May 2006
(Confer and Logan, 1997; McLoughlin and Crombie-Quilty, 1983).
Peptone is a complex mixture of different proteins that is routinely
used in microbiological media (Liu, Xing, Chang, Zhiya, and Liu,
2005) and therefore also included as a substrate for power generation.
The third substrate selected for study was wastewater from a meat
packing plant. These wastewaters typically consist of blood, meat and
fatty tissue, meat extracts, and paunch contents from animals (Randolph
Packing Company and North Carolina Agricultural Extension Service,
1986). There are over 1300 meat packing companies with more than
1400 establishments in the United States that comprise the meat
slaughtering industry (A.M. Best Company, Inc., 2003). Because
these wastewaters are high in biochemical oxygen demand (BOD)
and chemical oxygen demand (COD), they can be expensive to treat
by conventional aerobic treatment methods. Thus, there could be a
great economic benefit of treating these wastewaters with a technology that produced a useful product, such as electricity. To compare
levels of power generated with these substrates to power densities
with other substrates, we used an MFC system that has previously
been used to generate electricity from glucose, acetate, and butyrate
(Liu and Logan, 2004; Liu, Cheng, and Logan, 2005b).
Methods
Microbial Fuel Cell Construction. The single chamber MFCs
used here consisted of a cylindrical chamber (28 mL) with two
electrodes (each 3 cm in diameter) placed on opposite sides and no
proton exchange membrane, as previously described (Liu and
Logan, 2004). The cathode was wet proofed Toray carbon paper with
a surface loading of 0.35 mg platinum/cm2 on one side; the anode
was non-wet proofed Toray carbon paper (De Nora North America,
Inc., Somerset, New Jersey); and the circuit contained a 1000-ohm
resistor (except as noted). The surface area per volume of reactor was
25 m2/m3 based on the projected area of the anode. All reactors were
operated in batch mode in a temperature-controlled room at 308C.
Reactor Inoculation and Operation. Reactors were inoculated with either domestic wastewater or a meat packing and processing plant wastewater. Domestic wastewater was obtained from
the primary clarifier overflow at the Pennsylvania State University
Wastewater Treatment plant in State College. The meat packing wastewater (MPW) was a raw, non-settled effluent obtained from a plant
in Pennsylvania. The MPW was shipped on ice and stored at 48C.
Electricity generation was examined using three different feeds:
BSA, peptone, or unfiltered MPW. For tests using BSA or peptone,
the reactor was initially inoculated with domestic wastewater (DW
inoculum) supplemented with 300 mg/L of BSA or peptone. In tests
using the MPW, the reactor was inoculated using MPW diluted,
except as noted. In one test using MPW, the reactor was inoculated
with domestic wastewater and 300 mg/L BSA. Dilutions of the
MPW were made using ultrapure water (Milli-Q system; Millipore
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Heilmann and Logan
Table 1—Conditions used to inoculate reactor for each
substrate and the method used for power density curves.
Substrate
BSA
Peptone
MPW (1:4)
MPW (1:4) 1
NaCl (300 mg/L)
MPW (1:1)
Inoculum
Domestic wastewater 1
BSA (300 mg/L)
Domestic wastewater 1
peptone (300 mg/L)
MPW
MPW
MPW or domestic
wastewater
Power density
method
Single cycle and
multiple cycle
Multiple cycle
Multiple cycle
Multiple cycle
Single cycle
Corp., New Bedford, Massachusetts). To examine the effect of
conductivity on power, sodium chloride (NaCl) (300 mg/L) was
added to diluted MPW (1:4 with ultrapure water). Reactors fed BSA
or peptone were operated for at least eight fed-batch cycles before
being switched to the wastewater-free medium, as described by Liu
and Logan (2004). In all tests, the reactors were verified to exhibit
stable and reproducible power output cycles before obtaining data.
No effort was made to remove dissolved oxygen from the solutions
added to the anode chamber.
The maximum power density was measured using two different
methods. The ‘‘single cycle’’ method was based on varying the
resistance of the MFC circuit (between 50 and 1400 ohms) during
a single batch reactor cycle operating at its maximum potential (Liu
and Logan, 2004). The ‘‘multiple cycle’’ method was based on
conducting one full batch cycle at only a single circuit resistance (50
to 1400 ohms) and then switching to a new resistance for the next
batch cycle. Single cycle results are based on a single, stable
Figure 2—Maximum power density with peptone or BSA
as a function of substrate concentration.
measurement, while the multiple cycle results are averages obtained
over 7 hours (6 standard deviation [S.D.]). A variable resistance box
was used to change the circuit resistance (Elenco Electronics, Inc.,
Wheeling, Illinois). Table 1 summarizes the reactor configurations.
Analytical Techniques. For soluble COD, total organic carbon
(TOC), and protein concentration measurements, samples were
prefiltered to remove bacteria using 0.2-lm-pore-diameter cellulose
syringe filters (Corning, Acton, Massachusetts) and analyzed using
Standard Methods (APHA et al., 1995). Total and soluble COD were
measured using method 5220 (Hach COD system, Hach Company,
Loveland, Colorado). The BOD was measured using triplicate
samples (6 S.D.) using method 5210 with a dissolved oxygen meter
(YSI model 50B, YSI Inc., Yellow Springs, Ohio) and probe (YSI
model 5905, YSI Inc.). Soluble TOC was measured using single
samples (method 5310B; TOC 5000A and ASI-5000A autosampler,
Shimadzu Corporation, Torrance, California). Protein (total and soluble)
was quantified by the Bicinchoninic Acid Assay (BCA Protein Assay
Kit, Pierce, Rockford, Illinois) using a spectrophotometer (UV-1601,
Shimadzu Corporation), with BSA calibration standards.
Calculations. Potential was measured using a multimeter with
a data acquisition system (2700, Keithly, Cleveland, Ohio). Current
and power were calculated from eqs 1 and 2, respectively, as follows:
I ¼ V=R
P ¼ IV
ð1Þ
ð2Þ
Where
Figure 1—Startup of microbial fuel using peptone
(300 mg/L; domestic wastewater inoculum). Solid lines
indicate the time span used for calculating the average.
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I
V
R
P
5
5
5
5
current,
voltage,
resistance, and
power.
Power and current were normalized to the projected surface area of
the anode (7.06 cm2). The Coulombic efficiency was calculated
Water Environment Research, Volume 78, Number 5
Heilmann and Logan
Figure 3—Maximum power density using BSA (1100
mg/L) and peptone (500 mg/L) as a function of current density produced by the multiple cycle method.
by comparing the actual charge produced (integration of current
with respect to time) to the available charge, based on the observed
COD removal (Chang et al., 2004). To calculate the available
charge, a conversion factor of 8 g COD/mole electrons (i.e., 4 mole
electrons per mole oxygen) was used with Faradays constant (96 485
C/e2 eq.) to convert electron equivalents to total available charge
in Coulombs.
Results
Power Produced Using Bovine Serum Albumin and Peptone. A repeatable cycle of power generation was sustained by
BSA or peptone (300 mg/L) after an acclimation period of
approximately 130 hours (Figure 1). Once acclimated, each
subsequent fed batch cycle spanned a total of 30 hours, reaching
a maximum voltage with the peptone solution of 261 6 3 mV (6 1
S.D.; 96 mW/m2) over a 7-hour period. When the voltage was
reduced to ,25 mV, the solution was replaced. The MFC acclimated to BSA produced a higher maximum voltage of 331 6 8 mV
(155 mW/m2) over the same 7-hour period (data not shown).
The maximum power density using BSA and peptone was examined as function of substrate concentration and current density. The
maximum power density increased with substrate concentration,
reaching a maximum of 240 6 8 mW/m2 using peptone and 286 6
1 mW/m2 for BSA (Figure 2). Based on these results, power output
was examined as a function of current density at substrate concentrations of 1100 and 500 mg/L for BSA and peptone, respectively.
The maximum power output using BSA was 354 6 10 mW/m2, at
a current density of 0.11 mA/cm2. This power density was 29%
higher than that produced using peptone (269 6 14 mW/m2 at
0.08 mA/cm2), demonstrating the importance of the type of substrate
on power output (Figure 3).
To examine whether the maximum power output was affected by
acclimation to a specific external resistance, a power density curve
was also obtained by changing the resistor during a single batch
May 2006
Figure 4—Comparison of the single cycle and multiple
cycle methods for obtaining maximum power density
data using BSA (1100 mg/L).
cycle and recording the voltage once it had stabilized (single cycle
method). As shown in Figure 4, a current density in the range 0.05
to 0.11 mA/cm2 produced the maximum power in both tests. The
use of the multiple cycle method appeared to produce a slightly
greater power density at the higher current densities than that indicated in single cycle tests.
The Coulombic efficiency was significantly higher for BSA than
for peptone (Figure 5). Coulombic efficiencies ranged from 10.7 to
20.6% for BSA and were only 2.3 to 6.0% for peptone. These
results are consistent with Liu and Logan (2004), who found a
Coulombic efficiency range of 9 to 12% using glucose (600 mg/L)
in a similar MFC.
Meat Packing Plant Wastewater. The MPW was examined
for electricity production using only the bacteria initially present in
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Heilmann and Logan
Figure 5—Columbic efficiencies as a function of current
density using BSA (1100 mg/L) and peptone (500 mg/L).
the wastewater. This wastewater had a COD of 6010 mg/L, with
93% of this present as soluble COD (5540 mg/L). Using BSA as
a calibration standard, 47% of the COD was protein (2843 6 54
mg/L; 61 S.D.) with most of this present in the soluble form
(2664 6 46 mg/L). The BOD of the wastewater was 3250 6 710
mg/L, or approximately 54% of the total COD.
Power generation was rapidly established using MPW, but the
wastewater was diluted to reduce the time needed for a complete
batch cycle. The maximum voltage appeared to be unchanged at
dilutions of 1:2 and 1:4 (218.5 6 2.2 and 217.3 6 1.5 mV,
respectively; 61 S.D.), but the maximum voltage decreased at
a dilution of 1:10 (Figure 6). However, these results, showing that
power output was unaffected by dilution, were primarily a result of
using a high external circuit resistance for the test (1000 ohms). A
power density curve using multiple resistors showed that power
Figure 6—Startup of microbial fuel cell with MPW (values
indicate dilution of MPW with water).
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Figure 7—Power density profile of undiluted (1:1) and
diluted (1:4) MPW (MPW inoculum; single cycle method
for 1:1 case).
generation with a 1:1 dilution was substantially greater than that
obtained using a 1:4 diluted wastewater sample (Figure 7). The
maximum power output of the pure MPW was 139 mW/m2
compared to 80 6 1 mW/m2 for the diluted MPW. The maximum
current density for the pure MPW was 0.115 mA/cm2, which is
approximately twice that of the diluted MPW (0.057 mA/cm2).
The solution conductivity was an important factor in the
maximum power density achieved with the sample. Diluting the
sample with water decreased the conductivity from 5.8 to 1.5
mS/cm (1:4 dilution), contributing to the decrease in the maximum
power density (Figure 7). To further examine this effect, a power
density curve with the 1:4 diluted sample was compared to that
obtained after adding 300 mg/L of NaCl to the sample
(2.19 mS/cm). The maximum power increased by 33%, or to 108
mW/m2 (from 81 mW/m2) when the sample was supplemented with
NaCl (Figure 8). The addition of NaCl also increased the
Coulombic efficiency from 5.2 to 11.9%, to 8.4 to 15.4% (Figure
9). An increase in Coulombic efficiency with current density was
observed, consistent with the findings for the protein samples.
Effect of Inoculum on Power Generation. The MFC tests on
the MPW wastewater were conducted using bacteria already present
in the wastewater. However, we wondered if the inoculum that was
used would affect power generation. To examine this, we compared
power densities produced by an MFC inoculated with domestic
wastewater with that produced using a reactor inoculated only with
MPW (Figure 10). The power density of the MFC inoculated with
MPW wastewater was 139 mW/m2, compared with 93 mW/m2
when DW was used. Also, the current density range for the MPWinoculated MFC extended to a maximum of 0.12 mA/cm2, compared with 0.08 mA/cm2 for the MFC inoculated with DW.
Treatment Efficiency. The removal of organic matter in the
MFC for BSA, peptone, and MPW solutions was evaluated on the
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Heilmann and Logan
Figure 9—Columbic efficiencies as a function of current
density for MPW (1:4 dilution), and with the same solution
containing 300 mg/L of NaCl (multiple cycle method).
Discussion
These experiments demonstrate that electricity production at
relatively high power densities can be sustained using proteins and
protein-rich solutions. Previous MFC studies have primarily focused
on power production from carbohydrates, such as glucose and
acetate (Chaudhuri and Lovley, 2003; Liu, Cheng, and Logan,
Figure 8—Maximum voltage (A) and power generation (B)
as a function of current density using MPW (1:4 dilution;
1420 mg/L COD); ( ) indicates 300 mg/L NaCl addition.
basis of four types of measurements: protein, BOD, COD, and
TOC. In general, there was good agreement among the measurements, indicating that over 90% of the organic matter was degraded
during a cycle of power generation for all three substrates (Figure
11). Protein removal was greater than 94% for all three substrates.
The average removal for BOD increased in the order peptone
(86%), BSA (90%), and MPW (93%). These differences were
significantly different (P-value 5 0.0013 from ANOVA). For
MPW, 93% of the BOD and TOC was removed, but only 87% of
the COD was removed. However, COD measurements were not
replicated because of limited sample volume. The final BOD of the
treated MPW in the MFC was 62 6 8 mg/L.
May 2006
Figure 10—Power density with MFCs inoculated with
domestic wastewater or MPW (single cycle method).
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Heilmann and Logan
Figure 11—Removal of organic matter using BSA (1100
mg/L), peptone (500 mg/L), and MPW (540 mg/L as BSA;
1:4 dilution) on the basis of protein concentration, BOD,
COD, and TOC.
2005b), although an amino acid was also used in one study (Logan
et al., 2005). While power has been generated from wastewaters that
contained protein (e.g., Liu et al., 2004), power generation was not
shown to be directly connected with protein degradation. Differences
in the MFC construction can affect the power density (Chaudhuri and
Lovley, 2003; Liu and Logan, 2004), but here we used the same
MFC previously examined with acetate, butyrate, and glucose as the
substrate. It appears from comparison of these results with other data
that the power densities produced by proteins and protein-rich
wastewater is, in general, slightly lower than the maximum possible
with other substrates. In previous tests using this system, the
maximum power was 506 mW/m2 with acetate and 494 mW/m2 with
glucose, but power output was reduced (305 mW/m2) in tests with
butyrate. Although the tests with glucose were performed with a
cathode containing slightly more platinum (0.5 mg/cm2), it has been
shown that the platinum loading differences do not affect power
production (Cheng et al., 2005). The maximum power achieved in
this system using a single protein (BSA) was 354 6 10 mW/m2.
Thus, higher power densities are possible than those observed for
BSA by using other substrates, indicating that the bacterial degradation rate of the organic matter affects power generation.
The maximum power density produced also appears to be related
to the ‘‘complexity’’ of the substrate (i.e., a single compound versus
many compounds). With substrates such as the peptone and MPW,
solutions that contain many different amino acids and proteins, lower
power was produced (269 6 14 and 139 mW/m2, respectively) than
that achieved using BSA. This trend of reduced power production
has been observed in other studies also. For example, it was found
using the same system that power output was only 146 mW/m2 using
domestic wastewater versus 494 mW/m2 using glucose (Liu and
Logan, 2004). Min and Logan (2004) found, in a different type of
536
fuel cell, that power output was 86% less when dextran was used
instead of glucose in the feed. Thus, it appears that the effect of
multiple substrates or polymers in the organic solution can reduce the
maximum power output. Whether this is a result of the specific
bacteria present on the electrode (i.e., the inoculum source), intrinsic
rate kinetics, or the specific compounds, is not known.
Coulombic efficiencies increased in proportion to the maximum
power density, likely as a result of a shorter batch cycle time. For
example, the maximum power density was greater for BSA than
peptone, and Coulombic efficiencies for BSA of 10.7 to 20.6% were
larger than those of 2.3 to 6.0% measured for peptone (Figure 5).
For any single substrate, Coulombic efficiency increased with the
current density (Figures 5 and 9). An increase in the power generation means that the substrate is being degraded faster by the
bacteria, reducing the total amount of time available for oxygen
diffusion across the cathode into the anode chamber.
Oxygen transfer into the anode chamber has been shown to lower
Coulombic efficiencies in MFCs (Liu, Cheng, and Logan, 2005a;
Liu et al., 2004; Min et al., 2005), because the bacteria can use this
oxygen to degrade substrate. This aerobic degradation of the substrate makes less of the substrate available for electricity production,
lowering the maximum possible Coulombic efficiency. Fermentation of the substrate can also affect Coulombic efficiency. Min and
Logan (2004) found that using non-fermentable substrates, such as
acetate and butyrate, in a flat-plate MFC yielded Coulombic
efficiencies of 50 to 65%, while fermentable substrates, such as glucose, dextran, and starch, produced Coulombic efficiencies of only
14 to 21%. It is also possible that other electron acceptors are
present in the wastewater, which can account for the removal of
COD (such as sulfate). Methanogensis is also possible (Kim et al.,
2005), although it was not possible to measure methane here because of a lack of a headspace in the reactor.
The acclimation procedure, which is based on using a single
external fixed resistor of 1000 ohms, may also be a factor in the
maximum power density. As was shown in Figure 3, when a reactor
was allowed to reach a steady voltage over a complete batch cycle
(multiple cycle method) at different external resistances, there was
more variability in the power density curve than that obtained by
varying the resistors over a short period of time at the maximum
voltage of a single batch test (single cycle method). In addition, the
multiple cycle method appeared to result in a slightly greater power
density at the higher current densities than that obtained with the
single cycle method. This suggests that acclimation of the reactor
over a long period of time to different external resistances could
change the maximum power density that could be achieved for the
reactor. The effects of the resistor chosen for the acclimation
procedure on the maximum possible power output and on the
composition of the microbial community that develops in the
system are not well understood and should be further investigated.
Implications for Wastewater Treatment. These results demonstrate that MFCs can be used to obtain effective wastewater
treatment of MPW and other high-protein-containing wastewaters.
The removal of organic matter in terms of COD and BOD found
here for proteins and wastewater from the meat packing plant were
actually higher than that found previously in tests using domestic
wastewater. In MPW tests, 93 6 13% of the BOD was removed
compared to 78 6 2% found for domestic wastewater (Liu et al.,
2004). The COD of the diluted MPW (1420 mg/L) was more than
five times greater than that of domestic wastewater (250 mg/L);
thus, overall, there was more COD removal for the MPW than with
domestic wastewater on a mass basis. Because of the difference in
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Heilmann and Logan
wastewater strength, however, the final BOD of the MPW (62 6 8
mg/L) was higher than that of the domestic wastewater (approximately 48 mg/L; Liu et al., 2004).
The MFC technology has only so far been proven in the laboratory, but there is increasing evidence that this technology will be
useful if it can be economically scaled-up to full-size treatment
systems. Several different wastewaters have now been shown to be
effectively treated in an MFC while accomplishing electricity
generation (Liu et al., 2004; Min, 2005). The challenge will now be
to find methods to build larger systems that can be incorporated to
treatment systems used for different types of wastewaters.
Acknowledgments
Credits. We thank David Jones (Department of Civil and
Environmental Engineering, Penn State University, State College,
Pennyslvania) for help with TOC measurements. This research was
supported by National Science Foundation Grant BES-0331824
(National Science Foundation, Arlington, Virginia).
Authors. Jenna Heilmann is a graduate student and Bruce E.
Logan is the Kappe professor of Environmental Engineering in the
Department of Civil and Environmental Engineering, Penn State
University, University Park, Pennsylvania. In addition, Bruce E.
Logan is the director of the Penn State Hydrogen Energy (H2E)
Center, Penn State University. Correspondence should be addressed
to Bruce E. Logan, The Penn State Hydrogen Energy (H2E) Center,
212 Sackett Building, Penn State University, University Park, PA
16802; e-mail: [email protected].
Submitted for publication May 17, 2005; revised manuscript
submitted June 16, 2005; accepted for publication July 25, 2005.
The deadline to submit Discussions of this paper is August 15,
2006.
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