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Applicability of alginate film entrapped yeast for microbial fuel cell Ummy Mardiana a,b,c ,* Christophe Innocent
a , Marc Cretin a , Buchari b , Henry Setiyanto b , Rianti Nurpalah c , Meti Kusmiati c , a
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Institut Europen des Membranes, ENSCM - UM2 - CNRS, (UMR 5635), Universit de Montpellier 2, CC047,
place E. Bataillon, 34293 Montpellier Cedex 5, France
, email : mardiana.ramdan@gmail.com b Analytical Chemistry Research Group, I nstitut Teknologi Bandung,
Jalan Ganes ha
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10 Bandung, West of Java Indonesia 40132
c STIKEs Bakti Tunas Husada Tasikmalaya, Jl. Cilolohan No 36, West of Java Indonesia 46115 . Abstract -
New strategies are proposed for modification of the anode
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of a Microbial Fuel Cell (MFC)
. Immobilization of ye ast cells as electrogenic microorganism in MFC was reported using alginate. Yeast cells
entrapment within alginate matrices was done through films deposited at the surface of
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a carbon felt electrode and the
resulting anodes were characterized by chronoampe rometry. Yeast entrapped within alginate films on carbon
felt oxidized glucose and generates a current by direct and mediated electrons transfer from yeast cells to the
carbon electrode. The result substantiated that immobilization of yeast for MFC could b e a promising method
to product green electricity. Keyword s - Saccharomyces cerevisiae, Neutral red, Yeast immobilization,
Bioenergy . INTRODUCTION Microbial fuel cell (MFC) can be considered as a novel bioelectrochemical system
that can directly convert chemical energy into electricity [1,2]. Microorganisms as biocatalysts oxidize organic
compounds and produce electron flux ( i.e. electric current). Nowadays, t o improve performance of MFC have
been extensived efforts [3 - 7] . In previous studied, Saccharomyces cerevisiae have been applied as
biocatalyst in MFC [8 - 10]. Currently problems encountered is energy produced from yeast fuel cell is remain
too low, mainly due to the very low rate of direct electron transfer from MFC to electrode. It has been
previously shown that the present o f artificial mediator make more easier transfer electron to solid electrode
and rapid electron transfer from yeast to electrode might be a realized by the presence proper electron
mediator [8 - 11 ]. Potter et al [1] showed that Saccharomyces cerevisiae and E.coli , produced an anode
potential when applying mediator under 100 mV and could not generated without the present of mediator.
Artificial electron mediators allows electricity generation from m icroorganism which are unable direct
communication or produce low power density [12]. Mediators are fundamentally lipophilic chemical electron
carriers that are able to pass through the cell walls of microorganisms, and thereby move between intracellular
s pace and the extracellular environment. They are able to assist the microorganisms metabolism by acting as
a terminal electron acceptor. The desirable characteristic as redox - mediator are should have a good
electrochemical reversibility and have a prope r redox potential with substrate i.e. NAD + /NADH couple, which
is the major electron carrier in microbial respiration metabolism. Its have been observed that Neutral red (NR)
was one of the redox molecules with these properties [13,14]. Some microorganism s uch as Shewanella
putrefaciens , Geobacter sulfurreducens or Rhodeferax ferrireducens have been studied to generate elecitricity
in mediatorless MFC is due to they are able to direct electron transfer to electrode [ 15 - 17]
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. It has been reported that
physical contact between electrode and outer - membrane cytochromes or / and conductive pili of bacteria can
enable direct connection. Some bacteria also have endogenous electron mediator could also facilitate fast
electron transfer in pseudo - direct electron transfe r between electrode and bacteria [18]. Meanwhile, yeast,
they need some media for supporting electron transfer. As introduction, Prasad [19] have been explored the
possibility direct electrical communication between yeast, Hansenula anomala based mediatorless MFC which
is related to the redox protein present in the cell membrane and generated power density 2.9 w/m 3 . The
catalytic activity Saccharomyces cerevisiae have been investigated in mediatorless MFC. The mechanism
electron transfer from the y east cell to the anode was identified whether through the surface limited species or
t hrough the solution and produced 3 mW/m - 2 [20]. However, the relatively low current density and poor
energy conversion efficiency are allowed to the utilization of elect ron mediator in MFC based yeast as
biocatalyst . Studied of immobilization electrode - mediator have been resulted [12,13]. In conventional method,
by employing soluble electron - mediators can enhance performance of MFC, but it can cause environmental
polluti ng effect, not considered for continuously industrial process [12,21]. Previous studies have resulted that
mediator physically adsorbed on electrodes shown less efficiency because it was easier removed from surface
of anode and it was not easy physically immobilized in large amount of mediator directly on surface of anode
[22]. Beside of mediator immobilization, nowadays yeast immobilization are really known well [23 - 28] but only
a few were used as immobilize biocatalyst in MFC. Yeast cells can be entrappe d within alginate as a hydrogel
polymer to enhance electrochemical activity [29]. Yong et al [30], have introduced immobilization of biocatalyst
and can improve performance of MFC. The result reported that cells immobilization could a promising method
an d powerful strategy for increasing microorganism life time and stabilities. Moreover, research of biocatalyst
immobilization have also been explored [7,23,31]. Cells immobilization can be classified refers to the technique
carried out. There are physical e ntrapment within porous matrix ( i.e. encapsulation), adsorption or chemical
attachment. Entrapment of yeast cells has been widely developed. It simply consists to drop wise yeast -
alginate solution into divalent cation reticulating solution to produce microbeads by cross - linking [25,26,32,33].
Progresses in encapsulating yeast in alginate matrixes were obtained [24,34] and using some various
reticulating agent have also been studied [35,36].
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It has been proved that the
gelation process of alginate dep ends on the capacity of the polysaccharide to bind divalent cations which
leads to various structures. The use of calcium chloride as reticulating agent is the most efficient to get a
matrix with high loading capacity properties. Some methods using natural and synthetic polymer are also
described in the literature [23,33,37,38] but alginate was more commonly used because of good stability.
However, another technique of immobilization is to gained polymer formation containing yeast and mediator it
could be a promising method as alternative to modify electrodes. Moreover, by applying phsyco - chemical
immobilization between electron mediator and biocatalyst as simultaneously might reduce the cost of activation
and clean up dye waste water [39,40] and could be an effective method for improve bioanodic performance of
and clean up dye waste water [39,40] and could be an effective method for improve bioanodic performance of
MFC. In this study, we propose two ways to prepare the anodic part of a MFC working with Saccharomyces
cereviceae . The first route is to synthesize microbeads for yeast cells entrapment. Microbeads will work in
anolyte suspension in contact with a raw carbon felt. The second route is the deposit at the surface of a
carbon felt of an alginate film containing yeast cells at the surface of carbon felt. The aim of our research was
then to develop an ef ficient method for yeast cells immobilization. Chronoamperometry was used as the main
electrochemical method. Scanning electron microscopy was performed for identification of yeast electrode
surfaces.
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Methylene blue (MB) and neutral red (N
R) have been chos en as electron mediator to applied in MFC performances [10]. Further, by employing
immobilized mediator and biocatalyst as simultaneously could be contributed to self - sufficient MFC which can
be used for long term application. MATERIAL AND METHODS All chem ical used are of analytical grade.
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Preparation of electrodes Carbon felt (CF) (from Alfa Caesar, 1.27 cm thick) and nickel plate were used as
anode and cathode material respectively. Materials were previously washed in 1M HCl for 48 hours and then
rinsed with ultrapure water to clean from trash material . Procedure for the immobilization of yeast cells
Immobilization within alginate was done from a procedure previously designed [41], CaCl 2 (Sigma) was used
as gelation agent. A solution at 2% (w/w) of yeast, Saccharomyces cereviceae (Sigma) solution. Neutral Red
(NR) at 0.3% (w/w) as a mediator was prepared in buffer phosphate (PB) pH7. 2% (w/w) Na - alginate
powder (Sigma) was dissolved in ultrapure water at 75 - 80 o C for 30 min. Na - alginate and yeast cells
solutions were mixed in a ra tio 1:1 then NR was added in this solution.
The production of yeast - NR - Ca - alginate beads was obtained by dropping the solution containing of CaCl 2
0.05 M using syringe. Red beads of 2 (0.3) mm of diameter were then formed. On the other hand, films
formati on
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have been gained through the deeping of a carbon felt in a yeast - alginate solution Neutral Red (NR) at
0.3% (w/w). Carbon felt was immerged for 1
h our , followed 1 h our in CaCl 2 0.05 M then removed and left for 12 h ours for complete gel formation and le
ft for 12 h ours
for complete gel formation in desicator.
As a product two types of yeast immobilized were obtained
The product were washed with ultrapure water to remove excess calcium ion and unentrapped cells, and then
stored at 4 0 C prior used and simply activated at
30 0 C for 30 m inutes before applied . As described in previous study [8], we demonstrated a biological fuel
cell by ordinary yeast without need for sterilization or the maintenance live cultures. MFC design and
experimental procedure The MF C dual chamber (2*100
mL) is constituted of an anodic and a cathodic chamber separated by Nafion 117 (DuPont, USA) as proton
exchange membrane.
Prior to use, the Nafion membrane was prepared
by boiling the film in H 2 O 2 (30%), th
en rinse in ultrapure wate r, H 2 SO 4 and ultrapure water again. Carbon felt (5cm x 1.3 cm x 0.5 cm) and
nickel plate (5 cm x 1.5 cm) was used as anode and cathode electrodes respectively. A schematic of the
MFC system is shown in Fig . 1 . All chamber used have been closed by cover
compartment cell. Fig. 1. Design of the microbial fuel cell (MFC) system Anodic and cathodic chambers
preparation
Anodic chamber is constituted of a solution of glucose monohydrate
(Sigma Aldrich) prepared from 1.98 g of glucose (Glu) dissolved in 100 mL buffer pH 7 and followed by stirring
for 24h to homogeneity solution. The phosphate buffer was made from a mixture of Na 2 HPO 4 and NaH 2
PO 4 (Sigma Aldrich) with the ratio 4.08 g:3.28 g dissolved in 1L ultrapure water.
Yeast Saccharomyces cerevisiae as biocatalyst immobilizatio
n both in microbeads and film deposited are packed into anodic chamber. The totality of microbeads generated
following the procedure described previously is transferred to the anodic chamber. Film deposited was
generated from the same quantity of yeast cells as for microbeads and the alginate film deposited on carbon
felts was used as prepared. The biocatalyst will oxidize glucose and as product will release electron at the
anode.
Experiments were conducted with Neutral Red entrapped in the al ginate yeast solution as molecule
Experiments were conducted with Neutral Red entrapped in the al ginate yeast solution as molecule
facilitating electron transfer ( i.e
. mediator). The films generated from the same quantity of the yeast cells
. The cathodic compartment consists of potassium ferricyanide solution (Sigma Aldrich) at 0.02 M in
phosphate bu ffer pH 7 as reported in previous study [9]. Potassium ferricyanide
which receives the electrons from the external
circuit. Ferricyanide is then reduces to ferrocyanide at the nickel plate. Oxygen at the cathode chamber will
oxidize Fe(II) to Fe(III). The iron re - oxidation is needed for the MFC operation. Characterization To determine
anodes performances, electrochemical characterizations were performed by chronoamperometry using a
potentiostat VERSASTAT 3 (PAR AMETEK). The potential applied to the electro chemical half - cell to
characterize the anode was 0.3 V/SCE, to ensure mediator oxidation. The half - cell was consisted of 100 mL
of the test solution, carbon felt as a working electrode (WE),
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KCl saturated calomel electrode (SCE) a
s reference electrode (RE) and platinum as counter electrode (CE). A control experiment without any yeast cell
showed a baseline current of 5 A.m - 2 at the anode of the electrochemical half - cell, polarized under
0.3V/SCE.
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Scanning electron microscope (SEM) (Hitachi S - 4800) was us
ed to characterize yeast cells immobilization on carbon felt. The procedure to prepare samples for SEM
observations was the following: a piece of the modified felt was carefully cut to a dimension 1 cm x 1 cm and
fixed in 4% glutaraldehyde solution for more than 4h to stabilized microorganism immobilized. After a rinse
twice in phosphate buffer pH 7, samples were dehydrated in ethanol series 40, 60, 80, 100% for 30 min. The
last step was samples drying in desiccator for 3 h ours . - external loads to determine the maximal power
output as described elsewhere [9] and MFC
process was operated at ambient temperature (25 + 1 o C). The voltage (E
) generate d
was recorded using a digital multimeter Voltcraft model VC 850 and the current (I) were calculated from the
equation I = E/
R. RESULTS AND DISCUSSI ON
Yeast - alginate film on carbon felt as a product of yeast immobilization and effect of mediator in solutio n As
shown, the thickness of the alginate - yeast film is around 15 m with a high roughness because of the
presence of yeast cells (Fig . 2) . Yeast cells are well identified as spherical shape is around 4 m .Yeast cells
are shrouded within matrix of alginate with a homogeneous deployment on its surface favorable for
electrocatalysis.
Fig. 2. SEM images
showing yeast cells immobilization within an alginate film deposited on carbon felt
To study effect of nature of electrochemical mediator on catalytic performances, methylene blue and neutral
red were added to the solution containing glucose (Glu). CF modified by immobilization yeast - alg film
deposited has been prepared as anode. Results are presented Fig . 3. Fig. 3. Current density produced by
glucose oxidation as a functi on of time under a polarizatio of 0.3V/SCE. Conditions: in blue, Alginate - yeast
film in presence of Methylene Blue (MB) as mediator; in red, Alginate - yeast film in presence of Neutral Red
(NR) as mediator. The concentration of both NR and MB were 10 mM Fig . 3 . clearly proved that methylene
blue and neutral red are facilitates electron transfer to the anode because of the increase of current density
due to the electrocatalytic oxidation of glucose by yeast cells. In immobilized f orm, cells respiration is limited
because of the limitation of oxygen content inside of the matrix. Yeast are able to switch metabolism from
respiration in the present of oxygen to fermentation when anoxic. In our configuration, the addition of NR
promotes the reduction of the redox center of yeast cell, i.e. NADH reduction [18, 39]. Yeast was delivered a
redox potential close to redox potential of NR. NR and MB formal redox potentials are 0.385V and 0.53 V vs
SHE, meanwhile the formal redox potential of NADH/NAD + is - 0.320V vs SCE. NR has then a closer redox
potential to NADH/NAD + than MB. This can explain the higher electro catalytic current observed in presence
of NR. The use of NR
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as an intermediate molecule will be effective
and will undergo a revers ible reaction.
In the presence of a mediator molecule, the potential of the anode will be determined by the potential of the
oxidation reaction given in
Eq.1 . NR (oxidized) + NADH (yeast) NAD + (yeast) + NR (reduced) NR (reduced) NR (
oxidized) + 2e + H +
(1) Many different mediators have been experimentally studied [9,10,12], but relatively little has been reported
on why certain mediator work better than other. In previous study [9], reported that MB was selected as proper
elect ron mediator in MFC based yeast in suspension solution. However, in the present work, yeast was
entrapped in alginate matrix and in this condition NR was selected as suitable electron mediator. In the other
study, some mediator in poor performance, probab ly is due to depends on the conditions associated with the
culture [43,44]. Popov et al [12] have been observed that MB can be adsorbed onto surface of anode more
efficiently than NR by using simple pH shift. This is probably due to at high pH ( i.e. pH 12) which is likely
easier interact from MB + with the carbon surface since MB + charge ion produced when MB - Chloride was
dissolved in pH 12. However, the difference pH of anodic solution can be effect to kinetics of electron mediator
and types of mediator to be selected. In our configuration, NR more suitable as electron mediator, it is probably
due to the selection of a lower pH used ( i.e. 7), because by using high pH is not to be considered and it could
be affect to performance of yeast as biocatalyst [9 ] .
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S. cerevisiae like many other microorganisms can function in anaerobic conditions. It is an easily accessible
microorganism with a well understood metabolism. The presence of oxygen in the anode compartment is not
favorable for the overall fuel cell
fun ction because it
would disrupt the electron flow through the external
circuit. Yeast - alginate immobilization and effect of NR entrapment The capability of yeast in direct
communication with electrode surface has been demonstrated [20]. The next step in this study is now to
compare the electro activity between microbeads and film deposited of an alginate - yeast - NR. Current
densities products by glucose oxidation at the alginate - yeast immobilized entrapping NR are then presented
Fig . 4 . Fig. 4. Current density delivered by glucose oxidation as a function of time under a polarization of
0.3V/SCE from (A) microbeads and (B) film deposited on surface of CF in 0.1 M glucose PB pH7. The blank
current obtained from raw carbon felt CF and CF@Alg (CF at alginate beads). The resulting current was
observed during 2 hour after 30 minute of stabilization time. According to t he result, CF@Y - Alg can also
generate electrical current 0.01 A.m - 2 and 0.06 A.m - 2 from microbeads and film deposited, respectively. It
clearly evident the necessity to use a mediator because of the monitoring of a very low current density . The
current del ivered its might due to the yeast cells adhered on
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anode surface were the active biocatalyst for
oxidation of the cells that are entrapped on surface ther e is chemical leakage from the cells of the
electrochemically active molecules. NAD + and other electro - active compounds are diffusing out and these
act as extracellular mediators, meanwhile species in
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anolyte solution including the dispersed yeast cell di d not take a part in the electron transfer and
current generation [20]. This result confirms also, that performance improvement by introducing a mediator
delivered 90% and 82 % from microbeads and film deposited, respectively. The role of NR
to transfer electrons to the ano
de was clearly proves the necessity to use a mediator. Besides that, result obtained by film deposited could
improve 71% compared with microbeads. CF@Y - Alg - NR film proves that entrapment of yeast and NR
within alginate film deposited at the electrode surface is an efficient method to prepare electrocatalytic film for
MFC. Since mediator is immobilized outside of the cell and oxidized NR has to move into the cell become
reduced intracellular and then reduced mediator diffuses out the cell to become re - oxidized at the electrode
surface. Alginate holds the cell and mediator closer to the electrode, it is probably reason why deposited film
has higher current dens ity generated compared with microbeads. Fig. 5. Current density generated from
microbeads and film deposited immobilization and without immobilization in 0.1 M glucose PB pH 7. Potential
applied: 0.3 V/SCE; Pt as counter electrode. The concentrations of yeast a nd NR in solution were 2 g/100 and
10 mM, respectively. During 2 hours operation, after 30 minute of stabilization time, confirm that the use of NR
in solution at 10 mM allows electronic transfer which leads to a current density of 0.185A.m - 2 at CF/Y - NR.
Moreover, as previously proves ( Fig . 5 ) by chronoamperometric measurements confirm that CF@Y - Alg -
NR film is a better than microbeads and in suspension solution because of higher current generated (0.326 to
0.095 A.m - 2 and 0.185 A.m - 2 respectively). Furt her, it is clear that when yeast is entrapped within alginate -
NR microbeads (CF@Y - Alg - NR (beads)), current was limited by obstruction of NR reduced form to get out
of the matrix gel layer in to the electrode surface. Refers to result, CF@Y - Alg - NR film deposited could
improve stability and performance if compared with CF@Y - Alg - NR microbeads and CF/Y - NR suspension
solution, it was seen by highest current density produced from this method and it is might due to NR reduced
form more easily access to achie ve the surface of the electrode. MFC performance.
According results above, we have been applied immobilized yeast to prepare the anode of the MFC. The aim
of this part is to build a MFC and to determine its basic electrical properties through the monitorin g of the
discharge current (on a 1 k resistance) vs time
during 44 day. In our work, after observed
the best performance in terms of
maximum power generation where
was measured at the load of 1000
(result not reported). Anodic compartment were buil t
from a yeast cells suspension ( i.e. without immobilization) (CF/Y - NR in suspension) and from a yeast -
alginate film within NR (CF@Y - Alg - NR film). Results are presented in Fig
. 6 Fig. 6. (A) The evolution of the current
delivered by the MFC working in the anodic compartment with yeast cell
s in suspension ( square shape )
, and CF/Immob Y - Alg - NR f
ilm ( triangle shape ) in 0.1 M glucose. Arrows indicate the addition of glucose and replacement of K 3 Fe(CN)
6 as catholyte part , (
B) SEM image showing the anode of model C after use in MFC .
MFC which inoculated with the immobilized cell and mediator delivered a significant amount of electricity output
in the batch mode of MFC operation for 44 days. As the immobilization usually ca used partially loss of
microorganism viability or activity [45], a slight decrease of current density output is reasonable. After
replenishing glucose ( 12 th days ), the discharge power of model C increase ~ 105 % (from 1.9 W.m - 2 to 3.9
W.m - 2 ) and stabilizes at a current value similar to the first operating cycle. It was in contrast with current
delivered by the MFC working from the cells in suspension. This result proves that the MFC with immobilized
cell and mediator can deliver more stable electricity outp ut. Furthermore, after the second glucose addition, we
note the same comp a rtment of MFCs prepared by cells immobilization , which confirms the good stability of
yeast - alginate film and especially with NR entrapment. Same condition gained from the last cycle s, the
suspension cell quickly dropped into 0 . 2 W.m - 2 and it was stable until the end of observation. Nevertheless,
for the glucose addition at 36 th days , no current increase is reported. We clearly have two different evolutions
by using yeast cells and neutral red in solution (CF(Y - NR)) or model CF/Immob Y - NR ( immobilization of Y -
NR within alginate film). MFCs working with immobilized cells show a fast stabilization of current. The current
density is especially stable by using neutral red as mediator ent rapped within the film. Such results corroborate
the previous electrochemical characterization for the following reason. In contrast, the current output of the
MFC built from the yeast suspension is increasing with the time after glucose addition and becom e decreased
from higher value.
In CF/Immob Y - NR, it was assumed that, the electrons transfer occurs within alginate polymer and involving
neutral red molecule and the electron flux presents a high stability because of the encapsulation of NR and
yeast cell s close to the electrode surface within the alginate film. The very low current measured
at the start of the experiment for the configuration working with cells
in suspension can be linked to the fact that the contact of yeast to anode is
low but increase with time because of yeast cells growing . The recycling of NADH to NAD +
is important to keep the glycolysis process continuous [46]. Since glycolysis reaction takes place in the cytosol
of the cell rather than in the mitochondria, NADH is easily linked to a mediator molecule that is attached to
the cell membrane. The MFC based S. cerevisiae extracts the energy using NADH/NAD + redox cycle. The
organism can sustain life as long as the glycolysis pathway is no
t disturbed. When a mediator gets reduced, the ener gy
extraction process in the fuel cell does not interfere the glycolysis as NADH is oxidized back to
NAD + . CONCLUSION. The yeast Saccharomyces cerevisiae was successfully immobilized as electrogenic
microorganism to build the anode of a microbial fuel cell . Electrochemical characterization of the as - prepared
anode and MFC performances proved that the deposit of an alginate film entrapping yeast cells is an efficient
way to promote glucose oxidation and to transfer electron. The developed technique leads to the deposit of an
alginate based film of 15 m thick on carbon felt electrode used as anode. Yeast cells were identified as
spherical particles of 4 m of diameter, entrapped within the alginate matrix and showing a homogeneous
distribution. Glucose oxidation current measured at the anode depends on the presence of n eutral r ed (NR)
as mediator molecule to transfer electron from the fuel to the anode. P erformance of the MFC were evaluated
in terms of maximum power generation where was generated at the load of 1k
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. It has been shown that
an efficient electrochemical system can be designed by the deposit of a yeast - alginate film containing n eutral
r ed as m ediator molecule, on a carbon felt as anode. The as - prepared deposit is a few microns thick and
yeast cells of 4 m diameter have been identified with a homogeneous repartition. The easy and robust
yeast cells of 4 m diameter have been identified with a homogeneous repartition. The easy and robust
immobilization method of yeast cells presented in this pap er is a promising route to build new system to
product sustainable energy. The next step is now to develop an oxygen electrode as a cathode based for
example of an enzyme like laccase immobilized on the electrode [47]. Combining the reduction of oxygen at
the cathode with fuel oxidation by yeast cells at the anode, a self - sufficient microbial fuel cell will be usable for
long term applications like water desalination as recently proposed. ACKNOWLEDGEMENTS This work was
funded by Gr ant of Joint Collaboratio n Institution Research (PEKERTI) from
Higher Education Ministry of Indonesian (DIKTI
)
and partially supported by Institute European des Membranes (IEM) Montpellier France
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