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Photobiological Hydrogen Production from Synthesis Gas Carbon Sources KL a and Kinetics Evaluation.

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Dev. Chem. Eng. Mineral Process. 13(5/6), pp. 549-562, 2005.
Photobiological Hydrogen Production from
Synthesis Gas: Carbon Sources, KLa and
Kinetics Evaluation
G. Najafpour", H. Younesi, K.S.K. Ismail,
A.R. Mohamed and A.H. Kamaruddin
School of Chemical Engineering, Engineering Campus,
Universiti Sains Malaysia, Seri Ampangan, Nibong Tebal,
Seberang Perai Selatan, I4300 Penang, Malaysia
Photo-evolution of hydrogen fiom synthesis gas using RhodosDirillum rubrum was
studied in batch fermentation. Culture of R. rubrum was initially grown on malate,
also with various initial concentrations of acetate and synthesis gas. The synthesis
gas was a mixture of H2,CO and CO2. It was found that the doubling time of
bacterium on 2.5 g/l of malate, and 2.5 g/l and 6 g/l of acetate were 8.4, 31.8, and
48.6 h, respectively. The growth of & rubrum was not significant at high
concentration of acetate. The cell density of microbe was 0.3 g/l on 2.5 gh' malatefor
incubation period of 5 days. The cell concentrations of 1.4 and 0.41 g/l were obtained
in 2.5 and 6 g/l of acetate, respectivelyfor duration of 5 days. Inhibition of substrate
was clearly observed on cell yield and hydrogen production with high concentration
of acetate. Maximum hydrogen production (1.8 mmolll) was obtained when R. rubrum
was grown on 2.5 g/l of acetate. Efect of agitation rate was carried out and it was
found that more hydrogen production (1.8 mmol) was achieved at 250 rpm. Mass
transfer and kinetic studies were peflonned on 2.5 g/l of acetate. Maximum specific
growth rate
and Monod constant (KP)were obtained at 9.8 h-' and 0.14 atm,
respectively. No substrate inhibition occurred at CO concentration of 0.56 atm.
The current world dependence on conventional oil resources is at a critical point
where the recoverable resources are already half consumed [ 11. Therefore, research
on alternative hels has captured the interest of economists, engineers, academics and
business leaders around the world. One solution to this problem is the conversion of a
*Authorfor correspondence (
G. Najabour, H.Younesi, K.S.K. Ismail, A.R. Mohamed and A.H. Kamaruddin
low-value waste gas (synthesis gas) into a clean fuel, e.g. hydrogen (H2).Synthesis
gas is a mixture of carbon monoxide (CO) and hydrogen, which can be derived from
almost any source containing carbon [2]. Therefore, non-gaseous materials such as
biomass [3], coal [4],shale oil and tar sands [ 5 ] can be used as the raw material for
synthesis gas production. Agricultural wastes, which are abundantly available, can
also be gasified to produce synthesis gas. The composition of synthesis gas depends
upon the raw materials used, but usually the CO/H2molar ratio varied from 1:3 to 2: 1.
Usually the mixture of gases is deficient in hydrogen and rich in CO. In order for
the synthesis gas to be converted to fuels, the hydrogen concentration needs to be
increased. Conventionally,the process implemented was the Fischer-Tropsch reaction
where the water-gas shift reaction took place over supported metal oxide catalysts at
elevated temperatures. The reaction is shown as follows:
CO i- HzO ($ H2 + CO2
Apart from this reaction, increased biological research has identified some
microorganisms that could carry out similar reactions to the conventional chemical
processes. It has been discovered that photosynthetic bacteria, Cyanobacterium and
green algae, are active in photobiological hydrogen production [6]. Several
photosynthetic bacteria, such as Rhodobacter sp., Rhodopseudomonus gelatinosa,
Rhodospirillum rubrum, and a strictly anaerobic bacterium, Methanosarcina barkeri
are able to produce hydrogen. Among them, the photosynthetic purple non-sulphur
bacterium, R. rubrum, has much better criteria due to the high specific carbon
monoxide uptake and high conversion yield, close to the theoretical value [7].
R. rubrum was capable of growing photosynthetically under an anaerobic atmosphere
by utilizing CO, where CO was oxidized and hydrogen was produced [8]. This
reaction occurred under mild conditions,at ambient temperature and pressure, with the
formation of the specific products. All processes of biological hydrogen production
are fimdamentally dependant upon the presence of a hydrogen-producing enzyme. At
present, three enzymes carrying out this reaction are known, namely nitrogenase, Fehydrogenase, and Ni-Fe hydrogenase [9]. In photosynthetic bacteria, nitrogenase is
known as the main catalyst of hydrogen production [lo-121. The carbon monoxide
dehydrogenase(CODH) could be the key enzyme in CO metabolism [13]. Among the
metabolites of photosynthetic bacteria are organic acids or CO as single energy
source. During the fermentation process, bacteria need substrates such as glucose or
other carbon sources to obtain energy for growth, maintenance, and to produce coproducts such as organic acid, alcohols, and hydrogen during their metabolism [14].
Therefore, it is important to know the effect of carbon sources on bacterial growth and
hydrogen production. It was also reported that light and acetate are present during the
hydrogen formation phase, in which light was required for hydrogen evolution [ 151.
In this study, biological hydrogen production has been investigated using a
photosynthetic anaerobic bacterium, R. rubrum. Hydrogen production was studied
using acetate and malate as the carbon and energy sources. The purpose of this study
was to investigate the effect of initial carbon source on the hydrogen production.
Effect of agitation rate, mass transfer coefficient (KLa), and kinetics of the
bioconversion have also been studied.
Photobiological Hydrogen Productionji-om Synthesis Gas
Materials Used and Experimental Methods
(i) Propagation of Bacterium
The bacterium, Rhodospirillum rubrum (ATCC 25903), was obtained from the
American Type Culture Collection (ATCC), Virginia, USA. The strain obtained in a
freeze-dried condition was grown using ATCC media at 30°C under anaerobic
conditions. The culture was incubated under tungsten light.
The composition of growth media provided by ATCC in one liter solution was
prepared as follows: Malic acid (Merck) 2.5g neutralized with NaOH (Merck) at pH
6.9, Yeast Extract (Merck) lg, (NH4)2so4 (Merck) 1.25g, MgS04.7H20(Calbiochem)
0.2g, CaC12.2H20(Merck) O.O7g, Ferric citrate (Merck) O.Olg, EDTA (Sigma) O.O2g,
KH2PO4 (Sigma) 0.6g, K2HP04 (Sigma) 0.9g. Trace metal solution (1 ml);
ZnS04.7H20(Merck) O.Olg, MgS04.H20(Calbiochem) O.O2g, H3B03 (Merck) O.Olg,
Ferric Citrate (Merck) 3g, CuS04.5H20 (Merck) O.Olg, EDTA (Sigma) 0.5g,
(Sigma) O.O2g, CaC12.2H2O (Merck) 0.2g. B-Vitamin Solution
(7.5 ml); Nicotinamide (Sigma) 0.2g, Thiamine HCl (Sigma) 0.4g, Nicotinic acid
(Sigma) 0.2g, Biotin (Sigma) O.O08g, distilled water was added to make one liter
(ii) Experimental Description
The media composition for analyzing the effect of carbon source was similar to the
growth media explained above; only the malic acid was replaced with 2.5 and 6 g/l of
sodium acetate (Merck). A 50 ml of the liquid medium was distributed anaerobically
into serum bottles (Fisher Scientific, UK). The liquid media were sterilized at 121°C
for 15 minutes. After autoclave (Sebcta, Spain), the serum bottles were purged with
synthesis gas composed of 55% CO, 20% H2, 15% Ar, 10% C02(Sitt Tatt, Malaysia).
Argon was used as the internal standard. After cooling, the media were inoculated
with 5% (v/v) of seed culture using a sterile syringe (Becton Dickinson, Singapore).
The serum bottles were then placed horizontally on an orbital shaker (Stuart, UK) at
various agitation speeds (150 to 250 rpm). Experiments were performed at 30°C under
tungsten light (40 W) at 1000 lux. The light intensity was measured using a digital lux
meter (Sper Scientific, Taiwan).
(iii) Gas Analysis
Two hundred microliters of gas sample from the gas space of the serum bottle was
taken using a gas-tight syringe (Hamilton, Nevada). It was analysed by a gas
chromatograph (Perkin Elmer, Autosystem XL, USA) equipped with a Thermal
Conductivity Detector (TCD), a 15 ft x 1/8 inch Carboxen-1000 column (Supelco,
USA) with 100/120 mesh, and TotalChrom software was used. The oven temperature
was initially maintained at 40°C for 3.5 minutes and increased at the rate of 3O0C/min
to 220°C. The detector and injector temperatures were set at 200'C and 150°C
respectively. Helium (Sitt Tatt, Malaysia) was used as the carrier gas at a flow rate of
30 ml/min.
55 I
G. Najafiour, H. Younesi, K.S.K. Ismail, A.R.Mohamed and A.H.Kamaruddin
(iv) Biomass Quantification
About 1 ml of the culture was taken from the serum bottles at 12 hour intervals. The
diluted samples were poured into a quartz cuvette (Starna Brand, Essex) and the
optical cell density of liquid cultures was measured at the wavelength of 400 nm
using a spectrophotometer (Cecil 1000 series, UK). The absorbance and cell dry
weights were determined by a standard calibration curve used to read the cell
concentrationbased on optical density readings.
Results and Discussion
(0 Initid carbon source concentration
Malate and acetate were electron donors in the media. They were the most common
carbon sources for hydrogen production, which were utilized by photosynthetic
bacteria. Initially, R. rubrum was grown on acetate and malate under synthesis gas at
atmospheric pressure. Figure 1 shows the cell density of R. rubrum grown on malate
and acetate at different initial concentrations. It was found that the cell growth of R.
rubrum on malate was higher than on acetate.
0.3 - +Acetate
2.5 gll
6 QA
Malate 2.5 g/i
Time (days)
Figure 1. Cell density at different acetate and malate concentrations.
Comparing the three growth curves, it can be seen that at the same concentration
of 2.5 g/l, malate gave the highest cell density reaching 0.3 g/l compared to acetate of
only 0.15 g/l obtained. The growth of R. rubrum was doubled when grown on malate.
There was almost no growth observed with acetate concentration of 6 g/l, for the five
days of incubation period. This shows that acetate is a potential inhibitor when used at
PhotobiologicalHydrogen Production@om Synthesis Gas
high concentrations. The result indicated that cell growth varied with different carbon
sources. Inhibition was observed during the course of cell growth when the
microorganism was grown on high concentration of acetate (6 g/l), The preference of
growth shown in malate may be a result of the adaptation of bacteria with media
containing malate. It was also rehydrated fiom the freeze-dried condition using
malate as carbon source in the media.
Figure 2 shows the doubling time of R. rubrum on different initial malate and
acetate concentrations. The doubling time of R. rubrum was 8.4,31.8, and 68.6 hours
for 2.5 g/l malate, and 2.5 and 6 g/l acetate, respectively. The linear model shown in
Figure 2 for the growth of R. rubrum represents the exponential growth phase. By
comparing the slopes of the linear model for 2.5 g/l of acetate and 2.5 g/l of malate, it
can be seen that the specific growth rate of R. rubrum using malate is about 4 times
faster than acetate. However at 6 g/l of acetate, the doubling time was very long and
the growth was also slow, hence concluding that R. rubrum might be toxicated by the
high acetate concentration.
3.50 1
OAcetate, 2.m
rn Acetate, 6gil
A Malate,2.5g/l
-c 1.50
Time (days)
Figure 2. Doubling time of R. rubrum, grown on acetate and malate.
Experiments were carried out with 2.5 and 6 g/l of acetate in order to observe the
effect of initial concentration of carbon source on hydrogen production. The initial
acetate concentration was seen to have a significant effect on hydrogen production, as
well as the cell density of biomass. In the presence of malate, production of hydrogen
was notably lower than the use of acetate as electron donor.
Figure 3 shows the hydrogen production of R. rubrum using malate and acetate at
different concentrations. Evolution of hydrogen on acetate was observed when R.
rubrum was grown on a hgher concentration of acetate. From the hydrogen
production results in batch culture, 2.5 g/l acetate was found to give the highest
G. Najahour, H. Younesi, K.S.K. Ismail, A.R. Mohamed and A.H. Kamaruddin
production, 1.8 mmol Hz/l after 5 days of incubation. However, malate at the same
concentration was not showing enough hydrogen production. Even though malate
kept the cells growing at high densities, the hydrogen produced was not sufficient.
The hydrogen level with malate was about 0.25 mmol Hz/l for incubation period of
5 days. At 6 g/l of acetate, the hydrogen production was inhibited due to the low cell
density. In terms of hydrogen production, acetate was more favourable due to the
ability of acetate to be converted to acetyl-CoA and to initiate the tricarboxylic acid
(TCA) cycle. It was known that the hydrogen production in purple non sulfur bacteria
such as R. rubrum took place through the action of an anaerobic light-dependent TCA
cycle [16]. This indicated that acetate was a suitable carbon source but should only be
used in a moderated amount. Therefore, acetate was chosen as the suitable carbon
source throughout the batch reactor experiments because it gave high hydrogen
production at an adequate cell density.
5 1.8
E 1.4
Malate, 2.5 gll
2.5 gll
6 gA
3 0.8
& 0.4
2 0.2
= o
Time, days
Figure 3. Hydrogen production by R. rubrum on malate and acetate.
(ii) Shaking frequency
Mixing caused by shaking frequency has an mfluence on mass transfer. It is also
important to consider the transfer of sparingly soluble gases such as CO into the
media. More CO transferred into the cells resulted in higher hydrogen production.
The shaking frequencies tested were 150 to 250 rpm, and a static condition as blank.
Figure 4 shows the effect of agitation rates on CO consumption using 2.5 g/l of
acetate. From Figure 4, the partial pressure of CO dropped drastically at high
revolution rates of the shaker (200 and 250 rpm), while at 150 rpm and the static
condition, a very low CO uptake was observed. However, the most extreme drop in
CO partial pressure occurred in the agitated culture at 200 rpm.When the culture was
shaken at the higher rate of 250 rpm, the CO consumption started to drop. That was
probably due to the high shear causing cell damage and also resulting in insufficient
CO uptake.
Photobiological Hydrogen Productionfi-om Synthesis Gas
B 0*30
-0- 150 rpm
Erne, hr
Figure 4. Efect of shakingfi-equency on CO consumption.
Figure 5 shows the cell densities at various agitation rates. By comparing the
results between all the shaking rates and the blank, then 250 rprn gave the lowest cell
concentration. The cell densities at 150 and 200 rpm did not appear to produce
significant differences after a sufficient period of incubation. The maximum cell
concentration was approximately 0.35 gil. The lowest cell concentration was at 250
rpm, this was due to the shear effect caused by high agitation, whch resulted in cell
wall damage and also low CO uptake.
2 0.20
-0- 150 rpm
250 rpm
Time, hr
Figure 5. Efect of shakingfiequency on cell density.
G.Najafbour, H.Younesi, K.S.K. fsmail, A.R. Mohamed and A.H. Kamaruddin
In the static serum bottles (blank), the cell density reached the stationary phase
faster than shaken cultures and finally maintained at the same cell concentration with
cultures shaken at 150 and 200 rpm In static media, even though the cell growth was
high, without any agitation the CO may not be supplied adequately to the cells to be
converted to hydrogen. This result confirmed that even though the cell density was
high, without mixing the CO cannot be utilized by the cells. In other words, the CO
bubbles was not thoroughly mixed with the microbial culture, therefore, the interfacial
area of gas and liquid was limited. As a result, the oxidation of CO was also limited.
At high agitation rates, evolution of hydrogen was higher. This is clearly shown in
Figure 6. The hydrogen production at 250 rpm reached the highest level (0.43a h )
after 120 hours of incubation. The amount of hydrogen production at 150 rpm and the
stagnant condition was at the lowest level. The high partial pressure (in atm) showed
that the hydrogen production at 200 and 250 rpm were satisfactory, about 0.4 atm and
equivalent to 1.8 m o l e s of hydrogen. This was found to be in agreement with the
CO consumption result, where high CO consumption resulted in higher hydrogen
6 0.25
I" 0.10
Time, hr
Figure 6. Effect of shakingfiequency on hydrogenproduction.
(iii) Mass transfer studies
The transport of soluble substrate from gas phase to liquid phase has been described
by the following equation [17, 181:
Photobiological Hydrogen Productionfrom Synthesis Gas
where Q, is moles of CO transported; K,a is the overall mass transfer coefficient;
H is Henry's constant; P& is the partial pressure of carbon monoxide in the gas
phase; and P& is partial pressure of carbon monoxide in the liquid phase. The
material balance for CO and biomass in the gas and liquid phases is explained as
follows; rearranging the material balance for carbon monoxide in the gas phase,
where it has been expressed for the dissolved carbon monoxide in the liquid phase,
resulted in the following equation:
H 1 dNG,
pLW =pk+--K,a V,
The cell growth rate is given by:
x dt
The CO balance in the gas phase is given by:
1 dNk
- K,a
- -(P&
An assumption was made that the rate of reaction is completely controlled by the rate
of CO transported to the liquid phase, and all the CO was utilized by microorganisms.
Therefore, P& = 0 . Then Equation ( 5 ) can be simplified to yield the following
A plot of the rate of CO disappearance per volume of liquid versus partial
pressure of CO in the gas phase based on Equation (6) would give a straight line with
a slope of K,a/H . This is shown in Figure 7, where H, the Henry constant for CO at
30°C,is 1076 atm.Wmole [19]. From Figure 7, the KLa values at 200 and 250 rpm
were determined. The values of KLaobtained from the slopes of the lines at both 200
and 250 rpm were found to be very close, i.e. 0.48 h8. Based on these results, 200
rpm was chosen as the optimum shaking frequency for the batch bioconversion since
further increase did not enhance KLa.
(iv) Kinetics studies
The data for kinetics studies was obtained from the initial carbon source study. Figure
8 shows the cell density and the concentration of CO in the liquid phase using 2.5 g/l
of acetate in the liquid media shaken at 200 rpm It was observed that high cell
density resulted in high CO uptake. The entire CO was consumed within 4 days.
G. Najabour, H. Younesi, K.S.K. Ismail, A.R. Mohamed and A.H. Kamaruddin
0.25 -
0.20 -
Linear (200 rpm)
0.15 -
y = 0.4559~
R2 = 0.9851,250 rpm
0.10 -
0.00 7
Figure 7. Determination of mass transfer coefficient at 200 and 250 rpm.
Time (days)
Figure 8. Cell density and the concentrationof CO in the liquidphase.
In order to describe the kinetics parameters, Andrews expanded the simple Monod
equation (Vega et al., 1989):
1 dx
x dt
K, +P&
Photobiological Hydrogen Production porn Synthesis Gas
where pm is the maximum specific growth rate, and K, is the Monod constant for
growth. Equation (7) has been modified to include the substrate inhibition model as
given by:
K, + Pk + (P&)* / K i
where Ki is the substrate lnhibition constant. In order to obtain the maximum specific
growth rate and Monod constant, a plot of 1/p versus l/P& was made to monitor the
linear region. The data are shown in Figure 9, and the intercept with the x-axis
represents the value of -l/K,,, hence K,, is 0.14 atm. The intercept with the y-axis
represents I l k , and hence by calculation pm= 9.8 h-'.
To compute the substrate inhibition constant, Equation (8) can be rearranged as
The value of Ki was obtained using Sigma Plot Ver. 5.0 to yield the best correlation as
shown in Figure 10. This is a plot of partial pressure of CO in the liquid phase
reciprocal to the specific growth rate versus partial pressure of CO in the liquid phase.
The y-intercept is zero showing that no inhibition occurred for CO concentration of
0.56 atm utilizing 2.5 g/l of acetate. The same model can be used to investigate
mhibition at higher CO concentrations.
Figure 9. Determination of specific growth rate in liquid phase and Monod constant.
G. Najafour, H. Younesi, K.S.K. Ismail, A.R. Mohamed and A.H. Kamaruddin
Figure 10. Andrews modelfor substrate inhibition.
Hydrogen was successfully produced at ambient temperature and pressure utilizing
CO as substrate. The initial carbon source concentration was discovered to have a
strong effect on hydrogen production and cell density of R. rubrum. In the presence
of malate, production of hydrogen was notably lower than the use of acetate as
electron donor. R. rubrum could grow in a lower acetate concentration and at mild
conditions and increase hydrogen production. High concentrations of acetate caused
inhibition of hydrogen formation and slight decrease in cell density. A maximum
hydrogen production rate was obtained in a medium containing 2.5g/l acetate shaken
at 200 rpm. The CO consumption also depended upon the shalung frequency, where
the highest hydrogen produced was at 200 and 250 rpm. Shaking frequency of higher
than 200 rpm did not improve KLa, where the highest KLaachieved was 0.48 h-’. For
lunetics studies, Andrews model was chosen to show that CO concentration of
0.56 atm is not inhibiting the bioconversion, and can be used for fiuther studies.
This research was made possible through an IRPA grant no. 03-02-05-9016,
sponsored by Ministry of Science, Technology & Environment (MOSTE) and
Universiti Sains Malaysia. The authors wish to thank the R&D panel, Universiti Sains
Malaysia and MOSTE for their financial support.
Photobiological Hydrogen Production porn Synthesis Gas
Henry's law constant (L admole)
Overall mass transfer coefficient transported (h-')
Substrate inhibition constant (atm)
Monod constant (mole/l)
Monod constant for growth ( a h )
Amount of CO in the gas phase ( m o l e )
Amount of CO in the liquid phase ( m o l e )
Partial pressure of A in gas phase (am)
Partial pressure of CO in gas phase (atm)
Partial pressure of CO in liquid phase (am)
Volumetric gas flow rate (m3/min
Time (h)
Liquid volume (L)
Cell density (g/l)
Specific growth rate (h')
Maximum specific growth rate (h-I)
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