CO2 capture from air by Chlorella vulgaris microalgae in an airlift photobioreactor

Accepted Manuscript CO2 capture from air by Chlorella vulgaris microalgae in an airlift photobioreactor Aziz Sadeghizadeh, Farid Farhad dad, Leila Moghaddasi, Rahbar Rahimi PII: DOI: Reference:

S0960-8524(17)31051-9 http://dx.doi.org/10.1016/j.biortech.2017.06.147 BITE 18384

To appear in:

Bioresource Technology

Received Date: Revised Date: Accepted Date:

30 April 2017 24 June 2017 26 June 2017

Please cite this article as: Sadeghizadeh, A., Farhad dad, F., Moghaddasi, L., Rahimi, R., CO2 capture from air by Chlorella vulgaris microalgae in an airlift photobioreactor, Bioresource Technology (2017), doi: http://dx.doi.org/ 10.1016/j.biortech.2017.06.147

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CO2 capture from air by Chlorella vulgaris microalgae in an airlift photobioreactor Aziz Sadeghizadeha , Farid Farhad dada, Leila Moghaddasib, Rahbar Rahimia,*

*

Corresponding author: E-mail address: [email protected]

Tel: +989151419052

a

Department of Chemical Engineering, University of Sistan and Baluchestan, Zahedan, P.O.Box.98164-161, Iran b Natural Resources Department, Islamic Azad University, Bandar Abbas, P.O. Box.79158-93144, Iran

Abstract In this work, hydrodynamics and CO2 biofixation study was conducted in an airlift bioreactor at the temperature of 30 ± 2° C. The main objective of this work was to investigate the effect of high gas superficial velocity on CO 2 biofixation using Chlorella vulgaris microalgae and its growth. The study showed that Chlorella vulgaris in high input gas superficial velocity also had the ability to grow and remove the CO 2 by less than 80% efficiency. Keywords: Airlift, Holdup; Chlorella vulgaris; Bio-fixation; CO2 Capture 1.

Introduction Human population growth and industrial expansion lead to increased energy

consumption and the use of fossil fuels. Fossil fuel combustion releases carbon dioxide (CO2) and water vapour into the atmosphere. The CO2 is a pollutant that causes the greenhouse effect (Basu et al., 2014; Cheah et al., 2015). More than 50 percent of global warming is due to CO2 emissions into the atmosphere. Hence, it is necessary to reduce the uncontrolled emissions of CO2 and to prevent its release into the atmosphere (Wilbanks & Fernandez, 2014). Great efforts have been made by the international community to reduce CO2 emissions in the atmosphere. For instance, the Kyoto Protocol in 1997 and Paris COP 21 in 2015, advocate international restrictions on CO2 release (Nations, 2015). There are two general approaches to reduce emissions of CO2 into the atmosphere. One

way is to reduce consumption of fossil fuels, and the other, moving toward renewable energy, is to capture and utilize CO2. Among the CO2 capture methods, can be cited chemical absorption and the biological fixation process (Chiang et al., 2011; Kaithwas et al., 2012). The biological sequestration process can be performed using plants or microorganisms. Microalgae and cyanobacteria are among the microorganisms that consume CO2 to grow and lead to CO2 fixation. Microalgae and cyanobacteria also have the most conversion efficiency of CO2 into oxygen and biomass products (Chisti, 2007). The CO2 removal by microalgae depends on different parameters such as microalgae species, type of cultivation system, nutrients ratio, light intensity, temperature, pH, CO 2 concentration, and gas flow rate (Cheng et al., 2013). Many studies have been done on CO2 fixation using different algae species. Among them, Chlorella vulgaris, which can tolerate high concentrations of CO2, has high photosynthetic capacity, and can maintain high growth rate and CO 2 fixation rate in a wide range of CO2 concentrations from 0.04 to 18% (v/v), can be considered as a good species to fix CO2 (Singh & Singh, 2014; Yang et al., 2015). Algae cultivation systems play a crucial role in the process of CO 2 fixation. There are two types of algae cultivation system for fixing CO2 that include open raceway ponds and closed photobioreactors. Closed photobioreactors compared to open ponds provide better control of operating conditions and increase the efficiency of biofixation (Kasiri et al., 2015; Razzak et al., 2013). Other advantages of the bioreactor in the field of biochemicals are the ease of sterile operations and suitable hydrodynamics for biocatalysts sensitive to the tension and turbulence. Moreover, bioreactors have industrial applications such as in

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wastewater treatment, and in chemical and biochemical processes (Chisti, 1998). Different bioreactors could be employed in biochemical processes. Among them, simple bubble column and airlift reactor (ALR) with internal loop and external loop can be cited. ALR has better mixing, more suitable heat, and mass transfer than bubble column due to the existence of the draft tube, and some of its advantages include simple construction without moving parts such as agitator and low consumption of energy (Chen et al., 2016; Chisti, 1998). As CO2 and nutrients are essential for algal growth, ALR hydrodynamic parameters such as gas holdup and liquid circulation velocity play a key role. The gas holdup and liquid circulation velocity are a function of the input gas flow rate (Bitog et al., 2014; Nayak et al., 2014). In addition, the gas flow rate plays a great role in the algae growth, control of pH, creating optimal internal mixing, and preventing the accumulation of oxygen in the system (Kumar et al., 2010). Most of the studies in the CO2 biofixation field have focused on the effect of different levels of CO2, the impact of microalgae species, the effect of temperature, and the effect of light intensity on the rate of CO2 fixation (Basu et al., 2013; Cheng et al., 2013). The aim of this work was to investigate the effect of high gas superficial velocity on CO2 capture from air using Chlorella vulgaris microalgae and its growth in an airlift photobioreactor with internal loop and internal sparger in constant light intensity and gas CO2 level. This technology reduces CO2 emissions into the atmosphere and helps in reducing global warming. ALR hydrodynamics was also evaluated under different input gas superficial velocities.

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2. Materials and Methods 2.1. Culture Medium Chlorella vulgaris culture used in this study was provided by the Institute of Marine Sciences of Bandar Abbas in the amount of 20 L containing seawater and modified f/2 culture medium of Gillard (Guillard & Ryther, 1962) as nutrient with initial cell concentration about 5 × 106 cell/ml. Each litre of modified f/2 culture medium of Gillard contains 75g NaNO3, 5g NaH2PO4.H2O, 30g Na2SiO3.9H2O, 4.36g Na2.EDTA, 3.15g FeCl3.6H2O, 0.18g MnCl2.4H2O, 0.01g CoCl2.6H2O, 0.0098g CuSO4.5H2O, 0.022g ZnSO4.7H2O, 0.0063g Na2MoO4.2H2O, 0.1g vitamin B1, 0.0005g vitamin B12, and 0.0005g Biotin. 2.2. Laboratory setup and process conditions The schematic of the experimental design of ALR used in this study is shown in Fig. 1a. The ALR was made using plexiglass. The ALR floor was sealed by an o–ring gasket. The sparger was built from a stainless steel tube. The schematic diagram of the experimental setup used in the study is shown in Fig. 1b. In order to supply gas flow, an air compressor and CO2 cylinder were used. To achieve the desired concentration of CO 2 in the mixture of CO2/air, two rotameters were also used for measuring flow rates of air and CO 2, separately. Gas was sparged into the reactor through an internal sparger. A 100W heater (Sobo HC– 100 model) was used in the reactor to provide the constant temperature. Experiments were carried out at 30 ± 2° C. In all experiments, a volume of 20 L was considered for the bioreactor working volume. The ALR was filled to the height of 1.1 m prior to aeration. The experiments were conducted in two stages.

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In the first stage, the ALR was filled with 20 L tap water. The hydrodynamic of ALR was studied including gas holdup and liquid circulation velocity for the air–water system. The inlet gas superficial velocity range was 1.627 × 10-3–13.281 × 10-3 m/s at constant atmospheric pressure. In the second stage, the ALR was filled with 20 L algae culture. Enriched air, including 2% (v/v) CO2 (20,000 ppm) was sparged continuously in algae culture at two gas superficial velocities of 7.458 × 10-3 and 13.281 × 10-3 m/s for CO2 fixation, separately. The bioreactor was exposed under uniform light intensity of 1800 Lux using four fluorescent lamps with a light/dark cycle of 12:12 h for 11 days. The light intensity in the bioreactor was measured by a lux meter (TES–1339R, TES, Taiwan). During the culture periods, samples were taken at 24 h periods from the bioreactor effluent flow and algae culture medium in order to measure the outlet CO 2 concentration and the cell concentration of biomass, respectively. 2.3. Gas superficial velocity Gas superficial velocity in multiphase flow is considered as a hypothetical flow velocity. The gas superficial velocity,

(m/s), was calculated by using Eq. (1) (Chisti, 1989): (1)

where Qg is the gas flow rate (m3/s) and Ar is the cross-sectional area of riser (m2). 2.4. The gas holdup and bubble rise velocity The gas holdup was measured by observing the liquid height before (hi) and after aeration (hf). The gas holdup, bubble rise velocity,

was calculated by using Eq. (2). For the calculation of

(m/s), Eq. (3) was employed (Chisti, 1989; Yee-keung & Kin-

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chung): (2)

(3)

2.5. Liquid circulation velocity Linear velocity in the downcomer section was obtained by a conductivity meter probe (Hanna Instruments, USA, model HI8733) and the signal response of the probe to inject brine solution. The probe was placed horizontally at a distance of 0.11 m from the floor of the column in the downcomer section. The final results of the liquid linear velocity in the downcomer section were the average of four times’ measurement, using the above method. Brine solution was injected from a distance of 1.1 m from the floor of the column. The liquid linear velocity in the downcomer, Vld (m/s), was calculated using Eq. (4). Since the liquid superficial velocity in multiphase flow was more practical, therefore, the liquid superficial velocity in the downcomer,

(m/s), was calculated by using Eq. (5). In

addition, the liquid superficial velocity in the riser,

(m/s), was calculated by the

continuity equation (Eq. (6)) (Merchuk & Garcia Camacho, 1999). (4) (5) (6)

where Ad and Ar were cross-sectional areas of the downcomer and riser (m2), tm and lm were response time (s) and the distance between the brine injection and probe response (m).

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2.6. Determining the cell concentration, maximum growth rate and double time In order to evaluate the growth rate of microalgae during CO2 fixation, cell concentration, x (cell/ml), was measured using daily sampling and counting by biological microscope (Novel Optics Co. Ltd, China, model N–180M). In order to calculate the specific growth rate, μ(day -1), Eq. (7) was used (Abreu et al., 2012):

(7)

where x1 and x2 represent biomass cell concentration (cell/ml) at the culture time of t 1 and t2 (day) at the beginning and the end of each phase of the biomass growth. The slope of the ln(x) versus culture time curve was equal to specific growth rate, but in order to calculate the maximum growth rate, µmax(day -1), a linear regression on the logarithmic growth phase was considered (da Rosa et al., 2015). Although the specific growth rate refers to the ability of the biomass growth, double time is more meaningful and understandable than the growth rate. Double time is the time in which the number of living cells is doubled. The larger value of double time indicates a slower growth. The double time,

(day), was calculated

by using Eq. (8) (RAJASEKARAN et al., 2015). (8)

2.7. Estimating the CO2 removal efficiency In order to estimate the CO2 removal efficiency, the CO2 concentration was controlled and measured in input and output flow. The CO2 concentration in the input mixture flow of air/CO2 was set on 2% (v/v). The final result of the output CO2 concentration from the bioreactor (ppm), was an average of 20 times measurement during the day by the CO 2 8

meter (Testo, Germany, model 535). The CO2 removal efficiency (%) was calculated by using Eq. (9) (Cheng et al., 2013; Cheng et al., 2006). (9)

3.

Results and discussion

3.1. The gas holdup The result showed that with the increase of input gas velocity from 1.627 × 10 -3 to 13.281 × 10-3 m/s, the gas holdup increased linearly from 0.0044 to 0.024. The result is in agreement with Blažej et al. (2004) and Popović et al. (2004). At the riser gas superficial velocity lower than 6.955 × 10-3 m/s, the dominant regime was homogeneous bubbly flow. In this region, with increasing the gas superficial velocity, the amount of gas holdup linearly increased up to 0.015. The bubbles in this region were small and uniform and independently without coalescence and collision rise in a spiral path in the liquid. Furthermore, in the low gas velocities, the most bubbles had enough time to be separated from the liquid in the separator section. As a result, the amount of gas holdup in the downcomer section was negligible (Bello et al., 1985). With increasing gas superficial velocity, the flow regime passed into the transition region. This flow regime occurred in the gas superficial velocity of 6.955 × 10-3 m/s. During the transient flow regime, the number of bubbles increased and bubble coalescence began. Bigger bubbles formed due to the bubble coalescence. Big bubbles had higher rise velocity than small bubbles and, therefore, the retention time of big bubbles decreased. Fig. 2 showed that with the increase of input gas velocity from 1.627 × 10-3 to 13.281×10-3 m/s, bubble rise velocity enhanced from 0.36 to

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0.53 m/s and bubble rise time decreased from 2.7 to 1.9 s. In a similar study, Kommareddy and Anderson (2004) observed that with increase of input gas velocity, bubble rise velocity increases and bubble rise time decreases. This was a factor that reduced the slope of gas holdup versus gas superficial velocity in transient flow regime than the bubbly flow. The gas holdup in the region increased up to 0.024 at the gas velocity of 13.281 × 10 -3 m/s. In general, increasing the amount of gas holdup, on one hand, increases the driving force of liquid circulation and, on the other, increasing the interfacial gas–liquid leads to increase of mass transfer driving force (Bello et al., 1985). 3.2. Liquid circulation The liquid circulation in the ALR is caused by the fluid density difference and, thus, hydrostatic pressure difference between the riser and downcomer (Chisti et al., 1988). The amount of gas holdup in the downcomer was very low and negligible. The low gas holdup value in the downcomer section, on the one hand, and a greater amount of gas holdup in the riser section, on the other, caused liquid circulation in the ALR. The liquid circulation time in the downcomer as a function of the riser gas superficial velocity is shown in Fig. 3. The result showed that with the increase of input gas velocity from 1.627 × 10 -3 to 13.281 × 10-3 m/s, the liquid circulation time in the downcomer decreased from 11.5 to 5.7 s. At low velocities of input gas, liquid circulation time was strongly dependent on gas superficial velocity. By the increase of input gas superficial velocity, the amount of liquid circulation time decreased and the slope of liquid circulation time versus gas superficial velocity reduced. This is because the amount of gas holdup in the bubbly flow increases significantly. Therefore, the difference between gas holdup in the riser and the downcomer

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increases. The driving force of liquid circulation also increases and ultimately the liquid circulation time decreases. That clearly shows the dependency of liquid velocity on the gas holdup. With the arrival to the transition region, a slight increase of pressure difference occurs between the riser and the downcomer sections. Therefore, the liquid circulation time and liquid velocity in transient flow are less dependent on gas superficial velocity than bubbly flow (Gavrilescu & Tudose, 1995). As a result, the slope of the liquid circulation time and liquid superficial velocity versus gas superficial velocity reduces. In addition, Fig. 3 presented the liquid superficial velocity in the downcomer and riser as a function of gas superficial velocity, respectively. The results indicated that an increase in the gas superficial velocity increased the liquid superficial velocities in the riser and the downcomer. Similar results were also obtained by Nikakhtari and Hill (2005) and Kilonzo et al. (2010). Besides this, the liquid superficial velocity in the riser, according to the continuity equation with

ratio, was higher than the liquid superficial velocity in the

downcomer. 3.3. The growth of microalgae The effect of input gas superficial velocity on cell concentration over culture time is presented in Fig. 4. The results showed that with increasing input gas superficial velocity, microalgae growth decreased and, as a result, biomass decreased. Moreover, at a constant gas superficial velocity, the biomass increased over the culture time until the cell concentration reached the maximum, on the last day. In similar works, Anjos et al. (2013) showed that at low levels of gas flow rate and constant gas CO 2 level of 2%, the maximum biomass concentration of Chlorella vulgaris was obtained in maximum gas flow rate in a

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bubble column with working volume of 0.09 L. In addition, Merchuk et al. (2000) studied the effect of gas superficial velocity on Porphyridium Sp biomass concentration in an ALR. Although they observed that, with increasing gas superficial velocity to 1.6 × 10 -3 m/s, the maximum biomass concentration increased, they concluded that the gas velocity above 1.6 × 10-3 m/s reduced the maximum biomass concentration and may be harmful to microalgae. Whereas the effect of the gas flow rate on biomass concentration in their study was confirmed in our present work, the present study showed that in gas velocity 8 times higher than 1.6 × 10-3 m/s and large working volume of bioreactor, the Chlorella vulgaris can be grown. Our result indicated that the maximum cell concentration in the gas superficial velocity of 7.458 × 10-3 and 13.281×10-3 m/s was obtained as 23.5 × 106 and 18.3 × 106 cell/ml, respectively. In high gas superficial velocity, despite the low gas superficial velocity, the effect of gas retention time in the bioreactor has more preference compared to mixing and turbulence effect while, at low gas velocities, there is a direct correlation between the input gas superficial velocity and the growth of microalgae due to more gas retention time and sufficient mass transfer. At too low input gas superficial velocities, turbulence caused by aeration to prevent clotting, microalgae settling, and supply nutrients throughout the culture medium was not sufficient and cannot provide good mass transfer. By increasing input gas superficial velocity, a better mixing was performed in the bioreactor and mass transfer of gas–liquid increased. This increase in gas velocity not only avoided the settling of microalgae but also led to the spread of microalgae in all regions of the bioreactor and higher photonic energy absorbed for the photosynthesis of algae, consequently. Besides, aeration removes generated and accumulated oxygen during the photosynthesis from the culture medium. The presence of accumulated oxygen in the 12

culture medium leads to the reduction of photosynthesis efficiency (Camacho et al., 2011). At high gas velocity, by increasing input gas superficial velocity, bubble rise time decreased. The bubble rise time in the gas superficial velocity of 7.458 × 10 -3 and 13.281 × 10-3 m/s was obtained as 2.2 and 1.9 s, respectively. Therefore, where gas velocity is low, CO2 molecules are much vicinity to microorganisms. Thus, in high gas superficial velocity, the opportunities for microorganisms to consume CO2 decreased and, as a result, algal growth was reduced. In addition, although the high input gas superficial velocity may be harmful to microalgae cells and prevent the growth and even cause death due to shear stress, Chlorella vulgaris demonstrated that it is able to grow even under high input gas superficial velocity. In summary, it can be said that the effect of gas superficial velocity has an impact on the growth due to the shear stress, gas retention time, and CO 2 absorption in the media based on mass transfer and the solubility of CO2 in the media. Fig. 5 depicted the effect of gas superficial velocity on the growth rate over culture time. The result indicated that in both input gas superficial velocities during the first day, the lag phase is dominant on algae culture, and in this phase, the microorganisms adapted to the new condition and the specific growth rate was approximately equal to zero. The accelerating growth of cells in logarithmic phase (log) occurred in the period of 1 to 5 days. The maximum specific growth rate was obtained through linear regression in this phase. Maximum specific growth rate and doubling time results showed that with increasing gas superficial velocity and consequently retention time reduction, the amount of μ max reduced. By reducing the maximum specific growth rate, doubling time increased. In the same study, Zheng et al. (2012) (bubble column with working volume of 1 L) and Merchuk et al. (2000)

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observed that with increasing gas superficial velocity to 1.6 × 10 -3 m/s, the maximum specific growth rate of Chlorella vulgaris and Porphyridium Sp increased to 1.22 day-1 (double time of 0.56 day) and 0.48 day-1 (double time of 1.4 day) and then decreased. In our present work, the result demonstrated that maximum specific growth rate in the gas superficial velocities of 7.458 × 10-3 and 13.281×10-3 m/s were 0.2446 (R2 = 0.99) and 0.1843 day-1 (R2 = 0.97) and double time was 2.83 and 3.76 day, respectively. Although in the present work, similar to other studies, the maximum specific growth rate in high gas velocity decreased by increasing gas velocity, it showed Chlorella vulgaris’ resistance against shear stress. On the fifth day, the specific growth rate decreased sharply in both gas superficial velocities. During days 5 to 8, the cells went through the declining growth phase where specific growth rate was less than the maximum specific growth rate. That could be due to exhaustion of nutrients or inhibitory products that lower growth rate of algae. Finally, from days 8 to 11, the cells and culture medium went through a stationary phase. In this phase, the cell concentration was relatively constant and maximum cell concentration was achieved and the specific growth rate was approximately equal to zero. The summary of algal growth parameters, including the maximum cell concentration, x max(cell/ml), the maximum specific growth rate, μmax(day-1), and the double time, t D(day), in two input gas superficial velocities,

(m/s), are shown in Table 1.

3.4. CO2 removal When CO2 enters the reactor, it reaches equilibrium with the aqueous phase. Then CO 2, after passing through the gas–liquid film resistances, comes to the microorganism surface. Finally, during the photosynthesis reaction, CO2 is consumed and fixed in the presence of

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light and, therefore, biomass is produced (Cheng et al., 2013; Concas et al., 2012). Fig. 5 shows the effect of input gas superficial velocity on the concentration of output CO 2 from the top of the bioreactor over culture time, also. The result shows that at the end of the first day, the output CO2 concentrations from the top of the bioreactor in the gas superficial velocities of 7.458 × 10-3 and 13.281 × 10-3 m/s were 6300 and 10,000 ppm, respectively. Furthermore, these values on the last day were 4000 and 7200 ppm, respectively. The result demonstrated that the outlet CO2 concentration decreased over culture time in both gas velocity due to the increase of cell concentration and consumption of CO 2 during photosynthesis. Also, the culture viscosity is enhanced by increasing the culture cell density, which subsequently reduces outlet CO2 concentration due to increasing gas retention time and CO2 consumption (Chiu et al., 2008). As the input gas superficial velocity increases, the CO2 concentration from the top of the reactor increases due to the reduction of gas retention time and thus reduction of CO 2 consumption. More, the effect of gas superficial velocity on the CO2 removal efficiency over culture time has been shown in Fig. 6. The result showed that the CO2 removal efficiency increased over culture time in both gas velocities. In addition, the results demonstrated that with increasing input gas superficial velocity, CO2 removal efficiency decreased. Moreover, during the culture period, the average CO2 removal efficiency in gas superficial velocities of 7.458 × 10 -3 and 13.281×10-3 m/s were 76 and 57% respectively. The maximum CO2 removal efficiency was achieved in the maximum cell concentration of microalgae on the 11 th day and the maximum CO2 removal efficiencies in gas superficial velocities of 7.458 × 10 -3 and 13.281×10-3 m/s were 80 and 64%, respectively. The CO2 removal efficiency increased with increasing cell concentration. The result indicated that the CO 2 removal efficiency 15

increases linearly with the culture time in gas superficial velocities of 7.458 × 10 -3 and 13.281 × 10-3 m/s with the slope of 1.12 (R2 = 0.94) and 1.45 (R2=0.99), respectively. In similar works, Li et al. (2011) showed that with increasing gas flow rate from 0.05 to 0.5 vvm, the maximum CO2 removal efficiency of S. obliquus WUST4 obtained was 67% in 0.1 vvm of flow rate in an ALR (working volume of 0.1 m3), with operation condition of 12,000 Lux light intensity, and gas CO2 level of 12%. In addition, in gas flow rate of 0.5 vvm, CO2 removal efficiency decreased to 20%. Furthermore, although Ong et al. (2010) demonstrated that the CO2 fixation rate of Chlorella sp. MT–7 and Chlorella sp. MT–15 enhanced in a vertical bubble column with working volume of 40 L and gas CO2 level of 5%, by increasing gas flow rate from 10 to 20 L/min, Hulatt and Thomas (2011) indicated that in gas superficial velocities of 1 × 10-3, 2 × 10-3 and 5 × 10-3 m/s, the CO2 fixation efficiency of Chlorella vulgaris were 14.6, 8.5 and 3.8% in a bubble column with working volume of 1.4 L and gas CO2 level of 4%, and concluded that CO2 fixation efficiency decreases by increasing gas superficial velocity. Although, in our present work, in high gas velocity, the maximum CO2 removal efficiency decreased by increasing the gas superficial velocity, the Chlorella vulgaris can remove CO2 with efficiency of less than 80%. Briefly, although too low gas superficial velocity provides high gas retention time, it cannot provide sufficient mass transfer for CO2 and leads to low CO2 biofixation productivity. When CO2 molecules have sufficient time in the vicinity of microorganisms, CO 2 consumption increases. In addition, high gas superficial velocity provided better mass transfer for CO2 but decreased gas retention time for CO2 consumption. Since the bubble coalescence leads to further increase of bubble rise velocity, therefore, some of the reduction in the gas retention time is due to bubble coalescence. So in low gas superficial velocity, CO2 16

consumption is enhanced by increasing gas superficial velocity due to good mass transfer and sufficient gas retention time while in high gas superficial velocity, CO2 consumption decreases by increasing gas superficial velocity due to insufficient gas retention time in culture medium. The result demonstrated that Chlorella vulgaris in high gas superficial velocity of input gas also had the ability to grow and to fix the CO 2 despite the presence of shear stress. The CO2 removal efficiency slope versus culture time in both gas superficial velocities represents an increase in growth and the cell concentration of Chlorella vulgaris biomass, during the early days. On the fifth day, with the decrease of biomass growth rate due to the nutrients’ deficiency, CO2 removal efficiency slope got lower. 4.

Conclusion The study presented that the Chlorella vulgaris has the ability of growth and CO2

capture at high input gas superficial velocities and can resist shear stress. The results showed that with increasing input gas superficial velocity, the gas holdup and liquid superficial velocity in the riser increased. Furthermore, the maximum cell concentration, specific growth rate and CO2 removal efficiency in gas superficial velocity of 7.458×10-3 and 13.281×10-3 m/s were 23.5×106 and 18.3×106 cell/ml, 0.2446 and 0.1843 day-1, 80 and 64%, respectively. Therefore, Chlorella vulgaris can be a good choice for the CO2 capture of flue gasses in high gas velocity. Acknowledgment. This work was supported by the Research and Technology Organization and Department of Chemical Engineering of the University of Sistan and Baluchestan, Iran. Authors would like to express their appreciation to Marine Sciences, Bandar Abbas, Iran 17

for providing the required amount of Chlorella vulgaris microalgae.

Reference 1. Abreu, A.P., Fernandes, B., Vicente, A.A., Teixeira, J., Dragone, G. 2012. Mixotrophic cultivation of Chlorella vulgaris using industrial dairy waste as organic carbon source. Bioresource technology, 118, 61-66. 2. Anjos, M., Fernandes, B.D., Vicente, A.A ,.Teixeira, J.A., Dragone, G. 2013. Optimization of CO 2 bio-mitigation by Chlorella vulgaris. Bioresource technology, 139, 149-154. 3. Basu, S., Roy, A.S., Mohanty, K., Ghoshal, A.K. 2014. CO 2 biofixation and carbonic anhydrase activity in Scenedesmus obliquus SA1 cultivated in large scale open system. Bioresource technology, 164, 323-330. 4. Basu, S., Roy, A.S., Mohanty, K., Ghoshal, A.K. 2013. Enhanced CO 2 sequestration by a novel microalga: Scenedesmus obliquus SA1 isolated from biodiversity hotspot region of Assam, India. Bioresource technology, 143, 369-377. 5. Bello, R.A., Robinson, C.W., Moo‐Young, M. 1985. Gas holdup and overall volumetric oxygen transfer coefficient in airlift contactors. Biotechnology and bioengineering, 27(3), 369-381. 6. Bitog, J.P.P ,.Lee, I.-B., Oh, H.-M., Hong, S.-W., Seo, I.-H., Kwon, K.-S. 2014. Optimised hydrodynamic parameters for the design of photobioreactors using computational fluid dynamics and experimental validation. Biosystems engineering,

18

122, 42-61. 7. Blažej, M., Kiša, M ,.Markoš, J. 2004. Scale influence on the hydrodynamics of an internal loop airlift reactor. Chemical Engineering and Processing: Process Intensification, 43(12), 1519-1527. 8. Camacho, F.G., Rodríguez, J.G., Mirón, A.S., Belarbi, E., Chisti, Y., Grima, E.M .

.1122Photobioreactor scale-up for a shear-sensitive dinoflagellate microalga. Process Biochemistry, 46(4), 936-944. 9. Cheah, W.Y., Show, P.L., Chang, J.-S., Ling, T.C., Juan, J.C. 2015. Biosequestration of atmospheric CO 2 and flue gas-containing CO 2 by microalgae. Bioresource technology, 184, 190-201. 10. Chen, Z., Jiang, Z., Zhang, X., Zhang, J. 2016. Numerical and experimental study on the CO 2 gas–liquid mass transfer in flat-plate airlift photobioreactor with different baffles. Biochemical Engineering Journal, 106, 129-138. 11. Cheng, J., Huang, Y., Feng, J., Sun, J., Zhou, J., Cen, K. 2013. Improving CO 2 fixation efficiency by optimizing Chlorella PY-ZU1 culture conditions in sequential bioreactors. Bioresource technology, 144, 321-327. 12. Cheng, L., Zhang ,L., Chen, H., Gao, C. 2006. Carbon dioxide removal from air by microalgae cultured in a membrane-photobioreactor. Separation and purification technology, 50(3), 324-329. 13. Chiang, C.-L., Lee, C.-M., Chen, P.-C. 2011. Utilization of the cyanobacteria Anabaena sp. CH1 in biological carbon dioxide mitigation processes. Bioresource 19

technology, 102(9), 5400-5405. 14. Chisti, M., Halard, B., Moo-Young, M. 1988. Liquid circulation in airlift reactors. Chemical Engineering Science, 43(3), 451-457. 15. Chisti, Y. 1989. Airlift bioreactors Elsevier Applied Science, New York. 16. Chisti, Y. 2007. Biodiesel from microalgae. Biotechnology advances, 25(3), 294306. 17. Chisti, Y. 1998. Pneumatically agitated bioreactors in industrial and environmental bioprocessing: hydrodynamics, hydraulics, and transport phenomena. Applied Mechanics Reviews, 51, 33-112. 18. Chiu, S.-Y., Kao, C.-Y., Chen, C.-H., Kuan, T.-C., Ong, S.-C., Lin, C.-S. 2008. Reduction of CO 2 by a high-density culture of Chlorella sp. in a semicontinuous photobioreactor. Bioresource technology, 99(9), 3389-3396. 19. Concas, A., Lutzu, G.A., Pisu, M., Cao, G. 2012. Experimental analysis and novel modeling of semi-batch photobioreactors operated with Chlorella vulgaris and fed with 100%(v/v) CO 2. Chemical engineering journal, 213, 2.120-10 20. da Rosa, G.M., Moraes, L., Cardias, B.B., Costa, J.A.V. 2015. Chemical absorption and CO 2 biofixation via the cultivation of Spirulina in semicontinuous mode with nutrient recycle. Bioresource technology, 192, 321-327. 21. Gavrilescu, M., Tudose, R .2991 .Study of the liquid circulation velocity in external-loop airlift bioreactors. Bioprocess and Biosystems Engineering, 14(1), 3339.

20

22. Guillard, R.R., Ryther, J.H. 1962. Studies of marine planktonic diatoms: I. Cyclotella Nana Hustedt, and Detonula Confervacea (CLEVE) Gran. Canadian journal of microbiology, 8(2), 229-239. 23. Hulatt, C.J., Thomas, D.N. 2011. Productivity, carbon dioxide uptake and net energy return of microalgal bubble column photobioreactors. Bioresource technology, 102(10), 5775-5787. 24. Kaithwas, A., Prasad, M., Kulshreshtha, A., Verma, S. 2012. Industrial wastes derived solid adsorbents for CO 2 capture: a mini review. Chemical engineering research and design, 90(10), 1632-1641. 25. Kasiri, S., Ulrich, A., Prasad, V. 2015. Optimization of CO 1 fixation by Chlorella kessleri cultivated in a closed raceway photo-bioreactor. Bioresource technology, 194, 144-155. 26. Kilonzo, P.M., Margaritis, A., Bergougnou, M. 2010. Hydrodynamics and mass transfer characteristics in an inverse internal loop airlift -driven fibrous-bed bioreactor. Chemical Engineering Journal, 157(1), 146-160. 27. Kommareddy, A., Anderson, G. 2004. Analysis of Currents and mixing in a modified Bubble Column Reactor. 2004 ASAE Annual Meeting. American Society of Agricultural and Biological Engineers. pp. 1. 28. Kumar, A., Ergas, S., Yuan, X., Sahu, A., Zhang, Q., Dewulf, J., Malcata, F.X., Van Langenhove, H. 2010. Enhanced CO 2 fixation and biofuel production via microalgae: recent developments and future directions. Trends in biotechnology ,

21

.021-072 ,)7(12 29. Li, F.-F., Yang, Z.-H., Zeng, R., Yang, G., Chang, X., Yan, J.-B., Hou, Y.-L. 2011. Microalgae capture of CO2 from actual flue gas discharged from a combustion chamber. Industrial & Engineering Chemistry Research, 50(10), 6496-6502. 30. Merchuk, J., Garcia Camacho, F. 1999. Bioreactors: airlift reactors. Encyclopedia of Industrial Biotechnology. 31. Merchuk, J.C., Gluz, M., Mukmenev, I. 2000. Comparison of photobioreactors for cultivation of the red microalga Porphyridium sp. Journal of Chemical Technology and Biotechnology, 75(12), 1119-1126. 32. Nations, U. 2015. Adoption of the paris agreement, Paris. 33. Nayak, B.K., Roy, S., Das, D. 2014. Biohydrogen production from algal biomass (Anabaena sp. PCC 7120) cultivated in airlift photobioreactor. international journal of hydrogen energy, 39(14), 7553-7560. 34. Nikakhtari, H., Hill, G.A. 2005. Hydrodynamic and oxygen mass transfer in an external loop airlift bioreactor with a packed bed. Biochemical Engineering Journal, 27(2), 138-145. 35. Ong, S.-C., Kao, C.-Y ,.Chiu, S.-Y., Tsai, M.-T., Lin, C.-S. 2010. Characterization of the thermal-tolerant mutants of Chlorella sp. with high growth rate and application in outdoor photobioreactor cultivation. Bioresource technology, 101(8), 2880-2883. 36. Popović, M.K., Kiefner, A.W., Bajpai, R.K. 2004. Gas Hold‐up and Liquid

22

Circulation Velocity in Gas‐Liquid‐Solid Airlift Reactors. The Canadian Journal of Chemical Engineering, 82(6), 1273-1274. 37. RAJASEKARAN, C., AJEESH, C.M., BALAJI, S., SHALINI, M., Ramamoorthy, S., Ranjan, D ,.FULZELE, D.P., KALAIVANI, T. 2015. Effect of Modified Zarrouk’s Medium on Growth of Different Spirulina Strains. Walailak Journal of Science and Technology (WJST), 13(1), 67-75. 38. Razzak, S.A., Hossain, M.M., Lucky, R.A., Bassi, A.S., de Lasa, H. 2013. Integrated CO 2 capture, wastewater treatment and biofuel production by microalgae culturing—a review. Renewable and Sustainable Energy Reviews, 27, 622-653. 39. Singh, S., Singh, P. 2014. Effect of CO 2 concentration on algal growth: a review. Renewable and Sustainable Energy Reviews, 38, 172-179. 40. Wilbanks, T.J., Fernandez, S. 2014. Climate Change and Infrastructure, Urban Systems, and Vulnerabilities: Technical Report for the US Department of Energy in Support of the National Climate Assessment. Island Press. 41. Yang, B., Liu, J., Liu, B., Sun, P., Ma, X., Jiang, Y., Wei, D., Chen, F. 2015. Development of a stable genetic system for Chlorella vulgaris—A promising green alga for CO 2 biomitigation. Algal Research, 12, 134-141. 42. Yee-keung, W., Kin-chung, H. Optimization for cultivation of microalgae Chlorella vulgaris and lipid production in photobioreactor. 43. Zheng, H., Gao, Z., Yin, F., Ji, X., Huang, H. 2012. Effect of CO 2 supply

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conditions on lipid production of Chlorella vulgaris from enzymatic hydrolysates of lipid-extracted microalgal biomass residues. Bioresource technology, 126, 24-30.

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Figure Captions Fig. 1. Schematic diagram of: (a) experimental design (b) experimental setup Fig. 2. Effect of input gas superficial velocity on the bubbles rise velocity and bubbles rise time Fig. 3. Effect of input gas superficial velocity on the: liquid circulation time in the downcomer, liquid superficial velocity in the downcomer and liquid superficial velocity in the riser Fig. 4. Effect of input gas superficial velocity on the cell concentration over culture time Fig. 5. Effect of input gas superficial velocity over culture time on the growth rate and concentration of output CO2 from the top of bioreactor Fig. 6. Effect of gas superficial velocity on the CO2 removal efficiency over culture time

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Tables and Figures

Fig. 1. Schematic diagram of: (a) experimental design (b) experimental setup

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Fig. 2. Effect of input gas superficial velocity on the bubbles rise velocity and bubbles rise time

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Fig. 3. Effect of input gas superficial velocity on the: liquid circulation time in the downcomer, liquid superficial velocity in the downcomer and liquid superficial velocity in the riser

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Fig. 4. Effect of input gas superficial velocity on the cell concentration over culture time

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Fig. 5. Effect of input gas superficial velocity over culture time on the growth rate and concentration of output CO2 from the top of bioreactor

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Fig. 6. Effect of gas superficial velocity on the CO2 removal efficiency over culture time

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Table 1 Variation of growth parameters of Chlorella vulgaris Gas superficial velocity Ugr (m/s) 7.458×10-3 13.281×10-3

Culture time t (day) 11 11

Maximum cell concentration xmax (×106 cell/ml) 23.5 ± 0.06 18.3 ± 0.04

Maximum specific growth rate μmax (day -1) 0.2446 0.1843

R2 (for µmax) 0.99 0.97

Doubling time tD (day) 2.83 3.76

Highlights: 

The effect of gas superficial velocity on gas holdup and liquid circulation was investigated.



The effect of high gas superficial velocity on the Chlorella vulgaris microalgae growth and CO2 removal efficiency in an airlift photobioreactor was investigated.



In high gas superficial velocity, the amount of algae cell concentration and CO2 removal efficiency is inversely proportional to input gas superficial velocity.



CO2 removal efficiency by Chlorella vulgaris was achieved equal to 80% in the gas superficial velocity of 7.458×10-3 m/s.

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