CARBON DIOXIDE BIOFIXATION BY Chlorella sp. IN A BUBBLE COLUMN REACTOR AT DIFFERENT FLOW RATES AND CO₂ CONCENTRATIONS

Abstract

CO₂ biofixation of the microalgae Chlorella sp. for different CO₂ concentrations and gas flow rates in a bubble column reactor has been investigated in this study. Microalgae were cultivated under different CO₂ concentrations (at 1.75% and 9.45% v/v) and gas flow rates (at 30, 50 and 70 ml/min). The maximum specific growth rate of Chlorella sp. was obtained for the CO₂ concentration of 1.75 % and the gas flow rate of 50 mL/min. The highest biomass productivity rate (at 0.17 g L^-1 day^-1) was for a sample with 1.75 % CO₂ at a flow rate of 70 ml/min. Moreover, the results have shown that the specific growth rate and CO₂ biofixation have a direct relation with culturing of Chlorella sp. Also, limiting CO₂ supplementation noticeably decreased biomass concentration. Therefore, the results have shown that a high flow rate and low concentration of CO₂ might promote a decrease in CO₂ fixation efficiency by Chlorella sp.

Keywords:
CO₂ biofixation; Greenhouse gas; Microalgae; Biomass production; CO₂ concentration

INTRODUCTION

Climate change is considered to be an important issue for the environment and ecosystem. This phenomenon becomes far worse when more carbon dioxide (CO₂) is emitted into the atmospheric air (Schneider, 1989; Yen et al., 2015). According to some research, more carbon dioxide will be produced due to growing manufacturing industry, forms of transport and human activity (Belbute and Pereira, 2015; Monastersky, 2013). Despite the fact that the utilization of fossil fuels (oil and coal) is the decisive factor in global warming and climate change, the widespread use of an alternative renewable source of energies can play an important role in reducing environmental pollution and preventing using non-renewable resources, which are quite limited in the world (Gharabaghi et al., 2015; Amin, 2009; McKendry, 2002; Sawayama et al., 1999).

Microalgae are known as the third generation of renewable biomass resources for biofuel and bio-based chemical production (Lee and Lavoie, 2013). In addition, microalgae have been described as a biological technology for CO₂ capture because of their high ability of photosynthesis (Amin, 2009; Cuéllar-Franca and Azapagic, 2015; Martínez et al., 2013). Microalgae are mostly cultivated under atmospheric air (containing 0.03% of CO₂). They can also grow in high levels of CO₂ such as Flue gas from power plants (containing 12%-15% of CO₂). Several studies have investigated microalgae cultivation under CO₂-supplementation (Thomas et al., 2016; Watanabe and Fujii, 2016). Utilization of CO₂ for microalgae cultivation has some advantages such as low cost, direct CO₂ capturing from exhaust gas and simplicity in operation. Some researches confirm that microalgae are capable of biofixating 10-50 times more carbon dioxide than terrestrial plants (Li et al., 2008; Rosenberg et al., 2011; Soares et al., 2013).

Additional CO₂ is necessary for the cultivation of microalgae through the photosynthetic process. However, a high carbon dioxide level in the medium of culture will cause a drop in the pH value, which inhibits the microalgae growth. Furthermore, microalgae cultivation under limitation in carbon dioxide usually restricts growth (de Godos et al., 2014; Yen et al., 2015). There are some parameters for optimization of CO₂ biofixation depending on the species of microalgae, such as the nutrient availability, light intensity, temperature, pH, sufficiently high surface area to volume ratio (height to diameter ratio), and countercurrent flow of gas and liquid at optimal flow rates (Cheng et al., 2013; Di Iaconi et al., 2006; Jacob-Lopes et al., 2008; Janssen et al., 2003; Mohsenpour and Willoughby, 2016). Among microalgae species, Chlorella species are considered as a suitable choice for carbon dioxide fixation. In addition, Chlorella sp. have been highlighted because of their outstanding ability for converting high levels of CO₂ in the input air of a photobioreactor into biomass (Chiu et al., 2008; Maeda et al., 1995).

In order to obtain the best operational condition for CO₂ removal, the cultivation of Chlorella sp. was investigated under different CO₂ concentrations and gas flow rates. Accumulation of fixed CO₂ and daily CO₂ fixation rate were also obtained for different conditions.

MATERIALS AND METHODS

Microalgae and culture medium

A culture of Chlorella sp. (PTCC 6010, Persian Type Culture Collection) was obtained from the Iranian Research Organization for Science and Technology (IROST) (Tehran, Iran). The cells of Chlorella sp. were cultured in Rudic’s Medium (Delavari Amrei et al., 2015) (per liter), including 33 g Sea salt, 20 mg NaCl, 10 mg MgSO₄.7H₂O, 47 mg CaCl₂, 300 mg NaNO₃, 20 mg KH₂PO₄,80 mg K₂HPO₄, 0.1 mg ZnSO₄.7H₂O, 7.5 mg Na₂.EDTA, 17 mg FeCl₃ .6H₂O, 0.3 H₃BO₃, 0.3 mg (NH₄)₆Mo₇O₂₄.4H₂O, 17 mg FeCl₃.6H₂O, 0.2 mg Co(NO₃)₂.H₂O, 1.5 mg MnSO₄.H₂O, 0.08 mg CuSO₄.5H₂O, 0.1 mg ZnSO₄ .7H₂O.

Experimental setup and cultivation conditions

The microalgae were cultured in a cylindrical glass reactor (diameter 14 cm, height 1 m) with 10 L of working volume. Cultures were placed on a bench at 26 ± 1 ^◦C under cool-white fluorescent light (General Electric) for 16 days. Light intensity was approximately 87.75 μmol m⁻² s⁻¹ at the surface of the photobioreactor, measured with a Lux-meter (HTC, India; Model no. 102). The experimental set-up is presented in Fig. 1.

Figure 1
Experimental set-up.

Ambient air was mixed with CO₂ to give optional concentrations by a gas mixer instrument. Aeration gas was filter sterilized and pumped into the microalgae culture medium. The CO₂ and O₂ concentrations of the gas in the input and output of the photobioreactor were measured using a STAR GAS global diagnostics system. A portable multiparameter (pH/DO/Temp/EC) HANNA HI98194 instrument was used in each run of photobioreactor to monitor online and record dissolved oxygen (DO), temperature, and pH. In each case, the probes were put in the photobioreactor for 2 minutes. All the experiments were repeated in triplicate, and the average values were represented.

In this study, four runs of experiments for microalgae growth under various CO₂ concentration levels and gas flow rate were applied (Table 1).

Table 1
CO₂ concentration and gas flow rate for different runs.

Exp. No.	CO2 concentration (v/v %)	Gas flow rate (mL/min)
Run 1	9.45	50
Run 2	1.75	50
Run 3	1.75	30
Run 4	1.75	70

Growth monitoring and assessed parameters

The optical density of broth was measured by the absorbance at 560 nm in an Ultrospec 3300 pro UV/Visible spectrophotometer (Amersham Biosciences, Cambridge, UK). The relationship between the biomass concentration (X, g/L) or dry weight and optical density (OD₅₆₀) is obtained as follows (Delavari Amrei et al., 2014):

$$X=0.49\times O{D}_{560}$$ (1)

Various concentrations of carbon dioxide were utilized for aeration of the culture medium inside the photobioreactors. Air containing 0.03% CO₂, 1.75% and 9.45% CO₂ was used to evaluate the effect of improving CO₂ fixation rates. The selected proportion of CO₂ in these aeration conditions was based on the composition of CO₂ in industrial flue gases.

Based on the mass balance of microalgae, the fixation rate of CO₂ can be evaluated. The accumulation of fixed CO₂ (FA, g CO₂) was calculated based on Eq. 2 (Moraes et al., 2016):

$$FA=\left(X_t-X_0\right)\times C_c\times V\times \left(\frac{M_{C{O}_2}}{M_c}\right)$$ (2)

where X_t (g.L^-1) is the concentration of the biomass at time t (days), X₀ (g.L⁻¹) is the concentration of microalgae at time t₀, C_c (g_c/g_sample) is the fraction of carbon determined in the biomass, V (L) is the volume of the photobioreactor, and M_CO2 and M_C (gmol⁻¹) are the molar masses of carbon dioxide and carbon present in the microalgae biomasses, respectively. Carbon dioxide is the main source of the carbon content of the microalgae cell. A mole of CO₂ has a mass of 44 g including 12 g of carbon. The daily CO₂ fixation rate (FD, g_CO2BioFixed/g_{CO2InjectedDay}) was achieved during the growth period according to Eq. 3:

$$FD=\frac{\left(F{A}_{(t+1)}-F{A}_{(t)}\right)}{m_{id}}$$ (3)

where FA_(t+1) and FA_(t) are the CO₂ accumulated at time t+1 (day) and time t (day), respectively. Also, m_id (g_CO2) is the mass of daily injected of CO₂. Therefore, the maximum daily CO₂ fixation rate (F_CO2) was achieved at the maximal (FD) value during the growth period.

The specific growth rate (µ) is calculated according to the following equation. Substantially, the specific growth rate is the slope of the biomass productivity curve or, in other words, the daily rate of the biomass growth.

$$\mu =\frac{\ln \left(\frac{C_n}{C_{n-1}}\right)}{t_n-t_{n-1}}$$ (4)

where C_n and C_n-1 are the biomass concentrations (g L^-1) on the days t_n and t_n-1, respectively.

RESULTS AND DISCUSSION

Effect of different concentrations of CO₂ on microalgae culture

Fig. 2 presents the growth curves obtained for Chlorella sp. grown in air streams containing the different CO₂ concentrations and different flow rates that are presented in Table 1. Also, the pH variation of samples is shown in Fig. 3. The average range of pH is between 7 and 8. In the first run of experiments, the culture of microalgae was aerated after four days with 9.75 % CO₂ and a gas flow rate of 50 mL/min. The maximum growth of microalgae happened in the fifth and sixth days and the final dry cell concentrations were 2.15 g/L after 16 days.

Figure 2
Time course for cell growth at different concentrations of CO₂.

Figure 3
pH variations of the microalgae under different CO₂ aeration levels.

As shown in Figs. 4 and 5, the maximum level of CO₂ removal occurred on the day that µ was the maximum for all of the experiments. In fact, for the first run n the 6th day, the microalgae growth rate was the highest, at 0.81 1/day, and more CO₂ was consumed so that the maximum of daily CO₂ biofixation rate was about 17%. Therefore, the µ value and the percentage of CO₂ removal are closely linked. In the first run, there was a long lag phase due to high CO₂ concentration (at 9.45 %). Furthermore, the exponential phase, as well as the maximum level of CO₂ removal, occurred on the sixth day. Also, in the first run, with increasing mass concentration in the photobioreactor and turbidity of the solution after the eleventh day, the percentage of CO₂ in the output gas climbed by about 5.6% (from 7.7 to 8.13).

Figure 4
Specific growth rate variations of the microalgae under different CO₂ aeration levels.

Figure 5
CO₂ removal percent for different CO₂ aeration levels.

CO₂ concentration has an impact on the metabolism of carbon and algae photochemical properties (Zhao and Su, 2014). Because carbon dioxide is the main source of carbon, a limited supply of carbon dioxide concentration will inhibit algae productivity. A high CO₂ concentration could inhibit algae growth because of a decrease in pH to lower than 5.5 in the cultivation system.

In the second run of experiments, the solution of microalgae was aerated after two days with a CO₂ concentration 1.75 % and flow of 50 mL/min. Dry mass of algae in the second run reached its highest value at 2.5 g/L on the 12^th day. The dry mass of microalgae increased in comparison with the first run due to lower CO₂ concentration and a rise in the average pH from around 6.3 to 7.5. On the third day, the µ value peaked at 1.1 (day^-1).

In the third run of experiments, for investigating the effect of low gas flow rate and limited CO₂ access, the solution of microalgae was aerated with 1.75 % CO₂ and a low flow rate 30 mL/min. The dry mass concentration of algae fell to 2.25 g/L on the 16^th day (10% decrease in comparison with the second run) due to low CO₂ flow rate. The main cause is the lack of sufficient carbon dioxide that is considered as the main carbon source.

High mixing intensity could harm algae, while a sufficient mixing intensity is required for transferring of substances. In the fourth run of experiments, for the investigation of the effect of the high gas flow rate, the solution of microalgae was aerated with 1.75 % CO₂ and a flow rate of 70 ml/min.

As shown in Fig. 4, as in the second and third runs, in the fourth run, the µ value on the second day after aeration reached its highest value. Also, the maximum level of CO₂ fixation yield on the second day for the second, third, and fourth runs happened at 100 %, 97%, and 94%, respectively. The plus point of this test was that the dry mass concentration value peaked at 2.8 g/L in 13 days in comparison with the other runs due to proper mixing in the system and an adjusted pH value with the microalgae activity in the optimal condition.

The pH of the algae culture is related to the solubility and availability of carbon dioxide in the photobioreactor (Mohsenpour and Willoughby, 2016). Bicarbonate is the determining factor in the photosynthesis of microalgae. Variation of the pH results in changing proportions of carbon compounds (carbon dioxide, bicarbonate, and carbonate). Nevertheless, among these compounds, the consumption of carbonate in algae photosynthesis is still being investigated and discovered (Price et al., 2004). Therefore, the amounts of carbon dioxide and bicarbonate transporters may be the main contributing factor in determining the carbon transfer rate. It should also be noted that the carbon transfer rate may make changes in the ratios of assimilation of carbon and nitrogen and affect the cell composition (Hsueh et al., 2007). When the pH of the algae cultivation is between 6.8 and 8.4, more than 50% of the inlet CO₂ converts to bicarbonate and, at pH 8.4, the carbon dioxide converts to bicarbonate completely. So, the optimal condition for algae growth will be achieved in the range of approximately pH 6.8 to pH 8. Similarly, Hsueh et al. (2007) have shown that, whereas the maximum growth rate was achieved in approximately the above -mentioned range, this rate decreased at the higher pH. Thus, it was logical that the maximum dry mass concentration was obtained in the fourth run and the photosynthesis increased in this run.

As shown in Fig. 3, in the first run, the pH value of the solution rose exponentially (until the eleventh day) from 5.8 to 6.62 and declined steadily to 6.4 with decreasing microorganism activity.

In the second and fourth runs, with 1.75% CO₂ concentration, the initial value near neutral pH remained steady at 7.5 and 7.3 for a gas flow rate of 50 and 70 ml/min, respectively. There was a slight increase in the pH during the aeration flow of 50 and 70 mL/min; however, in the third run, there was an obvious increase in the pH and it remained steady at 8.5 because the amount of CO₂ in the solution was lower. This may be attributed to the relation between pH, biomass growth and photosynthetic demand. With increasing CO₂ in the algal solution, the pH will decline. On the other hand, with rising CO₂, photosynthesis and algae growth will rise and algae growth leads to an increase in the pH. The same results have been achieved by several authors. According to de Morais and Costa (2007) and Grobbelaar (2004), the photosynthetic process of CO₂ fixation, owing to the accumulation of OH^-, leads to a moderate rise in pH. On the other hand, the dissolution of CO₂ in water brings about acidification because of the formation of carbonic acid. Moreover, Chinnasamy et al. (2009) also observed that the initial pH decreased with increasing CO₂ concentration and consequently the pH increased with the growth of C. vulgaris.

As shown in Fig. 4, the specific growth rate of microalgae in the minimum of the concentration of CO₂ (at 1.75%) is more than at the maximum of the CO₂ concentration (at 9.45%). This is because of a plummet in the pH value with increasing CO₂ concentration of the solution.

As shown in Fig. 2, the CO₂ supplement has a positive effect on the growth rate and the mass production of the microalgae in comparison with the absence of CO₂ gas aeration. As a result, without CO₂ the growth curve was linear (R²=0.9145), while it changed with CO₂ aeration to an exponential shape. As shown in Figure 2, the maximum production of biomass was at 1.27 g/L in ambient air, which was significantly lower than biomass in culture under CO₂ supplementation.

Carbon fixation

The accumulation of fixed CO₂ (FA, g_CO2) by Chlorella sp., calculated using Equation (2) for the experimental runs, is reported in Table 2. The highest figure for the accumulation of fixed CO₂ of 49.5 g_CO2 was seen at a CO₂ air ratio of 1.75% and 70 ml/min. With increasing flow at 1.75% CO2 air ratio, the daily CO₂ biofixation rate decreased due to the limited capacity of algae photosynthetic.

Table 2
Maximal biomass concentration (Xmax, g L⁻¹), maximal specific growth rate (μ_max, day⁻¹), maximal daily CO₂ biofixation rate (F_CO2, % v/v) obtained for the runs of the experiment.

Exp. No.	Xmax (g.L-1)	μmax (day−1)	Biomass Productivity Rate (g L-1 day-1)	FCO2 (%)	FA (gCO2)
Run 1	2.14	0.81	0.12	17.67	37.2
Run 2	2.5	1.11	0.15	95.45	44.7
Run 3	2.25	0.82	0.14	100	40.0
Run 4	2.8	1.00	0.17	88.63	49.5

Also, as shown in Fig. 5, maximum daily CO₂ biofixation happened in the third run (at 1.75 % CO₂ air ratio and at 30 ml/min flow). In the third run, the CO₂ content in the output gas was roughly zero. Therefore, the maximum figure for removed carbon dioxide and produced oxygen can be easily calculated per gram of algae. The O₂ production and CO₂ consumption by the system per gram of algae is 0.603 g_O2g^-1day^-1 and 0.624 g_CO2 g^-1day^-1, respectively. Furthermore, on the second day, the CO₂ biofixation rate and µ value peaked simultaneously, owing to the high algae absorption in the exponential growth. The CO₂ biofixation rate also remained at 100% as the algae entirely consumed the inlet CO₂ to fix it.

CONCLUSIONS

This study reveals that culturing microalgae with different levels of CO₂ concentrations can lead to various microalgae specific growth rates. So, CO₂ biofixation is of major significance. The highest value of µ was found at 1.75% CO₂ and 50 mL/min flow rate in 1.11 day^-1. This paper shows that the best biofixation of CO₂ was 44.7 g_CO2 after 16 days, which occurred in the region where µ was high and CO₂ accumulation was the maximum. At 1.75 % CO₂ air ratio and at 30 mL/min flow, 100% CO₂ biofixation occurred, but a significant and high efficiency of the growth rate was not observed due to the lack of carbon dioxide. As a result, the microalgae Chlorella sp. has a great potential for biofuel production and CO₂ capturing so as to reduce the negative impacts of greenhouse gas and global warming.

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Publication Dates

• Publication in this collection
  30 Sept 2019
• Date of issue
  Apr-Jun 2019

History

• Received
  12 Apr 2018
• Reviewed
  29 Sept 2018
• Accepted
  20 Nov 2018