CO2, NOx and SOx removal from flue gas via ...

Biotechnology Journal

Biotechnol. J. 2015, 10

DOI 10.1002/biot.201400707

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Review

CO2, NOx and SOx removal from flue gas via microalgae cultivation: A critical review Hong-Wei Yen1, Shih-Hsin Ho2, Chun-Yen Chen3 and Jo-Shu Chang3,4,5 1 Department

of Chemical and Materials Engineering, Taichung, Taiwan of Advanced Science and Technology, Kobe University, Kobe, Japan 3 Center for Bioscience and Biotechnology, National Cheng Kung University, Tainan, Taiwan 4 Research Center for Energy Technology and Strategy, National Cheng Kung University, Tainan, Taiwan 5 Department of Chemical Engineering, National Cheng Kung University, Tainan, Taiwan 2 Organization

Flue gas refers to the gas emitting from the combustion processes, and it contains CO2, NOx, SOx and other potentially hazardous compounds. Due to the increasing concerns of CO2 emissions and environmental pollution, the cleaning process of flue gas has attracted much attention. Using microalgae to clean up flue gas via photosynthesis is considered a promising CO2 mitigation process for flue gas. However, the impurities in the flue gas may inhibit microalgal growth, leading to a lower microalgae-based CO2 fixation rate. The inhibition effects of SOx that contribute to the low pH could be alleviated by maintaining a stable pH level, while NOx can be utilized as a nitrogen source to promote microalgae growth when it dissolves and is oxidized in the culture medium. The yielded microalgal biomass from fixing flue gas CO2 and utilizing NOx and SOx as nutrients would become suitable feedstock to produce biofuels and bio-based chemicals. In addition to the removal of SOx, NOx and CO2, using microalgae to remove heavy metals from flue gas is also quite attractive. In conclusion, the use of microalgae for simultaneous removal of CO2, SOx and NOx from flue gas is an environmentally benign process and represents an ideal platform for CO2 reutilization.

Received 26 DEC 2014 Revised 16 MAR 2015 Accepted 04 APR 2015

Keywords: CO2 fixation · Flue gas · Microalgae · NOx · SOx

1 Introduction The issues of global warming and environmental pollution are of growing concern. One of the leading causes of global warming is the CO2 emissions in the flue gas produced in the combustion of fossil fuels. This provides an opportunity for the development of microalgae-based CO2 mitigation technology based on microalgae’s capability of photosynthesis to carry out carbon fixation. Microalgae are able to grow at a much faster rate than most terrestri-

al plants, thereby having higher CO2 fixation rates. Moreover, microalgae have been considered the most effective platform for CO2 reutilization, as the microalgal biomass obtained by the consumption of CO2 is a very useful feedstock for the production of biofuels and bio-based chemicals [1, 2]. Figure 1 depicts the biorefinery concepts based on conversion of flue gas CO2 to microalgal biomass. This suggests that the use of microalgae to reduce such CO2 emissions is a promising approach that has both economic and environmental benefits, especially for those areas with many combustion plants that produce enormous amounts of flue gas.

Correspondence: Prof. Jo-Shu Chang, Department of Chemical Engineering, National Cheng Kung University, Tainan 701, Taiwan E-mail: [email protected]

1.1 The treatment of flue gas

Abbreviations: DCW, dry cell weight; DIC, dissolved inorganic carbon; NOx, nitrogen oxides; PBR, photobioreactor; PM, particulate matter; SOx, sulfur oxides

Flue gas refers to the gas emitted from the combustion process using any substrates as the feedstock, although most often it is released from the burning of fossil-based

© 2015 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim

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Figure 1. Conceptual description of microalgae-based biorefinery routes and downstream applications of microalgal biomass while using microalgae cultivated autotrophically with flue gas CO2 from factories.

fuels. Among all the carbon-containing substrates, coal is one of the main fuels burned at power generators, with significant negative impacts on both the environment and human health. In 2014, about 36% of the world’s total primary energy supply, and 15 and 25% of that in the EU and Japan, was contributed by coal [3, 4]. In addition to CO2 emissions, the flue gas may also contain many other pollutants, such as SOx, NOx, particulate matter (PM) and trace pollutants, with up to 142 different compounds having been reported [5]. The component profiles of flue gas are highly varied and depend strongly on the quality of the fuel used, as well as the combustion techniques and the cleaning methods that are applied to the exhaust gas. The purpose of using cleaning methods is to prevent the emissions of both gas and particulate pollutants to the environment. Various methods are adopted to remove the gas pollutants in such emissions, and these range from cheap water to expensive carbon sorbents. A major disadvantage of using such solvent systems to remove pollutants is related to the recycling of the collected contaminated liquids used for cleaning of the flue gas. This provides another challenge for the reduction of the quantity of liquid used for cleaning purposes, and for avoiding the secondary contamination of solvents. Many wet methods are used for cleaning in a biomass boiler; for instance, scrubbers, electrified wet scrubbers, wet scrubbers with condensation, wet electrostatic precipitator and mopfan [6]. In addition to the use of solvents to remove gas pollutants, the processes of deposition or adsorption to a solid surface (representing the dry methods) are often applied to remove particulates from flue gas, as seen with the cone of a cyclone, collection of plates in electrostatic precipitator and so on [6]. The major obstacles in the conventional cleaning process of flue gas should be on how to deal with those solvents or solid adsorbent loaded with pollutants in an efficient and environmental-friendly way. Therefore, in

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recent years the potential for using microalgae technology in the cleaning of flue gas has attracted growing attention, especially with regard to reducing the concentrations of CO2, SOx and NOx in these emissions, and the related processes will be discussed in more detail in the following sections.

1.2 The growth of microalgae via photosynthesis It is known that the CO2 fixation process, which occurs via photosynthetic organisms, makes a significant contribution to the stabilization of the global carbon cycle. The autotrophic growth of microalgae results in zero CO2 emissions, and since the CO2 fixation and growth rates are much greater in microalgae than terrestrial plants, by about 10–50 times, microalgal biotechnology is seen as having considerable potential to serve as a commercially feasible way to mitigate CO2 emissions [1]. Moreover, the microalgal biomass that forms in the process of CO2 fixation can be converted to a variety of valuable compounds, which can then be used as biofuels, pigments, cosmetics, nutritious foods and animal feeds, and these by-products represent extra benefits associated with this particular form of CO2 fixation [2]. However, it is first necessary to find a fast-growing microalgal species with high CO2 fixation efficiency, so that economic and environmentally benign CO2 sequestration approaches can be developed [2].

1.3 The impacts of flue gas emissions on microalgae growth As noted in the previous section, CO2 is the main component in the flue gas produced by combustion, although the actual concentration depends greatly on the type of carbon fuel used. For example, when burning natural gas



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the flue gas contains 5 to 6% CO2, while the concentration ranges from 10 to 15% when burning coal at a power plant [7]. Moreover, the CO2 concentration in the flue gas from oxy-combustion processes can be as high as 75% in wet flue gas and 90% in dry flue gas [8]. Carbon dioxide is essential to the growth of microalgae through the photosynthesis pathway. However, the high CO2 content in the influent to microalgae culture will lead to a rapid pH drop, which inhibits the growth of microalgae. The CO2 tolerant concentration of microalgae is strongly dependent on the type of microalgae strains and the flow rate of inlet gas [9, 10]. According to the literature, the CO2 tolerant concentration can range from 14 to 100% of CO2 of the inlet gas [9–11]. To achieve a high CO2 fixation rate of flue gas, a microalgal strain with a high CO2 tolerance might be requisite. Among all the microalgae species, Chlorella sp. is known to have high CO2 tolerance. Literature also shows that Chlorella sp. can grow under 100% CO2, although 10% CO2 was sufficient to achieve the maximum growth rate. Scenedesmus sp. was also reported to be able to grow under 80% CO2 content, while the maximum biomass concentration was observed at a CO2 concentration of 10–20% [12]. In addition to the high concentration of CO2 in flue gas, the compounds of NOx and SOx are also significant components, with well-known negative impacts on the environment and human health. Flue gas contains different NOx species at various concentrations. Nitric oxide (NO) and nitrogen dioxide (NO2) are the major NOx species, and are major contributors to the formation of photochemical smog, acid rain and tropospheric ozone in urban air. Although NO and NO2 are not regarded as greenhouse gases, they can indirectly affect the earth’s radiative balance by catalyzing tropospheric ozone formation, with adverse impacts on human health [13]. Although an excessively high concentration of NOx might inhibit the growth of microalgae, moderate amounts of NOx present in flue gas can be used as nitrogen source to support the growth of microalgae. More detailed discussions are provided in later sections. In addition to NOx, it is estimated that about 220 ppm of SOx is produced in a typical power plant flue gas [14]. Sulfur oxides (SOx) are released when sulfur, hydrogen sulfides or organosulfur compounds are burned [15]. The proportioning of sulfur between the dioxide (SO2) and trioxide (SO3) forms depends on the chemistry of the sulfur in the fuel, the time sequence of temperature, the composition of flue gas, and the presence or absence of catalytic ash material, but generally only 2 to 4% of the sulfur appears as trioxide. Both substances contribute directly to acid rain formation and degradation of the ozone layer, and are thus also regarded as major air-pollutants in the flue gas emitted from power plants [16]. The major effects of SOx on the growth of microalgae should be on the pH drop. It is expected that high SOx concentration would decrease the pH value, which might have the negative


impacts to the growth of microalgae. Therefore, how to maintain a stable pH for the growth of microalgae could be crucial to the microalgae-based treatment of flue gas containing a high SOx concentration. The current study thus presents an overview of the carbon fixation of flue gas via the phototrophic growth of microalgae, as well as a summary of what is known about the effects of CO2, NOx and SOx on the growth of microalgae, and on the removal of these compounds by microalgae. Furthermore, this review highlights the potential of using microalgal biotechnology as a flue gas cleaning process to achieve CO2 fixation and reduce emissions of NOx and SOx compounds.

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CO2 fixation from flue gas by microalgae

2.1 Suitable microalgae strains for CO2 fixation from flue gas It has been widely reported that the CO2 fixation rate of microalgae is 10–50 times faster than that of terrestrial plants [17]. Through photosynthesis, microalgae can effectively convert CO2 into carbohydrates by the enzyme ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO), in a process known as the Calvin Cycle [18]. Theoretically, 1.65–1.83 ton CO2 can be mitigated for the biosynthesis of one ton of dried microalgal biomass, which is a potential feedstock of various end-products (e.g. biofuels and food additives) [9, 10]. A number of microalgae species have been explored for use in CO2-fixation, such as Scenedesmus [19], Chlamydomonas [20], Chlorella [21], and Botryococcus [22]. To date, most previous studies on microalgal CO2 fixation have focused on using artificial pure/mixed CO2 [10]. However, the use of pure commercial CO2 mixed with air may account for 8–27% of the total cost of algal biomass production [23]. The utilization of CO2 from actual flue gas could thus both address the issue of climate change and make the engineering process cheaper [9]. Typically, the main component of industrial flue gas is CO2, which is present at concentrations ranging from 3 to 25%, depending on the fuel source [24]. It has been demonstrated that CO2 from actual flue gas is a plentiful carbon source for growth of some microalgae species, as shown in Table 1. However, some studies reported that the growth of microalgae was strongly inhibited by the feeding of direct flue gas, due to the high CO2 concentration, presence of inhibitory compounds, or sudden stress of high temperature, as flue gas is often released at more than 150°C [10, 25, 26]. The screening for finding a suitable microalgae strain that can tolerate the high CO2 content and the high temperature should be the premise for CO2 fixation of flue gas.

3

4

0.25

Scenedesmus dimorphus

0.1

–

0.05

12

10–11

25

15

15

10.6

13.6

13

23–27

23–27

10–13

CO2 conc. (%)

Air-lift column, 100 L

Raceway pond, 600 L

Bubble column, 50 L

Air-lift column, 5.5 L

Bubble column, 0.1 L

Raceway pond, 20 000 L

–, 0.3 L

Raceway pond, 8000 L

Bubble column, 1200 L

Bubble column, 1L

Bubble column, 0.3 L

PBR type & size

160–175

Outdoor variable

Outdoor variable

200

100

Outdoor variable

200

Outdoor variable

Outdoor variable

300

1150

Light intensity (μmol/m2/s)

Continuous feeding; Pure flue gas; Batch


On-off feeding; Pure flue gas; Batch

On-off feeding; Pure flue gas; Semi-batch





On-off feeding; 1/2 diluted flue gas; Batch

Continuous feeding; 1/2 diluted flue gas; Batch


Operation strategy

–

0.45

2.80

–

3.63

–

1.70

0.32

1.56

2.86

13.5

Final biomass concentration (g DCW/L)

–

32

360

67

485

–

189

13

197

528

2500

– – –

370a) 25a) 355a)

–

60a)

67

60–70

677a)

–

–

75.6 113

889

94

25

877a)

–

–

4400

Biomass CO2 fixation CO2 productivity rate (mg/L/d) efficiency (mg DCW/L/d) (%)

DCW: dry cell weight

[31]

[47]

[28]

[62]

[29]

[23]

[61]

[36]

[26]

[26]

[35]

Reference

a) Calculated from the biomass productivity according to the following equation: CO2 fixation rate=1.88×biomass productivity (mg/L/d), which derived from the typical molecular formula of microalgae biomass, CO0.48H1.83N0.11P0.01 [63].

Scenedesmus obliquus WUST4

Nannochloropsis salina

Chlorella sp. MTF-7

–

0.005

Scenedesmus sp.

Chlorella emersonii

0.05

–

Chlorella sp. MTF-15

Monoraphidium minutum

0.2

Chlorella sp. MTF-15

0.02

0.83

Chlorella vulgaris

Nannochloropsis oceanic KA2

Flue gas flow rate (vvm)

Microalgal species

Table 1. The comparison of CO2 fixation rate and fixation efficiency of flue gases by using various microalgal strains

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2.2 The conditions affecting flue gas CO2 fixation by microalgae In addition to the selection of dominant species with high temperature tolerance, high CO2 concentration tolerance, or high growth rate, the microalgal CO2 fixation rate from flue gas mainly depends on feeding aeration (CO2 mass transfer), light regime/intensity, and cultivation temperature [10, 27]. As shown in Table 1, several successful attempts have been made to overcome these inhibitory effects by applying innovative operation strategies. For instance, Chiu et al. [28] reported that intermittent flue gas aeration was able to significantly improve the efficiency of CO2 removal by microalgae Chlorella sp.. Jiang et al. [29] applied a combined system of CaCO3 addition and intermittent sparging of flue gas controlled by pH-stat to overcome the problems of excess CO2 and SO2 concentrations in the culture medium. The results obtained with an on/off injection controller system are better than those from the continuous injection of flue gas, and achieved the aims of reducing the amount of flue gas emitted and minimizing atmospheric pollution. Kao et al. [26] showed that the use of diluted flue gas can reduce the impacts of a high CO2 concentration and high injection temperature seen with actual flue gas, resulting in a higher cell growth rate of Chlorella sp. and greater CO2 removal efficiency. In most reports concerning carbon fixation of flue gas by using microalgae, autotrophic cultivation was adopted. Nevertheless, in the mixotrophic cultivation of Chlorella sp. KR-1, a fed-batch operation with feedings of glucose and the supply of air in dark cycles by using the coal-fired flue gas showed the highest biomass (561 mg/L d) and fatty-acid methyl-ester (168 mg/L d) productivities [30]. In addition, Li et al. [31] reported the correlation between CO2 concentration and flow rate, and noted that the most important index to consider in this context is the concentration of dissolved CO2 in the medium. In other words, when low flow rates are applied, even a high CO2 concentration in the flue gas still leads to relatively low concentrations of dissolved carbon in the reactor, and thus less growth inhibition. However, there is still little information about this issue in the published literature. Moreover, higher (initial) cell density also makes microalgae more tolerant to environmental stresses, such as high CO2 concentrations, highly toxic components, or a high injection temperature from flue gas [21, 28]. However, it is not easy for the microalgae culture to receive sufficient light energy when it is at a high cell density due to so-called self-shading effects [10], and genetic modification to improve light utilization efficiency is often applied to address this. For instance, Mussgnug et al. [32] demonstrated that shortening specific photosynthetic antenna is an effective way to enhance photosynthetic efficiency and improve light utilization. Kizililsoley et al. [33] reported that reducing the chlorophyll concentration



of cells to increase light penetration efficiency is another way to improve the light utilization of microalgae. An effective photosynthesis bioreactor (PBR) represents a key step toward a successful microalgae-based CO2 mitigation process [10]. It is also widely recognized that a high CO2 mass transfer rate and more efficient light distribution are vital to the design of better bioreactors for CO2 mitigation [34]. Table 1 shows that the best CO2 fixation rates were often obtained in closed reactor systems (e.g. bubble column and air-lift column) in both indoor and outdoor environments [26, 28, 35]. Such systems usually have a larger light receiving area (high surface-to-volume ratio) and longer CO2 gas retention time, which apparently can enhance the distribution/penetration of light and the dissolving of inorganic carbon, along with the additional benefit of a low contamination risk and wellcontrolled hydrodynamics [10, 34]. However, it is doubtful whether such closed cultivation systems would be economically favorable, due to the high construction cost and limited reactor size of the photobioreactors. By contrast, raceway ponds are not expensive to construct and operate [36]. More importantly, raceway cultivation systems are currently the only large-scale engineered operation systems used on a commercial scale [37]. However, raceway ponds usually require a shallow depth to enhance the light utilization of cells, which may result in a shorter contact time between the flue gas and liquid phase, making the CO2 fixation process inefficient and losing most of the injected flue gas into the atmosphere. To address this issue, Pawlowski et al. [38] designed a ÒsumpÓ device to increase the residence time of flue gas in the liquid phase, and combined this with on/off controller (pH-stat) system to supply on-demand flue gas, thus significantly enhancing the CO2 removal rate and minimizing atmospheric contamination. Godos et al. [23] also demonstrated that the CO2 removal efficiency can reach 94% when using an optimized raceway system by carefully controlling the flue gas flow rate (0.005 vvm) and applying a specific sump position and fixed pH (pH 8). However, since the CO2 fixation rate is depending on the biomass concentration obtained, as shown in Table 1, the results obtained with raceway systems are still significantly lower than those seen with a bubble column or air-lift column, due to the lower light receiving area (low surface-to-volume ratio) and poor dissolving efficiency of inorganic carbon. It is thus necessary to develop more effective engineering strategies (e.g. semi-continuous, continuous, or hybrid) or suitable genetic modifications of cells (e.g. shortening the photosynthetic antenna or reducing the chlorophyll concentration in microalgae) in order to improve microalgaebased CO2 fixation systems at outdoor raceway ponds or in other innovative photobioreactors.

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3 Removal of NOx and SOx in flue gas by microalgae

ever, when 400 ppm of SO2 was presented in the inlet gas, the pH would rapidly drop and the growth ceased after 20 hours of cultivation. The results thus indicated that a high concentration of SO2 inhibited the growth of microalgae, due to the low pH obtained when purging it. In addition to the effects of SO2, those of 15% of CO2 and 300 ppm of NO on the growth of Nannochloropsis salina and P. tricornutum were also examined. The growth of both microalgae was greatly affected with 300 ppm NO in the inlet gas, even though the pH profiles remained constant at about 6.0. The growth inhibition seen in the batches with additional NO thus did not contribute to a fall in pH. The measurement of NO2– concentration in the medium was performed in the culture of N. salina and P. tricornutum with supplemental of 300 ppm NO in the inlet gas, the results suggested that some nitrogen oxides were assimilated by microalgal strains after NO was converted to NO2– abiotically [40]. The accumulation rate of NO2– in the cell-free medium depends on the O2 tension in the sparging gas [41]. It is assumed that the possible NO removal

The studies reviewed in the previous section show that capturing CO2 in flue gas using microalgal cultures is a promising way to achieve CO2 mitigation. However, in addition to the high CO2 concentration, flue gas also contains sulfur and nitrogen oxides, and these compounds may be toxic for the growth of microalgae, both by reducing the pH and also by direct inhibition [39]. The removing performances of SOx and NOx through the route of microalgae were shown in Table 2 and 3.

3.1 NOx removal by microalgae Negoro et al. [40] evaluated the effects of SOx and NOx on the growth of ten strains of marine and halotolerant microalgae. The results indicated that the growth of Nannochloris sp., Phaeodactylum tricornutum and Nannochloropsis sp. was not affected by 50 ppm of SO2. How-

Table 2. The comparison of NOx removal rate and removal ratio while using microalgae for the cleanup of flue gas

PBRa)

NOx in the flue gas (ppm)

NOx removal rate (mg/L day)

NOx removal ratio (%, v/v)

Final biomass (g DCW/L)

Reference

4 L column 38 W/m2

300

10

50

2.5

[42]

Counter-flow tubular column 38 W/m2

100

50.4

96

NA

[43]

1 L cylindrical 0.3 vvm 200

300

NA

80–85

0.54

[46]

Strain Nannochloris sp. Dunaliella tertiolecta Scenedesmus sp.

a) PBR: photobioreactor and cultivation conditions DCW: dry cell weight NA: not available

Table 3. The comparison of SOx concentration of flue gas and its effects on the growth rate of microalgal strains

PBRa)

SOx in the flue gas (ppm)

Relative growth rate ratio (%)b)

Reference

Nannochloris sp.

1 L Bottle 15% CO2 1000 lux

50 400

100 0

[40]

Chlorella sp. KR-1

0.125 L bottle 15% CO2 450 μmol/m2 s

60 100 150

60.5 36.4 0

[64]

0.29 L Column 0.038% CO2 (air) 10 μmol/m2 s

100 150 200

100 2.8 2.8

[49]

1 L Column 25% CO2 300 μmol/m2 s

80–90 15–20 150–190

183 204 160

[26]

Strain

Scenedesmus dimorphus

Chlorella sp.

a) PBR: photobioreactor and cultivation conditions b) Relative growth rate ratio = growth rate of flue gas containing SO2/growth rate of control batch without SO2

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mechanism in such a system is as follows: NO in the gas is first dissolved in the aqueous phase, after which it is oxidized to form NO2– and assimilated by the algal cells as a nitrogen source [41]. Yoshihara et al. [42] cultivated the marine microalgae NOA-13, trying to eliminate both NO and CO2 simultaneously. Using a 4 dm3 reactor column with an aeration of 300 ppm (v/v) NO and 15% (v/v) CO2 in N2 at a rate of 150 cm3/min, about 40 mg of NO (half of the NO supplied) and 3.5 g of CO2 were eliminated per day. Nagase et al. [41, 43, 44] investigated the potential of using Dunaliella tertiolecta to remove NOx from fuel flue gas, and about 65% of NO in the inlet flue gases (ranging from 25 to 500 ppm) was removed in this way. It is known that the elimination of NO is closely associated with both the strain of microalgae and the level of dissolved oxygen. When 85% N2 and 15% CO2 is supplied, some of the dissolved oxygen produced by algal photosynthesis might be purged out with the gas flow, and thus there is only a small chance that NO could be oxidized by O2 for the uptake of microalgae. However, the NO removal rate could be greatly enhanced if air is used in the inlet gas instead of nitrogen, as this supplies an enormous amount of dissolved oxygen to the cell culture. For example, by supplying 85% air and 15% CO2 inside the draft tube at 350 mL/min, the NO removal rate was increased to 96% [43]. Studies have applied various culture conditions, and concluded that the dissolution of NO in the aqueous phase is the rate-limiting step in a reactor system [41, 45], and thus enhancing this process is crucial to increasing the NO removal rate. To this end, increasing the gas-liquid contact area and time is seen as an effective method for improving NO removal. A bubble column and airlift reactors have also been evaluated for their NO elimination potential [43]. The highest NO removal rate of 96%, three times higher than that obtained in a simple bubble column reactor, was achieved with a counter-flow type airlift reactor when 100 ppm NO was supplied to the system. This procedure enhances the mass transfer of NO, increasing the mass transfer area and the concentration gradient (the driving force of mass transfer of NO from gaseous to liquid phases). In addition to applying a counter-flow type airlift reactor to overcome the problem of low NO dissolution, Santiago et al. [46] also evaluated the effects of the addition of Fe(II)-EDTA to the culture of microalga Scenedesmus sp. on NO removal. The results showed that this compound enhances the NO fixation to a greater degree than seen with bacterial denitrification systems. When a gas mixture containing 300 ppm NO was used with a Scenedesmus culture containing 5 mM Fe(II)-EDTA, a constant level of 80–85% NO removal was achieved for a prolonged period. It was concluded by Matsumoto et al. [47] that NO gas does not significantly influence the growth of microalgae. Instead, the NO absorbed in the medium is changed to NO2– and utilized as a nitrogen source. Indeed, in the


study of microalgae growth on three different types of flue gas (namely, flue gas from coke oven, hot stove, and power plant, respectively), Kao et al. [26] found that the microalgal strain (Chlorella sp.) had a faster growth rate and higher final cell concentration when the flue gas containing higher NOx content (i.e. flue gas from coke oven) was used. This suggests that the presence of NOx at a sub-inhibitory level could be beneficial to the microalgal growth. In the development of an economically viable DeNOx process, it was found that the adverse effect of nitrite on cell growth and photosynthesis of Chlorella sp. C2 could be ignored when 17.65–88.25 mM nitrite was utilized as the nitrogen source [48].

3.2

SOx removal by microalgae

In addition to NOx, sulfur oxides (SOx) are also important compounds existing in flue gas, which are released when sulfur, hydrogen sulfides or organosulfur compounds are burned. The proportioning of sulfur between the dioxide (SO2) and trioxide (SO3) forms of SOx depends on the operating conditions during combustion, but generally only 2 to 4% of the sulfur appears as trioxide. All these compounds contribute directly to acid rain formation and degradation of the ozone layer. Matsumoto et al. [47] reported that the microalgae growth rate was not significantly influenced by a 50 ppm concentration of gas SO2. However, when this was raised to 400 ppm, the pH of the medium fell to less than 4.0 after 20 hours cultivation, and this gradually decreased the growth rate of microalgae. However, even in this high SO2 concentration case, when the pH could be maintained at 8.0 with the use of NaOH solution, no significant reduction in the growth rate was observed. It was thus concluded that the low pH arising from the presence of SO2 caused the growth rate to decrease. Unfortunately, however, the authors did not provide any data on SO2 removal in their report. Several flue gas streams from varied sources of coke oven, hot stove and power plant were evaluated for the growth of microalgae by Kao et al. [26]. The maximum growth rates of Chlorella sp. MTF-15 obtained in the batches with the gas emitted from varied sources of the coke oven, hot stove and power plants were 0.515, 0.314 and 0.342 g/L day, respectively, approximately 2.0-, 1.2and 1.3-fold higher than that obtained with simply 25% CO2. These results indicate that these three gases are suitable for use in the growth of Chlorella sp. MTF-15. The higher cell concentrations obtained in the batches using the flue gas, as opposed to only CO2, may be attributed to the presence of NOx and SOx in the former. The NOx and SOx in the flue gas served as additional nitrogen and sulfur sources that were able to better support the growth of microalgae [26]. Nevertheless, the extremely low pH, as well as the accumulation of bisulfite caused by SO2, can inhibit microalgae growth. In the cultivation of Scene-

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desmus dimorphus with a simulated flue gas consisting of 15% CO2, 400 ppm SO2 and 300 ppm NO, both pH maintenance methods of adding CaCO3 and the intermittent sparging of flue gas could achieve the cell density of 3.2 g/L. The results indicated that the pH control was a crucial factor when using flue gas for microalgae cultivation [49].

4 Key issues on microalgae-based removal of CO2, NOx and SOx 4.1 Effects of flue gas CO2 capture methods on microalgae-based CO2 fixation One of the major limitations for flue gas CO2 reduction is the availability of a CO2 source. In general, the microalgae cultivation system needs to be very close to the factories that generate the flue gas. However, normally, the factories have limited available space to construct large-scale algae cultivation systems. In that case, one of the alternatives is to capture the flue gas CO2 via chemical (e.g. NaOH or KOH absorption) or physical (e.g. adsorption) means [50]. After that, the dissolved inorganic carbon (DIC; in the form of carbonates or bi-carbonates) or the adsorbed CO2 in solid phase are transported to the algae cultivation plants for CO2 fixation and microalgae growth. The DIC solution can be directly introduced into the microalgae culture to support cell growth with an appro-

priate adjustment of DIC concentration simply by dilution [51]. For the adsorbed CO2, the CO2 molecules need to be released from the adsorbent via desorption process. In this way, high-purity CO2 can be supplied for microalgae growth to allow high-value applications of the resulting microalgal products but the desorption procedures might be very energy intensive. In general, the relative high temperature is required for CO2 desorption from adsorbents (such as 70°C for the desorption from activated carbons). Although using microwave treatment can enhance the CO2 desorption rate, the energy required for the desorption process is still considerable [52]. Table 4 describes the advantages and disadvantages of using molecular CO2 or DIC for CO2 fixation by microalgae culture. The major advantage of using DIC as the carbon source for microalgae growth is to provide a higher concentration of inorganic carbon, which could enhance the growth of microalgae from reaction kinetics perspective since the carbon substrate concentration is higher. Therefore, the CO2 fixation rate can be markedly increased when using higher concentrations of DIC (e.g. bicarbonates) as the carbon source [1]. In contrast, directly sparging flue gas CO2 into the microalgae culture would encounter major mass transfer limitation, as the rate determining step becomes the dissolution of CO2 into the medium. Thus, the CO2 removal efficiency would be poor when directly introducing CO2 gas into microalgal culture unless the mass transfer efficiency of gaseous CO2 can be much improved by designing more efficient aeration

Table 4. The comparison of the advantages and disadvantages of using gaseous CO2 or absorbed CO2 for carbon fixation with microalgae

Strategy I (Direct method)

Strategy II (Indirect method)

Process Direct introduce CO2 from flue gas into the microalgae culture

Process Absorb flue gas CO2 chemically to form DIC (HCO3– or CO32–) and feed the DIC to the microalgae culture

Advantage Simpler process

Advantage DIC (HCO3–) is water soluble, thus there will be less mass transfer limitations on the CO2 fixation reaction

Allow simultaneous removal of CO2 and air pollutants (e.g. NOx, SOx, etc.)

DIC concentration in the medium can be very high, thus could result in a higher CO2 fixation rate

Appropriate CO2 feeding may improve mixing of the microalgae culture

Can be operated in open system, thus is easier to scale up the photobioreactor with a lower capital cost The flue gas source does not need to be close to the microalgae cultivation site since transportation of DIC is much easier than CO2 gas

Disadvantage Low CO2 solubility, thus mass transfer control is dominant

Disadvantage Need to use chemicals to absorb CO2, thus leading to wastewater treatment issues

Closed photobioreactor may be required, thus may lead to higher capital costs

Need additional unit operations (e.g. CO2 absorber and NaOH/KOH recovery)

The microalgae culture system needs to be very close to the factory (flue gas sources)

Some microalgae strains cannot grow efficiently on bicarbonates alone

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devices or using better photobioreactor configuration [53]. Nevertheless, using DIC as carbon source for microalgae growth would require additional unit operation step with consumption of a large amount of chemicals (NaOH or KOH), which may lead to a higher operating cost and more complicated wastewater treatment. As shown in the previous studies, NOx and SOx might be beneficial to the growth of microalgae as they can provide additional nutrients. However, this is true only when the culture pH is stably controlled and the NOx/SOx concentrations should be lower than the inhibitory level [40], while the tolerance concentration of NOx and SOx would be strongly microalgal-strain-dependent. [43].

4.2 Effects of heavy metals in flue gas on microalgae-based CO2 fixation In addition to the uptake of organic compounds, using microalgal biomass as the adsorbent to remove heavy metals offers a potential alternative to conventional routes, mainly because of their low cost, strong metal binding capacity, high efficiency at low metal concentrations and high environmental compatibility [54]. According to Adaikpoh et al. [55], the mean heavy metal concentration in coal was 0.256–0.389 mg/kg for Mn, 0.214–0.267 mg/kg for Cr, 0.036–0.043 mg/kg for Cd, 0.016–0.018 mg/kg for As, 0.064–0.067 mg/kg for Ni, and 0.013–0.017 mg/kg for Pb. The heavy metals contained in the fuels (in particular, coal) may evaporate after their combustion at high temperatures. This results in the presence of heavy metals or metal compounds in the flue gas, such as Fe, Pb, Cu and so on [56]. The biosorption of heavy metals by microalgae is well known [52], as the microalgal biomass exhibits high metal-binding capacities due to the presence of polysaccharides, proteins and/or lipids on the surface of their cell walls. Those components contain charged functional groups that can attract and bind to heavy metals [57]. Several factors would affect the efficiency of heavy metals removal using microalgal cells, including the specific surface properties and the concentration of the biomass, as well as the physicochemical parameters of the solution, such as pH and initial metal ion concentration [58]. Both viable and inactivated microalgal cells can be the matrixes used to remove toxic metals from solution. A variety of technologies, such as using conventional scrubber to absorb CO2 or using activated carbon to adsorb CO2, have been used for the removal of heavy metals from flue gases. It was found that using microalgae to remove heavy metals from flue gas has the advantages as compared to conventional treatments [59, 60]. Although the high metal binding capacity of microalgal biomass offers an additional benefit to remove heavy metals present in the flue gas, there is also a drawback of accumulating heavy metals on the microalgal biomass. This is mainly due to the limited subsequent applications


of the microalgal biomass when it has a heavy metal content. For example, the metal-laden microalgae cannot be used as cosmetic products, health foods, animal/aquacultural feeds, or other high-value applications of the biomass. The heavy-metal-containing microalgal biomass even cannot be directly dumped as wastes due to its potential environmental risks. Therefore, when the microalgae are grown by using flue gas as the carbon source, the heavy metals content of the microalgal biomass should be carefully examined prior to further utilization. Therefore, if the obtained microalgae will be applied in food/feed, pharmaceuticals, or personal care products, it is recommended that the heavy metal content in the flue gas should be reduced to a safety level by adsorption or other effective methods before being used for the cultivation of microalgae. However, if the grown microalgae will be used for making biofuels, the heavy metal content in the microalgal biomass would no longer be a major issue.

5 Conclusions The use of microalgae to achieve CO2 mitigation is attracting growing research interest. Many studies thus examine the application of microalgae technology to flue gas cleaning, including CO2 removal and reducing the NOx and SOx concentrations. This review reveals that the use of microalgae to capture CO2 from flue gas with simultaneous removal of NOx and SOx seems to be very effective and is a potentially economic and environmentally benign approach to the problems associated with CO2 emissions and air pollution, especially for those areas with many combustion plants that can provide enormous amounts of flue gas as the carbon source. In addition to the mitigation of CO2 and simultaneous NOx/SOx removal, the microalgal biomass also exhibits high metal-binding capacities, making the removal of heavy metals in flue gas by microalgae a potential application. Conclusively, using flue gas to cultivate microalgae also offers a promising route for producing useful microalgal biomass as the feedstock for biofuels production and biorefineries.

This work was financially supported by the Ministry of Science and Technology, Taiwan, in the framework of the project MOST-104-3113-E-006-003 and MOST-103-2221E-006-190-MY3. This work is also partially supported by the Top University Project of National Cheng Kung University granted by Ministry of Education, Taiwan. The authors declare no financial or commercial conflict of interest.

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