Valorization of Flue Gas by Combining Photocatalytic Gas

Feb 3, 2016 - Shijian Ge , Pascale Champagne , William C. Plaxton , Gustavo B. Leite , Francesca Marazzi. Biofuels, Bioproducts and Biorefining 2017 1...
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Valorization of Flue Gas by Combining Photocatalytic Gas Pretreatment with Microalgae Production Erik Van Eynde,*,† Britt Lenaerts,† Tom Tytgat,† Ronny Blust,‡ and Silvia Lenaerts† †

Research Group Sustainable Energy, Air & Water Technology, Department of Bioscience Engineering and ‡Systemic Physiological and Ecotoxicological Research (SPHERE), University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium ABSTRACT: Utilization of flue gas for algae cultivation seems to be a promising route because flue gas from fossil-fuel combustion processes contains the high amounts of carbon (CO2) and nitrogen (NO) that are required for algae growth. NO is a poor nitrogen source for algae cultivation because of its low reactivity and solublilty in water and its toxicity for algae at high concentrations. Here, we present a novel strategy to valorize NO from flue gas as feedstock for algae production by combining a photocatalytic gas pretreatment unit with a microalgal photobioreactor. The photocatalytic air pretreatment transforms NO gas into NO2 gas and thereby enhances the absorption of NOx in the cultivation broth. The absorbed NOx will form NO2− and NO3− that can be used as a nitrogen source by algae. The effect of photocatalytic air pretreatment on the growth and biomass productivity of the algae Thalassiosira weissflogii in a semicontinuous system aerated with a model flue gas (1% CO2 and 50 ppm of NO) is investigated during a long-term experiment. The integrated system makes it possible to produce algae with NO from flue gas as the sole nitrogen source and reduces the NOx content in the exhaust gas by 84%.

1. INTRODUCTION Microalgae are very attractive subjects because of their fast and efficient conversion of CO2 into biomass.1,2 In addition, microalgal biomass is a highly valuable product that can be used for biodiesel production, aquaculture nutrition, pharmaceuticals, and as feedstock for chemicals and food products.3−5 Large-scale commercial cultivation of microalgae is still limited because of its high production cost in relation to the acquired benefits.6 At the moment, only for a very limited amount of applications algae cultivation is cost-effective. For microalgae to be suitable as a source of biofuels, the cost of algae cultivation needs to be reduced. The use of flue gas from fossil-fuel combustion processes as a carbon and nitrogen source for algae cultivation can reduce the cultivation expenditures.7,8 Flue gas from combustion processes contains environmentally important concentrations of carbon dioxide and nitrogen oxide (i.e. 3−15% CO2 and 100−500 ppm of NOx).9 In flue gas, 95% of NOX is NO.10 Several studies indicate that the utilization of flue gas as a carbon source for algae cultivation is feasible and can reduce costs of microalgal production, taking into account that high concentrations of NO can inhibit algal growth.11−17 In batch cultures of Chlorella HA sp., Duniella tertiolecta and Nannochloris sp. aerated with a model flue gas with 300 ppm of NO could grow well, while Chlorella KR sp., Chlorococcum littorale, and Nannochloropsis sp. are completely inhibited.11,12,17 A comparison of the conducted studies is difficult because nitric oxide in the gas stream impacts growth and productivity of algae as well as operation mode and design of the reactor, inoculum concentration, and microalgae species.8,11−22 © 2016 American Chemical Society

The inhibition effect was assumed to be due to either lowering the pH or direct inhibition of the NO gas.8,22 Table 1 summarizes studies that investigated the effect of NO on the growth of different microalgae species. Nitric oxide is considered an important second messenger molecule and growth regulator in algae.15,23 NO can also inhibit the adhesion on the reactor surface, a common problem in long-term reactor operations. NO may cause inhibition of adhesion by blocking the secretion of adhesives or by causing the production of less sticky adhesives.24 Different studies indicate that NO can be used as nitrogen source for algae cultivation. There are two different uptake pathways described for NO uptake by microalgae: (1) dissolved NO is oxidized to nitrate in the medium by dissolved oxygen and nitrate is subsequently taken up by the cells and (2) NO diffuses directly into the cells and is oxidized inside the cells.25 The latter mechanism is only described by one study and is not considered to be a common mechanism for algae. The first mechanism requires the dissolution of NO in the water phase as a first step, which is limited by the very low solubility and reactivity of NO.21,26 In practice, only a small fraction of the administered NO ends up in the water phase. This also explains the low efficiency of conventional wetscrubbing methods for NO removal.21 For the enhancement of the NO removal efficiency of wet-scrubbing methods, addiReceived: Revised: Accepted: Published: 2538

October 1, 2015 January 26, 2016 February 3, 2016 February 3, 2016 DOI: 10.1021/acs.est.5b04824 Environ. Sci. Technol. 2016, 50, 2538−2545

Article

Environmental Science & Technology Table 1. Overview of Studies Investigating the Effect of Nitrogen Oxide on Algae Growth microalgae

flue gas

reactor

growth inhibition

reference

Dunaniella tertiolecta Dunaniella tertiolecta Dunaniella parva Nannochloris sp. Nannochloris sp. Nannochloropsis sp. Chlorococcum littorale Chlorella KR1 Chlorella KR1 Chlorella sp. Chlorella sp. Scendesmus sp. Micrasterias denticulata

100 ppm of NO 20 ppm of NO 20 ppm of NO 300 ppm 300 ppm 300 ppm 100 ppm 100 ppm 300 ppm 38 ppm 300 ppm 300 ppm 300 ppm

air lift reactor bubble column bubble column tubular reactor glass bottles (1000 mL) glass bottles (1000 mL) glass bottles (50 mL) glass bottles (50 mL) glass bottles (50 mL) bubble column glass bottles (1000 mL) cylindric glass bioreactor glass flask

no no no yes yes yes yes no yes no no no yes

Nagase et al., 1998 Vunjak-Novakovic et al., 2005 Vunjak-Novakovic et al., 2005 Yoshihara et al., 1996 Negoro et al., 1991 Negoro et al., 1991 Lee et al, 2000a, Lee et al., 2000b Lee et al, 2000a, Lee et al., 2000b Lee et al., 2000 Kastanek et al., 2010 Doucha et al., 2005 Jin et al., 2008 Lehner et al., 2009

illuminated from above with 5 Sylvania GROLUX 24W T5 tubes, resulting in decreasing light intensities from top to bottom in the range of 120−15 μmol s−1m−2. The ambient temperature during the experiment was kept constant at 20 °C ± 2 °C. The microalgal cultures were aerated continuously with a model flue gas at a rate of 1 L·min−1 (0.5 vvm). 2.3. Model Flue Gas. A synthetic gas mixture of air, CO2 and NO was mixed in the desired concentration by mass-flow controllers (MFC) as shown in Figure 1. NO concentration

tional oxidizing agents can be added to transform NO to the more soluble NO2. Photocatalytic oxidation (PCO) of NO by titania photocatalysts offers an environmentally friendly alternative for the transformation of NO into NO2 and HNO3 to improve the solubility of nitrogen. This soluble nitrogen is then available for uptake by microalgae. Photocatalysis only uses light to convert NO into NO2. The present study investigates the effect of combining photocatalytic air pretreatment with an algae cultivation system. The effect of this integrated system on the biomass production and biomass composition of Thalassiosira weissflogii is investigated in a vertical flat panel photobioreactor operated in a semicontinuous mode and aerated by a gas stream with 1% CO2 and 50 ppm of NO. We also evaluated the NO removal efficiency during long-term operation.

2. EXPERIMENTAL PROCEDURES 2.1. Microalgae Culture and Medium. The marine microalgae T. weissflogii was originally obtained from Diatom Culture Collection (Ghent, Strain DCG 0320). The cells were grown in modified f/2 medium with following composition (per liter): 12.7 g of NaCl, 0.1 g of NaHCO3, 3.2 g of MgSO4· 7H2O, 2.4 g of MgCl2·6H2O, and 0.66 g of CaCl2·2H2O and 1 mL of trace elemental solution. The trace elemental solution (per liter) contains 5.83 g of FeCl3·6H2O, 23.0 g of K2HPO4, 44.96 g of Na2SiO3·5H2O, 8.7 g of EDTA·Na2·2H2O, 0.36 g of MnCl2·4H2O, 0.03 g of ZnSO4·7H2O, 0.03 g of CoCl2·6H2O, 0.012 g of Na2MnO4·2H20, 0.0012 g of CuSO4·5H20, 0.1 g of thiamin-HCl, 0.0005 g of biotin, and 0.0005 g of vitamin B12. As can be noticed, the prepared medium contained no nitrogen source. Nitrogen was supplied by model flue gas in the form of nitrogen oxide. Only for the reference growth experiment was f/2 medium with nitrate used. For this control experiment, an additional amount of 0.12 g NaNO3 was added to the prepared medium. Strains were maintained in falcon tubes (each 10 mL) at 20 °C with a 18:6 light/dark cycle and a photon flux density of about 40 μmol s−1m−2. Cultures were up-scaled by transferring them into sterile, aerated (pressured air) 1 L bottles. 2.2. Culture Condition and Photobioreactor Design. T. weissflogii was cultured in ProviAPT reactors, (i.e. vertical tubular flat-panel-type photobioreactors designed for semi continuous operation; dimensions: 45 cm wide × 55 cm high, with an internal tube thickness of 2.5 cm). The reactor has a working volume of 2.0 L and is made entirely out of polypropylene foil (Proviron, Belgium). The panels were

Figure 1. Schematic overview of model flue gas mixing (full line) and gas detection (dotted line).

was varied between 0 and 50 ppm, and CO2 concentration was kept constant during the experiments at 1% because these conditions are optimal for biomass production of Thalassiosira in the current semicontinuous system. The gas flow was supplied to a photocatalytic gas pretreatment (PCO reactor) that was placed in front of two photobioreactors (PBR) in parallel. The PCO reactor could also be bypassed to test the situation without gas pretreatment. The used PCO reactor is a tubular packed bed photoreactor equipped with a 25 W UV lamp (Sadechaf). The photoreactor design is described in more detail by Verbruggen et al. (2011).27 The photoreactor is fully loaded with photocatalystcoated glass beads (approximately 85 g) and is operated in a continuous flow mode. The titania-based photocatalyst was prepared according to the procedure described by Van Eynde et al. (2013).28 2539

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Figure 2. Preliminary NO adsorption experiment without algae: (A) nitrate and nitrite concentration in PBR aerated with 50 ppm of NO and 1% CO2. (B) nitrate and nitrite concentration in PBR equipped with a PCO reactor and aerated with 50 ppm of NO and 1% CO2. (C) pH during the experiments with and without PCO. (D) NO gas concentration during the test with and without PCO during the different stages.

water to wash out the salt of the marine algae. Microalgae biomass was dried at 105 °C for 24 h for dry weight measurement. A linear relationship between culture absorbance and dry weight was observed. 2.6. Chemical Analyses. The reactors were equipped with pH electrodes that measured pH during cultivation. Culture broth from the microalgae culture was collected and filtered with a membrane filter. Determination of nitrite and nitrate content in the broth was done by the Griess spectrometric method measured at 540 nm. The biomass composition was determined by quantification of the protein content of microalgae biomass. The microalgae cells were obtained by centrifugation of 500 mL of harvested broth at 1500g for 5 min and a subsequent centrifugation at 3000g for 15 min. Dried biomass was obtained by freeze-drying. Total nitrogen content was quantified by total nitrogen test kit (Hach) and correlated with the protein content using the nitrogen-to-protein conversion factor proposed by Lourenço et al. (2004).30 All the analyses were carried out in triplicate.

During the experiments, the NO concentration was monitored at three different locations in the setup (e.g., inlet, outlet, and after the PCO reactor). Detection of NO and NO2 was carried out using a Nicolet 380 FTIR spectrometer (Thermo Fisher Scientific) with ZnSe windows and a 2 m heated gas cell. Spectra were recorded in a range of 4000−400 cm−1. Using the Macros Basic software (Thermo Fisher Scientific), the peak heights of different characteristic bands of the species of interest were monitored online during the entire experiment. The νNO stretching vibrations of NO and NO2 are located at 1900 and 1597 cm−1, respectively. The NO removal in the system was calculated from the difference in NO concentration between the inlet and outlet gas phase. 2.4. Semicontinuous Cultivation System. The semicontinuous cultivation process was applied in a system with two parallel Provi-APT flat panel photobioreactors. Each unit of photobioreactor contained 2000 mL cultured microalgae. The culture was started as a batch culture. Precultured microalgae were inoculated into the photobioreactor under 1% CO2 aeration without NO. When cell density reached 0.1 g·L−1, the system was changed into a semicontinuous system. A total of 500 mL (25%) of culture broth was replaced by fresh medium daily. The harvested culture was sampled to determine microalgae dry weight and biomass composition. The amount of NOx removed from the airstreams was determined from the difference between the NOx concentrations in influent and effluent airstreams of the photobioreactors. 2.5. Microalgae Dry Weight. Growth of algae was monitored turbidimetrically at 540 nm with a spectrophotometer (Shimadzu, UV-2510PC) and correlated with biomass concentration with a calibration curve. Microalgae dry weight was determined with the method reported by Zhu and Lee (1997).29 The cells were collected on a preweighted membrane filter in triplicate (Whatman) and washed twice with deionized

3. RESULTS AND DISCUSSION 3.1. Nitrogen Supply in PBR: Effect of Photocatalytic Air Pretreatment in Batch Experiment without Algae. The use of NO as a nitrogen source for algae cultivation requires the dissolution of NO in the water phase and further specification to nitrite (NO2−) and nitrate (NO3−). Nitrogen oxide has a very low solubility and reactivity that seriously limits the amount of NO that can be taken up by microalgae. However, the solubility of nitrogen dioxide is an order of magnitude higher, and this results in a higher reaction rate. Moreover, soluble nitrogen dioxide reacts further to nitrite and nitrate. Photocatalysis is able to convert NO gas to NO2 gas. To prove the concept of enhanced nitrogen supply to the 2540

DOI: 10.1021/acs.est.5b04824 Environ. Sci. Technol. 2016, 50, 2538−2545

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Environmental Science & Technology bioreactor by using a photocatalytic gas pretreatment unit, we performed preliminary tests that determined the effect of the photocatalytic gas pretreatment unit on the amount of soluble nitrogen species in the medium. The preliminary test compared the available amount of nitrogen with and without the application of a photocatalytic pretreatment in a batch experiment. The flat panel reactor, filled with 2.0 L of medium, was aerated with a model flue gas containing 1% CO2 and 50 ppm of NO at a rate of 1 L·min−1. During the experiment, nitrite and nitrate built up in the medium were monitored simultaneously with pH, as illustrated in Figure 2. Evidently, the used f/2 medium contained no nitrate at the beginning of the experiment. Figure 2A shows the evolution of nitrite and nitrate concentration in the photobioreactors aerated with the model flue gas containing 50 ppm of NO and 1% CO2. During the first 196 h no nitrate is detected, whereas the amount of nitrite is slowly increasing, reaching a maximum NO2− concentration of 8 mgN.L−1. After 196 h, nitrate starts to appear in the medium. The formation of nitrate and decrease in nitrite corresponds to a drop in the pH from 6 to 3.9 (Figure 2C). The rise in nitrite concentration can be explained by the observations of Karitinov et al. (1994) who investigated the autoxidation of NO to HNO2 in an oxygen-rich, buffered solution.26 The reaction mechanism they propose is given by eq 12. In buffered conditions, HNO2 dissociates rapidly to form NO2−. The drop in pH results in the movement of the reaction equilibrium (eq 17) toward HNO2 that in turn is transformed into HNO3 as described by eq 16. It should be noticed that the total amount of nitrogen that is present in the form of nitrite and nitrate in the medium after 10 days of aeration with 50 ppm of NO is very limited and corresponds to less than 1% of the total supplied nitrogen in the form of NO. Figure 2B shows the evolution of nitrite and nitrate concentration in the photobioreactors aerated with model flue gas containing 50 ppm of NO and 1% CO2 that was pretreated by a photocatalytic gas pretreatment reactor. Both nitrite and nitrate concentrations start to rise almost immediately. Nitrite concentrations reach a maximum at 50 h that again corresponds to a sharp drop in pH from 6.5 to 3.3. However, nitrate concentrations increased during the entire experiment, reaching a concentration of 110 mg(N)·.L−1 after 300 h. The effect of the application of the PCO reactor on the amount of nitrite and nitrate in the medium can be determined at the end of the test (300 h). The nitrate concentration increased from 4 mg(N)·L−1 for the test without pretreatment to 110 mg·L−1 for the test with the photocatalytic pretreatment unit. The application of a photocatalytic air pretreatment unit clearly enhances the amount of dissolved nitrogen in the water phase. Figure 2D shows the inlet and outlet concentration of NOx (NO and NO2) in the air stream detected by FTIR. The inlet concentration in the gas stream is 46 ppm of NO and 4 ppm of NO2. By the auto-oxidation of NO with O2, 4 ppm of NO is already transformed to NO2. After the passage through the photobioreactor filled with 2L F/2 medium, the air stream contains 37 ppm of NO and 11 ppm of NO2. Application of PCO results in an outlet gas stream containing 15 ppm of NO and 16 ppm of NO2. The transformation of NO to NO2 by photocatalysis assists the absorption of NOx (NO, NO2, N2O3, and N2O4) in water and produces nitrate and nitrite through the complex reaction mechanisms described below.26,31

Gas reactions: 2NO + O2 → 2NO2

(1)

2NO2 ↔ N2O4

(2)

NO + NO2 ↔ N2O3

(3)

NO + NO2 + H 2O ↔ 2HNO2

(4)

3NO2 + H 2O ↔ 2HNO3 + NO

(5)

Gas−liquid reactions: NO(g) ↔ NO(aq)

(6)

NO2 (g) ↔ NO2 (aq)

(7)

N2O3(g) ↔ N2O3(aq)

(8)

N2O4 (g) ↔ N2O4 (aq)

(9)

HNO2 (g) ↔ HNO2 (aq)

(10)

HNO3(g) ↔ HNO3(aq)

(11)

Liquid reactions: 4NO + O2 + 2H 2O → 4HNO2

(12)

2NO2 + H 2O → HNO2 + HNO3

(13)

N2O4 + H 2O → HNO2 + HNO3

(14)

N2O3 + H 2O → 2HNO2

(15)

3HNO2 → HNO3 + 2NO + H 2O

(16)

HNO2 → NO2− + H+

(17)

HNO3 → NO3− + H+

(18)

Figure 3 shows a general overview of the possible reactions that can occur when flue gas is bubbled through a liquid medium. The photocatalytic gas pretreatment unit provides alternative pathways that result in the enhanced formation of nitrate and nitrite in the liquid medium. In this study, this NO oxidation step is performed by photocatalysis. However, other techniques, such as O3 (ozonation), corona discharge, or

Figure 3. Comparison of general reaction pathways of NO in conditions with and without a PCO gas pretreatment unit. 2541

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Figure 4. (A) Growth profiles of T. weissflogii cultured in semicontinuous mode and aerated with, respectively, 1% CO2 (blue line), 1% CO2 and 50 ppm of NO (green line), and 1% CO2 and 50 ppm of NO pretreated in PCO reactor (red line). (B) Nitrate and nitrite profiles of the cultivation broth of T. weissflogii operated in semicontinuous mode aerated with, respectively, 1% CO2 (blue dots), 1% CO2 and 50 ppm of NO (green dots), and 1% CO2 and 50 ppm of NO pretreated in PCO reactor (red dots). (C) pH profiles. (D) Measured NO inlet and outlet concentrations.

Figure 4. shows the microalgal growth, NO2− and NO3− evolution in the broth, the pH and NO gas removal of T. weissflogii cultivated under three different growth conditions. The microalgae cells were sampled just before harvest and just after refill of the reactor with fresh medium. The results show that the growth profile of T. weissflogii aerated with the PCO-treated flue gas is similar to that of the reference with nitrate addition without NO in the gas stream (Figure 4A). For these two growth conditions a pseudo-steadystate condition was achieved as a result of the constant cell concentration at the end of each day over a long period. In general, the semicontinuous operation mode improves the efficiency of the microalgae production because they are less sensitive to contamination and thus provides a cultivation medium with a more stable composition.32 For commercial applications, these semi continuous systems are favored above batch cultures. In contrast, the growth profile of T. weissflogii aerated with 50 ppm of NO and 1% CO2 is steadily decreasing. An explanation of the difference can be found in the nitrate and nitrite concentration in the broth (Figure 4B). The cultures (reference and 50 ppm of NO + PCO) that display normal growth have enough nitrate and nitrite available; the test condition (50 ppm of NO) that displays diminished growth has no nitrate and nitrite available in the medium due to the slow dissolution of NO in the broth. Algae require nitrogen for their growth, and a lack of nitrogen will therefore limit the growth. The daily harvest and replenishment of 25% of the culture broth by new medium enhances the diminishment of the biomass concentration in the culture aerated with 50 ppm of NO and 1% CO2. The diminished growth is accompanied by a decrease of pH from 7.4 at the beginning of the test to 6.3. For the semicontinuous growth experiment aerated with the PCO-treated flue gas, the nitrite and nitrate concentrations stabilized after 10 days at levels of 30.5 mg(N)·L−1 and 9.5

catalytic oxidation, can also be used.33,34 Ozonation entails the risk that O3 ends up in the gas stream and is fed to the microalgae culture, whereas corona discharge requires highenergy input. These techniques are therefore not very suited for the gas pretreatment. Compared to catalytic oxidation, photocatalytic oxidation has the advantage that the photocatalyst is alo able to oxidize unburned hydrocarbons, present in industrial flue gas, into CO2 and water.27 In this way, the photocatalytic gas pretreatment system provides additional carbon and nitrogen for the microalgae culture and minimize the potential toxic effects of these compounds. Thus, photocatalytic gas pretreatment delivers a cleaner flue gas that is better suited for algae cultivation. 3.2. NO as Nitrogen Source for Microalgae Production. 3.2.1. Growth Profile, pH, and Nitrogen in Broth. The potential of nitrogen oxide from flue gas as nitrogen source for algae cultivation and the beneficial effect of photocatalytic gas pretreatment system was investigated using the marine microalgae T. weissflogii in a semicontinuous system at 20 °C decreasing light intensities from top to bottom of the reactor in the range of 120−15 μmol/m2·s. Each 24 h, about 500 mL of culture broth was replaced by fresh medium. A total of three different growth conditions were applied. The first condition is considered as the reference condition in which T. weissflogii is replenished daily by 25% fresh medium with nitrate and aerated with 1% CO2. In the second condition, T. weissflogii is aerated with a gas stream containing 50 ppm of NO and 1% CO2 and replenished daily with 25% fresh medium without nitrate. During the third growth condition, the administered gas flow containing 50 ppm of NO and 1% CO2 is first pretreated in a photocatalytic reactor to convert NO to NO2. The culture broth was replenished daily with 25% fresh medium without nitrate. 2542

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Environmental Science & Technology mg(N)·L−1, respectively. Thus, PCO pretreatment of flue gas delivers sufficient nitrogen to the cultivation medium, and the sustained growth suggests that the nitrogen supplied in this manner is used by the algae. Therefore, the novel approach of combining photocatalysis with a microalgae photobioreactor makes it possible to produce algae with NOx from flue gas as the sole nitrogen source. The reference growth test aerated with 1% CO2 and where 25% of the medium was daily replenished by fresh medium, with nitrate reaching a stable level of 10 mg(N)·L−1. Aeration with 1% CO2 in semi continuous operation mode maintained the pH at 7.4 (Figure 4C). Through aeration by PCO pretreated flue gas, the pH decreased to 6.8 (Figure 4C). This is mainly due the dissolution of NO and NO2 in water with the formation of nitric acid through oxidation with dissolved oxygen. The semicontinuous system tempers the pH decrease through the daily replacement of 25% broth culture by fresh medium with higher pH. Thalassiosira is known to grow in a wide pH range (i.e., from 6.5 to 8.8), as described by Chen and Durbin (1994).35 The amount of NO and NO2 gas in influent (IN), effluent (PBR), and after the PCO reactor (PCO) were recorded (Figure 4D), and NOx removal efficiency was calculated. The NOx concentrations in the influent of the cultures aerated with model flue gas and PCO pretreated model flue gas were 46 ppm of NO and 4 ppm of NO2, respectively. The influent gas of the experiment aerated with PCOpretreated model flue gas (50 ppm of NO + PCO) was first fed to an PCO reactor, resulting in 16 ppm of NO and 32 ppm of NO2 in the gas stream after treatment. Thus, a large fraction of the NO was converted into NO2 by photocatalysis. The gas stream was subsequently fed into the PBR, resulting in 0 ppm of NO and 8 ppm of NO2 in the effluent gas. The NOx removal efficiency is 84%, and the removed NOx ends up as nitrite and nitrate in the cultivation broth. Therefore, pretreatment of flue gas by photocatalysis can have a double benefit; it delivers a cleaner flue gas that is better suited for use in algae cultivation. Photocatalysis is known to oxidize unburned hydrocarbons into CO2 and water and converts NO into nitrite and nitrate. In this way, it provides additional carbon and nitrogen for the algae culture and minimizes the potential toxic effect of these compounds onto algal growth. Mitigation of flue gas compounds as CO2 and NOx contributes to a solution for environmental problems such as global warming, air pollution, and acid rain. For the experiment aerated with model flue gas (50 ppm of NO), the influent gas stream was directly fed to the PBR, resulting in 36 ppm of NO and 11 ppm of NO2 in the effluent. The NOx removal efficiency is 6%, which means hardly any NOx is removed from the gas stream. As a result, nitrate and nitrite concentrations in the broth are zero, and algae growth was diminished. From these results, it can be said that NO is not directly taken up by T. weissflogii. 3.3.2. Effect of NO on Biomass Composition and Productivity in a Semi Continuous System. T. weissflogii is highly favored because of the suited biochemical composition of the biomass.36 Changes in culture conditions can initiate an alteration in biomass composition. Nutrients such as carbon and nitrogen are not limiting under the present cultivation conditions, so only the effect of NOx on the productivity and biomass composition will be studied. Table 2 summarizes the total biomass productivity in the semi continuous system under

different aeration conditions and the relative nitrogen and protein content of the produced biomass. Table 2. Biomass Productivity and Composition of T. weissflogii Cultured in the Semi Continuous System under Different Aeration Conditions dry weight composition NO concentration

total biomass productivity (g/L/d)

nitrogen (% DW)

proteina (% DW)

0 ppm 50 ppm 50 ppm + PCO

0.094 ± 0.012 0.019 ± 0.004 0.084 ± 0.003

5.6 ± 0.3 − 5.9 ± 0.5

35 ± 2 − 37 ± 3

a

Calculated with a nitrogen-to-protein conversion factor of 6.25 (n = 9).

The protein content of the reference test and the growth experiment aerated with PCO-pretreated flue gas was, respectively, 35 and 37 wt % DW. There is no significant difference between the two treatments. 3.3.3. Nitrogen Mass Balance. The nitrogen mass balance was examined to investigate the use of NO as nitrogen source and to elucidate the nitrogen input, output, and uptake by algal cells in the semicontinuous system. Table 3 shows the amount of nitrogen that comes into the reactor and exits the reactor at the end of each day. In the medium, the amount of nitrogen is calculated from the nitrate concentration. The nitrogen in the gas is calculated from the NO concentration in the gas phase. This concentration was measured with a NO sensor. The amount of nitrogen in the microalgae biomass was calculated, taking into account the biomass concentration and the nitrogen content of the biomass. In the semicontinuous system, 500 mL of culture broth is replaced daily by 500 mL of fresh medium. The input of nitrogen by the fresh medium for the reference experiment is 9.9 mg N. The amount of nitrogen in the harvested culture broth is dependent on the concentration of NO in the gas stream. In a gas stream without NO, the amount of nitrogen in the harvested broth is 4.5 mg N. When the culture is aerated with 50 ppm of NO, the amount of nitrogen increases to 20.0 mg N. This is mainly due to the dissolution of NO in the medium with formation of NO2− and NO3−. The difference in amount of nitrogen between incoming gas and outgoing gas does mainly end up in the medium as nitrate or is outgassed as NO2 gas. In summary, we present a novel strategy to valorize NO from flue gas as feedstock for algae production by combining a photocatalytic gas pretreatment unit with a microalgal photobioreactor. The photocatalytic gas pretreatment unit transforms NO gas into NO2 gas that, in the culture broth, further converts into nitrite and nitrate that are available for uptake by algae. The flue gas pretreatment by photocatalysis has the additional benefit that it is also able to oxidize unburned hydrocarbons, present in industrial flue gas, into CO2 and water. In this way, the photocatalytic gas pretreatment system provides additional carbon and nitrogen for the microalgae culture and minimizes the potential toxic effects of these compounds. The mitigation of flue gas compounds as CO2 and NOx contributes to a solution for environmental problems such as global warming, air pollution, and acid rain. Future research should investigate real flue gas and expand toward other algae species. To transform this novel concept into a practical and affordable 2543

DOI: 10.1021/acs.est.5b04824 Environ. Sci. Technol. 2016, 50, 2538−2545

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Environmental Science & Technology Table 3. Mass Balance for Nitrogen in the Semi Continuous System daily input NO aeration

daily output

medium (mg N)a

NO gas (mg N)b

NO2 gas (mg N)c

medium (mg N)d

NO gas (mg N)e

NO2 gas (mg N)f

microalgal biomass (mg N)g

9.9 0

0 37.7

0 4.2

4.5 20.0

0 0

0 6.7

5.6 5.9

0 ppm of NO 50 ppm of NO + PCO

Calculated from the daily replacement of 500 mL harvest by fresh medium with 120 mg·L−1 NaNO3. bDaily input of nitrogen calculated from 1 L· min−1 gas flow, taking into account the density of NO gas. cDaily input of nitrogen calculated from 1 L·min−1 gas flow, taking into account the density of NO2 gas. dMeasured nitrate and nitrite concentration converted to mg N at day 10 of NO aeration. eDaily output of nitrogen calculated from 1 L·min−1 gas flow, taking into account the density of NO gas. fDaily output of nitrogen calculated from 1 L·min−1 gas flow, taking into account the density of NO2 gas. gCalculated amount of N in harvested biomass, taking into account the N content given in Table 2. a

(14) Lee, J. S.; Kim, D. K.; Lee, J. P.; Park, S. C.; Koh, J. H.; Cho, H. S.; Kim, S. W. Effects of SO2 and NO on growth of Chlorella sp KR-1. Bioresour. Technol. 2002, 82 (1), 1−4. (15) Lehner, C.; Kerschbaum, H. H.; Lütz-Meindl, U. Nitric oxide suppresses growth and development in the unicellular green alga Micrasterias denticulate. J. Plant Physiol. 2009, 166 (2), 117−127. (16) Yoshihara, K. I.; Nagase, H.; Eguchi, K.; Hirata, K.; Miyamoto, K. Biological elimination of nitric oxide and carbon dioxide from flue gas by marine microalga NOA-113 cultivated in a long tubular photobioreactor. J. Ferment. Bioeng. 1996, 82 (4), 351−354. (17) Nagase, H.; Eguchi, K.; Yoshihara, K. I.; Hirata, K.; Miyamoto, K. Improvement of microalgal NOx removal in bubble column and airlift reactors. J. Ferment. Bioeng. 1998, 86 (4), 421−423. (18) Vunjak-Novakovic, G.; Kim, Y.; Wu, X.; Berzin, I.; Merchuk, J. C. Airlift bioreactor for algal growth on flue gas: mathematical modelling and pilot plant studies. Ind. Eng. Chem. Res. 2005, 44 (16), 6154−6163. (19) Kastánek, F.; Sabata, S.; Solcová, O.; Maléterová, Y.; Kastánek, P.; Brányiková, I.; Kuthan, K.; Zachleder, V. In field experimental verification of cultivation of microalgae Chlorella sp. using the flue gas from cogeneration unit as a source. Waste Manage. Res. 2010, 28 (11), 961−966. (20) Doucha, J.; Straka, F.; Lívanský, K. Utillisation of flue gas for cultivation of microalgae (Chlorella sp.) in an outdoor open thin-layer photobioreactor. J. Appl. Phycol. 2005, 17, 403−412. (21) Jin, H.; Santiago, D. E. O.; Park, J.; Lee, K. Enhancement of nitric oxide solubility using Fe-EDTA and its removal by green algae Scenedesmus sp. Biotechnol. Bioprocess Eng. 2008, 13 (1), 48−52. (22) Zhang, Z. B.; Lin, C.; Liu, C. Y.; Xing, L.; Wu, Z. Z.; Sun, F. Study on patterns and chemical features of NO effect on marine phytoplankton growth. Sci. China, Ser. B: Chem. 2005, 48 (4), 376− 384. (23) Van Den Hende, S.; Vervaeren, H.; Boon, N. Flue gas compounds and microalgae: (Bio-)chemical interactions leading to biotechnological opportunities. Biotechnol. Adv. 2012, 30 (6), 1405− 1424. (24) Thompson, S. E. M.; Taylor, A. R.; Brownlee, C.; Callow, M. E.; Callow, J. A. The role of nitric oxide in diatom adhesion in relation to substratum properties. J. Phycol. 2008, 44 (4), 967−976. (25) Nagase, H.; Yoshihara, K. I.; Eguchi, K.; Okamoto, Y.; Murasaki, S.; Yamashita, R.; Hirata, K.; Miyamoto, K. Uptake pathway and continuous removal of nitric oxide from flue gas using microalga. Biochem. Eng. J. 2001, 7 (3), 241−246. (26) Kharitonov, V. G.; Sundquist, A. R.; Sharma, V. S. Kinetics of nitric oxide autoxidation in aqueous solution. J. Biol. Chem. 1994, 269 (8), 5881−5883. (27) Verbruggen, S. W.; Ribbens, S.; Tytgat, T.; Hauchecorne, B.; Smits, M.; Meynen, V.; Cool, P.; Martens, J. A.; Lenaerts, S. The benefit of glass bead supports for efficient gas phase photocatalysis: Case study of a commercial and a synthesised photocatalyst. Chem. Eng. J. 2011, 174 (1), 318−325. (28) Van Eynde, E.; Tytgat, T.; Smits, M.; Verbruggen, S. W.; Hauchecorne, B.; Lenaerts, S. Biotemplated diatom silica-titania materials for photocatalytic air purification. Photochem. Photobiol. Sci. 2013, 12 (4), 690−696.

reality, one must establish as well the cost effectiveness and environmental impact of this system.

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AUTHOR INFORMATION

Corresponding Author

*Telephone: +32 3 265 35 17; fax: +32 3 265 32 25; e-mail: [email protected]. Notes

The authors declare no competing financial interest.

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REFERENCES

(1) Lim, S.; Teong, L. K. Recent trends, opportunities and challenges of biodiesel in Malaysia: An overview. Renewable Sustainable Energy Rev. 2010, 14 (3), 938−954. (2) Singh, A.; Nigam, P. S.; Murphy, J. D. Renewable fuels from algae: An answer to debatable land based fuels. Bioresour. Technol. 2011, 102 (1), 10−16. (3) Araujo, G. S.; Matos, L. J. B. L.; Goncalves, L. R. B.; Fernandes, F. A. N.; Farias, W. R. L. Bioprospecting for oil producing microalgal strains: Evaluation of oil and biomass production for ten microalgal strains. Bioresour. Technol. 2011, 102 (8), 5248−5250. (4) Najafi, G.; Ghobadian, B.; Yusaf, T. F. Algae as a sustainable energy source for biofuel production in Iran: A case study. Renewable Sustainable Energy Rev. 2011, 15 (8), 3870−3876. (5) Ryckebosch, E.; Bruneel, C.; Termote-Verhalle, R.; Goiris, K.; Muylaert, K.; Foubert, I. Nutritional evaluation of microalgae oils rich in omega-3 long chain polyunsaturated fatty acids as an alternative for fish oil. Food Chem. 2014, 160 (1), 393−400. (6) Wijffels, R. H.; Barbosa, M. J.; Eppink, M. H. M. Microalgae for the production of bulk chemicals and biofuels. Biofuels, Bioprod. Biorefin. 2010, 4 (3), 287−295. (7) Douskova, I.; Doucha, J.; Livansky, K.; Machat, J.; Novak, P.; Umysova, D.; Zachleder, V.; Vitova, M. Simultaneous flue gas bioremediation and reduction of microalgal biomass production costs. Appl. Microbiol. Biotechnol. 2009, 82 (1), 179−185. (8) Yen, H. W.; Ho, S. H.; Chen, C. Y.; Chang, J. S. CO2, NOx and SOx removal from flue gas via microalgae cultivation: A critical review. Biotechnol. J. 2015, 10 (6), 829−839. (9) Chakravarti, S., Gupta A. and Hunek, B. Advanced Technology for the Capture of Carbon Dioxide from Flue Gases. First National Conference on Carbon Sequestration; Washington, DC, 2001. (10) Johnsson, J. E. Urban sources of air pollution: Stationary sources. In Urban Air Pollution: European Aspects. Fenger, J., Hertel, O. and Palmgren, F., eds; Kluwer Academic Publishers, Dordrecht, Germany, 1998, 35−62. (11) Negoro, M.; Shioji, N.; Miyamoto, K.; Micira, Y. Growth of microalgae in high CO2 gas and effects of SOx and NOx. Appl. Biochem. Biotechnol. 1991, 28 (1), 877−886. (12) Lee, J. H.; Lee, J. S.; Shin, C. S.; Park, S. C.; Kim, S. W. Effects of NO and SO2 on growth of highly-CO2,-tolerant microalgae. J. Microbiol. Biotechnol. 2000, 10 (3), 338−343. (13) Lee, J. N.; Lee, J. S.; Shin, C. S.; Park, S. C.; Kim, S. W. Methods to enhance tolerances of Chlorella KR-1 to toxic compounds in flue gas. Appl. Biochem. Biotechnol. 2000, 84 (1), 329−342. 2544

DOI: 10.1021/acs.est.5b04824 Environ. Sci. Technol. 2016, 50, 2538−2545

Article

Environmental Science & Technology (29) Zhu, C. J.; Lee, Y. K. Determination of biomass dry weight of marine microalgae. J. Appl. Phycol. 1997, 9, 189−194. (30) Lourenço, S. O.; Barbarino, E.; Lavin, P. L.; Lanfer Marquez, U. M. L.; Aidar, E. Distribution of intracellular nitrogen in marine microalgae: Calculation of new nitrogen-to-protein conversion factors. Eur. J. Phycol. 2004, 39 (1), 17−32. (31) de Paiva, J. L.; Kachan, G. C. Absorption of nitrogen oxides in aqueous solutions in a structured packing pilot column. Chem. Eng. Process. 2004, 43 (7), 941−948. (32) Bezerra, R. P.; Montoya, E. Y. O.; Sato, S.; Perego, P.; de Carvalho, J. C. M.; Converti, A. Effects of light intensity and dilution rate on the semicontinuous cultivation of Arthrospira (Spirulina) platensis. A kinetic Monod-type approach. Bioresour. Technol. 2011, 102 (3), 3215−3219. (33) Mok, Y. S.; Kim, J. H.; Nam, I. S.; Ham, S. W. Removal of no and formation of byproducts in a positive-pulsed corona discharge reactor. Ind. Eng. Chem. Res. 2000, 39 (10), 3938−3944. (34) Jin, Y.; Veiga, M. C.; Kennes, C. Bioprocesses for the removal of nitrogen oxides from polluted air. J. Chem. Technol. Biotechnol. 2005, 80, 483−494. (35) Chen, C. Y.; Durbin, E. G. Effects of pH on the growth and carbon uptake of marine phytoplankton. Mar. Ecol.: Prog. Ser. 1994, 109, 83−94. (36) Soler, C.; Claquin, P.; Goutx, M.; Ragueneau, O.; Moriceau, B. Impact of nutrient starvation on the biochemical composition of the marine diatom Thalassiosira weissf logii: from the whole cell to the frustule fraction. Biogeosciences Discuss. 2010, 7, 5953−5995.

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DOI: 10.1021/acs.est.5b04824 Environ. Sci. Technol. 2016, 50, 2538−2545