A novel porous nickel-foam filled CO2 absorptive photobioreactor system to promote CO2 conversion by microalgal biomass

Science of the Total Environment 713 (2020) 136593

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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

A novel porous nickel-foam filled CO2 absorptive photobioreactor system to promote CO2 conversion by microalgal biomass Wangbiao Guo a, Jun Cheng a,⁎, Shuzheng Liu a, Lingchong Feng a, Yongning Su b, Yuguo Li b a b

State Key Laboratory of Clean Energy Utilization, Zhejiang University, Hangzhou 310027, China Inner Mongolia Rejuve Biotech Co., Ltd, Ordos 016199, China

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• A porous nickel-foam filled CO2 absorptive photobioreactor system was developed. • CO2 conversion to NaHCO3 in a short time was improved to enhance algal photosynthesis. • Nickel-foam promoted Na2CO3 solution radial velocity and CO2 volume fraction. • Conversion efficiency of CO2 gas into NaHCO3 increased with increase of pore diameter. • Sufficient HCO–3 supply promoted the quantum ratio used for electron transfer.

a r t i c l e

i n f o

Article history: Received 11 December 2019 Received in revised form 5 January 2020 Accepted 6 January 2020 Available online xxxx Editor: Huu Hao Ngo

a b s t r a c t In order to solve problems associated with a short residence time and low conversion efficiency when CO2 gas is aerated directly into raceway ponds, a novel porous nickel-foam filled CO2 absorptive photobioreactor system was developed to promote CO2 conversion to NaHCO3 in a short time to improve photosynthesis of microalgal cells. Numerical simulation showed that the porous nickel-foam promoted the Na2CO3 solution radial velocity and CO2 volume fraction in the CO2 absorption reactor, which enhanced the reaction rate of CO2 gas and soluble Na2CO3. The conversion efficiency of CO2 gas to soluble NaHCO3 gradually increased with an increasing nickelfoam pore diameter and a decreasing CO2 gas outflow rate, while it first increased and then decreased with an increasing relative nickel-foam height in the CO2 absorption reactor. The conversion efficiency from soluble NaHCO3 to microalgal biomass first increased and then decreased with an increasing nickel-foam pore diameter (peaking at 2 mm) and relative height (peaking at 0.24); and CO2 gas outflow rate (peaking at 2 L/min). The chlorophyll fluorescence measurements showed that a sufficient HCO–3 supply promoted the quantum ratio used for electron transfer (from 0.19 to 0.23) and the maximum photochemical efficiency (from 0.48 to 0.52), resulting in an increased biomass growth rate (by 1.1 times) when the nickel-foam pore diameter increased from 0.1 to 2 mm. © 2020 Elsevier B.V. All rights reserved.

1. Introduction

⁎ Corresponding author. E-mail address: [email protected] (J. Cheng).

https://doi.org/10.1016/j.scitotenv.2020.136593 0048-9697/© 2020 Elsevier B.V. All rights reserved.

Severe CO2 emission is a global issue that triggers many problems (Cheng et al., 2018a; Cheng et al., 2019). Thus, studies are looking for an effective method for CO2 utilization. Microalgae-based technologies are a major method because of their high growth rate (Cheng et al.,

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Nomenclature PBR CCM NFCAP NF SBS SCS CGO CIM COM CAR CAP IPF OPF FI h/H ABS/RC DIo/RC TRo/RC ETo/RC TIC PGA DGA G3P RuBP

Photobioreactor CO2 concentrating mechanism Porous nickel-foam filled CO2 absorptive photobioreactor Nickel-foam NaHCO3 solution Na2CO3 solution CO2 gas outflow CO2 inlet flow meter CO2 outlet flow meter CO2 absorption reactor CO2 absorption product Inlet porous face Outlet porous face Fluorescence intensity Relative height of nickel-foam to CO2 absorption reactor height Absorbed light energy of the unit PSII reaction center Consumed light energy of the unit PSII reaction center Light energy used for the reduction of QA of unit PSII reaction center Light energy used for electron transfer of unit PSII reaction center Total inorganic carbon 3-phosphoglyceric acid 1,3-diphosphate glyceric acid Glyceraldehyde 3-phosphate Riboketose 1,5 diphosphate

Greek alphabet γ porosity 1/α viscous resistance C2 inertial resistance Dp pore diameter μ turbulent viscosity σ molecular viscosity ρ phase density k turbulent kinetic energy α volume fraction ε turbulent dissipation φPo maximum photochemical efficiency φEo quantum ratio used for the electron transfer φDo the quantum ratio used for the heat dissipation ηg-l CO2 fixation efficiency from CO2 gas to NaHCO3 solution ηl-s CO2 fixation efficiency from NaHCO3 solution to microalgae biomass δ difference of CO2 gas volume fraction between IPF and OPF

2016). However, their CO2 conversion efficiency is currently still too low to remediate the enormous amount of CO2 emissions. Normally, CO2 gas is aerated directly into photobioreactors (PBR) using aerators, which generate CO2 bubbles that can be absorbed by microalgal cells (Cheng et al., 2018a). To improve the CO2 conversion efficiency, researchers are devoted to reducing the CO2 bubble generation diameter and increasing the resistance time by modifying the aerators and baffles in the PBR. Cheng et al. (2016, 2018 and 2019) developed a strip aerator, a volute aerator and microporous fibrous-diaphragm aerators for use in raceway ponds. They successfully reduced the bubble generation diameter to 0.45 mm while increasing the bubble resistance time to 126 ms (Cheng et al., 2018a; Cheng et al., 2019; Cheng et al., 2016). Tesař et al. (2006) designed an aerator coupled with a bubble

control valve and feedback circulation channel. The generated pressure difference and self-excited oscillation converted the continuous airflow into small bubbles, which subsequently reduced the pressure and friction energy loss (Tesař et al., 2006). Additionally, Huang et al. (2017) designed a circular gas distributor to reduce the bubble generation diameter in a PBR (Huang et al., 2017). However, these aerators still produce CO2 bubbles with diameters on the millimeter-scale and resistance times on the microsecond-scale, which is insufficient for CO2 utilization by microalgal cells. As a result, a great proportion of CO2 gas is wasted and flows to the atmosphere again. Optimizing baffles in PBRs is another frequent method for improving the CO2 conversion efficiency. The vortex flow generated by the baffles is helpful for increasing the CO2 bubble resistance time. Researchers have proposed several baffles in the PBRs so as to increase the CO2 conversion efficiency (Cheng et al., 2018b; Cheng et al., 2018c; Zhang et al., 2015; Ye et al., 2018; Kumar et al., 2019). However, this method still does not address the bottleneck of CO2 bubble resistance time being on the microsecond-scale. The conversion efficiency by microalgal biomass of CO2 gas directly aerated into PBRs is still too low to satisfy the enormous CO2 fixation requirements. It was realized that a CO2 concentrating mechanism (CCM) exists in microalgal cells, such as the Spirulina sp. Microalgal cells can adopt the bicarbonate ion (HCO− 3 ) as a carbon source to avoid carbon limitation in the atmosphere (Cheng et al., 2018d; Mackinder et al., 2017; Rosenzweig et al., 2017). HCO–3 can sequentially pass through the plasma membrane, chloroplast envelope and thylakoid membrane, finally arriving at the thylakoid lumen where it is catalyzed to CO2. Next, the CO2 molecule is fixed by the RubisCO enzyme and reacts in the Calvin cycle. HCO–3 in the periplasmic space can also be converted by carbonic anhydrase to CO2, which diffuses to the stroma and is then captured by RubisCO. Therefore, adopting HCO–3 as a carbon source is more beneficial for microalgal growth. The flue gas from coal-fired power plants or coal chemical plants, which have an abundance of CO2 gas, can be first converted to HCO–3 and then fixed by microalgae as biomass. The biggest benefit of this method is that the HCO–3 converted from CO2 gas can be theoretically absorbed completely by the microalgal cells, which would be a huge breakthrough for CO2 fixation by microalgae. Researchers have proposed several systems to convert CO2 gas to HCO–3 to promote microalgal growth. Song et al. (2019a, 2019b, 2019c, 2019d) proposed an absorption-microalgae hybrid CO2 utilization system that uses an ammonia-rich solution as a nutrient source for microalgal cultivation (Song et al., 2019a; Song et al., 2019b; Song et al., 2019c; Song et al., 2019d). They successfully combined ammonia absorption and biological fixation, resulting in a high CO2 recovery efficiency and low energy consumption. However, the structure of the proposed absorption system that converts flue gas and ammonia is relatively simple and the absorption efficiency may be limited. Furthermore, the CO2 fixation efficiencies from CO2 gas to NH4HCO3 solution, and NH4HCO3 solution to microalgal biomass is important but was not clearly discussed. A previous study developed a CO2 bicarbonation absorber for promoting the microalgal growth rate using a CO2 gas distributor to reduce the bubble diameter. The reaction time, reaction pressure, volume ratio of sodium carbonate solution and initial sodium carbonate concentration were subsequently optimized (Guo et al., 2019). However, the optimized reaction time was up to 90 min, which is too long to satisfy the engineering production requirements. Moreover, previous work has focused more on the CO2 fixation amount and NaHCO3 content, while the CO2 fixation efficiency has not been studied. Similar to the work of Song et al. (2019) (Song et al., 2019a; Song et al., 2019b; Song et al., 2019c; Song et al., 2019d), the structure of the CO2 bicarbonation absorber was too simple and was not beneficial for the reaction of CO2 gas with sodium carbonate solution. The contribution of the present work is five-fold: 1) a novel porous nickel-foam-filled CO2 absorptive photobioreactor (NFCAP) was developed. 2) The pore diameter and relative height of the nickel-foam (NF) was optimized to improve the CO2 conversion efficiency. 3) The CO2 conversion efficiency from CO2 gas to the sodium bicarbonate

W. Guo et al. / Science of the Total Environment 713 (2020) 136593

solution (SBS), and from the SBS to microalgal biomass were clearly elucidated. 4) A numerical simulation model was established to investigate the CO2 gas distribution within the porous NF. 5) The chlorophyll fluorescence of the microalgal cells in different CO2 absorption products was investigated. Therefore, the NFCAP system could be used to alleviate the bottleneck of CO2 conversion efficiency by microalgal biomass, thereby satisfying the enormous CO2 fixation requirements. 2. Materials and methods 2.1. Design of a novel porous nickel-foam filled CO2 absorptive photobioreactor system A diagram of the porous nickel-foam filled CO2 absorptive photobioreactor system (NFCAP) is provided in Fig. 1(a). The dimensions of the CO2 absorption reactor (CAR) were φ10 × 100 cm. Sodium carbonate solution was initially added to the CAR at a Na2CO3 concentration of 0.2 M and a solution height of 50 cm, which was based on a previous study (Guo et al., 2019). During the experiment, the 100% CO2 gas successively flowed from the CO2 storage tank and crossed

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the gas switch, drier, pressure valve and CO2 inlet flow meter (CIM) to the bottom of the CAR. The pressure valve was used to keep the reactor pressure at 0.3 MPa. The NF filled the inside of the CAR to provide a porous zone so as to improve the CO2 conversion efficiency. After the reaction, the residual CO2 gas outflow (CGO) flowed from the top of the CAR crossing the drier, CO2 outlet flow meter (COM) and gas switch. The CIM and COM were used to measure the inlet and outlet instantaneous flow rates and the total flow volume. The pore diameter and the relative height of the NF to the CAR height (h/H) were modified. After approximately 10 min of reaction, the CO2 absorption product, which is the mixture of Na2CO3 and NaHCO3, flowed to the PBR for microalgal cultivation. The PBR was a transparent glassy column with dimensions of φ 10 × 40 cm. The microalgae Spirulina sp. was inoculated into the PBR in advance. The initial inoculation absorbance at 560 nm (OD560) was kept at 0.15 and the solution depth was maintained at 35 cm. The light intensity was kept at 8000 ± 200 lx and the solution temperature was around 28 °C. Fresh air with a volume rate of 0.5 vvm was aerated to the PBR to maintain the microalgal suspension. Along with CAP, the Zarrouk medium contained 2.5 g/L NaNO3, 0.5 g/L K2HPO4, 0.2 g/L

(a) Porous nickel-foam filled CO2-absorptive photobioreactor (NFCAP) system

(b) CO2 conversion into sodium bicarbonate for photosynthesis reaction in microalgae cell Fig. 1. Porous nickel-foam filled CO2-absorptive photobioreactor (NFCAP) system improved CO2 conversion into sodium bicarbonate for photosynthesis reaction in microalgae cells.

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MgSO4·7H2O, 1.0 g/L K2SO4, 0.01 g/L FeSO4·7H2O, 0.08 g/L Na2EDTA, 0.04 g/L CaCl2 and 3 mL HCl (35%w/v). The total cultivation time was 65 h, after which the CO2 gas was ultimately converted to carbohydrate. In this study, several aspects of the NFCAP system were improved based on the previous structure (Guo et al., 2019). First, the NF was applied to the CO2 absorption reactor, which consisted of a porous zone to reduce the bubble diameter and increase the possibility for CO2 gas to contact the sodium carbonate solution. Second, the CGO flowed out of the CAR. Although a small proportion of CO2 gas was wasted, more CO2 gas was aerated to the CAR and reacted with the sodium carbonate solution, which is helpful for increasing the CO2 conversion efficiency. Third, the reaction time was dramatically decreased to several minutes, which is more applicable for industry. 2.2. Numerical simulation of the CO2 absorption reactor In order to investigate the influence of the NF pore diameter on the chemical reaction of CO2 gas with sodium carbonate solution, a 3D CFD simulation model was developed. The NF was placed inside the CAR and the inlet porous face (IPF) and outlet porous face (OPF) were defined (Fig. 1 (a)). The model was conducted using ANSYS Fluent 2019R2. The gas-liquid multiphase was modeled using the implicit Eulerian approach. The realizable k-ε model was chosen to account for the turbulence flow in the porous zone. Both viscous resistance and inertial resistance were considered for the porous zone and the transient time type was chosen. A CO2 inlet hole (diameter: 1 cm) was opened on the bottom of the CAR. The boundary type of the CO2 inlet was chosen as a velocity-inlet with a gas velocity magnitude of 2.24 m/s. The boundary type of the CO2 outlet was chosen as a pressure-outlet. The phase coupled SIMPLE method was chosen for pressure-velocity coupling. Least squares cell-based PRESTO! first and second order upwind schemes were used for the spatial discretization of pressure, momentum and volume fraction. The maximum iteration number was 40 at each time step and the time step size was 0.01 s. The overall calculation time was set as 10 s. The porosity of the NF (γ) was defined as: γ ¼ 1−ρNF =ρnickel

ð1Þ

where ρnickel is 8.902 g/cm3. The viscous resistance (1/α) and inertial resistance (C2) of the porous zone were determined by the Ergun equation (Kim et al., 1956; Pham et al., 2015): 1=α ¼ 150ð1−γ Þ2 =Dp 2  γ 3

ð2Þ

C 2 ¼ 3:5ð1−γ Þ=Dp  γ3

ð3Þ

where Dp is the pore diameter of the NF. The radial velocity, turbulent viscosity (μ) of air and molecular viscosity (σ) were recorded. The realizable k-ε model contains an alternative formulation for turbulent viscosity. Molecular viscosity plays a dominant role in the momentum and heat or mass transfer in the near-wall region. μ and σ were calculated as (ANSYS, 2011): 2

μ ¼ ρ  C μ  k =ε σ¼

X

αi μ i

ð4Þ

sp. The fast induction kinetic curve of chlorophyll fluorescence (as measured by the OJIP test) is usually used to evaluate the photochemical reaction of PSII (Krause and Weis, 1991; Strasserf and Srivastava, 2010; Strasser, 2004; Xu et al., 2019). The multi-function plant efficiency analyzer (M-PEA, Hansatech, UK) produces instantaneous fluorescence measurements within several seconds at a resolution ratio of 100 kHz. The dark adaption was sustained for 10 min, after which the FI was lowest, which is known as the “O” point (as was shown in Fig. 5). The electron is then transferred to the P680 reaction center of PSII and is activated. As shown in Fig. 1 (b), the electron will be transferred to QA and then reduced to Q− A . The electron that is transferred from P680 to QA needs 250–300 ps, while the transfer from Q− A to QB needs around 100–200 μs (Krause and Weis, 1991), which causes an accumulation of Q− A . During this process, the FI increases rapidly to the “J” point (Strasser, 2004; Govindjee, 1995). The electron is continually trans2− ferred from Q− A to QB and is then reduced to QB , after which the PSII reaction center is completely closed. The FI increases to the maximum (“P”) and then gradually decreases (as was shown in Fig. 5). The mechanism of “I” is still unclear. The OJIP curve was correctly recorded by PEA because of its high-resolution ratio. In this study, the OJIP curve was recorded for the microalgal cells, except for when some conditions of SBS were similar in the CAP. Several parameters were acquired according to the OJIP curves. For example, the maximum photochemical efficiency (φPo), the quantum ratio used for the electron transfer (φEo) and the quantum ratio used for the heat dissipation (φDo). Meanwhile, some specific activity parameters were recorded, including ABS/RC and DIo/RC, which reflect the absorbed and consumed light energy of the unit PSII reaction center, respectively; and TRo/RC and ETo/RC, which reflect the light energy used for the reduction of QA and electron transfer of the unit PSII reaction center, respectively. More detailed discussions have been provided by previous studies (Krause and Weis, 1991; Strasser, 2004; Krüger et al., 2010; Srivastava et al., 1997). 2.4. CO2 conversion efficiency The CO2 gas in the NFCAP system was first converted to SBS and then fixed to the microalgal cells. During this process, the CO2 gas undergoes a conversion from gas to liquid to solid. Understanding the specific conversion efficiency of each process is of significant importance. The system is complicated; therefore, to determine its CO2 fixation efficiency, several assumptions are necessary: • All of the CO2 gas in the CAR was fixed in the solution and was converted to inorganic carbon (H2CO3, NaHCO3 and Na2CO3). • CO2 gas on the top of the CAR was not considered. • Material loss during the experiment was not considered. • The carbon content of the microalgal biomass was 50%. • All of the carbon source during microalgal growth came from NaHCO3 (CO2 from atmosphere was not taken into account).

Based on the above assumptions, the CO2 conversion efficiency in the NFCAP system can be defined as:  ηg−l ¼

 V inlet−CO2 gas −V outlet−CO2 gas  100% V inlet−CO2 gas

ð6Þ

ð5Þ

where ρ is the phase density, Cμ is the constant, k is the turbulent kinetic energy, ε is the turbulent dissipation and α is the volume fraction. 2.3. The chlorophyll fluorescence of microalgal cells The different CAP concentrations resulted in different biomass growth rates because HCO–3 is the dominant carbon source of Spirulina

ηl−s ¼

Total increased biomass  50%  100% Total decreased NaHCO3  M C

ð7Þ

where ηg-l and ηl-s represent the conversion efficiencies from CO2 gas to NaHCO3, and from NaHCO3 to microalgal biomass (%), respectively; Vinlet-CO2 gas and Voutlet-CO2 gas represent the volumes of CIM and COM (m3), respectively; Total_increased_biomass is the increased weight of the microalgal biomass in the PBR (g); Total_decreased_NaHCO3 is the

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increasing the solution pH gradually with the growth of the microalgae (HCO–3 → CO2 + OH−). The TIC concentration at 17 h was lower than the initial time (0 h) (Fig. 2 (B)), which may be because the addition of HCl in the culture medium caused the reaction of 2HCl + Na2CO3 → 2NaCl + H2O + CO2. Furthermore, the results indicate that the NF pore diameter has a direct influence on the CAP. With an increase of pore diameter, the pH and Na2CO3 concentration gradually decreased, while the TIC and NaHCO3 concentrations gradually increased during the CAR process. When pore diameter was 0.1 mm, the decreasing rate of solution pH was slower than the other conditions. The NaHCO3 concentration at a pore diameter of 0.1 mm was lower than the other conditions. It may be that the smaller pore diameter increased the flow resistance of the CO2 gas. It can be shown from the Ergun equation that the viscous resistance and inertial resistance are negatively correlated to the NF pore diameter (Kim et al., 1956; Pham et al., 2015). The higher flow resistance blocked the aeration of CO2 gas, thereby decreasing the reaction rate of CO2 and Na2CO3. Therefore, the larger NF pore diameter in the CAR is beneficial to the reaction of CO2 and Na2CO3. Moreover, the CO2 conversion efficiency in the NFCAP system was investigated (Fig. 3(a)). As the pore diameter increased from 0.1 to 2 mm, the biomass growth rate increased gradually from 21 to 44 g/ (m2·d); and the ηg-l and ηl-s increased from 61% to 73% and 18% to 31%, respectively. This may be because the smaller pore diameter increased the flow resistance and reduced the inlet CO2 volume. This means that more CO2 gas was consumed and reacted with Na2CO3, and that the larger NF pore diameter provides more space for the CO2

molar concentration of consumed NaHCO3 in the PBR (mol); and Mc, which is the molar weight of carbon, is 12 g/mol. Because the HCl (35%) added to the culture medium caused a decrease in initial TIC, so we took the NaHCO3 concentration of 17 h as the initial state. 3. Results and discussion 3.1. Optimization of the nickel-foam filled CO2-absorptive photobioreactor system During the operation of NFCAP, the solution pH, TIC, NaHCO3 and Na2CO3 concentrations underwent two stages as the solution pH and Na2CO3 concentration first decreased in the CAR and then increased in the PBR (Fig. 2). Conversely, the solution TIC and NaHCO3 concentrations first increased in the CAR and then decreased in the PBR. The CO2 gas was first converted to NaHCO3 and then to microalgal biomass, as outlined in the following chemical formulas: CO2 + Na2CO3 + H2O → 2NaHCO3, HCO–3 → CO2 + OH– and CO2 + H2O → (C6H12O6)n + O2 (Cheng et al., 2017). During the NFCAP operation, CO2 gas was continually dissolved and reacted with Na2CO3 in the CAR. The dissolved CO2 gas and subsequent NaHCO3 resulted in a lower solution pH and higher TIC. After the reaction in the CAR, the CAP flowed to the PBR where the HCO–3 was captured by microalgal cells and converted to carbohydrate. Microalgal cells adopted HCO–3 as the main carbon source because of the CCM (Tiwari et al., 2019), so the NaHCO3 concentration decreased gradually in the PBR. It has been suggested that OH– is expelled out of the cell, thereby 12.0

Reaction of CO2 and Na2CO3 in CAR

Reaction of CO2 and Na2CO3 in CAR

Microalgae cultivation in PBR

A

HCO3

CO2+Na2CO3 + H2O

CO2 (C6H12O6)n+ O2

CO2+H2O

2NaHCO3

Solution pH

11.0

10.5

10.0

Pore diameter of nickel-foam

9.5

0.5 mm 1.0 mm 1.5 mm 2.0 mm

9.0

Cultivation of microalgae in PBR

B

500 -

Total inorganic carbon concentration (mM)

11.5

HCO3-

CO2+Na2CO3 + H2O

2NaHCO3

CO2

CO2+H2O

(C6H12O6)n+ O2

400

300

Pore diameter of nickel-foam 0.1 mm 0.5 mm 1.0 mm 1.5 mm 2.0 mm

200

8.5 0

2

4

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0 10 10/0

8

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Reaction of CO2 and Na2CO3 in CAR

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70

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10 10/0 0

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C

HCO3

CO2+Na2CO3 + H2O

-

CO2

CO2+H2O

2NaHCO3

Reaction of CO2 and Na2CO3 in CAR 200

200

Pore diameter of nickel-foam

CO2

2NaHCO3 CO2+H2O

(C6H12O6)n+ O2

150

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0.1 mm 0.5 mm 1.0 mm 1.5 mm 2.0 mm

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Cultivation of microalgae in PBR HCO3-

CO2+Na2CO3 + H2O

300

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(C6H12O6)n+ O2

Na2CO3 concentration (mM)

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0.1 mm 0.5 mm 1.0 mm 1.5 mm 2.0 mm

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Fig. 2. Improving conversion of CO2 gas to NaHCO3 solution for microalgal cultivation in photobioreactors (PBRs) with an increased pore diameter of nickel-foam in CO2 absorption reactors (CARs).

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Except for the pore diameter, the relative height of the NF, which is the height ratio of the NF to the CAR (h/H), is another key parameter that affects CAP. As h/H increased under a constant pore diameter of 2 mm, the biomass growth rate increased from 22 to 41 g/(m2·d) and then decreased to 26 g/(m2·d). The ηg-l first increased from 68% to 78% and then decreased to 73%. The ηl-s first increased from 17% to 38% and then decreased to 19%, peaking at an h/H of 0.24. This may be because with a higher h/H, the CO2 gas existing in the porous zone increased, which is beneficial for the reaction of CO2 gas with Na2CO3, causing the ηg-l to gradually increase with an increasing h/H. With a further increase of h/H, the pressure drops in the porous zone became serious, as did the flow resistance of CO2 gas along the flow path, which may have reduced the reaction rate. Additionally, a higher h/H would occupy more physical space, decreasing the inlet CO2 volume. The subsequently decreased reactant would reduce the reaction rate, causing a lower ηg-l. Therefore, the NaHCO3 concentration first increased and then decreased with the increasing h/H. During the experiment, we found that the CO2 gas outflow rate extremely influenced the NaHCO3 concentration, which affected the CO2 fixation efficiency by the microalgae. As the CO2 gas outflow rate increased from 0 to 5 L/min, the ηg-l decreased gradually from 100% to 67% (Fig. 3 (c)). This is because the increased outflow rate caused more CO2 gas to flow to the NF, thereby enhancing the reaction of CO2 gas and Na2CO3. Sufficient NaHCO3 production promotes the biomass growth rate (Cheng et al., 2017). However, further increase of the CO2 gas outflow rate decreased the solution pH below 8, which is unsuitable for biomass growth. Therefore, the biomass growth rate first increased from 24 to 36 g/(m2·d) and then decreased to 22 g/(m2·d). The solution pH and produced NaHCO3 both affected the absorption of NaHCO3; thus, the ηl-s first increased from 17% to 38% and then decreased to 19%. As introduced above, Song et al. (2019) also proposed an absorptionmicroalgae hybrid CO2 utilization system for microalgal cultivation (Song et al., 2019a; Song et al., 2019b; Song et al., 2019c; Song et al., 2019d). We all combined the CO2 absorber and PBRs together for the flue gas removal and microalgae cultivation. However, we have adopted the nickel-foam to increase the CO2 resistance time and to improve the reaction of CO2 gas with HCO− 3 . As a result, our CO2 fixation rate is 86% at CO2 outflow rate of 1 mL/min, while their highest CO2 fixation rate is 78%. It is fully confirmed that the adoption of nickel-foam in the CO2 absorption reactor is useful and helpful to the reaction of CO2 gas with HCO− 3 . 3.2. Exploring the CO2 gas distribution and Na2CO3 solution radial velocity in the nickel-foam by numerical simulation

Fig. 3. Improving the CO2 fixation efficiency and biomass growth rate in a PBR with an increase of pore diameter and relative height of NF and the CO2 gas outflow rate in a CO2 absorption reactor. Note: ηg-l: CO2 conversion efficiency of CO2 gas to soluble NaHCO3, %. ηl-s: Conversion efficiency of soluble NaHCO3 to microalgal biomass, %/. h/H: The relative height of nickel-foam to CO2 absorption reactor height.

reaction. Therefore, the ηg-l increased gradually. The biomass growth rate was closely affected by the CAP. The pH and NaHCO3 concentration varied from 9.44 to 8.83 and 294 to 387 mM/L, respectively, when the pore diameter increased from 0.1 to 2 mm. The solution pH (8.8–9.4) was within the most suitable range for Spirulina growth (8.0–11) (Ogbonda et al., 2007). The NaHCO3 concentration increased gradually, which means that more carbon source was provided for biomass growth. Therefore, the biomass growth rate gradually increased. These results show that the NF pore diameter affects the Na2CO3 and NaHCO3 concentrations of the CAP, which then affects the biomass growth rate.

In order to further investigate the influence of NF on the chemical reaction of CO2 gas with Na2CO3, a numerical simulation model on CO2 volume fraction and Na2CO3 solution radial velocity in the CAR was established by CFD simulation. The CO2 volume fraction at the IPF and OPF are displayed (Fig. 4(a)). The OPF is the outlet surface of the porous zone at h/H = 0.12 and IPF is the inlet of the porous zone at h/H = 0.06. The difference for the CO2 gas volume fraction between IPF and OPF is defined as δ. When pore diameter increased from 0.1 to 2 mm, δ increased from 353 to 1606 mL, which confirmed that a higher proportion of CO2 gas existed in the porous zone. Moreover, the CO2 gas volume fraction in the porous zone gradually increased from 11% to 74%. There may be two reasons for this result: first, the increased pore diameter provides more physical space for the CO2 gas; and second, the low resistance (Hwangbo et al., 2018) of the porous zone promotes the inlet of CO2 gas. Therefore, the CO2 gas volume fraction increased with the pore diameter. In addition, the turbulent parameters changed. With an increased pore diameter, the radial velocity of the NF increased from 0.06 to 0.93 cm/s (Fig. 4(b)). The turbulent viscosity and molecular viscosity increased from 2.6 to 8.7 × 10−4 kg/(m·s) and 2.8 to 6.1 × 10−4 kg/(m·s), respectively. These results show that the irregular porous structure of

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Fig. 4. Increasing CO2 gas volume fraction, molecular viscosity, turbulent viscosity and radial velocity with the increase of pore diameter of nickel-foam.

the NF enhanced the horizontal velocity of the CO2 gas, which is beneficial for the spread of CO2 gas through the porous zone, thus increasing the molecular contact possibility of CO2 with Na2CO3. Moreover, the porous structure is beneficial for decreasing the CO2 bubble diameter, while the larger pore diameter provides sufficient space for the reaction of CO2 with Na2CO3 (Fig. 1 (b)). Another benefit is that the irregular porous structure disturbs the velocity direction of the CO2 flow, which can possibly increase the turbulent kinetic energy (Ye et al., 2018), thereby increasing the turbulent viscosity in the NF. Molecular viscosity is the product of the volume fraction and turbulent viscosity of each phase (Kim et al., 1956), the increased CO2 volume fraction and turbulent viscosity collectively contribute to the increased molecular viscosity. Therefore, the NF is beneficial for the reaction of CO2 with Na2CO3. These results give further insight into the data displayed in Fig. 2: with an increased pore diameter, the solution pH and Na2CO3 concentration

gradually decreased while the solution TIC and NaHCO3 concentrations gradually increased in the CAR. 3.3. Investigating the photochemical efficiency and electron transfer of microalgal cells The molecular CO2 and Na2CO3 first reacted in the NF and then the subsequently produced HCO–3 is transferred to the Spirulina cells (Fig. 1 (b)). The extracellular HCO–3 is captured by the enzyme HLA3 and crosses the cell membrane to the cytoplasmic matrix (Mackinder et al., 2017; Rosenzweig et al., 2017). Thereafter, the HCO–3 is transported by LCIA, LCIB and LCI11, passing through the chloroplast and thylakoid membranes. The HCO–3 is catalyzed by CAH3 in thylakoid lumen to CO2, after which the CO2 will participate to the Calvin cycle (Mackinder et al., 2017; Rosenzweig et al., 2017) and will subsequently

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log10(fluorescence time (µs)) Fig. 5. The chlorophyll fluorescence test with the growth of microalgal cells in the photobioreactor with an increase of pore diameters of nickel-foam.

be converted to PGA, DGA and G3P in turn. Some of the G3P are converted to carbohydrate, while some other G3P are converted to RuBP, which is combined with CO2 to produce PGA (Tiwari et al., 2019). During the Calvin cycle, Pi, NADP+ and ADP are continually produced and subsequently transferred to the light reaction (Xu et al., 2019; Fu et al., 2019). Meanwhile, the light reaction is conducted in the thylakoid membrane (Sun et al., 2015). The P680 reaction center in PSII is activated by the light quantum to decompose the H2O molecule. An

electron is released at the same time and is transferred through the chain as follows: P680 → QA → QB → PQ pool → b6f → PC → P700 → Fd → FNR. Next, NADPH is produced by FNR catalysis (Tiwari et al., 2019). Additionally, ATP is continually produced by ATP synthase. Therefore, HCO–3 affects both the Calvin cycle and light reaction (Hwangbo et al., 2018) in the microalgal cell. The chlorophyll fluorescence of the OJIP curve is effective for evaluating the PSII electron transfer and photochemical efficiency (Krause and Weis, 1991;

W. Guo et al. / Science of the Total Environment 713 (2020) 136593

Fig. 6. The quantum ratio used for electron transfer (φEo) and heat dissipation (φDo), maximum photochemical efficiency (φPo), the absorbed (ABS/RC) and consumed (DIo/ RC) light energy of unit reaction center and the light energy used for QA reduction (TRo/ RC) and electron transfer (ETo/RC) of unit reaction center of microalgal cells in a photobioreactor with an increase of pore diameter, relative height and CO2 gas outflow rate.

Strasserf and Srivastava, 2010). With the growth of microalgae, the FI gradually increased. At a pore diameter of 0.1 mm, the FI was far lower than under other conditions. This can be explained by the low NaHCO3 concentration at the initial cultivation time (Fig. 2 (c)). With the increased pore diameter, the FI gradually increased with the growth

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of the microalgal cells, which is also evidence of a higher photosynthesis rate. When the pore diameter increased from 0.1 to 2.0 mm, the φPo and ABS/RC increased from 0.48 to 0.52 and 5.5 to 6.3, respectively (Fig. 6 (a)). This means that the maximum photochemical efficiency (Undurraga et al., 2016) and the absorbed light energy of the unit reaction center (Gan et al., 2019) were increased. As with the increase of NF pore diameter, the HCO–3 concentration of the CAP was gradually increased. The sufficient amount of HCO–3 promoted the Calvin cycle reaction, thus the requirements for ATP and NADPH intensified, which promoted the antenna pigment (Liu et al., 2014) to absorb more light energy. The higher absorbed light energy enhanced the maximum light energy conversion efficiency of the PSII reaction center, so the φPo gradually increased. Moreover, the φEo, ETo/RC and TRo/RC increased from 0.19 to 0.23, 1.1 to 1.3 and 2.68 to 2.79, respectively, which indicates that the electron transfer chain was accelerated. The higher φEo and ETo/RC show that electron transfer from QA to QB was enhanced. Furthermore, the φDo and DIo/RC decreased from 0.54 to 0.48 and 3.3 to 2.6, respectively, indicating that the light energy used for heat dissipation decreased. The absorbed light energy by the antenna pigment includes three aspects: heat dissipation, fluorescence and conservation of energy trapped by the reaction center (Prasad et al., 2016). The decreased heat dissipation indicates that a higher proportion of light energy was used for photosynthesis. Therefore, the photosynthesis rate was gradually increased with the increased NF pore diameter. Ultimately, the CO2 fixation efficiency of ηg-l was increased to 73% at a pore diameter of 2 mm. Additionally, the FI at h/H 0.12, 0.18 and 0.24 was recorded (the CAPs that were similar to other conditions were not considered). With the growth of microalgae, the FI increased, especially at 65 h (Fig. 6 (b)). With an increased h/H from 0.12 to 0.24, the φPo and ABS/RC increased from 0.45 to 0.52 and 5.6 to 6.8, respectively. It is evident that the light energy absorbed by the antenna pigment increased, which indicates an increase of the optical photochemical efficiency, thereby increasing the φPo. Moreover, the φEo, ETo/RC and TRo/RC increased from 0.16 to 0.23, 0.9 to 1.2 and 2.6 to 2.9, respectively. The higher quantum ratio and absorbed light energy of the reaction center, which is used for electron transfer, means that the PSII process was enhanced. This may be because of the higher content of HCO− 3 . The higher ETo/RC value shows that the electron transfer rate was increased, which is helpful for biomass growth. Furthermore, the φDo and DIo/RC decreased from 0.55 to 0.44 and 4.1 to 3.5, respectively. The decreased heat dissipation energy means that the light energy utilization efficiency increased. With the increase of h/H from 0.06 to 0.3, the CO2 gas volume fraction in the porous zone increased. Furthermore, the flow resistance of the CO2 gas increased simultaneously, which resulted in the ηg-l first increasing and then decreasing. In addition, with the increased h/H, the NaHCO3 concentration first increased and then decreased, which influenced light energy absorption (Chen et al., 2014) by the reaction center and the electron transfer chain of PSII during photosynthesis. As a result, the biomass growth rate first increased and then decreased. Both the absorbed NaHCO3 concentration and biomass growth rate resulted in the ηl-s first increasing and then decreasing. Ultimately, the ηg-l, ηl-s and biomass growth rate reached to 78%, 38% and 41 g/(m2·d), respectively, at an h/H of 0.24. The FI of the microalgal cells with CO2 gas outflow rates of 0, 1, 2 and 5 L/min were recorded (Fig. 6(c)). With the increased CO2 gas outflow rate, the φPo and ABS/RC first increased from 0.39 to 0.48 and 5.6 to 8.1, respectively, and then decreased to 0.44 and 6.9, respectively. The φEo, ETo/RC and TRo/RC increased from 0.17 to 0.20, 0.95 to 1.22 and 2.7 to 2.9, respectively, and then decreased to 0.16, 0.95 and 2.8, respectively. The φDo and DIo/RC decreased from 0.55 to 0.44 and 4.1 to 3.5, respectively. These parameters peaked at a CO2 gas outflow rate of 2 L/ min, which follows the tendency of the biomass growth rate. This may be because with the increased CO2 gas outflow rate, the reaction of CO2 with Na2CO3 is enhanced. The NaHCO3 concentration increased,

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which promoted the Calvin cycle. The accelerated Calvin cycle generated higher ADP and NADPH contents, which enhanced the electron transfer chain of PSII (Xu et al., 2019). Furthermore, the high amount of antenna pigment increased the light energy absorbed by the reaction center. These factors resulted in increased microalgal growth. However, with a further increase in the CO2 gas outflow rate, the biomass growth rate decreased. Even the carbonation effect was enhanced in the CAR, but the lower solution pH (below 8) reduced enzymatic activities. Thus, the biomass growth rate decreased thereafter. Therefore, the increased CO2 gas outflow rate decreased the ηg-l, but the NaHCO3 concentration increased gradually. This would affect the light energy absorbed by the reaction center and the electron transfer chain, which causes the biomass growth rate first increase and then decrease. The biomass growth rate peaked at 36 g/(m2·d) with the CO2 gas outflow rate of 2 L/min. Therefore, it is suggested that the CO2 gas outflow rate of the NFCAP system should be kept at 2 L/min. 4. Conclusion A novel porous nickel-foam filled CO2 absorptive photobioreactor system was developed to strengthen CO2 conversion into NaHCO3 within a short time to improve the photosynthesis of microalgal cells. Numerical simulation showed that porous nickel-foam promoted the Na2CO3 solution radial velocity and CO2 volume fraction in the CO2 absorption reactor. The conversion efficiency from soluble NaHCO3 to microalgal biomass first increased and then decreased with an increased pore diameter (peaking at 2 mm) and relative nickel-foam height (peak: 0.24) and CO2 gas outflow rate (peak: 2 L/min). A sufficient HCO–3 supply promoted the quantum ratio used for electron transfer and the maximum photochemical efficiency, increasing the biomass growth rate 1.1 times when the pore diameter of the nickel-foam increased from 0.1 to 2 mm. The present work has successfully reduced the reaction time of CO2 gas with the Na2CO3 solution to several minutes; however, it is still far away from satisfying the requirements of large-scale applications because the contact time of CO2 gas with the Na2CO3 solution is only several seconds. Therefore, further research is still needed to reduce the reaction time of CO2 gas with the Na2CO3 solution. Declaration of competing interest We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review, of the manuscript entitled “A novel porous nickel-foam filled CO2 absorptive photobioreactor system improving CO2 conversion with microalgae biomass”. Acknowledgements This study was supported by the National Key Research and Development Program-China (2016YFB0601003) and the 2018 Zhejiang University Academic Award for Outstanding Doctoral Candidates. References ANSYS I, 2011. ANSYS FLUENT User’s Guide. Canonsburg, PA. Chen, L., et al., 2014. Two photon absorption energy transfer in the light-harvesting complex of photosystem II (LHC-II) modified with organic boron dye. Spectrochim. Acta A Mol. Biomol. Spectrosc. 128, 295–299. Cheng, J., Yang, Z., Ye, Q., Zhou, J., Cen, K., 2016. Improving CO2 fixation with microalgae by bubble breakage in raceway ponds with up-down chute baffles. Bioresour. Technol. 201, 174–181. Cheng, J., Lu, H., He, X., Yang, W., Zhou, J., Cen, K., 2017. Mutation of Spirulina sp. by nuclear irradiation to improve growth rate under 15% carbon dioxide in flue gas. Bioresour. Technol. 238, 650–656.

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