Carbon dioxide sequestration and its enhanced utilization by photoautotroph microalgae

Environmental Development xxx (xxxx) xxx–xxx

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Environmental Development journal homepage: www.elsevier.com/locate/envdev

Carbon dioxide sequestration and its enhanced utilization by photoautotroph microalgae Ritu Verma, Aradhana Srivastava

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University School of Chemical Technology, Guru Gobind Singh Indraprastha University, Sec-16C, Dwarka, New Delhi 110078, India

A R T IC LE I N F O

ABS TRA CT

Keywords: CO2 sequestration Microalgae Illumination Aeration Agitation Photobioreactor

The ceaseless use of non-renewable fuels leads to the emission of CO2 and other GHG’s. Annual Greenhouse Gas Index by National Oceanic and Atmospheric Administration (NOAA) Earth System Research laboratory (ESRL) shows an exponential increase in greenhouse gases led by CO2. Controlling CO2 levels is dire need considering the current trends. The present review highlights different CO2 sequestration (CS) methods including microalgae based CO2 sequestration as the main focal point. It amalgamates the potential microalgae types, their cultivation conditions for lipid and biomass build-up at the expense of sequestered CO2 from air when grown in closed systems. In convention, closed systems are photobioreactors. Photobioreactor design features such as agitation, aeration, and illumination, ought to be ideal for microalgae growth using substrate CO2 economically. Suitable bioreactor design features are highlighted for high cell density microalgae cultivation in photobioreactor. Some successful configurations are also critically reviewed and highlighted for high CO2 sequestration producing enhanced biomass and lipid. Stirred tank photobioreactor, when growing potential microalgae strain, is concluded as best configuration for achieving highest CO2 sequestration rate and hence high cell density biomass with lipid biosynthesis. In addition, coherent and cost-effective CO2 sequestration techniques using microalgae are required in order to increase the effectiveness of the cultivation process in photobioreactor.

1. Introduction Increased GHGs in the earth’s atmosphere is causing many drastic climatic changes including global warming. This is mainly due to industrialization, combustion of municipal solid waste and transportation. Rising CO2 is contributing 76% share in global warming causing melting of glaciers and extinction of ice in the polar regions of the earth. It resulted in average earth’s temperature rise of 1.4 °C in the period of 1993–2003. The combined effect of thermal expansion of sea, melting glaciers, ice caps and polar ice sheets, had caused an average rise in sea level of 1.8 mm/year (Pachauri, 2007). Global temperature rise causes uneven rainfall patterns which directly affects agriculture by decreasing crop production (Ruchita and Rohit, 2017). Biodiversity is affected due to presence of GHGs trapped in the troposphere which changes the characteristics of the soil, water, and air. Sustaining the microflora balance in the atmosphere requires removal of GHGs and adding oxygen via increased photosynthesis (APA, Relatorio, 2009). International Energy Agency (IEA) and Natural Gas Intelligence (NGI), based on daily Gas Price Index (GPI) calculations, estimates the annual CO2 emission to be 32.1 billion metric tons (Source: http://www.naturalgasintel.com). Generally, the concentration of CO2 in the atmosphere can be reduced by using three major strategies that include reducing and controlling CO2 emissions in the

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Corresponding author. E-mail address: [email protected] (A. Srivastava).

https://doi.org/10.1016/j.envdev.2018.07.004 Received 12 October 2017; Received in revised form 11 May 2018; Accepted 5 July 2018 2211-4645/ © 2018 Elsevier B.V. All rights reserved.

Please cite this article as: Verma, R., Environmental Development (2018), https://doi.org/10.1016/j.envdev.2018.07.004

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atmosphere; capture existing CO2 for long-term storage; and by developing alternatives to carbon-based fuel. CO2 sequestration techniques should be analyzed considering their efficiency, cost, environmental impact, and the stability of captured carbon with time. The present review discusses various CO2 sequestration processes with critical analysis for their applicability. The limiting factors must be known for analyzing the overall efficiency of any sequestration process being used. Most methods sequestrate CO2 but it is present as intact molecule. However, biological sequestration by microalgae has better stability of captured carbon with time by transforming CO2 to glucose via photosynthesis which is utilized further for the lipid biosynthesis. Therefore, current review also discuss about potential microalgae, its required growth condition, and the bioreactor types used for cultivation. Only drawbacks with microalgae are their slow growth rate and shear sensitivity (Tang et al., 2012; Michels et al., 2016; Rodriguez et al., 2016). Enhanced CO2 sequestration rates are possible if high cell density microalgae is cultivated in novel photobioreactor. Therefore, this work also discusses critical engineering parameters to be employed in this photobioreactor to cultivate shear sensitive microalgae. Suitable illumination system; aeration and agitation assembly with their effective designs are discussed for cultivation of shear sensitive microalgae. This review is one of its kinds as it focuses all together a critical analysis of biological CO2 sequestration using microalgae; engineering parameters used in novel photobioreactor to get high cell density resulting in enhanced CO2 sequestration rate; and potential microalgae types to deliver high lipid content and other value added products along with CO2 sequestration. 2. CO2 sequestration processes CO2 sequestration processes are mainly of two types i.e. biological and non-biological. They are elaborated on the basis of carbon sinks for sequestration and their environmental impacts. Potential processes are described below. 2.1. Non biological sequestration processes Non biological processes comprises of oceanic, geological and chemical sequestration. Their details are summarized below. 2.1.1. Oceanic sequestration Ocean covering 2/3rd of the earth reserves highest CO2 content i.e. 50 times more than atmospheric CO2 (Raven and Falkowski, 1999). Oceanic carbon sequestration is facilitated by both biotic and abiotic processes. Abiotic process involves the direct injection of carbon dioxide into sea water. Injection made to maximum feasible depths of ocean for minimizing the CO2 leakage. However, biotic processes are unique as they involve oceanic fertilization that favours further utilization for useful products (Lal, 2008). High salinity in oceanic water and high temperature negatively regulates the CO2 solubility in marine water. Considering this, the ocean closer to equator line will have lowest carbon dioxide sequestration. Sequestrating CO2 at depths of the ocean makes the process efficient but uneconomical due to high depth (̴3000 m) pipelines. 2.1.2. Geological sequestration Geological sequestration involves storage of carbon from the atmosphere via underground geological formations. This method has been used by numerous petroleum industries since the 1970s. It not only reduces greenhouse gas emission but also contributes in economic oil recovery process. A large volume of CO2 usage and its leakage probability may only enhance the cost (Kovscek and Cakici, 2005; Gunter et al., 1997). Geological sequestration is preferred for a limited period CO2 sequestration and short time storage. 2.1.3. Chemical sequestration Chemical sequestration comprises of selective chemical reactions. CO2 transforms to a modified and stable compound, carbonates of magnesium and calcium obtained from rocks (Maroto-Valero et al., 2005; Kojima et al., 1997). High volume reduction capability of sequestered CO2 in this process makes it attractive. Engineers are working on optimizing the factors such as temperature, pressure, raw material generation and its chemistry to enhance rate of reaction at low cost so that it can become an industrially applicable strategy. 2.2. Biological sequestration processes Biological sequestration techniques are categorized as oceanic fertilization, terrestrial sequestration via soil carbon and phyto sequestration. Carbon dioxide sequestration using microalgae cultivation is an efficient process which is also explained below in detail. 2.2.1. Terrestrial sequestration Sequestration occurs via either phyto sequestration or soil carbon sequestration. Assurance of long term storage of carbon content and high volume carbon sinks are prime attraction. It provides sustainable CO2 cycle between atmosphere and earth. Management of ecosystem such as enhanced plantation on global level prevents deforestation and hence improves the efficiency of this naturally occurring sequestration process. However, this dependency on environmental factors becomes a disadvantage too (Lal, 2008; Post et al., 2009). 2

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2.2.2. Oceanic fertilization Phytoplankton in marine water utilizes dissolved CO2 via photosynthesis generating storage carbon sugars that further metabolizes. Carbon is in a continuous cycle within the ocean in this method. Fertilization can be performed by enhancing limiting nutrients in the ocean that prompts the phytoplanktonic evolution (Yang et al., 2008; Wolff et al., 2011). 2.2.3. Microalgae based sequestration Microalgae cells have carbon concentration mechanisms (CCMs) in which their carbon concentrating structures i.e. pyrenoids concentrates CO2 around enzyme ribulose 1,5-bisphosphate carboxylase oxygenase (RuBisCo) and hence improves photosynthetic efficiency of microalgae cells (Price, 2011). This strategy is leading among others due to high photosynthetic efficiency of microalgae in bioconversion of carbon into no-fuel co-products (Xie et al., 2014). 1 kg of microalgae biomass can sequestrate 1.83 kg of carbon dioxide (Jiang et al., 2013). Microalga captures energy in light cycle and stores it for converting ADP and NADP into ATP and NADPH respectively, then utilize these energy molecules in dark cycle for transforming CO2 into valuable organic compounds via Calvin Benson cycle (Zhao and Su, 2014). All other mentioned methods are site specific but microbial CO2 sequestration is the only possible way to implement at any part of the globe if required. There is a thrust to identify potential flora and fauna like microalgae. Optimum temperature, pH, salinity, illumination, mixing, aeration and proper nutrition for microalgae are the major conditions to be maintained for maximizing CO2 sequestration and microalgae growth (Subashchandrabose et al., 2013; WeiBao et al., 2013). In addition, there is demand to develop a closed system (bioreactor) type, scalable in nature. Potential microalgae selection, essential design parameter in bioreactor combining CO2 sequestration is the focal point of the review. Effective engineered design would bring major breakthrough in sustainable technology for CO2 sequestration by microalgae. 3. Potential microalgae and their growth requirements These unicellular photoautotrophs are commercially attractive. They have 10 times greater efficiency of utilizing light than terrestrial plants; higher efficiency of directing energy into growth, faster growth rates, higher CO2 fixation rate, easy cultivation and harvesting of value added products as compared to other plants (Xie et al., 2014). Although it is widely accepted for CO2 sequestration and biofuel production, but the economic process feasibility is still under extensive research. Microalgae have the capability to grow in open systems i.e. uncontrolled and unregulated system. Adverse process conditions may not fully inhibit the growth but slow it down. The theoretical yield of microalgae was reported about 300tons/Ha/Year in open system (ponds, microalgae farms) due to slow growth (Zhao and Su, 2014; Sheehan et al., 1998). For waste CO2 utilization, microalgae farms are generally placed alongside polluting industries. Soluble CO2 and NOx are used for microalgae growth. The same process can also be performed in a closed system (photobioreactor) using flue gases for the production of algal biomass (Singh and Singh, 2014). Macronutrients like phosphorous, carbon and nitrogen, micronutrients (iron, calcium, molybdenum, chloride, boron, manganese, cobalt, copper and zinc) and vitamins like H (Biotin), B1 (thiamine) and B12 (cyanocobalamin) are the nutrients required for microalgae growth (Razzak et al., 2013; Verma et al., 2017). Carbon is supplied for growth as sequestered CO2 from the air (CO2 as 0.05% v/v where v/v denotes volume of CO2 per volume of air). Brackish water, fresh water, and seawater support microalgae growth as they consist of nitrates, phosphates, carbonates, minerals and other ions. These nutrients and CO2 utilized by microalgae via photosynthesis for the build-up of microalgae biomass and lipid biosynthesis. Studies reveal that wastewater supports high lipid induction in microalgae along with high biomass production (Table 1). Table 1 shows several microalgae strains cultivated under different conditions utilizing the CO2 as a carbon source (except in study 4). Lipid content and growth of microalgae are dependent on temperature, pH, nutrient (carbon source) supply under nitrogen limited/ rich conditions, illumination and aeration pattern. Nitrogen limitation and high illumination favor lipid metabolism in microalgae, however, this will restrict the biomass concentration build up. The high lipid and the biomass production is a result of increased CO2 sequestration volume. About 2–5%, (v/v) CO2 in air supports the microalgae growth. Overall reviewing the various strains, two species Nannochloropsis sp. and Chlorella emerged to have potential in terms of high CO2 sequestration based fermentation. The fermentative metabolism for the biomass generation and the lipid biosynthesis is summarized here in two phases i.e. carbon limiting and nitrogen limiting conditions. Overall reaction in aerobic carbon limiting medium is triggered with the two incident light energy photons allow sugar generation via photosynthesis, resulting in biomass generation using glycolysis followed by tri carboxylic acid cycle. Carbon flux to algal biomass synthesis is enhanced if Mg2+, Mn2+, K+ are present as cofactors however fatty acid synthesis is triggered in presence of Mg2+, Mn2+, biotin, Flavin, and NADPH (Gruyter, 1988). The overall stoichiometry can predict theoretical yield of biomass when nitrogen source is defined. Lipid and fatty acid biosynthesis process is triggered under nitrogen limiting condition, catalysed by fatty acid synthase, in which fatty acid carbon chain is formed stepwise manner from 2-carbon units derived from the malonyl groups, with subsequent decarboxylation. Malonyl CoA is synthesized in a biotin dependent carboxylation of acetyl –CoA. One mole of CO2 is added per mole of malonyl CoA synthesized, and hence CO2 sequestration rate increased (Gruyter, 1988). Combined starvation of nitrogen and phosphorous under CO2 enriched condition in microalgae triggers the lipid synthesis with increased in C16 and C18 carbon content (Sharma et al., 2012). Not only the nitrogen limitation in media, the stress induced by addition of salts (NaCl), heavy metals (Cadmium, Iron, Copper and Zinc), Acid/Base (Low or Alkaline pH), and UV radiation to medium also reported to have enhanced lipid production (C15 to C17 fatty acids) by photoautotrophic microalgae (Sharma et al., 2012). Many of such conditions do not favor autotrophic microalgae 3

4

Chlorella sp. Chlorella vulgaris #259 (UTEX) Chlorella vulgaris YSW-04 Chlorella pyrenoidosa Chlamydomonas reinhardtii

UTEX 2341 Chlorella sorokiniana UTEX 1230 Chlorella protothecoides

Chlorella minutissima

CCAP211/11 N Chlorella vulgaris Biejerinck

Municipal wastewater, Biocoil photobioreactor, pH-7.5, Injection of air and small amount of CO2

Stirred tank bioreactor, Temperature-25 °C, Agitation-200 rpm, Illumination- 25 µmol m-2 s-1, Aeration-1LPM carrying 5% CO2, 14 days, Watnabe’s (Nitrogen abundance)- Low nitrogen medium -doHeterotrophic cultivation, JAH(Jerusalem artichoke hydrolysate), Erlenmeyer flask, Temperature-28 °C, Agitation-220rpm Heterotrophic cultivation, Medium-glucose Heterotrophic, Medium-Glucose+Corn powder hydrolysate (CPH) Cylindrical glass photobioreactor, Temperature-26 °C, Illumination300 µmolm-1 s-1, Air+ Pure CO2 supply (0.25vvm), Modified f/2 medium, 8 days Polycarbonate bottles, Air flow rate-0.2LPM, Constant fluorescent light, Phototrophic, CO2 Heterotrophic, glucose, acetate Mixotrophic, glucose, glycerol Pre-treated piggery wastewater (Total Nitrogen-510-85 mg/l, Total Phosphate-54.3-13.3 mg/l) diluted to Bold basal medium, Illumination-45–50 µmol photon m-2 s-1, Temperature-27 °C, Agitation-150 rpm Mixotrophic cultivation, Diluted piggery wastewater (Total Nitrogen-25–100 mg/l, Total Phosphate-4–16mg/l), pH-8, Air supply-0.3LPM, Illumination-63 µmol m-2 s-1, Temperature-27 °C

Shihira & Kraus

CCAP211/11 N Chlorella emersonii Shihira & Kraus

-do-

Chlorella emersonii

CCAP 211/11BH

Tubular photobioreactor, Liquid velocity-0.63 m/s, Air supply5LPM, Illumination- 130 µmol m-2 s-1, Temperature-25 °C, 3 days, Watnabe’s medium (Nitrogen abundance)-Low nitrogen medium

25.5

23–36 21–34 28–29 13–23

33–38

50.3–57.8 46.1 32–34

31–57 20–22 43–46

18–40

29–63

25–34

28–58

33.6

39.8

Erlenmeyer flasks in orbital shaker incubator, Temperature-25 °C, Continuous illumination-100 µmol photons/m2/s, Single batch-2 weeks, Input air contained 5% carbon dioxide -do-

Chaetoceros calcitrans

CS 178 Chaetoceros muelleri F&M-M43 Chlorella vulgaris Biejerinck

Lipid Content (% DW of cell)

Substrate and cultivation conditions

Microalgae strain

Table 1 Different microalgae used under controlled cultivation conditions with lipid content as % Dry weight (DW) of cell.

(Kong et al., 2010)

(Xu et al., 2006) (Chiu et al., 2008) (Liang et al., 2009) (Ji et al., 2013) (Wang et al., 2012)

(Cheng et al., 2009) (Xiong et al., 2008)

(Scragg et al., 2002) (Illman et al., 2000)

(Rodolfi et al., 2009)

Ref.

(continued on next page)

Chlamydomonas mexicana exhibited 22.7% higher lipid content than Chlamydomonas reinhardtii due to effective agitation and sufficient nutrients obtained from diluted anaerobic piggery wastewater effluent.

Maximum lipid is produced in Chlorella emersonii under nitrogen limiting condition as 63%. However, Chlorella vulgaris, Chlorella minutissima and Chlorella protothecoides also exhibited comparable lipid content under favourable operating conditions of nitrogen limiting medium, high intensity illumination, stirred tank bioreactor and heterotrophic cultivation with glucose enrichment. Results highlighted the potential of Chlorella genus for heterotrophic conditions, high CO2 utilization for lipid production and waste water treatment.

Under same operating conditions, Chaetoceros calcitrans CS 178 exhibited 15.57% higher lipid content than Chaetoceros muelleri F&MM43 suggesting specie calcitrans has better potential for CO2 sequestration during lipid synthesis.

Remarks

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Batch lipid data obtained during exponential growth, (during growth in nitrate limited medium) Initially grown in airlift bioreactors then in polyethylene bags & finally in open raceways in presence of air, Illumination150 µmol m-2 s-1 during reactor operation Semi continuous bench scale reactors, f/2 medium, Air supply, Anaerobically digested wastewater effluent (Diluted 3–18%) (Total Nitrogen-80 mg/l, Total Phosphate-11.43 mg/l), pH- 7–7.5 Combination of aerobic/ anaerobically treated swine wastewater (Ammonium-418.8 mg/l, Nitrate-11.3 mg/l, Phosphate-5.4 mg/l) with 50% dilution, Temperature-25 °C, Continuous illumination45–50 µmol m-2 s-1, Air+CO2 supply (0.5 vvm containing 2%v/v) Erlenmeyer flasks in orbital shaker incubator, Temperature-25 °C, Continuous illumination-100 µmol photons/m2/s, Single batch-2 weeks, Input air contained 5% carbon dioxide -doN-Deprived medium, 0.6 L bubble tubes/Flat photobioreactor, 4 day cycle, Temperature-25 °C, Continuous illumination (Daylight fluorescent tubes-100/150 µmol photons/m2/s)

CCMP525

Nannochloropsis CS 246 Nannochloropsis sp. F&M-M24 F&M-M26 F&M-M27 F&M-M28 F&M-M29 Nannochloropsis sp. F&M-M24

Nannochloropsis oculata

CCAP 849/6

Nannochloropsis salina

Nannochloropsis sp.

Flat panel photobioreactor, 3.5 L reactor volume

Nannochloropsis oculata

NCTU-3

Nannochloropsis oculata

Nannochloris sp. UTEX LB1999

Isochrysis sp. F&M-M37

(Rodolfi et al., 2009)

29.2

24.4 35.7 21.6 60–62

29.6

30.9

(Rodolfi et al., 2009)

(Wu et al., 2013)

30

35

28.7

(Leow et al., 2015) (Gouveia and Oliveira, 2009) (Cai et al., 2013)

(Chiu et al., 2009)

30.7–59.5

29.7-22.7

(Takagi, Karseno (2006))

(Rodolfi et al., 2009)

27.4

29.9–40.3

(Rodolfi et al., 2009)

Erlenmeyer flasks in orbital shaker incubator, Temperature-25 °C, Continuous illumination-100 µmol photons/m2/s, Single batch-2 weeks, Input air contained 5% carbon dioxide Erlenmeyer flasks in orbital shaker incubator, Temperature-25 °C, Continuous illumination-100 µmol photons/m2/s, Single batch-2 weeks, Input air contained 5% carbon dioxide Modified NORO medium, pH-8, Roux bottle, CO2 enriched air0.25LPM carrying 3% CO2, Temperature-30 °C, Illumination- 150 µmol m-2 s-1 Shake flask studies, Phototrophic, CO2 Cylindrical glass photobioreactor, Temperature-26 °C, Illumination300 µmol m-2 s-1, CO2 in input air (0.2LPM, 0.25 vvm) CO2 supply (2–15%)

Ellipsoidion sp. F&M-M31

ATCC 30929 27.4

(Takagi, Karseno (2006))

60.6–67.8

Dunaliella tertiolecta

(Abou-Shanab et al., (2013))

33

Temperature-27 °C, Agitation-150 rpm, Illumination-45–50 µmol ms-1, Anaerobic piggery wastewater effluent (Total Nitrogen-53mg/ l, Total Phosphate-7.1 mg/l) diluted to Bold basal medium. Modified NORO medium, pH-8, Roux bottle, CO2 enriched air0.25 LPM carrying 3% CO2, Temperature-30 °C, Illumination- 150 µmol m-2 s-1 Shake flask studies, Phototrophic

2

Chlamydomonas mexicana GU732420

Ref.

Lipid Content (% DW of cell)

Substrate and cultivation conditions

Microalgae strain

Table 1 (continued)

(continued on next page)

Species of Nannochloropsis exhibited lipid formation even at enhanced CO2 input rate ranging up to 15% in air. Also exhibited high CO2 utilization for lipid production (62%) when grown in flat plate photobioreactor under nitrogen deprived medium. Usage of wastewater as cultivation medium for Nannochloropsis specie does not appeal as alternative for high CO2 sequestration and lipid production.

However, both species of Chlamydomonas didn’t show a great potential for high CO2 sequestration as they both utilized small amount of CO2 and produced cells with less lipid content. It exhibited a great amount of lipid content in cell grown in shake flask utilizing 3% CO2 in air. Results motivated researchers to cultivate Dunaliella tertiolecta in efficient photobioreactor under favourable operating conditions to promote its potential for high lipid production sequestrating high CO2 concentration. It didn’t exhibit any comparable results with other species in 2 weeks cycle. It might be a result of absence of dark cycle and lesser capability of consuming high CO2 concentration. It didn’t exhibit comparable results with other species in 2 weeks cycle. It might be a result of absence of dark cycle and lesser capability of consuming high CO2 concentration. It exhibited a moderate prospective in CO2 utilization for lipid production that gave a possibility of improvement if grown in appropriate bioreactor and operating conditions.

Remarks

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Initially grown in airlift bioreactors then in polyethylene bags & finally in open raceways in presence of air, Illumination150 µmol m-2 s-1 during reactor operation Glass bubble column bioreactor, Continuous stirring, Air supply, Bristol medium, Temperature- 30 °C, CO2, Continuous illumination150 µE m-2 s-1 covering dark cycle also, 18 days fermentation Modified Soil Extract medium, Column form flasks, Temperature30 °C, Continuous illumination-360 µmol m-2 s-1, Enriched air stream carrying 5% CO2 supply – 0.5 vvm, Agitation using magnetic stirrer Erlenmeyer flasks in orbital shaker incubator, Temperature-25 °C, Continuous illumination-100 µmol photons/m2/s, Single batch-2 weeks, Input air contained 5% carbon dioxide -doPrimary clarifier effluent supplemented with CO2 (Ammonium and phosphate-39 mg/l & 2.1 mg/l respectively), Air supply, Agitation300 RPM, Illumination-40 W fluorescent bulbs, 16 h light followed by 8 h dark cycle, pH-6.5–8.9, Temperature- 25–37 °C Temperature-20–35 °C, Magnetic stirring, Air bubbling, Illumination-11,344 lux, Thermostatic control, Jacketed cylindrical bioreactor, Urban waste water effluent 28.1 mg/l & 8.7–11.8 mg/l respectively) (Ammonium and phosphateErlenmeyer flasks in orbital shaker incubator, Temperature-25 °C, Continuous illumination-100 µmol photons/m2/s, Single batch-2 weeks, input air contained 5% carbon dioxide

Neochloris oleabundans

Scenedesmus sp. DM

Scenedesmus obliquus 276-3a

Pavlova salina CS 49 Polyculture (Mixed of Chlorella sp., Micractinium sp., Actinastrum sp.)

Pavlova lutheri CS 182

UTEX 1185

Substrate and cultivation conditions

Microalgae strain

Table 1 (continued)

21.1

(Rodolfi et al., 2009)

(Martinez et al., 2000)

31–31.4

(Rodolfi et al., 2009)

30.9

(Woertz et al., 2009)

(Li et al., 2008)

7–40.3

35.5 4.9–29

(Gouveia et al., 2009)

(Gouveia and Oliveira, 2009)

29

15.9–56

Ref.

Lipid Content (% DW of cell)

Species of Scenedesmus exhibited a great potential for wastewater treatment. However, results highlighted the need to improve the operating conditions for achieving high CO2 sequestration and lipid production.

Species of Pavlova and Polyculture (Mixed of Chlorella sp., Micractinium sp., Actinastrum sp) didn’t show high lipid production. Probably cultivation conditions need to be optimized for this genotype.

Neochloris oleabundans exhibited 9.6% lesser lipid content than Nannochloropsis.Neochloris oleabundans utilizes CO2 in glass bubble column photobioreactor provided with continuous agitation and aeration along with proper photoperiod (Light:dark cycle).

Remarks

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Table 2 Comparison between open systems and closed systems. Factor

Open systems

Photobioreactors or closed systems

Space required Evaporation Water losses CO2 sequestration rate CO2 losses Temperature Weather dependence

High High Extremely high Low High Highly variable Absolute, production impossible during rain

Process control Shear Cleaning Contamination risk Algal species variability Biomass quality Population density Harvesting efficiency Cost of harvesting Light utilization capability Most costly parameters Energy requirement(W) Capital investments Biomass concentration Treatment processes efficiency

Difficult Low None High Restricted microalgae species may be cultivated Not susceptible Low Low High Poor Mixing High Low Low during production, approx. 0.1–0.2 g/l Low, large volume flows due to low concentrations and time consuming processes Almost impossible

Low No evaporation Almost none High Almost none Required cooling Insignificant because they allow production in any conditions of weather Easy High Required None Nearby all microalgae species may be cultivated Susceptible High High Lower Good Oxygen and temperature control Low High High approx. 2–8 g/l High, small volume flows and short time process

Standardization

Possible

growth and hence suggested to be induced during non-growth phase after considerable biomass build-up (Verma et al., 2017). 3.1. Potential microalgae species Species of Chlorella and Nannochloropsis have been emerged as the potential ones for biomass and lipid production sequestering high percentage of CO2 (Table-1). Chlorella originated from fresh water whereas Nannochloropsis from marine. Chlorella has a capability of growing in 40% CO2 at a wide temperature range of 5–30 °C (Singh and Singh, 2014). It produced high lipid content at varying operational conditions (Ji et al., 2013; Cheng et al., 2009; Xiong et al., 2008; Xu et al., 2006). Various studies exhibited the potential of Chlorella sp. for high biomass productivity of 0.421 g of biomass produced per litre per day (g/l/d) at the uptake of high CO2 sequestration (Eloka-Eboka and Inambao, 2017). Nannochloropsis sp. also exhibited high CO2 sequestration rate of 0.42 g of CO2 sequestered per gram of biomass per hour (g/g/h) when cultivated in modified stirred tank photobioreactor (Verma et al., 2017). 4. Microalgae cultivation Open and closed systems are operated at different conditions for microalgae cultivation. An open system having an area approximately 1000–5000 m2 associated with agitation can be commercially successful (Xu et al., 2009) if the agitation system is properly designed. Open ponds usually produces low cell concentration biomass (0.5–0.7 g/l) resulting in high cost of harvesting (Milledge and Heaven, 2013). High cell density cultivation is in demand at present for economics and sustainability. The comparison between closed and open systems is given in Table 2 that emphasize on the demand of an economic and efficient photobioreactor for high cell density culture and high CO2 sequestration (Chen et al., 2014a and 2014b; Rawat et al., 2013). Innumerable types of closed photobioreactors equipped with monitors and controllers have been designed for microalgae growth (Table 1). However, main configurations of photobioreactor are tubular (vertical/horizontal), bubble column or airlift (vertical) and flat plate (FP) (Huang et al., 2017). Characteristics of these photobioreactors are described in Table 3. For high CO2 sequestration rate, the higher gas-liquid mass transfer rate is required. Bubble column exhibits highest gas-liquid mass transfer rates among the above mentioned three configurations. 4.1. Tubular photobioreactor Tubular photobioreactor comprises of looped, straight or coiled tubes (Fig. 1(a)) generally made up of plastics and glass equipped with least monitors and controllers and operated aseptically. Temperature control is possible with the help of keeping submerged or floated tubes. CO2 is given by either supplied medium saturated with CO2 through tubes or by continuously bubbling CO2 in the medium by placing the CO2 line along with inner tube wall. Liquid pumps or airlift device circulates the culture broth through the tubes (Ho et al., 2011; Fernendez et al., 2001). Pumping/airlifting is advantageous with respect to transfer and removal of CO2/ O2 in a liquid medium, no mechanical pumping, no operating parts in tubes and minimum damage of shear sensitive microalgae cells 7

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Table 3 Characteristics of the three main types of closed reactors. Reactor type

Characteristics

Configuration Remarks based on CO2 sequestration

Tubular

High volumetric biomass density but O2 accumulation, photoinhibition and large requirement of land

Bubble Column (Vertical Tube)

Greatest gas exchange, best photosynthetic efficiency, best exposure to light and dark cycles, less land requirement but high cost and scalability problem

Flat plate

Low power consumption, shortest O2 path but low photosynthetic efficiency and sometimes shear damage to cells from aeration Contains all advantages of bubble column, efficient agitation and aeration system, favourable hydrodynamic conditions, no settling of cells due to impellers

CO2/O2 concentration imbalance throughout the tubular length due to CO2 utilization, and only respiration in the night but the photosynthesis and respiration during day hours. In case O2 +CO2 added with tube then it becomes configuration similar to bubble column. Bigger bubbles rise may cause rising of the cells and may also produce shear effects. Best CO2 sequestration rates can be expected from this configuration as compared to Tubular and Flat plate configuration. There might be dead pockets in the flat panels due to imperfect gas mixing.

Stirred tank

O2/CO2 balance supply is possible in stirred tank reactor. Agitation and aeration assembly can be improved or modified as per the shear sensitivity of microalgae type and better CO2 utilization (Verma et al., 2017)

Fig. 1. Schematics of different Configurations of Microalgae Bioreactors (a) Vertical and Horizontal tubular Bioreactor (b) Flat Plate Bioreactor (c) Bubble Column Bioreactor (d) Stirred tank Bioreactor.

(Tredici, 2010). Dimensions of the tubular reactor must be carefully taken as increased diameter inversely influences the surface/ volume ratio and illumination homogeneity. The increase in tube length increases the chances of CO2 and pH gradient in liquid, the formation of air pockets during photosynthesis preventing CO2 sequestration; and retention time of liquid inside the tube (Ho et al., 2011; Razzak et al., 2013). The option of static mixers in tubular photobioreactor might improve mass transfer of gases. Scalability of tubular photobioreactor is questionable even at pilot scale for above-mentioned reasons (Ugwu et al., 2005; Eriksen, 2008; Zhao and Su, 2014). 4.2. Flat plate photobioreactor Unique characteristics of flat plate photobioreactor are laminar morphology; high surface/volume ratio and hence higher illuminating surface area; and narrow U-turns resulting in less space requirement than tubular photobioreactor (Fig. 1(b)). However, this configuration promotes lower metabolic activity as seen from little dissolved O2 generation (Sanchez et al., 2003; Razzak et al., 2013). CO2 supplied through the perforated tube at the base of plate provides only air movement parallel to the plates resulting in large dead pockets where microalgae might be present with limited CO2 sequestration. Published work on use of angled plates and their different other orientations suggested best angle and direction to capture optimum sunlight for enhanced biomass cultivation (Carvalho et al., 2006; Sierra et al., 2008; Ho et al., 2011). However, authors believe that these conditions affect CO2 flow pattern in 8

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reactor and result in low CO2 sequestration by cells. Configuration being incompatible with sterilization, algal wall adhesion, high power supply requirement (53 W m−3) than bubble column (40 W m−3) (Sierra et al., 2008), unconventional temperature sensors and controllers requirements, are some limitations to be checked before choosing this configuration. This photobioreactor is preferred over tubular only due to lesser power input (Fernendez et al., 2001). Also, high shear stress damages the cells due to enhanced aeration (Razzak et al., 2013). Exceptionally, a study on the semi-continuous operation of vertical flat plate photobioreactor exhibited high biomass build-up (80–85 g/l) but authors believe that CO2 fixation rate of 16.7 g/l/d to build up biomass is very high to maintain in 1.4 l bioreactor (Hu et al., 1998). Addition to that use of 20–30% of CO2 enriched air did not show inhibiting effects due to the pH change in the medium during CO2 supply. 4.3. Airlift/bubble column photobioreactor It is the simplest photobioreactor configuration, has applications in wastewater treatment, bioprocessing and chemical process industry (Fig. 1(c)) (Ronda et al., 2014; Li et al., 2011). Pneumatically agitated photobioreactor achieves rigorous liquid circulation and mass transfer coefficient with least power input as compared to the other configurations (Verma et al., 2017). Compared to bubble column, airlift provides better mixing and uniform substrate throughout the reactor medium and hence results in 33–50% higher microalgae growth rate (Fernandes et al., 2014). However, added CO2 in air for mixing and circulation would make the operations expensive. Fitting rubber membrane diffuser or dual point sparger; would reduce the cost to some extent by enhancing mass transfer (Poulsen and Iversen, 1998). Parameters like bubble size and aeration rate which affects microalgae growth and metabolism needs to be optimized for each microalgae type as different species are influenced differently by hydrodynamic stress (Ho et al., 2011; Lam et al., 2012). In industries, vertical bubble column photobioreactors are preferred due to less space requirement (less capital cost) and ease of operation. The large diameter columns may have the problem of penetration of light to the cell as light radiation decreases exponentially with distance traveled from the light source (Chisti, 1998; Fernandes et al., 2014). 4.4. Stirred tank photobioreactor Stirred tank photobioreactors given in Fig. 1(d) were initially proposed to cultivate microalgae photo autotrophically in the laboratory and industrial level (Sanchez et al., 2003). It’s simple structure, ease of operation and suitability for large biomass production makes it an ideal choice for microalgae and other cells cultivation (Verma et al., 2017). They are beneficial for studying the microalgae physiology under different growth conditions. These model equipments are provided with monitors and controllers to maintain different growth conditions. It can turn into other different configurations such as bubble column, airlift etc. based on the requirement of operation (Munoz et al., 2005). It can be concluded from Table 3 that stirred tank photobioreactor has more potential than other configurations considering high CO2 sequestration for commercial applications. Bubble column photobioreactor performs better than tubular photobioreactor because of less energy requirement for cooling due to the low surface to volume ratio and high suitability for scale-up. Vertical photobioreactors experience less photoinhibition under high intensity of light and captures more reflected light under the low intensity of light. But flat plate photobioreactor exhibits excellent light harvesting efficiency in comparison to tubular and vertical photobioreactors. The greatest disadvantage of horizontal and helical tubular photobioreactors is that tube length is limited by pH variations, O2 accumulation, and CO2 depletion. 5. Design essentials for photobioreactors Designing photobioreactor for microalgae cultivation and high CO2 sequestration rate is the main focal point for the past decade. Design parameters that affect biomass build up and CO2 sequestration rate are illuminations, mixing and aeration. Their complimentary and co-existing roles are necessary to understand in order to develop an efficient system for high cell density cultivation and higher CO2 sequestration rate. 5.1. Illumination system A proper illumination system increases light intensity and hence penetration and its frequency of exposure to photoautotrophic cells. An optimized surface area to volume ratio and a unique geometry of reactor is essential for efficient illumination distribution. No light saturation or inhibition is desirable. Spatial dilution of light or its distribution over a large surface area prevents light saturation, mutual shading of cells and hence increases the microalgae growth rate and CO2 sequestration (Zeng et al., 2011; Razzak et al., 2013). Each photoautotrophic microalgae species responds differently to a different wavelength of light. So an optimized wavelength can be achieved in the case of single artificial light instead of the natural source (Al-Qasmi and Raut, 2012). When sunlight is the growth rate-limiting component, the maximum value of the light conversion efficiency attained by large-scale culture may lead to a yield of 30–40 g/m2 day (Goldman, 1979). A previous study recommends red light to promote microalgae growth as compared to the combination of blue and red (Mehan et al., 2018). Duration of light and dark cycles influences the photosynthetic efficiency and growth of microalgae. According to a study, biomass losses might reach 25% during night cycle due to variations in light intensity and temperature (Liao et al., 2014). The duration of the dark reactions may be considered as the rate-limiting factor for overall growth (Gordon and Polle, 2007). The 9

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subsequent dark cycle duration depends on the photon flux density of the previous light cycle duration and the fluid residence time during the exposure of different irradiance of light. This combination of light intensity and duration of light/ dark cycle affects photo acclimatization and chlorophyll content of microalgae cells (Pires et al., 2012; Razzak et al., 2013). CO2 sequestration rate is dependent on chlorophyll content of microalgae. Up to the irradiance of 500 µEinst m−2 s−1, photosynthetic rate increases but thereafter becomes constant (Verma et al., 2017). Various illumination source options are present which can be analyzed for their suitability before its use in a photobioreactor. Heterotrophic and mixotrophic microalgae cultivations require special consideration for photoperiod depending on organic substrates and operating conditions used (Perez-Garcia et al., 2011; Chang et al., 2011; Kong et al., 2012). 5.2. Agitation and aeration Agitation and aeration are combined to develop a suitable fluid flow regime of air/ CO2 in the liquid medium to grow shear sensitive microalgae cells in photobioreactor. Growing cells exposure to illumination also affects microalgae growth and CO2 sequestration even under favourable environmental conditions (Suh and Lee, 2003). An ideal agitation and aeration assembly in photobioreactor would increase the mass transfer of nutrients and gases in liquid to the solid culture cells; evenly distributes the illumination to each cell; reduces cell damage due to hydrodynamic stress; and leads to high biomass productivity and high CO2 sequestration (Suh and Lee, 2003; Verma et al., 2017). The mass transfer coefficient of CO2 is dependent on agitation rate, sparger type and the fluid properties (Ugwu et al., 2005). Use of point sparger in conventional bioreactor generates large size bubbles, poor mass transfer, and low CO2 fixation but it can be improved by the installation of static agitator or baffle in the photobioreactor (Ugwu et al., 2008). Bubble formation is more responsible for cell death instead of bubble rise and its bursting in gas sparged reactors, and often gas entrance velocity is used as a measure for analyzing cell damage in these reactors (Ugwu et al., 2005; Freedman and Davidson, 1969). Gas velocity at the exit of sparger should be lower than the critical velocity (threshold value) for minimizing cell damage that can be maintained by more number of nozzles or enhanced nozzle diameter. Sparged gas including carbon dioxide is also a primary substrate for microalgae performing photosynthesis (Barbosa et al., 2005). Excess CO2 (greater than 8% v/v) supplied shows deteriorating effect on photosynthesis and hence the cell growth. Therefore, suitable sparger design is required in photobioreactor considering microalgae as shear sensitive cells. Sparger and impeller govern the hydrodynamic conditions in stirred tank photobioreactor (Deckwer, 1992). Sparger design is challenging if aspect ratio in the reactor is low (Joshi, 2001). Improper selection of sparger and impeller cause various operational problems such as high-pressure drop, plugging of holes, undesirable residence time distribution and formation of dead zones. Low positive pressure drop should be maintained in reactor involve operating cost (Deckwer, 1992; Joshi, 2001). There are more practical concerns involving (a) Maximum possible number of pipes that might be accommodated in the column of the reactor. (b) Sparger location from bottom side considering liquid height in the reactor. (c) Provision of the appropriate sparger types inlet. Authors recommend usage of sieve plate, radial, spider and ring type for the commercial production as described in the literature (Kulkarni and Joshi, 2011). Conventional reactors having impellers and spargers need suitable modifications considering shear sensitivity of microalgae. Unusual but appropriate design features such as use of combination of Rushton (Above) and Marine (Below) impellers along with micro sparger for aeration produces four way flow regime. This combination provided appropriate hydrodynamic conditions for sustainable growth of shear sensitive microalgae in reactor that exhibited high biomass build up along with high specific CO2 sequestration rate of 0.44 g/g/h (Verma et al., 2017). 6. Conclusion The main challenge to researchers working on microalgae based CO2 sequestration at present appear to lie on the effective design of the photobioreactor ensuring high CO2 sequestration rate which will overcome the extra investment on reactor and thus become competitive. High biomass and lipid productivites are a bonus in the process. The potential of microalgae’s contributions to carbon dioxide sequestration has not been given attention worldwide as scientists focused on bio-diesel/ lipid production from microalgae as prime process. In 2015, calculated CO2 emission was 62.92 g CO2/m2 area (Source: IEA, NGI’s Daily GPI calculations) which if utilized for microalgae cultivation contributed 103.14 g of biomass/m2 considering stoichiometry (Rosenberg et al., 2011). High CO2 sequestration rate ensures only by high cell density microalgae cultivation and vice versa. Literature also supports high cell density microalgae cultivation in suitable stirred tank PBRs to attain comparable amount (Doucha and Livansky, 2012; Graverholt and Eriksen, 2007). Coherent and cost-effective CO2 sequestration methods with the assistance of microalgae are required in order to increase the effectiveness of the cultivation process in photobioreactor. Photobioreactor configurations used in laboratory are Flat plate, Tubular, Airlift and Bubble Column, and the Stirred tank reactors. Stirred tank reactor is preferred for microalgae cultivation if sequestered CO2 is used as carbon substrate which also found as best for lipid biosynthesis. In addition, it is scalable. Emphasis has been given to the design of an economical and sustainable photobioreactor by considering the engineering framework. Major challenges such as shear sensitivity of microalgae, and effective use of illumination energy and CO2 are addressed in the technical literature of this review. In future, high cell density microalgae cultivated in stirred tank photobioreactor with enhanced CO2 sequestration rate can be improved upon to have modified photobioreactors configurations or scaling up the same based on the carbon emissions at point source. CO2 sequestration by microalgae will only get due attention of policy and decision makers if it is presented as prime project of 10

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importance decoupled with bio-diesel production. Acknowledgement We are thankful to University School of Chemical Technology, Guru Gobind Singh Indraprastha University, New Delhi, for all the facilities and infrastructure provided. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. References Abou-Shanab, R.A., Ji, M.K., Kim, H.C., Paeng, K.J., Jeon, B.H., 2013. Microalgal species growing on piggery wastewater as a valuable candidate for nutrient removal and biodiesel production. J. Environ. Manag. 115, 257–264. Al-Qasmi M., Raut N., 2012. A review of effect of light on microalgae growth. World Congress on Engineering, Vol I, UK. APA, Relatorio do Estado do Ambiente, 2009. Lisboa: Agencia Portoguesa do Ambiente. Barbosa, M.J., Zijffers, J.W., Nisworo, A., Vaes, W., Schoonhoven, J.V., Wijffeles, R.H., 2005. 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