Bicarbonate produced from carboncapture for algae cultureZhanyou Chi, James V O’Fallon and Shulin Chen

Department of Biological Systems Engineering, Washington State University, Pullman, WA 99164-6120, USA

Opinion

Using captured CO2 to grow microalgae is limited by thehigh cost of CO2 capture and transportation, as well assignificant CO2 loss during algae culture. Moreover, algaegrow poorly at night, but CO2 cannot be temporarilystored until sunrise. To address these challenges, wediscuss a process where CO2 is captured as bicarbonateand used as feedstock for algae culture, and the carbonateregenerated by the culture process is used as an absor-bent to capture more CO2. This process would significant-ly reduce carbon capture costs because it does not requireadditional energy for carbonate regeneration. Further-more, not only would transport of the aqueous bicarbon-ate solution cost less than for that of compressed CO2, butusing bicarbonate would also provide a superior alterna-tive for CO2 delivery to an algae culture system.

Challenges to capturing CO2 for algae cultureThe combustion of fossil fuels, such as coal, petroleum andnatural gas, for energy is a major cause of the increasedCO2 concentration in the atmosphere, and has led to con-cerns about its role in global climate change and oceanacidification [1]. The production of 1 kWh of electricity fromcoal combustion results in the emission of 0.95 kg CO2 [2].A small 50 MW coal-fired power plant produces approxi-mately 1140 metric ton (MT) CO2/day, whereas a mid-sized500 MW plant produces 11 400 MT CO2/day [3].

One potential way to reduce this emission is to capture,transport and store CO2 in geologic formations. However,compared with processes without carbon capture, the coalcombustion process with carbon capture and storage has avery high cost, and becomes a favored technology only if theemission price of CO2 reaches US$67/MT [4,5]. In addition,storage of CO2 in geologic formations could lead to newenvironmental issues such as induction of earthquakeactivity, threat of CO2 leakage, or potential contaminationof groundwater [5,6].

An ideal alternative solution would be to capture CO2 inbiomass, so that it can be either recycled into the bioticcarbon pool, or stored in soil carbon pools as organic orinorganic carbon [7–9]. Production of biofuel from the newlygenerated biomass would reduce the usage of fossil fuels,thus contributing to a reduction in CO2 emissions [10,11].

Biodiesel can be produced from a variety of traditionaloil crops, such as soybeans, canola, palm, corn and jatro-pha. Unfortunately, the production of these crops competeswith that of food resources, and could suffer from produc-tion limitations in the future. By contrast, microalgae

Corresponding author: Chen, S. (chens@wsu.edu).

0167-7799/$ – see front matter � 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tibtech.20

culture has high productivity, does not compete with foodsources and generates valuable co-products [12,13]. How-ever, key challenges, such as high cost of algal biomassproduction, harvesting and oil extraction, must be solvedbefore such cultures are ready for industrial application.

The high cost of feedstock CO2 is the major obstaclefor algal biomass production. All current carbon capturetechnologies require large amounts of extra energy to re-generate the absorbent, leading to significantly decreasedpower plant efficiency and corresponding increased cost ofelectricity (COE). For example, based on the reaction ofCO3

2– + CO2 + H2O Ð 2HCO3–, Honeywell UOP Inc. devel-

oped the BenfieldTM process, which uses a high concentra-tion of potassium carbonate to absorb CO2and convert it intopotassium bicarbonate [5]. Using heat, the bicarbonate isthen converted back to carbonate by releasing CO2. Thisprocess consumes 1381–2549 MJ of extra thermal energy toremove 1 MT CO2 [14], approximately 36.4–67.3% of thetotal electricity produced from coal combustion.

Usually, the land available around power plants is limit-ed, and, thus, CO2 has to be captured and transported toalgae ponds some distance away. However, this is limited bythe high costs of carbon transportation. Typically, CO2 iscompressed to a pressure of 150 atm to be transportedthrough a pipeline. This compression process consumesconsiderable energy and enhances the transportation cost.The cost estimated by Kadam et al. [15] for transporting CO2

100 km was US$8.48/MT CO2 for compression and drying,as well as US$3.30/MT CO2 for pipeline transportation.

Using captured carbon for algae culture also faces otherkey challenges. For example, the captured CO2 cannot betemporarily stored during the night or winter, when algaedo not grow. In addition, there is a significant loss of CO2

from outgas if the algae are cultured in an open system. Asa result of these problems, a maximum of only 25% CO2 iscurrently captured by algae culture*. This is not satisfac-tory for a successful carbon capture process, which requiresthat 90% of the CO2 in flue gas be recovered [4]*.

As a summary, current technology to capture CO2 foralgae culture is limited by the high costs of carbon captureand CO2 transportation, the difficulty of storing CO2 tem-porarily and the low efficiency process. An alternative wayof capturing, transporting and delivering CO2 is thereforerequired for an industrial-scale algal biomass productionsystem.

Handling captured carbon as an aqueous solutionTransport problems arise because captured carbon is storedas compressed CO2, rather than in a water solution under

11.06.006 Trends in Biotechnology, November 2011, Vol. 29, No. 11 537

Opinion Trends in Biotechnology November 2011, Vol. 29, No. 11

normal atmospheric pressure. However, inorganic carbon(Ci) exists not only as CO2 gas, but also as carbonate orbicarbonate salts, the solubility of which in water is veryhigh. For example, the solubility of sodium bicarbonate at25 8C is 9.32% (w/w). If the captured carbon is converted intoa bicarbonate/carbonate aqueous solution, it can be easilytransported in a water pipeline under normal pressure.

Bicarbonate as feedstock for photosynthesisPrevious research on carbon concentration mechanisms(CCM) has revealed that most microalgae and cyanobac-teria can import both CO2 and HCO3

– through the cellmembrane [16–18]. Price et al. [18] presented a detailedsummary on the pathway of bicarbonate and CO2 utiliza-tion (Figure 1).

Once imported into the cell, CO2 or HCO3– accumulate

mainly as HCO3–. Lipid membranes are approximately

1000-fold more permeable to CO2 than to HCO3– and

severe leakage can result if a rapid equilibration betweenCO2 and HCO3

– occurs in the cytosol. Thus, HCO3– is

normally held at a steady state, where its concentrationcan reach 20–40 mM, despite the extracellular CO2 con-centration of 15 mM in fresh water and 2 mM in seawater[18]. In the carboxysome, where carbonic anhydrase (CA)exists [16], rapid equilibration between CO2 and HCO3

–

occurs. Corresponding with the accumulated HCO3–, this

rapid equilibration leads to a high concentration of CO2

around ribulose-1,5-bisphosphate carboxylase oxygenase(Rubisco) in cyanobacterial carboxysomes. In the presenceof this high substrate concentration, Rubisco fixes CO2 inthe Calvin cycle, converting it into organic carbon.

Compared with cyanobacteria, less information is avail-able on Ci transport systems in eukaryotic algae [19].However, it has been reported that, in addition to Citransporters in the cell membrane, eukaryotic algae suchas Chlamydomonas also have chloroplast Ci transporters,

Recyclingleaked CO2

Energy

CO2

CO2e

ActiveCi pumps

e

HCO3-

HCO3-

Accumulated atHCO3

- chemicaldisequilibria

Figure 1. Basic operational components for bicarbonate and CO2 utilization in cyano

ribulose-1,5-bisphosphate carboxylase oxygenase. Reproduced, with permission, from

538

because photosynthesis in eukaryote microalgae occurs inthe chloroplast [19,20]. Thus, HCO3

– might be accumulat-ed and stored in chloroplast stroma. In addition, CA mightcontribute to the transport of HCO3

– into the thylakoidlumen and its conversion into CO2 in the acidic lumen [19].The elevated concentration of CO2 in the thylakoid lumenthen diffuses through pyrenoid tubules in the thylakoidmembrane to the pyrenoid matrix, where it is fixed byRubisco.

According to the equilibrium H+ + HCO3–Ð CO2 + H2O,

H+ is consumed during the conversion of HCO3– to CO2, and

this CO2 is ultimately fixed by Rubisco during photosynthe-sis. Thus, steady-state usage of HCO3

–as the original carbonsource for photosynthesis leaves OH– in the cell, and this hasto be neutralized by H+ uptake from the extracellular envi-ronment. The reduction of H+ in the culture medium un-avoidably leads to an increased pH, which subsequentlychanges the equilibrium between different Ci species. ThepKa of HCO3

– in fresh water at 25 8C and 1 atm is 10.33;thus, the acid/base bicarbonate/carbonate pair can act as astrong buffer around this pH. The increased pH will ulti-mately result in higher CO3

2–:HCO3– ratio. Thus, the algae

culture process regenerates carbonate by means of solarenergy.

Closed-loop bicarbonate/carbonate recirculation foralgae culture and carbon captureBased on the above analysis, it appears feasible to usebicarbonate produced from the carbon capture process asfeedstock for algae or cyanobacteria culture, and to recir-culate the regenerated carbonate for carbon capture, asindicated in Figure 2. If successfully developed, such aprocess will have many benefits for algae culture andcarbon capture, as summarized in Table 1.

In this process, CO2 can be transported as a bicarbonatewater solution, rather than as compressed gas. Zhou and

Leak barrier

Carbonicanhydrase

CO2

Rubisco

Compartment forlocalized CO2elevation andfixation

HCO3-

CA

H+

H+pH regulation

TRENDS in Biotechnology

bacteria. Abbreviations: CA, carbonic anhydrase; Ci, inorganic carbon; Rubisco,

[18].

Alkaliphiliccyanobacteria

culture

Carboncapture

Flue gas

Transport pipeline for regenerated carbonate

Bicarbonate watersolution for

temporarily storage

Transport pipeline for bicarbonate solution

TRENDS in Biotechnology

Figure 2. Closed-loop bicarbonate/carbonate recirculation for algae culture and carbon capture.

Table 1. Advantages of closed loop recirculation of carbonate for algae culture and carbon capture

Factor Traditional process Closed-loop process

Transportation of captured carbon As compressed gas As bicarbonate water solution; cost is significantly reduced

Carbonate regeneration Heating or reduced pressure Carbonate regenerated in algae culture, energy is saved

Captured carbon for permanent storage Geologic storage as CO2 gas Converted into biomass; potential biofuel production

Captured carbon for temporary storage Not feasible to store as gas Store as bicarbonate solution, used when sun light is available

CO2 absorption facility Indispensible Not necessary

CO2 loss in algae culture High Low

Contamination control Difficult Simple in high pH culture

* Benemann, J. (2009) Growth and productivity of algae biomass. Algae BiomassSummit, 6–9 October 2009, San Diego, USA.

Opinion Trends in Biotechnology November 2011, Vol. 29, No. 11

Richard estimated the cost to transport water horizontallyfor 100 km to be US$0.05–0.06/m3 by canal and US$0.104–

0.125/m3 by water tunnel [21]. A bicarbonate solution islikely to have a much lower transportation cost than thecorresponding amount of compressed CO2. In addition, thetransportation cost of a water solution can be linearly re-duced if the transport distance is shortened, whereas com-pression is obligatory for any distance of CO2 gastransportation.

For the algae culture process, the bicarbonate watersolution can be stored during the night or over winter andsupplied to the algae culture system during the day andsummer. For example, the daily emission of 1140 tons ofCO2 from a small 50 MW power plant can be stored as a 22800 m3 sodium bicarbonate solution. In addition, deliveryof this bicarbonate solution to an algae culture system doesnot require a gas sparging system. Also, algae culture athigh pH would prevent invading and undesirable speciesfrom contaminating the designated culture systems.

Using bicarbonate and a high pH environment mightlead to less CO2 loss during the algae or cyanobacteriaculture process. The concentration of dissolved CO2 con-centration can be expressed as a function of dissolved Ciconcentration and H+ concentration [22] (Equation 1):

½CO2� ¼ Ci=ð1 þ K1=½Hþ� þ K1K2=½Hþ�2Þ (1)

Furthermore, the rate of CO2 outgassing through anair–water surface to the atmosphere can be calculatedusing Equation 2:

dC=dt ¼ KL að½CO2� � C�Þ (2)

where KL is the transfer coefficient in m/s, a is thespecific area to volume ratio in m2/m3 and C* is the dis-solved CO2 concentration in equilibrium with the atmo-sphere.

With assumed conditions, the [CO2] and outgassingrates are calculated and shown in Table 2. For example,even if 1.0 M bicarbonate is used in the assumed process,the lower CO2 concentration in the high pH environmentwould lead to a slower CO2 loss rate than from the tradi-tional algae pond (Table 2), which is usually maintained atpH 7.5–8.5 [23]*. Also, when the [CO2] is even lower athigher pH, its solution might absorb CO2 from the atmo-sphere (Table 2).

Alkaliphilic algae and cyanobacteria in natural sodalakesAlthough it appears promising, the challenge for such aculture system is to screen for strains of algae or cyano-bacteria that can grow in a high bicarbonate concentrationenvironment. To grow in such an environment, the algae orcyanobacteria must overcome the high pH and high ionstrength.

Fortunately, the same conditions occur naturally inmany soda lakes. Zavarzin et al. summarized the param-eters of some soda lakes, and showed that their pH rangesfrom 8.4 to 10.8, and the CO3

2– concentration from 0.3 to90.2 g/L (1.5 M) [24–27]. Even in this extreme environ-ment, blooms of cyanobacteria can occur, and their biomass

539

Table 2. Calculated CO2 concentrations and outgassing rates in open ponds under assumed conditions

Condition Cia (M) pH [CO2]a (mM) Rate of CO2

outgassing b (mol�L–1�s–1)

Equilibrium with 10% CO2

in flue gas at pH 7.5

0.131 7.5 2.839 9.39c � 10–9

8.0 0.845 2.77 � 10–9

8.5 0.218 6.89 � 10–10

20 mM Ci maintained 0.020 7.5 0.432 1.40 � 10–9

8.0 0.129 3.93 � 10–10

8.5 0.033 7.59 � 10–11

5 mM Ci maintained 0.005 7.5 0.108 3.25 � 10–10

8.0 0.032 7.25 � 10–11

8.5 0.008 –6.92 � 10–12

1.0 M bicarbonate in

envisioned process

1.000 9.5 0.048 1.24 � 10–10

10.0 0.006 –1.60 � 10–11

10.5 0.001 –3.26 � 10–11

aSeawater with salinity S = 35, and T = 25 8C; pK1 = 5.86, pK2 = 8.92.

bKL = 1 � 10–6 m/s; pond depth = 0.3m.

cNegative value indicates absorption of CO2 from the atmosphere to water.

Opinion Trends in Biotechnology November 2011, Vol. 29, No. 11

productivity can reach 10 g C/m2/day [25]. If the carboncontent in the produced algal biomass is 50%, the drybiomass productivity would be approximately 20 g/m2/day, which is at the same level as an artificial open-pondalgae culture system designed for biofuel production [28].Our unpublished preliminary research on alkaliphilic cya-nobacteria culture within the pH range 9.5 to 10.5 resultedin a biomass productivity of 0.1 g/L/day, which is similar tothe growth rate of other common microalgae, reported to be0.117 g/L/day [12]. Further efforts to optimize culture con-ditions should improve this productivity.

These halophilic and alkaliphilic cyanobacteria strainscan be isolated and used in the integrated culture systemproposed in Figure 2. It has been reported that benthiccyanobacteria isolated from Lake Magadi, Kenya includeSynechocystis salina, Aphanothece stagnina, Chamaesi-phon subglobosus, Rhabdoderma lineare, Synechococcuselongates, Phormidium ambiguum, Phormidium foveo-larum, Phormidium retzii, Oscillatoria splendid, Sscilla-toria limnetica, Spirulina fusiformis and Spirulinalaxissima. All these strains are extreme akaliphiles, grow-ing optimally at pH 9.9–10.4. Among these strains, P.ambiguum grew optimally at pH 9.9, 105 g/L sodium car-bonate, with a total mineral salts concentration of 165 g/L,whereas Phormidium orientale isolated from Lake Tuva,Russia grew optimally at pH 10.3 and 100 g/L sodiumcarbonate, with a total mineral salts concentration of145 g/L [25]. Additionally, Microcoleus sp. was found tobe the predominate species in the cyanobacteria mat grow-ing at pH 9.5 in Lake Khilganta, Russia. In addition tothese examples, eukaryotic green algae growing at pH 10.2and a sodium carbonate concentration of 200–260 g/L havealso been isolated from Lake Magadi [25].

Concluding remarksAlthough previous research has provided positive results,such as the ability of microalgae and cyanobacteria tosurvive in extremely harsh conditions, more research mustbe conducted to prove the feasibility of this proposedprocess and turn it into reality. Ideal strains of microalgaeor cyanobacteria need to be screened and used in theintegrated process described above. To be selected, these

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strains must grow fast in these extreme conditions, so thatthis process would be rapid enough to use the captured CO2

as required. Strains obtained from soda lakes containinghigh pH and high salt concentrations, as cited above, areideal starting points for this screening process. Using theselected strains, the productivity and yield of algal biomassfrom consumed bicarbonate can be investigated. Cultureconditions, such as light intensity, temperature, salinityand culture media compositions will need to be optimizedto result in maximum productivity. Based on this informa-tion, technical and economical assessments of this processcan then be made.

Transport systems for high concentration bicarbonatemust also be studied as previously related research hasfocused on CCM; that is, on bicarbonate transport under Cilimited conditions [18]. Cyanobacteria exhibited a basaland low transporter affinity form of the CCM when grownat a high level of exogenous Ci [18]. A study of transportsystems for the natronophilic cyanobacterium Euhalothecespp. grown on a high concentration of HCO3

– (1.0 M) andpH 10.0 indicated that the substrate affinity of its twotransport systems were several orders of magnitude lowerthan that of freshwater cyanobacteria [29]. This seemsreasonable given that if the concentration of intracellularbicarbonate is too high it will be harmful, or even fatal.These transport systems need to be investigated further toreveal the mechanism of bicarbonate transport in thesehalophilic and alkaliphilic cyanobacteria, and how it pro-vides a sufficient and well-regulated supply of Ci for pho-tosynthesis.

High alkalinity and high salinity also affect the growthof cyanobacteria in other aspects. For example, high salin-ity leads to inhibition of photosynthesis in most plants, butenhances the photosynthetic activity in the halophiliceukaryotic microalgae Dunaliella [30]. It has also beenreported that transition from pH 7.5 to pH 10.0 alteredthe CO2:HCO3

– ratio in cells of cyanobacteria Synechocys-tis PCC 6803, and three inducible bicarbonate transporters(BCT1, SbtA and NDH-1S) were upregulated. This transi-tion affected photosynthesis and resulted in increasedtranscripts of photosystem II genes [31]. It would beimportant to investigate the corresponding response of

Opinion Trends in Biotechnology November 2011, Vol. 29, No. 11

photosynthesis to high alkalinity and high salinity condi-tions for the screened cyanobacteria, as well as its primarymetabolism, such as synthesis of amino acids, carbohy-drates and fatty acids. This research will result in a betterunderstanding of cell growth in such extreme environ-ments, and provide potential solutions for CO2 captureand enhancement of biomass productivity.

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