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Lipid accumulation and CO2 utilization of two marine oil-rich microalgal strains in response to CO2 aeration
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Shuai WANG1, Li ZHENG1, 2, *, Xiaotian HAN3, Baijuan YANG1, Jingxi LI1, Chengjun SUN1
Acta Oceanologica Sinica | 2018, 37(2) : 119 - 126
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Acta Oceanologica Sinica | 2018, 37(2): 119-126
• Marine Biology •
Lipid accumulation and CO2 utilization of two marine oil-rich microalgal strains in response to CO2 aeration
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Shuai WANG1, Li ZHENG1, 2, *, Xiaotian HAN3, Baijuan YANG1, Jingxi LI1, Chengjun SUN1
Affiliations
  • 1 Key Laboratory for Marine Bioactive Substances and Modern Analytical Technology, the First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China
  • 2 Laboratory of Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
  • 3 Key Laboratory of Marine Ecology and Environmental Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
Published: 2018-02-25 doi: 10.1007/s13131-018-1171-y
Outline
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Biological CO2 sequestration by microalgae is a promising and environmentally friendly technology applied to sequester CO2. The characteristics of neutral lipid accumulation by two marine oil-rich microalgal strains, namely, Isochrysis galbana and Nannochloropsis sp., through CO2 enrichment cultivation were investigated in this study. The optimum culture conditions of the two microalgal strains are 10% CO2 and f medium. The maximum biomass productivity, total lipid content, maximum lipid productivity, carbon content, and CO2 fixation ability of the two microalgal strains were obtained. The corresponding parameters of the two strains were as follows: ((142.42±4.58) g/(m2·d), (149.92±1.80) g/(m2·d)), ((39.95±0.77)%, (37.91±0.58)%), ((84.47±1.56) g/(m2·d), (89.90±1.98) g/(m2·d)), ((45.98±1.75)%, (46.88±2.01)%), and ((33.74±1.65) g/(m2·d), (34.08±1.32) g/(m2·d)). Results indicated that the two marine microalgal strains with high CO2 fixation ability are potential strains for marine biodiesel development coupled with CO2 emission reduction.

Isochrysis galbana  /  Nannochloropsis sp.  /  CO2 enrichment cultivation  /  neutral lipid  /  biodiesel  /  open raceway pond
Shuai WANG, Li ZHENG, Xiaotian HAN, Baijuan YANG, Jingxi LI, Chengjun SUN. Lipid accumulation and CO2 utilization of two marine oil-rich microalgal strains in response to CO2 aeration[J]. Acta Oceanologica Sinica, 2018 , 37 (2) : 119 -126 . DOI: 10.1007/s13131-018-1171-y
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1 Introduction
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The CO2 concentration in the atmosphere continuously increases; as a consequence, this increase significantly affects the global environment. Extensive CO2 emissions from anthropogenic activities cause global warming (Ramanan et al., 2010). These emissions can be reduced through biological CO2 sequestration by using photosynthetic microalgae because these organisms unlikely compete with food crops for arable land and fresh water resources (Kumar et al., 2010). Cultivated microalgae not only exhibit high CO2 fixation ability but also produce significant amounts of renewable biomass for biofuels. These organisms also yield value-added products from biomass, such as proteins, fatty acids, and dietary supplements for humans, animals and fish (Pulz and Gross, 2004).
Studies on carbon sequestration based on microalgae, specifically the CO2 tolerance of microalgae, have achieved certain progress. However, research objects mostly include freshwater algae, such as Scenedesmus sp., Spirulina platensis, and Chlorella sp., and the CO2 tolerance of these algae ranges from 5% to 40% (Yang et al., 2011). Present research on carbon sequestration of marine microalgae is mainly concentrated on several species, such as Nannochloropsis sp., Dunaliella salina, Chlorella sp., and Phaeodactylum tricornulum (Salih, 2011). Results show that the growth rate and biomass accumulation are inhibited to a certain degree when the CO2 concentration exceeds 5% (Lee and Tay, 1991), and the CO2 emission concentration of power plants is approximately 10% (Bai et al., 2006). Therefore, carbon emission reduction based on marine microalgae must withstand 10% of CO2. Meanwhile, research on lipid accumulation of these microalgae under carbon-rich conditions, especially the accumulation of neutral lipid, is rarely undertaken.
Biodiesel is formed by the fatty acid methyl esthers derived from a transesterification reaction between triglycerides and methanol (Chisti, 2008). Neutral lipids or triglycerides, which are mainly found as storage lipids in microalgae, are essential for biodiesel production (Wang et al., 2010). The chemical and physical qualities of biodiesel are closely related to the properties of its parent oil. Therefore, the feasibility of microalgal species as a biodiesel feedstock depends on the optimization of its biomass and neutral lipid content. To enhance the novel feedstock, researchers should select suitable strains and CO2 concentration for mass scale cultivation. Adverse environmental effects of high CO2 emissions can be reduced by using biofuels. Biodiesel can be produced from microalgae in a small scale. However, large-scale biodiesel production by microalgae remains economically unviable (Liu et al., 2006; Xu et al., 2011). However, the characteristics of neutral lipid accumulation under CO2-enriched cultivation in covered raceway ponds have yet to be reported. Therefore, microalgal cultivation under CO2-enriched conditions in covered raceway ponds must be improved.
Two marine oil-rich microalgal strains, namely, Isochrysis galbana CCMM5001 and Nannochloropsis sp. CCMM7001, exhibit high environmental adaptability (Wei et al., 2015; Liu and Wang, 2014). The outdoor-cultured biomass of these microalgae can reach 26.4 g/(m2·d) (Liu et al., 2013) and 9.9 g/(m2·d) (Bondioli et al., 2012), respectively. The lipid content of these marine microalgae is also high. Their lipid content is 7.0%–40.0% (Mata et al., 2010) and 22.7%–52.0% (Bondioli et al., 2012; Moazami et al., 2012). The two microalgal strains can strongly tolerate CO2 (>15%, v/v) (Chiu et al., 2009). The CO2 concentrations of the two microalgal strains in industrial flue gases from power plants usually range from 10% to 15%, and these concentrations may provide a carbon source for large-scale microalgal cultivation. Isochrysis galbana and Nannochloropsis sp. were selected from marine microalgal strains with high biomass and high lipid contents (neutral lipid and total lipid) in our preliminary experiment. Mass cultivation coupled with CO2 emission reduction was conducted in a covered raceway pond. This study provided a basis for CO2 sequestration and biodiesel technology.
2 Materials and methods
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2.1 Microalgal strains
Isochrysis galbana CCMM5001 and Nannochloropsis sp. CCMM7001 were provided by Han Xiaotian from the Institute of Oceanology, Chinese Academy of Science. These strains were maintained in f/2 medium at (20±1)°C with continuous illumination at 100 μmol/(m2·s).
2.2 The open raceway pond
The open raceway pond was 200 cm×30 cm×40 cm in dimension, the water surface height is 30 cm. The speed is 30 r/min (Moheimani and Borowitzka, 2007).
2.3 Culture conditions
The two marine microalgal strains were grown in a 100 L photobioreactor, and inoculated in the exponential phase with an initial cell concentration of 2.12×106 cells/mL in an open raceway pond in autumn of 2014 in Qingdao (35°35′–37°09′N; 119°30′–121°E). The culture temperature ranged from 10°C to 30°C, and illumination ranged from 447 µmol/(m2·s) to 1 081 µmol/(m2·s). Light intensity was measured at 12 o’clock. Seawater continuously bubbled with filtered air at the aeration rate of 0.1 vvm by flow counter for 12 h (6:00–18:00). The range of CO2 concentrations (0%, 0.04%, 10%, and 15%), nutrient concentrations (f/4 [0.5-fold f/2 medium], f/2, f [two-fold f/2 medium], and 2f [four-fold f/2 medium]) were set up and compared. This experiment was performed in triplicate. Sampling was conducted by transfer liquid gun and graduated flask at a fixed time every other day. The biomass was harvested at the plateau phase.
2.4 Dry weight and neutral lipid analysis
The tube was dried at 105°C for 24 h and weighed (DW0). After growth, the biomass was separated from the medium by centrifugation at 10 000 g for 10 min, then freeze dried (DW1)
Dry weight was calculated by the equation:
M=( D W 1 −D W 0 )/0.01,
where M is the dry algae biomass (g/L).
Neutral lipid was determined with Nile red method (Chen et al., 2009, 2011). Unit volume of fluorescence value (excitation wavelength 480 nm, emission wavelength 580 nm) was measured to characterize the change of neutral lipid accumulation.
Fluorescence value in single algal cell was calculated by the equation:
FI=( F NL −F )/Y,
where FI is fluorescence value in single algal cell, FNL is the total of fluorescence value, F is fluorescence value in the medium, and Y is cell concentration (Wang et al., 2010).
2.5 Biomass productivity, total lipid and lipid productivity analysis
The biomass productivity was calculated by the equation:
W=( m 2 − m 1 )/( t 2 − t 1 )×1 000×0.3,
where W is biomass productivity (g/(m2·d)), m is biomass dry weight (g/L) when the time is t, t is culture time (d).
Lipid productivity was calculated by the equation:
L=WP,
where L is lipid productivity (g/(m2·d)), W is biomass productivity (g/(m2·d)), P is the content of lipid (%) (Huerlimann et al., 2010; Tang et al., 2011).
2.6 Total lipid and fatty acids analysis
Microalgae were harvested at the late exponential growth phase by centrifugation at 10 000 g for 5 min. Total lipid was extracted and determined by the modified method (Huerlimann et al., 2010; Tang et al., 2011). Fatty acids were extracted and determined by the method (Yang et al., 2013).
2.7 Carbon content and CO2 fixation rate analysis
CO2 fixation rate was calculated by the equation:
F CO 2 = C C ×W×( M CO 2 / M C )/100,
where $ {{F}_{\rm{C}{{\rm{O}}_{2}}}} $ is CO2 fixation rate (g/(m2·d)), CC is carbon content (g/g), W is the average of biomass productivity (g/(m2·d)), $ {{F}_{\rm{C}{{\rm{O}}_{2}}}} $ is molecular weight of CO2 (44 g/mol), MC is molecular weight of carbon (12 g/mol) (Zhao et al., 2011).
2.8 Statistical analysis
All data were obtained by using at least three replicated biological samples. Experimental results were expressed as mean value±SD. Statistical analysis was performed using the SPSS11.5 statistical package. The statistical significance was achieved when p<0.05.
3 Results
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3.1 The pH changes and growth curve of the two marine microalgae
The pH value is shown in Fig. 1. The pH value of the culture medium with CO2 remains generally stable (acid condition pH 6.5). Under different concentrations of CO2, the pH values of the culture medium differ significantly. The concentration of CO2 is high, and the pH value is low. Under conditions without CO2 access, the pH value of the culture medium is higher than 7.0, and baseline drift occurs. The pH value of the culture medium will increase with culture time. Under the non-inflation condition, the pH values of the two strains of microalgae are kept at 9.5. Under conditions with or without CO2, the pH values of the two strains of microalgae retain stability in the plateau phase.
The growth curves of the two strains of microalgae under different culture conditions are shown in Fig. 2. Isochrysis galbana enters the exponential growth phase under different CO2 and nutrient concentrations on the 4th day and enters the plateau phase on the 10th day. Except for the low-nutrient concentration (f/4), the biomass of I. galbana exhibits no significant difference with the increase of the nutrient concentration. Nannochloropsis sp. enters the exponential growth phase under different concentrations of CO2 and nutrients on the 4th day and enters the plateau phase in the 12th day. The cell density of Nannochloropsis sp. increased with nutrient concentration. The highest biomass is (0.98 ± 0.02) g/L. With CO2 access, a significant increase in biomass is observed. Optimal growth of the two marine microalgae were detected under the 10% CO2 concentration ((0.71±0.08) g/L and (0.78±0.03) g/L).
3.2 The dynamics changes of the neutral lipid accumulation of the two marine microalgae
The dynamic changes of the neutral lipids in the two marine microalgae are shown in Fig. 3. With increased culture time, the fluorescence intensity of the neutral lipid of a single algal cell initially decreased then increased. Neutral lipid accumulates in the plateau phase. No significant difference in the content of neutral lipid of the two marine microalgae was observed under the different concentrations of CO2 in the plateau phase. However, under different nutrient concentrations, the fluorescence value of a single algal cell in I. galbana is f/4>f/2>f>2f. In particular, the fluorescence intensity of the neutral lipid of I. galbana can be as high as 490.00±4.60 in the case of f/4. With increased nutrient concentrations, the content of neutral lipid in Nannochloropsis sp. gradually decreases. After being accumulated in the plateau phase, the fluorescence intensity of the neutral lipid is f/4≈f/2>f>2f, the highest value of which is 322.00±20.60.
3.3 The dry weight and total lipid content of the two marine microalgae
The dry weight and total lipid content of the two marine microalgae are presented in Fig. 4. The biomass and total lipid content of the two marine microalgae significantly increased and reached the highest values ((0.71±0.08) g/L, (40.78±2.54)%) and ((0.78±0.03) g/L, (37.54±1.78)%) under the 10% CO2 concentration. Under different nutrient concentrations, the biomass and total lipid content of I. galbana in the f/4 treatment group were the lowest, and those of the f treatment group were the highest ((0.95±0.03) g/L and (39.95±0.77)%). The biomass and total lipid content of Nannochloropsis sp. were the highest ((0.98±0.01) g/L and (37.91±0.58)%) in the f treatment group. However, the total lipid content is the lowest ((24.85±1.63)%) in the 2f treatment group.
3.4 The carbon content, the maximum biomass productivity, the maximum lipid productivity and CO2 fixation rate of the two marine microalgae
Figure 5 shows the carbon contents, maximum biomass productivity, maximum lipid productivity, and CO2 fixation rate of the two marine microalgae. The optimum culture conditions of the two microalgal strains are 10% CO2 and f medium. The carbon content, maximum biomass productivity, maximum lipid productivity and CO2 fixation ability of the two microalgal strains were obtained. The corresponding parameters of the two strains were as follows: ((45.98±1.75)%, (46.88±2.01)%), ((142.42±4.58) g/(m2·d), (149.92±1.80) g/(m2·d)), ((84.47±1.56) g/(m2·d), (89.90±1.98) g/(m2·d)), and ((33.74±1.65) g/(m2·d), (34.08±1.32) g/(m2·d)).
3.5 The fatty acid compositions of the two marine microalgae
The fatty acid compositions of the two marine microalgae are shown in Tables 1 and 2. The fatty acid compositions of I. galbana are mainly C14:0, C16:0, C18:1, and C20:6. Under different concentrations of CO2, no significant changes in C20:6 and C14–C18 are observed. Their concentrations are maintained at 14% and 83%, respectively. The content of PUFAs will increase with the concentrations of CO2. With increased nutrient concentration, C14–C18 and SFAs of I. galbana gradually decreased and C20:6 and PUFAs significantly increase. The fatty acid compositions of Nannochloropsis sp. are mainly C16:0, C16:1, C18:1, and C20:5. The most important difference is that access to CO2 facilitates the accumulation of C20:5 and PUFAs and prevents the accumulation of C14–C18 (the main components of biodiesel). Under the low nutrient concentrations (f/4), Nannochloropsis sp. exhibits low content of C20:5 and PUFAs, and high contents of C14–C18, SFAs, and MUFAs.
4 Discussion
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The main carbon source of marine microalgae through the open culture is CO2. Different microalgae exhibit different resistances to CO2 (Wang et al., 2014; Salih, 2011). CO2 access will cause the pH of the algal solution to decrease. The pH will directly influence the solubility of CO2 and the dissolved oxygen concentration and consequently affect the carbon fixation of microalgae (Kumar et al., 2010). The results show that the increase of CO2 concentration facilitates the growth and lipid accumulation of Nannochloropsis sp. and I. galbana. However, if the concentration of CO2 is more than 10%, the growth indices of the two microalgae gradually decrease. The concentration of CO2 significantly affects the fatty acid composition of the two marine microalgae. However, compared with that of control group without CO2, the contents of EPA and PUFAs in I. galbana increased and that of C14–C18 (the main components of biodiesel) decreased. The results of Hu and Gao (2003, 2006) and Hoshida et al. (2005) are consistent with that of this work. The changes in EPA and PUFA contents may be attributed to the synthesis of polyunsaturated fatty acids in the microalgae, which starts from C16:0. Increasing the concentration of CO2 is equivalent to reducing the concentration of oxygen in the air, which will influence the activity of related desaturases. For the preparation of biodiesel by microalgae lipid, the increase in the contents of unsaturated fatty acids influences the combustion of biodiesel. Thus, CO2 emission reduction and the preparation of microalgae biodiesel using I. galbana can guarantee the quality of biodiesel.
Nutrients are one of the reasons why large-scale cultivation of marine microalgae is expensive. The dosage of nutrients influences the production of biodiesel. This factor also has a certain influence on the ecological environment resources (Fixen, 2007). Therefore, determining the appropriate dosage of nutrient is important. The sufficiency of the nutrients was associated with optimal algal growth and lipid accumulation. This is confirmed by the fact that the growth indices exhibit the highest values in the f culture medium, similar to the results of Wei et al. (2000a). Therefore, the f culture medium is more appropriate for the large-scale culture of the two microalgae. A low nutrient concentration restricts cell growth (Liu and Wang, 2014; Wang et al., 2006; Wei et al., 2000b), whereas a high nutrient concentration will result in an extremely high content of trace metal elements, thus inhibiting the growth of microalgae (Sun et al., 2005). Previous studies indicated that low nutrient concentration causes the accumulation of microalgae lipid but prevents the growth of microalgae. In particular, the content of PUFAs will increase with the concentration of nutrients. The opposite result was observed for MUFAs. The results of Huang et al. (2013) also verified this finding. In this study, the total lipid content and maximum lipid productivity are low under the f/4 culture medium probably because the concentrations of N and P are less than the growth concentration. The two microalgae rapidly undergo the decline phase. Enzyme activity associated with lipid synthesis in cells decreases or is partially inactivated. Moreover, lipid accumulation is blocked, thus reducing content (Yu et al., 2011).
The results from the Nile red method show that the neutral lipid content of the two marine oil-rich microalgae accumulates in the growth plateau phase. This finding is consistent with the results obtained by Wei et al. (2000b) and Wang et al. (2010). The plateau phase is the accumulation period of neutral lipid because the nitrogen sources required by synthetic amino acid in the culture medium decrease with protein synthesis after the cells enter the plateau phase. Moreover, energy accumulation occurs in carbohydrate and lipids synthesized by the carbon from photosynthetic assimilation (Li et al., 2013; Ma et al., 2012; Xu et al., 2012; Shi and Pan, 2004). Increasing the concentration of CO2 can provide rich carbon for the accumulation of carbohydrates and lipids. During the entire growth phase, the two marine microalgae initially decrease and then increase in neutral lipid because the initial microalgae are in the late stage of the logarithmic phase and the neutral lipid content of a single algal cell is high. When microalgae are cultured in the logarithmic phase, the ATP that microalgal cells split and consume in large amounts partly come from the neutral lipids (Zhu et al., 2011). Previous studies demonstrated that neutral lipid content does not increase in the logarithmic phase (Wang et al., 2014; Wei et al., 2000b), thereby causes the neutral lipid content to decrease because of its consumption in the logarithmic phase. To date, the dynamic metabolism of neutral lipids and the mechanism of the cell growth cycle remains to be clarified (Salih, 2011).
5 Conclusions
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Isochrysis galbana CCMM5001and Nannochloropsis sp. CCMM7001 can be potentially used as a renewable biodiesel feedstock that can reduce CO2 emission. The optimum culture conditions of the two marine oil-rich microalgae are 10% CO2 and f medium. At 10% CO2, the two microalgal strains accumulate neutral lipids of up to 490.00±4.60 (FI of single cell is 10–6) in single cells. Among the neutral lipids, triglycerides are the most abundant component. The maximum biomass productivity, total lipid content, lipid productivity, carbon content, and CO2 fixation ability of the two microalgal strains were obtained.
Funding
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  • The Basic Scientific Fund for National Public Research Institutes of China under contract Nos 2017Q09 and 2016Q02; the National Natural Science Foundation of China under contract No. 41776176; the National Key Research and Development Program of China under contract No. 2017YFC1404604; the Shandong Provincial Natural Science Foundation under contract No. ZR2015PD003; the 2012 Taishan Scholar.
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Article Info
doi: 10.1007/s13131-018-1171-y
  • Receive Date：2017-05-04
  • Online Date：2026-04-13
  • Published：2018-02-25
Article Data
Affiliations
History
  • Received：2017-05-04
  • Accepted：2017-06-09
Funding
The Basic Scientific Fund for National Public Research Institutes of China under contract Nos 2017Q09 and 2016Q02; the National Natural Science Foundation of China under contract No. 41776176; the National Key Research and Development Program of China under contract No. 2017YFC1404604; the Shandong Provincial Natural Science Foundation under contract No. ZR2015PD003; the 2012 Taishan Scholar.
Affiliations
    1 Key Laboratory for Marine Bioactive Substances and Modern Analytical Technology, the First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China
    2 Laboratory of Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
    3 Key Laboratory of Marine Ecology and Environmental Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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