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High CO2 increases lipid and polyunsaturated fatty acid productivity of the marine diatom Skeletonema costatum in a two-stage model

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Abstract

Lipid and polyunsaturated fatty acids (PUFA) from microalgae can be used as biodiesel and health care products. How to enhance their productivity is crucial for successful commercial production. In this study, a two-stage model was used to stimulate the production of lipids and PUFA in a bloom-forming marine diatom Skeletonema costatum. Cells were cultured in ambient air (0.04% CO2) in the first stage and transferred to two high CO2 levels (5% and 10%) in the second stage. The medium CO2 level (5%) increased both specific growth rate and lipid content and hence almost doubled lipid productivity compared to 0.04% CO2 level. Although a 10% CO2 level induced the highest lipid content, it had negative effects on the specific growth rate and soluble carbohydrate synthesis, and the lipid productivity was not as high as 5% CO2. Neither CO2 level affected the cell size, chlorophyll a content, or soluble protein content. High CO2 levels also increased the synthesis of PUFA, e.g., eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA). Although high CO2 levels increased iodine value and decreased the cetane number of oil exacted from S. costatum, they fall in the range of the European standard, suggesting its suitability for biodiesels. These findings indicate that a two-stage model with high CO2 induction is an effective approach for the production of biodiesel and PUFA from S. costatum, which could be used in both biofuel and health care markets.

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Data availability

The raw data in the present study are available from the corresponding author on reasonable request.

References

  • Adeniyi OM, Azimov U, Burluka A (2018) Algae biofuel: current status and future applications. Renew Sustain Energy Rev 90:316–335

    Article  Google Scholar 

  • Aléman-Nava GS, Muylaert K, Bermudez SPC, Depraetere O, Rittmann B, Parra-Saldivar R, Vandamme D (2017) Two-stage cultivation of Nannochloropsis oculata for lipid production using reversible alkaline flocculation. Bioresour Technol 226:18–23

    Article  Google Scholar 

  • Boelen P, van Dijk R, Damsté JSS, Rijpstra WIC, Buma AGJ (2013) On the potential application of polar and temperate marine microalgae for EPA and DHA production. AMB Express 3:26

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Brennan L, Owende P (2010) Biofuels from microalgae-a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sustain Energy Rev 14:557–577

    Article  CAS  Google Scholar 

  • Deriaz R (1961) Routine analysis of carbohydrates and lignin in herbage. J Sci Food Ag 12:152–160

    Article  CAS  Google Scholar 

  • Dickinson S, Mientus M, Frey D, Amini-Hajibashi A, Ozturk S, Shaikh F, Sengupta D, El-Halwagi MM (2017) A review of biodiesel production from microalgae. Clean Technol Envir 19:637–668

    Article  CAS  Google Scholar 

  • Francisco EC, Neves DB, Jacob-Lopes E, Franco TT (2010) Microalgae as feedstock for biodiesel production: carbon dioxide sequestration, lipid production and biofuel quality. J Chem Technol Biot 85:395–403

    Article  CAS  Google Scholar 

  • Gao G, Gao KS, Giordano M (2009) Responses to solar UV radiation of the diatom Skeletonema costatum(Bacillariophyceae) grown at different Zn2+concentrations. J Phycol 45:119–129

    Article  CAS  Google Scholar 

  • Gao G, Clare AS, Rose C, Caldwell GS (2017) Eutrophication and warming-driven green tides (Ulva rigida) are predicted to increase under future climate change scenarios. Mar Pollut Bull 114:439–447

    Article  CAS  Google Scholar 

  • Gao G, Beardall J, Bao M, Wang C, Ren WW, Xu JT (2018a) Ocean acidification and nutrient limitation synergistically reduce growth and photosynthetic performances of a green tide alga Ulva linza. Biogeosciences 15:3409–3420

    Article  CAS  Google Scholar 

  • Gao G, Clare AS, Chatzidimitriou E, Rose C, Caldwell G (2018b) Effects of ocean warming and acidification, combined with nutrient enrichment, on chemical composition and functional properties of Ulva rigida. Food Chem 258:71–78

    Article  CAS  Google Scholar 

  • Gao G, Xia J, Yu J, Zeng XP (2018c) Physiological response of a red tide alga (Skeletonema costatum) to nitrate enrichment, with special reference to inorganic carbon acquisition. Mar Environ Res 133:15–23

    Article  CAS  Google Scholar 

  • Gao G, Wu M, Fu Q, Li XS, Xu JT (2019a) A two-stage model with nitrogen and silicon limitation enhances lipid productivity and biodiesel features of the marine bloom-forming diatom Skeletonema costatum. Bioresour Technol 289:121717

    Article  CAS  Google Scholar 

  • Gao G, Fu Q, Beardall J, Wu M, Xu J (2019b) Combination of ocean acidification and warming enhances the competitive advantage of Skeletonema costatum over a green tide alga Ulva linza. Harmful Algae 85:101698

    Article  CAS  PubMed  Google Scholar 

  • Gao G, Liu W, Zhao X, Gao K (2021) Ultraviolet radiation stimulates activity of CO2 concentrating mechanisms in a bloom-forming diatom under reduced CO2 availability. Front Microbiol 12:590

    Google Scholar 

  • Gao G, Liu Y, Li X, Feng ZH, Xu JT (2016) An ocean acidification acclimatised green tide alga is robust to changes of seawater carbon chemistry but vulnerable to light stress. PLoS One 11(12):e0169040

  • Gao G, Burgess JG, Wu M, Wang SJ, Gao KS (2020) Using macroalgae as biofuel: current opportunities and challenges. Bot Mar 63:355–370

  • Gordillo FJL, Goutx M, Figueroa FL, Niell FX (1998) Effects of light intensity, CO2 and nitrogen supply on lipid class composition of Dunaliella viridis. J Appl Phycol 10:135–144

    Article  CAS  Google Scholar 

  • Griffiths MJ, Harrison ST (2009) Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J Appl Phycol 21:493–507

    Article  CAS  Google Scholar 

  • Gu N, Lin Q, Li G, Tan YH, Huang LM, Lin JD (2012) Effect of salinity on growth, biochemical composition, and lipid productivity of Nannochloropsis oculata CS 179. Eng Life Sci 12:631–637

    Article  CAS  Google Scholar 

  • Hopkinson BM, Dupont CL, Allen AE, Morel FMM (2011) Efficiency of the CO2-concentrating mechanism of diatoms. Proc Nat Acad Sci USA 108:3830–3837

    Article  CAS  Google Scholar 

  • Hu S, Wang Y, Wang Y, Zhao Y, Zhang XX, Zhang YS, Jiang M, Tang XX (2018) Effects of elevated pCO2 on physiological performance of marine microalgae Dunaliella salina (Chlorophyta, Chlorophyceae. J Oceanol Limnol 36:317–328

    Article  CAS  Google Scholar 

  • Jaiswal KK, Banerjee I, Singh D, Sajwan P, Chhetri V (2020) Ecological stress stimulus to improve microalgae biofuel generation: a review. Octa J Biosci 8:48–54

    CAS  Google Scholar 

  • Jiang X, Han Q, Gao X, Gao G (2016) Conditions optimising on the yield of biomass, total lipid, and valuable fatty acids in two strains of Skeletonema menzelii. Food Chem 194:723–732

    Article  CAS  Google Scholar 

  • Lei X, Jiang L, Zhang Y, Zhou GW, Lian JS, Lian JS (2020) Response of coralline algae Porolithon onkodes to elevated seawater temperature and reduced pH. Acta Oceanol Sin 39:132–137

    Article  CAS  Google Scholar 

  • Levitan O, Dinamarca J, Hochman G, Falkowski PG (2014) Diatoms: a fossil fuel of the future. Trends Biotechnol 32:117–124

    Article  CAS  Google Scholar 

  • Li FT, Beardall J, Collins S, Gao KS (2017) Decreased photosynthesis and growth with reduced respiration in the model diatom Phaeodactylum tricornutum grown under elevated CO2 over 1800 generations. Global Change Biol 23:17–137

    Google Scholar 

  • Mercado JM, Javier F, Gordillo L, Niell FX, Figueroa FL (1999) Effects of different levels of CO2 on photosynthesis and cell components of the red alga Porphyra leucosticta. J Appl Phycol 11:455–461

    Article  Google Scholar 

  • Nayak M, Suh WI, Chang YK, Lee B (2019) Exploration of two-stage cultivation strategies using nitrogen starvation to maximize the lipid productivity in Chlorella sp. HS2. Bioresource Technol 276:110–118

    Article  CAS  Google Scholar 

  • Olofsson M, Lindehoff E, Frick B, Svensson F, Legrand C (2015) Baltic Sea microalgae transform cement flue gas into valuable biomass. Algal Res 11:227–233

    Article  Google Scholar 

  • Peng L, Fu D, Chu H, Wang ZZ, Qi HY (2020) Biofuel production from microalgae: a review. Environ Chem Lett 18:285–297

    Article  CAS  Google Scholar 

  • Reid WV, Ali MK, Field CB (2020) The future of bioenergy. Global Change Biol 26:274–286

    Article  Google Scholar 

  • Rodolfi L, Chini Zittelli G, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2009) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102:100–112

    Article  CAS  Google Scholar 

  • Saini RK, Keum YS (2018) Omega-3 and omega-6 polyunsaturated fatty acids: dietary sources, metabolism, and significance-a review. Life Sci 203:255–267

    Article  CAS  Google Scholar 

  • Sibi G, Shetty V, Mokashi K (2016) Enhanced lipid productivity approaches in microalgae as an alternate for fossil fuels–a review. J Energy Inst 89:330–334

    Article  CAS  Google Scholar 

  • Singh SP, Singh P (2014) Effect of CO2 concentration on algal growth: a review. Renew Sustain Energy Rev 38:172–179

    Article  CAS  Google Scholar 

  • Su CH, Chien LJ, Gomes J, Lin YS, Yu YK, Liou JS, Syu RJ (2011) Factors affecting lipid accumulation by Nannochloropsis oculata in a two-stage cultivation process. J Appl Phycol 23:903–908

    Article  CAS  Google Scholar 

  • Subhadra B, Edwards M (2010) An integrated renewable energy park approach for algal biofuel production in United States. Energy Policy 38:4897–4902

    Article  CAS  Google Scholar 

  • Tang D, Han W, Li P, Miao XL, Zhong JJ (2011) CO2 biofixation and fatty acid composition of Scenedesmus obliquus and Chlorella pyrenoidosa in response to different CO2 levels. Bioresour Technol 102:3071–3076

    Article  CAS  Google Scholar 

  • Vargas MA, Rodriguez H, Moreno J, Olivares H, Del Campo JA, Rivas J, Guerrero MG (1998) Biochemical composition and fatty acid content of filamentous nitrogen-fixing cyanobacteria. J Phycol 34:812–817

    Article  CAS  Google Scholar 

  • Xu Z, Gao G, Xu J, Wu HY (2017) Physiological response of a golden tide alga (Sargassum muticum) to the interaction of ocean acidification and phosphorus enrichment. Biogeosciences 14:671–681

    Article  CAS  Google Scholar 

  • Zheng S, Chen S, Zou S, Yan YW, Gao G, He ML, Wang CH, Chen H, Wang Q (2021) Bioremediation of Pyropia-processing wastewater coupled with lipid production using Chlorella sp. Bioresource Technol 321:124428

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2018YFD0900703), the National Natural Science Foundation of China (42076154), the Fundamental Research Funds for the Central Universities (20720200111), and the MEL Internal Research Program (MELRI2004).

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Author notes

  1. Min Wu and Guang Gao contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Marine Environmental Science & College of Ocean and Earth Sciences, Xiamen University, Xiamen, 361005, China

    Min Wu, Guang Gao & Youwen Jian

  2. Jiangsu Key Laboratory of Marine Biotechnology, Jiangsu Ocean University, Lianyungang, 222005, China

    Min Wu & Juntian Xu

  3. Jiangsu Key Laboratory of Marine Bioresources and Environment, Jiangsu Ocean University, Lianyungang, 222005, China

    Juntian Xu

  4. Co-Innovation Center of Jiangsu Marine Bio-Industry Technology, Jiangsu Ocean University, Lianyungang, 222005, China

    Juntian Xu

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  1. Min Wu
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  2. Guang Gao
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  4. Juntian Xu
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Correspondence to Guang Gao.

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Wu, M., Gao, G., Jian, Y. et al. High CO2 increases lipid and polyunsaturated fatty acid productivity of the marine diatom Skeletonema costatum in a two-stage model. J Appl Phycol 34, 43–50 (2022). https://doi.org/10.1007/s10811-021-02619-5

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  • DOI: https://doi.org/10.1007/s10811-021-02619-5

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