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Glycerol changes the growth and lipid profile of the marine microalga Isochrysis galbana via the regulation of photosynthetic and respiratory metabolic pathways

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Abstract

Isochrysis galbana is widely used in the aquaculture industry and is a potential industrial biodiesel producer. The growth of I. galbana has been enhanced in mixotrophic conditions with glycerol supplementation. Nevertheless, the effect mechanism of glycerol on I. galbana remains unclear. This study aimed to reveal how glycerol supplementation (0.1% by volume fraction) altered the growth, photosynthesis, respiration, fatty acid profile and transcriptome of I. galbana. Glycerol was shown to favor the growth of I. galbana under light. The increase in oxygen uptake rate indicates that glycerol is involved in the respiratory carbon metabolism of I. galbana. Furthermore, the added glycerol downregulated the photosynthetic activity of the alga, with a decrease in light-harvesting pigments, i.e., chlorophyll c and carotenoids, and a decrease in photosynthetic electron transfer activity as indicators. In addition, the fatty acid profile of I. galbana was affected by the supplementation of glycerol with a pronounced increase in oleic acid to 36.47%. Meanwhile, the ratio of Σ(saturated fatty acids + monounsaturated fatty acids)/Σ(polyunsaturated fatty acids) in glycerol-treated samples (3.43) was significantly higher than that in control samples (2.13), indicating a better composition for biodiesel. Transcriptomic analysis further revealed the molecular mechanisms involved in the impacts of glycerol on I. galbana. DEGs enriched to photosynthesis, light harvesting, chlorophyll binding, and chloroplast thylakoid membrane were mainly downregulated, and the DEGs enriched in translation, nitrate transport, stearoyl-CoA 9-desaturase activity were mainly upregulated, consistent with the results of photosynthesis, biomass and the fatty acid profile. This study demonstrated the essential role of 0.1% glycerol in accelerating the growth and altering the fatty acid profiles of I. galbana, as well as the preliminary molecular mechanism underlying these physiological changes.

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The data that support the findings of this study are available on request from the corresponding author.

References

  • Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL et al (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol 66:4–119

    PubMed  PubMed Central  Google Scholar 

  • Agarwal A, Patil S, Gharat K, Pandit RA, Lali AM (2019) Modulation in light utilization by a microalga Asteracys sp. under mixotrophic growth regimes. Photosynth Res 139:553–567

  • Alkhamis Y, Qin JG (2013) Cultivation of Isochrysis galbana in phototrophic, heterotrophic, and mixotrophic conditions. Biomed Res Int 2013:983465

    PubMed  PubMed Central  Google Scholar 

  • Ariyarathna RAIS, Weerasena SL, Beneragama CK (2020) Application of polyphasic OJIP chlorophyll fluorescent transient analysis as an indicator for testing of seedling vigour of common bean (Phaseolus vulgaris L.). Trop Ag Res 31:106

  • Baldisserotto C, Popovich C, Giovanardi M, Sabia A, Ferroni L, Constenla D, Leonardi P, Pancaldi S (2016) Photosynthetic aspects and lipid profiles in the mixotrophic alga Neochloris oleoabundans as useful parameters for biodiesel production. Algal Res 16:255–265

    Google Scholar 

  • Ballottari M, Girardon J, Dall'Osto L, Bassi R (2012) Evolution and functional properties of Photosystem II light harvesting complexes in eukaryotes. Biochim Biophys Acta - Bioenergetics 1817:143-157

  • Bonfanti C, Cardoso C, Afonso C, Matos J, Garcia T, Tanni S, Bandarra NM (2018) Potential of microalga Isochrysis galbana: bioactivity and bioaccessibility. Algal Res 29:242–248

    Google Scholar 

  • Che CA, Kim SH, Hong HJ, Kityo MK, Sunwoo IY, Jeong GT, Kim SK (2019) Optimization of light intensity and photoperiod for Isochrysis galbana culture to improve the biomass and lipid production using 14-L photobioreactors with mixed light emitting diodes (LEDs) wavelength under two-phase culture system. Bioresour Technol 285:121323

    CAS  PubMed  Google Scholar 

  • Chen H, Fu Q, Jiang P, Wu C (2022) Mitigation of photoinhibition in Isochrysis galbana by the construction of microalgal-bacterial consortia. J Appl Phycol 34:2883–2894

    CAS  Google Scholar 

  • Chew KW, Chia SR, Show PL, Yap YJ, Ling TC, Chang JS (2018) Effects of water culture medium, cultivation systems and growth modes for microalgae cultivation: A review. J Taiwan Inst Chem Eng 91:332–344

  • Danesh A, Zilouei H, Farhadian O (2019) The effect of glycerol and carbonate on the growth and lipid production of Isochrysis galbana under different cultivation modes. J Appl Phycol 31:3411–3420

    CAS  Google Scholar 

  • Daneshvar E, Sik Ok Y, Tavakoli S, Sarkar B, Shaheen SM, Hong H, Luo Y, Rinklebe J, Song H, Bhatnagar A (2021) Insights into upstream processing of microalgae: A review. Bioresour Technol 329:124870

  • De Morais EG, Druzian JI, Nunes IL, De Morais MG, Vieira Costa JA (2019) Glycerol increases growth, protein production and alters the fatty acids profile of Spirulina (Arthrospira) sp LEB 18. Process Biochem 76:40–45

  • Dragone G (2022) Challenges and opportunities to increase economic feasibility and sustainability of mixotrophic cultivation of green microalgae of the genus Chlorella. Renew Sust Energy Rev 160:112284

  • Eastmond PJ (2004) Glycerol-insensitive Arabidopsis mutants: gli1 seedlings lack glycerol kinase, accumulate glycerol and are more resistant to abiotic stress. Plant J 37:617–625

    CAS  PubMed  Google Scholar 

  • Eisele R, Ullrich WR (1977) Effect of glucose and CO2 on nitrate uptake and coupled OH- flux in Ankistrodesmus braunii. Plant Physiol 59:18–21

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flowers MT, Ntambi JM (2008) Role of stearoyl-coenzyme A desaturase in regulating lipid metabolism. Curr Opin Lipidol 19:248–256

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao P, Guo L, Gao M, Zhao Y, Jin C, She Z (2022) Regulation of carbon source metabolism in mixotrophic microalgae cultivation in response to light intensity variation. J Environ Manage 302:114095

  • Gladue RM, Maxey JE (1994) Microalgal feeds for aquaculture. J Appl Phycol 6:131–141

    Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 29–60

    Google Scholar 

  • Gupta PL, Choi HJ, Lee SM (2016) Enhanced nutrient removal from municipal wastewater assisted by mixotrophic microalgal cultivation using glycerol. Environ Sci Pollut Res Int 23:10114–10123

    CAS  PubMed  Google Scholar 

  • Hellebust JA, Craigie JS (eds) (1978) Handbook of phycological methods: Physiological and biochemical methods. Cambridge University Press, Cambridge

    Google Scholar 

  • Hu H, Ma LL, Shen XF, Li JY, Wang HF, Zeng RJ (2018) Effect of cultivation mode on the production of docosahexaenoic acid by Tisochrysis lutea. AMB Express 8:50

    PubMed  PubMed Central  Google Scholar 

  • Joun J, Sirohi R, Sim SJ (2023) The effects of acetate and glucose on carbon fixation and carbon utilization in mixotrophy of Haematococcus pluvialis. Bioresour Technol 367:128218

    CAS  PubMed  Google Scholar 

  • Kindle KL (1987) Expression of a gene for a light-harvesting chlorophyll a/b-binding protein in Chlamydomonas reinhardtii: effect of light and acetate. Plant Mol Biol 9:547–563

    CAS  PubMed  Google Scholar 

  • Knothe G (2008) “Designer” biodiesel: Optimizing fatty ester composition to improve fuel properties. Energy Fuels 22:1358–1364

    CAS  Google Scholar 

  • Koyande AK, Chew KW, Rambabu K, Tao Y, Chu D-T, Show P-L (2019a) Microalgae: A potential alternative to health supplementation for humans. Food Sci Human Wellness 8:16–24

    Google Scholar 

  • Koyande AK, Show PL, Guo R, Tang B, Ogino C, Chang JS (2019b) Bio-processing of algal bio-refinery: a review on current advances and future perspectives. Bioengineered 10:574–592

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kroymann J, Schneider W, Zetsche K (1995) Opposite regulation of the copy number and the expression of plastid and mitochondrial genes by light and acetate in the green flagellate Chlorogonium. Plant Physiol 108:1641–1646

    PubMed  PubMed Central  Google Scholar 

  • Lari Z, Abrishamchi P, Ahmadzadeh H, Soltani N (2019) Differential carbon partitioning and fatty acid composition in mixotrophic and autotrophic cultures of a new marine isolate Tetraselmis sp. KY114885. J Appl Phycol 31:201–210

  • Lv J, Zhao F, Feng J, Liu Q, Nan F, Liu X, Xie S (2019) Transcriptomic analysis reveals the mechanism on the response of Chlorococcum sp. GD to glucose concentration in mixotrophic cultivation. Bioresour Technol 288:121568

  • Mandal MK, Chanda B, Xia Y, Yu K, Sekine KT, Gao QM, Selote D, Kachroo A, Kachroo P (2011) Glycerol-3-phosphate and systemic immunity. Plant Signal Behav 6:1871–1874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Markou G, Kougia E, Kefalogianni I, Tsagou V, Arapoglou D, Chatzipavlidis I (2019) Effect of glycerol concentration and light intensity on growth and biochemical composition of Arthrospira (Spirulina) Platensis: A study in semi-continuous mode with non-aseptic conditions. Appl Sci 9:4703

    CAS  Google Scholar 

  • Matos J, Cardoso C, Gomes A, Campos AM, Falé P, Afonso C, Bandarra NM (2019) Bioprospection of Isochrysis galbana and its potential as a nutraceutical. Food Funct 10:7333–7342

    CAS  PubMed  Google Scholar 

  • Neilson AH, Lewin RA (1974) The uptake and utilization of organic carbon by algae: An essay in comparative biochemistry. Phycologia 13:227–264

    CAS  Google Scholar 

  • Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ok JH, Jeong HJ, Lim AS, You JH, Kang HC, Kim SJ, Lee SY (2019) Effects of light and temperature on the growth of Takayama helix (Dinophyceae): Mixotrophy as a survival strategy against photoinhibition. J Appl Phycol 55:1181–1195

    CAS  Google Scholar 

  • Patel AK, Joun JM, Hong ME, Sim SJ (2019) Effect of light conditions on mixotrophic cultivation of green microalgae. Bioresour Technol 282:245–253

    CAS  PubMed  Google Scholar 

  • Penhaul Smith JK, Hughes AD, McEvoy L, Day JG (2023) Use of crude glycerol for mixotrophic culture of Phaeodactylum tricornutum. Algal Res 69:102929

    Google Scholar 

  • Poddar N, Sen R, Martin GJO (2018) Glycerol and nitrate utilisation by marine microalgae Nannochloropsis salina and Chlorella sp. and associated bacteria during mixotrophic and heterotrophic growth. Algal Res 33:298–309

    Google Scholar 

  • Poddar N, Sen R, Martin GJO (2020) Bacterial abundance and diversity in Microchloropsis salina (formerly Nannochloropsis salina) cultures in response to the presence of ammonium, nitrate and glycerol. J Appl Phycol 32:839–850

    CAS  Google Scholar 

  • Rahimi M, Jazini M (2021) Mixotrophic cultivation of Chromochloris zofingiensis on glycerol, acetate, and vinasse. J Appl Phycol 33:3579–3590

    CAS  Google Scholar 

  • Rai MP, Nigam S, Sharma R (2013) Response of growth and fatty acid compositions of Chlorella pyrenoidosa under mixotrophic cultivation with acetate and glycerol for bioenergy application. Biomass Bioenergy 58:251–257

    CAS  Google Scholar 

  • Ramanna L, Rawat I, Bux F (2017) Light enhancement strategies improve microalgal biomass productivity. Renew Sustain Energy Rev 80:765–773

  • Rana M, Prajapati SK (2021) Stimulating effects of glycerol on the growth, phycoremediation and biofuel potential of Chlorella pyrenoidosa cultivated in wastewater. Environ Technol Innov 24:102082

    CAS  Google Scholar 

  • Ritchie RJ (2008) Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46:115–126

    CAS  Google Scholar 

  • Shah S, Ahmad A, Othman MHD, Abdullah MA (2014) Enhancement of lipid content in Isochrysis Galbana and Pavlova Lutheri using palm oil mill effluent as an alternative medium. Chem Eng Trans 37:733–738

    Google Scholar 

  • Shen W, Wei Y, Dauk M, Zheng Z, Zou J (2003) Identification of a mitochondrial glycerol-3-phosphate dehydrogenase from Arabidopsis thaliana: evidence for a mitochondrial glycerol-3-phosphate shuttle in plants. FEBS Lett 536:92–96

    CAS  PubMed  Google Scholar 

  • Tham PE, Lim HR, Khoo KS, Chew KW, Yap YJ, Munawaroh HSH, Ma Z, Rajendran S, Gnanasekaran L, Show PL (2023) Insights of microalgae-based aquaculture feed: A review on circular bioeconomy and perspectives. Algal Res 74:103186

    Google Scholar 

  • Wang B, Pan X, Wang F, Liu L, Jia J (2022) Photoprotective carbon redistribution in mixotrophic Haematococcus pluvialis under high light stress. Bioresour Technol 362:127761

    CAS  PubMed  Google Scholar 

  • Wang P, Grimm B (2021) Connecting chlorophyll metabolism with accumulation of the photosynthetic apparatus. Trends Plant Sci 26:484–495

    PubMed  Google Scholar 

  • Xu S, Elsayed M, Ismail GA, Li C, Wang S, Abomohra AE-F (2019) Evaluation of bioethanol and biodiesel production from Scenedesmus obliquus grown in biodiesel waste glycerol: A sequential integrated route for enhanced energy recovery. Energy Convers Manag 197:111907

    CAS  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: Accounting for selection bias. Genome Biol 11:R14

    PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Tang X, Quigg A, Lv M, Zhao Y (2019) The toxic mechanisms of BDE-47 to the marine diatom Thalassiosira pseudonana-a study based on multiple physiological processes. Aquat Toxicol 212:20–27

    CAS  PubMed  Google Scholar 

  • Zhu CJ, Lee YK (1997) Determination of biomass dry weight of marine microalgae. J Appl Phycol 9:189–194

    Google Scholar 

  • Zulfiqar S, Sharif S, Saeed M, Tahir A (2021) Role of carotenoids in photosynthesis. In: Zia-Ul-Haq M, Dewanjee S, Riaz M (eds) Carotenoids: structure and function in the human body. Springer, Cham, pp 147–187

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Funding

This work is supported by the National Natural Science Foundation of China (grant no. 42107307), the National Natural Science Foundation of China (grant no. 32002411), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), the Jiangsu Innovation Center for Marine Bioresources (822153216) and the Innovation and Entrepreneurship Project for College Students of Hohai University (No. 202310294184Y).

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Authors and Affiliations

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

    Feifei Yang

  2. Jiangsu Institute of Marine Resources Development, Jiangsu Ocean University, Lianyungang, 222005, China

    Feifei Yang

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

    Feifei Yang

  4. Jiangsu Marine Intelligent Equipment Engineering Research Center, Jiangsu Ocean University, Lianyungang, 222005, China

    Feifei Yang

  5. College of Marine Science and Fisheries, Jiangsu Ocean University, Lianyungang, 222005, China

    Wenhao Liu

  6. Jiangsu Province Engineering Research Center for Marine Bioresources Sustainable Utilization, Key Laboratory of Marine Hazards Forecasting, Ministry of Natural Resources, Hohai University, #1 Xikang Road, Gulou District, Nanjing, 210098, China

    Yongfu Li, Xingkai Che & Shuchen Liu

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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by [Feifei Yang], [Yongfu Li], [Wenhao Liu], [Xinkai Che] and [Shuchen Liu]. The first draft of the manuscript was written by [Feifei Yang] and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Yongfu Li.

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Yang, F., Liu, W., Li, Y. et al. Glycerol changes the growth and lipid profile of the marine microalga Isochrysis galbana via the regulation of photosynthetic and respiratory metabolic pathways. J Appl Phycol 36, 57–71 (2024). https://doi.org/10.1007/s10811-023-03148-z

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