Skip to main content

Advertisement

Log in

Nitrogen, phosphorus and high CO2 modulate photosynthesis, biomass and lipid production in the green alga Chlorella vulgaris

  • Original article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Climate change could impact nutrient bioavailability in aquatic environment. To understand the interaction of nutrient bioavailability and elevated CO2, Chlorella vulgaris cells were grown in ambient air or 5% CO2 in different concentrations of nitrogen and phosphorus in a photobioreactor. The chlorophyll content, photosynthesis and respiration rates increased in 5% CO2 to support higher biomass production. The nutrient limitation in the growth media resulted in reduced photosynthetic rates of the algal cells and their PSI, PSII, and whole chain electron transport rates and biomass production. Conversely, their lipid content increased partly due to upregulation of expression of several lipid biosynthesis genes. The order of downregulation of photosynthesis and upregulation in lipid production due to nutrient limitation was in the order of N > P. The N-50 and 5% CO2 culture had only 10% reduction in biomass and 32% increase in lipids having 85% saturated fat required for efficient biofuel production. This growth condition is ideal for generation of biodiesel required to reduce the consumption of fossil fuel and combat global warming.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Allakhverdiev SI (2020) Editorial for the special issue on photosynthesis and hydrogen energy research for sustainability—2019. Photosynth Res 146:1–3. https://doi.org/10.1007/s11120-020-00764-5

    Article  CAS  PubMed  Google Scholar 

  • Ambastha V, Sopory SK, Tiwari BC, Tripathy BC (2017) Photo-modulation of programmed cell death in rice leaves triggered by salinity. Apoptosis 22:41–56

    Article  CAS  PubMed  Google Scholar 

  • Aro EM (2016) From first generation biofuels to advanced solar biofuels. Ambio 45:24–31

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1016/j.algal.2016.03.022

    Article  Google Scholar 

  • Basova MM (2005) Fatty acid composition of lipids in microalgae. Int J Algae 7:33–57

    Article  Google Scholar 

  • Berdalet E, Latasa M, Estrada M (1994) Effects of nitrogen and phosphorus starvation on nucleic acid and protein content of Heterocapsa sp. J Plankton Res 16:303–316

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Breuer G, Lamers PP, Martens DE, Draaisma RB, Wijffels RH (2013) Effect of light intensity, pH, and temperature on triacylglycerol (TAG) accumulation induced by nitrogen starvation in Scenedesmus obliquus. Bioresour Technol 143:1–9

    Article  CAS  PubMed  Google Scholar 

  • Cakmak T, Angun P, Demiray Y, Ozkan A, Elibol Z, Tekinay T (2012) Differential effects of nitrogen and sulfur deprivation on growth and biodiesel feedstock production of Chlamydomonas reinhardtii. Biotechnol Bioeng 109:1947–57

    Article  CAS  PubMed  Google Scholar 

  • Chakraborty N, Tripathy BC (1992) Involvement of singlet oxygen in 5-aminolevulinic acid induced photodynamic damage of cucumber (Cucumis sativus L.) Chloroplasts. Plant Physiol 98:7–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306

    Article  CAS  PubMed  Google Scholar 

  • Chiu SY, Kao CY, Tsai MT, Ong SC, Chen CH, Lin CS (2009) Lipid accumulation and CO2 utilization of Nannochloropsis oculata in response to CO2 aeration. Bioresour Technol 100:833–838

    Article  CAS  PubMed  Google Scholar 

  • Ehimen EA, Sun ZF, Carrington CG, Birch EJ, Eaton-Rye JJ (2011) Anaerobic digestion of microalgae residues resulting from the biodiesel production process. Applied Energy 88:3454–3463

    Article  CAS  Google Scholar 

  • Fan LH, Zhang YT, Cheng LH, Zhang L, Tang DS, Chen HL (2008) Optimization of carbon dioxide fixation by Chlorella vulgaris cultivated in a membrane-photobioreactor. Chem Eng Tech: Indust Chem, Plant Equip, Proc Eng Biotech 30:1094–1099

    Article  Google Scholar 

  • Fredeen AL, Raab TK, Rao IM, Terry N (1990) Effects of phosphorus nutrition on photosynthesis in Glycine max (L.) Merr. Planta 181:399–405

    Article  CAS  PubMed  Google Scholar 

  • Gouveia L, Oliveira AC (2009) Microalgae as a raw material for biofuels production. J Ind Microbiol Biotechnol 36:269–274

    Article  CAS  PubMed  Google Scholar 

  • Hsueh H, Li W, Chen H, Chu H (2009) Carbon bio-fixation by photosynthesis of Thermosynechococcus sp. CL-1 and Nannochloropsis oculta. J Photochem Photobiol B 95:33–39

    Article  CAS  PubMed  Google Scholar 

  • Hu H, Gao K (2003) Optimization of growth and fatty acid composition of a unicellular marine picoplankton, Nannochloropsis sp., with enriched carbon sources. Biotechnol Lett 25:421–425

    Article  CAS  PubMed  Google Scholar 

  • Huerlimann R, de Nys R, Heimann K (2010) Growth, lipid content, productivity, and fatty acid composition of tropical microalgae for scale-up production. Biotechnol bioeng 107:245–257

    Article  CAS  PubMed  Google Scholar 

  • Jayaraman A, Puranik S, Rai NK, Vidapu S, Sahu PP, Lata C, Prasad M (2008) cDNA-AFLP analysis reveals differential gene expression in response to salt stress in foxtail millet (Setaria italica L.). Mol Biotechnol 40:241–251

    Article  CAS  PubMed  Google Scholar 

  • Jiang CD, Wang X, Gao HY, Shi L, Chow WS (2011) Systemic regulation of leaf anatomical structure, photosynthetic performance, and high-light tolerance in sorghum. Plant Physiol 155:1416–1424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jilani A, Kar S, Bose S, Tripathy BC (1996) Regulation of the carotenoid content and chloroplast development by levulinic acid. Physiol Plant 96:139–145

    Article  CAS  Google Scholar 

  • Kavanova M, Lattanzi FA, Grimodi AA, Schnyder H (2006) Phosphorus deficiency decreases cell division and elongation in grass leaves. Plant Physiol 141:766–775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khozin-Goldberg I, Cohen Z (2006) The effect of phosphate starvation on the lipid and fatty acid composition of the fresh water eustigmatophyte Monodus subterraneus. Phytochemistry 67:696–701

    Article  CAS  PubMed  Google Scholar 

  • Kim G, Bae J, Lee K (2016) Nitrate repletion strategy for enhancing lipid production from marine microalga Tetraselmis sp. Bioresour Technol 205:274–279

    Article  CAS  PubMed  Google Scholar 

  • Klaus D, Ohlrogge JB, Neuhaus HE, Dormann P (2004) Increased fatty acid production in potato by engineering of acetyl-CoA carboxylase. Planta 219:389–396

    Article  CAS  PubMed  Google Scholar 

  • Konopka A, Schnur M (1981) Biochemical composition and photosynthetic carbon metabolism of nutrient limited cultures of Merismopedia tenuissima (Cyanophyceae). J Phycol 17:118–122

    Article  CAS  Google Scholar 

  • Larkum, AWD (2020) Light-Harvesting in Cyanobacteria and Eukaryotic Algae: An Overview. In: Larkum, Anthony W. D., Grossmann, Arthur, Raven, John (eds.) Photosynthesis in algae: Biochemical and physiological mechanisms. Springer Nature Switzerland AG, pp 207-260

  • Lee HS, Vermaas WFJ, Rittmann BE (2010) Biological hydrogen production: prospects and challenges. Trends Biotechnol 28:262–271

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Horsman M, Wu N, Lan CQ, Dubois-Calero N (2008) Biofuels from microalgae. Biotechnol Prog 24:815–820

    CAS  PubMed  Google Scholar 

  • Liu Y, Lotero E, Goodwin JG Jr, Mo X (2007) Transesterification of poultry fat with methanol using Mg–Al hydrotalcite derived catalysts. Appl Catal A Gen 331:138–148

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu JM, Cheng LH, Xu XH, Zhang L, Che HL (2010) Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresource Technology 101:6797–6804

    Article  Google Scholar 

  • Mandal S, Patnaik R, Singh AK, Mallick N (2013) Comparative assessment of various lipid extraction protocols and optimization of transesterification process for microalgal biodiesel production. Environ Technol 34:2009–2018

    Article  CAS  PubMed  Google Scholar 

  • Matsuda Y (2011) Inorganic carbon utilization by aquatic photoautotrophs and potential usages of algal primary production. Photosynth Res 109:1–5

    Article  CAS  PubMed  Google Scholar 

  • Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulate the rate of photodamage in vivo? Trends Plant Sci Rev 4:130–135

    Article  CAS  Google Scholar 

  • Melis A (2007) Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae). Planta 226:1075–1086

    Article  CAS  PubMed  Google Scholar 

  • Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122:127–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mhatre A, Patil S, Agarwal A, Pandit R (2019) Influence of nitrogen source on photochemistry and antenna size of the photosystems in marine green macroalgae, Ulva lactuca. Photosynth Res 139:539–551. https://doi.org/10.1007/s11120-018-0554-4

    Article  CAS  PubMed  Google Scholar 

  • Moroney JV, Wee JL (2014) CCM8: the eighth international symposium on inorganic carbon uptake by aquatic photosynthetic organisms. Photosynth Res 121:107–110

    Article  CAS  PubMed  Google Scholar 

  • Myers J (1947) Culture conditions and the development of the photosynthetic mechanism. V. Influence of the composition of the culture medium. Plant Physiol 22:590–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Myers J, Phillips JN, Graham JR (1951) On the mass culture of algae. Plant Physiol 26:539–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Negi S, Barry AN, Friedland N, Sudasinghe N, Subramanian S, Pieris S, Holguin FO, Dungan B, Schaub T, Sayre R (2016) Impact of nitrogen limitation on biomass, photosynthesis, and lipid accumulation in Chlorella sorokiniana. J Appl Phycol 28:803–812. https://doi.org/10.1007/s10811-015-0652-z

    Article  CAS  Google Scholar 

  • Negi S, Perrine Z, Friedland N, Kumar A, Tokutsu R, Minagawa J, Berg H, Barry AN, Govindjee G, Sayre R (2020) Light regulation of light-harvesting antenna size substantially enhances photosynthetic efficiency and biomass yield in green algae. Plant J. https://doi.org/10.1111/tpj.14751

    Article  PubMed  Google Scholar 

  • Nelson DL, Cox MM (2000) Lehninger, principles of biochemistry, 3rd edn. Worth Publishing, New York

    Google Scholar 

  • Nilsson F, Simpson DJ, Jansson C, Andersson B (1992) Ultrastructural and biochemical characterization of a Synechocystis 6803 mutant with inactivated psbA genes. Arch Biochem Biophys 295:340–347

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pancha I, Chokshi K, George B, Ghosh T, Paliwal C, Maurya R, Mishra S (2014) Nitrogen stress triggered biochemical and morphological changes in the microalgae Scenedesmus sp. CCNM 1077. Bioresour Technol 156:146–54

    Article  CAS  PubMed  Google Scholar 

  • Pattanayak GK, Tripathy BC (2002) Catalytic function of a novel protein protochlorophyllide oxidoreductase C of Arabidopsis thaliana. Biochem Biophys Res Commun 291:921–924

    Article  CAS  PubMed  Google Scholar 

  • Pattanayak GK, Tripathy BC (2011) Overexpression of protochlorophyllide oxidoreductase C regulates oxidative stress in Arabidopsis. PLoS One 6:e26532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perrine Z, Negi S, Sayre RT (2012) Optimization of photosynthetic light energy utilization by microalgae. Algal Res 1:134–142

    Article  Google Scholar 

  • Pohl P, Wagner H (1972) Control of fatty acid and lipid biosynthesis in Euglena gracilis by ammonia, light and DCMU. Z Naturforsch 27:53–61

    Article  CAS  Google Scholar 

  • Pyliotis NA, Goodchild DJ (1975) Induced and normal crystalline inclusions in plastids revealed by freeze-fracturing. Protoplasma 85:277–285

    Article  Google Scholar 

  • Rai L, Mallick N, Singh J, Kumar H (1991) Physiological and biochemical characteristics of a copper tolerant and a wild type strain of Anabaena doliolum under copper stress. J Plant Physiol 138:68–74

    Article  CAS  Google Scholar 

  • Razeghifard R (2013) Algal biofuels. Photosynth Res 117:207–219

    Article  CAS  PubMed  Google Scholar 

  • Reitan KI, Rainuzzo JR, Olsen Y (1994) Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J Phycol 30:972–979

    Article  CAS  Google Scholar 

  • Sartory D, Grobbelaar J (1984) Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114:177–187

    Article  CAS  Google Scholar 

  • Sato N, Wada H (2009) Lipid Biosynthesis and its Regulation in Cyanobacteria. In: Wada H, Murata N (eds) Advances in Photosynthesis and Respiration: Lipids in Photosynthesis, Essential and Regulatory Functions, vol 30. Springer, Netherlands, pp 157–177

    Chapter  Google Scholar 

  • Sayre R (2010) Microalgae: the potential for carbon capture. Bioscience 60:722–727

    Article  Google Scholar 

  • Sayre RT, Negi S, Govindjee G (2020) Light regulation of photosynthetic light harvesting doubles the biomass yield in the green alga Chlamydomonas. Photosynthetica 58:974–975

    Article  Google Scholar 

  • Siegenthaler P-A, Murata N (eds) (1998) Lipids in Photosynthesis: Structure. Function and Genetics, Springer, Dordrecht

    Google Scholar 

  • Siron R, Giusti G, Berland B (1989) Changes in the fatty acid composition of Phaeodactylum tricornutum and Dunaliella tertiolecta during growth and under phosphorus deficiency. Mar Ecol Prog Ser 55:95–100

    Article  CAS  Google Scholar 

  • Soeder CJ, Bolze A (1981) Sulfate deficiency stimulates release of dissolved organic matter in synchronous cultures of Scenedesmus obliquus. Physiol Plant 52:233–238

    Article  CAS  Google Scholar 

  • Sood S, Gupta V, Tripathy BC (2005) Photoregulation of the greening process of wheat seedlings grown in red light. Plant Mol Biol 59:269–287

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Cao Y, Xu H, Liu Y, Sun J, Qiao D, Cao Y (2015) Effect of nitrogen-starvation, light intensity and iron on triacylglyceride/carbohydrate production and fatty acid profile of Neochloris oleoabundans HK-129 by a two-stage process. Bioresour Technol 155:204–212

    Article  Google Scholar 

  • Tang D, Han W, Li P, Miao X, Zhong J (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  PubMed  Google Scholar 

  • Ueno Y, Shimakawa G, Aikawa S, Miyake C, Akimoto S (2020) Photoprotection mechanisms under diferent CO2 regimes during photosynthesis in a green alga Chlorella variabilis. Photosynth Res. https://doi.org/10.1007/s11120-020-00757-4

    Article  PubMed  Google Scholar 

  • Valledor L, Furuhashi T, Recuenco-Muñoz L, Wienkoop S, Weckwerth W (2014) System-level network analysis of nitrogen starvation and recovery in Chlamydomonas reinhardtii reveals potential new targets for increased lipid accumulation. Biotechnol Biofuels 7:171

    Article  PubMed  PubMed Central  Google Scholar 

  • Wada H, Murata N (2009) Lipids in thylakoid membranes and photosynthetic cells. In: Wada H, Murata N (eds) Lipids in Photosynthesis Essential and Regulatory Functions. Springer, Dordrecht, pp 1–9

    Chapter  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Xin L, Hong-ying H, Ke G, Ying-xue S (2010) Effects of different nitrogen and phosphorus concentrations on the growth, nutrient uptake, and lipid accumulation of a freshwater microalga Scenedesmus sp. Bioresour Technol 101:5494–5500

    Article  CAS  PubMed  Google Scholar 

  • Yang D, Song D, Kind T, Ma Y, Hoefkens J, Fiehn O (2015) Lipidomic analysis of Chlamydomonas reinhardtii under nitrogen and sulfur Deprivation. PLoS One 10:e0137948

    Article  PubMed  PubMed Central  Google Scholar 

  • Yodsuwan N, Sawayama S, Sirisansaneeyakula S (2017) Effect of nitrogen concentration on growth, lipid production and fatty acid profiles of the marine diatom Phaeodactylum tricornutum. Agric. Nat. Resour. 51:190–197

    Google Scholar 

  • Zhang Y, Wu H, Sun M, Peng Q, Li A (2018) Photosynthetic physiological performance and proteomic profiling of the oleaginous algae Scenedesmus acuminatus reveal the mechanism of lipid accumulation under low and high nitrogen supplies. Photosynth Res 138:73–102. https://doi.org/10.1007/s11120-018-0549

    Article  CAS  PubMed  Google Scholar 

  • Zhu S, Huang W, Xu J, Wang Z, Xu J, Yuan Z (2014) Metabolic changes of starch and lipid triggered by nitrogen starvation in the microalga Chlorella zofingiensis. Bioresour Technol 152:292–298

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Li Z, Hiltunen E (2016) Strategies for lipid production improvement in microalgae as a biodiesel feedstock. Biomed Res 8. Article ID 8792548

Download references

Acknowledgements

This work was supported by a grant from the Department of Biotechnology, Government of India (2/662017 -IBSD) to BCT and DBS.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Dinabandhu Sahoo or Baishnab C Tripathy.

Ethics declarations

Conflict of interest

Authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumari, K., Samantaray, S., Sahoo, D. et al. Nitrogen, phosphorus and high CO2 modulate photosynthesis, biomass and lipid production in the green alga Chlorella vulgaris. Photosynth Res 148, 17–32 (2021). https://doi.org/10.1007/s11120-021-00828-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-021-00828-0

Keywords

Navigation