Abstract
Microalgae are considered feedstock for biodiesel production due to their capability to accumulate triacylglycerols, which have a 99% conversion rate into biodiesel, under certain conditions. This study aims to evaluate thirty native microalgal strains as feedstock for biodiesel production based on their biomass and lipid productivities, and total lipid and triacylglycerol contents under nitrogen-sufficient and nitrogen starvation conditions. In addition, Chlamydomonas reinhardtii cw15 mutant strain was utilized as a reference strain for triacylglycerol accumulation. Among the eight potent strains, Chlorella vulgaris KP2 was considered as a most promising strain with the highest triacylglycerol content, highest total lipid content (28.56% of dry cell weight), and the highest lipid productivity (4.56 mg/L/day) under nitrogen starvation. Under nitrogen starvation, the major fatty acids in the triacylglycerol of Chlorella vulgaris KP2 were C18:1 (37.56%), C16:0 (23.16%), C18:0 (23.07), C18:2 (7.00%), and C18:3 (3.12%), and the percentages of saturated fatty acids, monounsaturated fatty acids, and polyunsaturated fatty acids represented 49.26, 38.73, and 10.12% of the total fatty acids, respectively. Furthermore, the fatty acid methyl esters of triacylglycerol displayed remarkable biodiesel properties with a lower iodine value (59.00 gI2/100 g), higher oxidative stability (14.24 h) and higher cetane number (58.73) under nitrogen starvation. This study suggests that nitrogen-starved Chlorella vulgaris KP2 could be used as a feedstock for biodiesel production due to the considerable amounts of triacylglycerol and favorable biodiesel properties.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306. https://doi.org/10.1016/j.biotechadv.2007.02.001
Schenk PM, Thomas-Hall SR, Stephens E et al (2008) Second generation biofuels: high-efficiency microalgae for biodiesel production. BioEnergy Res 1:20–43. https://doi.org/10.1007/s12155-008-9008-8
Draaisma RB, Wijffels RH, Slegers PME et al (2013) Food commodities from microalgae. Curr Opin Biotechnol 24:169–177. https://doi.org/10.1016/j.copbio.2012.09.012
Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: A review. Renew Sustain energy Rev 14:217–232. https://doi.org/10.1016/j.rser.2009.07.020
Rawat I, Ranjith Kumar R, Mutanda T, Bux F (2013) Biodiesel from microalgae: A critical evaluation from laboratory to large scale production. Appl Energy 103:444–467. https://doi.org/10.1016/j.apenergy.2012.10.004
Mandal S, Mallick N (2009) Microalga Scenedesmus obliquus as a potential source for biodiesel production. Appl Microbiol Biotechnol 84:281–291. https://doi.org/10.1007/s00253-009-1935-6
Singh P, Guldhe A, Kumari S et al (2015) Investigation of combined effect of nitrogen, phosphorus and iron on lipid productivity of microalgae Ankistrodesmus falcatus KJ671624 using response surface methodology. Biochem Eng J 94:22–29. https://doi.org/10.1016/j.bej.2014.10.019
Sun Z, gang Zhou Z, Gerken H et al (2015) Screening and characterization of oleaginous Chlorella strains and exploration of photoautotrophic Chlorella protothecoides for oil production. Bioresour Technol 184:53–62. https://doi.org/10.1016/j.biortech.2014.09.054
Sun LY, Cui WJ, Chen KM (2018) Two Mychonastes isolated from freshwater bodies are novel potential feedstocks for biodiesel production. Energy Sources, Part A Recover Util Environ Eff 40:1452–1460. https://doi.org/10.1080/15567036.2018.1477869
Yun HS, Ji MK, Park YT et al (2016) Microalga, Acutodesmus obliquus KGE 30 as a potential candidate for CO2 mitigation and biodiesel production. Environ Sci Pollut Res 23:17831–17839. https://doi.org/10.1007/s11356-016-6971-z
Allen JW, DiRusso CC, Black PN (2015) Triacylglycerol synthesis during nitrogen stress involves the prokaryotic lipid synthesis pathway and acyl chain remodeling in the microalgae Coccomyxa subellipsoidea. Algal Res 10:110–120. https://doi.org/10.1016/j.algal.2015.04.019
Breuer G, Lamers PP, Martens DE et al (2012) The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresour Technol 124:217–226. https://doi.org/10.1016/j.biortech.2012.08.003
EIA 2016 Intermational biodiesel production statistics (2016) The U.S. Energy Information Administration (EIA). https://www.eia.gov/beta/international/data/browser. Accessed 06 May 2019
Uysal D, Yilmaz KÇ, Taş T (2015) Enerji ithalatı ve cari açık ilişkisi Türkiye örneği. Anemon Muş Alparslan Üniversitesi Sos Bilim Derg. https://doi.org/10.18506/anemon.22254
Rippka R, Deruelles J, Waterbury JB (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61. https://doi.org/10.1099/00221287-111-1-1
Borowitzka MA (1988) Algal growth media and sources of cultures. In: Micro-algal Biotechnology. Cambridge University Press, pp 456–465
Siaut M, Cuine S, Cagnon C et al (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol 11:7. https://doi.org/10.1186/1472-6750-11-7
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc 18:315–322. https://doi.org/10.1016/b978-0-12-372180-8.50042-1
Mishra SK, Suh WI, Farooq W et al (2014) Rapid quantification of microalgal lipids in aqueous medium by a simple colorimetric method. Bioresour Technol 155:330–333. https://doi.org/10.1016/j.biortech.2013.12.077
Chen W, Zhang C, Song L et al (2009) A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae. J Microbiol Methods 77:41–47. https://doi.org/10.1016/j.mimet.2009.01.001
Hara A, Radin NS (1978) Lipid extraction of tissues with a low-toxicity solvent. Anal Biochem 90:420–426. https://doi.org/10.1016/0003-2697(78)90046-5
Msanne J, Xu D, Konda AR et al (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry 75:50–59. https://doi.org/10.1016/j.phytochem.2011.12.007
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917. https://doi.org/10.1139/y59-099
Hoekman SK, Broch A, Robbins C et al (2012) Review of biodiesel composition, properties, and specifications. Renew Sustain energy Rev 16:143–169. https://doi.org/10.1016/j.rser.2011.07.143
Park JY, Kim DK, Lee JP et al (2008) Blending effects of biodiesels on oxidation stability and low temperature flow properties. Bioresour Technol 99:1196–1203. https://doi.org/10.1016/j.biortech.2007.02.017
Sajjadi B, Chen W-Y, Raman AAA, Ibrahim S (2018) Microalgae lipid and biomass for biofuel production: A comprehensive review on lipid enhancement strategies and their effects on fatty acid composition. Renew Sustain Energy Rev 97:200–232. https://doi.org/10.1016/j.rser.2018.07.050
Lv J-M, Cheng L-H, Xu X-H et al (2010) Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresour Technol 101:6797–6804. https://doi.org/10.1016/j.biortech.2010.03.120
Wong YK, Ho YH, Ho KC, et al. (2017) Growth medium screening for Chlorella vulgaris growth and lipid production. J Aquac Mar Biol Doi: https://doi.org/10.15406/jamb.2017.06.00143
Sharma T, Gour RS, Kant A, Chauhan RS (2015) Lipid content in Scenedesmus species correlates with multiple genes of fatty acid and triacylglycerol biosynthetic pathways. Algal Res 12:341–349. https://doi.org/10.1016/j.algal.2015.09.006
Shen X-F, Qin Q-W, Yan S-K et al (2019) Biodiesel production from Chlorella vulgaris under nitrogen starvation in autotrophic, heterotrophic, and mixotrophic cultures. J Appl Phycol 31:1589–1596. https://doi.org/10.1007/s10811-019-01765-1
Ren HY, Liu BF, Ma C et al (2013) A new lipid-rich microalga Scenedesmus sp strain R-16 isolated using Nile red staining: effects of carbon and nitrogen sources and initial pH on the biomass and lipid production. Biotechnol Biofuels. https://doi.org/10.1186/1754-6834-6-143
Yuan C, Liu J, Fan Y et al (2011) Mychonastes afer HSO-3-1 as a potential new source of biodiesel. Biotechnol Biofuels 4:47. https://doi.org/10.1186/1754-6834-4-47
Ho SH, Chen CY, Chang JS (2012) Effect of light intensity and nitrogen starvation on CO2 fixation and lipid/carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N. Bioresour Technol 113:244–252. https://doi.org/10.1016/j.biortech.2011.11.133
Álvarez-Díaz PD, Ruiz J, Arbib Z et al (2014) Lipid production of microalga Ankistrodesmus falcatus increased by nutrient and light starvation in a two-stage cultivation process. Appl Biochem Biotechnol 174:1471–1483. https://doi.org/10.1007/s12010-014-1126-5
Zhao L-S, Li K, Wang Q-M et al (2017) Nitrogen starvation impacts the photosynthetic performance of Porphyridium cruentum as revealed by chlorophyll a fluorescence. Sci Rep 7:1–11. https://doi.org/10.1038/s41598-017-08428-6
Gour RS, Chawla A, Singh H et al (2016) Characterization and screening of native Scenedesmus sp isolates suitable for biofuel feedstock. PLoS ONE. https://doi.org/10.1371/journal.pone.0155321
Nascimento IA, Marques SSI, Cabanelas ITD et al (2013) Screening microalgae strains for biodiesel production: Lipid productivity and estimation of fuel quality based on fatty acids profiles as selective criteria. Bioenergy Res 6:1–13. https://doi.org/10.1007/s12155-012-9222-2
Griffiths MJ, van Hille RP, Harrison STL (2014) The effect of nitrogen limitation on lipid productivity and cell composition in Chlorella vulgaris. Appl Microbiol Biotechnol 98:2345–2356. https://doi.org/10.1007/s00253-013-5442-4
Mujtaba G, Choi W, Lee CG, Lee K (2012) Lipid production by Chlorella vulgaris after a shift from nutrient-rich to nitrogen starvation conditions. Bioresour Technol 123:279–283. https://doi.org/10.1016/j.biortech.2012.07.057
Belotti G, Bravi M, de Caprariis B et al (2013) Effect of nitrogen and phosphorus starvations on Chlorella vulgarislipids productivity and quality under different trophic regimens for biodiesel production. Am J Plant Sci 04:44–51. https://doi.org/10.4236/ajps.2013.412a2006
Griffiths MJ, Van Hille RP, Harrison STL (2014) The effect of degree and timing of nitrogen limitation on lipid productivity in Chlorella vulgaris. Appl Microbiol Biotechnol 98:6147–6159. https://doi.org/10.1007/s00253-014-5757-9
Silaban A, Bai R, Gutierrez-Wing MT et al (2014) Effect of organic carbon, C: N ratio and light on the growth and lipid productivity of microalgae/cyanobacteria coculture. Eng Life Sci 14:47–56. https://doi.org/10.1002/elsc.201200219
Kim HS, Park W-K, Lee B et al (2019) Optimization of heterotrophic cultivation of Chlorella sp. HS2 using screening, statistical assessment, and validation. Sci Rep 9:1–13. https://doi.org/10.1038/s41598-019-55854-9
Knothe G (2009) Improving biodiesel fuel properties by modifying fatty ester composition. Energy Environ Sci 2:759–766. https://doi.org/10.1039/B903941D
Adamakis I-D, Lazaridis PA, Terzopoulou E et al (2018) Cultivation, characterization, and properties of Chlorella vulgaris microalgae with different lipid contents and effect on fast pyrolysis oil composition. Environ Sci Pollut Res 25:23018–23032. https://doi.org/10.1007/s11356-018-2368-5
Shen P-L, Wang H-T, Pan Y-F et al (2016) Identification of characteristic fatty acids to quantify triacylglycerols in microalgae. Front Plant Sci 7:162. https://doi.org/10.3389/fpls.2016.00162
Li X, Moellering ER, Liu B et al (2012) A galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24:4670–4686. https://doi.org/10.1105/tpc.112.105106
Azam MM, Waris A, Nahar NM (2005) Prospects and potential of fatty acid methyl esters of some non-traditional seed oils for use as biodiesel in India. Biomass Bioenerg 29:293–302. https://doi.org/10.1016/j.biombioe.2005.05.001
Bart JCJ, Palmeri N, Cavallaro S (2010) Biodiesel science and technology from soil to oil. Elsevier, pp 226–284. https://doi.org/https://doi.org/10.1533/9781845697761.22650.
Demirbas A (2008) Biodiesel. Springer, pp 111−119.
Acknowledgements
The authors express their gratitude to TÜBİTAK (The Scientific and Technological Research Council of Turkey, 116Y345) and the University of Nevsehir Hacı Bektas Veli, Scientific Research Projects Unit (NEUBAP15F26), for their financial support.
Funding
This study was funded by TÜBİTAK (The Scientific and Technological Research Council of Turkey, 116Y345) and the University of Nevsehir Hacı Bektas Veli, Scientific Research Projects Unit (NEUBAP15F26).
Author information
Authors and Affiliations
Contributions
EEA performed the experiments, analyzed and interpreted the data, wrote the paper, and prepared figures and/or tables. SO and BA planned and designed the research, interpreted the data, and wrote and edited the paper.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Research involving human participants and/or animals
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Andeden, E.E., Ozturk, S. & Aslim, B. Evaluation of Thirty Microalgal Isolates as Biodiesel Feedstocks Based on Lipid Productivity and Triacylglycerol (TAG) Content. Curr Microbiol 78, 775–788 (2021). https://doi.org/10.1007/s00284-020-02340-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-020-02340-5