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Effect of different iron concentrations on growth, lipid accumulation, and fatty acid profile for biodiesel production from Tetradesmus obliquus

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Abstract

The present study investigated the effect of ferric iron on growth and lipid content of the green microalga Tetradesmus obliquus as a promising feedstock with favorable features for biodiesel production. The microalga was isolated from a freshwater body and cultured for 20 days in five types of modified BG11 medium with different concentrations (0, 10−4, 10−3, 10−2, 10−1 mmol L−1) of ferric iron. The algae grown in medium supplemented with 10−2 mmol L−1 ferric iron had the highest specific growth rate of 0.36 ± 0.04 day−1 and remained in the exponential growth phase over the next 6 days compared with those grown in medium without iron supplementation. The peak of lipid content (34.19 ± 1.93% dry weight, DW) and biomass productivity (459.20 ± 2.37 mg L−1 day−1) was obtained in the media supplemented with 10−2 and 10−1 mmol L−1 ferric iron, respectively. The highest proportion of saturated fatty acids and the lowest proportion of unsaturated fatty acids were also achieved by adding 10−1 mmol L−1 ferric iron to the growth medium. These findings may lead to a two-step process for lipid production from T. obliquus, in which biomass should be separated from the culture supplemented with 10−2 mmol L−1 ferric iron concentration to achieve the maximum algal biomass in the first step and then inoculated to the culture supplemented with 10−1 mmol L−1 ferric iron concentration to reach the highest lipid productivity in the second step, leading to optimization of lipid production from T. obliquus. Although the quality of biodiesel produced from T. obliquus met the specification of the European biodiesel standard (EN14214) in all media, ferric iron supplementation could be used to optimize the lipid characteristics of T. obliquus for biodiesel production.

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References

  • Abomohra AE, Jin W, El-Sheekh M (2016) Enhancement of lipid extraction for improved biodiesel recovery from the biodiesel promising microalga Scenedesmus obliquus. Energy Convers Manag 108:23–39

    CAS  Google Scholar 

  • Abomohra AE, Jin W, Sagar V, Ismail GA (2018) Optimization of chemical flocculation of Scenedesmus obliquus grown on municipal wastewater for improved biodiesel recovery. Renew Energy 115:880–886

    CAS  Google Scholar 

  • Ahmad AL, Yasin NH, Derek CJC, Lim JK (2011) Microalgae as a sustainable energy source for biodiesel production: a review. Renew Sust Energ Rev 15:584–593

    CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Álvarez-Díaz PD, Ruiz J, Arbib Z, Barragán J, Garrido-Pérez MC, Perales JA (2015) Wastewater treatment and biodiesel production by Scenedesmus obliquus in a two-stage cultivation process. Bioresour Technol 181:90–96

    PubMed  Google Scholar 

  • Amaro HM, Guedes AC, Malcata FX (2011) Advances and perspectives in using microalgae to produce biodiesel. Appl Energy 88:3402–3410

    CAS  Google Scholar 

  • Anahas AMP, Muralitharan G (2018) Characterization of heterocystous cyanobacterial strains for biodiesel production based on fatty acid content analysis and hydrocarbon production. Energy Convers Manag 157:423–437

    CAS  Google Scholar 

  • APHA (1998) Standard methods for examination of water and wastewater, twentieth ed. American Public Health Association, Washington, DC

    Google Scholar 

  • Arias-Peñaranda MT, Cristiani-Urbina E, Montes-Horcasitas CM, Esparza-Garćıa F, Torzillo G, Cañizares-Villanueva RO (2013) Scenedesmus incrassatulus CLHE-Si01: A potential source of renewable lipid for high quality biodiesel production. Bioresour Technol 140:158–164

    PubMed  Google Scholar 

  • Ashokkumar V, Salam Z, Tiwari ON, Chinnasamy S, Mohammed S, Ani FN (2015) An integrated approach for biodiesel and bioethanol production from Scenedesmus bijugatus cultivated in a vertical tubular photobioreactor. Energy Convers Manag 101:778–786

    CAS  Google Scholar 

  • Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Med Cell Longev 2014:1–31

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Borowitzka MA (1992) Algal biotechnology products and processes - matching science and economics. J Appl Phycol 4:267–279

    Google Scholar 

  • Borowitzka MA, Moheimani NR (2013) Sustainable biofuels from algae. Mitig Adapt Strateg Glob Chang 18:13–25

    Google Scholar 

  • Brennan L, Owende P (2010) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and coproducts. Renew Sust Energ Rev 14:557–577

    CAS  Google Scholar 

  • Cakmak T, Angun P, Demiray YE, Ozkan AD, Elibol Z, Tekinay T (2012) Differential effects of nitrogen and sulfur deprivation on growth and biodiesel feedstock production of Chlamydomonas reinhardtii. Biotechnol Bioeng 109:1947–1957

    CAS  PubMed  Google Scholar 

  • Che R, Huang L, Yu X (2015) Enhanced biomass production, lipid yield and sedimentation efficiency by iron ion. Bioresour Technol 192:795–798

    CAS  PubMed  Google Scholar 

  • Chia MA, Lombardi AT, Melão MDGG, Parrish CC (2013) Effects of cadmium and nitrogen on lipid composition of Chlorella vulgaris (Trebouxiophyceae, Chlorophyta). Eur J Phycol 48:1–11

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Concas A, Steriti A, Pisu M, Cao G (2014) Comprehensive modeling and investigation of the effect of iron on the growth rate and lipid accumulation of Chlorella vulgaris cultured in batch photobioreactors. Bioresour Technol 153:340–350

    CAS  PubMed  Google Scholar 

  • Demirbas MF (2011) Biofuels from algae for sustainable development. Appl Energy 88:3473–3480

    CAS  Google Scholar 

  • Dlouhy AC, Outten CE (2013) The iron metallome in eukaryotic organisms. Met Ions Life Sci 12:241–278

    PubMed  PubMed Central  Google Scholar 

  • Doubnerová V, Ryšlavá H (2011) What can enzymes of C4 photosynthesis do for C3 plants under stress? Plant Sci 180:575–583

    PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Fan J, Andre C, Xu C (2011) A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii. FEBS Lett 585:1985–1991

    CAS  PubMed  Google Scholar 

  • Glaesener AG, Merchant SS, Blaby-Haas CE (2013) Iron economy in Chlamydomonas reinhardtii. Front Plant Sci 4:337

    PubMed  PubMed Central  Google Scholar 

  • Glass JB, Wolfe-Simon F, Anbar AD (2009) Coevolution of metal availability and nitrogen assimilation in cyanobacteria and algae. Geobiology 7:100–123

    CAS  PubMed  Google Scholar 

  • Goncalves EC, Wilkie AC, Kirst M, Rathinasabapathi B (2016) Metabolic regulation of triacylglycerol accumulation in the green algae: identification of potential targets for engineering to improve oil yield. Plant Biotechnol J 14:1649–1660

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Gris B, Morosinotto T, Giacometti GM, Bertucco A, Sforza E (2014) Cultivation of Scenedesmus obliquus in photobioreactors: effects of light intensities and light-dark cycles on growth, productivity, and biochemical composition. Appl Biochem Biotechnol 172:2377–2389

    CAS  PubMed  Google Scholar 

  • Hernández-Torres A, Zapata-Morales AL, Ochoa Alfaro AE, Soria-Guerra RE (2016) Identification of gene transcripts involved in lipid biosynthesis in Chlamydomonas reinhardtii under nitrogen, iron and sulfur deprivation. World J Microbiol Biotechnol 32:55

    PubMed  Google Scholar 

  • Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54:621–639

    CAS  PubMed  Google Scholar 

  • Huang X, Wei L, Huang Z, Yan JW (2014) Effect of high ferric ion concentrations on total lipids and lipid characteristics of Tetraselmis subcordiformis, Nannochloropsis oculata and Pavlova viridis. J Appl Phycol 26:105–114

    CAS  Google Scholar 

  • Illman AM, Scragg AH, Shales SW (2000) Increase in Chlorella strains calorific values when grown in low nitrogen medium. Enzym Microb Technol 27:631–635

    CAS  Google Scholar 

  • Islam MA, Ayoko GA, Brown R, Stuart D, Heimann K (2013) Influence of fatty acid structure on fuel properties of algae derived biodiesel. Procedia Eng 56:591–596

    CAS  Google Scholar 

  • Kadar E, Tarran GE, Jha AW, Al-Subiai SN (2011) Stabilisation of engineered zero-valent nanoiron with Na-acrylic copolymer enhances spermiotoxicity. Environ Sci Technol 45:3245–3251

    CAS  PubMed  Google Scholar 

  • Keenan C, Goth-Goldstein R, Lucas D, Sedlak LD (2009) Oxidative stress induced by zero-valent iron nanoparticles and Fe(II) in human bronchial epithelial cells. Environ Sci Technol 43:4555–4560

    CAS  PubMed  Google Scholar 

  • Kehrer JP (2000) The Haber-Weiss reaction and mechanisms of toxicity. Toxicology. 149:43–50

    CAS  PubMed  Google Scholar 

  • Knothe G (2012) Fuel properties of highly polyunsaturated fatty acid methyl esters. Prediction of fuel properties of algal biodiesel. Energy Fuel 26:5265–5273

    CAS  Google Scholar 

  • Koller M, Muhr A, Braunegg G (2014) Microalgae as versatile cellular factories for valued products. Algal Res 6:52–63

    Google Scholar 

  • Lang X, Dalai AK, Bakhshi NN, Reaney MJ, Hertz PB (2001) Preparation and characterization of bio-diesels from various bio-oils. Bioresour Technol 80:53–62

    CAS  PubMed  Google Scholar 

  • Lari Z, Moradi-kheibari N, Ahmadzadeh H, Abrishamchi P, Moheimani NR, Murry MA (2016) Bioprocess engineering of microalgae to optimize lipid production through nutrient management. J Appl Phycol 28:3235–3250

    CAS  Google Scholar 

  • Li Y, Han D, Sommerfeld M, Hu Q (2011) Photosynthetic carbon partitioning and lipid production in the oleaginous microalga Pseudochlorococcum sp. (Chlorophyceae) under nitrogen-limited conditions. Bioresour Technol 102:123–129

    CAS  PubMed  Google Scholar 

  • Li-Beisson Y, Thelen JJ, Fedosejevs E, Harwood JL (2019) The lipid biochemistry of eukaryotic algae. Prog Lipid Res 74:31–68

    CAS  PubMed  Google Scholar 

  • Liu ZY, Wang GC, Zhou BC (2008) Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresour Technol 99:4717–4722

    CAS  PubMed  Google Scholar 

  • Marchetti A, Maldonado MT (2016) Iron. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 233–279

    Google Scholar 

  • Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sustain Energy Rev 14(1):217–232

    CAS  Google Scholar 

  • Miller GW, Huang IJ, Welkie GW, Pushnik JC (1995) Function of iron in plants with special emphasis on chloroplasts and photosynthetic activity. In: Abadía J (ed) Iron nutrition in soils and plants. Springer, Dordrecht, pp 19–28

    Google Scholar 

  • Nascimento IA, Marques SSI, Cabanelas ITD, Pereira SA, Druzian JI, de Souza CO, Vich DV, de Carvalho GC, Nascimento MA (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

    CAS  Google Scholar 

  • Osundeko O, Davis H, Pittman JK (2013) Oxidative stress-tolerant microalgae strains are highly efficient for biofuel feedstock production on wastewater. Biomass Bioenergy 56:284–294

    CAS  Google Scholar 

  • Pádrová K, Lukavský J, Nedbalová L, Čejková A, Cajthaml T, Sigler K, Vítová M, Řezanka T (2015) Trace concentrations of iron nanoparticles cause overproduction of biomass and lipids during cultivation of cyanobacteria and microalgae. J Appl Phycol 27:1443–1451

    Google Scholar 

  • Patil V, Tran KQ, Giselrød HR (2008) Towards sustainable production of biofuels from microalgae. Int J Mol Sci 9:1188–1195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Predojević Z, Škrbić B, Durišić-Mladenović N (2012) Transesterification of linoleic and oleic sunflower oils to biodiesel using CaO as a solid base catalyst. J Serb Chem Soc 77:815–832

    Google Scholar 

  • Qiu R, Gao S, Lopez PA, Ogden KL (2017) Effects of pH on cell growth, lipid production and CO2 addition of microalgae Chlorella sorokiniana. Algal Res 28:192–199

    Google Scholar 

  • Rai MP, Gupta S (2016) Effect of media composition and light supply on biomass, lipid content and FAME profile for quality biofuel production from Scenedesmus abundans. Energy Convers Manag 141:85–92

    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 1:100–112

    Google Scholar 

  • Ruangsomboon S, Ganmanee M, Choochote S (2013) Effects of different nitrogen, phosphorus, and iron concentrations and salinity on lipid production in newly isolated strain of the tropical green microalga, Scenedesmus dimorphus KMITL. J Appl Phycol 25:867–874

    CAS  Google Scholar 

  • Salamaa E, Kuradea MB, Abou-Shanabb RAI, El-Dalatonya MM, Yanga IS, Minc B, Jeona BH (2017) Recent progress in microalgal biomass production coupled with wastewater treatment for biofuel generation. Renew Sust Energ Rev 79:1189–1211

    Google Scholar 

  • Schenk PM, Thomas-Hall SR, Stephens E, Marx UC, Mussgnug JH, Posten C, Olaf Kruse O, Hankamer B (2008) Second generation biofuels: high-efficiency microalgae for biodiesel production. Bioenergy Res 1:20–43

    Google Scholar 

  • Shao Y, Fang H, Zhou H, Wang Q, Zhu Y, He Y (2017) Detection and imaging of lipids of Scenedesmus obliquus based on confocal Raman microspectroscopy. Biotechnol Biofuels 10:300

    PubMed  PubMed Central  Google Scholar 

  • Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553

    CAS  Google Scholar 

  • Shuba ES, Kifle D (2018) Microalgae to biofuels: ‘promising’ alternative and renewable energy, review. Renew Sust Energ Rev 81:743–755

    CAS  Google Scholar 

  • Singh B, Guldhe A, Rawat A, Bux F (2014) Towards a sustainable approach for development of biodiesel from plant and microalgae. Bioresour Technol 102:57–70

    Google Scholar 

  • Sivaramakrishnan R, Incharoensakdi A (2017) Enhancement of total lipid yield by nitrogen, carbon, and iron supplementation in isolated microalgae. J Phycol 53:855–868

    CAS  PubMed  Google Scholar 

  • Søndergaard M (2009) Redox potential. In: Likens GE (ed) Encyclopedia of inland waters. Academic Press, Oxford, pp 852–859

    Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (Chroococcales). Bacteriol Rev 35:171–205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stephenson AL, Dennis JS, Howe CJ, Scott SA, Smith AG (2010) Influence of nitrogen-limitation regime on the production by Chlorella vulgaris of lipids for biodiesel feedstocks. Biofuels 1:47–58

    CAS  Google Scholar 

  • Sun X, Cao Y, Xu H, Liu Y, Sun JR, Qiao DR, Cao Y (2014) 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

    CAS  PubMed  Google Scholar 

  • Sunda WG, Price NM, Morel FMM (2005) Trace metal ion buffers and their use in culture studies. In: Andersen RA (ed) Algal culturing techniques. Elsevier, Amsterdam, pp 35–63

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Terauchi AM, Peers G, Kobayashi MC, Niyog KK, Merchant SS (2010) Trophic status of Chlamydomonas reinhardtii influences the impact of iron deficiency on photosynthesis. Photosynth Res 105:39–49

    CAS  PubMed  PubMed Central  Google Scholar 

  • Urzica EI, Vieler A, Hong-Hermesdorf A, Page MD, Casero D, Gallaher SD, Kropat J, Pellegrini M, Benning C, Merchant SS (2013) Remodeling of membrane lipids in iron-starved Chlamydomonas. J Biol Chem 288:30246–30258

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wan M, Jin X, Xia J, Rosenberg JN, Yu G, Nie Z, Oyler GA, Betenbaugh MJ (2014) The effect of iron on growth, lipid accumulation, and gene expression profile of the freshwater microalga Chlorella sorokiniana. Appl Microbiol Biotechnol 98:9473–9481

    CAS  PubMed  Google Scholar 

  • Wu H, Miao X (2014) Biodiesel quality and biochemical changes of microalgae Chlorella pyrenoidosa and Scenedesmus obliquus in response to nitrate levels. Bioresour Technol 170:421–427

    CAS  PubMed  Google Scholar 

  • Wu Y, Zhou S, Qin F, Zheng K, Ye X (2010) Modeling the oxidation kinetics of Fenton’s process on the degradation of humic acid. J Hazard Mater 179:533–539

    CAS  PubMed  Google Scholar 

  • Xu Y, Boeing WJ (2014) Modeling maximum lipid productivity of microalgae: review and next step. Renew Sust Energ Rev 32:29–39

    CAS  Google Scholar 

  • Yeesang C, Cheirsilp B (2011) Effect of nitrogen, salt, and iron content in the growth medium and light intensity on lipid production by microalgae isolated from freshwater sources in Thailand. Bioresour Technol 102:3034–3040

    CAS  PubMed  Google Scholar 

  • Zhao P, Gu W, Huang A, Wu S, Liu C, Huan L, Gao S, Xie X, Wa G (2018) Effect of iron on the growth of Phaeodactylum tricornutum via photosynthesis. J Phycol 54:34–43

    CAS  PubMed  Google Scholar 

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Rajabi Islami, H., Assareh, R. Effect of different iron concentrations on growth, lipid accumulation, and fatty acid profile for biodiesel production from Tetradesmus obliquus. J Appl Phycol 31, 3421–3432 (2019). https://doi.org/10.1007/s10811-019-01843-4

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