Abstract
Improving the competitiveness of biodiesel production by microalgae cultures requires the application of several strategies to obtain a high content of lipids, rapid biomass growth and a capacity to adapt to different kinds of environment, with the aim of using non-renewable nutrient sources. Therefore, the use of an individual indigenous microalgae strain or a consortium from natural or anthropogenic sites is now considered an alternative for biofuel production. This study examined the temporal behaviour of secondary metabolites produced by a native microalgae and yeast consortium isolated from wastewater, which was characterized by a genetic identification method based on the MiSeq system. The predominant species in the consortium was Scenedesmus obliquus, representing 68% of the organisms. In addition, the consortium contained a number of yeast species, including Candida pimensis (43%), Arthroderma vanbreuseghemii (23%), Diaporthe aspalathi/Diaporthe meridionalis (25%) and Hericium americanum (3%). This indigenous co-culture of microalgae and yeast showed biomass productivity of 0.06 g l−1 day−1, with a content of 30% (w/w) carbohydrates, 4% (w/w) proteins and 55% (w/w) lipids. Transesterification of the extracted lipids produced fatty acid methyl esters (FAMEs), which were analysed by gas chromatography (GC). The FAMEs included methyl pentadecanoate (1.90%), cis-10-pentanedecanoic acid methyl ester (1.36%), methyl palmitate (2.64%), methyl palmitoleate (21.36%), methyl oleate (64.95%), methyl linolenate (3.83%) and methyl linolelaidate (3.95%). This composition was relevant for biodiesel production based on the co-culture of indigenous microalgae and yeast consortia.
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Arora N, Patel A, Mehtani J, Pruthi PA, Pruthi V, Poluri KM (2019) Co-culturing of oleaginous microalgae and yeast: paradigm shift towards enhanced lipid productivity. Environ Sci Pollut Res Int 26:16952–16973
Bellou S, Baeshen MN, Elazzazy AM, Aggeli D, Sayegh F, Aggelis G (2014) Microalgal lipids biochemistry and biotechnological perspectives. Biotechnol Adv 32:1476–1493
Biller P, Ross AB (2014) Pyrolysis GC–MS as a novel analysis technique to determine the biochemical composition of microalgae. Algal Res 6:91–97
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
British Petroleum (2018) Renewable energy BP statistical review of world energy 2018. British Petroleum, London
Cai S, Hu C, Du S (2007) Comparisons of growth and biochemical composition between mixed culture of alga and yeast and monocultures. J Biosci Bioeng 104:391–397
Cheng J, Xu J, Huang Y, Li Y, Zhou J, Cen K (2015) Growth optimisation of microalga mutant at high CO2 concentration to purify undiluted anaerobic digestion effluent of swine manure. Bioresour Technol 177:240–246
Cho HU, Kim YM, Park JM (2017) Enhanced microalgal biomass and lipid production from a consortium of indigenous microalgae and bacteria present in municipal wastewater under gradually mixotrophic culture conditions. Bioresour Technol 228:290–297
Coates J (2000) Interpretation of infrared spectra, a practical approach. In: Meyers RA (ed) Encyclopedia of analytical chemistry. Wiley, Chichester, pp 10815–10837
Cuellar-Bermudez SP, Aleman-Nava GS, Chandra R, García-Perez JS, Contreras-Angulo JR, Markou G, Parra-Saldivar R (2017) Nutrients utilization and contaminants removal. A review of two approaches of algae and cyanobacteria in wastewater. Algal Res 24:438–449
Delrue F, Álvarez-Díaz PD, Fon-Sing S, Fleury G, Sassi JF (2016) The environmental biorefinery: using microalgae to remediate wastewater, a win-win paradigm. Energies 9:132
Demirbas A, Demirbas MF (2010) Algae energy: algae as a new source of biodiesel. Springer, London
Demirbas A, Fatih Demirbas M (2011) Importance of algae oil as a source of biodiesel. Energy Convers Manag 52:163–170
Deng XY, Gao K, Zhang RC, Addy M, Lu Q, Ren HY, Chen P, Liu YH, Ruan R (2017) Growing Chlorella vulgaris on thermophilic anaerobic digestion swine manure for nutrient removal and biomass production. Bioresour Technol 243:417–425
DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Feng P, Yang K, Xu Z, Wang Z, Fan L, Qin L, Zhu S, Shang C, Chai P, Yuan Z, Hu L (2014) Growth and lipid accumulation characteristics of Scenedesmus obliquus in semi-continuous cultivation outdoors for biodiesel feedstock production. Bioresour Technol 173:406–414
Forfang K, Zimmermann B, Kosa G, Kohler A, Shapaval V (2017) FTIR spectroscopy for evaluation and Mmonitoring of lipid extraction efficiency for oleaginous fungi. PLoS One 12:e0170611
Gour RS, Chawla A, Singh H, Chauhan RS, Kant A (2016) Characterization and screening of native Scenedesmus sp. isolates suitable for biofuel feedstock. PLoS One 11:e0155321
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
Gupta J, Agarwal M, Dalai AK (2016) Optimization of biodiesel production from mixture of edible and nonedible vegetable oils. Biocatal Agric Biotechnol 8:112–120
He Q, Yang H, Hu C (2016) Culture modes and financial evaluation of two oleaginous microalgae for biodiesel production in desert area with open raceway pond. Bioresour Technol 218:571–579
Henry EC (2004) Handbook of microalgal culture: biotechnology and applied phycology. J Phycol 40:1001–1002
Jazzar S, Quesada-Medina J, Olivares-Carrillo P, Marzouki MN, Acién-Fernández FG, Fernández-Sevilla JM, Molina-Grima E, Smaali I (2015) A whole biodiesel conversion process combining isolation, cultivation and in situ supercritical methanol transesterification of native microalgae. Bioresour Technol 190:281–288
Kim GY, Yun YM, Shin HS, Han JI (2017) Cultivation of four microalgae species in the effluent of anaerobic digester for biodiesel production. Bioresour Technol 224:738–742
Knothe G (2005) Dependence of biodiesel fuel properties on the structure of fatty acid alkyl esters. Fuel Process Technol 86:1059–1070
Knothe G (2008) “Designer” biodiesel: optimizing fatty ester composition to improve fuel properties. Energy Fuel 22:1358–1364
Komolafe O, Velasquez Orta SB, Monje-Ramirez I, Yáñez Noguez I, Harvey AP, Orta Ledesma MT (2014) Biodiesel production from indigenous microalgae grown in wastewater. Bioresour Technol 154:297–304
Lananan F, Hamid SHA, Din WNS, Khatoon H, Jusoh A, Endut A (2014) Symbiotic bioremediation of aquaculture wastewater in reducing ammonia and phosphorus utilizing effective microorganism (EM-1) and microalgae (Chlorella sp.). Int Biodeterior Biodegrad 95:127–134
Levine RB, Costanza-Robinson MS, Spatafora GA (2011) Neochloris oleoabundans grown on anaerobically digested dairy manure for concomitant nutrient removal and biodiesel feedstock production. Biomass Bioenergy 35:40–49
Ling Y, Sun L, Wang S, Lin CSK, Sun Z, Zhou Z (2019) Cultivation of oleaginous microalga Scenedesmus obliquus coupled with wastewater treatment for enhanced biomass and lipid production. Biochem Eng J 148:162–169
Liu F, Monroe E, Davis RW (2019) Engineering microbial consortia for bioconversion of multisubstrate biomass streams to biofuels. In: Al Qubeissi M (ed) Biofuels - challenges and opportunities. IntechOpen, London
Mandal S, Mallick N (2009) Microalga Scenedesmus obliquus as a potential source for biodiesel production. Appl Microbiol Biotechnol 84:281–291
Martinez-Silveira A, Villarreal R, Garmendia G, Rufo C, Vero S (2019) Process conditions for a rapid in situ transesterification for biodiesel production from oleaginous yeasts. Electron J Biotechnol 38:1–9
Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energ Rev 14:217–232
Mayers JJ, Flynn KJ, Shields RJ (2013) Rapid determination of bulk microalgal biochemical composition by Fourier-transform infrared spectroscopy. Bioresour Technol 148:215–220
McGinn PJ, Dickinson KE, Park KC et al (2012) Assessment of the bioenergy and bioremediation potentials of the microalga Scenedesmus sp. AMDD cultivated in municipal wastewater effluent in batch and continuous mode. Algal Res 1:155–165
Milano J, Ong HC, Masjuki HH, Chong WT, Lam MK, Loh PK, Vellayan V (2016) Microalgae biofuels as an alternative to fossil fuel for power generation. Renew Sust Energ Rev 58:180–197
Moser BR (2014) Impact of fatty ester composition on low temperature properties of biodiesel-petroleum diesel blends. Fuel 115:500–506
Muradov N, Taha M, Miranda AF, Wrede D, Kadali K, Gujar A, Stevenson T, Ball AS, Mouradov A (2015) Fungal-assisted algal flocculation: application in wastewater treatment and biofuel production. Biotechnol Biofuels 8:24
Myerson AL (1954) Algal culture: from laboratory to pilot plant. J Frankl Inst 257:147
Olguín EJ (2012) Dual purpose microalgae-bacteria-based systems that treat wastewater and produce biodiesel and chemical products within a biorefinery. Biotechnol Adv 30:1031–1046
Piligaev AV, Sorokina KN, Bryanskaya AV, Peltek SE, Kolchanov NA, Parmon VN (2015) Isolation of prospective microalgal strains with high saturated fatty acid content for biofuel production. Algal Res 12:368–376
Prajapati SK, Kumar P, Malik A, Vijay VK (2014) Bioconversion of algae to methane and subsequent utilization of digestate for algae cultivation: a closed loop bioenergy generation process. Bioresour Technol 158:174–180
Ramos MJ, Fernández CM, Casas A, Rodriguez L, Pérez A (2009) Influence of fatty acid composition of raw materials on biodiesel properties. Bioresour Technol 100:261–268
Rea G, Antonacci A, Lambreva MD, Mattoo AK (2018) Features of cues and processes during chloroplast-mediated retrograde signaling in the alga Chlamydomonas. Plant Sci 272:193–206
Rohman A, Che Man YB (2010) Fourier transform infrared (FTIR) spectroscopy for analysis of extra virgin olive oil adulterated with palm oil. Food Res Int 43:886–892
Salama ES, Kurade MB, Abou-Shanab RA, El-Dalatony MM, Yang IS, Min B, Jeon BH (2017) Recent progress in microalgal biomass production coupled with wastewater treatment for biofuel generation. Renew Sust Energ Rev 79:1189–1211
Schulze C, Reinhardt J, Wurster M, Ortiz-Tena JG, Sieber V, Mundt S (2016) A one-stage cultivation process for lipid- and carbohydrate-rich biomass of Scenedesmus obtusiusculus based on artificial and natural water sources. Bioresour Technol 218:498–504
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
Shen QH, Jiang JW, Chen LP, Cheng LH, Xu XH, Chen HL (2015) Effect of carbon source on biomass growth and nutrients removal of Scenedesmus obliquus for wastewater advanced treatment and lipid production. Bioresour Technol 190:257–263
Shin DY, Cho HU, Utomo JC, Choi YN, Xu X, Park JM (2015) Biodiesel production from Scenedesmus bijuga grown in anaerobically digested food wastewater effluent. Bioresour Technol 184:215–221
Show PL, Tang MSY, Nagarajan D, Ling TC, Ooi CW, Chang JS (2017) A holistic approach to managing microalgae for biofuel applications. Int J Mol Sci 18:215
Shuba ES, Kifle D (2018) Microaglae to biofuels: 'promising' alternative and renewable energy, review. Renew Sust Energ Rev 81:743–755
Singh P, Guldhe A, Kumari S, Rawat I, Bux F (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
Tao R, Lakaniemi AM, Rintala JA (2017) Cultivation of Scenedesmus acuminatus in different liquid digestates from anaerobic digestion of pulp and paper industry biosludge. Bioresour Technol 245:706–713
Timmins M, Thomas-Hall SR, Darling A, Zhang E, Hankamer B, Marx UC, Schenk PM (2009) Phylogenetic and molecular analysis of hydrogen-producing green algae. J Exp Bot 60:1691–1702
Wang L, Li Y, Chen P, Min M, Chen Y, Zhu J, Ruan RR (2010) Anaerobic digested dairy manure as a nutrient supplement for cultivation of oil-rich green microalgae Chlorella sp. Bioresour Technol 101:2623–2628
Wang R, Tian Y, Xue S, Zhang D, Zhang Q, Wu X, Kong D, Cong W (2016) Enhanced microalgal biomass and lipid production via co-culture of Scenedesmus obliquus and Candida tropicalis in an autotrophic system. J Chem Technol Biotechnol 91:1387–1396
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
Youssef M, Valdez-Ojeda R, Ku-Cauich JR, Escobedo-GraciaMedrano RM (2015) Enhanced protocol for isolation of plant genomic DNA. J Agric Environ Sci 4:172–180
Zhang C, Zhang Y, Zhuang B, Zhou X (2014) Strategic enhancement of algal biomass, nutrient uptake and lipid through statistical optimization of nutrient supplementation in coupling Scenedesmus obliquus-like microalgae cultivation and municipal wastewater treatment. Bioresour Technol 171:71–79
Acknowledgements
We give special acknowledgements to the Laboratorio Nacional de Desarrollo y Aseguramiento de la Calidad de Biocombustibles (LaNDACBio) and Centro de Innovación en Insumos para Bioenergéticos y Co-productos (CIBIOC) for allowing the use of laboratory infrastructure.
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This research was financially supported by CONACYT-Project No. 255107 and SIP-IPN multidisciplinary Project No. 2019-2011-SIP-20195299.
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Suastes-Rivas, J.K., Hernández-Altamirano, R., Mena-Cervantes, V.Y. et al. Efficient production of fatty acid methyl esters by a wastewater-isolated microalgae-yeast co-culture. Environ Sci Pollut Res 27, 28490–28499 (2020). https://doi.org/10.1007/s11356-019-07286-1
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DOI: https://doi.org/10.1007/s11356-019-07286-1