Enhacment of biomass, carbohydrates, lipids, and proteins content using co-culture of Glagah consortium and Lipomyces starkeyi
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Abstract
Microorganisms have a high potential as biofuel sources. Co-culture of microalgae and yeasts can result in high lipid production as a modification treatment. The goal of this study was to see how the co-culture of the Glagah consortium (diversity of associated microalgae and bacteria from Glagah Lagoon, Yogyakarta) and Lipomyces starkeyi affected the production of biomass, lipids, proteins, and carbohydrates. The culture was performed under airtight conditions on a shaker at 127 rpm, with a light intensity of 27.75 mol/m2/s and a temperature of 30°C. The culture was subjected to a dark: light (6:18) treatment. Biomass was measured by dry weight, lipids by the Bligh and Dyer method, proteins by the Bradford method and carbohydrates by the phenol-sulfuric acid method. On day 3, L. starkey culture produced the most biomass, yielding 2.21 g/L with a productivity of 0.49 g/L/day. On day 4, the highest lipids produced from co-culture treatment yielded 1.03 g/g with a productivity of 0.21 g/L/day. The highest protein yield was obtained from L. starkeyi culture treatment on day 4, yielding 0.60 g/g with a productivity of 0.12 g/L/day. On day 6, co-culture produced the total carbohydrates, yielding 4.78 g/g with a productivity of 0.68 g/L/day. The co-culture treatment produced the highest lipids and carbohydrates production (1.03 g/g and 4.78 g/g) and productivity (0.21 g/L/day and 0.68 g/L/day), while L. starkeyi culture produced the highest total biomass and protein production (2.21 g/L and 0.6 g/g) and productivity (0.49 g\L\day and 0.12 g/L/day). In microalgae culture, CO2 generally given directly through the aeration process. In this study, the source of CO2 was yeast, whereas yeast also obtained O2 from microalgae in the consortium for their metabolic process. This mutualism symbiosis will help in providing benefits in reducing the costs for the cultivation process, especially in optimizing the production of biomass an lipids.
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Keywords
Biomass, Carbohydrates, Co-culture, Glagah consortium, Lipids, Lipomyces starkeyi, Primary metabolites, Proteins
References
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Aresta, M. & Dibendettp, A. (2019). Bioenergy with carbon capture and storage: bioenergy with carbon capture and storage (pp 173-193). Academic Press, Cambridge
Rakesh, S. & Karthikeyan, S. (2019). Co-cultivation of microalgae with oleaginous yeast for economical biofuel production. Journal of Farm Sciences, 32(2), 125-130. doi.org/10.13140/RG.2.2.10506.41928
Arora, N., Patel, A., Mehtani, J., Pruthi, P.A., Pruthi, V. & Poluri, K.M. (2019). Co-culturing of oleaginous microalgae and yeast: paradigm shift towards enhanced lipid productivity. Environmental Science and Pollution Research, 26(17), 16952-16973. doi.org/10.1007/s11356-019-05138-6
Bashir, K.M.I., Mansoor, S., Kim, N.R., Grohmann, F.R., Shah, A.A. & Cho, M.G. (2019). Effect of organic carbon sources and environmental factors on cell growth and lipid content of Pavlolva lutheri. Annals of Microbiology, 69(2019), 353-368. doi.org/10.1007/s13213-018-1423-2
Bligh, E.G. & Dyer, W.J. (1959). A Rapid method for total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8), (912-917). https://doi.org/10.1139/o59-099
Bonturi, N., Matsakas, L., Nilsson, R., Christakopoulus. P., Miranda, E.A., Berglund, K.A. & Rova, U. (2015). Single cell oil producing yeasts Lipomyces starkeyi and Rhodosporidium toruloides: selection of extraction strategies and biodiesel property prediction. Energies, 8(6), 5040-5052. doi.org/10.3390/en8065040
Cai, S., Hu, C. & Du, S. (2007). Comparisons of growth and biochemical composition between mixed culture of alga and yeast and monocultures. Journal of Bioscience and Bioengineering, 104(5), 391-397. doi.org/10.1263/jbb.104.391
Cheirsilp, B., Kitcha, S. & Torpee, S. (2011). Co-culture of an oleganious yeast Rhodoturula glutinis and a microalga Chlorella vulgaris for biomass and lipid production using pure and crude glycerol as a sole carbon source. Annals of Microbiology, 62(2012), 987-993. doi.org/ 10.1007/s13213-011-0338-y
Cheirsilp, B., Suwarannat, W. & Niyomdecha, R. (2011). Mixed culture of oleaginous yeast Rhodoturula glutinis and microalga Chlorella vulgaris for lipid production from industrial wastes and its use as biodiesel feedstock. New Biotechnology, 28(4), 362-368. doi.org/ 10.1016/j.nbt.2011.01.004
Griffths, M.J. & Harrison, S.T.L. (2009). Lipid productivity as a key characteristic for choosing algal species for biodiesel production. Journal of Applied Phycology, 21(2009), 493-507. doi.org/10.1007/s10811-008-9392-7
Hayes, M., Skomedal, H., Skjanes, K., Mazur-Marzec, H., Torunska-Sitarz, A., Catala, M., Hosoglu, M.I. & Garcia-Vaquero, M. (2017). Microalgae-based biofuels and bioproducts (pp 347-368). Woodhead publishers . Elesevier, Cambridge
Jiang, X., Liu, L., Chen J. & Wei, D. (2018). Effects of Xanthophyllomyces dendrohous on cell growth, lipid, and astaxanthin production of Chromochloris zofingiensis by mixed culture strategy. Journal Applied Phycology, 30(2008), 3009-3015. doi.org/10.1007/s10811-018-1553-8
Kitcha, S. & Cheirsilp, B. (2014). Enhanced lipid production by co-cultivation and co-encapsulation of oleaginous yeast Trichosporonoides spathulate with microalgae in alginate gel bead. Applied Biochemistry and Biotechnology, 173(2), 522-534. doi.org/10.1007/s12010-014-0859-5
Knothe, G., Krahl, J. & Jerpen, G.V. (2010). The Biodiesel Handbook (pp 1-3). AOCS Press, Urbana
Krishnan, V., Uemura, Y., Thanh, N.T., Khalid, N.A., Osman, N. & Mansor, N. (2015). Three types of marine microalge and Nannochloropsis oculate cultivation for potential source of biomass production, Journal of Physics, 622(2015), 1-7. doi.org/10.1088/1742-6596/622/1/012034
Kwak, H.S., Kim, J.Y.H., Woo, H.M., Jin, E.S., Min, B.K. & Sim, S.J. (2016). Synergistic effect of multiple stress conditions for improving microalgal lipid production. Algal Research, 19(2016), 215-224. doi.org/10.1016/j.algal.2016.09.003
Markou, G., Angelidaki, I. & Georgakakis, D. (2012). Microalgal carbohydrates: An overview of the factors influencing carbohydrates production, and of main bioconversion technologies for production of biofuels. Applied Microbiology and Biotechnology, 96(3), 631-45. doi.org/10.1007/s00253-012-4398-0
Mcneil, B.A. & Stuart, D.T. (2018). Lipomyces starkeyi: an emerging cell factory for production of lipids, oleochemicals and biotechnology applications. World Journal of Microbiology and Biotechnology, 34(10): 147. doi.org/10.1007/s11274-018-2532-6
Moscoso, J.LG., Obied, W., Kumar, S. & Hatcher, P.G. (2013). Flash hydrolysis of microalgae (Scenedesmus sp.) for protein extraction and production of biofuels intermediates. The Journal of Supercritical Fluids, 82(2013), 183-190. doi.org/10.1016/j.supflu.2013.07.012
Nielsen, S.S. (2009). Phenol-Sulfuric Acid Method for Total Carbohydrates (pp 47-53). Springer, Berlin
Pedro, I.S.H. (2015). Evaluation of photoperiod effect on the growth and protein content of microalgae (p 4). Ines Soraia Hipolito Pedro, Leiria
Pradana, Y.S., Sudibyom H., Suyono, A.E., Indarto & Budiman, A. (2017). Oil algae extraction of selected microalgae species grown in monoculture and mixed cultures for biodiesel production. Energy Procedia, 105(2017), 277-282. doi.org/10.1016/j.egypro.2017.03.314
Prasad M.N.V. & Shih, K. 2016. Environmental materials and waste: resource recovery and pollution prevention (pp 179-212). Elsevier, London
Putra, I.K.R.W., Anggreni, A.A.M.D. & Arnata, I.W. (2015). Pengaruh jenis media terhadap konsentrasi biomassa dan klorofil mikroalga Tetraselmis chuii. Jurnal Rekayasa dan Manajemen Agroindustri, 3(2), 40-46. (in Indonesia)
Safi, C., Charton M., Ursu A.V., Laroche C., Zebib B., Pontalier P.Y. & Vaca-Garcia C. (2014). Release of hydro-soluble microalgal proteins using mechanical and chemical treatments. Algal Research, 3(2014), 55-60. doi.org/10.1016/j.algal.2013.11.017
Sharma, K.K., Schuhmann, H. & Schenk, P.M. (2012). High lipid induction in microalgae for biodiesel production. Energies, 5(5), 1532-1553. doi.org/10.3390/en5051532
Shu, C.H., Tsai, C.C., Chen, K.Y., Liao, W.H. & Huang, H.C. (2013). Enhancing high quality oil accumulation and CO2 fixation by a mixed culture of Chlorella sp. and Saccharomyces cerevisiae. Journal of the Taiwan Institute of Chemical Engineers, 44(6), 936-942. doi.org/10.1016/j.jtice.2013.04.001
Sudibyo, H., Yano, S.P. Samudra, T.T., Budiman, A., Indarto & Suyono, E.A. (2017). Study of cultivation under different colors of light and growth kinetic study of Chlorella zofinginesis Donz for biofuel production. Energy Procedia, 105(2017), 270-276. doi.org/10.1016/j.egypr o.2017.0 3.313
Suyono, E.A., Fahrunnida, Nopitasari, A. & Utama, I.V. (2016). Identification of microalgae species and lipid profiling of glagah consortium for biodiesel development from local marine resource. ARPN Journal of Engineering and Applied Sciences, 11(16), 9970-9973
Suyono, E.A., Haryadi, W., Zusron, M., Nuhamunada, M., Rahayu, S. & Nugroho, A.P. (2015). The effect of salinity on growth, dry weight and lipid content of the mixed microalgae culture isolated from glagah as biodiesel substrate. Journal of Life Sciences, 9(2015), 229-233. doi.org/10.17265/1934-7391/2015.05.006
Taiz, L. & Zeiger,E. (2010). Plant Physiology 5th edn (p 201). Sinauer Associated Inc, Los Angeles
Turcotte, B., Liang, X.B., Robert, F. & Soontorngun, N. (2010.) Transcriptional regulation of nonfermentable carbon utilization in budding yeast. FEMS Yeast Research, 10(1), 2-13. doi.org/10.1111/j.1567-1364.2009.00555.x
Walker, John M. (2002). The Protein Protocols Handbook (pp 15-21). Humana Press, New Jersey
Winasti, N.M.S. (2021). Ko-kultur Konsorsium Glagah dan Lipomyces starkeyi untuk Optimasi Produksi Biomassa, Lipid, Protein dan Karbohidrat (pp 36-43). UGM Library, Yogyakarta
Yen, H.W., Chen, P.W. & Chen, L.J. (2015). The synergistic effects for the co-cultivation of oleaginous yeast Rhodoturula glutinis and microalgae-Scenedesmus obliquus on the biomass and total lipids accumulation. Bioresource Technology, 184(2015), 148-152. doi.org/10.1016/j.biortech.2014.09.113
Zhang, Z., Ji, H., Gong, G., Zhang, X. & Tan, T. (2014). Synergistic effects of oleaginous yeast Rhodoturula glutinis and microalga Chlorella vulgaris for enchanement of biomass and lipid yields. Bioresource Technology, 164(2014), 93-99. doi.org/10.1016/j.biortech.2014.04.039
Zuccaro, G., Mondo A.d., Pinto, G., Polio, A. & Natale, A.D. (2021). Biorefinery-based approach to exploit mixed cultures of Lipomyces starkeyi and Chlororidium saccharophilum for single cell oil production. Energies, 14(5), 1-22. doi.org/10.3390/en14051340
Zullaikah S., Utomo A.T., Yasmin M., Ong L.K & Ju Y.H. (2018). Advances in eco-fuels for a sustainable environment (pp 237-276). Woodhead Publishing Series in Energy, Cambridge
Aresta, M. & Dibendettp, A. (2019). Bioenergy with carbon capture and storage: bioenergy with carbon capture and storage (pp 173-193). Academic Press, Cambridge
Rakesh, S. & Karthikeyan, S. (2019). Co-cultivation of microalgae with oleaginous yeast for economical biofuel production. Journal of Farm Sciences, 32(2), 125-130. doi.org/10.13140/RG.2.2.10506.41928
Arora, N., Patel, A., Mehtani, J., Pruthi, P.A., Pruthi, V. & Poluri, K.M. (2019). Co-culturing of oleaginous microalgae and yeast: paradigm shift towards enhanced lipid productivity. Environmental Science and Pollution Research, 26(17), 16952-16973. doi.org/10.1007/s11356-019-05138-6
Bashir, K.M.I., Mansoor, S., Kim, N.R., Grohmann, F.R., Shah, A.A. & Cho, M.G. (2019). Effect of organic carbon sources and environmental factors on cell growth and lipid content of Pavlolva lutheri. Annals of Microbiology, 69(2019), 353-368. doi.org/10.1007/s13213-018-1423-2
Bligh, E.G. & Dyer, W.J. (1959). A Rapid method for total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8), (912-917). https://doi.org/10.1139/o59-099
Bonturi, N., Matsakas, L., Nilsson, R., Christakopoulus. P., Miranda, E.A., Berglund, K.A. & Rova, U. (2015). Single cell oil producing yeasts Lipomyces starkeyi and Rhodosporidium toruloides: selection of extraction strategies and biodiesel property prediction. Energies, 8(6), 5040-5052. doi.org/10.3390/en8065040
Cai, S., Hu, C. & Du, S. (2007). Comparisons of growth and biochemical composition between mixed culture of alga and yeast and monocultures. Journal of Bioscience and Bioengineering, 104(5), 391-397. doi.org/10.1263/jbb.104.391
Cheirsilp, B., Kitcha, S. & Torpee, S. (2011). Co-culture of an oleganious yeast Rhodoturula glutinis and a microalga Chlorella vulgaris for biomass and lipid production using pure and crude glycerol as a sole carbon source. Annals of Microbiology, 62(2012), 987-993. doi.org/ 10.1007/s13213-011-0338-y
Cheirsilp, B., Suwarannat, W. & Niyomdecha, R. (2011). Mixed culture of oleaginous yeast Rhodoturula glutinis and microalga Chlorella vulgaris for lipid production from industrial wastes and its use as biodiesel feedstock. New Biotechnology, 28(4), 362-368. doi.org/ 10.1016/j.nbt.2011.01.004
Griffths, M.J. & Harrison, S.T.L. (2009). Lipid productivity as a key characteristic for choosing algal species for biodiesel production. Journal of Applied Phycology, 21(2009), 493-507. doi.org/10.1007/s10811-008-9392-7
Hayes, M., Skomedal, H., Skjanes, K., Mazur-Marzec, H., Torunska-Sitarz, A., Catala, M., Hosoglu, M.I. & Garcia-Vaquero, M. (2017). Microalgae-based biofuels and bioproducts (pp 347-368). Woodhead publishers . Elesevier, Cambridge
Jiang, X., Liu, L., Chen J. & Wei, D. (2018). Effects of Xanthophyllomyces dendrohous on cell growth, lipid, and astaxanthin production of Chromochloris zofingiensis by mixed culture strategy. Journal Applied Phycology, 30(2008), 3009-3015. doi.org/10.1007/s10811-018-1553-8
Kitcha, S. & Cheirsilp, B. (2014). Enhanced lipid production by co-cultivation and co-encapsulation of oleaginous yeast Trichosporonoides spathulate with microalgae in alginate gel bead. Applied Biochemistry and Biotechnology, 173(2), 522-534. doi.org/10.1007/s12010-014-0859-5
Knothe, G., Krahl, J. & Jerpen, G.V. (2010). The Biodiesel Handbook (pp 1-3). AOCS Press, Urbana
Krishnan, V., Uemura, Y., Thanh, N.T., Khalid, N.A., Osman, N. & Mansor, N. (2015). Three types of marine microalge and Nannochloropsis oculate cultivation for potential source of biomass production, Journal of Physics, 622(2015), 1-7. doi.org/10.1088/1742-6596/622/1/012034
Kwak, H.S., Kim, J.Y.H., Woo, H.M., Jin, E.S., Min, B.K. & Sim, S.J. (2016). Synergistic effect of multiple stress conditions for improving microalgal lipid production. Algal Research, 19(2016), 215-224. doi.org/10.1016/j.algal.2016.09.003
Markou, G., Angelidaki, I. & Georgakakis, D. (2012). Microalgal carbohydrates: An overview of the factors influencing carbohydrates production, and of main bioconversion technologies for production of biofuels. Applied Microbiology and Biotechnology, 96(3), 631-45. doi.org/10.1007/s00253-012-4398-0
Mcneil, B.A. & Stuart, D.T. (2018). Lipomyces starkeyi: an emerging cell factory for production of lipids, oleochemicals and biotechnology applications. World Journal of Microbiology and Biotechnology, 34(10): 147. doi.org/10.1007/s11274-018-2532-6
Moscoso, J.LG., Obied, W., Kumar, S. & Hatcher, P.G. (2013). Flash hydrolysis of microalgae (Scenedesmus sp.) for protein extraction and production of biofuels intermediates. The Journal of Supercritical Fluids, 82(2013), 183-190. doi.org/10.1016/j.supflu.2013.07.012
Nielsen, S.S. (2009). Phenol-Sulfuric Acid Method for Total Carbohydrates (pp 47-53). Springer, Berlin
Pedro, I.S.H. (2015). Evaluation of photoperiod effect on the growth and protein content of microalgae (p 4). Ines Soraia Hipolito Pedro, Leiria
Pradana, Y.S., Sudibyom H., Suyono, A.E., Indarto & Budiman, A. (2017). Oil algae extraction of selected microalgae species grown in monoculture and mixed cultures for biodiesel production. Energy Procedia, 105(2017), 277-282. doi.org/10.1016/j.egypro.2017.03.314
Prasad M.N.V. & Shih, K. 2016. Environmental materials and waste: resource recovery and pollution prevention (pp 179-212). Elsevier, London
Putra, I.K.R.W., Anggreni, A.A.M.D. & Arnata, I.W. (2015). Pengaruh jenis media terhadap konsentrasi biomassa dan klorofil mikroalga Tetraselmis chuii. Jurnal Rekayasa dan Manajemen Agroindustri, 3(2), 40-46. (in Indonesia)
Safi, C., Charton M., Ursu A.V., Laroche C., Zebib B., Pontalier P.Y. & Vaca-Garcia C. (2014). Release of hydro-soluble microalgal proteins using mechanical and chemical treatments. Algal Research, 3(2014), 55-60. doi.org/10.1016/j.algal.2013.11.017
Sharma, K.K., Schuhmann, H. & Schenk, P.M. (2012). High lipid induction in microalgae for biodiesel production. Energies, 5(5), 1532-1553. doi.org/10.3390/en5051532
Shu, C.H., Tsai, C.C., Chen, K.Y., Liao, W.H. & Huang, H.C. (2013). Enhancing high quality oil accumulation and CO2 fixation by a mixed culture of Chlorella sp. and Saccharomyces cerevisiae. Journal of the Taiwan Institute of Chemical Engineers, 44(6), 936-942. doi.org/10.1016/j.jtice.2013.04.001
Sudibyo, H., Yano, S.P. Samudra, T.T., Budiman, A., Indarto & Suyono, E.A. (2017). Study of cultivation under different colors of light and growth kinetic study of Chlorella zofinginesis Donz for biofuel production. Energy Procedia, 105(2017), 270-276. doi.org/10.1016/j.egypr o.2017.0 3.313
Suyono, E.A., Fahrunnida, Nopitasari, A. & Utama, I.V. (2016). Identification of microalgae species and lipid profiling of glagah consortium for biodiesel development from local marine resource. ARPN Journal of Engineering and Applied Sciences, 11(16), 9970-9973
Suyono, E.A., Haryadi, W., Zusron, M., Nuhamunada, M., Rahayu, S. & Nugroho, A.P. (2015). The effect of salinity on growth, dry weight and lipid content of the mixed microalgae culture isolated from glagah as biodiesel substrate. Journal of Life Sciences, 9(2015), 229-233. doi.org/10.17265/1934-7391/2015.05.006
Taiz, L. & Zeiger,E. (2010). Plant Physiology 5th edn (p 201). Sinauer Associated Inc, Los Angeles
Turcotte, B., Liang, X.B., Robert, F. & Soontorngun, N. (2010.) Transcriptional regulation of nonfermentable carbon utilization in budding yeast. FEMS Yeast Research, 10(1), 2-13. doi.org/10.1111/j.1567-1364.2009.00555.x
Walker, John M. (2002). The Protein Protocols Handbook (pp 15-21). Humana Press, New Jersey
Winasti, N.M.S. (2021). Ko-kultur Konsorsium Glagah dan Lipomyces starkeyi untuk Optimasi Produksi Biomassa, Lipid, Protein dan Karbohidrat (pp 36-43). UGM Library, Yogyakarta
Yen, H.W., Chen, P.W. & Chen, L.J. (2015). The synergistic effects for the co-cultivation of oleaginous yeast Rhodoturula glutinis and microalgae-Scenedesmus obliquus on the biomass and total lipids accumulation. Bioresource Technology, 184(2015), 148-152. doi.org/10.1016/j.biortech.2014.09.113
Zhang, Z., Ji, H., Gong, G., Zhang, X. & Tan, T. (2014). Synergistic effects of oleaginous yeast Rhodoturula glutinis and microalga Chlorella vulgaris for enchanement of biomass and lipid yields. Bioresource Technology, 164(2014), 93-99. doi.org/10.1016/j.biortech.2014.04.039
Zuccaro, G., Mondo A.d., Pinto, G., Polio, A. & Natale, A.D. (2021). Biorefinery-based approach to exploit mixed cultures of Lipomyces starkeyi and Chlororidium saccharophilum for single cell oil production. Energies, 14(5), 1-22. doi.org/10.3390/en14051340
Zullaikah S., Utomo A.T., Yasmin M., Ong L.K & Ju Y.H. (2018). Advances in eco-fuels for a sustainable environment (pp 237-276). Woodhead Publishing Series in Energy, Cambridge
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Enhacment of biomass, carbohydrates, lipids, and proteins content using co-culture of Glagah consortium and Lipomyces starkeyi. (2023). Journal of Applied and Natural Science, 15(1), 15-22. https://doi.org/10.31018/jans.v15i1.4018
