Abstract
Microbial biomass which mostly generated from the microbial processes of bacteria, yeasts, and microalgae is an important resource. Recent concerns in microbial biomass production field, especially microbial lipid production for biofuel, have been focused towards the mixed culture of microalgae and yeast. To more comprehensive understanding of the mixed culture for microbial biomass, mono Chlorella pyrenoidosa, mono Yarrowia lipolytica and the mixed culture were investigated in the present work. Results showed that the mixed culture achieved significantly faster cell propagation of microalga and yeast, smaller individual cell size of yeast and higher relative chlorophyll content of microalga. The mixed culture facilitated the assimilation of carbon and nitrogen and drove the carbon flow to carbohydrate. Besides higher lipid yield (0.77 g/L), higher yields of carbohydrates (1.82 g/L), protein (1.99 g/L) and heating value (114.64 kJ/L) indicated the microbial biomass harvested from the mixed culture have more potential utilization in renewable energy, feedstuff, and chemical industry.
Similar content being viewed by others
References
Guccione A, Biondi N, Sampietro G, Rodolfi L, Bassi N, Tredici MR (2014) Chlorella for protein and biofuels: from strain selection to outdoor cultivation in a Green Wall Panel photobioreactor. Biotechnol Biofuels 7:84
Ledesma-Amaro R, Nicaud JM (2016) Yarrowia lipolytica as a biotechnological chassis to produce usual and unusual fatty acids. Prog Lipid Res 61:40–50
Rywinska A, Juszczyk P, Wojtatowicz M, Robak M, Lazar Z, Tomaszewska L, Rymowicz W (2013) Glycerol as a promising substrate for Yarrowia lipolytica biotechnological applications. Biomass Bioenerg 48:148–166
Rywinska A, Rymowicz W, Zarowska B, Skrzypinski A (2010) Comparison of citric acid production from glycerol and glucose by different strains of Yarrowia lipolytica. World J Microbiol Biotechnol 26(7):1217–1224
Barth G, Gaillardin C (1997) Physiology and genetics of the dimorphic fungus Yarrowia lipolytica. FEMS Microbiol Rev 19(4):219–237
Cheirsilp B, Suwannarat W, Niyomdecha R (2011) Mixed culture of oleaginous yeast Rhodotorula glutinis and microalga Chlorella vulgaris for lipid production from industrial wastes and its use as biodiesel feedstock. N Biotechnol 28(4):362–368
Cheirsilp B, Kitcha S, Torpee S (2012) Co-culture of an oleaginous yeast Rhodotorula glutinis and a microalga Chlorella vulgaris for biomass and lipid production using pure and crude glycerol as a sole carbon source. Ann Microbiol 62(3):987–993
Xue F, Miao J, Zhang X, Tan T (2010) A new strategy for lipid production by mix cultivation of Spirulina platensis and Rhodotorula glutinis. Appl Biochem Biotechnol 160(2):498–503
Ling J, Nip S, Cheok WL, de Toledo RA, Shim H (2014) Lipid production by a mixed culture of oleaginous yeast and microalga from distillery and domestic mixed wastewater. Bioresour Technol 173:132–139
Santos CA, Ferreira ME, da Silva TL, Gouveia L, Novais JM, Reis A (2011) A symbiotic gas exchange between bioreactors enhances microalgal biomass and lipid productivities: taking advantage of complementary nutritional modes. J Ind Microbiol Biotechnol 38(8):909–917
Yen HW, Chen PW, Chen LJ (2015) The synergistic effects for the co-cultivation of oleaginous yeast-Rhodotorula glutinis and microalgae-Scenedesmus obliquus on the biomass and total lipids accumulation. Bioresour Technol 184:148–152
Budhi S, Mukarakate C, Iisa K, Pylypenko S, Ciesielski PN, Yung MM, Donohoe BS, Katahira R, Nimlos MR, Trewyn BG (2015) Molybdenum incorporated mesoporous silica catalyst for production of biofuels and value-added chemicals via catalytic fast pyrolysis. Green Chem 17(5):3035–3046
Zhang Z, Ji H, Gong G, Zhang X, Tan T (2014) Synergistic effects of oleaginous yeast Rhodotorula glutinis and microalga Chlorella vulgaris for enhancement of biomass and lipid yields. Bioresour Technol 164:93–99
Tzur A, Moore JK, Jorgensen P, Shapiro HM, Kirschner MW (2011) Optimizing optical flow cytometry for cell volume-based sorting and analysis. PloS One 6:1
Borcier E, Morvezen R, Boudry P, Miner P, Charrier G, Laroche J, Hegaret H (2017) Effects of bioactive extracellular compounds and paralytic shellfish toxins produced by Alexandrium minutum on growth and behaviour of juvenile great scallops Pecten maximus. Aquat Toxicol 184:142–154
Spagnolo F (1953) Spectrophotometric determination of glycerol as sodium-cupri-glycerol complex. AnaCh 25(10):1566–1568
Nielsen SS (2010) Phenol-sulfuric acid method for total carbohydrates. Springer, New York
Qin L, Shu Q, Wang Z, Shang C, Zhu S, Xu J, Li R, Zhu L, Yuan Z (2014) Cultivation of Chlorella vulgaris in dairy wastewater pretreated by UV irradiation and sodium hypochlorite. Appl Biochem Biotechnol 172(2):1121–1130
Higgs RJ, Chase LE, Ross DA, Van Amburgh ME (2015) Updating the Cornell Net Carbohydrate and Protein System feed library and analyzing model sensitivity to feed inputs. J Dairy Sci 98(9):6340–6360
Friedl A, Padouvas E, Rotter H, Varmuza K (2005) Prediction of heating values of biomass fuel from elemental composition. Anal Chim Acta 544(1–2):191–198
Geisseler D, Horwath WR, Joergensen RG, Ludwig B (2010) Pathways of nitrogen utilization by soil microorganisms—a review. Soil Biol Biochem 42(12):2058–2067
Qin L, Wei D, Wang Z, Alam MA (2018) Advantage Assessment of mixed culture of Chlorella vulgaris and Yarrowia lipolytica for treatment of liquid digestate of yeast industry and cogeneration of biofuel feedstock. Appl Biochem Biotechnol 187(3):856–869
Qin L, Liu L, Wang Z, Chen W, Wei D (2018) Efficient resource recycling from liquid digestate by microalgae-yeast mixed culture and the assessment of key gene transcription related to nitrogen assimilation in microalgae. Bioresour Technol 264:90–97
Markou G, Georgakakis D (2011) Cultivation of filamentous cyanobacteria (blue-green algae) in agro-industrial wastes and wastewaters: a review. ApEn 88(10):3389–3401
Vachova L, Palkova Z (2005) Physiological regulation of yeast cell death in multicellular colonies is triggered by ammonia. J Cell Biol 169(5):711–717
Ramanna L, Guldhe A, Rawat I, Bux F (2014) The optimization of biomass and lipid yields of Chlorella sorokiniana when using wastewater supplemented with different nitrogen sources. Bioresour Technol 168:127–135
Addy MM, Kabir F, Zhang R, Lu Q, Deng X, Current D, Griffith R, Ma Y, Zhou W, Chen P, Ruan R (2017) Co-cultivation of microalgae in aquaponic systems. Bioresour Technol 245:27–34
Rai MP, Nigam S, Sharma R (2013) Response of growth and fatty acid compositions of Chlorella pyrenoidosa under mixotrophic cultivation with acetate and glycerol for bioenergy application. Biomass Bioenerg 58:251–257
Collier JL (2010) Flow cytometry and the single cell in phycology. J Phycol 36(4):628–644
Jorgensen P, Tyers M (2004) How cells coordinate growth and division. Curr Biol 14(23):R1014–R1027
Johnston GC, Singer RA, Mcfarlane S (1977) Growth and cell division during nitrogen starvation of the yeast Saccharomyces cerevisiae. J Bacteriol 132(2):723
Lopes M, Gomes N, Goncalves C, Coelho MAZ, Mota M, Belo I (2008) Yarrowia lipolytica lipase production enhanced by increased air pressure. Lett Appl Microbiol 46(2):255–260
Lee K, Lee CG (2001) Effect of light/dark cycles on wastewater treatments by microalgae. Biotechnol Bioproc Eng 6(3):194–199
Giordano M, Bowes G (1997) Gas exchange and C allocation in Dunaliella salina cells in response to the N source and CO2 concentration used for growth. Plant Physiol 115(3):1049–1056
Singh SP, Singh P (2015) Effect of temperature and light on the growth of algae species: a review. Renew Sustain Energy Rev 50:431–444
Benvenuti G, Bosma R, Cuaresma M, Janssen M, Barbosa MJ, Wijffels RH (2015) Selecting microalgae with high lipid productivity and photosynthetic activity under nitrogen starvation. J Appl Phycol 27(4):1–7
Shtaida N, Khozingoldberg I, Boussiba S (2015) The role of pyruvate hub enzymes in supplying carbon precursors for fatty acid synthesis in photosynthetic microalgae. PsynR 125(3):407–422
Streb S, Zeeman SC (2012) Starch metabolism in Arabidopsis. Arabidopsis Book 10(e0160):e0160
Lu L, Chen J, Lim PE, Dong W (2018) Dual-species cultivation of microalgae and yeast for enhanced biomass and microbial lipid production. J Appl Phycol 30(6):1–11
Vardon DR, Sharma BK, Blazina GV, Rajagopalan K, Strathmann TJ (2012) Thermochemical conversion of raw and defatted algal biomass via hydrothermal liquefaction and slow pyrolysis. Bioresour Technol 109:178–187
Acknowledgements
This work was supported by the Sciences and Technology of Guangzhou [Grant no. 201704030084], the National Natural Science Foundation of China [Grant no. 21606230], the Natural Science Foundation for research team of Guangdong Province [Grant no. 2016A030312007], and the National Key Research and Development Program-China [Grant no. 2016YFB0601004]. The authors are grateful to Mohammad Asraful Alam for his kind help in English editing.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Qin, L., Liu, L., Wang, Z. et al. The mixed culture of microalgae Chlorella pyrenoidosa and yeast Yarrowia lipolytica for microbial biomass production. Bioprocess Biosyst Eng 42, 1409–1419 (2019). https://doi.org/10.1007/s00449-019-02138-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00449-019-02138-1