Valorization of shalgam juice plant waste for the production of carotenoids by Rhodotorula glutinis

Yıl 2023, , 79 - 87, 27.03.2023

Abdulkadir Keskin , Melis Fırat , Ayşe Ezgi Ünlü Büyüktopcu

https://doi.org/10.31015/jaefs.2023.1.9

Öz

Food waste is an emerging global problem that should not be underestimated. One of the most abundant wastes in Türkiye and neighbour countries is the waste of shalgam juice plants (WSJP). In this study, WSJP was used as a growth medium for Rhodotorula glutinis. The effects of initial medium pH (3.4-5.4), carbon (0-60 g/L glycerol) and nitrogen sources (0-1 g/L urea) were investigated on biomass, medium pH, reducing sugar concentration, total lipid and carotenoid contents, as well as carotenoid composition (torulene, torularhodin, β-carotene). When crude waste extract (no additional nutrient) was used as growth medium (initial medium pH 3.4, 6.14 g/L sugar), biomass was relatively low (1.47±0.055 g/L), due to acidic pH and insufficient nutrients. However, these stress conditions increased the production of total lipid and carotenoid contents by R. glutinis. The highest lipid and carotenoid contents were obtained as 0.14±0.0004 g/g dry cell weight (dcw) and 1221.57±0.59 µg/g dcw, respectively, under these circumstances. As additional stress factor fermentation medium -crude WSJP extract- was illuminated for 72 h. This increased lipid content by 1.7-fold, while showing low impact on carotenoid content. Interestingly, illumination changed the carotenoid composition by decreasing torulene and β-carotene percentages, but increasing torularhodin percentage. On the other hand, tuning the initial pH to an ambient value (5.4) and the addition of carbon and nitrogen sources stimulated cell growth (4.67±0.07 g/L). This study presents the first time use of WSJP extract as a growth medium, without any additional nutrition, moreover, the simultaneous production of high-value added carotenoids.  

Anahtar Kelimeler

Rhodotorula glutinis, waste, shalgam juice, lipid, carotenoid

Kaynakça

• Agcam, E., Akyıldız, A. & Balasubramaniam, V. M. (2017). Optimization of anthocyanins extraction from black carrot pomace with thermosonication. Food Chemistry, 237, 461–470. https://doi.org/10.1016/j.foodchem.2017.05.098
• Agcam, E., Akyıldız, A., Kamat, S. & Balasubramaniam, V. M. (2021). Bioactive Compounds Extraction from the Black Carrot Pomace with Assistance of High Pressure Processing: An Optimization Study. Waste and Biomass Valorization, 12(11), 5959–5977. https://doi.org/10.1007/s12649-021-01431-z
• Bhosale, P. (2004). Environmental and cultural stimulants in the production of carotenoids from microorganisms. Applied Microbiology and Biotechnology, 63(4), 351–361. https://doi.org/10.1007/s00253-003-1441-1
• Bhosale, P. & Gadre, R. V. (2002). Manipulation of temperature and illumination conditions for enhanced β-carotene production by mutant 32 of Rhodotorula glutinis. Letters in Applied Microbiology, 34(5), 349–353. https://doi.org/10.1046/j.1472-765X.2002.01095.x
• Bligh, E. G. & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8), 911–917.
• Britton, G. (1995). Structure and properties of carotenoids in relation to function. FASEB Journal, 9, 1551–1558.
• Bröring, S., Laibach, N. & Wustmans, M. (2020). Innovation types in the bioeconomy. Journal of Cleaner Production, 266, 121939. https://doi.org/10.1016/j.jclepro.2020.121939
• Buzzini, P. & Martini, A. (2000). Production of carotenoids by strains of Rhodotorula glutinis cultured in raw materials of agro-industrial origin. Bioresource Technology, 71(1), 41–44. https://doi.org/10.1016/S0960-8524(99)00056-5
• Coşkun, F. (2017). A Traditional Turkish Fermented Non-Alcoholic Beverage, “Shalgam.” Beverages, 3(49), 1–13.
• De Souza Mesquita, L. M., Ventura, S. P. M., Braga, A. R. C., Pisani, L. P., Dias, A. C. R. V. & De Rosso, V. V. (2019). Ionic liquid-high performance extractive approach to recover carotenoids from: Bactris gasipaes fruits. Green Chemistry, 21(9), 2380–2391. https://doi.org/10.1039/c8gc03283a
• Gizir, A. M., Turker, N. & Artuvan, E. (2008). Pressurized acidified water extraction of black carrot [Daucus carota ssp. sativus var. atrorubens Alef.] anthocyanins. European Food Research and Technology, 226(3), 363–370. https://doi.org/10.1007/s00217-006-0546-z
• Goiris, K., Van Colen, W., Wilches, I., León-Tamariz, F., De Cooman, L. & Muylaert, K. (2015). Impact of nutrient stress on antioxidant production in three species of microalgae. Algal Research, 7, 51–57. https://doi.org/10.1016/j.algal.2014.12.002
• Gu, W. L., An, G. H. & Johnson, E. A. (1997). Ethanol increases carotenoid production in Phaffia rhodozyma. Journal of Industrial Microbiology and Biotechnology, 19, 114–117.
• Hanedar, A., Gül, B., Güneş, E., Kaykıoğlu, G. & Güneş, Y. (2021). Waste management and zero waste practices in educational institutions. Environmental Research & Technology, 4(2), 126–133.
• Hernández-Almanza, A., Montañez, J., Martínez, G., Aguilar-Jiménez, A., Contreras-Esquivel, J. C. & Aguilar, C. N. (2016). Lycopene: Progress in microbial production. Trends in Food Science and Technology, 56, 142–148. https://doi.org/10.1016/j.tifs.2016.08.013
• Johnson, E. A. & Lewis, M. J. (1979). Astaxanthin formation by the yeast Phaffia rhodozyma. Journal of General Microbiololgy, 115, 173–183.
• Kammerer, D., Carle, R. & Schieber, A. (2004). Quantification of anthocyanins in black carrot extracts (Daucus carota ssp. sativus var. atrorubens Alef.) and evaluation of their color properties. European Food Research and Technology, 219, 479–486. https://doi.org/10.1007/s00217-004-0976-4
• Keskin, B. & Güneş, E. (2021). Social and cultural aspects of traditional drinks: A review on traditional Turkish drinks. International Journal of Gastronomy and Food Science, 25(July), 100382. https://doi.org/10.1016/j.ijgfs.2021.100382
• Kot, A. M., Błazejak, S., Gientka, I., Kieliszek, M. & Bryś, J. (2018). Torulene and torularhodin: “New” fungal carotenoids for industry? Microbial Cell Factories, 17(49), 1–14. https://doi.org/10.1186/s12934-018-0893-z
• Kot, A. M., Błażejak, S., Kurcz, A., Bryś, J., Gientka, I., Bzducha-Wróbel, A., Maliszewska, M. & Reczek, L. (2017). Effect of initial pH of medium with potato wastewater and glycerol on protein, lipid and carotenoid biosynthesis by Rhodotorula glutinis. Electronic Journal of Biotechnology, 27, 25–31. https://doi.org/10.1016/j.ejbt.2017.01.007
• Kumar, M., Dahuja, A., Sachdev, A., Kaur, C., Varghese, E., Saha, S. & Sairam, K. V. S. S. (2019). Valorisation of black carrot pomace: microwave assisted extraction of bioactive phytoceuticals and antioxidant activity using Box–Behnken design. Journal of Food Science and Technology, 56(2), 995–1007. https://doi.org/10.1007/s13197-018-03566-9
• Maiani, G., Castón, M. J. P., Catasta, G., Toti, E., Cambrodón, I. G., Bysted, A., Granado-Lorencio, F., Olmedilla-Alonso, B., Knuthsen, P., Valoti, M., Böhm, V., Mayer-Miebach, E., Behsnilian, D. & Schlemmer, U. (2009). Carotenoids: Actual knowledge on food sources, intakes, stability and bioavailability and their protective role in humans. Molecular Nutrition and Food Research, 53(SUPPL. 2), 194–218. https://doi.org/10.1002/mnfr.200800053
• Marsh, A. J., Hill, C., Ross, R. P. & Cotter, P. D. (2014). Fermented beverages with health-promoting potential: Past and future perspectives. Trends in Food Science and Technology, 38(2), 113–124. https://doi.org/10.1016/j.tifs.2014.05.002
• Mata-Gómez, L. C., Montañez, J. C., Méndez-Zavala, A. & Aguilar, C. N. (2014). Biotechnological production of carotenoids by yeasts: An overview. Microbial Cell Factories, 13(12), 1–11. https://doi.org/10.1186/1475-2859-13-12
• Mayne, S. T. (1996). Beta-carotene, carotenoids, and disease prevention in humans. FASEB Journal, 10, 690–701.
• Miller, G. L. (1959). Modified DNS method for reducing sugars. Analytical Chemistry, 31(3), 426–428.
• Moise, A. R., Al-Babili, S. & Wurtzel, E. T. (2014). Mechanistic aspects of carotenoid biosynthesis. Chemical Reviews, 114(1), 164–193. https://doi.org/10.1021/cr400106y
• Mussagy, C. U., Gonzalez-Miquel, M., Santos-Ebinuma, V. C. & Pereira, J. F. B. (2022). Microbial torularhodin–a comprehensive review. Critical Reviews in Biotechnology, 0(0), 1–19. https://doi.org/10.1080/07388551.2022.2041540
• Nistor, M., Diaconeasa, Z., Frond, A. D., Stirbu, I., Socaciu, C., Pintea, A. & Rugina, D. (2021). Comparative efficiency of different solvents for the anthocyanins extraction from chokeberries and black carrots, to preserve their antioxidant activity. Chemical Papers, 75(2), 813–822. https://doi.org/10.1007/s11696-020-01344-6
• Omrak, H. (2021). Bitkisel Üretim. Türk Tarım Dergisi. http://www.turktarim.gov.tr/Haber/591/dusuk-maliyetiyle-salgam-uretimde-ciftcinin-tercihi#:~:text=Şalgam ülkemizde üretimi her geçen,bin 599 ton olarak gerçekleşmiştir.
• Orosa, M., Franqueira, D., Cid, A. & Abalde, J. (2005). Analysis and enhancement of astaxanthin accumulation in Haematococcus pluvialis. Bioresource Technology, 95(3), 373–378.
• Peng, T., Fakankun, I. & Levin, D. B. (2021). Accumulation of neutral lipids and carotenoids of Rhodotorula diobovata and Rhodosporidium babjevae cultivated under nitrogen-limited conditions with glycerol as a sole carbon source. FEMS Microbiology Letters, 368(18), 1–7. https://doi.org/10.1093/femsle/fnab126
• Rapoport, A., Guzhova, I., Bernetti, L., Buzzini, P., Kieliszek, M. & Kot, A. M. (2021). Carotenoids and some other pigments from fungi and yeasts. Metabolites, 11(2), 1–17. https://doi.org/10.3390/metabo11020092
• Rodriguez-Concepcion, M., Avalos, J., Bonet, M. L., Boronat, A., Gomez-Gomez, L., Hornero-Mendez, D., Limon, M. C., Meléndez-Martínez, A. J., Olmedilla-Alonso, B., Palou, A., Ribot, J., Rodrigo, M. J., Zacarias, L. & Zhu, C. (2018). A global perspective on carotenoids: Metabolism, biotechnology, and benefits for nutrition and health. Progress in Lipid Research, 70(February), 62–93. https://doi.org/10.1016/j.plipres.2018.04.004
• Sucheta, Misra, N. N. & Yadav, S. K. (2020). Extraction of pectin from black carrot pomace using intermittent microwave, ultrasound and conventional heating: Kinetics, characterization and process economics. Food Hydrocolloids, 102(December 2019), 105592. https://doi.org/10.1016/j.foodhyd.2019.105592
• Turker, N., Aksay, S. & Ekiz, H. I. (2004). Effect of storage temperature on the stability of anthocyanins of a fermented black carrot (Daucus carota var. L.) beverage: Shalgam. Journal of Agricultural and Food Chemistry, 52(12), 3807–3813. https://doi.org/10.1021/jf049863s
• Ünal, M. Ü. & Bellur, E. (2009). Extraction and characterisation of pectin methylesterase from black carrot (Daucus carota L.). Food Chemistry, 116(4), 836–840. https://doi.org/10.1016/j.foodchem.2009.03.031
• Wrolstad, R. E. (2004). Anthocyanin Pigments-Bioactivity and Coloring Properties. Food Chemistry and Toxicology, 69(5), 419–425.
• Young, A. J. & Lowe, G. L. (2018). Carotenoids—antioxidant properties. Antioxidants, 7(2), 10–13. https://doi.org/10.3390/antiox7020028