A FUNCTIONAL PROPERTY OF A DOMESTIC APPLE ISOLATE: PULCHERRIMIN PRODUCTION BY METSCHNIKOWIA PULCHERRIMA ELM-GS-3 VIA WASTE VALORIZATION

Year 2025, Volume: 50 Issue: 2, 165 - 177

Gamze Nur Müjdeci

https://doi.org/10.15237/gida.GD25012

Abstract

Metschnikowia pulcherrima ELM-GS-3 was isolated from damaged Granny Smith apples and identified via MALDI-TOF MS and ITS sequencing (97.89% similarity, NCBI database). Pulcherrimin production was confirmed on FeCl3-supplemented media by maroon-red pigment formation and microscopic analysis. Food waste-derived media, including potato peel, onion skin, watermelon rind extracts, and diluted molasses, were evaluated for biomass and pigment production. Onion skin extract yielded the highest biomass (9.78±0.1 g/L) and pulcherrimin (7.63±0.6 g/L), followed by molasses and watermelon rind. FTIR analysis confirmed iron presence, while SEM revealed an amorphous microporous 3D structure. Absorbance peaked at 420 nm in alkali solution, consistent with low solubility except in alkaline conditions. The pigment’s low solubility profile, except in alkali, aligns with its stability characteristics observed in the literature. This study demonstrates the potential of food waste in pulcherrimin production and the biotechnological relevance of M. pulcherrima ELM-GS-3.

Keywords

Metchnikowia pulcherrima, pulcherrimin, waste, fermentation, ITS sequencing

YERLİ BİR ELMA İZOLATININ FONKSİYONEL ÖZELLİĞİ: ATIKLARIN DEĞERLENDİRİLMESİ YOLUYLA METSCHNIKOWIA PULCHERRIMA ELM-GS-3 TARAFINDAN PULKERİMİN ÜRETİMİ

Abstract

Metschnikowia pulcherrima ELM-GS-3, hasar görmüş Granny Smith elmalarından izole edilmiş ve MALDI-TOF MS ile ITS dizileme yöntemleri kullanılarak tanımlanmıştır (%97.89 benzerlik, NCBI veritabanı). Pulcherrimin üretimi, FeCl₃ içeren besiyerinde bordo-kırmızı pigment oluşumu ve mikroskobik analiz ile doğrulanmıştır. Patates kabuğu, soğan kabuğu, karpuz kabuğu ekstreleri ve seyreltilmiş melas gibi gıda atıklarından türetilmiş besiyerleri, biyokütle ve pigment üretimi açısından değerlendirilmiştir. En yüksek biyokütle (9.78±0.1 g/L) ve pulcherrimin (7.63±0.6 g/L) üretimi soğan kabuğu ekstresinde gözlemlenmiş, bunu sırasıyla melas ve karpuz kabuğu takip etmiştir. FTIR analizi pigmentin demir içerdiğini doğrularken, SEM analizi amorf ve mikroporoz 3D bir yapı ortaya koymuştur. Pigmentin alkali çözeltide maksimum absorpsiyon dalga boyu 420 nm olarak belirlenmiş ve düşük çözünürlük profili, literatürde bildirilen stabilite özellikleriyle uyumlu bulunmuştur. Bu çalışma, gıda atıklarının pulcherrimin üretiminde potansiyelini ve M. pulcherrima ELM-GS-3’ün biyoteknolojik önemini ortaya koymaktadır.

Keywords

Metchnikowia pulcherrima, pulkerimin, soğan kabuğu, atık, fermantasyon, ITS dizileme

References

• Abomohra, A. E. F., Wang, Q., Huang, J., Saad‐Allah, K. M. (2021). A sustainable approach for bioconversion of food and lignocellulosic wastes into liquid biofuel using a new Metschnikowia pulcherrima isolate. International Journal of Energy Research 45(2): 3430-3441, doi: 10.1002/er.6028.
• Bernard, A., Rossignol, T., Park, Y. K. (2024). Biotechnological approaches for producing natural pigments in yeasts. Trends in Biotechnology 42(12): 1644-1662, doi: 10.1016/ j.tibtech.2024.06.012.
• Charron-Lamoureux, V., Haroune, L., Pomerleau, M., Hall, L., Orban, F., Leroux, J., Beauregard, P. B. (2023). Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions. Nature Communications 14(1): 2536, doi: 10.1038/s41467-023-38222-0.
• Di Salvo, E., Lo Vecchio, G., De Pasquale, R., De Maria, L., Tardugno, R., Vadalà, R., Cicero, N. (2023). Natural pigments production and their application in food, health and other industries. Nutrients, 15(8): 1923, doi: 10.3390/nu15081923.
• Dufossé, L. (2006). Microbial production of food grade pigments. Food technology and Biotechnology, 44(3): 313-321, doi: 10.17113/ftb.
• FAOSTAT (2022). Food and Agriculture Organization https://www.fao.org/faostat/ en/#data (Accessed 15 October 2024).
• Galanakis, C. M. (2012). Recovery of high added-value components from food wastes: Conventional, emerging technologies and commercialized applications. Trends in Food Science and Technology, 26(2): 68-87, doi: 10.1016/ j.tifs.2012.03.003.
• Genemo, T. G., Erebo, D. L., Gabr, A. K. (2021). Optimizing bio-ethanol production from cabbage and onion peels waste using yeast (Saccharomyces cerevisiae) as fermenting agent. International Journal of Life Science Research Archive, 1(1): 24-35, doi: 10.53771/ijlsra.2021.1.1.0012.
• Graça, A., Santo, D., Esteves, E., Nunes, C., Abadias, M., Quintas, C. (2015). Evaluation of microbial quality and yeast diversity in fresh-cut apple. Food Microbiology, 51: 179-185, doi: 10.1016/j.fm.2015.06.003.
• FAO (2011). Global food losses and food waste – Extent, causes and prevention. Rome, Italy.
• Hsueh, C. C., Roxas, T. J., Chan, Y. H., Juan, C. N., Tayo, L. L., Chen, Y. Y., Chen, B. Y. (2023). Feasibility study of value-added production from onion peel agricultural wastes for circular economy. Journal of the Taiwan Institute of Chemical Engineers, 145: 104851, doi: 10.1016/ j.jtice.2023.104851.
• Joshi, V. K., Attri, D., Bala, A., Bhushan, S. (2003). Microbial pigments. Indian Journal of Biotechnology, 2: 362-369, doi: 10.1007/978-1-4020-9942-7_8.
• Kalra, R., Conlan, X. A., Goel, M. (2020). Fungi as a potential source of pigments: harnessing filamentous fungi. Frontiers in Chemistry, 8: 369, doi: 10.3389/fchem.2020.00369.
• Kampen, W.H. (2014). Nutritional requirements in fermentation processes. In: Fermentation and Biochemical Engineering Handbook, Vogel, H.C, Todaro, C.M. (eds.), William Andrew Publishing, Norwich New York, pp. 35-57.
• Kántor, A., Hutková, J., Petrová, J., Hleba, L., Kačániová, M. (2015). Antimicrobial activity of pulcherrimin pigment produced by Metschnikowia pulcherrima against various yeast species. Journal of Microbiology, Biotechnology and Food Sciences, 5(3): 282-285, doi: 10.15414/jmbfs.2015/16.5.3.282-285.
• Karasu-Yalcin, S., Soylemez-Milli, N., Eren, O., Eryasar-Orer, K. (2021). Reducing time in detection of Listeria monocytogenes from food by MALDI-TOF mass spectrometry. Journal of Food Science and Technology, 58: 4102-4109, doi: 10.1007/s13197-020-04869-6.
• Kim, H. M., Choi, I. S., Lee, S., Yang, J. E., Jeong, S. G., Park, J. H., Park, H. W. (2019). Biorefining process of carbohydrate feedstock (agricultural onion waste) to acetic acid. ACS Omega, 4(27): 22438-22444, doi: 10.1021/acsomega.9b03093.
• Kosseva, M.R. (2013). Recovery of commodities from food wastes using solid-state fermentation, In: Food Industry Wastes: Assessment and Recuperation of Commodities, Kosseva, M.R., Webb, C. (eds.), Academic Press, Cambridge, USA, pp. 77-102.
• Koutinas, A. A., Vlysidis, A., Pleissner, D., Kopsahelis, N., Garcia, I. L., Kookos, I. K., Lin, C. S. K. (2014). Valorization of industrial waste and by-product streams via fermentation for the production of chemicals and biopolymers. Chemical Society Reviews, 43(8): 2587-2627, doi: 10.1039/c3cs60293a.
• Kregiel, D., Krajewska, A., Kowalska-Baron, A., Czarnecka-Chrebelska, K. H., Nowak, A. (2024). Photoprotective Effects of Yeast Pulcherrimin. Molecules, 29(20): 4873, doi: 10.3390/molecules29204873.
• Kregiel, D., Nowacka, M., Rygala, A., Vadkertiová, R. (2022). Biological activity of pulcherrimin from the Meschnikowia pulcherrima Clade. Molecules, 27(6); 1855, doi: 10.3390/ molecules27061855.
• Lin, C. S. K., Koutinas, A. A., Stamatelatou, K., Mubofu, E. B., Matharu, A. S., Kopsahelis, N., Luque, R. (2014). Current and future trends in food waste valorization for the production of chemicals, materials and fuels: a global perspective. Biofuels, Bioproducts and Biorefining, 8(5): 686-715, doi: 10.1002/bbb.1506.
• Lyu, X., Lyu, Y., Yu, H., Chen, W., Ye, L., Yang, R. (2022). Biotechnological advances for improving natural pigment production: A state-of-the-art review. Bioresources and Bioprocessing, 9(1): 8, doi: 10.1186/s40643-022-00497-4.
• Mažeika, K., Šiliauskas, L., Skridlaitė, G., Matelis, A., Garjonytė, R., Paškevičius, A., Melvydas, V. (2021). Features of iron accumulation at high concentration in pulcherrimin-producing Metschnikowia yeast biomass. JBIC Journal of Biological Inorganic Chemistry, 26: 299-311, doi: 10.1007/s00775-021-01853-z.
• MacDonald, J. C. (1963). The structure of pulcherriminic acid. Canadian Journal of Chemistry, 41(1): 165-172, doi: 10.1139/v63-021.
• Mishra, K., Siwal, S. S., Nayaka, S. C., Guan, Z., Thakur, V. K. (2023). Waste-to-chemicals: Green solutions for bioeconomy markets. Science of the Total Environment, 887: 164006, doi: 10.1016/j.scitotenv.2023.164006.
• Mujdeci, G. N. (2021). Natural melanin synthesized by Aureobasidium pullulans using food wastes and its characterization. Applied Food Biotechnology, 8(4): 307-318, doi: 10.22037/afb.v8i4.34599.
• Müjdeci, G. N. (2022). Experimental modeling and optimization of melanin production by Aureobasidium pullulans NBRC 100716 in carrot peel extract. Environmental Progress and Sustainable Energy, 41(6): e13919, doi: 10.1002/ep.13919.
• Mushimiyimana, I., Tallapragada, P. (2016). Bioethanol production from agro wastes by acid hydrolysis and fermentation process. CSIR-NIScPR, 75(06): 383-388.
• Nair, R.B., Lennartsson, P.R., Taherzadeh, M.J. (2017). Bioethanol production from agricultural and municipal wastes, In: Current Developments in Biotechnology and Bioengineering, Wong, J.W.C., Tyagi, R.D., Pandey, A. (eds.), Elsevier, Amsterdam, Holland, pp. 157-190.
• Panesar, R., Kaur, S., Panesar, P. S. (2015). Production of microbial pigments utilizing agro-industrial waste: a review. Current Opinion in Food Science, 1: 70-76, doi: 10.1016/j.cofs.2014.12.002.
• Pawlikowska, E., Kolesińska, B., Nowacka, M., Kregiel, D. (2020). A new approach to producing high yields of pulcherrimin from Metschnikowia yeasts. Fermentation, 6(4): 114, doi: 10.3390/fermentation6040114.
• Ramesh, C., Prasastha, V. R., Venkatachalam, M., Dufossé, L. (2022). Natural substrates and culture conditions to produce pigments from potential microbes in submerged fermentation. Fermentation, 8(9): 460, doi: 10.3390/ fermentation8090460.
• Sarker, A., Ahmmed, R., Ahsan, S. M., Rana, J., Ghosh, M. K., Nandi, R. (2024). A comprehensive review of food waste valorization for the sustainable management of global food waste. Sustainable Food Technology, 2: 48-69, doi: 10.1039/d3fb00156c.
• Sipiczki, M. (2006). Metschnikowia strains isolated from botrytized grapes antagonize fungal and bacterial growth by iron depletion. Applied and Environmental Microbiology, 72(10): 6716-6724, doi: 10.1128/AEM.01275-06.
• Sipiczki, M. (2020). Metschnikowia pulcherrima and related pulcherrimin-producing yeasts: Fuzzy species boundaries and complex antimicrobial antagonism. Microorganisms, 8(7): 1029, doi: 10.3390/microorganisms8071029.
• SlÁviková, E., Vadkertiová, R., Vránová, D. (2009). Yeasts colonizing the leaves of fruit trees. Annals of Microbiology, 59: 419-424, doi: 10.1007/BF03175125.
• Taşar, Ö. C., Taşar, G. E. Use of onion peels as an economical substrate for microbial inulinase production under solid state fermentation. Eurasian Journal of Biological and Chemical Sciences, 5: 144-150, doi: 10.46239/ ejbcs.1163946.
• Tatay-Núñez, J., Albi-Puig, J., Garrigós, V., Orejas-Suárez, M., Matallana, E., Aranda, A. (2024). Isolation of local strains of the yeast Metschnikowia for biocontrol and lipid production purposes. World Journal of Microbiology and Biotechnology, 40(3): 88, doi: 10.1007/s11274-024-03918-y.
• Tiwari, A., Khawas, R. (2021). Food waste and agro by-products: a step towards food sustainability. In: Innovation in the food sector through the valorization of food and agro-food by-products, Baros, A.N. (ed), IntechOpen.
• Türkel, S., Ener, B. (2009). Isolation and characterization of new Metschnikowia pulcherrima strains as producers of the antimicrobial pigment pulcherrimin. Zeitschrift für Naturforschung C, 64(5-6): 405-410, doi: 10.1515/znc-2009-5-618.
• Vea, E. B., Romeo, D., Thomsen, M. (2018). Biowaste valorisation in a future circular bioeconomy. Procedia CIRP, 69: 591-596, doi: 10.1016/j.procir.2017.11.062.