Abstract
Phaffia rhodozyma is a basidiomycetous yeast characterized by its production of the carotenoid pigment astaxanthin, which holds high commercial value for its significance in aquaculture, cosmetics and as nutraceutics, and the UV-B-absorbing compound mycosporine-glutaminol-glucoside (MGG), which is of great biotechnological relevance for its incorporation into natural sunscreens. However, the industrial exploitation has been limited to the production of astaxanthin in small quantities. On the other hand, the accumulation of MGG in P. rhodozyma was recently reported and could add value to the simultaneous production of both metabolites. In this work, we obtain a mutant strain that overproduces both compounds, furthermore we determined how the accumulation of each is affected by the carbon-to-nitrogen ratio and six biotic and abiotic factors. The mutant obtained produces 159% more astaxanthin (470.1 μg g−1) and 220% more MGG (57.9 mg g−1) than the parental strain (295.8 μg g−1 and 26.2 mg g−1 respectively). Furthermore, we establish that the carotenoids accumulate during the exponential growth phase while MGG accumulates during the stationary phase. The carbon-to-nitrogen ratio affects each metabolite differently, high ratios favoring carotenoid accumulation while low ratios favoring MGG accumulation. Finally, the accumulation of both metabolites is stimulated only by photosynthetically active radiation and low concentrations of hydrogen peroxide. The mutant strain obtained is the first hyper-productive mutant capable of accumulating high concentrations of MGG and astaxanthin described to date. The characterization of how both compounds accumulate during growth and the factors that stimulate their accumulation, are the first steps toward the future commercial exploitation of strains for the simultaneous production of two biotechnologically important metabolites.
Similar content being viewed by others
Data availability
The data underlying this article are available in the article and in its online supplementary material. The raw datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
An G-H, Johnson EA (1990) Influence of light on growth and pigmentation of the yeast Phaffia rhodozyma. Antonie Van Leeuwenhoek 57:191–203. https://doi.org/10.1007/BF00400151
An G-H, Schuman DB, Johnson EA (1989) Isolation of Phaffia rhodozyma mutants with increased astaxanthin content. Appl Environ Microbiol 55:116–124. https://doi.org/10.1128/aem.55.1.116-124.1989
An G-H, Chang K-W, Johnson E-A (1996) Effect of oxygen radicals and aeration on carotenogenesis and growth of Phaffia rhodozyma (Xanthophyllomyces dendrorhous). J Microbiol Biotechnol 6:103–109
Andrewes AG, Phaff HJ, Starr MP (1976) Carotenoids of Phaffia rhodozyma, a red-pigmented fermenting yeast. Phytochemistry 15:1003–1007. https://doi.org/10.1016/S0031-9422(00)84390-3
Bandaranayake WM (1998) Mycosporines: are they nature’s sunscreens? Nat Prod Rep 15:159–172. https://doi.org/10.1039/A815159Y
Barbachano-Torres A, Ramos-Valdivia AC, Cerda-García-Rojas CM et al (2012) Carotenogenesis induction with hydrogen peroxide in Xanthophyllomyces dendrorhous colored mutants. Microb Appl Res:598–602. https://doi.org/10.1142/9789814405041_0122
Bellora N, Moliné M, David-Palma M et al (2016) Comparative genomics provides new insights into the diversity. physiology. and sexuality of the only industrially exploited tremellomycete: Phaffia rhodozyma. BMC Genomics 17:1–16. https://doi.org/10.1186/s12864-016-3244-7
Bhosale P, Gadre RV (2001) Production of β-carotene by a Rhodotorula glutinis mutant in sea water medium. Bioresour Technol 76:53–55. https://doi.org/10.1016/S0960-8524(00)00075-4
Bjørklund G, Gasmi A, Lenchyk L et al (2022) The role of Astaxanthin as a nutraceutical in health and age-related conditions. Molecules 27:7167. https://doi.org/10.3390/molecules27217167
Bon JA, Leathers TD, Jayaswal RK (1997) Isolation of astaxanthin-overproducing mutants of Phaffia rhodozyma. Biotechnol Lett 19:109–112. https://doi.org/10.1023/A:1018391726206
Bouillant M-L, Pittet J-L, Bernillon J et al (1981) Mycosporins from Ascochyta pisi Cladosporium Herbarum and Septoria Nodorum. Phytochemistry 20:2705–2707. https://doi.org/10.1016/0031-9422(81)85272-7
Brendler T, Williamson EM (2019) Astaxanthin: how much is too much? A Safety Review. Phytother Res 33:3090–3111. https://doi.org/10.1002/ptr.6514
Britton G, Liaaen-Jensen S, Pfander H (2004) Carotenoids: handbook. Springer Science & Business Media
Brombacher K, Fischer BB, Rüfenacht K et al (2006) The role of Yap1p and Skn7p-mediated oxidative stress response in the defence of Saccharomyces cerevisiae against singlet oxygen. Yeast 23:741–750. https://doi.org/10.1002/yea.1392
Calo P, Velazquez JB, Sieiro C et al (1995) Analysis of astaxanthin and other carotenoids from several Phaffia rhodozyma mutants. J Agric Food Chem 43:1396–1399. https://doi.org/10.1021/jf00053a049
Capelli B, Bagchi D, Cysewski GR (2013) Synthetic astaxanthin is significantly inferior to algal-based astaxanthin as an antioxidant and may not be suitable as a human nutraceutical supplement. Nutrafoods 12:145–152. https://doi.org/10.1007/s13749-013-0051-5
Chan HY, Ho KP (1999) Growth and carotenoid production by pH-stat cultures of Phaffia rhodozyma. Biotechnol Lett 21:953–958. https://doi.org/10.1023/A:1005638610564
Chrapusta E, Kaminski A, Duchnik K et al (2017) Mycosporine-Like amino acids: potential health and beauty ingredients. Mar Drugs 15:326. https://doi.org/10.3390/md15100326
Colabella F, Moline M, Libkind D (2014) UV sunscreens of microbial origin: mycosporines and mycosporine- like aminoacids. Recent Pat Biotechnol 8:179–193. https://doi.org/10.2174/1872208309666150102104520
Domínguez-Bocanegra AR, Torres-Muñoz JA (2004) Astaxanthin hyperproduction by Phaffia rhodozyma (now Xanthophyllomyces dendrorhous) with raw coconut milk as sole source of energy. Appl Microbiol Biotechnol 66:249–252. https://doi.org/10.1007/s00253-004-1686-3
Ducrey Santopietro LM, Spencer JFT, Siñeriz F (1998) Fed-batch and continuous culture of Phaffia rhodozyma (Xanthophyllomyces dendrorhous). Folia Microbiol 43:169–172. https://doi.org/10.1007/BF02816504
Fang TJ, Cheng Y-S (1993) Improvement of astaxanthin production by Phaffia rhodozyma through mutation and optimization of culture conditions. J Ferment Bioeng 75:466–469. https://doi.org/10.1016/0922-338X(93)90099-T
Favre-Bonvin J, Bernillon J, Salin N et al (1987) Biosynthesis of mycosporines: mycosporine glutaminol in Trichothecium roseum. Phytochemistry 26:2509–2514. https://doi.org/10.1016/S0031-9422(00)83866-2
Figueroa FL, Bueno A, Korbee N et al (2008) Accumulation of mycosporine-like amino acids in Asparagopsis armata grown in tanks with fishpond effluents of Gilthead Sea Bream. Sparus Aurata J World Aquac Soc 39:692–699. https://doi.org/10.1111/j.1749-7345.2008.00199.x
Florêncio JA, Soccol CR, Furlanetto LF et al (1998) A factorial approach for a sugarcane juice-based low cost culture medium: increasing the astaxanthin production by the red yeast Phaffia rhodozyma. Bioprocess Eng 19:161–164. https://doi.org/10.1007/PL00009008
Flores-Cotera LB, Sánchez S (2001) Copper but not iron limitation increases astaxanthin production by Phaffia rhodozyma in a chemically defined medium. Biotechnol Lett 23:793–797. https://doi.org/10.1023/A:1010358517806
Flores-Cotera L, Martín R, Sánchez S (2001) Citrate a possible precursor of astaxanthin in Phaffia rhodozyma: influence of varying levels of ammonium, phosphate and citrate in a chemically defined medium. Appl Microbiol Biotechnol 55:341–347. https://doi.org/10.1007/s002530000498
Frengova GI, Beshkova DM (2009) Carotenoids from Rhodotorula and Phaffia: yeasts of biotechnological importance. J Ind Microbiol Biotechnol 36:163. https://doi.org/10.1007/s10295-008-0492-9
Gervasi T, Pellizzeri V, Benameur Q et al (2018) Valorization of raw materials from agricultural industry for astaxanthin and β-carotene production by Xanthophyllomyces dendrorhous. Nat Prod Res 32:1554–1561. https://doi.org/10.1080/14786419.2017.1385024
Gu W-L, An G-H, Johnson EA (1997) Ethanol increases carotenoid production in Phaffia rhodozyma. J Ind Microbiol Biotechnol 19:114–117. https://doi.org/10.1038/sj.jim.2900425
Ho KP, Tam CY, Zhou B (1999) Growth and carotenoid production of Phaffia rhodozyma in fed-batch cultures with different feeding methods. Biotechnol Lett 21:175–178. https://doi.org/10.1023/A:1005487709974
Hussein G, Sankawa U, Goto H, Matusumoto KH, Watanabe (2006) Astaxanthin a carotenoid with potential in human health and nutrition. J Nat Prod 69:443–449. https://doi.org/10.1021/np050354+
Jacobson GK, Jolly SO, Sedmak JJ et al (2002) Astaxanthin over-producing strains of Phaffia rhodozyma. methods for their cultivation. and their use in animal feeds. Patent US6015684A
Jiang G-L, Zhou L-Y, Wang Y-T et al (2017) Astaxanthin from Jerusalem artichoke: production by fed-batch fermentation using Phaffia rhodozyma and application in cosmetics. Process Biochem 63:16–25. https://doi.org/10.1016/j.procbio.2017.08.013
Johnson EA (2003) Phaffia rhodozyma: colorful odyssey. Int Microbiol 6:169–174. https://doi.org/10.1016/10.1007/s10123-003-0130-3
Johnson EA, An G-H (1991) Astaxanthin from microbial sources. Crit Rev Biotechnol 11:297–326. https://doi.org/10.3109/07388559109040622
Johnson EA, Lewis MJY (1979) Astaxanthin formation by the yeast Phaffia rhodozyma. Microbiology 115:173–183. https://doi.org/10.1099/00221287-115-1-173
Johnson EA, Villa TG, Lewis MJ (1980) Phaffia rhodozyma as an astaxanthin source in salmonid diets. Aquaculture 20:123–134. https://doi.org/10.1016/0044-8486(80)90041-1
Kogej T, Gostinčar C, Volkmann M et al (2006) Mycosporines in extremophilic fungi—novel complementary osmolytes? Environ Chem 3:105–110. https://doi.org/10.1071/EN06012
Kogej T, Stein M, Volkmann M, Gorbushina AA et al (2007) Osmotic adaptation of the halophilic fungus Hortaea werneckii, role of osmolytes and melanization. Microbiol 153:4261–4273. https://doi.org/10.1099/mic.0.2007/010751-0
Korbee N, Figueroa FL, Aguilera J (2005) Effect of light quality on the accumulation of photosynthetic pigments. proteins and mycosporine-like amino acids in the red alga Porphyra leucosticta (Bangiales, Rhodophyta). J Photochem Photobiol B 80:71–78. https://doi.org/10.1016/j.jphotobiol.2005.03.002
Korbee N, Teresa Mata M, Figueroa FL (2010) Photoprotection mechanisms against ultraviolet radiation in Heterocapsa sp. (Dinophyceae) are influenced by nitrogen availability: mycosporine-like amino acids vs. xanthophyll cycle. Limnol Oceanogr 55:899–908. https://doi.org/10.4319/lo.2010.55.2.0899
Lai J-X, Chen X, Bu J et al (2022) Direct production of astaxanthin from food waste by Phaffia rhodozyma. Process Biochem 113:224–233. https://doi.org/10.1016/j.procbio.2022.01.003
Li C, Zhang N, Li B et al (2017) Increased torulene accumulation in red yeast Sporidiobolus pararoseus NGR as stress response to high salt conditions. Food Chem 237:1041–1047. https://doi.org/10.1016/j.foodchem.2017.06.033
Libkind D, Brizzio S, van Broock M (2004) Rhodotorula mucilaginosa a carotenoid producing yeast strain from a patagonian high-altitude lake. Folia Microbiol 49:19–25. https://doi.org/10.1007/BF02931640
Libkind D, Sommaruga R, Zagarese H et al (2005) Mycosporines in carotenogenic yeasts. Syst Appl Microbiol 28:749–754. https://doi.org/10.1016/j.syapm.2005.05.005
Libkind D, Diéguez MC, Moliné M et al (2006) Occurrence of photoprotective compounds in yeasts from freshwater ecosystems of northwestern Patagonia (Argentina). Photochem Photobiol 82:972–980. https://doi.org/10.1562/2005-09-09-RA-679
Libkind D, Moliné M, de García V et al (2008) Characterization of a novel South American population of the astaxanthin producing yeast Xanthophyllomyces dendrorhous (Phaffia rhodozyma). J Ind Microbiol Biotechnol 35:151–158. https://doi.org/10.1007/s10295-007-0275-8
Libkind D, Moliné M, Sampaio JP et al (2009) Yeasts from high-altitude lakes: influence of UV radiation. FEMS Microbiol Ecol 69:353–362. https://doi.org/10.1111/j.1574-6941.2009.00728.x
Libkind D, Moline M, van Broock M (2011a) Production of the UVB-absorbing compound mycosporine–glutaminol–glucoside by Xanthophyllomyces dendrorhous (Phaffia rhodozyma). FEMS Yeast Res 11:52–59. https://doi.org/10.1111/j.1567-1364.2010.00688.x
Libkind D, Moliné M, Sommaruga R et al (2011b) Phylogenetic distribution of fungal mycosporines within the Pucciniomycotina (Basidiomycota). Yeast 28:619–627. https://doi.org/10.1002/yea.1891
Libkind D, Moliné M, Colabella F (2018) Isolation and selection of new astaxanthin-producing strains of Phaffia rhodozyma. In: Barreiro C, Barredo J-L (eds) Microbial carotenoids: methods and protocols. Springer, New York, pp 297–310. https://doi.org/10.1007/978-1-4939-8742-9_18
Lim KC, Yusoff FM, Shariff M et al (2018) Astaxanthin as feed supplement in aquatic animals. Rev Aquac 10:738–773. https://doi.org/10.1111/raq.12200
Liu YS, Wu JY (2006) Hydrogen peroxide-induced astaxanthin biosynthesis and catalase activity in Xanthophyllomyces dendrorhous. Appl Microbiol Biotechnol 73:663–668. https://doi.org/10.1007/s00253-006-0501-8
Liu YS, Wu JY (2007) Perfusion culture process plus H2O2 stimulation for efficient astaxanthin production by Xanthophyllomyces dendrorhous. Biotechnol Bioeng 97:568–573. https://doi.org/10.1002/bit.21256
Lorenz RT, Cysewski GR (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167. https://doi.org/10.1016/S0167-7799(00)01433-5
Luna-Flores CH, Wang A, von Hellens J, Speight R (2022) Towards commercial levels of astaxanthin production in Phaffia rhodozyma. J Biotechnol 350:42–54. https://doi.org/10.1016/j.jbiotec.2022.04.001
Marcoleta A, Niklitschek M, Wozniak A et al (2011) Glucose and ethanol-dependent transcriptional regulation of the astaxanthin biosynthesis pathway in Xanthophyllomyces dendrorhous. BMC Microbiol 11:190. https://doi.org/10.1186/1471-2180-11-190
Marova I, Breierova E, Koci R et al (2004) Influence of exogenous stress factors on production of carotenoids by some strains of carotenogenic yeasts. Ann Microbiol 54:73–86
Martínez-Cárdenas A, Chávez-Cabrera C, Vasquez-Bahena JM et al (2018) A common mechanism explains the induction of aerobic fermentation and adaptive antioxidant response in Phaffia rhodozyma. Microb Cell Factories 17:53. https://doi.org/10.1186/s12934-018-0898-7
Meyer PS, du Preez JC (1994a) Astaxanthin production by a Phaffia rhodozyma mutant on grape juice. World J Microbiol Biotechnol 10:178–183. https://doi.org/10.1007/BF00360882
Meyer PS, Du Preez JC (1994b) Photo-regulated astaxanthin production by Phaffia rhodozyma mutants. Syst Appl Microbiol 17:24–31. https://doi.org/10.1016/S0723-2020(11)80027-5
Meyer PS, du Preez JC, Kilian SG (1993) Selection and evaluation of astaxanthin-overproducing mutants of Phaffia rhodozyma. World J Microbiol Biotechnol 9:514–520. https://doi.org/10.1007/BF00386286
Miao L, Chi S, Wu M et al (2019) Deregulation of phytoene-β-carotene synthase results in derepression of astaxanthin synthesis at high glucose concentration in Phaffia rhodozyma astaxanthin-overproducing strain MK19. BMC Microbiol 19:133. https://doi.org/10.1186/s12866-019-1507-6
Moliné M, Libkind D, del Carmen DM et al (2009) Photoprotective role of carotenoids in yeasts: response to UV-B of pigmented and naturally-occurring albino strains. J Photochem Photobiol B 95:156–161. https://doi.org/10.1016/j.jphotobiol.2009.02.006
Moliné M, Arbeloa EM, Flores MR et al (2010a) UVB photoprotective role of mycosporines in yeast: photostability and antioxidant activity of mycosporine-glutaminol-glucoside. Radiat Res 175:44–50. https://doi.org/10.1667/RR2245.1
Moliné M, Flores MR, Libkind D et al (2010b) Photoprotection by carotenoid pigments in the yeast Rhodotorula mucilaginosa: the role of torularhodin. Photochem Photobiol Sci 9:1145–1151. https://doi.org/10.1039/c0pp00009d
Moliné M, Libkind D, de Garcia V et al (2014) Production of Pigments and photo-protective compounds by cold-adapted yeasts. In: Buzzini P, Margesin R (eds) Cold-adapted yeasts: biodiversity. adaptation strategies and biotechnological significance. Springer, Berlin/Heidelberg, pp 193–224. https://doi.org/10.1007/978-3-642-39681-6_9
Ni H, Chen Q, Ruan H et al (2007) Studies on optimization of nitrogen sources for astaxanthin production by Phaffia rhodozyma. J Zhejiang Univ Sci B 8:365–370. https://doi.org/10.1631/jzus.2007.B0365
Nutakor C, Kanwugu ON, Kovaleva EG et al (2022) Enhancing astaxanthin yield in Phaffia rhodozyma: current trends and potential of phytohormones. Appl Microbiol Biotechnol 106:3531–3538. https://doi.org/10.1007/s00253-022-11972-5
Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol Lett 269:1–10. https://doi.org/10.1111/j.1574-6968.2007.00650.x
Paz S, Tzafra C, Yael L, Khutorian M et al (2022) Astaxanthin over-producing strains of Phaffia rhodozyma. Patent WO2021019409A1
Peinado NK, Abdala Díaz RT, Figueroa FL et al (2004) Ammonium and UV Radiation stimulate the accumulation of Mycosporine-like amino acids in Porphyra columbina (rhodophyta) from Patagonia, Argentina. J Phycol 40:248–259. https://doi.org/10.1046/j.1529-8817.2004.03013.x
Portwich A, Garcia-Pichel F (1999) Ultraviolet and osmotic stresses induce and regulate the synthesis of mycosporines in the cyanobacterium Chlorogloeopsis PCC 6912. Arch Microbiol 172:187–192. https://doi.org/10.1007/s002030050759
Ramı́rezGutierrezGschaedler JHA (2001) Optimization of astaxanthin production by Phaffia rhodozyma through factorial design and response surface methodology. J Biotechnol 88:259–268. https://doi.org/10.1016/S0168-1656(01)00279-6
Reynders MB, Rawlings DE, Harrison STL (1996) Studies on the growth. modelling and pigment production by the yeast Phaffia rhodozyma during fed-batch cultivation. Biotechnol Lett 18:649–654. https://doi.org/10.1007/BF00130759
Reynders MB, Rawlings DE, Harrison STL (1997) Demonstration of the Crabtree effect in Phaffia rhodozyma during continuous and fed-batch cultivation. Biotechnol Lett 19:549–552. https://doi.org/10.1023/A:1018341421122
Rosic NN (2019) Mycosporine-like amino acids: making the foundation for organic personalised sunscreens. Mar Drugs 17:638. https://doi.org/10.3390/md17110638
Rubinstein L, Altamirano A, Santopietro LD et al (1998) Isolation and characterization of Phaffia rhodozyma mutants. Folia Microbiol 43:626–630. https://doi.org/10.1007/BF02816380
Sakaki H, Nochide H, Nakanishi T et al (1999) Effect of culture condition on the biosynthesis of carotenoids in Rhodotorula glutinis No. 21. J Biosci Bioeng 3:400
Sanderson GW, Jolly SO (1994) The value of Phaffia yeast as a feed ingredient for salmonid fish. Aquaculture 124:193–200. https://doi.org/10.1016/0044-8486(94)90377-8
Santopietro LMD, Spencer JFT, Spencer DM et al (1998) Effects of oxidative stress on the production of carotenoid pigments by Phaffia rhodozyma (Xanthophyllomyces dendrorhous). Folia Microbiol 43:173–176. https://doi.org/10.1007/BF02816505
Schmid D, Schürch C, Zülli F (2006) Mycosporine-like amino acids from red algae protect against premature skin-aging. Euro Cosmet 9
Schmidt I, Schewe H, Gassel S et al (2011) Biotechnological production of astaxanthin with Phaffia rhodozyma/Xanthophyllomyces dendrorhous. Appl Microbiol Biotechnol 89:555–571. https://doi.org/10.1007/s00253-010-2976-6
Schroeder WA, Johnson EA (1995) Singlet oxygen and peroxyl radicals regulate carotenoid biosynthesis in Phaffia rhodozyma. J Biol Chem 270:18374–18379. https://doi.org/10.1074/jbc.270.31.18374
Sepúlveda D, Campusano S, Moliné M et al (2023) Unraveling the molecular basis of mycosporine biosynthesis in fungi. Int J Mol Sci 24:5930. https://doi.org/10.3390/ijms24065930
Shi Z, He X, Zhang H et al (2022) Whole genome sequencing and RNA-seq-driven discovery of new targets that affect carotenoid synthesis in Phaffia rhodozyma. Front Microbiol 13:837894. https://doi.org/10.3389/fmicb.2022.837894
Silva CM, Borba TM, Burkert CAV, Burkert JFM (2012) Carotenoid production by Phaffia rhodozyma using raw glycerol as an additional carbon source. Int J Food Eng 8. https://doi.org/10.1515/1556-3758.2843
Singh A, Čížková M, Bišová K et al (2021) Exploring mycosporine-like amino acids (MAAs) as safe and natural protective agents against UV-induced skin damage. Antioxidants 10:683. https://doi.org/10.3390/antiox10050683
Sommaruga R, Libkind D, van Broock M et al (2004) Mycosporine-glutaminol-glucoside. A UV-absorbing compound of two Rhodotorula yeast species. Yeast 21:1077–1081. https://doi.org/10.1002/yea.1148
Stachowiak B (2013a) Efficiency of selected mutagens in generating Xanthophyllomyces dendrorhous strains hyperproducing astaxanthin. Pol J Microbiol 62:67–72
Stachowiak B (2013b) Effect of illumination intensities on astaxanthin synthesis by Xanthophyllomyces dendrorhous and its mutants. Food Sci Biotechnol 22:1033–1038. https://doi.org/10.1007/s10068-013-0180-z
Stachowiak B, Szulc P (2021) Astaxanthin for the food industry. Molecules 26:2666. https://doi.org/10.3390/molecules26092666
Szafraniec K, Wloch DM, Sliwa P et al (2003) Small fitness effects and weak genetic interactions between deleterious mutations in heterozygous loci of the yeast Saccharomyces cerevisiae. Genet Res 82:19–31. https://doi.org/10.1017/S001667230300630X
Tognetti C, Moliné M, van Broock M et al (2013) Favored isolation and rapid identification of the astaxanthin-producing yeast Xanthophyllomyces dendrorhous (Phaffia rhodozyma) from environmental samples. J Basic Microbiol 53:766–772. https://doi.org/10.1002/jobm.201200274
Torres A, Hochberg M, Pergament I et al (2004) A new UV-B absorbing mycosporine with photo protective activity from the lichenized ascomycete Collema cristatum. Eur J Biochem 271:780–784. https://doi.org/10.1111/j.1432-1033.2004.03981.x
van Broock M, Libkind D, Moliné M (2009) Composiciones que absorben UVB y antioxidantes. Procedimientos y usos. Patente CONICET-UNComahue. Patent P090103845
Veal EA, Toone WM, Jones N et al (2002) Distinct roles for glutathione S-transferases in the oxidative stress response in Schizosaccharomyces pombe. J Biol Chem 277:35523–35531. https://doi.org/10.1074/jbc.M111548200
Villarreal P, Carrasco M, Barahona S et al (2016) Tolerance to ultraviolet radiation of psychrotolerant yeasts and analysis of their carotenoid, mycosporine, and ergosterol content. Curr Microbiol 72:94–101. https://doi.org/10.1007/s00284-015-0928-1
Volkmann M, Gorbushina AA (2006) A broadly applicable method for extraction and characterization of mycosporines and mycosporine-like amino acids of terrestrial, marine and freshwater origin. FEMS Microbiol Lett 255:286–295. https://doi.org/10.1111/j.1574-6968.2006.00088.x
Vustin MM, Belykh EN, Kishilova SA (2004) Relationship between astaxanthin production and the intensity of anabolic processes in the yeast Phaffia rhodozyma. Microbiology 73:643–649. https://doi.org/10.1007/s11021-005-0004-0
Yamane Y, Higashida K, Nakashimada Y et al (1997) Astaxanthin production by Phaffia rhodozyma enhanced in fed-batch culture with glucose and ethanol feeding. Biotechnol Lett 19:1109–1111. https://doi.org/10.1023/A:1018492611011
Yaqoob S, Riaz M, Shabbir A et al (2021) Commercialization and marketing potential of carotenoids. In: Zia-Ul-Haq M, Dewanjee S, Riaz M (eds) Carotenoids: structure and function in the human body. Springer, Cham, pp 799–826. https://doi.org/10.1007/978-3-030-46459-2_27
Zhang J, Li Q-R, Zhang M-H et al (2019) Enhancement of carotenoid biosynthesis in Phaffia rhodozyma PR106 under stress conditions. Biosci Biotechnol Biochem 83:2375–2385. https://doi.org/10.1080/09168451.2019.1650633
Zwietering MH, Jongenburger I, Rombouts FM, Van't Riet, KJAEM (1990) Modeling of the bacterial growth curve. Appl Environ Microbiol 56:1875–1881. https://doi.org/10.1128/aem.56.6.1875-1881.1990
Acknowledgements
This work was supported by Universidad Nacional del Comahue Project (project B247), CONICET (project PIP 11220200102948CO), and FONCYT (project PICT-2017-2083). We thank Julieta Burini and Mailen Latorre for providing a for critical reading and improving the writing style of the manuscript.
Funding
This work was supported by Universidad Nacional del Comahue Project (project B247), CONICET (project PIP 11220200102948CO), and FONCYT (project PICT-2017–2083).
Author information
Authors and Affiliations
Contributions
Martín Moliné (Conceptualization, Investigation, Formal analysis, Writing – original draft), Diego Libkind (Conceptualization, Writing – review & editing, Funding acquisition), and María van Broock (Conceptualization, Supervision).
Corresponding author
Ethics declarations
Competing interests
The authors have no relevant financial or non-financial interests to disclose. No conflict of interest exits in the submission of this manuscript.
Ethics approval
Not required.
Consent to participate/consent to publish
Not required.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Moliné, M., Libkind, D. & van Broock, M.R. Two at once: simultaneous increased production of astaxanthin and mycosporines in a single batch culture using a Phaffia rhodozyma mutant strain. World J Microbiol Biotechnol 40, 87 (2024). https://doi.org/10.1007/s11274-024-03901-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-024-03901-7