Skip to main content
Log in

Carotenoids from Rhodotorula and Phaffia: yeasts of biotechnological importance

  • Review
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

Carotenoids represent a group of valuable molecules for the pharmaceutical, chemical, food and feed industries, not only because they can act as vitamin A precursors, but also for their coloring, antioxidant and possible tumor-inhibiting activity. Animals cannot synthesize carotenoids, and these pigments must therefore be added to the feeds of farmed species. The synthesis of different natural commercially important carotenoids (β-carotene, torulene, torularhodin and astaxanthin) by several yeast species belonging to the genera Rhodotorula and Phaffia has led to consider these microorganisms as a potential pigment sources. In this review, we discuss the biosynthesis, factors affecting carotenogenesis in Rhodotorula and Phaffia strains, strategies for improving the production properties of the strains and directions for potential utility of carotenoid-synthesizing yeast as a alternative source of natural carotenoid pigments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Johnson E, Schroeder W (1995) In: Fiechter A (ed) Microbial carotenoids. Advances in biochemical engineering/biotechnology, vol 53. Springer, Berlin, pp 119–178

  2. Bhosale P, Bernstein PS (2004) β-Carotene production by Flavobacterium multivorum in the presence of inorganic salts and urea. J Ind Microbiol Biotechnol 31:565–571. doi:10.1007/s10295-004-0187-9

    PubMed  CAS  Google Scholar 

  3. Chen D, Han Y, Gu Z (2006) Application of statistical methodology to the optimization of fermentative medium for carotenoids production by Rhodobacter sphaeroides. Process Biochem 41:1773–1778. doi:10.1016/j.procbio.2006.03.023

    CAS  Google Scholar 

  4. Jeon YC, Cho WC, Yun Y (2006) Combined effects of light intensity and acetate concentration on the growth of unicellular microalga Haematococcus pluvialis. Enzyme Microb Technol 39:490–495. doi:10.1016/j.enzmictec.2005.12.021

    CAS  Google Scholar 

  5. Raja R, Haemaiswarya S, Rengasamy R (2007) Exploitation of Dunaliella for β-carotene production. Appl Microbiol Biotechnol 74:517–523. doi:10.1007/s00253-006-0777-8

    PubMed  CAS  Google Scholar 

  6. Kuzina V, Cerda-Olmedo E (2006) Modification of sexual development and carotene production by acetate and other small carboxylic acids in Blakeslea trispora and Phycomyces blakesleanus. Appl Environ Microbiol 72:4917–4922. doi:10.1128/AEM.02845-05

    PubMed  CAS  Google Scholar 

  7. Nanou K, Roukas T, Kotzekidou P (2007) Role of hydrolytic enzymes and oxidative stress in autolysis and morphology of Blakeslea trispora during β-carotene production in submerged fermentation. Appl Microbiol Biotechnol 74:447–453. doi:10.1007/s00253-006-0666-1

    PubMed  CAS  Google Scholar 

  8. An G, Jang B, Cho M (2001) Cultivation of the carotenoid-hyperproducing mutant 2A2n of the red yeast Xanthophyllomyces dendrorhous (Phaffia rhodozyma) with molasses. J Biosci Bioeng 92:121–125. doi:10.1263/jbb.92.121

    PubMed  CAS  Google Scholar 

  9. Bhosale P, Gadre RV (2001) Optimization of carotenoid production from hyper-producing Rhodotorula glutinis mutant 32 by a factorial approach. Lett Appl Microbiol 33:12–16. doi:10.1046/j.1472-765X.2001.00940.x

    PubMed  CAS  Google Scholar 

  10. Bhosale P, Gadre RV (2001) β-Carotene production in sugarcane molasses by a Rhodotorula glutinis mutant. J Ind Microbiol Biotechnol 26:327–332. doi:10.1038/sj.jim.7000138

    PubMed  CAS  Google Scholar 

  11. Buzzini P, Martin A (1999) Production of carotenoids by strains of Rhodotorula glutinis cultured in raw materials of agro-industrial origin. Bioresour Technol 71:41–44. doi:10.1016/S0960-8524(99)00056-5

    Google Scholar 

  12. Buzzini P, Martini A, Gaetani M, Turchetti B, Pagnoni UM, Davoli P (2005) Optimization of carotenoid production by Rhodotorula graminis DBVPG 7021 as a function of trace element concentration by means of response surface analysis. Enzyme Microb Technol 36:687–692. doi:10.1016/j.enzmictec.2004.12.028

    CAS  Google Scholar 

  13. Davoli P, Weber RWC (2002) Carotenoid pigments from the red mirror yeast, Sporobolomyces roseus. Mycologist 16:102–108. doi:10.1017/S0269915X02001027

    Google Scholar 

  14. Flores-Cotera LB, Martin R, Sanchez S (2001) Citrate, a possible precursor of astaxanthin in Phaffia rhodozyma: influence of varying levels of a ammonium, phosphate and citrate in a chemically defined medium. Appl Microbiol Biotechnol 55:341–347. doi:10.1007/s002530000498

    PubMed  CAS  Google Scholar 

  15. Frengova G, Simova E, Pavlova K, Beshkova D, Grigorova D (1994) Formation of carotenoids by Rhodotorula glutinis in whey ultrafiltrate. Biotechnol Bioeng 44:888–894. doi:10.1002/bit.260440804

    PubMed  CAS  Google Scholar 

  16. Frengova GI, Simova ED, Beshkova DM (2003) Carotenoid production by lactoso-negative yeasts co-cultivated with lactic acid bacteria in whey ultrafiltrate. Z Naturforsch 58c:562–567

    Google Scholar 

  17. Hu ZC, Zeng YG, Wang Z, Shen YC (2006) pH control strategy in astaxanthin fermentation bioprocess by Xanthophyllomyces dendrorhous. Enzyme Microb Technol 39:586–590. doi:10.1016/j.enzmictec.2005.11.017

    CAS  Google Scholar 

  18. Libkind D, van Brook M (2006) Biomass and carotenoid pigment production by Patagonian native yeasts. World J Microbiol Biotechnol 22:687–692. doi:10.1007/s11274-005-9091-3

    CAS  Google Scholar 

  19. Liu YS, Wu JY (2006) Use of n-hexadecane as an oxygen vector to imorove Phaffia rhodozyma growth and carotenoid production in shake-flask cultures. J Appl Microbiol 101:1033–1038. doi:10.1111/j.1365-2672.2006.03009.x

    PubMed  CAS  Google Scholar 

  20. Martin A, Acheampong E, Patel T, Chornet E (1993) Study of growth parameters for Phaffia rhodozyma cultivated in peat hydrolysates. Appl Biochem Biotechnol 37:235–241. doi:10.1007/BF02788875

    Google Scholar 

  21. Martin A, Lu C, Patel T (1993) Growth parameters for the yeast Rhodotorula rubra grown in peat extracts. J Ferment Bioeng 76:321–325. doi:10.1016/0922-338X(93)90202-J

    CAS  Google Scholar 

  22. Ni H, Chen Q, Ruan H, Yang Y, Li L, Wu G, Hu Y, He G (2007) Studies on optimization of nitrogen sources for astaxanthin production by Phaffia rhodozyma. J Zhejiang Univ Sci B 8:365–370. doi:10.1631/jzus.2007.B0365

    PubMed  CAS  Google Scholar 

  23. Perrier V, Dubreucq E, Galzy P (1995) Fatty acid and carotenoid composition of Rhodotorula strains. Arch Microbiol 164:173–179. doi:10.1007/BF02529968

    PubMed  CAS  Google Scholar 

  24. Simova ED, Frengova GI, Beshkova DM (2004) Synthesis of carotenoids by Rhodotorula rubra GED8 co-cultivated with yogurt starter cultures in whey ultrafiltrate. J Ind Microbiol Biotechnol 31:115–121. doi:10.1007/s10295-004-0122-0

    PubMed  CAS  Google Scholar 

  25. Somashekar D, Joseph R (2000) Inverse relationship between carotenoid and lipid formation in Rhodotorula gracilis according to the C/N ratio of the growth medium. World J Microbiol Biotechnol 16:491–493. doi:10.1023/A:1008917612616

    CAS  Google Scholar 

  26. Sperstad S, Lutnaes BF, Stormo SK, Liaaen-Jensen S, Landfald B (2006) Torularhodin and torulene are the major contributors to the carotenoid pool of marine Rhodosporidium babjevae (Golubev). J Ind Microbiol Biotechnol 33:269–273. doi:10.1007/s10295-005-0065-0

    PubMed  CAS  Google Scholar 

  27. Tada M, Shiroishi M (1982) Mechanism of photoregulated carotenogenesis in Rhodotorula minuta. I. Photocontrol of carotenoid production. Plant Cell Physiol 23:541–547

    CAS  Google Scholar 

  28. Tinoi J, Rakariyatham N, Deming RL (2006) Utilization of mustard waste isolated for improved production of astaxanthin by Xanthophyllomyces dendrohous. J Ind Microbiol Biotechnol 33:309–314. doi:10.1007/s10295-005-0054-3

    PubMed  CAS  Google Scholar 

  29. Weber RWC, Madhour A, Anke H, Mucci A, Davoli P (2005) 2-Hydroxytorularhodin, a new xanthophylls from the red yeast Sporobolomyces coprosmae. Helv Chim Acta 88:2960–2966. doi:10.1002/hlca.200590239

    CAS  Google Scholar 

  30. Zalashko M (1990) In: Solokova E (ed) Biotechnology of milk whey processing. Science Press, Moscow, pp 161–163

  31. Zheng YG, Hu ZC, Wang Z, Shen YC (2006) Large-scale production of astaxanthin by Xanthophyllomyces dendrorhous. Food Bioprod Process 84:164–166. doi:10.1205/fbp.05030

    CAS  Google Scholar 

  32. Britton G (1995) Structure and properties of carotenoids in relation to fuction. FASEB J 9:1551–1558

    PubMed  CAS  Google Scholar 

  33. Bast A, Haenen GRM, van den Berg R, van den Berg H (1998) Antioxidant effects of carotenoids. Int J Vitam Nutr Res 68:3999–4003

    Google Scholar 

  34. Hughes DA (1999) Beta-carotene and immune function: is it a case of defining the right intake? Nutr 15:405–407. doi:10.1016/S0899-9007(99)00025-8

    CAS  Google Scholar 

  35. Jimenez-Escrig A, Jimenez-Jimenez I, Sanchez-Moreno C, Saura-Calixto F (2000) Evaluation of free radical scavenging of dietary carotenoids by the stable radical 2,2-diphenyl-1-picrylhydrazyl. J Sci Food Agric 80:1686–1690. doi :10.1002/1097-0010(20000901)80:11<1686::AID-JSFA694>3.0.CO;2-Y

    CAS  Google Scholar 

  36. Kiokias S, Gordon MH (2004) Antioxidant properties of carotenoids in vitro and in vivo. Food Rev Int 20:99–121. doi:10.1081/FRI-120037155

    CAS  Google Scholar 

  37. Lee JH, Ozcelik B, Min DB (2003) Electron donation mechanisms of β-carotene as a free radical scavenger. J Food Sci 68:861–865. doi:10.1111/j.1365-2621.2003.tb08256.x

    CAS  Google Scholar 

  38. Simpson K (1983) Relative value of carotenoids as precursors of vitamin A. Proc Nutr Soc 2:7–17

    Google Scholar 

  39. Baker R, Guenther C (2004) The role of carotenoids in consumer choice and the likely benefits from their inclusion into products for human consumption. Trends Food Sci Technol 15:484–488. doi:10.1016/j.tifs.2004.04.0094

    CAS  Google Scholar 

  40. Berset C (1999) The multiple effects of carotenoids. Med Nutr 35:215–223

    CAS  Google Scholar 

  41. Clark RM, Herron KL, Waters D, Fernandez ML (2006) Hypo- and hyperresponse to egg cholesterol predicts plasma lutein and β-carotene concentrations in men and women. J Nutr 136:601–607

    PubMed  CAS  Google Scholar 

  42. Forman MR, Hursting SD, Umar A, Barret JC (2004) Nutrition and cancer prevention: a multidisciplinary perspective on human trials. Annu Rev Nutr 24:223–254. doi:10.1146/annurev.nutr.24.012003.132315

    PubMed  CAS  Google Scholar 

  43. Goswami UC, Sharma N (2005) Efficience of a few retinoids and carotenoids in vivo in controlling benzo[α] pyrene-induced forestomach tumor in female Swiss mice. Br J Nutr 94:540–543. doi:10.1079/BJN20051484

    PubMed  CAS  Google Scholar 

  44. Henneckens CH (1997) β-Carotene supplementation and cancer prevention. Nutrition 13:697–699. doi:10.1016/S0899-9007(97)83019-5

    Google Scholar 

  45. Bendich A, Olson JA (1989) Biological actions of carotenoids. FASEB J 3:1927–1932

    PubMed  CAS  Google Scholar 

  46. van den Berg H, Faulks R, Fernando-Granado H, Hirschberg J, Olmedilla B, Sandmann G, Southon S, Stath W (2000) The potential for the improvement of carotenoid levels in foods and the likely systemic effects. J Sci Food Agric 80:880–912. doi :10.1002/(SICI)1097-0010(20000515)80:7<880::AID-JSFA646>3.0.CO;2-1

    Google Scholar 

  47. Choubert G, Mendes-Pinto MM, Morais R (2006) Pigmenting efficacy of astaxanthin fed to rainbow trout Oncorhynchus mykiss: effect of dietary astaxanthin and lipid sources. Aquaculture 257:429–436. doi:10.1016/j.aquaculture.2006.02.055

    CAS  Google Scholar 

  48. Frankis F (2000) Carotenoids as food colorants. J Cereal Food World 45:198–203

    Google Scholar 

  49. Leeason S, Caston I (2004) Enrichment of eggs with lutein. Poult Sci 83:1709–1712

    Google Scholar 

  50. Tantillo G, Storelli MM, Aprile A, Matrella R (2000) Quantitative and legislative aspects regarding canthxanthin and astaxanthin in smoked salmon fillets. Ital J Food Sci 12:463–468

    CAS  Google Scholar 

  51. Ausich RL (1997) Commercial opportunities for carotenoid production by biotechnology. Pure Appl Chem 69:2169–2173. doi:10.1351/pac199769102169

    CAS  Google Scholar 

  52. Lee PC, Schmidt-Dannert C (2002) Metabolic engineering towards biotechnological production of carotenoids in microorganisms. Appl Microbiol Biotechnol 60:1–11

    PubMed  CAS  Google Scholar 

  53. Nelis HJ, De Leenheer AP (1991) Microbial sources of carotenoid pigments used in foods and feeds. J Appl Bacteriol 70:181–191

    CAS  Google Scholar 

  54. Coulson J (1980) Miscellaneous naturally occurring coloring materials for food stuff. In: Walford J (ed) Developments in food colour. Applied Science, London, pp 189–218

    Google Scholar 

  55. Counsell J (1980) Some synthetic carotenoids as food colours. In: Walford J (ed) Developments in food colour. Applied Science, London, pp 151–187

    Google Scholar 

  56. De Haan A, Burke R, Bont J (1991) Microbial production of food colorants. Med Fac Landbouww Rijisuniv Gent 56:1655–1660

    Google Scholar 

  57. Simpson KL, Nakayama TOM, Chichester CO (1964) Biosynthesis of yeast carotenoids. J Bacteriol 88:1688–1694

    PubMed  CAS  Google Scholar 

  58. Goodwin TW (1980) Biosynthesis of carotenoids. In: Goodwin TW (ed) The biochemistry of the carotenoids, vol 1. Chapman and Hall, London, pp 33–76

  59. Goodwin TW (1993) Biosynthesis of carotenoids: an overview. In: Packer L (ed) Methods in enzymology carotenoids. Part B. Metabolism, genetic and biosynthesis, vol 214. Academic, San Diego, pp 330–340

  60. Andrewes AG, Phaffia HJ, Starr MP (1976) Carotenoids of Phaffia rhodozyma, a red-pigmented fermenting yeast. Phytochemistry 15:1003–1007. doi:10.1016/S0031-9422(00)84390-3

    CAS  Google Scholar 

  61. Johnson EA, Lewis M (1979) Astaxanthin formation by the yeast Phaffia rhodozyma. J Gen Microbiol 115:173–183

    CAS  Google Scholar 

  62. An G, Schuman D, Johnson E (1989) Isolation of Phaffia rhodozyma mutants with increased astaxanthin content. Appl Environ Microbiol 55:116–124

    PubMed  CAS  Google Scholar 

  63. Buzzini P (2000) An optimization study of carotenoid production by Rhodotorula glutinis DBVPG 3853 from substrates containing concentrated rectified grape must as the sole carbohydrate source. J Ind Microbiol Biotechnol 24:41–45. doi:10.1038/sj.jim.2900765

    CAS  Google Scholar 

  64. Buzzini P (2001) Batch and fed-batch carotenoid production by Rhodotorula glutinis-Debaryomyces castelli co-cultures in corn syrup. J Appl Microbiol 90:843–847. doi:10.1046/j.1365-2672.2001.01319.x

    PubMed  CAS  Google Scholar 

  65. Davoli P, Mierau V, Weber RWS (2004) Carotenoids and fatty acids in red yeasts Sporobolomyces roseus and Rhodotorula glutinis. Appl Biochem Microbiol 40:392–397. doi:10.1023/B:ABIM.0000033917.57177.f2

    CAS  Google Scholar 

  66. Frengova G, Simova E, Beshkova D (2004) Improvement of carotenoid-synthesizing yeast Rhodotorula rubra by chemical mutagenesis. Z Naturforsch 59c:99–103

    Google Scholar 

  67. Frengova G, Simova E, Beshkova D (2004) Use of whey ultrafiltrate as a substrate for production of carotenoids by the yeast Rhodotorula rubra. Appl Biochem Biotechnol 112:133–141. doi:10.1385/ABAB:112:3:133

    PubMed  CAS  Google Scholar 

  68. Cruz JM, Parajo JC (1998) Improved astaxanthin production by Xanthophyllomyces dendrorhous growing on enzymatic wood hydrolysates containing glucose and cellobiose. Food Chem 63:479–484. doi:10.1016/S0308-8146(98)00061-2

    CAS  Google Scholar 

  69. Fontana JD, Chocial MB, Baron M, Guimaraes MF, Maraschin M, Ulhoa C, Florencio JA, Bonfim TMB (1997) Astaxanthinogenesis in the yeast Phaffia rhodozyma. Optimization of low-cost culture media and yeast cell wall lysis. Appl Biochem Biotechnol 63:305–314. doi:10.1007/BF02920432

    PubMed  Google Scholar 

  70. Hu ZC, Zheng YG, Wang Z, Shen YC (2005) Effect of sugar-feeding strategies on astaxanthin production by Xanthophyllomyces dendrorhous. World J Microbiol Biotechnol 21:771–775. doi:10.1007/s11274-004-5566-x

    Google Scholar 

  71. Kusdiyantini E, Gaudin P, Goma G, Blanc PJ (1998) Growth kinetics and astaxanthin production of Phaffia rhodozyma on glycerol as a carbon source during batch fermentation. Biotechnol Lett 20:929–934. doi:10.1023/A:1005345224510

    CAS  Google Scholar 

  72. Longo E, Siero C, Velazquez JB, Calo P, Cansado J, Villa TG (1992) Astaxanthin production from Phaffia rhodozyma. Biotechnol Forum Eur 9:565–567

    CAS  Google Scholar 

  73. Moriel DG, Chociai MB, Machado IMP, Fontana JD, Bonfim TMB (2005) Effect of feeding methods on the astaxanthin production by Phaffia rhodozyma in fed-batch process. Braz Arch Biol Technol 48:397–401. doi:10.1590/S1516-89132005000300010

    Google Scholar 

  74. Parajo JC, Santos V, Vazguez M (1998) Optimization of carotenoid production by Phaffia rhodozyma cells grown on xylose. Process Biochem 2:181–187. doi:10.1016/S0032-9592(97)00045-9

    Google Scholar 

  75. Parajo JC, Santos V, Vazguez M (1998) Production of carotenoids by Phaffia rhodozyma growing on media made from hemicellulosic hydrolysates of eucalyptus globulus wood. Biotechnol Bioeng 59:501–506. doi :10.1002/(SICI)1097-0290(19980820)59:4<501::AID-BIT13>3.0.CO;2-C

    PubMed  CAS  Google Scholar 

  76. Ramirez J, Obledo N, Arellano M, Herrera E (2006) Astaxanthin production by Phaffia rhodozyma in a fed-batch culture using a low cost medium feeding. E-Gnosis 4:1–9

    Google Scholar 

  77. Vazquez M, Martin AM (1998) Mathematical model for Phaffia rhodozyma growth using peat hydrolysates as substrate. J Sci Food Agric 76:481–487. doi :10.1002/(SICI)1097-0010(199804)76:4<481::AID-JSFA973>3.0.CO;2-Z

    CAS  Google Scholar 

  78. Sguina FM, Yamashita F, Pereira JL, Mercadante AZ (2002) Production of carotenoids by Rhodotorula rubra and Rhodotorula glutinis in culture medium supplemented with sugar cane juice. Food Biotechnol 16:227–235. doi:10.1081/FBT-120016776

    Google Scholar 

  79. Goodwin TW (1972) Carotenoids in fungi and non-photosynthetic bacteria. Prog Ind Microbiol 11:29–88

    PubMed  CAS  Google Scholar 

  80. Bhosale P, Gadre RV (2002) Manipulation of temperature and illumination conditions for enhanced β-carotene production by mutant 32 of Rhodotorula glutinis. Lett Appl Microbiol 34:349–353. doi:10.1046/j.1472-765X.2002.01095.x

    PubMed  CAS  Google Scholar 

  81. Chan HY, Ho KP (1999) Growth and carotenoid production by pH-stat cultures of Phaffia rhodozyma. Biotechnol Lett 21:953–958. doi:10.1023/A:1005638610564

    CAS  Google Scholar 

  82. Hu ZC, Zheng YG, Wang Z, Shen YC (2007) Production of astaxanthin by Xanthophyllomyces dendrorhous ZJUT46 with fed-batch fermentation in 2.0 m3 fermentor. Food Technol Biotechnol 45:209–212

    CAS  Google Scholar 

  83. Kim JH, Kang SW, Kim SW, Chang HI (2005) High-level production of astaxanthin by Xanthophyllomyces dendrorhous mutant JH1 using statistical experimental designs. Biosci Biotechnol Biochem 69:1743–1748. doi:10.1271/bbb.69.1743

    PubMed  CAS  Google Scholar 

  84. Latha BV, Jeevaratnam K, Murali HS, Manja KS (2005) Influence of growth factors on carotenoid pigmentation of Rhodotorula glutinis DER-PDY from natural source. Indian J Biotechnol 4:353–357

    CAS  Google Scholar 

  85. Sun N, Lee S, Song KB (2004) Characterization of a carotenoid-hyperproducing yeast mutant isolated by low-dose gamma irradiation. Int J Food Microbiol 94:263–267. doi:10.1016/S0168-1605(03)00311-8

    PubMed  CAS  Google Scholar 

  86. Vijayalakshmi G, Shobha B, Vanajakshi V, Divakar S, Manohar B (2001) Response surface methodology for optimization of growth parameters for the production of carotenoids by a mutasnt strain of Rhodotorula gracilis. Eur Food Res Technol 213:234–239. doi:10.1007/s002170100356

    CAS  Google Scholar 

  87. Polulyakh OV, Podoprigova OI, Eliseev SA, Ershov YV, Bykhovsky VY, Dmitrovski AA (1991) Biosynthesis of torulene and torularhodin in the yeast Phaffia rhodozyma. Prikl Biokhim Mikrobiol 27:541–545

    CAS  Google Scholar 

  88. Wang SL, Zhang X, Zhang H, Lin K (2001) Effects of some additives on the growth and carotenoids content of Rhodotorula. Food Sci Technol 2:20–21

    Google Scholar 

  89. Meyer P, Du Preez J (1994) Astaxanthin production by a Phaffia rhodozyma mutant on grape juice. World J Microbiol Biotechnol 10:178–183. doi:10.1007/BF00360882

    CAS  Google Scholar 

  90. Vazquez M, Martin AM (1998) Optimization of Phaffia rhodozyma continuous culture through response surface methodology. Biotechnol Bioeng 57:314–320. doi :10.1002/(SICI)1097-0290(19980205)57:3<314::AID-BIT8>3.0.CO;2-K

    PubMed  CAS  Google Scholar 

  91. Tinoi J, Rakariyatham N, Deming RL (2005) Simplex optimization of carotenoid production by Rhodotorula glutinis using hydrolyzed mung bean waste flour as substrate. Process Biochem 40:2551–2557. doi:10.1016/j.procbio.2004.11.005

    CAS  Google Scholar 

  92. Aksu Z, Eren AT (2005) Carotenoids production by the yeast Rhodotorula mucilaginosa: use of agricultural wastws as a carbon source. Process Biochem 40:2985–2991. doi:10.1016/j.procbio.2005.01.011

    CAS  Google Scholar 

  93. Park PK, Cho DH, Kim EY, Chu KH (2005) Optimization of carotenoid production by Rhodotorula glutinis using statistical experimental design. World J Microbiol Biotechnol 21:429–434. doi:10.1007/s11274-004-1891-3

    CAS  Google Scholar 

  94. Jacobson CK, Jolly SO, Sedmark JJ, Skatrud TJ, Wasilevski JM (2000) Astaxanthin over-producing strains of Phaffia rhodozyma. Method for their cultivation and their use in animal feeds. US Patent 6015684

  95. Kesava SS, An GH, Kim CH, Rhee SK, Choi ES (1998) An industrial medium for improved production of carotenoids from a mutant strain of Phaffia rhodozyma. Bioprocess Biosyst Eng 19:165–170

    CAS  Google Scholar 

  96. Demain A, Phaff H, Kurtzzmanu C (1998) The industrial importance of yeasts. In: Kurtzmann C, Fell J (eds) The yeasts. A taxonomic study. Elsevier, Amsterdam, pp 13–19

    Google Scholar 

  97. 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. doi:10.1023/A:1018341421122

    CAS  Google Scholar 

  98. Ramirez J, Gutierrer H, Gschaedler A (2001) Optimization of astaxanthin production by Phaffia rhodozyma through factorial design and response surface methodology. J Biotechnol 88:259–268. doi:10.1016/S0168-1656(01)00279-6

    PubMed  CAS  Google Scholar 

  99. Yamane YI, Higashida K, Nakashimada Y, Kakizono T, Nishio N (1997) Influence of oxygen and glucose on primary metabolism and astaxanthin production by Phaffia rhodozyma in batch and fed-batch cultures: kinetic and stoichiometric analysis. Appl Environ Microbiol 63:4471–4478

    PubMed  CAS  Google Scholar 

  100. Bhosale P, Gadre RV (2001) Production of β-carotene by a mutant of Rhodotorula glutinis. Appl Microbiol Biotechnol 55:423–427. doi:10.1007/s002530000570

    PubMed  CAS  Google Scholar 

  101. Girard P, Falconnier B, Bricout J, Vladescu B (1994) β-Carotene producing mutants of Phaffia rhodozyma. Appl Microbiol Biotechnol 41:183–191. doi:10.1007/BF00186957

    CAS  Google Scholar 

  102. Kim JH, Kim CW, Chang HI (2004) Screening and characterization of red yeast Xanthophyllomyces dendrorhous mutants. J Microbiol Biotechnol 14:570–575

    CAS  Google Scholar 

  103. Kim SK, Lee JH, Lee CH, Yoon YC (2007) Increased carotenoid production in Xanthophyllomyces dendrorhous G276 using plant extracts. J Microbiol 45:128–132

    PubMed  CAS  Google Scholar 

  104. Ramirez J, Nunez ML, Valdivia R (2000) Increased astaxanthin production by a Phaffia rhodozyma mutant grown on date juice from Yucca fillifera. J Ind Microbiol Biotechnol 24:187–190. doi:10.1038/sj.jim.2900792

    CAS  Google Scholar 

  105. Wang SL, Sun JS, Han BZ, Wu XZ (2007) Optimization of β-carotene production by Rhodotorula glutinis using high hydrostatic pressure and response surface methodology. J Food Sci 72:325–329. doi:10.1111/j.1750-3841.2007.00495.x

    Google Scholar 

  106. Girard P, Javelot C, Vladescu B (1997) Phaffia rhodozyma mutants, process for producing β-carotene rich biomass. US Patent 5691190

  107. De Boer L, Van Hell B, Krouwer AJJ (1999) Strains of Phaffia rhodozyma containing high levels of astaxanthin and low levels of 3-hydroxy-3′,4′-didehydro-β, ψ-caroten-4-one (HDCO). US Patent 5879927

  108. Puchala M, Schessler H (1993) Oxygen effect in the radiolysis of proteins. Int J Radiat Biol 64:149–156. doi:10.1080/09553009314551231

    PubMed  CAS  Google Scholar 

  109. Nagy A, Palagyi Z, Ferenczy L, Vagvolgyi C (1997) Radiation-induced chromosomal rearrangement as an aid to analysis of the genetic constitution of Phaffia rhodozyma. FEMS Microbiol Lett 152:249–254. doi:10.1111/j.1574-6968.1997.tb10435.x

    PubMed  CAS  Google Scholar 

  110. Schroeder WA, Calo P, DeClercq ML, Johnson EA (1996) Selection for carotenogenesis in the yeast Phaffia rhodozyma by dark-generated singlet oxygen. Microbiology 142:2923–2929

    Article  CAS  Google Scholar 

  111. Schroeder WA, Johnson EA (1995) Singlet oxygen and peroxyl radicals regulate carotenoid biosynthesis in Phaffia rhodozyma. J Biol Chem 270:18374–18379. doi:10.1074/jbc.270.31.18374

    PubMed  CAS  Google Scholar 

  112. Schuessler H, Schilling K (1984) Oxygen effect in the radiolysis of proteins. Int J Radiat Biol 45:267–281. doi:10.1080/09553008414550381

    CAS  Google Scholar 

  113. Fleno B, Christensen I, Larsen R, Johansen SR, Johnson E (1997) Astaxanthin-producing yeast cells, methods for their preparation and their use. US Patent 5599711

  114. Calo P, Miguel T, Velazquez JB, Villa TG (1995) Mevalonic acid increases trans-astaxanthin and carotenoid biosynthesis in Phaffia rhodozyma. Biotechnol Lett 17:575–578. doi:10.1007/BF00129380

    CAS  Google Scholar 

  115. Hoshino T, Masuda S, Setoguchi Y (2005) Process for producing carotenoids. US Patent 2005/0260700 A1

  116. Verdoes JC, Sandmann G, Visser H, Diaz M, Van Mossel M, Van Ooyen AJJ (2003) Metabolic engineering of the carotenoid biosynthetic pathway in the yeast Xanthophyllomyces dendrorhous (Phaffia rhodozyma). Appl Environ Microbiol 69:3728–3738. doi:10.1128/AEM.69.7.3728-3738.2003

    PubMed  CAS  Google Scholar 

  117. Miura Y, Kondo K, Saito T, Shimada H, Fraser PD, Misawa N (1998) Production of the carotenoids lycopene, β-carotene, and astaxanthin in the food yeast Candida utilis. Appl Environ Microbiol 64:1226–1229

    PubMed  CAS  Google Scholar 

  118. Verwaal R, Wang J, Meijnen JP, Visser H, Sandmann G, Van den Berg J, Van Ooyen AJJ (2007) High-level production of beta-carotene in Saccharomyces cerevisiae by successive transformation with carotenogenic genes from Xanthophyllomyces dendrorhous. Appl Environ Microbiol 73:4342–4350. doi:10.1128/AEM.02759-06

    PubMed  CAS  Google Scholar 

  119. Tada M, Tsubouchi M, Matsuo K, Takimoto H, Kimura Y, Takagi S (1990) Mechanism of photoregulated carotenogenesis in Rhodotorula minuta. VIII. Effect of mevinolin on photoinduced carotenogenesis. Plant Cell Physiol 31:319–323

    CAS  Google Scholar 

  120. Sakaki H, Nakanishi T, Tada A, Miki W, Komemushi S (2001) Activation of torularhodin production by Rhodotorula glutinis using weak white light irradiation. J Biosci Bioeng 92:294–297. doi:10.1263/jbb.92.294

    PubMed  CAS  Google Scholar 

  121. An GH, Johnson EA (1990) Influence of light on growth and pigmentation of the yeast Phaffia rhodozyma. Antonie Van Leeuwenhoek 57:91–103. doi:10.1007/BF00400151

    Google Scholar 

  122. Vazquez M (2001) Effect of the light on carotenoid profiles on Xanthophyllomyces dendrorhous strains (formely Phaffia rhodozyma). Food Technol Biotechnol 39:123–128

    CAS  Google Scholar 

  123. Ducrey Sanpietro LM, Kula MR (1998) Studies of astaxanthin biosynthesis in Xanthophyllomyces dendrorhous (Phaffia rhodozyma). Effect of inhibitors and low temperature. Yeast 14:1007–1016. doi :10.1002/(SICI)1097-0061(199808)14:11<1007::AID-YEA307>3.0.CO;2-U

    PubMed  CAS  Google Scholar 

  124. Frengova GI, Simova ED, Beshkova DM (1995) Effect of temperature changes on the production of yeast pigments co-cultivated with lacto-acid bacteria in whey ultrafiltrate. Biotechnol Lett 17:1001–1006. doi:10.1007/BF00127443

    CAS  Google Scholar 

  125. Hayman EP, Yokoyama H, Chichester CO, Simpson KL (1974) Carotenoid biosynthesis in Rhodotorula glutinis. J Bacteriol 120:1339–1343

    PubMed  CAS  Google Scholar 

  126. Simova ED, Frengova GI, Beshkova DM (2003) Effect of aeration on the production of carotenoid pigments by Rhodotorula rubra-Lactocacillus casei subsp. casei co-cultures in whey ultrafiltrate. Z Naturforsch 58c:225–229

    Google Scholar 

  127. Sakaki H, Nochide H, Nakanishi T, Miki W, Fujita T, Komemushi S (1999) Effects of culture conditions on the biosynthesis of carotenoids in Rhodotorula glutinis N21. Seibutsu-kogaku Kaishi 77:55–59

    CAS  Google Scholar 

  128. Komemushi S, Sakaki H, Yokoyama H, Fujita T (1994) Effect of barium and other metals on the growth of a d-lactic acid assimilating yeast Rhodotorula glutinis N21. J Antibact Antifung Agt 22:583–587

    CAS  Google Scholar 

  129. An GH, Chang KW, Johnson EA (1996) Effect of oxygen radicals and aeration on carotenogenesis and growth of Phaffia rhodozyma (Xanthophyllomyces dendrorhous). J Microbiol Biotechnol 6:103–109

    CAS  Google Scholar 

  130. An GH, Jang BG, Sun OS, Kim CJ, Song KB (2001) Iron (III) decreases astaxanthin production in Phaffia rhodozyma (Xanthophyllomyces dendrorhous). Food Sci Biotechnol 10:204–207

    Google Scholar 

  131. Flores-Cotera LB, Sanchez S (2001) Copper but not iron limitation increases astaxanthin production by Phaffia rhodozyma in a chemically defined medium. Biotechnol Lett 23:793–797. doi:10.1023/A:1010358517806

    CAS  Google Scholar 

  132. Culotta VC, Liu SJ, Schmidt P, Klomp LW, Casareno RL, Gitlin J (1999) Intracellular pathways of copper trafficking in yeast and humans. Adv Exp Med Biol 448:247–254

    PubMed  CAS  Google Scholar 

  133. Tamai KT, Gralla EB, Ellerby LM, Valentine JS, Thiele DJ (1993) Yeast and mammalian metallothioneins functionally substitute for yeast copper-zinc superoxide dismutase. Proc Natl Acad Sci USA 90:8013–8017. doi:10.1073/pnas.90.17.8013

    PubMed  CAS  Google Scholar 

  134. Kim SJ, Kim GJ, Park DH, Ryu YW (2003) High-level production of astaxanthin by fed-batch culture of mutant strain Phaffia rhodozyma AJ–6–1. J Microbiol Biotechnol 13:175–181

    CAS  Google Scholar 

  135. Yamane Y, Higashida K, Nakashimada Y, Kakizono T, Nishio N (1997) Astaxanthin production by Phaffia rhodozyma enhanced in fed-batch culture with glucose and ethanol feeding. Biotechnol Lett 19:1109–1111. doi:10.1023/A:1018492611011

    CAS  Google Scholar 

  136. Gu WL, An GH, Johnson EA (1997) Ethanol increases carotenoid production in Phaffia rhodozyma. J Ind Microbiol Biotechnol 19:114–117. doi:10.1038/sj.jim.2900425

    PubMed  CAS  Google Scholar 

  137. Hoshino T, Ojima K, Setoguchi Y (2001) 3-Hydroxy-3-methylglutaral-CoA reductase polynucleotides in isoprenoid production. US Patent 6284506

  138. Kim BK, Park PK, Chae HJ, Kim EY (2004) Effect of phenol on β-carotene content in total carotenoids production in cultivation of Rhodotorula glutinis. Korean J Chem Eng 21:689–692. doi:10.1007/BF02705506

    CAS  Google Scholar 

  139. Liu YS, Wu JY (2006) Hydrogen peroxide-induced astaxanthin biosynthesis and catalase activity in Xanthophyllomyces dendrorhous. Appl Microbiol Biotechnol 73:663–668. doi:10.1007/s00253-006-0501-8

    PubMed  CAS  Google Scholar 

  140. Echavarri-Erasun C, Johnson EA (2004) Stimulation of astaxanthin formation in the yeast Xanthophyllomyces dendrorhous by the fungus Epicoccum nigrum. FEMS Yeast Res 4:511–519. doi:10.1016/S1567-1356(03)00177-6

    PubMed  CAS  Google Scholar 

  141. Wang W, Yu L, Zhou P (2006) Effects of different fungal elicitors on growth, total carotenoids and astaxanthin formation by Xanthophyllomyces dendrorhous. Bioresour Technol 97:26–31. doi:10.1016/j.biortech.2005.02.012

    PubMed  CAS  Google Scholar 

  142. Schroeder AW, Johnson EA (1995) Carotenoids protect Phaffia rhodozyma against singlet oxygen damage. J Ind Microbiol Biotechnol 14:502–507

    CAS  Google Scholar 

  143. Olson J (1989) Provitamin A function of carotenoids: the conversion of β-carotene into vitamin A. J Nutr 119:105–108

    PubMed  CAS  Google Scholar 

  144. Edge R, McGarvey D, Truscott T (1997) The carotenoids as antioxidants–a review. J Photochem Photobiol 41:189–200. doi:10.1016/S1011-1344(97)00092-4

    CAS  Google Scholar 

  145. Nishino H, Tokuda H, Satomi Y, Masuda M, Bu P, Onozuka M (1999) Cancer prevention by carotenoids. Pure Appl Chem 71:2273–2278. doi:10.1351/pac199971122273

    CAS  Google Scholar 

  146. Meyer SP (1994) Developments in world aquaculture, formulations, and the role of carotenoids. Pure Appl Chem 66:1069–1076. doi:10.1351/pac199466051069

    Google Scholar 

  147. Johnson EA (2003) Phaffia rhodozyma: colorful odyssey. Int Microbiol 6:169–174. doi:10.1007/s10123-003-0130-3

    PubMed  CAS  Google Scholar 

  148. Johnson EA, Conklin DE, Lewis MJ (1977) The yeast Phaffia rhodozyma as a dietary pigment source for salmonids and crustaceans. J Fish Res Board Can 34:2417–2421

    CAS  Google Scholar 

  149. An GH, Song JY, Kwak WK, Lee BD, Song KB, Choi JE (2006) Improved astaxanthin availability due to drying and rupturing of the red yeast, Xanthophyllomyces dendrorhous. Food Sci Biotechnol 15:506–510

    CAS  Google Scholar 

  150. Bhosale P, Jogdand VV, Gadre RV (2003) Stability of β-carotene in spray dried preparation of Rhodotorula glutinis mutant 32. J Appl Microbiol 95:584–590. doi:10.1046/j.1365-2672.2003.02018.x

    PubMed  CAS  Google Scholar 

  151. Fang TJ, Wang JM (2002) Extractability of astaxanthin in a mixed culture of a carotenoid over-producing mutant of Xanthophyllomyces dendrorhous and Bacillus circulans in two-stage batch fermentation. Process Biochem 37:1235–1245. doi:10.1016/S0032-9592(02)00011-0

    CAS  Google Scholar 

  152. Frengova G, Simova E, Beshkova D (1997) Caroteno-protein and exopolysaccharide production by co-cultures of Rhodotorula glutinis and Lactobacillus helveticus. J Ind Microbiol Biotechnol 18:272–277. doi:10.1038/sj.jim.2900379

    PubMed  CAS  Google Scholar 

  153. Frengova G, Simova E, Beshkova D (2006) β-Carotene rich carotenoid-protein preparation and exopolysaccharide production by Rhodotorula rubra GED8 grown with a yogurt starter culture. Z Naturforsch 61c:571–577

    Google Scholar 

  154. Han JY, Lee SJ, Jung MK, Choi SK, Roh JS (2003) Process for extracting astaxanthin pigment from yeast and extracted pigment thereof. US Patent 2003/0087335 A1

  155. Storebakken T, Sorensen M, Bjerkend B, Hiu S (2004) Utilization of astaxanthin from red yeast, Xanthophyllomyces dendrorhous, in rainbow trout, Oncorhynchus mykiss: effects of enzymatic cell wall disruption and feed extrusion temperature. Aquaculture 236:391–403. doi:10.1016/j.aquaculture.2003.10.035

    CAS  Google Scholar 

  156. Johnson E, Lewis M, Grau C (1980) Pigmentation of egg-yolks with astaxanthin from the yeast Phaffia rhodozyma. Poult Sci 59:1777–1782

    CAS  Google Scholar 

  157. Johnson E, Villa T, Lewis M (1980) Phaffia rhodozyma as an astaxanthin source in salmonid diets. Aquaculture 20:123–124. doi:10.1016/0044-8486(80)90041-1

    Google Scholar 

  158. Akiba Y, Sato K, Takahashi K, Toyomizu M, Takahashi Y, Tsunekawa H, Hayasaka Y, Nagao H (2000) Availability of cell wall-fractured yeast, Phaffia rhodozyma, containing high concentration of astaxanthin for egg yolk pigmentation. Anim Sci J 71:255–260

    Google Scholar 

  159. Akiba Y, Sato K, Takahashi K, Matsushita K, Komiyama H, Tsunekawa H, Nagao H (2001) Meat color modification in broiler chickens by feeding yeast Phaffia rhodozyma, containing high concentration of astaxanthin. J Appl Poult Res 10:154–161

    Google Scholar 

  160. Whyte JNC, Sherry KL (2001) Pigmentation and composition of flesh of Atlantic salmon fed diets supplemented with the yeast Phaffia rhodozyma. N Am J Aquac 63:52–57. doi :10.1577/1548-8454(2001)063<0052:PACOFO>2.0.CO;2

    Google Scholar 

  161. Kagan M, Braun S (2004) Processes for extracting carotenoids and for preparing feed materials. US Patent 6818239 B2

  162. Miki W (1991) Biological functions and activities of animal carotenoids. Pure Appl Chem 63:141–146. doi:10.1351/pac199163010141

    CAS  Google Scholar 

  163. An GH, Song JY, Chang KS, Lee BD, Chae HS, Jang BG (2004) Pigmentation and delayed oxidation of broiler chickens by the red carotenoid, astaxanthin, from chemical synthesis and the yeast, Xanthophyllomyces dendrorhous. Asian Aust J Anim Sci 17:1–6

    Google Scholar 

  164. Nakano T, Kanmuri T, Sato M, Takeuchi M (1999) Effect of astaxanthin rich red yeast (Phaffia rhodozyma) on oxidative stress in rainbow trout. Biochim Biophys Acta 1426:119–125

    PubMed  CAS  Google Scholar 

  165. Rapta P, Polovka M, Zalibera M, Breierova E, Zitnanova I, Marova I, Certik M (2005) Scavenging and antioxidant properties of compounds synthesized by carotenogenic yeasts stressed by heavy metals—EPR spin trapping study. Biophys Chem 116:1–9. doi:10.1016/j.bpc.2005.01.006

    PubMed  CAS  Google Scholar 

  166. Kim JH, Choi SK, Choi SY, Kim HK, Chang HI (2005) Suppresive effect of astaxanthin isolated from the Xanthophyllomyces dendrorhous mutant on ethanol-induced gastric mucosal injury in rats. Biosci Biotechnol Biochem 69:1300–1305. doi:10.1271/bbb.69.1300

    PubMed  CAS  Google Scholar 

  167. Kim JH, Choi SK, Lim WJ, Chang HI (2004) Protective effect of astaxanthin produced by Xanthophyllomyces dendrorhous mutant on indomethacin-induced gastric mucosal injury in rats. J Microbiol Biotechnol 14:996–1003

    CAS  Google Scholar 

  168. Bhosale P, Motiwale L, Ingle A, Gadre RV, Rao KVK (2002) Protective effect of Rhodotorula glutinis NCIM 3353 on the development of hepatic preneoplastic lesions. Curr Sci 83:303–308

    Google Scholar 

  169. It T, Chui C, Tang JC, Lau FY, Cheng GY, Wong RC, Kok SH, Cheng CH, Chan AS, Ho KP (2005) Antiproliferation and induction of cell death of Phaffia rhodozyma extract fermented by brewer malt waste on breast cancer cells. Int J Mol Med 16:931–936

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ginka I. Frengova.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Frengova, G.I., Beshkova, D.M. Carotenoids from Rhodotorula and Phaffia: yeasts of biotechnological importance. J Ind Microbiol Biotechnol 36, 163–180 (2009). https://doi.org/10.1007/s10295-008-0492-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10295-008-0492-9

Keywords

Navigation