Abstract
Carotenoids are one of the most common classes of pigments that occur in nature. Due to their biological properties, they are widely used in phytomedicine and in the chemical, pharmaceutical, cosmetic, food and feed industries. Accordingly, their global market is continuously growing, and it is expected to reach about US$1.4 billion in 2018. Carotenoids can be easily produced by chemical synthesis, although their biotechnological production is rapidly becoming an appealing alternative to the chemical route, partly due to consumer concerns against synthetic pigments. Among the yeasts, and apart from the pigmented species Phaffia rhodozyma (and its teleomorph Xanthophyllomyces dendrorhous), a handful of species of the genera Rhodosporidium, Rhodotorula, Sporobolomyces and Sporidiobolus are well known carotenoid producers. These are known as ‘red yeasts’, and their ability to synthesize mixtures of carotenoids from low-cost carbon sources has been broadly studied recently. Here, in agreement with the renewed interest in microbial carotenoids, the recent literature is reviewed regarding the taxonomy of the genera Rhodosporidium, Rhodotorula, Sporobolomyces and Sporidiobolus, the stress factors that influence their carotenogenesis, and the most advanced analytical tools for evaluation of carotenoid production. Moreover, a synopsis of the molecular and “-omic” tools available for elucidation of the metabolic pathways of the microbial carotenoids is reported.
Similar content being viewed by others
References
Abbott EP, Ianiri G, Castoria R, Idnurm A (2013) Overcoming recalcitrant transformation and gene manipulation in Pucciniomycotina yeasts. Appl Microbiol Biotechnol 97:283–295
Aksu Z, Eren AT (2005) Carotenoids production by the yeast Rhodotorula mucilaginosa: use of agricultural wastes as carbon source. Process Biochem 40:2985–2991. doi:10.1016/j.procbio.2005.01.011
Amorim-Carrilho KT, Cepeda A, Fente C, Regal P (2014) Review of methods for analysis of carotenoids. TrAC Trends Anal Chem 56:49–73
BCC Research (2011) The global market for carotenoids. http://www.bccresearch.com/market-research/food-and-beverage/carotenoids-global-market-fod025d.html. Published Sept 2011
Bhosale P (2004) Environmental and cultural stimulants in the production of carotenoids from microorganisms. Appl Microbiol Biotechnol 63:351–361
Bhosale PB, Gadre RV (2001a) Production of β-carotene by a mutant of Rhodotorula glutinis. Appl Microbiol Biotechnol 55(4):423–427
Bhosale PB, Gadre RV (2001b) β-Carotene production in sugar cane molasses by a Rhodotorula glutinis mutant. J Ind Microbiol Biotechnol 26(6):327–332
Boekhout T (2011) Bulleromyces Boekhout & Fonseca (1991). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. Elsevier, London, pp 1391–1394
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(5–6):687–692
Buzzini P, Innocenti M, Turchetti B, Libkind D, van Broock M, Mulinacci N (2007) Carotenoid profiles of yeasts belonging to the genera Rhodotorula, Rhodosporidium, Sporobolomyces, and Sporidiobolus. Can J Microbiol 53:1024–1031
Buzzini P, Goretti M, Branda E, Turchetti B (2010) Basidiomycetous yeasts for production of carotenoids. In: Flickinger MC (ed) Encyclopedia of industrial biotechnology: bioprocess, bioseparation, and cell technology, vol 1. Wiley, New York, pp 469–481
Cutzu R, Clemente A, Nobre B, Mannazzu I, Roseiro J, Lopes da Silva T (2013a) Assessment of β-carotene content, cell physiology and morphology of the yellow yeast Rhodotorula glutinis mutant 400A15 using flow cytometry. J Ind Microbiol Biotechnol 40:865–875
Cutzu R, Coi A, Rosso F, Bardi L, Ciani M, Budroni M, Zara G, Zara S, Mannazzu I (2013b) From crude glycerol to carotenoids by using a Rhodotorula glutinis mutant. World J Microbiol Biotechnol 29(6):1009–1017
Davoli P, Mierau V, Weber RWS (2004) Carotenoids and fatty acids in red yeast Sporobolomyces roseus and Rhodotorula glutinis. Appl Biochem Microbiol 40(4):392–397
Debarati P, Magbanua Z, Arick M II, French T, Bridges SM, Burgess SC, Lawrence ML (2014) Genome sequence of the oleaginous yeast Rhodotorula glutinis ATCC 204091. Genome Announc 2(1):e00046-14. doi:10.1128/genomeA.00046-14
Deligios M, Fraumene C, Abbondio M, Mannazzu I, Tanca A, Addis MF, Uzzau S (2015) Draft genome sequence of Rhodotorula mucilaginosa, an emergent opportunistic pathogen. Genome Announc 3(2):e00201–e00215. doi:10.1128/genomeA.00201-15
Dufossé L (2006) Food grade pigments. Food Technol Biotech 44(3):313–321
Fell JW, Johnson EA (2011) Phaffia M.W. Miller, Yoneyama & Soneda (1976). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. Elsevier, London, pp 1853–1856
Fell JW, Johnson EA, Scorzetti G (2011) Xanthophyllomyces Golubev (1995). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. Elsevier, London, pp 1595–1601
Ferrao M, Garg S (2012) Shake flask optimization of & β-carotene production in Rhodotorula graminis RC04. Afr J Biotechnol 11(52):11431–11437
Freitas C, Nobre B, Gouveia L, Roseiro J, Reis A, Lopes da Silva T (2014) New at-line flow cytometric protocols for determining carotenoid content and cell viability during Rhodosporidium toruloides NCYC 921 batch growth. Proc Biochem 49:554–562
Guo W, Tang H, Zhang L (2014) Lycopene cyclase and phytoene synthase activities in the marine yeast Rhodosporidium diobovatum are encoded by a single gene crtYB. J Basic Microbiol 54:1053–1061
Guo W, Liu Y, Yan X, Liu M, Tang H, Liu Z, Zhang L (2015) Cloning and characterization of a phytoene dehydrogenase gene from marine yeast Rhodosporidium diobovatum. DOI, A van Leeuw J Microb. doi:10.1007/s10482-015-0394-6
Hamamoto M, Boekhout T, Nakase T (2011) Sporobolomyces Kluyver & van Niel (1924). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. Elsevier, London, pp 1929–1990
Hernandez-Almanza A, Montanez JC, Aguilar-Gonzalez MA, Martinez-Avila C, Rodriguez-Herrera R, Aguilar CN (2014) Rhodotorula glutinis as source of pigments and metabolites for food industries. Food Biosci 5:64–72
Herrero M, Cacciola F, Donato P, Giuffrida D, Dugo G, Dugo P, Mondello L (2008) Serial coupled columns reversed-phase separations in high-performance liquid chromatography: tool for analysis of complex real samples. J Chromatogr 1188:208–215
Hu C, Zhao X, Zhao J, Wu S, Zhao ZK (2009) Effect of biomass hydrolysis by-products on oleaginous yeast Rhodosporidium toruloides. Bioresour Technol 100:4843–4847
Ianiri G, Wright SAI, Castoria R, Idnurm A (2011) Development of resources for the analysis of gene function in Pucciniomycotina red yeasts. Fungal Genet Biol 48:685–695
Irazusta V, Estévez C, Amoroso MJ, de Figueroa LJ (2012) Proteomic study of the yeast Rhodotorula mucilaginosa RCL-11 under copper stress. Biometals 25:517–527
Irazusta V, Nieto-Penalver CG, Cabral ME, Amoroso MJ, de Figueroa LIC (2013) Relationship among carotenoid production, copper bioremediation and oxidative stress in Rhodotorula mucilaginosa RCL-11. Process Biochem 48:803–809
Johnson EA (2013) Biotechnology of non-Saccharomyces yeasts—the basidiomycetes. Appl Microbiol Biotechnol 97:7563–7577
Johnson EA, Echavarri-Erasun C (2011) Yeast biotechnology. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts. A taxonomy study, vol 1. Elsevier, New York, pp 21–44
Johnson EA, Schroeder WA (1995) Microbial carotenoids. In: Fiechter A (ed) Adv Biochem Eng Biotechnol 53:119–178
Kaiser P, Surmann P, Vallentin G, Fuhmann H (2007) A small-scale method for quantitation of carotenoids in bacteria and yeasts. J Microbiol Method 70:142–149
Kirti K, Amita S, Priti S, Kumar AM, Jyoti S (2014) Colorful world of microbes: carotenoids and their applications. Adv Biol ID837891
Koh CMJ, Liu Y, Moehninsi MD, Ji L (2014) Molecular characterization of KU70 and KU80 homologues and exploitation of a KU70-deficient mutant for improving gene deletion frequency in Rhodosporiudium toruloides. BMC Microbiol 14:50
Kumar S, Kushwaha H, Bachhawat AK, Raghava GPS, Ganesan K (2012) Genome sequence of the oleaginous red yeast Rhodosporidium toruloides MTCC 457. Eukaryot Cell 11(8):1083–1084
Li Z, Sun H, Mo X, Li X, Xu B, Tian P (2013) Overexpression of malic enzyme (ME) of Mucor circinelloides improved lipid accumulation in engineered Rhodotorula glutinis. Appl Microbiol Biotechnol 97:4927–4936
Lin X, Wang Y, Zhang S, Zhu Z, Zhou YJ, Yang F, Sun W, Wang X, Zhao ZK (2014) Functional integration of multiple genes into the genome of the oleaginous yeast Rhodosporidium toruloides. Yeast 14:547–555
Liu H, Zhao X, Wang F, Li F, Li Y, Jiang X, Ye M, Zhao ZK, Zou H (2009) Comparative proteomic analysis of Rhodosporidium toruloides during lipid accumulation. Yeast 26:553–566
Liu Y, Chong Mei JK, Longhua S, Mya Myintzu H, Minge Du, Ni P, Lianghui J (2013) Characterization of glyceraldehyde-3-phosphate dehydrogenase gene RtGPD1 and development of genetic transformation method by dominant selection in oleaginous yeast Rhodosporidium toruloides. Appl Microbiol Biotechnol 97:719–729
Mahmoud AGY, Abo-Shady MA, El-Sheekh MM, Hamza TW (2014) The role of some stress factors including hydrogen peroxide, methylen blue, sodium chloride and ultraviolet on Rhodotorula glutinis DBVPG# 4400 total carotenoids production. Int J Biosci (IJB) 4(9):10–19
Maldonade IR, Rodriguez-Amaya DB, Scamparini ARP (2008) Carotenoids of yeasts isolated from Brazilian ecosystem. Food Chem 107(1):145–150
Malisorn C, Suntornsuk W (2008) Optimization of & β-carotene production by Rhodotorula glutinis DM28 in fermented radish brine. Bioresour Technol 99:2281–2287
Marcoleta A, Niklitschek M, Wozniak A, Lozano C, Alcaíno J, Baeza M, Cifuentes V (2011) Glucose and ethanol-dependent transcriptional regulation of the astaxanthin biosynthesis pathway in Xanthophyllomyces dendrorhous. BMC Microbiol 11:190
Marova I, Breierova E, Koci R, Friedl Z, Slovak B, Pokorna J (2004) Influence of exogenous stress factors on production of carotenoids by some strains of carotenogenic yeasts. Ann Microbiol 54:73–85
Marova I, Carnecka M, Halienova A, Koci R, Breierova E (2010) Production of carotenoid/ergosterol supplemeted biomass by red yeast Rhodotorula glutinis grown under external stress. Food Technol Biotech 48:56–61
Marova I, Certik M, Breierova E (2011) Production of enriched biomass by carotenogenic yeasts—application of whole-cell yeast biomass to production of pigments and other lipid compounds, biomass—detection, production and usage. Darko Matovic (ed), ISBN:978-953-307-492-4
Marova I, Carnecka M, Halienova A, Certik M, Dvorakova T, Haronikova A (2012) Use of several waste substrates for carotenoid-rich yeast biomass production. J Environ Manag 95:S338–S342
Martinez-Moya P, Niehaus K, Alcaíno J, Baeza M, Cifuentes V (2015) Proteomic and metabolomic analysis of the carotenogenic yeast Xanthophyllomyces dendrorhous using different carbon sources. BMG Genomics 16:289
Mata-Gomez LC, Montañez JC, Méndez-Zavala Aguilar CN (2014) Biotechnological production of carotenoids by yeasts: an overview. Microb Cell Fact 13:12
Morin N, Calcas X, Devillers H, Durrens P, Sherman DJ, Nicaud J-M, Neuveglise C (2014) Draft genome of Rhodosporidium toruloides CECT1137, an oleaginous yeast of biotechnological interest. Genome Announc 2(4):e00641-14
Nishida H, Robert V, Sugiyama J (2011) Mixia C.L. Kramer emend. H. Nishida, K. Ando, Y. Ando, Hirata & Sugiyama (1995). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. Elsevier, London, pp 1499–1502
Nishijima M, Araki-Sakai M, Sano H (1997) Identification of isoprenoid quinones by frit-FAB liquid chromatography–mass spectrometry for the chemotaxonomy of microorganisms. J Microbiol Methods 28:113–122
Park PK, Kim EY, Chu KH (2007) Chemical disruption of yeast cells for the isolation of carotenoid pigments. Sep Purif Technol 53:148–152
Petrik S, Marova I, Haronikova A, Kostovova I, Breierova E (2013) Production of biomass, carotenoid and other lipid metabolites by several red yeasts strains cultivated on waste glycerol from biofuel production—a comparative screening study. Ann Microbiol 63:1537–1551
Provesi JG, Dias CO, Amante ER (2011) Changes in carotenoids during processing and storage of pumpkin puree. Food Chem 128:195–202
Rapta P, Polovka M, Zalibera M, Breierova E, Zitnanova I, Marova I, Certik M (2005) Scavenging andantioxidant properties of compounds synthesized by carotenogenic yeasts stressed by heavy metals—EPR spin trapping study. Biophys Chem 116:1–9
Razavi SH (2006) UV-HPLC/APCI/MS method for separation and identification of the carotenoids produced by Sporobolomyces ruberrimus H110. Iran J Chem Chem Eng 25:1–10
Rodríguez-Amaya D (2001) In: Rodríguez-Amaya D (ed) A guide to carotenoid analysis in foods. ILSI Press, Washington DC
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
Sampaio JP (2011a) Cystofilobasidium Oberwinkler & Bandoni (1983). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. Elsevier, London, pp 1423–1432
Sampaio JP (2011b) Rhodosporidium Banno (1967). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. Elsevier, London, pp 1523–1540
Sampaio JP (2011c) Rhodotorula Harrison (1928). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. Elsevier, London, pp 1873–1928
Sampaio JP (2011d) Sporidiobolus Nyland (1949). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. Elsevier, London, pp 1549–1562
Sampaio JP, Oberwinkler F (2011a) Cystobasidium (Lagerheim) Neuhoff (1924). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. Elsevier, London, pp 1419–1422
Sampaio JP, Oberwinkler F (2011b) Occultifur Oberwinkler (1990). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study. Elsevier, London, pp 1515–1518
Somashekar D, Joseph R (2000) Inverse relationship between carotenoid and lipid formation in Rhodotorula gracilis according to the C/N ratio of growth medium. World J Microbiol Biotechnol 16:491–493
Soroka IM, Narushin VG, Turiyansky YD, Tyurenkov AA (2012) Spectroscopy analysis for simultaneous determination of lycopene and β-carotene in fungal biomass of Blakeslea trispora. Acta Biochim Pol 59:65–69
Squina FM, Mercadante AZ (2005) Influence of nicotine and dyphenylamine on the carotenoid composition of Rhodotorula strains. J Food Biochem 29(6):638–652
Takahashi S, Okada H, Abe K, Kera Y (2014) Genetic transformation of the yeast Rhodotorula gracilis ATCC 26217 by electroporation. Appl Biochem Microbiol 50(6):624–628
Tinoi T, Rakariyatham N, Deming RL (2005) Simplex optimization of carotenoid production by Rhodotorula glutinis using hydrolyzed mung bean waste flour as substrate. Proc Biochem 40:2551–2557
Tully M, Gilbert HJ (1985) Transformation of Rhodosporidium toruloides. Gene 36(3):235–240
Ukibe K, Katsuragi T, Tani Y, Takagi H (2008) Efficient screening for astaxanthin-overproducing mutants of the yeast Xanthophyllomyces dendrorhous by flow cytometry. FEMS Microbiol Lett 286:241–248
Vachali P, Bhosale P, Bernstein PS (2012) Microbial carotenoids. In: Barredo J-L (ed) Microbial carotenoids from fungi: methods and protocols. Methods Mol Biol 898:41–59
Verdoes JC, Krubasik KP, Sandman G, van Ooyen AJ (1999) Isolation and functional characterization of a novel type of carotenoid biosynthetic gene from Xanthophyllomyces dendrorhous. Mol Gen Genet 262:453–461
Wang SL, Sun JS, Han BZ, Wu XZ (2008) Enhanced β-carotene production by Rhodotorula glutinis using high hydrostatic pressure. Korean J Chem Eng 25(3):513–516
Wang C, Wang CY, Zhao XQ, Chen RF, Lan P, Shen RF (2013) Proteomic analysis of a high aluminium tolerant yeast Rhodotorula taiwanensis RS1 in response to aluminium stress. Biochim Biophys Acta 1834:1969–1975
Yen HW, Zhang Z (2011) Enhancement of cell wall growth rate by light irradiation in the cultivation of Rhodotorula glutinis. Bioresour Technol 102:9279–9281
Zhu Z, Zhang S, Liu H, Shen H, Lin X, Yang F, Zhou YJ, Jin G, Ye M, Zou H, Zhao ZK (2012) A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides. Nat Commun 3:1112. doi:10.1038/ncomms2112
Zoz L, Carvalho JC, Soccol VT, Casagrande TC, Cardoso L (2015) Torularhodin and torulene: bioproduction, properties, and prospective applications in food and cosmetics—a review. Braz Arch Biol Technol 58(2):278–288
Acknowledgments
This study was partially supported by Regione Autonoma della Sardegna (LR7/07-2010; grant to I.M. and fellowship to S.L.). The authors are grateful to Benedetta Turchetti for valuable help in drawing the phylogenetic tree of red yeasts.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mannazzu, I., Landolfo, S., da Silva, T.L. et al. Red yeasts and carotenoid production: outlining a future for non-conventional yeasts of biotechnological interest. World J Microbiol Biotechnol 31, 1665–1673 (2015). https://doi.org/10.1007/s11274-015-1927-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11274-015-1927-x