Skip to main content

Production of Pigments and Photo-Protective Compounds by Cold-Adapted Yeasts

  • Chapter
  • First Online:
Cold-adapted Yeasts

Abstract

The structure of microbial communities in cold environments is not only shaped by temperature, but also other factors determine which species can survive. Ultraviolet radiation (UVR) is one of these factors and only microorganisms bearing photo-protective defence mechanisms colonize environments exposed to high UVR levels. In yeasts collected from Patagonia, among other cold environments, secondary metabolites such as carotenoids and mycosporines appeared to be produced as the most frequent photo-protective compounds. Production of carotenoids is quite common in cold-adapted yeasts, and some species produce unique carotenoids, like plectaniaxanthin and astaxanthin, which are not found in mesophilic species. On the other hand, the production of mycosporines appears in several yeasts species and has been intensively studied in yeasts isolated from high-altitude Patagonian lakes, revealing that several cold-adapted yeasts, including Phaffia and Dioszegia, are mycosporine-producing species. Both compounds effectively protect yeast cells against UVR.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aksu Z, Eren AT (2005) Carotenoids production by the yeast Rhodotorula mucilaginosa: use of agricultural wastes as a carbon source. Process Biochem 40:2985–2991

    Article  CAS  Google Scholar 

  • Alcaino J, Barahona S, Carmona M, Lozano C, Marcoleta A, Niklitschek M, Sepulveda D, Baeza M, Cifuentes V (2008) Cloning of the cytochrome p450 reductase (crtR) gene and its involvement in the astaxanthin biosynthesis of Xanthophyllomyces dendrorhous. BMC Microbiol 8:169

    Article  PubMed  CAS  Google Scholar 

  • Alvarez V, Rodriguez-Saiz M, de la Fuente J, Gudina E, Godio R, Martin J, Barredo J (2006) The crtS gene of Xanthophyllomyces dendrorhous encodes a novel cytochrome-P450 hydroxylase involved in the conversion of beta-carotene into astaxanthin and other xanthophylls. Fungal Genet Biol 43:261–272

    Article  PubMed  CAS  Google Scholar 

  • An G-H, Cho M-H, Johnson EA (1999) Monocyclic carotenoid biosynthetic pathway in the yeast Phaffia rhodozyma (Xanthophyllomyces dendrorhous). J Biosci Bioeng 88:189–193

    Article  PubMed  CAS  Google Scholar 

  • Andrewes AG, Phaff HJ, Starr MP (1976) Carotenoids of Phaffia rhodozyma, a red-pigmented fermenting yeast. Phytochemistry 15:1003–1007

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • Arbeloa EM, Uez MJ, Bertolotti SG, Churio MS (2010) Antioxidant activity of gadusol and occurrence in fish roes from Argentine Sea. Food Chem 119:586–591

    Article  CAS  Google Scholar 

  • Arbeloa EM, Bertolotti SG, Churio MS (2011) Photophysics and reductive quenching reactivity of gadusol in solution. Photochem Photobiol Sci 10:133–142

    Article  PubMed  CAS  Google Scholar 

  • Arpin N, Bouillant M (1981) Light and mycosporines. The fungal spore, morphogenetic controls. Academic Press, London, pp 435–454

    Google Scholar 

  • Arpin N, Favre-Bonvin J, Thivend S (1977) Structure de la mycosporine 2, nouvelle molecule, isolee de Botrytis cinerea. Tetrahedron Lett 18:819–820

    Article  Google Scholar 

  • Ausich RL (1997) Commercial opportunities for carotenoid production by biotechnology. Pure Appl Chem 69:2169–2174

    Article  CAS  Google Scholar 

  • Bae M, Lee TH, Yokoyama H, Boettger HG, Chichester CO (1971) The occurrence of plectaniaxanthin in Cryptococcus laurentii. Phytochemistry 10:625–629

    Article  CAS  Google Scholar 

  • Balskus EP, Walsh CT (2010) The genetic and molecular basis for sunscreen biosynthesis in cyanobacteria. Science 329:1653–1656

    Article  PubMed  CAS  Google Scholar 

  • Bandaranayake W (1998) Mycosporines: are they nature’s sunscreens? Nat Prod Rep 15:159–172

    Article  PubMed  CAS  Google Scholar 

  • Bergauer P, Fonteyne P-A, Nolard N, Schinner F, Margesin R (2005) Biodegradation of phenol and phenol-related compounds by psychrophilic and cold-tolerant alpine yeasts. Chemosphere 59:909–918

    Article  PubMed  CAS  Google Scholar 

  • Bernillon J, Bouillant M-L, Pittet J-L, Favre-Bonvin J, Arpin N (1984) Mycosporine glutamine and related mycosporines in the fungus Pyronema omphalodes. Phytochemistry 23:1083–1087

    Article  CAS  Google Scholar 

  • Bhosale P (2004) Environmental and cultural stimulants in the production of carotenoids from microorganisms. Appl Microbiol Biotechnol 63:351–361

    Article  PubMed  CAS  Google Scholar 

  • Birgisson H, Delgado O, Arroyo LG, Hatti-Kaul R, Mattiasson B (2003) Cold-adapted yeasts as producers of cold-active polygalacturonases. Extremophiles 7:185–193

    PubMed  CAS  Google Scholar 

  • Branda E, Turchetti B, Diolaiuti G, Pecci M, Smiraglia C, Buzzini P (2010) Yeast and yeast-like diversity in the southernmost glacier of Europe (Calderone Glacier, Apennines, Italy). FEMS Microbiol Ecol 72:354–369

    Article  PubMed  CAS  Google Scholar 

  • Brandão LR, Libkind D, Vaz ABM, Espírito Santo LC, Moliné M, de García V, van Broock M, Rosa CA (2011) Yeasts from an oligotrophic lake in Patagonia (Argentina): diversity, distribution and synthesis of photoprotective compounds and extracellular enzymes. FEMS Microbiol Ecol 76:1–13

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Britton G (2004) Carotenoids handbook. Birkhäuser Verlag, Basel

    Book  Google Scholar 

  • Britton G (2008) Functions of intact carotenoids. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 4. Birkhäuser, Basel, pp 189–212

    Chapter  Google Scholar 

  • Brook P (1981) Protective function of an ultraviolet-absorbing compound associated with conidia of Glomerella cingulata. N Z J Bot 19:299–304

    Article  Google Scholar 

  • Buzzini P, Turchetti B, Diolaiuti G, D’Agata C, Martini A, Smiraglia C (2005) Culturable yeasts in meltwaters draining from two glaciers in the Italian Alps. Annals Glaciol 40:119–122

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Buzzini P, Goretti M, Branda E, Turchetti B (2010) Basidiomycetous yeasts for production of carotenoids. In: Flickinger M (ed) Encyclopedia of industrial biotechnology: bioprocess, bioseparation, and cell technology, vol 1. Wiley, New York, pp 469–481

    Google Scholar 

  • Buzzini P, Branda E, Goretti M, Turchetti B (2012) Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiol Ecol 82:217–241

    Article  PubMed  CAS  Google Scholar 

  • Carreto JI, Carignan MO (2011) Mycosporine-like amino acids: relevant secondary metabolites. Chemical and ecological aspects. Mar Drugs 9:387–446

    Article  PubMed  CAS  Google Scholar 

  • Carreto JI, Marco S, Lutz V (1989) UV-absorbing pigments in the dinoflagellates Alexandrium excavatum and Prorocentrum micans. Effects of light intensity. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides; biology, environmental science and toxicology. Elsevier, Amsterdam, pp 333–336

    Google Scholar 

  • Cockell CS, Knowland J (1999) Ultraviolet radiation screening compounds. Biol Rev 74:311–345

    CAS  Google Scholar 

  • Conde FR, Churio MS, Previtali CM (2000) The photoprotector mechanism of mycosporine-like amino acids. Excited-state properties and photostability of porphyra-334 in aqueous solution. J Photochem Photobiol B: Biology 56:139–144

    Article  PubMed  CAS  Google Scholar 

  • Conde FR, Churio MS, Previtali CM (2004) The deactivation pathways of the excited-states of the mycosporine-like amino acids shinorine and porphyra-334 in aqueous solution. Photochem Photobiol Sci 3:960–967

    Article  PubMed  CAS  Google Scholar 

  • Conde FR, Churio MS, Previtali CM (2007) Experimental study of the excited-state properties and photostability of the mycosporine-like amino acid palythine in aqueous solution. Photochem Photobiol Sci 6:669–674

    Article  PubMed  CAS  Google Scholar 

  • Connell LB, Redman R, Rodriguez R, Barrett A, Iszard M, Fonseca A (2010) Dioszegia antarctica sp. nov. and Dioszegia cryoxerica sp. nov., psychrophilic basidiomycetous yeasts from polar desert soils in Antarctica. Int J Syst Evol Microbiol 60:1466–1472

    Article  PubMed  CAS  Google Scholar 

  • Davoli P, Weber RWS (2002) Carotenoid pigments from the red mirror yeast, Sporobolomyces roseus. Mycol 16:102–108

    Google Scholar 

  • Davoli P, Mierau V, Weber RWS (2004) Carotenoids and fatty acids in red yeasts Sporobolomyces roseus and Rhodotorula glutinis. App Biochem Microbiol 40:392–397

    Article  CAS  Google Scholar 

  • de García V, Brizzio S, Libkind D, Buzzini P, van Broock M (2007) Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia, Argentina. FEMS Microbiol Ecol 59:331–341

    Article  PubMed  CAS  Google Scholar 

  • Diaz MR, Fell JW (2000) Molecular analyses of the IGS & ITS regions of rDNA of the psychrophilic yeasts in the genus Mrakia. A van Leeuwenhoek 77:7–12

    Article  CAS  Google Scholar 

  • Diffey BL (1991) Solar ultraviolet radiation effects on biological systems. Phys Med Biol 36:299–328

    Article  PubMed  CAS  Google Scholar 

  • Disch A, Rohmer M (1998) On the absence of the glyceraldehyde 3-phosphate/pyruvate pathway for isoprenoid biosynthesis in fungi and yeasts. FEMS Microbiol Lett 168:201–208

    Article  PubMed  CAS  Google Scholar 

  • Dunlap WC, Yamamoto Y (1995) Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine. Comp Biochem Physiol B: Biochem Mol Biol 112:105–114

    Article  Google Scholar 

  • Ende G, Cornelis JJ (1970) The induction of sporulation in sclerotinia fructicola and some other fungi and the production of “P310”. Netherlands J Plant Pathol 76:183–191

    Article  Google Scholar 

  • Favre-Bonvin J, Arpin N, Brevard C (1976) Structure de la mycosporine (P 310). Can J Chem 54:1105–1113

    Article  CAS  Google Scholar 

  • Favre-Bonvin J, Bernillon J, Salin N, Arpin N (1987) Biosynthesis of mycosporines: mycosporine glutaminol in Trichothecium roseum. Phytochemistry 26:2509–2514

    Article  CAS  Google Scholar 

  • Fernández Zenoff V, Siñeriz F, Farías ME (2006) Diverse responses to UV-B radiation and repair mechanisms of bacteria isolated from high-altitude aquatic environments. Appl Environ Microbiol 72:7857–7863

    Article  PubMed  CAS  Google Scholar 

  • Fernández NV, Cecilia Mestre M, Marchelli P, Fontenla SB (2012) Yeast and yeast-like fungi associated with dry indehiscent fruits of Nothofagus nervosa in Patagonia, Argentina. FEMS Microbiol Ecol 80:179–192

    Article  PubMed  CAS  Google Scholar 

  • Fiasson JL (1972) Carotenoids in various anascosporous yeasts. C R Acad Sci D Sci Nat 274:3465

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Frengova G, Beshkova D (2009) Carotenoids from Rhodotorula and Phaffia: yeasts of biotechnological importance. J Ind Microbiol Biotechnol 36:163–180

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Garcia-Pichel F (1994) A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39:1704–1717

    Article  Google Scholar 

  • Garcia-Pichel F, Castenholz RW (1993) Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Appl Environ Microbiol 59:163–169

    PubMed  CAS  Google Scholar 

  • Goodwin TW (1980) The biochemistry of the carotenoids. Academic Press, London

    Book  Google Scholar 

  • Gounot AM (1999) Microbial life in permanently cold soils. In: Margesin R, Schinner F (eds) Cold-adapted organisms. Springer, Berlin, pp 3–15

    Chapter  Google Scholar 

  • Grant PT, Plack PA, Thomson RH (1980) Gadusol, a metabolite from fish eggs. Tetrahedron Lett 21:4043–4044

    Article  CAS  Google Scholar 

  • Gu WL, An GH, Johnson EA (1997) Ethanol increases carotenoid production in Phaffia rhodozyma. J Ind Microbiol Biotech 19:114–117

    Article  CAS  Google Scholar 

  • Gunasekera T, Paul N, Ayres P (1997) Responses of phylloplane yeasts to UV-B (290–320 nm) radiation: interspecific differences in sensitivity. Mycol Res 101:779–785

    Article  CAS  Google Scholar 

  • Gunde-Cimerman N, Plemenitaš A (2006) Ecology and molecular adaptations of the halophilic black yeast Hortaea werneckii. Rev Environ Sci Biotechnol 5:323–331

    Article  CAS  Google Scholar 

  • Häder D-P (1991) Effects of enhanced solar ultraviolet radiation on aquatic ecosystems. In: Lenci F, Ghetti F, Colombetti G, Häder DP, Song P-S (eds) Biophysics of photoreceptors and photomovements in microorganisms, vol 211., NATO ASI seriesSpringer, New York, pp 157–172

    Chapter  Google Scholar 

  • Hanelt D, Tüg H, Bischof K, Groß C, Lippert H, Sawall T, Wiencke C (2001) Light regime in an Arctic fjord: a study related to stratospheric ozone depletion as a basis for determination of UV effects on algal growth. Mar Biol 138:649–658

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • He Y-Y, Häder D-P (2002) UV-B-induced formation of reactive oxygen species and oxidative damage of the cyanobacterium Anabaena sp.: protective effects of ascorbic acid and N-acetyl-l-cysteine. J Photochem Photobiol B: Biol 66:115–124

    Article  CAS  Google Scholar 

  • He Y-Y, Klisch M, Häder D-P (2002) Adaptation of cyanobacteria to UV-B stress correlated with oxidative stress and oxidative damage. Photochem Photobiol 76:188–196

    Article  PubMed  CAS  Google Scholar 

  • Herrmann KM, Weaver LM (1999) The shikimate pathway. Ann Rev Plant Biol 50:473–503

    Article  CAS  Google Scholar 

  • Herz S, Weber RWS, Anke H, Mucci A, Davoli P (2007) Intermediates in the oxidative pathway from torulene to torularhodin in the red yeasts Cystofilobasidium infirmominiatum and C. capitatum (Heterobasidiomycetes, Fungi). Phytochemistry 68:2503–2511

    Article  PubMed  CAS  Google Scholar 

  • Hoyer K, Karsten U, Wiencke C (2002) Induction of sunscreen compounds in Antarctic macroalgae by different radiation conditions. Mar Biol 141:619–627

    Article  CAS  Google Scholar 

  • Inácio J, Portugal L, Spencer-Martins I, Fonseca A (2005) Phylloplane yeasts from Portugal: seven novel anamorphic species in the Tremellales lineage of the Hymenomycetes (Basidiomycota) producing orange-coloured colonies. FEMS Yeast Res 5:1167–1183

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Johnson EA, Schroeder WA (1995) Astaxanthin from the yeast Phaffia rhodozyma. Stud Mycol 38:81–90

    Google Scholar 

  • Johnson E, Schroeder W (1996) Microbial carotenoids. In: Downstream processing biosurfactants carotenoids, vol 53. Adv Biochem Engin/Biotechnol. Springer, Berlin, pp 119–178

    Google Scholar 

  • Kaiser P, Geyer R, Surmann P, Fuhrmann H (2012) LC–MS method for screening unknown microbial carotenoids and isoprenoid quinones. J Microbiol Methods 88:28–34

    Article  PubMed  CAS  Google Scholar 

  • Kamio M, Kicklighter CE, Nguyen L, Germann MW, Derby CD (2011) Isolation and structural elucidation of novel mycosporine-like amino acids as alarm cues in the defensive ink secretion of the sea hare Aplysia californica. Helv Chim Acta 94:1012–1018

    Article  CAS  Google Scholar 

  • Karsten U, Franklin LA, Lüning K, Wiencke C (1998) Natural ultraviolet radiation and photosynthetically active radiation induce formation of mycosporine-like amino acids in the marine macroalga Chondrus crispus (Rhodophyta). Planta 205:257–262

    Article  CAS  Google Scholar 

  • Kicklighter CE, Kamio M, Nguyen L, Germann MW, Derby CD (2011) Mycosporine-like amino acids are multifunctional molecules in sea hares and their marine community. Proc Natl Acad Sci USA 108:11494–11499

    Article  PubMed  CAS  Google Scholar 

  • Klisch M, Häder D-P (2002) Wavelength dependence of mycosporine-like amino acid synthesis in Gyrodinium dorsum. J Photochem Photobiol B: Biol 66:60–66

    Article  CAS  Google Scholar 

  • Klisch M, Sinha RP, Richter PR, Häder D-P (2001) Mycosporine-like amino acids (MAAs) protect against UV-B-induced damage in Gyrodinium dorsum Kofoid. J Plant Physiol 158:1449–1454

    Article  CAS  Google Scholar 

  • Knaggs AR (2003) The biosynthesis of shikimate metabolites. Nat Prod Rep 20:119–136

    Article  PubMed  CAS  Google Scholar 

  • Kogej T, Gostinčar C, Volkmann M, Gorbushina AA, Gunde-Cimerman N (2006) Mycosporines in Extremophilic fungi—novel complementary osmolytes? Environ Chem 3:105–110

    Article  CAS  Google Scholar 

  • Kogej T, Stein M, Volkmann M, Gorbushina AA, Galinski EA, Gunde-Cimerman N (2007) Osmotic adaptation of the halophilic fungus Hortaea werneckii: role of osmolytes and melanization. Microbiology 153:4261–4273

    Article  PubMed  CAS  Google Scholar 

  • Kräbs G, Watanabe M, Wlencke C (2004) A Monochromatic action spectrum for the photoinduction of the UV-absorbing mycosporine-like amino acid shinorine in the red alga Chondrus crispus. Photochem Photobiol 79:515–520

    Article  PubMed  Google Scholar 

  • Lampila LE, Wallen SE, Bullerman LB (1985) A review of factors affecting biosynthesis of carotenoids by the order Mucorales. Mycopathology 90:65–80

    Article  CAS  Google Scholar 

  • Laurion I, Ventura M, Catalan J, Psenner R, Sommaruga R (2000) Attenuation of ultraviolet radiation in mountain lakes: factors controlling the among-and within-lake variability. Limn Oceanogr 45:1274–1288

    Article  Google Scholar 

  • Leach CM (1965) Ultraviolet-absorbing substances associated with light-induced sporulation in fungi. Can J Bot 43:185–200

    Article  CAS  Google Scholar 

  • Leach CM, Trione E (1966) Action spectra for light-induced sporulation of the fungi Pleospora Herbarum and Alernaria dauci. Photochem Photobiol 5:621–630

    Article  CAS  Google Scholar 

  • Leite B, Nicholson RL (1992) Mycosporine-alanine: a self-inhibitor of germination from the conidial mucilage of Colletotrichum graminicola. Exp Mycol 16:76–86

    Article  CAS  Google Scholar 

  • Liaaen-Jensen S, Andrewes AG (1972) Microbial carotenoids. Annu Rev Microbiol 26:225–248

    Article  PubMed  CAS  Google Scholar 

  • Libkind D, van Broock M (2006) Biomass and carotenoid pigment production by patagonian native yeasts. World J Microbiol Biotechnol 22:687–692

    Article  CAS  Google Scholar 

  • Libkind D, Brizzio S, van Broock M (2004a) Rhodotorula mucilaginosa, a carotenoid producing yeast strain from a patagonian high-altitude lake. Folia Microbiol 49:19–25

    Article  CAS  Google Scholar 

  • Libkind D, Pérez P, Sommaruga R, del Carmen Diéguez M, Ferraro M, Brizzio S, Zagarese H, van Broock M (2004b) Constitutive and UV-inducible synthesis of photoprotective compounds (carotenoids and mycosporines) by freshwater yeasts. Photochem Photobiol Sci 3:281–286

    Article  PubMed  CAS  Google Scholar 

  • Libkind D, Sommaruga R, Zagarese H, van Broock M (2005) Mycosporines in carotenogenic yeasts. Syst Appl Microbiol 28:749–754

    Article  PubMed  CAS  Google Scholar 

  • Libkind D, Diéguez MC, Moliné M, Pérez P, Zagarese HE, Broock M (2006) Occurrence of photoprotective compounds in yeasts from freshwater ecosystems of northwestern Patagonia (Argentina). Photochem Photobiol 82:972–980

    Article  PubMed  CAS  Google Scholar 

  • Libkind D, Moliné M, de García V, Fontenla S, van Broock M (2008) Characterization of a novel South American population of the astaxanthin producing yeast Xanthophyllomyces dendrorhous (Phaffia rhodozyma). J Ind Microbiol Biotechnol 35:151–158

    Article  PubMed  CAS  Google Scholar 

  • Libkind D, Moliné M, Sampaio JP, van Broock M (2009a) Yeasts from high-altitude lakes: influence of UV radiation. FEMS Microbiol Ecol 69:353–362

    Article  PubMed  CAS  Google Scholar 

  • Libkind D, Gadanho M, van Broock M, Sampaio JP (2009b) Cystofilobasidium lacus-mascardii sp. nov., a basidiomycetous yeast species isolated from aquatic environments of the Patagonian Andes, and Cystofilobasidium macerans sp. nov., the sexual stage of Cryptococcus macerans. Int J Syst Evol Microbiol 59:622–630

    Article  PubMed  CAS  Google Scholar 

  • Libkind D, Moliné M, Bellora N, Hittinger C, Giraudo M (2011a) Genomic analysis of the astaxanthin producing yeast Phaffia rhodozyma (Xanthophyllomyces dendrorhous) with special focus on antioxidant-related genes. In: Proceeding meeting on comparative genomics of eukaryotic microorganisms: understanding the complexity of diversity, Saint Feliux de Guixols, España, 15–20 Oct 2011

    Google Scholar 

  • Libkind D, Moliné M, Sommaruga R, Sampaio JP, van Broock M (2011b) Phylogenetic distribution of fungal mycosporines within the Pucciniomycotina (Basidiomycota). Yeast 28:619–627

    Article  PubMed  CAS  Google Scholar 

  • Libkind D, Moliné M, van Broock M (2011c) Production of the UVB-absorbing compound mycosporine–glutaminol–glucoside by Xanthophyllomyces dendrorhous (Phaffia rhodozyma). FEMS Yeast Res 11:52–59

    Article  PubMed  CAS  Google Scholar 

  • Madeo F, Fröhlich E, Ligr M, Grey M, Sigrist SJ, Wolf DH, Fröhlich K-U (1999) Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 145:757–767

    Article  PubMed  CAS  Google Scholar 

  • Madhour A, Anke H, Mucci A, Davoli P, Weber RWS (2005) Biosynthesis of the xanthophyll plectaniaxanthin as a stress response in the red yeast Dioszegia (Tremellales, Heterobasidiomycetes, Fungi). Phytochemistry 66:2617–2626

    Article  PubMed  CAS  Google Scholar 

  • Margalith P, Meydav S (1968) Some observations on the carotenogenesis in the yeast Rhodotorula mucilaginosa. Phytochemistry 7:765–768

    Article  CAS  Google Scholar 

  • Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162:346–361

    Article  PubMed  Google Scholar 

  • Margesin R, Schinner F (1994) Properties of cold-adapted microorganisms and their potential role in biotechnology. J Biotechnol 33:1–14

    Article  CAS  Google Scholar 

  • Martelli H, da Silva IM (1993) β-carotene synthesis in Rhodotorula. In: Lester P (ed) Methods in enzymology, vol 214. Academic Press, New York, pp 386–390

    Google Scholar 

  • Masaki K, Dunlap W, Yamamoto Y, Karube I, Larsen R, Matsukawa R (1996) A natural antioxidant and its production process. Japanese Patent 9604230

    Google Scholar 

  • Maxwell WA, Macmillan JD, Chichester C (1966) Function of carotenoids in protection of Rhodotorula glutinis against irradiation from a gas laser. Photochem Photobiol 5:567–577

    Article  CAS  Google Scholar 

  • Méndez-Álvarez S, Rüfenacht K, Eggen RI (2000) The oxidative stress-sensitive yap1 null strain of Saccharomyces cerevisiae becomes resistant due to increased carotenoid lLevels upon the introduction of the Chlamydomonas reinhardtii cDNA, coding for the 60S ribosomal protein L10a. Biochem Biophys Res Comm 267:953–959

    Article  PubMed  CAS  Google Scholar 

  • Miller NJ, Sampson J, Candeias LP, Bramley PM, Rice-Evans CA (1996) Antioxidant activities of carotenes and xanthophylls. FEBS Lett 384:240–242

    Article  PubMed  CAS  Google Scholar 

  • Moliné M (2010) Produccion de compuestos fotoprotectores (carotenoides y micosporinas) por levaduras. PhD thesis, Universidad Nacional de Tucumán, Tucumán

    Google Scholar 

  • Moliné M, Libkind D, del Carmen Diéguez M, van Broock M (2009) Photoprotective role of carotenoids in yeasts: response to UV-B of pigmented and naturally-occurring albino strains. J Photochem Photobiol B: Biol 95:156–161

    Article  CAS  Google Scholar 

  • Moliné M, Flores MR, Libkind D, del Carmen Diéguez M, Farías ME, van Broock M (2010) Photoprotection by carotenoid pigments in the yeast Rhodotorula mucilaginosa: the role of torularhodin. Photochem Photobiol Sci 9:1145–1151

    Article  PubMed  CAS  Google Scholar 

  • Moliné M, Arbeloa EM, Flores MR, Libkind D, Farías ME, Bertolotti SG, Churio MS, van Broock MR (2011) UVB photoprotective role of mycosporines in yeast: photostability and antioxidant activity of mycosporine-glutaminol-glucoside. Rad Res 175:44–50

    Article  CAS  Google Scholar 

  • Moliné M, Libkind D, van Broock M (2012) Production of torularhodin, torulene, and β-carotene by Rhodotorula yeasts. In: Barredo J-L (ed) Microbial carotenoids from fungi, vol 898. Methods Mol Biol. Humana Press, New York, pp 275–283

    Google Scholar 

  • Moore MM, Breedveld MW, Autor AP (1989) The role of carotenoids in preventing oxidative damage in the pigmented yeast, Rhodotorula mucilaginosa. Arch Biochem Biophys 270:419–431

    Article  PubMed  CAS  Google Scholar 

  • Mrak EM, Phaff HJ, Mackinney G (1949) A simple test for carotenoid pigments in yeasts. J Bacteriol 57:409–411

    PubMed  CAS  Google Scholar 

  • Muñoz M (2010) Levaduras y hongos dimórficos del filoplano de Nothofagus pumilio y el papel de la exposición solar en su distribución y producción de metabolitos fotoprotectores. Undergraduate thesis, Universidad Nacional del Comahue, Bariloche

    Google Scholar 

  • Nakayama T, Mackinney G, Phaff HJ (1954) Carotenoids in asporogenous yeasts. A van Leeuwenhoek 20:217–228

    Article  CAS  Google Scholar 

  • Nam HS, Cho SY, Rhee JS (1988) High-performance liquid chromatographic analysis of major carotenoids from Rhodotorula glutinis. J Chromat A:445–447

    Google Scholar 

  • Ojima K, Breitenbach J, Visser H, Setoguchi Y, Tabata K, Hoshino T, Berg J, Sandmann G (2006) Cloning of the astaxanthin synthase gene from Xanthophyllomyces dendrorhous (Phaffia rhodozyma) and its assignment as a β-carotene 3-hydroxylase/4-ketolase. Mol Genet Genomics 275:148–158

    Article  PubMed  CAS  Google Scholar 

  • Ordoñez O, Flores M, Dib J, Paz A, Farías M (2009) Extremophile culture collection from Andean lakes: extreme pristine environments that host a wide diversity of microorganisms with tolerance to UV radiation. Microb Ecol 58:461–473

    Article  PubMed  Google Scholar 

  • Oren A (1997) Mycosporine-like amino acids as osmotic solutes in a community of halophilic cyanobacteria. Geomicrobiol J 14:231–240

    Article  CAS  Google Scholar 

  • Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol Lett 269:1–10

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Perrone GG, Tan SX, Dawes IW (2008) Reactive oxygen species and yeast apoptosis. Biochim Biophys Acta 1783:1354–1368

    Article  PubMed  CAS  Google Scholar 

  • Peterson WJ, Bell TA, Etchells JL, Smart WWG (1954) A procedure for demonstrating the presence of carotenoid pigments in yeasts. J Bacteriol 67:708–713

    PubMed  CAS  Google Scholar 

  • Peterson WJ, Evans WR, Lecce E, Bell TA, Etchells JL (1958) Quantitative determination of the carotenoids in yeasts of the genus Rhodotorula. J Bacteriol 75:586–591

    PubMed  CAS  Google Scholar 

  • Pittet J-L, Bouillant M-L, Bernillon J, Arpin N, Favre-Bonvin J (1983a) Sur la presence de mycosporines-glutamine reduites, nouvelles molecules, chez plusieurs deuteromycetes. Tetrahedron Lett 24:65–68

    Article  CAS  Google Scholar 

  • Pittet J-L, Létoublon R, Frot-Coutaz J, Arpin N (1983b) Soluble uridine diphospho-d-glucose: mycosporin glucosyltransferase from spores of Ascochyta fabae Speg. Planta 159:159–164

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pospíšil P (2009) Production of reactive oxygen species by photosystem II. Biochim. Biophys. Acta 1787:1151–1160

    Article  PubMed  CAS  Google Scholar 

  • Ravanat J-L, Douki T, Cadet J (2001) Direct and indirect effects of UV radiation on DNA and its components. J Photochem Photobiol B: Biol 63:88–102

    Article  CAS  Google Scholar 

  • Rodríguez-Sáiz M, de la Fuente JL, Barredo JL (2010) Xanthophyllomyces dendrorhous for the industrial production of astaxanthin. Appl Microbiol Biotechnol 88:645–658

    Article  PubMed  CAS  Google Scholar 

  • Rossi V, Bolognesi M, Languasco L, Giosuè S (2006) Influence of environmental conditions on infection of peach shoots by Taphrina deformans. Phytopathology 96:155–163

    Article  PubMed  CAS  Google Scholar 

  • Rothschild LJ (1999) Microbes and radiation. In: Seckbach (ed) Enigmatic microorganisms and life in extreme environments. Kluwer Academic Publishers, Amsterdam, pp 551–562

    Google Scholar 

  • Sakaki H, Nochide H, Nakanishi T, Miki W, Fujita T, Komemushi S (1999) Effect of culture condition on the biosynthesis of carotenoids in Rhodotorula glutinis No. 21. J Biosci Bioeng 87:400

    Google Scholar 

  • Sakaki H, Nakanishi T, Satonaka K-Y, Miki W, Fujita T, Komemushi S (2000) Properties of a high-torularhodin-producing mutant of Rhodotorula glutinis cultivated under oxidative stress. J Biosci Bioeng 89:203–205

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Sakaki H, Nochide H, Komemushi S, Miki W (2002) Effect of active oxygen species on the productivity of torularhodin by Rhodotorula glutinis No. 21. J Biosci Bioeng 93:338–340

    PubMed  CAS  Google Scholar 

  • Santopietro LMD, Spencer JFT, Spencer DM, Siñeriz F (1998) Effects of oxidative stress on the production of carotenoid pigments by Phaffia rhodozyma (Xanthophyllomyces dendrorhous). Folia Microbiol 43:173–176

    Article  CAS  Google Scholar 

  • Scherer S, Chen T, Böger P (1988) A new UV-A/B protecting pigment in the terrestrial cyanobacterium Nostoc commune. Plant Physiol 88:1055–1057

    Article  PubMed  CAS  Google Scholar 

  • Schisler DA, Janisiewicz W, Boekhout T, Kurtzman CP (2011) Agriculturally important yeasts. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study, vol 1. Elsevier, London, pp 45–52

    Chapter  Google Scholar 

  • Schroeder WA, Johnson EA (1993) Antioxidant role of carotenoids in Phaffia rhodozyma. J Gen Microbiol 139:907–912

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schroeder WA, Johnson EA (1995b) Singlet oxygen and peroxyl radicals regulate carotenoid biosynthesis in Phaffia rhodozyma. J Biol Chem 270:18374–18379

    Article  PubMed  CAS  Google Scholar 

  • Shan L, Terence HL, Yokoyama H, Simpson KL, Chichester CO (1973) Isolation and identification of 2-hydroxyplectaniaxanthin from Rhodotorula aurantiaca. Phytochemistry 12:2953–2956

    Article  Google Scholar 

  • Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262

    Article  PubMed  CAS  Google Scholar 

  • Shick JM, Romaine-Lioud S, Ferrier-Pages C, Gattuso J (1999) Ultraviolet-B radiation stimulates shikimate pathway-dependent accumulation of mycosporine-like amino acids in the coral Stylophora pistillata despite decreases in its population of symbiotic dinoflagellates. Limnol Oceanogr 44:1667–1682

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Singh SP, Klisch M, Sinha RP, Häder DP (2008) Effects of abiotic stressors on synthesis of the mycosporine-like amino acid shinorine in the cyanobacterium Anabaena variabilis PCC 7937. Photochem Photobiol 84:1500–1505

    Article  PubMed  CAS  Google Scholar 

  • Singh SP, Klisch M, Sinha RP, Häder D-P (2010) Genome mining of mycosporine-like amino acid (MAA) synthesizing and non-synthesizing cyanobacteria: a bioinformatics study. Genomics 95:120–128

    Article  PubMed  CAS  Google Scholar 

  • Sinha RP, Klisch M, Walter Helbling E, Häder D-P (2001) Induction of mycosporine-like amino acids (MAAs) in cyanobacteria by solar ultraviolet-B radiation. J Photochem Photobiol B: Biol 60:129–135

    Article  CAS  Google Scholar 

  • Sinha RP, Singh SP, Häder D-P (2007) Database on mycosporines and mycosporine-like amino acids (MAAs) in fungi, cyanobacteria, macroalgae, phytoplankton and animals. J Photochem Photobiol B: Biol 89:29–35

    Article  CAS  Google Scholar 

  • Sommaruga R (2001) The role of solar UV radiation in the ecology of alpine lakes J Photochem Photobiol B. Biol 62:35–42

    CAS  Google Scholar 

  • Sommaruga R, Libkind D, van Broock M, Whitehead K (2004) Mycosporine-glutaminol-glucoside, a UV-absorbing compound of two Rhodotorula yeast species. Yeast 21:1077–1081

    Article  PubMed  CAS  Google Scholar 

  • Sperstad S, Lutnæs B, Stormo S, 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 Biotech 33:269–273

    Article  CAS  Google Scholar 

  • Squina FM, Mercadante AZ (2005) Influence of nicotine and diphenylamine on the carotenoid composition of Rhodotorula strains. J Food Biochem 29:638–652

    Article  CAS  Google Scholar 

  • Suh HJ, Lee HW, Jung J (2003) Mycosporine glycine protects biological systems against photodynamic damage by quenching singlet oxygen with a high efficiency. Photochem Photobiol 78:109–113

    Article  PubMed  CAS  Google Scholar 

  • Tada M, Shiroishi M (1982a) Mechanism of Photoregulated Carotenogenesis in Rhodotorula minuta I. Photocontrol of carotenoid production. Plant Cell Physiol 23:541–547

    CAS  Google Scholar 

  • Tada M, Shiroishi M (1982b) Mechanism of photoregulated carotenogenesis in Rhodotorula minuta II. Aspects of photoregulative reaction. Plant Cell Physiol 23:549–556

    CAS  Google Scholar 

  • Tao C, Sugawara T, Maeda S, Wang X, Hirata T (2008) Antioxidative activities of a mycosporine-like amino acid, porphyra-334. Fish Sci 74:1166–1172

    Article  CAS  Google Scholar 

  • Tefft RE, Goodwin TW, Simpson KL (1970) Aspects of the stereochemistry of torularhodin biosynthesis. Biochem J 117:921–927

    PubMed  CAS  Google Scholar 

  • Tognetti C, Moliné M, van Broock M, Libkind D (2013) Favored isolation and rapid identificationof the astaxanthin-producing yeast Xanthophyllomyces dendrorhous (Phaffia rhodozyma) from environmental samples. J Basic Microbiol 53:1–7

    Article  CAS  Google Scholar 

  • Torres A, Hochberg M, Pergament I, Smoum R, Niddam V, Dembitsky VM, Temina M, Dor I, Lev O, Srebnik M (2004) A new UV-B absorbing mycosporine with photo protective activity from the lichenized ascomycete Collema cristatum. Eur J Biochem 271:780–784

    Article  PubMed  CAS  Google Scholar 

  • Trione E, Leach C, Mutch JT (1966) Sporogenic substances isolated from fungi. Nature 212:163

    Article  PubMed  CAS  Google Scholar 

  • Tsimako M, Guffogg S, Thomas-Hall S, Watson K (2002) Resistance to UVB radiation in Antarctic yeasts. Redox Rep 7:312–314

    Article  PubMed  Google Scholar 

  • Turchetti B, Buzzini P, Goretti M, Branda E, Diolaiuti G, D’Agata C, Smiraglia C, Vaughan-Martini A (2008) Psychrophilic yeasts in glacial environments of Alpine glaciers. FEMS Microbiol Ecol 63:73–83

    Article  PubMed  CAS  Google Scholar 

  • Turchetti B, Thomas Hall SR, Connell LB, Branda E, Buzzini P, Theelen B, Muller WH, Boekhout T (2011) Psychrophilic yeasts from Antarctica and European glaciers: description of Glaciozyma gen. nov., Glaciozyma martinii sp. nov. and Glaciozyma watsonii sp. nov. Extremophiles 15:573–586

    Article  PubMed  CAS  Google Scholar 

  • Valadon L (1976) Carotenoids as additional taxonomic characters in fungi: a review. Trans British Mycol Soc 67:1–15

    Article  Google Scholar 

  • Van Eijk G, Roeymans H (1982) Distribution of carotenoids and sterols in relation to the taxonomy of Taphrina and Protomyces. A van Leeuwenhoek 48:257–264

    Article  Google Scholar 

  • Vaz ABM, Rosa LH, Vieira MLA, Garcia Vd, Brandão LR, Teixeira LCRS, Moliné M, Libkind D, van Broock M, Rosa CA (2011) The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica. Braz J Microbiol 42:937–947

    Article  PubMed  CAS  Google Scholar 

  • Vincent WF, Neale PJ (2000) Mechanisms of UV damage to aquatic organisms. In: de Mora S, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, pp 149–176

    Google Scholar 

  • Vishniac HS (1996) Biodiversity of yeasts and filamentous microfungi in terrestrial Antarctic ecosystems. Biodivers Conserv 5:1365–1378

    Article  Google Scholar 

  • Volkmann M, Whitehead K, Rütters H, Rullkötter J, Gorbushina AA (2003) Mycosporine-glutamicol-glucoside: a natural UV-absorbing secondary metabolite of rock-inhabiting microcolonial fungi. Rap Comm Mass Spectrom 17:897–902

    Article  CAS  Google Scholar 

  • Wang Q-M, Jia J-H, Bai F-Y (2008) Diversity of basidiomycetous phylloplane yeasts belonging to the genus Dioszegia (Tremellales) and description of Dioszegia athyri sp. nov., Dioszegia butyracea sp. nov. and Dioszegia xingshanensis sp. nov. A van Leeuwenhoek 93:391–399

    Article  Google Scholar 

  • Weber RWS, Madhour A, Anke H, Mucci A, Davoli P (2005) 2-Hydroxytorularhodin, a new xanthophyll from the red yeast Sporobolomyces coprosmae. Helv Chim Acta 88:2960–2966

    Article  CAS  Google Scholar 

  • Whitehead K, Hedges JI (2005) Photodegradation and photosensitization of mycosporine-like amino acids. J Photochem Photobiol B: Biol 80:115–121

    Article  CAS  Google Scholar 

  • Yakovleva I, Bhagooli R, Takemura A, Hidaka M (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine. Comp Biochem Physiol Part B: Biochem Mol Biol 139:721–730

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Young H, Patterson VJ (1982) A uv protective compound from Glomerella cingulata—a mycosporine. Phytochemistry 21:1075–1077

    Article  CAS  Google Scholar 

  • Yurkov AM, Vustin MM, Tyaglov BV, Maksimova IA, Sineokiy SP (2008) Pigmented basidiomycetous yeasts are a promising source of carotenoids and ubiquinone Q10. Microbiology 77:1–6

    Article  CAS  Google Scholar 

  • Zagarese HE, Tartarotti B, Cravero W, Gonzalez P (1998) UV damage in shallow lakes: the implications of water mixing. J Plankton Res 20:1423–1433

    Article  Google Scholar 

  • Zalar P, Gostinčar C, De Hoog G, Uršič V, Sudhadham M, Gunde-Cimerman N (2008) Redefinition of Aureobasidium pullulans and its varieties. Studies Mycol 61:21–38

    Article  CAS  Google Scholar 

  • Zhang L, Li L, Wu Q (2007) Protective effects of mycosporine-like amino acids of Synechocystis sp. PCC 6803 and their partial characterization. J Photochem Photobiol B: Biol 86:240–245

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martín Moliné .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Moliné, M., Libkind, D., de Garcia, V., Giraudo, M.R. (2014). Production of Pigments and Photo-Protective Compounds by Cold-Adapted Yeasts. In: Buzzini, P., Margesin, R. (eds) Cold-adapted Yeasts. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-39681-6_9

Download citation

Publish with us

Policies and ethics