Abstract
Yeasts, widely distributed across the Earth, have successfully colonized cold environments despite their adverse conditions for life. Lower eukaryotes play important ecological roles, contributing to nutrient recycling and organic matter mineralization. Yeasts have developed physiological adaptations to optimize their metabolism in low-temperature environments, which affect the rates of biochemical reactions and membrane fluidity. Decreased saturation of fatty acids helps maintain membrane fluidity at low temperatures and the production of compounds that inhibit ice crystallization, such as antifreeze proteins, helps microorganisms survive at temperatures around the freezing point of water. Furthermore, the production of hydrolytic extracellular enzymes active at low temperatures allows consumption of available carbon sources. Beyond their ecological importance, interest in psychrophilic yeasts has increased because of their biotechnological potential and industrial uses. Long-chain polyunsaturated fatty acids have beneficial effects on human health, and antifreeze proteins are attractive for food industries to maintain texture in food preserved at low temperatures. Furthermore, extracellular cold-active enzymes display unusual substrate specificities with higher catalytic efficiency at low temperatures than their mesophilic counterparts, making them attractive for industrial processes requiring high enzymatic activity at low temperatures. In this minireview, we describe the physiological adaptations of several psychrophilic yeasts and their possible biotechnological applications.
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Abd El Razak A, Ward AC, Glassey J (2014) Screening of marine bacterial producers of polyunsaturated fatty acids and optimisation of production. Microb Ecol 67:454–464
Abdullah SK (1989) Extracellular enzymatic activity of aquatic and aero-aquatic conidial fungi. Hydrobiologia 174:217–223
Alias N, Ahmad Mazian M, Salleh AB, Basri M, Rahman RN (2014) Molecular cloning and optimization for high level expression of cold-adapted serine protease from Antarctic yeast Glaciozyma antarctica PI12. Enzyme Res 2014:197938
Anwar A, Saleemuddin M (1998) Alkaline proteases: a review. Bioresour Technol 64:175–183
Bang JK, Lee JH, Murugan RN, Lee SG, Do H, Koh HY, Shim HE, Kim HC, Kim HJ (2013) Antifreeze peptides and glycopeptides, and their derivatives: potential uses in biotechnology. Mar Drugs 11:2013–2041
Bhuiyan M, Tucker D, Watson K (2014) Gas chromatography-mass spectrometry analysis of fatty acid profiles of Antarctic and non-Antarctic yeasts. Antonie Van Leeuwenhoek 106:381–389
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
Brandao LR, Libkind D, Vaz AB, Espirito Santo LC, Moline M, de Garcia 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
Burhan H, Ravinder SR, Deepak C, Poonam S, Fayaz AM, Sanjay S, Ishfaq A (2014) Psychrophilic yeasts and their biotechnological applications—a review. Afr J Biotechnol 13:2188–2197
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
Carrasco M, Rozas JM, Barahona S, Alcaino J, Cifuentes V, Baeza M (2012) Diversity and extracellular enzymatic activities of yeasts isolated from King George Island, the sub-Antarctic region. BMC Microbiol 12:251
Contreras G, Barahona S, Sepulveda D, Baeza M, Cifuentes V, Alcaino J (2015) Identification and analysis of metabolite production with biotechnological potential in Xanthophyllomyces dendrorhous isolates. World J Microbiol Biotechnol 31:517–526
D’Amico S, Sohier JS, Feller G (2006) Kinetics and energetics of ligand binding determined by microcalorimetry: insights into active site mobility in a psychrophilic alpha-amylase. J Mol Biol 358:1296–1304
Davies PL (2014) Ice-binding proteins: a remarkable diversity of structures for stopping and starting ice growth. Trends Biochem Sci 39:548–555
Davies PL, Baardsnes J, Kuiper MJ, Walker VK (2002) Structure and function of antifreeze proteins. Philos Trans R Soc Lond B Biol Sci 357:927–935
De Caterina R (2011) n-3 fatty acids in cardiovascular disease. N Engl J Med 364:2439–2450
de Garcia 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
de Garcia V, Brizzio S, van Broock MR (2012) Yeasts from glacial ice of Patagonian Andes, Argentina. FEMS Microbiol Ecol 82:540–550
DeVries AL, Wohlschlag DE (1969) Freezing resistance in some Antarctic fishes. Science 163:1073–1075
Duman J, Mark O (1993) Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology 30:322–328
Galdino AS, Silva RN, Lottermann MT, Alvares AC, de Moraes LM, Torres FA, de Freitas SM, Ulhoa CJ (2011) Biochemical and Structural characterization of amy1: an alpha-amylase from Cryptococcus flavus expressed in Saccharomyces cerevisiae. Enzyme Res 2011:157294
Gerday C, Aittaleb M, Bentahir M, Chessa JP, Claverie P, Collins T, D’Amico S, Dumont J, Garsoux G, Georlette D (2000) Cold-adapted enzymes: from fundamentals to biotechnology. Trends Biotechnol 18:103–107
Gilichinsky D, Rivkina E, Bakermans C, Shcherbakova V, Petrovskaya L, Ozerskaya S, Ivanushkina N, Kochkina G, Laurinavichuis K, Pecheritsina S, Fattakhova R, Tiedje JM (2005) Biodiversity of cryopegs in permafrost. FEMS Microbiol Ecol 53:117–128
Gomes FC, Safar SV, Marques AR, Medeiros AO, Santos AR, Carvalho C, Lachance MA, Sampaio JP, Rosa CA (2015) The diversity and extracellular enzymatic activities of yeasts isolated from water tanks of Vriesea minarum, an endangered bromeliad species in Brazil, and the description of Occultifur brasiliensis f.a., sp. nov. Antonie Van Leeuwenhoek 107:597–611
Guffogg SP, Thomas-Hall S, Holloway P, Watson K (2004) A novel psychrotolerant member of the hymenomycetous yeasts from Antarctica: Cryptococcus watticus sp. nov. Int J Syst Evol Microbiol 54:275–277
Gunde-Cimerman N, Plemenitaš A, Buzzini P (2014) Changes in lipids composition and fluidity of yeast plasma membrane as response to cold. In: Buzzini P, Margesin R (eds) Cold-adapted yeasts biodiversity, adaptation strategies and biotechnological significance. Springer, New York, pp 225–242
Gurung N, Ray S, Bose S, Rai V (2013) A broader view: microbial enzymes and their relevance in industries, medicine, and beyond. Biomed Res Int 2013:329121
Hashim NH, Bharudin I, Nguong DL, Higa S, Bakar FD, Nathan S, Rabu A, Kawahara H, Illias RM, Najimudin N, Mahadi NM, Murad AM (2013) Characterization of Afp1, an antifreeze protein from the psychrophilic yeast Glaciozyma antarctica PI12. Extremophiles 17:63–73
Hawes TC, Marshall CJ, Wharton DA (2011) Antifreeze proteins in the Antarctic springtail, Gressittacantha terranova. J Comp Physiol B 181:713–719
Heisig M, Abraham NM, Liu L, Neelakanta G, Mattessich S, Sultana H, Shang Z, Ansari JM, Killiam C, Walker W, Cooley L, Flavell RA, Agaisse H, Fikrig E (2014) Antivirulence properties of an antifreeze protein. Cell Rep 9:417–424
Iefuji H, Iimura Y, Obata T (1994) Isolation and characterization of a yeast sp. S-2 that produces raw starch-digesting-amylase, xylanase, and polygalacturonase. Biosci Biotechnol Biochem 58:2261–2262
Janeček Š, Ševčík J (1999) The evolution of starch-binding domain. FEBS Lett 456:119–125
Janeček S, Svensson B, MacGregor EA (2014) alpha-Amylase: an enzyme specificity found in various families of glycoside hydrolases. Cell Mol Life Sci 71:1149–1170
Joseph B, Ramteke PW, Thomas G (2008) Cold active microbial lipases: some hot issues and recent developments. Biotechnol Adv 26:457–470
Jung W, Gwak Y, Davies PL, Kim HJ, Jin E (2014) Isolation and characterization of antifreeze proteins from the antarctic marine microalga Pyramimonas gelidicola. Mar Biotechnol (NY) 16:502–512
Kádár Z, Szengyel Z, Réczey K (2004) Simultaneous saccharification and fermentation (SSF) of industrial wastes for the production of ethanol. Ind Crops Prod 20:103–110
Kasana RC, Gulati A (2011) Cellulases from psychrophilic microorganisms: a review. J Basic Microbiol 51:572–579
Koh HY, Lee JH, Han SJ, Park H, Lee SG (2015) Effect of the antifreeze protein from the arctic yeast Leucosporidium sp. AY30 on cryopreservation of the marine diatom Phaeodactylum tricornutum. Appl Biochem Biotechnol 175:677–686
Kumar V, Sinha AK, Makkar HPS, Becker K (2010) Dietary roles of phytate and phytase in human nutrition: a review. Food Chem 120:945–959
Lan DM, Yang N, Wang WK, Shen YF, Yang B, Wang YH (2011) A novel cold-active lipase from Candida albicans: cloning, expression and characterization of the recombinant enzyme. Int J Mol Sci 12:3950–3965
Lee JK, Park KS, Park S, Park H, Song YH, Kang SH, Kim HJ (2010) An extracellular ice-binding glycoprotein from an Arctic psychrophilic yeast. Cryobiology 60:222–228
Lee SG, Koh HY, Lee JH, Kang SH, Kim HJ (2012) Cryopreservative effects of the recombinant ice-binding protein from the arctic yeast Leucosporidium sp. on red blood cells. Appl Biochem Biotechnol 167:824–834
Libkind D, Arts MT, van Broock M (2008) Fatty acid composition of cold-adapted carotenogenic basidiomycetous yeasts. Rev Argent Microbiol 40:193–197
Loperena L, Soria V, Varela H, Lupo S, Bergalli A, Guigou M, Pellegrino A, Bernardo A, Calvino A, Rivas F, Batista S (2012) Extracellular enzymes produced by microorganisms isolated from maritime Antarctica. World J Microbiol Biotechnol 28:2249–2256
Ma C, Ni X, Chi Z, Ma L, Gao L (2007) Purification and characterization of an alkaline protease from the marine yeast Aureobasidium pullulans for bioactive peptide production from different sources. Mar Biotechnol 9:343–351
Margesin R, Feller G (2010) Biotechnological applications of psychrophiles. Environ Technol 31:835–844
Margesin R, Gander S, Zacke G, Gounot AM, Schinner F (2003) Hydrocarbon degradation and enzyme activities of cold-adapted bacteria and yeasts. Extremophiles 7:451–458
Margesin R, Neuner G, Storey KB (2007) Cold-loving microbes, plants, and animals—fundamental and applied aspects. Naturwissenschaften 94:77–99
McMurrough I, Rose AH (1973) Effects of temperature variation on the fatty acid composition of a psychrophilic Candida species. J Bacteriol 114:451–452
Pathan AA, Bhadra B, Begum Z, Shivaji S (2010) Diversity of yeasts from puddles in the vicinity of midre lovenbreen glacier, arctic and bioprospecting for enzymes and fatty acids. Curr Microbiol 60:307–314
Ramli AN, Mahadi NM, Rabu A, Murad AM, Bakar FD, Illias RM (2011) Molecular cloning, expression and biochemical characterisation of a cold-adapted novel recombinant chitinase from Glaciozyma antarctica PI12. Microb Cell Fact 10:94
Ratledge C (2004) Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie 86:807–815
Rossi M, Buzzini P, Cordisco L, Amaretti A, Sala M, Raimondi S, Ponzoni C, Pagnoni UM, Matteuzzi D (2009) Growth, lipid accumulation, and fatty acid composition in obligate psychrophilic, facultative psychrophilic, and mesophilic yeasts. FEMS Microbiol Ecol 69:363–372
Russell NJ (1990) Cold adaptation of microorganisms. Philos Trans R Soc Lond B Biol Sci 326:595–608
Russell NJ (2006) Antarctic microorganisms: coming in from the cold. Culture 27:1–8
Russell NJ (2008) Membrane components and cold sensing. In: Margesin R, Schinner F, Marx JC, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 177–190
Sharp KA (2011) A peek at ice binding by antifreeze proteins. Proc Natl Acad Sci USA 108:7281–7282
Shivaji S, Prasad GS (2009) Antarctic yeasts: biodiversity and potential applications. In: Satyanarayana T, Kunze G (eds) Yeast biotechnology: diversity and applications. Springer, Dordrecht, pp 3–18
Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731
Singh P, Tsuji M, Singh SM, Roy U, Hoshino T (2013) Taxonomic characterization, adaptation strategies and biotechnological potential of cryophilic yeasts from ice cores of Midre Lovenbreen glacier, Svalbard, Arctic. Cryobiology 66:167–175
Singh P, Singh SM, Tsuji M, Prasad GS, Hoshino T (2014) Rhodotorula svalbardensis sp. nov., a novel yeast species isolated from cryoconite holes of Ny-Alesund, Arctic. Cryobiology 68:122–128
Thomas-Hall S, Watson K (2002) Cryptococcus nyarrowii sp. nov., a basidiomycetous yeast from Antarctica. Int J Syst Evol Microbiol 52:1033–1038
Thomas-Hall S, Watson K, Scorzetti G (2002) Cryptococcus statzelliae sp. nov. and three novel strains of Cryptococcus victoriae, yeasts isolated from Antarctic soils. Int J Syst Evol Microbiol 52:2303–2308
Thomas-Hall SR, Turchetti B, Buzzini P, Branda E, Boekhout T, Theelen B, Watson K (2010) Cold-adapted yeasts from Antarctica and the Italian Alps-description of three novel species: Mrakia robertii sp. nov., Mrakia blollopis sp. nov. and Mrakiella niccombsii sp. nov. Extremophiles 14:47–59
Todde G, Hovmoller S, Laaksonen A (2015) Influence of antifreeze proteins on the ice/water interface. J Phys Chem B 119:3407–3413
Tsuji M, Singh SM, Yokota Y, Kudoh S, Hoshino T (2013a) Influence of initial pH on ethanol production by the Antarctic basidiomycetous yeast Mrakia blollopis. Biosci Biotechnol Biochem 77:2483–2485
Tsuji M, Yokota Y, Shimohara K, Kudoh S, Hoshino T (2013b) An application of wastewater treatment in a cold environment and stable lipase production of Antarctic basidiomycetous yeast Mrakia blollopis. PLoS One 8:e59376
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
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
Vaca I, Faundez C, Maza F, Paillavil B, Hernandez V, Acosta F, Levican G, Martinez C, Chavez R (2013) Cultivable psychrotolerant yeasts associated with Antarctic marine sponges. World J Microbiol Biotechnol 29:183–189
Venketesh S, Dayananda C (2008) Properties, potentials, and prospects of antifreeze proteins. Crit Rev Biotechnol 28:57–82
Vihinen M, Mantsala P (1989) Microbial amylolytic enzymes. Crit Rev Biochem Mol Biol 24:329–418
Wanderley KJ, Torres FAG, Moraes LÄMP, Ulhoa CJ (2004) Biochemical characterization of alpha-amylase from the yeast Cryptococcus flavus. FEMS Microbiol Lett 231:165–169
Warude D, Joshi K, Harsulkar A (2006) Polyunsaturated fatty acids: biotechnology. Crit Rev Biotechnol 26:83–93
Yu P, Wang XT, Liu JW (2015) Purification and characterization of a novel cold-adapted phytase from Rhodotorula mucilaginosa strain JMUY14 isolated from Antarctic. J Basic Microbiol 54:1–11
Zhang X, Hua M, Song C, Chi Z (2012) Occurrence and diversity of marine yeasts in Antarctica environments. J Ocean Univ China 11:70–74
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This work was funded by Grants Fondecyt 1130333 from Comisión Nacional de Investigación y Tecnología (Conicyt, Chile), and RT_07-13 from Instituto Antártico Chileno (INACH, Chile).
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Alcaíno, J., Cifuentes, V. & Baeza, M. Physiological adaptations of yeasts living in cold environments and their potential applications. World J Microbiol Biotechnol 31, 1467–1473 (2015). https://doi.org/10.1007/s11274-015-1900-8
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DOI: https://doi.org/10.1007/s11274-015-1900-8