Abstract
Urmia Lake, located in northwest Iran, is an oligotrophic and extremely hypersaline habitat that supports diverse forms of life. Owing to its unique biodiversity and special environmental conditions, Urmia Lake National Park has been designated as one of the biosphere reserves by UNESCO. This study was aimed to characterize basidiomycetous yeasts in hypersaline soils surrounding the Urmia Lake National Park using a polyphasic combination of molecular and physiological data. Soil samples were collected from eight sites in Lake Basin and six islands insides the lake. Yeast strains were identified by sequencing the D1/D2 domains of the 26S rRNA gene. When D1/D2 domain sequencing did not resolve the identity of the species, strain identification was obtained by ITS 1 & 2 sequencing. Twenty-one species belonging to the genera Cystobasidium, Holtermanniella, Naganishia, Rhodotorula, Saitozyma, Solicoccozyma, Tausonia, Vanrija, and Vishniacozyma were identified. Solicoccozyma aeria represented the dominant species. The ability of isolates to grow at 10 and 15 % of NaCl was checked; about two-thirds of the strains grew at 10 %, while about 13 % of the isolates grew in medium with 15 % NaCl. this study is the first study on the culturable yeast diversity in hypersaline soils surrounding an Asian lake.
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References
Alipour S (2006) Hydrochemistry of seasonal variation of Urmia Salt Lake, Iran. Saline Syst 2:1–8
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Arenz BE, Held BW, Jurgens JA, Farrell RL, Blanchette RA (2006) Fungal diversity in soils and historic wood from the Ross Sea region of Antarctica. Soil Biol Biochem 38:3057–3064
Asem A, Eimanifar A, Djamali M, De los Rios P, Wink M (2014) Biodiversity of the hypersaline Urmia Lake National Park (NW Iran). Diversity 6:102–132
Borovikova D, Muiznieks I, Rapoport A (2015) New test-system based on the evaluation of yeast cells resistance to dehydration–rehydration stress. Open Biotechnol J 9:49–53
Botha A (2006) Yeasts in soil. In: Peter G, Rosa CA (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 221–240
Botha A (2011) The importance and ecology of yeasts in soil. Soil Biol Biochem 43:1–8
Boundy-Mills K (2014) Methods for the isolation and investigation of the diversity of cold-adapted yeasts and their in situ preservation in worldwide collections. In: Buzzini P, Margesin R (eds) Cold-adapted yeasts. Biodiversity, adaptation stategies and biotechnological significance. Springer, Berlin, pp 23–45
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
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
Breuer U, Harms H (2006) Debaryomyces hansenii—an extremophilic yeast with biotechnological potential. Yeast 23:415–437
Brizzio S, Turchetti B, de Garcia V, Libkind D, Buzzini P, van Brook M (2007) Extracellular enzymatic activities of basidiomycetous yeasts isolated from glacial and subglacial waters of northwest Patagonia (Argentina). Can J Microbiol 53:519–525
Burgaud G, Arzur D, Durand L, Cambon-Bonavita MA, Barbier G (2010) Marine culturable yeasts in deep-sea hydrother-mal vents: species richness and association with fauna. FEMS Microbiol Ecol 73:121–133
Butinar L, Sonjak S, Zalar P, Plemenitaš A, Gunde-Cimerman N (2005a) Melanized halophilic fungi are eukaryotic members of microbial communities in hypersaline waters of solar salterns. Bot Mar 48:73–79
Butinar L, Santos S, Spencer-Martins I, Oren A, Gunde-Cimerman N (2005b) Yeast diversity in hypersaline habitats. FEMS Microbiol Lett 244:229–234
Butinar L, Spencer-Martins I, Gunde-Cimerman N (2007) Yeasts in high Arctic glaciers: the discovery of a new habitat for eukaryotic microorganisms. Anton Leeuw Int J G 97:277–289
Buzzini P, Margesin R (2014) Cold-adapted yeasts: biodiversity, adaptation strategies and biotechnological significance. Springer, Berlin, Heidelberg
Buzzini P, Branda E, Goretti M, Turchetti B (2012) Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiol Ecol 82:1161–1174
Chi Z, Chi Z, Zhang T, Liu G, Li J, Wang X (2009) Production, characterization and gene cloning of the extracellular enzymes from the marine-derived yeasts and their potential applications. Biotechnology 27:236–255
Connell LB, Redman R, Craig S, Rodriguez R (2006) Distribution and abundance of fungi in the soils of Taylor Valley, Antarctica. Soil Biol Biochem 38:3083–3094
Connell LB, Redman R, Craig S, Scorzetti G, Iszard M, Rodriguez R (2008) Diversity of soil yeasts isolated from South Victoria Land, Antarctica. Microbiol Ecol 56:448–459
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
de García V, Brizzio S, Russo G, Rosa CA, Boekhout T, Theelen B, Libkind D, van Broock MR (2010) Cryptococcus spencermartinsiae sp. nov., a basidiomycetous yeast isolated from glacial waters and apple fruits. Int J Syst Evol Microbiol 60:707–711
Deák T (2006) Environmental factors influencing yeasts. In: Rosa CA, Peter G (eds) Biodiversity and ecophysiology of yeasts. Springer-Verlag, Berlin, pp 155–174
Dupont S, Rapoport A, Gervais P, Beney L (2014) The survival kit of Saccharomyces cerevisiae for anhydrobiosis. Appl Microbiol Biotechnol 98:8821–8834
Eimanifar A, Mohebbi F (2007) Urmia Lake (Northwest Iran): a brief review. Saline Syst 3:2–8
Fell JW, Boekhout T, Fonseca Á, Scorzetti G, Statzell- Tallman A (2000) Biodiversity and systematics of basidiomycetous yeasts as determined by large-subunit rDNA D1/D2 domain sequence analysis. Int J Syst Evol Microbiol 50:1351–1372
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fonseca Á, Inácio J (2006) Phylloplane yeasts. In: Péter G, Rosa CA (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 263–301
Fonseca A, Scorzetti G, Fell JW (2000) Diversity in the yeast Cryptococcus albidus and related species as revealed by ribosomal DNA sequence analysis. Can J Microbiol 46:7–27
Fonseca A, Boekhout T, Fell JW (2011) Cryptococcus Vuillemin (1901). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, Amsterdam, pp 1661–1737
França L, Sannino C, Turchetti B, Buzzini P, Margesin R (2016) Seasonal and altitudinal changes of culturable bacterial and yeast diversity in Alpine forest soils. Extremophiles. doi:10.1007/s00792-016-0874-2
Fraser JA, Lim SMC, Diezmann S, Wenink EC, Arndt CG, Cox GM, Dietrich FS, Heitman J (2006) Yeast diversity sampling on the San Juan Islands reveals no evidence for the spread of the Vancouver Island Cryptococcus gattii outbreak to this locale. FEMS Yeast Res 6:620–624
Gadanho M, Sampaio JP (2002) Polyphasic taxonomy of the basidiomycetous yeast genus Rhodotorula: Rh. glutinis sensu strict and Rh. dairenensis comb. nov. FEMS Yeast Res 2:47–58
Gadanho M, Sampaio JP (2005) Occurrence and diversity of yeasts in the mid-atlantic ridge hydrothermal fields near the Azores Archipelago. Microb Ecol 50:408–417
Gadanho M, Almeida JMGCF, Sampaio JP (2003) Assessment of yeast diversity in a marine environment in the south of Portugal by microsatellite-primed PCR. Anton Leeuw Int J G 84:217–227
Gadanho M, Libkind D, Sampaio JP (2006) Yeast diversity in the extreme acidic environments of the Iberian Pyrite Belt. Microb Ecol 52:552–563
Gao L, Chi Z, Sheng J, WangL Li J, Gong F (2007) Inulinase-producing marine yeasts: evaluation of their diversity and inulin hydrolysis by their crude enzymes. Microb Ecol 54:722–729
Gildemacher PR, Heijne B, Houbraken J, Vromans T, Hoekstra ES, Boekhout T (2004) Can phyllosphere yeasts explain the effect of scab fungicides on russeting of Elstar apples? Eur J Plant Pathol 110:929–937
Gildemacher PR, Heijne B, Silvestri M, Houbraken J, Hoekstra E, Boekhout T (2006) Interactions between yeasts, fungicides and apple fruit russeting. FEMS Yeast Res 6:1149–1156
Grum-Grzhimaylo AA, Georgieva ML, Bondarenko SA, Debets AJM, Bilanenko EN (2016) On the diversity of fungi from soda soils. Fungal Divers 76:27–74
Gunde-Cimerman AO, Plemenitaš A (eds) (2005) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer-Verlag, Heidelberg
Gunde-Cimerman AO, Zalar P, de Hoog S, Plemenitaš A (2000) Hypersaline waters in salterns—natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32:235–240
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, 5th edn. Elsevier, Amsterdam, pp 1929–1990
Inácio J, Pereira P, Carvalho M, Fonseca A, Amaral-Collaco MT, Spencer-Martins I (2002) Estimation and diversity of phylloplane mycobiota on selected plants in a mediterranean-type ecosystem in Portugal. Microb Ecol 44:344–353
Inácio J, Portugal L, Spencer-Martins I, Fonseca Á (2005) Phylloplane yeasts from Portugal: seven novel anamorphic species in the Tremellales lineage of the Hymenomycetes (Basidiomycota) producing orangecolouredm colonies. FEMS Yeast Res 5:1167–1183
Kurtzman CP, Fell JW, Boekhout T (2011a) The yeasts: a taxonomic study, 5th edn. Elsevier, Amsterdam
Kurtzman CP, Fell JW, Boekhout T, Robert V (2011b) Methods for isolation, phenotypic characterization and maintenance of yeasts. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study, 5th edn. Elsevier, Amsterdam, pp 87–110
Lahav R, Fareleira P, Nejidat A, Abeliovich A (2002) The identification and characterization of osmotolerant yeast isolates from chemical wastewater evaporation ponds. Microb Ecol 43:388–396
Legendre P, Legendre L (1998) Numerical ecology. Elsevier
Libkind D, Brizzio S, Ruffini A, Gadanho M, van Broock M, Sampaio JP (2003) Molecular characterization of carotenogenic yeasts from aquatic environments in Patagonia Argentina. Anton Leeuw Int J G 84:313–322
Libkind D, Gadanho M, van Broock M, Sampaio JP (2009) Cystofilobasidium lacus-mascardii sp. nov., a new teleomorphic basidiomycetous yeast species isolated fromaquatic environments in the Patagonian Andes, and Cystofilobasidium macerans sp. nov., the sexual stage of Cryptococcus macerans. Int J Syst Evol Microbiol 59:622–630
Lisichkina GA, Babeva IP, Sorokin DYu (2003) Alkalitolerant yeasts from natural biotopes. Microbiology (Moscow) 72:695–698
Liu XZ, Wang QM, Groenewald M, Kachalkin AV, Lumbsch HT, Millanes AM, Wedin M, Yurkov AM, Boekhout T, Bai FY (2015) Towards an integrated phylogenetic classification of tremellomycetous yeasts. Stud Mycol 81:84–146
Madigan MT, Martinko JM, Parker J (1997) Brock biology of microorganisms, 6th edn. Prentice hall, Upper Saddle River
Maksimova IA, Chernov IYu (2004) Community structure of yeast fungi in forest biogeocenoses. Microbiology (Moscow) 73:474–481
Maráz A, Kovács M (2013) Food spoilage by cold-adapted yeasts. In: Buzzini P, Margesin R (eds) Cold-adapted yeasts: biodiversity, adaptation strategies and biotechnological significance. Springer, Heidelberg, pp 497–532
Mestre MC, Rosa CA, Fontenla SB (2011) Lindnera rhizosphaerae sp. nov., a novel yeast species isolated from rhizospheric soil in a Patagonian native forest (Argentina). Int J Syst Evol Microbiol 61:985–988
Mokhtarnejad L, Arzanlou M, Babai-ahari A (2015) Molecular and phenotypic characterization of ascomycetous yeasts in hypersaline soils of Urmia Lake basin (NW Iran). Rostaniha 16:174–185
Nagahama T, Hamamoto M, Nakase T, Takami H, Horikoshi K (2001) Distribution and identification of red yeasts in deep-sea environments around the northwest Pacific Ocean. Anton Leeuw Int J G 80:101–110
Nelson DW, Sommers LP (1986) Total carbon, organic carbon and organic matter. In: Page AL (ed) Methods of soil analysis: part 2: chemical methods. American Society of Agronomy and Soil Science, Madison, pp 539–579
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: community ecology package. R package version 2.0-10. http://CRAN.Rproject.org/package=vegan. Accessed 07 Oct 2016
Papouskova K, Sychrova H (2007) The co-action of osmotic and high temperature stresses results in a growth improvement of Debaryomyces hansenii cells. Int J Food Microbiol 118:1–7
Praphailong W, Fleet GH (2000) Debaryomyces. In: Robinson RK, Batt CA, Patel P (eds) Encyclopedia of food microbiology. Academic Press, London, pp 515–520
Prista C, Almagro A, Loureiro-Días MC, Ramos J (1997) Physiological basis for the high tolerance of Debaryomyces hansenii. Appl Environ Microbiol 63:4005–4009
Prista C, Loureiro-Dias MC, Montiel V, García R, Ramos J (2005) Mechanisms underlying the halotolerant way of Debaryomyces hansenii. FEMS Yeast Res 5:693–701
R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed 07 Oct 2016
Rapoport A, Turchetti B, Buzzini P (2016) Application of anhydrobiosis and dehydration of yeasts for non-conventional biotechnological goals. World J Microbiol Biotechnol 32:104
Raspor P, Zupan J (2006) Yeasts in Extreme environments. In: Rosa CA, Péter G (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin., pp 371–417
Rosa CA, Péter G (2006) Biodiversity and ecophysiology of yeasts. Springer, Berlin
Russo G, Libkind D, Ulloa RJ, de García V, Sampaio JP, van Broock MR (2010) Cryptococcus agrionensis sp. nov., a basidiomycetous yeast of the acidic rock drainage ecoclade, isolated from acidic aquatic environment of volcanic origin (River Agrio, Argentina). Int J Syst Evol Microbiol 60:996–1000
Sampaio JP (2011) Rhodotorula Harrison (1928). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, Amsterdam, pp 1873–1927
Sampaio JP, Gadanho M, Santos S, Duarte F, Pais C, Fonseca A, Fell JW (2001) Polyphasic taxonomy of the genus Rhodosporidium: R. kratochvilovae and related anamorphic species. Int J Syst Evol Microbiol 51:687–697
Samson RA, Hoekstra ES, Frisvad JC, Filtenborg O (2000) Introduction to food and airborne fungi. Centraalbureau voor Schimmelcultures, Utrecht
Schaaf T, Clamote Rodrigues D (2016) Harmonising the management of Multi-Internationally Designated Areas: Ramsar Sites, World Heritage sites, Biosphere Reserves and UNESCO Global Geoparks. IUCN, Gland, Switzerland
Schoch CL, Seifert KA, Huhndorf A, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 109:6241–6246
Scorzetti G, Fell JW, Fonseca A, Statzell-Tallman A (2002) Systematics of basidiomycetous yeasts: a comparison of large sub-unit D1/D2 and internal transcribed spacer rDNA regions. FEMS Yeast Res 2:495–517
Selbmann L, Zucconi L, Onofri S, Cecchini C, Isola D, Turchetti B, Buzzini P (2013) Taxonomic and phenotypic characterization of yeasts isolated from worldwide cold rock-associated habitats. Fungal Biol 118(1):61–71
Sláviková E, Vadkertiová R (2000) The occurrence of yeasts in the forest soils. J Basic Microbiol 40:207–212
Sláviková E, Vadkertiová R (2003) The diversity of yeasts in the agricultural soil. J Basic Microbiol 43:430–436
Soares CAG, Maury M, Pagnocca FC, Araujo FV, Mendoca-Hagler LC (1997) Ascomycetous yeast from tropical intertidal dark mud of southeast Brazilian estuaries. J Gen Appl Microbiol 43:265–272
Spencer JFT, Spencer DM (1997) Yeasts in natural and artificial habitat. Springer-Verlag, Berlin
Starmer WT, Lachance MA (2011) Yeast ecology. In: Kurtzman CP, J Fell, Boekhout T (eds) The yeasts: a taxonomic study, 5th ed. Elsevier, pp 65–83
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tosi S, Onofri S, Brusoni M, Zucconi L, Vishniac HS (2005) Response of Antarctic soil fungal assemblages to experimental warming and reduction of UV radiation. Polar Biol 28:470–482
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 martini sp. nov. and Glaciozyma watsonii sp. nov. Extremophiles 15:573–586
Turchetti B, Goretti M, Branda E, Diolaiuti G, D’Agata C, Smiraglia C, Onofri A, Buzzini P (2013) Influence of abiotic variables on culturable yeast diversity in two distinct Alpine glaciers. FEMS Microbiol Ecol 86:327–340
Vishniac HS (2006) A multivariate analysis of soil yeasts isolated from a latitudinal gradient. Microb Ecol 52:90–103
Wang QM, Yurkov AM, Göker M, Lumbsch HT, Leavitt SD, Groenewald M, Theelen B, Liu XZ, Boekhout T, Bai FY (2015) Phylogenetic classification of yeasts and related taxa within Pucciniomycotina. Stud Mycol 81:149–189
Wuczkowski M, Metzger E, Sterflinger K, Prillinger H (2005) Diversity of yeasts isolated from litter and soil of different natural forest sites in Austria. Die Bodenkultur 56:201–208
Yurkov AM, Kemler M, Begerow D (2011) Species accumulation curves and incidence-based species richness estimators to appraise the diversity of cultivable yeasts from beech forest soils. PLoS One 6:e23671
Yurkov AM, Kemler M, Begerow D (2012) Assessment of yeast diversity in soils under different management regimes. Fungal Ecol 5:24–35
Yurkov AM, Inácio J, Chernov IY, Fonseca A (2015) Yeast biogeography and the effects of species recognition approaches: the case study of widespread basidiomycetous species from birch forests in Russia. Curr Microbiol 70:587–601
Yurkov AM, Röhl O, Pontes A, Carvalho C, Maldonado C, Sampaio JP (2016) Local climatic conditions constrain soil yeast diversity patterns in Mediterranean forests, woodlands and scrub biome. FEMS Yeast Res 16: fov103
Zalar P, Gunde-Cimerman N (2014) Cold-adapted yeasts in Antarctic habitats. In: Buzzini P, Margesin R (eds) Cold-adapted yeasts: biodiversity, adaptation strategies and biotechnological significance. Springer, Berlin, Heidelberg, pp 49–73
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This work was accomplished with financial aid from the University of Tabriz, Iran. This work was also supported by the DBVPG at the University of Perugia, Italy.
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Mokhtarnejad, L., Arzanlou, M., Babai-Ahari, A. et al. Characterization of basidiomycetous yeasts in hypersaline soils of the Urmia Lake National Park, Iran. Extremophiles 20, 915–928 (2016). https://doi.org/10.1007/s00792-016-0883-1
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DOI: https://doi.org/10.1007/s00792-016-0883-1