Skip to main content
Log in

Characterization of basidiomycetous yeasts in hypersaline soils of the Urmia Lake National Park, Iran

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

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.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alipour S (2006) Hydrochemistry of seasonal variation of Urmia Salt Lake, Iran. Saline Syst 2:1–8

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Botha A (2006) Yeasts in soil. In: Peter G, Rosa CA (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 221–240

    Chapter  Google Scholar 

  • Botha A (2011) The importance and ecology of yeasts in soil. Soil Biol Biochem 43:1–8

    Article  CAS  Google Scholar 

  • 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

    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  CAS  PubMed  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  Google Scholar 

  • Breuer U, Harms H (2006) Debaryomyces hansenii—an extremophilic yeast with biotechnological potential. Yeast 23:415–437

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Butinar L, Santos S, Spencer-Martins I, Oren A, Gunde-Cimerman N (2005b) Yeast diversity in hypersaline habitats. FEMS Microbiol Lett 244:229–234

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Buzzini P, Margesin R (2014) Cold-adapted yeasts: biodiversity, adaptation strategies and biotechnological significance. Springer, Berlin, Heidelberg

    Book  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 82:1161–1174

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    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  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Deák T (2006) Environmental factors influencing yeasts. In: Rosa CA, Peter G (eds) Biodiversity and ecophysiology of yeasts. Springer-Verlag, Berlin, pp 155–174

    Chapter  Google Scholar 

  • Dupont S, Rapoport A, Gervais P, Beney L (2014) The survival kit of Saccharomyces cerevisiae for anhydrobiosis. Appl Microbiol Biotechnol 98:8821–8834

    Article  CAS  PubMed  Google Scholar 

  • Eimanifar A, Mohebbi F (2007) Urmia Lake (Northwest Iran): a brief review. Saline Syst 3:2–8

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fonseca Á, Inácio J (2006) Phylloplane yeasts. In: Péter G, Rosa CA (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 263–301

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gadanho M, Libkind D, Sampaio JP (2006) Yeast diversity in the extreme acidic environments of the Iberian Pyrite Belt. Microb Ecol 52:552–563

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gunde-Cimerman AO, Plemenitaš A (eds) (2005) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer-Verlag, Heidelberg

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Kurtzman CP, Fell JW, Boekhout T (2011a) The yeasts: a taxonomic study, 5th edn. Elsevier, Amsterdam

    Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lisichkina GA, Babeva IP, Sorokin DYu (2003) Alkalitolerant yeasts from natural biotopes. Microbiology (Moscow) 72:695–698

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Madigan MT, Martinko JM, Parker J (1997) Brock biology of microorganisms, 6th edn. Prentice hall, Upper Saddle River

    Google Scholar 

  • Maksimova IA, Chernov IYu (2004) Community structure of yeast fungi in forest biogeocenoses. Microbiology (Moscow) 73:474–481

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Praphailong W, Fleet GH (2000) Debaryomyces. In: Robinson RK, Batt CA, Patel P (eds) Encyclopedia of food microbiology. Academic Press, London, pp 515–520

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Rosa CA, Péter G (2006) Biodiversity and ecophysiology of yeasts. Springer, Berlin

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Samson RA, Hoekstra ES, Frisvad JC, Filtenborg O (2000) Introduction to food and airborne fungi. Centraalbureau voor Schimmelcultures, Utrecht

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Sláviková E, Vadkertiová R (2000) The occurrence of yeasts in the forest soils. J Basic Microbiol 40:207–212

    Article  PubMed  Google Scholar 

  • Sláviková E, Vadkertiová R (2003) The diversity of yeasts in the agricultural soil. J Basic Microbiol 43:430–436

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Spencer JFT, Spencer DM (1997) Yeasts in natural and artificial habitat. Springer-Verlag, Berlin

    Book  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  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 martini sp. nov. and Glaciozyma watsonii sp. nov. Extremophiles 15:573–586

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Vishniac HS (2006) A multivariate analysis of soil yeasts isolated from a latitudinal gradient. Microb Ecol 52:90–103

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yurkov AM, Kemler M, Begerow D (2012) Assessment of yeast diversity in soils under different management regimes. Fungal Ecol 5:24–35

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pietro Buzzini.

Additional information

Communicated by A. Oren.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 761 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-016-0883-1

Keywords

Navigation