Skip to main content
Log in

Two yeast species Cystobasidium psychroaquaticum f.a. sp. nov. and Cystobasidium rietchieii f.a. sp. nov. isolated from natural environments, and the transfer of Rhodotorula minuta clade members to the genus Cystobasidium

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Many species of dimorphic basidiomycetes are known only in their asexual phase and typically those pigmented in different hues of red have been classified in the large polyphyletic genus Rhodotorula. These yeasts are ubiquitous and include a few species of some clinical relevance. The phylogenetic distribution of Rhodotorula spans three classes: Microbotryomycetes, Cystobasidiomycetes and Exobasidiomycetes. Here, the presented multi-gene analyses resolved phylogenetic relationships between the second largest group of Rhodotorula and the mycoparasite Cystobasidium fimetarium (Cystobasidiales, Cystobasidiomycetes, Pucciniomycotina). Based on the results, we propose the transfer of nine species belonging to the Rhodotorula minuta clade into the genus Cystobasidium. As a result, the clinically relevant species R. minuta will be renamed Cystobasidium minutum. This proposal follows ongoing reassessments of the anamorphic genus Rhodotorula reducing the polyphyly of this genus. The delimitation of the R. minuta clade from Rhodotorula species comprised in Sporidiobolales including the type species Rhodotorula glutinis is an important step to overcome obsolete generic placements of asexual basidiomycetous yeasts. Our proposal will also help to distinguish most common red yeasts from clinical samples such as members of Sporidiobolales and Cystobasidiales. The diagnosis of the genus Cystobasidium is amended by including additional characteristics known for the related group of species. The taxonomic change enables us to classify two novel species with the phylogenetically related members of the R. minuta clade in Cystobasidium. The recently from natural environments isolated species are described here as Cystobasidium psychroaquaticum f.a. sp. nov. (K-833T = KBP 3881T = VKPM Y-3653T = CBS 11769T = MUCL 52875T = DSM 27713T) and Cystobasidium rietchiei f.a. sp. nov. (K-780T = KBP 4220T = VKPM Y-3658T = CBS 12324T = MUCL 53589T = DSM 27155T). The new species were registered in MycoBank under MB 809336 and MB 809337, respectively.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aime MC, Matheny PB, Henk DA, Frieders EM, Nilsson RH, Piepenbring M, McLaughlin DJ, Szabo LJ, Begerow D, Sampaio JP, Bauer R, Weiss M, Oberwinkler F, Hibbett D (2006) An overview of the higher level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences. Mycologia 98:896–905

    Article  CAS  PubMed  Google Scholar 

  • Bandoni RJ (1995) Dimorphic heterobasidiomycetes: taxonomy and parasitism. Stud Mycol 38:13–27

    Google Scholar 

  • Bauer R, Begerow D, Sampaio JP, Weiß M, Oberwinkler F (2006) The simple-septate basidiomycetes: a synopsis. Mycological Progress 5:41–66

    Article  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. Antonie Van Leeuwenhoek 91:277–289

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • Connell L, Redman R, Craig S, Scorzetti G, Iszard M, Rodriguez R (2008) Diversity of soil yeasts isolated from South Victoria Land, Antarctica. Microb Ecol 56:448–459

    Article  CAS  PubMed  Google Scholar 

  • Daniel HM, Rosa CA, São Thiago-Calaça PS, Antonini Y, Bastos EM, Evrard P, Huret S, Fidalgo-Jiménez A, Lachance MA (2013) Starmerella neotropicalis f.a. sp. nov., a yeast species found in bees and pollen. Int J Syst Evol Microbiol 63:3896–3903

    Article  CAS  PubMed  Google Scholar 

  • de Azeredo LAI, Gomes EAT, Mendonça-Hagler LC, Hagler AN (1998) Yeast communities associated with sugarcane in Campos, Rio de Janeiro, Brazil. Int Microbiol 1:205–208

    PubMed  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 

  • Diederich P (1996) The lichenicolous heterobasidiomycetes. Bibliotheca Lichenologica 61:1-198

  • Fell JW, Boekhout T, Freshwater DW (1995) The role of nucleotide sequence analysis in the systematics of the yeast genera Cryptococcus and Rhodotorula. Stud Mycol 38:129–146

    Google Scholar 

  • Fell JW, Boekhout T, Fonseca A, 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 50:1351–1371

    Article  CAS  PubMed  Google Scholar 

  • Fonseca A (1992) Utilization of tartaric acid and related compounds by yeasts: taxonomic implications. Can J Microbiol 38:1242–1251

    Article  CAS  PubMed  Google Scholar 

  • Fonseca A, Inacio J (2006) Phylloplane yeasts. In: Rosa CA, Peter G (eds) Biodiversity and Ecophysiology of Yeasts. The Yeast Handbook. Springer-Verlag, Heidelberg, pp 263–303

    Chapter  Google Scholar 

  • Glushakova AM, Chernov IY (2010) Seasonal dynamics of the structure of epiphytic yeast communities. Microbiology 79:830–839

    Article  CAS  Google Scholar 

  • Glushakova AM, Maximova IA, Kachalkin AV, Yurkov AM (2010) Ogataea cecidiorum sp. nov., a methanol-assimilating yeast isolated from galls on willow leaves. Antonie Van Leeuwenhoek 98:93–101

    Article  CAS  PubMed  Google Scholar 

  • Golubtsova YuV, Glushakova AM, Chernov IYu (2007) The seasonal dynamics of yeast communities in the rhizosphere of soddy-podzolic soils. Eurasian Soil Sci 40:875–879

    Article  Google Scholar 

  • Groenewald M, Smith MTh (2013) The teleomorph state of Candida deformans Langeron & Guerra and description of Yarrowia yakushimensis comb. nov. Anthonie Van Leeuwenhoek 103:1023–1028

    Article  CAS  Google Scholar 

  • Hawksworth DL (2011) A new dawn for the naming of fungi: impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal names. IMA Fungus 2:155–162

    Article  PubMed Central  PubMed  Google Scholar 

  • Hibbett DS (2006) A phylogenetic overview of the Agaricomycotina. Mycologia 98:917–925

    Article  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Inácio J, Landell MF, Valente P, Wang PH, Wang YT, Yang SH, Manson JS, Lachance MA, Rosa CA, Fonseca A (2008) Farysizyma gen. nov., an anamorphic genus in the Ustilaginales to accommodate three novel epiphytic basidiomycetous yeast species from America, Europe and Asia. FEMS Yeast Res 8:499–508

    Article  PubMed  Google Scholar 

  • Kachalkin AV (2010) New data on the distribution of certain psychrophilic yeasts in Moscow oblast. Microbiology 79:840–844

    Article  CAS  Google Scholar 

  • Kachalkin AV (2014) Yeasts of the White Sea intertidal zone and description of Glaciozyma litorale sp. nov. Antonie Van Leeuwenhoek 105:1073–1083

    Article  CAS  PubMed  Google Scholar 

  • Kachalkin AV, Yurkov AM (2012) Yeast communities in Sphagnum phyllosphere along the temperature-moisture ecocline in the boreal forest-swamp ecosystem and description of Candida sphagnicola sp. nov. Antonie Van Leeuwenhoek 102:29–43

    Article  PubMed  Google Scholar 

  • Kachalkin AV, Glushakova AM, Yurkov AM, Chernov IYu (2008) Characterization of yeast groupings in the phyllosphere of sphagnum mosses. Microbiology 77:474–481

    Article  CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform (describes the FFT-NS-1, FFT-NS-2 and FFT-NS-i strategies). Nucleic Acids Res 30:3059–3066

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kurtzman CP, Fell JW, Boekhout T, Robert V (2011) Methods for isolation, phenotypic characterization and maintenance of yeasts. In: Kurtzman CP, Fell JW, Boekhout T (eds), The yeasts, a taxonomic study, 5th edn, vol. 1. Elsevier, Amsterdam, p 87–111

  • Lachance MA (2012) In defense of yeast sexual life cycles: the forma asexualis: an informal proposal. Yeast Newslett 61:24–25

    Google Scholar 

  • Libkind D, Sampaio JP (2010) Rhodotorula. In: Liu, D. (Ed.). Molecular detection of foodborne pathogens. CRC Press-Taylor & Francis Group, Boca Raton, p 603–618

  • Libkind D, Brizzio S, Ruffini A, Gadanho M, van Broock M, Paulo Sampaio J (2003) Molecular characterization of carotenogenic yeasts from aquatic environments in Patagonia, Argentina. Antonie Van Leeuwenhoek 84:313–322

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Libkind D, Sampaio JP, van Broock M (2010) Cystobasidiomycetes yeasts from Patagonia (Argentina): description of Rhodotorula meli sp. nov. from glacial meltwater. Int J Syst Evol Microbiol 60:2251–2256

    Article  CAS  PubMed  Google Scholar 

  • Matheny PB, Wang Z, Binder M, Curtis JM, Lim YW, Nilsson RH, Hughes KW, Hofstetter V, Ammirati JF, Schoch CL, Langer E, Langer G, McLaughlin DJ, Wilson AW, Frøslev T, Ge ZW, Kerrigan RW, Slot JC, Yang ZL, Baroni TJ, Fischer M, Hosaka K, Matsuura K, Seidl MT, Vauras J, Hibbett DS (2006) Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). Mol Phylogenet Evol 43:430–451

    Article  PubMed  Google Scholar 

  • McNeill J, Turland NJ (2011) Major changes to the Code of Nomenclature-Melbourne, July 2011. Taxon 60:1495–1497

    Google Scholar 

  • Millanes AM, Diederich P, Ekman S, Wedin M (2011) Phylogeny and character evolution in the jelly fungi (Tremellomycetes, Basidiomycota, Fungi). Mol Phylogenet Evol 61:12–28

    Article  PubMed  Google Scholar 

  • Nagahama T (2006) Yeast biodiversity in freshwater, marine and deep-sea environments. In: Rosa CA, Peter G (eds) Biodiversity and Ecophysiology of Yeasts. The Yeast Handbook. Springer-Verlag, Heidelberg, pp 241–263

    Chapter  Google Scholar 

  • Nagahama T, Hamamoto M, Nakase T, Shimamura S, Horikoshi K (2006) Phylogenetic relationship within the Erythrobasidium clade: molecular phylogenies, secondary structure, and intron positions inferred from partial sequences of ribosomal RNA and elongation factor-1 α genes. J Gen Appl Microbiol 52:37–45

    Article  CAS  PubMed  Google Scholar 

  • Norkrans B (1966) On the occurrence of yeasts in an estuary off the Swedish west coast. Svenska Botaniska Foreningen 60:463–482

    Google Scholar 

  • Nylander JA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67

    Article  PubMed  Google Scholar 

  • Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-alpha sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98

    Article  CAS  PubMed  Google Scholar 

  • Sampaio JP (1999) Utilization of low molecular weight aromatic compounds by heterobasidiomycetous yeasts: taxonomic implications. Can J Microbiol 45:491–512

    Article  CAS  PubMed  Google Scholar 

  • Sampaio JP (2011) Rhodotorula Harrison (1928). In: Kurtzman C.P., Fell J.W., Boekhout T (eds), The yeasts, a taxonomic study, 5th edn, vol. 3. Elsevier, Amsterdam, p 1873–1927

  • Sampaio JP, Oberwinkler F (2011a) Cystobasidium (Lagerheim) Neuhoff (1924). In: Kurtzman C.P., Fell J.W., Boekhout T (eds), The yeasts, a taxonomic study, 5th edn, vol. 3. Elsevier, Amsterdam, p 1419–1422

  • Sampaio JP, Oberwinkler F (2011b) Occultifur Oberwinkler (1990). In: Kurtzman C.P., Fell J.W., Boekhout T (eds), The yeasts, a taxonomic study, 5th edn, vol. 3. Elsevier, Amsterdam, p 1515–1518

  • Sampaio JP, Gadanho M, Bauer R, Weiß M (2003) Taxonomic studies in the Microbotryomycetidae: Leucosporidium golubevii sp. nov., Leucosporidiella gen. nov. and the new orders Leucosporidiales and Sporidiobolales. Mycol Prog 2:53–68

    Article  Google Scholar 

  • Satoh K, Maeda M, Umeda Y, Sugamata M, Makimura K (2013) Cryptococcus lacticolor sp. nov. and Rhodotorula oligophaga sp. nov., novel yeasts isolated from the nasal smear microbiota of Queensland koalas kept in Japanese zoological parks. Antonie Van Leeuwenhoek 104:83–93

    Article  CAS  PubMed  Google Scholar 

  • Scorzetti G, Fell JW, Fonseca A, Statzell-Tallman A (2002) Systematics of basidiomycetous yeasts: a comparison of large subunit D1/D2 and internal transcribed spacer rDNA regions. FEMS Yeast Res 2:495–517

    Article  CAS  PubMed  Google Scholar 

  • Selbmann L, Turchetti B, Yurkov A, Cecchini C, Zucconi L, Isola D, Buzzini P, Onofri S (2014) Description of Taphrina antarctica f.a. sp. nov., a new anamorphic ascomycetous yeast species associated with Antarctic endolithic microbial communities and transfer of four Lalaria species in the genus Taphrina. Extremophiles 18:707–721

    Article  CAS  PubMed  Google Scholar 

  • Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337

    Article  Google Scholar 

  • Sláviková E, Vadkertiová R (1997) Seasonal occurrence of yeasts and yeast-like organisms in the river Danube. Antonie Van Leeuwenhoek 72:77–80

    Article  PubMed  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75:758–771

    Article  Google Scholar 

  • Suh SO, Maslov DA, Molestina RE, Zhou JJ (2012) Microbotryozyma collariae gen. nov., sp. nov., a basidiomycetous yeast isolated from a plant bug Collaria oleosa (Miridae). Antonie Van Leeuwenhoek 102:99–104

    Article  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Toome M, Roberson RW, Aime MC (2013) Meredithblackwellia eburnea gen. et sp. nov., Kriegeriaceae fam. nov. and Kriegeriales ord. nov. – toward resolving higher-level classification in Microbotryomycetes. Mycologia 105:486–495

    Article  PubMed  Google Scholar 

  • Tuon FF, Costa SF (2008) Rhodotorula infection. A systematic rewiew of 128 cases from literature. Revista Iberoamericana de Micologia 25:135–140

    Article  PubMed  Google Scholar 

  • Turchetti B, Thomas Hall SR, Connell LB, Branda E, Buzzini P, Theelen B, Müller 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  CAS  PubMed  Google Scholar 

  • Valente P, Boekhout T, Landell MF, Crestani J, Pagnocca FC, Sette LD, Passarini MR, Rosa CA, Brandão LR, Pimenta RS, Ribeiro JR, Garcia KM, Lee CF, Suh SO, Péter G, Dlauchy D, Fell JW, Scorzetti G, Theelen B, Vainstein MH (2012) Bandoniozyma gen. nov., a genus of fermentative and non-fermentative tremellaceous yeast species. PLoS One 7:e46060

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang QM, Bai FY (2008) Molecular phylogeny of basidiomycetous yeasts in the Cryptococcus luteolus lineage (Tremellales) based on nuclear rRNA and mitochondrial cytochrome b gene sequence analyses: proposal of Derxomyces gen. nov. and Hannaella gen. nov., and description of eight novel Derxomyces species. FEMS Yeast Res 8:799–814

    Article  CAS  PubMed  Google Scholar 

  • Wang QM, Bai FY, Fungsin B, Boekhout T, Nakase T (2011) Proposal of Mingxiaea gen. nov. for the anamorphic basidiomycetous yeast species in the Bulleribasidium clade (Tremellales) based on molecular phylogenetic analysis, with six new combinations and four novel species. Int J Syst Evol Microbiol 61:210–219

    Article  CAS  PubMed  Google Scholar 

  • Wilgenbusch JC, Swofford D (2003) Inferring evolutionary trees with PAUP*. Current protocols in bioinformatics. Chap 6: Unit 6.4. John Wiley & Sons, Inc., Somerset, NJ

  • Wuczkowski M, Passoth V, Turchetti B, Andersson AC, Olstorpe M, Laitila A, Theelen B, van Broock M, Buzzini P, Prillinger H, Sterflinger K, Schnürer J, Boekhout T, Libkind D (2011) Description of Holtermanniella gen. nov., including Holtermanniella takashimae sp. nov. and four new combinations, and proposal of the order Holtermanniales to accommodate tremellomycetous yeasts of the Holtermannia clade. Int J Syst Evol Microbiol 61:680–689

    Article  CAS  PubMed  Google Scholar 

  • Yarrow D (1998) Methods for the isolation, maintenance and identification of yeasts. In: Kurtzman CP, Fell JW (eds) The yeasts: a taxonomic study, 4th edn. Elsevier, Amsterdam, pp 77–100

    Chapter  Google Scholar 

  • Yurkov AM, Chernov IY, Tiunov AV (2008a) Influence of Lumbricus terrestris earthworms on the structure of the yeast community of forest litter. Microbiology 77:107–111

    Article  CAS  Google Scholar 

  • Yurkov AM, Vustin MM, Tyaglov BV, Maksimova IA, Sineokiy SP (2008b) Pigmented basidiomycetous yeasts are a promising source of carotenoids and ubiquinone Q(10). Microbiology 77:5–10

    Google Scholar 

  • Yurkov AM, Kemler M, Begerow D (2012) Assessment of yeast diversity in soils under different management regimes. Fungal Ecol 5:23–35

    Article  Google Scholar 

  • Zhou J, Chen M, Chen H, Pan W, Liao W (2014) Rhodotorula minuta as onychomycosis agent in a Chinese patient: first report and literature review. Mycoses 57:191–195

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

EXF strains were maintained in Ex Culture Collection of the Department of Biology, Biotechnical Faculty, University of Ljubljana, Infrastructural Centre Mycosmo, MRIC UL. Authors are grateful to Mario Muñoz for his assistance in isolating strain CRUB 1888. This study was supported by UNComahue (DL: project B171), CONICET (DL: Project PIP 424), the Belgian Federal Science Policy (HMD: BCCM C4/10/017), and by the grant of the President of Russian Federation (AK: MK-788.2014.4). A research visit of Dr. Dilnora Gouliamova to CBS Fungal Biodiversity Centre was supported by The European Consortium of Microbial Resource Centres (EMbaRC) training program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. M. Yurkov.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 40 kb)

Supplementary material 2 (DOCX 139 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yurkov, A.M., Kachalkin, A.V., Daniel, H.M. et al. Two yeast species Cystobasidium psychroaquaticum f.a. sp. nov. and Cystobasidium rietchieii f.a. sp. nov. isolated from natural environments, and the transfer of Rhodotorula minuta clade members to the genus Cystobasidium . Antonie van Leeuwenhoek 107, 173–185 (2015). https://doi.org/10.1007/s10482-014-0315-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-014-0315-0

Keywords

Navigation