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Antonie van Leeuwenhoek

, Volume 107, Issue 1, pp 173–185 | Cite as

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

  • A. M. YurkovEmail author
  • A. V. Kachalkin
  • H. M. Daniel
  • M. Groenewald
  • D. Libkind
  • V. de Garcia
  • P. Zalar
  • D. E. Gouliamova
  • T. Boekhout
  • D. Begerow
Original Paper

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.

Keywords

Yeasts Fungi Basidiomycetes Pucciniomycotina New species Rhodotorula Cystobasidium 

Notes

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.

Supplementary material

10482_2014_315_MOESM1_ESM.doc (40 kb)
Supplementary material 1 (DOC 40 kb)
10482_2014_315_MOESM2_ESM.docx (139 kb)
Supplementary material 2 (DOCX 139 kb)

References

  1. 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 98:896–905PubMedCrossRefGoogle Scholar
  2. Bandoni RJ (1995) Dimorphic heterobasidiomycetes: taxonomy and parasitism. Stud Mycol 38:13–27Google Scholar
  3. Bauer R, Begerow D, Sampaio JP, Weiß M, Oberwinkler F (2006) The simple-septate basidiomycetes: a synopsis. Mycological Progress 5:41–66CrossRefGoogle Scholar
  4. 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 91:277–289PubMedCrossRefGoogle Scholar
  5. 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 53:1024–1031PubMedCrossRefGoogle Scholar
  6. 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 56:448–459PubMedCrossRefGoogle Scholar
  7. 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 63:3896–3903PubMedCrossRefGoogle Scholar
  8. de Azeredo LAI, Gomes EAT, Mendonça-Hagler LC, Hagler AN (1998) Yeast communities associated with sugarcane in Campos, Rio de Janeiro, Brazil. Int Microbiol 1:205–208PubMedGoogle Scholar
  9. 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 59:331–341PubMedCrossRefGoogle Scholar
  10. Diederich P (1996) The lichenicolous heterobasidiomycetes. Bibliotheca Lichenologica 61:1-198Google Scholar
  11. 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 38:129–146Google Scholar
  12. 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 50:1351–1371PubMedCrossRefGoogle Scholar
  13. Fonseca A (1992) Utilization of tartaric acid and related compounds by yeasts: taxonomic implications. Can J Microbiol 38:1242–1251PubMedCrossRefGoogle Scholar
  14. 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 263–303CrossRefGoogle Scholar
  15. Glushakova AM, Chernov IY (2010) Seasonal dynamics of the structure of epiphytic yeast communities. Microbiology 79:830–839CrossRefGoogle Scholar
  16. 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 98:93–101PubMedCrossRefGoogle Scholar
  17. Golubtsova YuV, Glushakova AM, Chernov IYu (2007) The seasonal dynamics of yeast communities in the rhizosphere of soddy-podzolic soils. Eurasian Soil Sci 40:875–879CrossRefGoogle Scholar
  18. Groenewald M, Smith MTh (2013) The teleomorph state of Candida deformans Langeron & Guerra and description of Yarrowia yakushimensis comb. nov. Anthonie Van Leeuwenhoek 103:1023–1028CrossRefGoogle Scholar
  19. 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 2:155–162PubMedCentralPubMedCrossRefGoogle Scholar
  20. Hibbett DS (2006) A phylogenetic overview of the Agaricomycotina. Mycologia 98:917–925PubMedCrossRefGoogle Scholar
  21. Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  22. 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 8:499–508PubMedCrossRefGoogle Scholar
  23. Kachalkin AV (2010) New data on the distribution of certain psychrophilic yeasts in Moscow oblast. Microbiology 79:840–844CrossRefGoogle Scholar
  24. Kachalkin AV (2014) Yeasts of the White Sea intertidal zone and description of Glaciozyma litorale sp. nov. Antonie Van Leeuwenhoek 105:1073–1083PubMedCrossRefGoogle Scholar
  25. 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 102:29–43PubMedCrossRefGoogle Scholar
  26. Kachalkin AV, Glushakova AM, Yurkov AM, Chernov IYu (2008) Characterization of yeast groupings in the phyllosphere of sphagnum mosses. Microbiology 77:474–481CrossRefGoogle Scholar
  27. 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 30:3059–3066PubMedCentralPubMedCrossRefGoogle Scholar
  28. 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 87–111Google Scholar
  29. Lachance MA (2012) In defense of yeast sexual life cycles: the forma asexualis: an informal proposal. Yeast Newslett 61:24–25Google Scholar
  30. Libkind D, Sampaio JP (2010) Rhodotorula. In: Liu, D. (Ed.). Molecular detection of foodborne pathogens. CRC Press-Taylor & Francis Group, Boca Raton, p 603–618Google Scholar
  31. 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 84:313–322PubMedCrossRefGoogle Scholar
  32. Libkind D, Sommaruga R, Zagarese H, van Broock M (2005) Mycosporines in carotenogenic yeasts. Syst Appl Microbiol 28:749–754PubMedCrossRefGoogle Scholar
  33. 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 60:2251–2256PubMedCrossRefGoogle Scholar
  34. 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 43:430–451PubMedCrossRefGoogle Scholar
  35. McNeill J, Turland NJ (2011) Major changes to the Code of Nomenclature-Melbourne, July 2011. Taxon 60:1495–1497Google Scholar
  36. Millanes AM, Diederich P, Ekman S, Wedin M (2011) Phylogeny and character evolution in the jelly fungi (Tremellomycetes, Basidiomycota, Fungi). Mol Phylogenet Evol 61:12–28PubMedCrossRefGoogle Scholar
  37. 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 241–263CrossRefGoogle Scholar
  38. 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 52:37–45PubMedCrossRefGoogle Scholar
  39. Norkrans B (1966) On the occurrence of yeasts in an estuary off the Swedish west coast. Svenska Botaniska Foreningen 60:463–482Google Scholar
  40. Nylander JA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67PubMedCrossRefGoogle Scholar
  41. 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 97:84–98PubMedCrossRefGoogle Scholar
  42. Sampaio JP (1999) Utilization of low molecular weight aromatic compounds by heterobasidiomycetous yeasts: taxonomic implications. Can J Microbiol 45:491–512PubMedCrossRefGoogle Scholar
  43. 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 1873–1927Google Scholar
  44. 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 1419–1422Google Scholar
  45. 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 1515–1518Google Scholar
  46. 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 2:53–68CrossRefGoogle Scholar
  47. 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 104:83–93PubMedCrossRefGoogle Scholar
  48. 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 2:495–517PubMedCrossRefGoogle Scholar
  49. 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 18:707–721PubMedCrossRefGoogle Scholar
  50. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337CrossRefGoogle Scholar
  51. Sláviková E, Vadkertiová R (1997) Seasonal occurrence of yeasts and yeast-like organisms in the river Danube. Antonie Van Leeuwenhoek 72:77–80PubMedCrossRefGoogle Scholar
  52. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75:758–771CrossRefGoogle Scholar
  53. 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 102:99–104PubMedCrossRefGoogle Scholar
  54. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729PubMedCentralPubMedCrossRefGoogle Scholar
  55. 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 105:486–495PubMedCrossRefGoogle Scholar
  56. Tuon FF, Costa SF (2008) Rhodotorula infection. A systematic rewiew of 128 cases from literature. Revista Iberoamericana de Micologia 25:135–140PubMedCrossRefGoogle Scholar
  57. 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 15:573–586PubMedCrossRefGoogle Scholar
  58. 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:e46060PubMedCentralPubMedCrossRefGoogle Scholar
  59. 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 8:799–814PubMedCrossRefGoogle Scholar
  60. 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 61:210–219PubMedCrossRefGoogle Scholar
  61. Wilgenbusch JC, Swofford D (2003) Inferring evolutionary trees with PAUP*. Current protocols in bioinformatics. Chap 6: Unit 6.4. John Wiley & Sons, Inc., Somerset, NJGoogle Scholar
  62. 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 61:680–689PubMedCrossRefGoogle Scholar
  63. 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 77–100CrossRefGoogle Scholar
  64. Yurkov AM, Chernov IY, Tiunov AV (2008a) Influence of Lumbricus terrestris earthworms on the structure of the yeast community of forest litter. Microbiology 77:107–111CrossRefGoogle Scholar
  65. 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 77:5–10Google Scholar
  66. Yurkov AM, Kemler M, Begerow D (2012) Assessment of yeast diversity in soils under different management regimes. Fungal Ecol 5:23–35CrossRefGoogle Scholar
  67. 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 57:191–195PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • A. M. Yurkov
    • 1
    Email author
  • A. V. Kachalkin
    • 2
  • H. M. Daniel
    • 3
  • M. Groenewald
    • 4
  • D. Libkind
    • 5
  • V. de Garcia
    • 5
  • P. Zalar
    • 6
  • D. E. Gouliamova
    • 7
  • T. Boekhout
    • 4
    • 8
    • 9
  • D. Begerow
    • 10
  1. 1.Leibniz Institute DSMZ-German Collection of Microorganisms and Cell CulturesBrunswickGermany
  2. 2.Faculty of Soil ScienceLomonosov Moscow State UniversityMoscowRussia
  3. 3.BCCM/MUCL, Earth and Life Institute, Applied Microbiology, MycologyUniversité catholique de LouvainLouvain-La-NeuveBelgium
  4. 4.CBS-KNAW Fungal Biodiversity CentreUtrechtThe Netherlands
  5. 5.Applied Microbiolgy and Biotechnology Lab., INIBIOMACONICET-UNComahueBarilocheArgentina
  6. 6.Department of Biology, Biotechnical FacultyUniversity of LjubljanaLjubljanaSlovenia
  7. 7.Department of General Microbiology, Institute of MicrobiologyBulgarian Academy of SciencesSofiaBulgaria
  8. 8.Department of Dermatology, Shanghai Key Laboratory of Molecular Medical Mycology, Institute of Dermatology and Medical Mycology, Changzheng HospitalSecond Military Medical UniversityShanghaiChina
  9. 9.State Key Laboratory of Mycology, Institute of MicrobiologyChinese Academy of SciencesBeijingChina
  10. 10.Geobotanik, Fakultät für Biologie und BiotechnologieRuhr-Universität BochumBochumGermany

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