1887

Abstract

is a pink yeast-like fungus that is not congeneric with other members of (Basidiomycota, Microbotryomycetes, Sporidiobolales). During our ongoing studies of pink yeasts we determined that was most closely related to (Ascomycota, Leotiomycetes, Thelebolales). A molecular phylogenetic analysis using sequences of the ITS region and the small and large subunit (SSU, LSU) rRNA genes, indicated that four isolates of , including three ex-type isolates, were placed in Thelebolales with maximum support. A new genus is proposed to accommodate , . This is the first pink yeast reported in Leotiomycetes.

Funding
This study was supported by the:
  • Institute of Food and Agricultural Sciences (Award Hatch project 1010662)
    • Principle Award Recipient: M.Catherine Aime
  • Division of Environmental Biology (Award DEB-2018098)
    • Principle Award Recipient: DannyHaelewaters
  • Agricultural Research Service (Award 8072-42000-077-00D)
    • Principle Award Recipient: M.Catherine Aime
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2021-07-02
2021-10-24
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References

  1. Valadon LRG. Carotenoids as additional taxonomic characters in fungi: A review. Trans Brit Mycol Soc 1976; 67:1–15 [View Article]
    [Google Scholar]
  2. Ratledge C. Microorganisms for lipids. Acta Biotechnol 1991; 11:429–438 [View Article]
    [Google Scholar]
  3. Urbina H, Aime MC. A closer look at Sporidiobolales: Ubiquitous microbial community members of plant and food biospheres. Mycologia 2018; 110:79–92 [View Article]
    [Google Scholar]
  4. Davoli P, Mierau V, Weber RW. Carotenoids and fatty acids in red yeasts Sporobolomyces roseus and Rhodotorula glutinis. Appl Biochem Microbiol 2004; 40:460–465 [View Article]
    [Google Scholar]
  5. Manimala MRA, Murugesan R. In vitro antioxidant and antimicrobial activity of carotenoid pigment extracted from Sporobolomyces sp. isolated from natural source. J Appl Nat Sci 2014; 6:649–653 [View Article]
    [Google Scholar]
  6. Frengova G, Beshkova M. Carotenoids from Rhodotorula and Phaffia: yeasts of biotechnological importance. J Ind Microbiolol Biotechnol 2009; 36:163–180 [View Article]
    [Google Scholar]
  7. Mannazzu I, Landolfo S, da ST, Buzzini P. Red yeasts and carotenoid production: outlining a future for non-conventional yeasts of biotechnological interest. World J Microbiol Biotechnol 2015; 31:1665–1673 [View Article]
    [Google Scholar]
  8. AH L, Yuan FX, Groenewald M, Bensch K, Yurkov AM et al. Diversity and phylogeny of basidiomycetous yeasts from plant leaves and soil: Proposal of two new orders, three new families, eight new genera and one hundred and seven new species. Stud Mycol 2020; 96:17–140 [View Article]
    [Google Scholar]
  9. Fell JW, Boekhout T, Fonseca A, Scorzetti G, Statzell-Tallman A. Biodiversity and systematics of basidiomycetous yeasts as determined by large-subunit rDNA D1/ D2 domain sequence analysis. Int J Syst Evol Microbiol 2000; 50:1351–1371 [View Article]
    [Google Scholar]
  10. Aime MC, Matheny PB, Henk DA, Frieders EM, Nilsson RH et al. An overview of the higher-level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences. Mycologia 2006; 98:895–905 [View Article]
    [Google Scholar]
  11. Bauer R, Begerow D, Sampaio JP, Weiβ M, Oberwinkler F. The simple-septate basidiomycetes: a synopsis. Mycol Prog 2006; 5:41–66 [View Article]
    [Google Scholar]
  12. Aime MC, Castlebury L, Abbasi M, Begerow D, Berndt R et al. Recommendations of generic names competing for use: Pucciniomycotina and Ustilaginomycotina, Basidiomycota. IMA Fungus 2018; 9:75–90 [View Article]
    [Google Scholar]
  13. Haelewaters D, Toome-Heller M, Albu S, Aime MC. Red yeasts from leaf surfaces and other habitats: three new species and a new combination of Symmetrospora (Pucciniomycotina, Cystobasidiomycetes. Fungal Syst Evol 2020; 5:187–196 [View Article]
    [Google Scholar]
  14. Wang QM, Yurkov AM, Göker M, Lumbsch HT, Leavitt SD et al. Phylogenetic classification of yeasts and related taxa within Pucciniomycotina. Stud Mycol 2015; 81:149–189 [View Article]
    [Google Scholar]
  15. Lorenzini M, Zapparoli G, Azzolini M, Carvalho C, Sampaio JP. Sporobolomyces agrorum sp. nov. and Sporobolomyces sucorum sp. nov., two novel basidiomycetous yeast species isolated from grape and apple must in Italy. Int J Syst Evol Microbiol 2019; 69:3385–3391 [View Article]
    [Google Scholar]
  16. Derx HG. Etude sur les Sporobolomycetes. Ann Mycol 1930; 28:1
    [Google Scholar]
  17. Tubaki K. Studies on the Sporobolomycetaceae in Japan. III. On Sporobolomyces and Bullera. Nagaoa 1953; 3:12–21
    [Google Scholar]
  18. Last FT. Seasonal incidence of Sporobolomyces on cereal leaves. Trans Brit Mycol Soc 1955; 38:221–239 [View Article]
    [Google Scholar]
  19. Hamamoto M, Nakase T. Ballistosporous yeasts found on the surface of plant materials collected in New Zealand. 1. Six new species in the genus Sporobolomyces. Anton Leeuw 1995; 67:151–171 [View Article]
    [Google Scholar]
  20. Nakase T. Expanding world of ballistosporous yeasts: distribution in the phyllosphere, systematics and phylogeny. J Gen Appl Microbiol 2000; 46:189–216 [View Article]
    [Google Scholar]
  21. Molnár O, Wuczkowski M, Prillinger H. Yeast biodiversity in the guts of several pests on maize; comparison of three methods: classical isolation, cloning and DGGE. Mycol Prog 2008; 7:111–123 [View Article]
    [Google Scholar]
  22. Debode J, Van Hemelrijck W, Creemers P, Maes M. Effect of fungicides on epiphytic yeasts associated with strawberry. MicrobiologyOpen 2013; 2:482–491 [View Article]
    [Google Scholar]
  23. Sláviková E, Grabiňska-Loniewska A. Sporobolomyces lactosus, a new species of ballistosporous yeast equipped with ubiquinone-10. Anton Leeuw 1992; 61:245–248 [View Article]
    [Google Scholar]
  24. Kurtzman CP, Fell JW, Boekhout T. The Yeasts, a Taxonomic Study, 5th ed. Amsterdam: Elsevier; 2011
    [Google Scholar]
  25. White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Innis M, Gelfand D, Sninsky J, White T. eds In PCR Protocols: a Guide to Methods and Applications New York: Academic Press; 1990 pp 315–322 [View Article]
    [Google Scholar]
  26. Gardes M, Bruns TD. ITS primers with enhanced specificity for Basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 1993; 2:113–118 [View Article]
    [Google Scholar]
  27. Vilgalys R, Hester M. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 1990; 172:4238–4246 [View Article]
    [Google Scholar]
  28. Hopple JS. Phylogenetic Investigations in the Genus Coprinus Based on Morphological and Molecular Characters (Phd Dissertation) Durham, North Carolina: Duke University; 1994
    [Google Scholar]
  29. Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article]
    [Google Scholar]
  30. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article]
    [Google Scholar]
  31. Miller M, Pfeiffer WT, Schwartz T. Creating the CIPRES Science Gateway for inferences of large phylogenetic trees. Proc Gateway Comp Environ Workshop 2010; 14:1–8 [View Article]
    [Google Scholar]
  32. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article]
    [Google Scholar]
  33. Kalyaanamoorthy K, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article]
    [Google Scholar]
  34. Chernomor O, Von Haeseler A, Minh BQ. Terrace aware data structure for phylogenomic inference from supermatrices. Syst Biol 2016; 65:997–1008 [View Article]
    [Google Scholar]
  35. Hoang DT, Chernomor O, Von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 2017; 35:518–522 [View Article]
    [Google Scholar]
  36. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012; 29:1969–1973 [View Article]
    [Google Scholar]
  37. Gernhard T. Using birth-death model on trees. J Theor Biol 2008; 253:769–778 [View Article]
    [Google Scholar]
  38. Yule GU. II.—A mathematical theory of evolution, based on the conclusions of Dr. JC Willis, F.R.S. Phil Trans R Soc Lond B Biol Sci 1925; 213:21–87 [View Article]
    [Google Scholar]
  39. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9:772 [View Article]
    [Google Scholar]
  40. Rambaut A, Suchard MA, Xie D, Drummond AJ. Tracer v1.6 (internet; 2014 http://tree.bio.ed.ac.uk/software/tracer/
  41. Kumar S, Stecher G, Tamura K. mega7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article]
    [Google Scholar]
  42. Minnis AM, Lindner DL. Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol 2013; 117:638–649 [View Article]
    [Google Scholar]
  43. Baral HO. Inoperculate discomycetes. Jaklitsch W, Baral H, Lücking R, Lumbsch H, Frey W. eds In Syllabus of Plant Families: A. Engler’s Syllabus der Pflanzenfamilien Part 1/2 Stuttgart: Borntraeger; 2016 pp 157–205
    [Google Scholar]
  44. Johnston PR, Quijada L, Smith CA, Baral HO, Hosoya T et al. A multigene phylogeny toward a new phylogenetic classification of leotiomycetes. IMA Fungus 2019; 10:1 [View Article]
    [Google Scholar]
  45. LoBuglio KF, Pfister DH. Placement of Medeolaria farlowii in the Leotiomycetes, and comments on sampling within the class. Mycol Prog 2010; 9:361–368 [View Article]
    [Google Scholar]
  46. Wang Z, Binder M, Schoch CL, Johnston PR, Spatafora JW et al. Evolution of helotialean fungi (Leotiomycetes, Pezizomycotina): A nuclear rDNA phylogeny. Mol Phylogenet Evol 2006; 41:295–312 [View Article]
    [Google Scholar]
  47. Wang Z, Johnston PR, Yang ZL, Townsend JP. Evolution of reproductive morphology in leaf endophytes. Plos One 2009; 4:e4246 [View Article]
    [Google Scholar]
  48. Tedersoo L, Pärtel K, Jairus T, Gates G, Põldmaa K et al. Ascomycetes associated with ectomycorrhizas: molecular diversity and ecology with particular reference to the Helotiales. Environ Microbiol 2009; 11:3166–3178 [View Article]
    [Google Scholar]
  49. U’Ren JM, Lutzoni F, Miadlkowska J, Arnold AE. Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb Ecol 2010; 60:340–353 [View Article]
    [Google Scholar]
  50. Ruibal C, Gueidan C, Selbmann L, Gorbushina AA, Crous PW et al. Phylogeny of rock-inhabiting fungi related to Dothideomycetes. Stud Mycol 2009; 64:123–133 [View Article]
    [Google Scholar]
  51. Ertz D, Lawrey JD, Common RS, Diederich P. Molecular data resolve a new order of Arthoniomycetes sister to the primarily lichenized Arthoniales and composed of black yeasts, lichenicolous and rock-inhabiting species. Fungal Divers 2014; 66:113–137 [View Article]
    [Google Scholar]
  52. Zupančič J, Novak Babič M, Zalar P, Gunde-Cimerman N. The black yeast Exophiala dermatitidis and other selected opportunistic human pathogens spread from dishwashers to kitchens. Plos One 2016; 11:e0148166 [View Article]
    [Google Scholar]
  53. Réblová M, Hubka V, Thureborn O, Lundberg J, Sallstedt T et al. From the tunnels into the treetops: New lineages of black yeasts from biofilm in the Stockholm metro system and their relatives among ant-associated fungi in the Chaetothyriales. Plos One 2016; 11:e0163396 [View Article]
    [Google Scholar]
  54. Teixeira MM, Moreno LF, Stielow BJ, Muszewska A, Hainaut M et al. Exploring the genomic diversity of black yeasts and relatives (Chaetothyriales, Ascomycota. Stud Mycol 2017; 86:1–28 [View Article]
    [Google Scholar]
  55. Wijayawardene NN, Hyde KD, Rajeshkumar KC, Hawksworth DL, Madrid H et al. Notes for genera: Ascomycota. Fungal Divers 2017; 86:1–594 [View Article]
    [Google Scholar]
  56. Baral HO, Weber E, Marson G, Quijada L. A new connection between wood saprobism and beetle endosymbiosis: the rarely reported saprobic discomycete Tromeropsis is congeneric with the symbiotic yeast Symbiotaphrina (Symbiotaphrinales, Xylonomycetes) and two asexual morphs misplaced in Hyphozyma. Mycol Prog 2018; 17:215–254 [View Article]
    [Google Scholar]
  57. Fryar SC, Haelewaters D, Catcheside DE. Annabella australiensis gen. & sp. nov. (Helotiales, Cordieritidaceae) from South Australian mangroves. Mycol Prog 2019; 18:973–981 [View Article]
    [Google Scholar]
  58. Jones EBG, Suetrong S, Sakayaroj J, Bahkali AH, Abdel-Wahab MA et al. Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Divers 2015; 73:1–72 [View Article]
    [Google Scholar]
  59. Landvik S, Kristiansen R, Schumacher T. Phylogenetic and structural studies in the Thelebolaceae (Ascomycota. Mycoscience 1998; 39:49–56 [View Article]
    [Google Scholar]
  60. de Hoog GS, Gottlich E, Platas G, Genilloud O, Leotta G et al. Evolution, taxonomy and ecology of the genus Thelebolus in Antarctica. Stud Mycol 2005; 51:33–76
    [Google Scholar]
  61. Robinson CH. Cold adaptation in Arctic and Antarctic fungi. New Phytol 2001; 151:341–353 [View Article]
    [Google Scholar]
  62. de Menezes GCA, Godinho VM, Porto BA, Gonçalves VN, Rosa LH et al. Antarctomyces pellizariae sp. nov., a new, endemic, blue, snow resident psychrophilic ascomycete fungus from Antarctica. Extremophiles 2017; 21:259–269 [View Article]
    [Google Scholar]
  63. Batista TM, Hilario HO, de Brito GAM, Moreira RG, Furtado C et al. Whole-genome sequencing of the endemic Antarctic fungus Antarctomyces pellizariae reveals an ice-binding protein, a scarce set of secondary metabolites gene clusters and provides insights on Thelebolales phylogeny. Genomics 2020; 112:2915–2921 [View Article]
    [Google Scholar]
  64. Peterson RA, Bradner JR, Roberts TH, Nevalainen KMH. Fungi from koala (Phascolarctos cinereus) faeces exhibit a broad range of enzyme activities against recalcitrant substrates. Lett Appl Microbiol 2009; 48:218–225 [View Article]
    [Google Scholar]
  65. Zalar P, Gostinčar C, de Hoog GS, Uršič V, Sudhadham M et al. Redefinition of Aureobasidium pullulans and its varieties. Stud Mycol 2008; 61:21–38 [View Article]
    [Google Scholar]
  66. Bills GF, Menéndez VG, Platas G. Kabatiella bupleuri sp. nov. (Dothideales), a pleomorphic epiphyte and endophyte of the Mediterranean plant Bupleurum gibraltarium (Apiaceae. Mycologia 2012; 104:962–973 [View Article]
    [Google Scholar]
  67. Boekhout T, Bai FY, Daniel HM, Groenewald M, Robert V et al. The yeasts trust database [Internet]; 2020 https://theyeasts.org/
  68. Pechak DG, Crang RE. An analysis of Aureobasidium pullulans developmental stages by means of scanning electron microscopy. Mycologia 1977; 69:783–792 [View Article]
    [Google Scholar]
  69. Stchigel AM, Cano J, Mac Cormack W, Guarro J. Antarctomyces psychrotrophicus gen. et sp. nov., a new ascomycete from Antarctica. Mycol Res 2001; 105:377–382 [View Article]
    [Google Scholar]
  70. Vu D, Groenewald M, Vries M, Gehrmann T, Stielow B et al. Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Stud Mycol 2019; 92:135–154 [View Article]
    [Google Scholar]
  71. Suh SO, Blackwell M. Molecular phylogeny of the cleistothecial fungi placed in Cephalothecaceae and Pseudeurotiaceae. Mycologia 1999; 91:836–848 [View Article]
    [Google Scholar]
  72. Malloch D, Sigler L, Hambleton S, Vanderwolf KJ, Gibas CFC et al. Fungi associated with hibernating bats in New Brunswick caves: the genus Leuconeurospora. Botany 2016; 94:1171–1181 [View Article]
    [Google Scholar]
  73. Schoch CL, Sung GH, López-Giráldez F, Townsend JP, Miadlikowska J et al. The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 2009; 58:224–239 [View Article] [PubMed]
    [Google Scholar]
  74. Sugiyama M, Ohara A, Mikawa T. Molecular phylogeny of onygenalean fungi based on small subunit ribosomal DNA (SSU rDNA) sequences. Mycoscience 1999; 40:251–258 [View Article]
    [Google Scholar]
  75. Schoch CL, Robbertse B, Robert V, Vu D, Cardinali G et al. Finding needles in haystacks: linking scientific names, reference specimens and molecular data for Fungi. Database 2014; 2014: [View Article] [PubMed]
    [Google Scholar]
  76. Rice AV, Currah RS. Two new species of Pseudogymnoascus with geomyces anamorphs and their phylogenetic relationship with Gymnostellatospora. Mycologia 2006; 98:307–318 [View Article] [PubMed]
    [Google Scholar]
  77. Pärtel K, Baral HO, Tamm H, Põldmaa K. Evidence for the polyphyly of Encoelia and Encoelioideae with reconsideration of respective families in Leotiomycetes. Fungal Divers 2017; 82:183–219 [View Article]
    [Google Scholar]
  78. Untereiner WA, Yue Q, Chen L, Li Y, Bills GF et al.. Phialophora section Catenulatae disassembled: New genera, species, and combinations and a new family encompassing taxa with cleistothecial ascomata and phialidic asexual states. Mycologia 2019; 111:998–1027 [View Article] [PubMed]
    [Google Scholar]
  79. Sogonov MV, Schroers HJ, Gams W, Dijksterhuis J, Summerbell RC. The hyphomycete Teberdinia hygrophila gen. nov., sp. nov. and related anamorphs of Pseudeurotium species. Mycologia 2005; 97:695–709 [View Article]
    [Google Scholar]
  80. Lorch JM, Lindner DL, Gargas A, Muller LK, Minnis AM et al. A culture-based survey of fungi in soil from bat hibernacula in the Eastern United States and its implications for detection of Geomyces destructans, the causal agent of bat white-nose syndrome. Mycologia 2013; 105:237–252 [View Article] [PubMed]
    [Google Scholar]
  81. Spatafora JW, Sung GH, Johnson D, Hesse C, O’Rourke B et al. A five-gene phylogeny of Pezizomycotina. Mycologia 2006; 98:1018–1028 [View Article]
    [Google Scholar]
  82. Hyde KD, Norphanphoun C, Abreu VP, Bazzicalupo A, Chethana KT et al. Fungal diversity notes 603–708: taxonomic and phylogenetic notes on genera and species. Fungal Divers 2017; 87:1–235 [View Article]
    [Google Scholar]
  83. Bovio E, Garzoli L, Poli A, Prigione V, Firsova D et al. The culturable mycobiota associated with three atlantic sponges, including two new species: Thelebolus balaustiformis and T. Spongiae. Fungal Syst Evol 2018; 1:141–167 [View Article] [PubMed]
    [Google Scholar]
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