Advertisement

Fungal Diversity

, Volume 66, Issue 1, pp 113–137 | Cite as

Molecular data resolve a new order of Arthoniomycetes sister to the primarily lichenized Arthoniales and composed of black yeasts, lichenicolous and rock-inhabiting species

  • Damien Ertz
  • James D. Lawrey
  • Ralph S. Common
  • Paul Diederich
Article

Abstract

Lichenicolous fungi belonging to the anamorph-typified genus Phaeosporobolus and to the teleomorph-typified genus Lichenostigma were isolated in pure culture or sequenced directly, with nuLSU and mtSSU sequences obtained. Phylogenetic analyses place the species of Phaeosporobolus in a strongly supported clade with the generic type of Lichenostigma (L. maureri), the genus Phaeococcomyces and several melanized rock-inhabiting isolates. This strongly supported nonlichenized lineage is sister to the primarily lichenized Arthoniales in the Arthoniomycetes and is here described as the Lichenostigmatales. The new order is characterized by cells multiplying by budding, either representing black yeasts, or species in which conidiomata and ascomata are entirely made of an organised agglomeration of spherical yeast-like cells. This way of life is not only very different from all other Arthoniomycetes that exist only in the mycelial stage, but ascomata and conidiomata representing a dense and organised agglomeration of yeast cells might be unique amongst fungi. A further difference with the Arthoniales is the absence of paraphysoids. Phylogenetic results suggest that Phaeosporobolus usneae is the asexual stage of Lichenostigma maureri. Most species of Phaeosporobolus are transferred to the genus Lichenostigma except P. trypethelii, for which the new genus Etayoa is described. The genus Diederimyces is reduced into synonymy with Lichenostigma. Several other members of Lichenostigma are placed in the Dothideomycetes and are intermixed with Lichenothelia species.

Keywords

Anamorphic fungi Arthoniomycetes Dothideomycetes Lichenostigmatales Phaeococcomycetaceae Yeasts 

Notes

Acknowledgments

We would like to thank the curators of herbaria cited in Materials and Methods for the loan of specimens. Ann Bogaerts, Myriam Dehaan and Wim Baert are thanked for technical assistance. Gisèle Van Cappellen, Trevor Goward, Nibedita Mukherjee and Paul Neuberg kindly provided fresh specimens used in this study. Finally, the first author acknowledges financial support from the Fonds National de la Recherche Scientifique (FNRS) from Belgium (F.R.F.C. # 2.4567.08).

References

  1. Alstrup V, Hawksworth DL (1990) The lichenicolous fungi of Greenland. Medd Grønland Biosci 31:1–90Google Scholar
  2. Baral HO (1987) Lugol’s solution/IKI versus Melzer’s reagent: hemiamyloidity, a universal feature of the ascus wall. Mycotaxon 29:399–450Google Scholar
  3. Berger F, Brackel W (2011) Eine weitere Art von Phaeosporobolus auf Lecanora chlarotera. Herzogia 24:351–356CrossRefGoogle Scholar
  4. Brackel W (2011) Lichenicolous fungi and lichens from Puglia and Basilicata (southern Italy). Herzogia 24:65–101CrossRefGoogle Scholar
  5. Calatayud V, Barreno E (2003) A new Lichenostigma on vagrant Aspicilia species. Lichenologist 35(4):279–285CrossRefGoogle Scholar
  6. Calatayud V, Hafellner J, Navarro-Rosinés P (2004) Lichenostigma. In: Nash TH III, Ryan BD, Diederich P, Gries C, Bungartz F (eds) Lichen flora of the Greater Sonoran Desert Region, vol 2, Lichens Unlimited. Arizona State University, Tempe, pp 664–669Google Scholar
  7. Calatayud V, Navarro-Rosinés P, Hafellner J (2002) A synopsis of Lichenostigma subgen. Lichenogramma (Arthoniales), with a key to the species. Mycol Res 106:1230–1242CrossRefGoogle Scholar
  8. Common RS (1991) The distribution and taxonomic significance of lichenan and isolichenan in the Parmeliaceae. I. Introduction and methods. II. The genus Alectoria and associated taxa. Mycotaxon 41:67–112Google Scholar
  9. Crous PW, Groenewald JZ, Shivas RG (2012) Phaeococcomyces eucalypti. Fungal Planet 113. Persoonia 29:158–159CrossRefGoogle Scholar
  10. Cunningham CW, Zhu H, Hillis DM (1998) Best-fit maximum likelihood models for phylogenetic inference: empirical tests with known phylogenies. Evolution 52:978–987CrossRefGoogle Scholar
  11. de Hoog GS (1979) Nomenclature notes on some black yeast-like hyphomycetes. Taxon 28:347–348CrossRefGoogle Scholar
  12. Diederich P (2004) Phaeosporobolus. In: Nash TH III, Ryan BD, Diederich P, Gries C, Bungartz F (eds) Lichen flora of the Greater Sonoran Desert Region. Lichens Unlimited, vol 2. Arizona State University, Tempe, pp 681–682Google Scholar
  13. Diederich P, Ertz D, Eichler M, Cezanne R, van den Boom P, Fischer E, Killmann D, Van den Broeck D, Sérusiaux E (2012a) New or interesting lichens and lichenicolous fungi from Belgium, Luxembourg and northern France. XIV. Bull Soc Nat Lux 113:95–115Google Scholar
  14. Diederich P, Lawrey JD, Sikaroodi M, van den Boom P, Ertz D (2012b) Briancoppinsia, a new coelomycetous genus of Arthoniaceae (Arthoniales) for the lichenicolous Phoma cytospora, with a key to this and similar taxa. Fungal Divers 52:1–12CrossRefGoogle Scholar
  15. Egea JM, Torrente P, Manrique E (1993) The Lecanactis grumulosa group (Opegraphaceae) in the Mediterranean region. Plant Syst Evol 187:103–114CrossRefGoogle Scholar
  16. Eriksson O, Hawksworth DL (1986) Notes on ascomycete systematics. Nos 1–224. Syst Ascomycetum 5:113–174Google Scholar
  17. Ertz D, Bungartz F, Diederich P, Tibell L (2011) Molecular and morphological data place Blarneya in Tylophoron (Arthoniaceae). Lichenologist 43:345–356CrossRefGoogle Scholar
  18. Ertz D, Tehler A (2011) The phylogeny of Arthoniales (Pezizomycotina) inferred from nucLSU and RPB2 sequences. Fungal Divers 49:47–71CrossRefGoogle Scholar
  19. Etayo J (1995) Two new species of lichenicolous fungi from the Pyrenees. Nova Hedwig 61:189–197Google Scholar
  20. Etayo J, Sancho LG (2008) Hongos liquenícolas del Sur de Sudamérica, especialmente de Isla Navarino (Chile). Bibl Lichen 98:1–302Google Scholar
  21. Fernández-Brime S, Llimona X, Navarro-Rosinés P (2010) Lichenostigma rupicolae (Lichenotheliaceae), a new lichenicolous species growing on Pertusaria rupicola. Lichenologist 42:241–247CrossRefGoogle Scholar
  22. Flakus A, Kukwa M (2012) New species of lichenicolous fungi from Bolivia. Lichenologist 44:469–477CrossRefGoogle Scholar
  23. Gueidan C, Ruibal CV, de Hoog GS, Gorbushina AA, Untereiner WA, Lutzoni F (2008) A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Stud Mycol 61:111–119PubMedCrossRefPubMedCentralGoogle Scholar
  24. Hafellner J (1982) Studien über lichenicole Pilze und Flechten II Lichenostigma maureri gen. et spec. nov., ein in den Ostalpen häufiger lichenicoler Pilz (Ascomycetes, Arthoniales). Herzogia 6:299–308Google Scholar
  25. Hafellner J, Calatayud V (1999) Lichenostigma cosmopolites, a common lichenicolous fungus on Xanthoparmelia species. Mycotaxon 72:107–114Google Scholar
  26. Harris RC, Lendemer JC (2009) The Fellhanera silicis group in eastern North America. Opuscula Philolichenum 6:157–174Google Scholar
  27. Hawksworth DL, Hafellner J (1986) Phaeosporobolus usneae, a new and widespread lichenicolous deuteromycete. Nova Hedwig 43:525–530Google Scholar
  28. Henssen A (1987) Lichenothelia, a genus of microfungi on rocks. In: Peveling E (ed) Progress and problems in lichenology in the eighties. Bibl Lichen 25. J Cramer, Berlin-Stuttgart, pp 257–293Google Scholar
  29. Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogeny. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  30. Ihlen PG (2004) A new species of Lichenostigma (Lichenotheliaceae, Arthoniales) from Scandinavia. Lichenologist 36:183–189CrossRefGoogle Scholar
  31. Kalb K, Hafellner J, Staiger B (1995) Haematomma-Studien, II. Lichenicole Pilze auf Arten der Flechtengattung Haematomma. Bibl Lichen 59:1–222Google Scholar
  32. Knudsen K, Kocourkova J (2010) A new Lichenostigma species (genus incertae sedis) from southern California. Bryologist 113:229–234CrossRefGoogle Scholar
  33. Kocourková J (2000) Lichenicolous fungi of the Czech Republic (the first commented checklist). Acta Mus Natl Pragae Ser B Hist Nat 55:59–169Google Scholar
  34. Lawrey JD, Diederich P (2003) Lichenicolous fungi: interactions, evolution, and biodiversity. Bryologist 106:80–120CrossRefGoogle Scholar
  35. Lawrey JD, Binder M, Diederich P, Molina MC, Sikaroodi M, Ertz D (2007) Phylogenetic diversity of lichen-associated homobasidiomycetes. Mol Phylogenet Evol 44:778–789PubMedCrossRefGoogle Scholar
  36. Lawrey JD, Diederich P, Nelsen MP, Sikaroodi M, Gillevet PM, Brand AM, van den Boom P (2011) The obligately lichenicolous genus Lichenoconium represents a novel lineage in the Dothideomycetes. Fungal Biology 115:176–187PubMedCrossRefGoogle Scholar
  37. Lawrey JD, Diederich P, Nelsen MP, Freebury C, Van den Broeck D, Sikaroodi M, Ertz D (2012) Phylogenetic placement of lichenicolous Phoma species in the Phaeosphaeriaceae (Pleosporales, Dothideomycetes). Fungal Divers 55:195–213CrossRefGoogle Scholar
  38. Liò P, Goldman N (1998) Models of molecular evolution and phylogeny. Genome Res 8:1233–1244PubMedGoogle Scholar
  39. Lumbsch HT, Huhndorf AM (2010) Myconet Volume 14. Part One. Outline of Ascomycota–2009. Part Two. Notes on ascomycete systematics. Nos. 4751–5113. Fieldiana 1:1–64Google Scholar
  40. Maddison D, Maddison W (2002) MacClade version 4.03PPC: analysis of phylogeny and character evolution. Sinauer, SunderlandGoogle Scholar
  41. Mason-Gamer RJ, Kellogg EA (1996) Testing for phylogenetic conflict among molecular datasets in the tribe Triticeae (Gramineae). Systematic Biol 45:524–545CrossRefGoogle Scholar
  42. McGinnis MR, Schell WA, Carson J (1985) Phaeoannellomyces and the Phaeococcomycetaceae, new dematiaceous blastomycete taxa. Sabouraudia 23:179–188PubMedCrossRefGoogle Scholar
  43. Miadlikowska J, McCune B, Lutzoni F (2002) Pseudocyphellaria perpetua, a new lichen from Western North America. Bryologist 105:1–10CrossRefGoogle Scholar
  44. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA, pp 1–8Google Scholar
  45. Muggia L, Gueidan C, Knudsen K, Perlmutter G, Grube M (2012) The lichen connections of Black fungi. Mycopathologia. doi: 10.1007/s11046-012-9598-8 PubMedGoogle Scholar
  46. Navarro-Rosinés P, Hafellner J (1996) Lichenostigma elongata spec. nov. (Dothideales), a lichenicolous ascomycete on Lobothallia and Aspicilia species. Mycotaxon 57:211–225Google Scholar
  47. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  48. Rambaut A, Drummond AJ (2007) Tracer v1.5., available from: http://beast.bio.ed.ac.uk/Tracer
  49. Rambaut A (2012) FigTree v1.3.1, available from: http://tree.bio.ed.ac.uk/software/figtree/
  50. Rich MA, Stern AM (1958) Studies of Cryptococcus nigricans n. sp. I. Identification and taxonomic classification. Mycopathol Mycol Appl 9(3):189–193PubMedCrossRefGoogle Scholar
  51. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  52. Ruibal C, Platas G, Bills GF (2008) High diversity and morphological convergence among melanised fungi from rock formations in the Central Mountain System of Spain. Persoonia 21:93–110PubMedCrossRefPubMedCentralGoogle Scholar
  53. Ruibal C, Gueidan C, Selbmann L, Gorbushina AA, Crous PW, Groenewald JZ, Muggia L, Grube M, Isola D, Schoch CL, Staley JT, Lutzoni F, de Hoog GS (2009) Phylogeny of rock-inhabiting fungi related to Dothideomycetes. Stud Mycol 64:123–133PubMedCrossRefPubMedCentralGoogle Scholar
  54. Ruibal C, Millanes AM, Hawksworth DL (2011) Molecular phylogenetic studies on the lichenicolous Xanthoriicola physciae reveal Antarctic rock-inhabiting fungi and Piedraia species among closest relatives in the Teratosphaeriaceae. IMA Fungus 2:97–103PubMedCrossRefPubMedCentralGoogle Scholar
  55. Stamatakis A, Ludwig T, Meier H (2005) RAxML-III: a fast program for maximum likelihood-based inference of large 437 phylogenetic trees. Bioinformatics 21:456–463PubMedCrossRefGoogle Scholar
  56. Stamatakis A (2006) RAxML-VI-HPC: Maximum Likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690Google Scholar
  57. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  58. Thor G (1985) A new species of Lichenostigma, a lichenicolous ascomycete. Lichenologist 17:269–272CrossRefGoogle Scholar
  59. Tsuneda A, Hambleton S, Currah RS (2011) The anamorph genus Knufia and its phylogenetically allied species in Coniosporium, Sarcinomyces, and Phaeococcomyces. Botany 89:523–536CrossRefGoogle Scholar
  60. Valadbeigi T, Brackel W (2011) Two new species of Lichenostigma (Lichenotheliaceae, lichenicolous fungi) from Iran. Willdenowia 41:191–195Google Scholar
  61. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246PubMedPubMedCentralGoogle Scholar
  62. von Arx JA (1963) Die Gattungen der Myriangiales. Persoonia 2:421–475Google Scholar
  63. Yang Z, Goldman N, Friday A (1994) Comparison of models for nucleotide substitution used in maximum-likelihood phylogenetic estimation. Mol Biol Evol 11:316–324PubMedGoogle Scholar
  64. Yoshimura I, Yamamoto Y, Nakano T, Finnie J (2002) Isolation and culture of lichen photobionts and mycobionts. In: Kranner I, Beckett RP, Varma A (eds) Protocols in lichenology – culturing, biochemistry, physiology and use in biomonitoring. Springer, Berlin, pp 3–33Google Scholar
  65. Zoller S, Scheidegger C, Sperisen C (1999) PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31:511–516CrossRefGoogle Scholar
  66. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph. D. dissertation, The University of Texas at Austin.Google Scholar

Copyright information

© Mushroom Research Foundation 2013

Authors and Affiliations

  • Damien Ertz
    • 1
  • James D. Lawrey
    • 2
  • Ralph S. Common
    • 3
  • Paul Diederich
    • 4
  1. 1.Jardin botanique national de BelgiqueDomaine de BouchoutBelgium
  2. 2.Department of Environmental Science and PolicyGeorge Mason UniversityFairfaxUSA
  3. 3.LansingUSA
  4. 4.Musée national d’histoire naturelleLuxembourgLuxembourg

Personalised recommendations