, Volume 175, Issue 5–6, pp 523–535 | Cite as

The Lichen Connections of Black Fungi

  • Lucia Muggia
  • Cecile Gueidan
  • Kerry Knudsen
  • Gary Perlmutter
  • Martin Grube


Many black meristematic fungi persist on rock surfaces—hostile and exposed habitats where high doses of radiation and periods of desiccation alternate with rain and temperature extremes. To cope with these extremes, rock-inhabiting black fungi show phenotypic plasticity and produce melanin as cell wall pigments. The rather slow growth rate seems to be an additional prerequisite to oligotrophic conditions. At least some of these fungi can undergo facultative, lichen-like associations with photoautotrophs. Certain genera presenting different lifestyles are phylogenetic related among the superclass Dothideomyceta. In this paper, we focus on the genus Lichenothelia, which includes border-line lichens, that is, associations of melanised fungi with algae without forming proper lichen thalli. We provide a first phylogenetic hypothesis to show that Lichenothelia belongs to the superclass Dothideomyceta. Further, culture experiments revealed the presence of co-occurring fungi in Lichenothelia thalli. These fungi are related to plant pathogenic fungi (Mycosphaerellaceae) and to other rock-inhabiting lineages (Teratosphaeriaceae). The Lichenothelia thallus-forming fungi represent therefore consortia of different black fungal strains. Our results suggest a common link between rock-inhabiting meristematic and lichen-forming lifestyles of ascomycetous fungi.


Algae Borderline lichens Dothideomyceta Lichenicolous Lichenothelia Symbiosis 



LM and MG are grateful to the Austrian Science Foundation for financial support (FWF P24114). We thank Cene Gostinčar and Josef Hafellner for constructive discussions and Jana Kocourková for field co-work.


  1. 1.
    Ahmadjian V. The lichen symbiosis. Massachusetts: Blaisdell Publishing Company; 1967.Google Scholar
  2. 2.
    Athienza V, Hawksworth DL. Lichenothelia renobalesiana sp. nov. (Lichenotheliaceae), for a lichenicolous ascomycete confused with Polycoccum opulentum (Dacampiaceae). The Lichenologist. 2008;40:87–96.Google Scholar
  3. 3.
    Brunauer G, Blaha J, Hager A, Turk R, Stocker-Worgotter E, Grube M. An isolated lichenicolous fungus forms lichenoid structures when co-cultured with various coccoid algae. Symbiosis. 2007;44:127–36.Google Scholar
  4. 4.
    Bubrick P, Galun M. Spore to spore resynthesis of Xanthoria parietina. The Lichenologist. 1986;18:47–9.CrossRefGoogle Scholar
  5. 5.
    Catalayud V, Naverro-Rosines P, Hafellner J. A synopsis of Lichenostigma subgen. Lichenogramma (Arthoniales), with a key to the species. Myc Res. 2002;106:1230–42.CrossRefGoogle Scholar
  6. 6.
    Cubero OF, Crespo A, Fatehi J, Bridge PD. DNA extraction and PCR amplification method suitable for fresh, herbarium stored and lichenized fungi. Plant Syst Evol. 1999;217:243–9.CrossRefGoogle Scholar
  7. 7.
    Fernadez-Brime S, Llimona X, Navarro-Rosines P. Lichenostigma rupicolae (Lichenotheliaceae), a new lichenocolous species growing on Pertusaria rupicola. The Lichenologist. 2010;42:241–7.CrossRefGoogle Scholar
  8. 8.
    Friedmann EI, Kappen L, Meyer MA, Nienow JA. Long-term productivity in the cryptoendolithic microbial community of the Ross Desert, Antarctica. Microb Ecol. 1993;25:51–69.PubMedCrossRefGoogle Scholar
  9. 9.
    Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes. Application for the identification of mycorrhizae and rust. Mol Ecol. 1993;2:113–8.PubMedCrossRefGoogle Scholar
  10. 10.
    Gargas A, Taylor JW. Polymerase chain reaction (PCR) primers for amplifying, sequencing nuclear 18S rDNA from lichenized fungi. Mycologia. 1992;84:589–92.CrossRefGoogle Scholar
  11. 11.
    Gorbushina AA, Broughton WJ. Microbiology of the atmosphere-rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Ann Rev Microbiol. 2009;63:431–50.CrossRefGoogle Scholar
  12. 12.
    Gorbushina AA, Beck A, Schulte A. Microcolonial rock inhabiting fungi and lichen photobionts: evidence for mutualistic interactions. Myc Res. 2005;109:1288–96.CrossRefGoogle Scholar
  13. 13.
    Gorbushina AA, Whitehead K, Dornieden T, Niesse A, Schulte A, Hedges JI. Black fungal colonies as units of survival: hyphal mycosporines synthesized by rock dwelling microcolonial fungi. Can J Bot. 2003;81:131–8.CrossRefGoogle Scholar
  14. 14.
    Gueidan C, Ruibal C, De Hoog GS, Schneider H. Rock-inhabiting fungi originated during periods of dry climate in the late Devonian and middle Triassic. Fun Biol. 2011;115:987–96.CrossRefGoogle Scholar
  15. 15.
    Hafellener J. Studien über lichenicole Pilze und Flechten II. Lichenostigma maureri gen et spec. nov., ein in den Ostalpen häufiger lichenicoler Pilz (Ascomycota, Arthoniales). Herzogia. 1982;6:299–308.Google Scholar
  16. 16.
    Halici MG, Kocakaya M, Aksoy A. Lichenostigma anatolicum sp. nov. (Ascomycota, Lichenotheliaceae) on a brown Acarospora from central Turkey. Mycotaxon. 2009;108:67–72.CrossRefGoogle Scholar
  17. 17.
    Hall TA. BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuc Ac Symp Ser. 1999;41:95–8.Google Scholar
  18. 18.
    Harutyunyan S, Muggia L, Grube M. Black fungi in lichens from seasonally arid habitats. Stud Mycol. 2008;61:83–90.PubMedCrossRefGoogle Scholar
  19. 19.
    Hawksworth DL. Lichenothelia, a new genus for the Microthelia aterrima group. The Lichenologist. 1981;13:141–53.CrossRefGoogle Scholar
  20. 20.
    Huelsenbeck JP, Ronquist F. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.CrossRefGoogle Scholar
  21. 21.
    Ihlen PG. A new species of Lichenostigma (Lichenotheliaceae, Arthoniales) from Scandinavia. The Lichenologist. 2004;36:183–9.CrossRefGoogle Scholar
  22. 22.
    Kauff F, Lutzoni F. Phylogeny of the Gyalectales and Ostropales (Ascomycota, Fungi): among and within order relationships based on nuclear ribosomal RNA small and large subunits. Mol Phyl Evol. 2002;25:138–56.CrossRefGoogle Scholar
  23. 23.
    Knudsen K, Kocourkova J. A new Lichenostigma species (genus incertae sedis) from southern California. The Bryologist. 2010;113:229–34.CrossRefGoogle Scholar
  24. 24.
    Kohlmeyer J, Hawksworth DL, Volkmann-Kohlmeyer B. Observations on two marine and maritime “borderline” lichens: Mastodia tessellata and Collemopsidium pelvetiae. Myc Progr. 2004;3:51–6.CrossRefGoogle Scholar
  25. 25.
    Lilly VG, Barnett HL. Physiology of fungi. New York: McGrow-Hill; 1951.Google Scholar
  26. 26.
    Meson-Gamer R, Kellogg E. Testing for phylogenetic conflict among molecular dataset in the tribe Triticeae (Gramiae). Syst Biol. 1996;45:524–45.CrossRefGoogle Scholar
  27. 27.
    Miadlikowska J, Kauff F, Hofstetter V, Fraker E, Grube M, Hafellner J, Reeb V, Hodkinson BP, Kukwa M, Lücking R, et al. New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia. 2006;98:1088–103.PubMedCrossRefGoogle Scholar
  28. 28.
    Muggia L, Hafellner J, Wirtz N, Hawksworth DL, Grube M. The sterile microfilamentous lichenized fungi Cystocoleus ebeneus and Racodium rupestre are relatives of plant pathogens and clinically important dothidealean fungi. Mycol Res. 2008;112:50–6.PubMedCrossRefGoogle Scholar
  29. 29.
    Muggia L, Gueidan C, Grube M. Phylogenetic placement of some morphologically unusual members of Verrucariales. Mycologia. 2010;102:835–46.PubMedCrossRefGoogle Scholar
  30. 30.
    Muggia L, Nelson P, Wheeler T, Yakovchenko LS, Tønsberg T, Spribille T. Convergent evolution of a symbiotic duet: the case of the lichen genus Polychidium (Peltigerales, Ascomycota). Am J Bot. 2011;98:1647–56.PubMedCrossRefGoogle Scholar
  31. 31.
    Nelsen MP, Lücking R, Mbatchou JS, Andrew CJ, Spielmann AA, Lumbsch HT. New insights into relationships of lichen-forming Dothideomycetes. Fun Div. 2011;51:155–62.CrossRefGoogle Scholar
  32. 32.
    Nelsen MP, Lucking R, Grube M, Mbatchou JS, Muggia L, Plata ER, Lumbsch HT. Unravelling the phylogenetic relationships of lichenised fungi in Dothideomyceta. Stud Mycol. 2009;64:135–44.PubMedCrossRefGoogle Scholar
  33. 33.
    Onofri S, Selbmann L, de Hoog GS, Grube M, Barreca D, Ruisi S, Zucconi L. Evolution and adaptation of fungi at boundaries of life. Adv Space Res. 2007;40:657–1664.CrossRefGoogle Scholar
  34. 34.
    Page RDM. TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 1996;12:357–8.PubMedGoogle Scholar
  35. 35.
    Perez-Ortega S, Catalayud V. Lichenostigma epirupestre, a new lichenicolous species on Pertusaria from Spain. Mycotaxon. 2009;107:189–95.CrossRefGoogle Scholar
  36. 36.
    Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinf Appl Notes. 1998;14:817–8.CrossRefGoogle Scholar
  37. 37.
    Reeb V, Lutzoni F, Roux C. Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Mol Phyl Evol. 2004;32:1036–60.CrossRefGoogle Scholar
  38. 38.
    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. Phylogeny of rock-inhabiting fungi related to Dothideomycetes. Stud Mycol. 2009;64:123–33.PubMedCrossRefGoogle Scholar
  39. 39.
    Schoch CL, Crous PW, Groenewald JZ, Boehm EWA, Burgess TI, et al. A class-wide phylogenetic assessment of Dothideomycetes. Stud Myc. 2009;64:1–15.CrossRefGoogle Scholar
  40. 40.
    Stamatakis A, Ludwig T, Meier H. RAxML-iii: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics. 2005;21:456–63.PubMedCrossRefGoogle Scholar
  41. 41.
    Stocker-Wörgötter E. Investigating the production of secondary compounds in cultured lichen mycobionts. In: Kanner I, Beckett RP, Varma AK, editors. Protocol in lichenology, culturing biochemistry, ecophysiology and use in biomonitoring. Berlin: Springer; 2002. p. 296–306.CrossRefGoogle Scholar
  42. 42.
    Turian G. Coniosporium aeroalgicolum sp. nov.—a dematiaceous fungus living in balanced parasitism with aerial algae. Bulletin de la Societe Botanique Suisse. 1977;87:19–24.Google Scholar
  43. 43.
    Vilgalys R, Hester M. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacter. 1990;172:4238–46.Google Scholar
  44. 44.
    Yamamoto Y, Kinoshita Y, Yoshimura I. Culture of thallus fragments and re-differentiation of lichens. In: Kanner I, Beckett RP, Varma AK, editors. Protocol in lichenology, culturing biochemistry, ecophysiology and use in biomonitoring. Berlin: Springer; 2002. p. 34–46.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Lucia Muggia
    • 1
    • 2
  • Cecile Gueidan
    • 3
  • Kerry Knudsen
    • 4
  • Gary Perlmutter
    • 5
  • Martin Grube
    • 1
  1. 1.Institute of Plant SciencesKarl-Franzens-University GrazGrazAustria
  2. 2.Department of Life ScienceUniversity of TriesteTriesteItaly
  3. 3.Department of Life ScienceThe Natural History MuseumLondonUK
  4. 4.The Herbarium, Department of Botany and Plant SciencesUniversity of CaliforniaRiversideUSA
  5. 5.UNC Herbarium, North Carolina Botanical GardenUniversity of North CarolinaChapel HillUSA

Personalised recommendations