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Stud Mycol 61(1): 111-119 2008
DOI: 10.3114/sim.2008.61.11
Copyright © 2008 CBS Fungal Biodiversity Centre
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A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages

C. Gueidan1,3, C. R. Villaseñor2,3, G. S. de Hoog3, A. A. Gorbushina4,5, W. A. Untereiner6 and F. Lutzoni1

1 Department of Biology, Duke University, Box 90338, Durham NC, 27708 U.S.A.
2 Departamento de Ingeniería y Ciencia de los Materiales, Escuela Técnica Superior de Ingenieros Industriales, Universidad Politécnica de Madrid (UPM), José Gutiérrez Abascal 2, 28006 Madrid, Spain
3 CBS Fungal Biodiversity Centre, P.O. Box 85167, NL-3508 AD Utrecht, The Netherlands
4 Geomicrobiology, ICBM, Carl von Ossietzky Universität, P.O. Box 2503, 26111 Oldenburg, Germany
5 LBMPS, Department of Plant Biology, Université de Genève, 30 quai Ernest-Ansermet, 1211 Genève 4, Switzerland
6 Department of Biology, Brandon University, Brandon, MB Canada R7A 6A9

Correspondence: Cécile Gueidan, c.gueidan{at}cbs.knaw.nl

Rock surfaces are unique terrestrial habitats in which rapid changes in the intensity of radiation, temperature, water supply and nutrient availability challenge the survival of microbes. A specialised, but diverse group of free-living, melanised fungi are amongst the persistent settlers of bare rocks. Multigene phylogenetic analyses were used to study relationships of ascomycetes from a variety of substrates, with a dataset including a broad sampling of rock dwellers from different geographical locations. Rock-inhabiting fungi appear particularly diverse in the early diverging lineages of the orders Chaetothyriales and Verrucariales. Although these orders share a most recent common ancestor, their lifestyles are strikingly different. Verrucariales are mostly lichen-forming fungi, while Chaetothyriales, by contrast, are best known as opportunistic pathogens of vertebrates (e.g. Cladophialophora bantiana and Exophiala dermatitidis, both agents of fatal brain infections) and saprophytes. The rock-dwelling habit is shown here to be key to the evolution of these two ecologically disparate orders. The most recent common ancestor of Verrucariales and Chaetothyriales is reconstructed as a non-lichenised rock-inhabitant. Ancestral state reconstructions suggest Verrucariales as one of the independent ascomycetes group where lichenisation has evolved on a hostile rock surface that might have favored this shift to a symbiotic lifestyle. Rock-inhabiting fungi are also ancestral to opportunistic pathogens, as they are found in the early diverging lineages of Chaetothyriales. In Chaetothyriales and Verrucariales, specific morphological and physiological traits (here referred to as extremotolerance) evolved in response to stresses in extreme conditions prevailing on rock surfaces. These factors facilitated colonisation of various substrates including the brains of vertebrates by opportunistic fungal pathogens, as well as helped establishment of a stable lichen symbiosis.

Keywords Evolution of rock-dwelling habit / evolution of lichenisation / multigene phylogeny / ancestral state reconstruction / Verrucariales and Chaetothyriales (Chaetothyriomycetidae, Eurotiomycetes)




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