Phylogeny of rock-inhabiting fungi related to Dothideomycetes

Abstract

The class Dothideomycetes (along with Eurotiomycetes) includes numerous rock-inhabiting fungi (RIF), a group of ascomycetes that tolerates surprisingly well harsh conditions prevailing on rock surfaces. Despite their convergent morphology and physiology, RIF are phylogenetically highly diverse in Dothideomycetes. However, the positions of main groups of RIF in this class remain unclear due to the lack of a strong phylogenetic framework. Moreover, connections between rock-dwelling habit and other lifestyles found in Dothideomycetes such as plant pathogens, saprobes and lichen-forming fungi are still unexplored. Based on multigene phylogenetic analyses, we report that RIF belong to Capnodiales (particularly to the family Teratosphaeriaceae s.l.), Dothideales, Pleosporales, and Myriangiales, as well as some uncharacterised groups with affinities to Dothideomycetes. Moreover, one lineage consisting exclusively of RIF proved to be closely related to Arthoniomycetes, the sister class of Dothideomycetes. The broad phylogenetic amplitude of RIF in Dothideomycetes suggests that total species richness in this class remains underestimated. Composition of some RIF-rich lineages suggests that rock surfaces are reservoirs for plant-associated fungi or saprobes, although other data also agree with rocks as a primary substrate for ancient fungal lineages. According to the current sampling, long distance dispersal seems to be common for RIF. Dothideomycetes lineages comprising lichens also include RIF, suggesting a possible link between rock-dwelling habit and lichenisation.

Keywords: Arthoniomycetes; Capnodiales; Dothideomycetes; evolution; extremotolerance; multigene phylogeny; rock-inhabiting fungi.

Fig 1.

Rock-inhabiting fungi related to Dothideomycetes. A–C: sampling localities (photos C. Ruibal and L. Selbmann). A. Metamorphic black slate from Atazar, Central Mountain System, Spain. B. Limestone from Cala Sant Vicenç, Serra de Tramuntana, Mallorca, Spain. C. Sandstone from Alatna Valley, McMurdo Dry Valleys, Antarctica. D–G: Coniosporium apollinis, a rock-inhabiting species from the Mediterranean region (CBS 100213, photos C. Gueidan). D. Colony on MEA. E. Melanised torulose hyphae. F. Hypha disarticulating into bi- to multi-cellular clumps; G. Meristematic growth. H–J: Antarctic rock-inhabiting fungi (photos L. Selbmann). H. RIF growing on a crystal of sandstone. I. Melanised hypha of Friedmanniomyces endolithicus. J. Meristematic growth of Cryomyces antarcticus. K–L: Cystocoleus ebeneus, a lichenised species assigned to Capnodiales (photos L. Muggia). K. Microfilamentous thallus. L. Melanised hyphae of the mycobiont forming a furrow around the filamentous algae. Scale bars: D = 2 mm, E–G and I–J = 10 μm, H = 0.5 mm, K–L = 20 μm.

Fig. 2.

Phylogenetic placement of 102 rock-inhabiting strains within Dothideomyceta (Dothideomycetes and Arthoniomycetes). The tree is based on a Maximum Likelihood analysis of the combined nucLSU, nucSSU and mtSSU (three-gene analysis). A black oval on a branch indicates a bootstrap support value of 100 %. Other bootstrap values ≥ 50 % are shown below or above branches. RIF are highlighted in red and lichens in green. Geographical origins are also labeled for RIF (Alp = Alps, And = Andes, Ant = Antarctica, Ari = Arizona desert, Cri = Crimea, Fra = France, Med = Mediterranean region, including Greece, Israel, Italy, Slovenia, Spain and Turkey). Phylogenetic relationships within Capnodiales are detailed in Fig. 3.

Fig. 3.

Phylogenetic placement of RIF within the order Capnodiales. The tree is based on a Maximum Likelihood analysis of the combined nucLSU, nucSSU and mtSSU (three-gene analysis). A black oval on a branch indicates a bootstrap support value of 100 %. Other bootstrap values ≥ 50 % are shown below or above branches. RIF are highlighted in red and lichens in green. Geographical origins are also labeled for RIF (Alp = Alps, And = Andes, Ant = Antarctica, Ari = Arizona desert, Cri = Crimea, Fra = France, Med = Mediterranean region, including Greece, Israel, Italy, Slovenia, Spain and Turkey).

Fig. 4.

Phylogenetic relationships of rock-inhabiting lineages with known groups of Dothideomyceta based on a Maximum Likelihood analysis of the combined nucLSU, nucSSU, mtSSU, RPB1 and RPB2 (five-gene analysis). A black dot on a branch indicates a bootstrap support value of 100 %. Other bootstrap values ≥ 50 % are shown below or above the branches. RIF are highlighted in red and lichens in green.