Polyextremotolerant black fungi: oligotrophism, adaptive potential, and a link to lichen symbioses

Abstract

Black meristematic fungi can survive high doses of radiation and are resistant to desiccation. These adaptations help them to colonize harsh oligotrophic habitats, e.g., on the surface and subsurface of rocks. One of their most characteristic stress-resistance mechanisms is the accumulation of melanin in the cell walls. This, production of other protective molecules and a plastic morphology further contribute to ecological flexibility of black fungi. Increased growth rates of some species after exposure to ionizing radiation even suggest yet unknown mechanisms of energy production. Other unusual metabolic strategies may include harvesting UV or visible light or gaining energy by forming facultative lichen-like associations with algae or cyanobacteria. The latter is not entirely surprising, since certain black fungal lineages are phylogenetically related to clades of lichen-forming fungi. Similar to black fungi, lichen-forming fungi are adapted to growth on exposed surfaces with low availability of nutrients. They also efficiently use protective molecules to tolerate frequent periods of extreme stress. Traits shared by both groups of fungi may have been important in facilitating the evolution and radiation of lichen-symbioses.

Keywords: melanin; oligotrophism; protective molecules; secondary metabolites; stress.

Figure 1

When do we call it lichen? (A) Lichen-like association of Cladosporium-like fungus (according to ITS sequences) with aerial algal cells, on polypropylene surface, Botanical Garden Graz, 2011. Arrows indicate coccal algal cells (a) attached to fungal hypha (f); Bar = 20 μm. (B) Habit of the “black” lichen Cystocoleus ebeneus; a closed sheath of black fungal hyphae (f) wrap a central algal thread (a); Bar = 10 μm.

Figure 2

Close relationships of life styles in a subgroup of the Teratosphaeriaceae (Dothideomycetes), including rock-inhabiting black fungi and lichens, and plant-surface colonizers. Bayesian analysis of combined nuSSU, nuLSU, mtSSU, and rRNA genes.