The crustose lichenized fungi in the Acarosporaceae are splendid examples of organisms managing to survive in extremely harsh environments, such as highly mineralized rocks and low-pH habitats. Some representatives of the Acarospora smaragdula complex are known to accumulate substantial amounts of potentially toxic metals including iron and copper, resulting in populations with highly divergent coloration and morphology. These populations have often been treated as distinct species by lichen taxonomists. Parsimony and parsimony jackknifing analyses of b-tubulin, nuclear ITS rDNA, and mtSSU rDNA sequence data sets was used to investigate the evolution of iron and copper accumulation and the production of the secondary compound norstictic acid in populations within the A. smaragdula species complex in Sweden, with additional samples mainly from Norway and the UK. Phylogenetic species recognition (concordance of single-gene phylogenies) was used to investigate species delimitations. Seven species are recognized in the complex. Atypically green, copper-accumulating samples, often given species rank, do not form a distinct group but are nested within A. smaragdula s. str., indicating that this ability is widespread in this species. Rust-coloured, iron-accumulating samples form two well supported separate groups, indicating that two morphologically distinct, obligate, ironaccumulating species are present, but facultatively iron-accumulating populations occur in at least one additional species. Norstictic acid, sometimes claimed to characterize the whole A. smaragdula complex, is only present in A. smaragdula s. str. The evolutionary significance of metal accumulation in Acarospora is discussed, as is the significance of our results for the application of phylogenetic species recognition ⁄ gene tree concordance-based species recognition, and DNA barcoding.
The upper cortex and extracellular hyphal wall matrix are mineralized in both rust-coloured Acarospora sinopica and the paler A. smaragdula 'f. subochracea' in the form of microgranular or microbotryoidal phases. Analysis confirmed the distinctive colours are not simply due to hydrated iron oxides, as previously believed, and suggests mixed sulphide and oxide phases with little crystallinity, as well as other elements arising from clay minerals are present. These aspects highlight the need for a more detailed study employing a range of micro-analytical techniques, including analytical TEM, which will allow mineral characterisation and localisation down to the nanometre scale.
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