Heavy-metal pollution induces changes in the genetic composition and anatomical properties of photobionts in pioneer lichens colonising post-industrial habitats

Abstract

Certain lichens are effective colonisers of polluted sites. However, little is known about the tolerance of photobionts and the degree of mycobiont selectivity to photobionts relative to metal pollution. The present study recognises the genetic and anatomical diversity of Asterochloris photobionts in epigeic lichens, i.e. Cladonia cariosa, C. rei, and Diploschistes muscorum, in relation to a wide spectrum of soil pollution. In accordance with phylogenetic analysis, photobionts were clustered in 7 moderately- to well-supported clades, including 19 haplotypes. The mycobionts of all studied lichens demonstrated a low level of selectivity and were capable of associating with various Asterochloris lineages. This tendency was also expressed by the frequent (~25%) occurrence of multiple algal genotypes in a single thallus. This indicates that identified Asterochloris lineages are generally tolerant to heavy-metal pollution, and the low level of selectivity of mycobionts enables them to select the most suitable and/or available partner. The trend of increasing incidence of certain Asterochloris lineages and decreasing frequency of others along with increasing soil pollution was observed. This proves the superior adaptation of some photobionts to polluted sites. Such symbiotic plasticity constitute an adaptive feature necessary for the successful colonisation. High number of haplotypes at polluted sites could be the result of multiple introduction events from different areas during the initial stages of spontaneous succession. Regardless of the genetic pattern, Asterochloris cells were considerably smaller, and the density and compaction of cells in the algal layer were higher, in lichen specimens from polluted sites, indicating that photobiont characteristics may be closely dependent on heavy-metal pollution.