Promiscuity in Lichens Follows Clear Rules: Partner Switching in Cladonia Is Regulated by Climatic Factors and Soil Chemistry

Abstract

Climatic factors, soil chemistry and geography are considered as major factors affecting lichen distribution and diversity. To determine how these factors limit or support the associations between the symbiotic partners, we revise the lichen symbiosis as a network of relationships here. More than one thousand thalli of terricolous Cladonia lichens were collected at sites with a wide range of soil chemical properties from seven biogeographical regions of Europe. A total of 18 OTUs of the algal genus Asterochloris and 181 OTUs of Cladonia mycobiont were identified. We displayed all realized pairwise mycobiont–photobiont relationships and performed modularity analysis. It revealed four virtually separated modules of cooperating OTUs. The modules differed in mean annual temperature, isothermality, precipitation, evapotranspiration, soil pH, nitrogen, and carbon contents. Photobiont switching was strictly limited to algae from one module, i.e., algae of similar ecological preferences, and only few mycobionts were able to cooperate with photobionts from different modules. Thus, Cladonia mycobionts generally cannot widen their ecological niches through photobiont switching. The modules also differed in the functional traits of the mycobionts, e.g., sexual reproduction rate, presence of soredia, and thallus type. These traits may represent adaptations to the environmental conditions that drive the differentiation of the modules. In conclusion, the promiscuity in Cladonia mycobionts is strictly limited by climatic factors and soil chemistry.

An Exception to the Rule? Could Photobiont Identity Be a Better Predictor of Lichen Phenotype than Mycobiont Identity?

“…The final dataset included 241 sequences, of which 205 were newly produced (51 sequences of mycobiont ITS rDNA, 30 of cox1, 29 of EF-1α, 27 of mtSSU, 32 of RPB2, 33 sequences of photobiont ITS rDNA and three of photobiont actin type I gene), 15 were retrieved from our previous datasets [55,56] and 21 downloaded from GenBank (https: //www.ncbi.nlm.nih.gov/ (accessed on 25 November 2021)). The newly obtained sequences have been deposited in GenBank (see Supplementary Table S1 for accession numbers).…”

“…Similarly, it has been reported that soredia attach to water drops on the podetium surface of another sorediate Cladonia species, and that bouncing drops carry soredia and disperse them [ 86 ]. Interestingly, Škvorová et al [ 56 ] found a negative association between the occurrence of A. italiana and the production of soredia in different Cladonia species, suggesting that a stable and humid climate might be disadvantageous for sorediate Cladonia species. The authors further found a strong positive association between soredia production and the occurrence of A. glomerata .…”

Composition, structure and robustness of Lichen guilds

“…For example, sporeproducing lichens that require a compatible photobiont upon reproduction are indirectly facilitated by the asexual lichens within their guild already established in that environment 28 . Previously, guilds have been defined by photobiont taxonomic identity, but this characterisation has been constrained by the scope of the data sets, which have often included a limited amount of species or geographical locations 16,21,[30][31][32][33][34] . An aggregated network perspective allows us to tackle the structural signature of lichen guilds and provides a solid foundation to address how the general patterns of association in the lichen symbiont network affect its robustness.…”

“…However, it is widely acknowledged that specificity of the mycobiont-photobiont association as well as the spatial distribution of their component species largely drives the formation of new lichen organisms 6,[14][15][16] . Indeed, many symbionts are quite stringent in the partnerships they form, which are often determined by biophysical gradients [17][18][19][20][21][22] . It has also been suggested that highly specific mycobionts are typically restricted to few environments and display limited ecological range 23,24 .…”

“…Much of our current understanding on photobiont-mycobiont partnerships comes from studies involving a few species or geographical areas 16,17,21,22,[31][32][33][34][35][36] . However, mycobiont-photobiont partnerships do not happen in isolation, they are part of a larger web of interactions supporting the assembly and maintenance of communities, and understanding them requires a systemic approach.…”