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.

Keywords: Asterochloris; Cladonia; green algae; lichens; photobiont; specificity; symbiosis.

FIGURE 1

Sampling design. Eight sites were sampled in seven of the biogeographical regions of Europe. Map copyright holder: Council of Europe (CoE), Directorate-General for Environment (DG ENV).

FIGURE 2

Variation partitioning of (A) algal and (B) fungal diversity. Variables significantly contributing to the variation explained (p < 0.001) are marked with ***.

FIGURE 3

Visualization of the photobiont-mycobiont (marked with photobionts species names and mycobionts OTU numbers, respectively) network resulting from the modularity analysis. No-overlap algorithm was used to spread nodes apart. Four major modules were found and they are distinguished by color.

FIGURE 4

Variation partitioning of the effects of environmental variables on the photobiont-mycobiont modules found by modularity analysis. Variables significantly contributing to the variation explained (p < 0.001) are marked with ***.

FIGURE 5

Comparison of climatic variables between the photobiont-mycobiont modules. Significance levels, calculated by Wilcoxon test, are given: “***” – p < 0.001, “*” – p < 0.05, “NS” – not significant. Bold lines represent the median and whiskers account for the 95% confidence interval of the data. Outliers appear as circles.

FIGURE 6

Comparison of soil properties between the photobiont-mycobiont modules. Significance levels, calculated by Wilcoxon test, are given: “***” – p < 0.001, “*” – p < 0.05, “NS” – not significant. Bold lines represent the median and whiskers account for the 95% confidence interval of the data. Outliers appear as circles.

FIGURE 7

Principal component analysis of the sampling sites based on six climatic variables (A,B) and four soil properties (C,D) that significantly differ between the photobiont-mycobiont modules. Large circles represented group centroids. The modules are distinguished by color.

FIGURE 8

Incidence of lichen morphological traits between the modules. Filled and empty circles display positive and negative associations between the module assignment and the trait values. Stronger associations are shown by larger circles and darker colors. The darker the color, the more distinct the observed value than the expected value if the data were random (calculated by Chi-squared test). The size of the circle is proportional to the amount of the cell contribution.