Photosymbiodemes are a special case of lichen symbiosis where one lichenized fungus engages in symbiosis with two different photosynthetic partners, a cyanobacterium and a green alga, to develop two distinctly looking photomorphs. We investigated differential gene expression in photosymbiodemes of the lichen Peltigera britannica at different temperatures representing mild and putatively stressful conditions and compared gene expression of thallus sectors containing cyanobacterial photobionts with thallus sectors with both green algal and cyanobacterial photobionts. Firstly, because of known ecological differences between photomorphs, we investigated symbiont-specific responses in gene expression to temperature increases. Secondly, we quantified photobiont-mediated differences in fungal gene expression. High temperatures expectedly led to an upregulation of genes involved in heat shock responses in all organisms in whole transcriptome data. As expected, the expression of genes involved in photosynthesis was increased in both photobiont types at 15 and 25 °C. The green algae exhibited thermal stress responses mainly at 25 °C, the fungus and the cyanobacteria already at 15 °C, demonstrating symbiont-specific responses to environmental cues and symbiont-specific ecological optima. Furthermore, photobiont-mediated differences in fungal gene expression could be identified, with upregulation of distinct biological processes in the different morphs, showing that interaction with specific symbiosis partners profoundly impacts fungal gene expression.

Anthropogenic climate change has led to unprecedented shifts in temperature across many ecosystems. In a context of rapid environmental changes, acclimation is an important process as it may influence the capacity of organisms to survive under novel thermal conditions. Mechanisms of acclimation could involve upregulation of stress response genes involved in protein folding, DNA damage repair and the regulation of signal transduction genes, along with a simultaneous downregulation of genes involved in growth or cell cycle, in order to maintain cellular functions and equilibria. We transplanted Lobaria pulmonaria lichens originating from different forests to determine the relative effects of long-term acclimation and genetic factors on the variability in expression of mycobiont and photobiont genes. We found a strong response of mycobiont and photobiont to high temperatures, regardless of sample origin. The green-algal photobiont had an overall lower response than the mycobiont. The gene expression of both symbionts was also influenced by acclimation to transplantation sites and by genetic factors. Lobaria pulmonaria seems to have evolved powerful molecular pathways to deal with environmental fluctuations and stress and can acclimate to new habitats by transcriptomic convergence. Although L. pulmonaria has the molecular machinery to counteract short-term thermal stress, survival of lichens like L. pulmonaria depends mostly on their long-term positive carbon balance, which can be compromised by warmer temperatures and reduced precipitation, and both these outcomes have been predicted for Central Europe in connection with global climate change