Symbiont-specific responses to environmental cues in a threesome lichen symbiosis

Abstract

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.

News from ‘black belt’ masters of symbiosis

“…This symbiotic strategy generates two distinct photomorphs with either cyanobacteria or green alga as primary photobionts. A recent study on the lichen Peltigera britannica explored how gene expression in the fungus varied between thallus sectors with only cyanobacterial photobionts, and those with green algal photobionts (where photobionts are hosted as auxiliary partners only in small, separated organs called cephalodia), particularly under different temperature conditions (Almer et al, 2022). Results of RNA-sequencing showed photobiont-mediated differences in fungal gene expression.…”

“…Genes associated with distinct biological processes are upregulated in association with specific symbionts, indicating that the type of symbiotic partner has a significant influence on the fungal gene expression. When examining the effects of temperature, Almer et al (2022) found that higher temperatures caused an increase in gene expression related to heat shock response across all involved organisms. Both types of photobionts showed increased expression of photosynthesis-related genes at 15°C and 25°C.…”