Lichen Symbiosis: Turning photosynthesis on & off via water (de)hydration as revealed by real-time kinetics of electron transport, O2 &CO2 exchange between alga & fungus

Lichens are a symbiosis of a fungus and at least one green alga or cyanobacterium. While lichens lack a vascular system like plants, so-called foliose and fruticose lichens do have specialised tissue that supports water and gas uptake and distribution inside the lichen leaf between the symbionts. Lichens are famous for their ability to tolerate deep desiccation, which enables them to survive in water-stressed environments. In the absence of stomata to control internal water content, lichens are adapted to daily hydration/desiccation cycles throughout their lifetime. To support their survival under such stressful conditions, they developed the unique capability of rapid light energy dissipation as heat during desiccation and rapid recovery of photosynthesis upon hydration. Thus far, analysis of lichen photosynthesis response to hydration conditions has focused on equilibrium measurements after equilibration with the atmosphere. Here, we investigated real-time response of photosynthesis to (de)hydration processes in lichen Flavoparmelia caperata. Simultaneous measurements of both water content and variable chlorophyll fluorescence showed two separate stages of water loss kinetics: high water loss rates from low-affinity fungal compartments, followed by exponentially decreasing water loss rate from high-affinity algal compartments. The latter stage coincided with non-linear dependence of photosynthesis described by sigmoidal (logistics) curve. Rehydration kinetics of photosynthesis (variable fluorescence) are 5x faster than dehydration kinetics. Our experiments showed that algal cells within hydrated lichens are fully active photosynthetically, but the O₂ they produce is trapped inside the lichen below an O₂ saturation limit. Above this threshold, release occurs largely through the lower cortex, made of fungal tissue. This strong asymmetry indicates that O₂ is consumed internally, presumably by fungal respiration, further extending the multiple interdependences of their symbiotic relationship.