Symbiosis extended: exchange of photosynthetic O(2) and fungal-respired CO(2) mutually power metabolism of lichen symbionts

Lichens are a symbiosis between a fungus and one or more photosynthetic microorganisms that enables the symbionts to thrive in places and conditions they could not compete independently. Exchanges of water and sugars between the symbionts are the established mechanisms that support lichen symbiosis. Herein, we present a new linkage between algal photosynthesis and fungal respiration in lichen Flavoparmelia caperata that extends the physiological nature of symbiotic co-dependent metabolisms, mutually boosting energy conversion rates in both symbionts. Measurements of electron transport by oximetry show that photosynthetic O(2) is consumed internally by fungal respiration. At low light intensity, very low levels of O(2) are released, while photosynthetic electron transport from water oxidation is normal as shown by intrinsic chlorophyll variable fluorescence yield (period-4 oscillations in flash-induced Fv/Fm). The rate of algal O(2) production increases following consecutive series of illumination periods, at low and with limited saturation at high light intensities, in contrast to light saturation in free-living algae. We attribute this effect to arise from the availability of more CO(2) produced by fungal respiration of photosynthetically generated sugars. We conclude that the lichen symbionts are metabolically coupled by energy conversion through exchange of terminal electron donors and acceptors used in both photosynthesis and fungal respiration. Algal sugars and O(2) are consumed by the fungal symbiont, while fungal delivered CO(2) is consumed by the alga. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s11120-019-00702-0) contains supplementary material, which is available to authorized users.