Algal-fungal symbionts share water, nutrients, and gases via an architecture unique to lichens. Because lichen activity is controlled by moisture dynamics, understanding water transport is prerequisite to understand their fundamental biology. We propose a model of water distributions within foliose lichens governed by laws of fluid motion. Our model differentiates between water stored in symbionts, on extracellular surfaces, and in distinct morphological layers. We parameterize our model with hydraulic properties inverted from laboratory measurements of Flavoparmelia caperata and validate for wetting and drying. We ask: (1) Where is the bottleneck to water transport? (2) How do hydration and dehydration dynamics differ? and (3) What causes these differences? Resistance to vapor flow is concentrated at thallus surfaces and acts as the bottleneck for equilibrium, while internal resistances are small. The model captures hysteresis in hydration and desiccation, which are shown to be controlled by nonlinearities in hydraulic capacitance. Muting existing nonlinearities slowed drying and accelerated wetting, while exaggerating nonlinearities accelerated drying and slowed wetting. The hydraulic nonlinearity of F. caperata is considerable, which may reflect its preference for humid and stable environments. The model establishes the physical foundation for future investigations of transport of water, gas, and sugar between symbionts.@en

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 O2 is consumed internally by fungal respiration. At low light intensity, very low levels of O2 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 O2 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 CO2 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 O2 are consumed by the fungal symbiont, while fungal delivered CO2 is consumed by the alga.@en

Lichens have developed unique strategies to control water, oxygen and photosynthate (sugar product) fluxes between the algal photobiont and its fungal host that provide a model for gas-liquid separation and transport. We measured in parallel the kinetics of dehydration (water content), light trapping by charge separation and oxygen evolution (chlorophyll fluorescence emission) from full hydration to the dehydrated state. Kinetics show two distinct temporal stages in lichen dehydration: rapid loss of free, extracellular water, followed by slower loss of intracellular water associated with a discontinuous (rapid) decrease in charge separation. The former shows that water saturation does not prevent lichens from being photosynthetically active and allows gas transport (CO2 and O2) to occur during water logging. The latter observation indicates that dehydration is used to cooperatively turn off photosynthesis. This is hypothesized to trigger transport of algal-derived sugars to the fungal host. Confocal microscopy of lichens shows that the 3D architecture has distinct zones of physical space for gas and water transport between alga and fungus. Algal cells are encased in a hydrophobic shell that limits water accessibility and channels CO2 and O2 gas respectively to the photobiont and fungus (for respiration). Algae are connected to a single hydrophilic fungal filament that delivers water and recovers algal products (sugar & O2), synchronized to the daily solar cycle. This bipolar chemical asymmetry enables such counter transport. Hence, the daily hydration/ dehydration cycle serves as a pump. @en