Alternative electron transport pathways contribute to tolerance to high light stress in lichenized algae

The photosynthetic apparatus of lichen photobionts has been well-characterized by chlorophyll fluorescence analysis (e.g., by pulse amplitude modulation [PAM]), which provides a proxy of the activity of photosystem II (PSII) and its antenna. However, such kinetics are unable to directly characterize photosystem I (PSI) activity and the associated alternative electron pathways that may be involved in photoprotection. Instead, PSI can be probed in vivo by near-infrared absorption, measured at the same time as standard chlorophyll fluorescence (e.g., using the WALZ Dual PAM). Here, we used the Dual PAM to investigate cyclic electron flow and photoprotection in a range of mostly temperate lichens sampled from shaded to more open microhabitats. Sun species displayed lower acceptor side limitation of PSI (Y[NA]) early in illumination when compared to shade species, indicative of higher flavodiiron-mediated pseudocyclic electron flow. In response to high irradiance, some lichens accumulate melanin, and Y[NA] was lower and NAD(P)H dehydrogenase (NDH-2)-type cyclic flow was higher in melanised than pale forms. Furthermore, non-photochemical quenching (NPQ) was higher and faster relaxing in shade than sun species, while all lichens displayed high rates of photosynthetic cyclic electron flow. In conclusion, our data suggest that (1) low acceptor side limitation of PSI is important for sun-exposed lichens; (2) NPQ helps shade species tolerate brief exposure to high irradiance; and (3) cyclic electron flow is a prominent feature of lichens regardless of habitat, although NDH-2-type flow is associated with high light acclimation.