Tolerance to Cyclic Desiccation in Lichen Microalgae is Related to Habitat Preference and Involves Specific Priming of the Antioxidant System

Abstract

Abstract Oxidative stress is a crucial challenge for lichens exposed to cyclic desiccation and rehydration (D/R). However, strategies to overcome this potential stress are still being unraveled. Therefore, the physiological performance and antioxidant mechanisms of two lichen microalgae, Trebouxia sp. (TR9) and Coccomyxa simplex (Csol), were analyzed. TR9 was isolated from Ramalina farinacea, a Mediterranean fruticose epiphytic lichen adapted to xeric habitats, while Csol is the phycobiont of Solorina saccata, a foliaceous lichen that grows on humid rock crevices. The tolerance to desiccation of both species was tested by subjecting them to different drying conditions and to four consecutive daily cycles of D/R. Our results show that a relative humidity close to that of their habitats was crucial to maintain the photosynthetic rates. Concerning antioxidant enzymes, in general, manganese superoxide dismutases (MnSODs) were induced after desiccation and decreased after rehydration. In TR9, catalase (CAT)-A increased, and its activity was maintained after four cycles of D/R. Ascorbate peroxidase activity was detected only in Csol, while glutathione reductase increased only in TR9. Transcript levels of antioxidant enzymes indicate that most isoforms of MnSOD and FeSOD were induced by desiccation and repressed after rehydration. CAT2 gene expression was also upregulated and maintained at higher levels even after four cycles of D/R in accordance with enzymatic activities. To our knowledge, this is the first study to include the complete set of the main antioxidant enzymes in desiccation-tolerant microalgae. The results highlight the species-specific induction of the antioxidant system during cyclic D/R, suggesting a priming of oxidative defence metabolism.