Symbiosis at its limits: ecophysiological consequences of lichenization in the genus Prasiola in Antarctica

Abstract

Background and Aims Lichens represent a symbiotic relationship between at least one fungal and one photosynthetic partner. The association between the lichen-forming fungus Mastodia tessellata (Verrucariaceae) and different species of Prasiola (Trebouxiophyceae) has an amphipolar distribution and represents a unique case study for the understanding of lichen symbiosis because of the macroalgal nature of the photobiont, the flexibility of the symbiotic interaction and the co-existence of free-living and lichenized forms in the same microenvironment. In this context, we aimed to (1) characterize the photosynthetic performance of co-occurring populations of free-living and lichenized Prasiola and (2) assess the effect of the symbiosis on water relations in Prasiola, including its tolerance of desiccation and its survival and performance under sub-zero temperatures. Methods Photochemical responses to irradiance, desiccation and freezing temperature and pressure–volume curves of co-existing free-living and lichenized Prasiola thalli were measured in situ in Livingston Island (Maritime Antarctica). Analyses of photosynthetic pigment, glass transition and ice nucleation temperatures, surface hydrophobicity extent and molecular analyses were conducted in the laboratory. Key Results Free-living and lichenized forms of Prasiola were identified as two different species: P. crispa and Prasiola sp., respectively. While lichenization appears to have no effect on the photochemical performance of the alga or its tolerance of desiccation (in the short term), the symbiotic lifestyle involves (1) changes in water relations, (2) a considerable decrease in the net carbon balance and (3) enhanced freezing tolerance. Conclusions Our results support improved tolerance of sub-zero temperature as the main benefit of lichenization for the photobiont, but highlight that lichenization represents a delicate equilibrium between a mutualistic and a less reciprocal relationship. In a warmer climate scenario, the spread of the free-living Prasiola to the detriment of the lichen form would be likely, with unknown consequences for Maritime Antarctic ecosystems.

Synergistic adaptations: freezing tolerance is associated with desiccation tolerance and activation of violaxanthin de-epoxidase in wintergreen ferns

“…In parallel, violaxanthin de-epoxidase is activated during both the freezing and desiccating processes, converting violaxanthin to zeaxanthin, even in the absence of light ( Fernández-Marín et al , 2021 a ). These findings align with previous studies, suggesting a broader trend across DT photosynthetic organisms that tolerate freezing ( Fernández-Marín et al, 2018 , 2019 , 2021 b ).…”

“…Are all DT plants also freezing tolerant? So far, we have evidence that some DT plants are also tolerant of some degree of freezing ( Fernández-Marín et al, 2018 , 2019 , 2020 , 2021 b ). It is possible that all DT plants achieve a glassy state at sufficiently low temperatures, and this may confer cellular freezing tolerance.…”

Lichen algae: the photosynthetic partners in lichen symbioses

“…There is considerable evidence that the surrounding fungal tissues and their secondary metabolites may help protect the lichenized alga from desiccation, photoinhibition, temperature extremes and herbivory (e.g. Solhaug & Gauslaa 1996;Kranner et al 2008;Kosugi et al 2009;Asplund & Wardle 2013;Gauslaa et al 2017;Míguez et al 2017;Sadowsky & Ott 2016;Beckett et al 2019;Fernández-Marín et al 2019). Symbiosis may significantly improve the alga's ability to avoid cellular damage caused by highly reactive forms of oxygen (ROS) generated under stress conditions (Kranner et al 2005).…”

Coexistent Heteroblastic Needles of Adult Pinus canariensis C.Sm. ex DC. in Buch Trees Differ Structurally and Physiologically

“…The contact angle (CA) of droplets of distilled water was measured over the surface of the needles, following [43] with small modifications. Briefly, sessile droplets of 5 µL were placed on the adaxial side of the central part of each needle.…”