Lichen Rehydration in Heavy Metal-Polluted Environments: Pb Modulates the Oxidative Response of Both Ramalina farinacea Thalli and Its Isolated Microalgae

Abstract

Lichens are adapted to desiccation/rehydration and accumulate heavy metals, which induce ROS especially from the photobiont photosynthetic pigments. Although their mechanisms of abiotic stress tolerance are still to be unravelled, they seem related to symbionts' reciprocal upregulation of antioxidant systems. With the aim to study the effect of Pb on oxidative status during rehydration, the kinetics of intracellular ROS, lipid peroxidation and chlorophyll autofluorescence of whole Ramalina farinacea thalli and its isolated microalgae (Trebouxia TR1 and T. TR9) was recorded. A genetic characterization of the microalgae present in the thalli used was also carried out in order to assess possible correlations among the relative abundance of each phycobiont, their individual physiological responses and that of the entire thallus. Unexpectedly, Pb decreased ROS and lipid peroxidation in thalli and its phycobionts, associated with a lower chlorophyll autofluorescence. Each phycobiont showed a particular pattern, but the oxidative response of the thallus paralleled the TR1's, agreeing with the genetic identification of this strain as the predominant phycobiont. We conclude that: (1) the lichen oxidative behaviour seems to be modulated by the predominant phycobiont and (2) Pb evokes in R. farinacea and its phycobionts strong mechanisms to neutralize its own oxidant effects along with those of rehydration.

Contrasting strategies used by lichen microalgae to cope with desiccation–rehydration stress revealed by metabolite profiling and cell wall analysis

“…In resurrection plants, constitutive protective mechanisms slow the rate of water loss and facilitate the ordered expression of inducible components of desiccation–rehydration tolerance (Lüttge and Büdel, ; Dinakar and Bartels, ; Gechev et al ., , Zagorchev et al ., ; Suguiyama et al ., ). Lichens do not develop either root‐like structures or a hydrophobic cuticle, and their microalgae are not as profusely vacuolated as the photosynthetic cells of vascular plants, making desiccation and rehydration more rapid in these organisms than in plants (Álvarez et al ., and citations therein). While desiccation–rehydration can take days or weeks in resurrection plants (Moore et al ., ; Suguiyama et al ., ), both processes take minutes or hours in entire lichen thalli (Beckett et al ., ) and isolated lichen microalgae (Gasulla et al ., ).…”

Amphitropical variation of the algal partners of Pseudephebe (Parmeliaceae, lichenized fungi)

“…Such complexity is even higher when considering the phenomenon of algal co-occurrence, that is, the co-existence of multiple genotypes (or even algae species) within a thallus (Bačkor et al 2010;Català et al 2016;Dal Grande et al 2018). In fact, evidence from these and other studies supports it to be more the rule than the exception and to be related to the lichen's performance against environmental stress (Casano et al 2011;Álvarez et al 2015;Vančurová et al 2018). At diverse spatial scales, the intrathalline community structure of lichen microalgae may be controlled by several factors, such as climate, altitude and substrate (Yahr et al 2006;Fernández-Mendoza et al 2011;Vargas Castillo and Beck 2012;Nadyeina et al 2014;Werth and Sork 2014;Singh et al 2017;Dal Grande et al 2018;Devkota et al 2019;Rolshausen et al 2020).…”

Innovative Approaches Using Lichen Enriched Media to Improve Isolation and Culturability of Lichen Associated Bacteria

“…These novel properties allow the colonization of diverse habitats and survival under extreme environmental and climatic conditions [ 6 – 9 ], even in outer space [ 10 ]. In addition, the intrathalline coexistence of different algal lineages with diverse physiological patterns of abiotic stress tolerance could be advantageous to lichens [ 11 – 13 ].…”