Terrestrial Green Algae Show Higher Tolerance to Dehydration than Do Their Aquatic Sister-Species

Abstract

Diverse algae possess the ability to recover from extreme desiccation without forming specialized resting structures. Green algal genera such as Tetradesmus (Sphaeropleales, Chlorophyceae) contain temperate terrestrial, desert, and aquatic species, providing an opportunity to compare physiological traits associated with the transition to land in closely related taxa. We subjected six species from distinct habitats to three dehydration treatments varying in relative humidity (RH 5%, 65%, 80%) followed by shortand long-term rehydration. We tested the capacity of the algae to recover from dehydration using the effective quantum yield of photosystem II as a proxy for physiological activity. The degree of recovery was dependent both on the habitat of origin and the dehydration scenario, with terrestrial, but not aquatic, species recovering from dehydration. Distinct strains of each species responded similarly to dehydration and rehydration, with the exception of one aquatic strain that recovered from the mildest dehydration treatment. Cell ultrastructure was uniformly maintained in both aquatic and desert species during dehydration and rehydration, but staining with an amphiphilic styryl dye indicated damage to the plasma membrane from osmotically induced water loss in the aquatic species. These analyses demonstrate that terrestrial Tetradesmus possess a vegetative desiccation tolerance phenotype, making these species ideal for comparative omics studies.

Convergent evolution of gene regulatory networks underlying plant adaptations to dry environments

“…DT, the ability to survive the loss of almost all cellular water without irreversible damage, appeared in the plant lineage during terrestrialization of their ancestor streptophyte algae (Figure 1 ) (Alpert, 2000 ; Leprince & Buitink, 2010 ; Oliver et al, 2000 ; Terlova et al, 2021 ; Wodniok et al, 2011 ). DT refers to survival after extreme dehydration (below 0.3 g H 2 O/g dry weight) where the cellular metabolic activity nearly stops, entering into a state of ‘anhydrobiosis’ (Hoekstra et al, 2001 ).…”

“…At least six independent major clades of green algae were able to colonize dry environments and to display this remarkable ability to withstand extreme dehydration (Lewis & McCourt, 2004 ; Terlova et al, 2021 ). The initial appearance of DT features in the ancestor green algae was a crucial step for plant radiation on land (Oliver et al, 2000 ; Rensing et al, 2008 ; Wodniok et al, 2011 ).…”

Convergent evolution of gene regulatory networks underlying plant adaptations to dry environments

“…3 Desiccation tolerance GRN in seeds and resurrection plants Desiccation tolerance (DT), the ability to survive the loss of almost all cellular water without irreversible damage, appeared in the plant lineage during terrestrialization of their ancestor streptophyte algae (Figure 1) (Alpert, 2000;Leprince & Buitink, 2010;Oliver et al, 2000;Terlova, Holzinger, & Lewis, 2021;Wodniok et al, 2011). DT refers to survival after extreme dehydration (below 0.3 g H 2 O/g dry weight) where the cellular metabolic activity nearly stops, entering into a state of 'anhydrobiosis' (Hoekstra, Golovina, & Buitink, 2001).…”

“…At least six independent major clades of green algae were able to colonize dry environments and to display this remarkable ability to withstand extreme dehydration (Lewis & McCourt, 2004;Terlova et al, 2021). The initial appearance of DT features in the ancestor green algae was a crucial step for plant radiation on land (Oliver et al, 2000;Rensing et al, 2008;Wodniok et al, 2011).…”

Metabolite Profiling in Green Microalgae with Varying Degrees of Desiccation Tolerance

“…Moreover, it remains an enigma why some phylogenetically closely related green algae vary strongly in their desiccation tolerance [ 36 ]. For example, in Tetradesmus spp., desiccation tolerance appears to be a common trait in temperate and desert soil crusts, but is missing in closely related aquatic species [ 38 ]. Differences in relative desiccation tolerance were also observed in closely related species, or even within the same species, in the Chlorellaceae and Scenedesmaceae [ 4 , 25 , 39 ].…”