Freezing and desiccation tolerance in the Antarctic bangiophyte Pyropia endiviifolia (Rhodophyta): a chicken and egg problem?

Antarctic macroalgal communities of the upper intertidal zone are particularly poor compared with other coastal regions. Exposure to desiccation and freezing combined with the abrasive effect of ice threatens the life of sessile organisms. One of the few species able to colonize this environment is the rhodophyte Pyropia endiviifolia. It belongs to the Bangiales, one of the oldest extant clades of photosynthetic eukaryotes, which has occurred for more than one billion years with basically the same morphological structure. Considering that the extent of Antarctic glaciation is a geologically recent event, we hypothesized that pre-adaptations to desiccation in bangiophytes may have contributed to the success of P. endiviifolia in Antarctica. To test this, we compared its photosynthetic performance and tolerance to desiccation and freezing with those from a related intertidal species, the temperate Atlantic species Porphyra linearis. As evidenced by gas exchange and chlorophyll fluorescence, P. endiviifolia is more adapted to high irradiances than P. linearis. The former species was also more desiccation-tolerant, and showed a higher glass transition temperature. Both species did not differ in chlorophyll content per dry weight, and tolerance to -20 degrees C, even though the ice-nucleation temperature was much higher in P. endiviifolia. Membrane integrity may depend on fatty acid composition in P. endiviifolia, while on enhanced tocopherol in P. linearis. Overall, both species show different strategies to deal with freezing temperatures: supercooling in P. linearis vs. freezing-tolerance in P. endiviifolia. This matches with the probability of being subjected to sub-zero temperatures in their natural environments (lower in the case of P. linearis). Surprisingly, the higher risk of dehydration in the natural habitat of P. linearis is not matched by a higher desiccation tolerance. This observation does not support the initial hypothesis of the study but suggests the opposite: the acclimation to a cold environment results in higher desiccation tolerance.HIGHLIGHTS? Porphyra linearis and Pyropia endiviifolia are remarkably tolerant to desiccation and freezing.? Antarctic P. endiviifolia is remarkably tolerant to desiccation and freezing.? Mechanisms of freezing tolerance could induce a higher tolerance to desiccation.

Automated summary

Macroalgal communities in the upper intertidal zone of Antarctica are poor compared to other coastal regions. However, the rhodophyte Pyropia endiviifolia is one of the few species able to colonize this environment successfully. It has better photosynthetic performance and higher tolerance to desiccation and freezing compared to the temperate Atlantic species Porphyra linearis. The study suggests that mechanisms for freezing tolerance may induce higher tolerance to desiccation.