https://orcid.org/0000-0001-6498-975X
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ABSTRACT
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°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.
Acknowledgements
Alba Vergés (University of Girona) for the update on the taxonomic status of the studied species. José Vicente Albero for kindly providing meteorological data from Livingston Island. The UTM staff at the Juan Carlos I Antarctic Research Station is also acknowledged for its exceptional support during our field campaigns. These results have been partially obtained at the Spanish Antarctic Station JCI after having accessed on 2017/2018. MIA received a pre-doctoral grant from the Basque Government. AVPC was awarded a predoctoral fellowship (FPU-02054) supported by the Ministerio de Educación, Cultura y Deporte (MECD), Spain.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Supplementary material
The following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2022.2136405
Supplementary fig. S1. Example of vapour pressure deficit (VPD) changes during 20 consecutive days in the two localities studied (Livingston Island and Azkorri Beach) during the growth period of both species (10th February-2nd March 2018 for P. endiviifolia and 1st February-20th February 2020 for P. linearis.
Supplementary fig. S2. Pigment changes during the desiccation and freezing experiments (80, 50 and 5%) shown in . 100%RH represents control for both desiccation and freezing experiments. Data are mean ± SE (n= 3-9). Different letters indicate significant differences between both species (Tukey’s test, P < 0.05).
Supplementary table S1. Absolute minimum temperature and mean minimum temperature during the growing period of the gametophytes of P. linearis in Azkorri (January-February) and P. endiviifolia in Livingston (February-March).
Author contributions
J.I. García-Plazaola: conceptualization, methodology, investigation, writing; M.I. Arzac: investigation; L. Brazales: investigation; J. Fernández: investigation; J.M. Laza: methodology, writing; J.L. Vilas: M. López-Pozo: investigation; A.V. Perera-Castro: methodology, investigation, writing; B. Fernández-Marín: conceptualization, methodology, investigation, writing. All authors contributed to the final version of the manuscript.