Cryoresistance of Antarctic endemic lichen Himantormia lugubris: Analysis of photosystem II functionality using a constant-rate cooling approach
It is well established that lichens from polar regions of the Earth are capable to perform photosynthesis at sub-zero temperatures. Majority of them show a high degree of cryoresistance, however, species-specific differences exist. Therefore, the aim of our study was to evaluate behaviour of primary photochemical processes of photosynthesis in Antarctic endemic species Himantormia lugubris at sub-zero temperature. For the purpose, the method of constant rate (2°C min-1) cooling (from +20 to -40°C) with simultaneous measurements of chlorophyll fluorescence parameters related to photosystem II (PSII) was used. During the cooling, potential yield of photosynthetic processes in PSII (FV/FM), and effective quantum yield of PSII (ΦPSII) were measured in 30 s interval. From the FV/FM and ΦPSII data sets, S-curves reflecting temperature dependence of the two chlorophyll fluorescence parameters were constructed and analyzed. The S-curves were found tri-phasic in response to sample temperature decline: (1) slight or no decline phase, (2) rapid decline phase, followed by (3) slow change reaching critical temperature at which the primary photosynthetic processes were fully inhibited. Critical temperature was found -30 and -20°C for FV/FM, and ΦPSII, respectively. The latter critical temperature was accompanied by an increase in background chlorophyll fluorescence (F0) indicating inhibition of energy transfer from light-harvesting complexes to core of PSII. A newly-designed chlorophyll fluorescence parameter (a differential, i.e. the difference between the maximum value-normalized FV/FM, and ΦPSII) was used in order to evaluate the temperature at which the processes related to photosynthetic electron flow through thylakoid membrane carriers (ΦPSII) and the energy flow through PSII (FV/FM) differed to a largest extent. This parameters proved to be temperature-dependent and useful in the evaluation of cryoresistance. Based on our study, H. lugubris, its primary photosynthetic processes in particular, might be considered as higly resistant to sub-zero temperature.
freezing; photosynthetic apparatus; cooling point; King George Island; differential method
Areche, C., Parra, J. R., Sepulveda, B., García-Beltrán, O. and Simirgiotis, M. J. (2022): UHPLC-MS metabolomic fingerprinting, antioxidant, and enzyme inhibition activities of Himantormia lugubris from Antarctica. Metabolites, 12: 560. doi: 10.3390/metabo12060560
Barták, M., Hájek, J., Orekhova, A., Villagra, J., Marín, C., Palfner, G. and Casanova-Katny, A. (2021): Inhibition of primary photosynthesis in desiccating antarctic lichens differing in their photobionts, thallus morphology, and spectral properties. Microorganisms, 9: 818. doi: 10.3390/microorganisms9040818
Buchner, O., Neuner, G. (2010): Freezing cytorrhysis and critical temperature thresholds for photosystem II in the peat moss Sphagnum capillifolium. Protoplasma, 243: 63-71.
Folgar-Cameán, Y., Barták, M. (2019): Evaluation of photosynthetic processes in Antarctic mosses and lichens exposed to controlled rate cooling: Species-specific responses. Czech Polar Reports, 9 (1): 114-124. doi: 10.5817/CPR2019-1-10
Hájek, J., Puhovkin, A., Giordano, D. and Sekerák Jr., J. (2022): What does critical temperature tell us about the resistance of polar lichens to freezing stress? Applicability of linear cooling method to ecophysiological studies. Czech Polar Reports, 12(2): 246-255. doi: 10.5817/CPR2022-2-18
Harańczyk, H., Grandjean, J., Olech, M. and Michalik, M. (2003): Freezing of water bound in lichen thallus as observed by 1H NMR. II. Freezing protection mechanisms in a cosmopolitan lichen Cladonia mitis and in Antarctic lichen species at different hydration levels. Colloids and Surfaces B: Biointerfaces, 28(4): 251-260.
Hejduková, E., Nedbalová, L. (2021): Experimental freezing of freshwater pennate diatoms from polar habitats. Protoplasma, 258(6): 1213-1229. doi: 10.1007/s00709-021-01648-8
Kvíderová, J., Hájek, J. and Worland, R. M. (2013): The ice nucleation activity of extremophilic algae. CryoLetters, 34 (2): 137-148.
Lyon, B. R., Mock, T. (2014): Polar microalgae: New approaches towards understanding adaptations to an extreme and changing environment. Biology, 3: 56-80. doi: 10.3390/biology3010056
Marečková, M., Barták, M. and Hájek, J. (2019): Temperature effects on photosynthetic performance of Antarctic lichen Dermatocarpon polyphyllizum: A chlorophyll fluorescence study. Polar Biology, 42: 685-701. doi: 10.1007/s00300-019-02464-w
Marín, C., Barták, M., Palfner, G., Vergara-Barros, P., Fernandoy, F., Hájek, J. and Casanova-Katny, A. (2022): Antarctic lichens under long-term passive warming: Species-specific photochemical responses to desiccation and heat shock treatments. Plants, 11: 2463. doi: 10.3390/plants11192463
Moffett, B. F., Getti, G., Henderson-Begg, S. K. and Hill, T. C. J. (2015): Ubiquity of ice nucleation in lichen – possible atmospheric implications. Lindbergia, 38: 39-43.
Mróz, T., Szufa, K., Frontasyeva, M. V., Tselmovich, V., Ostrovnaya, T., Kornaś, A., Olech, M. A., Mietelski, J. W. and Brudecki, K. (2018): Determination of element composition and extraterrestrial material occurrence in moss and lichen samples from King George Island (Antarctica) using reactor neutron activation analysis and SEM microscopy. Environmental Science and Pollution Research International, 25(1): 436-446. doi: 10.1007/s11356-017-0431-2
Orekhova, A., Barták, M., Özkar, A. and Elster, J. (2019): The effect of shock freezing on physiological properties and consequent growth of Antarctic filamentous (Stigeoclonium sp.) and coccal alga (Diplosphaera chodatii) on agar plates. Czech Polar Reports, 9(1): 37-48. doi: 10.5817/CPR2019-1-4.
Pichrtová, M., Hejduková, E., Nedbalová, L. and Elster, J. (2020): How to survive winter?: Adaptation and acclimation strategies of eukaryotic algae from polar terrestrial ecosystems. In: G. Di Prisco, H. Edwards, J. Elster, A. Huiskes (eds.): Life in Extreme Environments: Insights in Biological Capability (Ecological Reviews, pp. 101–125). Cambridge: Cambridge University Press. doi: 10.1017/9781108683319.008
Piñeiro, V., Eguren, G., Pereira, I. and Zaldúa, N. (2012): Neighborhood lichens of Uruguayan Antartic Scientific Station, Collins Bay, King George Island, Antarctica. Polibotánica, 33: 105-116.
Puhovkin, A., Hájek, J., Giordano, D., Sekerák, J. and Barták, M. (2023): Cryoresistance differences between species of autotrops from polar regions sensed by chlorophyll fluorescence. Problems of Cryobiology and Cryomedicine, 33(1): 025-037. doi: 10.15407/cryo33.01.025
Rodriguez, J. M., Passo, A. and Chiapella, J. O. (2018): Lichen species assemblage gradient in South Shetlands Islands, Antarctica: Relationship to deglaciation and microsite conditions. Polar Biology, 41: 2523-2531. doi: 10.1007/s00300-018-2388-0
Šabacká, M., Elster, J. (2006): Response of cyanobacteria and algae from Antarctic Wetland habitats to freezing and desiccation stress. Polar Biology, 30(1): 31-37. doi: 10.1007/s00300-006-0156-z
Sancho, L. G., de los Ríos, A., Pintado, A. I., Colesie, C., Raggio, J., Ascaso, C. and Green, A. T. (2020): Himantormia lugubris, an Antarctic endemic on the edge of the lichen symbiosis. Symbiosis, 82: 49-58. doi: 10.1007/s13199-020-00723-7
Smykla, J., Szarek-Gwiazda, E. and Krzewicka, B. (2005): Trace elements in the lichens Usnea aurantiaco-atra and Usnea antarctica from the vicinity of Uruguay’s Artigas research station on King George Island maritime Antarctic. Polish Botanical Studies, 19: 49-57.
Sojo, F., Romeike, J. and Ott, S. (2003): Himantormia lugubris (Hue) M. Lamb – vegetative and reproductive habit: Adaptations of an Antarctic endemic. Flora, 198: 118-126.
Trumhová, K., Holzinger, A., Obwegeser, S., Neuner, G. and Pichrtová, M. (2019): The conjugating green alga Zygnema sp. (Zygnematophyceae) from the Arctic shows high frost tolerance in mature cells (pre-akinetes). Protoplasma, 256: 1681-1694. doi: 10.1007/s00709-019-01404-z
Copyright © 2023 Josef Hájek, Angélica Casanova-Katny, Miloš Barták, Jiří Sekerák Jr.