The filamentous microalga Tribonema sp. (Stramenopiles, Xanthophyceae) plays an important role in shallow water polar (streams and seepages) and seasonally cold habitats in temperate regions (ponds). In these habitats, freezing and desiccation, and thus freeze-thawing and drying-rewetting cycles, are frequent. These regions produce visible biomass and are important components of low temperature-adapted communities. We characterized the annual cycles of a Tribonema cf. minus population in two habitats (seepage and stream) in the High Arctic, Svalbard. Seasonality, locality, and their combination (particularly changing environmental conditions) together with cultivation conditions of strains significantly affected their morphological characteristics. Morphological changes following hardening processes related to preparation for the winter period (transition from vegetative cells to akinete and/or pre-akinete) were recorded. Over the year, positive water temperatures (warmest 13.3°C) occurred for 5 months while negative (lowest temperature was -17.4°C) lasted for 7 months. In winter, there were two melt periods. Vitality staining protocol showed a high number of viable (77.4% and 53.8%) and dormant cells (1.7% and 4.1%; capable of growth and reproduction once suitable conditions return) in the winter seepage and stream, respectively. NPQ and OJIP chlorophyll fluorescence parameters revealed several hours recovery of photosynthesis (both field and control samples). During recovery, only minor or mild stress on photosynthesis was detected. FV /FM values (the photosynthetic efficiency of photosystem II in a dark-adapted state) in all field and control samples varied around 0.4. Tribonema cf. minus is capable of surviving winter Arctic conditions (perennial strategy).

Faculty of Science Charles University Viničná 7 12844 Prague 2 Czech Republic

Faculty of Science University of South Bohemia Na Zlaté Stoce 3 370 05 České Budějovice Czech Republic

Institute of Botany Czech Academy of Sciences Dukelská 135 379 82 Třeboň Czech Republic

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Adl, S. M., Simpson, A. G. B., Farmer, M. A., Andersen, R. A., Anderson, O. R., Barta, J. R., Bowser, S. S. et al. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52:399-451.

Aguilera, A., Souza-Egipsy, V., Gomez, F. & Amils, R. 2007. Development and structure of eukaryotic biofilms in an extreme acidic environment, Rio Tinto (SW, Spain). Microb. Ecol. 53:294-305.

Aleksandrova, V. D. 1980. The Arctic and Antarctic: Their division into geobotanical areas. Cambridge University Press, Cambridge, p 860.

Alpert, P. 2005. The limits and frontiers of desiccation-tolerant life. Integr. Comp. Biol. 45:685-95.

Alpert, P. 2006. Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J. Exp. Biol. 209:1575-84.

Arc, E., Pichrtová, M., Kranner, I. & Holzinger, A. 2020. Pre-akinete formation in Zygnema sp. from polar habitats is associated with metabolite re-arrangement. J. Exp. Bot. 71:3314-22.

Ban, A., Aikawa, S., Hattori, H., Sasaki, H., Sampei, M., Kudoh, S., Fukuchi, M., Satoh, K. & Kashino, Y. 2006. Comparative analysis of photosynthetic properties in ice algae and phytoplankton inhabiting Franklin Bay, the Canadian Arctic, with those in mesophilic diatoms during CASES 03-04. Polar Biosci. 19:11-28.

Bidle, K. D. 2016. Programmed cell death in unicellular phytoplankton. Curr. Biol. 26:R594-R607.

Callaghan, T. V., Björn, L. O., Chernov, Y., Chapin, T., Christensen, T. R., Huntley, B., Ims, R. A. et al. 2004a. Biodiversity, distributions and adaptations of Arctic species in the context of environmental change. Ambio 33:404-17.

Callaghan, T. V., Björn, L. O., Chernov, Y., Chapin, T., Christensen, T. R., Huntley, B., Ims, R. A. et al. 2004b. Responses to projected changes in climate and UV-B at the species level. Ambio 33:418-35.

Cooper, E. J. 2014. Warmer shorter winters disrupt Arctic terrestrial ecosystems. Annu. Rev. Ecol. Evol. Syst. 45:271-95.

Cota, G. F. 1985. Photoadaptation of high Arctic ice algae. Nature 315:219-22.

Dallmann, W. K., Ohta, Y., Birjikov, A. S., Karnoušenko, E. P., Sirotkin, A. N. & Piepjohn, K. 1994. Geological map of Svalbard 1:100000, sheet C7G Dicksonfjorden. Norsk Polarinstitut.

Davey, M. C. 1989. The effects of freezing and desiccation on photosynthesis and survival of terrestrial Antarctic algae and cyanobacteria. Polar Biol. 10:29-36.

Davey, M. C. 1991. Effects of physical factors on the survival and growth of antarctic terrestrial algae. Br. Phycol. J. 26:315-25.

Davey, M. C. & Rothery, P. 1992. Factors causing the limitation of growth of terrestrial algae in maritime Antarctica during late summer. Polar Biol. 12:595-601.

Davison, I. R. 1991. Environmental effects on algal photosynthesis: temperature. J. Phycol. 27:2-8.

de los Ríos, A., Ascaso, C., Wierzchos, J., Vincent, W. F. & Quesada, A. 2015. Microstructure and cyanobacterial composition of microbial mats from the High Arctic. Biodivers. Conserv. 24:841-63.

De Vries, P. & Hillebrand, H. 1986. Growth control of Tribonema minus (Wille) Hazen and Spirogyra singularis Nordstedt by light and temperature. Acta Bot. Neerl. 35:65-70.

Elster, J. 1991. Mass Occurrence of Algae and AQUATIC Plants in Biotopes Affected by Human Activity in the Lužnice River Catchment Area. Třeboň biosphere Reserve, Czech Republic. Ph.D., Institute of Botany, Třeboň, 155 pP.

Elster, J. 2002. Ecological classification of terrestrial algal communities in polar environments. In Beyer, L. & Bötler, M. [Eds.] Geoecology of Antarctic Ice-free Coastal Lanscapes. Springer-Verlag, pp 303-26.

Elster, J. & Benson, E. E. 2004. Life in the polar terrestrial environment with a focus on algae and cyanobacteria. In Fuller, B. J., Lane, N. & Benson, E. E. [Eds.] Life in the frozen state. CRC Press, Boca Raton, pp 111-50.

Elster, J., Degma, P., Kováčik, Ľ., Valentová, L., Šramková, K. & Pereira, A. B. 2008. Freezing and desiccation injury resistance in the filamentous green alga Klebsormidium from the Antarctic, Arctic and Slovakia. Biologia 63:843-51.

Elster, J., Komárek, J. & Svoboda, J. 1994. Algal communities of polar wetlands. Scripta Fac. Sci. Nat. Univ. Mas. Brun. 24:13-24.

Elster, J. & Komárek, O. 2003. Ecology of periphyton in a meltwater stream ecosystem in the maritime Antarctica. Antarct. Sci. 15:189-201.

Elster, J., Kvíderová, J., Hájek, T., Láska, K. & Šimek, M. 2012. Impact of warming on Nostoc colonies (Cyanobacteria) in a wet hummock meadow, Spitzbergen. Pol. Pol. Res. 33:395-420.

Elster, J., Svoboda, J. & Kanda, H. 2001. Controlled environmental platform used in temperature manipulation study of a stream periphyton in the Ny-Ålesund, Svalbard. In Elster, J., Seckbach, J., Vincent, W. F. & Lhotský, O. [Eds.] Algae and Extreme Environments. Cramer, Stuttgart, pp 63-75.

Elster, J., Svoboda, J., Komárek, J. & Marvan, P. 1997. Algal and cyanoprokaryote communities in a glacial stream, Sverdrup Pass, 79°N, Central Ellesmere Island, Canada. Algol. Stud. 85:57-93.

Ettl, H. 1978. Xanthophyceae, 1, Teil. ed. Fischer Verlag Stuttgart, New York, p 530.

Falkowski, P. & LaRoche, J. 1991. Acclimation to spectral irradiance in algae. J. Phycol. 27:8-14.

Falkowski, P. & Raven, J. A. 2007. Aquatic photosynthesis, 2nd edn. Princeton University Press, Princeton, p 484.

Fernández-Valiente, E., Camacho, A., Rochera, C., Rico, E., Vincent, W. F. & Quesada, A. 2007. Community structure and physiological characterization of microbial mats in byers peninsula, Livingston Island (South Shetland Islands, Antarctica). FEMS Microbiol. Ecol. 59:377-85.

Flemming, H. C. & Wingender, J. 2010. The biofilm matrix. Nat. Rev. Microbiol. 8:623-33.

Fuller, C. L. 2013. Examining morphological and physiological changes in Zygnema irregulare during a desiccation and recovery period. M.Sc., California State University, San Marcos, p 74.

García-Moyano, A., Austnes, A. E., Lanzén, A., González-Toril, E., Aguilera, Á. & Øvreås, L. 2015. Novel and unexpected microbial diversity in acid mine drainage in Svalbard (78 N), revealed by culture-independent approaches. Microorganisms 3:667-94.

Gorton, H. L., Williams, W. E. & Vogelmann, T. C. 2001. The light environment and cellular optics of the snow alga Chlamydomonas nivalis (Bauer) Wille. Photochem. Photobiol. 73:611-20.

Grant, J. 1986. Sensitivity of benthic community respiration and primary production to changes in temperature and light. Mar. Biol. 90:299-306.

Gudleifsson, B. 1984. Tribonema viride (Xanthophyta) on cultivated grassland during winter and spring. Acta Botanica Islandica 7:27-30.

Hawes, I. 1989. Filamentous green algae in freshwater streams on Signy Island, Antarctica. Hydrobiologia 172:1-18.

Hawes, I. 1990. Effects of freezing and thawing on a species of Zygnema (Chlorophyta) from the Antarctic. Phycologia 29:326-31.

Hawes, I., Howard-Williams, C. & Vincent, W. 1992. Desiccation and recovery of Antarctic cyanobacterial mats. Polar Biol. 12:587-94.

Hawes, I., Sumner, D. Y., Andersen, D. T., Jungblut, A. D. & Mackey, T. J. 2013. Timescales of growth response of microbial mats to environmental change in an ice-covered Antarctic lake. Biology 2:151-76.

Hillebrand, H. 1985. Growth Control of Filamentous Algae by Light and Temperature. Internationale Vereinigung für theoretische und angewandte Limnologie, Verhandlungen 22, p 2878.

Hjelle, A. 1993. The Geology of Svalbard. ed. Norsk Polarinstitutt, Oslo, p 163.

Hudák, J. & Salaj, J. 1999. Effect of low temperatures on the structure of plant cells. In Pessarakli, M. [Ed.] Handbook of Plant and Crop Stress. Marcel Dekker Inc. New York, Basel, pp. 441-64.

Hughes, R. F., Asner, G. P., Mascaro, J., Uowolo, A. & Baldwin, J. 2014. Carbon storage landscapes of lowland Hawaii: the role of native and invasive species through space and time. Ecol. Appl. 24:716-31.

Jones, A., Stolbovay, V., Tarnocai, C., Broll, G., Spaargaren, O. & Montanarella, L. 2010. Soil atlas of the Northern Circumpolar Region. ed. European Commission, Publications Office of the European Union, Luxembourg, p 144.

Karsten, U. & Holzinger, A. 2012. Light, temperature, and desiccation effects on photosynthetic activity, and drought-induced ultrastructural changes in the green alga Klebsormidium dissectum (Streptophyta) from a high alpine soil crust. Microb. Ecol. 63:51-63.

Karsten, U., Pröschold, T., Mikhailyuk, T. & Holzinger, A. 2013. Photosynthetic performance of different genotypes of the green alga Klebsormidium sp. (Streptophyta) isolated from biological soil crusts of the Alps. Algol. Stud. 142:45-62.

Kim, G. H., Klochkova, T. A., Han, J. W., Kang, S. H., Choi, H. G., Chung, K. W. & Kim, S. J. 2011. Freshwater and terrestrial algae from Ny-Ålesund and Blomstrandhalvøya Island (Svalbard). Arctic 64:25-31.

Knutson, T. R., Delworth, T., Dixon, K., Held, I., Lu, J., Ramaswamy, V., Schwarzkopf, M., Stenchikov, G. & Stouffer, R. 2006. Assessment of twentieth-century regional surface temperature trends using the GFDL CM2 coupled models. J. Climate 19:1624-51.

Krammer, K. & Lange-Bertalot, H. 1986. Bacillariophyceae, 1. Teil, Naviculaceae. ed. Gustav Fischer, Verlag, p 876.

Krammer, K. & Lange-Bertalot, H. 1991a. Bacillariophyceae. 3. Teil: Centrales, Fragilariaceae, Eunotiaceae. ed. Spektrum Akademischer Verlag, Heidelberg, p 576.

Krammer, K. & Lange-Bertalot, H. 1991b. Bacillariophyceae. Teil 4. Achnanthaceae, Kritische Erganzungen zu Navicula (Lineolatae) und Gomphonema. ed. Spektrum Akademischer Verlag, Heidleberg, p 436.

Kvernvik, A. C., Hoppe, C. J. M., Lawrenz, E., Prášil, O., Greenacre, M., Wiktor, J. M. & Leu, E. 2018. Fast reactivation of photosynthesis in arctic phytoplankton during the polar night. J. Phycol. 54:461-70.

Kvíderová, J. 2014. Sample database of the Centre for Polar Ecology - Database design and data management. Czech Polar Rep. 4:140-8.

Kvíderová, J. 2018. Internal structure and photosynthetic performance of Nostoc sp. colonies in the high Arctic. Acta Soc. Bot. Pol. 87:3602.

Kvíderová, J., Elster, J. & Iliev, I. 2015. Exploitation of databases in polar research-Data evaluation and outputs. Czech Polar Rep. 5:143-59.

Kvíderová, J., Elster, J. & Komárek, J. 2019. Ecophysiology of cyanobacteria in the Polar Regions. In Mishra, A. K., Tiwari, D. N. & Rai, A. N. [Eds.] Cyanobacteria, From basic Sciences to Applications. Academic Press, London San Diego Cambridge Oxford, pp 277-302.

Lokhorst, G. M. 2003. The genus Tribonema (Xanthophyceae) in the Netherlands. An integrated field and culture study. Nova Hedwigia 77:19-53.

Machová, K., Elster, J. & Adamec, L. 2008. Xanthophyceaen assembleges during winter-spring flood: autecology and ecophysiology Tribonema fonticolum and T. monochloron. Hydrobiologia 600:155-68.

Maistro, S., Broady, P. A., Andreoli, C. & Negrisolo, E. 2007. Molecular phylogeny and evolution of the order Tribonematales (Heterokonta, Xanthophyceae) based on analysis of plastidial genes rbcL and psaA. Mol. Phylogenet. Evol. 43:407-17.

Matuła, J., Pietryka, M., Richter, D. & Wojtun, B. 2007. Cyanoprokaryota and algae of Arctic terrestrial ecosystems in the Horsund area, Spitzbergen. Pol. Pol. Res. 28:283-315.

Maukonen, J., Mattila-Sandholm, T. & Wirtanen, G. 2000. Metabolic indicators for assessing bacterial viability in hygiene sampling using cells in suspension and swabbed biofilm. LWT-Food Sci. Technol. 33:225-33.

Miller, Gh, Brigham-Grette, J., Alley, Rb, Anderson, L., Bauch, Ha, Douglas, Msv, Edwards, Me et al. 2010. Temperature and precipitation history of the Arctic. Quat. Sci. Rev. 29:1679-715.

Nagao, M., Arakawa, K., Takezawa, D., Yoshida, S. & Fujikawa, S. 1999. Akinete formation in Tribonema bombycinum Derbes et Solier (Xanthophyceae) in relation to freezing tolerance. J. Plant Res. 112:163-74.

Nichols, H. 1992. New algae from prairie soils. I. The genus Tribonema Derbes et Solier (Xanthophyceae, Tribonematales, Tribonemataceae). Phytomorphology 42:15-33.

Nishida, I. & Murata, N. 1996. Chilling sensitivity in plants and cyanobacteria. Ann. Rev. Plant Physiol. Plant Mol. Biol. 47:541-68.

Norwegian Polar Institute. 2014. Kartdata Svalbard 1:100 000 (S100 Kartdata)/Map Data. Norwegian Polar Institute. https://doi.org/10.21334/npolar.2014.645336c7.

Oxborough, K. & Baker, N. R. 1997. Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components-calculation of qP and Fv-/Fm-; without measuring Fo. Photosynth. Res. 54:135-42.

Pascher, A. 1939. Heterokonten. ed. Akademische Verlagsgesselschaft MBH, Leipzig, p 1092.

Pichrtová, M., Arc, E., Stöggl, W., Kranner, I., Hájek, T., Hackl, H. & Holzinger, A. 2016. Formation of lipid bodies and changes in fatty acid composition upon pre-akinete formation in Arctic and Antarctic Zygnema (Zygnematophyceae, Streptophyta) strains. FEMS Microbiol. Ecol. 92:fiw096.

Pichrtová, M., Hájek, T. & Elster, J. 2014a. Osmotic stress and recovery in field populations of Zygnema sp. (Zygnematophyceae, Streptophyta) on Svalbard (High Arctic) subjected to natural desiccation. FEMS Microbiol. Ecol. 89:270-80.

Pichrtová, M., Kulichová, J. & Holzinger, A. 2014b. Nitrogen limitation and slow drying induce desiccation tolerance in conjugating green algae (Zygnematophyceae, Streptophyta) from polar habitats. PLoS ONE 9:e113137.

Przybylak, R. 2000. Temporal and spatial variation of surface air temperature over the period of instrumental observations in the Arctic. Int. J. Climatol. 20:587-614.

Rippin, M., Pichrtová, M., Arc, E., Kranner, I., Becker, B. & Holzinger, A. 2019. Metatranscriptomic and metabolite profiling reveals vertical heterogeneity within a Zygnema green algal mat from Svalbard (High Arctic). Environ. Microbiol. 21:4283-99.

Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M. & Stanier, R. Y. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111:1-61.

Rivkin, R. B. & Putt, M. 1987. Photosynthesis and cell division by Antarctic microalgae: comparison of benthic, plamktonic and ice algae. J. Phycol. 23:223-9.

Rochera, C., Villaescusa, J. A., Velázquez, D., Fernández-Valiente, E., Quesada, A. & Camacho, A. 2013. Vertical structure of bi-layered microbial mats from Byers Peninsula, Maritime Antarctica. Antarct. Sci. 25:270.

Roháček, K., Soukupová, J. & Barták, M. 2008. Chlorophyll fluorescence: a wonderful tool to study plant physiology and plant stress. In Schoefs, B. [Ed.] Plant Cell Compartments-Selected Topics. Research Signpost, Kerala, India, pp. 41-104.

Rubensdotter, L., Christiansen, H., Farnsworth, W. & Romundset, A. 2015. Landforms and sediments in Bjørndalen-Vestpynten, Svalbard. Quaternary geological map 1: 10,000. Geological survey of Norway.

Rybalka, N., Andersen, R. A., Kostikov, I., Mohr, K. I., Massalski, A., Olech, M. & Friedl, T. 2009. Testing for endemism, genotypic diversity and species concepts in Antarctic terrestrial microalgae of the Tribonemataceae (Stramenopiles, Xanthophyceae). Environ. Microbiol. 11:554-65.

Šabacká, M. & Elster, J. 2006. Response of cyanobacteria and algae from Antarctic wetland habitats to freezing and desiccation stress. Polar Biol. 30:31-7.

Shukla, S. P., Kvíderová, J., Adamec, L. & Elster, J. 2020. Ecophysiological features of polar soil unicellular microalgae. J. Phycol. 56:481-95.

Skulberg, O. M. 1996. Terrestrial and limnic algae and cyanobacteria. In Elvebakk, A. & Prestrud, P. [Eds.] A Catalogue of Svalbard Plants, Fungi, Algae and Cyanobacteria, Norsk Polarinstitutt, Skrifter, pp 383-95.

Stibal, M. & Elster, J. 2005. Growth and morphology variation as a response to changing environmental factors in two Arctic species Raphidonema (Trebouxiophyceae) from snow and soil. Polar Biol. 28:558-67.

Strasser, R. J., Tsimilli-Michael, M. & Srivastava, A. 2004. Analysis of the chlorophyll a fluorescence transient. In Papageorgiou, G. C. & Govindjee [Eds.] Chlorophyll a Fluorescence: A Signature of Photosynthesis. Springer, Dordrecht, pp 321-62.

Tashyreva, D. & Elster, J. 2015. Effect of nitrogen starvation on desiccation tolerance of Arctic Microcoleus strains (cyanobacteria). Front. Microbiol. 6:278.

Tashyreva, D. & Elster, J. 2016. Annual cycles of two cyanobacterial mat communities in hydro-terrestrial habitats of the High Arctic. Microb. Ecol. 71:887-900.

Tashyreva, D., Elster, J. & Billi, D. 2013. A novel staining protocol for multiparameter assessment of cell heterogeneity in Phormidium populations (Cyanobacteria) employing fluorescent dyes. PLoS ONE 8:e55283.

Vincent, W. F. 2000. Cyanobacterial dominance in the Polar Regions. In Whitton, B. A. & Potts, M. [Eds.] The ecology of cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp 321-40.

Vincent, W. F., Downes, M. T., Castenholz, R. W. & Howard-Williams, C. 1993. Community structure and pigment organisation of cyanobacteria-dominated microbial mats in Antarctica. Eur. J. Phycol. 28:213-21.

Zuccarello, G. C. & Lokhorst, G. M. 2005. Molecular phylogeny of the genus Tribonema (Xanthophyceae) using rbcL gene sequence data: monophyly of morphologically simple algal species. Phycologia 44:384-92.

Seasonal Dynamics of Zygnema (Zygnematophyceae) Mats from the Austrian Alps