Diatoms are among the most important primary producers in alpine and polar freshwaters. Although temperate diatoms are sensitive to freezing, polar diatoms often exhibit more resistance. This is particularly true for members of the (predominantly terrestrial) Pinnularia borealis species complex. However, it remains unclear to what extent this resistance applies to other representatives of the genus. Here, we compare the freezing-stress tolerance of 11 freshwater, benthic strains representing different species of Pinnularia (including Caloneis) from polar, alpine, and temperate habitats. As vegetative cells, strains were exposed to freezing temperatures of -4, -10, -20, -40, -80, and -196°C. Survival was assessed by light microscopy and photosynthetic measurements. We observed vegetative cells to be sensitive to low freezing temperatures; only "mild" freezing was survived by all tested strains, and most tested strains did not survive treatments ≤-10°C. However, individual strain sensitivities appeared related to their original habitats. For example, polar and alpine strains better withstood "mild" and "moderate" freezing (-4 and -10°C, respectively); although temperate strains were significantly affected by the "mild" freezing treatment, polar and alpine strains were not. The -10°C treatment was survived exclusively by polar strains, and only P. catenaborealis survived all treatments. Interestingly, this species exhibited the lowest survival in the -10°C treatment, potentially implying some metabolic activity even at freezing temperatures. Thus, despite more extensive sampling throughout the genus and finer temperature scaling compared to previous studies, the remarkable freezing-stress tolerance of the P. borealis species complex remains unique within the genus.

Department of Ecology Faculty of Science Charles University Prague Czech Republic

Department of Phycology Institute of Botany Czech Academy of Sciences Třeboň Czech Republic

Zobrazit více v PubMed

Adl, S. M., Simpson, A. G. B., Lane, C. E., Lukeš, J., Bass, D., Bowser, S. S., Brown, M. W., Burki, F., Dunthorn, M., Hampl, V., Heiss, A., Hoppenrath, M., Lara, E., Le Gall, L., Lynn, D. H., McManus, H., Mitchell, E. A. D., Mozley‐Stanridge, S. E., Parfrey, L. W., … Spiegel, F. W. (2012). The revised classification of eukaryotes. Journal of Eukaryotic Microbiology, 59(5), 429–514. https://doi.org/10.1111/j.1550‐7408.2012.00644.x

Agustí, S., Krause, J. W., Marquez, I. A., Wassmann, P., Kristiansen, S., & Duarte, C. M. (2020). Arctic (Svalbard islands) active and exported diatom stocks and cell health status. Biogeosciences, 17(1), 35–45. https://doi.org/10.5194/bg‐17‐35‐2020

Antoniades, D., & Douglas, M. S. V. (2002). Characterization of high arctic stream diatom assemblages from Cornwallis Island, Nunavut, Canada. Canadian Journal of Botany, 80(1), 50–58. https://doi.org/10.1139/b01‐133

Aslam, S. N., Cresswell‐Maynard, T., Thomas, D. N., & Underwood, G. J. C. (2012). Production and characterization of the intra‐ and extracellular carbohydrates and polymeric substances (EPS) of three sea‐ice diatom species, and evidence for a cryoprotective role for EPS. Journal of Phycology, 48(6), 1494–1509. https://doi.org/10.1111/jpy.12004

Billi, D., & Caiola, M. G. (1996). Effects of nitrogen limitation and starvation on Chroococcidiopsis sp. (Chroococcales). New Phytologist, 133(4), 563–571. https://doi.org/10.1111/j.1469‐8137.1996.tb01925.x

Cantonati, M., Corradini, G., Jüttner, I., & Cox, E. J. (2001). Diatom assemblages in high mountain streams of the Alps and the Himalaya. Nova Hedwigia, 123(1), 37–61.

Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17(4), 240–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334

Consalvey, M., Perkins, R. G., Paterson, D. M., & Underwood, G. J. C. (2005). PAM fluorescence: A beginners guide for benthic diatomists. Diatom Research, 20(1), 1–22. https://doi.org/10.1080/0269249X.2005.9705619

Cremer, H., Gore, D., Hultzsch, N., Melles, M., & Wagner, B. (2004). The diatom flora and limnology of lakes in the Amery Oasis, East Antarctica. Polar Biology, 27(9), 513–531. https://doi.org/10.1007/s00300‐004‐0624‐2

Davey, M. C. (1989). The effects of freezing and desiccation on photosynthesis and survival of terrestrial Antarctic algae and cyanobacteria. Polar Biology, 10(1), 29–36. https://doi.org/10.1007/BF00238287

Davey, M. C. (1991). Effects of physical factors on the survival and growth of Antarctic terrestrial algae. British Phycological Journal, 26(4), 315–325. https://doi.org/10.1080/00071619100650281

Dawson, H. M., Heal, K. R., Torstensson, A., Carlson, L. T., Ingalls, A. E., & Young, J. N. (2020). Large diversity in nitrogen‐ and sulfur‐containing compatible solute profiles in polar and temperate diatoms. Integrative and Comparative Biology, 60(6), 1401–1413. https://doi.org/10.1093/icb/icaa133

De Wever, A., Leliaert, F., Verleyen, E., Vanormelingen, P., Van Der Gucht, K., Hodgson, D. A., Sabbe, K., & Vyverman, W. (2009). Hidden levels of phylodiversity in Antarctic green algae: Further evidence for the existence of glacial refugia. Proceedings of the Royal Society B: Biological Sciences, 276(1673), 3591–3599. https://doi.org/10.1098/rspb.2009.0994

Duff, R. J., Ball, H., & Lavrentyev, P. J. (2008). Application of combined morphological‐molecular approaches to the identification of planktonic protists from environmental samples. Journal of Eukaryotic Microbiology, 55(4), 306–312. https://doi.org/10.1111/j.1550‐7408.2008.00328.x

Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with improved accuracy and speed. Proceedings. 2004 IEEE Computational Systems Bioinformatics Conference, 2004. CSB 2004., Csb, 689–690. https://doi.org/10.1109/CSB.2004.1332560

Elberling, B. (2007). Annual soil CO2 effluxes in the high Arctic: The role of snow thickness and vegetation type. Soil Biology and Biochemistry, 39(2), 646–654. https://doi.org/10.1016/j.soilbio.2006.09.017

Elster, J., Degma, P., Kováčik, L., Valentová, L., Šramková, K., & Batista Pereira, A. (2008). Freezing and desiccation injury resistance in the filamentous green alga Klebsormidium from the Antarctic, Arctic and Slovakia. Biologia, 63(6), 843–851. https://doi.org/10.2478/s11756‐008‐0111‐2

Guillard, R. R. L., & Lorenzen, C. J. (1972). Yellow‐green algae with chlorophyllide c. Journal of Phycology, 8(1), 10–14. https://doi.org/10.1111/j.1529‐8817.1972.tb03995.x

Hall, T. A. (1999). BioEdit: A user‐friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

Hamsher, S. E., Evans, K. M., Mann, D. G., Poulíčková, A., & Saunders, G. W. (2011). Barcoding diatoms: Exploring alternatives to COI‐5P. Protist, 162(3), 405–422. https://doi.org/10.1016/j.protis.2010.09.005

Hawes, I. (1990). Effects of freezing and thawing on a species of Zygnema (Chlorophyta) from the Antarctic. Phycologia, 29(3), 326–331. https://doi.org/10.2216/i0031‐8884‐29‐3‐326.1

Hawes, I., Howard‐Williams, C., & Vincent, W. F. (1992). Desiccation and recovery of antarctic cyanobacterial mats. Polar Biology, 12(6–7), 587–594. https://doi.org/10.1007/BF00236981

Hejduková, E., Elster, J., & Nedbalová, L. (2020). Annual cycle of freshwater diatoms in the high Arctic revealed by multiparameter fluorescent staining. Microbial Ecology, 80(3), 559–572. https://doi.org/10.1007/s00248‐020‐01521‐w

Hejduková, E., & Nedbalová, L. (2021). Experimental freezing of freshwater pennate diatoms from polar habitats. Protoplasma, 258(6), 1213–1229. https://doi.org/10.1007/s00709‐021‐01648‐8

Hejduková, E., Pinseel, E., Vanormelingen, P., Nedbalová, L., Elster, J., Vyverman, W., & Sabbe, K. (2019). Tolerance of pennate diatoms (Bacillariophyceae) to experimental freezing: Comparison of polar and temperate strains. Phycologia, 58(4), 382–392. https://doi.org/10.1080/00318884.2019.1591835

Izaguirre, I., Allende, L., & Romina Schiaffino, M. (2021). Phytoplankton in Antarctic lakes: Biodiversity and main ecological features. Hydrobiologia, 848(1), 177–207. https://doi.org/10.1007/s10750‐020‐04306‐x

Jones, H. M., Simpson, G. E., Stickle, A. J., & Mann, D. G. (2005). Life history and systematics of Petroneis (Bacillariophyta), with special reference to British waters. European Journal of Phycology, 40(1), 61–87. https://doi.org/10.1080/09670260400024675

Jones, V. J. (1996). The diversity, distribution and ecology of diatoms from Antarctic inland waters. Biodiversity and Conservation, 5(11), 1433–1449. https://doi.org/10.1007/BF00051986

Julius, M. L., & Theriot, E. C. (2010). The diatoms: A primer. In J. Smol & E. Stoermer (Eds.), The diatoms: Applications for the environmental and earth sciences (pp. 8–22). Cambridge University Press. https://doi.org/10.1017/CBO9780511763175.003

Kappen, L., Schroeter, B., Scheidegger, C., Sommerkorn, M., & Hestmark, G. (1996). Cold resistance and metabolic activity of lichens below 0°C. Advances in Space Research, 18(12), 119–128. https://doi.org/10.1016/0273‐1177(96)00007‐5

Karlsson, J. O. M., & Toner, M. (1996). Long‐term storage of tissues by cryopreservation: Critical issues. Biomaterials, 17(3), 243–256. https://doi.org/10.1016/0142‐9612(96)85562‐1

Karsten, U., Schumann, R., & Holzinger, A. (2019). Ecophysiology, cell biology and ultrastructure of a benthic diatom isolated in the Arctic. In J. Seckbach & R. Gordon (Eds.), Diatoms: Fundamentals and applications (pp. 273–287). Scrivener Publishing. https://doi.org/10.1002/9781119370741.ch12

Kollár, J., Kopalová, K., Kavan, J., Vrbická, K., Nývlt, D., Nedbalová, L., Stibal, M., & Kohler, T. J. (2023). Recently formed Antarctic lakes host less diverse benthic bacterial and diatom communities than their older counterparts. FEMS Microbiology Ecology, 99(9), fiad087. https://doi.org/10.1093/femsec/fiad087

Kopalová, K., Kociolek, J. P., Lowe, R. L., Zidarova, R., & Van de Vijver, B. (2015). Five new species of the genus Humidophila (Bacillariophyta) from the maritime Antarctic region. Diatom Research, 30(2), 117–131. https://doi.org/10.1080/0269249X.2014.998714

Krammer, K. (1992). Pinnularia: Eine Monographie der europäischen Taxa [Pinnularia: A monograph of the European taxa]. Bibliotheca Diatomologica.

Krammer, K. (2000). Diatoms of Europe, Volume 1: The genus Pinnularia. A.R.G. Gantner Verlag K.G.

Kuwata, A., Hama, T., & Takahashi, M. (1993). Ecophysiological characterization of two life forms, resting spores and resting cells, of a marine planktonic diatom, Chaetoceros pseudocurvisetus, formed under nutrient depletion. Marine Ecology Progress Series, 102(3), 245–256. https://doi.org/10.3354/meps102245

Kuwata, A., & Takahashi, M. (1999). Survival and recovery of resting spores and resting cells of the marine planktonic diatom Chaetoceros pseudocurvisetus under fluctuating nitrate conditions. Marine Biology, 134(3), 471–478. https://doi.org/10.1007/s002270050563

Lee, R. E. (2008). Heterokontophyta, Bacillariophyceae. In R. E. Lee (Ed.), Phycology (pp. 369–408). Cambridge University Press.

Lyon, B. R., Bennett‐Mintz, J. M., Lee, P. A., Janech, M. G., & Ditullio, G. R. (2016). Role of dimethylsulfoniopropionate as an osmoprotectant following gradual salinity shifts in the sea‐ice diatom Fragilariopsis cylindrus. Environmental Chemistry, 13(2), 181–194. https://doi.org/10.1071/EN14269

Mann, D. G. (1999). The species concept in diatoms. Phycologia, 38(6), 437–495. https://doi.org/10.2216/i0031‐8884‐38‐6‐437.1

Maxwell, K., & Johnson, G. N. (2000). Chlorophyll fluorescence – A practical guide. Journal of Experimental Botany, 51(345), 659–668. https://doi.org/10.1093/jexbot/51.345.659

McQuoid, M. R., & Hobson, L. A. (1996). Diatom resting stages. Journal of Phycology, 32(6), 889–902. https://doi.org/10.1111/j.0022‐3646.1996.00889.x

Meryman, H. T. (1974). Freezing injury and its prevention in living cells. Annual Review of Biophysics and Bioengineering, 3, 341–363. https://doi.org/10.1146/annurev.bb.03.060174.002013

Mock, T., & Valentin, K. (2004). Photosynthesis and cold acclimation: Molecular evidence from a polar diatom. Journal of Phycology, 40(4), 732–741. https://doi.org/10.1111/j.1529‐8817.2004.03224.x

Muldrew, K., & McGann, L. E. (1990). Mechanisms of intracellular ice formation. Biophysical Journal, 57(3), 525–532. https://doi.org/10.1016/S0006‐3495(90)82568‐6

Patterson, T., & Kelso, N. V. (2023). Natural earth. Free Vector and Raster Map Data. https://www.naturalearthdata.com

Peters, E. (1996). Prolonged darkness and diatom mortality: II. Marine temperate species. Journal of Experimental Marine Biology and Ecology, 207(1–2), 43–58. https://doi.org/10.1016/0022‐0981(95)02519‐7

Peters, E., & Thomas, D. N. (1996). Prolonged darkness and diatom mortality I: Marine Antarctic species. Journal of Experimental Marine Biology and Ecology, 207(1–2), 25–41. https://doi.org/10.1016/S0022‐0981(96)02520‐8

Pichrtová, M., Hájek, T., & Elster, J. (2014). Osmotic stress and recovery in field populations of Zygnema sp. (Zygnematophyceae, Streptophyta) on Svalbard (High Arctic) subjected to natural desiccation. FEMS Microbiology Ecology, 89(2), 270–280. https://doi.org/10.1111/1574‐6941.12288

Pichrtová, M., Hájek, T., & Elster, J. (2016). Annual development of mat‐forming conjugating green algae Zygnema spp. in hydro‐terrestrial habitats in the Arctic. Polar Biology, 39(9), 1653–1662. https://doi.org/10.1007/s00300‐016‐1889‐y

Pichrtová, M., Kulichová, J., & Holzinger, A. (2014). Nitrogen limitation and slow drying induce desiccation tolerance in conjugating green algae (Zygnematophyceae, Streptophyta) from polar habitats. PLoS ONE, 9(11), e113137. https://doi.org/10.1371/journal.pone.0113137

Pinseel, E., Hejduková, E., Vanormelingen, P., Kopalová, K., Vyverman, W., & Van De Vijver, B. (2017). Pinnularia catenaborealis sp. nov. (Bacillariophyceae), a unique chain‐forming diatom species from James Ross Island and Vega Island (maritime Antarctica). Phycologia, 56(1), 94–107. https://doi.org/10.2216/16‐18.1

Pinseel, E., Janssens, S. B., Verleyen, E., Vanormelingen, P., Kohler, T. J., Biersma, E. M., Sabbe, K., Van de Vijver, B., & Vyverman, W. (2020). Global radiation in a rare biosphere soil diatom. Nature Communications, 11(2382), 1–12. https://doi.org/10.1038/s41467‐020‐16181‐0

Pla‐Rabés, S., Hamilton, P. B., Ballesteros, E., Gavrilo, M., Friedlander, A. M., & Sala, E. (2016). The structure and diversity of freshwater diatom assemblages from Franz Josef Land archipelago: A northern outpost for freshwater diatoms. PeerJ, 2016(2), 1–22. https://doi.org/10.7717/peerj.1705

Remias, D., Procházková, L., Holzinger, A., & Nedbalová, L. (2018). Ecology, cytology and phylogeny of the snow alga Scotiella cryophila K‐1 (Chlamydomonadales, Chlorophyta) from the Austrian Alps. Phycologia, 57(5), 581–592. https://doi.org/10.2216/18‐45.1

Rimet, F., Gusev, E., Kahlert, M., Kelly, M. G., Kulikovskiy, M., Maltsev, Y., Mann, D. G., Pfannkuchen, M., Trobajo, R., Vasselon, V., Zimmermann, J., & Bouchez, A. (2019). Diat.Barcode, an open‐access curated barcode library for diatoms. Scientific Reports, 9(1), 15116. https://doi.org/10.1038/s41598‐019‐51500‐6

Round, F. E., Crawford, R. M., & Mann, D. G. (1990). Biology of diatoms. In F. E. Round, R. M. Crawford, & D. G. Mann (Eds.), Diatoms: Biology and morphology of the genera (pp. 1–130). Cambridge University Press.

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. https://doi.org/10.1007/s00300‐006‐0156‐z

Schmidt, S., Moskal, W., De Mora, S. J., Howard‐Williams, C., & Vincent, W. F. (1991). Limnological properties of Antarctic ponds during winter freezing. Antarctic Science, 3(4), 379–388. https://doi.org/10.1017/S0954102091000482

Scholz, B., & Liebezeit, G. (2013). Compatible solutes and fatty acid composition of five marine intertidal microphytobenthic Wadden Sea diatoms exposed to different temperature regimes. Diatom Research, 28(4), 337–358. https://doi.org/10.1080/0269249X.2013.802997

Smayda, T. J., & Mitchell‐Innes, B. (1974). Dark survival of autotrophic, planktonic marine diatoms. Marine Biology, 25(3), 195–202. https://doi.org/10.1007/BF00394965

Souffreau, C., Vanormelingen, P., Sabbe, K., & Vyverman, W. (2013). Tolerance of resting cells of freshwater and terrestrial benthic diatoms to experimental desiccation and freezing is habitat‐dependent. Phycologia, 52(3), 14–24. https://doi.org/10.2216/12‐087.1

Souffreau, C., Vanormelingen, P., Verleyen, E., Sabbe, K., & Vyverman, W. (2010). Tolerance of benthic diatoms from temperate aquatic and terrestrial habitats to experimental desiccation and temperature stress. Phycologia, 49(4), 309–324. https://doi.org/10.2216/09‐30.1

Souffreau, C., Verbruggen, H., Wolfe, A. P., Vanormelingen, P., Siver, P. A., Cox, E. J., Mann, D. G., Van De Vijver, B., Sabbe, K., & Vyverman, W. (2011). A time‐calibrated multi‐gene phylogeny of the diatom genus Pinnularia. Molecular Phylogenetics and Evolution, 61(3), 866–879. https://doi.org/10.1016/j.ympev.2011.08.031

Stock, W., Pinseel, E., De Decker, S., Sefbom, J., Blommaert, L., Chepurnova, O., Sabbe, K., & Vyverman, W. (2018). Expanding the toolbox for cryopreservation of marine and freshwater diatoms. Scientific Reports, 8(1), 4279. https://doi.org/10.1038/s41598‐018‐22460‐0

Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022–3027. https://doi.org/10.1093/molbev/msab120

Tashyreva, D., & Elster, J. (2015). Effect of nitrogen starvation on desiccation tolerance of Arctic Microcoleus strains (cyanobacteria). Frontiers in Microbiology, 6, 1–11. https://doi.org/10.3389/fmicb.2015.00278

Tashyreva, D., & Elster, J. (2016). Annual cycles of two cyanobacterial mat communities in hydro‐terrestrial habitats of the high Arctic. Microbial Ecology, 71(4), 887–900. https://doi.org/10.1007/s00248‐016‐0732‐x

Thomas, D. N., Fogg, G. E., Convey, P., Fritsen, C. H., Gili, J.‐M., Gradinger, R., Laybourn‐Parry, J., Reid, K., & Walton, D. W. H. (2008). Stress, adaptation, and survival in polar regions. In D. N. Thomas, G. E. Fogg, P. Convey, C. H. Fritsen, J.‐M. Gili, R. Gradinger, J. Laybourn‐Parry, K. Reid, & D. W. H. Walton (Eds.), The biology of polar regions (pp. 28–52). Oxford University Press. https://doi.org/10.1093/acprof:oso/9780199298112.003.0002

Trumhová, K., Holzinger, A., Obwegeser, S., Neuner, G., & Pichrtová, M. (2019). The conjugating green alga Zygnema sp. (Zygnematophyceae) from the Arctic shows high frost tolerance in mature cells (pre‐akinetes). Protoplasma, 256(6), 1681–1694. https://doi.org/10.1007/s00709‐019‐01404‐z

Váczi, P., Barták, M., Nedbalová, L., & Elster, J. (2011). Comparative analysis of temperature courses in Antarctic lakes of different morphology: Study from James Ross Island, Antarctica. Czech Polar Reports, 1(2), 78–87. https://doi.org/10.5817/cpr2011‐2‐7

Váczi, P., & Hájek, J. (2013). Annual water temperature courses in two contrasting lakes at James Ross Island, Antarctica. Czech Polar Reports, 3(2), 213–219. https://doi.org/10.5817/cpr2013‐2‐22

Van de Vijver, B., Gremmen, N. J. M., & Beyens, L. (2005). The genus Stauroneis (Bacillariophyceae) in the Antarctic region. Journal of Biogeography, 32(10), 1791–1798. https://doi.org/10.1111/j.1365‐2699.2005.01325.x

Van Kooten, O., & Snel, J. F. H. (1990). The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research, 25(7), 147–150. https://doi.org/10.1007/BF00033156

Vanormelingen, P., Verleyen, E., & Vyverman, W. (2008). The diversity and distribution of diatoms: From cosmopolitanism to narrow endemism. Biodiversity and Conservation, 17(2), 393–405. https://doi.org/10.1007/s10531‐007‐9257‐4

Vasselon, V., Rimet, F., Tapolczai, K., & Bouchez, A. (2017). Assessing ecological status with diatoms DNA metabarcoding: Scaling‐up on a WFD monitoring network (Mayotte Island, France). Ecological Indicators, 82, 1–12. https://doi.org/10.1016/j.ecolind.2017.06.024

Verleyen, E., Van de Vijver, B., Tytgat, B., Pinseel, E., Hodgson, D. A., Kopalová, K., Chown, S. L., Van Ranst, E., Imura, S., Kudoh, S., Van Nieuwenhuyze, W., Sabbe, K., & Vyverman, W. (2021). Diatoms define a novel freshwater biogeography of the Antarctic. Ecography, 44(4), 548–560. https://doi.org/10.1111/ecog.05374

Veselá, J., Urbánková, P., Černá, K., & Neustupa, J. (2012). Ecological variation within traditional diatom morphospecies: Diversity of Frustulia rhomboides sensu lato (Bacillariophyceae) in European freshwater habitats. Phycologia, 51(5), 552–561. https://doi.org/10.2216/11‐101.1

Veuger, B., & van Oevelen, D. (2011). Long‐term pigment dynamics and diatom survival in dark sediment. Limnology and Oceanography, 56(3), 1065–1074. https://doi.org/10.4319/lo.2011.56.3.1065

Vyverman, W., Verleyen, E., Wilmotte, A., Hodgson, D. A., Willems, A., Peeters, K., Van de Vijver, B., De Wever, A., Leliaert, F., & Sabbe, K. (2010). Evidence for widespread endemism among Antarctic micro‐organisms. Polar Science, 4(2), 103–113. https://doi.org/10.1016/j.polar.2010.03.006

Wilhelm, C., Büchel, C., Fisahn, J., Goss, R., Jakob, T., LaRoche, J., Lavaud, J., Lohr, M., Riebesell, U., Stehfest, K., Valentin, K., & Kroth, P. G. (2006). The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist, 157(2), 91–124. https://doi.org/10.1016/j.protis.2006.02.003

Wittek, B., Carnat, G., Tison, J. L., & Gypens, N. (2020). Response of dimethylsulfoniopropionate (DMSP) and dimethylsulfoxide (DMSO) cell quotas to salinity and temperature shifts in the sea‐ice diatom Fragilariopsis cylindrus. Polar Biology, 43(5), 483–494. https://doi.org/10.1007/s00300‐020‐02651‐0

Yoshida, K., Seger, A., Kennedy, F., McMinn, A., & Suzuki, K. (2020). Freezing, melting, and light stress on the photophysiology of ice algae: Ex situ incubation of the ice algal diatom Fragilariopsis cylindrus (Bacillariophyceae) using an ice tank. Journal of Phycology, 56(5), 1323–1338. https://doi.org/10.1111/jpy.13036

Zhang, Q., Gradinger, R., & Spindler, M. (1998). Dark survival of marine microalgae in the high Arctic (Greenland Sea). Polarforschung, 65(3), 111–116. https://doi.org/10.2312/polarforschung.65.3.111

Summer and autumn photosynthetic activity in High Arctic biological soil crusts and their winter recovery