Melting mountainous snowfields are populated by extremophilic microorganisms. An alga causing orange snow above timberline in the High Tatra Mountains (Poland) was characterised using multiple methods examining its ultrastructure, genetics, life cycle, photosynthesis and ecophysiology. Based on light and electron microscopy and ITS2 rDNA, the species was identified as Chloromonas krienitzii (Chlorophyceae). Recently, the taxon was described from Japan. However, cellular adaptations to its harsh environment and details about the life cycle were so far unknown. In this study, the snow surface population consisted of egg-shaped cysts containing large numbers of lipid bodies filled presumably with the secondary carotenoid astaxanthin. The outer, spiked cell wall was shed during cell maturation. Before this developmental step, the cysts resembled a different snow alga, Chloromonas brevispina. The remaining, long-lasting smooth cell wall showed a striking UV-induced blue autofluorescence, indicating the presence of short wavelengths absorbing, protective compounds, potentially sporopollenin containing polyphenolic components. Applying a chlorophyll fluorescence assay on intact cells, a significant UV-A and UV-B screening capability of about 30 and 50%, respectively, was measured. Moreover, intracellular secondary carotenoids were responsible for a reduction of blue-green light absorbed by chloroplasts by about 50%. These results revealed the high capacity of cysts to reduce the impact of harmful UV and high visible irradiation to the chloroplast and nucleus when exposed at alpine snow surfaces during melting. Consistently, the observed photosynthetic performance of photosystem II (evaluated by fluorometry) showed no decline up to 2100 μmol photons m-2 s-1. Cysts accumulated high contents of polyunsaturated fatty acids (about 60% of fatty acids), which are advantageous at low temperatures. In the course of this study, C. krienitzii was found also in Slovakia, Italy, Greece and the United States, indicating a widespread distribution in the Northern Hemisphere.

Botanical Institute Christian Albrechts University Kiel Kiel Germany

Faculty of Science Charles University Prague Czechia

Institute of Microbiology The Czech Academy of Sciences Prague Czechia

School of Engineering University of Applied Sciences Upper Austria Wels Austria

Zobrazit více v PubMed

Bilger W., Veit M., Schreiber L., Schreiber U. (1997). Measurement of leaf epidermal transmittance of UV radiation by chlorophyll fluorescence. Physiol. Plant. 101 754–763. 10.1034/j.1399-3054.1997.1010411.x PubMed DOI

Bischoff H. W., Bold H. C. (1963). Phycological Studies. IV. Some Soil Algae from Enchanted Rock and Related Algal Species. Austin, TX: University of Texas.

Bligh E. G., Dyer W. J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Phys. 37 911–917. PubMed

Brown S. P., Tucker A. E. (2020). Distribution and biogeography of Sanguina snow algae: fine-scale sequence analyses reveal previously unknown population structure. Ecol. Evol. 10 11352–11361. 10.1017/CBO9781107415324.004 PubMed DOI PMC

Cepák V., Lukavský J. (2012). Cryoseston in the Sierra Nevada Mountains (Spain). Nova Hedwigia 94 163–173. 10.1127/0029-5035/2012/0094-0163 DOI

Chodat R. (1921). Algues de la région du Grand St. Bernard. Bull. Soc. Bot. Genève 2 293–305.

Dembitsky V. M., Rezanka T., Rozentsvet O. A. (1993). Lipid composition of three macrophytes from the Caspian Sea. Phytochemistry 33 1015–1019. 10.1016/0031-9422(93)85014-I DOI

Di Mauro B., Garzonio R., Baccolo G., Franzetti A., Pittino F., Leoni B., et al. (2020). Glacier algae foster ice-albedo feedback in the European Alps. Sci. Rep. 10:4739. 10.1038/s41598-020-61762-0 PubMed DOI PMC

Engstrom C. B., Yakimovich K. M., Quarmby L. M. (2020). Variation in snow algae blooms in the coast mountains of British Columbia. Front. Microbiol. 11:569. 10.3389/fmicb.2020.00569 PubMed DOI PMC

Gorton H. L., Vogelmann T. C. (2003). Ultraviolet radiation and the snow alga Chlamydomonas nivalis (Bauer) Wille. Photochem. Photobiol. 77 608–615. 10.1562/0031-8655(2003)0770608URATSA2.0.CO2 PubMed DOI

Gray A., Krolikowski M., Fretwell P., Convey P., Peck L. S., Mendelova M., et al. (2020). Remote sensing reveals Antarctic green snow algae as important terrestrial carbon sink. Nat. Commun. 11:2527. 10.1038/s41467-020-16018-w PubMed DOI PMC

Hoham R. W. (1975). The life history and ecology of the snow alga Chloromonas pichinchae (Chlorophyta, Volvocales). Phycologia 14 213–226. 10.2216/i0031-8884-14-4-213.1 DOI

Hoham R. W., Berman J. D., Rogers H. S., Felio J. H., Ryba J. B., Miller P. R. (2006). Two new species of green snow algae from Upstate New York, Chloromonas chenangoensis sp. nov. and Chloromonas tughillensis sp. nov. (Volvocales, Chlorophyceae) and the effects of light on their life cycle development. Phycologia 45 319–330. 10.2216/04-103.1 DOI

Hoham R. W., Mullet J. E. (1977). The life history and ecology of the snow alga Chloromonas cryophila sp. nov. (Chlorophyta, Volvocales). Phycologia 16 53–68. 10.2216/i0031-8884-16-1-53.1 DOI

Hoham R. W., Mullet J. E., Roemer S. C. (1983). The life history and ecology of the snow alga Chloromonas polyptera comb. nov. (Chlorophyta, Volvocales). Phycologia 61 2416–2429. 10.1139/b83-266 DOI

Hoham R. W., Remias D. (2020). Snow and glacial algae: a review. J. Phycol. 56 264–282. 10.1111/jpy.12952 PubMed DOI PMC

Hoham R. W., Roemer S. C., Mullet J. E. (1979). The life history and ecology of the snow alga Chloromonas brevispina comb. nov. (Chlorophyta, Volvocales). Phycologia 18 55–70. 10.2216/i0031-8884-18-1-55.1 DOI

Holzinger A., Lütz C. (2006). Algae and UV irradiation: effects on ultrastructure and related metabolic functions. Micron 37 190–207. 10.1016/j.micron.2005.10.015 PubMed DOI

Khan A. L., Dierssen H., Scambos T., Höfer J., Cordero R. R. (2020). Spectral characterization, radiative forcing, and pigment content of coastal Antarctic snow algae: approaches to spectrally discriminate red and green communities and their impact on snowmelt. Cryosphere Discussions 10.5194/tc-2020-170 [Epub ahead of print]. DOI

Kol E. (1966). Snow algae from the valley of the Morskie Oko lake in the High Tatra. Ann. Hist. Nat. Mus. Natl. Hung. 58 161–168.

Kol E. (1968). “Kryobiologie; biologie und limnologie des schnees und eises. I. Kryovegetation,” in Die Binnengewässer, Band XXIV, eds Elster P., Ohle W. (Stuttgart: Schweizerbart’sche Verlagsbuchhandlung; ), 216.

Leya T. (2013). “Snow algae: adaptation strategies to survive on snow and ice,” in Cellular Origin, Life in Extreme Habitats and Astrobiology, Volume 27, Polyextremophiles: Life Under Multiple Forms of Stress, eds Seckbach J., Oren A., Stan-Lotter H. (Dordrecht: Springer; ), 401–423. 10.1007/978-94-007-6488-0_17 DOI

Leya T. (2020). The CCCryo culture collection of cryophilic algae as a valuable bioresource for algal biodiversity and for novel, industrially marketable metabolites. Appl. Phycol. 10.1080/26388081.2020.1753572 [Epub ahead of print]. DOI

Lukavský J., Cepák V. (2010). Cryoseston in Stara Planina (Balkan) Mountains, Bulgaria. Acta Bot. Croat. 69 163–171.

Lukeš M., Procházková L., Shmidt V., Nedbalová L., Kaftan D. (2014). Temperature dependence of photosynthesis and thylakoid lipid composition in the red snow alga Chlamydomonas cf. nivalis (Chlorophyceae). FEMS Microbiol. Ecol. 89 303–315. 10.1111/1574-6941.12299 PubMed DOI

Luo W., Ding H., Li H., Ji Z., Huang K., Zhao W., et al. (2020). Molecular diversity of the microbial community in coloured snow from the Fildes Peninsula (King George Island, Maritime Antarctica). Polar Biol. 43 1391–1405. 10.1007/s00300-020-02716-0 DOI

Lutz S., Procházková L., Benning L. G., Nedbalová L., Remias D. (2019). Evaluating amplicon high–throughput sequencing data of microalgae living in melting snow: improvements and limitations. Fottea 19 115–131. 10.5507/fot.2019.003 PubMed DOI PMC

Matsuzaki R., Kawachi M., Nozaki H., Nohara S., Suzuki I. (2020). Sexual reproduction of the snow alga Chloromonas fukushimae (Volvocales, Chlorophyceae) induced using cultured materials. PLoS One 15:e0238265. 10.1371/journal.pone.0238265 PubMed DOI PMC

Matsuzaki R., Kawai-Toyooka H., Hara Y., Nozaki H. (2015). Revisiting the taxonomic significance of aplanozygote morphologies of two cosmopolitan snow species of the genus Chloromonas (Volvocales, Chlorophyceae). Phycologia 54 491–502. 10.2216/15-33.1 DOI

Matsuzaki R., Nozaki H., Takeuchi N., Hara Y., Kawachi M. (2019). Taxonomic re-examination of “Chloromonas nivalis (Volvocales, Chlorophyceae) zygotes” from Japan and description of C. muramotoi sp. nov. PLoS One 14:e0210986. 10.1371/journal.pone.0210986 PubMed DOI PMC

Morgan-Kiss R. M., Priscu J. C., Pocock T., Gudynaite-Savitch L., Huner N. P. A. (2006). Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol. Mol. Biol. R. 70 222–252. 10.1128/MMBR.70.1.222 PubMed DOI PMC

Nedbalová L., Kociánová M., Lukavský J. (2008). Ecology of snow algae in the Giant Mts. Opera Corcontica 45 59–68.

Nichelmann L., Schulze M., Herppich W. B., Bilger W. (2016). A simple indicator for non-destructive estimation of the violaxanthin cycle pigment content in leaves. Photosynthesis Res. 128 183–193. 10.1007/s11120-016-0218-1 PubMed DOI

Onuma Y., Takeuchi N., Takeuchi Y. (2016). Temporal changes in snow algal abundance on surface snow in Tohkamachi, Japan. Bul. Glac. Res. 34 21–31. 10.5331/bgr.16A02 DOI

Pescheck F., Bilger W. (2018). Compensation of lack of UV screening by cellular tolerance in green macroalgae (Ulvophyceae) from the upper eulittoral. Mar. Biol. 165:132 10.1007/s00227-018-3393-0 DOI

Piercey-Normore M. D., DePriest P. T. (2001). Algal switching among lichen symbioses. Am. J. Bot. 88 1490–1498. 10.2307/3558457 PubMed DOI

Procházková L., Leya T., Křížková H., Nedbalová L. (2019a). Sanguina nivaloides and Sanguina aurantia gen. et spp. nov. (Chlorophyta): the taxonomy, phylogeny, biogeography and ecology of two newly recognised algae causing red and orange snow. FEMS Microbiol. Ecol. 95:fiz064. 10.1093/femsec/fiz064 PubMed DOI PMC

Procházková L., Remias D., Holzinger A., Řezanka T., Nedbalová L. (2018a). Ecophysiological and morphological comparison of two populations of Chlainomonas sp. (Chlorophyta) causing red snow on ice-covered lakes in the High Tatras and Austrian Alps. Eur. J. Phycol. 53 230–243. 10.1080/09670262.2018.1426789 PubMed DOI PMC

Procházková L., Remias D., Řezanka T., Nedbalová L. (2018b). Chloromonas nivalis subsp. tatrae, subsp. nov. (Chlamydomonadales, Chlorophyta): re–examination of a snow alga from the High Tatra Mountains (Slovakia). Fottea 18 1–18. 10.5507/fot.2017.010 PubMed DOI PMC

Procházková L., Remias D., Řezanka T., Nedbalová L. (2019b). Ecophysiology of Chloromonas hindakii sp. nov. (Chlorophyceae), causing orange snow blooms at different light conditions. Microorganisms 7:434. 10.3390/microorganisms7100434 PubMed DOI PMC

Remias D. (2012). “Cell structure and physiology of alpine snow and ice algae,” in Plants in Alpine Regions. Cell Physiology of Adaption and Survival Strategies, ed. Lütz C. (Wien: Springer; ), 175–186. 10.1007/978-3-7091-0136-0 DOI

Remias D., Karsten U., Lűtz C., Leya T. (2010). Physiological and morphological processes in the Alpine snow alga Chloromonas nivalis (Chlorophyceae) during cyst formation. Protoplasma 243 73–86. 10.1007/s00709-010-0123-y PubMed DOI

Remias D., Lütz-Meindl U., Lütz C. (2005). Photosynthesis, pigments and ultrastructure of the alpine snow alga Chlamydomonas nivalis. Eur. J. Phycol. 40 259–268. 10.1080/09670260500202148 DOI

Remias D., Nicoletti C., Krennhuber K., Möderndorfer B., Nedbalová L., Procházková L. (2020). Growth, fatty, and amino acid profiles of the soil alga Vischeria sp. E71.10 (Eustigmatophyceae) under different cultivation conditions. Folia Microbiol. 65, 1017–1023. 10.1007/s12223-020-00810-8 PubMed DOI PMC

Remias D., Pichrtová M., Pangratz M., Lütz C., Holzinger A. (2016). Ecophysiology, secondary pigments and ultrastructure of Chlainomonas sp. (Chlorophyta) from the European Alps compared with Chlamydomonas nivalis forming red snow. FEMS Microbiol. Ecol. 92:fiw030. 10.1093/femsec/fiw030 PubMed DOI PMC

Remias D., Wastian H., Lütz C., Leya T. (2013). Insights into the biology and phylogeny of Chloromonas polyptera (Chlorophyta), an alga causing orange snow in Maritime Antarctica. Antarct. Sci. 25 648–656. 10.1017/S0954102013000060 DOI

Řezanka T., Dembitsky V. (1999). Novel brominated lipidic compounds from lichens of Central Asia. Phytochemistry 51 963–968. 10.1016/S0031-9422(99)00034-5 PubMed DOI

Řezanka T., Nedbalová L., Procházková L., Sigler K. (2014). Lipidomic profiling of snow algae by ESI-MS and silver-LC/APCI-MS. Phytochemistry 100 34–42. 10.1016/j.phytochem.2014.01.017 PubMed DOI

Saunders R. D., Horrocks L. A. (1984). Simultaneous extraction and preparation for high-performance liquid chromatography of prostaglandins and phospholipids. Anal. Biochem. 143 71–75. 10.1016/0003-2697(84)90559-1 PubMed DOI

Segawa T., Matsuzaki R., Takeuchi N., Akiyoshi A., Navarro F., Sugiyama S., et al. (2018). Bipolar dispersal of red-snow algae. Nat. Commun. 9:3094. 10.1038/s41467-018-05521-w PubMed DOI PMC

Senger H., Pfau J., Werthmueller K. (1972). “Continuous automatic cultivation of homocontinuous and synchronized microalgae,” in Methods in Cell Physiology, ed. Prescott D. M. (New York, NY: Academic Press; ), 301–321. 10.1016/s0091-679x(08)60716-5 DOI

Spijkerman E., Wacker A., Weithoff G., Leya T. (2012). Elemental and fatty acid composition of snow algae in Arctic habitats. Front. Microbiol. 3:380. 10.3389/fmicb.2012.00380 PubMed DOI PMC

Starr R., Zeikus J. (1993). UTEX—the culture collection of algae at the University of Texas at Austin 1993 list of cultures. J. Phycol. 29 1–106. 10.1111/j.0022-3646.1993.00001.x DOI

Thompson G. A. (1996). Lipids and membrane function in green algae. Biochim. Biophys. Acta 1302 17–45. 10.1016/0005-2760(96)00045-8 PubMed DOI

VanWinkle-Swift K. P., Rickoll W. L. (1997). The zygospore wall of Chlamydomonas monoica (Chlorophyceae): morphogenesis and evidence for the presence of sporopollenin. J. Phycol. 33 655–665. 10.1111/j.0022-3646.1997.00655.x DOI

Versteegh G. J. M., Blokker P. (2004). Resistant macromolecules of extant and fossil microalgae. Phycol. Res. 52 325–339. 10.1111/j.1440-1835.2004.tb00342.x DOI

Vieler A., Wilhelm C., Goss R., Süß R., Schiller J. (2007). The lipid composition of the unicellular green alga Chlamydomonas reinhardtii and the diatom Cyclotella meneghiniana investigated by MALDI-TOF MS and TLC. Chem. Phys. Lipids 150 143–155. 10.1016/j.chemphyslip.2007.06.224 PubMed DOI

Webb W. L., Newton M., Starr D. (1974). Carbon dioxide exchange of Alnus rubra. A mathematical model. Oecologia 17 281–291. 10.1007/BF00345747 PubMed DOI

Xiong F., Komenda J., Kopecký J., Nedbal L. (1997). Strategies of ultraviolet-B protection in microscopic algae. Physiol. Plant. 100 378–388. 10.1034/j.1399-3054.1997.1000221.x PubMed DOI

Yakimovich K. M., Engstrom C. B., Quarmby L. M. (2020). Alpine snow algae microbiome diversity in the Coast Range of British Columbia. Front. Microbiol. 11:1721 10.3389/fmicb.2020.01721 PubMed DOI PMC

Phylogeny and lipid profiles of snow-algae isolated from Norwegian red-snow microbiomes

The snow alga Chloromonas kaweckae sp. nov. (Volvocales, Chlorophyta) causes green surface blooms in the high tatras (Slovakia) and tolerates high irradiance