Based on analyses of multiple molecular markers (18S rDNA, ITS1, ITS2 rDNA, rbcL), an alga that causes red snow on the melting ice cover of a high-alpine lake in the High Tatras (Slovakia) was shown to be identical with Chlainomonas sp. growing in a similar habitat in the Tyrolean Alps (Austria). Both populations consisted mostly of smooth-walled quadriflagellates. They occurred in slush, and shared similar photosynthetic performances (photoinhibition above 1300 µmol photons m-2 s-1), very high levels of polyunsaturated fatty acids (PUFA, 64% and 74% respectively) and abundant astaxanthin accumulation, comparable to the red spores of Chlamydomonas nivalis (Bauer) Wille. Physiological differences between the Slovak and Austrian populations included higher levels of α-tocopherol and a 13Z-isomer of astaxanthin in the former. High accumulation of secondary pigments in the Slovak population probably reflected harsher environmental conditions, since the collection was made later in the growing season when cells were exposed to higher irradiance at the surface. Using a polyphasic approach, we compared Chlainomonas sp. with Chlamydomonas nivalis. The latter causes 'conventional' red snow, and shows high photophysiological plasticity, with high efficiency under low irradiance and no photoinhibition up to 2000 µmol photons m-2 s-1. Its PUFA content was significantly lower (50%). An annual cycle of lake-to-snow colonization by Chlainomonas sp. from slush layers deeper in the ice cover is proposed. Our results point to an ecologically highly specialized cryoflora species, whose global distribution is likely to be more widespread than previously assumed.

Charles University Faculty of Science Department of Ecology Viničná 7 CZ 128 44 Prague Czech Republic

Department of Botany University of Innsbruck Austria

Institute of Microbiology of the Czech Academy of Sciences Czech Republic

University of Applied Sciences Upper Austria Stelzhamerstr 23 A 4600 Wels Austria

Zobrazit více v PubMed

Alfreider A., Pernthaler J., Amann R., Sattler B., Wille A. & Psenner R. (1996). Community analysis of the bacterial assemblages in the winter cover and pelagic layers of a high mountain lake by in situ hybridization. Applied and Environmental Microbiology, 62: 2138–2144. PubMed PMC

Bidigare R.R., Ondrusek M.E., Kennicutt II, Iturriaga M.C., Harvey R., Hoham H.R., W. R. & Macko S.A. (1993). Evidence for a photoprotective function for secondary carotenoids of snow algae. Journal of Phycology, 29: 427–434.

Bligh E.G. & Dyer W.J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37: 911–917. PubMed

Brown S.P., Ungerer M.C. & Jumpponen A. (2016). A community of clones: snow algae are diverse communities of spatially structured clones. International Journal of Plant Sciences, 177: 432–439.

Christen H.R. (1959). Flagellaten aus dem Schützenweiher bei Veltheim. Mitteilungen der Naturwissenschaftlichen Gesellschaft Winterthur, 29: 167–189.

De Maayer P., Anderson D., Cary C. & Cowan D.A (2014). Some like it cold: understanding the survival strategies of psychrophiles. EMBO Reports, 15: 508–517. PubMed PMC

Dembitsky V.M., Řezanka T., Bychek I.A. & Shustov M.V. (1991). Identification of fatty acids from Cladonia lichens. Phytochemistry, 30: 4015–4018.

Ettl H. (1968). Ein Beitrag zur Kenntnis der Algenflora Tirols. Berichte des Naturwissenschaftlich-Medizinischen Vereins in Innsbruck, 56: 177–354.

Felip M., Camarero L. & Catalan J. (1999). Temporal changes of microbial assemblages in the ice and snow cover of a high mountain lake. Limnology and Oceanography, 44: 973–987.

Felip M., Sattler B., Psenner R., & Catalan J. (1995). Highly active microbial communities in the ice and snow cover of high mountain lakes. Applied and Environmental Microbiology, 61: 2394–2401 PubMed PMC

Felip M., Wille A., Sattler B. & Psenner R. (2002). Microbial communities in the winter cover and the water column of an alpine lake: system connectivity and uncoupling. Aquatic Microbial Ecology, 29: 123–134.

Hardy J.T. (1966). Identification, culture, and physiological ecology of cryophilic algae. Oregon State University, Corvallis. M.S. thesis.

Hardy J.T. & Curl H.J. (1968). Red snow caused by a new species of Trachelomonas. Journal of Phycology, 4: 9–12. PubMed

Hoham R.W. (1974a). Chlainomonas kolii (Hardy et Curl) comb. nov. (Chlorophyta, Volvocales), a revision of the snow alga, Trachelomonas kolii Hardy et Curl (Euglenophyta, Euglenales). Journal of Phycology, 10: 392–396.

Hoham R.W. (1974b). New findings in the life history of the snow alga, Chlainomonas rubra (Stein et Brooke) comb. nov. (Chlorophyta, Volvocales). Syesis, 7: 239–247.

Hoham R.W. (1975). Optimum temperatures and temperatures ranges for growth of snow algae. Arctic and Alpine Research, 7: 13–24.

Hoham R.W. & Duval B. (2001). Microbial ecology of snow and freshwater ice with emphasis on snow algae In Snow Ecology: An Interdisciplinary Examination of Snow-Covered Ecosystems (Jones H.G., Pomeroy J.W., Walker D.A. & Hoham R.W., editors), 168–228. Cambridge University Press.

Holzinger A., Allen M.C. & Deheyn D.D. (2016). Hyperspectral imaging of snow algae and green algae from aeroterrestrial habitats. Journal of Photochemistry and Photobiology B: Biology, 162: 412–420. PubMed PMC

Hulatt C.J., Berecz O., Egeland E.S., Wijffels R.H. & Kiron V. (2017). Polar snow algae as a valuable source of lipids? Bioresource Technology, 235: 338–347. PubMed

Kamenik C., Koinig K.A., Schmidt R., Appleby P.G., Dearing J.A., & Psenner R. (2000). Eight hundred years of environmental changes in a high alpine lake (gossenkӧllesee, tyrol) inferred from sediment records. Journal of Limnology, 59 (Suppl. 1): 43–52.

Kawecka B. (1981). Biology and ecology of snow algae. 2. Formation of aplanospores in Chlamydomonas nivalis (Bauer) Wille (Chlorophyta, Volvocales). Acta Hydrobiologia, 23: 211 –215.

Kol E. (1969). Chlamydomonas sanguinea Lagerh. in the High Tatra. Annales Historico-Naturales Musei Nationalis Hungarici, 61: 111–115.

Kol E. (1975a). Cryobiological researches in the High Tatra I. Acta Botanica Academiae Scientiarum Hungaricae, 21: 61–75.

Kol E. (1975b). Cryobiological researches in the High Tatra II. Acta Botanica Academiae Scientiarum Hungaricae, 21: 279–287.

Kol E. (1968). Kryobiologie. Biologie und Limnologie des Schnees und Eises. I. Kryovegetation (Elster P. & Ohle W., editors). Die Binnengewässer, Band XXIV Schweizerbart’sche Verlagsbuchhandlung, Stuttgart.

Kopáček J., Stuchlík E. & Hardekopf D. (2006). Chemical composition of the Tatra Mountain lakes: recovery from acidification. Biologia, 61: S21–S33.

Lang I., Hodac L., Friedl T. & Feussner I. (2011). Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biology, 11: 124. PubMed PMC

Leya T., Müller T., Ling H.U. & Fuhr G.R. (2004). Snow algae from North-Western Spitsbergen (Svalbard) In The coastal ecosystem of Kongsfjorden, Svalbard : Synopsis of biological research performed at the Koldewey Station in the years 1991–2003 (Berichte zur Polar- und Meeresforschung 492) (Wiencke C., editor), 46–54. Bremerhaven.

Leya T., Rahn A., Lütz C. & Remias D. (2009). Response of arctic snow and permafrost algae to high light and nitrogen stress by changes in pigment composition and applied aspects for biotechnology. FEMS Microbiology Ecology, 67: 432–443. PubMed

Lukavský J., Furnadzhieva S. & Nedbalová L. (2009). First record of cryoseston in the Vitosha Mountains, Bulgaria. Nova Hedwigia, 88: 97–110.

Lutz S., Anesio A.M., Field K. & Benning L.G. (2015). Integrated “Omics”, targeted metabolite and single-cell analyses of arctic snow algae functionality and adaptability. Frontiers in Microbiology, 6: 1–17. PubMed PMC

Malmberg A.E. & VanWinkle-Swift K.P. (2001). Zygospore germination in Chlamydomonas monoica (Chlorophyta): timing and pattern of secondary zygospore wall degradation in relation to cytoplasmic events. Journal of Phycology, 37: 86–94.

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.

Mudimu P., Koopmann I. K., Rybalka N., Friedl T., Schulz R. & Bilger W. (2017). Screening of microalgae and cyanobacteria strains for α-tocopherol content at different growth phases and the influence of nitrate reduction on α-tocopherol production. Journal of Applied Phycology, 29: 2867–2875.

Müller T., Bleiẞ W., Rogaschewski C.-D.M.S. & Fuhr G. (1998). Snow algae from northwest Svalbard: their identification, distribution, pigment and nutrient content. Polar Biology, 20: 14–32.

Nedbalová L., Stuchlík E. & Strunecký O. (2006). Phytoplankton of a mountain lake (Ľadové pleso, the Tatra Mountains, Slovakia): seasonal development and first indications of a response to decreased acid deposition. Biologia, 61: S91–S100.

Niedzwiedz T. (1992). Climate of the Tatra Mountains. Mountain Research and Development, 12: 131–146.

Novikmec M., Svitok M., Kočický D., Šporka F. & Bitušík P. (2013). Surface water temperature and ice cover of Tatra Mountains lakes depend on altitude, topographic shading, and bathymetry. Arctic, Antarctic, and Alpine Research, 45: 77–87.

Novis P.M. (2001). Ecology and taxonomy of alpine algae, Mt Philistine, Arthur’s Pass National Park, New Zealand. University of Canterbury, Christchurch, New Zealand; PhD thesis.

Novis P.M. (2002a). Ecology of the snow alga Chlainomonas kolii (Chlamydomonadales, Chlorophyta) in New Zealand. Phycologia, 41: 280–292.

Novis P.M. (2002b). New records of snow algae for New Zealand, from Mt Philistine, Arthur’s Pass National Park. New Zealand Journal of Botany, 40: 297–312.

Novis P.M., Hoham R.W., Beer T. & Dawson M. (2008). Two snow species of the quadriflagellate green alga Chlainomonas (Chlorophyta, Volvocales): ultrastructure and phylogenetic position within the Chloromonas clade. Journal of Phycology, 44: 1001–1012. PubMed

Nozaki H., Nakada T. & Watanabe S. (2010). Evolutionary origin of Gloeomonas (Volvocales, Chlorophyceae), based on ultrastructure of chloroplasts and molecular phylogeny. Journal of Phycology, 46: 195–201.

Nozaki H., Onishi K. & Morita E. (2002). Differences in pyrenoid morphology are correlated with differences in the rbcL genes of members of the Chloromonas lineage (Volvocales, Chlorophyceae). Journal of Molecular Evolution, 55: 414–430. PubMed

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 Microbiology Ecology, 92: fiw096. PubMed PMC

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

Remias D., Karsten U., Lütz C. & Leya T. (2010). Physiological and morphological processes in the alpine snow alga Chloromonas nivalis (Chlorophyceae) during cyst formation. Protoplasma, 243: 73–86. PubMed

Remias D. & Lütz C. (2007). Characterisation of esterified secondary carotenoids and of their isomers in green algae: a HPLC approach. Algological Studies, 124: 85–94.

Remias D., Lütz-Meindl U. & Lütz C. (2005). Photosynthesis, pigments and ultrastructure of the alpine snow alga Chlamydomonas nivalis. European Journal of Phycology, 40: 259–268.

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 Microbiology Ecology, 92: fiw030. PubMed PMC

Řezanka T. (1990). Identification of very long polyenoic acids as picolinyl esters by Ag+ ion-exchange high-performance liquid chromatography, reversed-phase high-performance liquid chromatography and gas chromatography—mass spectrometry. Journal of Chromatography A, 513: 344–348.

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. PubMed

Řezanka T., Nedbalová L. & Sigler K. (2008). Unusual medium-chain polyunsaturated fatty acids from the snow alga Chloromonas brevispina. Microbiological Research, 163: 373–379. PubMed

Sattler B., Post B., Remias D., Lutz C., Lettner H. & Psenner R. (2012). Cold Alpine regions In Life at Extremes. Environments, Organisms, and Strategies for Survival (Bell E. editor), 138–154. CABI, Wallingford.

Saunders R. D. & Horrocks L. A. (1984). Simultaneous extraction and preparation for high-performance liquid chromatography of prostaglandins and phospholipids. Analytical Biochemistry, 143: 71–75. PubMed

Sommaruga R. & Psenner R. (1997). Ultraviolet radiation in a high mountain lake of the Austrian Alps: air and underwater measurements. Photochemistry and Photobiology, 65: 957–963.

Spijkerman E., Wacker A., Weithoff G. & Leya T. (2012). Elemental and fatty acid composition of snow algae in Arctic habitats. Frontiers in Microbiology, 3: 1–15. PubMed PMC

Šporka F., Livingstone D.M., Stuchlík E., Turek J. & Galas J. (2006). Water temperatures and ice cover in lakes of the Tatra Mountains. Biologia, 61: S77–S90.

Stein J.R. & Brooke R.C. (1964). Red snow from Mt. Seymour, British Columbia. Canadian Journal of Botany, 42: 1183–1188.

Tartarotti B., Trattner F., Remias D., Saul N., Steinberg C.E.W. & Sommaruga R. (2017). Distribution and UV protection strategies of zooplankton in clear and glacier-fed alpine lakes. Scientific Reports, 7: 4487. doi: 10.1038/s41598-017-04836-w. PubMed DOI PMC

VanWinkle-Swift K.P. & Rickoll W.L. (1997). The zygospore wall of Chlamydomonas monoica (Chlorophyceae): morphogenesis and evidence for the presence of sporopollenin. Journal of Phycology, 33: 655–665.

Walsby A.E. (1997). Modelling the daily integral of photosynthesis by phytoplankton: its dependence on the mean depth of the population. Hydrobiologia, 349: 65–74.

Novel insights in cryptic diversity of snow and glacier ice algae communities combining 18S rRNA gene and ITS2 amplicon sequencing

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

Ecophysiological and ultrastructural characterisation of the circumpolar orange snow alga Sanguina aurantia compared to the cosmopolitan red snow alga Sanguina nivaloides (Chlorophyta)

Spatial and Temporal Variations in Pigment and Species Compositions of Snow Algae on Mt. Tateyama in Toyama Prefecture, Japan

Cysts of the Snow Alga Chloromonas krienitzii (Chlorophyceae) Show Increased Tolerance to Ultraviolet Radiation and Elevated Visible Light

Evaluating High-Throughput Sequencing Data of Microalgae Living in Melting Snow: Improvements and Limitations1

Ecophysiology of Chloromonas hindakii sp. nov. (Chlorophyceae), Causing Orange Snow Blooms at Different Light Conditions

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

Ecology, cytology and phylogeny of the snow alga Scotiella cryophila K-1 (Chlamydomonadales, Chlorophyta) from the Austrian Alps