Melting polar and alpine ice surfaces frequently exhibit blooms of dark pigmented algae. These microbial extremophiles significantly reduce the surface albedo of glaciers, thus accelerating melt rates. However, the ecology, physiology and taxonomy of cryoflora are not yet fully understood. Here, a Swiss and an Austrian glacier dominated either by filamentous Ancylonema nordenskioeldii or unicellular Mesotaenium berggrenii var. alaskanum, were sampled. Molecular analysis showed that both species are closely related, sharing identical chloroplast morphologies (parietal-lobed for Ancylonema vs. axial plate-like for Mesotaenium sensu stricto), thus the unicellular species was renamed Ancylonema alaskana. Moreover, an ecophysiological comparison of the two species was performed: pulse-amplitude modulated (PAM) fluorometry confirmed that they have a high tolerance to elevated solar irradiation, the physiological light preferences reflected the conditions in the original habitat; nonetheless, A. nordenskioeldii was adapted to higher irradiances while the photosystems of A. alaskana were able to use efficiently low irradiances. Additionally, the main vacuolar polyphenol, which effectively shields the photosystems, was identical in both species. Also, about half of the cellular fatty acids were polyunsaturated, and the lipidome profiles dominated by triacylglycerols were very similar. The results indicate that A. alaskana is physiologically very similar and closely related but genetically distinct to A. nordenskioeldii.

Centre for Phycology Institute of Botany of the Czech Academy of Sciences Dukelská 135 379 82 Třeboň Czech Republic

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

Institute of Microbiology The Czech Academy of Sciences Vídeňská 1083 142 20 Prague Czech Republic

School of Engineering University of Applied Sciences Upper Austria Stelzhamerstr 23 4600 Wels Austria

Zobrazit více v PubMed

Anesio A.M., Lutz S., Chrismas N.A.M., Benning L.G. The microbiome of glaciers and ice sheets. NPJ Biofilms Microbiomes. 2017;3:10. doi: 10.1038/s41522-017-0019-0. PubMed DOI PMC

Boetius A., Anesio A.M., Deming J.W., Mikucki J.A., Rapp J.Z. Microbial ecology of the cryosphere: Sea ice and glacial habitats. Nat. Rev. Microbiol. 2015;13:677–690. doi: 10.1038/nrmicro3522. PubMed DOI

Hotaling S., Hood E., Hamilton T.L. Microbial ecology of mountain glacier ecosystems: Biodiversity, ecological connections and implications of a warming climate. Environ. Microbiol. 2017;19:2935–2948. doi: 10.1111/1462-2920.13766. PubMed DOI

Hoham R.W., Remias D. Snow and Glacial Algae: A Review. J. Phycol. 2020;56:264–282. doi: 10.1111/jpy.12952. PubMed DOI PMC

Ling H.U., Seppelt R.D. Snow algae of the Windmill Islands, continental Antarctica. Mesotaenium berggrenii (Zygnematales, Chlorophyta) the alga of grey snow. Antarct. Sci. 1990;2:143–148. doi: 10.1007/s003000050309. DOI

Remias D., Holzinger A., Lütz C. Physiology, ultrastructure and habitat of the ice alga Mesotaenium berggrenii (Zygnemaphyceae, Chlorophyta) from glaciers in the European Alps. Phycologia. 2009;48:302–312. doi: 10.2216/08-13.1. DOI

Remias D., Holzinger A., Aigner S., Lütz C. Ecophysiology and ultrastructure of Ancylonema nordenskiöldii (Zygnematales, Streptophyta), causing brown ice on glaciers in Svalbard (high arctic) Polar Biol. 2012;35:899–908. doi: 10.1007/s00300-011-1135-6. DOI

Kol E. Kryobiologie. Biologie und Limnologie des Schnees und Eises. I. Kryovegetation. In: Elster H.J., Ohle W., editors. Die Binnengewässer. Schweizerbart’sche Verlagsbuchhandlung; Stuttgart, Germany: 1968. Band XXIV.

Williamson C.J., Cameron K.A., Cook J.M., Žárský J.D., Stibal M., Edwards A. Glacier algae: A dark past and a darker future. Front. Microbiol. 2019;10:524. doi: 10.3389/fmicb.2019.00524. PubMed DOI PMC

Barcytė D., Pilátová J., Mojzeš P., Nedbalová L. The Arctic Cylindrocystis (Zygnematophyceae, Streptophyta) green algae are genetically and morphologically diverse and exhibit effective accumulation of polyphosphate. J. Phycol. 2020;56:217–232. doi: 10.1111/jpy.12931. PubMed DOI

Remias D., Schwaiger S., Aigner S., Leya T., Stuppner H., Lütz C. Characterization of an UV- and VIS-absorbing, purpurogallin-derived secondary pigment new to algae and highly abundant in Mesotaenium berggrenii (Zygnematophyceae, Chlorophyta), an extremophyte living on glaciers. FEMS Microbiol. Ecol. 2012;79:638–648. doi: 10.1111/j.1574-6941.2011.01245.x. PubMed DOI

Williamson C.J., Cook J., Tedstone A., Yallop M., McCutcheon J., Poniecka E., Campbell D., Irvine-Fynn T., McQuaid J., Tranter M., et al. Algal photophysiology drives darkening and melt of the Greenland Ice Sheet. Proc. Natl. Acad. Sci. USA. 2020;117:5694–5705. doi: 10.1073/pnas.1918412117. PubMed DOI PMC

Yallop M.L., Anesio A.M., Perkins R.G., Cook J., Telling J., Fagan D., MacFarlane J., Stibal M., Barker G., Bellas C., et al. Photophysiology and albedo-changing potential of the ice algal community on the surface of the Greenland ice sheet. ISME J. 2012;6:2302–2313. doi: 10.1038/ismej.2012.107. PubMed DOI PMC

Lutz S., Anesio A.M., Jorge Villar S.E., Benning L.G. Variations of algal communities cause darkening of a Greenland glacier. FEMS Microbiol. Ecol. 2014;89:402–414. doi: 10.1111/1574-6941.12351. PubMed DOI

Stibal M., Box J.E., Cameron K.A., Langen P.L., Yallop M.L., Mottram R.H., Khan A.L., Molotch N.P., Chrismas N.A.M., Quaglia F.C., et al. Algae drive enhanced darkening of bare ice on the Greenland ice sheet. Geophys. Res. Lett. 2017 doi: 10.1002/2017GL075958. DOI

McCutcheon J., Lutz S., Williamson C., Cook J.M., Tedstone A.J., Vanderstraeten A., Wilson S.A., Stockdale A., Bonneville S., Anesio A.M., et al. Mineral phosphorus drives glacier algal blooms on the Greenland Ice Sheet. Nat. Commun. 2021;12:570. doi: 10.1038/s41467-020-20627-w. PubMed DOI PMC

Williamson C., Anesio A.M., Cook J., Tedstone A., Poniecka E., Holland A., Fagan D., Tranter M., Yallop M. Ice algal bloom development on the surface of the Greenland Ice Sheet. FEMS Microbiol. Ecol. 2018;94:fiy025. doi: 10.1093/femsec/fiy025. PubMed DOI PMC

Di Mauro B., Garzonio R., Baccolo G., Franzetti A., Pittino F., Leoni B., Remias D., Colombo R., Rossini M. Glacier algae foster ice-albedo feedback in the European Alps. Sci. Rep. 2020;10:4739. doi: 10.1038/s41598-020-61762-0. PubMed DOI PMC

Procházková L., Leya T., Křížková H., Nedbalová L. 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. 2019;95:fiz064. doi: 10.1093/femsec/fiz064. PubMed DOI PMC

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

Gontcharov A.A., Melkonian M. Molecular phylogeny and revision of the genus Netrium (Zygnematophyceae, Streptophyta): Nucleotaenium gen. nov. J. Phycol. 2010;46:346–362. doi: 10.1111/j.1529-8817.2010.00814.x. DOI

Posada D. jModelTest: Phylogenetic model averaging. Mol. Biol. Evol. 2008;25:1253–1256. doi: 10.1093/molbev/msn083. PubMed DOI

Nedbalová L., Mihál M., Kvíderová J., Procházková L., Řezanka T., Elster J. Identity, ecology and ecophysiology of planktic green algae dominating in ice-covered lakes on James Ross Island (northeastern Antarctic Peninsula) Extremophiles. 2017;21:187–200. doi: 10.1007/s00792-016-0894-y. PubMed DOI

Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Phys. 1959;37:911–917. doi: 10.1139/o59-099. PubMed DOI

Kates M., Volcani B.E. Biosynthetic pathways for phosphatidylsulfocholine, the sulfonium analogue of phosphatidylcholine. In: Kiene R.P., Visscher P.T., Keller M.D., Kirst G.O., editors. Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds, in Diatoms. Springer; Boston, MA, USA: 1996. pp. 109–119.

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

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

Kol E. The snow and ice algae of Alaska. Smithson. Misc. Collect. 1942;101:1–36.

Takeuchi N. The altitudinal distribution of snow algae on an Alaska glacier (Gulkana Glacier in the Alaska Range) Hydrol. Process. 2001;15:3447–3459. doi: 10.1002/hyp.1040. DOI

Darcy S.K., Schmidt J.L. Phylogeny of ulotrichalean algae from extreme high-altitude and high-latitude ecosystems. Polar Biol. 2015;38:689–697.

Takeuchi N., Tanaka S., Irvine-Fynn T.D.L., Rassner S.M.E., Edwards A. Variations in phototroph communities on the ablating bare-ice surface of glaciers on Brøggerhalvøya, Svalbard. Front. Earth Sci. 2019;7:4. doi: 10.3389/feart.2019.00004. DOI

Lutz S., McCutcheon J., McQuaid J.B., Benning L.G. The diversity of ice algal communities on the Greenland Ice Sheet as revealed by oligotyping. Microbial. Genomics. 2018;4:e000159. doi: 10.1099/mgen.0.000159. PubMed DOI PMC

Takeuchi N., Uetake J., Fujita K., Aizen V.B., Nikitin S.D. A snow algal community on Akkem Glacier in the Russian Altai Mountains. Ann. Glaciol. 2006;43:378–384. doi: 10.3189/172756406781812113. DOI

Yoshimura Y., Kohshima S., Ohtani S. A community of snow algae on a Himalayan glacier: Change of algal biomass and community structure with altitude. Arctic Alpine Res. 1997;29:126–137. doi: 10.2307/1551843. DOI

Berggren S. Öfversigt af Kongl. Vetenskaps-Akademiens Förhandlingar. P. A. Norstedt & Söner; Stockholm, Sweden: 1871. Alger från Grönlands inlandis; pp. 293–297.

Wittrock B. Om snöns och isens flora, särskildt i de arktiska trakterna. In: Nordenskiöld A.E., editor. Studier och Forskningar Föranledda af Mina Resor i Hoga Norden. F. & G. Beijers Forlag; Stockholm, Sweden: 1883. pp. 63–124.

Lagerheim G. Die Schnee Flora des Pichincha. Ein Beitrag zur Kenntnis der Nivalen Algen und Pilzen. Ber. der Dtsch. Bot. Gessellschaft. 1892;10:517–534.

Turland N.J., Wiersema J.H., Barrie F.R., Greuter W., Hawksworth D.L., Herendeen P.S., Knapp S., Kusber W.-H., Li D.-Z., Marhold K., et al., editors. International Code of Nomenclature For algae, Fungi, and Plants (Shenzhen Code) Adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Koeltz Botanical Books; Glashütten, Germany: 2018. Regnum Veg. Glashütten 159. DOI

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

Takeuchi N., Kohshima S. A snow algal community on Tyndall Glacier in the Southern Patagonia Icefield, Chile. Arctic Alpine Res. 2004;36:92–99. doi: 10.1657/1523-0430(2004)036[0092:ASACOT]2.0.CO;2. DOI

Komárek O., Komárek J. Contribution to the taxonomy and ecology of green cryosestic algae in the summer season 1995-96 at King George Island, S. Shetland Islands. Nova Hedwig. Beiheft. 2001;123:121–140.

Kol E. Über roten and grünen Schnee der Alpen. Verh Intern. Ver. Limnol. 1961;XIV:912–917. doi: 10.1080/03680770.1959.11899387. DOI

Krieger W. Die Desmidiaceen Europas mit Berücksichtigung der aussereuropäischen Arten. Band 13. Abteilung 1, Teil 1, Lieferung 1 of Dr. L. Rabenhorst’s Kryptogamen-Flora von Deutschland, Österreich und der Schweiz. Akademische Verlagsgeselschaft M.B.H.; Leipzig, Germany: 1933.

Yoshimura Y., Kohshima S., Takeuchi N., Seko K., Fujita K. Himalayan ice-core dating with snow algae. J. Glaciol. 2000;46:335–340. doi: 10.3189/172756500781832918. DOI

Cheng S., Xian W., Fu Y., Marin B., Keller J., Wu T., Sun W., Li X., Xu Y., Zhang Y., et al. Genomes of subaerial Zygnematophyceae provide insights into land plant evolution. Cell. 2019;179:1057–1067.e14. doi: 10.1016/j.cell.2019.10.019. PubMed DOI

Stancheva R., Hall J.D., Herburger K., Lewis L.A., Mccourt R.M., Sheath R.G. Phylogenetic position of Zygogonium ericetorum (Zygnematophyceae, Charophyta) from a high alpine habitat and ultrastructural characterization of unusual aplanospores. J. Phycol. 2014;803:790–803. doi: 10.1111/jpy.12229. PubMed DOI PMC

Broady P.A. Six new species of terrestrial algae from Signy Island, South Orkney Islands, Antarctica. Brit. Phycol. J. 1976;11:387–405. doi: 10.1080/00071617600650451. DOI

Herburger K., Remias D., Holzinger A. The green alga Zygogonium ericetorum (Zygnematophyceae, Charophyta) shows high iron and aluminium tolerance: Protection mechanisms and photosynthetic performance. FEMS Microbiol. Ecol. 2016;92:1–15. doi: 10.1093/femsec/fiw103. PubMed DOI PMC

Nägeli C. Gattungen einzelliger Algen, physiologisch und systematisch bearbeitet. Neue Denkschr. der Allg Schweiz. Gesellschaft für die Gesammten Naturwissenschaften. 1849;10:1–139.

O’Neal S.W., Hoover A.M. Comparison of UVB effects on growth and induction of UVB screening compounds in isolates of metaphytic algae from temperate zone streams and ponds. J. Phycol. 2018;54:818–828. doi: 10.1111/jpy.12786. PubMed DOI

Nedbalová L., Sklenář P. New records of snow algae from the Andes of Ecuador. Arnaldoa. 2008;15:17–20.

Garduño-Solórzano G., Martínez-García M., Scotta Hentschke G., Lopes G., Castelo Branco R., Vasconcelos V.M.O., Campos J.E., López-Cano R., Quintanar-Zúñiga R.E. The phylogenetic placement of Temnogametum (Zygnemataceae) and description of Temnogametum iztacalense sp. nov., from a tropical high mountain lake in Mexico. Eur. J. Phycol. 2020;56:1–15. doi: 10.1080/09670262.2020.1789226. DOI

Kalisch B., Dörmann P., Hölzl G. DGDG and Glycolipids in Plants and Algae. In: Nakamura Y., Li-Beisson Y., editors. Lipids in Plant and Algae Development. Subcellular Biochemistry. Springer; Cham, Switzerland: 2016. pp. 51–83. PubMed

Mock T., Kroon B.M.A. Photosynthetic energy conversion under extreme conditions-II: The significance of lipids under light limited growth in Antarctic sea ice diatoms. Phytochemistry. 2002;61:41–51. doi: 10.1016/S0031-9422(02)00216-9. PubMed DOI

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

Wang X., Li W., Li M., Welti R. Profiling lipid changes in plant response to low temperatures. Physiol. Plantarum. 2006;126:90–96. doi: 10.1111/j.1399-3054.2006.00622.x. DOI

Holzinger A., Roleda M.Y., Lütz C. The vegetative arctic freshwater green alga Zygnema is insensitive to experimental UV exposure. Micron. 2009;40:831–838. doi: 10.1016/j.micron.2009.06.008. PubMed DOI

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

Gronnier J., Germain V., Gouguet P., Cacas J.L., Mongrand S. GIPC: Glycosyl inositol phospho ceramides, the major sphingolipids on earth. Plant Signal. Behav. 2016;11:1–7. doi: 10.1080/15592324.2016.1152438. PubMed DOI PMC

Markham J.E., Li J., Cahoon E.B., Jaworski J.G. Separation and identification of major plant sphingolipid classes from leaves. J. Biol. Chem. 2006;281:22684–22694. doi: 10.1074/jbc.M604050200. PubMed DOI

Lang I., Hodač L., Friedl T., Feussner I. Fatty acid profiles and their distribution patterns in microalgae: A comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biol. 2011;11:124. doi: 10.1186/1471-2229-11-124. PubMed DOI PMC

Pichrtová M., Arc E., Stöggl W., Kranner I., Hájek T., Hackl H., Holzinger A. 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. 2016;92:fiw096. doi: 10.1093/femsec/fiw096. PubMed DOI PMC

Morgan-Kiss R.M., Priscu J.C., Pocock T., Gudynaite-Savitch L., Huner N.P.A. Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol. Mol. Biol. R. 2006;70:222–252. doi: 10.1128/MMBR.70.1.222-252.2006. PubMed DOI PMC

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

A DUF3494 ice-binding protein with a root cap domain in a streptophyte glacier ice alga

Cryogenian Glacial Habitats as a Plant Terrestrialisation Cradle - The Origin of the Anydrophytes and Zygnematophyceae Split