The green algae of the genus Ancylonema, which belong to the zygnematophytes, are prevalent colonizers of glaciers worldwide. They display a striking reddish-brown pigmentation in their natural environment, due to vacuolar compounds related to gallic acid. This pigmentation causes glacier darkening when these algae bloom, leading to increased melting rates. The Ancylonema species known so far are true psychrophiles, which hinders experimental work and limits our understanding of these algae. For instance, the biosynthesis, triggering factors, and biological function of Ancylonema's secondary pigments remain unknown. In this study, we introduce a mesophilic Ancylonema species, A. palustre sp. nov., from temperate moorlands. This species forms the sister lineage to all known psychrophilic strains. Despite its morphological similarity to the latter, it exhibits unique autecological and photophysiological characteristics. It allows us to describe vegetative and sexual cellular processes in great detail. We also conducted experimental tests for abiotic factors that induce the secondary pigments of zygnematophytes. We found that low nutrient conditions combined with ultraviolet B radiation result in vacuolar pigmentation, suggesting a sunscreen function. Our thriving, bacteria-free cultures of Ancylonema palustre will enable comparative genomic studies of mesophilic and extremophilic zygnematophytes. These studies may provide insights into how Ancylonema species colonized the world's glaciers.

Department of Biology Technical University of Darmstadt Darmstadt Germany

Department of Biology University of Cologne Cologne Germany

Department of Ecology Faculty of Science Charles University Prague Czech Republic

Department of Environment and Biodiversity University of Salzburg Salzburg Austria

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Aigner, S., Remias, D., Karsten, U. & Holzinger, A. (2013) Unusual phenolic compounds contribute to ecophysiological performance in the purple‐coloured green alga Z ygogonium ericetorum (Zygnematophyceae, Streptophyta) from a high‐alpine habitat. Journal of Phycology, 49(4), 648–660.

Barcytė, D., Pilátová, J., Mojzeš, P. & Nedbalová, L. (2020) The arctic Cylindrocystis (Zygnematophyceae, Streptophyta) green algae are genetically and morphologically diverse and exhibit effective accumulation of polyphosphate. Journal of Phycology, 56(1) Article 1, 217–232.

Brook, A.J. & Williamson, D.B. (2010) A monograph on some British desmids. London, UK: The Ray Society, p. 364.

Busch, A. & Hess, S. (2022a) A diverse group of underappreciated zygnematophytes deserves in‐depth exploration. Applied Phycology, 3, 1–18.

Busch, A. & Hess, S. (2022b) Sunscreen mucilage: a photoprotective adaptation found in terrestrial green algae (Zygnematophyceae). European Journal of Phycology, 57(1), 107–124. Available from: https://doi.org/10.1080/09670262.2021.1898677

Coesel, P.F.M. & Meesters, K.J. (2007) Desmids of the lowlands: Mesotaeniaceae and Desmidiaceae of the European lowlands. Amsterdam, The Netherlands: BRILL.

Cook, J.M., Tedstone, A.J., Williamson, C., McCutcheon, J., Hodson, A.J., Dayal, A. et al. (2020) Glacier algae accelerate melt rates on the southwestern Greenland ice sheet. The Cryosphere, 14(1), 309–330. Available from: https://doi.org/10.5194/tc-14-309-2020

Dial, R.J., Ganey, G.Q. & Skiles, S.M. (2018) What color should glacier algae be? An ecological role for red carbon in the cryosphere. FEMS Microbiology Ecology, 94(3), fiy007. Available from: https://doi.org/10.1093/femsec/fiy007

Fürst‐Jansen, J.M.R., de Vries, S. & de Vries, J. (2020) Evo‐physio: on stress responses and the earliest land plants. Journal of Experimental Botany, 71(11), 3254–3269. Available from: https://doi.org/10.1093/jxb/eraa007

Garduño‐Solórzano, G., Martínez‐García, M., Scotta Hentschke, G., Lopes, G., Castelo Branco, R., Vasconcelos, V.M.O. et al. (2021) The phylogenetic placement of Temnogametum (Zygnemataceae) and description of Temnogametum iztacalense sp. nov., from a tropical high mountain lake in Mexico. European Journal of Phycology, 56(2), 159–173. Available from: https://doi.org/10.1080/09670262.2020.1789226

Geiger, R. (1954) Klassifikation der klimate nach W. Köppen. In: Landolt‐Börnstein: Zahlenwerte und Funktionen aus Physik, Chemie, Astronomie, Geophysik und Technik, Vol. 3. Berlin, Germany: Springer, pp. 603–607.

Gontcharov, A.A., Marin, B. & Melkonian, M. (2004) Are combined analyses better than single gene phylogenies? A case study using SSU rDNA and rbc L sequence comparisons in the Zygnematophyceae (Streptophyta). Molecular Biology and Evolution, 21(3), 612–624.

Hall, J.D. & McCourt, R.M. (2015) Chapter 9—conjugating green algae including desmids. In: Wehr, J.D., Sheath, R.G. & Kociolek, J.P. (Eds.) Freshwater algae of North America, 2nd edition. Cambridge, MA: Academic Press, pp. 429–457. Available from: https://doi.org/10.1016/B978-0-12-385876-4.00009-8

Hogetsu, T. & Yokoyama, M. (1979) Light, a nitrogen‐depleted medium and cell‐cell interaction in the conjugation process of Closterium ehrenbergii Meneghini. Plant and Cell Physiology, 20(4), 811–817. Available from: https://doi.org/10.1093/oxfordjournals.pcp.a075873

Jensen, M.B., Perini, L., Halbach, L., Jakobsen, H., Haraguchi, L., Ribeiro, S. et al. (2023) The dark art of cultivating glacier ice algae. Botany Letters, 1–10. Available from: https://doi.org/10.1080/23818107.2023.2248235

Kol, E. (1942) The snow and ice algae of Alaska, Vol. 101(16). Washington: The Smithsonian Institution, pp. 1–36.

Ling, H.U. & Seppelt, R.D. (1990) Snow algae of the Windmill Islands, continental Antarctica. Mesotaenium berggrenii (Zygnematales, Chlorophyta) the alga of grey snow. Antarctic Science, 2(2), 143–148. Available from: https://doi.org/10.1017/S0954102090000189

McFadden, G.I. & Melkonian, M. (1986) Use of HEPES buffer for microalgal culture media and fixation for electron microscopy. Phycologia, 25(4), 551–557.

Medlin, L., Elwood, H.J., Stickel, S. & Sogin, M.L. (1988) The characterization of enzymatically amplified eukaryotic 16S‐like rRNA‐coding regions. Gene, 71(2), 491–499. Available from: https://doi.org/10.1016/0378-1119(88)90066-2

Moye, J., Schenk, T. & Hess, S. (2022) Experimental evidence for enzymatic cell wall dissolution in a microbial protoplast feeder (Orciraptor agilis, Viridiraptoridae). BMC Biology, 20(1), 267. Available from: https://doi.org/10.1186/s12915-022-01478-x

Permann, C., Herburger, K., Felhofer, M., Gierlinger, N., Lewis, L.A. & Holzinger, A. (2021) Induction of conjugation and Zygospore Cell Wall characteristics in the alpine Spirogyra mirabilis (Zygnematophyceae, Charophyta): advantage under climate change scenarios? Plants, 10(8), 1740. Available from: https://doi.org/10.3390/plants10081740

Permann, C., Herburger, K., Niedermeier, M., Felhofer, M., Gierlinger, N. & Holzinger, A. (2021) Cell wall characteristics during sexual reproduction of Mougeotia sp. (Zygnematophyceae) revealed by electron microscopy, glycan microarrays and RAMAN spectroscopy. Protoplasma, 258(6), 1261–1275. Available from: https://doi.org/10.1007/s00709-021-01659-5

Permann, C., Gierlinger, N. & Holzinger, A. (2022) Zygospores of the green alga spirogyra: new insights from structural and chemical imaging. Frontiers in Plant Science, 13, 1080111. Available from: https://doi.org/10.3389/fpls.2022.1080111

Permann, C., Pichrtová, M., Šoljaková, T., Herburger, K., Jouneau, P.‐H., Uwizeye, C. et al. (2023) 3D‐reconstructions of zygospores in Zygnema vaginatum (Charophyta) reveal details of cell wall formation, suggesting adaptations to extreme habitats. Physiologia Plantarum, 175(4), e13988. Available from: https://doi.org/10.1111/ppl.13988

Pichrtová, M., Holzinger, A., Kulichová, J., Ryšánek, D., Šoljaková, T., Trumhová, K. et al. (2018) Molecular and morphological diversity of Zygnema and Zygnemopsis (Zygnematophyceae, Streptophyta) from Svalbard (high Arctic). European Journal of Phycology, 53(4), 492–508.

Poulíčková, A., Žižka, Z., Hašler, P. & Benada, O. (2007) Zygnematalean zygospores: morphological features and use in species identification. Folia Microbiologica, 52(2), 135–145. Available from: https://doi.org/10.1007/BF02932152

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 (Praha), 18(1), 1–18. Available from: https://doi.org/10.5507/fot.2017.010

Procházková, L., Řezanka, T., Nedbalová, L. & Remias, D. (2021) Unicellular versus filamentous: the glacial alga Ancylonema alaskana comb. et stat. nov. and its ecophysiological relatedness to Ancylonema nordenskioeldii (Zygnematophyceae, Streptophyta). Microorganisms, 9(5), 1103. Available from: https://doi.org/10.3390/microorganisms9051103

Remias, D. & Procházková, L. (2023) The first cultivation of the glacier ice alga Ancylonema alaskanum (Zygnematophyceae, Streptophyta): differences in morphology and photophysiology of field vs laboratory strain cells. Journal of Glaciology, 69(276), 1080–1084. Available from: https://doi.org/10.1017/jog.2023.22

Remias, D., Holzinger, A. & Lütz, C. (2009) Physiology, ultrastructure and habitat of the ice alga Mesotaenium berggrenii (Zygnemaphyceae, Chlorophyta) from glaciers in the European Alps. Phycologia, 48(4), 302–312. Available from: https://doi.org/10.2216/08-13.1

Remias, D., Holzinger, A., Aigner, S. & Lütz, C. (2012) Ecophysiology and ultrastructure of Ancylonema nordenskiöldii (Zygnematales, Streptophyta), causing brown ice on glaciers in Svalbard (high arctic). Polar Biology, 35(6) Article 6, 899–908.

Remias, D., Schwaiger, S., Aigner, S., Leya, T., Stuppner, H. & Lütz, C. (2012) Characterization of an UV‐and VIS‐absorbing, purpurogallin‐derived secondary pigment new to algae and highly abundant in M esotaenium berggrenii (Z ygnematophyceae, Chlorophyta), an extremophyte living on glaciers. FEMS Microbiology Ecology, 79(3) Article 3, 638–648.

Remias, D., Procházková, L., Nedbalová, L., Benning, L.G. & Lutz, S. (2023) Novel insights in cryptic diversity of snow and glacier ice algae communities combining 18S rRNA gene and ITS2 amplicon sequencing. FEMS Microbiology Ecology, 99(12), fiad134. Available from: https://doi.org/10.1093/femsec/fiad134

Stibal, M., Box, J.E., Cameron, K.A., Langen, P.L., Yallop, M.L., Mottram, R.H. et al. (2017) Algae drive enhanced darkening of bare ice on the Greenland ice sheet. Geophysical Research Letters, 44(22), 11463–11471. Available from: https://doi.org/10.1002/2017GL075958

Takano, T., Higuchi, S., Ikegaya, H., Matsuzaki, R., Kawachi, M., Takahashi, F. et al. (2019) Identification of 13 Spirogyra species (Zygnemataceae) by traits of sexual reproduction induced under laboratory culture conditions. Scientific Reports, 9(1), 7458.

Takeuchi, N. (2001) The altitudinal distribution of snow algae on an Alaska glacier (Gulkana glacier in the Alaska range). Hydrological Processes, 15(18), 3447–3459. Available from: https://doi.org/10.1002/hyp.1040

Takeuchi, N., Uetake, J., Fujita, K., Aizen, V.B. & Nikitin, S.D. (2006) A snow algal community on Akkem glacier in the Russian Altai mountains. Annals of Glaciology, 43, 378–384. Available from: https://doi.org/10.3189/172756406781812113

Takeuchi, N., Tanaka, S., Konno, Y., Irvine‐Fynn, T.D.L., Rassner, S.M.E. & Edwards, A. (2019) Variations in phototroph communities on the ablating bare‐ice surface of glaciers on Brøggerhalvøya, Svalbard. Frontiers in Earth Science, 7, 4. Available from: https://doi.org/10.3389/feart.2019.00004

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

Tiflickjian, J.D. & Raybum, W.R. (1986) Nutritional requirements for sexual reproduction in Mesotaenium Kramstai (chlorophyta) 1. Journal of Phycology, 22(1), 1–8. Available from: https://doi.org/10.1111/j.1529-8817.1986.tb02508.x

Timme, R.E., Bachvaroff, T.R. & Delwiche, C.F. (2012) Broad phylogenomic sampling and the sister lineage of land plants. PLoS One, 7(1), e29696.

de Vries, J., de Vries, S., Slamovits, C.H., Rose, L.E. & Archibald, J.M. (2017) How Embryophytic is the biosynthesis of Phenylpropanoids and their derivatives in Streptophyte algae? Plant and Cell Physiology, 58(5), 934–945. Available from: https://doi.org/10.1093/pcp/pcx037

de Vries, J., de Vries, S., Curtis, B.A., Zhou, H., Penny, S., Feussner, K. et al. (2020) Heat stress response in the closest algal relatives of land plants reveals conserved stress signaling circuits. The Plant Journal, 103(3), 1025–1048. Available from: https://doi.org/10.1111/tpj.14782

Walsby, A.E. (1997) Modelling the daily integral of photosynthesis by phytoplankton: its dependence on the mean depth of the population. Hydrobiologia, 349(1), 65–74. Available from: https://doi.org/10.1023/A:1003045528581

Wickett, N.J., Mirarab, S., Nguyen, N., Warnow, T., Carpenter, E., Matasci, N. et al. (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proceedings of the National Academy of Sciences of the United States of America, 111(45), E4859–E4868.

Williamson, C.J., Anesio, A.M., Cook, J., Tedstone, A., Poniecka, E., Holland, A. et al. (2018) Ice algal bloom development on the surface of the Greenland ice sheet. FEMS Microbiology Ecology, 94(3), fiy025. Available from: https://doi.org/10.1093/femsec/fiy025

Williamson, C.J., Cameron, K.A., Cook, J.M., Zarsky, J.D., Stibal, M. & Edwards, A. (2019) Glacier algae: a dark past and a darker future. Frontiers in Microbiology, 10, 1–8. Available from: https://doi.org/10.3389/fmicb.2019.00524

Williamson, C.J., Cook, J., Tedstone, A., Yallop, M., McCutcheon, J., Poniecka, E. et al. (2020) Algal photophysiology drives darkening and melt of the Greenland ice sheet. Proceedings of the National Academy of Sciences, 117(11), 5694–5705. Available from: https://doi.org/10.1073/pnas.1918412117

Wodniok, S., Brinkmann, H., Glöckner, G., Heidel, A.J., Philippe, H., Melkonian, M. et al. (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evolutionary Biology, 11(1), 104.

Yallop, M.L., Anesio, A.M., Perkins, R.G., Cook, J., Telling, J., Fagan, D. et al. (2012) Photophysiology and albedo‐changing potential of the ice algal community on the surface of the Greenland ice sheet. The ISME Journal, 6(12), 2302–2313. Available from: https://doi.org/10.1038/ismej.2012.107

Yamashita, T. & Sasaki, K. (1979) Conditions for the induction of the mating process and changes in contents of carbohydrates and nitrogen compounds during the mating process of spirogyra. Journal of the Faculty of Science, Hokkaido University, 11, 279–287.

Yoshimura, Y., Kohshima, S. & Ohtani, S. (1997) A Community of Snow Algae on a Himalayan glacier: change of algal biomass and community structure with altitude. Arctic and Alpine Research, 29(1), 126–137. Available from: https://doi.org/10.1080/00040851.1997.12003222

Zwirn, M., Chen, C., Uher, B. & Schagerl, M. (2013) Induction of sexual reproduction in spirogyra clones—does an universal trigger exist? Fottea, 13(1), 77–85. Available from: https://doi.org/10.5507/fot.2013.007

Phenolic Iron Complexes Protect Glacier Ice Algae (Zygnematophyceae) Against Excessive UV and VIS Irradiation

Genetic and morphological variation in the genus Zygogonium (Zygnematophyceae, Charophyta) from localities in Europe and North America and description of Z. angustum, sp. nov