In streptophytic green algae in the genus Zygnema, pre-akinete formation is considered a key survival strategy under extreme environmental conditions in alpine and polar regions. The transition from young, dividing cells to pre-akinetes is associated with morphological changes and the accumulation of storage products. Understanding the underlying metabolic changes could provide insights into survival strategies in polar habitats. Here, GC-MS-based metabolite profiling was used to study the metabolic signature associated with pre-akinete formation in Zygnema sp. from polar regions under laboratory conditions, induced by water and nutrient depletion, or collected in the field. Light microscopy and TEM revealed drastic changes in chloroplast morphology and ultrastructure, degradation of starch grains, and accumulation of lipid bodies in pre-akinetes. Accordingly, the metabolite profiles upon pre-akinete formation reflected a gradual shift in metabolic activity. Compared with young cells, pre-akinetes showed an overall reduction in primary metabolites such as amino acids and intermediates of the tricarboxylic acid (TCA) cycle, consistent with a lower metabolic turnover, while they accumulated lipids and oligosaccharides. Overall, the transition to the pre-akinete stage involves re-allocation of photosynthetically fixed energy into storage instead of growth, supporting survival of extreme environmental conditions.

Charles University Faculty of Science Department of Botany Prague Czech Republic

University of Innsbruck Department of Botany Innsbruck Austria

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Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate—a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B: Statistical Methodology 57, 289–300.

Bischoff HW, Bold HC. 1963. Some soil algae from enchanted rock and related algal species. Austin, TX: University of Texas.

Deng S, Wei T, Tan K, et al. . 2016. Phytosterol content and the campesterol:sitosterol ratio influence cotton fiber development: role of phytosterols in cell elongation. Science China. Life Sciences 59, 183–193. PubMed

de Vries J, Archibald JM. 2018. Plant evolution: landmarks on the path to terrestrial life. New Phytologist 217, 1428–1434. PubMed

de Vries J, Curtis BA, Gould SB, Archibald JM. 2018. Embryophyte stress signaling evolved in the algal progenitors of land plants. Proceedings of the National Academy of Sciences, USA 115, E3471–E3480. PubMed PMC

Fiehn O, Wohlgemuth G, Scholz M, Kind T, Lee DY, Lu Y, Moon S, Nikolau B. 2008. Quality control for plant metabolomics: reporting MSI-compliant studies. The Plant Journal 53, 691–704. PubMed

Fiehn O. 2016. Metabolomics by gas chromatography-mass spectrometry: combined targeted and untargeted profiling. Current Protocols in Molecular Biology 114, 30.4.1–30.4.32. PubMed PMC

Gutbrod K, Romer J, Dörmann P. 2019. Phytol metabolism in plants. Progress in Lipid Research 74, 1–17. PubMed

Hawes I. 1990. Effects of freezing and thawing on a species of Zygnema (Chlorophyta) from the Antarctic. Phycologia 29, 326–331.

Herburger K, Lewis LA, Holzinger A. 2015. Photosynthetic efficiency, desiccation tolerance and ultrastructure in two phylogenetically distinct strains of alpine Zygnema sp. (Zygnematophyceae, Streptophyta): role of pre-akinete formation. Protoplasma 252, 571–589. PubMed PMC

Holzinger A, Albert A, Aigner S, Uhl J, Schmitt-Kopplin P, Trumhová K, Pichrtová M. 2018. Arctic, Antarctic, and temperate green algae Zygnema spp. under UV-B stress: vegetative cells perform better than pre-akinetes. Protoplasma 255, 1239–1252. PubMed PMC

Holzinger A, Kaplan F, Blaas K, Zechmann B, Komsic-Buchmann K, Becker B. 2014. Transcriptomics of desiccation tolerance in the streptophyte green alga Klebsormidium reveal a land plant-like defense reaction. PLoS One 9, e110630. PubMed PMC

Holzinger A, Karsten U. 2013. Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms. Frontiers in Plant Science 4, 327. PubMed PMC

Holzinger A, Roleda MY, Lütz C. 2009. The vegetative arctic freshwater green alga Zygnema is insensitive to experimental UV exposure. Micron 40, 831–838. PubMed

Horemans N, Foyer CH, Potters G, Asard H. 2000. Ascorbate function and associated transport systems in plants. Plant Physiology and Biochemistry 38, 531–540.

Kaplan F, Lewis LA, Herburger K, Holzinger A. 2013. Osmotic stress in Arctic and Antarctic strains of the green alga Zygnema (Zygnematales, Streptophyta): effects on photosynthesis and ultrastructure. Micron 44, 317–330. PubMed PMC

Kind T, Wohlgemuth G, Lee DY, Lu Y, Palazoglu M, Shahbaz S, Fiehn O. 2009. FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Analytical Chemistry 81, 10038–10048. PubMed PMC

Kopka J, Schauer N, Krueger S, et al. . 2005. GMD@CSB.DB: the golm metabolome database. Bioinformatics 21, 1635–1638. PubMed

Kováts E. 1958. Gas-chromatographische Charakterisierung organischer Verbindungen. Teil 1: Retentionsindices aliphatischer halogenide, alkohole, aldehyde und ketone. Helvetica Chimica Acta 41, 1915–1932.

Lutz S, Anesio AM, Field K, Benning LG. 2015. Integrated ‘omics’, targeted metabolite and single-cell analysis of arctic snow algae functionality and adaptability. Frontiers Microbiology 6, 1323. PubMed PMC

McLean RJ, Pessoney GF. 1971. Formation and resistance of akinetes of Zygnema. In: Parker BC, Brown RM Jr, eds. Contributions in phycology. Lawrence, KS: Allen, 145–152.

Pichrtová M, Arc E, Stöggl W, Kranner I, Hájek T, Hackl H, Holzinger A. 2016a 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

Pichrtová M, Hájek T, Elster J. 2014a Osmotic stress and recovery in field populations of Zygnema sp. (Zygnematophyceae, Streptophyta) on Svalbard (High Arctic) subjected to natural desiccation. FEMS Microbiology Ecology 89, 270–280. PubMed

Pichrtová M, Hájek T, Elster J. 2016b Annual development of mat-forming conjugating green algae Zygnema spp. in hydro-terrestrial habitats in the Arctic. Polar Biology 39, 1653–1662.

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

Pichrtová M, Kulichová J, Holzinger A. 2014b Nitrogen limitation and slow drying induce desiccation tolerance in conjugating green algae (Zygnematophyceae, Streptophyta) from polar habitats. PLoS One 9, e113137. PubMed PMC

R Core Team 2019. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; https://www.R-project.org/.

Rippin M, Becker B, Holzinger A. 2017. enhanced desiccation tolerance in mature cultures of the streptophytic green alga Zygnema circumcarinatum revealed by transcriptomics. Plant & Cell Physiology 58, 2067–2084. PubMed PMC

Rippin M, Pichrtová M, Arc E, Kranner I, Becker B, Holzinger A. 2019. Metatranscriptomic and metabolite profiling reveals vertical heterogeneity within a Zygnema green algal mat from Svalbard (High Arctic). Environmental Microbiology 21, 4283–4299. PubMed PMC

Sengupta S, Mukherjee S, Basak P, Majumder AL. 2015. Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Frontiers in Plant Science 6, 656. PubMed PMC

Solovchenko AE. 2012. Physiological role of neutral lipid accumulation in eukaryotic microalgae under stresses. Russian Journal of Plant Physiology 59, 167–176.

Stein SE. 1999. An integrated method for spectrum extraction and compound identification from gas chromatography/mass spectrometry data. Journal of the American Society for Mass Spectrometry 10, 770–781.

Tohge T, Watanabe M, Hoefgen R, Fernie AR. 2013. Shikimate and phenylalanine biosynthesis in the green lineage. Frontiers in Plant Science 4, 62. PubMed PMC

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, 1681–1694. PubMed PMC

Vítová M, Bišová K, Kawano S, Zachleder V. 2014. Accumulation of energy reserves in algae: from cell cycles to biotechnological applications. Biotechnology Advances 33, 1204–1218. PubMed

Ward JH. 1963. Hierarchical grouping to optimize an objective function. Journal of the American Statistical Association 58, 236–244.

Wickham H. 2016. ggplot2. Elegant graphics for data analysis. New York: Springer-Verlag.

Wodniok S, Brinkmann H, Glöckner G, Heidel AJ, Philippe H, Melkonian M, Becker B. 2011. Origin of land plants: do conjugating green algae hold the key? BMC Evolutionary Biology 11, 104. PubMed PMC

Seasonal Dynamics of Zygnema (Zygnematophyceae) Mats from the Austrian Alps

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