BACKGROUND: Filamentous Zygnematophyceae are typical components of algal mats in the polar hydro-terrestrial environment. Under field conditions, they form senescent vegetative cells, designated as pre-akinetes, which are tolerant to desiccation and osmotic stress. KEY FINDINGS: Pre-akinete formation and desiccation tolerance was investigated experimentally under monitored laboratory conditions in four strains of Arctic and Antarctic isolates with vegetative Zygnema sp. morphology. Phylogenetic analyses of rbcL sequences revealed one Arctic strain as genus Zygnemopsis, phylogenetically distant from the closely related Zygnema strains. Algae were cultivated in liquid or on solidified medium (9 weeks), supplemented with or lacking nitrogen. Nitrogen-free cultures (liquid as well as solidified) consisted of well-developed pre-akinetes after this period. Desiccation experiments were performed at three different drying rates (rapid: 10% relative humidity, slow: 86% rh and very slow); viability, effective quantum yield of PS II, visual and ultrastructural changes were monitored. Recovery and viability of pre-akinetes were clearly dependent on the drying rate: slower desiccation led to higher levels of survival. Pre-akinetes survived rapid drying after acclimation by very slow desiccation. CONCLUSIONS: The formation of pre-akinetes in polar Zygnema spp. and Zygnemopsis sp. is induced by nitrogen limitation. Pre-akinetes, modified vegetative cells, rather than specialized stages of the life cycle, can be hardened by mild desiccation stress to survive rapid drying. Naturally hardened pre-akinetes play a key role in stress tolerance and dispersal under the extreme conditions of polar regions, where sexual reproduction and production of dormant stages is largely suppressed.

Charles University Prague Faculty of Science Department of Botany Prague Czech Republic

Charles University Prague Faculty of Science Department of Botany Prague Czech Republic; Academy of Sciences of the Czech Republic Institute of Botany Třeboň Czech Republic

University of Innsbruck Institute of Botany Functional Plant Biology Innsbruck Austria

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Rindi F, Allali HA, Lam DW, López-Bautista JM (2009) An overview of the biodiversity and biogeography of terrestrial green algae. In: Rescigno V, Maletta S, editors. Biodiversity Hotspots. Nova Science Publishers, Inc. pp. 105–122.

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

Lewis LA, Lewis PO (2005) Unearthing the molecular phylodiversity of desert soil green algae (Chlorophyta). Syst Biol 54: 936–947. PubMed

Cardon ZG, Gray DW, Lewis LA (2008) The green algal underground: evolutionary secrets of desert cells. Bioscience 58: 114–122.

Sanderson MJ, Thorne JL, Wikström N, Bremer K (2004) Molecular evidence on plant divergence times. Am J Bot 91: 1656–1665. PubMed

Wodniok S, Brinkmann H, Glöckner G, Heidel AJ, Philippe H, et al. (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evol Biol 11: 104. PubMed PMC

Timme RE, Bachvaroff TR, Delwiche CF (2012) Broad phylogenomic sampling and the sister lineage of land plants. PLoS One 7: e29696. PubMed PMC

Zhong B, Liu L, Yan Z, Penny D (2013) Origin of land plants using the multispecies coalescent model. Trends Plant Sci 18: 492–495. PubMed

Zhong B, Xi Z, Goremykin VV, Fong R, McLenachan PA, et al. (2014) Streptophyte algae and the origin of land plants revisited using heterogeneous models with three new algal chloroplast genomes. Mol Biol Evol 31: 177–183. PubMed

Kadlubowska JZ (1984) Conjugatophyceae I: Chlorophyta VIII: Zygnemales. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D, editors. Süsswasserflora von Mitteleuropa, Band 16. Jena: Gustav Fisher. pp. 1–532.

Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, et al. (2012) Phylogeny and molecular evolution of the green algae. CRC Crit Rev Plant Sci 31: 1–46.

Štastný J (2008) Desmids from ephemeral pools and aerophytic habitats from the Czech Republic. Biologia 63: 888–894.

Marshall WA, Chalmers MO (1997) Airborne dispersal of antarctic terrestrial algae and Cyanobacteria. Ecography 20: 585–594.

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: 302–312.

Remias D, Holzinger A, Aigner S, Lütz C (2011) Ecophysiology and ultrastructure of Ancylonema nordenskiöldii (Zygnematales, Streptophyta), causing brown ice on glaciers in Svalbard (high Arctic). Polar Biol 35: 899–908.

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

Kim GH, Klochkova TA, Kang SH (2008) Notes on freshwater and terrestrial algae from Ny-Ålesund, Svalbard (high Arctic sea area). J Environ Biol 29: 485–491. PubMed

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

Kim GH, Klochkova TA, Han JW, Kang S, Choi HG, et al. (2011) Freshwater and terrestrial algae from Ny-Ålesund and Blomstrandhalvøya Island (Svalbard). Arctic 64: 25–31. PubMed

Vilumbrales DM, Skácelová K, Barták M (2013) Sensitivity of Antarctic freshwater algae to salt stress assessed by fast chlorophyll fluorescence transient. Czech Polar Reports 3: 163–172.

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

Elster J, Svoboda J, Komárek J, Marvan P (1997) Algal and cyanoprocaryote communities in a glacial stream, Sverdrup Pass, 79°N, Central Ellesmere Island, Canada. Arch Hydrobiol Suppl Algol Stud 85: 57–93.

Büdel B (2011) Eukaryotic algae. In: Lüttge U, Beck E, Bartels D, editors. Plant desiccation tolerance. Springer. pp. 45–61.

Karsten U, Holzinger A (2014) Green algae in alpine biological soil crust communities: acclimation strategies against ultraviolet radiation and dehydration. Biodivers Conserv 23: 1845–1858. PubMed PMC

Karsten U, Holzinger A (2012) Light, temperature, and desiccation effects on photosynthetic activity, and drought-induced ultrastructural changes in the green alga Klebsormidium dissectum (Streptophyta) from a high alpine soil crust. Microb Ecol 63: 51–63. PubMed

Gray DW, Lewis LA, Cardon ZG (2007) Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant Cell Environ 30: 1240–1255. PubMed

Gasulla F, de Nova PG, Esteban-Carrasco A, Zapata JM, Barreno E, et al. (2009) Dehydration rate and time of desiccation affect recovery of the lichen alga Trebouxia erici: alternative and classical protective mechanisms. Planta 231: 195–208. PubMed

McLean RJ, Pessoney GF (1971) Formation and resistance of akinetes of Zygnema. In: Parker BC, Brown Jr RM, editors. Contributions in phycology. Allen. pp. 145–152.

Coleman AW (1983) The roles of resting spores and akinetes in chlorophyte survival. In: Fryxell GA, editor. Survival Strategies of the Algae. Cambridge: Cambridge University Press. pp. 1–21.

Morison MO, Sheath RG (1985) Response to desiccation stress by Klebsormidium rivulare (Ulotrichales, Chlorophyta) from a Rhode Island stream. Phycologia 24: 129–145.

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

Fuller C (2013) Examining morphological and physiological changes in Zygnema irregulare during a desiccation and recovery period. M. Sc. Thesis, California State University San Marcos.

Herburger K, Lewis LA, Holzinger A (2014) Photosynthetic efficiency, desiccation tolerance and ultrastructure in two phylogenetically distinct strains of alpine Zygnema sp. (Zygnematophyceae, Streptophyta): Role of pre-akinete formation. Protoplasma DOI 10.1007s0070901407033/s00709-014-0703-3 PubMed DOI PMC

Genkel PA, Pronina ND (1979) Ecology of Zygnema stellinum Vauch. during desiccation of a shallow body of water. Biol Bull Acad Sci USSR 6: 504–509. PubMed

Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: A review. Renew Sustain Energy Rev 14: 217–232.

Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, et al. (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54: 621–639. PubMed

Pichrtová M, Remias D, Lewis LA, Holzinger A (2013) Changes in phenolic compounds and cellular ultrastructure of arctic and antarctic strains of Zygnema (Zygnematophyceae, Streptophyta) after exposure to experimentally enhanced UV to PAR ratio. Microb Ecol 65: 68–83. PubMed PMC

Bischoff HW, Bold HC (1963) Phycological studies IV. Some soil algae from enchanted rock and related algal species. Univ Texas Publ No 6318.

McCourt RM, Karol KG, Bell J, Helm-Bychowski KM, Grajewska A, et al. (2000) Phylogeny of the conjugating green algae (Zygnemophyceae) based on rbcL sequences. J Phycol 36: 747–758. PubMed

Hall JD, Karol KG, McCourt RM, Delwiche CF (2008) Phylogeny of the conjugating green algae based on chloroplast and mitochondrial nucleotide sequence data. J Phycol 44: 467–477. PubMed

Stancheva R, Sheath RG, Hall JD (2012) Systematics of the genus Zygnema (Zygnematophyceae, Charophyta) from Californian watersheds. J Phycol 48: 409–422. PubMed

Nylander JAA (2004) MrModeltest 2.3. Distributed by the author. Evolutionary Biology Centre, Uppsala University, Sweden.

Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. PubMed

Rambaut A (2009) FigTree, Tree Figure drawing tool. Available: http://tree.bio.ed.ac.uk/software/figtree/.

Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph. D. Thesis, University of Texas at Austin, USA.

Swofford DL (2002) PAUP*4.0b10. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, Massachusetts, USA.

Karsten U, Herburger K, Holzinger A (2014) Dehydration, temperature and light tolerance in members of the aeroterrestrial green algal genus Interfilum (Streptophyta) from biogeographically different temperate soils. J Phycol 50: 804–816. PubMed PMC

Roháček K, Barták M (1999) Technique of the modulated chlorophyll fluorescence: basic concepts, useful parameters, and some applications. Photosynthetica 37: 339–363.

Ellis EA (2006) Solutions to the problem of substitution of ERL 4221 for vinyl cyclo-hexene dioxide in Spurr low viscosity embedding formulations. Micros Today 14: 32–33.

Guarnieri MT, Nag A, Smolinski SL, Darzins A, Seibert M, et al. (2011) Examination of triacylglycerol biosynthetic pathways via de novo transcriptomic and proteomic analyses in an unsequenced microalga. PLoS One 6: e25851. PubMed PMC

Shiratake T, Sato A, Minoda A, Tsuzuki M, Sato N (2013) Air-drying of cells, the novel conditions for stimulated synthesis of triacylglycerol in a Green Alga, Chlorella kessleri . PLoS One 8: e79630. PubMed PMC

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

Holzinger A, Lütz C, Karsten U (2011) Desiccation stress causes structural and ultrastructural alterations in the aeroterrestrial green alga Klebsormidium crenulatum (Klebsormidiophyceae, Streptophyta) isolated from an alpine soil crust. J Phycol 47: 591–602. PubMed

Gasulla F, Jain R, Barreno E, Guéra A, Balbuena TS, et al. (2013) The response of Asterochloris erici (Ahmadjian) Skaloud et Peksa to desiccation: a proteomic approach. Plant Cell Environ 36: 1363–1378. PubMed

Cruz de Carvalho R, Bernardes ds Silva A, Soares R, Almeida AM, Coelho AV, et al. (2014) Differential proteomics of dehydration and rehydration in bryophytes: evidence towards a common desiccation tolerance mechanism. Plant Cell Environ 37: 1499–1515. PubMed

Darling RB, Friedmann EI, Broady PA (1987) Heterococcus endolithicus sp. nov. (Xanthophyceae) and other terrestrial Heterococcus species from Antarctica: morphological changes during life history and reponse to temperature. J Phycol 23: 598–607. PubMed

Hoppert M, Reimer R, Kemmling A, Schröder A, Günzl B, et al. (2004) Structure and reactivity of a biological soil crust from a xeric sandy soil in Central Europe. Geomicrobiol J 21: 183–191.

Bartels D, Lüttge U, Beck E (2011) Introduction. In: Lüttge U, Beck E, Bartels D, editors. Plant desiccation tolerance. Springer. pp. 3–10.

Post A, Larkum AWD (1993) UV-absorbing pigments, photosynthesis and UV exposure in Antarctica: comparison of terrestrial and marine algae. Aquat Bot 45: 231–243.

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51: 659–668. PubMed

Štastný J (2010) Desmids (Conjugatophyceae, Viridiplantae) from the Czech Republic; new and rare taxa, distribution, ecology. Fottea 10: 1–74.

Fritsch FE (1916) The morphology and ecology of an extreme terrestrial form of Zygnema ericetorum (Kutz.) Hass. Ann Bot 30: 135–149.

Holzinger A, Tschaikner A, Remias D (2010) Cytoarchitecture of the desiccation-tolerant green alga Zygogonium ericetorum . Protoplasma 243: 15–24. PubMed

Aigner S, Remias D, Karsten U, Holzinger A (2013) Unusual phenolic compounds contribute to ecophysiological performance in the purple-colored green alga Zygogonium ericetorum (Zygnematophyceae, Streptophyta) from a high-alpine habitat. J Phycol 49: 648–660. PubMed PMC

Stancheva R, Hall JD, Herburger K, Lewis LA, McCourt RM, et al. (2014) Phylogenetic position of Zygogonium ericetorum (Zygnematophyceae, Charophyta) from a high alpine habitat and ultrastructural characterization of unusual aplanospores. J Phycol 50: 790–803. PubMed PMC

3D-reconstructions of zygospores in Zygnema vaginatum (Charophyta) reveal details of cell wall formation, suggesting adaptations to extreme habitats

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

Pre-akinete formation in Zygnema sp. from polar habitats is associated with metabolite re-arrangement

The conjugating green alga Zygnema sp. (Zygnematophyceae) from the Arctic shows high frost tolerance in mature cells (pre-akinetes)

Metatranscriptomic and metabolite profiling reveals vertical heterogeneity within a Zygnema green algal mat from Svalbard (High Arctic)

Molecular and morphological diversity of Zygnema and Zygnemopsis (Zygnematophyceae, Streptophyta) from Svalbard (High Arctic)

Arctic, Antarctic, and temperate green algae Zygnema spp. under UV-B stress: vegetative cells perform better than pre-akinetes

Evolutionarily Distant Streptophyta Respond Differently to Genotoxic Stress

Terrestrial adaptation of green algae Klebsormidium and Zygnema (Charophyta) involves diversity in photosynthetic traits but not in CO2 acquisition

Formation of lipid bodies and changes in fatty acid composition upon pre-akinete formation in Arctic and Antarctic Zygnema (Zygnematophyceae, Streptophyta) strains

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