Polar Biology

, Volume 39, Issue 9, pp 1653–1662 | Cite as

Annual development of mat-forming conjugating green algae Zygnema spp. in hydro-terrestrial habitats in the Arctic

Original Paper

Abstract

Conjugating green algae of the genus Zygnema (Zygnematophyceae, Streptophyta) are dominant eukaryotic components of hydro-terrestrial microbial mats in the Arctic. Considering the harsh environmental conditions, the aim of this study was to elucidate mechanisms that enable Zygnema spp. to thrive in this habitat. We hypothesized that changes in morphology, physiological performance, and stress tolerance take place during the annual life cycle of the algae. We thus selected four natural populations of Zygnema spp. on Svalbard and investigated them throughout the vegetation season by means of light microscopy and chlorophyll a fluorescence. Additionally, we also investigated one overwintering population. No formation of specialized resting stages (e.g., dormant zygospores) was observed. Markedly, Zygnema spp. survived harsh periods as modified vegetative cells, i.e., pre-akinetes. Pre-akinetes tolerate both desiccation during summer and freezing in winter. These cells are not dormant and therefore recover their physiological activity immediately after transfer to favorable conditions, undergoing rapid growth in the early spring. Nevertheless, once pre-akinetes begin to grow, these newly produced vegetative cells lose stress tolerance. Such rapid dehardening explains their high mortality due to frequent freeze–thaw cycles in the early spring. Arctic Zygnema spp. thus face a phenological trade-off between missing the early growing season and experiencing frost damage.

Keywords

Chlorophyll a fluorescence Desiccation Green algae Stress tolerance Svalbard Zygnematophyceae 

Supplementary material

300_2016_1889_MOESM1_ESM.tif (2.6 mb)
Online resource 1 (ESM1)Location of the investigated Zygnema spp. populations 1–4 in Petuniabukta, Svalbard (TIFF 2709 kb)
300_2016_1889_MOESM2_ESM.pdf (206 kb)
Online resource 2 (ESM2)Complete results of the statistical analyses used in the study: general linear model repeated-measures analysis of variance, Tukey’s post hoc test, and comparison of hyperbolae (PDF 206 kb)

References

  1. Adams WW III, Demmig-Adams B (2004) Chlorophyll fluorescence as a tool to monitor plant response to the environment. In: Papageorgiou GC (ed) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Berlin, pp 583–604CrossRefGoogle Scholar
  2. Aleksandrova VD (1988) The Arctic and Antarctic: their division into geobotanical areas. Cambridge University Press, CambridgeGoogle Scholar
  3. Arnold RJ, Convey P, Hughes KA, Wynn-Williams DD (2003) Seasonal periodicity of physical factors, inorganic nutrients and microalgae in Antarctic fellfields. Polar Biol 26:396–403Google Scholar
  4. Bischof K, Peralta G, Kräbs G, van de Poll WH, Pérez-Lloréns JL, Breeman AM (2002) Effects of solar UV-B radiation on canopy structure of Ulva communities from southern Spain. J Exp Bot 53:2411–2421CrossRefPubMedGoogle Scholar
  5. Bischoff HW, Bold HC (1963) Phycological studies IV. Univ Texas Publ No, Some soil algae from enchanted rock and related algal species 6318 Google Scholar
  6. Bisson MA, Kirst GO (1995) Osmotic acclimation and turgor pressure regulation in algae. Naturwissenschaften 82:461–471CrossRefGoogle Scholar
  7. Coleman AW (1983) The roles of resting spores and akinetes in chlorophyte survival. In: Fryxell GA (ed) Survival strategies of the algae. Cambridge University Press, Cambridge, pp 1–21Google Scholar
  8. Davey MC (1988) Ecology of terrestrial algae of the fellfield ecosystems of Signy Island, South Orkney Islands. Brit Antarct Surv B 81:69–74Google Scholar
  9. Davey MC (1989) The effects of freezing and desiccation on photosynthesis and survival of terrestrial Antarctic algae and Cyanobacteria. Polar Biol 10:29–36CrossRefGoogle Scholar
  10. Davey MC (1991a) The seasonal periodicity of algae on Antarctic fellfield soils. Holarctic Ecol 14:112–120Google Scholar
  11. Davey MC (1991b) Effects of physical factors on the survival and growth of Antarctic terrestrial algae. Brit Phycol J 26:315–325CrossRefGoogle Scholar
  12. Davey MC, Rothery P (1992) Factors causing the limitation of growth of terrestrial algae in maritime Antarctica during late summer. Polar Biol 12:595–601CrossRefGoogle Scholar
  13. De los Ríos A, Wierzchos J, Sancho LG, Ascaso C (2004) Exploring the physiological state of continental Antarctic endolithic microorganisms by microscopy. FEMS Microbiol Ecol 50:143–152CrossRefPubMedGoogle Scholar
  14. Elster J (2002) Ecological classification of terrestrial algal communities in polar environments. In: Beyer L, Bölter M (eds) Geoecology of Antarctic ice-free coastal landscapes, ecological studies, vol 154. Springer, Berlin, pp 303–326CrossRefGoogle Scholar
  15. Elster J, Rachlewicz G (2012) Petuniabukta, Billefjorden in Svalbard: Czech-Polish long term ecological and geographical research. Pol Polar Res 33:289–295Google Scholar
  16. 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. Algol Stud 85:57–93Google Scholar
  17. Fuller C (2013) Examining morphological and physiological changes in Zygnema irregulare during a desiccation and recovery period. M. Sc. thesis, California State University San MarcosGoogle Scholar
  18. Genkel PA, Pronina ND (1979) Ecology of Zygnema stellinum Vauch. during desiccation of a shallow body of water. Biol Bull Acad Sci USSR 6:504–509PubMedGoogle Scholar
  19. Gray DW, Lewis LA, Cardon ZG (2007) Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant, Cell Environ 30:1240–1255CrossRefGoogle Scholar
  20. Hawes I (1988) The seasonal dynamics of Spirogyra in a shallow maritime antarctic lake. Polar Biol 8:429–437CrossRefGoogle Scholar
  21. Hawes I (1990) Effects of freezing and thawing on a species of Zygnema (Chlorophyta) from the Antarctic. Phycologia 29:326–331CrossRefGoogle Scholar
  22. 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 252:571–589CrossRefPubMedGoogle Scholar
  23. Hogan EJ, McGowan S, Anderson NJ (2014) Nutrient limitation of periphyton growth in arctic lakes in south-west Greenland. Polar Biol 37:1331–1342CrossRefGoogle Scholar
  24. Holzinger A, Karsten U (2013) Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms. Front Plant Sci 4:327CrossRefPubMedPubMedCentralGoogle Scholar
  25. Holzinger A, Pichrtová M (2016) Abiotic stress tolerance in charophyte green algae: new challenges for omics techniques. Front Plant Sci 7:678CrossRefPubMedPubMedCentralGoogle Scholar
  26. Holzinger A, Roleda MY, Lütz C (2009) The vegetative arctic freshwater green alga Zygnema is insensitive to experimental UV exposure. Micron 40:831–838CrossRefPubMedGoogle Scholar
  27. Jackson AE, Seppelt RD (1995) The accumulation of proline in Prasiola crispa during winter in Antarctica. Physiol Plantarum 94:25–30CrossRefGoogle Scholar
  28. Kadlubowska JZ (1984) Conjugatophyceae I: Chlorophyta VIII: Zygnemales. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) Süsswasserflora von Mitteleuropa, vol 16. Gustav Fisher, JenaGoogle Scholar
  29. 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 44:317–330CrossRefPubMedPubMedCentralGoogle Scholar
  30. Karsten U, Pröschold T, Mikhailyuk T, Holzinger A (2013) Photosynthetic performance of different genotypes of the green alga Klebsormidium sp. (Streptophyta) isolated from biological soil crusts of the Alps. Algol Stud 142:45–62CrossRefGoogle Scholar
  31. Kim GH, Klochkova TA, Kang SH (2008) Notes on freshwater and terrestrial algae from Ny-Ålesund, Svalbard (high Arctic sea area). J Environ Biol 29:485–491PubMedGoogle Scholar
  32. Knowles EJ, Castenholz RW (2008) Effect of exogenous extracellular polysaccharides on the desiccation and freezing tolerance of rock-inhabiting phototrophic microorganisms. FEMS Microbiol Ecol 66:261–270CrossRefPubMedGoogle Scholar
  33. Komárek J, Kováčik L, Elster J, Komárek O (2012) Cyanobacterial diversity of Petunia-Bukta, Billefjorden, central Svalbard. Pol Polar Res 33:347–368Google Scholar
  34. Kvíderová J, Lukavský J (2001) A new unit for crossed gradients of temperature and light. Nova Hedwig Beih 123:541–550Google Scholar
  35. Láska K, Witoszová D, Prošek P (2012) Weather patterns of the coastal zone of Petuniabukta, central Spitsbergen in the period 2008–2010. Pol Polar Res 33:297–318Google Scholar
  36. Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, De Clerck O (2012) Phylogeny and molecular evolution of the green algae. Crit Rev Plant Sci 31:1–46CrossRefGoogle Scholar
  37. Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. In: Wrolstad RE, Acree TE, An H, Decker EA, Penner MH, Reid DS, Schwartz SJ, Shoemaker CF, Sporns P (eds) Current protocols in food analytical chemistry (CPFA). Wiley, New York, pp F4.3.1–F4.3.8Google Scholar
  38. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefPubMedGoogle Scholar
  39. McLean RJ, Pessoney GF (1971) Formation and resistance of akinetes of Zygnema. In: Parker BC, Brown RM Jr (eds) Contributions in phycology. Allen, Lawrence, pp 145–152Google Scholar
  40. Olofsson M, Lamela T, Nilsson E, Bergé JP, del Pino V, Uronen P, Legrand C (2012) Seasonal variation of lipids and fatty acids of the microalgae Nannochloropsis oculata grown in outdoor large-scale photobioreactors. Energies 5:1577–1592CrossRefGoogle Scholar
  41. Park JC, Choi SP, Hong M-E, Sim SJ (2014) Enhanced astaxanthin production from microalga, Haematococcus pluvialis by two-stage perfusion culture with stepwise light irradiation. Bioproc Biosyst Eng 37:2039–2047CrossRefGoogle Scholar
  42. 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 65:68–83CrossRefPubMedGoogle Scholar
  43. 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 Microbiol Ecol 89:270–280CrossRefPubMedGoogle Scholar
  44. 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:e113137CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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 Microbiol Ecol 92:fiw096CrossRefPubMedPubMedCentralGoogle Scholar
  46. Poulíčková A, Žižka Z, Hašler P, Benada O (2007) Zygnematalean zygospores: morphological features and use in species identification. Folia Microbiol 52:135–145CrossRefGoogle Scholar
  47. Rautio M, Dufresne F, Laurion I, Bonilla S, Vincent WF, Christoffersen KS (2011) Shallow freshwater ecosystems of the circumpolar Arctic. Ecoscience 18:204–222CrossRefGoogle Scholar
  48. Richmond A, Hu Q (2013) Handbook of microalgal culture: applied phycology and biotechnology, 2nd edn. Wiley-Blackwell, LondonCrossRefGoogle Scholar
  49. Robinson SA, Wasley J, Tobin AK (2003) Living on the edge—plants and global change in continental and maritime Antarctica. Global Change Biol 9:1681–1717CrossRefGoogle Scholar
  50. Šabacká M, Elster J (2006) Response of Cyanobacteria and algae from Antarctic wetland habitats to freezing and desiccation stress. Polar Biol 30:31–37CrossRefGoogle Scholar
  51. Seaburg KG, Parker BC, Wharton RA Jr, Simmons GM Jr (1981) Temperature-growth responses of algal isolates from Antarctic oases. J Phycol 17:353–360CrossRefGoogle Scholar
  52. Sheath RG, Vis ML, Hambrook JA, Cole KM (1996) Tundra stream macroalgae of North America: composition, distribution and physiological adaptations. Hydrobiologia 336:67–82CrossRefGoogle Scholar
  53. Stancheva R, Sheath RG, Hall JD (2012) Systematics of the genus Zygnema (Zygnematophyceae, Charophyta) from Californian watersheds. J Phycol 48:409–422CrossRefPubMedGoogle Scholar
  54. Tang EPY, Tremblay R, Vincent WF (1997) Cyanobacterial dominance of polar freshwater ecosystems: are high-latitude mat-formers adapted to low temperature? J Phycol 33:171–181CrossRefGoogle Scholar
  55. Tashyreva D, Elster J (2012) Production of dormant stages and stress resistance of polar cyanobacteria. In: Hanslmaier A, Kempe S, Seckbach J (eds) Life on Earth and other planetary bodies. Springer, Dordrecht, pp 367–386CrossRefGoogle Scholar
  56. Thomas DN, Fogg GE, Convey P, Fritsen CH, Gili J-M, Gradinger R, Laybourn-Parry J, Reid K, Walton DWH (2008) The biology of polar regions. Oxford University Press, OxfordCrossRefGoogle Scholar
  57. Vincent WF (2000) Cyanobacterial dominance in the polar regions. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria—their diversity in time and space. Kluwer, Dordrecht, pp 321–340Google Scholar
  58. Zwolicki A, Zmudczynska-Skarbek KM, Iliszko L, Stempniewicz L (2013) Guano deposition and nutrient enrichment in the vicinity of planktivorous and piscivorous seabird colonies in Spitsbergen. Polar Biol 36:363–372CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Martina Pichrtová
    • 1
  • Tomáš Hájek
    • 2
    • 3
  • Josef Elster
    • 2
    • 3
  1. 1.Department of Botany, Faculty of ScienceCharles University in PraguePragueCzech Republic
  2. 2.Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic
  3. 3.Institute of BotanyCzech Academy of SciencesTřeboňCzech Republic

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