, Volume 21, Issue 1, pp 187–200 | Cite as

Identity, ecology and ecophysiology of planktic green algae dominating in ice-covered lakes on James Ross Island (northeastern Antarctic Peninsula)

  • Linda NedbalováEmail author
  • Martin Mihál
  • Jana Kvíderová
  • Lenka Procházková
  • Tomáš Řezanka
  • Josef Elster
Original Paper


The aim of this study was to assess the phylogenetic relationships, ecology and ecophysiological characteristics of the dominant planktic algae in ice-covered lakes on James Ross Island (northeastern Antarctic Peninsula). Phylogenetic analyses of 18S rDNA together with analysis of ITS2 rDNA secondary structure and cell morphology revealed that the two strains belong to one species of the genus Monoraphidium (Chlorophyta, Sphaeropleales, Selenastraceae) that should be described as new in future. Immotile green algae are thus apparently capable to become the dominant primary producer in the extreme environment of Antarctic lakes with extensive ice-cover. The strains grew in a wide temperature range, but the growth was inhibited at temperatures above 20 °C, indicating their adaptation to low temperature. Preferences for low irradiances reflected the light conditions in their original habitat. Together with relatively high growth rates (0.4–0.5 day−1) and unprecedently high content of polyunsaturated fatty acids (PUFA, more than 70% of total fatty acids), it makes these isolates interesting candidates for biotechnological applications.


Monoraphidium Ice-covered lakes Antarctica Phylogeny Ecology Temperature Light Fatty acids 



The research was supported by the CzechPolar project LM2010009 and CzechPolar2 project LM2015078 supported by Ministry of Education Youth and Sports of the Czech Republic, Czech Science Foundation (GACR) project P503 14-00227S and by the Institutional Internal Project RVO67985939. We are indebted particularly to the staff and scientific infrastructure of the J. G. Mendel Czech Antarctic Station.


  1. Allen MM (1968) Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 4:1–4CrossRefPubMedGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  3. Bischoff HW, Bold HC (1963) Phycological studies IV. Some soil algae from enchanted rock and related algal species. Univ Tex Austin 6318:1–95Google Scholar
  4. Butler HG, Edworthy MG, Ellis-Evans JC (2000) Temporal plankton dynamics in an oligotrophic maritime Antarctic lake. Freshw Biol 43:215–230CrossRefGoogle Scholar
  5. Caisová L, Marin B, Melkonian M (2011) A close-up view on ITS2 evolution and speciation—a case study in the Ulvophyceae (Chlorophyta, Viridiplantae). BMC Evol Biol 11:262CrossRefPubMedPubMedCentralGoogle Scholar
  6. Caisová L, Marin B, Melkonian M (2013) A consensus secondary structure of ITS2 in the Chlorophyta identified by phylogenetic reconstruction. Protist 164:482–496CrossRefPubMedGoogle Scholar
  7. Coleman AW (2000) The significance of a coincidence between evolutionary landmarks found in mating affinity and a DNA sequence. Protist 151:1–9CrossRefPubMedGoogle Scholar
  8. Coleman AW (2003) ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends Genet 19:370–375CrossRefPubMedGoogle Scholar
  9. Darty K, Denise A, Ponty Y (2009) VARNA: interactive drawing and editing of the RNA secondary structure. Bioinformatics 25:1974–1975CrossRefPubMedPubMedCentralGoogle Scholar
  10. Davies BJ, Glasser NF, Carrivick JL, Hambrey MJ, Smellie JL, Nývlt D (2013) Landscape evolution and ice-sheet behaviour in a semi-arid polar environment: James Ross Island, NE Antarctic Peninsula. In: Hambrey MJ, Barker PF, Barrett PJ, Bowman VC, Davies BJ, Smellie JL, Tranter M (eds) Antarctic palaeoenvironments and earth surface processes, vol 381. Geological Society of London, Special Publications, London, pp 1–43Google Scholar
  11. Dembitsky VM, Rezanka T, Rozentsvet OA (1993) Lipid composition of 3 macrophytes from the Caspian Sea. Phytochemistry 33:1015–1019CrossRefGoogle Scholar
  12. Dolhi JM, Maxwell DP, Morgan-Kiss RM (2013) Review: the Antarctic Chlamydomonas raudensis: an emerging model for cold adaptation of photosynthesis. Extremophiles 17:711–722CrossRefPubMedGoogle Scholar
  13. Elster J, Nedbalová L, Vodrážka R, Láska K, Haloda J, Komárek J (2016) Unusual biogenic calcite structures in two shallow lakes, James Ross Island, Antarctica. Biogeosciences 13:535–549CrossRefGoogle Scholar
  14. Fawley MW, Dean ML, Dimmer SK, Fawley KP (2006) Evaluating the morphospecies concept in the Selenastraceae (Chlorophyceae, Chlorophyta). J Phycol 42:142–154CrossRefGoogle Scholar
  15. Guichardant M, Traitler H, Spielmann D, Sprecher H, Finot PA (1993) Stearidonic acid, an inhibitor of the 5-lipoxygenase pathway—a comparison with timnodonic and dihomogammalinolenic acid. Lipids 28:321–324CrossRefPubMedGoogle Scholar
  16. Hamby KR, Sims L, Issel L, Zimmer E (1988) Direct ribosomal RNA sequencing: optimization of extraction and sequencing methods for work with higher plants. Plant Mol Biol Rep 6:175–192CrossRefGoogle Scholar
  17. Hodač L, Brinkmann N, Mohr KI, Arp G, Hallmann C, Ramm J, Spitzer K, Friedl T (2015) Diversity of microscopic green algae (Chlorophyta) in calcifying biofilms of two karstic streams in Germany. Geomicrobiol J 32:275–290CrossRefGoogle Scholar
  18. Hodač L, Hallmann C, Spitzer K, Elster J, Faßhauer F, Brinkmann N, Lepka D, Diwan V, Friedl T (2016) Widespread green algae Chlorella and Stichococcus exhibit polar-temperate and tropical-temperate biogeography. FEMS Microbiol Ecol. doi: 10.1093/femsec/fiw122 PubMedGoogle Scholar
  19. Hoshina R (2014) DNA analyses of a private collection of microbial green algae contribute to a better understanding of microbial diversity. BMC Res Notes 7:592CrossRefPubMedPubMedCentralGoogle Scholar
  20. Izaguirre I, Allende L, Marinone MC (2003) Comparative study of the planktonic communities of three lakes of contrasting trophic status at Hope Bay (Antarctic Peninsula). J Plankton Res 25:1079–1097CrossRefGoogle Scholar
  21. Katana A, Kwiatowski J, Spalik K, Zakrys B, Szalacha E, Szymanska H (2001) Phylogenetic position of Koliella (Chlorophyta) as inferred from nuclear and chloroplast small subunit rDNA. J Phycol 37:443–451CrossRefGoogle Scholar
  22. Komárek J, Fott B (1983) Chlorophyceae (Grünalgen), Ordnung Chlorococcales. In: Huber-Pestalozzi G (ed) Das Phytoplankton des Süsswassers, Die Binnengewässer 16. Schweizerbart Verlag, Stuttgart, pp 629–645Google Scholar
  23. Komárek J, Nedbalová L, Hauer T (2012) Phylogenetic position and taxonomy of three heterocytous cyanobacteria dominating the littoral of deglaciated lakes, James Ross Island, Antarctica. Polar Biol 35:759–774CrossRefGoogle Scholar
  24. Komárková-Legnerová J (1969) The systematics and ontogenesis of the genera Ankistrodesmus Corda and Monoraphidium gen. nov. In: Fott B (ed) Studies in Phycology. Academia, Prague, pp 75–144Google Scholar
  25. Kopalová K, Nedbalová L, Nývlt D, Elster J, Van de Vijver B (2013) Diversity, ecology and biogeography of the freshwater diatom communities from Ulu Peninsula (James Ross Island, NE Antarctic Peninsula). Polar Biol 36:933–948CrossRefGoogle Scholar
  26. Krienitz L, Bock C (2012) Present state of the systematics of planktonic coccoid green algae of inland waters. Hydrobiologia 698:295–326CrossRefGoogle Scholar
  27. Krienitz L, Wirth M (2006) The high content of polyunsaturated fatty acids in Nannochloropsis limnetica (Eustigmatophyceae) and its implication for food web interactions, freshwater aquaculture and biotechnology. Limnologica 36:204–210CrossRefGoogle Scholar
  28. Krienitz L, Bock C, Nozaki H, Wolf M (2011) SSU rRNA gene phylogeny of morphospecies affiliated to the bioassay alga Selenastrum capricornutum recovered the polyphyletic origin of crescent-shaped Chlorophyta. J Phycol 47:880–893CrossRefPubMedGoogle Scholar
  29. Kvíderová J (2010) Rapid algal toxicity assay using variable chlorophyll fluorescence for Chlorella kessleri (Chlorophyta). Environ Toxicol 25:554–563CrossRefPubMedGoogle Scholar
  30. Kvíderová J, Henley WJ (2005) The effect of ampicillin plus streptomycin on growth and photosynthesis of two halotolerant chlorophyte algae. J Appl Phycol 17:301–307CrossRefGoogle Scholar
  31. Kvíderová J, Lukavský J (2001) A new unit for crossed gradients of temperature and light. Nova Hedwig Beih 123:541–550Google Scholar
  32. Lang IK, Hodač L, Friedl T, Feussner I (2011) 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 11(art. 124):16Google Scholar
  33. Láska K, Prošek P, Budík L (2010) Seasonal variation of air temperature at the Mendel Station, James Ross Island in the period of 2006–2009. In: EGU general assembly conference abstracts, vol 12, p 3880Google Scholar
  34. Laybourn-Parry J, Bayliss P (1996) Seasonal dynamics of the planktonic community in Lake Druzhby, Princess Elizabeth Land, Eastern Antarctica. Freshw Biol 35:57–67CrossRefGoogle Scholar
  35. Laybourn-Parry J, Pearce DA (2007) The biodiversity and ecology of Antarctic lakes: models for evolution. Philos Trans R Soc B 362:2273–2289CrossRefGoogle Scholar
  36. Laybourn-Parry J, Wadham J (2014) Antarctic lakes. Oxford University Press, OxfordCrossRefGoogle Scholar
  37. Lísa M, Holčapek M, Boháč M (2009) Statistical evaluation of triacylglycerol composition in plant oils based on high-performance liquid chromatography-atmospheric pressure chemical ionization mass spectrometry data. J Agric Food Chem 57:6888–6898CrossRefPubMedGoogle Scholar
  38. Morgan-Kiss R, Ivanov AG, Williams J, Khan M, Huner NPA (2002) Differential thermal effects on the energy distribution between photosystem II and photosystem I in thylakoid membranes of a psychrophilic and a mesophilic alga. BBA Biomembr 1561:251–265CrossRefGoogle Scholar
  39. Morgan-Kiss RM, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner NPA (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol Rev 70:222–252CrossRefPubMedPubMedCentralGoogle Scholar
  40. Morgan-Kiss RM, Ivanov AG, Modla S, Czymmek K, Huner NPA, Priscu JC, Lisle JT, Hanson TE (2008) Identity and physiology of a new psychrophilic eukaryotic green alga, Chlorella sp., strain BI, isolated from a transitory pond near Bratina Island, Antarctica. Extremophiles 12:701–711CrossRefPubMedGoogle Scholar
  41. Morita RY (1975) Psychrophilic bacteria. Bacteriol Rev 39:144–167PubMedPubMedCentralGoogle Scholar
  42. Nadeau TL, Castenholz RW (2000) Characterization of psychrophilic oscillatorians (Cyanobacteria) from Antarctic meltwater ponds. J Phycol 36:914–923CrossRefGoogle Scholar
  43. Nedbalová L, Nývlt D, Kopáček J, Šobr M, Elster J (2013) Freshwater lakes of Ulu Peninsula, James Ross Island, north-east Antarctic Peninsula: origin, geomorphology and physical and chemical limnology. Antarct Sci 25:358–372CrossRefGoogle Scholar
  44. Øvstedal DO, Lewis-Smith RI (2001) Lichens of Antarctica and South Georgia. A guide to their identification and ecology. Cambridge University Press, CambridgeGoogle Scholar
  45. Peksa O, Škaloud P (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol Ecol 20:3936–3948CrossRefPubMedGoogle Scholar
  46. Pocock T, Lachance MA, Proschold T, Priscu JC, Kim SS, Huner NPA (2004) Identification of a psychrophilic green alga from Lake Bonney Antarctica: Chlamydomonas raudensis Ettl. (UWO 241) Chlorophyceae. J Phycol 40:1138–1148CrossRefGoogle Scholar
  47. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefPubMedGoogle Scholar
  48. Rambaut A (2014) FigTree Version 1.4.2. Institute of Evolutionary Biology, University of Edinburgh. Accessed 15 June 2016
  49. Řezanka T, Nedbalová L, Sigler K (2008) Unusual medium-chain polyunsaturated fatty acids from the snow alga Chloromonas brevispina. Microbiol Res 163:373–379CrossRefPubMedGoogle Scholar
  50. Seaburg KG, Parker BC, Wharton RA, Simmons GM (1981) Temperature-growth responses of algal isolates from Antarctic oases. J Phycol 17:353–360CrossRefGoogle Scholar
  51. Škaloud P, Nedbalová L, Elster J, Komárek J (2013) A curious occurrence of Hazenia broadyi spec. nova in Antarctica and the review of the genus Hazenia (Ulotrichales, Chlorophyceae). Polar Biol 36:1281–1291CrossRefGoogle Scholar
  52. 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
  53. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  54. Vincent WF (1982) Autecology of an ultraplanktonic shade alga in Lake Tahoe. J Phycol 18:226–232CrossRefGoogle Scholar
  55. White TJ, Bruns T, Lee SJWT, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Methods Appl 18:315–322Google Scholar
  56. Wolf M, Chen SL, Song JY, Ankenbrand M, Muller T (2013) Compensatory base changes in ITS2 secondary structures correlate with the biological species concept despite intragenomic variability in ITS2 sequences—a proof of concept. PLoS One 8:e66726CrossRefPubMedPubMedCentralGoogle Scholar
  57. Yee W (2016) Microalgae from the Selenastraceae as emerging candidates for biodiesel production: a mini review. World J Microb Biotechnol 32:64CrossRefGoogle Scholar
  58. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415CrossRefPubMedPubMedCentralGoogle Scholar
  59. Zwickl DJ (2006) GARLI: genetic algorithm for rapid likelihood inference. Accessed 15 June 2016

Copyright information

© Springer Japan 2016

Authors and Affiliations

  • Linda Nedbalová
    • 1
    • 2
  • Martin Mihál
    • 1
  • Jana Kvíderová
    • 2
    • 3
  • Lenka Procházková
    • 1
  • Tomáš Řezanka
    • 4
  • Josef Elster
    • 2
    • 3
  1. 1.Department of Ecology, Faculty of ScienceCharles University in PraguePragueCzech Republic
  2. 2.Centre for PhycologyInstitute of Botany, CASTřeboňCzech Republic
  3. 3.Centre for Polar Ecology, Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic
  4. 4.Institute of Microbiology, CASPragueCzech Republic

Personalised recommendations