Skip to main content

Advertisement

Log in

Comparison of wintertime eukaryotic community from sea ice and open water in the Baltic Sea, based on sequencing of the 18S rRNA gene

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

The Baltic Sea is one of the world’s largest brackish water basins and is traditionally considered to be species poor. Here, we assessed the diversity of the nano-sized eukaryotic microbial wintertime community, using molecular ecological methods based on sequencing of small-subunit ribosomal RNA gene clone libraries. The results demonstrate that a rich community of small eukaryotes inhabits the Baltic Sea ice and water during winter. The community was dominated by alveolates and stramenopiles. Ciliates and cercozoans were the richest groups present, while in contrast to previous studies, diatoms showed a lower richness than expected. Furthermore, fungi and parasitic Syndiniales were present both in the water and in the sea ice. Some of the organisms in the sea-ice community were active, based on the RNA data, but a number of organisms were inactive or remnants from the freezing process. The results demonstrate that the sea-ice communities in the Baltic Sea are highly diverse and that water and ice of different ages include different protistan assemblages. Our study emphasizes the potential loss in biodiversity through diminishing ice cover as a result of climate change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alexander E, Stock A, Breiner H-W, Behnke A, Bunge J, Yakimov MM, Stoeck T (2009) Microbial eukaryotes in the hypersaline anoxic L’Atalante deep-sea basin. Environ Microbiol 11:360–381

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Amacher JA, Baysinger CW, Neuer S (2011) The importance of organism density and co-occurring organisms in biases associated with molecular studies of marine protist diversity. J Plankton Res 33:1762–1766

    Article  Google Scholar 

  • Behnke A, Barger KJ, Bunge J, Stoeck T (2010) Spatio-temporal variations in protistan communities along an O2/H2Sgradient in the anoxic Framvaren Fjord (Norway). FEMS Microbiol Ecol 72:89–102

    Article  PubMed  CAS  Google Scholar 

  • Cachon J, Cachon M (1987) Parasitic dinoflagellates. In: Taylor FJR (ed) The biology of dinoflagellates, botanical monographs 21. Blackwell, Oxford, pp 571–610

    Google Scholar 

  • Caron DA, Countway PD, Savai P et al (2009) Defining DNA-based operational taxonomic units for microbial-eukaryote ecology. Appl Environ Microbiol 75:5797–5808

    Article  PubMed  CAS  Google Scholar 

  • Chao A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43:783–791

    Article  PubMed  CAS  Google Scholar 

  • Coats DW, Park MG (2002) Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): parasite survival, infectivity, generation time, and host specificity. J Phycol 38:520–528

    Google Scholar 

  • Cole JR, Chai B, Marsh TL et al (2003) The ribosomal database project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31:442–443

    Article  PubMed  CAS  Google Scholar 

  • Colwell RK (2005) EstimateS: statistical estimation of species richness and shared species from samples. Version 7.5. http://purl.oclc.org/estimates. Accessed 21 April 2011

  • Comiso JC (2003) Large-scale characteristics and variability of the global sea ice cover. In: Thomas DN, Dieckmann GS (eds) Sea ice—an introduction to its physics, chemistry, biology and geology. Blackwell, Oxford, pp 112–142

    Google Scholar 

  • Díez B, Anta B, Pedrós-Alió C, Massana R (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67:2932–2941

    Article  PubMed  Google Scholar 

  • Eicken H (2003) From the microscopic, to the macroscopic, to the regional scale: growth, microstructure and properties of sea ice. In: Thomas DN, Dieckmann GS (eds) Sea ice—an introduction to its physics, chemistry, biology and geology. Blackwell, Oxford, pp 22–81

    Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • Gast RJ, Dennett MR, Caron DA (2004) Characterization of protistan assemblages in the Ross Sea, Antarctica, by denaturing gradient gel electrophoresis. Appl Environ Microbiol 70:2028–2037

    Article  PubMed  CAS  Google Scholar 

  • Gleason FH, Kagami M, Lefevre E, Sime-Ngando T (2008) The ecology of chytrids in aquatic ecosystems: roles in food web dynamics. Fungal Biol Rev 22:17–25

    Article  Google Scholar 

  • Granskog M, Kaartokallio H, Kuosa H, Thomas DN, Vainio J (2006) Sea ice in the Baltic Sea—a review. Estuar Coast Shelf S 70:145–160

    Article  Google Scholar 

  • Guillou L, Viprey M, Chambouvet A et al (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol 10:3349–3365

    Article  PubMed  CAS  Google Scholar 

  • Haecky P, Andersson A (1999) Primary and bacterial production in sea ice in the northern Baltic Sea. Aquat Microb Ecol 20:107–118

    Article  Google Scholar 

  • Haecky P, Jonsson S, Andersson A (1998) Influence of sea ice on the composition of the spring phytoplankton bloom in the northern Baltic Sea. Polar Biol 20:1–8

    Article  Google Scholar 

  • Hällfors G (2004) Checklist of Baltic Sea phytoplankton species (including some heterotrophic protistan groups). Baltic Sea Environ Proc 95:1–208

    Google Scholar 

  • Hällfors G, Niemi Å (1974) A Chrysochromulina (Haptophyceae) bloom under the ice in the Tvärminne Archipelago, southern coast of Finland. Mem Soc Fauna Flora Fenn 50:89–104

    Google Scholar 

  • Horner R, Ackley SF, Dieckmann GS, Gulliksen B, Hoshiai T, Legendre L, Melnikov IA, Reeburgh WS, Spindler M, Sullivan CW (1992) Ecology of sea ice biota. 1. Habitat, terminology, and methodology. Polar Biol 12:417–427

    Article  Google Scholar 

  • Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon; a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319

    Article  PubMed  CAS  Google Scholar 

  • Huttunen M, Niemi Å (1986) Sea-ice algae in the Northern Baltic Sea. Mem Soc Fauna Flora Fenn 62:58–62

    Google Scholar 

  • Ikävalko J (1998) Further observations on flagellates within sea ice in northern Bothnian Bay, the Baltic Sea. Polar Biol 19:323–329

    Article  Google Scholar 

  • Ikävalko J (2004) Checklist of unicellular and invertebrate organisms within and closely associated with sea ice in the arctic regions. Meri Rep Ser Finn Inst Mar Res 52:1–41

    Google Scholar 

  • Ikävalko J, Thomsen HA (1996) Scale-covered and loricate flagellates (Chrysophyceae and Synurophyceae) from the Baltic Sea ice. Nova Hedwigia Beih 114:147–160

    Google Scholar 

  • Ikävalko J, Thomsen HA (1997) The Baltic Sea ice biota (March 1994): a study of the protistan community. Eur J Protistol 33:229–243

    Article  Google Scholar 

  • Jobard M, Rasconi S, Sime-Ngando T (2010) Diversity and functions of microscopic fungi: a missing component in pelagic food webs. Aquat Sci 72:255–268

    Article  CAS  Google Scholar 

  • Kaartokallio H (2004) Food web components and physical and chemical properties of Baltic Sea ice. Mar Ecol Prog Ser 273:49–63

    Article  CAS  Google Scholar 

  • Kaartokallio H, Kuosa H, Thomas DN, Granskog MA, Kivi K (2007) Biomass, composition and activity of organism assemblages along a salinity gradient in sea ice subjected to river discharge in the Baltic Sea. Polar Biol 30:183–197

    Article  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  PubMed  CAS  Google Scholar 

  • Kautsky L, Kautsky N (2000) The Baltic Sea, including Bothnian Sea and Bothnian Bay. In: Sheppard CRC (ed) Seas at the millennium: an environmental evaluation. Elsevier, Amsterdam, pp 121–133

    Google Scholar 

  • Krembs C, Gradinger R, Spindler M (2000) Implications of brine channel geometry and surface area for the interaction of sympagic organisms in Arctic sea ice. J Exp Mar Biol Ecol 243:55–80

    Article  Google Scholar 

  • Lee S-H, Chao A (1984) Estimating population size via sample coverage for closed capture-recapture models. Biometrics 50:88–97

    Article  Google Scholar 

  • Lefèvre E, Bardot C, Noël C, Carrias J-F, Viscogliosi E, Amblard C, Sime-Ngando T (2007) Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environ Microbiol 9:61–71

    Article  PubMed  Google Scholar 

  • Leppäkoski E, Gollasch S, Olenin S (2002) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer, Dordrecht

    Google Scholar 

  • López-García P, Rodríguez-Valera F, Pedrós-Alió C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607

    Article  PubMed  Google Scholar 

  • Lovejoy C, Massana R, Pedrós-Alió C (2006) Diversity and distribution of marine microbial eukaryotes in the Arctic Ocean and adjacent seas. Appl Environ Microbiol 72:3085–3095

    Article  PubMed  CAS  Google Scholar 

  • Lozupone CA, Knight R (2008) Species divergence and the measurement of microbial diversity. FEMS Microbiol Rev 32:557–578

    Article  PubMed  CAS  Google Scholar 

  • Luo W, Li H, Cai M, He J (2009) Diversity of microbial eukaryotes in Kongsfjorden, Svalbard. Hydrobiologia 636:233–248

    Article  Google Scholar 

  • Lynn DH (2008) The ciliated protozoa. Characterization, classification, and guide to the literature. Springer, New York

    Google Scholar 

  • Maggs CA, Ward BA (1996) The genus Pikea (Dumontiaceae, Rhodophyta) in England and the North Pacific: comparative morphological, life history, and molecular studies. J Phycol 32:176–193

    Article  Google Scholar 

  • Meiners K, Fehling J, Granskog MA, Spindler M. (2002) Abundance, biomass and composition of biota in Baltic Sea ice and underlying water (March 2000). Polar Biol 25:761–770

    Google Scholar 

  • Melnikov IA (1997) The Arctic sea ice ecosystem. Gordon and Breach Science Publishers, Amsterdam

    Google Scholar 

  • Moon-van der Staay SY, De Wachter R, Vaulot D (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409:607–610

    Article  PubMed  CAS  Google Scholar 

  • Norrman B, Andersson A (1994) Development of ice biota in a temperate sea area (Gulf of Bothnia). Polar Biol 14:531–537

    Article  Google Scholar 

  • Not F, del Campo J, Balagué V, de Vargas C, Massana R (2009) New insights into the diversity of marine picoeukaryotes. PLOS One 4:e7143. doi:10.1371/journal.pone.0007143

    Article  PubMed  Google Scholar 

  • Pereyra RT, Bergström L, Kautsky L, Johannesson K (2009) Rapid speciation in a newly opened postglacial marine environment, the Baltic Sea. BMC Evol Biol 9:70. doi:10.1186/1471-2148-9-70

    Google Scholar 

  • Petrich C, Eicken H (2010) Growth, structure and properties of sea ice. In: Thomas DN, Dieckmann GS (eds) Sea ice, 2nd edn. Blackwell, Oxford, pp 23–77

    Google Scholar 

  • Piiparinen J, Kuosa H, Rintala J-M (2010) Winter-time ecology in the Bothnian Bay, Baltic Sea: nutrients and algae in fast ice. Polar Biol 33:1445–1461

    Article  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Prokopowich CD, Gregory TR, Crease TJ (2003) The correlation between rDNA copy number and genome size in eukaryotes. Genome 46:48–50

    Article  PubMed  CAS  Google Scholar 

  • Remane A (1934) Die Brackwasserfauna. Ver Deut Zool Ges 36:34–74

    Google Scholar 

  • Riedel A, Michel C, Poulin M, Lessard S (2003) Taxonomy and abundance of microalgae and protists at a first-year sea ice station near Resolute Bay, Nunavut, spring to early summer 2001. Can Data Rep Hydrogr Ocean Sci 159:vi+54

  • Rintala J-M, Piiparinen J, Ehn J, Autio R, Kuosa H (2006) Changes in phytoplankton biomass and nutrient quantities in sea ice as responses to light/dark manipulations during different phases of the Baltic winter 2003. Hydrobiologia 554:11–24

    Article  CAS  Google Scholar 

  • Rintala J-M, Hällfors H, Hällfors S, Hällfors G, Majaneva M, Blomster J (2010a) Heterocapsa arctica subsp. frigida, subsp. nov. (Peridiniales, Dinophyceae)—description of a new dinoflagellate and its occurrence in the Baltic Sea. J Phycol 46:751–762

    Article  CAS  Google Scholar 

  • Rintala J-M, Piiparinen J, Uusikivi J (2010b) Drift-ice and under-ice water communities in the Gulf of Bothnia (Baltic Sea). Polar Biol 33:179–191

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Różańska M, Gosselin M, Poulin M, Wiktor JM, Michel C (2009) Influence of environmental factors on the development of bottom ice protist communities during the winter-spring transition. Mar Ecol Prog Ser 386:43–59

    Article  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed  CAS  Google Scholar 

  • Schnepf E, Kühn SF (2000) Food uptake and fine structure of Cryothecomonas longipes sp. nov., a marine nanoflagellate incertae sedis feeding phagotrophically on large diatoms. Helgoland Mar Res 54:18–32

    Article  Google Scholar 

  • Spilling K (2007) Dense sub-ice bloom of dinoflagellates in the Baltic Sea, potentially limited by high pH. J Plankton Res 29:895–901

    Article  CAS  Google Scholar 

  • Stock A, Jürgens K, Bunge J, Stoeck T (2009) Protistan diversity in suboxic and anoxic water of the Gotland Deep (Baltic Sea) as revealed by 18S rRNA clone libraries. Aquat Microb Ecol 55:267–284

    Article  Google Scholar 

  • Stoecker DK, Buck KR, Putt M (1993) Changes in the sea-ice brine community during the spring-summer transition, McMurdo Sound, Antarctica. II. Phagotrophic protists. Mar Ecol Prog Ser 95:103–113

    Article  Google Scholar 

  • Thanh VN (2006) Yeast biodiversity and evolution. In: Sharma AK, Sharma A (eds) Plant genome: biodiversity and evolution. Science Publishers, Enfield, pp 241–284

    Google Scholar 

  • Voipio A (1981) The Baltic Sea. Elsevier oceanography series 30. Elsevier, Amsterdam

    Google Scholar 

  • Vørs N (1992) Heterotrophic amoebae, flagellates and heliozoan from the Tvärminne area, Gulf of Finland, in 1988–1990. Ophelia 36:1–109

    Article  Google Scholar 

  • Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100

    Article  PubMed  CAS  Google Scholar 

  • Wintzigerode F, Göbel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213–229

    Article  Google Scholar 

  • Zhu F, Massana R, Not F, Marie D, Vaulot D (2005) Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. FEMS Microbiol Ecol 52:79–92

    Article  PubMed  CAS  Google Scholar 

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

Download references

Acknowledgments

The Walter and Andrée de Nottbeck Foundation provided financial support for M.M. and J.-M.R and the Emil Aaltonen Foundation for M.P. and J.B. This work was supported by a grant from the Academy of Finland to D.P.F (1212943). We would like to thank Jonna Piiparinen for help in the ice sampling at Tvärminne Zoological Station and Vilma Rouvinen for her assistance in the preparations before and during the cruise to the Gulf of Bothnia. We owe our greatest gratitude to Prof. Klaus Jürgens who invited J.-M.R. to participate in the maiden voyage of the research vessel Maria S. Merian. This article is part of the Ph.D. thesis of M.M.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jaanika Blomster.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 219 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Majaneva, M., Rintala, JM., Piisilä, M. et al. Comparison of wintertime eukaryotic community from sea ice and open water in the Baltic Sea, based on sequencing of the 18S rRNA gene. Polar Biol 35, 875–889 (2012). https://doi.org/10.1007/s00300-011-1132-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-011-1132-9

Keywords

Navigation