Polar Biology

, Volume 39, Issue 11, pp 1933–1956 | Cite as

Contribution towards a morphological and molecular taxonomic reference library of benthic marine diatoms from two Arctic fjords on Svalbard (Norway)

  • K. Stachura-Suchoples
  • N. Enke
  • C. Schlie
  • I. Schaub
  • U. Karsten
  • R. Jahn
Original Research

Abstract

Knowledge on benthic diatom taxonomy and hence biodiversity from Arctic locations is rare, though the few existing analyses address morphological characteristics only. Morphological treatment is a time-consuming process and just allows the taxonomic identification of a low sample volume. In contrast, molecular sequencing is a faster and universally applicable approach, and also has the potential for refined analyses. Unfortunately, a lot of molecular information in databases is not trustable, and often existing genetic data do not fit together with morphological aspects. Therefore, the main goal of our study was for the first time to combine both morphological features and DNA information on benthic Arctic diatoms. In a first step, we studied the morphology of 26 strains from the Rostock Culture Collection of Arctic diatoms via light and electron microscopies. Secondly, we addressed their molecular taxonomy by sequencing the DNA barcode 18S V4 and the chloroplast marker rbcL. As a result, we could identify five species. Seven of the altogether twelve taxa could not be attributed to any known species, because listed sequences and morphology did not fit together. From these, three species were described as new to science here. Although the studied strains represent only a minor fraction of the diatom flora of Svalbard, this study is a first milestone in coupling morphological and molecular data of benthic diatoms in such high latitudes. By making these data available online, they contribute to a taxonomic reference library for Arctic benthic diatoms and are available for comparative studies.

Keywords

Morphology Molecular taxonomy DNA barcode 18S V4 rbc

References

  1. Abarca N, Jahn R, Zimmermann J, Enke N (2014) Does the cosmopolitan diatom Gomphonema parvulum (Kützing) Kützing have a biogeography? PLoS ONE 9(1):e86885. doi:10.1371/journal.pone.0086885 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Al-Handal AY, Wulff A (2008a) Marine benthic diatoms from Potter Cove, King George Island, Antarctica. Bot Mar 51:51–68Google Scholar
  3. Al-Handal AY, Wulff A (2008b) Marine epiphytic diatoms from the shallow sublittoral zone in Potter Cove, King George Island, Antarctica. Bot Mar 51:411–435Google Scholar
  4. Busse S, Snoeijs P (2002) Navicula sjoersii sp. nov., N. bossvikensis sp. nov. and N. perminuta Grunow from the Baltic Sea. Diatom Res 17:271–282CrossRefGoogle Scholar
  5. Busse S, Snoeijs P (2003) Gradient responses of diatom communities in the Bothnian Sea (northern Baltic Sea), with emphasis on responses to water movement. Phycologia 42:451–464CrossRefGoogle Scholar
  6. Campeau S, Pienitz R, Héquette A (1999) Diatoms as quantitative paleodepth indicators in coastal areas of the southeastern Beaufort Sea, Arctic Ocean. Palaeogeogr Palaeoclimatol Palaeoecol 146:67–97CrossRefGoogle Scholar
  7. Clavero E, Grimalt JO, Hernández-Mariné M (2000) The fine structure of two small Amphora species. A. tenerrima Aleem and Hustedt and A. tenuissima Hustedt. Diatom Res 15:195–208CrossRefGoogle Scholar
  8. Crawford RM, Gardner C, Medlin LK (1994) The genus Attheya I. A description of four new taxa, and the transfer of Goniceros septentrionalis and G. armatas. Diatom Res 9:27–51CrossRefGoogle Scholar
  9. Cremer H (1998) Diatoms in the Laptev Sea (Arctic Ocean): taxonomy and biogeographic distribution. Rep Polar Res 260:1–205Google Scholar
  10. De Brouwer JFC, de Deckere EMGT, Stal LJ (2003) Distribution of extracellular carbohydrates in three intertidal mudflats in Western Europe. Estuar Coast Shelf Sci 56:313–324CrossRefGoogle Scholar
  11. Flemming WD (1954) Naphrax: a synthetic mounting medium of high refractive index. New and improved methods of preparation. J R Microsc Soc 74:42CrossRefGoogle Scholar
  12. Fredriksen S, Karsten U, Bartsch I, Woelfel J, Koblowsky M, Schumann R, Moy S, Steneck B, Hop H, Wiktor J, Wiencke C (2015) Biodiversity of benthic micro- and macroalgae from Svalbard with special focus on Kongsfjorden. In: Hop H, Wiencke C (eds) Advances in polar ecology. SpringerGoogle Scholar
  13. Glud RN, Kühl M, Wenzhöfer F, Rysgaard S (2002) Benthic diatoms of a high Arctic fjord (Young Sound, NE Greenland): importance for ecosystem primary production. Mar Ecol Prog Ser 238:15–29CrossRefGoogle Scholar
  14. Glud RN, Woelfel J, Karsten U, Kuhl M, Rysgaard S (2009) Benthic microalgal production in the Arctic: applied methods and status of the current database. Bot Mar 52:559–571CrossRefGoogle Scholar
  15. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239CrossRefPubMedGoogle Scholar
  16. Guiry MD, Guiry GM (2014) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org. Searched on 09 Dec 2014
  17. Hällfors G (2004) Checklist of Baltic Sea phytoplankton species (including some heterotrophic protistan groups). Baltic Sea environment proceedings no. 95, pp 1–208Google Scholar
  18. Harper MA, Cassie Cooper V, Chang FH, Nelson WA, Broady PA (2012) Phylum Ochrophyta: brown and golden-brown algae, diatoms, silicoflagellates, and kin. In: Gordon DP (ed) New Zealand inventory of biodiversity. Kingdoms Bacteria, Protozoa, Chromista, Plantae, Fungi, vol 3. Canterbury University Press, Christchurch, pp 114–163Google Scholar
  19. Hasle GR, Medlin LK, Syvertsen EE (1994) Synedropsis gen. nov., a genus of araphid diatoms associated with sea ice. Phycologia 33:248–270CrossRefGoogle Scholar
  20. Hofmann G, Lange-Bertalot H, Werum M (2013) Diatomeen im Süßwasser-Benthos von Mitteleuropa. 2. Korr. Auflage. Koeltz Scientific Books, KönigsteinGoogle Scholar
  21. Hop H, Pearson T, Hegseth EN, Kovacs KM, Wiencke C, Kwasniewski S, Eiane K, Mehlum F, Gulliksen B, Wlodarska-Kowalczuk M, Lydersen C, Weslawski JM, Cochrane S, Gabrielsen GW, Leakey RJG, Lønne JO, Zajaczkowski M, Falk-Petersen S, Kendall M, Wängberg S, Bischof K, Voronkov AY, Kovaltchouk NA, Wiktor J, Poltermann M, di Prisco G, Papucci C, Gerland S (2002) The marine ecosystem of Kongsfjorden, Svalbard. Pol Res 21:167–208CrossRefGoogle Scholar
  22. Ivanova NV, Zemlak TS, Hanner RH, Hebert PDN (2007) Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes 7:544–548CrossRefGoogle Scholar
  23. Jahn R, Kusber WH (2005) Reinstatement of the genus Ceratoneis Ehrenberg and lectotypification of its type specimen: C. closterium Ehrenberg. Diatom Res 20:295–304CrossRefGoogle Scholar
  24. Jahn R, Zetzsche H, Reinhardt R, Gemeinholzer B (2007) Diatoms and DNA barcoding: a pilot study on an environmental sample. In: Kusber WH, Jahn R (eds) Proceedings of the 1st Central European Diatom Meeting 2007 Berlin, Botanic Garden and Botanical Museum Berlin-Dahlem, pp 63–68Google Scholar
  25. Karsten U, Schumann R, Rothe S, Jung I, Medlin L (2006) Temperature and light requirements for growth of two diatom species (Bacillariophyceae) isolated from an Arctic macroalga. Polar Biol 29:476–486CrossRefGoogle Scholar
  26. Karsten U, Schlie C, Woelfel J, Becker B (2012) Benthic diatoms in Arctic seas—ecological functions and adaptations. Polarforschung 81:77–84Google Scholar
  27. Krammer K, Lange-Bertalot H (1986) Bacillariophyceae 1. Teil Naviculaceae. In: Ettl H, Gerloff F, Heying H, Mollenhauer D (eds) Süßwasserflora von Mitteleuropa 2/1. Gustav Fischer Verlag, Stuttgart, pp 1–876Google Scholar
  28. Krammer K, Lange-Bertalot H (1987) Morphology and taxonomy of Surirella ovalis and related taxa. Diatom Res 2:77–95CrossRefGoogle Scholar
  29. Krammer K, Lange-Bertalot H (1988) Bacillariophyceae 2. Teil Bacillariaceae, Epithemiaceae, Surirellaceae. In: Ettl H, Gerloff H, Heynig H, Mollenhauer D (eds) Süßwasserflora von Mitteleuropa 2/2. Gustav Fischer Verlag, JenaGoogle Scholar
  30. Levkov Z (2009) Amphora sensu lato. In: Lange-Bertalot H (ed) Diatoms of Europe: diatoms of the European inland waters and comparable habitats, vol 5. A.R.G. Gantner Verlag K.G., Lichtenstein, pp 5–916Google Scholar
  31. Li H, Yang G, Sun Y, Wu S, Zhang X (2007) Cylindrotheca closterium is a species complex as was evidenced by the variations of rbcL gene and SSU rDNA. J Ocean Univ China 6:167–174CrossRefGoogle Scholar
  32. Liu JY (ed) (2008) Checklist of biota of Chinese seas. Science Press, Academia Sinica, Beijing, pp 1–1267Google Scholar
  33. MacGillivary ML, Kaczmarska I (2011) Survey of the efficacy of a short fragment of the rbcL gene as a supplemental DNA barcode for diatoms. J Eukaryot Microbiol 58:529–536CrossRefPubMedGoogle Scholar
  34. Mann DG (1999) The species concept in diatoms. Phycologia 38:437–495CrossRefGoogle Scholar
  35. Mather L, MacIntosh K, Kaczmarska I, Klein G, Martin JL (2010) A checklist of diatom species reported (and presumed native) from Canadian coastal waters. Can Tech Rep Fish Aquat Sci 2881:1–78Google Scholar
  36. Medlin LK, Hasle GR (1990) Some Nitzschia and related diatom species from fast ice samples in the Arctic and Antarctic. Polar Biol 10:451–479CrossRefGoogle Scholar
  37. Medlin LK, Kaczmarska I (2004) Evolution of the diatoms: V. Morphological and cytological support for the major clades and a taxonomic revision. Phycologia 43:245–270CrossRefGoogle Scholar
  38. Medlin LK, Jung I, Bahulikar R, Mendgen K, Kroth P, Kooistra WHCF (2008) Evolution of the diatoms: VI. Assessment of the new genera in the araphids using molecular data. Nova Hedwigia 133:81–100Google Scholar
  39. Messing J (1983) New M13 vectors for cloning. Methods Enzymol 101:20–78CrossRefPubMedGoogle Scholar
  40. Metzeltin D, Witkowski A (1996) Diatomeen der Bären-Insel. Süsswasser- und marine Arten. In: Lange-Bertalot H (ed) Iconographia Diatomologica. Annotated diatom micrographs, vol 4. Taxonomy. Koeltz Scientific Books, Königstein, pp 3–217Google Scholar
  41. Müller K, Müller J, Neinhuis C, Quandt D (2005) PhyDe®—phylogenetic data editor. http://www.phyde.de
  42. Nelles L, Fang BL, Volckaert G, Vandenberghe A, DeWachter R (1984) Nucleotide sequence of a crustacean 18S ribosomal RNA gene and secondary structure of eukaryotic small subunit ribosomal RNAs. Nucleic Acid Res 12:8749–8768CrossRefPubMedPubMedCentralGoogle Scholar
  43. Nickrent DL, Sargent ML (1991) An overview of the secondary structure of the V4 region of eukaryotic small-subunit ribosomal RNA. Nucleic Acid Res 19:227–235CrossRefPubMedPubMedCentralGoogle Scholar
  44. Osada K, Kobayashi H (1990) Observations on the forms of the diatom Entomoneis paludosa and related taxa. In: Simola H (ed) Proceedings of the 10th international diatom symposium, Bristol, pp 161–172Google Scholar
  45. Pawłowska J, Włodarska-Kowalczuk M, Zajaćzkowski M, Nygård H, Berge J (2011) Seasonal variability of meio- and macrobenthic standing stocks and diversity in an Arctic fjord (Adventfjorden, Spitsbergen). Polar Biol 34:833–845CrossRefGoogle Scholar
  46. Pawlowski J, Audic S, Adl S, Bass D, Belbahri L, Berney C, Bowser SS, Cepicka I, Decelle J, Dunthorn M, Fiore-Donno AM, Gile GH, Holzmann M, Jahn R, Jirků M, Keeling PJ, Kostka M, Kudryavtsev A, Lara E, Lukeš J, Mann DG, Mitchell EAD, Nitsche F, Romeralo M, Saunders GW, Simpson AGB, Smirnov AV, Spouge JL, Stern RF, Stoeck T, Zimmermann J, Schindel D, de Vargas C (2012) CBOL Protist Working Group: barcoding eukaryotic richness beyond the animal, plant and fungal kingdoms. PLoS Biol 10:e1001419CrossRefPubMedPubMedCentralGoogle Scholar
  47. Pickett-Heaps JD (1998) A rapid, highly efficient method for collecting, fixing and embedding planktonic and other small cells for electron microscopy. J Phycol 34:1088–1089CrossRefGoogle Scholar
  48. Reimann BEF, Lewin JC (1964) The diatom genus Cylindrotheca Rabenhorst. J R Microsc Soc 83:283–296CrossRefGoogle Scholar
  49. Reimann BEF, Volcani BE (1968) Studies on the biochemistry and fine structure of silica shell formation in diatoms 1: III. The structure of the cell wall of Phaeodactylum tricornutum Bohlin. J Ultrastr Res 21:182–193CrossRefGoogle Scholar
  50. Round FE, Crawford RM, Mann DG (1990) The diatoms: biology and morphology of the genera. Cambridge University Press, CambridgeGoogle Scholar
  51. Ruck EC, Kociolek JP (2004) Preliminary phylogeny of the family Surirellaceae (Bacillariophyta). In: Lange-Bertalot H, Kociolek P (eds) Bibliotheca Diatomologica Band 50. J Cramer in der Gebrüder Borntrager Verlagsbuchhandlung, StuttgartGoogle Scholar
  52. Schlie C, Woelfel J, Rüdiger F, Schumann R, Karsten U (2011) Ecophysiological performance of benthic diatoms from arctic waters. In: Seckbach J, Kociolek P (eds) COLE—cellular origin, life in extreme habitats and astrobiology. The diatom world, vol 19. Springer, Berlin, pp 425–436Google Scholar
  53. Sevilgen DS, de Beer D, Al-Handal AY, Brey T, Polerecky L (2014) Oxygen budgets in subtidal arctic (Kongsfjorden, Svalbard) and temperate (Helgoland, North Sea) microphytobenthic communities. Mar Ecol Prog Ser 504:27–42CrossRefGoogle Scholar
  54. Simonsen R (1987) Atlas and catalogue of the diatom types of Friedrich Hustedt, vol 1 Catalogue X, 525 vol 2 Atlas, plates 1–395, vol. 3 Atlas, plates 396–772. Cramer bei Borntraeger, BerlinGoogle Scholar
  55. Smetacek V (1999) Diatoms and the ocean carbon cycle. Protist 150:25–32CrossRefPubMedGoogle Scholar
  56. Stonik IV, Orlova TY, Crawford RM (2006) Attheya ussurensis sp. nov. (Bacillariophyta)—a new marine diatom from the coastal waters of the Sea of Japan and a reappraisal of the genus. Phycologia 45:141–147CrossRefGoogle Scholar
  57. Svendsen H, Beszczynska-Møller A, Hagen JO, Lefauconnier B, Tverberg V, Gerland S, Ørbaek JB, Bischof K, Papucci C, Zajaczkowski M, Azzolini R, Bruland O, Wiencke C, Winther JG, Dallmann W (2002) The physical environment of Kongsfjorden-Krossfjorden, an Arctic fiord system in Svalbard. Polar Res 21:167–208CrossRefGoogle Scholar
  58. UBA (2010) Qualitätssicherungsstelle des BLMP am UBA: Prüfverfahren-SOP Phytoplankton-Untersuchungen in Oberflächengewässern der Küste (qualitativ und quantitativ), version 02 (P-SOP-BLMP-PP_v02), Umweltbundesamt, 71 SGoogle Scholar
  59. Vyverman W, Verleyen E, Sabbe K, Vanhoutte K, Sterken M, Hodgson DA, Mann DG, Juggins S, Van der Vijer B, Jones V, Flower R, Roberts D, Chepurnov VA, Kilroy C, Vanormelingen P, De Wever A (2007) Historical processes constrain patterns in global diatom diversity. Ecology 88:1924–1931CrossRefPubMedGoogle Scholar
  60. Witkowski A, Lange-Bertalot H, Metzeltin D (2000) Diatom flora of marine coasts I. In: Lange-Bertalot H (ed) Iconographia Diatomologica. Annotated diatom micrographs. Diversity–taxonomy–identification, vol 7. A.R.G. Gantner Verlag K.G., Ruggell, pp 1–925Google Scholar
  61. Woelfel J, Schumann R, Leopold P, Wiencke C, Karsten U (2009) Microphytobenthic biomass along gradients of physical conditions in Arctic Kongsfjorden, Svalbard. Bot Mar 52:573–583CrossRefGoogle Scholar
  62. Woelfel J, Schumann R, Peine F, Flohr A, Kruss A, Tegowski J, Blondel P, Wiencke C, Karsten U (2010) Microphytobenthos of Arctic Kongsfjorden (Svalbard, Norway): biomass and potential primary production along the shore line. Polar Biol 33:1239–1253CrossRefGoogle Scholar
  63. Woelfel J, Eggert A, Karsten U (2014) Marginal impacts of rising temperature on Arctic benthic microalgae production based on in situ measurements and modelled estimates. Mar Ecol Prog Ser 501:25–40CrossRefGoogle Scholar
  64. Yool A, Tyrrell T (2003) Role of diatoms in regulating the ocean’s silicon cycle. Glob Biogeochem Cycles 17:1103CrossRefGoogle Scholar
  65. Zimmermann J, Jahn R, Gemeinholzer B (2011) Barcoding diatoms: evaluation of the V4 subregion on the 18S rRNA gene, including new primers and protocols. Org Divers Evol. doi:10.1007/s13127-011-0050-6 Google Scholar
  66. Zimmermann J, Abarca N, Skibbe O, Kusber WH, Enke N, Jahn R (2014) Taxonomic reference libraries for environmental barcoding: a best practice example from diatom research. PLoS ONE. doi:10.1371/journal.pone.0108793 Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • K. Stachura-Suchoples
    • 1
  • N. Enke
    • 1
  • C. Schlie
    • 2
  • I. Schaub
    • 2
  • U. Karsten
    • 2
  • R. Jahn
    • 1
  1. 1.Botanischer Garten und Botanisches Museum DahlemFreie Universität BerlinBerlinGermany
  2. 2.Institute of Biological Sciences, Applied Ecology and PhycologyUniversity of RostockRostockGermany

Personalised recommendations