Polar Biology

, Volume 37, Issue 9, pp 1271–1287 | Cite as

A molecular survey of protist diversity through the central Arctic Ocean

  • Estelle KiliasEmail author
  • Gerhard Kattner
  • Christian Wolf
  • Stephan Frickenhaus
  • Katja Metfies
Original Paper


The protist assemblage in the central Arctic Ocean is scarcely surveyed despite them being the major primary producers. Elucidating their response to changing environmental variables requires an a priori analysis of their current diversity, including abundant and rare species. In late summer 2011, samples were collected during the ARK-XXVI/3 expedition (RV Polarstern) to study Arctic protist community structures, by implementation of automated ribosomal intergenic spacer analysis (ARISA) and 454-pyrosequencing. Protist assemblages were related to the hydrology and environmental variables (temperature, salinity, ice coverage, nitrate, phosphate, and silicate). The abundant (≥1 %) biosphere and rare (<1 %) biosphere were considered separately in the diversity analysis in order to reveal their mutual relationships. A relation between hydrology and protist community structure was highly supported by ARISA and partially by 454-pyrosequencing. Sea ice showed a stronger influence on the local community structure than nutrient availability, making statements on the water mass influence more difficult. Dinoflagellates (Syndiniales), chlorophytes (Micromonas spp.), and haptophytes (Phaeocystis spp.) were important contributors to the abundant biosphere, while other dinoflagellates and stramenopiles dominated the rare biosphere. No significant correlation was found between the abundant and rare biosphere. However, relative contributions of major taxonomic groups revealed an unexpected stable community structure within the rare biosphere, indicating a potential constant protist reservoir. This study provides a first molecular survey of protist diversity in the central Arctic Ocean, focusing on the diversity and distribution of abundant and rare protists according to the environmental conditions, and can serve as baseline for future analysis.


18S rRNA gene 454-Pyrosequencing ARISA Biogeography Diversity Phytoplankton 



This study was accomplished within the Young Investigator Group PLANKTOSENS (VH-NG-500), funded by the Initiative and Networking Fund of the Helmholtz Association. We thank the captain and crew of the RV Polarstern for their support during the cruise ARKXXVI/3. We are especially indebted to F. Kilpert and B. Beszteri for their support in bioinformatics, to Steven Holland for providing access to the program Analytic Rarefaction 1.3, to Dr. E.M. Nöthig for providing the Chl a data, and very grateful to C. Burau, K.U. Ludwichowski, A. Nicolaus, and K. Oetjen for excellent technical support in the laboratory.

Supplementary material

300_2014_1519_MOESM1_ESM.pdf (41 kb)
Supplementary material 1 (PDF 41 kb)


  1. Amann R, Kuhl M (1998) In situ methods for assessment of microorganisms and their activities. Curr Opin Microbiol 1:352–358PubMedGoogle Scholar
  2. Anderson AF, Riemann L, Bertilsson S (2010) Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities. ISME J 4:171–181Google Scholar
  3. Ardyna M, Gosselin M, Michel C, Poulin M, Tremblay JE (2011) Environmental forcing of phytoplankton community structure and function in the Canadian High Arctic: contrasting oligotrophic and eutrophic regions. Mar Ecol Prog Ser 442:37–57Google Scholar
  4. Azam F, Fenchel T, Field JG, Gray JS, Meyerreil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263Google Scholar
  5. Baas-Becking L (1934) Geobiologie of inleiding tot de milieukunde. Van Stockkum and Zoon, The HagueGoogle Scholar
  6. Bachy C, Lopez-Garcia P, Vereshchaka A, Moreira D (2011) Diversity and vertical distribution of microbial eukaryotes in the snow, sea ice and seawater near the North Pole at the end of the polar night. Front Microbiol. doi: 10.3389/fmicb.2011.00106 PubMedCentralPubMedGoogle Scholar
  7. Behnke A, Engel M, Christen R, Nebel M, Klein RR, Stoeck T (2011) Depicting more accurate pictures of protistan community complexity using pyrosequencing of hypervariable SSU rRNA gene regions. Environ Microbiol 13:340–349. doi: 10.1111/j.1462-2920.2010.02332.x PubMedGoogle Scholar
  8. Beszczynska-Möller A, Fahrbach E, Schauer U, Hansen E (2012) Variability in Atlantic water temperature and transport at the entrance to the Arctic Ocean, 1997–2010. ICES J Mar Sci 69:852–863. doi: 10.1093/icesjms/fss056 Google Scholar
  9. Booth BC, Horner RA (1997) Microalgae on the Arctic Ocean section, 1994: species abundance and biomass. Deep Sea Res Part II Top Stud Oceanogr 44:1607–1622. doi: 10.1016/s0967-0645(97)00057-x Google Scholar
  10. Brown SL, Landry MR (2001a) Mesoscale variability in biological community structure and biomass in the Antarctic Polar Front region at 170 degrees W during austral spring 1997. J Geophys Res Oceans 106:13917–13930. doi: 10.1029/1999jc000188 Google Scholar
  11. Brown SL, Landry MR (2001b) Microbial community structure and biomass in surface waters during a Polar Front summer bloom along 170 degrees W. Deep Sea Res Part II Top Stud Oceanogr 48:4039–4058. doi: 10.1016/s0967-0645(01)00080-7 Google Scholar
  12. Caron DA, Countway PD (2009) Hypotheses on the role of the protistan rare biosphere in a changing world. Aquat Microb Ecol 57:227–238. doi: 10.3354/ame01352 Google Scholar
  13. Caron DA, Countway PD, Savai P, Gast RJ, Schnetzer A, Moorthi SD, Dennett MR, Moran DM, Jones AC (2009) Defining DNA-based operational taxonomic units for microbial-eukaryote ecology. Appl Environ Microbiol 75:5797–5808. doi: 10.1128/aem.00298-09 PubMedCentralPubMedGoogle Scholar
  14. Caron DA, Countway PD, Jones AC, Kim DY, Schnetzer A (2012) Marine protistan diversity. Ann Rev Mar Sci 4:467–493Google Scholar
  15. Comeau AM, Philippe B, Thaler M, Gosselin M, Poulin M, Lovejoy C (2013) Protists in Arctic drift and land-fast sea ice. J Phycol 49:229–240. doi: 10.1111/jpy.12026 Google Scholar
  16. Diez B, Pedros-Alio 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 67:2932–2941PubMedCentralPubMedGoogle Scholar
  17. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20Google Scholar
  18. Ebenezer V, Medlin LK, Ki JS (2012) Molecular detection, quantification, and diversity evaluation of microalgae. Mar Biotechnol 14:129–142. doi: 10.1007/s10126-011-9427-y PubMedGoogle Scholar
  19. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi: 10.1093/bioinformatics/btr381 PubMedCentralPubMedGoogle Scholar
  20. Edler L (1979) Recommendations on methods for marine biological studies in the Baltic Sea—phytoplankton and chlorophyll. Balt Mar Biol 5:1–38Google Scholar
  21. Elwood HJ, Olsen GJ, Sogin ML (1985) The small-subunit ribosomal RNA gene sequences from hypotrichous ciliates Oxytrichia nova and Stylonychia pustulata. Mol Biol Evol 2:399–410PubMedGoogle Scholar
  22. Evans CA, O’Reily JE (1987) A handbook for the measurement of chlorophyll a in netplankton and nanoplankton. BIOMASS Handb 9:1–14Google Scholar
  23. Fenchel T, Finlay BJ (1983) Respiration rates in heterotrophic, free-living protozoa. Microb Ecol 9:99–122. doi: 10.1007/bf02015125 PubMedGoogle Scholar
  24. Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063PubMedGoogle Scholar
  25. Finlay BJ, Fenchel T (2004) Cosmopolitan metapopulations of free-living microbial eukaryotes. Protist 155:237–244PubMedGoogle Scholar
  26. Foissner W (1999) Protist diversity: estimates of the near-imponderable. Protist 150:363–368PubMedGoogle Scholar
  27. Foissner W (2006) Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool 45:111–136Google Scholar
  28. Foulon E, Not F, Jalabert F, Carlou T, Massana R, Slmon N (2008) Ecological niche partitioning in the picoplanktonic green alga Micromonas pusilla: evidence from environmental surveys using phylogenetic probes. Environ Microbiol 10:2433–2443. doi: 10.1111/j.1462-2920.2008.01673.x PubMedGoogle Scholar
  29. Galand PE, Casamayor EO, Kirchman DL, Lovejoy C (2009a) Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci USA 106:22427–22432. doi: 10.1073/pnas.0908284106 PubMedCentralPubMedGoogle Scholar
  30. Galand PE, Casamayor EO, Kirchman DL, Potvin M, Lovejoy C (2009b) Unique archaeal assemblages in the Arctic Ocean unveiled by massively parallel tag sequencing. ISME J 3:860–869. doi: 10.1038/ismej.2009.23
  31. Galand PE, Lovejoy C, Hamilton AK, Ingram RG, Pedneault E, Carmack EC (2009b) Archaeal diversity and a gene for ammonia oxidation are coupled to oceanic circulation. Environ Microbiol 11:971–980. doi: 10.1111/j.1462-2920.2008.01822.x PubMedGoogle Scholar
  32. Gaspar JM, Thomas WK (2013) Assessing the consequences of denoising marker-based metagenomic data. PLoS One 8:e60458. doi: 10.1371/journal.pone.0060458 PubMedCentralPubMedGoogle Scholar
  33. Gilbert JA, Steele JA, Caporaso JG, Steinbrück L, Reeder J, Temperton B, Huse S, McHardy AC, Knight R, Joint I, Somerfield P, Fuhrman JA, Field D (2012) Defining seasonal marine microbial community dynamics. ISME J 6:298–308PubMedCentralPubMedGoogle Scholar
  34. Gradinger R (1996) Occurrence of an algal bloom under Arctic pack. Mar Ecol Prog Ser 131:301–305. doi: 10.3354/meps131301 Google Scholar
  35. Gradinger RR, Baumann MEM (1991) Distribution of phytoplankton communities in relation to the large-scale hydrographical regime in the Fram Strait. Mar Biol 111:311–321. doi: 10.1007/bf01319714 Google Scholar
  36. Groisillier A, Massana R, Valentin K, Vaulot D, Guillou L (2006) Genetic diversity and habitats of two enigmatic marine alveolate lineages. Aquat Microb Ecol 42:277–291. doi: 10.3354/ame042277 Google Scholar
  37. Grover JP (1991) Resource competition in a variable environment—phytoplankton growing according to the variable-internal-stores model. Am Nat 138:811–835. doi: 10.1086/285254 Google Scholar
  38. 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. doi: 10.1111/j.1462-2920.2008.01731.x PubMedGoogle Scholar
  39. Hamilton AK, Lovejoy C, Galand PE, Ingram RG (2008) Water masses and biogeography of picoeukaryote assemblages in a cold hydrographically complex system. Limnol Oceanogr 53:922–935Google Scholar
  40. Hedlund BP, Staley JT (2004) Microbial endemism and biogeography. In: Bull AT (ed) Microbial diversity and bioprospecting. ASM Press, Washington, pp 40–48Google Scholar
  41. Hein M, Pedersen MF, Sandjensen K (1995) Size-dependent nitrogen uptake in micro- and macroalgae. Mar Ecol Prog Ser 118:247–253. doi: 10.3354/meps118247 Google Scholar
  42. Holliday NP, Hughes SL, Bacon S, Beszczynska-Möller A, Hansen B, Lavin A, Loeng H, Mork KA, Osterhus S, Sherwin T, Walczowski W (2008) Reversal of the 1960s to 1990s freshening trend in the northeast North Atlantic and Nordic Seas. Geophys Res Lett. doi: 10.1029/2007GL032675 Google Scholar
  43. Holliday NP, Bacon S, Allen J, McDonagh EL (2009) Circulation and transport in the Western Boundary Currents at Cape Farewell, Greenland. J Phys Oceanogr 39:1854–1870. doi: 10.1175/2009jpo4160.1 Google Scholar
  44. Huse SM, Huber JA, Morrison HG, Sogin ML, Mark Welch D (2007) Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol. doi: 10.1186/gb-2007-8-7-r143 Google Scholar
  45. Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898. doi: 10.1111/j.1462-2920.2010.02193.x PubMedCentralPubMedGoogle Scholar
  46. Jones EP, Anderson LG, Swift JH (1998) Distribution of Atlantic and Pacific waters in the upper Arctic Ocean: implications for circulation. Geophys Res Lett 25:765–768. doi: 10.1029/98gl00464 Google Scholar
  47. Kattner G, Becker H (1991) Nutrients and organic nitrogenous compounds in the marginal ice zone of the Fram Strait. J Mar Syst 2:385–394Google Scholar
  48. Kerouel R, Aminot A (1997) Fluorometric determination of ammonia in sea and estuarine waters by direct segmented flow analysis. Mar Chem 57:265–275. doi: 10.1016/s0304-4203(97)00040-6 Google Scholar
  49. Kirchman DL, Moran XAG, Ducklow H (2009) Microbial growth in the polar oceans—role of temperature and potential impact of climate change. Nat Rev Microbiol 7:451–459. doi: 10.1038/nrmicro2115 PubMedGoogle Scholar
  50. Kirchman DL, Cottrell MT, Lovejoy C (2010) The structure of bacterial communities in the western Arctic Ocean as revealed by pyrosequencing of 16S rRNA genes. Environ Microbiol 12:1132–1143. doi: 10.1111/j.1462-2920.2010.02154.x PubMedGoogle Scholar
  51. Kirst GO, Wiencke C (1995) Ecophysiology of polar algae. J Phycol 31:181–199. doi: 10.1111/j.0022-3646.1995.00181.x Google Scholar
  52. Kunin V, Engelbrektson A, Ochman H, Hugenholtz P (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12:118–123. doi: 10.1111/j.1462-2920.2009.02051.x PubMedGoogle Scholar
  53. Lachance MA (2004) Here and there or everywhere? Bioscience 54:884Google Scholar
  54. Landry MR, Barber RT, Bidigare RR, Chai F, Coale KH, Dam HG, Lewis MR, Lindley ST, McCarthy JJ, Roman MR, Stoecker DK, Verity PG, White JR (1997) Iron and grazing constraints on primary production in the central equatorial Pacific: an EqPac synthesis. Limnol Oceanogr 42:405–418Google Scholar
  55. Le Borgne R, Feely RA, Mackey DJ (2002) Carbon fluxes in the equatorial Pacific: a synthesis of the JGOFS programme. Deep Sea Res Part II Top Stud Oceanogr 49:2425–2442. doi: 10.1016/s0967-0645(02)00043-7 Google Scholar
  56. Leu E, Soreide JE, Hessen DO, Falk-Petersen S, Berge J (2011) Consequences of changing sea-ice cover for primary and secondary producers in the European Arctic shelf seas: timing, quantity, and quality. Prog Oceanogr 90:18–32. doi: 10.1016/j.pocean.2011.02.004 Google Scholar
  57. Li WKW (1994) Primary production of prochlorophytes, cyanobacteria, and eukaryotic ultraphytoplankton—measurements from flow cytometric sorting. Limnol Oceanogr 39:169–175Google Scholar
  58. Li WKW, McLaughlin FA, Lovejoy C, Carmack EC (2009) Smallest algae thrive as the Arctic Ocean freshens. Science 326:539. doi: 10.1126/science.1179798 PubMedGoogle Scholar
  59. Lopez-Garcia P, Lopez-Lopez A, Moreira D, Rodriguez-Valera F (2001) Diversity of free-living prokaryotes from a deep-sea site at the Antarctic Polar Front. FEMS Microbiol Ecol 36:193–202. doi: 10.1016/s0168-6496(01)00133-7 PubMedGoogle Scholar
  60. Lovejoy C, Potvin M (2011) Microbial eukaryotic distribution in a dynamic Beaufort Sea and the Arctic Ocean. J Plankton Res 33:431–444. doi: 10.1093/plankt/fbq124 Google Scholar
  61. Lovejoy C, Legendre L, Martineau MJ, Bacle J, von Quillfeldt CH (2002) Distribution of phytoplankton and other protists in the North Water. Deep Sea Res Part II Top Stud Oceanogr 49:5027–5047Google Scholar
  62. Lovejoy C, Massana R, Pedros-Alio C (2006) Diversity and distribution of marine microbial eukaryotes in the Arctic Ocean and adjacent seas. Appl Environ Microbiol 72:3085–3095. doi: 10.1128/aem.72.5.3085-3095.2006 PubMedCentralPubMedGoogle Scholar
  63. Lovejoy C, Vincent WF, Bonilla S, Roy S, Martineau MJ, Terrado R, Potvin M, Massana R, Pedros-Alio C (2007) Distribution, phylogeny, and growth of cold-adapted picoprasinophytes in arctic seas. J Phycol 43:78–89. doi: 10.1111/j.1529-8817.2006.00310.x Google Scholar
  64. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371. doi: 10.1093/nar/gkh293 PubMedCentralPubMedGoogle Scholar
  65. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen ZT, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer MLI, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu PG, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380. doi: 10.1038/nature03959 PubMedCentralPubMedGoogle Scholar
  66. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112. doi: 10.1038/nrmicro1341 PubMedGoogle Scholar
  67. Massana R, Terrado R, Forn I, Lovejoy C, Pedros-Alio C (2006a) Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environ Microbiol 8:1515–1522. doi: 10.1111/j.1462-2920.2006.01042.x PubMedGoogle Scholar
  68. Massana R, Guillou L, Terrado R, Forn I, Pedros-Alio C (2006b) Growth of uncultured heterotrophic flagellates in unamended seawater incubations. Aquat Microb Ecol 45:171–180. doi: 10.3354/ame045171 Google Scholar
  69. Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S like rRNA coding regions. Gene 71:491–499PubMedGoogle Scholar
  70. Mock T, Krell A, Glockner G, Kolukisaoglu U, Valentin K (2006) Analysis of expressed sequence tags (ests) from the polar diatom Fragilariopsis cylindrus. J Phycol 42:78–85. doi: 10.1111/j.1529-8817.2005.00164.x Google Scholar
  71. 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. doi: 10.1038/35054541 PubMedGoogle Scholar
  72. Mundy CJ, Barber DG, Michel C (2005) Variability of snow and ice thermal, physical and optical properties pertinent to sea ice algae biomass during spring. J Mar Syst 58:107–120. doi: 10.1016/j.jmarsys.2005.07.003 Google Scholar
  73. Mundy CJ, Gosselin M, Ehn J, Gratton Y, Rossnagel A, Barber DG, Martin J, Tremblay JE, Palmer M, Arrigo KR, Darnis G, Fortier L, Else B, Papakyriakou T (2009) Contribution of under-ice primary production to an ice-edge upwelling phytoplankton bloom in the Canadian Beaufort Sea. Geophys Res Lett 36:L17601. doi: 10.1029/2009gl038837 Google Scholar
  74. Not F, Latasa M, Marie D, Cariou T, Vaulot D, Simon N (2004) A single species, Micromonas pusilla (Prasinophyceae), dominates the eukaryotic picoplankton in the western English channel. Appl Environ Microbiol 70:4064–4072. doi: 10.1128/aem.70.7.4064-4072.2004 PubMedCentralPubMedGoogle Scholar
  75. Not F, Massana R, Latasa M, Marie D, Colson C, Eikrem W, Pedros-Alio C, Vaulot D, Simon N (2005) Late summer community composition and abundance of photosynthetic picoeukaryotes in Norwegian and Barents Seas. Limnol Oceanogr 50:1677–1686Google Scholar
  76. Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2011) Vegan: community ecology package, R package version 1.17-6 edGoogle Scholar
  77. Patterson DJ (2009) Seeing the big picture on microbe distribution. Science 325:1506–1507. doi: 10.1126/science.1179690 PubMedGoogle Scholar
  78. Pedros-Alio C (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14:257–263PubMedGoogle Scholar
  79. Pedros-Alio C (2007) Dipping into the rare biosphere. Science 315:192–193. doi: 10.1126/science.1135933 PubMedGoogle Scholar
  80. Pedros-Alio C (2012) The rare bacterial biosphere. Ann Rev Mar Sci 4:449–466 Google Scholar
  81. Pernthaler J (2005) Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3(9):537–546PubMedGoogle Scholar
  82. Perovich DK, Roesler CS, Pegau WS (1998) Variability in Arctic sea ice optical properties. J Geophys Res Oceans 103:1193–1208. doi: 10.1029/97jc01614 Google Scholar
  83. Potvin M, Lovejoy C (2007) Comparisons of inshore and offshore arctic marine picoeukaryotes. J Phycol 43:160Google Scholar
  84. Potvin M, Lovejoy C (2009) PCR-based diversity estimates of artificial and environmental 18S rRNA gene libraries. J Eukaryot Microbiol 56:174–181. doi: 10.1111/j.1550-7408.2008.00386.x PubMedGoogle Scholar
  85. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig WG, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. doi: 10.1093/nar/gkm864 PubMedCentralPubMedGoogle Scholar
  86. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  87. Ramette A (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75:2495–2505. doi: 10.1128/aem.02409-08 PubMedCentralPubMedGoogle Scholar
  88. Rat’kova TN, Wassmann P (2002) Seasonal variation and spatial distribution of phyto- and protozooplankton in the central Barents Sea. J Mar Syst 38:47–75. doi: 10.1016/s0924-7963(02)00169-0 Google Scholar
  89. Richardson K, Markager S, Buch E, Lassen MF, Kristensen AS (2005) Seasonal distribution of primary production, phytoplankton biomass and size distribution in the Greenland Sea. Deep Sea Res Part I Oceanogr Res Pap 52:979–999. doi: 10.1016/j.dsr.2004.12.005 Google Scholar
  90. Rudels B, Larsson AM, Sehlstedt PI (1991) Stratification and water mass formation in the Arctic Ocean—some implications for the nutrient distribution. Polar Res 10:19–31. doi: 10.1111/j.1751-8369.1991.tb00631.x Google Scholar
  91. Sakshaug E, Slagstad D (1991) Light and productivity of phytoplankton in polar marine ecosystems—a physiological view. Polar Res 10:69–85. doi: 10.1111/j.1751-8369.1991.tb00636.x Google Scholar
  92. Schauer U, Loeng H, Rudels B, Ozhigin VK, Dieck W (2002) Atlantic water flow through the Barents and Kara Seas. Deep Sea Res Part I Oceanogr Res Papers 49:2281–2298. doi: 10.1016/s0967-0637(02)00125-5 Google Scholar
  93. Schauer U, Fahrbach E, Osterhus S, Rohardt G (2004) Arctic warming through the Fram Strait: oceanic heat transport from 3 years of measurements. J Geophys Res Oceans: C06026. doi: 10.1029/2003jc001823
  94. Sherr EB, Sherr BF, Fessenden L (1997) Heterotrophic protists in the Central Arctic Ocean. Deep Sea Res Part I Top Stud Oceanogr 44:1665. doi: 10.1016/s0967-0645(97)00050-7 Google Scholar
  95. Slapeta J, Lopez-Garcia P, Moreira D (2006) Global dispersal and ancient cryptic species in the smallest marine eukaryotes. Mol Biol Evol 23:23–29. doi: 10.1093/molbev/msj001 PubMedGoogle Scholar
  96. Smetacek V, Nicol S (2005) Polar ocean ecosystems in a changing world. Nature 437:362–368. doi: 10.1038/nature04161 PubMedGoogle Scholar
  97. Smith JL, Barrett JE, Tusnady G, Rejto L, Cary SC (2010) Resolving environmental drivers of microbial community structure in Antarctic soils. Antarct Sci 22:673–680. doi: 10.1017/s0954102010000763 Google Scholar
  98. Sogaard DH, Hansen PJ, Rysgaard S, Glud RN (2011) Growth limitation of three Arctic sea ice algal species: effects of salinity, pH, and inorganic carbon availability. Polar Biol 34:1157–1165. doi: 10.1007/s00300-011-0976-3 Google Scholar
  99. Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120. doi: 10.1073/pnas.0605127103 PubMedCentralPubMedGoogle Scholar
  100. Stoeck T, Bass D, Nebel M, Christen R, Jones MDM, Breiner HW, Richards TA (2010) Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol 19:21–31. doi: 10.1111/j.1365-294X.2009.04480.x PubMedGoogle Scholar
  101. Stroeve J, Holland MM, Meier W, Scambos T, Serreze M (2007) Arctic sea ice decline: faster than forecast. Geophys Res Lett. doi: 10.1029/2007GL029703 Google Scholar
  102. Terlizzi A, Anderson MJ, Bevilacqua S (2009) Beta diversity and taxonomic sufficiency: do higher-level taxa reflect heterogeneity in species composition? Divers Distrib 15:450–458Google Scholar
  103. Tremblay JE, Klein B, Legendre L, Rivkin RB, Therriault JC (1997) Estimation of f-ratios in oceans based on phytoplankton size structure. Limnol Oceanogr 42:595–601Google Scholar
  104. Tremblay G, Belzile C, Gosselin M, Poulin M, Roy S, Tremblay JE (2009) Late summer phytoplankton distribution along a 3500 km transect in Canadian Arctic waters: strong numerical dominance by picoeukaryotes. Aquat Microb Ecol 54:55–70. doi: 10.3354/ame01257 Google Scholar
  105. Vaulot D, Eikrem W, Viprey M, Moreau H (2008) The diversity of small eukaryotic phytoplankton (≤3 µm) in marine ecosystems. FEMS Microbiol Rev 32:795–820. doi: 10.1111/j.1574-6976.2008.00121.x PubMedGoogle Scholar
  106. Vergin KL, Beszteri B, Monier A et al (2013) High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences. ISME J 7:1322–1332. doi: 10.1038/ismej.2013.32 PubMedCentralPubMedGoogle Scholar
  107. von Quillfeldt CH (2004) The diatom Fragilariopsis cylindrus and its potential as an indicator species for cold water rather than for sea ice. Vie Milieu 54:137–143Google Scholar
  108. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  109. Worden AZ, Nolan JK, Palenik B (2004) Assessing the dynamics and ecology of marine picophytoplankton: the importance of the eukaryotic component. Limnol Oceanogr 49:168–179Google Scholar
  110. 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. doi: 10.1016/j.femsec.2004.10.006 PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Estelle Kilias
    • 1
    Email author
  • Gerhard Kattner
    • 1
  • Christian Wolf
    • 1
  • Stephan Frickenhaus
    • 1
  • Katja Metfies
    • 1
  1. 1.Alfred Wegener Institute for Polar and Marine ResearchBremerhavenGermany

Personalised recommendations