Polar Biology

, Volume 34, Issue 12, pp 1901–1914 | Cite as

Protist community composition during spring in an Arctic flaw lead polynya

  • Ramon TerradoEmail author
  • Emmanuelle Medrinal
  • Cindy Dasilva
  • Mary Thaler
  • Warwick F. Vincent
  • Connie Lovejoy
Original Paper


The overwintering deployment of an icebreaker during the Canadian Flaw Lead study provided an opportunity to evaluate how protist communities (phytoplankton and other single-celled eukaryotes) respond to changing spring irradiance conditions in flaw lead polynyas, where open water persists between the central pack ice and land fast ice. We combined microscopic analysis of the protist communities (all cell sizes) with clone libraries of 18S rRNA genes and 18S rRNA (from RNA converted to cDNA) of size-fractionated seawater (0.2–3.0 μm) from 10 to 12 m depth in the surface mixed layer. The rRNA gene analysis provided information on the presence of organisms, while the rRNA analysis provided information on the most active members of the community. There was little overlap between the two types of clone libraries, and there were large community shifts over time. Heterotrophic dinoflagellates and ciliates were the most common sequences recovered. The relative proportion of photosynthetic protist sequences increased in March and April, and there was greater representation of Bacillariophyta, Prasinophyta, Haptophyta, and Cryptophyta in the rRNA compared to rRNA gene libraries. Microscopy indicated that large-celled diatoms dominated the community in May, when chlorophyll concentrations were greatest. However, the RNA sequencing showed that heterotrophic and putative parasitic protists were proportionately more active, and the concomitant decrease in nutrients suggested that the spring phytoplankton bloom had begun to decline by this time. These observations provide evidence of substantial changes in protist community structure and function during the spring transition.


Euphotic zone Phytoplankton Protist Arctic Ocean Beaufort Sea Environmental clone libraries Biodiversity Microbial food webs 



We thank Marianne Potvin for her assistance with laboratory work, and our fellow scientists, officers, and crew of the CCCG Amundsen for their support during the cruise. We also would like to thank E. Sherr and two anonymous reviewers for constructive comments on earlier versions of this manuscript. This work is a contribution to the International Polar Year—Circumpolar Flaw Lead system study (IPY-CFL 2007/2008) led by D. Barber (University of Manitoba) supported through grants from the Canadian IPY Federal Program Office and the Natural Sciences and Engineering Council (NSERC Canada). This is a contribution to ArcticNet.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Adl SM, Simpson AGB, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MFJR (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451PubMedCrossRefGoogle Scholar
  2. Agatha S, Strüder-Kypke MC (2007) Phylogeny of the order Choreotrichida (Ciliophora, Spirotricha, Oligotrichea) as inferred from morphology, ultrastructure, ontogenesis, and SSrRNA gene sequences. Euro Protist 43:37–63CrossRefGoogle Scholar
  3. Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693PubMedCrossRefGoogle Scholar
  4. Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS One 4:e6372PubMedCrossRefGoogle Scholar
  5. Anderson CR, Siegel DA, Brzezinski MA, Guillocheau N (2008) Controls on temporal patterns in phytoplankton community structure in the Santa Barbara Channel, California. J Geophys Res-Oceans 113:C04038CrossRefGoogle Scholar
  6. Archibald JM (2007) Nucleomorph genomes: structure, function, origin and evolution. Bioessays 29:392–402PubMedCrossRefGoogle Scholar
  7. Barber DG, Asplin MG, Gratton Y, Lukovich J, Galley R, Raddatz RL, Leitch D (2010) The International Polar Year (IPY) Circumpolar Flaw Lead (CFL) system study: overview and the physical system. Atmosphere-Ocean (in press)Google Scholar
  8. Booth BC, Horner RA (1997) Microalgae on the Arctic Ocean Section, 1994: species abundance and biomass. Deep-Sea Res Pt II 44:1607–1622CrossRefGoogle Scholar
  9. Buckley BA, Szmant AM (2004) RNA/DNA ratios as indicators of metabolic activity in four species of Caribbean reef-building corals. Mar Ecol-Prog Ser 282:143–149CrossRefGoogle Scholar
  10. Carmack EC, Macdonald RW, Papadakis JE (1989) Water mass structure and boundaries in the Mackenzie shelf estuary. J Geophys Res 94(C12):18043–18055Google Scholar
  11. Carmack EC, Macdonald RW, Jasper S (2004) Phytoplankton productivity on the Canadian Shelf of the Beaufort Sea. Mar Ecol Prog Ser 277:37–50CrossRefGoogle Scholar
  12. Cavalier-Smith T (2005) Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Ann Bot Lond 95:147–175CrossRefGoogle Scholar
  13. Church MJ, Short CM, Jenkins BD, Karl DM, Zehr JP (2005) Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Appl Environ Microbiol 71:5362–5370PubMedCrossRefGoogle Scholar
  14. Diez 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 67:2932–2941PubMedCrossRefGoogle Scholar
  15. Felsenstein J (2005) PHYLIP—phylogeny inference package (Version 3.2). Cladistics 5:164–166Google Scholar
  16. Galand PE, Lovejoy C, Hamilton AK, Ingram RG, Pedneault E, Carmack EC (2009) Archaeal diversity and a gene for ammonia oxidation are coupled to oceanic circulation. Environ Microbiol 11:971–980PubMedCrossRefGoogle Scholar
  17. Garneau M, Roy S, Lovejoy C, Gratton Y, Vincent WF (2008) Seasonal dynamics of bacterial biomass and production in a coastal arctic ecosystem: Franklin Bay, western Canadian Arctic. J Geophys Res 113:C07S91, doi: 10.1029/2007JC004281
  18. Grasshoff K (1999) Methods of seawater analyses. Weinheim, New YorkCrossRefGoogle Scholar
  19. Greene CH, Pershing AJ (2007) Climate drives sea change. Science 315:1084–1085PubMedCrossRefGoogle Scholar
  20. Guillou L, Viprey M, Chambouvet A, Welsh RM, Kirkham AR, Massana R, Scanlan DJ, Worden AZ (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol 10:3349–3365PubMedCrossRefGoogle Scholar
  21. Hakkinen S, Rhines PB (2009) Shifting surface currents in the northern North Atlantic Ocean. J Geophys Res-Oceans 114:C04005CrossRefGoogle Scholar
  22. Hamilton AK, Lovejoy C, Galand PE, Ingram RG (2008) Water masses and biogeography of picoeukaryote assemblages in a cold hydrographically complex system. Limnol Oceanogr 53:922–935CrossRefGoogle Scholar
  23. Hanic LA, Sekimoto S, Bates SS (2009) Oomycete and chytrid infections of the marine diatom Pseudo-nitzschia pungens (Bacillariophyceae) from Prince Edward Island, Canada. Botany 87:1096–1105CrossRefGoogle Scholar
  24. Hansen PJ, Calado AJ (1999) Phagotrophic mechanisms and prey selection in free-living dinoflagellates. J Eukaryot Microbiol 46:382–389CrossRefGoogle Scholar
  25. Harada A, Ohtsuka S, Horiguch T (2007) Species of the parasitic genus Duboscquella are members of the enigmatic Marine Alveolate Group I. Protist 158:337–347PubMedCrossRefGoogle Scholar
  26. Hendriks L, Goris A, Neefs J-M, Van de Peer Y, Hennebert GL, De Wachter R (1989) The nucleotide sequence of the small ribosomal subunit RNA of the yeast Candida albicans and the evolutionary position of the fungi among the eukaryotes. Syst Appl Microbiol 12:223–229Google Scholar
  27. Ingram RG, Bâcle J, Barber DG, Gratton Y, Melling H (2002) An overview of physical processes in the North Water. Deep-Sea Res Pt II 49:4893–4906CrossRefGoogle Scholar
  28. Jeong HJ (1999) The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J Euk Microbiol 46:390–396CrossRefGoogle Scholar
  29. Kagami M, de Bruin A, Ibelings BW, Van Donk E (2007) Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 578:113–129CrossRefGoogle Scholar
  30. Larsen A, Flaten GAF, Sandaa R-A, Castberg T, Thyrhaug R, Erga SR, Jacquet S, Bratbak G (2004) Spring phytoplankton bloom dynamics in Norwegian coastal waters: Microbial community succession and diversity. Limnol Oceanogr 49:180–190CrossRefGoogle Scholar
  31. Li WKW, McLaughlin FA, Lovejoy C, Carmack EC (2009) Smallest algae thrive as the Arctic Ocean freshens. Science 326:539–539PubMedCrossRefGoogle Scholar
  32. Litchman E, Klausmeier CA, Miller JR, Schofield OM, Falkowski PG (2006) Multi-nutrient, multi-group model of present and future oceanic phytoplankton communities. Biogeosciences 3:585–606CrossRefGoogle Scholar
  33. López-García P, Rodríguez-Valera F, Pedrós-Alió C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607PubMedCrossRefGoogle Scholar
  34. Lovejoy C, Potvin M (2010) Microbial eukaryotic distribution in a dynamic Beaufort Sea and the Arctic Ocean. J Plankton Res, doi: 10.1093/plankt/fbq124
  35. Lovejoy C, Legendre L, Martineau M, Bâcle J, von Quillfeldt CH (2002) Distribution of phytoplankton and other protists in the North Water. Deep-Sea Res Pt II 49:5027–5047CrossRefGoogle Scholar
  36. Lovejoy C, Price NM, Legendre L (2004) Role of nutrient supply and loss in controlling protist species dominance and microbial food-webs during spring blooms. Aquat Microbiol Ecol 34:79–92CrossRefGoogle Scholar
  37. 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 72:3085–3095PubMedCrossRefGoogle Scholar
  38. Lovejoy C, Vincent WF, Bonilla S, Roy S, Martineau M-J, Terrado R, Potvin M, Massana R, Pedrós-Alió C (2007) Distribution, phylogeny, and growth of cold-adapted picoprasinophytes in arctic seas. J Phycol 43:78–89CrossRefGoogle Scholar
  39. Lynn DH (2008) The ciliated protozoa: characterization, classification, and guide to the literature. Springer Science, BerlinGoogle Scholar
  40. Massana R, Pedrós-Alió C (2008) Unveiling new microbial eukaryotes in the surface ocean. Curr Opin Microbiol 11:213–218PubMedCrossRefGoogle Scholar
  41. Massana R, Terrado R, Forn I, Lovejoy C, Pedrós-Alió C (2006) Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environ Microbiol 8:1515–1522PubMedCrossRefGoogle Scholar
  42. Medinger R, Nolte V, Pandey RV, Jost S, Ottenwälder B, Schlöterer C, Boenigk J (2010) Diversity in a hidden world: potential and limitation of next-generation sequencing for surveys of molecular diversity of eukaryotic microorganisms. Mol Ecol 19:32–40PubMedCrossRefGoogle Scholar
  43. Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499PubMedCrossRefGoogle Scholar
  44. Medlin LK, Metfies K, Mehl H, Wiltshire K, Valentin K (2006) Picoeukaryotic plankton diversity at the Helgoland time series site as assessed by three molecular methods. Microbiol Ecol 52:53–71CrossRefGoogle Scholar
  45. Mei Z-P, Legendre L, Gratton Y, Tremblay J-É, LeBlanc B, Mundy C, Klein B, Gosselin M, Larouche P, Papakyriakou T, Lovejoy C, von Quillfeldt CH (2002) Physical control of spring-summer phytoplankton dynamics in the North water, April-July 1998. Deep-Sea Res Pt II 49:4959–4982CrossRefGoogle Scholar
  46. Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 45:569–579CrossRefGoogle Scholar
  47. Middelboe M, Lundsgaard C (2003) Microbial activity in the Greenland Sea: role of DOC lability, mineral nutrients and temperature. Aquat Microb Ecol 32:151–163CrossRefGoogle Scholar
  48. Not F, del Campo J, Balague V, de Vargas C, Massana R (2009) New insights into the diversity of marine picoeukaryotes. Plos One 4:e7143PubMedCrossRefGoogle Scholar
  49. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, OxfordGoogle Scholar
  50. Pomeroy LR, Wiebe WJ, Deibel D, Thompson RJ, Rowe GT, Pakulski JD (1991) Bacterial responses to temperature and substrate concentration during the Newfoundland spring bloom. MEPS 75:143–159CrossRefGoogle Scholar
  51. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948CrossRefGoogle Scholar
  52. Potvin M, Lovejoy C (2009) PCR-Based Diversity Estimates of Artificial and Environmental 18S rRNA Gene Libraries. J Eukaryot Microbiol 56:174–181PubMedCrossRefGoogle Scholar
  53. Rodriguez F, Varela M, Zapata M (2002) Phytoplankton assemblages in the Gerlache and Bransfield Straits (Antarctic Peninsula) determined by light microscopy and CHEMTAX analysis of HPLC pigment data. Deep-Sea Res Pt Ii 49:723–747CrossRefGoogle Scholar
  54. Rodríguez-Martínez R, Labrenz M, del Campo J, Forn I, Juergens K, Massana R (2009) Distribution of the uncultured protist MAST-4 in the Indian Ocean, Drake Passage and Mediterranean Sea assessed by real-time quantitative PCR. Environ Microbiol 11:397–408PubMedCrossRefGoogle Scholar
  55. Romari K, Vaulot D (2004) Composition and temporal variability of picoeukaryote communities at a coastal site of the English Channel from 18S rDNA sequences. Limnol Oceanogr 49:784–798CrossRefGoogle Scholar
  56. Rose JM, Vora NM, Countway PD, Gast RJ, Caron DA (2009) Effects of temperature on growth rate and gross growth efficiency of an Antarctic bacterivorous protist. ISME J 3:252–260PubMedCrossRefGoogle Scholar
  57. Różańska M, Poulin M, Gosselin M (2008) Protist entrapment in newly formed sea ice in the coastal Arctic Ocean. J Marine Syst 74:887–901CrossRefGoogle Scholar
  58. Sakshaug E, Stein R, Macdonald RW (2004) Primary and secondary production in Arctic seas. In: Stein R, Macdonald RW (eds) The organic carbon cycle in the Arctic Ocean. Springer, BerlinGoogle Scholar
  59. Schloss P, Westcott S, Ryabin T, Hall J, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541PubMedCrossRefGoogle Scholar
  60. Seuthe L, Darnis G, Riser CW, Wassmann P, Fortier L (2007) Winter–spring feeding and metabolism of Arctic copepods: insights from faecal pellet production and respiration measurements in the southeastern Beaufort Sea. Polar Biol 30:427–436CrossRefGoogle Scholar
  61. Sherr EB, Sherr BF (2002) Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek 81:293–308PubMedCrossRefGoogle Scholar
  62. Sherr EB, Sherr BF, Wheeler P, Thompson K (2003) Temporal and spatial variation in stocks of autotrophic and heterotrophic microbes in the upper water column of the central Arctic Ocean. Deep-Sea Res Pt I 50:557–571CrossRefGoogle Scholar
  63. Sherr EB, Sherr BF, Hartz AJ (2009) Microzooplankton grazing impact in the Western Arctic Ocean. Deep-Sea Res Pt II 56:1264–1273CrossRefGoogle Scholar
  64. Skovgaard A, Massana R, Balague V, Saiz E (2005) Phylogenetic position of the copepod-infesting parasite Syndinium turbo (Dinoflagellata, Syndinea). Protist 156:413–423PubMedCrossRefGoogle Scholar
  65. Smith WO Jr, Sakshaug E (1990) Polar phytoplankton. In: Smith WO, (ed) Polar oceanography. Part B. Chemistry, biology, and geology. Academic Press, San Diego, pp 477–525Google Scholar
  66. Sogin ML, Gunderson JH (1987) Structural diversity of eukaryotic small subunit ribosomal RNAs. Ann NY Acad Sci 503:125–139PubMedCrossRefGoogle Scholar
  67. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. PNAS 103:12115–12120PubMedCrossRefGoogle Scholar
  68. Stentiford G, Shields J (2005) A review of the parasitic dinoflagellates Hematodinium species and Hematodinium-like infections in marine crustaceans. Dis Aquat Organ 66:47–70PubMedCrossRefGoogle Scholar
  69. Stoeck T, Kasper J, Bunge J, Leslin C, Ilyin V, Epstein S (2007a) Protistan diversity in the Arctic: a case of paleoclimate shaping modern biodiversity? Plos One 2:e728PubMedCrossRefGoogle Scholar
  70. Stoeck T, Zuendorf A, Breiner H-W, Behnke A (2007b) A molecular approach to identify active microbes in environmental eukaryote clone libraries. Microbiol Ecol 53:328–339CrossRefGoogle Scholar
  71. Strüder-Kypke MC, Lynn DH (2003) Sequence analyses of the small subunit rRNA gene confirm the paraphyly of oligotrich ciliates sensu lato and support the monophyly of the subclasses Oligotrichia and Choreotrichia (Ciliophora, Spirotrichea). J Zool Lond 260:87–97CrossRefGoogle Scholar
  72. Terrado R, Lovejoy C, Massana R, Vincent WF (2008) Microbial food web responses to light and nutrients beneath the coastal Arctic Ocean sea ice during the winter-spring transition. J Mar Syst 74:964–977CrossRefGoogle Scholar
  73. Terrado R, Vincent WF, Lovejoy C (2009) Mesopelagic protists: diversity and succession in a coastal Arctic ecosystem. Aquat Microbiol Ecol 56:25–39CrossRefGoogle Scholar
  74. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  75. Tremblay J-É, Simpson K, Martin J, Miller L, Gratton Y, Barber D, Price NM (2008) Vertical stability and the annual dynamics of nutrients and chlorophyll fluorescence in the coastal, southeast Beaufort Sea. J Geophys Res 113:C07S90Google Scholar
  76. Vaqué D, Guadayol O, Peters F, Felipe J, Angel-Ripoll L, Terrado R, Lovejoy C, Pedrós-Alió C (2008) Seasonal changes in planktonic bacterivory rates under the ice-covered coastal Arctic Ocean. Limnol Oceanogr 53:2427–2438CrossRefGoogle Scholar
  77. Vaulot D, Eikrem W, Viprey M, Moreau H (2008) The diversity of small eukaryotic phytoplankton (< 3 μm) in marine ecosystems. FEMS Microbiol Rev 32:795–820PubMedCrossRefGoogle Scholar
  78. von Wintzingerode F, Gobel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213–229CrossRefGoogle Scholar
  79. Weisse T, Muller H, Pinto-Coelho RM, Schweizer A, Springmann D, Baldringer G (1990) Response of the microbial loop to the phytoplankton spring bloom in a large prealpine lake. Limnol Oceanogr 35:781–794CrossRefGoogle Scholar
  80. Worden AZ (2006) Picoeukaryote diversity in coastal waters of the Pacific Ocean. Aquat Microbiol Ecol 43:165–175CrossRefGoogle Scholar
  81. 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 52:79–92PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Ramon Terrado
    • 1
    Email author
  • Emmanuelle Medrinal
    • 1
  • Cindy Dasilva
    • 1
  • Mary Thaler
    • 1
  • Warwick F. Vincent
    • 2
  • Connie Lovejoy
    • 1
  1. 1.Département de Biologie and Québec-OceanUniversité LavalQuébec CityCanada
  2. 2.Département de Biologie and Centre d’études nordiques (CEN)Université LavalQuébec CityCanada

Personalised recommendations