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Molecular diversity and temporal variation of picoeukaryotes in two Arctic fjords, Svalbard

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Abstract

Picoeukaryotes (protists <3 μm) form an important component of Arctic marine ecosystems, although knowledge of their diversity and ecosystem functioning is limited. In this study, the molecular diversity and autotrophic biomass contribution of picoeukaryotes from January to June 2009 in two Arctic fjords at Svalbard were examined using 18S environmental cloning and size-fractioned chlorophyll a measurements. A total of 62 putative picoeukaryotic phylotypes were recovered from 337 positive clones. Putative picoeukaryotic autotrophs were mostly limited to one species: Micromonas pusilla, while the putative heterotrophic picoeukaryote assemblage was more diverse and dominated by uncultured marine stramenopiles (MAST) and marine alveolate groups. One MAST-1A phylotype was the only phylotype to be found in all clone libraries. The diversity of picoeukaryotes in general showed an inverse relationship with total autotrophic biomass, suggesting that the conditions dominating during the peak of the spring bloom may have a negative impact on picoeukaryote diversity. Picoplankton could contribute more than half of total autotrophic biomass before and after the spring bloom and benefited from an early onset of the growth season, whereas larger cells dominated the bloom itself.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. doi:10.1016/S0022-2836(05)80360-2

    PubMed  CAS  Google Scholar 

  • 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(8):1607–1622. doi:10.1016/S0967-0645(97)00057-X

    Article  Google Scholar 

  • Booth BC, Smith WO (1997) Autotrophic flagellates and diatoms in the Northeast Water Polynya, Greenland: summer 1993. J Mar Syst 10(1–4):241–261. doi:10.1016/S0924-7963(96)00081-4

    Article  Google Scholar 

  • Brewin RJW, Sathyendranath S, Hirata T, Lavender SJ, Barciela RM, Hardman-Mountford NJ (2010) A three-component model of phytoplankton size class for the Atlantic Ocean. Ecol Modell 221(11):1472–1483. doi:10.1016/j.ecolmodel.2010.02.014

    Article  CAS  Google Scholar 

  • Caron DA, Lim EL, Dennett MR, Gast RJ, Kosman C, DeLong EF (1999) Molecular phylogenetic analysis of the heterotrophic Chrysophyte genus Paraphysomonas (Chrysophyceae), and the design of rRNA-targeted oligonucleotide probes for two species. J Phycol 35(4):824–837. doi:10.1046/j.1529-8817.1999.3540824.x

    Article  CAS  Google Scholar 

  • Chambouvet A, Morin P, Marie D, Guillou L (2008) Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science 322(5905):1254–1257. doi:10.1126/science.1164387

    Article  PubMed  CAS  Google Scholar 

  • Degerlund M, Eilertsen HC (2010) Main species characteristics of phytoplankton spring blooms in NE Atlantic and Arctic waters (68–80° N). Estuar Coast Shelf Sci 33(2):242–269. doi:10.1007/s12237-009-9167-7

    CAS  Google Scholar 

  • 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(7):2932–2941. doi:10.1128/AEM.67.7.2932-2941.2001

    Article  PubMed  CAS  Google Scholar 

  • Dobrzyn P, Tatur A, Keck A (2009) Photosynthetic pigments as indicators of phytoplankton development during spring and summer in Adventfjorden (Spitsbergen). Oceanology 49(3):368–376. doi:10.1134/S0001437009030096

    Article  Google Scholar 

  • Ekelund F, Daugbjerg N, Fredslund L (2004) Phylogeny of Heteromita, Cercomonas and Thaumatomonas based on SSU rDNA sequences, including the description of Neocercomonas jutlandica sp nov., gen. nov. Eur J Protistol 40(2):119–135. doi:10.1016/j.ejop.2003.12.002

    Article  Google Scholar 

  • Elwood HJ, Olsen GJ, Sogin ML (1985) The small subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Mol Biol Evol 2(5):399–410

    PubMed  CAS  Google Scholar 

  • Gradinger R, Lenz J (1995) Seasonal occurrence of picocyanobacteria in the Greenland Sea and central Arctic Ocean. Polar Biol 15(6):447–452. doi:10.1007/BF00239722

    Article  Google Scholar 

  • 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(12):3349–3365. doi:10.1111/j.1462-2920.2008.01731.x

    Article  PubMed  CAS  Google Scholar 

  • 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(3):922–935. doi:10.4319/lo.2008.53.3.0922

    Article  Google Scholar 

  • Hodal H, Kristiansen S (2008) The importance of small-celled phytoplankton in spring blooms at the marginal ice zone in the northern Barents Sea. Deep Sea Res Part II Top Stud Oceanogr 55(20–21):2176–2185. doi:10.1016/j.dsr2.2008.05.012

    Article  CAS  Google Scholar 

  • Holm-Hansen O, Riemann B (1978) Chlorophyll a determination: improvements in methodology. Oikos 30(3):438–447

    Article  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Evolution—Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294(5550):2310–2314. doi:10.1126/science.1065889

    Article  PubMed  CAS  Google Scholar 

  • IPCC (2007) Climate change 2007: Synthesis report. Geneva, Switzerland. doi:10.1136/bmj.39420.654583.25

  • Kaczmarska I, Lovejoy C, Potvin M, Macgillivary M (2009) Morphological and molecular characteristics of selected species of Minidiscus (Bacillariophyta, Thalassiosiraceae). Eur J Phycol 44(4):461–475. doi:10.1080/09670260902855873

    Article  CAS  Google Scholar 

  • Kolodziej K, Stoeck T (2007) Cellular identification of a novel uncultured marine stramenopile (MAST-12 clade) small-subunit rRNA gene sequence from a Norwegian estuary by use of fluorescence in situ hybridization-scanning electron microscopy. Appl Environ Microbiol 73(8):2718–2726. doi:10.1128/Aem.02158-06

    Article  PubMed  CAS  Google Scholar 

  • Li WKW (1998) Annual average abundance of heterotrophic bacteria and Synechococcus in surface ocean waters. Limnol Oceanogr 43(7):1746–1753

    Article  Google Scholar 

  • Li WKW, McLaughlin FA, Lovejoy C, Carmack EC (2009) Smallest algae thrive as the Arctic Ocean freshens. Science 326(5952):539. doi:10.1126/science.1179798

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Probert I, Uitz J, Claustre H, Aris-Brosou S, Frada M, Not F, de Vargas C (2009) Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans. Proc Natl Acad Sci USA 106(31):12803–12808. doi:10.1073/pnas.0905841106

    Article  PubMed  CAS  Google Scholar 

  • Lovejoy C, Potvin M (2011) Microbial eukaryotic distribution in a dynamic Beaufort Sea and the Arctic Ocean. J Plankton Res 33(3):431–444. doi:10.1093/plankt/fbq124

    Article  Google Scholar 

  • 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(5):3085–3095. doi:10.1128/aem.72.5.3085-3095.2006

    Article  PubMed  CAS  Google Scholar 

  • 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(1):78–89. doi:10.1111/j.1529-8817.2006.00310.x

    Article  CAS  Google Scholar 

  • Lovejoy C, Galand P, Kirchman D (2011) Picoplankton diversity in the Arctic Ocean and surrounding seas. Mar Biodivers 41(1):5–12. doi:10.1007/s12526-010-0062-z

    Article  Google Scholar 

  • Marie D, Shi XL, Rigaut-Jalabert F, Vaulot D (2010) Use of flow cytometric sorting to better assess the diversity of small photosynthetic eukaryotes in the English Channel. FEMS Microbiol Ecol 72(2):165–178. doi:10.1111/j.1574-6941.2010.00842.x

    Article  PubMed  CAS  Google Scholar 

  • Marin B, Melkonian M (2010) Molecular phylogeny and classification of the Mamiellophyceae class. nov (Chlorophyta) based on sequence comparisons of the nuclear- and plastid-encoded rRNA operons. Protist 161(2):304–336. doi:10.1016/j.protis.2009.10.002

    Google Scholar 

  • Massana R, Guillou L, Diez B, Pedros-Alio C (2002) Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Appl Environ Microbiol 68(9):4554–4558. doi:10.1128/Aem.68.9.4554-4558.2002

    Article  PubMed  CAS  Google Scholar 

  • Massana R, Balague V, Guillou L, Pedros-Alio C (2004a) Picoeukaryotic diversity in an oligotrophic coastal site studied by molecular and culturing approaches. FEMS Microbiol Ecol 50(3):231–243. doi:10.1016/j.femsec.2004.07.001

    Article  PubMed  CAS  Google Scholar 

  • Massana R, Castresana J, Balague V, Guillou L, Romari K, Groisillier A, Valentin K, Pedros-Alio C (2004b) Phylogenetic and ecological analysis of novel marine stramenopiles. Appl Environ Microbiol 70(6):3528–3534. doi:10.1128/Aem.70.6.3528-3534.2004

    Article  PubMed  CAS  Google Scholar 

  • Massana R, Guillou L, Terrado R, Forn I, Pedrós-Alió C (2006a) Growth of uncultured heterotrophic flagellates in unamended seawater incubations. Aquat Microb Ecol 45(2):171–180

    Article  Google Scholar 

  • Massana R, Terrado R, Forn I, Lovejoy C, Pedros-Alio C (2006b) Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environ Microbiol 8(9):1515–1522. doi:10.1111/j.1462-2920.2006.01042.x

    Article  PubMed  CAS  Google Scholar 

  • Massana R, Unrein F, Rodriguez-Martinez R, Forn I, Lefort T, Pinhassi J, Not F (2009) Grazing rates and functional diversity of uncultured heterotrophic flagellates. ISME J 3(5):588–596. doi:10.1038/ismej.2008.130

    Article  PubMed  CAS  Google Scholar 

  • McDonald SM, Sarno D, Scanlan DJ, Zingone A (2007) Genetic diversity of eukaryotic ultraphytoplankton in the Gulf of Naples during an annual cycle. Aquat Microb Ecol 50(1):75–89. doi:10.3354/ame01148

    Article  Google Scholar 

  • Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71(2):491–499. doi:10.1016/0378-1119(88)90066-2

    Article  PubMed  CAS  Google Scholar 

  • 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. Microb Ecol 52(1):53–71. doi:10.1007/s00248-005-0062-x

    Article  PubMed  CAS  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(6820):607–610. doi:10.1038/35054541

    Article  PubMed  CAS  Google Scholar 

  • Moustaka-Gouni M (1993) Phytoplankton succession and diversity in a warm monomictic, relatively shallow lake: Lake Volvi, Macedonia, Greece. Hydrobiol 249(1–3):33–42. doi:10.1007/BF00008841

    Article  Google Scholar 

  • Nitsche F, Weitere M, Scheckenbach F, Hausmann K, Wylezich C, Arndt H (2007) Deep sea records of choanoflagellates with a description of two new species. Acta Protozool 46(2):99–106

    CAS  Google Scholar 

  • Nolte V, Pandey RV, Jost S, Medinger R, Ottenwalder B, Boenigk J, Schlotterer C (2010) Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. Mol Ecol 19(14):2908–2915. doi:10.1111/j.1365-294X.2010.04669.x

    Article  PubMed  CAS  Google Scholar 

  • 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(5):1677–1686

    Article  CAS  Google Scholar 

  • Not F, Gausling R, Azam F, Heidelberg JF, Worden AZ (2007a) Vertical distribution of picoeukaryotic diversity in the Sargasso Sea. Environ Microbiol 9(5):1233–1252. doi:10.1111/j.1462-2920.2007.01247.x

    Article  PubMed  CAS  Google Scholar 

  • Not F, Valentin K, Romari K, Lovejoy C, Massana R, Tobe K, Vaulot D, Medlin L (2007b) Picobiliphytes: a marine picoplanktonic algal group with unknown affinities to other eukaryotes. Science (315):253–255. doi:10.1126/science.1136264

  • Not F, del Campo J, Balague V, de Vargas C, Massana R (2009) New insights into the diversity of marine picoeukaryotes. PLoS ONE 4(9):e7143. doi:10.1371/Journal.Pone.0007143

  • Piquet AMT, Scheepens JF, Bolhuis H, Wiencke C, Buma AGJ (2010) Variability of protistan and bacterial communities in two Arctic fjords (Spitsbergen). Polar Biol 33(11):1521–1536. doi:10.1007/s00300-010-0841-9

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9):817–818. doi:10.1093/bioinformatics/14.9.817

    Article  PubMed  CAS  Google Scholar 

  • Rhodes L, Burke B (1996) Morphology and growth characteristics of Chrysochromulina species (Haptophyceae = Prymnesiophyceae) isolated from New Zealand coastal waters. N Z J Mar Freshwater Res 30(1):91–103

    Article  Google Scholar 

  • Rodriguez-Martinez R, Labrenz M, del Campo J, Forn I, Jurgens 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(2):397–408. doi:10.1111/j.1462-2920.2008.01779.x

    Article  PubMed  CAS  Google Scholar 

  • 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(3):784–798

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574. doi:10.1093/bioinformatics/btg180

    Article  PubMed  CAS  Google Scholar 

  • Sherr EB, Sherr BF, Wheeler PA, 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 Part I Oceanogr Res Pap 50(5):557–571. doi:10.1016/s0967-0637(03)00031-1

    Article  Google Scholar 

  • Skovgaard A, Massana R, Balague V, Saiz E (2005) Phylogenetic position of the copepod-infesting parasite Syndinium turbo (Dinoflagellata, Syndinea). Protist 156(4):413–423. doi:10.1016/j.protis.2005.08.002

    Article  PubMed  CAS  Google Scholar 

  • Slapeta J, Lopez-Garcia P, Moreira D (2006) Global dispersal and ancient cryptic species in the smallest marine eukaryotes. Mol Biol Evol 23(1):23–29. doi:10.1093/molbev/msj001

    Article  PubMed  CAS  Google Scholar 

  • Smith JC, Platt T, Li WKW, Horne EPW, Harrison WG, Rao DVS, Irwin BD (1985) Arctic marine photoautotrophic picoplankton. Mar Ecol Prog Ser 20(3):207–220

    Article  CAS  Google Scholar 

  • Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526

    PubMed  CAS  Google Scholar 

  • Taylor DL, Lee CC (1971) New Cryptomonad from Antarctica: Cryptomonas cryophila sp. nov. Arch Mikrobiol 75(4):269–280

    Article  Google Scholar 

  • Vaulot D, Eikrem W, Viprey M, Moreau H (2008) The diversity of small eukaryotic phytoplankton (≤3 μm) in marine ecosystems. FEMS Microbiol Rev 32(5):795–820. doi:10.1111/j.1574-6976.2008.00121.x

    Article  PubMed  CAS  Google Scholar 

  • Wilgenbusch JC, Warren DL, Swofford DL (2004) AWTY: a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. http://www.ceb.csit.fsu.edu/awty

  • Worden AZ, Cuvelier ML, Bartlett DH (2006) In-depth analyses of marine microbial community genomics. Trends Microbiol 14(8):331–336. doi:10.1016/j.tim.2006.06.008

    Article  PubMed  CAS  Google Scholar 

  • Yoon HS, Price DC, Stepanauskas R, Rajah VD, Sieracki ME, Wilson WH, Yang EC, Duffy S, Bhattacharya D (2011) Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 332(6030):714–717. doi:10.1126/science.1203163

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by Svalbard Science Forum grant 3371 and a UNIS grant to TMG. The authors would like to thank Bioportal at the University of Oslo for providing CPU resources, Lilith Kuckero and Emma Johansson-Karlsson for chlorophyll a measurements and Svein Kristiansen for measuring nutrients. The authors would also like to thank Eike Müller for useful discussion when planning the molecular work and Sofia Isabel dos Santos Ribeiro, Daniel Vaulot and three anonymous reviewers for helpful criticism on earlier versions of this manuscript.

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Sørensen, N., Daugbjerg, N. & Gabrielsen, T.M. Molecular diversity and temporal variation of picoeukaryotes in two Arctic fjords, Svalbard. Polar Biol 35, 519–533 (2012). https://doi.org/10.1007/s00300-011-1097-8

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