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

Polar Biology

Volumn 35, Issue 4, 2012, Pages 519-533

  Sorensen N ^a,b   Daugbjerg, N ^a   Gabrielsen, T M ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY CENTRE IN SVALBARD   (Norway)

Author keywords

Arctic; Environmental cloning; Picobiliphytes; Picoplankton; Spring bloom

Indexed keywords

ALGAL BLOOM; AUTOTROPHY; BIOMASS; CHLOROPHYLL A; CLONE; ECOSYSTEM FUNCTION; GROWING SEASON; MARINE ECOSYSTEM; MOLECULAR ANALYSIS; PICOPLANKTON; PROTIST; SPECIES DIVERSITY; TEMPORAL VARIATION;

ARCTIC; SVALBARD; SVALBARD AND JAN MAYEN;

ALVEOLATA; MICROMONAS PUSILLA; PROTISTA; STRAMENOPILES;

EID: 84858005062     PISSN: 07224060     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00300-011-1097-8     Document Type: Article

References (63)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. Holm-Hansen O, Riemann B (1978) Chlorophyll a determination: improvements in methodology. Oikos 30(3): 438-447.
17. 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.
18. IPCC (2007) Climate change 2007: Synthesis report. Geneva, Switzerland. doi: 10. 1136/bmj. 39420. 654583. 25.
19. 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.
20. 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.
21. Li WKW (1998) Annual average abundance of heterotrophic bacteria and Synechococcus in surface ocean waters. Limnol Oceanogr 43(7): 1746-1753.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9): 817-818. doi: 10. 1093/bioinformatics/14. 9. 817.
49. 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.
50. 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.
51. 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.
52. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12): 1572-1574. doi: 10. 1093/bioinformatics/btg180.
53. 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.
54. 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.
55. 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.
56. 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.
57. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland.
58. 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.
59. Taylor DL, Lee CC (1971) New Cryptomonad from Antarctica: Cryptomonas cryophila sp. nov. Arch Mikrobiol 75(4): 269-280.
60. 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.
61. 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.
62. 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.
63. 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.