Small phytoplankton in Arctic seas: vulnerability to climate change

Biodiversity

Volumn 14, Issue 1, 2013, Pages 2-18

  Terrado, Ramon ^a   Scarcella, Karen ^a   Thaler, Mary ^a   Vincent, Warwick F ^a,b   Lovejoy, Connie ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b CENTRE D ÉTUDES NORDIQUES   (Canada)

Author keywords

Arctic; climate change; diversity; ecotype; Mamiellophyceae; microalgae; Micromonas; phytoplankton

Indexed keywords

EID: 84873927363     PISSN: 14888386     EISSN: 21600651     Source Type: Journal    
DOI: 10.1080/14888386.2012.704839     Document Type: Article

References (82)

1. Aljanabi, S and Martinez, I. 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25: 4692-3.
2. Ardyna, M, Gosselin, M, Michel, C, Poulin, M and Tremblay, J. 2011. Environmental forcing of phytoplankton community structure and function in the Canadian High Arctic: contrasting oligotrophic and eutrophic regions. Marine Ecology Progress Series, 442: 37-57.
3. Arrigo, KR, Dijken, Gvan and Pabi, S. 2008. Impact of a shrinking Arctic ice cover on marine primary production. Geophysical Research Letters, 35: L19603
4. Bachy, C, López-García, P, Vereshchaka, A and 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. Frontiers in Extreme Microbiology, 2: 106 doi:10.3389/fmicb.2011.00106
5. Balzano, S, Marie, D, Gourvil, P and Vaulot, D. 2012. Composition of the summer photosynthetic pico and nanoplankton communities in the Beaufort Sea assessed by T-RFLP and sequences of the 18S rRNA gene from flow cytometry sorted samples. The ISME Journal, doi:10.1038/ismej.2011.213
6. 2S gradient in a supersulfidic anoxic fjord (Framvaren, Norway). Applied and Environmental Microbiology, 72: 3626-36.
7. Booth, B and Horner, R. 1997. Microalgae on the Arctic Ocean Section, 1994: species abundance and biomass. Deep-Sea Research Part II, 44: 1607-22.
8. Borin, S, Crotti, E, Mapelli, F, Tamagnini, I, Corselli, C and Daffonchio, D. 2008. DNA is preserved and maintains transforming potential after contact with brines of the deep anoxic hypersaline lakes of the Eastern Mediterranean Sea. Saline Systems, 4: 10. doi:10.1186/1746-1448-4-10
9. Carmack, EC and McLaughlin, F. 2011. Towards recognition of physical and geochemical change in Subarctic and Arctic Seas. Progress In Oceanography, 90: 90-104.
10. Comeau, AM, Li, WKW, Tremblay, J-É, Carmack, EC and Lovejoy, C. 2011. Arctic Ocean microbial community structure before and after the 2007 record sea ice minimum. PLoS One, 6(11): e27492
11. Dale, B, Edwards, M and Reid, P. 2006. "Climate change and harmful algal blooms". In Ecology of harmful algae, Edited by: Granéli, E and Turner, JT. 367-78. Berlin: Springer Verlag.
12. del Campo, J and Massana, R. 2011. Emerging diversity within Chrysophytes, Choanoflagellates and Bicosoecids based on molecular surveys. Protist, 162: 435-48.
13. Doney, SC, Ruckelshaus, M, Emmett Duffy, J, Barry, JP, Chan, F, English, CAGalindo, HM. 2012. Climate change impacts on marine ecosystems. Annual Review of Marine Science, 4(1): 11-37.
14. Edgar, RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32: 1792-7.
15. Edvardsen, B, Eikrem, W, Throndsen, J, Sáez, AG, Probert, I and Medlin, LK. 2011. Ribosomal DNA phylogenies and a morphological revision provide the basis for a revised taxonomy of the Prymnesiales (Haptophyta). European Journal of Phycology, 46: 202-28.
16. Falk-Petersen, S, Pavlov, V, Timofeev, S and Sargent, JR. 2007. "Climate variability and possible effects on arctic food chains: the role of Calanus". In Arctic alpine ecosystems and people in a changing environment, Edited by: Orbaek, JB, Kallenborn, R, Tombre, I, Hegseth, EN, Falk-Petersen, S and Hoel, AH. 147-66. Berlin: Springer Verlag.
17. Foissner, W. 2006. Biogeography and dispersal of microorganisms: a review emphasizing protists. Acta Protozoologica, 45(2): 111-36.
18. Forest, A, Tremblay, J-É, Gratton, Y, Martin, J, Gagnon, J, Darnis, GSampei, M. 2011. Biogenic carbon flows through the planktonic food web of the Amundsen Gulf (Arctic Ocean): A synthesis of field measurements and inverse modeling analyses. Progress In Oceanography, 91: 410-36.
19. Franklin, DC and Marchant, HJ. 1995. Parmales in sediments of Prydz Bay, East Antartica: a new biofacies and paleoenvironmental indicator of cold water deposition?. Micropaleontology, 41(1): 89-94.
20. Gjøsæter, J, Lekve, K, Stenseth, NC, Leinaas, HP, Christie, H, Dahl, E, Danielssen, DS, Edvardsen, B, Olsgard, F and Oug, E. 2000. A long-term perspective on the Chrysochromulina bloom on the Norwegian Skagerrak coast 1988: a catastrophe or an innocent incident?. Marine Ecology Progress Series, 207: 201-18.
21. Gobler, C, Berry, D, Dyhrman, S and Wilhelm, S. 2011. Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proceedings of the National Academy of Sciences of the United States of America, 108: 4352-7.
22. Gobler, CJ, Lonsdale, DJ and Boyer, GL. 2005. A review of the causes, effects, and potential management of harmful brown tide blooms caused by Aureococcus anophagefferens (Hargraves and Sieburth). Estuaries and Coasts, 28: 726-49.
23. Good, P, Caesar, J, Bernie, D, Lowe, JA, van der Linden, P, Gosling, SNWarren, R. 2011. A review of recent developments in climate change science. Part I. Understanding of future change in the large-scale climate system. Progress in Physical Geography, 35: 281-96.
24. Gouy, M, Guindon, S and Gascuel, O. 2010. SeaView Version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27: 221-4.
25. Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59: 307-21.
26. Harding, T, Jungblut, AD, Lovejoy, C and Vincent, WF. 2011. Microbes in high Arctic snow and implications for the cold biosphere. Applied and Environmental Microbiology, 77: 3234-43.
27. Hendriks, L, Goris, A, Neefs, J-M, Peer, YVan de, Hennebert, GL and 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. Systematic and Applied Microbiology, 12: 223-9.
28. Ichinomiya, M, Yoshikawa, S, Kamiya, M, Ohki, K, Takaichi, S and Kuwata, A. 2010. Isolation and characterization of Parmales (Heterokonta/Hetreokontaphyta/stramenopiles) from the Oyashio region, Western North Pacific. Journal of Phycology, 47(1): 144-151.
29. Jacobsen, A and Veldhuis, MJW. 2005. Growth characteristics of flagellated cells of Phaeocystis pouchetii revealed by diel changes in cellular DNA content. Harmful Algae, 4: 811-21.
30. Jancek, S, Gourbiere, S, Moreau, H and Piganeau, G. 2008. Clues about the genetic basis of adaptation emerge from comparing the proteomes of two Ostreococcus ecotypes (Chlorophyta, Prasinophyceae). Molecular Biology and Evolution, 25: 2293-300.
31. Kahru, M, Brotas, V, Manzano-Sarabia, M and Mitchell, BG. 2011. Are phytoplankton blooms occurring earlier in the Arctic?. Global Change Biology, 17: 1733-9.
32. Kwok, R, Cunningham, G, Wensnahan, M, Rigor, I, Zwally, H and Yi, D. 2009. Thinning and volume loss of the Arctic Ocean sea ice cover: 2003-2008. Journal of Geophysical Research, 114(C7): C07005
33. Lasternas, S and Agustí, S. 2010. Phytoplankton community structure during the record Arctic ice-melting of summer 2007. Polar Biology, 33: 1709-17.
34. Leu, E, Søreide, JE, Hessen, DO, Falk-Petersen, S and Berge, J. 2011. Consequences of changing sea-ice cover for primary and secondary producers in the European Arctic shelf seas: timing, quantity, and quality. Progress in Oceanography, 90(1-4): 18-32.
35. Li, WKW. 1994. Primary production of prochlorophytes, cyanobacteria, and eucaryoticultraphytoplankton: measurements from flow cytometric sorting. Limnology and Oceanography, 39: 169-75.
36. Li, WKW, McLaughlin, FA, Lovejoy, C and Carmack, EC. 2009. Smallest algae thrive as the Arctic Ocean freshens. Science, 326(5952): 539
37. Lovejoy, C, Legendre, L, Martineau, M, Bācle, J and Quillfeldt, Cvon. 2002. Distribution of phytoplankton and other protists in the North Water. Deep Sea Research Part II: Topical Studies in Oceanography, 49: 5027-47.
38. Lovejoy, C, Massana, R and Pedros-Alio, C. 2006. Diversity and distribution of marine microbial eukaryotes in the Arctic Ocean and adjacent seas. Applied and Environmental Microbiology, 72: 3085-95.
39. Lovejoy, C and Potvin, M. 2011. Microbial eukaryotic distribution in a dynamic Beaufort Sea and the Arctic Ocean. Journal of Plankton Research, 33: 431-44.
40. Lovejoy, C, Vincent, WF, Bonilla, S, Roy, S, Martineau, M-J, Terrado, R, Potvin, M, Massana, R and Pedros-Alio, C. 2007. Distribution, phylogeny, and growth of cold-adapted picoprasinophytes in arctic seas. Journal of Phycology, 43(1): 78-89.
41. Luo, W, Li, H, Cai, M and He, J. 2009. Diversity of microbial eukaryotes in Kongsfjorden, Svalbard. Hydrobiologia, 636(1): 233-48.
42. Majaneva, M, Rintala, JM, Piisila, M, Fewer, DP and Blomster, J. 2012. Comparison of wintertime eukaryotic community from sea ice and open water in the Baltic Sea, based on sequencing of the 18S rRNA gene. Polar Biology, 35: 875-89.
43. Manton, I and Leadbeater, BSC. 1974. Fine-structural observations on six species of Chrysochromulina from wild Danish marine nanoplankton, including a description of C. campanulifera sp. nov. and a preliminary summary of the nanoplankton as a whole. Det Kongelige Danske Videnskabernes Selskab Biologiske Skrifter, 20: 1-26.
44. Marin, B and 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: 304-36.
45. McFadden, G, Moestrup, Ø and Wetherbee, R. 1982. Pyramimonas gelidicola sp. nov. (Prasinophyceae), a new species isolated from Antarctic sea ice. Phycologia, 21(2): 103-11.
46. McLaughlin, FA and Carmack, EC. 2010. Deepening of the nutricline and chlorophyll maximum in the Canada Basin interior, 2003-2009. Geophysical Research Letters, 37: L24602 doi:10.1029/2010GL045459
47. Medlin, L, Elwood, HJ, Stickel, S and Sogin, ML. 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene, 71: 491-9.
48. Mikkelsen, D, Rysgaard, S and Glud, R. 2008. Microalgal composition and primary production in Arctic sea ice: a seasonal study from Kobbefjord (Kangerluarsunnguaq), West Greenland. Marine Ecology Progress Series, 368: 65-74.
49. Nickrent, DL and Sargent, ML. 1991. An overview of the secondary structure of the V4 region of eukaryotic small-subunit ribosomal RNA. Nucleic Acids Research, 19: 227-35.
50. Niemi, A, Michel, C, Hille, K and Poulin, M. 2011. Protist assemblages in winter sea ice: setting the stage for the spring ice algal bloom. Polar Biology, 34: 1803-17.
51. Not, F, Massana, R, Latasa, M, Marie, D, Colson, C, Eikrem, W, Pedros-Alio, C, Vaulot, D and Simon, N. 2005. Late summer community composition and abundance of photosynthetic picoeukaryotes in Norwegian and Barents Seas. Limnology and Oceanography, 50: 1677-86.
52. Orsi, W, Song, YC, Hallam, S and Edgcomb, V. 2012. Effect of oxygen minimum zone formation on communities of marine protists. The ISME Journal, doi:10.1038/ismej.2012.7
53. Pawlowski, J, Christen, R, Lecroq, B, Bachar, D, Shahbazkia, HR, Amaral-Zettler, L and Guillou, L. 2011. Eukaryotic richness in the abyss: insights from pyrotag sequencing. PLoS One, 6(4): e18169
54. Pedrós-Alió, C. 2012. The rare bacterial biosphere. Annual Review of Marine Science, 4(1): 449-66.
55. Peterson, B, McClelland, J, Curry, R, Holmes, R, Walsh, J and Aagaard, K. 2006. Trajectory shifts in the Arctic and Subarctic freshwater cycle. Science, 313(5790): 1061-1066.
56. Piepenburg, D. 2005. Recent research on Arctic benthos: common notions need to be revised. Polar Biology, 28: 733-55.
57. Piganeau, G, Grimsley, N and Moreau, H. 2011. Genome diversity in the smallest marine photosynthetic eukaryotes. Research in Microbiology, 162: 570-7.
58. Potvin, M and Lovejoy, C. 2009. PCR-based diversity estimates of artificial and environmental 18S rRNA gene libraries. Journal of Eukaryotic Microbiology, 56(2): 174-81.
59. Poulin, M, Daugbjerg, N, Gradinger, R, Ilyash, L, Ratkova, T and von Quillfeldt, C. 2011. The pan-Arctic biodiversity of marine pelagic and sea-ice unicellular eukaryotes: a first-attempt assessment. Marine Biodiversity, 41: 13-26.
60. Ralph, PJ, Ryan, KG, Martin, A and Fenton, G. 2007. Melting out of sea ice causes greater photosynthetic stress in algae than freezing in. Journal of Phycology, 43: 948-56.
61. Riaux-Gobin, C, Poulin, M, Dieckmann, G, Labrune, C and Vétion, G. 2011. Spring phytoplankton onset after the ice break-up and sea-ice signature (Adélie Land, East Antarctica). Polar Research, 30: 5910. doi:10.3402/polar.v30i0.5910
62. Różańska, M, Poulin, M and Gosselin, M. 2008. Protist entrapment in newly formed sea ice in the Coastal Arctic Ocean. Journal of Marine Systems, 74: 887-901.
63. Schloss, I, Nozais, C, Mas, S, van Hardenberg, B, Carmack, E, Tremblay, J-É, Brugel, S and Demers, S. 2008. Picophytoplankton and nanophytoplankton abundance and distribution in the southeastern Beaufort Sea (Mackenzie Shelf and Amundsen Gulf) during Fall 2002. Journal of Marine Systems, 74: 978-93.
64. Schloss, P, Westcott, S and Ryabin, T. 2009. Introducing MOTHUR: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75: 7537-41.
65. Screen, JA and Simmonds, I. 2010. The central role of diminishing sea ice in recent Arctic temperature amplification. Nature, 464: 1334-7.
66. Sherr, EB, Sherr, BF, Wheeler, P and 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 Research Part I, 50: 557-71.
67. Slapeta, J, Lopez-Garcia, P and Moreira, D. 2006. Global dispersal and ancient cryptic species in the smallest marine eukaryotes. Molecular Biology And Evolution, 23(1): 23-9.
68. Søreide, JE, Leu, E, Berge, J, Graeve, M and Falk-Petersen, S. 2010. Timing of blooms, algal food quality and Calanus glacialis reproduction and growth in a changing Arctic. Global Change Biology, 16: 3154-63.
69. Sørensen, N, Daugbjerg, N and Gabrielsen, TM. 2012. Molecular diversity and temporal variation of picoeukaryotes in two Arctic fjords, Svalbard. Polar Biology, 35: 519-33.
70. Stroeve, JC, Serreze, MC, Holland, MM, Kay, JE, Malanik, J and Barrett, AP. 2011. The Arctic's rapidly shrinking sea ice cover: a research synthesis. Climatic Change, 110: 1005-27.
71. Syvertsen, EE. 1991. Ice algae in the Barents Sea: types of assemblages, origin, fate and role in the ice-edge phytoplankton bloom. Polar Research, 10: 277-88.
72. Tedesco, L, Vichi, M and Thomas, DN. 2012. Process studies on the ecological coupling between sea ice algae and phytoplankton. Ecological Modelling, 226: 120-38.
73. Terrado, R, Medrinal, E, Dasilva, C, Thaler, M, Vincent, WF and Lovejoy, C. 2011. Protist community composition during spring in an Arctic flaw lead polynya. Polar Biology, 34: 1901-14.
74. Terrado, R, Vincent, WF and Lovejoy, C. 2009. Mesopelagic protists: diversity and succession in a coastal Arctic ecosystem. Aquatic Microbial Ecology, 56(1): 25-39.
75. Tremblay, G, Belzile, C, Gosselin, M, Poulin, M, Roy, S and Tremblay, J-É. 2009. Late summer phytoplankton distribution along a 3500 km transect in Canadian Arctic waters: strong numerical dominance by picoeukaryotes. Aquatic Microbial Ecology, 54(1): 55-70.
76. Uitz, J, Claustre, H, Gentili, B and Stramski, D. 2010. Phytoplankton class-specific primary production in the world's oceans: Seasonal and interannual variability from satellite observations. Global Biogeochemical Cycles, 24(3): GB3016
77. Urban, MC, Tewksbury, JJ and Sheldon, KS. 2012. On a collision course: competition and dispersal differences create no-analogue communities and cause extinctions during climate change. Proceedings of the Royal Society B: Biological Sciences, doi:10.1098/rspb.2011.2367
78. Vaulot, D, Eikrem, W, Viprey, M and Moreau, H. 2008. The diversity of small eukaryotic phytoplankton (<3 μm). FEMS Microbiology Reviews, 32: 795-820.
79. Veldhuis, JW and Wassmann, P. 2005. Bloom dynamics and biological control of a high biomass HAB species in European coastal waters: a Phaeocystis case study. Harmful Algae, 4: 805-9.
80. Vincent, WF. 2010. Microbial ecosystem responses to rapid climate change in the Arctic. The ISME Journal, 4: 1089-91.
81. Walsh, JJ, Dieterle, DA, Chen, FR, Lenes, JM, Maslowski, W, Cassano, JJWhitledge, TE. 2011. Trophic cascades and future harmful algal blooms within ice-free Arctic Seas north of Bering Strait: a simulation analysis. Progress In Oceanography, 91: 312-43.
82. Wassmann, P, Duarte, CM, Agustí, S and Sejr, MK. 2010. Footprints of climate change in the Arctic marine ecosystem. Global Change Biology, 17: 1235-49.