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Microbial Ecology

, Volume 53, Issue 4, pp 549–561 | Cite as

Phenotypically Different Microalgal Morphospecies with Identical Ribosomal DNA: A Case of Rapid Adaptive Evolution?

  • Ramiro Logares
  • Karin Rengefors
  • Anke Kremp
  • Kamran Shalchian-Tabrizi
  • Andrés Boltovskoy
  • Torstein Tengs
  • Aaron Shurtleff
  • Dag Klaveness
Article

Abstract

The agents driving the divergence and speciation of free-living microbial populations are still largely unknown. We investigated the dinoflagellate morphospecies Scrippsiella hangoei and Peridinium aciculiferum, which abound in the Baltic Sea and in northern temperate lakes, respectively. Electron microscopy analyses showed significant interspecific differences in the external cellular morphology, but a similar plate pattern in the characteristic dinoflagellate armor. Experimentally, S. hangoei grew in a wide range of salinities (0–30), whereas P. aciculiferum only grew in low salinities (0–3). Despite these phenotypic differences and the habitat segregation, molecular analyses showed identical ribosomal DNA sequences (ITS1, ITS2, 5.8S, SSU, and partial LSU) for both morphospecies. Yet, a strong interspecific genetic isolation was indicated by amplified fragment length polymorphism (F ST = 0.76) and cytochrome b (cob) sequence divergence (∼1.90%). Phylogenetic reconstructions based on ribosomal (SSU, LSU) and mitochondrial (cob) DNA indicated a recent marine ancestor for P. aciculiferum. In conclusion, we suggest that the lacustrine P. aciculiferum and the marine-brackish S. hangoei diverged very recently, after a marine–freshwater transition that exposed the ancestral populations to different selective pressures. This hypothetical scenario agrees with mounting data indicating a significant role of natural selection in the divergence of free-living microbes, despite their virtually unrestricted dispersal capabilities. Finally, our results indicate that identical ITS rDNA sequences do not necessarily imply the same microbial species, as commonly assumed.

Keywords

Internal Transcribe Space Amplify Fragment Length Polymorphism Dinoflagellate Prorocentrum Minimum Plate Pattern 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The Swedish Research Council and the SEED project contract, GOCE-CT-2005-003875 (European Commission Directorate General Research), financed this study. We thank S. Bensch for his assistance with AFLP analyses and J. Pérez-Tris for comments on early versions of the manuscript. Dr. C. Luxoro is thanked for methodological help during the initial phase of this work and T. Rolfsen (UiO) for assistance with SEM. Preliminary parts of this work were carried out in D. Anderson's laboratory at Woods Hole. Special thanks to the three anonymous reviewers who have helped to improve this manuscript. Phylogenies were computed in the University of Oslo Bioportal, (http://www.bioportal.uio.no/).

References

  1. 1.
    Adachi, M, Sako, Y, Ishida, Y (1994) Restriction-fragment-length-polymorphism of ribosomal DNA internal transcribed spacer and 5.8s-regions in Japanese Alexandrium species (Dinophyceae). J Phycol 30: 857–863CrossRefGoogle Scholar
  2. 2.
    Anderson, JR, Bentley, S, Irwin, JAG, Mackie, JM, Neate, S, Pattemore, JA (2004) Characterization of Rhizoctonia solani isolates causing root canker of lucerne in Australia. Australas Plant Pathol 33: 241–247CrossRefGoogle Scholar
  3. 3.
    Avise, JC (2004) Molecular Markers, Natural History, and Evolution, 2nd ed. Sinauer Associates, MAGoogle Scholar
  4. 4.
    Baas-Becking, LGM (1934) Geobiologie of Inleiding Tot De Milieukunde, Serie 18/19. Van Stockum's Gravenhange, The Hague, The NetherlandsGoogle Scholar
  5. 5.
    Balech, E (1963) Dos dinoflagelados de una laguna salobre de la Argentina. Not Mus La Plata 20: 111–123Google Scholar
  6. 6.
    Bensch, S, Perez-Tris, J, Waldenstrom, J, Hellgren, O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58: 1617–1621PubMedGoogle Scholar
  7. 7.
    Berry, JP, Reece, KS, Rein, KS, Baden, DG, Haas, LW, Ribeiro, WL, Shields, JD, Snyder, RV, Vogelbein, WK, Gawley, RE (2002) Are Pfiesteria species toxicogenic? Evidence against production of ichthyotoxins by Pfiesteria shumwayae. Proc Natl Acad Sci USA 99: 10970–10975PubMedCrossRefGoogle Scholar
  8. 8.
    Bjorck, S (1995) A review of the history of the Baltic Sea, 13.0–8.0 Ka Bp. Quatern Int 27: 19–40Google Scholar
  9. 9.
    Bourelly, P (1968) Notes sur les Péridiniens d'eau douce. Protistologica 4: 5–14Google Scholar
  10. 10.
    Casamatta, DA, Vis, ML, Sheath, RG (2003) Cryptic species in cyanobacterial systematics: a case study of Phormidium retzii (Oscillatoriales) using RAPD molecular markers and 16S rDNA sequence data. Aquat Bot 77: 295–309CrossRefGoogle Scholar
  11. 11.
    Cavalier-Smith, T (2004) Only six kingdoms of life. Proc R Soc Lond B Biol 271 :1251–1262CrossRefGoogle Scholar
  12. 12.
    Connell, LB (2000) Nuclear ITS region of the alga Heterosigma akashiwo (Chromophyta: Raphidophyceae) is identical in isolates from Atlantic and Pacific basins. Mar Biol 136: 953–960CrossRefGoogle Scholar
  13. 13.
    Coyne, JA, Orr, HA (2004) Speciation. Sinauer Associates, MAGoogle Scholar
  14. 14.
    Darling, KF, Wade, CM, Stewart, IA, Kroon, D, Dingle, R, Brown, AJL (2000) Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers. Nature 405: 43–47PubMedCrossRefGoogle Scholar
  15. 15.
    Dawson, MN, Hamner, WM (2005) Rapid evolutionary radiation of marine zooplankton in peripheral environments. Proc Natl Acad Sci USA 102: 9235–9240PubMedCrossRefGoogle Scholar
  16. 16.
    Doebeli, M, Dieckmann, U, Metz, JAJ, Tautz, D (2005) What we have also learned: adaptive speciation is theoretically plausible. Evolution 59: 691–695PubMedGoogle Scholar
  17. 17.
    Edvardsen, B, Shalchian-Tabrizi, K, Jakobsen, KS, Medlin, LK, Dahl, E, Brubak, S, Paasche, E (2003) Genetic variability and molecular phylogeny of Dinophysis species (Dinophyceae) from Norwegian waters inferred from single cell analyses of rDNA. J Phycol 39: 395–408Google Scholar
  18. 18.
    Ekman, P, Fries, M (1970) Studies of sediments from Lake Erken, Eastern Central Sweden. GFF 92: 214–224Google Scholar
  19. 19.
    Fenchel, T (1993) There are more small than large species. Oikos 68: 375–378CrossRefGoogle Scholar
  20. 20.
    Finlay, BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296: 1061–1063PubMedCrossRefGoogle Scholar
  21. 21.
    Finlay, BJ (2004) Protist taxonomy: an ecological perspective. Philos Trans R Soc, B 359: 599–610CrossRefGoogle Scholar
  22. 22.
    Finlay, BJ, Clarke, KJ (1999) Ubiquitous dispersal of microbial species. Nature 400: 828CrossRefGoogle Scholar
  23. 23.
    Fukuyo, Y, Hideaki, T, Chihara, M, Matsuoka, K (1990) Red Tide Organisms in Japan—An Illustrated Taxonomic Guide. U Rokakuho Publ, TokyoGoogle Scholar
  24. 24.
    Gottschling, M, Keupp, H, Plotner, J, Knop, R, Willems, H, Kirsch, M (2005) Phylogeny of calcareous dinoflagellates as inferred from ITS and ribosomal sequence data. Mol Phylogenet Evol 36: 444–455.PubMedCrossRefGoogle Scholar
  25. 25.
    Guillard, RR, Lorenzen, CJ (1972) Yellow-green algae with Chlorophyllide C. J Phycol 8: 10–14CrossRefGoogle Scholar
  26. 26.
    Guillard, RR, Ryther, JH (1962) Studies of marine planktonic diatoms .1. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8: 229–239PubMedCrossRefGoogle Scholar
  27. 27.
    Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98Google Scholar
  28. 28.
    Hendry, AP, Wenburg, JK, Bentzen, P, Volk, EC, Quinn, TP (2000) Rapid evolution of reproductive isolation in the wild: evidence from introduced salmon. Science 290: 516–518PubMedCrossRefGoogle Scholar
  29. 29.
    Hewitt, G (2000) The genetic legacy of the Quaternary ice ages. Nature 405: 907–913PubMedCrossRefGoogle Scholar
  30. 30.
    Hewitt, GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58: 247–276CrossRefGoogle Scholar
  31. 31.
    Horiguchi, T, Pienaar, RN (1988) Ultrastructure of a new sand-dwelling dinoflagellate, Scrippsiella arenicola sp. nov. J Phycol 24: 426–438Google Scholar
  32. 32.
    Huelsenbeck, JP, Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755PubMedCrossRefGoogle Scholar
  33. 33.
    Kauserud, H, Stensrud, O, Decock, C, Shalchian-Tabrizi, K, Schumacher, T (2006) Multiple gene genealogies and AFLPs suggest cryptic speciation and long-distance dispersal in the basidiomycete Serpula himantioides (Boletales). Mol Ecol 15: 421–431PubMedCrossRefGoogle Scholar
  34. 34.
    Kim, E, Wilcox, L, Graham, L, Graham, J (2004) Genetically distinct populations of the dinoflagellate Peridinium limbatum in neighboring Northern Wisconsin lakes. Microbial Ecol 48: 521–527CrossRefGoogle Scholar
  35. 35.
    Kisselev, IA (1950) Pantzyrnye Zhgutikonostsy (Dinoflagellata) Morey i Presnovodnykh vod SSSR. Opredelitel po faune SSSR 33, Akad Nauka SSSR, MoskvaGoogle Scholar
  36. 36.
    Kremp, A, Elbrachter, M, Schweikert, M, Wolny, JL, Gottschling, M (2005) Woloszynskia halophila (Biecheler) comb. nov.: a bloom-forming cold-water dinoflagellate co-occurring with Scrippsiella hangoei (Dinophyceae) in the Baltic Sea. J Phycol 41: 629–642CrossRefGoogle Scholar
  37. 37.
    Larsen, J, Kuosa, H, Ikävalko, J, Kivi, K, Hällfors, S (1995) A redescription of Scrippsiella-hangoei (Schiller) comb. nov.—a red tide dinoflagellate from the Northern Baltic. Phycologia 34: 135–144Google Scholar
  38. 38.
    Leblond, JD, Chapman, PJ (2002) A survey of the sterol composition of the marine dinoflagellates Karenia brevis, Karenia mikimotoi, and Karlodinium micrum distribution of sterols within other members of the class Dinophyceae. J Phycol 38: 670–682CrossRefGoogle Scholar
  39. 39.
    Lee, CE, Bell, MA (1999) Causes and consequences of recent freshwater invasions by saltwater animals. Trends Ecol Evol 14: 284–288CrossRefPubMedGoogle Scholar
  40. 40.
    Lefèvre, M (1932) Monographie des espèces d'eau douce du genre Peridinium. Ehrb Arch Bot 2: 1–208Google Scholar
  41. 41.
    Lindemann, E (1919) Untersuchungen über süsswasserperidineen und ihre variationsformen. Arch Protistenk 39: 209–262Google Scholar
  42. 42.
    Lopez-Garcia, P, Rodriguez-Valera, F, Pedros-Alio, C, Moreira, D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603–607PubMedCrossRefGoogle Scholar
  43. 43.
    Loret, P, Tengs, T, Villareal, TA, Singler, H, Richardson, B, McGuire, P, Morton, S, Busman, M, Campbell, L (2002) No difference found in ribosomal DNA sequences from physiologically diverse clones of Karenia brevis (Dinophyceae) from the Gulf of Mexico. J Plankton Res 24: 735–739CrossRefGoogle Scholar
  44. 44.
    Lynch, M, Milligan, BG (1994) Analysis of population genetic-structure with RAPD markers. Mol Ecol 3: 91–99PubMedGoogle Scholar
  45. 45.
    Massana, R, DeLong, EF, Pedros-Alio, C (2000) A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Appl Environ Microbiol 66: 1777–1787PubMedCrossRefGoogle Scholar
  46. 46.
    McDonald, JH, Kreitman, M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652–654PubMedCrossRefGoogle Scholar
  47. 47.
    McKinnon, JS, Rundle, HD (2002) Speciation in nature: the three-spine stickleback model systems. Trends Ecol Evol 17: 480–488CrossRefGoogle Scholar
  48. 48.
    Mendelson, TC, Shaw, KL (2005) Rapid speciation in an arthropod. Nature 433: 375–376PubMedCrossRefGoogle Scholar
  49. 49.
    Miller, MP (1997) Tools for Population Genetic Analysis (TFPGA) 1.3: a Windows program for the analysis of allozyme and molecular population genetic data. Distributed by the authorGoogle Scholar
  50. 50.
    Miscampbell, AE, Lankester, MW, Adamson, ML (2004) Molecular and morphological variation within swim bladder nematodes, Cystidicola spp. Can J Fish Aquat Sci 61: 1143–1152CrossRefGoogle Scholar
  51. 51.
    Montresor, M (1995) Scrippsiella ramonii sp nov (Peridiniales, Dinophyceae), a marine dinoflagellate producing a calcareous resting cyst. Phycologia 34: 87–91Google Scholar
  52. 52.
    Montresor, M, Lovejoy, C, Orsini, L, Procaccini, G, Roy, S (2003) Bipolar distribution of the cyst-forming dinoflagellate Polarella glacialis. Polar Biol 26: 186–194Google Scholar
  53. 53.
    Montresor, M, Sgrosso, S, Procaccini, G, Kooistra, WHCF (2003) Intraspecific diversity in Scrippsiella trochoidea (Dinophyceae): evidence for cryptic species. Phycologia 42: 56–70CrossRefGoogle Scholar
  54. 54.
    Montresor, M, Zingone, A (1988) Scrippsiella precaria sp nov (Dinophyceae), a marine dinoflagellate from the Gulf of Naples. Phycologia 27: 387–394Google Scholar
  55. 55.
    Moon-van der Staay, SY, De Wachter, R, Vaulot, D (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409: 607–610PubMedCrossRefGoogle Scholar
  56. 56.
    Muir, G, Fleming, CC, Schlotterer, C (2001) Three divergent rDNA clusters predate the species divergence in Quercus petraea (Matt.) Liebl. and Quercus robur L. Mol Biol Evol 18: 112–119PubMedGoogle Scholar
  57. 57.
    Nei, M (1972) Genetic distance between populations. Am Nat 106: 283–292CrossRefGoogle Scholar
  58. 58.
    Niemi, Å (1975) Ecology of phytoplankton in the Tvärminne area, SW coast of Finland: II. Primary production and environmental conditions in the archipelago and the sea zone. Acta Bot Fenn 105: 1–73Google Scholar
  59. 59.
    Orr, MR, Smith, TB (1998) Ecology and speciation. Trends Ecol Evol 13: 502–506CrossRefGoogle Scholar
  60. 60.
    Ostenfeld, CH, Wesenberg-Lund, C (1906) A regular fortnightly exploration of the phytoplankton of the two Icelandic lakes, Thingvallavatn and Myvatn. Proc R Soc Edinburgh 25: 1092–1176Google Scholar
  61. 61.
    Pace, NR (1997) A molecular view of microbial diversity and the biosphere. Science 276: 734–740PubMedCrossRefGoogle Scholar
  62. 62.
    Page, RDM (1996) Treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12: 357–358PubMedGoogle Scholar
  63. 63.
    Papke, RT, Ramsing, NB, Bateson, MM, Ward, DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5 :650–659PubMedCrossRefGoogle Scholar
  64. 64.
    Papke, RT, Ward, DM (2004) The importance of physical isolation to microbial diversification. FEMS Microbiol Ecol 48: 293–303CrossRefPubMedGoogle Scholar
  65. 65.
    Pearce, I, Hallegraeff, GM (2004) Genetic affinities, ecophysiology and toxicity of Prorocentrum playfairii and P. foveolata (Dinophyceae) from Tasmanian freshwaters. Phycologia 43: 271–281CrossRefGoogle Scholar
  66. 66.
    Pfiester, LA, Anderson, DM (1987) Dinoflagellate reproduction. In: Taylor, FJR (Eds.) The Biology of Dinoflagellates. Botanical Monographs, vol. 21, Blackwell, Oxford, pp 611–648Google Scholar
  67. 67.
    Popovsky, J, Pfiester, LA (1990) Dinophyceae. In: Ettl, H, Gerloff, J, Heynig, H, Mollenhauer, D (Eds.) Süßwasserflora von Mitteleuropa, vol. 6, Gustav Fischer Verlag, StuttgartGoogle Scholar
  68. 68.
    Posada, D, Crandall, KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818PubMedCrossRefGoogle Scholar
  69. 69.
    Rainey, PB, Buckling, A, Kassen, R, Travisano, M (2000) The emergence and maintenance of diversity: insights from experimental bacterial populations. Trends Ecol Evol 15: 243–247PubMedCrossRefGoogle Scholar
  70. 70.
    Rainey, PB, Travisano, M (1998) Adaptive radiation in a heterogeneous environment. Nature 394: 69–72PubMedCrossRefGoogle Scholar
  71. 71.
    Rengefors, K (1998) Seasonal succession of dinoflagellates coupled to the benthic cyst dynamics in Lake Erken, Sweden. Arch Hydrobiol 51: 123–141Google Scholar
  72. 72.
    Riseberg, LH, Wendel, JF (1993) Introgression and its consequences. In: Harrison, RG (Eds.) Hybrid Zones and the Evolutionary Process. Oxford University Press, New York, pp 70–109Google Scholar
  73. 73.
    Rozas, J, Sanchez-DelBarrio, JC, Messeguer, X, Rozas, R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496–2497PubMedCrossRefGoogle Scholar
  74. 74.
    Rundle, HD, Nagel, L, Boughman, JW, Schluter, D (2000) Natural selection and parallel speciation in sympatric sticklebacks. Science 287: 306–308PubMedCrossRefGoogle Scholar
  75. 75.
    Rynearson, TA, Armbrust, EV (2000) DNA fingerprinting reveals extensive genetic diversity in a field population of the centric diatom Ditylum brightwellii. Limnol Oceanogr 45: 1329–1340CrossRefGoogle Scholar
  76. 76.
    Rynearson, TA, Armbrust, EV (2004) Genetic differentiation among populations of the planktonic marine diatom Ditylum brightwellii (Bacillariophyceae). J Phycol 40: 34–43Google Scholar
  77. 77.
    Saez, AG, Probert, I, Geisen, M, Quinn, P, Young, JR, Medlin, LK (2003) Pseudo-cryptic speciation in coccolithophores. Proc Natl Acad Sci USA 100: 7163–7168PubMedCrossRefGoogle Scholar
  78. 78.
    Saldarriaga, JF, Taylor, FJR, Keeling, PJ, Cavalier-Smith, T (2001) Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J Mol Evol 53: 204–213PubMedCrossRefGoogle Scholar
  79. 79.
    Schmidt, LE, Hansen, PJ (2001) Allelopathy in the prymnesiophyte Chrysochromulina polylepis: effect of cell concentration, growth phase and pH. Mar Ecol Prog Ser 216: 67–81Google Scholar
  80. 80.
    Scholin, CA, Herzog, M, Sogin, M, Anderson, DM (1994) Identification of group-specific and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae): II. Sequence analysis of a fragment of the LSU rRNA gene. J Phycol 30: 999–1011CrossRefGoogle Scholar
  81. 81.
    Smayda, TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42: 1137–1153CrossRefGoogle Scholar
  82. 82.
    Steidinger, KA, Balech, E (1977) Scrippsiella subsalsa (Ostenfeld) comb nov (Dinophyceae) with a discussion on Scrippsiella. Phycologia 16: 69–73Google Scholar
  83. 83.
    Taylor, FJR (1987) The biology of dinoflagellates. Botanical Monographs, vol. 21. Blackwell, OxfordGoogle Scholar
  84. 84.
    Tengs, T, Bowers, HA, Glasgow, HB, Burkholder, JM, Oldach, DW (2003) Identical ribosomal DNA sequence data from Pfiesteria piscicida (Dinophyceae) isolates with different toxicity phenotypes. Environ Res 93: 88–91PubMedCrossRefGoogle Scholar
  85. 85.
    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
  86. 86.
    Tyler, PA (1996) Endemism in freshwater algae. Hydrobiologia 336: 127–135Google Scholar
  87. 87.
    Uwe, J, Fensome, RA, Medlin, LK (2003) The application of a molecular clock based on molecular sequences and the fossil record to explain biogeographic distributions within the Alexandrium tamarense “Species Complex” (Dinophyceae). Mol Biol Evol 20: 1015–1027CrossRefGoogle Scholar
  88. 88.
    Vekemans, X (2002) AFLP-SURV v.1.0. Distributed by the author. Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles, BelgiumGoogle Scholar
  89. 89.
    von der Heyden, S, Chao, EE, Cavalier-Smith, T (2004) Genetic diversity of goniomonads: an ancient divergence between marine and freshwater species. Eur J Phycol 39: 343–350CrossRefGoogle Scholar
  90. 90.
    von Stosch, HA (1973) Observations on vegetative reproduction and sexual life cycles of two freshwater dinoflagellates Gymnodinium pseudopalustre Schiller and Woloszynkskia apiculata sp. nov. Br Phycol J 8: 105–134Google Scholar
  91. 91.
    Vos, P, Hogers, R, Bleeker, M, Reijans, M, Vandelee, T, Hornes, M, Frijters, A, Pot, J, Peleman, J, Kuiper, M, Zabeau, M (1995) AFLP—a new technique for DNA-fingerprinting. Nucleic Acids Res 23: 4407–4414PubMedCrossRefGoogle Scholar
  92. 92.
    Wetzel, RG (2001) Limnology. Lake and River Ecosystems, 3rd ed. Academic Press, CaliforniaGoogle Scholar
  93. 93.
    Weyhenmeyer, G (1999) Lake Erken: Meteorological, Physical, Chemical and Biological Data and List of Publications from 1933 to 1998. Norr Malma field station report, Evolutionary Biology Centre, Uppsala University http://www.ebc.uu.se/norr.malma/publikationer/Erken%20Data%20Report.pdf)
  94. 94.
    Whitaker, RJ, Grogan, DW, Taylor, JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301: 976–978PubMedCrossRefGoogle Scholar
  95. 95.
    Woloszynska, J (1928) Dinoflagellatae polskiego Baltyku i blot nad Piasnica. Arch Hydrobiol Ryb 3: 153–278Google Scholar
  96. 96.
    Zhang, H, Bhattacharya, D, Lin, S (2005) Phylogeny of dinoflagellates based on mitochondrial cytochrome b and nuclear small subunit rDNA sequence comparisons. J Phycol 41: 411–420CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2007

Authors and Affiliations

  • Ramiro Logares
    • 1
  • Karin Rengefors
    • 1
  • Anke Kremp
    • 2
  • Kamran Shalchian-Tabrizi
    • 3
  • Andrés Boltovskoy
    • 4
  • Torstein Tengs
    • 5
  • Aaron Shurtleff
    • 6
  • Dag Klaveness
    • 7
  1. 1.Limnology Division, Ecology DepartmentLund UniversityLundSweden
  2. 2.Tvärminne Zoological StationUniversity of HelsinkiHankoFinland
  3. 3.Department of ZoologyUniversity of OxfordOxfordUK
  4. 4.Departamento Científico FicologíaPaseo del Bosque s/n°, Museo de La PlataLa PlataArgentina
  5. 5.National Veterinary Institute, Section of Food and Feed MicrobiologyOsloNorway
  6. 6.FWC, Fish & Wildlife Research InstituteSt. PetersburgUSA
  7. 7.Department of Biology, Section LimnologyUniversity of OsloBlindern, OsloNorway

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