Fottea, 2014 (vol. 14), issue 2

Fottea 14(2): 179-190, 2014 | 10.5507/fot.2014.014

Seasonal variation of planktonic chrysophytes with special focus on Dinobryon.

Christina Bock*,1, Ralph Medinger1,2, Steffen Jost1, Roland Psenner2, Jens Boenigk1
1 Department of Biodiversity, University Duisburg-Essen, Universitätsstrasse 5, D-45117 Essen
2 Institute of Ecology, University of Innsbruck, Technikerstrasse 15, A-6020 Innsbruck

The diversity of chrysophytes is often underestimated in morphological surveys because of the limited amount of detectable characters under the light microscope. Addressing biodiversity issues solely based on morphological characters is further problematic since molecular analyses revealed a huge genetic diversity within morphotypes, even showing polyphyly in some morphological defined species. In order to address the seasonal variations of chrysophytes, 10 samples were collected in 2007 from the oligotrophic lake Fuschlsee (Salzkammergut, Austria). By using Dinobryon as a case study, we compared different gene phylogenies of single cells of the 18S, ITS (including ITS1, 5.8S, partial ITS2) and the mitochondrial marker COI. No clear molecular phylogenetic separation between morphological identified cells of D. divergens and D. bavaricum could be accomplished based on the 18S rDNA sequences. ITS and COI sequence data revealed a higher genetic diversity then the 18S, with several independent lineages consisting of D. divergens cells. We further encountered divergent phylogenies by comparing 18S/ITS sequence data with COI data within D. pediforme, D. sociale and D. bavaricum lineages. By combining the results of the single cell approach with seasonal data based on 454 pyrosequencing, we addressed the question in how far one morphological species may dominate in the water column over the course of a single year. The results of the 454 pyrosequencing revealed that the D.divergens/D. bavaricum lineage shows the highest abundance from all Chrysophyceae/Synurophyceae and strong seasonal variations with peaks in May and October.

Keywords: chrysophytes, Dinobryon, diversity, phylogeny, 454 pyrosequencing, single-cell PCR

Received: March 18, 2014; Accepted: June 5, 2014; Published: September 1, 2014

Download citation

References

  1. Andersson, J.O. (2005): Lateral gene transfer in eukaryotes. - Cell. Mol. Life Sci. 62: 1182-1197. Go to original source...
  2. Andersson, J.O.; Sjogren, A.M.; Davis, L. a. M.; Embley, T.M. & Roger, A.J. (2003): Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. - Curr. Biol. 13: 94- 104. Go to original source...
  3. Armstrong, G.D. (1985): Colonies as defense in the freshwater phytoplankton genus Dinobryon. University of British Columbia, Vancouver.
  4. Auinger, B.M.; Pfandl, K. & Boenigk, J. (2008): Improved methodology for identification of protists and microalgae from plankton samples preserved in Lugol's iodine solution: Combining microscopic analysis with single-cell PCR. - Appl. Environ. Microbiol. 74: 2505-2510. Go to original source...
  5. Beaver, J.R. & Crisman, T.L. (1989): Analysis of the community structure of planktonic ciliated Protozoa relative to trophic State in Florida Lakes. - Hydrobiologia 174: 177-184. Go to original source...
  6. Bird, D.F. & Kalff, J. (1986): Bacterial grazing by planktonic lake algae. - Science 231: 493-495. Go to original source...
  7. Bock, C.; Krienitz, L. & Pröschold, T. (2011): Taxonomic reassessment of the genus Chlorella (Trebouxiophyceae) using molecular signatures (barcodes), including description of seven new species. - Fottea 11: 293-312. Go to original source...
  8. Bock, C.; Pröschold, T. & Krienitz, L. (2011): Updating the genus Dictyosphaerium and description of Mucidosphaerium gen. nov. (Trebouxiophyceae) based on morphological and molecular data.- J. Phycol. 47: 638-652. Go to original source...
  9. Boenigk, J. & Arndt, H. (2002): Bacterivory by heterotrophic flagellates: community structure and feeding strategies. - Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 81: 465-480. Go to original source...
  10. Boenigk, J.; Pfandl, K.; Stadler, P. & Chatzinotas, A. (2005): High diversity of the 'Spumella-like' flagellates: an investigation based on the SSU rRNA gene sequences of isolates from habitats located in six different geographic regions. - Environ. Microbiol. 7: 685-697. Go to original source...
  11. Canter-Lund, H. & Lund, J.W.G. (1995): Freshwater algae: Their microscopic world explored. - 360 pp., Bristol, Biopress Ltd.
  12. Ehrenberg, C.G. (1834): Dritter Beitrag zur Erkenntniss grosser Organisation in der Richtung des kleinsten Raumes. - Abhandlungen der Königlichen Akademie der Wissenschaften 1833: 145-336.
  13. Findenig, B.M.; Chatzinotas, A. & Boenigk, J. (2010): Taxonomic and ecological characterization of stomatocysts of Spumella-like flagellates (Chrysophyceae). - J. Phycol. 46: 868-881. Go to original source...
  14. Finlay, B.J. & Esteban, G.F. (1998): Freshwater Protozoa: Biodiversity and ecological function. - Biodivers. Conserv. 7: 1163-1186. Go to original source...
  15. Gaedke, U. & Wickham, S.A. (2004): Ciliate dynamics in response to changing biotic and abiotic conditions in a large, deep lake (Lake Constance). - Aquat. Microb. Ecol. 34: 247-261. Go to original source...
  16. Galler, J. (2006): Eutrophierung: Ursachen und Maßnahmen. - 23 pp., Landwirtschaftskammer Salzburg
  17. Hepperle, D. (2004): SequentiX Alignment Editor: Distributed by Author.
  18. Hitchman, R.B. & Jones, H.L.J. (2000): The role of mixotrophic protists in the population dynamics of the microbial food web in small artificial pond. - Freshw. Biol. 43: 231-241. Go to original source...
  19. Huss, V. a. R.; Frank, C.; Hartmann, E.C.; Hirmer, M.; Kloboucek, A.; Seidel, B.M.; Wenzeler, P. & Kessler, E. (1999): Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta). - J. Phycol. 35: 587-598.
  20. Jena, M.; Bock, C.; Behera, C.; Adhikary, S.P. & Krienitz, L.(2014): Strain survey on three continents confirms the polyphyly of the genus Pediastrum (Hydrodictyaceae, Chlorophyceae). - Fottea 14: 63-76. Go to original source...
  21. Jobb, G.; Von Haeseler, A. & Strimmer, K. (2004): TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. - BMC Evol. Biol. 4.
  22. Jost, S.; Medinger, R. & Boenigk, J. (2010): Cultivation- independent species identification of Dinobryon species (Chrysophyceae) by means of multiplex single-cell PCR. - J. Phycol. 46: 901-906. Go to original source...
  23. Kamjunke, N.; Henrichs, T. & Gaedke, U. (2007): Phosphorus gain by bacterivory promotes the mixotrophic flagellate Dinobryon spp. during re- oligotrophication. - J. Plankton Res. 29: 39-46. Go to original source...
  24. Klaveness, D.; Brate, J.; Patil, V.; Shalchian-Tabrizi, K.; Kluge, R.; Gislerod, H.R. & Jakobsen, K.S. (2011): The 18S and 28S rDNA identity and phylogeny of the common lotic chrysophyte Hydrurus foetidus. - Eur. J. Phycol. 46: 282-291. Go to original source...
  25. Krienitz, L.; Bock, C.; Dadheech, P.K. & Pröschold, T. (2011): Taxonomic reassessment of the genus Mychonastes (Chlorophyceae, Chlorophyta) including the description of eight new species. - Phycologia 50: 89-106. Go to original source...
  26. Krienitz, L.; Bock, C.; Kotut, K. & Pröschold, T. (2012): Genotypic diversity of Dictyosphaerium- morphospecies (Chlorellaceae, Trebouxiophyceae) in African inland waters, including the description of four new genera. Fottea, 12: 231-253. Go to original source...
  27. Krienitz, L.; Bock, C.; Luo, W. & Pröschold, T. (2010): Polyphyletic Origin of the Dictyosphaerium Morphotype within Chlorellaceae (Trebouxiophyceae). - J. Phycol. 46: 559-563. Go to original source...
  28. Krienitz, L.; Hegewald, E.H.; Hepperle, D.; Huss, V. a. R.; Rohr, T. & Wolf, M. (2004): Phylogenetic relationship of Chlorella and Parachlorella gen. nov. (Chlorophyta, Trebouxiophyceae). - Phycologia 43: 529-542. Go to original source...
  29. Lee, R.E. (1980): Phycology. 1st ed. - 478 pp., New York, Cambridge University Press.
  30. Lefèvre, E.; Roussel, B.; Amblard, C. & Sime-Ngando, T. (2008): The molecular diversity of freshwater picoeukaryotes reveals high occurrence of putative parasitoids in the plankton. - Plos One 3: e2324. doi:10.1371. Go to original source...
  31. Luo, W., Bock, C., Li, H.R., Padisak, J. & Krienitz, L. (2011): Molecular and microscopic diversity of planktonic eukaryotes in the oligotrophic Lake Stechlin (Germany). - Hydrobiologia 661: 133-143. Go to original source...
  32. Luo, W.; Krienitz, L.; Pflugmacher, S. & Walz, N. (2005): Genus and species concept in Chlorella and Micractinium (Chlorophyta, Chlorellaceae): genotype versus phenotypical variability under ecosystem conditions. - Verh. Internat. Verein. Limnol. 29: 170-173.
  33. Luo, W.; Pflugmacher, S.; Pröschold, T.; Walz, N. & Krienitz, L. (2006): Genotype versus phenotype variability in Chlorella and Micractinium (Chlorophyta, Trebouxiophyceae). - Protist 157: 315-333. Go to original source...
  34. Lürling, M. (1998): Effect of grazing-associated infochemicals on growth and morphological, development in Scenedesmus acutus (chlorophyceae). - J. Phycol. 34: 578-586. Go to original source...
  35. Lürling, M. (1999): Grazer-induced coenobial formation in clonal cultures of Scenendesmus obliquus (Chlorococcales, Chlorophyceae). - J. Phycol. 35: 19-23. Go to original source...
  36. Matsen, F.A.; Kodner, R.B. & Armbrust, E.V. (2010): pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. - BMC Bioinformatics 11.
  37. Medinger, R. (2011): Diversity and distribution estimates with special focus on the chrysophyte Dinobryon [PhD thesis]. - 38 pp., University of Innsbruck, Insbruck.
  38. Medinger, R.; Nolte, V.; Pandey, R.V.; Jost, S.; Ottenwalder, B.; Schlotterer, 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: 32-40. Go to original source...
  39. Neustupa, J.; Nìmcová, Y.; Eliás, M. & ©kaloud, P. (2009): Kalinella bambusicola gen. et sp. nov. (Trebouxiophyceae, Chlorophyta), a novel coccoid Chlorella-like subaerial alga from Southeast Asia. - Phycol. Res. 57: 159-169. Go to original source...
  40. Nolte, V.; Pandey, R.V.; 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: 2908-2915. Go to original source...
  41. Padisák, J.; Krienitz, L.; Scheffler, W.; Koschel, R.; Kristiansen, J. & Grigorszky, I. (1998): Phytoplankton succession in the oligotrophic Lake Stechlin (Germany) in 1994 and 1995. - Hydrobiologia 370: 179-197. Go to original source...
  42. Pandey, R.V.; Nolte, V. & Schlötterer, C.(2010): CANGS: a user-friendly utility for processing and analyzing 454 GS-FLX data in biodiversity studies. - BMC Res Notes 3:3. Go to original source...
  43. Patil, V.; Brate, J.; Shalchian-Tabrizi, K. & Jakobsen, K.S. (2009): Revisiting the phylogenetic position of Synchroma grande. - J. Eukaryot. Microbiol. 56: 394-396. Go to original source...
  44. Pfandl, K.; Chatzinotas, A.; Dyal, P. & Boenigk, J. (2009): SSU rRNA gene variation resolves population heterogeneity and ecophysiological differentiation within a morphospecies (Stramenopiles, Chrysophyceae). - Limnol. Oceanogr. 54: 171-181. Go to original source...
  45. Philippe, H.; Lopez, P.; Brinkmann, H.; Budin, K.; Germot, A.; Laurent, J.; Moreira, D.; Muller, M. & Le Guyader, H. (2000): Early-branching or fast- evolving eukaryotes? An answer based on slowly evolving positions. - P. Roy. Soc. B-Biol. Sci. 267: 1213-1221.
  46. Pugnetti, A. & Bettinetti, R. (1999): Biomass and species structure of the phytoplankton of an high mountain lake (Lake Paione Superiore, Central Alps, Italy). - J. Limnol. 58: 127-130. Go to original source...
  47. Rambaut A. & Drummond, A.J. (2007): Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer.
  48. Reynolds, C.S. (1980): Phytoplankton Assemblages and their periodicity in stratifying lake systems. - Holarctic Ecol. 3: 141-159.
  49. Ronquist, F. & Huelsenbeck, J.P. (2003): MrBayes 3: Bayesian phylogenetic inference under mixed models. - Bioinformatics 19: 1572-1574. Go to original source...
  50. Sandgren, C.D. (1988): The ecology of chrysophyte flagellates: their growth and perennation strategies as freshwater phytoplankton - In: Sandgren, C.D. (ed.): Growth and Reproductive Strategies of Freshwater Phytoplankton. - pp. 9-104, Cambridge University Press, Cambridge.
  51. Shalchian-Tabrizi, K.; Eikrem, W.; Klaveness, D.; Vaulot, D.; Minge, M.A.; Gall, F.L.; Romari, K.; Throndsen, J.; Botnen, A.; Massana, R.; Thomsen, H.A. & Jakobsen, K.S. (2006): Telonemia, a new protist phylum with affinity to chromist lineages. - Proc. R. Soc. 273: 1833-1842. Go to original source...
  52. Silberfeld, T.; Leigh, J. W.; Verbruggen, H.; Cruaud, C.; De Reviers, B. & Rousseau, F. (2010): A multi- locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): Investigating the evolutionary nature of the "brown algal crown radiation". - Mol. Phylogen. Evol. 56: 659-674. Go to original source...
  53. Siver, P.A. & Chock, J.S. (1986): Phytoplankton dynamics in a chrysophycean lake. - In: Kristiansen, J. & Andersen, R.A. (eds): Chrysophytes: aspects and problems. - pp. 165-183, Cambridge University Press - Cambridge.
  54. Stamatakis, A.; Ludwig, T. & Meier, H. (2005): RAxML- III: a fast program for maximum likelihood- based inference of large phylogenetic trees. - Bioinformatics 21: 456-463. Go to original source...
  55. Starmach, K. (1985): Chrysophyceae und Haptophyceae. - 515 pp., Gustav Fischer Verlag, Stuttgart & New York.
  56. Stoeck, T.; Jost, S. & Boenigk, J. (2008): Multigene phylogenies of clonal Spumella-like strains, a cryptic heterotrophic nanoflagellate, isolated from different geographical regions. - Int. J. Syst. Evol. Microbiol. 58: 716-724. Go to original source...
  57. Swofford, D.L. (2002): Phylogenetic analysis using parsimony (and other methods), version 4.0b 10. Massachusetts: Sinauer Associates, Sunderland.
  58. Tas, B.; Gonulol, A. & Tas, E. (2010): Seasonal dynamics and biomass of mixotrophic flagellate Dinobryon sertularia Ehrenberg (Chrysophyceae) in Derbent Reservoir (Samsun, Turkey). - Turkish J. Fish. Aquat. Sci. 10: 305-313. Go to original source...
  59. Thompson, J.D.; Higgins, D.G. & Gibson, T.J. (1994): Clustal-W - Improving the Sensitivity of Progressive Multiple Sequence Alignment through Sequence Weighting, Position-Specific Gap Penalties and Weight Matrix Choice. - Nucl. Acids Res. 22: 4673- 4680. Go to original source...
  60. Tolotti, M.; Thies, H.; Cantonati, M.; Hansen, C.M.E. & Thaler, B. (2003): Flagellate algae (Chrysophyceae, Dinophyceae, Cryptophyceae) in 48 high mountain lakes of the Northern and Southern slope of the Eastern Alps: biodiversity, taxa distribution and their driving variables. - Hydrobiologia 502: 331-348. Go to original source...
  61. Trainor, F.R. (1998): Biological aspects of Scenedesmus (Chlorophyceae)-phenotypic plasticity. - Nova Hedwigia, Beiheft 117: 1-367.
  62. Veen, A. (1991): Ecophysiological studies on the phagotrophic phytoflagellate Dinobryon divergens Imhof. [PhD thesis]. - 125 pp., Universiteit van Amsterdam, Amsterdam.
  63. Watson, S.B.; Satchwill, T.; Dixon, E. & McCauley, E. (2001): Underice blooms and source-water odour in a nutrient-poor reservoir: biological, ecological and applied perspectives. - Freshw. Biol. 46: 1553-1567. Go to original source...
  64. Willen, E. (2003): Dominance patterns of planktonic algae in Swedish forest lakes. - Hydrobiologia 502: 315-324. Go to original source...