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Hidden diversity of eukaryotic plankton in the soda lake Nakuru, Kenya, during a phase of low salinity revealed by a SSU rRNA gene clone library

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Abstract

A SSU rRNA gene clone library was constructed to establish the diversity of eukaryotic plankton in the African soda lake Nakuru during a phase of low salinity (9.7 ppt = hyposaline). Normally, the lake is mesosaline (up to 50 ppt) and its phytoplankton is dominated by few species of cyanobacteria, in particular Arthrospira fusiformis, which is the main food resource of Lesser Flamingos. Our study recovered a unique phytoplankton species composition characterized by a high diversity of monadoid and coccoid green algae. Out of 77 clones detected, 52 belonged to Chlorophyta. Many of the chlorophytes were transported from the catchment area into the lake through small seasonal rivers and an outflow of the Nakuru town sewage treatment plant. Other phylogenetic groups detected were Fungi, Cryptophyta, Jakobida, Alveolata, Stramenopiles, and Metazoa. Our findings reveal a hidden diversity, which would not have been detected by traditional observations.

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References

  • Adl, S. M., A. G. B. Simpson, M. A. Farmer, R. A. Andersen, O. R. Anderson & J. R. Barta, 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology 52: 399–451.

    Article  PubMed  Google Scholar 

  • Aguinaldo, A. M., J. M. Turbeville, L. S. Linford, M. C. Rivera, J. R. Garey, R. A. Raff & J. A. Lake, 1997. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387: 489–493.

    Article  PubMed  CAS  Google Scholar 

  • Ballot, A., L. Krienitz, K. Kotut, C. Wiegand, J. S. Metcalf, G. A. Codd & S. Pflugmacher, 2004. Cyanobacteria and cyanobacterial toxins in three alkaline Rift Valley lakes of Kenya – Lakes Bogoria, Nakuru and Elmenteita. Journal of Plankton Research 26: 925–935.

    Article  CAS  Google Scholar 

  • Buchheim, M. A., A. E. Kirkwood, J. A. Buchheim, B. Verghese & W. J. Henley, 2010. Hypersaline soil supports a diverse community of Dunaliella (Chlorophyceae). Journal of Phycology 46: 1038–1047.

    Article  Google Scholar 

  • Cole, J. R., B. Chai, L. Marsh, J. Farris, Q. Wang, S. A. Kulam, S. Chandra, D. M. McGarrell, T. M. Schmidt, G. M. Garrity & M. Tiedje, 2003. The ribosomal database project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Research 31: 442–443.

    Article  PubMed  CAS  Google Scholar 

  • Douglas, S. E., C. A. Murphy, D. F. Spencer & M. W. Gray, 1991. Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350: 148–151.

    Article  PubMed  CAS  Google Scholar 

  • Ferroni, L., C. Baldisserotto, L. Pantaleoni, P. Billi, M. P. Fasulo & S. Pancaldi, 2007. High salinity alters chloroplast morpho-physiology in a freshwater Kirchneriella species (Selenastraceae) from Ethiopian Lake Awasa. American Journal of Botany 94: 1972–1983.

    Article  PubMed  Google Scholar 

  • Fulnečková, J., T. Hasíková, J. Fajkus, A. Lukešová, M. Eliás & E. Sýkorova, 2012. Dynamic evolution of telomeric sequences in the green algal order Chlamydomonadales. Genome Biology and Evolution 4: 248–264.

    Article  PubMed  Google Scholar 

  • Hammer, U. T., J. Shamess & R. C. Haynes, 1983. The distribution and abundance of algae in saline lakes Saskatchewan, Canada. Hydrobiologia 105: 1–26.

    Article  Google Scholar 

  • Hepperle, D., 2003. Align, Manual Sequence Alignment Editor for PCs. http://wwwuser.gwdg.de/~dhepper/.

  • Hepperle, D., H. Nozaki, S. Hohenberger, V. A. R. Huss, E. Morita & L. Krienitz, 1998. Phylogenetic position of the Phacotaceae within the Chlamydophyceaeas revealed by analysis of 18S rDNA and rbcL sequences. Journal of Molecular Evolution 47: 420–430.

    Article  PubMed  CAS  Google Scholar 

  • Hepperle, D., E. Hegewald & L. Krienitz, 2000. Phylogenetic position of Oocystaceae (Chlorophyta). Journal of Phycology 36: 590–595.

    Article  CAS  Google Scholar 

  • Hill, D. R. A. & R. Wetherbee, 1990. Guillardia theta gen. et sp. nov. (Cryptophyceae). Canadian Journal of Botany 68: 1873–1876.

    Google Scholar 

  • Huss, V. A. R., C. Frank, E. C. Hartmann, M. Hirmer, A. Kloboucek, B. M. Seidel, P. Wenzeler & E. Kessler, 1999. Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta). Journal of Phycology 35: 587–598.

    Article  CAS  Google Scholar 

  • Kagami, M., A. de Bruin, B. W. Ibelings & E. Van Donk, 2007. Parasitic chytrids: their effects on plankton communities and food-web dynamics. Hydrobiologia 578: 113–129.

    Article  Google Scholar 

  • Kessler, E., 1982. Chemotaxonomy in the Chlorococcales. In Round, F. E. & D. J. Chapman (eds) Progress in Phycological Research, Vol. 1. Elsevier Biomedical Press B.V. Amsterdam: 111–135.

  • Kotut, K., A. Ballot, C. Wiegand & L. Krienitz, 2010. Toxic cyanobacteria at Nakuru sewage oxidation ponds – a potential threat to wildlife. Limnologica 40: 47–53.

    Article  CAS  Google Scholar 

  • Krienitz, L. & K. Kotut, 2010. Fluctuating algal food populations and the occurrence of Lesser Flamingos (Phoeniconaias minor) in three Kenyan Rift Valley lakes. Journal of Phycology 46: 1088–1096.

    Article  Google Scholar 

  • Krienitz, L., C. Bock, K. Kotut & W. Luo, 2012a. Picocystis salinarum (Chlorophyta) in saline lakes and hot springs of East Africa. Phycologia 51: 22–32.

    Article  Google Scholar 

  • Krienitz, L., C. Bock, K. Kotut & T. Pröschold, 2012b. Genotypic diversity of Dictyosphaerium-morphospecies (Chlorellaceae, Trebouxiophyceae) in African inland waters, including the description of four new genera. Fottea 12: 231–253.

    Google Scholar 

  • Lara, E., A. Chatzinotas & A. G. B. Simpson, 2006. Andalucia (n. gen.) – the deepest branch within jacobids (Jacobida: Excavata), based on morphological and molecular study of a new flagellate from soil. Journal of Eukayotic Microbiology 53: 112–120.

    Article  CAS  Google Scholar 

  • Lara, E., C. Berney, F. Ekelund, H. Harms & A. Chatzinotas, 2007. Molecular comparison of cultivable protozoa from a pristine and a polycyclic aromatic hydrocarbon polluted site. Soil Biology and Biochemistry 39: 139–148.

    Google Scholar 

  • Lefèvre, E., B. Roussel, C. Amblard & T. Sime-Ngando, 2008. The molecular diversity of freshwater picoeukaryotes reveals high occurrence of putative parasitoids in the plankton. PLoS One 3: E2324.

    Article  PubMed  Google Scholar 

  • Leliaert, F., D. R. Smith, H. Moreau, M. D. Herron, H. Verbruggen, C. F. Delwiche & O. De Clerk, 2012. Phylogeny and molecular evolution of the green algae. Critical Reviews in Plant Sciences 31: 1–46.

    Article  Google Scholar 

  • Luo, W., H. R. Li, M. H. Cai & J. F. He, 2009. Diversity of microbial eukaryotes in Kongsfjorden, Svalbard. Hydrobiologia 636: 233–248.

    Article  Google Scholar 

  • Luo, W., C. Bock, H. R. Li, J. Padisák & L. Krienitz, 2011. Molecular and microscopic diversity of planktonic eukaryotes in oligotrophic Lake Stechlin (Germany). Hydrobiologia 661: 133–143.

    Article  CAS  Google Scholar 

  • Medlin, L. K., H. J. Elwood, S. Stickel & M. L. Sogin, 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71: 491–499.

    Article  PubMed  CAS  Google Scholar 

  • Melack, J. M., 1988. Primary producer dynamics associated with evaporative concentration in a shallow, equatorial soda lake (Lake Elmenteita, Kenya). Hydrobiologia 158: 1–14.

    Article  CAS  Google Scholar 

  • Monchy, S., G. Sanciu, M. Jobard, S. Rasconi, M. Gerphagnon, M. Chabe, A. Cian, D. Meloni, N. Niquil, U. Christaki, E. Viscogliosi & T. Sime-Ngando, 2011. Exploring and quantifying fungal diversity in freshwater lake ecosystems using rDNA cloning/sequencing and SSU tag pyrosequencing. Environmental Microbiology 13: 1433–1453.

    Article  PubMed  Google Scholar 

  • Nakada, T., H. Nozaki & T. Pröschold, 2008. Molecular phylogeny, ultrastructure, and taxonomic revision of Chlorogonium (Chlorophyta): emendation of Chlorogonium and description of Gungnir gen. nov. and Rusalka gen. nov. Journal of Phycology 44: 751–760.

    Article  Google Scholar 

  • Opticount, 2008. http://science.do-mix.de/software_opticount.php.

  • Padisák, J., 1992. Seasonal succession of phytoplankton in a large shallow lake (Balato, Hungary) – a dynamic approach to ecological memory, its possible role and mechanisms. Journal of Ecology 80: 217–230.

    Article  Google Scholar 

  • Padisák, J., 2009. The Bioogeography of Freshwater Algae. In Likens, G. (ed.), Encyclopedia of Inland Waters, Vol. I. Elsevier, Oxford: 219–223.

    Chapter  Google Scholar 

  • Padisák, J., E. Hajnal, L. Krienitz, J. Lakner & V. Üveges, 2010. Rarity, ecological memory, rate of floral change in phytoplankton – and the mystery of the Red Cock. Hydrobiologia 653: 45–64.

    Article  Google Scholar 

  • Park, J. S. & A. G. Simpson, 2010. Characterization of halotolerant Bicosoecida and Placididea (Stramenopila) that are distinct from marine forms, and the phylogenetic pattern of salinity preference in heterotrophic stramenopiles. Environmental Microbiology 12: 1173–1184.

    Article  PubMed  CAS  Google Scholar 

  • Pocock, T., M.-A. Lachance, T. Pröschold, J. C. Priscu, S. Kim & N. P. Huner, 2004. Identification of a psychrophilic green alga from Lake Bonney Antarctica: Chlamydomonas raudensis ETTL (UWO 241) (Chlorophyceae). Journal of Phycology 40: 1138–1148.

    Article  Google Scholar 

  • Pröschold, T., B. Marin, U. G. Schlösser & M. Melkonian, 2001. Molecular phylogeny and taxonomic revision of Chlamydomonas (Chlorophyta). I. Emendation of Chlamydomonas Ehrenberg and Chloromonas Gobi, and description of Oogamochlamys gen. nov. and Lobochlamys gen. nov. Protist 152: 265–300.

    Article  PubMed  Google Scholar 

  • Schagerl, M. & S. O. Oduor, 2008. Phytoplankton community relationship to environmental variables in three Kenyan Rift Valley saline–alkaline lakes. Marine & Freshwater Research 59: 125–136.

    Article  CAS  Google Scholar 

  • Simpson, A. G. B. & D. J. Patterson, 2001. On core jakobids and excavate taxa: the ultrastructure of: Jakoba incarcerata. Journal of Eukaryotic Microbiology 48: 480–492.

    Article  PubMed  CAS  Google Scholar 

  • Sommer, U., 1994. Planktologie. Springer, Berlin: 274.

    Book  Google Scholar 

  • Steidinger, K. A., J. H. Landsberg, P. L. Mason, W. K. Vogelbein, P. A. Tester & R. W. Litaker, 2006. Cryptoperidiniopsis broadyi gen. et sp. nov. (Dinophyceae), a small lightly armoured dinoflagellate in the Pfiesteriaceae. Journal of Phycology 42: 951–961.

    Article  Google Scholar 

  • Tuite, C. H., 2000. The distribution and density of Lesser Flamingos in East Africa in relation to food availability and productivity. Waterbirds (Special Publication) 23: 52–63.

    Google Scholar 

  • Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitteilungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 9: 1–38.

    Google Scholar 

  • Vareschi, E., 1982. The ecology of Lake Nakuru (Kenya) III. Abiotic factors and primary production. Oecologia 55: 81–101.

    Article  Google Scholar 

  • Voronin, L. V., 2008. Zoosporic fungi in freshwater ecosystems. Inland Water Biology 1: 341–346.

    Article  Google Scholar 

  • Wilson, C., T. M. Caton, J. A. Buchheim, M. A. Buchheim, M. A. Schneegurt & R. V. Miller, 2004. DNA-repair potential in Halomonas spp. From the salt plains microbial observatory of Oklahoma. Microbial Ecology 48: 541–549.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank the authorities of the Republic of Kenya, especially the National Council for Science and Technology for providing research permission (No. NCST/RRI/12/1/BS/232). W.L. thanks for the financial support of the State High-Tech Research and Development Project (863) of the Ministry of Science and Technology of China (2012AA021706), and the Shanghai Rising-Star Program (Grant No. 11QA1407300).

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Correspondence to Lothar Krienitz.

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Luo, W., Kotut, K. & Krienitz, L. Hidden diversity of eukaryotic plankton in the soda lake Nakuru, Kenya, during a phase of low salinity revealed by a SSU rRNA gene clone library. Hydrobiologia 702, 95–103 (2013). https://doi.org/10.1007/s10750-012-1310-y

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