Skip to main content
Log in

Molecular diversity of plankton in a tropical crater lake switching from hyposaline to subsaline conditions: Lake Oloidien, Kenya

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Salinity in the climate sensitive tropical endorheic crater lake Oloidien (Great African Rift Valley, Kenya) decreased from hyposaline to subsaline conditions during the period 2010–2015. The change in salinity was accompanied by a pronounced change in planktonic life forms—from blooms of the cyanobacterium Arthrospira supporting tens of thousands of Lesser Flamingos to highly diverse communities of cyanobacteria and algae which do not sustain the consumer birds. Besides the well-known macro- and microscopic lake life, a hidden diversity of microorganisms was detected using molecular methods. SSU rRNA gene clone libraries and data from Ilumina Miseq sequencing of samples collected at the two contrasting stages revealed distinct and highly diverse microbial communities. Different bacterial clades dominated the two samples. In 2011, Firmicutes (class Bacilli) whose origin was the fecal waste of birds were the dominant group. However, the Cyanobacteria and Chloroflexi were the most prevalent in 2015. From the microbial eukaryote samples obtained in 2011, rotifers and ciliates that feed on Arthrospira and rich bacterial food dominated the plankton, while the cryptophytes were the most prevalent in 2015. On the two occasions, a mixture of organisms previously not known to occur in saline or in freshwater habitats was found.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

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 

  • 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 

  • Ballot, A., L. Krienitz, E. Novelo & K. Kotut, 2009. Changes of phytoplankton communities in Lakes Naivasha and Oloidien, examples of degradation and salinization of lakes in the Kenyan Rift Valley. Hydrobiologia 632: 359–363.

    Article  CAS  Google Scholar 

  • Bass, D., A. T. Howe, A. P. Mylnikov, K. Vickerman, E. E. Chao, J. Edwards Smallbone, J. Snell, C. Cabral Jr. & T. Cavalier-Smith, 2009. Phylogeny and classification of Cercomonadida (Protozoa, Cercozoa): Cercomonas, Eocercomonas, Paracercomonas, and Cavernomonas gen. nov. Protist 160: 483–521.

    Article  PubMed  Google Scholar 

  • Beadle, L. C., 1974. The Inland Waters of Tropical Africa. Longman, London: 365.

    Google Scholar 

  • Beckmann, S., T. Lueders, M. Kruger, F. von Netzer, B. Engelen & H. Cypionka, 2011. Acetogens and acetoclastic methanosarcinales govern methane formation in abandoned coal mines. Applied Environmental Microbiology 77: 3749–3756.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Binder, M., K. H. Larsson, P. B. Matheny & D. S. Hibbett, 2010. Amylocorticiales ord. nov. and Jaapiales ord. nov.: early divergingclades of agaricomycetidae dominated by corticioid forms. Mycologia 102: 865–880.

    Article  CAS  PubMed  Google Scholar 

  • Borsodi, A. K., K. Márialigeti, G. Szabó, M. Palatinszky, B. Pollák, Z. Kéki, A. L. Kovács, P. Schumann & E. M. Tóth, 2008. Bacillus aurantiacus sp. nov., a novel alkaliphilic and moderately halophilic bacterium isolated from Hungarian soda lakes. International Journal of Systematic and Evolutionary Microbiology 58: 845–851.

    Article  PubMed  Google Scholar 

  • Borsodi, A. K., M. Knáb, K. Czeibert, K. Márialigeti, L. Vörös & B. Somogyi, 2013. Planktonic bacterial community composition of an extremely shallow soda pond during a phytoplankton bloom revealed by cultivation and molecular cloning. Extremophiles 17: 575–584.

    Article  PubMed  Google Scholar 

  • Boxhorn, J. E., D. A. Holen & M. E. Boraas, 1998. Toxicity of the chrysophyte flagellate Poterioochromonas malhamensis to the rotifer Brachionus angularis. Hydrobiologia 387(388): 283–287.

    Article  Google Scholar 

  • Bråte, J., R. Logares, C. Berney, D. K. Ree, D. Klaveness, K. S. Jakobsen & K. Shalchian-Tabrizi, 2010. Freshwater Perkinsea and marine-freshwater colonizations revealed by pyrosequencing and phylogeny of environmental rDNA. The ISME Journal 4: 1144–1153.

    Article  PubMed  CAS  Google Scholar 

  • Brown, L. H., 1959. The Mystery of the Flamingos. Country Life Ltd., London: 116.

    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 

  • Burian, A., M. Schagerl & A. Yasindi, 2013. Microzooplankton feeding behavior: grazing on the microbial and the classical food web of African soda lakes. Hydrobiologia 710: 61–72.

    Article  CAS  Google Scholar 

  • Callieri, C., G. Cronberg & J. Stockner, 2012. Freshwater picocyanobateria: single cells, microcolonies and colonial forms. In Whitton, B. (ed.), Ecology of Cyanobacteria: Their Diversity in Time and Space, 2nd ed. Springer Publishers, Berlin: 229–269.

    Chapter  Google Scholar 

  • Callieri, C., M. Coci, G. Corno, M. Macek, B. Modenutti, E. Balseiro & R. Bertoni, 2013. Phylogenetic diversity of nonmarine picocyanobacteria. FEMS Microbiology Ecology 85: 293–301.

    Article  CAS  PubMed  Google Scholar 

  • Caporaso, J. G., J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Peña, J. K. Goodrich, J. I. Gordon, G. A. Huttley, S. T. Kelley, D. Knights, J. E. Koenig, R. E. Ley, C. A. Lozupone, D. McDonald, B. D. Muegge, M. Pirrung, J. Reeder, J. R. Sevinsky, P. J. Turnbaugh, W. A. Walters, J. Widmann, T. Yatsunenko, J. Zaneveld & R. Knight, 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335–336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso, J. G., C. L. Lauber, W. A. Walters, D. Berg-Lyons, C. A. Lozupone, P. J. Turnbaugh, N. Fierer & R. Knight, 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Science of the United States of America 108(Suppl 1): 4516–4522.

    Article  CAS  Google Scholar 

  • Caporaso, J. G., C. L. Lauber, W. A. Walters, D. Berg-Lyons, J. Huntley, N. Fierer, S. M. Owens, J. Betley, L. Fraser, M. Bauer, N. Gormley, J. A. Gilbert, G. Smith & R. Knight, 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal 6: 1621–1624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavalier-Smith, T., R. Lewis, E. E. Chao, B. Oates & D. Bass, 2009. Helkesimastix marina n. sp. (Cercozoa: Sainouroidea superfam. n.) a gliding zooflagellate of novel ultrastructure and unusual ciliary behaviour. Protist 160: 452–479.

    Article  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Costello, M. J., M. Coll, R. Danovaro, P. Halpin, H. Ojaveer & P. Miloslavich, 2010. A census of marine biodiversity knowledge, resources, and future challenges. PLoS One 5: e12110.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dadheech, P. K., A. Ballot, P. Casper, K. Kotut, E. Novelo, B. Lemma, T. Pröschold & L. Krienitz, 2010. Phylogenetic relationship and divergence among planktonic strains of Arthrospira (Oscillatoriales, Cyanobacteria) of African, Asian and American origin deduced by 16S–23S ITS and phycocyanin operon sequences. Phycologia 49: 361–372.

    Article  CAS  Google Scholar 

  • Demergasso, C., E. O. Casamayor, G. Chong, P. Galleguillos, L. Escudero & C. Pedrós-Alió, 2004. Distribution of prokaryotic genetic diversity in athalassohaline lakes of the Atacama Desert, northern Chile. FEMS Microbiology Ecology 48: 57–69.

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Dudgeon, D., A. H. Arthington, M. O. Gessner, Z. Kawabata, D. J. Knowler, C. Leveque, R. J. Naiman, A. H. Prieur-Richard, D. Soto, M. L. Stiassny & C. A. Sullivan, 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews of the Cambridge Philosophical Society Journal 81: 163–182.

    Article  Google Scholar 

  • Dunbar, J., S. A. Eichorst, L. V. Gallegos-Graves, S. Silva, G. Xie, N. W. Hengartner, R. D. Evans, B. A. Hungate, R. B. Jackson, J. P. Megonigal, C. W. Schadt, R. Vilgalys, D. R. Zak & C. R. Kuske, 2012. Common bacterial responses in six ecosystems exposed to 10 years of elevated atmospheric carbon dioxide. Environmental Microbiology 14: 1145–1158.

    Article  CAS  PubMed  Google Scholar 

  • Dvořák, P., D. A. Casamatta, A. Pouličková, P. Hašler, V. Ondřej & R. Sanges, 2014. Synechococcus: 3 billion years of global dominance. Molecular Ecology 23: 5538–5551.

    Article  PubMed  CAS  Google Scholar 

  • Farrelly, V., F. A. Rainey & E. Stackebrandt, 1995. Effect of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species. Applied Environmental Microbiology 61: 2798–2801.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fawcett, R. C. & M. W. Parrow, 2012. Cytological and phylogenetic diversity of freshwater Esoptrodinium/Bernardinium species (Dinophyceae). Journal of Phycology 48: 793–807.

    Article  CAS  PubMed  Google Scholar 

  • Fawcett, R. C. & M. W. Parrow, 2014. Mixotrophy and loss of phototrophy among geographic isolates of freshwater Esoptrodinium/Bernardinium sp. (Dinophyceae). Journal of Phycology 50: 55–70.

    Article  CAS  PubMed  Google Scholar 

  • Garrity, G. M., M. Winters, A. W. Kuo & D. B. Searles, 2002. Taxonomic Outline of the Prokaryotes, Bergey’s Manual of Systematic Bacteriology, 2nd ed. Springer, New York.

    Google Scholar 

  • Gasse, F., P. Barker, P. A. Gell, S. C. Fritz & F. Chalié, 1997. Diatom-inferred salinity in paleolakes: an indirect tracer of climate change. Quaternary Science Reviews 16: 547–563.

    Article  Google Scholar 

  • Girma, M. B., D. Kifle & H. Jebessa, 2012. Deep underwater seismic explosion experiments and their possible ecological impact – the case of Lake Arenguade-Central Ethiopian highlands. Limnologica 42: 212–219.

    Article  CAS  Google Scholar 

  • Glöckner, F. O., B. M. Fuchs & R. Amann, 1999. Bacterioplankton composition of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Applied Environmental Microbiology 65: 3721–3726.

    PubMed  PubMed Central  Google Scholar 

  • Grant, W. D. & D. Y. Sorokin, 2011. Distribution and diversity of soda lake alkaliphiles. In Horikoshi, K., G. Antranikian, A. T. Bull, F. T. Robb & K. O. Stetter (eds), Extremophiles Handbook. Springer, New York: 27–54.

    Chapter  Google Scholar 

  • Grant, W. D. & B. E. Jones, 2016. Bacteria, Archaea and Viruses of soda lakes. In Schagerl, M. (ed.), Soda Lakes of East Africa. Springer Publishers, Switzerland: 97–147.

    Chapter  Google Scholar 

  • Grossart, H.-P. & K. Rojas-Jimenez, 2016. Targeting the forgotten in microbial ecology. Current Opionion in Microbiology 31: 140–145.

    Article  Google Scholar 

  • Hegewald, E., M. Wolf, A. Keller, T. Friedl & L. Krienitz, 2010. ITS2 sequence-structure phylogeny in the Scenedesmaceae with special reference to Coelastrum (Chlorophyta, Chlorophyceae), including the new genera Comasiella and Pectinodesmus. Phycologia 49: 325–335.

    Article  CAS  Google Scholar 

  • Hepperle, D., 2003. Align, Manual Sequence Alignment Editor for PCs. Distributed by the author [available on http://wwwuser.gwdg.de/~dhepper/].

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

    Article  Google Scholar 

  • Hugenholtz, P., B. M. Goebel & N. R. Pace, 1998. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. Journal of Bacteriology 180: 4765–4774.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Humayoun, S. B., N. Bano & J. T. Hollibaugh, 2003. Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Applied Environmental Microbiology 69: 1030–1042.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jasser, I., A. Karnkowska-Ishikawa, E. Kozlowska, A. Krolicka & M. Lukomska-Kowalczyk, 2010. Composition of picocyanobacteria community in the Great Mazurian Lakes: isolation of phycoerythrin-rich and phycocyanin-rich ecotypes from the system–comparison of two methods. Polish Journal of Microbiology 59: 21–31.

    CAS  PubMed  Google Scholar 

  • Jones, B. E., W. D. Grant, A. W. Duckworth & G. G. Owenson, 1998. Microbial diversity of soda lakes. Extremophiles 2: 191–200.

    Article  CAS  PubMed  Google Scholar 

  • Jost, S., R. Medinger & J. Boenigk, 2010. Cultivation-Independent species identification of Dinobryon species (Chrysophyceae) by means of multiplex single-cell PCR. Journal of Phycology 46: 901–906.

    Article  CAS  Google Scholar 

  • Kahn, P., L. Herfort, T. D. Peterson & P. Zuber, 2014. Discovery of a Katablepharis sp. in the Columbia River estuary that is abundant during the spring and bears a unique large ribosomal subunit sequence element. Microbiology Open 3: 764–776.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaggwa, M. N., M. Gruber, S. O. Oduor & M. Schagerl, 2013. A detailed time series assessment of the diet of Lesser Flamingos: further explanation for their itinerant behaviour. Hydrobiologia 710: 83–93.

    Article  CAS  Google Scholar 

  • Kalff, J. & S. Watson, 1986. Phytoplankton and its dynamics in two tropical lakes: a tropical and temperate zone comparison. Hydrobiologia 138: 161–176.

    Article  Google Scholar 

  • Kambura, A. K., R. K. Mwirichia, R. W. Kasili, E. N. Karanja, H. M. Makonde & H. I. Boga, 2016a. Bacteria and Archaea diversity within the hot springs of Lake Magadi and Little Magadi in Kenya. BMC Microbiology 16: 136–147.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kambura, A. K., R. K. Mwirichia, R. W. Kasili, E. N. Karanja, H. M. Makonde & H. I. Boga, 2016b. Diversity of fungi in sediments and water sampled from the hot springs of Lake Magadi and Little Magadi in Kenya. African Journal of Microbiology Research 10: 330–338.

    Article  CAS  Google Scholar 

  • Kaplan-Levy, R. N., A. Alster-Gloukhovski, Y. Benyamini & T. Zohary, 2016. Lake Kinneret phytoplankton: integrating classical and molecular taxonomy. Hydrobiologia. 764: 283–302.

    Article  CAS  Google Scholar 

  • Kebede, E., 2002. Phytoplankton distribution in lakes of the Ethiopian Rift Valley. In Tudorancea, C. & W. D. Taylor (eds), Ethiopian Rift Valley Lakes. Backhuys Publ, Leiden: 61–93.

    Google Scholar 

  • Kerkhof, L. & M. Speck, 1997. Ribosomal RNA gene dosage in marine bacteria. Molecular Marine Biology and Biotechnology 6: 260–267.

    CAS  PubMed  Google Scholar 

  • Keshri, J., B. Yousuf, A. Mishra & B. Jha, 2015. The abundance of functional genes, cbbL, nifH, amoA and apsA, and bacterial community structure of intertidal soil from Arabian Sea. Microbiol Research 175: 57–66.

    Article  CAS  Google Scholar 

  • Komárek, J. & K. Anagnostidis, 1999. Cyanoprokaryota 1: chroococcales. In: Ettl, H., G. Gärtner, H. Heynig & D. Mollenhauer (eds) Süßwasserflora von Mitteleuropa19/1, Gustav Fischer, Jena, Stuttgart, Lübeck, Ulm, 548 pp.

  • Korelusová, J., J. Kaštovský & J. Komárek, 2009. Diversity of the cyanobacterial genus Synechocystis Sauvegeau and Geminocystis genus nova. Journal of Phycology 45: 928–937.

    Article  PubMed  CAS  Google Scholar 

  • Krammer, K. & H. Lange-Bertalot, 1986. Süßwasserflora von Mitteleuropa, Bacillariophyceae 2/1. In Ettl, H., J. Gerloff, H. Heynig & D. Mollenhauer (eds), Süsswasserflora von Mitteleuropa. Gustav Fischer Verlag, Jena: 876.

    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. & M. Schagerl, 2016. Tiny and tough: microphytes of East African soda lakes. In Schagerl, M. (ed.), Soda Lakes of East Africa. Springer, Berlin: 149–177.

    Chapter  Google Scholar 

  • Krienitz, L., C. Bock, P. K. Dadheech & T. Pröschold, 2011. Taxonomic reassessment of the genus Mychonastes (Chlorophyceae, Chlorophyta) including the description of eight new species. Phycologia 50: 89–106.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Krienitz, L., P. K. Dadheech & K. Kotut, 2013a. Mass developments of a small sized ecotype of Arthrospira fusiformis in Lake Oloidien, Kenya, a new feeding ground for Lesser Flamingos in East Africa. Fottea 13: 215–225.

    Article  Google Scholar 

  • Krienitz, L., P. K. Dadheech & K. Kotut, 2013b. Mass developments of the cyanobacteria Anabaenopsis and Cyanospira (Nostocales) in the soda lakes of Kenya: ecological and systematic implications. Hydrobiologia 703: 79–93.

    Article  CAS  Google Scholar 

  • Krienitz, L., P. K. Dadheech, J. Fastner & K. Kotut, 2013c. The rise of potentially toxin producing cyanobacteria in Lake Naivasha, Great African Rift Valley, Kenya. Harmful Algae 27: 42–51.

    Article  CAS  Google Scholar 

  • Krienitz, L., D. Krienitz, P. K. Dadheech, T. Hübener, K. Kotut, W. Luo, K. Teubner & W. D. Versfeld, 2016a. Food algae for Lesser Flamingos: a stocktaking. Hydrobiologia 775: 21–50.

    Article  CAS  Google Scholar 

  • Krienitz, L., B. Mähnert & M. Schagerl, 2016b. Lesser Flamingo as a central element of the East African avifauna. In Schagerl, M. (ed.), Soda Lakes of East Africa. Springer, Berlin: 259–284.

    Chapter  Google Scholar 

  • Lanzén, A., A. Simachew, A. Gessesse, D. Chmolowska, I. Jonassen & L. Øvreås, 2013. Surprising prokaryotic and eukaryotic diversity, community structure and biogeography of Ethiopian soda lakes. PLoS One 8: e72577.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leander, B. S., O. N. Kuvardinap, V. V. Aleshin, A. P. Mylnikov & P. J. Keeling, 2003. Molecular phylogeny and surface morphology of Colpodella edax (Alveolata): insights into the phagotrophic ancestry of apicomplexans. Journal of Eukaryotic Microbiology 50: 334–340.

    Article  PubMed  Google Scholar 

  • Li, R. H., H. J. Debella & W. W. Carmichael, 2001. Isolates identifiable as Arthrospira maxima and Arthrospira fusiformis (Oscillatoriales, Cyanobacteria) appear identical on the basis of a morphological study in culture and 16S rRNA gene sequences. Phycologia 40: 367–371.

    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., T. Pröschold, C. Bock & L. Krienitz, 2010. Generic concept in Chlorella-related coccoid green algae (Chlorophyta, Trebouxiophyceae). Plant Biology 12: 545–553.

    Article  CAS  PubMed  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 

  • Luo, W., K. Kotut & L. Krienitz, 2013. 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.

    Article  CAS  Google Scholar 

  • Ma, Y., W. Zhang, Y. Xue, P. Zhou, A. Ventosa & W. D. Grant, 2004. Bacterial diversity of the Inner Mongolian Baer Soda Lake as revealed by 16S rRNA gene sequence analyses. Extremophiles 8: 45–51.

    Article  CAS  PubMed  Google Scholar 

  • MacColl, E., M. D. Therkelsen, T. Sherpa, H. Ellerbrock, L. A. Johnston, R. H. Jariwala, W. Chang, J. Gurtowski, M. C. Schatz, M. Mozammal Hossain, D. M. Cassidy-Hanley, T. G. Clark & W. J. Chang, 2015. Molecular genetic diversity and characterization of conjugation genes in the fish parasite Ichthyophthirius multifiliis. Molecular Phylogenetics and Evolution 86: 1–7.

    Article  CAS  PubMed  Google Scholar 

  • Macek, M., C. Callieri, K. Simek & A. L. Vazquez, 2006. Seasonal dynamics, composition and feeding patterns of ciliate assemblages in oligotrophic lakes covering a wide pH range. Archiv für Hydrobiologie 166: 261–287.

    Article  Google Scholar 

  • Matthews, R. A., 2005. Ichthyophthirius multifiliis Fouquet and ichthyophthiriosis in freshwater teleosts. Advances in Parasitology 59: 159–241.

    Article  CAS  PubMed  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 

  • 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  CAS  PubMed  Google Scholar 

  • Mengistou, S., 2016. Invertebrates of East African soda lakes. In Schagerl, M. (ed.), Soda Lakes of East Africa. Springer Publishers, Switzerland: 205–226.

    Chapter  Google Scholar 

  • Methé, B. A., W. D. Hiorns & J. P. Zehr, 1998. Contrasts between marine and freshwater bacterial community composition: analyses of communities in Lake George and six other Adirondack lakes. Limnology and Oceanography 43: 368–374.

    Article  Google Scholar 

  • Muyzer, G., E. C. de Waal & A. G. Uitterlinden, 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied Environmental Microbiology 59: 695–700.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mwirichia, R., S. Cousin, A. W. Muigai, H. I. Boga & E. Stackebrandt, 2011. Bacterial diversity in the haloalkaline Lake Elmenteita, Kenya. Current Microbiology 62: 209–221.

    Article  CAS  PubMed  Google Scholar 

  • Myshrall, K. L., J. M. Mobberley, S. J. Green, P. T. Visscher, S. A. Havemann, R. P. Reid & J. S. Foster, 2010. Biogeochemical cycling and microbial diversity in the thrombolytic microbialites of Highborne Cay, Bahamas. Geobiology 8: 337–354.

    Article  CAS  PubMed  Google Scholar 

  • Nakov, T., E. C. Ruck, Y. Galachyants, S. A. Spaulding & E. C. Theriot, 2014. Molecular phylogeny of the Cymbellales (Bacillariophyceae, Heterokontophyta) with a comparison of models for accommodating rate variation across sites. Phycologia 53: 359–373.

    Article  Google Scholar 

  • Nikouli, E., K. A. Kormas, P. Berillis, H. Karayanni & M. Moustaka-Gouni, 2013. Harmful and parasitic unicellular eukaryotes persist in a shallow lake under reconstruction (L. Karla, Greece). Hydrobiologia 718: 73–83.

    Article  Google Scholar 

  • Nübel, U., F. Garcia-Pichel & G. Muyzer, 1997. PCR primers to amplify 16S rRNA genes from cyanobacteria. Applied Environmental Microbiology 63: 3327–3332.

    PubMed  PubMed Central  Google Scholar 

  • Oduor, S. O. & M. Schagerl, 2007. Phytoplankton photosynthetic characteristics in three Kenyan Rift Valley saline-alkaline lakes. Journal of Plankton Research 29: 1041–1050.

    Article  CAS  Google Scholar 

  • Oikonomou, A., M. Katsiapi, H. Karayanni, M. Moustaka-Gouni & K. A. Kormas, 2012. Plankton microorganisms coinciding with two consecutive mass fish kills in a newly reconstructed lake. ScientificWorld Journal 2012: 504135.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ong’ondo, G. O., A. W. Yasindi, S. O. Oduor, S. Jost, M. Schagerl, P. Sonntag & J. Boenigk, 2013. Ecology and community structure of ciliated protists in two alkaline-saline Rift Valley lakes in Kenya with special emphasis on Frontonia. Journal of Plankton Research 35: 759–771.

    Article  Google Scholar 

  • Opticount, 2008. [available on http://science.do-mix.de/software_opticount.php].

  • Orr, R. J., S. A. Murray, A. Stuken, L. Rhodes & K. S. Jakobsen, 2012. When naked became armored: an eight-gene phylogeny reveals monophyletic origin of theca in dinoflagellates. PLoS One 7: E50004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peduzzi, P., M. Gruber, M. Gruber & M. Schagerl, 2014. The virus’s tooth – cyanophages affect the flamingo population of an African soda lake in a bottom up cascade. The ISME Journal 8: 1346–1351.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quast, C., E. Pruesse, P. Yilmaz, J. Gerken, T. Schweer, P. Yarza, J. Peplies & F. O. Glöckner, 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41: 590–596.

    Article  CAS  Google Scholar 

  • Rees, H. C., W. D. Grant, B. E. Jones & S. Heaphy, 2004. Diversity of Kenyan soda lake alkaliphiles assessed by molecular methods. Extremophiles 8: 63–71.

    Article  CAS  PubMed  Google Scholar 

  • Rossi, A., V. Boscaro, D. Carducci, V. Serra, L. Modeo, F. Verni, S. I. Fokin & G. Petroni, 2016. Ciliate communities and hidden biodiversity in freshwater biotopes of the Pistoia province (Tuscany, Italy). European Journal of Protistology 53: 11–19.

    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 

  • Schagerl, M. & R. W. Renaut, 2016. Dipping into soda lakes of East Afrika. In Schagerl, M. (ed.), Soda Lakes of East Africa. Springer, Berlin: 3–24.

    Chapter  Google Scholar 

  • Schagerl, M. & A. Burian, 2016. The ecology of African soda lakes: driven by variable and extreme conditions. In Schagerl, M. (ed.), Soda Lakes of East Africa. Springer, Berlin: 295–320.

    Chapter  Google Scholar 

  • Schloss, P. D., D. Gevers & S. L. Westcott, 2011. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-Based Studies. PLoS One 6: e27310. doi:10.1371/journal.pone.0027310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnepf, E. & M. Elbrächter, 1992. Nutritional strategies in dinoflagellates. A review with emphasis on cell biological aspects. European Journal of Protistology 28: 3–24.

    CAS  PubMed  Google Scholar 

  • Sekiguchi, Y., T. Yamada, S. Hanada, A. Ohashi, H. Harada & Y. Kamagata, 2003. Anaerolinea thermophila gen. nov., sp. nov. and Caldilinea aerophila gen. nov., sp. nov., novel filamentous thermophiles that represent a previously uncultured lineage of the domain Bacteria at the subphylum level. International Journal of Systematic and Evolutionary Microbiology 53: 1843–1851.

    Article  CAS  PubMed  Google Scholar 

  • Skovgaard, A. & E. Saiz, 2006. Seasonal occurrence and role of protistan parasites in coastal marine zooplankton. Marine Ecology Progress Series 327: 37–49.

    Article  Google Scholar 

  • Slapeta, J., D. Moreira & P. Lopez-Garcia, 2005. The extent of protist diversity: insights from molecular ecology of freshwater eukaryotes. Proceedings of the Royal Society of London, B Biological Sciences 272: 2073–2081.

    Article  CAS  Google Scholar 

  • Sorokin, D. Y., T. Berben, E. D. Melton, L. Overmars, C. D. Vavourakis & G. Muyzer, 2014. Microbial diversity and biogeochemical cycling in soda lakes. Extremophiles 18: 791–809.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stoddard, S. F., B. J. Smith, R. Hein, B. R. K. Roller & T. M. Schmidt, 2015. rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Research 43: D593–D598.

    Article  PubMed  Google Scholar 

  • Uphoff, H. U., A. Felske, W. Fehr & I. Wagner-Dobler, 2001. The microbial diversity in picoplankton enrichment cultures: a molecular screening of marine isolates. FEMS Microbiology Ecology 35: 249–258.

    Article  CAS  PubMed  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., 1978. The ecology of Lake Nakuru (Kenya) I. Abundance and feeding of the Lesser Flamingo. Oecologia 32: 11–35.

    Article  Google Scholar 

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

    Google Scholar 

  • Verschuren, D., 2003. Lake-based climate reconstruction in Africa: progress and challenges. Hydrobiologia 500: 315–330.

    Article  Google Scholar 

  • Verschuren, D., J. Tibby, P. R. Leavitt & C. N. Roberts, 1999. The environmental history of a climate-sensitive lake in the former White Highlands” of Central Kenya. Ambio 28: 494–501.

    Google Scholar 

  • Verschuren, D., J. Tibby, K. Sabbe & N. Roberts, 2000. Effects of depth, salinity, and substrate on the invertebrate community of a fluctuating tropical lake. Ecology 81: 164–182.

    Article  Google Scholar 

  • Vilela, R., J. E. Martins, C. N. Pereira, N. Melo & L. Mendoza, 2007. Molecular study of archival fungal strains isolated from cases of lacaziosis (Jorge Lobo’s disease). Mycoses 50: 470–474.

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Woese, C. R., E. Stackebrandt, T. J. Macke & G. E. Fox, 1985. A phylogenetic definition of the major eubacterial taxa. Systematic and Applied Microbiology 6: 143–151.

    Article  CAS  PubMed  Google Scholar 

  • Wood, R. B. & J. F. Talling, 1988. Chemical and algal relationships in a salinity series of Ethiopian inland waters. Hydrobiologia 158: 29–67.

    Article  CAS  Google Scholar 

  • Wu, Q. L., G. Zwart, M. Schauer, M. P. Kamst-van Agterveld & M. W. Hahn, 2006. Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan Plateau, China. Applied Environmental Microbiology 72: 5478–5485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasindi, A. W. & W. T. Tailor, 2016. The protozoa of Soda Lakes in East Africa. In Schagerl, M. (ed.), Soda Lakes of East Africa. Springer, Berlin: 179–204.

    Chapter  Google Scholar 

  • Yasindi, A. W., W. T. Taylor & D. H. Lynn, 2007. The community composition and biomass of pelagic ciliated protozoa in East African lakes. African Journal of Aquatic Science 32: 175–183.

    Article  Google Scholar 

  • Ye, T., H. Cai, X. Liu & H. L. Jiang, 2016. Dominance of Oscillospira and Bacteroides in the bacterial community associated with the degradation of high-concentration dimethyl sulfide under iron-reducing condition. Annals of Microbiology. doi:10.1007/s13213-016-1207-5.

    Google Scholar 

  • Zinabu, G.-M. & W. D. Taylor, 1997. Bacteria-chlorophyll relationships in Ethiopian lakes of varying salinity: are soda lakes different? Journal of Plankton Research 19: 647–654.

    Article  Google Scholar 

  • Zwart, G., M. P. Kamst-van Agterveld, I. van der Werff-Staverman, F. Hagen, H. L. Hoogveld & H. J. Gons, 2005. Molecular characterization of cyanobacterial diversity in a shallow eutrophic lake. Environmental Microbiology 7: 365–377.

    Article  CAS  PubMed  Google Scholar 

Download references

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 financial support of the State High-Tech Research and Development Project (863) of the Ministry of Science and Technology of China (2012AA021706, 2013AA065805), the National Natural Science Foundation of China (No. 41376191) and State Key Laboratory of Microbial Metabolism of Shanghai Jiao Tong University (MMLKF16-10).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lothar Krienitz.

Additional information

Handling editor: Luigi Naselli-Flores

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, W., Li, H., Kotut, K. et al. Molecular diversity of plankton in a tropical crater lake switching from hyposaline to subsaline conditions: Lake Oloidien, Kenya. Hydrobiologia 788, 205–229 (2017). https://doi.org/10.1007/s10750-016-2998-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-2998-x

Keywords

Navigation