Advertisement

Hydrobiologia

, Volume 659, Issue 1, pp 5–22 | Cite as

Hidden diversity among aquatic heterotrophic flagellates: ecological potentials of zoosporic fungi

  • Télesphore Sime-Ngando
  • Emilie Lefèvre
  • Frank H. Gleason
DISREGARDED DIVERSITY AND ECOLOGICAL POTENTIALS

Abstract

Since the emergence of the ‘microbial loop’ concept, heterotrophic flagellates have received particular attention as grazers in aquatic ecosystems. These microbes have historically been regarded incorrectly as a homogeneous group of bacterivorous protists in aquatic systems. More recently, environmental rDNA surveys of small heterotrophic flagellates in the pelagic zone of freshwater ecosystems have provided new insights. (i) The dominant phyla found by molecular studies differed significantly from those known from morphological studies with the light microscope, (ii) the retrieved phylotypes generally belong to well-established eukaryotic clades, but there is a very large diversity within these clades and (iii) a substantial part of the retrieved sequences cannot be assigned to bacterivorous but can be assigned instead to parasitic and saprophytic organisms, such as zoosporic true fungi (chytrids), fungus-like organisms (stramenopiles), or virulent alveolate parasites (Perkinsozoa and Amoebophrya sp.). All these microorganisms are able to produce small zoospores to assure dispersal in water during their life-cycles. Based on the existing literature on true fungi and fungus-like organisms, and on the more recently published eukaryotic rDNA environmental studies and morphological observations, we conclude that previously overlooked microbial diversity and related ecological potentials require intensive investigation (i) for an improved understanding of the roles of heterotrophic flagellates in pelagic ecosystems and (ii) to properly integrate the concept of ‘the microbial loop’ into modern pelagic microbial ecology.

Keywords

Aquatic systems Microbial diversity Heterotrophic flagellates Zoosporic fungi Food web dynamics 

Notes

Acknowledgements

EL was supported by a PhD Fellowship from the French Ministère de la Recherche et de la Technologie (MRT). This study was supported by a grant from the French ANR Programme Blanc DREP (Diversité et Rôles des Eumycètes dans le Pélagos, Cordinator TSN). The content was part of EL PhD dissertation and was presented as oral contribution to the topical session # 011 (Missing, Rare and Wrongfully Regarded Microbial Diversity in Aquatic Systems) of ASLO (Advancing the Science of Limnology and Oceanography) 2009 aquatic science meeting held at Nice, France (http://aslo.org/nice2009/topical_sessions.html).

References

  1. Adrian, R. & B. Schneider-Olt, 1999. Top-down effects of crustacean zooplankton on pelagic microorganisms in a mesotrophic lake. Journal of Plankton Research 21: 2175–2190.CrossRefGoogle Scholar
  2. Adrian, R., S. A. Wickham & N. M. Butler, 2001. Trophic interaction between zooplankton and the microbial community in contrasting food webs: the epilimnion and deep chlorophyll maximum of a mesotrophic lake. Aquatic Microbial Ecology 24: 83–97.CrossRefGoogle Scholar
  3. Amann, R. & W. Ludwig, 2000. Ribosomal RNA-targeted nucleic acid probes for studies in microbial ecology. FEMS Microbiology Reviews 24: 555–565.PubMedCrossRefGoogle Scholar
  4. Amann, R. I., W. Ludwig & K.-H. Schleifer, 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiological Reviews 59: 143–169.PubMedGoogle Scholar
  5. Amaral Zettler, L. A., F. Gomez, E. Zettler, B. G. Keenan, R. Amils & M. L. Sogin, 2002. Eukaryotic diversity in Spain’s River of Fire. Nature 417: 137.PubMedCrossRefGoogle Scholar
  6. Arndt, H., 1993. Rotifers as predators on components of the microbial web (bacteria, heterotrophic flagellates, ciliates)—a review. Hydrobiologia 255(256): 231–246.CrossRefGoogle Scholar
  7. Arndt, H., D. Dietrich, B. Auer, E. J. Cleven, T. Gräfenhan, M. Weitere & A. P. Myl’nikov, 2000. Functional diversity of heterotrophic flagellates in aquatic ecosystems. In Leadbeater, B. S. C. & J. C. Green (eds), The Flagellates: Unity, Diversity and Evolution. Taylor & Francis, London, UK: 240–268.Google Scholar
  8. Auer, B. & H. Arndt, 2001. Taxonomic composition and biomass of heterotrophic flagellates in relation to lake trophy and season. Freshwater Biology 46: 959–972.CrossRefGoogle Scholar
  9. Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil & F. Thingstad, 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10: 257–263.CrossRefGoogle Scholar
  10. Bärlocher, F., 1985. The role of fungi in the nutrition of stream invertebrates. Botanical Journal of the Linnean Society 91: 83–94.CrossRefGoogle Scholar
  11. Barr, D. J. S., 2001. Chytridiomycota. In McLaughlin, D. J., E. G. McLaughlin & P. A. Lemke (eds), The Mycota, Systematics and Evolution Part A. Springer-Verlag, New-York: 93–112.Google Scholar
  12. Barr, D. J. S. & C. J. Hickman, 1967. Chytrids and algae I: host-substrate range, and morphological variation of species of Rhizophydium. Canadian Journal of Botany 45: 423–430.CrossRefGoogle Scholar
  13. Barron, G. L., 2004. Fungal parasites and predators of rotifers, nematodes, and other invertebrates. In Mueller, G. M., G. F. Bills & M. S. Foster (eds), Biodiversity of Fungi, Inventory and Monitoring Methods. Elsevier Academic Press, Amsterdam: 435–450.Google Scholar
  14. Bec, A., C. Desvillettes, A. Vera, C. Lemarchand, D. Fontvieille & G. Bourdier, 2003. Nutritional quality of freshwater heterotrophic flagellates: trophic upgrading of its microalgal diet for Daphnia. Aquatic Microbial Ecology 32: 203–207.CrossRefGoogle Scholar
  15. Bec, A., D. Martin-Creuzburg & E. von Elert, 2006. Trophic upgrading of autotrophic picoplankton by the heterotrophic nanoflagellate Paraphysomonas sp. Limnology and Oceanography 51: 1699–1707.CrossRefGoogle Scholar
  16. Bennett, S. J., R. W. Sanders & K. G. Porter, 1990. Heterotrophic, autotrophic, and mixotrophic nanoflagellates: seasonal abundances and bacterivory in a eutrophic lake. Limnology and Oceanography 35: 1821–1832.CrossRefGoogle Scholar
  17. Berney, C., J. Fahrni & J. Pawlowski, 2004. How many novel eukaryotic ‘kingdoms’? Pitfalls and limitations of environmental DNA surveys. BMC Biology 2: 1–13.CrossRefGoogle Scholar
  18. Berninger, U. G., B. J. Finlay & P. Kuuppo-Leiniki, 1991. Protozoan control of bacterial abundances in freshwater. Limnology and Oceanography 36: 139–147.CrossRefGoogle Scholar
  19. Bettarel, Y., T. Sime-Ngando, M. Bouvy, R. Arfi & C. Amblard, 2005. Low consumption of virus-sized particles by heterotrophic nanoflagellates in two lakes of the French Massif Central. Aquatic Microbial Ecology 39: 205–209.CrossRefGoogle Scholar
  20. Bloem, J. & M.-J. B. Bar-Gilissen, 1989. Bacterial activity and protozoan grazing potential in a stratified lake. Limnology and Oceanography 34: 297–309.CrossRefGoogle Scholar
  21. Boenigk, J. & H. Arndt, 2002. Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Antonie van Leeuwenhoek 81: 465–480.PubMedCrossRefGoogle Scholar
  22. Boenigk, J., K. Pfandi, P. Stadler & A. Chatzinotas, 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. Environmental Microbiology 7: 685–697.PubMedCrossRefGoogle Scholar
  23. Bundy, M. H., H. A. Vanderploeg, P. J. Lavrentyev & P. A. Kovalcik, 2005. The importance of microzooplankton versus phytoplankton to copepod populations during late winter and early spring in Lake Michigan. Canadian Journal of Fisheries and Aquatic Sciences 62: 2371–2385.CrossRefGoogle Scholar
  24. Burreson, E. M., K. S. Reece & C. F. Dungan, 2005. Molecular, morphological, and experimental evidence support the synonymy of Perkinsus chesapeaki and Perkinsus andrewsi. The Journal of Eukaryotic Microbiology 52: 258–270.PubMedCrossRefGoogle Scholar
  25. Callieri, C. & J. G. Stockner, 2002. Freshwater autotrophic picoplankton: a review. Journal of Limnology 61: 1–14.Google Scholar
  26. Canter, H. M., 1950. Studies on British chytrids. VIII. On Rhizophidium anomalum n. sp. New Phytologist 49: 98–102.CrossRefGoogle Scholar
  27. Canter, H. M. & J. W. G. Lund, 1948. Studies on plankton parasites. I. Fluctuations in the numbers of Asterionella formosa Hass in relation to fungal epidemics. New Phytologist 47: 238–396.CrossRefGoogle Scholar
  28. Canter, H. M. & J. W. G. Lund, 1951. Studies on plankton parasites. III. Examples of the interaction between parasitism and other factors determining the growth of diatoms. Annals of Botany 15: 359–371.Google Scholar
  29. Caron, D. A., 1983. Technique for enumeration of heterotrophic and phototrophic nanoplankton, using epifluorescence microscopy, and comparison with other procedures. Applied and Environmental Microbiology 46: 491–498.PubMedGoogle Scholar
  30. Caron, D. A., 1991. Evolving role of protozoa in aquatic nutrient cycles. In Reid, P. C., C. M. Turley & P. H. Burkhill (eds), Protozoa and their Role in Marine Processes. Springer-Verlag, Berlin: 387–415.Google Scholar
  31. Caron, D. A., 1994. Inorganic nutrients, bacteria, and the microbial loop. Microbial Ecology 28: 295–298.CrossRefGoogle Scholar
  32. Carrias, J.-F., C. Amblard & G. Bourdier, 1996. Protistan bacterivory in an oligomesotrophic lake: importance of attached ciliates and flagellates. Microbial Ecology 31: 249–268.PubMedCrossRefGoogle Scholar
  33. Carrias, J. F., C. Quiblier-Lloberas & G. Bourdier, 1998. Seasonal dynamics of free and attached heterotrophic nanoflagellates in an oligomesotrophic lake. Freshwater Biology 39: 91–101.CrossRefGoogle Scholar
  34. Carrias, J. F., A. Thouvenot, C. Amblard & T. Sime-Ngando, 2001. Dynamics and growth estimates of planktonic protists during early spring in Lake Pavin, France. Aquatic Microbial Ecology 24: 163–174.CrossRefGoogle Scholar
  35. Carrick, H. J. & G. L. Fahnenstiel, 1989. Biomass, size structure, and composition of phototrophic and heterotrophic nanoflagellate communities in Lakes Huron and Michigan. Canadian Journal of Fisheries and Aquatic Sciences 46: 1922–1928.CrossRefGoogle Scholar
  36. Cavalier-Smith, T. & E. E. Chao, 2003. Phylogeny and classification of phylum Cercozoa (Protozoa). Protist 154: 341–358.PubMedCrossRefGoogle Scholar
  37. Chapman, H. C., 1985. Ecology and use of Coelomomyces species in biological control: a review. In Couch, J. N. & C. E. Bland (eds), The Genus Coelomomyces. Academic Press Inc, New York: 361–368.Google Scholar
  38. Chaput, O. & J. F. Carrias, 2002. Effects of commonly used fixatives on size parameters of freshwater planktonic protists. Archiv für Hydrobiologie 155: 517–526.Google Scholar
  39. Choi, J. W. & D. K. Stoecker, 1989. Effects of fixation on cell volume of marine planktonic protozoa. Applied and Environmental Microbiology 55: 1761–1765.PubMedGoogle Scholar
  40. Christoffersen, K. & J. M. Gonzalez, 2003. An approach to measure ciliates grazing on living heterotrophic nanoflagellates. Hydrobiologia 491: 159–166.CrossRefGoogle Scholar
  41. Cleven, E. J., 1996. Indirectly fluorescently labelled flagellates (IFLF): a tool to estimate the predation on free-living heterotrophic flagellates. Journal of Plankton Research 18: 429–442.CrossRefGoogle Scholar
  42. Cleven, E. J. & T. Weisse, 2001. Seasonal succession and taxon-specific bacterial grazing rates of heterotrophic nanoflagellates in Lake Constance. Aquatic Microbial Ecology 23: 147–161.CrossRefGoogle Scholar
  43. Coats, D. W., E. J. Adam, C. L. Gallegos & S. Hedrick, 1996. Parasitism of photosynthetic dinoflagellates in a shallow subestuary of Chesapeake Bay, USA. Aquatic Microbial Ecology 11: 1–9.CrossRefGoogle Scholar
  44. Comte, J., S. Jacquet, S. Viboud, D. Fontvieille, A. Millery, G. Paolini & I. Domaizon, 2004. Microbial community structure and dynamics in the largest natural French lake (Lake Bourget). Microbial Ecology 52: 72–89.CrossRefGoogle Scholar
  45. Coulter, D. B. & J. M. Aronson, 1977. Glycogen structure and utilization in Allomyces macrogynus. Experimental Mycology 1: 183–193.CrossRefGoogle Scholar
  46. Dawson, S. C. & N. R. Pace, 2002. Novel Kingdom-level eukaryotic diversity in anoxic environments. Proceedings of the National Academy of Sciences 99: 8324–8329.Google Scholar
  47. De Bruin, A., 2006. The potential for coevolution in aquatic host-parasite system. PhD thesis, Netherlands Institute of Ecology of the Royal Academy of arts and Sciences (NIOO-KNAW).Google Scholar
  48. Degans, H., E. Zöllner, K. Van der Gucht, L. De Meester & K. Jürgens, 2002. Rapid Daphnia-mediated changes in microbial community structure: an experimental study. FEMS Microbiology Ecology 42: 137–149.PubMedCrossRefGoogle Scholar
  49. Desvilettes, C. & A. Bec, 2009. Formation and transfer of fatty acids in aquatic microbial food webs—role of heterotrophic protists. In Arts, M. T., M. Brett & M. Kainz (eds), Lipids in Aquatic Ecosystems. Springer, New York: 25–42.CrossRefGoogle Scholar
  50. Dick, M. W., 2003. The Peronosporales and other flagellate fungi. In Howard, D. H. (ed.), Pathogenic Fungi in Humans and Animals, 2nd ed. Marcel Dekker Inc, New York: 17–66.Google Scholar
  51. Diez, B., C. Pedros-Alio & R. Massana, 2001. Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Applied and Environmental Microbiology 67: 2932–2941.PubMedCrossRefGoogle Scholar
  52. Digby, A. L., F. H. Gleason & P. A. McGee, 2010. Some fungi in the Chytridiomycota can assimilate both inorganic and organic sources of nitrogen. Fungal Ecology. doi: 10.1016/j.funeco.2009.11.002.
  53. Dolan, J. R. & C. L. Gallegos, 1991. Trophic coupling of rotifers, microflagellates, and bacteria during fall months in the Rhode River Estuary. Marine Ecology Progress Series 77: 147–156.CrossRefGoogle Scholar
  54. Domaizon, I., S. Viboud & D. Fontvieille, 2003. Taxon-specific and seasonal variations in flagellate grazing on heterotrophic bacteria in the oligotrophic Lake Annecy—importance of mixotrophy. FEMS Microbiology Ecology 46: 317–329.PubMedCrossRefGoogle Scholar
  55. Dorigo, U., L. Volatier & J.-F. Humbert, 2005. Molecular approaches to the assessment of biodiversity in aquatic microbial communities. Water Research 39: 2207–2218.PubMedCrossRefGoogle Scholar
  56. Eccleston-Parry, J. D. & B. S. C. Leadbeater, 1995. Regeneration of phosphorus and nitrogen by four species of heterotrophic nanoflagellates feeding on three nutritional states of a single bacterial strain. Applied and Environmental Microbiology 61: 1033–1038.PubMedGoogle Scholar
  57. Edgcomb, V. P., D. T. Kysela, A. Teske, A. de Vera Gomez & M. L. Sogin, 2002. Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proceedings of the National Academy of Sciences 99: 7658–7662.Google Scholar
  58. Fenchel, T., 1982. Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Marine Ecology Progress Series 8: 225–231.CrossRefGoogle Scholar
  59. Fenton, A. & M. A. Brockhurst, 2008. The role of specialist parasites in structuring host communities. Ecological Research 23: 795–804.CrossRefGoogle Scholar
  60. Freeman K. R., A. P. Martin, D. Karki, R. C. Lynch, M. S. Mitter, A. F. Meyer, J. E. Longcore, D. R. Simmons & S. K. Schmidt, 2009. Evidence that chytrids dominate fungal communities in high-elevation soils. Proceedings of the National Academy of Sciences 106: 18315–18320.Google Scholar
  61. Fukami, K., N. Murata, Y. Morio & T. Nishijima, 1996. Distribution of heterotrophic nanoflagellates and their importance as the bacterial consumer in a eutrophic coastal seawater. Journal of Oceanography 52: 399–407.CrossRefGoogle Scholar
  62. Gachon, C. M. M., M. Strittmatter, D. G. Müller, J. Kleinteich & F. C. Küpper, 2009. Differential host susceptibility to the marine oomycete pathogen Eurychasma dicksonii detected by real-time PCR: not all algae are equal. Applied and Environmental Microbiology 75: 322–328.PubMedCrossRefGoogle Scholar
  63. Gasol, J. M. & D. Vaqué, 1993. Lack of coupling between heterotrophic nanoflagellates and bacteria: a general phenomenon across aquatic systems? Limnology and Oceanography 38: 657–665.CrossRefGoogle Scholar
  64. Gasol, J. M., A. M. Simons & J. Kalff, 1995. Patterns in the top-down versus bottom-up regulation of heterotrophic nanoflagellates in temperate lakes. Journal of Plankton Research 17: 1879–1905.CrossRefGoogle Scholar
  65. Gestal, C., B. Novoa, D. Posada, A. Figueras & C. Azevedo, 2006. Perkinsoide chabelardi n. gen., a protozoan parasite with an intermediate evolutionary position: possible cause of the decrease of sardine fisheries? Environmental Microbiology 8: 1105–1114.PubMedCrossRefGoogle Scholar
  66. Gleason, F. H., M. Kagami, E. Lefèvre & T. Sime-Ngando, 2008. The ecology of chytrids in aquatic ecosystems: roles in food web dynamics. Fungal Biology Reviews 22: 17–25.CrossRefGoogle Scholar
  67. Gleason, F. H., M. Kagami, A. V. Marano & T. Sime-Ngando, 2009. Fungal zoospores are valuable food resources in aquatic ecosystems. Inoculum 60: 1–3.Google Scholar
  68. Graham, J. M., 1991. Symposium introductory remarks: a brief history of aquatic microbial ecology. Journal of Protozoology 38: 66–69.Google Scholar
  69. Gutman, J., A. Zarka & S. Boussiba, 2009. The host-range of Paraphysoderma sedebokerensis a chytrid that infects Haematococcus pluvialis. European Journal of Phycology 44: 509–514.CrossRefGoogle Scholar
  70. Hahn, M. W. & M. G. Höfle, 2001. Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiology Ecology 35: 113–121.PubMedCrossRefGoogle Scholar
  71. Hartmann, H. J., T. Hassan, L. Aleya & N. Lair, 1993. Predation on ciliates by suspension-feeding calanoid copepod Acanthodiaptomus denticornis. Canadian Journal of Fisheries and Aquatic Sciences 50: 1382–1393.CrossRefGoogle Scholar
  72. Hobbie, J. E., R. J. Daley & S. Jasper, 1977. Use of nucleopore filter for counting bacteria by epifluorescence microscopy. Applied and Environmental Microbiology 33: 1225–1228.PubMedGoogle Scholar
  73. Holben, W. E. & J. M. Tiedje, 1988. Applications of nucleic acid hybridization in microbial ecology. Ecology 69: 561–568.CrossRefGoogle Scholar
  74. Holen, D. A. & M. Boraas, 1991. The feeding behavior of Spumella sp. as a function of particle size: implications for bacterial size in pelagic systems. Hydrobiologia 220: 73–88.CrossRefGoogle Scholar
  75. Holfeld, H., 1998. Fungal infections of the phytoplankton: seasonality, minimal host density, and specificity in a mesotrophic lake. New Phytologist 138: 507–517.CrossRefGoogle Scholar
  76. Hudson, J. J., W. D. Taylor & D. W. Schindler, 1999. Planktonic nutrient regeneration and cycling efficiency in temperate lakes. Nature 400: 659–661.CrossRefGoogle Scholar
  77. Hudson, P. J., A. P. Dobson & K. D. Lafferty, 2006. Is a healthy ecosystem one that is rich in parasites? Trends in Ecology & Evolution 21: 381–385.CrossRefGoogle Scholar
  78. Hwang, S.-J. & R. T. Heath, 1997. The distribution of protozoa across a trophic gradient: factors controlling their abundance and importance in the plankton food web. Journal of Plankton Research 19: 491–518.CrossRefGoogle Scholar
  79. Ibelings, B. W., A. De Bruin, M. Kagami, M. Rijkeboer, M. Brehm & E. Van Donk, 2004. Host parasite interactions between freshwater phytoplankton and chytrid fungi (Chytridiomycota). Journal of Phycology 40: 437–453.CrossRefGoogle Scholar
  80. James, T. Y., D. Porter, C. A. Leander, R. Vilgalys & J. E. Longcore, 2000. Molecular phylogenetics of the Chytridiomycota supports the utility of ultrastructural data in chytrid systematics. Canadian Journal of Botany 78: 336–350.CrossRefGoogle Scholar
  81. James, Y. T., P. M. Letcher, J. E. Longcore, S. E. Mozley-Standridge, M. J. Powell, G. W. Griffith & R. Vilgalys, 2006. A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98: 860–871.PubMedCrossRefGoogle Scholar
  82. Johnson, P. T. J., J. E. Longcore, D. E. Stanton, R. B. Carnegie, J. D. Shields & E. R. Preu, 2006. Chytrid infections of Daphnia pulicaria: development, ecology, pathology and phylogeny of Polycaryum laeve. Freshwater Biology 51: 634–648.CrossRefGoogle Scholar
  83. Jürgens, K. & H. Güde, 1991. Seasonal changes in the grazing impact of phagotrophic flagellates on bacteria in Lake Constance. Marine Microbial Food Webs 5: 27–37.Google Scholar
  84. Jürgens, K. & E. Jeppesen, 2000. The impact of metazooplankton on the structure of the microbial food web in a shallow, hypertrophic lake. Journal of Plankton Research 22: 1047–1070.CrossRefGoogle Scholar
  85. Jürgens, K. & G. Stolpe, 1995. Seasonal dynamics of crustacean zooplankton, heterotrophic nanoflagellates and bacteria in a shallow, eutrophic lake. Freshwater Biology 33: 27–38.CrossRefGoogle Scholar
  86. Jürgens, K., S. A. Wickham, K. O. Rothhaupt & B. Santer, 1996. Feeding rates of macro- and microzooplankton on heterotrophic nanoflagellates. Limnology and Oceanography 41: 1833–1839.CrossRefGoogle Scholar
  87. Kagami, M., E. Van Donk, A. De Bruin, M. Rijkeboer & B. W. Ibelings, 2004. Daphnia can protect diatoms from fungal parasitism. Limnology and Oceanography 49: 680–685.CrossRefGoogle Scholar
  88. Kagami, M., A. de Bruin, B. W. Ibelings & E. van Donk, 2007. Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 578: 113–129.CrossRefGoogle Scholar
  89. Karling, J. S., 1977. Chytridiomycetarum iconographia. J. Cramer, Montecello, NY.Google Scholar
  90. Kisand, V. & P. Zingel, 2000. Dominance of ciliate grazing on bacteria during spring in a shallow eutrophic lake. Aquatic Microbial Ecology 22: 135–142.CrossRefGoogle Scholar
  91. Koch, W. J., 1968. Studies on motile cells of chytrids. IV. Planonts in the experimental taxonomy of aquatic phycomycetes. Journal of the Elisha Mitchell Scientific Society 84: 69–83.Google Scholar
  92. Koob, D. B., 1966. Parasitism of Asterionella formosa Hass by a chytrid in two lakes of Rawah wild area of Colorado. Journal of Phycology 2:41–45. 433.Google Scholar
  93. Köthe, A. & J. Benndorf, 1994. Top-down impact of Daphnia galeata on pelagic heterotrophic flagellates in a whole-lake biomanipulation experiment. Marine Microbial Food Webs 8: 325–335.Google Scholar
  94. Kudoh, S. & M. Takahashi, 1990. Fungal control of population changes of the planktonic diatom Asterionella formosa in a shallow eutrophic lake. Journal of Phycology 26: 239–244.CrossRefGoogle Scholar
  95. Laferty, K. D. & A. M. Kuris, 2009. Parasites reduce food web robustness because they are sensitive to secondary extinction as illustrated by an invasive estuarine snail. Philosophical Transactions of the Royal Society B: Biological Sciences 364: 1659–1663.CrossRefGoogle Scholar
  96. Landry, M. R. & A. Calbet, 2004. Microzooplankton production in the oceans. ICES Journal of Marine Science 61: 501–507.CrossRefGoogle Scholar
  97. Lavrentyev, P. J., W. S. Gardner & J. R. Johnson, 1997. Cascading trophic effects on aquatic nitrification: experimental evidence and potential implications. Aquatic Microbial Ecology 13: 161–175.CrossRefGoogle Scholar
  98. Lawley, B., S. Ripley, P. Bridge & P. Convey, 2004. Molecular analysis of geographic patterns of eukaryotic diversity in Antarctic soils. Applied and Environmental Microbiology 70: 5963–5972.PubMedCrossRefGoogle Scholar
  99. Laybourn-Parry, J. & M. Walton, 1998. Seasonal heterotrophic flagellate and bacterial plankton dynamics in a large oligotrophic lake—Loch Ness, Scotland. Freshwater Biology 39: 1–8.CrossRefGoogle Scholar
  100. Laybourn-Parry, J., J. C. Elis-Evans & P. Bayliss, 1995. The dynamics of heterotrophic nanoflagellates and bacterioplankton in a large ultra-oligotrophic Antarctic lake. Journal of Plankton Research 17: 1835–1850.CrossRefGoogle Scholar
  101. Lee, W. J. & D. J. Patterson, 1998. Diversity and geographic distribution of free-living heterotrophic flagellates—analysis by PRIMER. Protist 149: 229–244.CrossRefGoogle Scholar
  102. Lee, W. J., A. G. B. Simpson & D. J. Patterson, 2005. Free-living heterotrophic flagellates from freshwater sites in Tasmania (Australia), a field survey. Acta Protozoologica 44: 321–350.Google Scholar
  103. Lefèvre, E., C. Bardot, C. Noel, J. F. Carrias, E. Viscogliosi, C. Amblard & T. Sime-Ngando, 2007. Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environmental Microbiology 9: 61–71.PubMedCrossRefGoogle Scholar
  104. 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.PubMedCrossRefGoogle Scholar
  105. Lefranc, M., A. Thénot, C. Lepère & D. Debroas, 2005. Genetic diversity of small eukaryotes in lakes differing by their trophic status. Applied and Environmental Microbiology 71: 5935–5942.PubMedCrossRefGoogle Scholar
  106. Lepère, C., I. Domaizon & D. Debroas, 2008. Unexpected importance of potential parasites in the composition of the freshwater small-eukaryote community. Applied and Environmental Microbiology 74: 2940–2949.PubMedCrossRefGoogle Scholar
  107. Lim, E. L., M. R. Dennett & D. A. Caron, 1999. The ecology of Paraphysomonas imperforata based on studies employing oligonucleotide probe identification in coastal water samples and enrichment cultures. Limnology and Oceanography 44: 37–51.CrossRefGoogle Scholar
  108. Lopez-Garcia, P., H. Philippe, F. Gail & D. Moreira, 2003. Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge. Proceedings of the National Academy of Sciences 100: 697–702.Google Scholar
  109. Lopez-Garcia, P., F. Rodriguez-Valera, C. Pedros-Alio & D. Moreira, 2001. Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603–607.PubMedCrossRefGoogle Scholar
  110. Marano, A. V., C. L. A. Pires-Zottarelli, M. D. Barreta, M. M. Steciow & F. H. Gleason, 2010. Diversity, role in decomposition, and succession of zoosporic fungi and straminipiles on submerged decaying leaves in a woodland stream. Hydrobiologia. doi: 10.1007/s10750-009-0006-4.
  111. Marcogliese, D. J. & D. K. Cone, 1997. Food web: a plea for parasites. Trends in Ecology & Evolution 12: 320–325.CrossRefGoogle Scholar
  112. Martin, W. W., 1984. The dynamics of aquatic fungi parasites in a stream population of the midge, Chironomus attenuatus. Journal of Invertebrate Pathology 44: 36–45.CrossRefGoogle Scholar
  113. Massana, R., L. Guillou, B. Diez & C. Pedros-Alios, 2002. Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Applied and Environmental Microbiology 68: 4554–4558.PubMedCrossRefGoogle Scholar
  114. Massana, R., V. Balagué, L. Guillou & C. Pedros-alio, 2004. Picoeukaryotic diversity in an oligotrophic coastal site studied by molecular and culturing approaches. FEMS Microbiology Ecology 50: 231–243.PubMedCrossRefGoogle Scholar
  115. Massana, R., R. Terrado, I. Forn, C. Lovejoy & C. Pedros-Alio, 2006. Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environmental Microbiology 8: 1515–1522.PubMedCrossRefGoogle Scholar
  116. Moon-van der Staay, S. Y., R. De Wachter & D. Vaulot, 2001. Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409: 607–610.PubMedCrossRefGoogle Scholar
  117. Moreira, D. & P. Lopez-Garcia, 2002. The molecular ecology of microbial eukaryotes unveils a hidden world. Trends in Microbiology 10: 31–38.PubMedCrossRefGoogle Scholar
  118. Okamoto, N. & I. Inouye, 2005. The Katablepharids are a distant sister group of the Cryptophyta: a proposal for Kathablepharida division nova/Katablepharida phylum novum based on SSU rDNA and Beta-tubulin phylogeny. Protist 156: 163–179.PubMedCrossRefGoogle Scholar
  119. Pace, M. L. & M. D. Bailiff, 1987. An evaluation of the fluorescent microsphere technique for measuring grazing rate of phagotrophic organisms. Marine Ecology Progress Series 40: 185–193.CrossRefGoogle Scholar
  120. Pace, N. R., D. A. Stahl, D. J. Lane & G. J. Olsen, 1986. The analysis of natural microbial populations by ribosomal RNA sequences. Advances in Microbial Ecology 9: 1–55.Google Scholar
  121. Pace, M. L., G. B. McManus & S. E. G. Findlay, 1990. Planktonic community structure determines the fate of bacterial production in a temperate lake. Limnology and Oceanography 25: 795–808.CrossRefGoogle Scholar
  122. Park, M. G., W. Yih & D. W. Coats, 2004. Parasites and phytoplankton, with special emphasis on dinoflagellate infections. The Journal of Eukaryotic Microbiology 51: 145–155.PubMedCrossRefGoogle Scholar
  123. Patterson, D. J., 1993. The current status of the free-living heterotrophic flagellates. The Journal of Eukaryotic Microbiology 40: 606–609.CrossRefGoogle Scholar
  124. Pearson, A., M. Budin & J. J. Brocks, 2003. Phylogenetic and biochemical evidence for sterol synthesis in the bacterium Gemmata obscuriglobus. Proceedings of the National Academy of Sciences 100: 15352–15357.Google Scholar
  125. Pernthaler, J., 2005. Predation on prokaryotes in the water column and its ecological implications. Nature Reviews Microbiology 3: 1–10.Google Scholar
  126. Pernthaler, J., K. Simek, B. Sattler, A. Scharzenbacher, J. Bobkova & R. Psenner, 1996. Short-term changes of protozoan control on autotrophic picoplankton in an oligo-mesotrophic lake. Journal of Plankton Research 18: 443–462.CrossRefGoogle Scholar
  127. Pomeroy, L. R., 1974. The ocean’s food webs, a changing paradigm. BioScience 24: 499–504.CrossRefGoogle Scholar
  128. Pomeroy, L. R. & W. J. Wiebe, 1988. Energetics of microbial food webs. Hydrobiologia 159: 7–18.Google Scholar
  129. Pongratz, E., 1966. De quelques champignons parasites d’organismes planctoniques du Léman. Aquatic Sciences 28: 104–132.Google Scholar
  130. Powell, M. J., 1993. Looking at mycology with a Janus face: a glimpse at Chytridiomycetes active in the environment. Mycologia 85: 1–20.CrossRefGoogle Scholar
  131. Premke, K. & H. Arndt, 2000. Predation on heterotrophic flagellates by protists: food selectivity determined using a live-staining technique. Archiv für Hydrobiologie 150: 17–28.Google Scholar
  132. Rasconi, S., M. Jobard, L. Jouve & T. Sime-Ngando, 2009. Use of calcofluor white for detection, identification and quantification of phytoplanktonic fungal parasites. Applied and Environmental Microbiology 75: 2545–2553.PubMedCrossRefGoogle Scholar
  133. Richards, T. A., A. A. Vepritskiy, D. E. Gouliamova & S. A. Nierzwicki-Bauer, 2005. The molecular diversity of freshwater picoeukaryotes from oligotrophic lake reveals diverse, distinctive and globally dispersed lineages. Environmental Microbiology 7: 1413–1425.PubMedCrossRefGoogle Scholar
  134. Rivkin, R. B. & L. Legendre, 2001. Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291: 2398–2400.PubMedCrossRefGoogle Scholar
  135. Romari, K. & D. Vaulot, 2004. Composition and temporal variability of picoeukaryote communities at a coastal site of the English Chanel from 18S rDNA sequences. Limnology and Oceanography 49: 784–798.CrossRefGoogle Scholar
  136. Sanders, R. W., K. G. Porter, S. J. Bennett & A. E. DeBiase, 1989. Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and clasocerans in a freshwater planktonic community. Limnology and Oceanography 34: 673–687.CrossRefGoogle Scholar
  137. Sanders, R. W., D. A. Caron & U. G. Berninger, 1992. Relationships between bacteria and heterotrophic nanoplankton in marine and fresh waters: an inter-ecosystem comparison. Marine Ecology Progress Series 86: 1–14.CrossRefGoogle Scholar
  138. Sanders, R. W., D. A. Leeper, C. H. King & K. G. Porter, 1994. Grazing by rotifers and crustacean zooplankton on nanoplanktonic protists. Hydrobiologia 288: 167–181.CrossRefGoogle Scholar
  139. Savin, M. C., J. L. Martin, M. Giewat & J. Rooney-Varga, 2004. Plankton diversity in the Bay of Fundy as measured by morphological and molecular methods. Microbial Ecology 48: 51–65.PubMedCrossRefGoogle Scholar
  140. Seena, S., N. Wynberg & F. Bärlocher, 2008. Fungal diversity during leaf decomposition in a stream assessed through clone libraries. Fungal Diversity 30: 1–14.Google Scholar
  141. Shearer, C. A., E. Descals, B. Kohlmeyer, J. Kohlmeyer, L. Marvanová, D. Padgett, D. Porter, H. A. Raja, J. P. Schmit, H. A. Thornton & H. Voglmayr, 2007. Fungal biodiversity in aquatic habitats. Biodiversity and Conservation 16: 49–67.CrossRefGoogle Scholar
  142. Sherr, E. B., 1988. Direct use of high molecular weight polysaccharide by heterotrophic flagellates. Nature 335: 348–351.CrossRefGoogle Scholar
  143. Sherr, E. B. & B. F. Sherr, 1988. Role of microbes in pelagic food webs: a revised concept. Limnology and Oceanography 33: 1225–1227.CrossRefGoogle Scholar
  144. Sherr, B. F., E. B. Sherr & R. D. Fallon, 1987. Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Applied and Environmental Microbiology l53: 958–965.Google Scholar
  145. Simek, K. & T. H. Chzanowski, 1992. Direct and indirect evidence of size-selective grazing on pelagic bacteria by freshwater nanoflagellates. Applied and Environmental Microbiology 58: 3715–3720.PubMedGoogle Scholar
  146. Simek, K. & V. Straskrabova, 1992. Bacterioplankton production and protozoan bacterivory in a mesotrophic reservoir. Journal of Plankton Research 14: 773–787.CrossRefGoogle Scholar
  147. Simek, K., P. Hartman, J. Nedoma, J. Pernthaler, D. Springmann, J. Vrba & R. Psenner, 1997. Community structure, picoplankton grazing and zooplankton control of heterotrophic nanoflagellates in a eutrophic reservoir during the summer phytoplankton maximum. Aquatic Microbial Ecology 12: 49–63.CrossRefGoogle Scholar
  148. Simek, K., K. Hornàk, M. Masin, U. Christaki, J. Nedoma, M. G. Weinbauer & J. R. Dolan, 2003. Comparing the effects of resource enrichment and grazing on the bacterioplankton community of a meso-eutrophic reservoir. Aquatic Microbial Ecology 31: 123–135.CrossRefGoogle Scholar
  149. Sime-Ngando, T. & A. S. Pradeep Ram, 2005. Grazer effects on prokaryotes and viruses in a freshwater microcosm experiment. Aquatic Microbial Ecology 41: 115–124.CrossRefGoogle Scholar
  150. 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 B: Biological Sciences 272: 2073–2081.Google Scholar
  151. Sonntag, B., T. Posh & R. Psenner, 2000. Comparison of three methods for determining flagellates abundance cell size and biovolume in cultures and natural freshwater samples. Archiv für Hydrobiologie 149: 337–351.Google Scholar
  152. Sonntag, B., T. Posh, S. Klammer, K. Teubner & R. Psenner, 2006. Phagotrophic ciliates and flagellates in an oligotrophic, deep, alpine lake; contrasting variability with seasons and depths. Aquatic Microbial Ecology 43: 193–207.CrossRefGoogle Scholar
  153. Sparrow, F. K., 1960. Aquatic Phycomycetes, 2nd ed. University of Michigan Press, Ann Arbor.Google Scholar
  154. Stoeck, T. & S. Epstein, 2003. Novel Eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen-depleted marine environments. Applied and Environmental Microbiology 69: 2657–2663.PubMedCrossRefGoogle Scholar
  155. Stoeck, T., G. Taylor & S. Epstein, 2003. Novel Eukaryotes from the permanently anoxic Cariaco Basin (Caribbean Sea). Applied and Environmental Microbiology 69: 5656–5663.PubMedCrossRefGoogle Scholar
  156. Strom, S. L., 2000. Bacterivory: interactions between bacteria and their grazers. In Kirchman, D. L. (ed.), Microbial Ecology of the Oceans. Wiley-Liss, New York: 351–386.Google Scholar
  157. Takishita, K., H. Miyake, M. Kawato & T. Maruyama, 2005. Genetic diversity of microbial eukaryotes in anoxic sediment around fumaroles on a submarine caldera floor based on the small-subunit rDNA phylogeny. Extremophiles 9: 185–196.PubMedCrossRefGoogle Scholar
  158. Thingstad, T. F. & R. Lignell, 1997. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquatic Microbial Ecology 13: 19–27.CrossRefGoogle Scholar
  159. Tranvik, L. J., E. B. Sherr & B. F. Sherr, 1993. Uptake and utilization of ‘colloidal DOM’ by heterotrophic flagellates in seawater. Marine Ecology Progress Series 92: 301–309.CrossRefGoogle Scholar
  160. Van Donk, H. & J. Ringelberg, 1983. The effect of fungal parasitism on the succession of diatoms in Lake Maarsseveen-I (The Netherlands). Freshwater Biology 13: 241–251.CrossRefGoogle Scholar
  161. Vaqué, D. & L. M. Pace, 1992. Grazing on bacteria by flagellates and cladocerans in lake contrasting food-web structure. Journal of Plankton Research 14: 307–321.CrossRefGoogle Scholar
  162. Weete, J. D., M. S. Fuller, M. Q. Huang & S. Gandhi, 1989. Fatty acids and sterols of selected Hyphochytriomycetes and Chytridiomycetes. Experimental Mycology 13: 183–195.CrossRefGoogle Scholar
  163. Weisse, T., 2002. The significance of inter- and intraspecific variation in bacterivorous and herbivorous protists. Antonie van Leeuwenhoek 81: 327–341.PubMedCrossRefGoogle Scholar
  164. Weisse, T., H. Müller, R. M. Pinto-Coelho, A. Schweizer, D. Springmann & G. Baldringer, 1990. Response of the microbial loop to the phytoplankton spring bloom in a large prealpine lake. Limnology and Oceanography 35: 781–794.CrossRefGoogle Scholar
  165. Weitere, M. & H. Arndt, 2003. Structure of the heterotrophic flagellate community in the water column of the River Rhine (Germany). European Journal of Protistology 39: 287–300.CrossRefGoogle Scholar
  166. Whisler, H. C., 1985. Life history of species of Coelomomyces. In Couch, J. N. & C. E. Bland (eds), The Genus Coelomomyces. Academic Press Inc, New York: 9–22.Google Scholar
  167. Wieltschnig, C., K. T. Kirschner, A. Steitz & B. Velimirnov, 2001. Weak coupling between heterotrophic nanoflagellates and bacteria in a eutrophic freshwater environment. Microbial Ecology 42: 159–167.PubMedGoogle Scholar
  168. Work, K., K. Havens, B. Sharfstein & T. East, 2005. How important is bacterial carbon to planktonic grazers in a turbid, subtropical lake? Journal of Plankton Research 27: 357–372.CrossRefGoogle Scholar
  169. Yuan, J., M. Y. Chen, P. Shao, H. Zhou, Y. Q. Chan & L. H. Qu, 2004. Genetic diversity of small eukaryotes from the coastal waters of Nansha Islands in China. FEMS Microbiology Letters 240: 163–170.PubMedCrossRefGoogle Scholar
  170. Zöllner, E., B. Santer, M. Boersma, H. G. Hoppe & K. Jürgens, 2003. Cascading predation effects of Daphnia and copepods on microbial food web components. Freshwater Biology 48: 2174–2193.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Télesphore Sime-Ngando
    • 1
  • Emilie Lefèvre
    • 1
    • 3
  • Frank H. Gleason
    • 2
  1. 1.LMGE, Laboratoire Microorganismes: Génome & Environnement, UMR CNRS 6023Université Blaise PascalAubière CedexFrance
  2. 2.School of Biological Sciences A12University of SydneySydneyAustralia
  3. 3.Biology DepartmentThe University of AlabamaTuscaloosaUSA

Personalised recommendations