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

Hydrobiologia

Volumn 659, Issue 1, 2011, Pages 5-22

  Sime Ngando, Télesphore ^a   Lefèvre, Emilie ^a,c   Gleason, Frank H ^b  

^a UNIVERSITÉ BLAISE PASCAL   (France)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF ALABAMA   (United States)

Author keywords

Aquatic systems; Food web dynamics; Heterotrophic flagellates; Microbial diversity; Zoosporic fungi

Indexed keywords

BACTERIVORY; DISPERSAL; DIVERSITY INDEX; DOMINANCE; FLAGELLATE; FUNGUS; HETEROTROPHY; LIFE CYCLE; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; MICROBIAL LOOP; MICROSCOPY; MOLECULAR ANALYSIS; MORPHOLOGY; PELAGIC ENVIRONMENT; PROTIST; SPECIES DIVERSITY; SPORE;

ALVEOLATA; AMOEBOPHRYA SP.; EUKARYOTA; FUNGI; MASTIGOPHORA (FLAGELLATES); PERKINSEA; PROTISTA; STRAMENOPILES;

EID: 79955575441     PISSN: 00188158     EISSN: 15735117     Source Type: Journal    
DOI: 10.1007/s10750-010-0230-y     Document Type: Article

References (170)

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.
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.
3. Amann, R. & W. Ludwig, 2000. Ribosomal RNA-targeted nucleic acid probes for studies in microbial ecology. FEMS Microbiology Reviews 24: 555-565.
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.
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.
6. Arndt, H., 1993. Rotifers as predators on components of the microbial web (bacteria, heterotrophic flagellates, ciliates)-a review. Hydrobiologia 255(256): 231-246.
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.
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.
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.
10. Bärlocher, F., 1985. The role of fungi in the nutrition of stream invertebrates. Botanical Journal of the Linnean Society 91: 83-94.
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.
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.
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.
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.
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.
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.
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.
18. Berninger, U. G., B. J. Finlay & P. Kuuppo-Leiniki, 1991. Protozoan control of bacterial abundances in freshwater. Limnology and Oceanography 36: 139-147.
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.
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.
21. Boenigk, J. & H. Arndt, 2002. Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Antonie van Leeuwenhoek 81: 465-480.
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.
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.
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.
25. Callieri, C. & J. G. Stockner, 2002. Freshwater autotrophic picoplankton: a review. Journal of Limnology 61: 1-14.
26. Canter, H. M., 1950. Studies on British chytrids. VIII. On Rhizophidium anomalum n. sp. New Phytologist 49: 98-102.
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.
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.
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.
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.
31. Caron, D. A., 1994. Inorganic nutrients, bacteria, and the microbial loop. Microbial Ecology 28: 295-298.
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.
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.
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.
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.
36. Cavalier-Smith, T. & E. E. Chao, 2003. Phylogeny and classification of phylum Cercozoa (Protozoa). Protist 154: 341-358.
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.
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.
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.
40. Christoffersen, K. & J. M. Gonzalez, 2003. An approach to measure ciliates grazing on living heterotrophic nanoflagellates. Hydrobiologia 491: 159-166.
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.
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.
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.
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.
45. Coulter, D. B. & J. M. Aronson, 1977. Glycogen structure and utilization in Allomyces macrogynus. Experimental Mycology 1: 183-193.
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.
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).
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.
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.
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.
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.
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.
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.
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.
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.
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.
58. Fenchel, T., 1982. Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Marine Ecology Progress Series 8: 225-231.
59. Fenton, A. & M. A. Brockhurst, 2008. The role of specialist parasites in structuring host communities. Ecological Research 23: 795-804.
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.
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.
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.
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.
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.
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.
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.
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.
68. Graham, J. M., 1991. Symposium introductory remarks: a brief history of aquatic microbial ecology. Journal of Protozoology 38: 66-69.
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.
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.
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.
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.
73. Holben, W. E. & J. M. Tiedje, 1988. Applications of nucleic acid hybridization in microbial ecology. Ecology 69: 561-568.
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.
75. Holfeld, H., 1998. Fungal infections of the phytoplankton: seasonality, minimal host density, and specificity in a mesotrophic lake. New Phytologist 138: 507-517.
76. Hudson, J. J., W. D. Taylor & D. W. Schindler, 1999. Planktonic nutrient regeneration and cycling efficiency in temperate lakes. Nature 400: 659-661.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
89. Karling, J. S., 1977. Chytridiomycetarum iconographia. J. Cramer, Montecello, NY.
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.
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.
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.
93. Köthe, A. & J. Benndorf, 1994. Top-down impact of Daphnia galeata on pelagic heterotrophic flagellates in a wholelake biomanipulation experiment. Marine Microbial Food Webs 8: 325-335.
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.
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.
96. Landry, M. R. & A. Calbet, 2004. Microzooplankton production in the oceans. ICES Journal of Marine Science 61: 501-507.
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.
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.
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.
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.
101. Lee, W. J. & D. J. Patterson, 1998. Diversity and geographic distribution of free-living heterotrophic flagellates-analysis by PRIMER. Protist 149: 229-244.
102. Lee, W. J., A. G. B. Simpson & D. J. Patterson, 2005. Freeliving heterotrophic flagellates from freshwater sites in Tasmania (Australia), a field survey. Acta Protozoologica 44: 321-350.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
117. Moreira, D. & P. Lopez-Garcia, 2002. The molecular ecology of microbial eukaryotes unveils a hidden world. Trends in Microbiology 10: 31-38.
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.
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.
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.
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.
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.
123. Patterson, D. J., 1993. The current status of the free-living heterotrophic flagellates. The Journal of Eukaryotic Microbiology 40: 606-609.
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.
125. Pernthaler, J., 2005. Predation on prokaryotes in the water column and its ecological implications. Nature Reviews Microbiology 3: 1-10.
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.
127. Pomeroy, L. R., 1974. The ocean's food webs, a changing paradigm. BioScience 24: 499-504.
128. Pomeroy, L. R. & W. J. Wiebe, 1988. Energetics of microbial food webs. Hydrobiologia 159: 7-18.
129. Pongratz, E., 1966. De quelques champignons parasites d'organismes planctoniques du Léman. Aquatic Sciences 28: 104-132.
130. Powell, M. J., 1993. Looking at mycology with a Janus face: a glimpse at Chytridiomycetes active in the environment. Mycologia 85: 1-20.
131. Premke, K. & H. Arndt, 2000. Predation on heterotrophic flagellates by protists: food selectivity determined using a livestaining technique. Archiv für Hydrobiologie 150: 17-28.
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.
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.
134. Rivkin, R. B. & L. Legendre, 2001. Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291: 2398-2400.
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.
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.
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.
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.
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.
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.
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.
142. Sherr, E. B., 1988. Direct use of high molecular weight polysaccharide by heterotrophic flagellates. Nature 335: 348-351.
143. Sherr, E. B. & B. F. Sherr, 1988. Role of microbes in pelagic food webs: a revised concept. Limnology and Oceanography 33: 1225-1227.
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 153: 958-965.
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.
146. Simek, K. & V. Straskrabova, 1992. Bacterioplankton production and protozoan bacterivory in a mesotrophic reservoir. Journal of Plankton Research 14: 773-787.
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.
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.
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.
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.
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.
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.
153. Sparrow, F. K., 1960. Aquatic Phycomycetes, 2nd ed. University of Michigan Press, Ann Arbor.
154. Stoeck, T. & S. Epstein, 2003. Novel Eukaryotic lineages inferred from small-subunit rRNA analyses of oxygendepleted marine environments. Applied and Environmental Microbiology 69: 2657-2663.
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.
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.
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.
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.
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.
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.
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.
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.
163. Weisse, T., 2002. The significance of inter-and intraspecific variation in bacterivorous and herbivorous protists. Antonie van Leeuwenhoek 81: 327-341.
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.
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.
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.
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.
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.
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.
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.