Phytoplankton chytridiomycosis: Community structure and infectivity of fungal parasites in aquatic ecosystems

Environmental Microbiology

Volumn 14, Issue 8, 2012, Pages 2151-2170

  Rasconi, Serena ^a,c   Niquil, Nathalie ^b   Sime Ngando, Télesphore ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b UNIVERSITÉ DE LA ROCHELLE   (France)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

FRESH WATER;

ANIMAL; ARTICLE; BIODIVERSITY; CHEMISTRY; CHYTRIDIOMYCETES; DIATOM; ECOSYSTEM; FOOD CHAIN; GENETICS; HOST RANGE; MICROBIOLOGY; PHYSIOLOGY; PHYTOPLANKTON; POPULATION DENSITY; SEASON;

ANIMALS; BIODIVERSITY; CHYTRIDIOMYCOTA; DIATOMS; ECOSYSTEM; FOOD CHAIN; FRESH WATER; HOST SPECIFICITY; PHYTOPLANKTON; POPULATION DENSITY; SEASONS;

ALGAE; ANABAENA; ANABAENA FLOSAQUAE; BACILLARIOPHYTA; CYANOBACTERIA; DESMIDIALES; FUNGI;

EID: 84864390702     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02690.x     Document Type: Article

References (83)

1. Alster, A., and Zohary, T. (2007) Interactions between the bloom-forming dinoflagellate Peridinium gatunense and the chytrid fungus Phlyctochytrium sp. Hydrobiologia 578: 131-139.
2. Barr, D.J.S. (1990) Phylum Chytridiomycota. In Handbook of Protoctista. Margulis, L., Corliss, J.O., Melkonian, M., and Chapman, D.J. (eds). Boston, USA: Jones and Bartlett Publishers, pp. 454-466.
3. Barr, D.J.S. (1992) Evolution and kingdoms of organisms from the perspective of a mycologist. Mycologia 84: 1-11.
4. Beakes, G.W., Canter, H.M., and Jaworski, G.H.M. (1992a) Comparative ultrastructural ontogeny of zoosporangia of Zygorhizidium affluens and Z. planktonicum, chytrid parasites of the diatom Asterionella formosa. Mycol Res 96: 1047-1059.
5. Beakes, G.W., Canter, H.M., and Jaworski, G.H.M. (1992b) Ultrastructural study of operculation (discharge apparatus) and zoospore discharge in zoosporangia of Zygorhizidium affluens and Z. planktonicum, chytrid parasites of the diatom Asterionella formosa. Mycol Res 96: 1060-1067.
6. Beakes, G.W., Canter, H.M., and Jaworski, G.H.M. (1993) Sporangium differentiation and zoospore fine-structure of the chytrid Rhizophydium planktonicum, a fungal parasite of Asterionella formosa. Mycol Res 97: 1059-1074.
7. Begon, M., Harper, J.L., and Townsend, C.R. (1990) Ecology: Individuals, Populations, and Communities. Oxford, UK: Blackwell Scientific Publications.
8. Bourrelly, P. (1970) Les Algues d'eau douce. Paris, France: N. Boubée & Cie.
9. ter Braak, C.J.F., and Verdonschot, P.F.M. (1995) Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquat Sci 57: 255-289.
10. Bruning, K. (1991) Effects of temperature and light on the population dynamics of the Asterionella -Rhizophydium association. J Plankton Res 13: 707-719.
11. Bruning, K., and Ringelberg, J. (1987) The influence of phosphorus limitation of the diatom Asterionella formosa on the zoospore production of its fungal parasite Rhizophydium planktonicum. Aquat Ecol 21: 49-54.
12. Bruning, K., Lingeman, R., and Ringelberg, J. (1992) Estimating the impact of fungal parasites on phytoplankton populations. Limnol Oceanogr 37: 252-260.
13. Bush, A.O., Lafferty, K.D., Lotz, J.M., and Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis etal. revisited. J Parasitol 83: 575-583.
14. Canter, H.M. (1949) The importance of fungal parasitism in limnology. Verh Int Verein Limnol 10: 107-108.
15. Canter, H.M. (1950) Fungal parasites of the phytoplankton. I: Studies on British chytrids, X. Ann Bot 14: 263-289.
16. Canter, H.M. (1951) Fungal parasites of the phytoplankton. II. Studies on British chytrids, XII. Ann Bot 15: 129-156.
17. Canter, H.M. (1953) Annotated list of British aquatic chytrids. Trans Br Mycol Soc 36: 278-301.
18. Canter, H.M. (1972) A guide to the fungi occurring on planktonic blue-green algae. In Taxonomy and Biology of Blue-Green Algae. Desikachary, T.V. (ed.). Madras, India: University of Madras, pp. 145-159.
19. Canter, H.M., and Jaworski, G.H.M. (1981) The effect of light and darkness upon infection of Asterionella formosa Hassall by the chytrid Rhizophydium planktonicum Canter emend. Ann Bot 47: 13-30.
20. Canter, H.M., and Lund, J.W.G. (1948) Studies on plankton parasites. I. Fluctuations in the numbers of Asterionella formosa Hass. in relation to fungal epidemics. New Phytol 47: 238-261.
21. Canter, H.M., and Lund, J.W.G. (1951) Studies on plankton parasites: III. Examples of the interaction between parasitism and other factors determining the growth of diatoms. Ann Bot 15: 359-371.
22. Canter, H.M., and Lund, J.W.G. (1953) Studies on plankton parasites: II. The parasitism of diatoms with special reference to lakes in the English Lake District. Trans Br Mycol Soc 36: 13-37.
23. Canter, H.M., and Lund, J.W.G. (1968) Studies on British chytrids: XXVII. Rhizophydium Fugax sp.nov., a parasite of planktonic cryptomonads with additional notes and records of Planktonic fungi. Trans Br Mycol Soc 51: 699-705.
24. Canter, H.M., and Lund, J.W.G. (1969) The parasitism of planktonic desmids by fungi. Plant Syst Evol 116: 351-377.
25. Cavalier-Smith, T. (1993) Kingdom protozoa and its 18 phyla. Microbiol Mol Biol Rev 57: 953-994.
26. Cook, W.R.I. (1932) An account of some uncommon British species of the Chytridiales found in algae. New Phytol 31: 133-144.
27. Czaplewski, R.L., and Parker, M. (1973) Use of a BOD oxygen probe for estimating primary productivity. Limnol Oceanogr 18: 152-154.
28. Doggett, M.S., and Porter, D. (1995) Further evidence for host-specific variants in Zygorhizidium planktonicum. Mycologia 87: 161-171.
29. Gaarder, T., and Gran, H.H. (1927) Investigations of the production of plankton in the Oslo Fjord. Rapp P V Reun Cons Int Explor Mer 42: 1-48.
30. Gleason, F.H., Kagami, M., Lefevre, E., and Sime-Ngando, T. (2008) The ecology of chytrids in aquatic ecosystems: roles in food web dynamics. Fungal Biol Rev 22: 17-25.
31. Grami, B., Rasconi, S., Niquil, N., Jobard, M., Saint-Béat, B., and Sime-Ngando, T. (2011) Functional effects of parasites on food web properties during the spring diatom bloom in Lake Pavin: a linear inverse modeling analysis. PLoS ONE 6: e23273.
32. Hageage, G.J., and Harrington, B.J. (1984) Use of calcofluor white in clinical mycology. Lab Med 15: 109-112.
33. Harrington, B.J., and Hageage, G.J. (2003) Calcofluor white: a review of its uses and applications in clinical mycology and parasitology. Lab Med 34: 361-367.
34. Holfeld, H. (1998) Fungal infections of the phytoplankton: seasonality, minimal host density, and specificity in a mesotrophic lake. New Phytol 138: 507-517.
35. Holfeld, H. (2000) Relative abundance, rate of increase, and fungal infections of freshwater phytoplankton. J Plankton Res 22: 987-995.
36. Huber-Pestalozzi, G. (1944) Chytridium oocystidis (spec. nova?) ein Parasit auf Oocystis lacustris Chodat. Aquat Sci 10: 117-120.
37. Huber-Pestalozzi, G. (1983) Das Phytoplankton des Süßwassers. Stuttgart, Germany: Schweizerbart.
38. Huisman, J. (2010) Comment on 'Patterns of Diversity in Marine Phytoplankton'. Science 329: 512.
39. Ibelings, B.W., De Bruin, A., Kagami, M., Rijkeboer, M., Brehm, M., and Van Donk, E. (2004) Host parasite interactions between freshwater phytoplankton and chytrid fungi (chytridiomycota). J Phycol 40: 437-453.
40. Ingold, C.T. (1940) Endocoenobium eudorinae gen. et sp. nov., a chytridiaceous fungus parasitizing Eudorina elegans Ehrenb. New Phytol 39: 97-103.
41. Jobard, M., Rasconi, S., and Sime-Ngando, T. (2010) Diversity and functions of microscopic fungi: a missing component in pelagic food webs. Aquat Sci 72: 255-268.
42. Kagami, M., and Urabe, J. (2002) Mortality of the planktonic desmid, Staurastrum dorsidentiferum, due to interplay of fungal parasitism and low light conditions. Verh Internat Verein Limnol 28: 1001-1005.
43. Kagami, M., Van Donk, E., Bruin, A., Rijkeboer, M., and Ibelings, B.W. (2004) Daphnia can protect diatoms from fungal parasitism. Limnol Oceanogr 49: 680-685.
44. Kagami, M., de Bruin, A., Ibelings, B., and Van Donk, E. (2007) Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 578: 113-129.
45. Krasnov, B., Stanko, M., Miklisova, D., and Morand, S. (2006) Host specificity, parasite community size and the relation between abundance and its variance. Evol Ecol 20: 75-91.
46. Kudoh, S., and Tokahashi, M. (1990) Fungal control of population changes of the planktonic diatom Asterionella formosa in a shallow eutrophic lake. J Phycol 26: 239-244.
47. Lafferty, K.D., Dobson, A.P., and Kuris, A.M. (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103: 11211-11216.
48. Lefèvre, E., Bardot, C., Noël, C., Carrias, J.-F., Viscogliosi, E., Amblard, C., and Sime-Ngando, T. (2007) Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environ Microbiol 9: 61-71.
49. Lefèvre, E., Roussel, B., Amblard, C., and Sime-Ngando, T. (2008) The molecular diversity of freshwater picoeukaryotes reveals high occurrence of putative parasitoids in the plankton. PLoS ONE 3: 2324.
50. Lefranc, M., Thenot, A., Lepere, C., and Debroas, D. (2005) Genetic diversity of small eukaryotes in lakes differing by their trophic status. Appl Environ Microbiol 71: 5935-5942.
51. Letcher, P.M., Powell, M.J., Chambers, J.G., Longcore, J.E., Churchill, P.F., and Harris, P.M. (2005) Ultrastructural and molecular delineation of the Chytridiaceae (Chytridiales). Can J Bot 83: 1561-1573.
52. Letcher, P.M., Powell, M.J., Churchill, P.F., and Chambers, J.G. (2006) Ultrastructural and molecular phylogenetic delineation of a new order, the Rhizophydiales (Chytridiomycota). Mycol Res 110: 898-915.
53. López-García, P., Rodriguez-Valera, F., Pedros-Alio, C., and Moreira, D. (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603-607.
54. Lund, J.W.G. (1957) Fungal diseases of plankton algae. In Biological Aspects of the Transmission of Diseases. Horton-Smith, C. (ed.). Edinburgh, UK: Oliver and Boyd, pp. 19-23.
55. Lund, J.W.G., Kipling, C., and Cren, E.D. (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11: 143-170.
56. Müller, U., and Sengbusch, P. (1983) Visualization of aquatic fungi (Chytridiales) parasitizing on algae by means of induced fluorescence. Arch Hydrobiol 97: 471-485.
57. Padisak, J., Tóth, L.G., and Rajczy, M. (1988) The role of storms in the summer succession of the phytoplankton community in a shallow lake (Lake Balaton, Hungary). J Plankton Res 10: 249-265.
58. Pongratz, E. (1966) De quelques champignons parasites d'organismes planctoniques du Léman. Aquat Sci 28: 104-132.
59. Powell, M.J. (1978) Phylogenetic implications of the microbody - lipid globule complex in zoosporic fungi. Biosystems 10: 167-180.
60. Prescott, G.W. (1961) Algae of the Western Great Lakes Area. Dubuque, IA, USA: WMC Company Publishers.
61. Raghukumar, S., and Schaumann, K. (1993) An epifluorescence microscopy method for direct detection and enumeration of the fungi like marine protists, the Thraustochytrids. Limnol Oceanogr 38: 182-187.
62. Rasconi, S., Jobard, M., Jouve, L., and Sime-Ngando, T. (2009) Use of calcofluor white for diagnosing, identifying and counting phytoplanktonic fungal parasites. Appl Environ Microbiol 75: 2545-2553.
63. Rasconi, S., Jobard, M., Jouve, L., and Sime-Ngando, T. (2011) Parasitic fungi of phytoplankton: ecological roles and implications for microbial food websAquat. Microb Ecol 62: 123-137.
64. Reynolds, N. (1940) Seasonal variations in Staurastrum paradoxum eyen. New Phytol 39: 86-89.
65. Reynolds, N. (1984) The Ecology of Freshwater Phytoplankton. Cambridge, UK: Cambridge University Press.
66. Rohde, K. (1994) Niche Restriction in Parasites: Proximate and Ultimate Causes. Cambridge, UK: Cambridge University Press.
67. Sen, B. (1987a) Fungal parasitism of planktonic algae in Shearwater. I. Occurrence of Zygorhizidium affluens Canter on Asterionella formosa Hass. in relation to the s asonal periodicity of the alga. Arch Hydrobiol Suppl 76: 101-127.
68. Sen, B. (1987b) Fungal parasitism of planktonic algae in Shearwater. II. A study of the chytrid parasites of the diatom Fragilaria crotonenis Kitton. Arch Hydrobiol Suppl 76: 129-144.
69. Sen, B. (1988a) Fungal parasitism of planktonic algae in Shearwater. IV. Parasitic occurrence of a new chytrid species on the blue-green alga Microcystis aeruginosa Kuetz. emend. Elenkin. Arch Hydrobiol Suppl 79: 177-184.
70. Sen, B. (1988b) Fungal parasitism of planktonic algae in Shearwater. III. Fungal parasites of centric diatoms. Arch Hydrobiol Suppl 79: 167-175.
71. Sigee, D.C. (2005) Freshwater Microbiology: Biodiversity and Dynamic Interactions of Microorganisms in the Aquatic Environment. Chichester, UK: John Wiley and Sons.
72. Sime-Ngando, T., Lefèvre, E., and Gleason, F. (2011) Hidden diversity among aquatic heterotrophic flagellates: ecological potentials of zoosporic fungi. Hydrobiologia 659: 5-22.
73. Sommer, U. (1981) The role of r-and K-selection in the succession of phytoplankton in Lake Constance. Acta Oecol 2: 327-342.
74. Sommer, U. (1987) Factors controlling the seasonal variation in phytoplankton species composition. A case study for a deep, nutrient rich lake. Prog Phycol Res 5: 123-178.
75. Sommer, U., Maciej Gliwicz, Z., Lampert, W., and Duncan, A. (1986) The PEG-model of seasonal succession of planktonic events in fresh waters. Arch Hydrobiol 106: 433-471.
76. Sparrow, F.K. (1960) Aquatic Phycomycetes. Ann Arbor, MI, USA: University of Michigan Press.
77. Tartari, G.A., and Mosello, R. (1997) Metodologie analitiche e controlli di qualità nel laboratorio chimico dell'Istituto Italiano di Idrobiologia. Consiglio nazionale delle ricerche, Pallanza, Italy: Istituto italiano di idrobiologia.
78. Thioulouse, J., Cadet, P., and Albrecht, A. (1995) The use of permutation tests in co-inertia analysis: application to the study of nematode-soil relationships. Biomed Bull 13: 144-142.
79. Tsui, C.K., and Hyde, K.D. (2003) Freshwater Mycology. Hong Kong, China: Fungal diversity press.
80. Upatham, E.S., Viyanant, V., Brockelman, W.Y., Kurathong, S., Lee, P., and Chindaphol, U. (1989) Prevalence, incidence, intensity and associated morbidity of intestinal helminths in south Thailand. Int J Parasitol 19: 217-228.
81. Utermöhl, H. (1958) Zur vervollkommnung der quantitativen phytoplankton-methodik. Mitt Int Ver Theor Angew Limnol 9: 1-38.
82. Van Donk, E. (1989) The role of fungal parasites in phytoplankton succession. Plankton Ecologya review. In Plankton Ecology: Succession in Plankton Communities. Sommer, U. (ed.). Berlin, Germany: Springer-Verlag, pp. 171-194.
83. Van Donk, E., and Ringelberg, J. (1983) The effect of fungal parasitism on the succession of diatoms in Lake Maarsseveen I (The Netherlands). Freshw Biol 13: 241-251.