Molecular and morphological diversity of fungi and the associated functions in three European nearby lakes

Environmental Microbiology

Volumn 14, Issue 9, 2012, Pages 2480-2494

  Jobard, Marlène ^a   Rasconi, Serena ^a   Solinhac, Laurent ^b   Cauchie, Henry Michel ^b   Sime Ngando, Télesphore ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b LUXEMBOURG INSTITUTE OF SCIENCE AND TECHNOLOGY   (Luxembourg)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOSOME DNA;

ARTICLE; BIODIVERSITY; CHYTRIDIOMYCETES; CLASSIFICATION; CYTOLOGY; FUNGUS; GENETIC VARIABILITY; GENETICS; LAKE; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLANKTON; POLYMERASE CHAIN REACTION; SEASON;

BIODIVERSITY; CHYTRIDIOMYCOTA; DNA, RIBOSOMAL; FUNGI; GENETIC VARIATION; LAKES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANKTON; POLYMERASE CHAIN REACTION; SEASONS; WATER MICROBIOLOGY;

ASCOMYCOTA; BASIDIOMYCOTA; CHYTRIDIOMYCOTA; FUNGI;

EID: 84865784911     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02771.x     Document Type: Article

References (101)

1. Alexander, E., Stock, A., Breiner, H.W., Behnke, A., Bunge, J., Yakimav, M.M., and Stoeck, T. (2009) Microbial eukaryotes in the hypersaline anoxic l'Atalante deep-sea basin. Environ Microbiol 11: 360-381.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Bärlocher, F. (2005) Freshwater fungal communities. In The Fungal Community: Its Organization and Role in the Ecosystem, 3rd edn. Dighton, J., White, J.F., and Oudemans, P. (eds). New York, USA: Marcel Dekker, pp. 39-59.
4. Bärlocher, F., Nikolcheva, L.G., Wilson, K.P., and Williams, D.D. (2006) Fungi in the hyporheic zone of a springbrook. Microb Ecol 52: 708-715.
5. Bass, D., Howe, A., Brown, N., Barton, H., Demidova, M., Michelle, H., etal. (2007) Yeast forms dominate fungal diversity in the deep oceans. Proc R Soc B 274: 3069-3077.
6. Bhadury, P., Bridge, P.D., Austen, M.C., Bilton, D.T., and Smerdon, G.R. (2009) Detection of fungal 18S rRNA sequences in conjunction with marine nematode 18S rRNA amplicons. Aquat Biol 5: 149-155.
7. Bruning, K., Lingeman, R., and Ringelberg, J. (1992) Estimating the impact of fungal parasites on phytoplankton populations. Limnol Oceanogr 37: 252-260.
8. Burgaud, G., Le Calvez, T., Arzur, D., Vandenkoornhuyse, P., and Barbier, G. (2009) Diversity of culturable marine filamentous fungi from deep-sea hydrothermal vents. Environ Microbiol 1: 1588-1600.
9. Butinar, L., Santos, S., Spencer-Martins, I., Oren, A., and Gunde-Cimerman, N. (2005) Yeast diversity in hypersaline habitats. FEMS Microbiol Lett 244: 229-234.
10. Canter, H.M., and Lund, J.W.G. (1969) The parasitism of planktonic desmids by Fungi. Österr Bot Z 116: 351-377.
11. Chen, M., Chen, F., Yu, Y., Ji, J., and Kong, F. (2008) Genetic diversity of eukaryotic microorganisms in Lake Taihu, a large shallow subtropical lake in China. Microb Ecol 56: 572-583.
12. Czeczuga, B., Kozlowska, M., and Godlewska, A. (2002) Zoosporic aquatic fungi growing on dead specimens of 29 freshwater crustacean species. Limnology 32: 180-193.
13. Damare, S.R., and Raghukumar, C. (2008) Fungi and macroaggregation in deep-sea sediments. Microb Ecol 56: 168-177.
14. De Garcia, V., Brizzio, S., Libkind, D., Buzzini, P., and van Broock, M. (2007) Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia, Argentina. FEMS Microbiol Ecol 59: 331-341.
15. Diez, B., Pedro-Alio, C., and Massana, R. (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67: 2932-2941.
16. Duarte, S., Pascoal, C., Cassio, F., and Bärlocher, F. (2006) Aquatic hyphomycetes diversity and identity affect leaf decomposition in microcosms. Oecologia 147: 658-666.
17. Fabre, E. (1998) Aquatic hyphomycetes in three rivers of southwestern France. III. Relationships between spatial and temporal dynamics. Can J Bot 76: 115-121.
18. Freeman, K.R., Martin, A.P., Karki, D., Lynch, R.C., Mitter, M.S., Meyer, A.F., etal. (2009) Evidence that chytrids dominate fungal communities in high-elevation soils. Proc Natl Acad Sci USA 106: 18315-18320.
19. Gadanho, M., and Sampaio, J.P. (2004) Application of temperature gradient gel electrophoresis to the study of yeast diversity in the estuary of the Tagus river, Portugal. FEMS Yeast Res 5: 253-261.
20. Gadanho, M., Libkind, D., and Sampaio, J.P. (2006) Yeast diversity in the extreme acidic environments of the Iberan Pyrite Belt. Microb Ecol 52: 552-563.
21. Gao, Z., Li, B.L., Zheng, C.C., and Wang, G.Y. (2008) Molecular detection of fungal communities in the Hawaiian Marine sponges Suberites zeteki and Mycale armata. Appl Environ Microbiol 74: 6091-6101.
22. Gao, Z., Johnson, Z.I., and Wang, G. (2009) Molecular characterization of the spatial diversity and novel lineages of mycoplankton in Hawaiian coastal waters. ISME J 4: 111-120.
23. Gleason, F.H., Kagami, M., Lefèvre, E., and Sime-Ngando, T. (2008) The ecology of chytrids in aquatic ecosystems: roles in food web dynamics. Fungal Biol Rev 2: 17-25.
24. Grami, B., Rasconi, S., Niquil, N., Jobard, M., Saint-Béat, B., etal. (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. doi:10.1371/journal.pone.0023273.
25. Gromov, B., Pljusch, A.V., and Mamkaeva, K.A. (1999a) Cultures of Rhizophydium spp. (Chytridiales)-parasites of chlorococalean algae. Algol Stud 95: 115-123.
26. Gromov, B., Pljusch, A.V., and Mamkaeva, K.A. (1999b) Morphology and possible host range of Rhizophydium algavorum sp. nov. (Chytridiales) - an obligate parasite of algae. Protistology 1: 62-65.
27. Hagler, A.N., and Mendonça-Hagler, L.C. (1981) Yeasts from marine and estuarine waters with different levels of pollution in the state of Rio de Janeiro, Brazil. Appl Environ Microbiol 41: 173-178.
28. Hawksworth, D.L. (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105: 1422-1432.
29. Hawksworth, D.L., and Mueller, G.M. (2005) Fungal communities: their diversity and distribution. In The Fungal Community: Its Organization and Role in the Ecosystem, 3rd edn. Dighton, J., Oudemans, P., and White, J. (eds). New York, USA: Marcel Dekker, pp. 27-37.
30. Hawksworth, D.L., and Rossman, A.Y. (1997) Where are all the undescribed fungi? Phytopathology 87: 888-891.
31. Held, A.A. (1972) Host-parasite relations between Allomyces and Rozella - parasite penetration depends on growth response of host cell-wall. Arch Microbiol 82: 128-139.
32. Hibbett, D.S., Binder, M., Bischoff, J.F., Blackwell, M., Cannon, P.F., Eriksson, O.E., etal. (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111: 509-547.
33. Hoffman, Y., Aflalo, C., Zarka, A., Gutman, J., James, T.Y., and Boussiba, S. (2008) Isolation and characterization of a novel chytrid species (phylum Blastocladiomycota), parasitic on the green alga Haematococcus. Mycol Res 112: 70-81.
34. Holfeld, H. (2000) Infection of the single-celled diatom Stephanodiscus alpinus by the chytrid Zygorhizidium: parasite distribution within host population, changes in host cell size, and host-parasite size relationship. Limnol Oceanogr 45: 1440-1444.
35. Huber, T., Faulkner, G., and Hugenholtz, P. (2004) Bellerophon; a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319.
36. 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.
37. Ingold, C.T. (1942) Aquatic hyphomycetes of decaying alder leaves. Trans Br Mycol Soc 25: 339-417.
38. Ingold, C.T. (1975) An illustrated guide to aquatic and water-borne hyphomycetes (Fungi imperfecti) with notes on their biology. Freshw Biol Assoc Sci Pub 30: 1-96.
39. James, T.Y., Letcher, P.M., Longcore, J.E., Mozley-Standridge, S.E., Porter, D., Powell, M.J., etal. (2006) A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98: 860-871.
40. Jobard, M., Rasconi, S., and Sime-Ngando, T. (2010a) Diversity and functions of microscopic fungi: a missing component in pelagic food webs. Aquat Sci 72: 255-268.
41. Jobard, M., Rasconi, S., and Sime-NGando, T. (2010b) Fluorescence in situ hybridization of uncultured zoosporic fungi: testing with clone-FISH and application to freshwater samples using CARD-FISH. J Microbiol Methods 83: 236-243.
42. Johnson, P.T.J., Longcore, J.E., Stanton, D.E., Carnegie, R.B., Shields, J.D., and Preu, E.R. (2006) Chytrid infections of Daphnia pulicaria: development, ecology, pathology and phylogeny of Polycaryum laeve. Freshw Biol 51: 634-648.
43. Johnson, P.T.J., Ives, A.R., Lathrop, R.C., and Carpenter, S.R. (2009) Long-term disease dynamics in lakes: causes and consequences of chytrid infections in Daphnia populations. Ecology 90: 132-144.
44. Jones, M.D.M., Forn, I., Gadelha, C., Egan, M.J., Bass, D., Massana, R., and Richards, T.A. (2011) Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474: 200-205.
45. Jørgensen, N.O.G., and Stepanauskas, R. (2009) Biomass of pelagic fungi in Baltic rivers. Hydrobiology 623: 105-112.
46. Kagami, M., Van Donk, E., de Bruin, A., Rijkeboer, M., and Ibelings, B.W. (2004) Daphnia can protect diatoms from fungal parasitism. Limnol Oceanogr 49: 680-685.
47. Kagami, M., de Bruin, A., Ibelings, B.W., and Van Donk, E. (2007a) Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiology 578: 113-129.
48. Kagami, M., Elert, E., Ibelings, B.W., de Bruin, A., and Van Donk, E. (2007b) The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella. Proc R Soc B 274: 1561-1566.
49. Karakousis, A., Tan, L., Ellis, D., Alexiou, H., and Wormald, P.J. (2006) An assessment of the efficiency of fungal DNA extraction methods for maximizing the detection of medically important fungi using PCR. J Microbiol Methods 65: 38-48.
50. Kohlmeyer, J., and Demoulin, V. (1981) Parasitic and symbiotic Fungi on marine algae. Botanica Marina 24: 9-18.
51. Kudoh, S., and Takahashi, M. (1990) Fungal control of population-changes of the planktonic diatom Asterionella formosa in a shallow eutrophic lake. J Phycol 26: 239-244.
52. Kutty, S.N., and Philip, R. (2008) Marine yeasts - a review. Yeast 25: 465-483.
53. Kurtzman, C.P., and Fell, J.W. (2004) Yeast. In Biodiversity of Fungi: Inventory and Monitoring Methods. Mueller, G.M., Bills, G.F., and Foster, M.S. (eds). Amsterdam, the Netherlands: Elsevier Academic Press, pp. 337-342.
54. Lafferty, K.D., Dobson, A.P., and Kuris, A.M. (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103: 11211-11216.
55. Lafferty, K.D., Allesina, S., Arim, M., Briggs, C.J., DeLeo, G., Dobson, A.P., etal. (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11: 533-546.
56. Lampert, W., and Sommer, U. (2007) Limnoecology - The Ecology of Lakes and Streams, 2nd edn, Oxford, UK: Oxford University Press.
57. Landeweert, R., Leeflang, P., Kuyper, T.W., Hoffland, E., Rosling, A., Wernars, K., and Smit, E. (2003) Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl Environ Microbiol 69: 327-333.
58. Le Calvez, T., Burgaud, G., Mahé, S., Barbier, G., and Vandenkoornhuyse, P. (2009) Fungal diversity in deep sea hydrothermal ecosystems. Appl Environ Microbiol 75: 6415-6421.
59. Lefèvre, E., Bardot, C., Noel, 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.
60. 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: e2324.
61. Lefranc, M., Thénot, A., Lepère, C., and Debroas, D. (2005) Genetic diversity of small eukaryotes in lakes differing by their trophic status. Appl Environ Microbiol 71: 5935-5942.
62. Lepère, C., Boucher, D., Jardillier, L., Domaizon, I., and Debroas, D. (2006) Succession and regulation factors of small eukaryote community composition in a lacustrine ecosystem (Lake Pavin). Appl Environ Microbiol 74: 2971-2981.
63. Lepère, C., Domaizon, I., and Debroas, D. (2007) Community composition of lacustrine small eukaryotes in hyper-eutrophic conditions in relation to top-down and bottom-up factors. FEMS Microbiol Ecol 61: 483-495.
64. Lepère, C., Domaizon, I., and Debroas, D. (2008) Unexpected importance of potential parasites in the composition of the freshwater small-eukaryote community. Appl Environ Microbiol 74: 2940-2949.
65. Lichtwardt, R.W., White, M.M., and Cafaro, M.J. (2003) Freshwater Trichomycetes and their arthropod hosts. In Freshwater Mycology. Tsui, C.K.M., and Hyde, K.D. (eds). Hong Kong, China: Fungal Diversity Press, pp. 81-100.
66. López-Archilla, A.I., González, A.E., Terrón, M.C., and Amils, R. (2004) Ecological study of the fungal populations of the acidic Tinto River in southwestern Spain. Can J Microbiol 50: 923-934.
67. López-García, P., Vereshchaka, A., and Moreira, D. (2006) Eukaryotic diversity associated with carbonates and fluid-seawater interface in Lost City hydrothermal field. Environ Microbiol 9: 546-554.
68. Lozupone, C.A., and Klein, D.A. (2002) Molecular and cultural assessment of chytrid and spizellomyces population in grassland soils. Mycologia 94: 411-420.
69. Masclaux, H., Bec, A., Kagami, M., Perga, M.E., Sime-Ngando, T., Desvilettes, C., and Bourdier, G. (2011) Food quality of anemophilous plant pollen for freshwater zooplankton. Limnol Oceanogr 56: 939-946.
70. Massana, R., Balague, V., Guillou, L., and Pedros-Alio, C. (2004) Picoeukaryotic diversity in an oligotrophic coastal site studied by molecular and culturing approaches. FEMS Microbiol Ecol 50: 231-243.
71. Nikolcheva, L.G., and Bärlocher, F. (2002) Phylogeny of Tetracladium based on 18S rDNA. Czech Mycol 53: 285-295.
72. Nikolcheva, L.G., and Bärlocher, F. (2004) Taxon-specific fungal primers reveal unexpectedly high diversity during leaf decomposition in a stream. Mycol Prog 3: 41-49.
73. Nikolcheva, L.G., and Bärlocher, F. (2005) Seasonal and substrate preferences of fungi colonizing leaves in streams: traditional versus molecular evidence. Environ Microbiol 7: 270-280.
74. Nikolcheva, L.G., Cockshutt, A.M., and Bärlocher, F. (2003) Determining diversity of freshwater fungi on decaying leaves: comparison of traditional and molecular approaches. Appl Environ Microbiol 69: 2548-2554.
75. Niquil, N., Kagami, M., Urabe, J., Christaki, U., Viscogliosi, E., and Sime-Ngando, T. (2011) Potential role of fungi in plankton food web functioning and stability: a simulation analysis based on Lake Biwa inverse model. Hydrobiologia 659: 65-79.
76. O'Brien, H.E., Parrent, J.L., Jackson, J.A., Moncalvo, J.M., and Vilgalys, R. (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71: 5544-5550.
77. Raghukumar, S. (2006) The role of fungi in marine detrital processes. In Marine Microbiology Facets and Opportunities. Ramaiah, N. (ed.). Goa: National Institute of Oceanography, pp. 125-140.
78. Rasconi, S., Jobard, M., Jouve, L., and Sime-Ngando, T. (2009) Use of calcofluor white for detection, identification, and quantification of phytoplanktonic fungal parasites. Appl Environ Microbiol 75: 2545-2553.
79. Rasconi, S., Jobard, M., and Sime-Ngando, T. (2011) Parasitic fungi of phytoplankton: ecological roles and implications for microbial food webs. Aquat Microb Ecol 62: 123-137.
80. Rasconi, S., Niquil, N., and Sime-Ngando, T. (2012) Phytoplankton chytridiomycosis: community structure and infectivity of fungal parasites in aquatic systems. Environ Microbiol. doi:10.1111/j.1462-2920.2011.02690.x.
81. Romari, K., and Vaulot, D. (2004) Composition and temporal variability of picoeukaryote communities at a coastal site of the English Channel from 18S rDNA sequences. Limnol Oceanogr 49: 784-798.
82. Ronquist, F., and Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
83. Rösel, S., Rychla, A., Wurzbacher, C., and Grossart, H.P. (2012) Effects of pollen leaching and microbial degradation on organic carbon and nutrient availability in lake water. Aquat Sci 74: 87-99.
84. Russo, G., Diego, L., Sampaio, J.P., and van Broock, M.R. (2008) Yeast diversity in the acidic Rio Agrio-Lake Caviahue volcanic environment (Patagonia, Argentina). FEMS Microbiol Ecol 65: 415-424.
85. Sampaio, A., Sampaio, J.P., and Leao, C. (2007) Dynamics of yeast populations recovered from decaying leaves in a nonpolluted stream: a 2-year study on the effects of leaf litter type and decomposition time. FEMS Yeast Res 7: 595-603.
86. Sasaki, F., Miyamoto, T., Yamamoto, A., Tamai, Y., and Yajima, T. (2008) Morphological and genetic characteristics of the entomopathogenic fungus Ophiocordyceps nutans and its host insects. Mycol Res 112: 1241-1244.
87. Schmit, J.P., and Mueller, G.M. (2007) An estimate of the lower limit of global fungal diversity. Biodivers Conserv 16: 99-111.
88. Schoenlein-Crusius, I.H., and Milanez, A.I. (1998) Fungal succession on leaves of Alchornea triplinervia (Spreng.) Muell. Arg. submerged in a stream of an Atlantic Rainforest in the state of São Paulo, Brazil. Rev Bras Bot 21: 253-259.
89. Seena, S., Wynberg, N., and Bärlocher, F. (2008) Fungal diversity during leaf decomposition in a stream assessed through clone libraries. Fungal Divers 30: 1-14.
90. Sigee, D.C. (2005) Freshwater Microbiology. Chichester, UK: John Wiley & Sons.
91. Sime-Ngando, T., Lefèvre, E., and Gleason, F.H. (2011) Hidden diversity among aquatic heterotrophic flagellates: ecological potentials of zoosporic fungi. Hydrobiologia 659: 5-22.
92. Sparrow, F.K. (1960) Aquatic Phycomycetes. Ann Arbor, MI, USA: University of Michigan Press.
93. Stock, A., Jürgens, K., Bunge, J., and Stoeck, T. (2009) Protistan diversity in suboxic and anoxic waters of the Gotland Deep (Baltic Sea) as revealed by 18S rRNA clone libraries. Aquat Microb Ecol 55: 267-284.
94. Sung, G.H., Sung, J.M., Hywel-Jones, N.L., and Spatafora, J.W. (2007) A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): identification of localized incongruence using a combinational bootstrap approach. Mol Phylogenet Evol 44: 1204-1223.
95. Takano, K., Ishikawa, Y., Mikami, H., Igarashi, S., Hino, S., and Yoshioka, T. (2008) Fungal infection for cyanobacterium Anabaena smithii by two chytrids in eutrophic region of large reservoir Lake Shumarinai, Hokkaido, Japan. Limnology 9: 213-218.
96. Tang, K.W., Hutalle, K.M.L., and Grossart, H.P. (2006) Microbial abundance, composition and enzymatic activity during decomposition of copepod carcasses. Aquat Microb Ecol 45: 219-227.
97. Van Donk, E., and Bruning, K. (1992) Ecology of aquatic fungi in and on algae. In Algal Symbiosis - Plants, Animals, Fungi, Interactions Explored. Reisser, W. (ed.). Bristol, UK: Biopress, pp. 567-592.
98. Wang, G., Li, Q., and Zhu, P. (2008) Phylogenetic diversity of culturable fungi associated with the Hawaiian sponges Suberites zeteki and Gelliodes fibrosa. Antonie Van Leeuwenhoek 93: 163-174.
99. White, T.J., Bruns, T., Lee, S., and Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to Methods and Application. Innis, M.A., Gelfand, D.H., Sninsky, J.J., and White, T.J. (eds). San Diego, CA, USA: Academic Press, pp. 315-322.
100. Wilkinson, H.T. (1987) Yellow ring on Poa pratensis caused by Trechispora alnicola. Plant Dis 71: 1141-1143.
101. Wurzbacher, C.M., Bärlocher, F., and Grossart, H.P. (2010) Fungi in lake ecosystems. Aquat Microb Ecol 59: 125-149.