Temporal variation of the small eukaryotic community in two freshwater lakes: Emphasis on zoosporic fungi

Aquatic Microbial Ecology

Volumn 67, Issue 2, 2012, Pages 91-105

  Lefèvre, Emilie ^a,b   Letcher, Peter M ^a   Powell, Martha J ^a  

^a UNIVERSITY OF ALABAMA   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

Freshwater lakes; Molecular diversity; Plankton; Temporal variation; Zoosporic fungi

Indexed keywords

EID: 84867391874     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01592     Document Type: Article

References (75)

1. Barr DJS (1980) An outline for the reclassification of the Chytridiales, and for a new order, the Spizellomycetales. Can J Bot 58: 2380-2394
2. Borneman J, Hartin RJ (2000) PCR primers that amplify fungal rRNA genes from environmental samples. Appl Environ Microbiol 66: 4356-4360
3. Canter HM, Lund JWG (1951) Studies on plankton parasites. III. Examples of the interaction between parasitism and other factors determining the growth of diatoms. Ann Bot (Lond) 15: 359-371
4. Carlson RE (1977) A trophic state index for lakes. Limnol Oceanogr 22: 361-369
5. Chen M, Chen F, Yu Y, Ji J, Kong F (2008) Genetic diversity of eukaryotic microorganisms in Lake Taihu, a large shallow subtropical lake in China. Microb Ecol 56: 572-583
6. Freeman KR, Martin AP, Karli D, Lynch RC and others (2009) Evidence that chytrids dominate fungal communities in high-elevation soils. Proc Natl Acad Sci USA 106: 18315-18320
7. Fuller MS, Jaworski A (1987) Zoosporic fungi in teaching and research. Southeastern Publishing, Athens, GA
8. Genitsaris S, Kormas KA, Moustaka-Gouni M (2009) Microscopic eukaryotes living in a dying lake (Lake Koronia, Greece). FEMS Microbiol Ecol 69: 75-83
9. Gleason FH, Kagami M, Lefèvre E, Sime-Ngando T (2008) The ecology of chytrids in aquatic ecosystems: roles in food web dynamics. Fungal Biol Rev 22: 17-25
10. Gromov BV, Pljusch AV, Mamkaeva KA (1999) Morphology and possible host range of Rhizophydium algavorum sp. nov (Chytridiales) and obligate parasite of algae. Protistology 1: 62-65
11. Hall TA (1998) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98
12. Hibbett DS, Binder M, Bischoff JF, Blackwell M and others (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111: 509-547 (Pubitemid 46915419)
13. Hillebrand H, Durselen CD, Kirshtel D, Pollingher U, Zohari T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35: 403-424 (Pubitemid 29228867)
14. Ibelings BW, de Bruin A, KagamiM, Rijkeboer M, Brehm M, Van Donk E (2004) Host parasite interactions between freshwater phytoplankton and chytrid fungi (Chytridiomycota). J Phycol 40: 437-453 (Pubitemid 38740373)
15. James TY, Letcher PM, Longcore JE, Mozley-Standridge SE and others (2006a) A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98: 860-871 (Pubitemid 46683210)
16. James TY, Kauff F, Schoch CL, Matheny PB and others (2006b) Reconstructing the early evolution of the fungi using a six gene phylogeny. Nature 443: 818-822 (Pubitemid 44622687)
17. JobardM, Rasconi S, Sime-Ngando T (2010) 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
18. Kagami M, 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
19. Kagami M, van Donk E, de Buin A, Rijkeboer M, Ibelings BW (2004) Daphnia can protect diatoms from fungal parasitism. Limnol Oceanogr 49: 680-685 (Pubitemid 38730111)
20. Kagami M, von Elert E, Ibelings BW, de Bruin A, van Donk E (2007a) The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella. Proc Biol Sci 274: 1561-1566 (Pubitemid 47056681)
21. Kagami M, de Bruin A, Ibelings BW, van Donk E (2007b) Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 578: 113-129 (Pubitemid 46352485)
22. Kagami M, Yosuke A, Nobuyoshi I (2012) Community structure of planktonic fungi and the impact of parasitic chytrids on phytoplankton in Lake Inba, Japan. Microb Ecol 63: 358-368
23. Le Calvez T, Burgaud G, Mahé S, Barbier G, Vandenkoornhuyse P (2009) Fungal diversity in deep-sea hydrothermal ecosystems. Appl Environ Microbiol 75: 6415-6421
24. Lee SM, Chao A (1994) Estimating population size via sample coverage for closed capture-recapture models. Biometrics 50: 88-97 (Pubitemid 24138576)
25. Lefèvre E, Bardot C, Noël C, Carrias JF, Viscogliosi E, Amblard C, 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 (Pubitemid 46058999)
26. Lefèvre E, Roussel B, Amblard C, Sime-Ngando T (2008) The molecular diversity of freshwater picoeukaryotes reveals high occurrence of putative parasitoids in the plankton. PLoS ONE 3: e2324
27. Lefèvre E, Jobard M, Venisse JS, Bec A, Kagami M, Amblard C, Sime-Ngando T (2010) Development of a Real-Time PCR assay for quantitative assessment of uncultured freshwater zoosporic fungi. J Microbiol Methods 81: 69-76
28. Lefranc M, Thénot A, Lepère C, Debroas D (2005) Genetic diversity of small eukaryotes in lakes differing by their trophic status. Appl Environ Microbiol 71: 5935-5942 (Pubitemid 41456887)
29. Lepère C, Domaizon I, Debroas D (2008) Unexpected importance of potential parasites in the composition of the freshwater small-eukaryote community. Appl Environ Microbiol 74: 2940-2949 (Pubitemid 351746995)
30. Letcher PM, Powell MJ (2001) Distribution of zoosporic fungi in forest soils of the Blue Ridge and Appalachian Mountains of Virginia. Mycologia 93: 1029-1041
31. Letcher PM, Powell MJ (2002) Frequency and distribution patterns of zoosporic fungi from moss-covered and exposed soils. Mycologia 94: 761-771 (Pubitemid 36166481)
32. Letcher PM, Powell MJ (2005a) Kappamyces, a new genus in the Chytridiales (Chytridiomycota). Nova Hedwigia 80: 115-133
33. Letcher PM, Powell MJ (2005b) Phylogenetic position of Phlyctochytrium planicorne (Chytridiales, Chytridiomycota) based on zoospore ultrastructure and partial nuclear LSU rRNA gene sequence analysis. Nova Hedwigia 80: 135-146
34. Letcher PM, Powell MJ, Chambers JG, Holznagel WE (2004a) Phylogenetic relationships among Rhizophydium isolates from North America and Australia. Mycologia 96: 1339-1351 (Pubitemid 40177936)
35. Letcher PM, McGee PA, Powell MJ (2004b) Diversity of chytrids from soils of four vegetation types in New South Wales Australia. Can J Bot 82: 1490-1500 (Pubitemid 40059448)
36. Letcher PM, Powell MJ, Chambers JG, Longcore JE, Churchill PF, Harris PM (2005) Ultrastructural and molecular delineation of the Chytridiaceae (Chytridiales). Can J Bot 83: 1561-1573 (Pubitemid 43799430)
37. Letcher PM, Powell MJ, Churchill PF, Chambers JG (2006) Ultrastructural and molecular phylogenetic delineation of a new order, the Rhizophydiales. Mycol Res 110: 898-915 (Pubitemid 44279411)
38. Letcher PM, Vélez CG, Barrantes ME, Powell MJ, Churchill PF, Wakefield WS (2008a) Ultrastructural and molecular analyses of Rhizophydiales (Chytridiomycota) isolates from North America and Argentina. Mycol Res 112: 759-782
39. Letcher PM, Powell MJ, Barr DJS, Churchill PF, Wakefield WS, Picard KT (2008b) Rhizophlyctidales - a new order in Chytridiomycota. Mycol Res 112: 1031-1048
40. Letcher PM, Powell MJ, Viusent MC (2008c) Rediscovery of an unusual chytridiaceous fungus new to the order Rhizophydiales. Mycologia 100: 325-334
41. Liggenstoffer AS, Youssef NH, Couger MB, Elshahed MS (2010) Phylogenetic diversity and community structure of anaerobic gut fungi (phylum Neocallimastigomycota) in ruminant and non-ruminant herbivores. ISME J 4: 1225-1235
42. LuoW, Bock C, Li HR, Padisak J, Krienitz L (2011) Molecular and microscopic diversity of planktonic eukaryotes in the oligotrophic Lake Stechlin (Germany). Hydrobiologia 661: 133-143
43. Miki T, Takimoto G, Kagami M (2011) Roles of parasitic fungi in aquatic food webs: a theoretical approach. Freshw Biol 56: 1173-1183
44. Monchy S, Sanciu G, Jobard M, Rasconi S and others (2011) Exploring and quantifying fungal diversity in freshwater lake ecosystems using rDNA cloning/sequencing and SSU tag pyrosequencing. Environ Microbiol 13: 1433-1453
45. Mozley-Standridge SE, Letcher PM, Longcore JE, Porter D, Simmons DR (2009) Cladochytriales - a new order in Chytridiomycota. Mycol Res 113: 498-507
46. Nagahama T, Takahashi E, Nagano Y, Abdel-Wahab MA, Masayuki M (2011) Molecular evidence that deepbranching fungi are major components in deep-sea methane cold-seep sediments. Environ Microbiol 13: 2359-2370
47. Nikolcheva LG, Bärlocher F (2004) Taxon-specific fungal primers reveal unexpected high diversity during leaf decomposition in a stream. Mycol Prog 3: 41-49
48. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817-818 (Pubitemid 28552116)
49. Powell MJ (1993) Looking at mycology with a Janus face: a glimpse at Chytridiomycetes active in the environment. Mycologia 85: 1-20 (Pubitemid 24411572)
50. Rasconi S, Jobard M, Jouve L, Sime-Ngando T (2009) Use of calcofluor white for detection, identification, and quanti - fication of phytoplanktonic fungal parasites. Appl Environ Microbiol 75: 2545-2553
51. Rasconi S, Niquil N, Sime-Ngando T (2012) Phytoplankton chytridiomycosis: community structure and infectivity of fungal parasites in aquatic ecosystems. Environ Microbiol 14: 2151-2170
52. Richards TA, Vepritskiy AA, Gouliamova DE, Nierzwicki-Bauer SA (2005) The molecular diversity of freshwater picoeukaryotes from an oligotrophic lake reveals di - verse, distinctive and globally dispersed lineages. Environ Microbiol 7: 1413-1425 (Pubitemid 41204935)
53. Seena S, Wynberg N, Bärlocher F (2008) Fungal diversity during leaf decomposition in a stream assessed through clone libraries. Fungal Divers 30: 1-14
54. Sigee DC (2005) Freshwater microbiology: biodiversity and dynamic interactions of microorganisms in the fresh - water environment. John Wiley and Sons, Chichester
55. Sikes DS, Lewis PO (2001) Beta software, version 1. PAUPRat: PAUP* implementation of the parsimony ratchet. Distributed by the authors. Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT
56. Simmons DR, James TY, Meyer AF, Longcore JE (2009) Lobulomycetales, a new order in the Chytridiomycota. Mycol Res 113: 450-460
57. Slapeta J, Moreira D, Lopez-Garcia P (2005) The extent of protist diversity: insights from molecular ecology of freshwater eukaryotes. Proc Biol Sci 272: 2073-2081 (Pubitemid 41416043)
58. Smith G (1950) The freshwater algae of the United States, 2nd edn. McGraw-Hill Book Company, Stanford, CA
59. Sogin ML, Morrison HG, Huber JA, Welch DM and others (2006) Microbial diversity in the deep sea and the unexplored 'rare biosphere'. Proc Natl Acad Sci USA 103: 12115-12120 (Pubitemid 44215820)
60. Sønstebø JH, Rohrlack T (2011) Possible implications of chytrid parasitism for population subdivision in fresh - water cyanobacteria of the genus Planktothrix. Appl Environ Microbiol 77: 1344-1351
61. Sparrow FK (1960) Aquatic phycomycetes, 2nd edn. The University of Michigan Press, Ann Arbor, MI
62. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), Version 4.0b10. Sinauer Associates, Sunderland, MA
63. Tanabe Y, Watanabe MM, Sugiyama J (2005) Evolutionary relationship among basal fungi (Chytridiomycota and Zygomycota): insights from molecular phylogenetics. J Gen Appl Microbiol 51: 267-276 (Pubitemid 41800141)
64. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882 (Pubitemid 28022245)
65. Vainio EJ, Hantula J (2000) Direct analysis of wood-inhabiting fungi using denaturing gradient electrophoresis of amplified ribosomal DNA. Mycol Res 104: 927-936
66. van Donk H, Ringelberg J (1983) The effect of fungal parasitism on the succession of diatoms in Lake Maarsseveen I (The Netherlands). Freshw Biol 13: 241-251 (Pubitemid 14272967)
67. Vélez CG, Letcher PM, Schultz S, PowellMJ (2011) Molecular phylogenetic and zoospore ultrastructural analyses of Chytridium olla establish the limits of a monophyletic Chytridiales. Mycologia 103: 118-130
68. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172: 4238-4246 (Pubitemid 20236711)
69. Wakefield WS, Powell MJ, Letcher PM, Barr DJF, Churchill PF, Longcore JE, Chen SF (2010) A molecular phylogenetic evaluation of the Spizellomycetales. Mycologia 102: 596-604
70. Ward GM, Harris PM, Ward AK (2005) Gulf Coast rivers of the southeastern United States. In: Benke AC, Cushing CE (eds) Rivers of North America. Elsevier Academic Press, Oxford, p 56-77
71. Wehr JD, Sheath RG (2003) Freshwater algae of North America: ecology and classification. Academic Press, San Diego, CA
72. Wetzel RG (2001) Limnology: lake and river ecosystems, 3rd edn. Academic Press, San Diego, CA
73. Wetzel RG, Likens GE (1990) Limnological analyses, 3rd edn. Springer, New York, NY
74. White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, London, p 315-322
75. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD dissertation, University of Texas, Austin, TX