The molecular diversity of freshwater picoeukaryotes reveals high occurrence of putative parasitoids in the plankton

PLoS ONE

Volumn 3, Issue 6, 2008, Pages

  Lefèvre, Emilie ^a   Roussel, Balbine ^a   Amblard, Christian ^a   Sime Ngando, Télesphore ^a  

^a UNIVERSITÉ BLAISE PASCAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA 18S; FRESH WATER; RNA 18S;

AQUATIC ENVIRONMENT; ARTICLE; AUTUMN; BACTERIVORE; BIODIVERSITY; EUKARYOTE; FLAGELLATE; FRANCE; FRESHWATER ENVIRONMENT; FRESHWATER SPECIES; FUNGUS; MOLECULAR GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE; PARASITOID; PELAGIC ZONE; PHYLOGENY; PLANKTON; SAPROTROPH; SPECIES DIVERSITY; SPRING; SUMMER; TAXONOMY; BAYES THEOREM; ECOLOGY; EUKARYOTIC CELL; GENETICS; MICROBIOLOGY; SPECIES DIFFERENCE;

ALVEOLATA; EUKARYOTA; FUNGI; MASTIGOPHORA (FLAGELLATES); OTUS; STRAMENOPILES; TELONEMA;

BAYES THEOREM; ECOLOGY; EUKARYOTIC CELLS; FRESH WATER; PHYLOGENY; PLANKTON; RNA, RIBOSOMAL, 18S; SPECIES SPECIFICITY; WATER MICROBIOLOGY;

EID: 48649090241     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002324     Document Type: Article

References (68)

1. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, et al. (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10: 257-263.
2. Laybourn-Parry J, Parry J (2000) Fagellates and the microbial loop. In The flagellates: Unity, diversity and evolution. Leadbeater BSC, Green JC, eds. London: Taylor and Francis. pp 216-239.
3. Gasol JM, Vaqué D (1993) Lack of coupling between heterotrophic nanoflagellates and bacteria: a general phenomenon across aquatic systems? Limnol Oceanogr 38: 657-665.
4. Gonzalez JM, Sultle CA (1993) Grazing by marine nanoflagellates on viruses and virus-sized particules: ingestion and digestion. Mar Ecol Prog Ser 94: 1-10.
5. Bettarel Y, Sime-Ngando T, Bouvy M, Arfi R, Amblard C (2005) Low consumption of virus-sized particles by heterotrophic nanonflagellates in two lakes of the French Massif Central. Aquat Microb Ecol 39: 205-209.
6. Sherr EB (1988) Direct use of high molecular weight polysaccharide by heterotrophic flagellates. Nature 335: 318-351
7. Tranvik LJ, Sherr EB, Sherr BF (1992) Uptake and utilization of 'colloidal DOM' by heterotrophic flagellates in seawater. Mar Ecol Prog Ser 92: 301-309.
8. Patterson DJ (1993) The current status of the free-living heterotrophic flagellates. J Eukaryot Microbiol 40: 606-609.
9. Carrias JF, Quiblier-Lloberas C, Bourdier G (1998) Seasonal dynamics of free and attached heterotrophic nanoflagellates in an oligomesotrophic lake. Freshwater Biol 39: 91-101.
10. Auer B, Arndt H (2001) Taxonomic composition and biomass of heterotrophic flagellates in relation to lake trophy and season. Freshwater Biol 46: 959-972.
11. Cleven E.-J, Weisse T (2001) Seasonal succession and taxon-specific bacterial grazing rates of heterotrophic nanolagellates in Lake Constance. Aquat Microb Ecol 23: 147-161.
12. Domaizon I, Viboud S, Fontvieille D (2003) Taxon-specific and seasonal variations in flagellates gazing on heterotrophic bacteria in the oligotrophic Lake Annecy - importance of mixotrophy. FEMS microbiol Ecol 46: 317-329.
13. Comte J, Jacquet S, Viboud S, Fontvieille D, Millery A, et al. (2006) Microbial community structure and dynamics in the largest natural French lake (Lake Bourget). Microb Ecol 52: 72-89.
14. Sonntag B, Posch T, Klammer S, Teubner K, Psenner R (2006) Phagotrophic ciliates and flagellates in an oligotrophic, deep, alpine lake: contrasting variability with seasons and depths. Aquat Microb Ecol 43: 193-207.
15. Wieltschnig C, Kirschner AKT, Steitz A, Velimirov B (2001) Weak coupling between heterotrophic nanoflagellates and becteria in a eutrophic freshwater environment. Microb Ecol 42: 159-167.
16. Diez B, Pedros-Alio C, 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.
17. Lopez-Garcia P, Rodriguez-Valera F, Pedro-Alio C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603-607.
18. Moon-van der Staay SY, De Wachter R, Vaulot D (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409: 607-610.
19. Moreira D, Lopez-Garcia P (2002) The molecular ecology of microbial eukaryotes unveils a hidden world. Trends Microbiol 10: 31-38.
20. Massana R, Balagué V, Guillou L, Pedros-alio C (2004) Picoeukaryotic diversity in an oligotrophic, coastal site studied by molecular and culturing approaches. FEMS Microbiol Ecol 50: 231-243.
21. Romari K, Vaulot D (2001) Composition and temporal variability of picoeukaryote communities at a coastal site or the english channel from 18S rDNA sequences. Limnol Occanogr 49: 784-798.
22. Not F, Gausling R, Azam F, Heidelberg JF, Worden AZ (2007) Vertical disuibution of picoeukaryotic diversity in the Sargasso Sea. Environ Microbiol 9: 1233-1252.
23. Lefevre E, Bardot C, Noël C, Carrias J.-F., Viscogliosi E, et al. (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.
24. Slapeta J, Moreira D, Lopez-Garcia P (2005) The extent of protist diversity. insights from molecular ecology of freshwater eukaryotes. Proc R Sac B 272: 2073-2081.
25. Lefrane 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.
26. Richards TA, Vepritskiy AA, Gouliamova DE, Nierzwicki-Bauer SA (2005) The molecular diversity of freshwater picoeukaryotes from oligotrophic lake reveals diverse, distinctive and globally dispersed lineages. Environ Microbiol 7: 1413-1425.
27. Lee WJ, Patterson DJ (1998) Diversity and geographic distribution of free-living heterotrophic flagellates - analysis by PRIMER. Protist 149: 229-244.
28. Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJM (2001) Counting the uncountable: Statistical approaches to estimating microbial diversity. Appl Environ Microbiol 67: 4399-4406.
29. Sleigh MA (2000) Trophic strategies. In The flagellates: Unity, diversity and evolution. Leadbeater BSC, Green JC, eds. London: Taylor and Francis. pp 147-165.
30. Leander BS, Kuvardina ON, Aleshin VV, Mylnikov AP, Keeling PJ (2003) Molecular phylogeny and surface morphology of Colpodella edax (Alveolata): insights into the phagotrophic ancestry of Apicomplexans. J Eukaryot Microbiol 50: 334-340.
31. Gleason FG, Gordon GLR (1989) Anaerobic growth and fermentation in Blastocladia. Mycologia 81: 811-815.
32. Edgcomb VP, Kysela DT, Teske A, de Vera Gomez A, Sogin ML (2002) Benthic eukaryotic diversity in the Guaymas basin hydrothermal vent environment. Proc Natl Acad Sci 99: 7658-7662.
33. Dawson SC, Pace NR (2002) Novel Kingdom-level eukaryotic diversity in anoxic environments. Proc Natl Acad Sci 99: 8324-8329.
34. Takishita K, Miyake H, Kawato M, Maruyama T (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.
35. Amaral Zettler LA, Gomez F, Zettler E, Keenan BG, Amils R, et al. (2002) Eukaryotic diversity in Spain's River of Fire. Nature 417: 137.
36. Burreson EM, Reece KS, Dungan CF (2005) Molecular, morphological, and experimental evidence support the synonymy of Perkinsus chesapeaki and Perkinsus andrewsi. J Eukaryot Microbiol 52: 258-270.
37. Brugerolle G (2002) Cryptophagus subtilis: a new parasite of cryptophytes affiliated with the perkinsozoa lineage. Europ J Protistol 37: 379-390.
38. Park MG, Cooney SK, Yih W, Coats DW (2002) Effect or two strains of the parasitic dinoflagellate Amoebopyrga on growth, photosynthesis, light absorption, and quantum yield of bloom-forming dinoflagellates. Mar Ecol Prog Ser 227: 281-292.
39. Arndt H, Dietrich D, Auer B, Cleven EJ, Gräfenhan T, et al. (2000) Functional diversity of heterotrophic flagellates in aquatic ecosystems. In The flagellates: Unity, diversity and evolution. Leadbeater BSC, Green JC, eds. London: Taylor and Francis. pp 240-268.
40. Sherr EB, Sherr BF (2008) Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Mar Ecol Prog Ser. 352: 187-197.
41. Letcher PM, Powell MJ, Churchill PF, Chambers JG (2006) Ultrastructural and molecular phylogenetic delineation of a new order, the Rhizophydiales (Chytridiomycota). Mycol. Res. 110: 898-915.
42. James TY, Porter D, Leander CA, Vilgalys R, Longcore JE (2000) Molecular phylogenetics of the Chytridiomycota supports the utility of ultrastructural data in chytrid systematics. Can J Bot 78: 336-350.
43. Bass D, Cavalier-Smith T (2004) Phylum-specific environmental DNA analysis reveals remarkably high global biodiversity of Cercozoa (Protozoa). Int J Syst Evol Microbiol 54: 2393-2404.
44. Shalchian-Tabrizi K, Eikrem W, Klaveness D, Vaulot D, Minge MA, et al. (2006) Telonemia, a new protist phylum with affinity to chromist lineages. Proc R Soc B 273: 1833-1842.
45. Klaveness D, Shalchian-Tabrizi K, Thomsen HA, Eikrem W, Jakobsen KS (2005) Telonema antarcticum sp. nov., a common marine phagotrophic flagellate. Int J Syst Evol Microbiol 55: 2595-2604.
46. Carrias J-F, Thouvenot A, Amblard C, Sime-Ngando T (2001) Dynamics and growth estimates of planktonic protists during early spring in Lake Pavin, France. Aquat Microb Ecol 24: 163-174.
47. Soudant P, Chu F-UE, Lund ED (2005) Assessment of the cell viability of cultured Perkinsus marinus (Perkinsea), a parasitic protozoan of the eastern oyster, Crassostrea virginica, using SYBRgreen-propidium iodide double staining and flow cytometry. J. Eukaryot Microbiol 52: 192-199.
48. Dugan CF, Reece KS, Moss JA, Hamilton RM, Diggles BK (2007) Perkinsus olsenii in vitro isolates from the New Zealand Clam Austrovenus slutchburyi. J Eukaryot Microbiol 51: 263-270.
49. Gestal C, Novoa B, Posada D., Figueras A, Azevedo C (2006) Perkinsoide chabelardi n. gen., a protozoan parasite with an intermediate evolutionary position: possible cause of the decrease of sardine fisheries? Environ Microbiol 8: 1105-1114.
50. Park MG, Yih W, Coats DW (2001) Parasites and phytoplankton, with special emphasis on dinoflagellate infections. J Eukaryot Microbiol 51: 145-155.
51. Coats DW, Adam EJ, Gallegos CL, Hedrick S (1996) Parasitism of photosynthetic dinoflagellates in a shallow subestuary of Chesapeake Bay, USA. Aquat Microb Ecol 11: 1-9.
52. Brugerolle G, Mignot JP (1979) Observations sur le cycle, l'ukrastructure et la position systémadque de Spiromonas perforans (Bodo perforans Hollande 1938), flagellé parasite cle Chilomonas paramecium: ses relations avec les dinoflagellés et sporozoaires. Protistologica 2: 183-196.
53. Siddall ME, Reece KS, Nerad TA, Buresson EM (2001) Molecular determination of the phylogenetic position of a species in the genus Colpodella (Alveolata). Am Mus Novit 3314: 1-10.
54. Alster A, Zohary T (2007) Interaction between the bloom-forming dinoflagellate Peridinium gatunense and the chytrid fungus Phlycloclytrium sp. Hydrobiologia 578: 131-139.
55. Ibelings BW, De Bruin A, Kagami M, Rijkeboer M, Brehm M, et al. (2004) Host parasite interactions between freshwater phytoplankton and chytrid Fungi (Chytridiomycota). J Phycol 40: 437-453.
56. Hausner G, Belkhiri A, Klassen GR (2000) Phylogenetic analysis of the small subunit ribosomal RNA gene of the hyphochytrid Rhizidiomyces apophysatus. Can J Bot 78: 124-128.
57. Nikolaev SI, Berney C, Fahrm J, Mylnikov AP, Aleshin VV, et al. (2003) Gymnophrys cometa and Lecythium sp. are core Cercozoa: Evolutionary implications. Acta Protozool 42: 183-190.
58. Mil'nikov AP, Karpov SA (2004) Review of diversity and taxonomy of cercomonads. Protistology 3: 201-217.
59. Schnepf E, Kühn SF (2000) Food uptake and line structure of Cryothecomonas longipes sp. nov., a marine nanciflagellate incertae sedis feeding phagotrophically on large diatoms. Helgol Mar Res 54: 18-32.
60. Debres G, Kühn SF, Gmelch A, Schnepf E (1996) Cryothecamonas aestwalis sp. nov., a colourless nanoflagellate feeding on the marine centric diatom Guinardia delicatula (Cleve) Hasle. Helgol Mar Res 50: 197-515.
61. Vickerman K, Le Ray D, Hoef-Emden K, De Jonckheere J (2002) The soil flagellate Proleptomonas faecicola: cell organisation and phylogeny suggest that the only described free-living trypanosomatid is not a kinetoplastid but has cercomonad affinities. Protist 153: 9-24.
62. Pomeroy LR (1974) The ocean's food webs, a changing paradigm. Bioscience 21: 499-504.
63. Hagström A, Azant F, Andersson A, Wikner J, Rassoulzadegan F (1988) Microbial loop in an oligotrophic pelagic marine ecosystem: possible roles of cyanobacteria and nanoflagellates in the organic fluxes. Mar Ecol Prog Ser 49: 171-178.
64. Pomeroy LR, Wiebe WJ (1988) Energetics of microbial food webs. Hydrobiologia 159: 7-18.
65. Sherr EB, Sheer BF (1988) Role of microbes in pelagic food webs: a revised concept. Limnol Oceanogr 33: 1225-1227.
66. Kagami M, Van Donk E, de Bruin A, Rijkeboer M, Ibelings BW (2004) Daphnia can protect diatoms from fungal parasitism. Limnol Oceanogr 49: 680-685.
67. Kagami M, De Bruin A, Ibelings BW, Van Donk E (2007a) Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydobiologia 578: 113-129.
68. Kagami M, von Alert E, Ibelings BW, de Bruin A, 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.