Microbial eukaryote life in the new hypersaline deep-sea basin Thetis

Extremophiles

Volumn 16, Issue 1, 2012, Pages 21-34

  Stock, Alexandra ^a   Breiner, Hans Werner ^a   Pachiadaki, Maria ^a   Edgcomb, Virginia ^b   Filker, Sabine ^a   La Cono, Violetta ^c   Yakimov, Michail M ^c   Stoeck, Thorsten ^a  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^b WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^c CNR   (Italy)

Author keywords

Brine basins; Community analyses; Microbial eukaryotes; Protistan cell counts; SSU rRNA

Indexed keywords

COMPLEMENTARY DNA; RNA 18S; SEA WATER; SODIUM CHLORIDE;

ARTICLE; CHEMISTRY; GENETICS; MARINE BIOLOGY; MICROBIOLOGY; PHYLOGENY;

DNA, COMPLEMENTARY; MARINE BIOLOGY; PHYLOGENY; RNA, RIBOSOMAL, 18S; SEAWATER; SODIUM CHLORIDE; WATER MICROBIOLOGY;

CILIOPHORA; EUKARYOTA; FUNGI; PROTISTA; STRAMENOPILES;

EID: 84155180940     PISSN: 14310651     EISSN: 14334909     Source Type: Journal    
DOI: 10.1007/s00792-011-0401-4     Document Type: Article

References (74)

1. Alexander E, Stock A, Breiner HW, Behnke A, Bunge J, Yakimov MM, Stoeck T (2009) Microbial eukaryotes in the hypersaline anoxic L'Atalante deep-sea basin. Environ Microbiol 11: 360-381.
2. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
3. Bass D, Howe A, Brown N, Barton H, Demidova M, Michelle H, Li L, Sanders H, Watkinson SC, Willcock S, Richards TA (2007) Yeast forms dominate fungal diversity in the deep oceans. Proc Royal Soc Lond Ser B Biol Sci 274: 3069-3077.
4. Burgaud G, Le Calvez T, Arzur D, Vandenkoornhuyse P, Barbier G (2009) Diversity of culturable marine filamentous fungi from deep-sea hydrothermal vents. Environ Microbiol 11: 1588-1600.
5. Butschinsky P (1897) Die Protozooenfauna der Salzsee-Limane bei Odessa. Zool Anz 20: 194-197.
6. Cantrell SA, Casillas-Martinez L, Molina M (2006) Characterization of fungi from hypersaline environments of solar salterns using morphological and molecular techniques. Mycol Res 110: 962-970.
7. Caron DA, Gast RJ (2008) The diversity of free-living protists seen and unseen, cultured and uncultured. In: Zengler K (ed) Accessing uncultivated microorganisms. From the environment to organisms and genomes and back. ASM Press, Washington, pp 67-93.
8. Caron DA, Countway PD, Savai P, Gast RJ, Schnetzer A, Moorthi SD, Dennett MR, Moran DM, Jones AC (2009) Defining DNA-based operational taxonomic units for microbial-eukaryote ecology. Appl Environ Microbiol 75: 5797-5808.
9. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
10. Chao A, Shen TJ (2003-2005) Program SPADE (species prediction and diversity estimates). http://chao. stat. nthu. edu. tw.
11. Chao A, Chazdon RL, Colwell RK, Shen TJ (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8: 148-159.
12. Clarke KJ, Finlay BJ, Esteban G, Guhl BE, Embley TM (1993) Cyclidium porcatum n. sp: a free-living anaerobic scuticociliate containing a stable complex of hydrogenosomes, eubacteria and archaeobacteria. Eur J Protistol 29: 262-270.
13. Colwell RK (2009) EstimateS: statistical estimation of species richness and shared species from samples. Version 8. 2. User's Guide and application.
14. Cox CS (1993) Roles of water molecules in bacteria and viruses. Orig Life Evol Biosph 23: 29-36.
15. D'Elia T, Veerapaneni R, Theraisnathan V, Rogers SO (2009) Isolation of fungi from Lake Vostok accretion ice. Mycologia 101: 751-763.
16. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
17. 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 USA 99: 7658-7662.
18. Edgcomb V, Orsi W, Leslin C, Epstein S, Bunge J, Jeon S, Yakimov MM, Behnke A, Stoeck T (2009) Protistan community patterns within the brine and halocline of deep hypersaline anoxic basins in the eastern Mediterranean Sea. Extremophiles 13: 151-167.
19. Edgcomb VP, Beaudoin D, Gast R, Biddle JF, Teske A (2011) Marine subsurface eukaryotes: the fungal majority. Environ Microbiol 13: 172-183.
20. Elloumi J, Carrias J-F, Ayadi H, Sime-Ngando T, Boukhris M, Bouain A (2006) Composition and distribution of planktonic ciliates from ponds of different salinity in the solar saltwork of Sfax, Tunisia. Estuar Coast Shelf Sci 67: 21-29.
21. Enz G (1879) Über einige Infusorien des Salzteiches zu Szamosfalva. Termes Füzetek 3: 1-40.
22. Epstein S, López-García P (2007) "Missing" protists: a molecular prospective. Biodivers Conserv 17: 261-276.
23. Esteban GF, Finlay BJ (2003) Cryptic freshwater ciliates in a hypersaline lagoon. Protist 154: 411-418.
24. Fenchel T, Bernard C (1996) Behavioural responses in oxygen gradients of ciliates from microbial mats. Eur J Protistol 32: 55-63.
25. Finlay BJ, Esteban GF, Brown S, Fenchel T, Hoef-Emden K (2006) Multiple cosmopolitan ecotypes within a microbial eukaryote morphospecies. Protist 157: 377-390.
26. Florentin R (1899) Etudes sur la faune des mares salées de Lorraine. Ann Sci Nat Zool 10: 209-350.
27. Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12: 543-548.
28. Giovannoni SJ, DeLong EF, Olsen GJ, Pace NR (1988) Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells. J Bacteriol 170: 720-726.
29. Gomez F, Moreira D, Benzerara K, López-García P (2011) Solenicola setigera is the first characterized member of the abundant and cosmopolitan uncultured marine stramenopile group MAST-3. Environ Microbiol 13(1): 193-202.
30. Guillou L, Viprey M, Chambouvet A, Welsh RM, Kirkham AR, Massana R, Scanlan DJ, Worden AZ (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol 10: 3349-3365.
31. Gunde-Cimerman N, Zalar P, de Hoog S, Plemenitaš A (2000) Hypersaline waters in salterns-natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32: 235-240.
32. Gunde-Cimerman N, Ramos J, Plemenitaš A (2009) Halotolerant and halophilic fungi. Mycol Res 113: 1231-1241.
33. Henneguy F (1890) Sur un Infusoire heterotriche, Fabrea salina. Ann d'Micrographie 3: 118-135.
34. Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol Ecol 10: 1855-1871.
35. Iwataki M, Kawami H, Matsuoka K (2007) Cochlodinium fulvescens sp. nov. (Gymnodiniales, Dinophyceae), a new chain-forming unarmored dinoflagellate from Asian coasts. Phycol Res 55: 231-239.
36. Jebaraj CS, Raghukumar C, Behnke A, Stoeck T (2010) Fungal diversity in oxygen-depleted regions of the Arabian Sea revealed by targeted environmental sequencing combined with cultivation. FEMS Microbiol Ecol 71: 399-412.
37. Kunte HJ, Trüper H, Stan-Lotter H (2002) Halophilic microorganisms. In: Horneck G, Baumstark-Khan C (eds) Astrobiology: the quest for the conditions of life. Springer, Berlin, pp 185-200.
38. La Cono V, Smedile F, Bortoluzzi G, Arcadi E, Maimone G, Messina E, Borghini M, Olliveri E, Mazzola S, L'Haridon S, Toffin L, Genovese L, Ferrer M, Giuliano L, Golyshin PN, Yakimov MM (2011) Unveiling microbial life in new deep-sea hypersaline Lake Thetis. Part I: prokaryotes and environmental settings. Environ Microbiol 13(8): 2250-2268.
39. Lahav R, Fareleira P, Nejidat A, Abeliovich A (2002) The identification and characterization of osmotolerant yeast isolates from chemical wastewater evaporation ponds. Microb Ecol 43: 388-396.
40. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115-148.
41. Le Calvez T, Burgaud G, Mahe S, Barbier G, Vandenkoornhuyse P (2009) Fungal diversity in deep-sea hydrothermal ecosystems. Appl Environ Microbiol 75: 6415-6421.
42. Liu H, Probert I, Uitz J, Claustre H, Aris-Brosou S, Frada M, Not F, de Vargas C (2009) Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans. Proc Natl Acad Sci USA 106: 12803-12808.
43. Lozupone C, Knight R (2008) Species divergence and the measurement of microbial diversity. FEMS Microbiol Rev 32: 557-578.
44. Ma Y, Galinski EA, Grant WD, Oren A, Ventosa A (2010) Halophiles 2010: life in saline environments. Appl Environ Microbiol 76: 6971-6981.
45. MacGregor BJ, Moser DP, Baker BJ, Alm EW, Maurer M, Nealson KH, Stahl DA (2001) Seasonal and spatial variability in Lake Michigan sediment small-subunit rRNA concentrations. Appl Environ Microbiol 67: 3908-3922.
46. Massana R, Guillou L, Díez B, Pedrós-Alió C (2002) Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Appl Environ Microbiol 68: 4554-4558.
47. Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71: 491-499.
48. Mills HJ, Martinez RJ, Story S, Sobecky PA (2005) Characterization of microbial community structure in Gulf of Mexico gas hydrates: comparative analysis of DNA- and RNA-derived clone libraries. Appl Environ Microbiol 71: 3235-3247.
49. Nagahama T, Hamamoto M, Nakase T, Takami H, Horikoshi K (2001) Distribution and identification of red yeasts in deep-sea environments around the northwest Pacific Ocean. Antonie van Leeuwenhoek 80: 101-110.
50. Nebel M, Pfabel C, Stock A, Dunthorn M, Stoeck T (2010) Delimiting operational taxonomic units for assessing ciliate environmental diversity using small-subunit rRNA gene sequences. Environ Microbiol Rep 3: 154-158.
51. Oren A (2005) A hundred years of Dunaliella research: 1905-2005. Saline Syst 1: 2.
52. Park JS, Simpson AG (2010) Characterization of halotolerant Bicosoecida and Placididea (Stramenopila) that are distinct from marine forms, and the phylogenetic pattern of salinity preference in heterotrophic stramenopiles. Environ Microbiol 12: 1173-1184.
53. Park JS, Kim H, Choi DH, Cho BC (2003) Active flagellates grazing on prokaryotes in high salinity waters of a solar saltern. Aquat Microb Ecol 33: 173-179.
54. Park JS, Cho BC, Simpson AG (2006) Halocafeteria seosinensis gen. et sp. nov. (Bicosoecida), a halophilic bacterivorous nanoflagellate isolated from a solar saltern. Extremophiles 10: 493-504.
55. Park JS, Simpson AG, Lee WJ, Cho BC (2007) Ultrastructure and phylogenetic placement within Heterolobosea of the previously unclassified, extremely halophilic heterotrophic flagellate Pleurostomum flabellatum (Ruinen 1938). Protist 158: 397-413.
56. Patterson DJ, Simpson AG (1996) Heterotrophic flagellates from coastal marine and hypersaline sediments in Western Australia. Eur J Protistol 32: 423-448.
57. Pedrós-Alió C (2004) Trophic ecology of solar salterns. In: Ventosa A (ed) Halophilic microorganisms. Springer, Berlin, pp 33-48.
58. Pedrós-Alió C, Calderón-Paz JI, MacLean MH, Medina G, Marrasé C, Gasol JM, Guixa-Boixereu N (2000) The microbial food web along salinity gradients. FEMS Microbiol Ecol 32: 143-155.
59. Pernthaler J, Glöckner FO, Schönhuber W, Amann R (2001) Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. In: Paul JH (ed) Methods in microbiology. Academic Press, San Diego, pp 207-226.
60. Post FJ, Borowitzka LJ, Borowitzka MA, Mackay B, Moulton T (1983) The protozoa of a western Australian hypersaline lagoon. Hydrobiologia 105: 95-113.
61. Prokopowich CD, Gregory TR, Crease TJ (2003) The correlation between rDNA copy number and genome size in eukaryotes. Genome 46: 48-50.
62. Ruinen J (1938a) Notizen über Ciliaten aus konzentrierten Salzgewässern. Zool Meded 20: 243-256.
63. Ruinen J (1938b) Notizen über Salzflagellaten II. Über die Verbreitung der Salzflagellaten. Arch Protistenk 90: 210-258.
64. Skovgaard A, Legrand C (2005) Observation of live specimens of Pseudotontonia cornuta (Ciliophora: Oligotrichida) reveals new distinctive characters. J Mar Biol Ass UK 85: 783-786.
65. Stamatakis A, Hoover P, Rougemont J (2008) A fast bootstrapping algorithm for the RAxML web-servers. Syst Biol 57: 758-771.
66. Stoeck T, Zuendorf A, Breiner HW, Behnke A (2007) A molecular approach to identify active microbes in environmental eukaryote clone libraries. Microbiol Ecol 53: 328-339.
67. Stoecker DK, Gustafson DE, Merrell JR, Black MMD, Baier CT (1997) Excystment and growth of chrysophytes and dinoflagellates at low temperatures and high salinities in Antarctic sea-ice. J Phycol 33: 585-595.
68. Tucolesco J (1962) Etudes Protozoologiques sur les eaux Roumaines. I. Espèces nouvelles d'Infusoires de la mer Noire et des bassins salés paramarins. Arch Protistenk 106: 1-36.
69. Vaupotič T, Gunde-Cimerman N, Plemenitaš A (2007) Novel 3′-phosphoadenosine-5′-phosphatases from extremely halotolerant Hortaea werneckii reveal insight into molecular determinants of salt tolerance of black yeasts. Fungal Genet Biol 44: 1109-1122.
70. Vengosh A, Starinsky A (1993) Relics of evaporated sea water in deep basins of the eastern Mediterranean. Mar Geol 1: 15-19.
71. Voronin LV (2010) The fungi of small acid lakes. Inland Water Biol 3: 254-259.
72. Wilbert N (1995) Benthic ciliates of salt lakes. Acta Protozool 34: 271-288.
73. Zhadanova NN, Zakharchenko V, Vember VV, Nakonechnaya LT (2000) Fungi from Chernobyl: mycobiota of the inner regions of the containment structures of the damaged nuclear reactor. Mycol Res 104: 1421-1426.
74. Zhu F, Massana R, Not F, Marie D, Vaulot D (2005) Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. FEMS Microb Ecol 52: 79-92.