Protistan microbial observatory in the Cariaco Basin, Caribbean. II. Habitat specialization

ISME Journal

Volumn 5, Issue 8, 2011, Pages 1357-1373

  Orsi, William ^a   Edgcomb, Virginia ^b   Jeon, Sunok ^c   Leslin, Chesley ^a   Bunge, John ^d   Taylor, Gordon T ^e   Varela, Ramon ^f   Epstein, Slava ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^c Kangwon National University   (South Korea)

^d Cornell University ^*  (United States)

^e STONY BROOK UNIVERSITY   (United States)

^f FUNDACIÓN LA SALLE DE CIENCIAS NATURALES   (Venezuela)

Author keywords

18S rRNA approach; anoxic; diversity; protists

Indexed keywords

PROTOZOAL RNA; RIBOSOME RNA; SEA WATER;

ANOXIC CONDITIONS; CANONICAL ANALYSIS; COMPARATIVE STUDY; EUKARYOTE; GENETIC ANALYSIS; HABITAT TYPE; MICROBIAL ACTIVITY; OBSERVATIONAL METHOD; PHYLOGENETICS; POPULATION DISTRIBUTION; SPATIOTEMPORAL ANALYSIS; SPECIALIZATION; SPECIES DIVERSITY; SPECIES RICHNESS; TAXONOMY; WATER COLUMN;

ARTICLE; CENTRAL AMERICA; ECOSYSTEM; EUKARYOTE; GENETICS; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; VENEZUELA;

CARIBBEAN REGION; ECOSYSTEM; EUKARYOTA; PHYLOGENY; RNA, PROTOZOAN; RNA, RIBOSOMAL; SEAWATER; VENEZUELA;

ATLANTIC OCEAN; CARIACO BASIN; CARIBBEAN SEA;

EUKARYOTA; OTUS; PROTISTA;

EID: 79960558703     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2011.7     Document Type: Article

References (91)

1. Alexander E, Stock A, Breiner HW, Behnke A, Bunge J, Yakimov MM et al. (2009). Microbial eukaryotes in the hypersaline anoxic L0Atalante deep-sea basin. Environ Microbiol 11: 360-381.
2. Aristegui J, Gasol JM, Duarte CM, Herndl GJ. (2009). Microbial oceanography of the dark ocean's pelagic realm. Limnol Oceanogr 54: 1501-1529.
3. Astor Y, Muller-Karger F, Scranton MI. (2003). Seasonal and interannual variation in the hydrography of the Cariaco Basin: implications for basin ventilation. Cont Shelf Res 23: 125-144. (Pubitemid 36093284)
4. Azam F, Fenchel T, Field J, Gray J, Meyer-Reil L, Thingstad F. (1983). The ecological role of water column microbes in the sea. Mar Ecol Prog Ser 10: 257-263.
5. Bass D, Richards TA, Matthai L, Marsh V, Cavalier-Smith T. (2007). DNA evidence for global dispersal and probable endemicity of protozoa. BMC Evol Biol 7: 162.
6. Behnke A, Bunge J, Barger K, Breiner HW, Alla V, Stoeck T. (2006). Microeukaryote community patterns along an O2/H2S gradient in a supersulfidic anoxic fjord (Framvaren, Norway). Appl Environ Microbiol 72: 3626-3636. (Pubitemid 43728019)
7. Beijerinck MW. (1913). De Infusies En De Ontdekking Der Backteriën. Jaarboek Van De Koninklijke Akademie Voor Wetenschappen. Müller: Amsterdam, The Netherlands.
8. Berman T, Nawrocki M, Taylor GT, Karl DM. (1987). Nutrient flux between bacteria, bacterivorous nano-protozoans and algae. Mar Microb Food Webs (now Aquat Microb Ecol) 2: 69-82.
9. Bernhard JM, Buck KR, Farmer MA, Bowser SS. (2000). The Santa Barbara Basin is a symbiosis oasis. Nature 403: 77-80. (Pubitemid 30038523)
10. Boenigk J, Pfandl K, Garstecki T, Harms H, Novarino G, Chatzinotas A. (2006). Evidence for geographic isolation and signs of endemism within a protistan morphospecies. Appl Environ Microbiol 72: 5159-5164.
11. Bunge J. (2011). Estimating the number of species with CatchAll. Proceedings of the 2011 Pacific Symposium on Biocomputing.
12. Caron DA. (1994). Inorganic nutrients, bacteria, and the microbial loop. Microb Ecol 28: 295-298.
13. Caron DA (ed.) (2000). Protistan Herbivory and Bacter-ivory. Academic Press: London, pp 289-315.
14. Cavalier-Smith T. (2004). Only six kingdoms of life. Proc Biol Sci 271: 1251-1262. (Pubitemid 38789317)
15. Chambouvet A, Morin P, Marie D, Guillou L. (2008). Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science 322: 1254-1257.
16. Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA. (2003). The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31: 442-443. (Pubitemid 36150424)
17. Countway PD, Gast RJ, Dennett MR, Savai P, Rose JM, Caron DA. (2007). Distinct protistan assemblages characterize the euphotic zone and deep sea (2500m) of the western North Atlantic (Sargasso Sea and Gulf Stream). Environ Microbiol 9: 1219-1232. (Pubitemid 46697275)
18. Countway PD, Gast RJ, Savai P, Caron DA. (2005). Protistan diversity estimates based on 18S rDNA from seawater incubations in the Western North Atlantic. J Eukaryot Microbiol 52: 95-106. (Pubitemid 43934158)
19. Dolven JK, Lindqvist C, Albert VA, Bjorklund KR, Yuasa T, Takahashi O et al. (2007). Molecular diversity of alveolates associated with neritic north atlantic radio-larians. Protist 158: 65-76. (Pubitemid 44969623)
20. Edgcomb V, Orsi W, Leslin C, Epstein SS, Bunge J, Jeon S et al. (2009). Protistan community patterns within the brine and halocline of deep hypersaline anoxic basins in the eastern Mediterranean Sea. Extremophiles 13: 151-167.
21. 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. (Pubitemid 34568747)
22. Ewing B, Green P. (1998). Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8: 186-194. (Pubitemid 28177230)
23. Ewing B, Hillier L, Wendl MC, Green P. (1998). Base-calling of automated sequencer traces using phred.I. Accuracy assessment. Genome Res 8: 175-185. (Pubitemid 28177229)
24. Fenchel T. (1987). Ecology of Protozoa. Springer: Berlin.
25. Fenchel T, Blackburn N. (1999). Motile chemosensory behaviour of phagotrophic protists: mechanisms for and efficiency in congregating at food patches. Protist 150: 325-336. (Pubitemid 29532243)
26. Fenchel T, Finlay BJ. (2004). The ubiquity of small species: patterns of local and global diversity. Bioscience 54: 777-784. (Pubitemid 39073976)
27. Finlay BJ. (2002). Global dispersal of free-living microbial eukaryote species. Science 296: 1061-1063. (Pubitemid 34517112)
28. Finlay BJ, Clarke KJ. (1999). Apparent global ubiquity of species in the protist genus Paraphysomonas. Protist 150: 419-430. (Pubitemid 30097590)
29. Finlay BJ, Esteban GF, Clarke KJ, Olmo JL. (2001). Biodiversity of terrestrial protozoa appears homogeneous across local and global spatial scales. Protist 152: 355-366. (Pubitemid 34085319)
30. Finlay BJ, Fenchel T. (1999). Divergent perspectives on protist species richness. Protist 150: 229-233. (Pubitemid 29532235)
31. Finlay BJ, Fenchel T. (2001). Protozoan community structure in a fractal soil environment. Protist 152: 203-218. (Pubitemid 32956403)
32. Foissner W. (1999). Protist diversity: estimates of the near-imponderable. Protist 150: 363-368. (Pubitemid 30097585)
33. Foissner W. (2006). Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool 45: 111-136. (Pubitemid 43772500)
34. Frias-Lopez J, Thompson A, Waldbauer J, Chisholm SW. (2009). Use of stable isotope-labelled cells to identify active grazers of picocyanobacteria in ocean surface waters. Environ Microbiol 11: 512-525.
35. Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL et al. (2008). A latitudinal diversity gradient in planktonic marine bacteria. Proc Natl Acad Sci USA 105: 7774-7778. (Pubitemid 351872714)
36. Guillou L, Viprey M, Chambouvet A, Welsh RM, Kirkham AR, Massana R et al. (2008). Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol 10: 3349-3365.
37. Heino J, Mauricio Bini L, Karjalainen SM, Mykra H, Soininen J, Vieira LCG et al. (2010). Geographical patterns of micro-organismal community structure: are diatoms ubiquitously distributed across boreal streams? Oikos 119: 129-137.
38. Heino J, Soininen J. (2006). Regional occupancy in unicellular eukaryotes: a reflection of niche breadth, habitat availability or size-related dispersal capacity? Freshwater Biol 51: 672-685.
39. Hong SH, Bunge J, Jeon SO, Epstein SS. (2006). Predicting microbial species richness. Proc Natl Acad Sci USA 103: 117-122. (Pubitemid 43076114)
40. Jeon SO, Bunge J, Stoeck T, Barger KJ, Hong SH, Epstein SS. (2006). Synthetic statistical approach reveals a high degree of richness of microbial eukaryotes in an anoxic water column. Appl Environ Microbiol 72: 6578-6583. (Pubitemid 44582896)
41. Jumars PA, Penry DL, Baross JA, Perry MJ, Frost BW. (1989). Closing the the microbial loop: dissolved carbon pathway to heterotrophic bacteria from incomplete ingestion, digestion and absorption in animals. Deep-Sea Res 36: 483-495.
42. Jurgens K, Massana R (eds). (2008). Protistan Grazing on Marine Bacterioplankton. Wiley: New York, pp 383-441.
43. Kolchin VF, Chistyakov VP. (1975). Combinatorial problems of probability theory. J Math Sci 4: 217-243.
44. Kolodziej K, Stoeck T. (2007). Cellular identification of a novel uncultured marine stramenopile (MAST-12 Clade) small-subunit rRNA gene sequence from a Norwegian estuary by use of fluorescence in situ hybridization scanning electron microscopy. Appl Environ Microbiol 73: 2718-2726. (Pubitemid 46668766)
45. Lara E, Moreira D, Vereshchaka A, Lopez-Garcia P. (2009). Pan-oceanic distribution of new highly diverse clades of deep-sea diplonemids. Environ Microbiol 11: 47-55.
46. Lawley B, Ripley S, Bridge P, Convey P. (2004). Molecular analysis of geographic patterns of eukaryotic diversity in Antarctic soils. Appl Environ Microbiol 70: 5963-5972. (Pubitemid 39471842)
47. Li XN, Taylor GT, Astor Y, Scranton M. (2008). Relationship of sulfur speciation to hydrographic conditions and chemoautotrophic production in the Cariaco Basin. Marine Chem 112: 53-64.
48. Lin X, Wakeham SG, Putnam IF, Astor YM, Scranton MI, Chistoserdov AY et al. (2006). Comparison of vertical distributions of prokaryotic assemblages in the anoxic Cariaco Basin and Black Sea by use of fluorescence in situ hybridization. Appl Environ Microbiol 72: 2679-2690.
49. Lin XJ, Scranton MI, Chistoserdov AY, Varela R, Taylor GT. (2008). Spatiotemporal dynamics of bacterial populations in the anoxic Cariaco Basin. Limnol Oceanogr 53: 37-51. (Pubitemid 351186008)
50. Lin XJ, Scranton MI, Varela R, Chistoserdov A, Taylor GT. (2007). Compositional responses of bacterial communities to redox gradients and grazing in the anoxic Cariaco Basin. Aquat Microb Ecol 47: 57-72. (Pubitemid 47343608)
51. Lopez-Garcia P, Rodriguez-Valera F, Pedros-Alio C, Moreira D. (2001). Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603-607. (Pubitemid 32154809)
52. Lopez-Garcia P, Vereshchaka A, Moreira D. (2007). Eukaryotic diversity associated with carbonates and fluid-seawater interface in Lost city hydrothermal field. Environ Microbiol 9: 546-554. (Pubitemid 46072140)
53. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhu kumar et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371. (Pubitemid 38854737)
54. Madsen EL, Sinclair JL, Ghiorse WC. (1991). In situ biodegradation: microbiological patterns in a contaminated aquifer. Science 252: 830-833. (Pubitemid 121000521)
55. Martiny JB, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL et al. (2006). Microbial bio-geography: putting microorganisms on the map. Nat Rev Microbiol 4: 102-112. (Pubitemid 43158153)
56. Massana R, Castresana J, Balague V, Guillou L, Romari K, Groisillier A et al. (2004). Phylogenetic and ecological analysis of novel marine stramenopiles. Appl Environ Microbiol 70: 3528-3534. (Pubitemid 38745900)
57. Massana R, Guillou L, Diez B, Pedros-Alio C. (2002). Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Appl Environ Microbiol 68: 4554-4558. (Pubitemid 34988141)
58. Massana R, Terrado R, Forn I, Lovejoy C, Pedros-Alio C. (2006). Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environ Microbiol 8: 1515-1522. (Pubitemid 44167978)
59. Massana R, Unrein F, Rodriguez-Martinez R, Forn I, Lefort T, Pinhassi J et al. (2009). Grazing rates and functional diversity of uncultured heterotrophic flagellates. ISME J 3: 588-596.
60. McCune B, Grace JB. (2002). Analysis of Ecological Communities. MJM Software Design. Gleneden: Oregon.
61. 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. (Pubitemid 32154810)
62. Muller-Karger F, Varela R, Thunell R, Scranton M, Bohrer R, Taylor GT et al. (2001a). Annual cycle of primary production in the Cariaco Basin: response to upwelling and implications for vertical transport. J Geophys Res 106: 4527-4542.
63. Muller-Karger F, Varela R, Thunell R, Scranton M, Bohrer R, Taylor GT et al. (2001b). Annual cycle of primary production in the Cariaco Basin: response to upwelling and implications for vertical export. J Geophys. Res. 106: 4527-4542.
64. Not F, Gausling R, Azam F, Heidelberg JF, Worden AZ. (2007). Vertical distribution of picoeukaryotic diversity in the Sargasso Sea. Environ Microbiol 9: 1233-1252. (Pubitemid 46697276)
65. Pernthaler J. (2005). Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3: 537-546. (Pubitemid 40903877)
66. Piganeau G, Desdevises Y, Derelle E, Moreau H. (2008). Picoeukaryotic sequences in the Sargasso sea meta-genome. Genome Biol 9: R5.
67. Piganeau G, Moreau H. (2007). Screening the Sargasso Sea metagenome for data to investigate genome evolution in Ostreococcus (Prasinophyceae, Chlorophyta). Gene 406: 184-190. (Pubitemid 350225638)
68. Richards F. (1975). The Cariaco Basin (Trench). Oceanogr Mar Bio Ann Rev 13: 11-67.
69. Richards TA, Bass D. (2005). Molecular screening of free-living microbial eukaryotes: diversity and distribution using a meta-analysis. Curr Opin Microbiol 8: 240-252. (Pubitemid 40813065)
70. Rutherford S, D0Hondt S, Prell W. (1999). Environmental controls on the geographic distribution of zooplankton diversity. Nature 400: 749-753. (Pubitemid 29399533)
71. Scranton M, Astor Y, Bohrer R, Ho T, Muller-Karger F. (2001). Controls on temporal variability of the geochemistry of the deep Cariaco Basin. Deep-Sea Res I 48: 1605-1625. (Pubitemid 32411735)
72. Scranton M, Sayles F, Bacon M, Brewer P. (1987). Temporal changes in the hydrography and chemistry of the Cariaco Trench. Deep-Sea Res I 34: 945-963.
73. Sherr EB, Sherr BF. (1994). Bacterivory and herbivory: key roles of phagotrophic protists in pelagic food webs. Microb Ecol 28: 223-235.
74. Sherr EB, Sherr BF. (2002). Significance of predation by protists in aquatic microbial food webs. Antonie Leeuwenhoek 81: 293-308. (Pubitemid 35314618)
75. Skovgaard A, Massana R, Balague V, Saiz E. (2005). Phylo-genetic position of the copepod-infesting parasite Syndinium turbo (Dinoflagellata, Syndinea). Protist 156: 413-423. (Pubitemid 41682019)
76. Soininen J, Heino J. (2007). Variation in niche parameters along the diversity gradient of unicellular eukaryote assemblages. Protist 158: 181-191. (Pubitemid 46467507)
77. Stoeck T, Bass D, Nebel M, Christe R, Jones MDH, Breiner H-W et al. (2010). Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol 19: 21-31.
78. Stoeck T, Behnke A, Christen R, Amaral-Zettler L, Rodriguez-Mora MJ, Chistoserdov A et al. (2009). Massively parallel tag sequencing reveals the complexity of anaerobic marine protistan communities. BMC Biol 7: 72.
79. Stoeck T, Hayward B, Taylor GT, Varela R, Epstein SS. (2006). A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples. Protist 157: 31-43. (Pubitemid 43220715)
80. Stoeck T, Kasper J, Bunge J, Leslin C, Ilyin V, Epstein S. (2007). Protistan diversity in the arctic: a case of paleoclimate shaping modern biodiversity? PLoS ONE 2: e728.
81. Stoeck T, Taylor GT, Epstein SS. (2003). Novel eukaryotes from the permanently anoxic Cariaco Basin (Caribbean Sea). Appl Environ Microbiol 69: 5656-5663. (Pubitemid 37150793)
82. Taylor GT. (1982). The role of pelagic heterotrophic protozoa in nutrient cycling: a review. Ann Inst Oceanogr (Suppl.), Paris 58: 227-241.
83. Taylor GT, Iabichella-Armas M, Varela R, Müller-Karger F, Lin X, Scranton MI. (2006). Microbial ecology of the Cariaco basin's redoxcline. In: Neretin NL (ed.). Past and Present Water Column Anoxia. Springer: Dordrecht, The Netherlands, pp 473-499.
84. Taylor GT, Scranton MI, Iabichella I, Ho T-Y, Thunell RC, Muller-Karger F et al. (2001a). Chemoautotrophy in the redox transition zone of the Cariaco Basin: a significant midwater source of organic carbon production. Limnol Oceanogr 46: 148-163. (Pubitemid 32106544)
85. Taylor GT, Scranton MI, Iabichella M, Y HT, Thunell RC, Muller-Karger F et al. (2001b). Chemoautotrophy in the redox transition zone of the Cariaco Basin: a significant midwater source of organic carbon production. Limnol Oceanogr 46: 148-163. (Pubitemid 32106544)
86. Telford RJ, Vandvik V, Birks HJ. (2006). Dispersal limitations matter for microbial morphospecies. Science 312: 1015.
87. Thompson JD, Higgens DG, Gibson TJ. (1994). Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 33: 4673-4680. (Pubitemid 24354800)
88. Treusch AH, Vergin KL, Finlay LA, Donatz MG, Burton RM, Carlson CA et al. (2009). Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J 3: 1148-1163.
89. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74. (Pubitemid 38451457)
90. Yubuki N, Edgcomb VP, Bernhard JM, Leander BS. (2009). Ultrastructure and molecular phylogeny of Calkinsia aureus: cellular identity of a novel clade of deep-sea euglenozoans with epibiotic bacteria. BMC Microbiol 9: 16.
91. Zuendorf A, Bunge J, Behnke A, Barger KJ, Stoeck T. (2006). Diversity estimates of microeukaryotes below the chemocline of the anoxic Mariager Fjord, Denmark. FEMS Microbiol Ecol 58: 476-491. (Pubitemid 44748156)