Novel active kinetoplastids associated with hypersaline anoxic basins in the Eastern Mediterranean deep-sea

Deep-Sea Research Part I: Oceanographic Research Papers

Volumn 58, Issue 10, 2011, Pages 1040-1048

  Edgcomb, V P ^a   Orsi, W ^b   Breiner, H W ^c   Stock, A ^c   Filker, S ^c   Yakimov, M M ^d   Stoeck, T ^c  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

^c University of Koblenz Landau   (Germany)

^d CNR   (Italy)

Author keywords

Brine; Deep hypersaline anoxic basin; E. Mediterranean; FISH; Kinetoplastids; RNA

Indexed keywords

ANOXIC BASINS; CHEMOCLINE; E. MEDITERRANEAN; EASTERN MEDITERRANEAN; EASTERN MEDITERRANEAN SEA; FLUORESCENT IN SITU HYBRIDIZATION; HIGH DENSITY; HIGH HYDROSTATIC PRESSURE; HYPERSALINE; KINETOPLASTIDS; RIBOSOMAL RNA; SATURATED SALTS; SMALL SUBUNITS;

BRINES; ECOSYSTEMS; FISH; GENES; HYDROSTATIC PRESSURE; RNA;

ANOXIC SEDIMENTS;

ANOXIA; ANOXIC CONDITIONS; CLADISTICS; COMMUNITY STRUCTURE; CONCENTRATION (COMPOSITION); DEEP SEA; FLUORESCENCE; FRACTIONATION; GENE EXPRESSION; GENETIC ANALYSIS; HABITAT TYPE; HYBRIDIZATION; HYDROSTATIC PRESSURE; HYPERSALINE ENVIRONMENT; PLASTID; PROTIST; SALT; SATURATION; SELECTION;

MEDITERRANEAN SEA; MEDITERRANEAN SEA (EAST);

BODONIDAE; KINETOPLASTIDA; MASTIGOPHORA (FLAGELLATES); PROTISTA;

EID: 80052305524     PISSN: 09670637     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dsr.2011.07.003     Document Type: Article

References (76)

1. Alexander E., Stock A., Breiner H.W., Behnke A., Bunge J., Yakimov M.M., Stoeck T. Microbial eukaryotes in the hypersaline anoxic L'Atalante deep-sea basin. Environ. Microbiol. 2009, 11:360-381.
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J.H., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
3. Arndt H., Dietrich D., Auer B., Cleven E.J., Graefenhahn T., Weitere M., Mylnikov A.P. Functional diversity of heterotrophic flagellates in aquatic ecosystems. The Flagellates 2000, 240-268. Taylor & Francis, London, UK. B.S.C. Leadbeater, J.C. Green (Eds.).
4. Atkins M.S., Teske A.P., Anderson O.R. A survey of flagellate diversity at four deep-sea hydrothermal vents in the Eastern Pacific Ocean using structural and molecular approaches. J. Euk. Microbiol. 2000, 47:400-411.
5. Bass D., Cavalier-Smith T. Phylum-specific environmental DNA analysis reveals remarkably high global biodiversity of Cercozoa (Protozoa). Int. J. Syst. Evol. Microbiol. 2004, 54:2393-2404.
6. Behnke A., Bunge J., Barger K., Breiner H.W., Alla V., Stoeck T. Microeukaryote community patterns along an O2/H2S gradient in a supersulfidic anoxic Fjord (Framvaren, Norway). Appl. Environ. Microbiol. 2006, 72:3626-3636.
7. Behnke A., Engel M., Christen R., Nebel M., Klein R.R., Stoeck T. Depicting more accurate pictures of protistan community complexity using pyrosequencing of hypervariable SSU rRNA gene regions. Environ. Microbiol. 2010, 13:340-349.
8. Brandt S. Protista incertae sedis (heterotrophic species). European register of marine species: a check-list of the marine species in Europe and a bibliography of guides to their identification 2001, Collection Patrimoines Naturels. M. Costello (Ed.).
9. Caron D.A., Countway P.D., Savai P., Gast R.J., Schnetzer A., Moorthi S.D., et al. Defining DNA-based operational taxonomic units for microbial-eukaryote ecology. Appl. Environ. Microbiol. 2009, 75:5797-5808.
10. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 2000, 17:540-552.
11. Cavalier-Smith T. Eukaryote kingdoms: seven or nine?. Biosystems 1981, 14:461-481.
12. Cita M.B. Exhumation of Messinian evaporites in the deep-sea and creation of deep anoxic brine filled collapsed basins. Sediment. Geol. 2006, 188-189:357-378.
13. Coleman R.G. Geological evolution of the Red Sea 1993, Clarendon Press, Oxford.
14. Countway P.D., Gast R.J., Dennett M.R., Savai P., Rose J.M., Caron D.A. Distinct protistan assemblages characterize the euphotic zone and deep sea (2500m) of the western North Atlantic (Sargasso Sea and Gulf Stream). Environ. Microbiol. 2007, 9:1219-1232.
15. Daffonchio D., Borin S., Brusa T., Brusetti L., van der Wielen P.W., Bolhuis H., Yakimov M.M., D'Auria G., Giuliano L., Marty D., Tamburini C., McGenity T.J., Hallsworth J.E., Sass A.M., Timmis K.N., Tselepides A., de Lange G.J., Hubner A., Thomson J., Varnavas S.P., Gasparoni F., Gerber H.W., Malinverno E., Corselli C., Garcin J., McKew B., Golyshin P.N., Lampadariou N., Polymenakou P., Calore D., Cenedese S., Zanon F., Hoog S. Stratified prokaryote network in the oxic-anoxic transition of a deep-sea halocline. Nature 2006, 440:203-207.
16. Danovaro R., Dell'Anno A., Pusceddu A., Gambi C., Heiner I., Kristensen R. The first metazoa living in permanently anoxic conditions. BMC Biol. 2010, 8:30.
17. Davila A.M.R., Lukes J. Towards a framework for the evolutionary genomics of Kinetoplastids: what kind of data and how much?. Kinetoplastid Biol. Disease 2003, 2:16.
18. Dykova I., Fiala I., Lom J., Lukes J. Perkinsiella amoebae-like endosymbionts of Neoparamoeba spp., relative of the kinetoplastid Ichthyobodo. Eur. J. Protistol. 2003, 39:37-52.
19. Eder W., Jahnke L.L., Schmidt M., Huber R. Microbial diversity of the brine-seawater interface of the Kebrit Deep, Red Sea, studied via 16S rRNA gene sequences and cultivation methods. Appl. Environ. Microbiol. 2001, 67:3077-3085.
20. Eder W., Ludwig W., Huber R. Novel 16S rRNA gene sequences retrieved from highly saline brine sediments of kebrit deep, red Sea. Arch. Microbiol. 1999, 172:213-218.
21. Eder W., Schmidt M., Koch M., Garbe-Schonberg D., Huber R. Prokaryotic phylogenetic diversity and corresponding geochemical data of the brine-seawater interface of the Shaban Deep, Red Sea. Environ. Microbiol. 2002, 4:758-763.
22. Edgar R.C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformat. 2004, 5:1-19.
23. Edgcomb V., Orsi W., Bunge J., Jeon S.O., Christen R., Leslin C., Holder M., Taylor G.T., Suarez P., Varela R., Epstein S. Protistan microbial observatory in the Cariaco Basin, Caribbean. I. Pyrosequencing vs. Sanger insights into species richness. ISME J. 2011, 5:1344-1356.
24. Edgcomb V., Orsi W., Leslin C., Epstein S.S., Bunge J., Jeon S., Yakimov M.M., Behnke A., Stoeck T. Protistan community patterns within the brine and halocline of deep hypersaline anoxic basins in the Eastern Mediterranean Sea. Extremophiles 2009, 13:151-167.
25. Foissner W. Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool. 2006, 45:111-136.
26. Fusi N., deLarderel G.A., Borelu A., Amelio O., Castradori D., Negri A. Marine geology of the Medriff Corridor, Mediterranean Ridge. Island Arch. 1996, 5:420-439.
27. Galtier N., Guouy M., Gautier C. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 1996, 12:543-548.
28. Garcia H.E., Gordon L.I. Oxygen solubility in seawater: Better fitting equations. Limnol. Oceanogr. 1992, 37:1307-1312.
29. Genitsaris S., Moustaka-Gouni M., Kormas K.A. Airborne microeukaryote colonists in experimental water containers: diversity, succession, life histories and established food webs. Aquat. Microbiol. Ecol. 2011, 62:139-152.
30. Guillou L., Viprey M., Chambouvet A., et al. Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ. Microbiol. 2008, 10:3349-3365.
31. Hallsworth J.E., Yakimov M.M., Golyshin P.N., Gillion J.L., D'Auria G., de Lima Alves F., La Cono V., Genovese M., McKew B.A., Hayes S.L., Harris G., Giuliano L., Timmis K.N., McGenity T.J. Limits of life in MgCl2-containing environments: chaotropicity defines the window. Environ. Microbiol. 2007, 9:801-813.
32. Hauer G., Rogerson A. Heterotrophic protozoa from hypersaline environments. Adaptation to Life at High Salt Concentrations in Archaea, Bacteria, and Eukarya 2005, 519-540. Springer, Dordrecht, The Netherlands. N. Gunde-Cimerman, A. Oren, A. Plemenitas (Eds.).
33. Hausmann K., Hülsmann N, Polianski I, Schade S, Weitere M Benthic protozoans along a transect at different depth (150 to 4600m) in the Eastern Mediterranean. Deep-Sea Res. I 2002, 49:1959-1970.
34. Hoff K.J. The effect of sequencing errors on metagenomic gene prediction. BMC Genom. 2009, 10:520.
35. Horowitz N.H., Cameron R.E., Hubbard J.S. Microbiology of the Dry Valleys of Antarctica. Science 1972, 176:242-245.
36. Kolodziej K., Stoeck T. Cellular identity of a novel uncultured MAST-12 lineage and phylogeny of the uncultured marine stramenopile sequence clade MAST-12. Appl. Environ. Microbiol. 2007, 73:2718-2726.
37. Landweber L.F., Gilbert W. Phylogenetic analysis of RNA editing: a primitive genetic phenomenon. Proc. Natl. Acad. Sci. USA 1994, 91:918-921.
38. Lara E., Moreira D., Vereshchaka A., Loópez-Garcióa P. Pan-oceanic distribution of new highly diverse clades of deep-sea diplonemids. Environ. Microbiol. 2009, 11:47-55.
39. Lee W.J. Some free-living heterotrophic flagellates from marine sediments. Ocean Sci. J 2006, 41:75-95.
40. Lee W.J., Patterson D.J. Diversity and geographic distribution of free-living heterotrophic flagellates-analysis by PRIMER. Protist 1988, 149:229-243.
41. López-García P., Philippe H., Gail F., Moreira D. Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge. Proc. Natl. Acad. Sci. USA 2003, 100:697-702.
42. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004, 32:1363-1371.
43. Massana R., Terrado R., Forn I., Lovejoy C., Pedros-Alio C. Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environ. Microbiol. 2006, 8:1515-1522.
44. Michels P.A.M., Hannaert V. Structure, function, and biogenesis of glycosomes in Kinetoplastida. J. Bioenergy Biomembr. 1994, 26:205-212.
45. Moreira D., López-García P., Vickerman K. An updated view of kinetoplastid phylogeny using environmental sequences and a closer outgroup: proposal for a new classification of the class Kinetoplastea. Int. J. Syst. Evol. Microbiol. 2004, 54:1861-1875.
46. Not F., Gausling R., Azam F., Heidelberg J.F., Worden A.Z. Vertical distribution of picoeukaryotic diversity in the Sargasso Sea. Environ. Microbiol. 2007, 9:1233-1252.
47. Oren A. Microbiological studies in the Dead Sea: future challenges toward the understanding of life at the limit of salt concentrations. Hydrobiologia 1999, 405:1-9.
48. Patterson D.J., Larsen J. The Biology of Free-Living Heterotrophic Flagellates 1991, Clarendon Press, Oxford.
49. Patterson D.J., Simpson A.G. Heterotrophic flagellates from coastal marine and hypersaline sediments in Western Australia. Eur. J. Protistol. 1996, 32:423-448.
50. Pawlowski J., Fontaine D., da Silva A.A., Gulard J. Novel lineages of Southern Ocean deep-sea foraminifera revealed by environmental DNA sequencing. Deep-Sea Res. II 2011, 10.1016/j.dsr2.2011.01.009.
51. Robison-Cox J.F., Bateson M.M., Ward D.M. Evaluation of nearest-neighbor methods for detection of chimeric small-subunit rRNA sequences. Appl. Environ. Microbiol. 1995, 61:1240-1245.
52. Sass A.M., Sass H., Coolen M.J., Cypionka H., Overmann J. Microbial communities in the chemocline of a hypersaline deep-sea basin (Urania basin, Mediterranean Sea). Appl. Environ. Microbiol. 2001, 67:5392-5402.
53. Scheckenbach, F., Hausman, K., Wylezich, C., Weitere, M., Arndt, H., 2011. Wide distribution ranges of several microbial eukaryotes of nanofaunal size at abyssal depths of the South-East Atlantic and the Mediterranean. Appl. Environ. Microbiol. doi:10.1128/AEM.00068-10.
54. Scheckenbach F., Wylezich C., Mylnikov A.P., Weitere M., Arndt H. Molecular comparisons of freshwater and marine isolates of the same morphospecies of heterotrophic flagellates. Appl. Environ. Microbiol. 2006, 72:6638-6643.
55. Siegel B.Z., Mcmurty G., Siegel S.M., Chen J., Larock P. Life in the Calcium-Chloride Environment of Don-Juan Pond, Antarctica. Nature 1979, 280:828-829.
56. Simpson A.G.B., Roger A.J. Protein phylogenies robustly resolve the deep-level relationships within Euglenozoa. Mol. Phylogenet. Evol. 2004, 30:201-212.
57. Simpson A.G.B., Lukes J., Roger A.J. The evolutionary history of kinetoplastids and their kinetoplasts. Mol. Biol. Evol. 2002, 19:2071-2083.
58. Simpson A.G.B., Stevens J.R., Lukes J. The evolution and diversity of kinetoplastid flagellates. Trends Parasitol. 2006, 22:168-174.
59. Stamatakis A., Hoover P., Rougemont J. A rapid bootstrap algorithm for the RAxML Web servers. Syst. Biol. 2008, 57:758-771.
60. Stevens J.R. One million insects-a lot of parasites?. Trends Parasitol. 2001, 17:119-120.
61. Stoeck T., Epstein S.S. Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen-depleted marine environments. Appl. Environ. Microbiol. 2003, 69:2657-2663.
62. Stoeck T., Fowle W.H., Epstein S.S. Methodology of protistan discovery: from rRNA detection to quality scanning electron microscope images. Appl. Environ. Microbiol. 2003, 69:6856-6863.
63. Stoeck T., Schwarz M.V.J., Boenigk J., Schweikert M., von der Heyden S., Behnke A. Cellular identity of an 18S rRNA gene sequence clade within the class Kinetoplastea: the novel genus Actuariola gen. nov (Neobodonida) with description of the type species Actuariola framvarensis sp. nov. Int. J. Syst. Evol. Microbiol. 2005, 55:2623-2635.
64. Stoeck T., Taylor G.T., Epstein S.S. Novel eukaryotes from the permanently anoxic Cariaco Basin (Caribbean Sea). Appl. Environ. Microbiol. 2003, 69:5656-5663.
65. Symposium on the Classification of Brackish Waters The Venice system for the classification of marine waters according to salinity. Oikos 1958, 9:311-312.
66. van der Wielen P.W., Bolhuis H., Borin S., Daffonchio D., Corselli C., Giuliano L., D'Auria G., de Lange G.J., Huebner A., Varnavas S.P., Thomson J., Tamburini C., Marty D., McGenity T.J., Timmis K.N. The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 2005, 307:121-123.
67. van der Wielen P.W., Heijs S.K. Sulfate-reducing prokaryotic communities in two deep hypersaline anoxic basins in the Eastern Mediterranean deep sea. Environ. Microbiol. 2007, 9:1335-1340.
68. The Diversity of the Kinetoplastid Flagellates 1976, Academic Press, London. K. Vickerman (Ed.).
69. Vickerman K. DNA throughout the single mitochondrion of a Kinetoplastid flagellate: observations on the ultrastructure of Cryptobia vaginalis (Hesse, 1910). J. Protozool. 1977, 24:221-233.
70. von der Heyden S., Cavalier-Smith T. Culturing and environmental DNA sequencing uncover hidden kinetoplastid biodiversity and a major marine clade within ancestrally freshwater Neobodo designis. Int. J. Syst. Evol. Microbiol. 2005, 55:2605-2621.
71. von der Heyden S., Chao E.E., Vickerman K., Cavalier-Smith T. Ribosomal RNA phylogeny of bodonid and diplonemid flagellates and the evolution of euglenozoa. J. Eukaryot. Microbiol. 2004, 51:402-416.
72. Wallmann K., Aghib F.S., Castradori D., Cita M.B., Suess E., Greinert J., Rickert D. Sedimentation and formation of secondary minerals in the hypersaline Discovery Basin, Eastern Mediterranean. Mar. Geol. 2002, 186:9-28.
73. Wallmann K.J., Suess E., Westbrook G.H., Winckler G., Cita M.B. Medriff consortium. Salty brines on the Mediterranean sea floor. Nature 1997, 387:31-32.
74. Woo P.T.K. Cryptobiosis and its control in North American fishes. Int. J. Parasitol. 2001, 31:566-574.
75. Yakimov M.M., Giuliano L., Cappello S., Denaro R., Golyshin P.N. Microbial community of a hydrothermal mud vent underneath the deep-sea anoxic brine lake Urania (Eastern Mediterranean). Orig. Life Evol. Biosph. 2007, 37:177-188.
76. Yakimov M.M., La Cono V., Denaro R., D'auria G., Decembrini F., Timmis K.N., Golyshin P.N., Giuliano L. Primary producing prokaryotic communities of brine, interface and seawater above the halocline of deep anoxic lake L'Atalante, Eastern Mediterranean Sea. ISME J. 2007, 1:743-755.