Microbial and chemical characterization of underwater fresh water springs in the dead sea

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Ionescu, Danny ^a   Siebert, Christian ^b   Polerecky, Lubos ^a   Munwes, Yaniv Y ^c   Lott, Christian ^a,d   Häusler, Stefan ^a   Bižić Ionescu, Mina ^a,e   Quast, Christian ^a   Peplies, Jörg ^f   Glöckner, Frank Oliver ^a,g   Ramette, Alban ^a   Rödiger, Tino ^b   Dittmar, Thorsten ^a,h   Oren, Aharon ⁱ   Geyer, Stefan ^b   Stärk, Hans Joachim ^b   Sauter, Martin ^j   Licha, Tobias ^j   Laronne, Jonathan B ^c   de Beer, Dirk ^a  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^d HYDRA Institute for Marine Sciences   (Italy)

^e LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^f RIBOCON GMBH   (Germany)

^g JACOBS UNIVERSITY BREMEN   (Germany)

^h UNIVERSITY OF OLDENBURG   (Germany)

ⁱ HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^j UNIVERSITY OF GÖTTINGEN   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

LAKE WATER; LANTHANIDE; NITROGEN; ORGANIC CARBON; ORGANIC MATTER; PHOSPHORUS; SEA WATER; SULFIDE; SURFACE WATER; YTTRIUM; FRESH WATER; RNA 16S;

16S RRNA GENE; AQUIFER; ARCHAEON; ARTICLE; BIOFILM; BIOGEOCHEMISTRY; CHEMICAL REACTION; CHLOROBI; COMMUNITY STRUCTURE; CYANOBACTERIUM; DILUTION; LITOTROPHY; MICROBIAL COMMUNITY; NATURAL SPRING; NONHUMAN; OXIDATION; PHOTOTROPHY; PYROSEQUENCING; RNA GENE; SEDIMENT; UNDERWATER FRESH WATER SPRING; WATER ANALYSIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY;

ARCHAEA; BACTERIA (MICROORGANISMS); CHLOROBI; CYANOBACTERIA;

ARCHAEA; BIOFILMS; CHLOROBI; CYANOBACTERIA; FRESH WATER; RNA, RIBOSOMAL, 16S; SEAWATER; WATER MICROBIOLOGY;

EID: 84861867881     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038319     Document Type: Article

References (94)

1. Anati DA, Stiller M, Shasha S, Gat, Joel R, (1987) Changes in the thermo-haline structure of the Dead Sea?: 1979-1984. Earth Planet Sci Lett 84: 109 121.
2. Oren A, (2010) The dying Dead Sea: The microbiology of an increasingly extreme environment. Lakes Reservoirs: Res Manage 15: 215 222.
3. Steinhorn I, Assaf G, Gat, JR, Nishry A, Nissenbaum A, (1979) The dead sea: deepening of the mixolimnion signifies the overture to overturn of the water column. Science 206: 55 57.
4. Wilkansky B, (1936) Life in the Dead Sea. Nature 138: 467 467.
5. Elazari-Volcani B, (1940) Algae in the bed of the Dead Sea. Nature 145: 975 975.
6. Elazari-Volcani B, (1943) Bacteria in the bottom sediments of the Dead Sea. Nature 152: 301 302.
7. Elazari-Volcani B, (1943) A dimastigamoeba in the bed of the Dead Sea. Nature 152: 301 302.
8. Elazari-Volcani B, (1944) A ciliate from the Dead Sea. Nature 154: 335 335.
9. Oren A, Gurevich P, (1995) Dynamics of a bloom of halophilic archaea in the Dead Sea. Hydrobiologia 315: 149 158.
10. Laronne Ben-Itzhak L, Gvirtzman H, (2005) Groundwater flow along and across structural folding: an example from the Judean Desert, Israel. J Hydrol 312: 51 69.
11. Gvirtzman H, Stanislavsky E, (2000) Large-scale flow of geofluids at the Dead Sea Rift. J Geochem Explor 69: 207 211.
12. Dulski P, (1994) Interferences of oxide, hydroxide and chloride analyte species in the determination of rare earth elements in geological samples by inductively coupled plasma-mass spectrometry. Fresenius J Anal Chem 350: 194 203.
13. Cline JD, (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14: 454 458.
14. Dulski P, (2001) Reference Materials for Geochemical Studies?: New Analytical Data by ICP-MS and Critical Discussion of Reference Values. Geostandard Newslett 25: 87 125.
15. Ionescu D, Penno S, Haimovich M, Rihtman B, Goodwin A, (2009) Archaea in the Gulf of Aqaba. FEMS Microbiol Ecol 69: 425 438.
16. Lane DJ, (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. pp. 115 175 editors. Nucleic Acid Techniques in Bacterial Systematics. John Wiley and Sons, New York.
17. Ovreås L, Forney L, Daae FL, Torsvik V, (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63: 3367 3373.
18. Delong EF, (1992) Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89: 5685 5689.
19. Dowd SE, Sun Y, Wolcott RD, Domingo A, Carroll JA, (2008) Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathogens And Disease 5: 459-472. doi:10.1089/fpd.2008.0107.
20. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188 7196.
21. Ludwig W, Strunk O, Westram R, Richter L, Meier H, (2004) ARB: a software environment for sequence data. Nucleic Acids Research 32: 1363 1371.
22. Gart JJ, Siegel AF, German RZ, (1982) Rarefaction and Taxonomic Diversity. Biometrics 38: 235 241.
23. Ramette A, (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75: 2495 2505.
24. Amann RI, Krumholz L, Stahl DA, (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172: 762 770.
25. Amann RI, Ludwig W, Schleifer KH, (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59: 143 169.
26. Tujula NA, Holmstro C, Mußmann M, Amann RI, Kjelleberg S, (2006) A CARD - FISH protocol for the identification and enumeration of epiphytic bacteria on marine algae. J Microbiol Methods 65: 604 607.
27. Teira E, Reinthaler T, Pernthaler A, Pernthaler J, Herndl GJ, (2004) Combining Catalyzed Reporter Deposition-Fluorescence In Situ Hybridization and Microautoradiography To Detect Substrate Utilization by Bacteria and Archaea in the Deep Ocean. Appl Environ Microbiol 70: 4411 4414.
28. Polerecky L, Bissett A, Al-Najjar M, Faerber P, Osmers H, (2009) Modular spectral imaging system for discrimination of pigments in cells and microbial communities. Appl Environ Microbiol 75: 758 771.
29. Hammer Ø, Harper DAT, Ryan PD, (2009) PAST: Paleontological Statistics Software Package for Education and Data Analysis. 2001. Palaeontol Electronica 4.
30. Möller P, Rosenthal E, Dulski P, Geyer S, Guttman Y, (2003) Rare earths and yttrium hydrostratigraphy along the Lake Kinneret-Dead Sea-Arava transform fault, Israel and adjoining territories. Appl Geochem 18: 1613 1628.
31. Laronne Ben-Itzhak L, Gvirtzman H, (2005) Groundwater flow along and across structural folding: an example from the Judean Desert, Israel. J Hydrol 312: 51 69.
32. Siebert C, Geyer S, Möller P, Berger D, Guttman Y, (2009) Lake Tiberias and its dynamic hydrochemical environment. In: Möller P, Rosenthal E, editors. pp. 219 246 editors. The Water of The Jordan Valley. Berlin-Heidelberg: Springer-Verlag.
33. Bodaker I, Sharon I, Suzuki MT, Feingersch R, Shmoish M, (2010) Comparative community genomics in the Dead Sea: an increasingly extreme environment. ISME J 4: 399 407.
34. Rhodes ME, Fitz-Gibbon ST, Oren A, House CH, (2010) Amino acid signatures of salinity on an environmental scale with a focus on the Dead Sea. Environ Microbiol 12: 2613 2623.
35. Waddell E, Elliott T, Vahrenkamp J, Roggenthen W, Sani R, (2010) Phylogenetic evidence of noteworthy microflora from the subsurface of the former Homestake gold mine, Lead, South Dakota. Environ Technol 31: 979 991.
36. Salman V, Amann RI, Girnth A-C, Polerecky L, Bailey JV, (2011) A single-cell sequencing approach to the classification of large, vacuolated sulfur bacteria. Syst Appl Microbiol 34: 243 259.
37. Hannigan RE, Sholkovitz ER, (2001) The development of middle rare earth element enrichments in freshwaters: weathering of phosphate minerals. Chem Geol 175: 495 508.
38. Johannesson KH, Farnham IM, Guo C, Stetzenbach KJ, (1999) Rare earth element fractionation and concentration variations along a groundwater flow path within a shallow, basin-fill aquifer, southern Nevada, USA. Geochim Cosmochim Acta 63: 2697 2708.
39. Gavrieli I, Yechieli Y, Halicz L, Spiro B, Bein A, (2001) The sulfur system in anoxic subsurface brines and its implication in brine evolutionary pathways: the Ca-chloride brines in the Dead Sea area. Earth Planet Sci Lett 186: 199 213.
40. Bau M, (1999) Scavenging of dissolved yttrium and rare earths by precipitating iron oxyhydroxide?: Experimental evidence for Ce oxidation, Y-Ho fractionation, and lanthanide tetrad effect. Geochim Cosmochim Acta 63: 67 77.
41. Siebert C, (2006) Seasonal chemical variations of lake Genezareth, its inflows and their cause. Unpublished PhD thesis, Freiei Universitaet Berlin, in German: Saisonale chemische Variationen des See Genezareth, seiner Zuflüsse und deren Ursachen.
42. Möller P, Rosenthal E, Geyer S, Guttman J, Dulski P, (2007) Hydrochemical processes in the lower Jordan valley and in the Dead Sea area. Chem Geol 239: 27 49.
43. Gross S, (1977) The mineralogy of the Haturim Formation, Israel. Bull Geol Surv Israel 70: 1 80.
44. Nissenbaum A, Baedecker MJ, Kaplan IR, (1972) Organic geochemistry of Dead Sea sediments. Geochim Cosmochim Acta 36: 709 727.
45. Katz A, Starinsky A, (2009) Geochemical history of the Dead Sea. Aquat Geochem 15: 159 194.
46. Yechieli Y, Ronen D, (1997) Early diagenesis of highly saline lake sediments after exposure. Chem Geol 138: 93 106.
47. Barkan E, Luz B, (2001) Dynamics of the carbon dioxide system in the Dead Sea. Geochim Cosmochim Acta 65: 355 368.
48. Hansell DA, Carlson CA, (2002) Biogeochemistry of marine dissolved organic matter. Hansell DA, Carlson CA, editors San Diego: Academic Press. 774 p.
49. Gavrieli I, Yechieli Y, Halicz L, Spiro B, Bein A, (2001) The sulfur system in anoxic subsurface brines and its implication in brine evolutionary pathways: the Ca-chloride brines in the Dead Sea area. Earth Planet Sci Lett 186: 199 213.
50. Macalady JL, Jones DS, Lyon EH, (2007) Extremely acidic, pendulous cave wall biofilms from the Frasassi cave system, Italy. Environ Microbiol 9: 1402 1414.
51. Katz A, Agnon A, Marco S, (2009) Earthquake-induced barium anomalies in the Lisan Formation, Dead Sea Rift Valley, Israel. Earth Planet Sci Lett 286: 219 229.
52. Reznik IJ, Gavrieli I, Ganor J, (2009) Kinetics of gypsum nucleation and crystal growth from Dead Sea brine. Geochim Cosmochim Acta 73: 6218 6230.
53. Usdowski E, (1973) Das geochemische Verhalten des Strontiums bei der Genese und Diagenese von Ca-Karbonat-und Ca-Sulfat-Mineralen. Contrib Minera Petrol 38: 177 195.
54. DeLong EF, Taylor LT, Marsh TL, Preston CM, (1999) Visualization and enumeration of marine planktonic archaea and bacteria by using polyribonucleotide probes and fluorescent in situ hybridization. Appl Environ Microbiol 65: 5554 5563.
55. Ravenschlag K, Sahm K, Knoblauch C, Jorgensen BB, Amann RI, (2000) Community structure, cellular rRNA content, and activity of sulfate-reducing bacteria in marine Arctic sediments. Appl Environ Microbiol 66: 3592-3602. doi pp. 10.1128/AEM.66.8.3592 3602.2000.Updated.
56. Pedersen K, (1990) Distribution and activity of bacteria in deep granitic groundwaters of southeastern Sweden. Microb Ecol 20: 37 52.
57. Haveman SA, Pedersen K, (2010) Distribution and Metabolic Diversity of Microorganisms in Deep Igneous Rock Aquifers of Finland. Mol Biol pp. 37 41.
58. Goldscheider N, Hunkeler D, Rossi P, (2006) Review: Microbial biocenoses in pristine aquifers and an assessment of investigative methods. Hydrogeol J 14: 926 941.
59. Straub KL, Benz M, Schink B, Widdel F, (1996) Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl Environ Microbiol 62: 1458 1460.
60. Clement J, Shrestha J, Ehrenfeld J, Jaffe P, (2005) Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils. Soil Biol Biochem 37: 2323 2328.
61. Keough BP, Schmidt TM, Hicks RE, (2003) Archaeal nucleic acids in picoplankton from great lakes on three continents. Microb Ecol 46: 238 248.
62. O'Connell SP, Lehman RM, Snoeyenbos-West O, Winston VD, Cummings DE, (2003) Detection of Euryarchaeota and Crenarchaeota in an oxic basalt aquifer. FEMS Microbiol Ecol 44: 165 173.
63. Elshahed MS, Najar FZ, Roe BA, Oren A, Dewers TA, (2004) Survey of archaeal diversity reveals an abundance of halophilic Archaea in a low-salt, sulfide-and sulfur-rich spring. Appl Environ Microbiol 70: 2230 2239.
64. Graças DA, Miranda PR, Baraúna RA, McCulloch JA, Ghilardi R, (2011) Microbial Diversity of an Anoxic Zone of a Hydroelectric Power Station Reservoir in Brazilian Amazonia. Microbial Ecology 62: 853 861.
65. Lazar M, Ben-Avraham Z, (2002) First images from the bottom of the Dead Sea-Indications of recent tectonic activity. Israel J Earth Sci 51 3-4: 211 218.
66. Swarieh A, (2000) Geothermal energy resources in Jordan, country update report. Proceedings World Geothermal Geothermal Congress pp. 469 474.
67. Shalev E, Levitte D, Gabay R, Zemach E, (2008) Assessment of geothermal resources in Israel. Geological Survey of Israel. 23 p.
68. Overmann J, (2006) The family Chlorobiaceae. In: Dworking M, Falkow S, Rosenberg S, Schleifer K-H, E S, editors. 7: 359 378 editors. The Prokaryotes. Springer, Vol.
69. Frigaard NU, Bryant DA, (2004) Seeing green bacteria in a new light: genomics-enabled studies of the photosynthetic apparatus in green sulfur bacteria and filamentous anoxygenic phototrophic bacteria. Arch Microbiol 182: 265 276.
70. Cohen Y, Jørgensen BB, Revsbech NP, Poplawski R, (1986) Adaptation to Hydrogen Sulfide of Oxygenic and Anoxygenic Photosynthesis among Cyanobacteria. Appl Environ Microbiol 51: 398 407.
71. Oren A, Ionescu D, Lipski A, Altendorf K, (2005) Fatty acid analysis of a layered community of cyanobacteria developing in a hypersaline gypsum crust. Arch Hydrobiol Suppl Algol Stud 117: 339 347.
72. Shatkay M, Anati DA, Gat JR, (1993) Dissolved oxygen in the Dead Sea- seasonal changes during the holomictic stage. Int J Salt Lake Res 2: 93 110.
73. Benlloch S, López-López A, Casamayor EO, Øvreås L, Goddard V, (2002) Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ Microbiol 4: 349 360.
74. van der Wielen PWJJ, Bolhuis H, Borin S, Daffonchio D, Corselli C, (2005) The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307: 121 123.
75. La Cono V, Smedile F, Bortoluzzi G, Arcadi E, Maimone G, (2011) Unveiling microbial life in new deep-sea hypersaline Lake Thetis. Part I: Prokaryotes and environmental settings. Environ Microbiol 13: 2250 2268.
76. Stiller M, Nissenbaum A, (1999) Geochemical investigation of phosphorus and nitrogen in the hypersaline Dead Sea. Geochim Cosmochim Acta 63: 3467 3475.
77. Sand W, Gerke T, Hallmann R, (1995) Sulfur chemistry, biofilm, and the (in)direct attack mechanism - a critical evaluation of bacterial leaching. Appl Microbiol Biotechnol 43: 961 966.
78. Bosecker K, (1997) Bioleaching: metal solubilization by microorganisms. FEMS Microbiol Rev 20: 591 604.
79. Semenza M, Viera M, Curutchet G, (2002) The role of Acidithiobacillus Caldud in the bioleaching of metal sulfides. Latin Am Appl Res 32: 303 306.
80. Caccavo FJ, Coates JD, Rossello-Mora RA, Ludwig W, Schleifer K-H, (1996) Geovibrio ferrireducens, a phylogenetically distinct dissimilatory Fe (III)-reducing bacterium. Arch Microbiol 165: 370 376.
81. Greene AC, Patel BKC, Sheehy AJ, (1997) Deferribacter thermophilus gen. nov., sp. nov., a novel thermophilic manganese-and iron-reducing bacterium isolated from a petroleum reservoir. Int J Syst Bacteriol 47: 505 509.
82. Huber H, Stetter, K O, (2002) Class I. Deferribacteres class. nov. In: Boone, D R, Castenholz, R W, editors. editors. Bergey's Manual of Systematic Bacteriology. New York: Springer-Verlag,. p.
83. Lovley DR, Phillips EJ, Lonergan DJ, Widman PK, (1995) Fe(III) and S0 reduction by Pelobacter carbinolicus. Appl Environ Microbiol 61: 2132 2138.
84. Schink B, (2006) The genus Pelobacter. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, editors. 7: 5 11 editors. The Prokaryotes. New York: Springer, Vol.
85. Nishri A, Stiller M, (1984) Iron in the Dead Sea. Earth Planet Sci Lett 71: 405 414.
86. Oren A, (2002) Halophilic microorganisms and their environments. Seckbach J, editor Dordrecht (Nl): Kluwer Academic Press. 600 p.
87. Akawwi E, Al-zouabi A, Kakish M, Koehn F, Sauter M, (2008) Using Thermal Infrared Imagery (TIR) for illustrating the submarine groundwater discharge into the eastern shoreline of the Dead Sea-Jordan. Am J Environ Sci 4: 693 700.
88. Oren A, Gavrieli I, Gavrieli J, Kohen M, Lati J, (2004) Biological effects of dilution of Dead Sea brine with seawater: implications for the planning of the Red Sea-Dead Sea "Peace Conduit." J Marine Syst 46: 121 131.
89. Closson D, Abou Karaki N, (2009) Salt karst and tectonics: sinkholes development along tension cracks between parallel strike-slip faults, Dead Sea, Jordan. Earth surface processes and landforms 34: 1408 1421.
90. Engel AS, Stern LA, Bennett PC, (2004) Microbial contributions to cave formation: New insights into sulfuric acid speleogenesis. Geology 32: 369.
91. Shen Y, Buick R, (2004) The antiquity of microbial sulfate reduction. Earth-Sci Rev 64: 243 272.
92. Engel AS, Lee N, Porter ML, Stern LA, Bennett PC, (2003) Filamentous "Epsilonproteobacteria" dominate microbial mats from sulfidic cave springs. Appl Environ Microbiol 69: 5503.
93. Stein M, Migowski C, Bookman R, (2004) Temporal changes in radiocarbon reservoir age in the Dead Sea-Lake Lisan system. Radiocarbon 46: 649 655.
94. Good IJ, Toulmin GH, (1956) The number of new species, and the increase in population coverage, when a sample is increased.Biometrika 43: 45 63.