Community composition of a hypersaline endoevaporitic microbial mat

Applied and Environmental Microbiology

Volumn 71, Issue 11, 2005, Pages 7352-7365

  Sørensen, Ketil Bernt ^a   Canfield, Donald E ^b   Teske, Andreas P ^c   Oren, Aharon ^d  

^a UNIVERSITY OF HAWAII   (United States)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CYANOBACTERIA; HALOBACTERIALES; HALOTHECE; SPIRULINA;

BIOLOGICAL ORGANS; BIOMASS; GENES; OXYGEN; RNA;

MICROBIOLOGY;

RNA 16S; SODIUM CHLORIDE;

COMMUNITY COMPOSITION; HYPERSALINE ENVIRONMENT; MICROBIAL MAT; POLYMERASE CHAIN REACTION;

ALPHAPROTEOBACTERIA; ARCHAEBACTERIUM; ARTICLE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; BIOMASS; CHLOROFLEXI; CYANOBACTERIUM; DELTAPROTEOBACTERIA; EURYARCHAEOTA; GAMMAPROTEOBACTERIA; GENE AMPLIFICATION; HALOBACTERIALES; ISRAEL; METHANOSARCINA; MICROFLORA; MICROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SALINITY; UNINDEXED SEQUENCE;

ARCHAEA; BACTERIA; CALCIUM SULFATE; DNA FINGERPRINTING; DNA, ARCHAEAL; DNA, BACTERIAL; ECOSYSTEM; FRESH WATER; GENES, RRNA; GEOLOGIC SEDIMENTS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PRECIPITATION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SODIUM CHLORIDE;

ASIA; EILAT; EURASIA; ISRAEL; MIDDLE EAST; SOUTHERN DISTRICT;

ALPHAPROTEOBACTERIA; ARCHAEA; BACTERIA (MICROORGANISMS); BACTEROIDETES; CHLOROFLEXI; CHLOROFLEXI (CLASS); CYANOBACTERIA; DELTAPROTEOBACTERIA; EURYARCHAEOTA; FIRMICUTES; GAMMAPROTEOBACTERIA; HALOBACTERIALES; HALOTHECE; METHANOSARCINA; METHANOSARCINALES; PHORMIDIUM; PLANCTOMYCETES; SPIRULINA;

EID: 32044445998     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.11.7352-7365.2005     Document Type: Article

References (77)

1. Altschul, S. F., T. L, Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-blast: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Anton, J., R. Rossello-Mora, F. Rodríguez-Valera, and R. Amann. 2000. Extremely halophilic Bacteria in crystallizer ponds from solar salterns. Appl. Environ. Microbiol. 66:3052-3057.
3. Benlloch, S., S. G. Acinas, J. Antón, A. López- López, S. P. Luz, and F. Rodríguez-Valera. 2001. Archaeal biodiversity in crystallizer ponds from a solar saltern: culture versus PCR. Microb. Ecol. 41:12-19.
4. Benlloch, S., A. López-López, E. O. Casamayor, L. OØvreås, V. Goddard, F. L. Daae, G. Smerdon, R. Massana, I. Joint, F. Thingstad, C. Pedrós-Alió, and F. Rodriguez-Valera. 2002. Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ. Microbiol. 4:349-360.
5. Bowman, J. P., S. M. Rea, S. A. McCammon, and T. A. McMeekin. 2000. Diversity and community structure within anoxic sediment from marine salinity meromictic lakes and a coastal meromictic marine basin, Vestfold Hills, Eastern Antarctica. Environ. Microbiol. 2:227-237.
6. Brandt, K. K., B. K. C. Patel, and K. Ingvorsen. 1999. Desulfocella halophila gen. nov., sp. nov., a halophilic, fatty-acid-oxidizing, sulfate-reducing bacterium isolated from sediments of the Great Salt Lake. Int. J. Syst. Bacteriol. 49:193-200.
7. Brandt, K. K., F. Vester, A. N. Jensen, and K. Ingvorsen. 2001. Sulfate reduction dynamics and enumeration of sulfate-reducing bacteria in hypersaline sediments of the Great Salt Lake. Microb. Ecol. 41:1-11.
8. Canfield, D. E., K. B. Sørensen, and A. Oren. 2004. Biogeochemistry of a gypsum-encrusted microbial ecosystem. Geobiology 2:133-150.
9. Caumette, P. 1993. Ecology and physiology of phototrophic bacteria and sulphate-reducing bacteria in marine salterns. Experientia 49:473-481.
10. Caumette, P., R. Baulaigue, and R. Malheron. 1988. Characterization of Chromatium salexigens sp. nov., a halophilic Chromatiaceae isolated from Mediterranean salinas. Syst. Appl. Microbiol. 10:284-292.
11. Caumette, P., R. Baulaigue, and R. Malheron. 1991. Thiocapsa halophila sp. nov., a new halophilic phototrophic purple sulfur bacterium. Arch. Microbiol. 155:170-176.
12. Caumette, P., R. Malheron, N. Raymond, and J. C. Relexans. 1994. Microbial mats in the hypersaline ponds of Mediterranean salterns (Salins-de-Giraud, France). FEMS Microbiol. Ecol. 13:273-286.
13. Cytryn, E., D. Minz, R. S. Oremland, and Y. Cohen. 2000. Distribution and diversity of Archaea corresponding to the limnological cycle of a hypersaline stratified lake (Solar Lake, Sinai, Egypt). Appl. Environ. Microbiol. 66:3269-3276.
14. de Souza, M. P., A. Amini, M. A. Dojka, I. J. Pickering, S. C. Dawson, N. R. Pace, and N. Terry. 2001. Identification and characterization of bacteria in a selenium-contaminated hypersaline evaporation pond. Appl. Environ. Microbiol. 67:3785-3794.
15. Eder, W., W. Ludwig, and R. Huber. 1999. Novel 16S rRNA gene sequences retrieved from highly saline brine sediments of Kebrit Deep, Red Sea. Arch. Microbiol. 172:213-218.
16. Elshahed, M. S., F. Z. Najar, B. A. Roe, A. Oren, T. A. Dewers, and L. R. Krumholz. 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.
17. Felsenstein, J. 1989. PHYLIP: phylogeny inference package (version 3.2). Cladistics 5:164-166.
18. Fuhrman, J. A., and A. A. Davis. 1997. Widespread archaea and novel bacteria from the deep sea as shown by 16S rRNA gene sequences. Mar. Ecol. Prog. Ser. 150:275-285.
19. Garcia J.-L., B. K. C. Patel, and B. Ollivier. 2000. Taxonomic, phylogenetic, and ecological diversity of methanogenic Archaea. Anaerobe 6:205-226.
20. Garcia-Pichel, F., U. Nübel, and G. Muyzer. 1998. The phytogeny of unicellular, extremely halotolerant cyanobacteria. Arch. Microbiol. 169:469-482.
21. Gilbert, D. G. 1995. SeqPup 0.5b: a biosequence editor and analysis application. Indiana University, Bloomington.
22. Gonzalez, J. M., and M. A. Moran. 1997. Numerical dominance of a group of marine bacteria in the α-subclass of the class Proteobacteria in coastal seawater. Appl. Environ. Microbiol. 63:4237-4242.
23. González, J. M., R. P. Kiene, and M. A. Moran. 1999. Transformation of sulfur compounds by an abundant lineage of marine Bacteria in the α-subclass of the class Proteobacteria. Appl. Environ. Microbiol. 65:3810-3819.
24. Guyoneaud, R., S. Moune, C. Ealock, V. Bothorel, A. S. Hirschler-Rea, J. Willison, R. Duran, W. Liesack, R. Herbert, R. Malheron, and P. Caumette. 2002. Characterization of three spiral-shaped purple nonsulfur bacteria isolated from coastal lagoon sediments, saline sulfur springs, and microbial mats: emended description of the genus Roseospira and description of Roseospira marina sp. nov., Roseospira navarrensis sp. nov., and Roseospira thiosulfatophila sp. nov. Arch. Microbiol. 178:315-324.
25. Hartmann, R., H. D. Sickinger, and D. Oesterhelt. 1980. Anaerobic growth of halobacteria. Proc. Natl. Acad. Sci. USA 77:3821-3825.
26. Huber, T., G. Faulkner, and Hugenholtz, P. 2004. Bellerophon; a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317-2319.
27. Imhoff, J. F. 2001. True marine and halophilic anoxygenic phototrophic bacteria. Arch. Microbiol. 176:243-254.
28. Imhoff, J. F., J. Sülling, and R. Petri. 1998. Phylogenetic relationships among the Chromatiaceae, their taxonomic reclassification and description of the new genera Allochromatium, Halochromatium, Isochromatium, Marichromatium, Thiococcus, Thiohalocapsa, and Thermochromatium. Int. J. Syst. Bacteriol. 48:1129-1143.
29. Jonkers, H. M., and R. M. M. Abed. 2003. Identification of aerobic heterotrophic bacteria from the photic zone of a hypersaline microbial mat. Aquat. Microb. Ecol. 30:127-133.
30. Jonkers, H. M., R. Ludwig, R. de Wit, O. Pringault, G. Muyzer, H. Niemann, N. Finke, and D. de Beer. 2003. Structural and functional analysis of a microbial mat ecosystem from a unique permanent hypersaline inland lake: 'La Salada de Chiprana' (NE Spain). FEMS Microbiol. Ecol. 44:175-189.
31. Kersters, K., P. de Vos, M. Gillis, J. Swings, P. Vandamme, and E. Stackebrandt. 2003. Introduction to the Proteobacteria. In M. Dworkin et al. (ed.), The prokaryotes: an evolving electronic resource for the microbiological community, 3rd ed., release 3.12. [Online.] Springer-Verlag, New York, N.Y. http://link.springer-ny.com/link/service/books/10125/.
32. Kirchman, D. L. 2002. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol. Ecol. 39:91-100.
33. Klappenbach, J. A., and B. K. Pierson. 2004. Phylogenetic and physiological characterization of a filamentous anoxygenic photoautotrophic bacterium "Candidatus Chlorothrix halophila" gen. nov., sp. nov., recovered from hypersaline microbial mats. Arch. Microbiol. 181:17-25.
34. Klappenbach, J. A., J. M. Dunbar, and T. M. Schmidt. 2000. rRNA operon copy number reflects ecological strategies of bacteria. Appl. Environ. Microbiol. 66:1328-1333.0.
35. Krekeler, D., P. Sigalevich, A. Teske, H. Cypionka, and Y. Cohen. 1997. A sulfate reducing bacterium from the oxic layer of a microbial mat from Solar Lake (Sinai), Desulfovibrio oxyclinae sp. nov. Arch. Microbiol. 167:369-375.
36. Labrenz, M., M. D. Collins, P. A. Lawson, B. J. Tindall, P. Schumann, and P. Hirsch. 1999. Roseovarius tolerans gen. nov., sp. nov., a budding bacterium with variable bacteriochlorophyll a production from hypersaline Lake Ekho. Int. J. Syst. Bacteriol. 49:137-147.
37. Madigan, M. T. 2003. Anoxygenic phototrophic bacteria from extreme environments. Photosynth. Res. 76:157-171.
38. Minz, D. J., L. Flax, S. J. Green, G. Muyzer, Y. Cohen, M. Wagner, B. E. Rittmann, and D. A. Stahl. 1999. Diversity of sulfate-reducing bacteria in oxic and anoxic regions of a microbial mat characterized by comparative analysis of dissimilatory sulfite reductase genes. Appl. Environ. Microbiol. 65:4666-4671.
39. Moran, M. A., J. M. Gonzalez, and R. P. Kiene. 2003. Linking a bacterial taxon to sulfur cycling in the sea: studies of the marine Roseobacter group. Geomicrobiol. J. 20:375-388.
40. Mouné, S., N. Manac'h, A. Hirschler, P. Caumette, J. C. Willison, and R. Matheron. 1999. Haloanaerobacter salinarius sp. nov., a novel halophilic fermentative bacterium that reduces glycine-betaine to trimethylamine with hydrogen or serine as electron donors; emendation of the genus Haloanaerobacter. Int. J. Syst. Bacteriol. 49:103-112.
41. Moune, S., P. Caumette, R. Matheron, and J. Willison. 2003. Molecular sequence analysis of prokaryotic diversity in the anoxic sediments underlying cyanobacterial mats of two hypersaline ponds in Mediterranean salterns. FEMS Microbiol. Ecol. 44:117-130.
42. Muyzer, G., E. C. de Waal, and A. G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695-700.
43. Nübel, U., F. Garcia-Pichel, E. Clavero, and G. Muyzer. 2000. Matching molecular diversity and ecophysiology of benthic cyanobacteria and diatoms in communities along a salinity gradient. Environ. Microbiol. 2:217-226.
44. Nübel, U., F. Garcia-Pichel, and G. Muyzer. 2000. The halotolerance and phytogeny of cyanobacteria with tightly coiled trichomes (Spirulina Turpin) and the description of Halospirulina tapeticola gen. nov. sp. nov. Int. J. Syst. Evol. Microbiol. 50:1265-1277.
45. Nübel, U., M. M. Bateson, M. T. Madigan, M. Kühl, and D. M. Ward. 2001. Diversity and distribution in hypersaline microbial mats of bacteria related to Chloroflexus spp. Appl. Environ. Microbiol. 67:4365-4371.
46. Nübel, U., M. M. Bateson, V. Vandieken, A. Wieland, M. Kühl, and D. M. Ward. 2002. Microscopic examination of distribution and phenotypic properties of phylogenetically diverse Chloroflexaceae-related bacteria in hot spring microbial mats. Appl. Environ. Microbiol. 68:4593-4603.
47. Ollivier, B., P. Caumette, J. L. Garcia, and R. A. Mah. 1994. Anaerobic bacteria from hypersaline environments Microbiol. Rev. 58:27-38.
48. Oren, A. 1999. Bioenergetic aspects of halophilism. Microbiol. Mol. Biol. Rev. 63:334-348.
49. Oren, A. 2000. Change of the names Haloanaerobiales, Haloanaerobiaceae and Haloanaerobium to Halanaerobiales, Halanaerobiaceae and Halanaerobium, respectively, and further nomenclatural changes within the order Halanaerobiales. Int. J. Syst. Evol. Microbiol. 50:2229-2230.
50. Oren, A. 2002. Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J. Indust. Microbiol. Biotechnol. 28:55-63.
51. Oren, A., and F. Rodríguez-Valera. 2001. The contribution of halophilic bacteria to the red coloration of saltern crystallizer ponds. FEMS Microbiol. Ecol. 36:123-130.
52. Oren, A., and H. G. Trüper. 1990. Anaerobic growth of halophilic archaeobacteria by reduction of dimethylsulfoxide and trimethylamine N-oxide. FEMS Microbiol. Lett. 70:33-36.
53. Oren, A., M. Kühl, and U. Karsten. 1995. An endoevaporitic microbial mat within a gypsum crust: zonation of phototrophs, photopigments, and light penetration. Mar. Ecol. Prog. Ser. 128:151-159.
54. 53a. OØvreås, L., L. Forney, F. L. Daae, and V. Torsvik. 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.
55. Paterek J. R., and P. H. Smith. 1988. Methanohalophilus mahii gen. nov. sp. nov., a methylotrophic halophilic methanogen. Int. J. Syst. Bacteriol. 38: 122-123.
56. Pierson, B. K., D. Valdez, M. Larsen, E. Morgan, and E. E. Mack. 1994. Chloroflexus-like organisms from marine and hypersaline environments: distribution and diversity. Photosynth. Res. 41:35-52.
57. Porter, K., and Y. Feig. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol.Oceanogr. 25:943-948.
58. Rainey, F. A., T. N. Zhilina, E. S. Boulygina, E. Stackebrandt, T. P. Tourova, and G. A. Zavarzin. 1995. The taxonomic status of the fermentative halophilic anaerobic bacteria: description of Halobacteriales ord. nov., Halobacteroidaceae fam. nov., Orenia gen. nov., and further taxonomic rearrangements at the genus and species level. Anaerobe 1:185-199.
59. Ravot, G., M. Magot, B. Ollivier, B. K. C. Patel, E. Ageron, P. A. D. Grimont, P. Thomas, and J. L. Garcia. 1997. Haloanaerobium congolense sp. nov., an anaerobic, moderately halophilic, thiosulfate- and sulfur-reducing bacterium from an African Oil Field. FEMS Microbiol. Lett. 147:81-88.
60. Reichenbach, H. 1991. The order Cytophagales, p. 3631-3675. In A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer (ed.), The prokaryotes, 2nd ed., vol. 3. Springer-Verlag, New York, N.Y.
61. Rothschild, L. J., L. J. Giver, M. R. White, and R. L. Mancinelli. 1994. Metabolic activity of microorganisms in evaporites. J. Phycol. 30:431-438.
62. Rouvière, P., L. Mandelco, S. Winker, and C. R. Woese. 1992. A detailed phytogeny for the Methanomicrobiales. Syst. Appl. Microbiol. 15:363-371.
63. Shen, Y., R. Buick, and D. E. Canfield. 2001. Isotopic evidence for microbial sulphate reduction in the early Archaean era. Nature 410:77-81.
64. Sorokin, D. Y., A. M. Lysenko, L. L. Mityushina, T. P. Tourova, B. E. Jones, F. A. Rainev, L. A. Robertson, and J. G. Kuenen. 2001. Thioalkalimicrobium aerophilum gen. nov., sp. nov. and Thioalkalitnicrobium sibericum sp. nov., and Thioalkalivibrio versutus gen. nov., sp. nov., Thioalkalivibrio nitratis sp. nov., and Thioalkalivibrio denitrificans sp. nov., novel obligately alkaliphilic and obligately chemolithoautotrophic sulfur-oxidizing bacteria from soda lakes. Int. J. Syst. Evol. Microbiol. 51:565-580.
65. Soørensen, K. B. 2002. Microbial ecology of gradient systems. Ph.D. dissertation. Institute of Biology, University of Southern Denmark, Odense, Denmark.
66. SoøBrensen, K. B., D. E. Canfield, and A. Oren. 2004. Salinity response of benthic microbial communities in a solar saltern (Eilat, Israel). Appl. Environ. Microbiol. 70:1608-1616.
67. Spear, J. R., R. E. Ley, A. B. Berger, and N. R. Pace. 2003. Complexity in natural microbial ecosystems: the Guerrero Negro experience. Biol. Bull. 204:168-173.
68. Squyres, S. W., J. P. Grotzinger, R. E. Arvidson, J. F. Bell, W. Calvin, P. R. Christensen, B. C. Clark, J. A. Crisp, W. H. Farrand, K. E. Herkenhoff, J. R. Johnson, G. Klingelhofer, A. H. Knoll, S. M. McLennan, H. Y. McSween, R. V. Morris, J. W. Rice, R. Rieder, and L. A. Soderblom. 2004. In situ evidence for an ancient aqueous environment at Meridiani Planum, Mars. Science 306:1709-1714.
69. Squyres, S. W., R. E. Arvidson, J. F. Bell, J. Bruckner, N. A. Cabrol, W. Calvin, M. H. Carr, P. R. Christensen, B. C. Clark, L. Grumpier, D. J. DesMarais, C. d'Uston, T. Economou, J. Farmer, W. Farrand, W. Folkner, M. Golombek, S. Gorevan, J. A. Grant, R. Greeley, J. Grotzinger, L. Haskin, K. E. Herkenhoff, S. Hviid, J. Johnson, G. Klingelhofer, A. H. Knoll, G. Landis, M. Lemmon, R. Li, M. B. Madsen, M. C. Malin, S. M. McLennan, H. Y. McSween, D. W. Ming, J. Moersch, R. V. Morris, T. Parker, J. W. Rice, L. Richter, R. Rieder, M. Sims, M. Smith, P. Smith, L. A. Soderblom, R. Sutlivan, H. Wanke, T. Wdowiak, M. Wolff, and A. Yen. 2004. The Opportunity Rover's Athena science investigation at Meridiani Planum, Mars. Science 306:1698-1703.
70. Suzuki, T., Y. Muroga, M. Takahama, and Y. Nishimura. 1999. Roseivivax halodurans gen. nov., sp. nov., and Roseivivax halotolerans sp. nov., aerobic bacteriochlorophyll-containing bacteria isolated from a saline lake. Int. J. Syst. Bacteriol. 49:629-634.
71. Takai, K., and K. Horikoshi. 1999. Genetic diversity of Archaea in deep sea hydrothermal vent environments. Genetics 152:1285-1297.
72. Teske, A., K. U. Hinrichs, V. Edgcomb, G. A. de Vera, D. Kysela, S. P. Sylva, M. L. Sogin, and H. W. Jannasch. 2002. Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Appl. Environ. Microbiol. 68:1994-2007.
73. van der Wielen, P. W. J. J., H. Bolhuis, S. Borin, D. Daffonchio, C. Corselli, L. Giuliano, G. D'Auria, G. J. de Lange, A. Huebner, S. P. Varnavas, J. Thomson, C. Tamburini, D. Marty, T. J. McGenity, K. N. Timmis, and BioDeep Scientific Party. 2005. The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307:121-123.
74. Vetriani, C., H. W. Jannasch, B. J. MacGregor, D. A. Stahl, and A. L. Reysenbach. 1999. Population structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediments. Appl. Environ. Microbiol. 65:4375-4384.
75. Ward, D. M., C. M. Santegoeds, S. C. Nold, and N. B. Ramsing. 1997. Biodiversity within hot spring microbial communities: molecular monitoring of enrichment cultures. Antonie Leeuwenhoek 71:143-150.
76. Waterbury, J. B. 1991. The cyanobacteria: isolation, purification, and identification, p. 2058-2078. In A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer (ed.), The prokaryotes, 2nd ed., vol. 2. Springer-Verlag, New York, N.Y.
77. Zeikus, J. G., P. W. Hegge, T. E. Thompson, T. J. Phelps, and T. A. Langworthy. 1983. Isolation and description of Haloanaerobium praevalens gen. nov. and sp. nov., an obligately anaerobic halophilic common to Great Salt Lake sediments. Curr. Microbiol. 9:225-234.