Depth distribution of microbial diversity in mono lake, a meromictic soda lake in California

Applied and Environmental Microbiology

Volumn 69, Issue 2, 2003, Pages 1030-1042

  Humayoun, Shaheen B ^a,b   Bano, Nasreen ^a   Hollibaugh, James T ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; DNA; GENETIC ENGINEERING; LAKES;

DEPTH DISTRIBUTION;

BACTERIOLOGY;

SURFACE WATER;

BACTERIUM; BIODIVERSITY; COMMUNITY COMPOSITION; MICROBIAL COMMUNITY; VERTICAL DISTRIBUTION;

ACTINOBACTERIA; ARTICLE; BACILLUS; BACTEROIDES; CLOSTRIDIUM; FLEXIBACTERACEAE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; LAKE; MICROBIAL DIVERSITY; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE ANALYSIS; UNINDEXED SEQUENCE; UNITED STATES;

BACTERIA; CALIFORNIA; DNA, RIBOSOMAL; ECOSYSTEM; FRESH WATER; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SODIUM CHLORIDE; VARIATION (GENETICS);

UNITED STATES;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); BACTEROIDES; CLOSTRIDIUM; CYTOPHAGA; DELTAPROTEOBACTERIA; FLEXIBACTER; FLEXIBACTERACEAE; GAMMAPROTEOBACTERIA; NEGIBACTERIA; POSIBACTERIA; PROTEOBACTERIA; VERRUCOMICROBIALES;

EID: 0037315929     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.69.2.1030-1042.2003     Document Type: Article

References (75)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Amann, R., W. Ludwig, and K. H. Schleifer. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59:143-169.
3. Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Riel, and F. Thingstad. 1983. Ecological role of water column microbes in the sea. Mar. Ecol. Prog. Ser. 10:257-263.
4. Azam, F., and R. A. Long. 2001. Oceanography - sea snow microcosms. Nature 414:495.
5. Bowman, J. P., S. M. Rea, S. A. McCammon, and 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. Brinkhoff, T., and G. Muyzer. 1997. Increased species diversity and extended habitat range of sulfur-oxidizing Thiomicrospira spp. Appl. Environ. Microbiol. 63:3789-3796.
7. Britschgi, T. B., and S. J. Giovannoni. 1991. Phylogenetic analysis of a natural marine bacterioplankton population by rRNA cloning and sequencing. Appl. Environ. Microbiol. 57:1707-1713.
8. Brosius, J., M. L. Palmer, J. K. Poindexter, and H. F. Noller. 1978. Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc. Natl. Acad. Sci. USA 75:4801-4805.
9. Casamayor, E. O., C. Pedros-Alio, G. Muyzer, and R. Amann. 2002. Microheterogeneity in 16S ribosomal DNA-defined bacterial populations from a stratified planktonic environment is related to temporal changes and to ecological adaptations. Appl. Environ. Microbiol. 68:1706-1714.
10. Curtis, T. P., W. T. Sloan, and J. W. Scannell. 2002. Estimating prokaryotic diversity and its limits. Proc. Natl. Acad. Sci. USA 99:10494-10499.
11. DeLong, E. E., and N. R. Pace. 2001. Environmental diversity of Bacteria and Archaea. Syst. Biol. 50:470-478.
12. 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.
13. Dojka, M. A., P. Hugenholtz, S. K. Haack, and N. R. Pace. 1998. Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl. Environ. Microbiol. 64:3869-3877.
14. Domagalski, J. L., W. H. Orem, and H. P. Eugster. 1989. Organic geochemistry and brine composition in Great Salt, Mono, and Walker Lakes. Geochim. Cosmochim. Acta 53:2857-2872.
15. Duckworth, A. W., W. D. Grant, B. E. Jones, and R. van Steenbergen. 1996. Phylogenetic diversity of soda lake alkaliphiles. FEMS Microbiol. Ecol. 19:181-191.
16. Farrelly, V., F. A. Rainey, and E. Stackebrandt. 1995. Effect of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species. Appl. Environ. Microbiol. 61:2798-2801.
17. Felsenstein, J. 1993. PHYLIP (Phylogeny Inference Package), v. 3.5 ed. University of Washington, Seattle.
18. Ferguson, R. L., E. N. Buckley, and A. V. Palumbo. 1984. Response of marine bacteria to differential filtration and confinement. Appl. Environ. Microbiol. 47:49-55.
19. Ferrari, V. C., and J. T. Hollibaugh. 1999. Distribution of microbial assemblages in the central Arctic Ocean basin studied by PCR/DGGE: analysis of a large data set. Hydrobiologia 401:55-68.
20. Garcia-Martinez, J., and F. Rodriguez-Valera. 2000. Microdiversity of uncultured marine prokaryotes: the SAR11 cluster and the marine Archaea of group I. Mol. Ecol. 9:935-948.
21. Giovannoni, S. J., T. B. Britschgi, C. L. Moyer, and K. G. Field. 1990. Genetic diversity in Sargasso Sea bacterioplankton. Nature 345:60-63.
22. Giovannoni, S. J., and M. Rappe. 2000. Evolution, diversity and molecular ecology of marine prokaryotes, p. 47-84. In D. L. Kirchman (ed.), Microbial ecology of the oceans. Wiley-Liss, New York, N.Y.
23. Glöckner, F. O., E. Zaichikov, N. Belkova, L. Denissova, J. Pernthaler, A. Pernthaler, and R. Amann. 2000. Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria. Appl. Environ. Microbiol. 66:5053-5065.
24. Grant, W. D., W. E. Mwatha, and B. E. Jones. 1990. Alkaliphiles: ecology, diversity, and applications. FEMS Microbiol. Rev. 75:255-270.
25. Hagstrom, A., J. Pinhassi, and U. L. Zweifel. 2000. Biogeographical diversity among marine bacterioplankton. Aquat. Microb. Ecol. 21:231-244.
26. Heck, K. L., Jr., G. Van Belle, and D. Simberloff. 1975. Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology 56:1459-1461.
27. Hollibaugh, J. T., P. S. Wong, N. Bano, S. K. Pak, E. M. Prager, and C. Orrego. 2001. Stratification of microbial assemblages in Mono Lake, California, and response to a mixing event. Hydrobiologia 466:45-60.
28. Horikoshi, K., and T. Akiba. 1982. Alkaliphilic microorganisms. Springer-Verlag KG, Berlin, Germany.
29. Jellison, R., R. F. Anderson, J. M. Melack, and D. Heil. 1996. Organic matter accumulation in sediments of hypersaline Mono Lake during a period of changing salinity. Limnol. Oceanogr. 41:1539-1544.
30. Jellison, R., and J. M. Melack. 1993. Meromixis in hypersaline Mono Lake, California. 1. Stratification and vertical mixing during the onset, persistence, and breakdown of meromixis. Limnol. Oceanogr. 38:1008-1019.
31. Jensen, K. M., and R. P. Cox. 1992. Effects of sulfide and low redox potential on the inhibition of nitrous-oxide reduction by acetylene in Pseudomonas nautica. FEMS Microbiol. Lett. 96:13-17.
32. Jones, B. E., W. D. Grant, A. W. Duckworth, and G. G. Owenson. 1998. Microbial diversity of soda lakes. Extremophiles 2:191-200.
33. Joye, S. B., T. L. Connell, L. G. Miller, R. S. Oremland, and R. S. Jellison. 1999. Oxidation of ammonia and methane in an alkaline, saline lake. Limnol. Oceanogr. 44:178-188.
34. Joye, S. B., and J. T. Hollibaugh. 1995. Sulfide inhibition of nitrification influences nitrogen regeneration in sediments. Science 270:623-625.
35. Kerkhof, L., and M. Speck. 1997. Ribosomal RNA gene dosage in marine bacteria. Mol. Mar. Biol. Biotechnol. 6:260-267.
36. Kerkhof, L. J., M. A. Voytek, R. M. Sherrell, D. Millie, and O. Schofield. 1999. Variability in bacterial community structure during upwelling in the coastal ocean. Hydrobiologia 401:139-148.
37. Lane, D. J. 1991. 16S/23S rRNA sequencing, p. 115-175. In E. Stackebrandt and M. Goodfellow (ed.), Nucleic acid techniques in bacterial systematics. Academic Press, Chichester, England.
38. Lee, H. K., J. Chun, E. Y. Moon, S. H. Ko, D. S. Lee, H. S. Lee, and K. S. Bae. 2001. Hahella chejuensis gen. nov., sp. nov., an extracellular-polysaccharide-producing marine bacterium. Int. J. Syst. Bacteriol. 51:661-666.
39. Lewin, R. A., L. Krienitz, R. Goericke, H. Takeda, and D. Hepperle. 2000. Picocystis salinarum gen. et sp. nov. (Chlorophyta) - a new picoplanktonic green alga. Phycologia 39:560-565.
40. Li, L. N., C. Kato, and K. Horikoshi. 1999. Bacterial diversity in deep-sea sediments from different depths. Biodivers. Conserv. 8:659-677.
41. MacIntyre, S., and R. Jellison. 2001. Nutrient fluxes from upwelling and enhanced turbulence at the top of the pycnocline in Mono Lake, California. Hydrobiologia 384:21-39.
42. Madrid, V., G. Taylor, M. Scranton, and A. Chistoserdov. 2001. Phylogenetic diversity of bacterial and archaeal communities in the anoxic zone of the Cariaco Basin. Appl. Environ. Microbiol. 67:1663-1674.
43. Magurran, A. E. 1988. Ecological diversity and its measurement. Princeton University Press, Princeton, N.J.
44. Melack, J. M., and R. Jellison. 1998. Limnological conditions in Mono Lake: contrasting monomixis and meromixis in the 1990s. Hydrobiologia 384:21-39.
45. Meyers, P. A. 1994. Preservation of elemental and isotopic source identification of sedimentary organic matter. Chem. Geol. 114:289-302.
46. Milford, A. D., L. A. Achenbach, D. O. Jung, and M. T. Madigan. 2000. Rhodobaca bogoriensis gen. nov. and sp. nov., an alkaliphilic purple nonsulfur bacterium from African Rift Valley soda lakes. Arch. Microbiol. 174:18-27.
47. Moore, L. R., G. Rocap, and S. W. Chisholm. 1998. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393:464-467.
48. Mullins, T. D., T. B. Britschgi, R. L. Krest, and S. J. Giovannoni. 1995. Genetic comparisons reveal the same unknown bacterial lineages in Atlantic and Pacific bacterioplankton communities. Limnol. Oceanogr. 40:148-158.
49. Oremland, R. S., S. E. Hoeft, J. M. Santini, N. Bano, R. A. Hollibaugh, and J. T. Hollibaugh. 2002. Anaerobic oxidation of arsenite in Mono Lake water and by a facultative chemoautotroph, strain MLHE-1. Appl. Environ. Microbiol. 68:4795-4802.
50. Ovreas, 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.
51. Paabo, S., and A. C. Wilson. 1988. Polymerase chain reaction revealing cloning artifacts. Nature 334:387-388.
52. Paul, J. H., and B. Myers. 1982. Fluorometric determination of DNA in aquatic microorganisms by use of Hoechst 33258. Appl. Environ. Microbiol. 43:1393-1399.
53. Pinhassi, J., F. Azam, J. Hempälä, R. A. Long, J. Martinez, U. L. Zweifel, and Å. Hagström. 1999. Coupling between bacterioplankton species composition, population dynamics, and organic matter degradation. Aquat. Microb. Ecol. 17:13-26.
54. Porter, K. G., and Y. S. Feig. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25:943-948.
55. Prowe, S. G., and G. Antranikian. 2001. Anaerobranca gottschalkii sp. nov., a novel thermoalkaliphilic bacterium that grows anaerobically at high pH and temperature. Int. J. Syst. Evol. Microbiol. 51:457-465.
56. Reysenbach, A., L. J. Giver, G. S. Wickham, and N. Pace. 1992. Differential amplification of rRNA genes by polymerase chain reaction. Appl. Environ. Microbiol. 58:3417-3418.
57. Riemann, L., G. F. Steward, and F. Azam. 2000. Dynamics of bacterial community composition and activity during a mesocosm diatoni bloom. Appl. Environ. Microbiol. 66:578-587.
58. Rijkenberg, M. J., R. Kort, and K. J. Hellingwerf. 2001. Alkalispirillum mobile gen. nov., sp. nov., an alkaliphilic non-phototrophic member of the Ectothiorhodospiraceae. Arch. Microbiol. 175:369-375.
59. Sakano, Y., and L. Kerkhof. 1998. Assessment of changes in microbial community structure during operation of an ammonia biofilter with molecular tools. Appl. Environ. Microbiol. 64:4877-4882.
60. Singleton, D. R., M. A. Furlong, S. L. Rathbun, and W. B. Whitman. 2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl. Environ. Microbiol. 67:4374-4376.
61. Sorokin, D. Y., V. M. Gorlenko, T. P. Tourova, T. V. Kalganova, A. L. Tsapin, K. H. Nealson, and G. J. Kuenen. 2002, Thioalkalimicrobium cyclicum sp. nov., and Thioalkalivibrio jannaschii sp. nov., new species of haloalkaliphilic, obligately chemolithoautotrophic sulfur-oxidizng bacteria from hypersaline alkaline Mono Lake (California). Int. J. Syst. Evol. Microbiol. 52:913-920.
62. Sorokin, D. Y., A. M. Lysenko, L. L. Mityushina, T. P. Tourova, B. E. Jones, F. A. Rainey, L. A. Robertson, and G. J. Kuenen. 2001. Thioalkalimicrobium aerophilum gen. nov., sp. nov., Thioalkalimicrobium sibericum sp. nov., 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.
63. Sorokin, D. Y., T. P. Tourova, A. M. Lysenko, and J. G. Kuenen. 2001. Microbial thiocyanate utilization under highly alkaline conditions. Appl. Environ. Microbiol. 67:528-538.
64. Sorokin, D. Y., T. P. Turova, B. B. Kuznetsov, I. A. Briantseva, and V. M. Gorlenko. 2000. Roseinatronobacter thiooxidans gen. nov., sp. nov., a new alkaliphilic aerobic bacteriochlorophyll-alpha-containing bacteria from a soda lake. Mikrobiologiia 69:89-97.
65. Speksnijder, A. G. C. L., G. A. Kowalchuk, S. De Jong, E. Kline, J. R. Stephen, and H. J. Laanbroek. 2001. Microvariation artifacts introduced by PCR and cloning of closely related 16S rRNA gene sequences. Appl. Environ. Microbiol. 67:469-472.
66. Stackebrandt, E., and B. M. Goebel. 1994. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Bacteriol. 44:846-849.
67. Suzuki, M. T., and S. J. Giovannoni. 1996. Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl. Environ. Microbiol. 62:625-630.
68. Ward, B. B., D. P. Martino, M. C. Diaz, and S. B. Joye. 2000. Analysis of ammonia-oxidizing bacteria from hypersaline Mono Lake, California, on the basis of 16S rRNA sequences. Appl. Environ. Microbiol. 66:2873-2881.
69. Weisenburg, W. G., S. M. Barns, D. A. Pelletier, and D. J. Lane. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173:697-703.
70. Wintzingerode, F., U. B. Gôbel, and E. Stackebrandt. 1997. Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol. Rev. 21:213-329.
71. Yager, P. L., T. L. Connelly, B. B. Mortazavi, K. E. Wommack, N. Bano, J. Bauer, S. Opsahl, and J. T. Hollibaugh. 2001. Dynamic microbial response to an Arctic algal bloom at sub-zero temperatures. Limnol. Oceanogr. 46:790-801.
72. Yakimov, M. M., L. Giuliano, T. N. Chernikova, G. Gentile, W. R. Abraham, H. Lunsdorf, K. N. Timmis, and P. N. Golyshin. 2001. Alcalilimnicola halodurans gen. nov., sp. nov., an alkaliphilic, moderately halophilic and extremely halotolerant bacterium, isolated from sediments of soda-depositing Lake Natron, East Africa Rift Valley. Int. J. Syst. Evol. Microbiol. 51:2133-2143.
73. Zehr, J. P., R. W. Harvey, R. S. Oremland, J. E. Cloern, L. H. George, and J. L. Lane. 1987. Big Soda Lake (Nevada). 1. Pelagic bacterial heterotrophy and biomass. Limnol. Oceanogr. 32:781-793.
74. Zhilina, T. N., G. A. Zavarzin, F. A. Rainey, V. V. Kevbrin, N. A. Kostrikina, and A. M. Lysenko. 1996. Spirochaeta alkalica sp. nov., Spirochaeta africana sp. nov., and Spirochaeta asiatica sp. nov., alkaliphilic anaerobes from the continental Soda Lakes in Central Asia and the East African Rift. Int. J. Syst. Bacteriol. 46:305-312.
75. Zhilina, T. N., G. A. Zavarzin, F. A. Rainey, E. N. Pikuta, G. A. Osipov, and N. A. Kostrikina. 1997. Desulfonatronovibrio hydrogenovorans gen. nov., sp. nov., an alkaliphilic, sulfate-reducing bacterium. Int. J. Syst. Bacteriol. 47:144-149.