Microbial biogeography of six salt lakes in Inner Mongolia, China, and a salt lake in Argentina

Applied and Environmental Microbiology

Volumn 75, Issue 18, 2009, Pages 5750-5760

  Pagaling, Eulyn ^a   Wang, Huanzhi ^a   Venables, Madeleine ^a   Wallace, Andrew ^a   Grant, William D ^a   Cowan, Don A ^b   Jones, Brian E ^c   Ma, Yanhe ^d   Ventosa, Antonio ^e   Heaphy, Shaun ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF THE WESTERN CAPE   (South Africa)

^c Genencor International BV   (Netherlands)

^d INSTITUTE OF MICROBIOLOGY   (China)

^e UNIVERSITY OF SEVILLE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE; 16S RRNA GENE SEQUENCE; ARCHAEAL; ARGENTINA; DISTANCE MATRICES; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL FACTORS; INNER MONGOLIA; ION CONCENTRATIONS; MANTEL TESTS; MICROBIAL COMMUNITY COMPOSITION; PH VALUE; SALT COMPOSITION; SALT LAKES; WATER COLUMNS;

CHEMICAL ANALYSIS; CLONING; LAKES;

GENES;

BICARBONATE; MAGNESIUM ION; RNA 16S; SODIUM ION;

BIOGEOGRAPHY; CONCENTRATION (COMPOSITION); ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL FACTOR; MICROBIAL COMMUNITY; MICROORGANISM; SALINE LAKE;

ARCHAEAL GENE; ARCHAEBACTERIUM; ARGENTINA; ARTICLE; BACTERIAL FLORA; BACTERIAL GENE; BIOGEOGRAPHY; CHINA; ENVIRONMENTAL FACTOR; ENVIRONMENTAL TEMPERATURE; GENE LIBRARY; GENE SEQUENCE; GEOGRAPHIC DISTRIBUTION; LAKE ECOSYSTEM; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MONGOLIA; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; RNA GENE; SALT LAKE; UNINDEXED SEQUENCE;

ARCHAEA; ARGENTINA; BACTERIA; BIODIVERSITY; CHINA; CLUSTER ANALYSIS; DNA, ARCHAEAL; DNA, BACTERIAL; DNA, RIBOSOMAL; GENES, RRNA; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, ARCHAEAL; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SALTS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; WATER; WATER MICROBIOLOGY;

ARGENTINA; ASIA; CHINA; EURASIA; FAR EAST; NEI MONGGOL; SOUTH AMERICA;

ARCHAEA; BACTERIA (MICROORGANISMS); PROKARYOTA;

EID: 70149120519     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00040-09     Document Type: Article

References (70)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment tool. J. Mol. Biol. 215:403-410.
2. Antón, J., R. Rosselló-Mora, F. Rodríguez-Valera, and R. Amann. 2000. Extremely halophilic Bacteria in crystallizer ponds from solar salterns. Appl. Environ. Microbiol. 66:3052-3057.
3. Ashelford, K. E., N. A. Chuzhanova, J. C. Fry, A. J. Jones, and A. J. Weightman. 2005. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 71:7724-7736.
4. Baas-Becking, L. G. M. 1934. Geobiologie of inleiding tot de milieukunde. W. P. van Stockum and Zoon, Gravenhange, The Netherlands.
5. Bano, N., S. Ruffin, B. Ransom, and J. T. Hollibaugh. 2004. Phylogenetic comparison of Arctic Ocean archaeal assemblages and comparison with Antarctic assemblages. Appl. Environ. Microbiol. 70:781-789.
6. Beijerinck, M. W. 1913. De infusies en de ontdekking der backterien, p. 119-140. In F. Bruckmann et al. (ed.), Jaarboek van de Koninklijke Akademie voor Wetenschappen. Müller, Amsterdam, The Netherlands.
7. Benlloch, S., A. López-López, E. O. Casamayor, L. Øvreås, V. Goddard, F. L. Daae, G. Smerdon, R. Massana, I. Joint, F. Thingstad, C. Pedrós-Alió, and F. Rodríguez-Valera. 2002. Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ. Microbiol. 4:349-360.
8. Bonnet, E., and Y. Van der Peer. 2002. zt: a software tool for simple and partial Mantel tests. J. Stat. Software 7:1-12. (Pubitemid 39217779)
9. Brown, J. H., B. R. Riddle, and M. V. Lomolino. 2005. Biogeography. Sinauer Associates, Inc., Sunderland, MA.
10. Burns, D. G., H. M. Camakaris, P. H. Janssen, and M. L. Dyall-Smith. 2004. Combined use of cultivation-dependent and cultivation-independent methods indicates that members of most haloarchaeal groups in an Australian crystallizer pond are cultivable. Appl. Environ. Microbiol. 70:5258-5265.
11. Casamayor, E. O., R. Massana, S. Benlloch, L. Øvreås, B. Díez, V. J. Goddard, J. M. Gasol, I. Joint, F. Rodríguez-Valera, and C. Pedrós-Alió. 2002. Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environ. Microbiol. 4:338-348.
12. Cho, J.-C., and J. M. Tiedje. 2000. Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl. Environ. Microbiol. 66:5448-5456.
13. Cox, C. B., and P. D. Moore. 2000. Biogeography: an ecological and evolutionary approach. Blackwell Science, Ltd., Oxford, United Kingdom.
14. Crump, B. C., C. S. Hopkinson, M. L. Sogin, and J. E. Hobbie. 2004. Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl. Environ. Microbiol. 70:1494-1505.
15. Del Moral, A., E. Quesada, V. Bejar, and A. Ramos-Cormenzana. 1987. Evolution of bacterial flora from a subterranean saline well by gradual salinity changes in enrichment media. J. Appl. Bacteriol. 62:465-471.
16. Demergasso, C. S., E. O. Casamayor, G. Chong, P. A. Galleguillos, L. V. Escudero, and C. Pedrós-Alió. 2004. Distribution of prokaryotic genetic diversity in athalassohaline lakes of the Atacama Desert, Northern Chile. FEMS Microbiol. Ecol. 48:57-69.
17. Dimitriu, P. A., H. C. Pinkart, B. M. Peyton, and M. R. Mormile. 2008. Spatial and temporal patterns in the microbial diversity of a meromictic soda lake in Washington State. Appl. Environ. Microbiol. 74:4877-4888.
18. Echigo, A., M. Hino, T. Fukushima, T. Mizuki, M. Kamekura, and R. Usami. 2005. Endospores of halophilic bacteria of the family Bacillaceae isolated from non-saline Japanese soil may be transported by Kosa event (Asian dust storm). Saline Syst. 1:1-13.
19. Empadinhas, N., and M. S. da Costa. 2008. Osmoadaptation mechanisms in prokaryotes: distribution of compatible solutes. Int. Microbiol. 11:151-161.
20. Fierer, N., and R. B. Jackson. 2006. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. USA 103:626-631.
21. Finlay, B. J. 2002. Global dispersal of free-living microbial eukaryote species. Science 296:1061-1063. (Pubitemid 34517112)
22. Foti, M., S. Ma, D. Y. Sorokin, J. L. W. Rademaker, J. G. Kuenen, and G. Muyzer. 2006. Genetic diversity and biogeography of haloalkaliphilic sulphur-oxidizing bacteria belonging to the genus Thioalkalivibrio. FEMS Microbiol. Ecol. 56:95-101.
23. Galinski, E. A., and H. G. Trüper. 1994. Microbial behaviour in salt-stressed ecosystems. FEMS Microbiol. Rev. 15:95-108.
24. Good, I. J. 1953. The population frequencies of species and the estimation of population parameters. Biometrika 40:237-264.
25. Grant, S., W. D. Grant, B. E. Jones, C. Kato, and L. Li. 1999. Novel archaeal phylotypes from an East African alkaline saltern. Extremophiles 3:139-145.
26. Grant, W. D., M. Kamekura, T. J. McGenity, and A. Ventosa. 2001. Class III Halobacteria class nov., p. 294-334. In D. R. Boone, R. Castenholz, and G. M. Garrity (ed.), Bergey's manual of systematic bacteriology, 2nd ed., vol.1. Springer, New York, NY.
27. Grant, W. D. 2004. Life at low water activity. Philos. Trans. R. Soc. Lond. B 359:1249-1267.
28. Gunde-Cimerman, N., A. Oren, and A. Plemenitaš. 2005. Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer, New York, NY.
29. 2-containing environments: chaotropicity defines the window. Environ. Microbiol. 9:801-813.
30. Head, I. M., J. R. Saunders, and R. W. Pickup. 1998. Microbial evolution, diversity and ecology: a decade of ribosomal RNA analysis of uncultivated microorganisms. Microb. Ecol. 35:1-21.
31. Horner-Devine, M. C., M. Lage, J. B. Hughes, and B. J. M. Bohannan. 2004. A taxa-area relationship for bacteria. Nature 432:750-753.
32. Horner-Devine, M. C., K. M. Carney, and B. J. M. Bohannan. 2004. An ecological perspective on bacterial biodiversity. Proc. R. Soc. Lond. B 271:113-122.
33. Hua, N.-P., F. Kobayashi, Y. Iwasaka, G.-Y. Shi, and T. Naganuma. 2007. Detailed identification of desert-originated bacteria carried by Asian dust storms to Japan. Aerobiologia 23:291-298.
34. Humayoun, S. B., N. Bano, and J. T. Hollibaugh. 2003. Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Appl. Environ. Microbiol. 69:1030-1042.
35. Jiang, H., H. Dong, G. Zhang, B. Yu, L. R. Chapman, and M. W. Fields. 2006. Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Appl. Environ. Microbiol. 72:3832-3845.
36. Jones, B. E., W. D. Grant, A. W. Duckworth, and G. G. Owenson. 1998. Microbial diversity of soda lakes. Extremophiles 2:191-200.
37. Junfeng, L. 1997. Renewable energy development in China: resource assessment, technology status, and greenhouse gas mitigation potential. Appl. Energy 56:381-394. (Pubitemid 127422312)
38. Kulp, T. R., S. Han, C. W. Saltikov, B. D. Lanoil, K. Zargar, and R. S. Oremland. 2007. Effects of imposed salinity gradients on dissimilatory arsenate reduction, sulfate reduction, and other microbial processes in sediments from two California soda lakes. Appl. Environ. Microbiol. 73:5130-5137.
39. Kumar, S., K. Tamura, and M. Nei. 2004. MEGA 3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5:150-163.
40. Lanyi, J. K. 1974. Salt-dependent properties of proteins from extremely halophilic bacteria. Bacteriol. Rev. 38:272-290.
41. Lindström, E. S., M. P. Kamst-van Agterveld, and G. Zwart. 2005. Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl. Environ. Microbiol. 71:8201-8206.
42. Martiny, J. B. H., B. J. M. Bohannan, J. H. Brown, R. K. Colwell, J. A. Fuhrman, J. L. Green, M. C. Horner-Devine, M. Kane, J. A. Krumins, C. R. Kuske, P. J. Morin, S. Naeem, L. Øvreås, A. Reysenbach, V. H. Smith, and J. T. Staley. 2006. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4:102-112.
43. McCraig, A. E., L. A. Glover, and J. I. Prosser. 1999. Molecular analysis of bacterial community structure and diversity in unimproved and improved upland grass pastures. Appl. Environ. Microbiol. 65:1721-1730.
44. Mesbah, N. M., S. H. Abou-El-Ela, and J. Wiegel. 2007. Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun, Egypt. Microb. Ecol. 54:598-617.
45. Mevarech, M., F. Frolow, and L. M. Gloss. 2000. Halophilic enzymes: proteins with a grain of salt. Biophys. Chem. 86:155-164.
46. Nesbø, C. L., M. Dlutek, O. Zhaxybayeva, and W. F. Doolittle. 2006. Evidence for existence of "Mesotogas," members of the order Thermotogales adapted to low-temperature environments. Appl. Environ. Microbiol. 72:5061-5068.
47. O'Connor, K., and L. N. Csonka. 2003. The high salt requirement of the moderate halophile Chromohalobacter salexigens DSM3043 can be met not only by NaCl but by other ions. Appl. Environ. Microbiol. 69:6334-6336.
48. Oren, A., M. Heldal, S. Norland, and E. A. Galinski. 2002. Intracellular ion and organic solute concentrations of the extremely halophilic bacterium Salinibacter ruber. Extremophiles 6:491-498. (Pubitemid 41504963)
49. Oren, A. 2005. A hundred years of Dunaliella research: 1905-2005. Saline Syst. 1:1-14.
50. Pagaling, E. 2007. Ph.D. thesis. University of Leicester, Leicester, United Kingdom.
51. Papke, R. T., N. B. Ramsing, M. M. Bateson, and D. M. Ward. 2003. Geographic isolation in hot spring cyanobacteria. Environ. Microbiol. 5:650-659.
52. Radosevich, J. L., W. J. Wilson, J. H. Shinn, T. Z. DeSantis, and G. L. Andersen. 2002. Development of a high-volume aerosol collection system for the identification of air-bourne micro-organisms. Lett. Appl. Microbiol. 34:162-167.
53. Rees, H. C., W. D. Grant, B. E. Jones, and S. Heaphy. 2004. Diversity of Kenyan soda lake alkaliphiles assessed by molecular methods. Extremophiles 8:63-71.
54. Rengpipat, S., S. E. Lowe, and J. G. Zeikus. 1988. Effect of extreme salt concentrations on the physiology and biochemistry of Halobacteroides acetoethylicus. J. Bacteriol. 170:3065-3071.
55. Reysenbach, A. 2001. Phylum BI. Aquificae phy. nov., p. 359-367. In D. R. Boone, R. Castenholz, and G. Garrity (ed.), Bergey's manual of systematic bacteriology, 2nd ed., vol.1. Springer, New York, NY.
56. Roberts, M. F. 2005. Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst. 1:5. doi:10.1186/1746-1448-1-5.
57. Rodríguez-Valera, F., F. Ruiz-Berraquero, and A. Ramos-Cormenzana. 1980. Behaviour of mixed populations of halophilic bacteria in continuous cultures. Can. J. Microbiol. 26:1259-1263.
58. Rosselló-Mora, R., M. Lucio, A. Pena, J. Brito-Echeverría, A. López-López, M. Valens-Vadell, M. Frommberger, J. Antón, and P. Schmitt-Kopplin. 2008. Metabolic evidence for biogeographic isolation of the extremophilic bacterium Salinibacter ruber. ISME J. 2:242-253. (Pubitemid 351334273)
59. Schloss, P. D., and J. Handelsman. 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71:1501-1506.
60. Skulachev, V. P., H. Kobayashi, T. A. Krulwich, G. Schafer, R. H. Fillingame, R. K. Poole, G. M. Cook, M. J. Dimroth, W. N. Konings, and J. B. Stock. 1999. Bacterial energetics at high pH: what happens to the H+ cycle when the extracellular H+ concentration decreases? Bacterial response to pH. Novartis Found. Symp. 221:200-217.
61. Venter, J. C., K. Remington, J. F. Heidelberg, A. L. Halpern, D. Rusch, J. A. Eisen, D. Wu, I. Paulsen, K. E. Nelson, W. Nelson, D. E. Fouts, S. Levy, A. H. Knap, M. W. Lomas, K. Nealson, O. White, J. Peterson, J. Hoffman, R. Parsons, H. Baden-Tillson, C. Pfannkoch, Y.-H. Rogers, and H. O. Smith. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66-74. (Pubitemid 38451457)
62. Wang, G. C., and Y. Wang. 1996. The frequency of chimeric molecules as a consequence of PCR co-amplification of 16S rRNA genes from different bacterial species. Microbiology 142:1107-1114.
63. Whitaker, R. J., D. W. Grogan, and J. W. Taylor. 2003. Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976-978.
64. Williams, W. D., and J. E. Sherwood. 1994. Definition and measurement of salinity in salt lakes. Int. J. Salt Lake Res. 3:53-63.
65. Wu, Q. L., G. Zwart, M. Schauer, M. P. Kamst-van Agterveld, and M. W. Hahn. 2006. Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan plateau, China. Appl. Environ. Microbiol. 72:5478-5485.
66. Xiyu, Z., Z. Minggang, and D. Jihe. 1992. Salt lakes in Inner Mongolia. Science Press, Beijing, China.
67. Yannarell, A. C., and E. W. Triplett. 2005. Geographic and environmental sources of variation in lake bacterial community composition. Appl. Environ. Microbiol. 71:227-239.
68. Yu, G., S. P. Harrison, and B. Xue. 2001. Lake status records from China: data base documentation. MPI-BGC Technical Report 4.
69. Zheng, X., M. Zhang, J. Dong, Z. Gao, C. Xu, Z. Han, B. Zhang, D. Sun, and K. Wang. 1992. Salt lakes in Inner Mongolia of China. Science Press, Beijing, China.
70. Zhongling, L. 1963. An outline of stipa steppes in Inner Mongolia. Acta Phytoecol. Geobot. Sin. 1:156-158.