Metagenomic and stable isotopic analyses of modern freshwater microbialites in Cuatro Ciénegas, Mexico

Environmental Microbiology

Volumn 11, Issue 1, 2009, Pages 16-34

  Breitbart, Mya ^a   Hoare, Ana ^a   Nitti, Anthony ^a   Siefert, Janet ^b   Haynes, Matthew ^c   Dinsdale, Elizabeth ^c,d   Edwards, Robert ^e,f   Souza, Valeria ^g   Rohwer, Forest ^c   Hollander, David ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b Rice University   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

^d FLINDERS UNIVERSITY   (Australia)

^e San Diego State University   (United States)

^f ARGONNE NATIONAL LABORATORY   (United States)

^g UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONIC ACID DERIVATIVE; FRESH WATER; POLYMER;

ARTICLE; BIODIVERSITY; CHEMISTRY; DNA SEQUENCE; ISOTOPE LABELING; METABOLISM; MEXICO; MICROBIOLOGY; SEDIMENT;

BIODIVERSITY; CARBONATES; FRESH WATER; GEOLOGIC SEDIMENTS; ISOTOPE LABELING; MEXICO; POLYMERS; SEQUENCE ANALYSIS, DNA;

EID: 58149291858     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2008.01725.x     Document Type: Article

References (106)

1. Abraham, W.-R., Strompl, C., Vancanneyt, M., Bennasar, A., Swings, J., Lunsdorf, H., et al. (2004) Woodsholea maritima gen. nov., sp. nov., a marine bacterium with a low diversity of polar lipids. Int J Syst Evol Microbiol 54 : 1227 1234.
2. Akagawa-Matsushita, M., Matsuop, M., Koga, Y. Yamasato, K. (1992) Alteromonas atlantica sp. nov. and Alteromonas carrageenovora sp. nov. bacteria that decompose algal polysaccharides. Int J Syst Bacteriol 42 : 621 627.
3. Alcaraz, L., Olmedo, G., Bonilla, G., Cerritos, R., Hernandez, G., Cruz, A., et al. (2008) The genome of Bacillus coahuilensis reveals adaptations essential for survival in the relic of an ancient marine environment. Proc Natl Acad Sci USA 105 : 5803 5808.
4. Aldama Rodriguez, Á.A., Aparicio Mijares, F.J., Gutiérrez Ojeda, C., Martínez Morales, M., González Hita, L., Herrera Zamarrón, G., et al. (2005) Estudio Hidrogeológico de los Acuíferos el Hundido y Cuatrociénegas, Coahuila. México : Instituto Méxicano de Tecnología del Agua (IMTA).
5. Allwood, A., Walter, M., Kamber, B., Marshall, C. Burch, I. (2006) Stromatolite reef from the early archaean era of Australia. Nature 441 : 714 718.
6. Andres, M., Sumner, D., Reid, R. Swart, P. (2006) Isotopic fingerprints of microbial respiration in aragonite from Bahamian stromatolites. Geology 34 : 973 976.
7. Atlas, E., Gordon, L., Hager, S. Park, P. (1971) A Practical Manual for Use of the Technicon AutoAnalyzer in Seawater Nutrient Analysis (Revised): Corvallis. In Department of Oceanography Technical Report 215. Corvallis, Oregon, USA : Oregon State University, pp. 1 49.
8. Awramik, S. (1992) The history and significance of stromatolites. In Early Organic Evolution, Implications for Mineral and Energy Resources. Schidlowski, M., Golubic, S. Kimberley, M. (eds). Berlin, Germany : Springer-Verlag, pp. 435 449.
9. 2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54 : 609 622.
10. Badino, G., Bernabel, T., de Vivo, A., Giulivo, I. Savino, G., eds. (2004) Under the desert: the mysterious waters of Cuatro Cienegas. Italy : La Venta - Explorazioni Geografiche.
11. Barreto, M., Jedlicki, E. Holmes, D. (2005) Identification of a gene cluster for the formation of extracellular polysaccharide precursors in the chemolithoautotroph Acidithiobacillus ferrooxidans. Appl Environ Microbiol 71 : 2902 2909.
12. Baumgartner, L., Reid, R., Dupraz, C., Decho, A., Buckley, D., Spear, J., et al. (2006) Sulfate reducing bacteria in microbial mats: changing paradigms, new discoveries. Sediment Geol 185 : 131 145.
13. Bosak, T. Newman, D. (2005) Microbial kinetic controls on calcite morphology in supersaturated solutions. J Sediment Res 75 : 190 199.
14. Braissant, O., Decho, A., Dupraz, C., Glunk, C., Przekop, K. Visscher, P. (2007) Exopolymeric substances of sulfate-reducing bacteria: Interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology 5 : 401 411.
15. Breitbart, M., Thompson, L., Suttle, C. Sullivan, M. (2007) Exploring the vast diversity of marine viruses. Oceanography 20 : 135 139.
16. Brocks, J., Logan, G., Buick, R. Summons, R. (1999) Archean molecular fossils and the early rise of eukaryotes. Science 285 : 1033 1036.
17. Bryant, D.A. Frigaard, N.U. (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14 : 488 496.
18. Burns, B.P., Goh, F., Allen, M. Neilan, B.A. (2004) Microbial diversity of extant stromatolites in the hypersaline marine environment of Shark Bay. Aust Environ Microbiol 6 : 1096 1101.
19. Canfield, D. (2001) Isotope fractionation by natural populations of sulfate-reducing bacteria. Geochim Cosmochim Acta 65 : 1117 1124.
20. Cline, J. Kaplin, I. (1975) Isotopic fractionation of dissolved nitrate during denitrification in the eastern tropical North Pacific Ocean. Mar Chem 3 : 271 299.
21. Cole, J., Chai, B., Farris, R., Wang, Q., Kulam-Syed-Mohideen, A., McGarrell, D., et al. (2007) The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35 : D169 D172.
22. Danese, P., Pratt, L. Kolter, R. (2000) Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol 182 : 3593 3596.
23. Davies, D. (1999) Regulation of matrix polymer in biofilm formation and dispersion. In Microbial Extracellular Polymeric Substances: Characterization, Structure and Function. Wingender, J., Neu, T. Flemming, H. (eds). Berlin, Germany : Springer-Verlag, pp. 93 118.
24. Davies, A.G., Parsek, M.R., Pearson, J.P., Iglewski, B.H., Costerton, J.W. Greenberg, E.P. (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280 : 295 298.
25. Decho, A.W. (1990) Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes. Annu Rev Mar Biol 28 : 73 153.
26. Decho, A. (1999) Chemical communication within microbial biofilms: chemotaxis and quorum sensing in bacteria cells. In Microbial Extracellular Polymeric Substances: Characterization, Structure and Function. Wingender, J., Neu, T. Flemming, H., eds. Berlin, Germany : Springer-Verlag, pp. 155 169.
27. Decho, A. (2000) Microbial biofilms in intertidal systems: an overview. Continental Shelf Res 20 : 1257 1273.
28. Decho, A., Visscher, P. Reid, P. (2005) Production and cycling of natural microbial exopolymers (EPS) within a marine stromatolite. Palaeogeogr Palaeoclimatol Palaeoecol 219 : 71 86.
29. Degeest, B., Janssens, B. De Vuyst, L. (2001) Exopolysaccharide (EPS) biosynthesis by Lactobacillus sakei 0-1: production kinetics, enzyme activities and EPS yields. J Appl Microbiol 91 : 470 477.
30. DeGraaf, R.M., Visscher, J. Schwartz, A.W. (1997) Reactive phosphonic acids as prebiotic carriers of phosphorus. J Mol Evol 44 : 237 241.
31. Des Marais, D. (1991) Microbial mats, stromatolites and the rise of oxygen in the Precambrian atmosphere. Palaeogeogr Palaeoclimatol Palaeoecol 97 : 93 96.
32. Des Marais, D., Cohen, Y., Nguyen, H., Cheatham, M., Cheatham, T. Munoz, E. (1989) Carbon isotopic trends in the hypersaline ponds and microbial mats at Guerrero Negro, Baja California Sur, Mexico: implications for precambrian stromatolites. In Microbial Mats: Physiological Ecology of Benthic Microbial Communities. Rosenberg, E. (ed). Washington DC, USA : American Society for Microbiology, pp. 191 203.
33. Desnues, C., Rodriguez-Brito, B., Rayhawk, S., Kelley, S., Tran, T., Haynes, M., et al. (2008) Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature 452 : 340 343.
34. Diez-Roux, G. Ballabio, A. (2005) Sulfatases and human disease. Annu Rev Genomics Hum Genetics 6 : 355 379.
35. Dinsdale, E., Edwards, R., Hall, D., Angly, F., Breitbart, M., Brulc, J., et al. (2008) Functional metagenomic profiling of nine biomes. Nature 452 : 629 633.
36. Dupraz, C. Visscher, P. (2005) Microbial lithification in marine stromatolites and hypersaline mats. Trends Microbiol 13 : 429 438.
37. Dupraz, C., Visscher, P., Baumgartner, L. Reid, R. (2004) Microbe-mineral interactions: early carbonate precipitation in a hypersaline lake (Eleuthera Island, Bahamas). Sedimentology 51 : 745 765.
38. Dyhrman, S.T., Chappell, P.D., Haley, S.T., Moffett, J.W., Orchard, E.D., Waterbury, J.B. Webb, E.A. (2006) Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439 : 68 71.
39. Edwards, R., Rodriguez-Brito, B., Wegley, L., Haynes, M., Breitbart, M., Peterson, D., et al. (2006) Comparative metagenomics of microbial communities from the Soudan banded iron mine. BMC Genomics 7 : 57.
40. Eichhorn, E., Van der Ploeg, J.R. Leisinger, T. (2000) Deletion analysis of the Escherichia coli taurine and alkanesulfonate transport systems. J Bacteriol 182 : 2687 2695.
41. Elser, J., Schampel, J., Garcia-Pichel, F., Wade, B., Souza, V., Eguiarte, L., et al. (2005a) Effects of phosphorus enrichment and grazing snails on modern stromatolitic microbial communities. Freshw Biol 50 : 1808 1825.
42. Elser, J.J., Schampel, J.H., Kyle, M., Watts, J., Carson, E.W., Dowling, T.E., et al. (2005b) Response of grazing snails to phosphorus enrichment of modern stromatolitic microbial communities. Freshw Biol 50 : 1826 1835.
43. Emrich, K., Ehhalt, D. Vogel, J. (1970) Carbon isotopic fractionation during the precipitation of calcium carbonate. Earth Planet Sci Lett 8 : 363 371.
44. Engel, M.H. Macko, S.A., eds. (1993) Organic geochemistry: principles and applications. New York, USA : Plenum Press.
45. Falcon, L., Cerritos, R., Eguiarte, L. Souza, V. (2007) Nitrogen fixation in microbial mat and stromatolite communities from Cuatro Cienegas. Mexico Microb Ecol 54 : 363 373.
46. Farres, J., Caminal, G. LopezSantin, J. (1997) Influence of phosphate on rhamnose-containing exopolysaccharide rheology and production by Klebsiella I-714. Appl Microbiol Biotechnol 48 : 522 527.
47. Farrimond, P., Head, I. Innes, H. (2000) Environmental influence on the biohopanoid composition of recent sediments. Geochim Cosmochim Acta 64 : 2985 2992.
48. Ferris, F., Thompson, J. Beveridge, T. (1997) Modern freshwater microbialites from Kelly Lake, British Columbia. Can Palaios 12 : 213 219.
49. Flemming, H., Neu, T. Wozniak, D. (2007) The EPS matrix: the 'house of biofilm cells'. J Bacteriol 189 : 7945 7947.
50. Fogel, M. Cifeuntes, L. (1993) Isotope fractionation during primary production. In Organic Geochemistry. Engel, M. Macko, S. (eds). New York, USA : Plenum.
51. Garcia-Pichel, F., Al-Horani, F., Farmer, J., Ludwig, R. Wade, B. (2004) Balance between microbial calcification and metazoan bioerosion in modern stromatolitic oncolites. Geobiology 2 : 49 57.
52. Ghannoum, M. O'Toole, G., eds. (2004) Microbial Biofilms. Washington DC, USA : American Society for Microbiology Press.
53. Golden, S. Canales, S. (2003) Cyanobacterial circadian clocks - timing is everything. Nat Rev Microbiol 1 : 191 199.
54. Gordon, L., Jennings, J., Ross, A. Krest, J. (1993) A suggested protocol for continuous flow automated analysis of seawater nutrients. WOCE Oper Man 77 : 1 52.
55. Grasshoff, K. (1976) Methods of Seawater Analysis. Weinheim, NY, USA : Verlag Chemie.
56. Grotzinger, J. Knoll, A. (1999) Stromatolites in Precambrian carbonates: evolutionary mileposts or environmental dipsticks? Annu Rev Earth Planet Sci 27 : 313 358.
57. Hagele, D., Leinfelder, R., Grau, J., Burmeister, E.-G. Struck, U. (2006) Oncoids from the river Alz (southern Germany): tiny ecosystems in a phosphorus-limited environment. Palaeogeogr Palaeoclimatol Palaeoecol 237 : 378 395.
58. Hammes, F. Verstraete, W. (2002) Key roles of pH and calcium metabolism in microbial carbonate precipitation. Re/Views Environ Sci Bio/Technol 1 : 3 7.
59. 13C contents of sedimentary organic compounds: principles and evidence. Mar Geol 113 : 111 125.
60. Hoshi, M. Moriya, T. (1980) Arylsulfatase of sea-urchin sperm. 2. Arylsulfatase as a lysin of sea-urchins. Dev Biol 74 : 343 350.
61. Ingalls, A., Lee, C. Druffel, E. (2003) Preservation of organic matter in mound-forming coral skeletons. Geochim Cosmochim Acta 67 : 2827 2841.
62. Jahnke, L., Eder, W., Huber, R., Hope, J., Hinrichs, K., Hayes, J., et al. (2001) Signature lipids and stable carbon isotope analyses of octopus spring hyperthermophilic communities compared with those of Aquificales representatives. Appl Environ Microbiol 67 : 5179 5189.
63. Jahnke, L., Embaye, T., Hope, J., Turk, K., Van Zullen, M., Des Marais, D., et al. (2004) Lipid biomarker and carbon isotopic signatures for stromatolite-forming, microbial mat communities and Phormidium cultures from Yellowstone National Park. Geobiology 2 : 31 47.
64. Karl, D., Michaels, A., Bergman, B., Capone, D., Carpenter, E., Letelier, R., et al. (2002) Dinitrogen fixation in the world's oceans. Biogeochemistry 57/58 : 47 98.
65. Ke, B. (2001) Photosynthesis: Photobiochemistry and Photobiophysics. Berlin, Germany : Springer.
66. Kim, D.-E., Kim, K.-H., Bae, Y.-J., Lee, J.-H., Jang, Y.-H. Nam, S.-W. (2005) Purification and characterization of the recombinant arylsulfatase cloned from Pseudoalteromonas carrageenovora. Protein Expr Purif 39 : 109 115.
67. Kononova, S.V. Nesmeyanova, M.A. (2002) Phosphonates and their degradation by microorganisms. Biochemistry-Moscow 67 : 184 195.
68. Kornberg, A. (1995) Inorganic polyphosphate: Towards making a forgotten polymer unforgettable. J Bacteriol 177 : 491 496.
69. Krumbein, W., Cohen, Y. Shilo, M. (1977) Solar Lake (Sinai). 4. Stromatolite cyanobacterial mats. Limnol Oceanogr 22 : 635 656.
70. 2S coexistence in stromatolites. Naturwissenschaften 66 : 381 389.
71. Lakin-Thomas, P. (2006) New models for circadian systems in microorganisms. FEMS Microbiol Lett 259 : 1 6.
72. Lin, Y. Singer, P. (2005) Inhibition of calcite crystal growth by polyphosphates. Water Res 39 : 4835 4843.
73. Lopez-Garcia, P., Kazmierczak, J., Benzerara, K., Kempe, S., Guyot, F. Moreira, D. (2005) Bacterial diversity and carbonate precipitation in the giant microbialites from the highly alkaline Lake Van, Turkey. Extremophiles 9 : 263 274.
74. Margulies, M., Egholm, M., Altman, W., Attiya, S., Bader, J., Bemben, L., et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437 : 376 380.
75. Minckley, W. (1969) Environments of the Bolson of Cuatro Cienegas, Cuahuila, Mexico, with special reference to the aquatic biota. University of Texas El Paso Science Series 2 : 1 65.
76. Mook, W., Bommerson, J. Staverman, W. (1974) Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Planet Sci Lett 22 : 169 176.
77. Moreira, D. Brochier-Armanet, C. (2008) Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol Biol 8 : 12.
78. O'Toole, G. Kolter, R. (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30 : 295 304.
79. Omelchenko, M., Makarova, K., wolf, Y., Rogozin, I. Koonin, E. (2003) Evolution of mosaic operons by horizontal gene transfer and gene displacement in situ. Genome Biol 4 : R55.
80. Overbeek, R., Belgley, T., Butler, R., Choudhuri, J., Chuang, H., Cohoon, M., et al. (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33 : 5691 5702.
81. Papineau, D., Walker, J.J., Mojzsis, S.J. Pace, N.R. (2005) Composition and structure of microbial communities from stromatolites of Hamelin Pool in Shark Bay, Western Australia. Appl Environ Microbiol 71 : 4822 4832.
82. Peant, B., LaPointe, G., Gilbert, C., Atlan, D., Ward, P. Roy, D. (2005) Comparative analysis of the exopolysaccharide biosynthesis gene clusters from four strains of Lactobacillus rhamnosus. Microbiology 151 : 1839 1851.
83. Quail, P. (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3 : 85 93.
84. Reid, R.P., Visscher, P.T., Decho, A.W., Stolz, J.F., Bebout, B.M., Dupraz, C., et al. (2000) The role of microbes in accretion, lamination and early lithification of modern marine stromatolites. Nature 406 : 989 992.
85. Riding, R. (2006) Cyanobacterial calcification, carbon dioxide concentrating mechanisms, and Proterozoic-Cambrian changes in atmospheric composition. Geobiology 4 : 299 316.
86. Schidlowski, M. (1985) Carbon isotope discrepancy between precambrian stromatolites and their modern analogs - inferences from hypersaline microbial mats of the Sinai Coast. Orig Life Evol Biosph 15 : 263 277.
87. Schidlowski, M. (2000) Carbon isotopes and microbial sediments. In Microbial Sediments. Riding, R. Awramik, S. (eds). Berlin, Germany : Springer-Verlag, pp. 84 95.
88. Schidlowski, M., Hayes, J. Kaplan, I. (1983) Isotopic inferences of ancient biochemistries: carbon, sulfur, hydrogen, and nitrogen. In Earth's Earliest Biosphere: its Origin and Evolution. Schopf, J., (ed.). Princeton, NJ, USA : Princeton University Press, pp. 149 186.
89. Schopf, J., ed. (1983) Earth's Earliest Biosphere: Its Origin and Evolution. Princeton, NJ, USA : Princeton University Press.
90. Schopf, J., Hayes, J. Walter, M. (1983) Evolution of Earth's earliest ecosystems: recent progress and unsolved problems. In Earth's Earliest Biosphere: its Origin and Evolution. Schopf, J. (ed.). Princeton, NJ, USA : Princeton University Press, pp. 361 384.
91. Sigman, D., Altabet, M., Michener, R., McCorkle, D., Fry, B. Holmes, R. (1997) Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: an adaptation of the ammonia diffusion method. Mar Chem 57 : 227 242.
92. Souza, V., Espinosa-Asuar, L., Escalante, A.E., Eguiarte, L.E., Farmer, J., Forney, L., et al. (2006) An endangered oasis of aquatic microbial biodiversity in the Chihuahuan desert. Proc Natl Acad Sci USA 103 : 6565 6570.
93. Stein, B., Kutner, L. Adams, J., eds. (2000) Precious Heritage: The Status of Biodiversity in the United States. Oxford, UK : Oxford University Press.
94. Sutherland, I. (2004) Microbial exopolysaccharides. In Polysaccharides: Structural Diversity and Functional Versatility. Dumitriu, S. (ed.). New York, USA : CRC Press, pp. 431 458.
95. Telford, J., Barocchi, M., Margarit, I., Rappuoli, R. Grandi, G. (2006) Pili in Gram-positive pathogens. Nat Rev Microbiol 4 : 509 519.
96. Thompson, J. Ferris, F. (1990) Cyanobacterial precipitation of gypsum, calcite, and magnesite from natural alkaline lake water. Geology 18 : 995 998.
97. Tomich, M., Planet, P.J. Figurski, D.H. (2007) The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol 5 : 363 375.
98. Van Mooy, B.A.S., Rocap, G., Fredricks, H.F., Evans, C.T. Devol, A.H. (2006) Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc Natl Acad Sci USA 103 : 8607 8612.
99. Vasconcelos, G. McKenzie, J. (1997) Microbial mediation of modern dolomite precipitation and diagenesis under anoxic conditions (Lagoa Vermelha, Rio de Janeiro, Brazil). J Sediment Res 67 : 378 390.
100. Vasconcelos, G., McKenzie, J., Bernasconi, S., Grujie, D. Tien, A. (1995) Microbial mediation as a possible mechanism for natural dolomite formation at low temperature. Nature 337 : 220 222.
101. Visscher, P. Stolz, J. (2005) Microbial mats as bioreactors: populations, processes and products. Palaeo 219 : 87 100.
102. Visscher, P., Gritzer, R. Leadbetter, E. (1999) Low-molecular-weight sulfonates, a major substrate for sulfate reducers in marine microbial mats. Appl Environ Microbiol 65 : 3272 3278.
103. Visscher, P.T., Reid, R.P., Bebout, B.M., Hoeft, S.E., Macintyre, I.G. Thompson, J.A. (1998) Formation of lithified micritic laminae in modern marine stromatolites (Bahamas): the role of sulfur cycling. Am Mineral 83 : 1482 1493.
104. Visscher, P.T., Reid, R.P. Bebout, B.M. (2000) Microscale observations of sulfate reduction: correlation of microbial activity with lithified micritic laminae in modern marine stromatolites. Geology 28 : 919 922.
105. Wolfaardt, G., Lawrence, J. Korber, D. (1999) Function of EPS. In Microbial Extracellular Polymeric Substances: Characterization, Structure and Function. Wingender, J., Neu, T. Flemming, H.-C. (eds). Berlin, Germany : Springer, pp. 171 200.
106. Yancey, P. (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208 : 2819 2830.