Spatially resolved genomic, stable isotopic, and lipid analyses of a modern freshwater microbialite from Cuatro Ciénegas, Mexico

Astrobiology

Volumn 12, Issue 7, 2012, Pages 685-698

  Nitti, Anthony ^a   Daniels, Camille A ^a   Siefert, Janet ^b   Souza, Valeria ^c   Hollander, David ^a   Breitbart, Mya ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b Rice University   (United States)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Genomics; Microbe mineral interactions; Microbial ecology; Microbial mats; Stromatolites

Indexed keywords

BIOLOGICAL MARKER; CARBON; CARBONIC ACID DERIVATIVE; FRESH WATER; LIPID; RIBOSOME DNA;

ARTICLE; BACTERIUM; BIOLOGICAL MODEL; GENETICS; GENOMICS; ISOTOPE LABELING; METABOLISM; METHODOLOGY; MEXICO; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY;

BACTERIA; BASE SEQUENCE; BIOLOGICAL MARKERS; CARBON ISOTOPES; CARBONATES; DNA, RIBOSOMAL; FRESH WATER; GENOMICS; ISOTOPE LABELING; LIPIDS; MEXICO; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY;

BACTERIA (MICROORGANISMS); PROTEOBACTERIA;

EID: 84865488137     PISSN: 15311074     EISSN: None     Source Type: Journal    
DOI: 10.1089/ast.2011.0812     Document Type: Article

References (79)

1. Allen, M., Goh, F., Burns, B. P., and Neilan, B. A. (2009) Bacterial, archaeal and eukaryotic diversity of smooth and pustular microbial mat communities in the hypersaline lagoon of Shark Bay. Geobiology 7:82-96.
2. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402. (Pubitemid 27359211)
3. Andres, M., Sumner, D., Reid, R., and Swart, P. (2006) Isotopic fingerprints of microbial respiration in aragonite from Bahamian stromatolites. Geology 34:973-976. (Pubitemid 44734365)
4. Bauer, C., Bollivar, D., and Suzuki, J. (1993) Genetic analyses of photopigment biosynthesis in eubacteria: a guiding light for algae and plants. J Bacteriol 175:3919-3925. (Pubitemid 23206883)
5. Bauer, M., Kube, M., Teeling, H., Richter, M., Lombardot, T., Allers, E., Wurdemann, C., Quast, C., Kuhl, H., Knaust, F., Woebken, D., Bischof, K., Mussmann, M., Choudhuri, J. V., Meyer, F., Reinhardt, R., Amann, R. I., and Glöckner, F. O. (2006) Whole genome analysis of the marine Bacteroidetes Gramella forsetii' reveals adaptations to degradation of polymeric organic matter. Environ Microbiol 8:2201-2213. (Pubitemid 44730250)
6. Baumgartner, L., Dupraz, C., Buckley, D., Spear, J., Pace, N., and Visscher, P. (2009a) Microbial species richness and metabolic activities in hypersaline microbial mats: insight into biosignature formation through lithification. Astrobiology 9:861-874.
7. Baumgartner, L., Spear, J., Buckley, D., Pace, N., Reid, R., Dupraz, C., and Visscher, P. (2009b) Microbial diversity in modern marine stromatolites, Highborne Cay, Bahamas. Environ Microbiol 11:2710-2719.
8. Benner, R., Fogel, M. L., Sprague, E. K., and Hodson, R. E. (1987) Depletion of 13C in lignin and its implications for stable carbon isotope studies. Nature 329:708-710.
9. Bosak, T., Greene, S., and Newman, D. (2007) A likely role for anoxygenic photosynthetic microbes in the formation of ancient stromatolites. Geobiology 5:119-126. (Pubitemid 46808900)
10. Boschker, H. and Middelburg, J. (2002) Stable isotopes and biomarkers in microbial ecology. FEMS Microbiol Ecol 40:85-95. (Pubitemid 34607172)
11. Breitbart, M., Hoare, A., Nitti, A., Siefert, J., Haynes, M., Dinsdale, E., Edwards, R., Souza, V., Rohwer, F., and Hollander, D. (2009) Metagenomic and stable isotopic analyses of modern freshwater microbialites in Cuatro Ciénegas, Mexico. Environ Microbiol 11:16-34.
12. Brocks, J. J. and Banfield, J. (2009) Unravelling ancient microbial history with community proteogenomics and lipid geochemistry. Nat Rev Microbiol 7:601-609.
13. Bruckner, C., Bahulikar, H., Rahalkar, M., Schink, B., and Kroth, P. (2008) Bacteria associated with benthic diatoms from Lake Constance: phylogeny and influences on diatom growth and secretion of extracellular polymeric substances. Appl Environ Microbiol 74:7740-7749.
14. Bryant, D. A. and Frigaard, N. U. (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488-496. (Pubitemid 44537806)
15. Buhring, S., Smittenberg, R., Sachse, D., Lipp, J., Golubic, S., Sachs, J., Hinrichs, K. U., and Summons, R. (2009) A hypersaline microbial mat from the Pacific Atoll Kiritimati: insights into composition and carbon fixation using biomarker analyses and a 13C-labeling approach. Geobiology 7:1-16.
16. Burne, R. V. and Moore, L. S. (1987) Microbialites: organosedimentary deposits of benthic microbial communities. Palaios 2:241-254.
17. Burns, B. P., Goh, F., Allen, M., and Neilan, B. A. (2004) Microbial diversity of extant stromatolites in the hypersaline marine environment of Shark Bay, Australia. Environ Microbiol 6:1096-1101. (Pubitemid 39275264)
18. Calder, J. and Parker, P. (1973) Geochemical implications of induced changes in C13 fractionation by blue-green algae. Geochim Cosmochim Acta 37:133-140.
19. Casanova, J., Bodénan, F., Négrel, P., and Azaroual, M. (1999) Microbial control on the precipitation of modern ferrihydrite and carbonate deposits from the Cézallier hydrothermal springs (Massif Central, France). Sediment Geol 126:125-145.
20. Chao, A. (1984) Non-parametric estimation of the number of classes in a population. Scand Stat Theory Appl 11:783-791.
21. De Graaf, W., Sinninghe Damsté, J. S., and de Leeuw, J. W. (1992) Laboratory simulation of natural sulphurization: I. Formation of monomeric and oligomeric isoprenoid polysulphides by low-temperature reactions of inorganic polysulphides with phytol and phytadienes. Geochim Cosmochim Acta 56:4321-4328. (Pubitemid 23377940)
22. De Philippis, R., Faraloni, C., Margheri, M., Sili, C., Herdman, M., and Vincenzini, M. (2000) Morphological and biochemical characterization of the exocellular investments of polysaccharideproducing Nostoc strains from the Pasteur Culture Collection. World J Microbiol Biotechnol 16:655-661. (Pubitemid 32116633)
23. Decho, A. W., Visscher, P. T., and Reid, R. P. (2005) Production and cycling of natural microbial exopolymers (EPS) within a marine stromatolite. Palaeogeogr Palaeoclimatol Palaeoecol 219:71-86. (Pubitemid 40406309)
24. Deines, P. (1980) The isotopic composition of reduced organic carbon. In Handbook of Environmental Geochemistry, edited by P. Fritz and J. Fontess, Elsevier, New York, pp 239-406.
25. Elser, J., Schampel, J., Garcia-Pichel, F., Wade, B., Souza, V., Eguiarte, L., Escalante, A., and Farmer, J. (2005) Effects of phosphorus enrichment and grazing snails on modern stromatolitic microbial communities. Freshw Biol 50:1808-1825. (Pubitemid 43906866)
26. Emrich, K., Ehhalt, D., and Vogel, J. (1970) Carbon isotopic fractionation during the precipitation of calcium carbonate. Earth Planet Sci Lett 8:363-371.
27. Foster, J. and Green, S. (2011) Microbial diversity in modern stromatolites. In Cellular Origin, Life in Extreme Habitats and Astrobiology: Stromatolites: Interaction of Microbes with Sediments, edited by V. Tewari and J. Seckbachs, Springer, Berlin, pp 385-405.
28. Fouke, B., Bonheyo, G., Sanzenbacher, B., and Frias-Lopez, J. (2003) Partitioning of bacterial communities between travertine depositional facies at Mammoth Hot Springs, Yellowstone National Park, U. S. A. Can J Earth Sci 40:1531-1548. (Pubitemid 38306040)
29. Fukushima, K., Yasukawa, M., Muto, N., Uemura, H., and Ishiwatari, R. (1992) Formation of C20 isoprenoid thiophenes in modern sediments. Org Geochem 18:83-91.
30. Garcia-Pichel, F., Al-Horani, F., Farmer, J., Ludwig, R., and Wade, B. (2004) Balance between microbial calcification and metazoan bioerosion in modern stromatolitic oncolites. Geobiology 2:49-57.
31. Goh, F., Allen, M., Leuko, S., Kawaguchi, T., Decho, A., Burns, B., and Neilan, B. (2009) Determining the specific microbial populations and their spatial distribution within the stromatolite ecosystem of Shark Bay. ISME J 3:383-396.
32. Golubic, S. (1976) Taxonomy of extant stromatolite building cyanophytes. In Developments in Sedimentology 20, Stromatolites, edited by M. Walters, Elsevier, Amsterdam, pp 127.140.
33. Grossi, V., Hirschler, A., Raphel, D., Rontani, J.-F., de Leeuw, J., and Bertrand, J.-C. (1998) Biotransformation pathways of phytol in recent anoxic sediments. Org Geochem 29:845-861. (Pubitemid 29020027)
34. Grotzinger, J. and Knoll, A. (1999) Stromatolites in Precambrian carbonates: evolutionary mileposts or environmental dipsticks? Annu Rev Earth Planet Sci 27:313-358. (Pubitemid 30024338)
35. Harwood, J. L. and Guschina, I. A. (2009) The versatility of algae and their lipid metabolism. Biochimie 91:679-684.
36. Havemann, S. and Foster, J. (2008) Comparative characterization of the microbial diversities of an artificial microbialite model and a natural stromatolite. Appl Environ Microbiol 74:7410-7421. (Pubitemid 352773610)
37. Hebting, Y., Schaeffer, P., Behrens, A., Adam, P., Schmitt, G., Schneckenburger, P., Bernasconi, S. M., and Albrecht, P. (2006) Biomarker evidence for a major preservation pathway of sedimentary organic carbon. Science 312:1627-1631. (Pubitemid 43902657)
38. Jahnke, L., Embaye, T., Hope, J., Turk, K., Van Zullen, M., Des Marais, D., Farmer, J., and Summons, R. (2004) Lipid biomarker and carbon isotopic signatures for stromatoliteforming, microbial mat communities and Phormidium cultures from Yellowstone National Park. Geobiology 2:31-47.
39. Jeffrey, S. and Hallergraeff, G. (1987) Chlorophyllase distribution in ten classes of phytoplankton: a problem for chlorophyll analysis. Mar. Ecol Prog Ser 35:293-304.
40. Jungblut, A.-D., Hawes, I., Mountfort, D., Hitzfeld, B., Dietrich, D., Burns, B., and Neilan, B. (2005) Diversity within cyanobacterial mat communities in variable salinity meltwater ponds of McMurdo Ice Shelf, Antarctica. Environ Microbiol 7:519-529. (Pubitemid 40441025)
41. 3 precipitation. Prep Biochem Biotechnol 32:51-63. (Pubitemid 34248715)
42. Kersters, K., De Vos, P., Gillis, M., Swings, J., Vandamme, P., and Stackerbrandt, E. (2006) Introduction to the Proteobacteria. In Prokaryotes, edited by M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer, and E. Stackebrandt, Springer, New York, p 919.
43. Kirchman, D. L. (2002) The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39:91-100. (Pubitemid 34251208)
44. Klock, J.-H., Wieland, A., Seifert, R., and Michaelis, W. (2007) Extracellular polymeric substances (EPS) from cyanobacterial mats: characterisation and isolation method optimisation. Mar. Biol 152:1077-1085. (Pubitemid 47415531)
45. Koster, J., Volkman, J., Rullkotter, J., Schloz-Bottcher, B., Rethmeier, J., and Fischer, U. (1999) Mono-, di-and trimethyl-branched alkanes in cultures of the filamentous cyanobacterium Calothrix scopulorum. Org Geochem 30:1367-1379.
46. Krumbein, W. (1983) Stromatolites.the challenge of a term in space and time. Precambrian Res 20:493-531.
47. Lyons, W., Long, D., Hines, M., Gaudette, H., and Armstrong, P. (1984) Calcification of cyanobacterial mats in Solar Lake, Sinai. Geology 12:623-626.
48. Minckley, W. (1969) Environments of the Bolson of Cuatro Ciénegas, Coahuila, Mexico, with Special Reference to the Aquatic Biota, Science Series No. 2, University of Texas at El Paso, Texas Western Press, El Paso, TX.
49. Minckley, W. L. and Cole, G. A. (1968) Preliminary limnologic information on waters of the Cuatro Ciénegas Basin, Coahuila, Mexico. Southwest Nat 13:421-431.
50. Mook, W. G., Bommerson, J. C., and Staverman, W. H. (1974) Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Planet Sci Lett 22:169-176.
51. Myshrall, K. L., Mobberley, J. M., Green, S. J., Visscher, P. T., Havemann, S. A., Reid, R. P., and Foster, J. S. (2010) Biogeochemical cycling and microbial diversity in the thrombolitic microbialites of Highborne Cay, Bahamas. Geobiology 8:337-354.
52. Papineau, D., Walker, J. J., Mojzsis, S. J., and 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. (Pubitemid 41129541)
53. Pardue, J., Scalan, R., van Baalen, C., and Parker, P. (1976) Maximum carbon isotope fractionation in photosynthesis by blue-green algae and a green alga. Geochim Cosmochim Acta 40:309-312.
54. Poinar, H. (1998) Preservation of DNA in the fossil record. In Nitrogen-Containing Macromolecules in the Bio-and Geosphere, ACS Symposium Series 707, edited by B. Stankiewicz and P. van Bergens, American Chemical Society, Washington DC, pp 132.146.
55. Rontani, J.-F. and Volkman, J. (2003) Phytol degradation products as biogeochemical tracers in aquatic environments. Org Geochem 34:1-35. (Pubitemid 36178154)
56. Rontani, J.-F., Raphel, D., and Cuny, P. (1996) Early diagenesis of the intact and photooxidized chlorophyll phytyl chain in a recent temperate sediment. Org Geochem 24:825-834.
57. Rontani, J.-F., Bonin, P., and Volkman, J. (1999) Biodegradation of free phytol by bacterial communities isolated from marine sediments under aerobic and denitrifying conditions. Appl Environ Microbiol 65:5484-5492. (Pubitemid 129520640)
58. Santos, F., Peña, A., Nogales, B., Soria-Soria, E., del Cura, M., González-Martín, J., and Antón, J. (2010) Bacterial diversity in dry modern freshwater stromatolites from Ruidera Pools Natural Park, Spain. Syst Appl Microbiol 33:209-221.
59. Šantrůcková, H., Bird, M. I., and Lloyd, J. (2000) Microbial processes and carbon-isotope fractionation in tropical and temperate grassland soils. Funct Ecol 14:108-114. (Pubitemid 30194917)
60. Shannon, C. E. and Weaver, W. (1963) The Mathematical Theory of Communication, University of Illinois Press, Urbana, IL.
61. Shiea, J., Brassell, S., and Ward, D. (1990) Mid-chain branched mono-and dimethyl alkanes in hot spring cyanobacterial mats: a direct biogenic source for branched alkanes in ancient sediments? Org Geochem 15:223-231.
62. Sinninghe Damsté, J. S., van Koert, E. R., Kock-van Dalen, A. C., de Leeuw, J. W., and Schenck, P. A. (1989) Characterisation of highly branched isoprenoid thiophenes occurring in sediments and immature crude oils. Org Geochem 14:555-567. (Pubitemid 20633194)
63. Staal, M., Thar, R., Kuhl, M., van Loosdrecht, M., Wolf, G., de Brouwer, J., and Rijstenbil, J. (2007) Different carbon isotope fractionation patterns during the development of phototrophic freshwater and marine biofilms. Biogeosciences 4:613-626. (Pubitemid 47245246)
64. Sutherland, I. (1999) Polysaccharases in biofilms.sources. action. consequences! In Microbial Extracellular Polymeric Substances: Characterization, Structure, and Function, edited by J. Wingender, T. Neu, and H.-C. Flemmings, Springer, Berlin, pp 201.216.
65. Taylor, J. and Parkes, R. (1983) The cellular fatty acids of the sulphate-reducing bacteria, Desulfobacter sp., Desulfobulbus sp. and Desulfovibvio desulfuvicans. J Gen Microbiol 129:3303-3309. (Pubitemid 14200345)
66. Thiel, V., Merz-Preib, M., Reitner, J., and Michaelis, W. (1997) Biomarker studies on microbial carbonates: extractable lipids of a calcifying cyanobacterial mat (Everglades, USA). Facies 136:163-172.
67. Thompson, P. A. and Calvert, S. E. (1994) Carbon-isotope fractionation by a marine diatom: the influence of irradiance, daylength, pH, and nitrogen source. Limnol Oceanogr 39:1835-1844.
68. van Gemerden, H. (1993) Microbial mats: a joint venture. Mar. Geol 113:3-25. (Pubitemid 24393444)
69. Vestal, J. R. and White, D. C. (1989) Lipid analysis in microbial ecology. Bioscience 39:535-541.
70. Visscher, P. and Stolz, J. (2005) Microbial mats as bioreactors: populations, processes and products. Palaeo 219:87-100. (Pubitemid 40406310)
71. Visscher, P. T. and van Gemerden, H. (1991) Production and consumption of dimethylsulfoniopropionate in marine microbial mats. Appl Environ Microbiol 57:3237-3242.
72. Visscher, P. T., Reid, R. P., Bebout, B. M., Hoeft, S. E., Macintyre, I. G., and Thompson, J. A. (1998) Formation of lithified micritic laminae in modern marine stromatolites (Bahamas): the role of sulfur cycling. Am Mineral 83:1482-1493.
73. Visscher, P. T., Reid, R. P., and 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. (Pubitemid 32849517)
74. Volkman, J. and Maxwell, J. (1986) Acyclic isoprenoids as biological markers. In Biological Markers and the Sedimentary Record, Methods in Geochemistry and Geophysics 24, edited by R. B. Johns, Elsevier, New York, pp 1-42.
75. Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261-5267. (Pubitemid 47326658)
76. Weisburg, W. G., Barns, S. M., Pelletier, D. A., and Lane, D. J. (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697-703.
77. Wieland, A., Pape, T., Möbius, J., Klock, J-H., and Michaelis, W. (2008) Carbon pools and isotopic trends in a hypersaline cyanobacterial mat. Geobiology 6:171-186. (Pubitemid 351190182)
78. Winters, K., Parker, P., and van Baalen, C. (1969) Hydrocarbons of blue-green algae: geochemical significance. Science 163:467-468.
79. Yu, Y., Breitbart, M., McNairnie, P., and Rohwer, F. (2006) FastGroupII: a web-based bioinformatics platform for analyses of large 16S rDNA libraries. BMC Bioinformatics 7:57