Molecular indicators of microbial diversity in oolitic sands of Highborne Cay, Bahamas

Geobiology

Volumn 11, Issue 3, 2013, Pages 234-251

  Edgcomb, V P ^a   Bernhard, J M ^a   Beaudoin, D ^a   Pruss, S ^b   Welander, P V ^c,d   Schubotz, F ^c   Mehay, S ^c,e   Gillespie, A L ^c   Summons, R E ^c  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b SMITH COLLEGE   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d STANFORD UNIVERSITY   (United States)

^e SCHLUMBERGER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CALCIUM CARBONATE; LIPID; RNA 16S; SILICON DIOXIDE;

BACTERIUM; BIOINDICATOR; BIOMARKER; CALCIUM CARBONATE; COMMUNITY STRUCTURE; CYANOBACTERIUM; FRAGMENTATION; LIPID; MINERALIZATION; MOLECULAR ANALYSIS; OOLITE; ORGANIC MATTER; SPECIES DIVERSITY; STROMATOLITE; TAXONOMY; THROMBOLITE;

ARTICLE; BACTERIUM; BAHAMAS; BIODIVERSITY; BIOTA; CHEMISTRY; DNA SEQUENCE; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEDIMENT;

BACTERIA; BAHAMAS; BASE SEQUENCE; BIODIVERSITY; BIOLOGICAL MARKERS; BIOTA; CALCIUM CARBONATE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GEOLOGIC SEDIMENTS; LIPIDS; MOLECULAR SEQUENCE DATA; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SILICON DIOXIDE;

BAHAMAS; HIGHBORNE CAY;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); CYANOBACTERIA; DELTAPROTEOBACTERIA; GAMMAPROTEOBACTERIA; PLANCTOMYCES;

EID: 84876153167     PISSN: 14724677     EISSN: 14724669     Source Type: Journal    
DOI: 10.1111/gbi.12029     Document Type: Article

References (87)

1. Allen MA, Burns BP, Neilan BA, Jahnke LL, Summons RE (2010) Lipid biomarkers in Hamelin Pool microbial mats and stromatolites. Organic Geochemistry 41, 1207-1218.
2. Allwood AC, Walter MR, Kamber BS, Marshall CP, Burch IW (2006) Stromatolite reef from the Early Archaean era of Australia. Nature 441, 714-718.
3. Baumgartner LK (2007) Diversity and lithification in microbial mats and stromatolites. PhD dissertation, University of Connecticut, Mansfield, CT, pp. 55-74.
4. Baumgartner LK, Reid RP, Dupraz C, Decho AW, Buckley DH, Spear JR, Przekop KM, And Visscher PT (2006) Sulfate reducing bacteria in microbial mats: changing paradigms, new discoveries. Sedimentary Geology 185, 131-145.
5. Berner RA (1971) Principles of Chemical Sedimentology, McGraw-Hill, NY, 240 pp.
6. Bernhard JM, Visscher PT, Bowser SS (2003) Submillimeter life positions of bacteria, protists, and metazoans in laminated sediments of the Santa Barbara Basin. Limnology and Oceanography 48, 813-828.
7. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911-917.
8. Blumenberg M, Kruger M, Nauhaus K, Talbot HM, Oppermann BI, Seifert R, Pape T, Michaelis W (2006) Biosynthesis of hopanoids by sulfate-reducing bacteria (genus Desulfovibrio). Environmental Microbiology 8, 1220-1227.
9. Bowlin EM, Klaus JS, Foster JS, Andres MS, Custals L, Reid RP (2012) Environmental controls on microbial community cycling in modern marine stromatolites. Sedimentary Geology 263-264, 45-55.
10. Brehm U, Palinska KA, Krumbein WE (2004) Laboratory cultures of calcifying biomicrospheres generate ooids - a contribution to the origin of oolites. Carnets de Geologie/Notebooks on Geology, Maintenon, Letter 2004/03, 1-6.
11. Brehm U, Krumbein WE, Palinska KA (2006) Laboratory cultures of calcifying biomicrospheres generate ooids - a contribution to the origin of oolites Carnets de Geologie/Notebooks on Geology, Maintenon, Letter 2004/03, p. CG2004_L03.
12. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335-336.
13. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, Garrity GM, Tiedje JM. (2005) The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33, D294-D296.
14. Davaud E, Girardclos S (2001) Recent freshwater ooids and oncoids from western Lake Geneva (Switzerland): indications of a common organically mediated origin. Journal of Sedimentary Research 71, 423-429.
15. Davies PJ, Bubela B, Ferguson J (1978) The formation of ooids. Sedimentology 25, 703-729.
16. Decho AW, Visscher PT, Reid RP (2005) Production and cycling of natural microbial exopolymers (EPS) within a marine stromatolite. Palaeogeography, Palaeoclimatology, Palaeoecology 219, 71-86.
17. Des Marais DJ (2003) Biogeochemistry of hypersaline microbial mats illustrates the dynamics of modern microbial ecosystems and the early evolution of the biosphere. Biological Bulletin 204, 160-167.
18. Donohue J (1969) Genesis of oolite and posolite grains: an energy index. Journal of Sedimentary Petrology 39, 1399-1411.
19. Dowling NJE, Widdel F, White DC (1986) Phospholipid ester-linked fatty acid biomarkers of acetate-oxidizing sulphate-reducers and other sulphide-forming bacteria. Journal of General Microbiology 132, 1815-1825.
20. Dowling NJE, Nichols PD, White DC (1988) Phospholipid fatty acid and infra-red spectroscopic analysis of a sulphate-reducing consortium. FEMS Microbiology Letters 53, 325-333.
21. Duguid SMA, Kyser K, James NP, Rankey EC (2010) Microbes and ooids. Journal of Sedimentary Research 80, 236-251.
22. Folk RL, Lynch FL (2001) Organic matter, putative nannobacteria and the formation of ooids and hardgrounds. Sedimentology 48, 215-229.
23. Foster J.S., Green S.J. (2011) Microbial diversity in modern stromatolites. In Stromatolites: interaction of Microbes with Sediments, Cellular Origin, Life in Extreme Habitats and Astrobiology (eds Tewari VC, Seckbach J) 18:383-405.
24. Foster JS, Green SJ, Ahrendt SR, Golubic S, Reid RP, Hetherington KL, Bebout L (2009) Molecular and morphological characterization of cyanobacterial diversity in the stromatolites of Highborne Cay, Bahamas. The ISME Journal 3, 573-587.
25. Geiger O, Röhrs V, Weissenmayer B, Finan TM, Thomas-Oates JE (1999) The regulator gene phoB mediates phosphate stress-controlled synthesis of the membrane lipid diacylglyceroyl-N, N, N-trimethylhomoserine in Rhizobium (Sinorhizobium) meliloti. Molecular Microbiology 32, 63-73.
26. Geiger O, Gonzáles-Silva N, López-lara IM, Sohlenkamp C (2010) Amino acid-containing membrane lipids in bacteria. Progress in Lipid Research 49, 46-60.
27. Glumac B, Curran HA, Weigner MM, Motti SA, Pruss SB (2012) Distribution of oolitic sediment along a beach-to-offshore transect, Pigeon Cay, Cat Island, Bahamas: New insights into modern ooid formation. In Proceedings of the 15th Symposium on the Geology of the Bahamas and other Carbonate Regions (eds Gamble DW, Kindler P). 69-79.
28. Golubic S, Browne KM (1996) Schizothrix gebeleinii sp. nov. builds subtidal stromatolites, Lee Stocking Island, Bahamas. Algological Studies 83, 273-290.
29. Green SJ, Blackford C, Bucki P, Jahnke LL, Prufert-Bebout L (2008) A salinity and sulfate manipulation of hypersaline microbial mats reveals stasis in the cyanobacterial community structure. The ISME Journal 2, 457-470.
30. Grotzinger JP, Knoll AH (1999) Stromatolites in Precambrian carbonates: evolutionary mileposts or environmental dipsticks? Annual Review of Earth and Planetary Sciences 27, 313-358.
31. Guyoneaud R, Moune S, Eatock C, Bothorel V, Hirschler-Rea A, et al. (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 thiosulfatophila sp. nov. Archives of Microbiology 178, 315-324.
32. Handley L, Talbot HM, Cooke MP, Anderson KE, Wagner T (2010) Bacteriohopanepolyols as tracers for continental and marine organic matter supply and phases of enhanced nitrogen cycling on the late Quaternary Congo deep sea fan. Organic Geochemistry 41, 910-914.
33. Harris PM, Halley RB, Lukas KJ (1979) Endolith microborings and their preservation in Holocene-Pleistocene (Bahamas-Florida) ooids. Geology 7, 216-220.
34. Jahnke LL, Eder W, Huber R, Hope JM, Hinrichs K-U, Hayes JM, Des Marais DJ, Cady SL, Summons RE (2001) Signature lipids and stable carbon isotope analyses of Octopus Spring hyperthermophilic communities compared to those of Aquificales representatives. Applied and Environmental Microbiology 67, 5179-5189.
35. Jahnke LL, Embaye T, Hope JM, Turk KA, van Zuillen M, Des Marais DJ, Farmer JD, Summons RE (2004) Lipid biomarker and carbon isotopic signatures for stromatolite-forming, microbial mat communities and Phormidium cultures from Yellowstone National Park. Geobiology 2, 31-47.
36. Kennard JM, James NP (1986) Thrombolites and stromatolites: two distinct types of microbial structures. Palaios 1, 492-503.
37. Lane DJ (1991) 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics (eds Stackebrandt E, Goodfellow M). Wiley, Chichester, pp. 115-175.
38. Lepage G, Roy CC (1986) Direct transesterification of all classes of lipids in a one-step reaction. Journal of Lipid Research 27, 114-120.
39. Londry KL, Jahnke LL, Des Marais DJ (2004) Stable carbon isotope ratios of lipid biomarkers of sulfate-reducing bacteria. Applied and Environmental Microbiology 70, 745-751.
40. Lowenstam HA, Epstein A (1957) On the origin of sedimentary aragonite needles of the Great Bahama Bank. Journal of Geology 65, 364-375.
41. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüssmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Research 32, 1363-1371.
42. Minz D, Fishbain S, Green SJ, Muyzer G, Cohen Y, Rittmann BE, Stahl DA (1999) Unexpected population distribution in a microbial mat community: sulfate-reducing bacteria localized to the highly oxic chemocline in contrast to a eukaryotic preference for anoxia. Applied and Environment Microbiology 65, 4659-4665.
43. Mitterer RM (1972) Biogeochemistry of aragonite mud and oolites. Geochimica et Cosmochimica Acta. 36, 1407-1422.
44. Myshrall KL, Mobberley JM, Green SJ, Visscher PT, Havemann SA, Reid RP, et al. (2010) Biogeochemical cycling and microbial diversity in the thrombolitic microbialites of Highborne Cay, Bahamas. Geobiology 8, 337-354.
45. Nebel ME, Wild S, Holzhauser M, Huttenberger L, Reitzig R, Sperber M, Stoeck T (2011) JAguc - a software package for environmental diversity analyses. Journal of Bioinformatics and Computational Biology 9, 749-773.
46. Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify16S rRNA genes from cyanobacteria. Applied and Environmental Microbiology 63, 3327-3332.
47. Pacton M, Ariztegui D, Wacey D, Kilburn MR, Rollion-Bard C, Farah R, Vasconcelos C (2012) Going nano: a new step toward understanding the processes governing freshwater ooid formation. Geology 40, 547-550.
48. Palmisano AC, Summons RE, Cronin SJ, Des Marais DJ (1989) Lipophilic pigments from cyanobacterial (blue-green algal) and diatom mats in Hamelin Pool, Shark Bay, Western Australia. Journal of Phycology 25, 655-661.
49. Pearson A, Eglinton TI (2000) The origin of n-alkanes in Santa Monica Basin surface sediment: a model based on compound-specific Δ14C and δ13C data. Organic Geochemistry 31, 1103-1116.
50. Pearson A, McNichol AP, Benitez-Nelson BC, Hayes JM, Eglinton TI (2001) Origins of lipid biomarkers in Santa Monica Basin surface sediment: a case study using compound-specific Δ14C analysis. Geochimica et Cosmochimica Acta 65, 3123-3137.
51. Pearson A, Leavitt WD, Sáenz JP, Summons RE, Tam MCM, Close HG (2009) Diversity of hopanoids and squalene-hopene cyclases across a tropical land-sea gradient. Environmental Microbiology 11, 1208-1223.
52. Planavsky N, Ginsburg RN (2009) Taphonomy of modern marine Bahamian microbialites. Palaios 24, 5-17.
53. Plée K, Pacton M, Ariztegui D (2010) Discriminating the role of photosynthetic and heterotrophic microbes triggering low-Mg calcite precipitation in freshwater biofilms (Lake Geneva, Switzerland). Geomicrobiology Journal 27, 391-399.
54. Rashby SE, Sessions AL, Summons RE, Newman DK (2007) Biosynthesis of 2- methylbacteriohopanepolyols by an anoxygenic phototroph. Proceedings of the National Academy of Science of the USA 104, 15099-15104.
55. Reid RP, Visscher PT, Decho AW, Stolz JF, Bebout BM, Dupraz C, et al. (2000) The role of microbes in accretion, lamination, and early lithification of modern marine stromatolites. Nature 406, 989-992.
56. Reitner J, Arp G, Thiel V, Gautret P, Galling U, Michaelis W (1997) Organic matter in Great Salt Lake ooids (Utah, USA) - First approach to a formation via organic matrices. Facies 36, 210-219.
57. Riding R (2000) Microbial carbonates: the geological record of calcified bacterial-algal mats and biofilms. Sedimentology 47, 179-214.
58. Rohmer M, Bouvier-Nave P, Ourisson G (1984) Distribution of hopanoid triterpanes in prokaryotes. Journal of General Microbiology 130, 1137-1150.
59. Rütters H, Sass H, Cypionka H, Rullkötter J (2002) Phospholipid analysis as a tool to study complex microbial communities in marine sediments. Journal of Microbiological Methods 48, 149-160.
60. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environmental Microbiology 71, 1501-1506.
61. Schubotz F, Wakeham SG, Lipp JS, Fredricks HF, Hinrichs K-U (2009) Detection of microbial biomass by intact polar membrane lipid analysis in the water column and surface sediments of the Black Sea. Environmental Microbiology 11, 2720-2734.
62. Shiea J, Brassell SC, Ward DM (1990) Mid-chain branched mono- and dimethyl alkanes in hot spring cyanobacterial mats: a direct biogenic source for branched alkanes in ancient sediments? Organic Geochemistry 15, 223-231.
63. Shiea J, Brassell SC, Ward DM (1991) Comparative analysis of extractable lipids in hot spring microbial mats and their component photosynthetic bacteria. Organic Geochemistry 17, 309-319.
64. Sinninghe Damsté JS, Rijpstra WIC, Schouten S, Fuerst JA, Jetten MSM, Strous M (2004) The occurrence of hopanoids in planctomycetes: implications for the sedimentary biomarker record. Organic Geochemistry 35, 561-566.
65. Sohlenkamp C, López-Lara IM, Geiger O (2003) Biosynthesis of phosphatidycholine in bacteria. Progress in Lipid Research 42, 115-162.
66. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690.
67. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758-771.
68. Stolz JF, Feinstein TN, Salsi J, Visscher PT, Reid RP (2001) TEM analysis of microbial mediated sedimentation and lithification in modern marine stromatolites. American Mineralogist 86, 826-833.
69. Sturt HF, Summons RE, Smith K, Elvert M, Hinrichs KU (2004) Intact polar membrane lipids in prokaryotes and sediments deciphered by high-performance liquid chromatography/electrospray ionization multistage mass spectrometry - new biomarkers for biogeochemistry and microbial ecology. Rapid Communications in Mass Spectrometry 18, 617-628.
70. Summons RE, Lincoln SA (2012) Biomarkers: Informative Molecules for Studies in Geobiology. Fundamentals of Geobiology, First Edition. Eds Knoll A.H., Canfield D.E. and Konhauser K.O., Blackwell Publishing Ltd., In, pp. 269-296.
71. Summons RE, Bird LR, Gillespie AL, Pruss SB, Sessions AL (2010) Lipid biomarkers in ooids from different locations and ages provide evidence for a common bacterial flora, American Geophysical Union, Fall Meeting, abstract #PP42A-05.
72. Talbot HM, Farrimond P (2007) Bacterial populations recorded in diverse sedimentary biohopanoid distributions. Organic Geochemistry 38, 1212-1225.
73. Talbot HM, Squier AH, Keely BJ, Farrimond P (2003) Atmospheric pressure chemical ionisation reversed-phase liquid chromatography/ion trap mass spectrometry of intact bacteriohopanepolyols. Rapid Communications in Mass Spectrometry 17, 728-737.
74. Talbot HM, Rohmer M, Farrimond P (2007a) Rapid structural elucidation of composite bacterial hopanoids by atmospheric pressure chemical ionisation liquid chromatography/ion trap mass spectrometry. Rapid Communications in Mass Spectrometry 21, 880-892.
75. Talbot HM, Rohmer M, Farrimond P (2007b) Structural characterisation of unsaturated bacterial hopanoids by atmospheric pressure chemical ionisation liquid chromatography/ion trap mass spectrometry. Rapid Communications in Mass Spectrometry 21, 1613-1622.
76. Talbot HM, Summons RE, Jahnke LL, Cockell CS, Rohmer M, Farrimond P (2008) Cyanobacterial bacteriohopanepolyol signatures from cultures and natural environmental settings. Organic Geochemistry 39, 232-263.
77. Taylor J, Parkes RJ (1983) The cellular fatty acids of the sulphate-reducing bacteria, Desulfobacter sp., Desulfobulbus sp. and Desulfovibrio desulfuricans. Journal of General Microbiology 129, 3303-3309.
78. Tucker ME, Wright VP (1990) Carbonate Sedimentology. Blackwell Science.
79. Visscher PT, Stolz JF (2005) Microbial mats as bioreactors: populations, processes and products. Palaeogeography, Palaeoclimatology, Palaeoecology 219, 87-100.
80. Volkman JK (2003) Sterols in microorganisms. Applied Microbiology and Biotechnology 60, 495-506.
81. Volkman JK (2005) Sterols and other triterpenoids: source specificity and evolution of biosynthetic pathways. Organic Geochemistry 36, 139-159.
82. Wada H, Murata N (1998) Membrane Lipids in cyanobacteria. In Lipids in Photosynthesis: Strucutre, Function and Genetics (eds Siegenthaler P-A, Murate N). Kluwer Academic Publishers, the Netherlands, pp. 65-81.
83. Walter MR, Buick R, Dunlop JSR (1980) Stromatolites 3, 400-3, 500 Myr old from the North-Pole area, Western-Australia. Nature 284, 443-445.
84. Welander PV, Summons RE (2012) Discovery, taxonomic distribution and phenotypic characterization of a gene required for 3-methylhopanoid production. Proceedings of the National Academy of Sciences of the USA, www.pnas.org/cgi/doi/10.1073/pnas.1208255109.
85. Welander PV, Coleman M, Sessions AL, Summons RE, Newman DK (2010) Identification of a methylase required for 2-methylhopanoid production and implications for the interpretation of sedimentary hopanes. Proceedings of the National Academy of Sciences of the USA 107, 8537-8542.
86. White DC, Ringelberg DB (1998) Signature lipid biomarker analysis. In Echniques in Microbial Ecology (eds Burlage RS, Atlas R, Stahl DA, Geesey G, Sayler G). Oxford University Press, New York, N.Y., pp. 255-272.
87. Zhang Y-M, Rock CO (2008) Membrane lipid homoestastis in bacteria. Nature Reviews Microbiology 6, 222-233.