Mineralogical, chemical and biological characterization of an anaerobic biofilm collected from a borehole in a deep gold mine in South Africa

Geomicrobiology Journal

Volumn 24, Issue 6, 2007, Pages 491-504

  MacLean, L C W ^a   Pray, T J ^b   Onstott, T C ^b   Brodie, E L ^c   Hazen, T C ^c   Southam, G ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b PRINCETON UNIVERSITY   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Community structure; Deep subsurface; Framboidal pyrite; Sulfate reducing bacteria; ZnS

Indexed keywords

BACTERIUM; BIOFILM; COMMUNITY STRUCTURE; GOLD MINE; MINERALOGY; POPULATION DYNAMICS; PYRITE; TRANSMISSION ELECTRON MICROSCOPY;

AFRICA; EAST AFRICA; GEITA MINE; MWANZA [TANZANIA]; SOUTH AFRICA; SOUTHERN AFRICA; SUB-SAHARAN AFRICA; TANZANIA;

BACTERIA (MICROORGANISMS);

EID: 35148880782     PISSN: 01490451     EISSN: 15210529     Source Type: Journal    
DOI: 10.1080/01490450701572416     Document Type: Conference Paper

References (72)

1. Abulencia, C. B., Wyborski, D. L., Garcia, J. A., Podar, M., Chen, W., Chang, S. H., Chang, H. W., Watson, D., Brodie, E. L., Hazen, T. C. and Keller, M. (2006) Environmental whole-genome amplification to access microbial populations in contaminated sediments. Appl. Environ Microbiol, 72, pp. 3291-3301.
2. Banfield, J. F., Welch, S. A., Zhang, H., Ebert, T. T. and Penn, R. L. (2000) Aggregation-based crystal growth and microstructure development in natural iron oxyhydroxide biomineralization products. Science, 289, pp. 751-754.
3. Banfield, J. F., Moreau, J. W., Chan, C. S., Welch, S. A. and Little, B. (2001) Mineralogical biosignatures and the search for life on Mars. Astrobiol, 1, pp. 447-467.
4. Beller, H. R., Chain, P SG, Letain, T. E., Chakicherla, A., Latimer, F. W., Richardson, P. M., Coleman, M. A., Wood, A. P. and Kelly, D. P. (2006) The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J Bacteriol, 188, pp. 1473-1488.
5. Benzerara, K., Menguy, N., Lopez-Garcia, P., Yoon, T. H., Kazmierczak, J., Tyliszczak, T., Guyot, F. and Brown, G. E. (2006) Nanoscale detection of organic signatures in carbonate microbialites. Proc Natl Acad Sci USA, 103, pp. 9440-9445.
6. Berner, R. A. (1969) The synthesis of frambiodal pyrite. Econ Geol, 64, pp. 383-384.
7. Berner, R. A. (1970) Sedimentary pyrite formation. Amer J Sci, 268, pp. 1-23.
8. Bodrossy, L., Holmes, E. M., Holmes, A. J., Kovacs, K. L. and Murrell, J. C. (1997) Analysis of 16S rRNA and methane monooxygenase gene sequences reveals a novel group of thermotolerant and thermophilic methanotrophs, Methylocaldum gen. nov. Arch. Microbiol, 168, pp. 493-503.
9. Bonin, A. S. (2005) Deep subsurface microbiology of the south African gold mines, Ph.D. Dissertation. p. 116. Portland State University
10. Bowman, J. P. and McCuaig, R. D. (2003) Biodiversity, community structural shifts, and biogeography of prokaryotes within Antarctic Continental Shelf sediment. Appl Environ Microbiol, 69, pp. 2463-2483.
11. Brodie, E. L., De Santis, T. Z., Joyner, D. C., Baek, S. M., Larsen, J. T., Andersen, G. L., Hazen, T. C., Richardson, P. M., Herman, D. J., Tokunaga, T. K., Wan, J. M. and Firestone, M. K. (2006) Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation. Appl Environ Microbiol, 72, pp. 6288-6298.
12. Butler, I. B. and Rickard, D. T. (2000) The origin of framboids. Lithos, 3, pp. 269-293.
13. Butler, I. B. and Rickard, D. (2000) Framboidal pyrite formation via the oxidation of iron (II) monosulphide by hydrogen sulphide. Geochim Cosmochim Acta, 64, pp. 2665-2672.
14. Cady, S. L., Farmer, J. D., Grotzinger, J. P., Schopf, J. W. and Steele, A. (2003) Morphological biosignatures and the search for life on Mars. Astrobiol, 3, pp. 351-368.
15. Chao, A. (1984) Non-parametric estimation of the number of classes in a population. Scand J Stat, 11, pp. 265-270.
16. Chen, X. G., Geng, A. L., Yan, R., Gould, W. D., Ng, Y. L. and Liang, D. T. (2004) Isolation and characterization of sulphur-oxidizing Thiomonas sp. and its potential application in biological deodorization. Lett Appl Microbiol, 39, pp. 95-503.
17. Chen, C. L., Macarie, H., Ramirez, I., Olmos, A., Ong, S. L., Monroy, O. and Liu, W. T. (2004) Microbial community structure in a thermophilic anaerobic hybrid reactor degrading terephthalate. Microbiology (Reading, Engl.), 150, pp. 3429-3440.
18. Dedysh, S. N., Ricke, P. and Liesack, W. (2004) NifH and NifD phylogenies: An evolutionary basis for understanding nitrogen fixation capabilities of methanotrophic bacteria. Microbiology (Reading, Engl.), 150, pp. 1301-1313.
19. Dedysh, S. N., Pankratov, T. A., Belova, S. E., Kulichevskaya, I. S. and Liesack, W. (2006) Phylogenetic analysis and in situ identification of bacteria community composition in an acidic Sphagnum peat bog. Appl Environ Microbiol, 72, pp. 2110-2117.
20. Donald, R. and Southam, G. (1999) Low temperature anaerobic bacterial diagenesis of ferrous monosulfide to pyrite. Geochim Cosmochim Acta, 63, pp. 2019-2023.
21. Drobner, E., Huber, H., Rachel, R. and Stetter, K. O. (1992) Thiobacillus plumbophilus sp. nov., a novel galena and hydrogen oxidizer. Arch Microbiol, 157, pp. 213-217.
22. Druschel, G. K., Labrenz, M., Thomsen-Ebert, T., Fowle, D. A. and Banfield, J. F. (2002) Geochemical modeling of ZnS in biofilms: An example of ore depositional processes. Econ Geol, 97, pp. 1319-1329.
23. Eder, W., Ludwig, W. and Huber, R. (1999) Novel 16S rRNA gene sequences retrieved from highly saline brine sediments of Kebrit Deep, Red Sea. Arch Microbiol, 172, pp. 213-218.
24. Finneran, K. T., Forbush, H. M., Van Praagh, C. V. and Lovley, D. R. (2002) Desulfitobacterium metallireducens sp. nov., an anaerobic bacterium that couples growth to the reduction of metals and humic acids as well as chlorinated compounds. Int J Syst Evol Microbiol, 52, pp. 1929-1935.
25. Fortin, D., Davis, B., Southam, G. and Beveridge, T. J. (1995) Biogeochemical phenomena induced by bacteria within sulfidic mine tailings. J Indust Microbiol, 14, pp. 178-185.
26. Fredrickson, J. K. and Onstott, T. C. (1996) Microbes deep inside the Earth. Sci Amer, 275, pp. 68-73.
27. Geesey, G. G. (2001) Bacterial behavior at surfaces. Curr Op Microbiol, 4, pp. 296-300.
28. Gihring, T. M., Moser, D. P., Lin, L-H, Davidson, M., Onstott, T. C., Morgan, L., Milleson, M., Kieft, T., Trimarco, E., Balkwill, D. L. and Dollhopf, M. (2006) The distribution of microbial taxa in the subsurface water of the Kalahari Shield, South Africa. Geomicrobiol J, 23, pp. 415-430.
29. Giovannoni, S. J. (1991) The polymerase chain reaction. Nucleic acid techniques in bacterial systematics, pp. 177-203. John Wiley & Sons, New York
30. Inagaki, F., Nunoura, T., Nakagawa, S., Teske, A., Lever, M., Lauer, A., Suzuki, M., Takai, K., Delwiche, M., Colwell, F. S., Nealson, K. H., Horikoshi, K., D'Hondt, S. and Jorgensen, B. B. (2006) Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. Proc Natl Acad Sci USA, 103, pp. 2815-2820.
31. Inagaki, F., Suzuki, M., Takai, K., Oida, H., Sakamoto, T., Aoki, K., Nealson, K. H. and Horikoshi, K. (2003) Microbial communities associated with geological horizons in coastal subseafloor sediments from the sea of Okhotsk. Appl Environ Microbiol, 69, pp. 7224-7235.
32. Kaksonen, A. H., Plumb, J. J., Robertson, W. J., Franzmann, P. D., Gibson, J AE and Puhakka, J. A. (2004) Culturable diversity and community fatty acid profiling of sulfate-reducing fluidized-bed reactors treating acidic, metal-containing wastewater. Geomicrobiol J, 2, pp. 469-480.
33. Kasai, Y., Takahata, Y., Hoaki, T. and Watanabe, K. (2005) Physiological and molecular characterization of a microbial community established in unsaturated, petroleum-contaminated soil. Environ Microbiol, 7, pp. 806-818.
34. Labrenz, M., Druchel, G., Thomsen-Ebert, T., Gilbert, B., Welch, S. A., Kemner, K. M., Logan, G. A., Summons, R. E., De Stasio, G., Bond, P. L., Lai, B., Kelly, S. D. and Banfield, J. F. (2000) Formation of sphalerite (ZnS) deposits in natural biofilms of sulfate-reducing bacteria. Science, 290, pp. 1744-1747.
35. Lane, D. J. (1991) Nucleic acid techniques in bacterial systematics. Nucleic Acid Techniques in Bacterial Systematics, pp. 115-175. Wiley, New York
36. Ley, R. E., Harris, J. K., Wilcox, J., Spear, J. R., Miller, S. R., Bebout, B. M., Maresca, J. A., Bryant, D. A., Sogin, M. L. and Pace, N. R. (2006) Unexpected diversity and complexity of the guerrero negro hypersaline microbial mat. Appl Environ Microbiol, 72, pp. 3685-3695.
37. Lin, L-H., Gihring, T. M., Lollar, B Sherwood, Boice, E., Pratt, L. M., Lippmann-Pipke, J., Bellamy, R ES, Hall, J. and Onstott, T. C. (2006) Planktonic microbial communities associated with fracture-derived groundwater in a deep gold mine of South Africa. Geomicrobiol J, 23, pp. 474-497.
38. Little, B. J., Wagner, P. A. and Lewandowski, Z. (1997) Spatial relations between bacteria and metal surfaces. Geomicrobiology: Interactions between microbes and minerals, 35, pp. 123-159. Mineral Geochem
39. Lovley, D. R. and Klug, M. J. (1983) Sulfate reducers can outcompete methanogens at freshwater sulfate concentrations. Appl Environ Microbiol, 45, pp. 187-192.
40. Mills, H. J., Hodges, C., Wilson, K., MacDonald, I. R. and Sobecky, P. A. (2003) Microbial diversity in sediments associated with surface-breaching gas hydrate mounds in the Gulf of Mexico. FEMS Microbiol Ecol, 46, pp. 39-52.
41. Miyoshi, T., Iwatsuki, T. and Naganuma, T. (2005) Phylogenetic characterization of 16S rRNA gene clones from deep-groundwater microorganisms that pass through 0.2-micrometer-pore-size filters. Appl Environ Microbiol, 71, pp. 1084-1088.
42. Moser, D. P., Onstott, T. C., Fredrickson, J. K., Brockman, F. J., Takai, K., Balkwill, D. L., Drake, G., Pfiffner, S., White, D. C., Baker, B. J., Pratt, L. M., Fong, J., Lollar, B Sherwood, Slater, G., Phelps, T. J., Spoelstra, N., DeFlaun, M., Southam, G., Welty, A. T. and Hoek, J. (2003) Evolution of microbial community structure and geochemistry in an ultradeep south african gold mine borehole. Geomicrobiol J, 20, pp. 517-548.
43. Nakagawa, S., Inagaki, F., Suzuki, Y., Steinsbu, B. O., Lever, M. A., Takai, K., Engelen, B., Sako, Y., Wheat, C. G. and Horikoshi, K. (2006) Microbial community in black rust exposed to hot ridge flank crustal fluids. Appl. Environ. Microbiol, 72, pp. 6789-6799.
44. Onstott, T. C., Moser, D. P., Fredrickson, J. K., Brockman, F. J., Pfiffner, S. M., Phelps, T. J., White, D. C., Peacock, A., Balkwill, D., Hoover, R., Krumholz, L. R., Borscik, M., Kieft, T. L. and Wilson, R. B. (2003) Indigenous versus contaminant microbes in ultradeep mines. Env Microbiol, 5, pp. 1168-1191.
45. Onstott, T. C., Lin, L-H, Davidson, M., Mislowack, B., Borcsik, M., Hall, J., Slater, G., Ward, J., Lollar, B Sherwood, Lippmann-Pipke, J., Boice, E., Pratt, L. M., Pfiffner, S. M., Moser, D. P., Gihring, T. M., Kieft, T., Phelps, T. J., van Heerden, E., Litthaur, D., De Flaun, M., Rothmel, R., Wanger, G. and Southam, G. (2006) The origin and age of biogeochemical trends in deep fracture water of the Witwatersrand Basin, South Africa. Geomicrobiol J, 23, pp. 369-414.
46. Pedersen, K., Hallbeck, L., Arlinger, J., Erlandson, A. C. and Jahromi, N. (1997) Investigation of the potential for microbial contamination of deep granitic aquifers during drilling using 16S rRNA gene sequencing and culturing methods. J Microbiol Meth, 30, pp. 179-192.
47. Penn, R. L. and Banfield, J. F. (1998) Imperfect oriented attachment: A mechanism for dislocation generation in defect-free nanocrystals. Science, 281, pp. 969-971.
48. Pudry, K. J., Munson, M. A., Nedwell, D. B. and Embley, T. M. (2002) Comparison of the molecular diversity of the methanogenic community at the brackish and marine ends of a UK estuary. FEMS Microbiol Ecol, 39, pp. 17-21.
49. Raghoebarsing, A. A., Pol, A., van de Pas-Schoonen, K. T., Smolders, A JP, Ettwig, K. F., Rijpstra, I. C., Schouten, S., Damste, J S Sinninghe, Camp, H JM Op den, Jetten, M SM and Strous, M. (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature, 440, pp. 918-921.
50. Rickard, D. (1975) Kinetics and mechanism of pyrite formation at low temperatures. Amer J Sci, 275, pp. 636-652.
51. 2S oxidation of iron (II) monosulfide in aqueous solutions between 25 and 125°C: The rate equation. Geochim Cosmochim Acta, 61, pp. 115-134.
52. 2S oxidation of iron (II) monosulfide in aqueous solutions between 25 and 125°C: The mechanism. Geochim Cosmochim Acta, 61, pp. 135-147.
53. Rozanova, E. P., Tourova, T. P., Kolganova, T. V., Lysenko, A. M., Mityushina, L. L., Yusupov, S. K. and Belyaev, S. S. (2001) Desulfacinum subterraneum sp. nov., a new thermophilic sulfate-reducing bacteria isolated from a high-temperature oil field. Microbiol, 70, pp. 466-471.
54. Sait, M., Hugenholtz, P. and Janssen, P. H. (2002) Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys. Environ Microbiol, 4, pp. 654-666.
55. Sanford, R. A., Cole, J. R. and Tiedje, J. M. (2002) Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl-halorespiring facultative anaerobic myxobacterium. Appl Environ Microbiol, 68, pp. 893-900.
56. Schoonen, M AA (2004) Mechanisms of sedimentary pyrite formation. In: Sulfur Biogeochemistry-Past and present (Amend J.P., Edwards K.J., Lyons T.W., eds). GSA Special Paper, 379, pp. 117-134.
57. Schrenk, M. O., Kelley, D. S., Delaney, J. R. and Baross, J. A. (2003) Incidence and diversity of microorganisms within the walls of an active deep-sea sulfide chimney. Appl Environ Microbiol, 69, pp. 3580-3592.
58. Lollar, B Sherwood, Lacrampe-Couloume, G., Slater, G. F., Ward, J. A., Moser, D. P., Gihring, T. M., Lin, L-H and Onstott, T. C. (2006) Unravelling abiogenic and biogenic sources of methane in the Earth's deep subsurface. Chem Geol, 226, pp. 328-339.
59. Shigematsu, T., Tang, Y., Mizuno, Y., Kawaguchi, H., Morimura, S. and Kida, K. (2006) Microbial diversity of mesophilic methanogenic consortium that can degrade long-chain fatty acids in chemostat cultivation. J Biosci Bioeng, 102, pp. 535-544.
60. Tringe, S. G., von Mering, C., Kobayashi, A., Salamov, A. A., Chen, K., Chang, H. W., Podar, M., Short, J. M., Mathur, E. J., Detter, J. C., Bork, P., Hugenholtz, P. and Rubin, E. M. (2005) Comparative metagenomics of microbial communities. Science, 308, pp. 554-557.
61. Trudinger, P. A., Chambers, L. A. and Smith, J. W. (1985) Low-temperature sulphate reduction: Biological versus abiological. Can J Earth Sci, 22, pp. 1910-1918.
62. Tuttle, J. H., Dugan, C. B. and Randles, C. I. (1969) Microbial sulfate reduction and its potential utility as an acid mine water pollution abatement procedure. Appl Microbiol, 17, pp. 297-302.
63. Tweedie, E. B. (1981) The geology of the Evander Basin, Southeastern Transvaal, Republic of South Africa, M.Sc. thesis. p. 221. Univ. of the Witswatersrand, Jhb
64. Vetriani, C., Tran, H. V. and Kerkhof, L. J. (2003) Fingerprinting Microbial Assemblages from the Oxic/Anoxic Chemocline of the Black Sea. Appl Environ Microbiol, 69, pp. 6481-6488.
65. Weber, K. A., Urrutia, M. M., Churchill, P. F., Kukkadapu, R. K. and Roden, E. E. (2006) Anaerobic redox cycling of iron by freshwater sediment microorganisms. Environ Microbiol, 8, pp. 100-113.
66. Wilkin, R. T. and Barnes, H. L. (1997) Formation processes of framboidal pyrite. Geochim Cosmochim Acta, 61, pp. 323-339.
67. Wilson, A JC (1963) Mathematical Theory of X-ray Powder Diffraction, Philips Technical Library, Eindhoven, The Netherlands
68. Xie, C. H. and Yokota, A. (2006) Zoogloea oryzae sp. nov., a nitrogen-fixing bacterium isolated from rice paddy soil, and reclassification of the strain ATCC 19623 as Crabtreella saccharophila gen. nov., sp. nov. Int J Syst Evol Microbiol, 56, pp. 19-624.
69. Yamada, T., Sekiguchi, Y., Imachi, H., Kamagata, Y., Ohashi, A. and Harada, H. (2005) Diversity, localization, and physiological properties of filamentous microbes belonging to Chloroflexi subphylum I in mesophilic and thermophilic methanogenic sludge granules. Appl Environ Microbiol, 71, pp. 7493-7503.
70. Yoshida, N., Takahashi, N. and Hiraishi, A. (2005) Phylogenetic characterization of a polychlorinated-dioxin-dechlorinating microbial community by use of microcosm studies. Appl Environ Microbiol, 71, pp. 4325-4334.
71. Zhang, H., Sekiguchi, Y., Hanada, S., Hugenholtz, P., Kim, H., Kamagata, Y. and Nakamura, K. (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol, 53, pp. 1155-1163.
72. Zobell, C. E. (1946) Studies of redox potential of marine sediments. Bull Am Assoc Petrol Geol, 30, pp. 477-513.