Carbon and hydrogen stable isotope fractionation associated with the anaerobic degradation of propane and butane by marine sulfate-reducing bacteria

Environmental Microbiology

Volumn 16, Issue 1, 2014, Pages 130-140

  Jaekel, Ulrike ^a,d   Vogt, Carsten ^b   Fischer, Anko ^b,c   Richnow, Hans Hermann ^b   Musat, Florin ^a,d  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^c Isodetect GmbH   (Germany)

^d HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS);

BUTANE; CARBON; DEUTERIUM; PROPANE; SEA WATER; SULFATE;

ANAEROBIC GROWTH; ARTICLE; BACTERIUM; BIOREMEDIATION; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION;

ANAEROBIOSIS; BACTERIA; BIODEGRADATION, ENVIRONMENTAL; BUTANES; CARBON ISOTOPES; DEUTERIUM; OXIDATION-REDUCTION; PROPANE; SEAWATER; SULFATES;

EID: 84891633482     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12251     Document Type: Article

References (65)

1. Aeppli, C., Berg, M., Cirpka, O.A., Holliger, C., Schwarzenbach, R.P., and Hofstetter, T.B. (2009) Influence of mass-transfer limitations on carbon isotope fractionation during microbial dechlorination of trichloroethene. Environ Sci Technol 43: 8813-8820.
2. Boreham, B.C.J., Hope, J.M., and Hartung-Kagi, B. (2001) Understanding source, distribution and preservation of Australian natural gas: a geochemical perspective. APPEA J 41: 523-547.
3. Bouchard, D., Hunkeler, D., and Höhener, P. (2008) Carbon isotope fractionation during aerobic biodegradation of n-alkanes and aromatic compounds in unsaturated sand. Org Geochem 39: 23-33.
4. Bowles, M.W., Samarkin, V.A., and Bowles, K.M. (2011) Weak coupling between sulfate reduction and the anaerobic oxidation of methane in methane-rich seafloor sediments during ex situ incubation. Geochim Cosmochim Acta 75: 500-519.
5. Callaghan, A.V., Wawrik, B., Ní Chadhain, S.M., Young, L.Y., and Zylstra, G.J. (2008) Anaerobic alkane-degrading strain ak-01 contains two alkylsuccinate synthase genes. Biochem Biophys Res Comm 366: 142-148.
6. Callaghan, A.V., Morris, B.E.L., Pereira, I.A.C., McInerney, M.J., Austin, R.N., Groves, J.T., etal. (2012) The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation. Environ Microbiol 14: 101-113.
7. Cichocka, D., Siegert, M., Imfeld, G., Andert, J., Beck, K., Diekert, G., etal. (2007) Factors controlling the carbon isotope fractionation of tetra- and trichloroethene during reductive dechlorination by Sulfurospirillum ssp. And Desulfitobacterium sp. Strain PCE-S. FEMS Microbiol Ecol 62: 98-107.
8. Claypool, G.E., and Kvenvolden, K.A. (1983) Methane and other hydrocarbon gases in marine sediment. Annu Rev Earth Planet Sci 11: 299-327.
9. Coplen, T.B. (2011) Guidelines and recommended terms for expression of stableisotope-ratio and gas-ratio measurement results. Rapid Commun Mass Spectrom 25: 2538-2560.
10. Cord-Ruwisch, R. (1985) A quick method for the determination of dissolved and precipitated sulfides in cultures of sulfate-reducing bacteria. J Microbiol Methods 4: 33-36.
11. Dean, J.A. (1992) Lange's Handbook of Chemistry. New York, NY, USA: McGraw Hill.
12. Elsner, M. (2010) Stable isotope fractionation to investigate natural transformation mechanisms of organic contaminants: principles, prospects and limitations. J Environ Monit 12: 2005-2031.
13. Elsner, M., Zwank, L., Hunkeler, D., and Schwarzenbach, R.P. (2005) A new concept linking observable stable isotope fractionation to transformation pathways of organic pollutants. Environ Sci Technol 39: 6896-6916.
14. Elsner, M., McKelvie, J., Lacrampe Couloume, G., and Sherwood Lollar, B. (2007) Insight into methyl tert-butyl ether (MTBE) stable isotope fractionation from abiotic reference experiments. Environ Sci Technol 41: 5693-5700.
15. Etiope, G., and Ciccioli, P. (2009) Earth's degassing: a missing ethane and propane source. Science 323: 478.
16. Feisthauer, S., Vogt, C., Modrzynski, J., Szlenkier, M., Krüger, M., Siegert, M., and Richnow, H.-H. (2011) Different types of methane monooxygenases produce similar carbon and hydrogen isotope fractionation patterns during methane oxidation. Geochim Cosmochim Acta 75: 1173-1184.
17. Fischer, A., Theuerkorn, K., Stelzer, N., Gehre, M., Thullner, M., and Richnow, H.H. (2007) Applicability of stable isotope fractionation analysis for the characterization of benzene biodegradation in a BTEX-contaminated aquifer. Environ Sci Technol 41: 3689-3696.
18. Fischer, A., Herklotz, I., Herrmann, S., Thullner, M., Weelink, S.A.B., Stams, A.J.M., etal. (2008) Combined carbon and hydrogen isotope fractionation investigations for elucidating benzene biodegradation pathways. Environ Sci Technol 42: 4356-4363.
19. Fischer, A., Gehre, M., Breitfeld, J., Richnow, H.-H., and Vogt, C. (2009) Carbon and hydrogen isotope fractionation of benzene during biodegradation under sulfate-reducing conditions: a laboratory to field site approach. Rapid Commun Mass Spectrom 23: 2439-2447.
20. Formolo, M.J., Lyons, T.W., Zhang, C., Kelley, C., Sassen, R., Horita, J., and Cole, D.R. (2004) Quantifying carbon sources in the formation of authigenic carbonates at gas hydrate sites in the Gulf of Mexico. Chem Geol 205: 253-264.
21. Head, I.M., Jones, D.M., and Larter, S.R. (2003) Biological activity in the deep subsurface and the origin of heavy oil. Nature 426: 344-352.
22. Herrmann, S., Vogt, C., Fischer, A., Kuppardt, A., and Richnow, H.-H. (2009) Characterization of anaerobic xylene biodegradation by two-dimensional isotope fractionation analysis. Environ Microbiol Rep 1: 535-544.
23. Holler, T., Wegener, G., Niemann, H., Deusner, C., Ferdelman, T.G., Boetius, A., etal. (2011) Carbon and sulfur back flux during anaerobic microbial oxidation of methane and coupled sulfate reduction. Proc Natl Acad Sci USA 108: E1484-E1490.
24. Hunkeler, D. (2002) Quantification of isotope fractionation in experiments with deuterium-labeled substrate. Appl Environ Microbiol 68: 5205-5207.
25. Huskey, P.W. (1991) Enzyme mechanism from isotope effects. In Enzyme Mechanism from Isotope Effects. Cook, P.F. (ed.). Boca Raton, FL, USA: CRC Press, pp. 37-69.
26. Jaekel, U., Musat, N., Adam, B., Kuypers, M., Grundmann, O., and Musat, F. (2013) Anaerobic degradation of propane and butane by sulfate-reducing bacteria enriched from marine hydrocarbon cold seeps. ISME J 7: 885-895.
27. James, A.T., and Burns, B.J. (1984) Microbial alterations of subsurface natural gas accumulations. Am Assoc Pet Geol Bull 68: 957-960.
28. Joye, S.B., Boetius, A., Orcutt, B.N., Montoya, J.P., Schulz, H.N., Erickson, M.J., and Lugo, S.K. (2004) The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps. Chem Geol 205: 219-238.
29. Kampara, M., Thullner, M., Richnow, H.H., Harms, H., and Wick, L.Y. (2008) Impact of bioavailability restrictions on microbially induced stable isotope fractionation. 2. Experimental evidence. Environ Sci Technol 42: 6552-6558.
30. Kampara, M., Thullner, M., Harms, H., and Wick, L. (2009) Impact of cell density on microbially induced stable isotope fractionation. Appl Microbiol Biotechnol 81: 977-985.
31. Kinnaman, F.S., Valentine, D.L., and Tyler, S.C. (2007) Carbon and hydrogen isotope fractionation associated with the aerobic microbial oxidation of methane, ethane, propane and butane. Geochim Cosmochim Acta 71: 271-283.
32. Kleindienst, S., Ramette, A., Amann, R., and Knittel, K. (2012) Distribution and in situ abundance of sulfate-reducing bacteria in diverse marine hydrocarbon seep sediments. Environ Microbiol 14: 2689-2710.
33. Kniemeyer, O., Musat, F., Sievert, S.M., Knittel, K., Wilkes, H., Blumenberg, M., etal. (2007) Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449: 898-901.
34. Kristensen, A.H., Henriksen, K., Mortensen, L., Scow, K.M., and Moldrup, P. (2010) Soil physical constraints on intrinsic biodegradation of petroleum vapors in a layered subsurface. Vadose Zone J 9: 137-147.
35. Larter, S.R., Head, I.M., Huang, H., Bennet, B., Jones, M., Aplin, A.C., etal. (2005) Biodegradation, gas destruction and methane generation in deep subsurface petroleum reservoirs: an overview. Geological Society, London, Petroleum Geology Conference series 6 6: 633-639.
36. Mancini, S.A., Devine, C.E., Elsner, M., Nandi, M.E., Ulrich, A.C., Edwards, E.A., and Sherwood Lollar, B. (2008) Isotopic evidence suggests different initial reaction mechanisms for anaerobic benzene biodegradation. Environ Sci Technol 42: 8290-8296.
37. Mariotti, A., Germon, J.C., Hubert, P., Kaiser, P., Letolle, R., Tardieux, A., and Tardieux, P. (1981) Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant Soil 62: 413-430.
38. Mastalerz, V., de Lange, G.J., and Dählmann, A. (2009) Differential aerobic and anaerobic oxidation of hydrocarbon gases discharged at mud volcanoes in the Nile deep-sea fan. Geochim Cosmochim Acta 73: 3849-3863.
39. Millington, R.J. (1959) Gas diffusion in porous media. Science 130: 100-102.
40. Morasch, B., Richnow, H.H., Schink, B., and Meckenstock, R.U. (2001) Stable hydrogen and carbon isotope fractionation during microbial toluene degradation: mechanistic and environmental aspects. Appl Environ Microbiol 67: 4842-4849.
41. Niemann, H., Duarte, J., Hensen, C., Omoregie, E., Magalhães, V.H., Elvert, M., etal. (2006) Microbial methane turnover at mud volcanoes of the Gulf of Cadiz. Geochim Cosmochim Acta 70: 5336-5355.
42. Nijenhuis, I., Andert, J., Beck, K., Kästner, M., Diekert, G., and Richnow, H.-H. (2005) Stable isotope fractionation of tetrachloroethene during reductive dechlorination by Sulfurospirillum multivorans and Desulfitobacterium sp. Strain PCE-S and abiotic reactions with cyanocobalamin. Appl Environ Microbiol 71: 3413-3419.
43. Orcutt, B., Boetius, A., Elvert, M., Samarkin, V., and Joye, S.B. (2005) Molecular biogeochemistry of sulfate reduction, methanogenesis and the anaerobic oxidation of methane at Gulf of Mexico cold seeps. Geochim Cosmochim Acta 69: 4267-4281.
44. Orcutt, B.N., Boetius, A., Lugo, S.K., MacDonald, I.R., Samarkin, V.A., and Joye, S.B. (2004) Life at the edge of methane ice: microbial cycling of carbon and sulfur in Gulf of Mexico gas hydrates. Chem Geol 205: 239-251.
45. Orcutt, B.N., Joye, S.B., Kleindienst, S., Knittel, K., Ramette, A., Reitz, A., etal. (2010) Impact of natural oil and higher hydrocarbons on microbial diversity, distribution, and activity in Gulf of Mexico cold-seep sediments. Deep Sea Res Part II Top Stud Oceanogr 57: 2008-2021.
46. Pozzer, A., Pollmann, J., Taraborrelli, D., Jöckel, P., Helmig, D., Tans, P., etal. (2010) Observed and simulated global distribution and budget of atmospheric c2-c5 alkanes. Atmos Chem Phys 10: 4403-4422.
47. Quistad, S.D., and Valentine, D.L. (2011) Anaerobic propane oxidation in marine hydrocarbon seep sediments. Geochim Cosmochim Acta 75: 2159-2169.
48. Rosell, M., Finsterbusch, S., Jechalke, S., Hübschmann, T., Vogt, C., and Richnow, H.H. (2009) Evaluation of the effects of low oxygen concentration on stable isotope fractionation during aerobic MTBE biodegradation. Environ Sci Technol 44: 309-315.
49. Sassen, R., Roberts, H.H., Carney, R., Milkov, A.V., DeFreitas, D.A., Lanoil, B., and Zhang, C. (2004) Free hydrocarbon gas, gas hydrate, and authigenic minerals in chemosynthetic communities of the northern Gulf of Mexico continental slope: relation to microbial processes. Chem Geol 205: 195-217.
50. Savage, K.N., Krumholz, L.R., Gieg, L.M., Parisi, V.A., Suflita, J.M., Allen, J., etal. (2010) Biodegradation of low-molecular-weight alkanes under mesophilic, sulfate-reducing conditions: metabolic intermediates and community patterns. FEMS Microbiol Ecol 72: 485-495.
51. Shennan, J.L. (2006) Utilisation of c2-c4 gaseous hydrocarbons and isoprene by microorganisms. J Chem Technol Biotechnol 81: 237-256.
52. Sloan, E.D. (2003) Fundamental principles and applications of natural gas hydrates. Nature 426: 353-363.
53. Staal, M., Thar, R., Kühl, M., van Loosdrecht, M.C.M., Wolf, G., de Brouwer, J.F.C., and Rijstenbil, J.W. (2007) Different carbon isotope fractionation patterns during the development of phototrophic freshwater and marine biofilms. Biogeosciences 4: 613-626.
54. Templeton, A.S., Chu, K.-H., Alvarez-Cohen, L., and Conrad, M.E. (2006) Variable carbon isotope fractionation expressed by aerobic CH4-oxidizing bacteria. Geochim Cosmochim Acta 70: 1739-1752.
55. Thullner, M., Kampara, M., Richnow, H.H., Harms, H., and Wick, L.Y. (2008) Impact of bioavailability restrictions on microbially induced stable isotope fractionation. 1. Theoretical calculation. Environ Sci Technol 42: 6544-6551.
56. Tissot, B.P., and Welte, D.H. (1984) Petroleum Formation and Occurrence. Berlin, Germany: Springer Verlag.
57. Tobler, N.B., Hofstetter, T.B., and Schwarzenbach, R.P. (2008) Carbon and hydrogen isotope fractionation during anaerobic toluene oxidation by Geobacter metallireducens with different Fe(III) phases as terminal electron acceptors. Environ Sci Technol 42: 7786-7792.
58. Vieth, A., and Wilkes, H. (2006) Deciphering biodegradation effects on light hydrocarbons in crude oils using their stable carbon isotopic composition: a case study from the Gullfaks oil field, offshore Norway. Geochim Cosmochim Acta 70: 651-665.
59. Vogt, C., Cyrus, E., Herklotz, I., Schlosser, D., Bahr, A., Herrmann, S., etal. (2008) Evaluation of toluene degradation pathways by two-dimensional stable isotope fractionation. Environ Sci Technol 42: 7793-7800.
60. Welte, D.H., Kratochvil, H., Rullkötter, J., Ladwein, H., and Schaefer, R.G. (1982) Organic geochemistry of crude oils from the Vienna Basin and an assessment of their origin. Chem Geol 35: 33-68.
61. Widdel, F., and Bak, F. (1992) Gram-negative mesophilic sulfate-reducing bacteria. In The Prokaryotes. Balows, A., Trüper, H.G., Dworkin, M., Harder, W., and Schleifer, K.H. (eds). Berlin, Germany: Springer-Verlag, pp. 2278-3352.
62. Widdel, F., and Grundmann, O. (2010) Biochemistry of the anaerobic degradation of non-methane alkanes. In Handbook of Hydrocarbon and Lipid Microbiology. Timmis, K.N. (ed.). Berlin, Heidelberg, Germany: Springer Berlin Heidelberg, pp. 909-924.
63. Wilkes, H., Vieth, A., and Elias, R. (2008) Constraints on the quantitative assessment of in-reservoir biodegradation using compound-specific stable carbon isotopes. Org Geochem 39: 1215-1221.
64. Wöhlbrand, L., Jacob, J.H., Kube, M., Mussmann, M., Jarling, R., Beck, A., etal. (2012) Complete genome, catabolic sub-proteomes and key-metabolites of Desulfobacula toluolica Tol2, a marine, aromatic compound-degrading, sulfate-reducing bacterium. Environ Microbiol 15: 1334-1355.
65. Zwank, L., Berg, M., Elsner, M., Schmidt, T.C., Schwarzenbach, R.P., and Haderlein, S.B. (2005) New evaluation scheme for two-dimensional isotope analysis to decipher biodegradation processes: application to groundwater contamination by MTBE. Environ Sci Technol 39: 1018-1029.