Abstract
At temperatures up to about 80 °C, petroleum in subsurface reservoirs is often biologically degraded, over geological timescales, by microorganisms that destroy hydrocarbons and other components to produce altered, denser 'heavy oils'. This temperature threshold for hydrocarbon biodegradation might represent the maximum temperature boundary for life in the deep nutrient-depleted Earth. Most of the world's oil was biodegraded under anaerobic conditions, with methane, a valuable commodity, often being a major by-product, which suggests alternative approaches to recovering the world's vast heavy oil resource that otherwise will remain largely unproduced.
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References
Roadifer, R. E. in Exploration for Heavy Crude Oil and Natural Bitumen (ed. Meyer, R.F.) 3–23 (Am. Assoc. Petrol. Geol., Tulsa, 1987).
Connan, J. in Advances in Petroleum Geochemistry Vol. 1 (eds Brooks, J. & Welte, D. H.) 299–335 (Academic, London, 1984).
Bastin, E. Microorganisms in oilfields. Science 63, 21–24 (1926).
Krejci-Graf, K. Rule of density of oils. Bull. Am. Assoc. Petrol. Geol. 16, 1038 (1932).
Bailey, N. J. L., Jobson, A. M. & Rogers, M. A. Bacterial degradation of crude oil: comparison of field and experimental data. Chem. Geol. 11, 203–221 (1973).
Rubinstein, I., Strausz, O. P., Spyckerelle, C., Crawford, R. J. & Westlake, D. W. S. The origin of the oil sand bitumens of Alberta: a chemical and microbiological simulation study. Geochim. Cosmochim. Acta 41, 1341–1353 (1977).
Alexander, R., Kagi, R. I., Woodhouse, G. W. & Volkman, J. K. The geochemistry of some biodegraded Australian oils. Aus. Petrol. Explor. Assoc. J. 23, 53–63 (1983).
Volkman, J. K., Alexander, R., Kagi, R. I., Rowland, S. J. & Sheppard, P. N. Biodegradation of aromatic hydrocarbons in crude oils from the Barrow Sub-basin of Western Australia. Org. Geochem. 6, 619–632 (1984).
Rowland, S. J., Alexander, R., Kagi, R. I., Jones, D. M. & Douglas, A. G. Microbial degradation of aromatic components of crude oils: A comparison of laboratory and field observations. Org. Geochem. 9, 153–161 (1986).
Hunkeler, D., Jorger, D., Haberli, K., Hohener, P. & Zeyer, P. Petroleum hydrocarbon mineralisation in anaerobic laboratory aquifer columns. J. Contaminant Hydrol. 32, 41–61 (1998).
Meredith, W., Kelland, S.-J. & Jones, D. M. Influence of biodegradation on crude oil acidity and carboxylic acid composition. Org. Geochem. 31, 1059–1073 (2000).
Taylor, P. N., Bennett, B., Jones, D. M. & Larter, S. The effect of biodegradation and water washing on the occurrence of alkylphenols in crude oils. Org. Geochem. 32, 341–358 (2001).
Wenger, L. M., Davis, C. L. & Isaksen, G. H. Multiple Controls on Petroleum Biodegradation and Impact in Oil Quality. (SPE 71450, Society of Petroleum Engineers, 2001).
Peters, K. E. & Fowler, M. G. Applications of petroleum geochemistry to exploration and reservoir management. Org. Geochem. 33, 5–36 (2002).
Evans, C. R., Rogers, M. A. & Bailey, N. J. L. Evolution and alteration of petroleum in Western Canada. Chem. Geol. 8, 147–170 (1971).
Hunt, J. M. Petroleum Geochemistry and Geology. (Freeman, San Francisco, 1979).
Fedorak, P. M. & Westlake, D. W. S. Microbial degradation of alkyl carbazoles in Norman Wells crude oils. Appl. Environ. Microbiol. 47, 858–862 (1984).
Zhang, C. et al. Effect of biodegradation on carbazole compounds in crude oils [in Chinese with English abstract]. Shiyou yu tianranqi dizhi (Oil and Gas Geology) 20, 341–343 (1999).
Huang, H. P., Bowler, B. F. J., Zhang, Z. W., Oldenburg, T. B. P. & Larter S. R. Inþuence of biodegradation on carbazole and benzocarbazole distributions in oil columns from the Liaohe basin, NE China. Org. Geochem. 34, 951–969 (2003).
Mackenzie, A. S., Wolff, G. A. & Maxwell, J. R. in Advances in Organic Geochemistry 1981 (eds Bjoroy, M. et al.) 637–649 (Wiley Heyden, London, 1983).
Thorn, K. A. & Aiken, G. R. Biodegradation of crude oil into non-volatile acids in a contaminated aquifer near Bemidji, Minnesota. Org.Geochem. 29, 909–931 (1998).
Tomczyk, N. A., Winans, R. E., Shinn, J. H. & Robinson, R. C. On the nature and origin of acidic species in petroleum, 1. Detailed acid type distribution in a California Crude Oil. Energy Fuels 15, 1498–1504 (2001).
James, A. T. & Burns, B. J. Microbial alteration of subsurface natural gas accumulations. Bull. Am. Assoc. Petrol. Geol. 68, 957–960 (1984).
Horstad, I. & Larter, S. R. Petroleum migration, alteration, and remigration within Troll Field, Norwegian North Sea. Bull. Am. Assoc. Petrol. Geol. 81, 222–248 (1997).
Boreham,C. J., Hope, J. M. & Hartung-Kagi, B. Understanding source, distribution and preservation of Australian natural gas: A geochemical perspective. Aus. Petrol. Explor. Assoc. J. 41, 523–547 (2001).
Larter, S. R. et al. When biodegradation preserves petroleum! Petroleum geochemistry of N. Sea Oil Rimmed Gas Accumulations (ORGAs). Proc. AAPG Hedberg Research Conference on Natural Gas Formation and Occurrence, Durango, Colorado (1999).
England, W. A., Mackenzie, A. S., Mann, D. M. & Quigley, T. M. The movement and entrapment of petroleum fluids in the subsurface. J. Geol. Soc. Lond. 144, 327–347 (1987).
Barnard, P. C. & Bastow, M. A. in Petroleum Migration (eds England, W. A. & Fleet, A. J.) 167–190 (Spec. Publ. No. 59, Geol. Soc., London, 1991).
Larter, S. et al. The controls on the composition of biodegraded oils. (Part 1) Biodegradation rates in petroleum reservoirs in the deep subsurface. Org. Geochem. 34, 601–613 (2003).
Masterson, W. D., Dzou, L. I. P., Holba, A. G., Fincannon, A. L. & Ellis, L. Evidence for biodegradation and evaporative fractionation in West Sak, Kuparuk and Prudhoe Bay field areas, North Slope, Alaska. Org. Geochem. 32, 411–441 (2001).
Volkman, J. K., Alexander, R., Kagi, R. I. & Woodhouse, G. W. Demethylated hopanes in crude oils and their applications in petroleum geochemistry. Geochim. Cosmochim. Acta 47, 785–794 (1983).
Peters, K. E. & Moldowan, J. M. The Biomarker Guide (Prentice Hall, New York, 1993).
Moldowan, J. M. & McCaffrey, M. A. A novel microbial hydrocarbon degradation pathway revealed by hopane demethylation in a petroleum reservoir. Geochim. Cosmochim. Acta 59, 1891–1894 (1995).
Pepper, A. & Santiago, C. Impact of biodegradation on petroleum exploration and production: Observations and outstanding problems. Abstracts of Earth Systems Processes. (Geol. Soc. London, Geol. Soc of America., Edinburgh, 24-28 June 2001).
Wilhelms, A., Larter, S. R., Head, I., Farrimond, P., di-Primio, R. & Zwach, C. Biodegradation of oil in uplifted basins prevented by deep-burial sterilisation. Nature 411, 1034–1037 (2000).
Wellsbury, P., Goodman, K., Barth, T., Cragg, B. A., Barnes, S. P. & Parkes, R.J. Deep marine biosphere fuelled by increasing organic matter availability during burial and heating. Nature 388, 573–576 (1997).
Winters, J. C. & Williams, J. A. Microbial alteration of crude oil in the reservoir. Am. Chem. Soc. Div. Petr. Chem. Preprints 14, E22–E31 (1969).
Horstad, I., Larter, S. R. & Mills N. A quantitative model of biological petroleum degradation within the Brent Group reservoir in the Gullfaks field, Norwegian North Sea. Org. Geochem. 19, 107–117 (1992).
Warren, E. A. & Smalley, P. C. North Sea Formation Waters Atlas (Geol. Soc. Lond., 1994).
Magot, M., Ollivier, B. & Patel, B. K.C. Microbiology of petroleum reservoirs. Antonie Van Leeuwenhoek 77, 103–116 (2000).
Orphan, V. J., Taylor, L. T., Hafenbradl, D. & Delong, E. F. Culture-dependent and culture-independent characterization of microbial assemblages associated with high-temperature petroleum reservoirs. Appl. Environ. Microbiol. 66, 700–711 (2001).
Röling, W. F. M., Head, I. M. & Larter, S. R. The microbiology of hydrocarbon degradation in subsurface petroleum reservoirs: perspectives and prospects. Res. Microbiol. 154, 321–328 (2003).
Kartsev, A. A., Tabasaranskii, Z. A., Subbota, M. I. & Mogilevski, G. A. in Geochemical Methods of Prospecting and Exploration for Petroleum and Natural Gas (eds Witherspoon, P. A., Romey, W. D.) 347 (Univ. California, California, 1959).
Connan, J., Lacrampe-Coulombe, G. & Magot, M. Origin of gases in reservoirs. Proc. 1995 International Gas Research Conference, Government Institutes, Rockville, USA 21–61 (1996).
Nilsen, R. K. & Torsvik, T. Methanococcus thermolithotrophicus isolated from North Sea oil field reservoir water. Appl. Environ. Microbiol. 62, 1793–1798 (1996).
Nilsen, R. K., Beeder, J., Thorstenson, T. & Torsvik, T. Distribution of thermophilic sulfate reducers in North Sea oil field reservoir waters and oil reservoirs. Appl. Environ. Microbiol. 62, 1793–1798 (1996).
Zengler, K., Richnow, H. H., Rossello-Mora, R., Michaelis, W. & Widdel, F. Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401, 266–269 (1999).
Wilkes, H., Rabus, R., Fischer, T., Armstroff, A., Behrends, A. & Widdel, F. Anaerobic degradation of n-hexane in a denitrifying bacterium: Further degradation of the initial intermediate (1-methylpentyl) succinate via C-skeleton rearrangement. Arch. Microbiol. 177, 235–243 (2002).
Widdel, F. & Rabus, R. Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr. Opin. Biotechnol. 12, 259–276 (2001).
Annweiler, E., Michaelis, W. & Meckenstock, R. U. Identical ring cleavage products during anaerobic degradation of naphthalene, 2-methylnaphthalene, and tetralin indicate a new metabolic pathway. Appl. Environ. Microbiol. 68, 852–858 (2002).
Aitken, C. M, Jones, D. M. & Larter, S. R. Isolation and Identification of Biomarkers Indicative of Anaerobic Biodegradation in Petroleum Reservoirs. (Geol. Soc. Lond., London, 2002).
Rueter, P. et al. Anaerobic oxidation of hydrocarbons in crude-oil by new types of sulfate-reducing bacteria. Nature 372, 455–458 (1994).
Anderson, R. T. & Lovley, D. R. Biogeochemistry – hexadecane decay by methanogenesis. Nature 404, 722–723 (2000).
Holba, A.G., Dzou, L. I. P., Hickey, J. J., Franks, S. G., May, S. J. & Lenney, T. Reservoir geochemistry of South Pass 61 field Gulf of Mexico: Compositional heterogeneities reflecting field filling history and biodegradation. Org. Geochem. 24, 1179–1198 (1996).
Scott, A. R., Kaiser, W. R. & Ayers, W. B. J. Thermogenic and secondary biogenic gases, San-Juan Basin, Colorado and New Mexico – Implications for coalbed gas producibility. Bull. Am. Assoc. Petrol. Geol. 78, 1186–1209 (1994).
Sweeney, R. E. & Taylor, P. Biogenic methane derived from biodegradation of petroleum under environmental conditions and in oil & gas reservoirs. Proc. AAPG Hedberg Research Conference on Natural Gas Formation and Occurrence, Durango, Colorado (1999).
Pallasser, R. J. Recognising biodegradation in gas/oil accumulations through the delta 13C composition of gas components. Org. Geochem. 31, 1363–1373 (2000).
Dimitrakopoulos, R. & Meulenbachs, K. Biodegradation of petroleum as a source of 13C enriched carbon dioxide in the formation of carbonate cement. Chem. Geol. 65, 283–289 (1987).
Barson, D., Bachu, S. & Esslinger, P. Flow systems in the Mannville Group in the east-Central Athabasca area and implications for steam-assisted gravity drainage (SAGD) operations for in situ bitumen production. Bull. Can. Petrol. Geol. 49, 376–392 (2001).
Nazina, T. N., Ivanova, A. E., Borzenkov, I. A., Belyaev, S. S. & Ivanov, M. V. Occurrence and geochemical activity of microorganisms in high-temperature, water-flooded oil fields of Kazakhstan and Western Siberia. Geomicrobiol. J. 13, 181–192 (1995).
Ng, T. K., Weimer, P. J. & Gawel, L. J. Possible nonanthropogenic origin of 2 methanogenic isolates from oil-producing wells in the San-Miguelito field, Ventura County, California. Geomicrobiol. J. 7, 185–192 (1989).
Obraztsova, A. Y., Shipin, O. V., Bezrukova, L. V. & Belyaev, S. S. Properties of the coccoid methylotrophic methanogen, methanococcoides-euhalobius sp-nov. Microbiol. 56, 523–527 (1987).
Rozanova, E. P., Savvichev, A. S., Karavaiko, S. G. & Miller, Y. M. Microbial processes in the Savuiskoe oil-field in the Ob region. Microbiology 64, 85–90 (1995).
Charlou, J. L., Donval, J. P., Fouquet, Y., Jean-Baptiste, P. & Holm, N. Geochemistry of high H-2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36 degrees14' N, MAR). Chem. Geol. 191, 345–359 (2002).
Chapelle, F. H. et al. A hydrogen-based subsurface microbial community dominated by methanogens. Nature 415, 312–315 (2002).
Helgeson, H. C., Knox, A. M., Owens, D. H. & Shock, E. L. Petroleum, oil-field waters, and authigenic mineral assemblages – are they in metastable equilibrium in hydrocarbon reservoirs. Geochim. Cosmochim. Acta 57, 3295–3339 (1993).
Manning, D. A. C. & Hutcheon, I. E. Distribution and mineralogical controls on ammonium in deep groundwaters. Appl. Geochem. (in the press).
Oldenburg, T., Huang, H., Donohoe, P., Willsch, H. & Larter, S. R. High molecular weight aromatic nitrogen and other novel hopanoid-related compounds in crude oils. Org. Geochem. (in the press).
Hiebert, F. K. & Bennett, P. C. Microbial control of silicate weathering in organic-rich ground-water. Science 258, 278–281 (1992).
Rogers, J. R., Bennett, P. C. & Choi, W. J. Feldspars as a source of nutrients for microorganisms. J. Am. Miner. 83, 1532–1540 (1998).
Bennett, P. C, Hiebert, F. K. & Rogers, J. R. Microbial control of mineral-groundwater equilibria: macroscale to microscale. Hydrogeol. J. 8, 47–62 (2000).
Bennett, P. C., Rogers, J. R. & Choi, W. J. Silicates, silicate weathering, and microbial ecology. Geomicrobiol. J. 18, 3–19 (2001).
Ehrenberg, S. N. & Jakobsen, K. G. Plagioclase dissolution related to biodegradation of oil in Brent Group sandstones (Middle Jurassic) of Gullfaks Field, Northern North Sea. Sedimentol. 48, 703–721 (2001).
Whelan, J. K., Eglinton, L., Kennicutt, M. C. & Qian, Y. R. Short-time-scale (year) variations of petroleum fluids from the US Gulf Coast. Geochim. Cosmochim. Acta 65, 3529–3555 (2001).
Yu, A. et al. How to predict biodegradation risk and reservoir fluid quality. World Oil 1–5 (April 2002).
Bjorlykke, K. in Growth, Dissolution and Pattern Formation in Geosystems (eds Jamtveit, B. & Meakin, P.) 381–404 (Kluwer, Netherlands, 1999).
Murphy, E. M. & Schramke, J. A. Estimation of microbial respiration rates in groundwater by geochemical modelling constrained with stable isotopes. Geochim. Cosmochim. Acta 62, 3395–3406 (1998).
Blöchl, E., Rachel, R., Burggraf, S., Hafenbradl, D., Jannasch, H. W. & Stetter, K. O. Pyrolobus fumarii, gen. and sp. nov., represents a novel group of archaea, extending the upper temperature limit for life to 113 degrees C. Extremophiles 1, 14–21 (1997).
Kashefi, K. & Lovley, D. R. Extending the upper temperature limit for life. Science 301, 934–934 (2003).
Stetter, K.O. Extremeophiles and their adaptation to hot environments. FEBS Lett. 452, 22–25 (1999).
Takahata, Y., Hoaki, T. & Maruyama, T. Starvation survivability of Thermococcus strains isolated from Japanese oil reservoirs. Arch. Microbiol. 176, 264–270 (2001).
Parkes, R. J. et al. Deep bacterial biosphere in Pacific Ocean sediments. Nature 371, 410–413 (1994).
Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: The unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998).
Demaison, G. J. Tar sands and supergiant oil fields. Bull. Am. Assoc. Petrol. Geol. 61, 1950–1961 (1977).
Creaney, S. & Allan, J. in Classic Petroleum Provinces (ed. Brooks, J.) 189–202 (Geol. Soc., London, 1990).
Piggott, N. & Lines, M. D. in Petroleum Migration (eds England, W. A. and Fleet, A. J.) 207–226 (Geol. Soc., London, 1991).
James, K. H. in Classic Petroleum Provinces (ed. Brooks, J.) 9–36 (Geol. Soc., London, 1990).
Butler, R. M. Some recent developments in SAGD. J. Can. Petrol. Technol. 40, 18–22 (2001).
Brooks, P. W., Fowler, M. G. & Macqueen, R. W. Organic geochemistry of Western Canada Basin tar sands and heavy oils. Org. Geochem. 12, 519–538 (1988).
Riediger, C. L., Fowler, M. G., Snowdon, L. R., MacDonald, R. & Sherwin, M. D. Origin and alteration of Lower Cretaceous Mannville Group l oils from the Provost oil field, east Central Alberta, Canada. Bull. Can. Petrol. Geol. 47, 43–62 (1999).
Rowland, S., Donkin, P., Smith, E. & Wraige, E. Aromatic hydrocarbon 'humps' in the marine environment: Unrecognized toxins? Environ. Sci. Tech. 35, 2640–2644 (2001).
Acknowledgements
Much of our work referenced in this insights article was funded and supported intellectually by two oil industry consortia, Phoenix (Norsk Hydro) and Bacchus (Shell, TexacoChevron, ExxonMobil, ConocoPhillips, Norsk Hydro, JNOC, Petrobras, Enterprise, TotalFinaElf, BP) and by NERC JREI awards. Specifically we acknowledge the contributions made to this article by our group at Newcastle and by colleagues elsewhere who have contributed comments and information. We acknowledge from Newcastle, B. Bennett, H. Huang, C. Aitken, A. Rowan, W. Röling, G. Love, P. Farrimond, A. Ross, B. Bowler, G. Rock, A. Aplin, K. Noke and from collaborating organizations, A. Wilhelms, M. Erdmann, H. Penteado, L. Trindade, L. Arauco, A. Murray, C. Riedieger, S. Creaney, T. Dunn, L. Wenger, M. Li, M. Koopmans, M. Bowen, C. Zhang, J. Cody and M. Fowler for past contributions.
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Head, I., Jones, D. & Larter, S. Biological activity in the deep subsurface and the origin of heavy oil. Nature 426, 344–352 (2003). https://doi.org/10.1038/nature02134
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