Direct evaluation of in situ biodegradation in athabasca oil sands tailings ponds using natural abundance radiocarbon

Environmental Science and Technology

Volumn 47, Issue 18, 2013, Pages 10214-10222

  Ahad, Jason M E ^a   Pakdel, Hooshang ^b  

^a GEOLOGICAL SURVEY OF CANADA   (Canada)

^b CENTRE EAU TERRE ENVIRONNEMENT   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ATHABASCA OIL SANDS; MICROBIAL COMMUNITIES; MICROBIAL POPULATIONS; ORGANIC CONTAMINANT; PETROLEUM HYDROCARBONS; PHOSPHOLIPID FATTY ACIDS; REMEDIATION STRATEGIES; SITU BIODEGRADATIONS;

BIODEGRADATION; BIOGEOCHEMISTRY; BIOLOGICAL MATERIALS; BITUMINOUS MATERIALS; ISOTOPES; OIL SANDS; ORGANIC COMPOUNDS; PETROLEUM CHEMISTRY; PHOSPHOLIPIDS;

CARBON;

ASPHALT; CARBON; CARBON 13; CARBON 14; OIL; ORGANIC MATTER; PETROLEUM; PETROLEUM DERIVATIVE; WATER;

BIODEGRADATION; BIOREMEDIATION; BITUMEN; CARBON ISOTOPE; FATTY ACID; HETEROTROPHY; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; OIL SAND; ORGANIC POLLUTANT; PETROLEUM HYDROCARBON; PHOSPHOLIPID; SURFICIAL SEDIMENT; TAILINGS;

ARTICLE; BIODEGRADATION; CARBON SOURCE; CONTROLLED STUDY; EXTRACTION; FOSSIL; METABOLISM; MICROBIAL COMMUNITY; MINE TAILINGS; NONHUMAN; SAND; SEDIMENT;

ALBERTA; ATHABASCA OIL SANDS; ATHABASCA RIVER; CANADA;

BIODEGRADATION, ENVIRONMENTAL; CARBON ISOTOPES; FATTY ACIDS; GEOLOGIC SEDIMENTS; HYDROCARBONS; INDUSTRIAL WASTE; OIL AND GAS FIELDS; PHOSPHOLIPIDS; WATER POLLUTANTS, CHEMICAL;

EID: 84884218664     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es402302z     Document Type: Article

References (70)

1. ST98-2012: Alberta's Energy Reserves 2011 and Supply/Demand Outlook 2012-2021. Energy Resources Conservation Board (ERCB): Calgary, Alberta, 2012; 290 p.
2. Proemse, B. C.; Mayer, B.; Chow, J. C.; Watson, J. G. Isotopic characterization of nitrate, ammonium and sulfate in stack PM 2.5 emissions in the Athabasca Oil Sands Region, Alberta, Canada Atmos. Environ. 2012, 60, 555-563
3. Jautzy, J.; Ahad, J. M. E.; Gobeil, C.; Savard, M. M. Century-long source apportionment of PAHs in Athabasca oil sands region lakes using diagnostic ratios and compound-specific carbon isotope signatures Environ. Sci. Technol. 2013, 47, 6155-6163
4. Kelly, E. N.; Short, J. W.; Schindler, D. W.; Hodson, P. V.; Ma, M. S.; Kwan, A. K.; Fortin, B. L. Oil sands development contributes polycyclic aromatic compounds to the Athabasca River and its tributaries Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 22346-22351
5. Kurek, J.; Kirk, J. L.; Muir, D. C. G.; Wang, X.; Evans, M. S.; Smol, J. P. Legacy of a half century of Athabasca oil sands development recorded by lake ecosystems Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 1761-1766
6. Kelly, E. N.; Schindler, D. W.; Hodson, P. V.; Short, J. W.; Radmanovich, R.; Nielsen, C. C. Oil sands development contributes elements toxic at low concentrations to the Athabasca River and its tributaries Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 16178-16183
7. Allen, E. W. Process water treatment in Canada's oil sands industry: II. A review of emerging technologies J. Environ. Eng. Sci. 2008, 7, 499-524
8. Ahad, J. M. E.; Pakdel, H.; Savard, M. M.; Calderhead, A. I.; Gammon, P. R.; Rivera, A.; Headley, J. V.; Peru, K. M. Characterization and quantification of mining-related "naphthenic acids" in groundwater near a major oil sands tailings pond Environ. Sci. Technol. 2013, 47, 5023-5030
9. Oiffer, A. A. L.; Barker, J. F.; Gervais, F. M.; Mayer, K. U.; Ptacek, C. J.; Rudolph, D. L. A detailed field-based evaluation of naphthenic acid mobility in groundwater J. Contam. Hydrol. 2009, 108, 89-106
10. Rooney, R. C.; Bayley, S. E.; Schindler, D. W. Oil sands mining and reclamation cause massive loss of peatland and stored carbon Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 4933-4937
11. Siddique, T.; Fedorak, P. M.; Foght, J. M. Biodegradation of short-chain n-alkanes in oil sands tailings under methanogenic conditions Environ. Sci. Technol. 2006, 40, 5459-5464 (Pubitemid 44373113)
12. Siddique, T.; Fedorak, P. M.; McKinnon, M. D.; Foght, J. M. Metabolism of BTEX and naphtha compounds to methane in oil sands tailings Environ. Sci. Technol. 2007, 41, 2350-2356 (Pubitemid 46595197)
13. Siddique, T.; Penner, T.; Semple, K.; Foght, J. M. Anaerobic biodegradation of longer-chain n-alkanes coupled to methane production in oil sands tailings Environ. Sci. Technol. 2011, 45, 5892-5899
14. Clemente, J. S.; Fedorak, P. M. A review of the occurrence, analyses, toxicity, and biodegradation of naphthenic acids Chemosphere 2005, 60, 585-600
15. Del Rio, L. F.; Hadwin, A. K. M.; Pinto, L. J.; MacKinnon, M. D.; Moore, M. M. Degradation of naphthenic acids by sediment micro-organisms J. Appl. Microbiol. 2006, 101, 1049-1061 (Pubitemid 44581896)
16. Quagraine, E. K.; Peterson, H. G.; Headley, J. V. In situ bioremediation of naphthenic acids contaminated tailing pond waters in the Athabasca oil sands region-demonstrated field studies and plausible options: A review J. Environ. Sci. Health, Part A: Toxic/Hazard. Subst. Environ. Eng. 2005, 40, 685-722 (Pubitemid 40283886)
17. Videla, P. P.; Farwell, A. J.; Butler, B. J.; Dixon, D. G. Examining the microbial degradation of naphthenic acids using stable isotope analysis of carbon and nitrogen Water Air Soil Pollut. 2009, 197, 107-119
18. Scott, A. C.; MacKinnon, M. D.; Fedorak, P. M. Naphthenic acids in Athabasca oil sands tailings waters are less biodegradable than commercial naphthenic acids Environ. Sci. Technol. 2005, 39, 8388-8394
19. 2 time series for North American continental air. J. Geophys. Res. [Atmos.] 2007, 112; DOI: 10.1029/2006JD008184.
20. Ahad, J. M. E.; Burns, L.; Mancini, S.; Slater, G. F. Assessing microbial uptake of petroleum hydrocarbons in groundwater systems using natural abundance radiocarbon Environ. Sci. Technol. 2010, 44, 5092-5097
21. 14C analysis of PLFA Environ. Sci. Technol. 2010, 44, 2322-2327
22. Mahmoudi, N.; Fulthorpe, R. R.; Burns, L.; Mancini, S.; Slater, G. F. Assessing microbial carbon sources and potential PAH degradation using natural abundance 14C analysis Environ. Pollut. 2013, 175, 125-130
23. 14C analysis Environ. Sci. Technol. 2005, 39, 2552-2558
24. 14C analysis Org. Geochem. 2006, 37, 981-989 (Pubitemid 44292849)
25. Wakeham, S. G.; McNichol, A. P.; Kostka, J. E.; Pease, T. K. Natural-abundance radiocarbon as a tracer of assimilation of petroleum carbon by bacteria in salt marsh sediments Geochim. Cosmochim. Acta 2006, 70, 1761-1771
26. Headley, J. V.; Peru, K. M.; McMartin, D. W.; Winkler, M. Determination of dissolved naphthenic acids in natural waters by using negative-ion electrospray mass spectrometry J. AOAC Int. 2002, 85, 182-187 (Pubitemid 135691687)
27. White, H. K.; Reddy, C. M.; Eglinton, T. I. Isotopic constraints on the fate of petroleum residues sequestered in salt marsh sediments Environ. Sci. Technol. 2005, 39, 2545-2551
28. White, D. C.; Davis, W. M.; Nickels, J. S.; King, J. D.; Bobbie, R. J. Determination of the sedimentary microbial biomass by extractible lipid phosphate Oecologia 1979, 40, 51-62
29. Cherkinsky, A.; Ravi Prasad, G. V.; Dvoracek, D. AMS measurement of samples smaller than 300 μg at center for applied isotope studies, University of Georgia Nucl. Instrum. Methods Phys. Res., Sect. B 2013, 294, 87-90
30. Guckert, J. B.; Antworth, C. P.; Nichols, P. D.; White, D. C. Phospholipid, ester-linked fatty acid profiles as reproducible assay for change in prokaryotic community structure of estuarine sediments FEMS Microbiol. Ecol. 1985, 31, 147-158
31. 13C) analysis of dissolved inorganic carbon and dissolved organic carbon in continuous-flow using a total organic carbon analyser Rapid Commun. Mass Spectrom. 2003, 17, 419-428 (Pubitemid 36267977)
32. Vogel, J. S.; Southon, J. R.; Nelson, D. E.; Brown, T. A. Performance of catalytically condensed carbon for use in accelerator mass spectrometry Nucl. Instrum. Methods Phys. Res., Sect. B 1984, 5, 289-293
33. 14C data Radiocarbon 1977, 19, 355-363
34. Eglinton, T. I.; Aluwihare, L. I.; Bauer, J. E.; Druffel, E. R. M.; McNichol, A. P. Gas chromatographic isolation of individual compounds from complex matrices for radiocarbon dating Anal. Chem. 1996, 68, 904-912
35. Ahad, J. M. E.; Ganeshram, R. S.; Bryant, C. L.; Cisneros-Dozal, L. M.; Ascough, P. L.; Fallick, A. E.; Slater, G. F. Sources of n-alkanes in an urbanized estuary: Insights from molecular distributions and compound-specific stable and radiocarbon isotopes Mar. Chem. 2011, 126, 239-249
36. Aries, E.; Doumenq, P.; Artaud, J.; Acquaviva, M.; Bertrand, J. C. Effects of petroleum hydrocarbons on the phospholipid fatty acid composition of a consortium composed of marine hydrocarbon-degrading bacteria Org. Geochem. 2001, 32, 891-903
37. Doumenq, P.; Aries, E.; Asia, L.; Acquaviva, M.; Artaud, J.; Gilewicz, M.; Mille, G.; Bertrand, J. C. Influence of n-alkanes and petroleum on fatty acid composition of a hydrocarbonoclastic bacterium: Marinobacter hydrocarbonoclasticus strain 617 Chemosphere 2001, 44, 519-528 (Pubitemid 32641457)
38. Greenwood, P. F.; Wibrow, S.; George, S. J.; Tibbett, M. Hydrocarbon biodegradation and soil microbial community response to repeated oil exposure Org. Geochem. 2009, 40, 293-300
39. Hallmann, C.; Schwark, L.; Grice, K. Community dynamics of anaerobic bacteria in deep petroleum reservoirs Nat. Geosci. 2008, 1, 588-591
40. So, C. M.; Young, L. Y. Initial reactions in anaerobic alkane degradation by a sulfate reducer, strain AK-01 Appl. Environ. Microbiol. 1999, 65, 5532-5540 (Pubitemid 129520647)
41. Green, C. T.; Scow, K. M. Analysis of phospholipid fatty acids (PLFA) to characterize microbial communities in aquifers Hydrogeol. J. 2000, 8, 126-141
42. Gibson, J. J.; Birks, S. J.; Moncur, M.; Yi, Y.; Tattrie, K.; Jasechko, S.; Richardson, K.; Eby, P. Isotopic and Geochemical Tracers for Fingerprinting Process-Affected Waters in the Oil Sands Industry: A Pilot Study; Oil Sands Research and Information Network, University of Alberta, School of Energy and the Environment: Edmonton, Alberta, 2011; p 109.
43. Jha, K. N.; Gray, J.; Strausz, O. P. The isotopic composition of carbon in the Alberta oil sand Geochim. Cosmochim. Acta 1979, 43, 1571-1573
44. Ahad, J. M. E.; Pakdel, H.; Savard, M. M.; Simard, M.-C.; Smirnoff, A. Extraction, separation and intramolecular carbon isotope characterization of Athabasca oil sands acids in environmental samples Anal. Chem. 2012, 84, 10419-10425
45. Boschker, H. T. S.; Kromkamp, J. C.; Middelburg, J. J. Biomarker and carbon isotopic constraints on bacterial and algal community structure and functioning in a turbid, tidal estuary Limnol. Oceanogr. 2005, 50, 70-80 (Pubitemid 40199028)
46. Hayes, J. M. Fractionation of carbon and hydrogen isotopes in biosynthetic processes. In Stable Isotope Geochemistry; Mineralogical Soc America: Washington, D.C, 2001; Vol. 43, pp 225-277.
47. Teece, M. A.; Fogel, M. L.; Dollhopf, M. E.; Nealson, K. H. Isotopic fractionation associated with biosynthesis of fatty acids by a marine bacterium under oxic and anoxic conditions Org. Geochem. 1999, 30, 1571-1579
48. Londry, K. L.; Jahnke, L. L.; Marais, D. J. D. Stable carbon isotope ratios of lipid biomarkers of sulfate-reducing bacteria Appl. Environ. Microbiol. 2004, 70, 745-751 (Pubitemid 38568194)
49. Siddique, T.; Penner, T.; Klassen, J.; Nesbø, C.; Foght, J. M. Microbial communities involved in methane production from hydrocarbons in oil sands tailings Environ. Sci. Technol. 2012, 46, 9802-9810
50. Saidi-Mehrabad, A.; He, Z.; Tamas, I.; Sharp, C. E.; Brady, A. L.; Rochman, F. F.; Bodrossy, L.; Abell, G. C. J.; Penner, T.; Dong, X.; Sensen, C. W.; Dunfield, P. F. Methanotrophic bacteria in oilsands tailings ponds of northern Alberta ISME J. 2012, 7, 908-921
51. Bodelier, P. L. E.; Bär Gillisen, M. J.; Hordijk, K.; Sinninghe Damsté, J. S.; Rijpstra, W. I. C.; Geenevasen, J. A. J.; Dunfield, P. F. A reanalysis of phospholipid fatty acids as ecological biomarkers for methanotrophic bacteria ISME J. 2009, 3, 606-617
52. Whiticar, M. J. Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane Chem. Geol. 1999, 161, 291-314 (Pubitemid 30130536)
53. Dijkman, N. A.; Boschker, H. T. S.; Middelburg, J. J.; Kromkamp, J. C. Group-specific primary production based on stable-isotope labeling of phospholipid-derived fatty acids Limnol. Oceanogr.: Methods 2009, 7, 612-625
54. Taipale, S.; Kankaala, P.; Hämäläinen, H.; Jones, R. I. Seasonal shifts in the diet of lake zooplankton revealed by phospholipid fatty acid analysis Freshwater Biol. 2009, 54, 90-104
55. Risse-Buhl, U.; Trefzger, N.; Seifert, A. G.; Schönborn, W.; Gleixner, G.; Küsel, K. Tracking the autochthonous carbon transfer in stream biofilm food webs FEMS Microbiol. Ecol. 2012, 79, 118-131
56. Leung, S. S.-C.; MacKinnon, M. D.; Smith, R. E. H. Aquatic reclamation in the Athabasca, Canada, oil sands: Naphthenate and salt effects on phytoplankton communities Environ. Toxicol. Chem. 2001, 20, 1532-1543 (Pubitemid 32550014)
57. Leung, S. S.; MacKinnon, M. D.; Smith, R. E. H. The ecological effects of naphthenic acids and salts on phytoplankton from the Athabasca oil sands region Aquat. Toxicol. 2003, 62, 11-26 (Pubitemid 36159006)
58. Quesnel, D. M.; Bhaskar, I. M.; Gieg, L. M.; Chua, G. Naphthenic acid biodegradation by the unicellular alga Dunaliella tertiolecta Chemosphere 2011, 84, 504-511
59. Headley, J. V.; Du, J. L.; Peru, K. M.; Gurprasad, N.; McMartin, D. W. Evaluation of algal phytodegradation of petroleum naphthenic acids J. Environ. Sci. Health, Part A: Toxic/Hazard. Subst. Environ. Eng. 2008, 43, 227-232
60. Van Den Meersche, K.; Van Rijswijk, P.; Soetaert, K.; Middelburg, J. J. Autochthonous and allochthonous contributions to mesozooplankton diet in a tidal river and estuary: Integrating carbon isotope and fatty acid constraints Limnol. Oceanogr. 2009, 54, 62-74
61. Zhang, J.; Quay, P. D.; Wilbur, D. O. Carbon isotope fractionation during gas-water exchange and dissolution of CO2 Geochim. Cosmochim. Acta 1995, 59, 107-114
62. Baniulyte, D.; Favila, E.; Kelly, J. J. Shifts in microbial community composition following surface application of dredged river sediments Microb. Ecol. 2009, 57, 160-169
63. Olsson, P. A. Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil FEMS Microbiol. Ecol. 1999, 29, 303-310 (Pubitemid 29339089)
64. McCallister, S. L.; Del Giorgio, P. A. Evidence for the respiration of ancient terrestrial organic C in northern temperate lakes and streams Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 16963-16968
65. 14N) to trace exposure to oil sands processed material in the Alberta oil sands region J. Toxicol. Environ. Health, Part A 2009, 72, 385-396
66. Kasperski, K. Natural Resources Canada. Personal communication, July, 2013.
67. Seifert, A. G.; Trumbore, S.; Xu, X.; Zhang, D.; Gleixner, G. Variable effects of plant colonization on black slate uptake into microbial PLFAs Geochim. Cosmochim. Acta 2013, 106, 391-403
68. Seifert, A. G.; Trumbore, S.; Xu, X.; Zhang, D.; Kothe, E.; Gleixner, G. Variable effects of labile carbon on the carbon use of different microbial groups in black slate degradation Geochim. Cosmochim. Acta 2011, 75, 2557-2570
69. Fontaine, S.; Barot, S.; Barre, P.; Bdioui, N.; Mary, B.; Rumpel, C. Stability of organic carbon in deep soil layers controlled by fresh carbon supply Nature 2007, 450, 277-280 (Pubitemid 350100539)
70. Bianchi, T. S. The role of terrestrially derived organic carbon in the coastal ocean: A changing paradigm and the priming effect Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 19473-19481