Abstract
Open-pit mining of the Athabasca oil sands has generated large volumes of waste termed fluid fine tailings (FFT), stored in tailings ponds. Accumulation of toxic organic substances in the tailings ponds is one of the biggest concerns. Gamma irradiation (GI) treatment could accelerate the biodegradation of toxic organic substances. Hence, this research investigates the response of the microbial consortia in GI-treated FFT materials with an emphasis on changes in diversity and organism-related stimuli. FFT materials from aged and fresh ponds were used in the study under aerobic and anaerobic conditions. Variations in the microbial diversity in GI-treated FFT materials were monitored for 52 weeks and significant stimuli (p < 0.05) were observed. Chemoorganotrophic organisms dominated in fresh and aged ponds and showed increased relative abundance resulting from GI treatment. GI-treated anaerobic FFTaged reported stimulus of organisms with biodegradation potential (e.g., Pseudomonas, Enterobacter) and methylotrophic capabilities (e.g., Syntrophus, Smithella). In comparison, GI-treated anaerobic FFTfresh stimulated Desulfuromonas as the principle genus at 52 weeks. Under aerobic conditions, GI-treated FFTaged showed stimulation of organisms capable of sulfur and iron cycling (e.g., Geobacter). However, GI-treated aerobic FFTfresh showed no stimulus at 52 weeks. This research provides an enhanced understanding of oil sands tailings biogeochemistry and the impacts of GI treatment on microorganisms as an effect for targeting toxic organics. The outcomes of this study highlight the potential for this approach to accelerate stabilization and reclamation end points.
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Yergeau E, Lawrence JR, Sanschagrin S, Waiser MJ, Korber DR, Greer CW (2012) Next-generation sequencing of microbial communities in the Athabasca River and its tributaries in relation to oil sands mining activities. Appl. Environ. Microbiol. 78:7626–7637
Quagraine EK, Peterson HG, Headley JV (2005) 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 40:685–722
Holowenko FM, MacKinnon MD, Fedorak PM (2000) Methanogens and sulfate-reducing bacteria in oil sands fine tailings waste. Can. J. Microbiol. 46:927–937
Scott AC, MacKinnon MD, Fedorak PM (2005) Naphthenic acids in Athabasca oil sands tailings waters are less biodegradable than commercial naphthenic acids. Environ Sci Technol 39:8388–8394
Grewer DM, Young RF, Whittal RM, Fedorak PM (2010) Naphthenic acids and other acid-extractables in water samples from Alberta: what is being measured? Sci. Total Environ. 408:5997–6010
Boudens R, Reid T, VanMensel D, Prakasan MRS, Ciborowski JJH, Weisener CG (2016) Bio-physicochemical effects of gamma irradiation treatment for naphthenic acids in oil sands fluid fine tailings. Sci. Total Environ. 539:114–124
Clemente JS, Fedorak PM (2005) A review of the occurrence, analyses, toxicity, and biodegradation of naphthenic acids. Chemosphere 60:585–600
Frank RA, Kavanagh R, Burnison BK, Arsenault G, Headley JV, Peru KM, et al. (2008) Toxicity assessment of collected fractions from an extracted naphthenic acid mixture. Chemosphere 72:1309–1314
Marentette JR, Frank RA, Bartlett AJ, Gillis PL, Hewitt LM, Peru KM, Headley JV, Brunswick P, Shang D, Parrott JL (2015) Toxicity of naphthenic acid fraction components extracted from fresh and aged oil sands process-affected waters, and commercial naphthenic acid mixtures, to fathead minnow (Pimephales promelas) embryos. Aquat. Toxicol. 164:108–117
Bataineh MP, Scott AC, Fedorak PM, Martin JW (2006) Capillary HLC/QTOF-MS for characterizing complex naphthenic acid mixtures and their microbial transformation. Anal. Chem. 78:8354–8361
Johnson RJ, Smith BE, Sutton PA, McGenity TJ, Rowland SJ, Whitby C (2010) Microbial degradation of aromatic alkanoic naphthenic acids is affected by the degree of alkyl side chain branching. ISME J 2010:1–11
Scott AC, Zubot W, MacKinnon MD, Smith DW, Fedorak PM (2008) Ozonation of oil sands process water removes naphthenic acids and toxicity. Chemosphere 71:156–160
Martin JW, Barri T, Han X, Fedorak PM, Gamal El-Din M, Perez L, et al. (2010) Ozonation of oil sands process-affected water accelerates microbial bioremediation. Environ Sci Technol 44:8350–8356
McMartin DW, Headley JV, Friesen DA, Peru KM, Gillies JA (2004) Photolysis of naphthenic acids in natural surface water. J Environ Sci Health, Part A 39:1361–1383
Siddique T, Penner T, Semple K, Foght JM (2011) Anaerobic biodegradation of longer-chain n-alkanes coupled to methane production in oil sands tailings. Environ Sci Technol 45:5892–5899
Siddique T, Penner T, Klassen J, Nesbø C, Foght JM (2012) Microbial communities involved in methane production from hydrocarbons in oil sands tailings. Environ Sci Technol 46:9802–9810
Tan B, Dong X, Sensen CW, Foght J (2013) Metagenomic analysis of an anaerobic alkane-degrading microbial culture: potential hydrocarbon-activating pathways and inferred roles of community members. Genome 611:599–611
Toor NS, Han X, Franz E, MacKinnon MD, Martin JW, Liber K (2013) Selective biodegradation of naphthenic acids and a probable link between mixture profiles and aquatic toxicity. Environ. Toxicol. Chem. 32:2207–2216
Berdugo-Clavijo C, Gieg LM (2014) Conversion of crude oil to methane by a microbial consortium enriched from oil reservoir production waters. Front. Microbiol. 5:1–10
Gieg LM, Fowler SJ, Berdugo-Clavijo C (2014) Syntrophic biodegradation of hydrocarbon contaminants. Curr. Opin. Biotechnol. 27:21–29
Clavero MRS, Monk JD, Beuchat LR, Doyle MP, Brackett RE (1994) Inactivation of Escherichia coli O157:H7, Salmonellae, and Campylobacter jejuni in raw ground beef by gamma irradiation. Appl. Environ. Microbiol. 60:2069–2275
Aparecida, da Silva Aquino K (2012) Sterilization by gamma irradiation. Gamma Radiat ISBN: 978–953–51-0316-5, InTech, Available at: http://www.intechopen.com/books/gamma-radiation/sterilization-by-gamma-irradiation.
Tuominen L, Kairesalo T, Hartikainen H (1994) Comparison of methods for inhibiting bacterial activity in sediment. Appl. Environ. Microbiol. 60:3454–3457
Trevors TJ (1996) Sterilization and inhibition of microbial activity in soil. J. Microbiol. Methods 26:53–59
McNamara NP, Black HIJ, Beresford NA, Parekh NR (2003) Effects of acute gamma irradiation on chemical, physical and biological properties of soils. Appl. Soil Ecol. 24:117–132
Wolf DC, Dao TH, Scott HD, Lavy TL (1989) Influence of sterilization methods on selected microbiological, physical, and chemical properties. J. Environ. Qual. 18:39–44
Lotrario JB, Stuart BJ, Lam T, Arands RR, O’Connor OA, Kosson DS (1995) Effects of sterilization methods on the physical characteristics of soil: implications for sorption isotherm analyses. Bull. Environ. Contam. Toxicol. 54:668–675
Bank TL, Kukkadapu RK, Madden AS, Ginder-Vogel MA, Baldwin ME, Jardine PM (2008) Effects of gamma-sterilization on the physico-chemical properties of natural sediments. Chem. Geol. 251:1–7
Chen M, Walshe G, Chi Fru E, Ciborowski JJH, Weisener CG (2013) Microcosm assessment of the biogeochemical development of sulfur and oxygen in oil sands fluid fine tailings. Appl Geochemistry 37:1–11
Anderson JC, Wiseman SB, Wang N, Moustafa A, Perez-Estrada L, Gamal El-Din M, et al. (2012) Effectiveness of ozonation treatment in eliminating toxicity of oil sands process-affected water to Chironomus dilutus. Environ Sci Technol 46:486–493
Jia W, He Y, Ling Y, Hei D, Shan Q, Zhang Y, Li J (2015) Radiation-induced degradation of cyclohexanebutyric acid in aqueous solutions by gamma ray irradiation. Radiat. Phys. Chem. 109:17–22
Siddique T, Kuznetsov P, Kuznetsova A, Arkell N, Young R, Li C, Guigard S, Underwood E, Foght JM (2014) Microbially-accelerated consolidation of oil sands tailings. Pathway I: changes in porewater chemistry. Front. Microbiol. 5:106
Siddique T, Kuznetsov P, Kuznetsova A, Li C, Young R, Arocena JM, Foght JM (2014) Microbially-accelerated consolidation of oil sands tailings. Pathway II: solid phase biogeochemistry. Front. Microbiol. 5:107
Fedorak PM, Coy DL, Dudas MJ, Simpson MJ, Renneberg AJ, MacKinnon MD (2003) Microbially-mediated fugitive gas production from oil sands tailings and increased tailings densification rates. J. Environ. Eng. Sci. 2:199–211
Eckert WF, Masliyah JH, Gray MR, Fedorak PM (1996) Prediction of sedimentation and consolidation of fine tails. AICHE J. 42:960–972
Kannel PR, Gan TY (2012) Naphthenic acids degradation and toxicity mitigation in tailings wastewater systems and aquatic environments: a review. J Environ Sci Health, Part A 47:1–21
Chi Fru E, Chen M, Walshe G, Penner T, Weisener C (2013) Bioreactor studies predict whole microbial population dynamics in oil sands tailings ponds. Appl. Microbiol. Biotechnol. 97:3215–3224
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10:996–998
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electronica 4:9
Stasik S, Wendt-Potthoff K (2014) Interaction of microbial sulphate reduction and methanogenesis in oil sands tailings ponds. Chemosphere 103:59–66
Penner TJ, Foght JM (2010) Mature fine tailings from oil sands processing harbour diverse methanogenic communities. Can. J. Microbiol. 56:459–470
Harner NK, Richardson TL, Thompson KA, Best RJ, Best AS, Trevors JT (2011) Microbial processes in the Athabasca Oil Sands and their potential applications in microbial enhanced oil recovery. J. Ind. Microbiol. Biotechnol. 38:1761–1775
Bernardet JF, Nakagawa Y (2006) An introduction to the family Flavobacteriaceae. Prokaryotes 7:455–480
Pommier T, Canback B, Riemann L, Bostrom KH, Simu K, Lundberg P, Tunlid A, Hagstrom A (2007) Global patterns of diversity and community structure in marine bacterioplankton. Mol. Ecol. 16:867–880
Thomas F, Hehemann J, Rebuffet E, Czjzek M, Michel G (2011) Environmental and gut Bacteroidetes: the food connection. Front. Microbiol. 2:1–16
Shirokova VL, Ferris FG (2013) Microbial diversity and biogeochemistry of a shallow pristine Canadian Shield groundwater system. Geomicrobiol J. 30:140–149
Tian J, Lu J, Zhang Y, Li JC, Sun LC, Hu ZL (2014) Microbial community structures and dynamics in the O3/BAC drinking water treatment process. Int. J. Environ. Res. Public Health 11:6281–6290
Kersters K, De Vos P, Gillis M, Swings J, Vandamme P, Stakebrandt E (2006) Introduction to the proteobacteria. Prokaryotes 5:3–37
Bowman DD (2011) Introduction to the alpha-proteobacteria: Wolbachia and Bartonella, Rickettsia, Brucella, Ehrlichia, and Anaplasma. Top Companion Anim Med 26:173–177
Hedrich S, Schlomann M, Johnson DB (2011) The iron-oxidizing proteobacteria. Microbiol 157:1551–1564
Kaplan CW, Kitts CL (2004) Bacterial succession in a petroleum land treatment unit. Appl. Environ. Microbiol. 70:1777–1786
Bernardet JF, Bowman JP (2006) The genus Flavobacterium. Prokaryotes 7:481–531
An D, Brown D, Chatterjee I, Dong X, Ramos-Padron E, Wilson S, et al. (2013) Microbial community and potential functional gene diversity involved in anaerobic hydrocarbon degradation and methanogenesis in an oil sands tailings pond. Genome 56:612–618
Reeburgh WS (1983) Rates of biogeochemical processes in anoxic sediments. Annu. Rev. Earth Planet. Sci. 11:269–298
Stasik S, Loick N, Knӧller K, Weisener C, Wendt-Potthoff K (2014) Understanding biogeochemical gradients of sulfur, iron and carbon in an oil sands tailings pond. Chem. Geol. 382:44–53
Golby S, Ceri H, Gieg LM, Chatterjee I, Marques LLR, Turner RJ (2012) Evaluation of microbial biofilm communities from an Alberta oil sands tailings pond. FEMS Microbiol. Ecol. 79:240–250
Ahmed AW, Alzubaidi FS, Hamza SJ (2014) Biodegradation of crude oil in contaminated water by local isolates of Enterobacter cloacae. Iraqi J Sci 55:1025–1033
Khorasani AC, Mashreghi M, Yaghmaei S (2013) Study on biodegradation of Mazut by newly isolated strain Enterobacter cloacae BBRC10061: improving and kinetic investigation. Iranian J Environ Health Sci Eng 10:1–7
Razika B, Abbes B, Messaoud C, Soufi K (2010) Phenol and benzoic acid degradation by Pseudomonas aeruginosa. JWARP 2:788–791
Mahiudddin MD, Fakhruddin ANM, Abdullah-Al-Mahin (2012) Degradation of phenol via meta cleavage pathway by Pseudomonas fluorescens PU1. ISRN Microbiol 2012:1–6
Kostka JE, Prakash O, Overholt WA, Green SJ, Freyer G, Canion A, et al. (2011) Hydrocarbon-degrading bacteria and the bacterial community response in Gulf of Mexico beach sands impacted by the Deepwater Horizon oil spill. Appl. Environ. Microbiol. 77:7962–7974
Johnson RJ, Smith BE, Sutton PA, McGenity TJ, Rowland SJ, Whitby C (2011) Microbial biodegradation of aromatic alkanoic naphthenic acids is affected by the degree of alkyl side chain branching. ISME J 5:486–496
Ma J, Xu L, Jia L (2012) Degradation of polycyclic aromatic hydrocarbons by Pseudomonas sp. JM2 isolated from active sewage sludge of chemical plant. J. Environ. Sci. 24:2141–2148
Chistoserdova L, Kalyuzhnaya M, Lidstrom M (2009) The expanding world of methylotrophic metabolism. Annu. Rev. Microbiol. 63:477–499
Liu Y, Balkwill DL, Aldrich HC, Drake GR, Boone DR (1999) Characterization of the anaerobic propionate-degrading syntrophs Smithella propionica gen. nov., sp. nov. and Syntrophobacter wolinii. Int. J. Syst. Bacteriol. 49:545–556
Dojka MA, Hugenholtz P, Haack SK, Pace NR (1998) Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl. Environ. Microbiol. 64:3869–3877
Tan B, Nesbø C, Foght J (2014) Re-analysis of omics data indicates Smithella may degrade alkanes by addition to fumarate under methanogenic conditions. ISME J 8:2353–2356
Caccavo F, Lonergan DJ, Lovley DR, Davis M, Stolz JF, McInerney MJ (1994) Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl. Environ. Microbiol. 60:3752–3759
Butler JE, He Q, Nevin KP, He Z, Zhou J, Lovley DR (2007) Genomic and microarray analysis of aromatics degradation in Geobacter metallireducens and comparison to a Geobacter isolate from a contaminated field site. BMC Genomics 8:180
Finneran KT, Anderson RT, Nevin KP, Lovley DR (2002) Potential for bioremediation of uranium-contaminated aquifers with microbial U(VI) reduction. Soil Sediment Contam. 11:339–357
Byrne-Bailey KG, Weber KA, Chair AH, Bose S, Knox T, Spanbauer TL, et al. (2010) Completed genome sequence of the anaerobic iron-oxidizing bacterium Acidovorax ebreus strain TPSY. J. Bacteriol. 192:1475–1476
Taft S (2009) Identification and analysis of genes involved in anaerobic nitrate-dependent iron oxidation. Dissertation. Retrieved from ProQuest Dissertations and Theses. (Accession Order No. AAT 3372571)
Khan ST, Hiraishi A (2002) Diaphorobacter nitroreducens gen. nov., sp. nov., a poly(3-hydroxybutyrate)-degrading denitrifying bacterium isolated. J. Gen. Appl. Microbiol. 308:299–308
Klankeo P, Nopcharoenkul W, Pinyakong O (2009) Two novel pyrene-degrading Diaphorobacter sp. and Pseudoxanthomonas sp. isolated from soil. J. Biosci. Bioeng. 108:488–495
Wang X, Hu M, Xia Y, Wen X, Ding K (2012) Pyrosequencing analysis of bacterial diversity in 14 wastewater treatment systems in China. Appl. Environ. Microbiol. 78:7042–7047
Hersikorn BD, Ciborowski JJH, Smits JEG (2010) The effects of oil sands wetlands on wood frogs (Rana sylvatica). Toxicol. Environ. Chem. 92:1513–1527
Pfennig N, Biebl H (1976) Desulfuromonas acetoxidans gen. nov. and sp. nov., a new anaerobic, sulfur-reducing, acetate-oxidizing bacterium. Arch. Microbiol. 110:3–12
Lovley DR (2002) Dissimilatory metal reduction: from early life to bioremediation. ASM News 68:231–237
Zhang L, Zhang Q, Luo X, Tang Y, Dai J, Li Y, et al. (2008) Pontibacter korlensis sp. nov., isolated from the desert of Xinjiang, China. Int. J. Syst. Evol. Microbiol. 58:1210–1214
Xu L, Zeng XC, Nie Y, Luo X, Zhou E, Zhou L, et al. (2014) Pontibacter diazotrophicus sp. Nov., a novel nitrogen-fixing bacterium of the family Cytophagaceae. PLoS One 9:e92294
Singh AK, Garg N, Lata P, Kumar R, Negi V, Vikram S, Lal R (2014) Pontibacter indicus sp. nov., isolated from hexachlorocyclohexane-contaminated soil. Int. J. Syst. Evol. Microbiol. 64:254–259
Nedashkovskaya OI, Bum Kim S, Suzuki M, Shevchenko LS, Sook Lee M, Hyun Lee K, et al. (2005) Pontibacter actiniarum gen. nov., sp. nov., a novel member of the phylum ‘Bacteroidetes’, and proposal of Reichenbachiella gen. nov. as a replacement for the illegitimate prokaryotic generic name Reichenbachiella Nedashkovskaya et al 2003. Int. J. Syst. Evol. Microbiol. 55:2583–2588
Joshi MN, Sharma AC, Pandya RV, Patel RP, Saiyed ZM, Saxena AK, Bagatharia SB (2012) Draft genome sequence of Pontibacter sp. nov. BAB1700, a halotolerant, industrially important bacterium. J. Bacteriol. 194:6329–6330
Rabus R, Hansen T, Widdel F (2004) The prokaryotes: an evolving electronic resource for the microbiological community. Springer-Verlang New York, LLC
Barlett M, Zhuang K, Mahadevan R, Lovley D (2012) Integrative analysis of Geobacter spp. and sulfate-reducing bacteria during uranium bioremediation. Biogeosciences 9:1033–1040
Acknowledgements
The authors wish to thank Suncor Energy Incorporated, Syncrude Canada Limited, Total E & P., Shell Canada, Imperial Oil Resources, and Canadian Natural Resources Limited for funding support and cooperation to make this research project possible. We thank Robert Pasuta (McMaster University Nuclear Reactor Supervisor) for providing off-site research facilities and logistical support for the GI treatments. We thank former Suncor technical program manager, Christine Daly, for her support and encouragement during early stages of the program, as well as Joshua Martin who is the current program coordinator for the industrial partners. We also thank collaborative reviewers for their constructive comments throughout the process of creating this manuscript. Research funding provided by grants from the Natural Sciences and Engineering Council of Canada (NSERC) Discovery program and CEMA-NSERC Collaborative Research and Development grant.
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VanMensel, D., Chaganti, S.R., Boudens, R. et al. Investigating the Microbial Degradation Potential in Oil Sands Fluid Fine Tailings Using Gamma Irradiation: A Metagenomic Perspective. Microb Ecol 74, 362–372 (2017). https://doi.org/10.1007/s00248-017-0953-7
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DOI: https://doi.org/10.1007/s00248-017-0953-7