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Biodegradation of Short-Chain n-Alkanes in Oil Sands Tailings under Methanogenic Conditions

Biodegradation of Short-Chain n -Alkanes in Oil Sands Tailings under Methanogenic Conditions

T A R I Q S I D D I Q U E ,P H I L L I P M .F E D O R A K ,A N D J U L I A M .F O G H T *

Department of Biological Sciences,University of Alberta,Edmonton,Alberta T6G 2E9,Canada

The biodegradation of a mixture of low molecular weight n -alkanes (C 6,C 7,C 8,and C 10)was assessed under

methanogenic conditions using mature fine tailings (MFT)produced by the oil sands industry in Alberta,Canada.Microorganisms present in the MFT mineralized the added n -alkane mixture,producing 16.2((0.3)or 20.5((0.1)mmol of methane in the headspace of microcosms spiked with 0.2%or 0.5%w/v n -alkanes,respectively,during 29weeks of incubation.The spiked n -alkanes biodegraded in the sequence C 10>C 8>C 7>C 6.Degradation of 100%C 10,97%C 8,74%C 7,and 44%C 6occurred in a mixture of n -alkanes in the MFT spiked at 0.2%after 25weeks of incubation.The same pattern of biodegradation was also observed in the MFT spiked with 0.5%n -alkanes.

Stoichiometric calculations confirmed the mineralization of the degraded n -alkanes to methane.This study showed that the short-chain n -alkanes,which comprise a

significant portion of the unrecovered naphtha used in bitumen extraction and released into the settling basins,can be biodegraded into methane.These findings may influence decisions regarding extraction processes and long-term management of MFT,and they suggest that intrinsic,methanogenic metabolism of these n-alkanes may occur in other anoxic environments.

Introduction

Enormous volumes of tailings are produced during the recovery of bitumen from Alberta oils sands.In 2005,total production of crude bitumen reached 1million barrels per day,accounting for 50%of Canadian oil production (Ca-nadian Association of Petroleum Producers,https://www.wendangku.net/doc/8013140554.html,/wiki/Athabasca ?Tar ?Sands),and it is estimated that by 2015Canadian oil production may reach 4million barrels per day.With the extraction of 1m 3of oil sands,about 4m 3of tailings waste comprising a slurry of alkaline water,sand,silt,clay,and bitumen is produced (1).Oil sands tailings produced by Syncrude Canada Ltd.contain not only residual bitumen but also a fraction of the organic diluent used in oil extraction processes.The diluents may be naphtha (used by Syncrude)or a mixture of pentanes and hexanes (C 5and C 6)(used by Albian Sands Energy,Inc.).After bitumen extraction,tailings are pumped into tailings ponds or settling basins where the sand fraction settles,and most of the aqueous slurry of fines (silts and clays plus residual hydro-carbon)slowly densifies to a suspension called mature fine tailings (MFT).It was estimated that 315000tonnes of tailings

per day were pumped into the Mildred Lake Settling Basin (MLSB),Fort McMurry,Alberta,by Syncrude (2)over a period of more than 25years.

Biodegradation of the residual hydrocarbons and den-sification of MFT are important factors in the long-term management of oil sands tailings.Recently,MLSB,which was a primary tailings pond for Syncrude,began to evolve methane gas,releasing an estimated 108L of methane per day (3).Because MLSB first became methanogenic in the area receiving diluent-enriched tailings,we hypothesized that a suite of anaerobic bacteria in MLSB utilize the lighter hydrocarbons from the diluent (naphtha)used in the extraction process and thereby support methanogenesis by providing hydrocarbon metabolites to the methanogenic consortium.Recently,Fedorak et al.(1)reported an unex-pected increase in the rate of densification of MFT ac-companying the microbially mediated production of methane (CH 4).Therefore,it is important to determine the source of biogenic gases evolved from MFT because this may lead to engineered options to enhance densification,reduce MFT inventories,and improve reclamation options.Assessing and understanding the role of naphtha inputs on maintaining methanogenesis would be useful in developing strategies for future tailings management decisions.

The naphtha used by Syncrude Ltd.Canada (CAS No.64742-49-0)is a mixture of aliphatic and aromatic compounds (C 3-C 14)containing a significant portion of n -alkanes (hep-tane (C 7),1-5%by wt;octane (C 8),5-10%by wt;nonane (C 9),1-5%by wt)in addition to benzene,toluene,ethyl-benzene,and xylenes (BTEX)compounds.Biodegradability of alkanes has been studied extensively under aerobic conditions (4-9),but less is known about their biodegrada-tion in anoxic environments.Rueter et al.(10)demonstrated that hydrocarbons in crude oil were used directly by sulfate-reducing bacteria growing under strictly anoxic conditions.A moderately thermophilic pure culture isolated from the sediment of the Guaymas Basin (Gulf of California,Mexico)utilized alkanes in oil during sulfate reduction (10).Massias et al.(11)studied in situ anaerobic degradation of petroleum alkanes in marine sediments and reported significant (>50%)depletion of C 17,C 18,and C 30after 24months of incubation.There are other reports of anaerobic alkane degradation under sulfate-reducing (12-14)and denitrifying,iron-reduc-ing,and methanogenic conditions (12,15-17),but attention has been focused on monitoring the degradation of long-chain n -alkanes (g C 12).In most cases,the fate of a single compound has been studied as a model to elucidate the metabolic pathway,and if more than one compound was used,then biodegradation of each compound was assessed in individual microcosms (12)rather than investigating their biodegradation in a mixture of compounds,which would be more realistic.

In the present study,anaerobic degradation of low molecular weight n -alkanes (C 6,C 7,C 8,and C 10)added collectively to the MFT was assessed for its contribution to methanogenesis.Stoichiometric calculations were performed to evaluate the complete mineralization of the added n -alkanes to methane.We observed a unique pattern of degradation among the spiked n -alkanes.This is the first demonstration that short-chain n -alkanes can support methanogenesis in MFT and thereby contribute to the CH 4flux from the oil sands tailings ponds.

Experimental Section

Chemicals.n -Octane (C 8;>99%pure)and n -decane (C 10;>99%pure)were purchased from Sigma-Aldrich,Oakville,

*Corresponding author phone:(780)492-3279;fax:(780)492-9234;e-mail:julia.foght@ualberta.ca.

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Ontario,Canada.n-Heptane(C7;>99%pure)was from Caledon Laboratories Ltd.,Georgetown,Ontario,Canada. n-Hexane(C6;>99%pure),methanol(HPLC grade),and other chemicals(analytical reagent grade)were purchased from Fisher Scientific,Ontario,Canada.

Description of the Mature Fine Tailings.Fresh MFT(a slurry with61%moisture content)was collected by Syncrude Canada Ltd.from MLSB at6m depth in July2005.EnviroTest Laboratories,Edmonton,Canada,analyzed the MFT(Table 1)for aliphatic hydrocarbons(Canadian Council of Min-isters of the Environment,2001;https://www.wendangku.net/doc/8013140554.html,me.ca/assets/ pdf/final_phc_method_rvsd_e.pdf),BTEX compounds(EPA 5030/8260-P&T GC-MS;https://www.wendangku.net/doc/8013140554.html,/epahome/ index/),and polycyclic aromatic hydrocarbons(PAHs)and alkylated PAHs(EPA3540/8270-GC/MS;http://www. https://www.wendangku.net/doc/8013140554.html,/epahome/index/).The MFT was stored at4°C for use in the experiments.

Mineralization of Added n-Alkanes(C6,C7,C8,and C10). This experiment was conducted in158mL microcosms with 50mL of MFT and50mL of methanogenic medium,sealed with butyl rubber stoppers.Methanogenic medium was prepared using inorganic salts,vitamins,a redox indicator (resazurin),and a reducing agent(sulfide),as described by Fedorak and Hrudey(18).The headspace in the microcosms was flushed with O2-free30%CO2balance N2,at atmospheric pressure.Before being amended with any carbon source (hydrocarbons or acetate),microcosms were preincubated at22°C for2weeks in the dark to allow for the activation and growth of a methanogenic community and the reduction of alternative electron acceptors in the MFT(19).Each microcosm was then flushed with O2-free30%CO2balance N2gas to remove any CH4produced during the preincubation period.A mixture of n-alkanes(n-hexane(C6)2.89mL,specific gravity0.66;n-heptane(C7)2.74mL,specifiic gravity0.68; n-octane(C8)2.72mL,specific gravity0.7;n-decane(C10) 2.58mL,specific gravity0.73)was prepared,and0.29or0.72 mL of the mixture was then added to the microcosms to give final concentrations of0.2%or0.5%w/v of total n-alkanes, respectively.The microcosms were prepared in triplicate.In addition to these treatments,sodium acetate(～1400mg L-1) was added to some microcosms containing0.5%n-alkanes. Parallel heat-killed sterilized controls were prepared in the same manner as the experimental cultures and autoclaved four times on four consecutive days.Two types of viable controls were also included:a baseline control consisting of unamended MFT to account for any methane production from indigenous substrates in the MFT and a positive control amended with acetate but no alkanes.All microcosms were incubated at22°C(ca.in situ temperature in MLSB near the source of the MFT)in the dark without shaking.Samples were withdrawn periodically for chemical analyses.

Chemical Analyses.Methane production in the micro-cosms was measured by removing0.1mL of headspace from each microcosm and analyzing by gas chromatography with a flame ionization detector(GC-FID)(3).While the methane concentration in the headspace was monitored over time,a measured volume of headspace was removed from the microcosms periodically to release the very high pressure produced by methane production during alkane degradation and replaced by a measured volume of30%CO2balance N2, using a sterile needle and syringe.The volumes of gases removed and replenished were accounted for when calcu-lating the total mass of methane produced in the microcosms.

For acetate analysis,0.1mL samples drawn from the microcosms were centrifuged in a microcentrifuge(Eppen-dorf5415D),then80μL of the supernatant was mixed with 10μL of4N phosphoric acid plus10μL of propionic acid solution(1500mg L-1)as an internal standard and analyzed by GC-FID(20).

Residual alkanes were analyzed using a GC-FID equipped with a purge and trap system.One milliliter of MFT sampled from the experimental microcosms was shaken for30min at room temperature with10mL of methanol in a20mL EPA glass vial capped with a Teflon-coated septum.Vials were stored at4°C for30min to allow the sediment particles to settle.Two milliliters of supernatant were then transferred to a44mL Teflon-sealed EPA glass vial(Fisher Scientific, catalog no.03-339-14C)and filled completely with deionized water to avoid any headspace.Vials were sonicated for2min in a bath sonicator to mix the solution and put on an autosampler for analyses of alkanes(C6-C10)on a Hewlett-Packard model HP6890GC-FID equipped with purge and trap system.The line temperature in the purge and trap system was set at180°C.Analytes were desorbed at225°C for4min and then heated at225°C for10min before passing to the GC.The capillary column used was a30m DB-1with 0.53mm internal diameter and1.50μm film thickness(J&W Scientific/Agilent Technologies).The front inlet tempera-ture was maintained at200°C with a split ratio of50:1.The column was initially held at36°C for4min and was then increased at15.0°C min-1to350°C.Helium was used as a carrier gas with a flow rate of7.4mL min-1.The FID was kept at250°C.

Stoichiometry of n-Alkane Mineralization.After quan-tification of the methane and alkane concentrations in the microcosms by GC analysis,theoretical calculations were

TABLE1.Characteristics of Mature Fine Tailings Used in the Experiment

General Characteristics

solids(%by weight)39.5 bitumen(%by weight) 4.4 naphtha(%by weight)0.4 pH7.8 conductivity(μS cm-1)4200 alkalinity(as ppm of CaCO3)1570 Aliphatic Hydrocarbons(mg kg-1(Dry Weight))

C8-C10160

C10-C12480

C12-C163400

C16-C216000

BTEX(mg kg-1(Dry Weight))

benzene0.26 toluene0.35 ethylbenzene13

o-,m-and p-xylenes12 Polycyclic Aromatic Compounds(mg kg-1(Dry Weight)) naphthalene<0.5

C2-naphthalenes a0.8

C3-naphthalenes7.3

C4-naphthalenes15

C1-fluorenes 2.0

C2-fluorenes 6.9 dibenzothiophene0.8

C1-dibenzothiophenes 5.6

C2-dibenzothiophenes17

C3-dibenzothiophenes23

C4-dibenzothiophenes22 phenanthrene 2.4

C1-phenanthrenes or-anthracenes12

C2-phenanthrenes or-anthracenes18

C3-phenanthrenes or-anthracenes19

C4-phenanthrenes or-anthracenes10 pyrene0.7

C1-fluoranthenes or-pyrenes 3.2

C1-benzo[b/k]fluoranthenes or-benzo[a]pyrenes 2.2

C2-benzo[b/k]fluoranthenes or-benzo[a]pyrenes0.9

C1-benzo[a]anthracenes or-chrysenes 2.9

C2-benzo[a]anthracenes or-chrysenes 4.9

a Where C n refers to n alkyl carbon substitutions on the parent polycyclic aromatic compound.

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made to compare the actual and predicted values of methane production upon the mineralization of known amounts of n-alkanes.Calculations were based on the following stoi-chiometric equations derived from the Symons and Buswell equation(21),which describe the complete oxidation of n-alkanes and acetate to CO2and CH4under methanogenic conditions

Results

Methane Production.Methane production was monitored as a quantitative indicator of anaerobic microbial metabolism of n-alkanes in the MFT.Figure1shows the time course of cumulative methanogenesis with and without the addition of n-alkanes.After29weeks of incubation,amendment with alkanes yielded a high amount of methane,with16.2((0.3) or20.5((0.1)mmol produced in the microcosms spiked with0.2%or0.5%w/v n-alkanes,respectively(Figure1).In the acetate-amended microcosms, 1.9((0.03)mmol of methane was observed by6weeks of incubation,which slightly increased to2.8((0.02)mmol by week29.Autoclaved microcosms did not produce any methane(not shown).Only 0.26((0.02)mmol of methane was recorded in the live unamended MFT(baseline control)after29weeks of incubation.Methane production in all replicate cultures amended with alkanes started within the first week(Figure 1,inset).A slight delay in methane formation was observed in the microcosms spiked with the higher concentration (0.5%)of alkanes compared with methane produced in0.2% alkane-amended microcosms(Figure1,inset).Initially,the addition of0.5%alkanes to acetate-amended microcosms also reduced methane production(Figure1,inset)with significantly lower average methane yields(t-test;P)0.0024) from acetate plus0.5%alkane than acetate-amended MFT at week5.However,the amounts of methane produced in the acetate-amended microcosms were the same by week9, with or without0.5%alkanes.After a plateau of3weeks, methane started increasing again in the microcosms with 0.5%alkanes plus acetate,and17.6((0.2)mmol of methane was measured after29weeks of incubation(Figure1).

Acetate Consumption.Acetate was added(as a positive control)to the MFT with and without n-alkanes to determine the methanogenic potential of MFT.Depletion of acetate over10weeks of incubation is shown in Figure2.In the acetate-amended microcosms that initially contained1450 ((15)mg acetate L-1,all acetate was consumed during5 weeks of incubation.The presence of0.5%alkanes in acetate-amended microcosms delayed acetate consumption,with 540((48)mg acetate L-1(ca.37%)remaining at week5. Acetate was depleted faster in the microcosms without n-alkanes than in those with n-alkanes.This is consistent with the faster production of methane in the acetate-amended microcosms without n-alkanes(Figure1,inset). No significant acetate depletion was noted in the sterile acetate-amended controls during the incubation period (Figure2).

n-Alkane Biodegradation.The concentrations of residual n-alkanes recovered after25weeks of incubation from the heat-killed and live microcosms were used to calculate the percentage biodegradation of individual alkanes in each culture(Figure3).In all the treatments,no significant change in the concentrations of the added n-alkanes in the MFT could be detected during the first5weeks of incubation. n-Decane(C10)was the first alkane to be depleted,with the concentration at10weeks dropping from800((14)to370 ((21)mg L-1and from1900((220)to1440((140)mg L-1 in the microcosms spiked with0.2%and0.5%w/v of total n-alkanes,respectively.Concentrations of other n-alkanes (C6,C7,and C8)were not significantly changed during10 weeks of incubation.The biodegradation pattern for the n-alkanes became clear with analysis performed after20 weeks of incubation,when significant degradation of all four n-alkanes(C6,C7,C8,and C10)was observed in live cultures. The higher molecular weight alkanes in the mixture were preferentially metabolized by the microbial populations in the MFT.In the25week analysis,no C10was detected in microcosms spiked with0.2%n-alkanes whereas a small amount of C8(25(2.0mg L-1),210((32)mg L-1of C7,and 290((23)mg L-1of C6were detected,compared to

FIGURE1.Methane production in microcosms containing MFT amended with n-alkanes(C6,C7,C8,and C10)with or without acetate, during29weeks of incubation at22°C:(b)unamended live tailings, ([)acetate-amended tailings,(2)0.2%C6-C10spiked tailings,(/) 0.5%C6-C10spiked tailings,(9)0.5%C6-C10+acetate-amended tailings.Symbols represent the mean from analysis of triplicate microcosms,and error bars(where visible)represent1standard deviation.Inset shows methane production during the first10weeks of incubation.

n-hexane C6H14+2.5H2O f1.25CO2+4.75CH4(1) n-heptane C7H16+3.0H2O f1.50CO2+5.50CH4(2) n-octane C8H18+3.5H2O f1.75CO2+6.25CH4(3) n-decane C10H22+4.5H2O f2.25CO2+7.75CH4(4) acetate CH3COO-+H2O f HCO3-+CH4(5)

FIGURE2.Acetate concentrations in MFT amended with acetate with or without C6-C10during10weeks of incubation:(b)heat-killed MFT,([)microcosms amended with acetate only,(9) microcosms amended with0.5%C6-C10plus acetate.Symbols represent the mean from analysis of triplicate microcosms,and error bars(where visible)represent1standard deviation.

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concentrations of 760((35),990((69),810((56),and 570((39)mg L -1,respectively,in heat-killed controls.GC analyses of the heat-killed alkane-amended microcosms revealed that 82-105%of the spiked C 6-C 10were still present in the microcosms after 25weeks of incubation.The same trend of alkane degradation was also observed in the other treatments (0.5%alkanes and 0.5%alkanes plus acetate-amended microcosms)(Figure 3),although alkane degrada-tion was delayed in the 0.5%alkane-amended microcosms containing acetate compared with those containing only 0.5%alkanes.

Stoichiometries.The mass of individual alkanes con-sumed (quantified by GC)during incubation was fit into the respective stoichiometric equation (eqs 1-5)to estimate maximum theoretical methane production resulting from complete mineralization of the added n -alkanes.Results are presented in Table 2.In the microcosms spiked with 0.2%n -alkanes,slightly more CH 4was measured in the headspace than was predicted by the stoichiometric equations.In the treatments where a higher concentration of n -alkanes (0.5%)was present,with and without acetate amendment,less methane was measured for 0.5%and 0.5%plus acetate-amended microcosms than the predicted values.

Discussion

Although anaerobic biodegradation of hydrocarbons has been reported and is now accepted as a significant process in natural environments (10,22-23),relatively little is known about the prevalence of this process.We studied the biodegradation of low molecular weight n -alkanes in oil sands tailings under methanogenic conditions.Currently,there are three oil sands extraction plants in northeastern Alberta,and tailings ponds at each site are methanogenic.The onset of methanogenesis in an oil sands tailings pond requires the depletion of sulfate (which originates from oil sands ore during the extraction process)from the tailings,and suitable carbon sources.Holowenko et al.(3)demonstrated that sulfate concentrations in MFT decreased with depth in the MLSB,which equates to age of deposition in the basin.Sulfate-reducing bacteria and methanogens were detected at each sample depth,and the numbers of methanogens often exceeded the numbers of sulfate-reducing bacteria in samples with depleted sulfate concentrations (3).Thus,over time,microbial activity has depleted sulfate,creating condi-tions that are suitable for methanogenesis.

The carbon sources for sulfate reduction or methano-genesis in the tailings ponds were unknown.The major organic material in the oil sands tailing is bitumen which escapes during the extraction process and comprises ap-proximately 2-5%of the weight of MFT (24)and contains insoluble and complex asphaltenes.Due to its high molecular weight,bitumen is unlikely to undergo rapid biodegradation to contribute to methanogenesis in the short term.Holo-wenko (25)amended MFT samples with increasing con-centrations of bitumen and incubated for nearly 250days under methanogenic conditions but did not detect any enhanced methane production in bitumen-amended mi-crocosms.Table 1shows substantial amounts of some potential substrates (aliphatic hydrocarbons;C 12-C 21)in MFT,but their quantities resulted in only a small amount of methane production in unamended microcosms during the incubation period (Figure 1).

The biodegradation of various n -alkanes (13,26-27)and alicyclic hydrocarbons (28)under sulfate-reducing conditions has been demonstrated,and these may also serve as electron donors to drive MFT methanogenesis,as n -hexadecane (16)and the n -alkanes in crude oil (26)can be biodegraded to yield methane.In the present study,biodegradation of a mixture of short-chain n -alkanes in MFT under methanogenic conditions started producing methane in the microcosms

FIGURE 3.Biodegradation of n -alkanes (C 6,C 7,C 8,and C 10)in microcosms amended with 0.2%,0.5%,or 0.5%n -alkanes plus acetate during 25weeks of incubation at 22°C.Bars represent the mean from analysis of triplicate microcosms,and error bars (where visible)represent 1standard deviation.

TABLE 2.Predicted and Measured Methane Production in Mature Fine Tailings with Degradation of n -Alkanes after 25Weeks of Incubation

treatment

substrate consumed (mmol)

theoretical CH 4

production a (mmol)

measured CH 4

production (mmol)

percent of theoretical production 0.2%C 6-C 10C 6)0.2611.3((0.2)12.9((0.1)

114

C 7)0.48C 8)0.67C 10)0.42

0.5%C 6-C 10C 6)0.3718.7((0.8)14.4((0.1)

C 7)0.49C 8)1.16C 10)0.91

0.5%C 6-C 10C 6)0.3314.7((0.8)11.6((0.2)79

+acetate C 7)0.34

C 8)0.49C 10)0.81acetate )1.95

Based on eqs 1-5and on GC quantitation of alkane concentrations.Values represent the mean from analysis of triplicate microcosms ((1standard deviation).

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within one week of amendment.In contrast,consortia derived from a marine-estuarine site heavily polluted with petroleum products were incubated under four different anaerobic conditions(12);there was no methanogenic activity in the enrichment culture amended with octane for more than13 weeks whereas in the decane-spiked culture methanogenic activity began in3-8weeks(12).Therefore,we assume that the MFT is already acclimated to utilization of n-alkanes as a methanogenic substrate.Branched and cyclic alkanes, which might also be present in the MFT,would be far less abundant than the spiked n-alkanes.Thus,only the degra-dation of the n-alkanes was followed in the current study.

Substantial methane production in the n-alkane-amended microcosms(Figure1)indicates that the alkanes were readily metabolized by anaerobes in the MFT.Similar results have been reported in other studies but for longer-chain n-alkanes. For example,in crude-oil-amended methanogenic incu-bations,endogenous electron donors resulted in evolution of314μmol of methane over475days of incubation,with the complete removal of the n-alkane fraction of crude oil (C13-C34)in13months by the microorganisms from an anoxic aquifer previously contaminated by natural gas condensate (26).Salminen et al.(29)studied the anaerobic biodegradation of mineral oil in boreal subsurface soil and observed methane production with removal of n-alkanes(C11-C15)during mineral oil degradation.

In the acetate-amended MFT where n-alkanes were also added,initially methane production was observed with the metabolism of acetate.After the consumption of acetate,no further increase in the methane production was noted for almost3weeks,after which methanogenesis resumed, presumably utilizing the added n-alkanes.This rise in methane after a short lag period may be due to a shift in species dominance after acetate exhaustion to permit metabolism of n-alkanes,a less-preferred substrate.Forma-tion of methane by the resident microflora in the MFT is supported by the work of Penner(30)who reported the presence of active microbial populations in MFT and identified various bacterial and archaeal species potentially in syntrophic relationships involved in methanogenesis in MLSB.

Methane production due to n-alkane metabolism in the MFT is consistent with the loss of n-alkanes quantified by GC analyses and agrees with the work of Townsend et al.(26) who reported that the n-alkane fraction of crude oil (C13-C34)was consumed under methanogenic conditions in anoxic aquifer samples.Massias et al.(11)studied in situ anaerobic degradation of petroleum alkanes in marine sediments and found a marked decrease in alkanes(e C25) after24months.In the present study,it is interesting that the highest molecular weight compound(C10)started disap-pearing first and supported methanogenesis.The spiked n-alkanes biodegraded selectively depending on the length of their C-chains in the sequence C10>C8>C7>C6. Degradation of100%C10,97%C8,74%C7,and49%C6in a mixture of n-alkanes in the MFT spiked at0.2%during25 weeks of incubation revealed a definite pattern of biodeg-radation.This preferential degradation among spiked n-alkanes may be attributed either to their octanol/water partition coefficients(P ow)which increase with increasing chain length(P ow for C6)3.9,C7)4.66,C8)5.18,C10)5.98; International Program on Chemical Safety,2004,http:// https://www.wendangku.net/doc/8013140554.html,/public/english/protection/safework/cis/prod-ucts/icsc/dtasht/)or to selective uptake across cell mem-branes of the n-alkane-degrading microorganisms as pro-posed by Kim et al.(31).This sequence of biodegradation is in contrast to the sequence observed by Davidova et al.(27) who studied the biodegradation of C6-C12n-alkanes under sulfate-reducing conditions.They reported rates of degrada-tion that were C6>C10>C12.Some studies have shown that

short-chain n-alkanes tend to be removed faster than longer-chain n-alkanes,the latter being removed faster than branched hydrocarbons(32-34),but still there is some debate on the exact order in which different compounds are removed during biodegradation.

In general,there is good agreement between the measured and the predicted methane yields based on the stoichiometric conversion of the n-alkanes(Table2).The reason for slightly greater than expected methane production in the microcosms with0.2%n-alkanes cannot be explained.However,the methane production values(77%and79%of predicted)from the other two amendments(0.5%n-alkanes and0.5% n-alkanes plus acetate)agree with findings of earlier inves-tigators.For example,in studies of benzene biodegradation by methanogenic consortia,Kazumi et al.(35)reported73% of the predicted methane production,and Weiner and Lovley (36)found80%of the predicted methane production.Of course,eqs1-5do not account for carbon assimilation into biomass involved with the biodegradation of substrates.In addition,the methanogenic biodegradation of hydrocarbons depends on a consortium of anaerobic bacteria,and the overall methane yield will depend on the efficiency of interspecies H2transfer.

Two of the oil sands plants use naphtha(containing some short-chain alkanes),and the third plant uses a mixture of C5-and C6-alkanes to recover bitumen from oil sands ores. The results of this study show that the microbial communities in the MFT are capable of utilizing the added C6-C10n-alkanes under methanogenic conditions and support the hypothesis that components of unrecovered naphtha in oil sands tailings can sustain the methanogenesis in the settling basins.This would explain the evolution of significant volumes of methane from oil sands tailings and has implications for the manage-ment of those wastes regarding future densification of MFT and emission of greenhouse gases.We are currently evaluat-ing the contribution of BTEX components in naphtha and of whole naphtha to methanogenesis to expand this obser-vation.Our study extends observations of anaerobic bio-degradation of alkanes to the mineralization of a mixture of short-chain n-alkanes under methanogenic conditions.In addition,it is quite conceivable that these compounds may support methanogenesis in other anaerobic environments, such as petroleum-contaminated aquifers and petroleum reservoirs.Finally,this is the first report that describes the sequential methanogenic biodegradation of n-alkanes in order of their decreasing molecular weights. Acknowledgments

The authors gratefully acknowledge funding from the Natural Sciences and Engineering Research Council of Canada (Postdoctoral Fellowship to T.S.),Syncrude Canada Ltd.,and Canadian Natural Resources Ltd.We particularly thank Mike MacKinnon(Syncrude)for his assistance in establishing this research program,helpful discussions,and providing samples. Thanks to Jela Burkus(Civil and Environmental Engineering, University of Alberta)for assistance with GC-FID purge and trap analysis and Debbi Coy for technical advice. Literature Cited

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