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The Quantitative Significance of Syntrophaceae and Syntrophic Partnerships in Methanogenic Degradation of Crude Oil Alkanes

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The Quantitative Significance of Syntrophaceae and Syntrophic Partnerships in Methanogenic Degradation of Crude Oil Alkanes Environmental Microbiology (2011) 13(11), 2957–2975 doi:10.1111/j.1462-2920.2011.02570.x The quantitative significance of Syntrophaceae and syntrophic partnerships in methanogenic degradation View metadata, citation and similar papers at core.ac.uk brought to you by CORE of crude oil alkanesemi_2570 2957..2975 provided by PubMed Central N. D. Gray,1* A. Sherry,1 R. J. Grant,1 A. K. Rowan,1 (Methanocalculus spp. from the Methanomicrobi- C. R. J. Hubert,1 C. M. Callbeck,1,3 C. M. Aitken,1 ales). Enrichment of hydrogen-oxidizing methano- D. M. Jones,1 J. J. Adams,2 S. R. Larter1,2 and gens relative to acetoclastic methanogens was I. M. Head1 consistent with syntrophic acetate oxidation mea- 1School of Civil Engineering and Geosciences, sured in methanogenic crude oil degrading enrich- Newcastle University, Newcastle upon Tyne, NE1 7RU, ment cultures. qPCR of the Methanomicrobiales UK. indicated growth characteristics consistent with mea- Departments of 2Geoscience and 3Biological Sciences, sured rates of methane production and growth in University of Calgary, Calgary, Alberta, T2N 1N4, UK. partnership with Smithella. Summary Introduction Libraries of 16S rRNA genes cloned from methano- Methanogenic degradation of pure hydrocarbons and genic oil degrading microcosms amended with North hydrocarbons in crude oil proceeds with stoichiometric Sea crude oil and inoculated with estuarine sediment conversion of individual hydrocarbons to methane and indicated that bacteria from the genera Smithella CO . (Zengler et al., 1999; Anderson and Lovley, 2000; (Deltaproteobacteria, Syntrophaceace) and Marino- 2 Townsend et al., 2003; Siddique et al., 2006; Gieg et al., bacter sp. (Gammaproteobacteria) were enriched 2008; 2010; Jones et al., 2008; Wang et al., 2011). Com- during degradation. Growth yields and doubling parison of methanogenic degradation of crude oil in times (36 days for both Smithella and Marinobacter) estuarine sediment microcosms with patterns of hydrocar- were determined using qPCR and quantitative data on bon removal in degraded petroleum reservoirs has alkanes, which were the predominant hydrocarbons suggested that preferential removal of alkanes in degraded. The growth yield of the Smithella sp. biodegraded petroleum reservoirs is driven by methano- [0.020 g /g ], assuming it utilized all alkanes (cell-C) (alkane-C) genesis and is probably responsible for the formation of removed was consistent with yields of bacteria that the world’s deposits of heavy oil (Jones et al., 2008). It degrade hydrocarbons and other organic compounds has even been proposed that stimulation of in situ metha- in methanogenic consortia. Over 450 days of incuba- nogenic biodegradation of crude oil may be harnessed to tion predominance and exponential growth of Smith- enhance energy recovery from petroleum reservoirs (Gieg ella was coincident with alkane removal and et al., 2008; Jones et al., 2008; Gray et al., 2009; Mbad- exponential accumulation of methane. This growth is inga et al., 2011). From a wider perspective hydrocarbons consistent with Smithella’s occurrence in near are common contaminants of surface and shallow envi- surface anoxic hydrocarbon degrading systems and ronments (Keith and Telliard, 1979; Hippensteel, 1997) their complete oxidation of crude oil alkanes to and in situ methanogenic biodegradation of crude oil is an acetate and/or hydrogen in syntrophic partnership important component of the attenuation of contaminant with methanogens in such systems. The calculated plumes in such environments (Gray et al., 2010). growth yield of the Marinobacter sp., assuming it A meta-analysis of microbial communities in hydrocar- grew on alkanes, was [0.0005 g /g ] suggest- (cell-C) (alkane-C) bon impacted environments has indicated that communi- ing that it played a minor role in alkane degradation. ties in near surface sediments are distinct from those The dominant methanogens were hydrogenotrophs found in deeper warmer petroleum reservoirs (Gray et al., Received 3 February, 2011; accepted 17 July, 2011. *For correspon- 2010; Wang et al., 2011). On this basis the estuarine dence. E-mail [email protected]; Tel. (+44) (0) 191 246 4887; system studied by Jones and colleagues (2008) best rep- Fax (+44) (0) 191 222 6502. resents a model for direct comparison with near surface Re-use of this article is permitted in accordance with the Terms and Conditions set out at http://wileyonlinelibrary.com/ hydrocarbon impacted environments contaminated with onlineopen#OnlineOpen_Terms crude oil. In comparison with pure hydrocarbons, crude © 2011 Society for Applied Microbiology and Blackwell Publishing Ltd 2958 N. D. Gray et al. 686 B A 3.5 Substrate oil 3.0 2.5 450 2.0 BES Inhibited (mmoles) 686 days 4 1.5 response CH 302 1.0 Added standards 22 96 176 0.5 686 days 0 0 200 400 600 800 10 20 30 40 50 60 70 80 Time (days) Time (minutes) Fig. 1. A. Methane production from 300 mg North Sea crude oil added to estuarine sediments incubated under methanogenic conditions in laboratory microcosms (100 ml) for 686 days. The error bars show Ϯ1 ¥ standard error (n = 3). Closed circles indicate methane production from crude oil amended microcosms and open triangles indicate methane production from microcosms, which did not receive crude oil (data previously presented in Jones et al., 2008). Closed squares indicate methane production from crude oil and BES amended microcosms. Arrows indicate sacrificial sampling events at 22, 176, 302, 450 and 686 days. B. Gas chromatograms of total hydrocarbon fractions from the undegraded substrate oil, crude oil amended and crude oil and BES amended microcosms incubated for 686 days. Time 0 on the chromatograms, which are displayed from 5 to 80 min, corresponds to injection. oils contain a complex mixture of chemicals including Denaturing gradient gel electrophoresis (DGGE) refractory and or toxic components in addition to degrad- analysis of bacterial and archaeal communities able hydrocarbons. This complexity is likely to influence Denaturing gradient gel electrophoresis analysis of the the activity and selection of alkane degrading microorgan- microbial communities in replicate microcosms over time isms enriched on crude oil. Here we have determined the demonstrated reproducible changes associated with deg- relative importance of different organisms potentially radation of the crude oil and methane formation relative to involved in methanogenic crude oil degradation in surface control microcosms with no oil added. There was a high sediments by quantification of their growth in relation to degree of similarity in the DGGE profiles of communities methane production and removal of crude oil alkanes. from replicate microcosms that were sacrificially sampled at different time points (Table 1). On day 22 there was no Results significant difference in the bacterial or archaeal commu- nity profiles between treatments; whereas, at 302 and 686 Methanogenic oil degradation days there were statistically significant differences Oil conversion to methane in oil degrading microcosms between treatments in both the bacterial and archaeal inoculated with estuarine sediment and amended with communities (Table 1, Fig. S1). North Sea oil was confirmed by comparison of methane yields and oil alterations in oil amended, unamended and Bacterial and archaeal community composition in (BES) inhibited control microcosms (Fig. 1). Methano- Tyne sediment inoculum genic oil degradation was characterized by an apparent 200 day lag phase (Fig. 1A). Methane production corre- More detailed bacterial community analysis was con- lated stoichiometrically with the removal of alkanes (nC7- ducted on microcosm samples from day 22, 302 and 686 nC34) (Jones et al., 2008, Fig. 1B). Furthermore, near using 16S rRNA gene clone libraries (see Fig. 2 legend for complete degradation of alkanes occurred before any sig- individual library sizes). Clone libraries for individual nificant removal of aromatic hydrocarbon (Jones et al., samples were prepared on the basis that there was high 2008). Microcosms sacrificially sampled after 0, 22, 176, similarity between DGGE profiles from replicate samples 302, 450 and 686 days for analysis of residual crude oil and therefore individual samples were considered to be were also used for analysis of the microbial communities representative. 16S rRNA sequences from the sediment present. microcosms were classified using the RDP Naïve Baye- © 2011 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 13, 2957–2975 Syntrophaceae in methanogenic oil degrading consortia 2959 Table 1. Average similarity between bacterial and archaeal DGGE profiles from methanogenic microcosms. Bacterial profiles Archaeal profiles Similarity within Similarity between oil Similarity within Similarity between oil Time (days) replicates and no-oil treatments replicates and no-oil treatments 22 84.7 Ϯ 5.1 79.4 Ϯ 4.5 80.8 Ϯ 5.0 75.1 Ϯ 4.1 302 79.1 Ϯ 7.2* 32.7 Ϯ 4.7* 73.3 Ϯ 3.4* 57.3 Ϯ 1.1* 686 72.8 Ϯ 1.6* 36.9 Ϯ 5.8* 81.1 Ϯ 3.8* 40.3 Ϯ 3.8* The asterisk indicates a statistically significant difference between oil treated and untreated samples (t-test P < 0.05). sian rRNA Classifier (Wang et al., 2007). Samples taken grove and cold seep sediments as well as sequences on day 22 and from the sediment inoculum were com- recovered from anaerobic sludges and soil (data not pared using the RDP library compare tool and were found shown). A number of these bacterial or archaeal not to be significantly different for the bacterial or archaeal sequences were
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