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Massive dominance of Epsilonproteobacteria in formation waters from a Canadian oil sands reservoir containing severely biodegraded oil

Hubert, Casey R. J., Oldenburg, Thomas B. P., Fustic, Milovan, Gray, Neil D., Larter, Stephen R., Penn, Kevin, Rowan, Arlene K., Seshadri, Rekha, Sherry, Angela, Swainsbury, Richard, Voordouw, Gerrit, Voordouw, Johanna K., Head, Ian M.·2012·Environmental Microbiology
DOI 10.1111/j.1462-2920.2011.02521.xPMC PMC3490369
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Abstract

Summary: The subsurface microbiology of an Athabasca oil sands reservoir in western Canada containing severely biodegraded oil was investigated by combining 16S rRNA gene‐ and polar lipid‐based analyses of reservoir formation water with geochemical analyses of the crude oil and formation water. Biomass was filtered from formation water, DNA was extracted using two different methods, and 16S rRNA gene fragments were amplified with several different primer pairs prior to cloning and sequencing or community fingerprinting by denaturing gradient gel electrophoresis (DGGE). Similar results were obtained irrespective of the DNA extraction method or primers used. Archaeal libraries were dominated by Methanomicrobiales (410 of 414 total sequences formed a dominant phylotype affiliated with a Methanoregula sp.), consistent with the proposed dominant role of CO 2 ‐reducing methanogens in crude oil biodegradation. In two bacterial 16S rRNA clone libraries generated with different primer pairs, > 99% and 100% of the sequences were affiliated with Epsilonproteobacteria ( n = 382 and 72 total clones respectively). This massive dominance of Epsilonproteobacteria sequences was again obtained in a third library (99% of sequences; n = 96 clones) using a third universal bacterial primer pair (inosine‐341f and 1492r). Sequencing of bands from DGGE profiles and intact polar lipid analyses were in accordance with the bacterial clone library results. Epsilonproteobacterial OTUs were affiliated with Sulfuricurvum , Arcobacter and Sulfurospirillum spp. detected in other oil field habitats. The dominant organism revealed by the bacterial libraries (87% of all sequences) is a close relative of Sulfuricurvum kujiense – an organism capable of oxidizing reduced sulfur compounds in crude oil. Geochemical analysis of organic extracts from bitumen at different reservoir depths down to the oil water transition zone of these oil sands indicated active biodegradation of dibenzothiophenes, and stable sulfur isotope ratios for elemental sulfur and sulfate in formation waters were indicative of anaerobic oxidation of sulfur compounds. Microbial desulfurization of crude oil may be an important metabolism for Epsilonproteobacteria indigenous to oil reservoirs with elevated sulfur content and may explain their prevalence in formation waters from highly biodegraded petroleum systems.

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Fig 1 Geographic location of the Athabasca oil sands. Three formation water samples were taken from around the Muskeg River open pit mine site where unconventional heavy oil recovery operations take place. The approximate location of the Pelican Lake oil reservoir where conventional recovery is practised (Grabowski et al., 2005a,b) is also indicated (P).
Fig 1 Geographic location of the Athabasca oil sands. Three formation water samples were taken from around the Muskeg River open pit mine site where unconventional heavy oil recovery operations take place. The approximate location of the Pelican Lake oil reservoir where conventional recovery is practised (Grabowski et al., 2005a,b) is also indicated (P).CC BY · PubMed Central
Fig 2 Denaturing gradient gel electrophoresis of bacterial 16S rRNA gene fragments following two-step nested PCR. Amplification with different universal bacterial primers (indicated above gel lanes; see also Table S1) was followed by a second round of amplification using DGGE primers to create amplicons 233 base pairs in length (including a 40-base-pair GC clamp) for DGGE, as described in the text. Arrows indicate bands from lanes 2–3 and 5–6 that were excised and sequenced. All sequences were closely related to the Sulfuricurvum OTU detected in the bacterial 16S rRNA gene clone libraries.
Fig 2 Denaturing gradient gel electrophoresis of bacterial 16S rRNA gene fragments following two-step nested PCR. Amplification with different universal bacterial primers (indicated above gel lanes; see also Table S1) was followed by a second round of amplification using DGGE primers to create amplicons 233 base pairs in length (including a 40-base-pair GC clamp) for DGGE, as described in the text. Arrows indicate bands from lanes 2–3 and 5–6 that were excised and sequenced. All sequences were closely related to the Sulfuricurvum OTU detected in the bacterial 16S rRNA gene clone libraries.CC BY · PubMed Central
Fig 3 Neighbour joining phylogenetic tree indicating taxonomic affiliations of cloned archaeal 16S rRNA gene sequences from Athabasca oil sands formation waters. For each of the archaeal OTUs the most closely related sequences from GenBank and other related sequences of interest (e.g. from other petroleum reservoirs or methanogenic hydrocarbon-degrading systems) are indicated. Bootstrap values next to branching nodes are based on 100 resamplings.
Fig 3 Neighbour joining phylogenetic tree indicating taxonomic affiliations of cloned archaeal 16S rRNA gene sequences from Athabasca oil sands formation waters. For each of the archaeal OTUs the most closely related sequences from GenBank and other related sequences of interest (e.g. from other petroleum reservoirs or methanogenic hydrocarbon-degrading systems) are indicated. Bootstrap values next to branching nodes are based on 100 resamplings.CC BY · PubMed Central
Fig 4 Neighbour joining phylogenetic tree indicating taxonomic affiliations of cloned bacterial 16S rRNA gene sequences from Athabasca oil sands formation waters. For each of the bacterial OTUs the most closely related sequences from GenBank and other related sequences of interest (e.g. from other petroleum reservoir habitats) are indicated. Bootstrap values next to branching nodes are based on 100 resamplings.
Fig 4 Neighbour joining phylogenetic tree indicating taxonomic affiliations of cloned bacterial 16S rRNA gene sequences from Athabasca oil sands formation waters. For each of the bacterial OTUs the most closely related sequences from GenBank and other related sequences of interest (e.g. from other petroleum reservoir habitats) are indicated. Bootstrap values next to branching nodes are based on 100 resamplings.CC BY · PubMed Central
Fig 5 Concentrations of dibenzothiophenes (the sum of C0–2-alkyl dibenzothiophenes) in crude oil (white squares) and of C0–5-alkyl naphthalenes in crude oil (black circles) as a function of reservoir depth in Athabasca oil sands at the Muskeg River mine. The profiles are indicative of microbial degradation of crude oil compounds catalysed at the oil water transition zone over geological timescales (Head et al., 2003). Formation waters were obtained from dewatering wells penetrating the basal water leg at c. 80 m depth.
Fig 5 Concentrations of dibenzothiophenes (the sum of C0–2-alkyl dibenzothiophenes) in crude oil (white squares) and of C0–5-alkyl naphthalenes in crude oil (black circles) as a function of reservoir depth in Athabasca oil sands at the Muskeg River mine. The profiles are indicative of microbial degradation of crude oil compounds catalysed at the oil water transition zone over geological timescales (Head et al., 2003). Formation waters were obtained from dewatering wells penetrating the basal water leg at c. 80 m depth.CC BY · PubMed Central
Fig 6 Results from 19 published bacterial clone libraries (references are given in B) from subsurface fossil fuel reservoirs were evaluated for the occurrence of dominant taxa. Seven of the habitats were low-temperature environments (reported as < 50°C in situ) as indicated by the dashed line in (A), and 12 were high-temperature oil reservoirs (> 50°C). (A) shows that Epsilonproteobacteria are the third most frequently occurring group overall and were detected in five out of seven low-temperature systems. The abundance of Epsilonproteobacteria in these oil field clone libraries is summarized in (B), which indicates that Epsilonproteobacteria are particularly abundant in low-temperature oil fields in western Canada. The hatched bar indicates the discrepancy in results reported from the Kuji oil storage cavity (Watanabe et al., 2000; 2002) as described in the Introduction.
Fig 6 Results from 19 published bacterial clone libraries (references are given in B) from subsurface fossil fuel reservoirs were evaluated for the occurrence of dominant taxa. Seven of the habitats were low-temperature environments (reported as < 50°C in situ) as indicated by the dashed line in (A), and 12 were high-temperature oil reservoirs (> 50°C). (A) shows that Epsilonproteobacteria are the third most frequently occurring group overall and were detected in five out of seven low-temperature systems. The abundance of Epsilonproteobacteria in these oil field clone libraries is summarized in (B), which indicates that Epsilonproteobacteria are particularly abundant in low-temperature oil fields in western Canada. The hatched bar indicates the discrepancy in results reported from the Kuji oil storage cavity (Watanabe et al., 2000; 2002) as described in the Introduction.CC BY · PubMed Central

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Metadata

Authors
Hubert, C. R. J., Oldenburg, T. B. P., Fustic, M., Gray, N. D., Larter, S. R., Penn, K., Rowan, A. K., Seshadri, R., Sherry, A., Swainsbury, R., Voordouw, G., Voordouw, J. K., & Head, I. M.
Venue
Environmental Microbiology
Publisher
Wiley
Published
2011-08-08
Volume
14
Issue
2
Pages
387-404
ISSN
  • 1462-2912
  • 1462-2920
DOI
10.1111/j.1462-2920.2011.02521.x
PMC
PMC3490369
Cited by
124
References
1
Language
en
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)

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