Genome-Resolved Metagenomic Analysis Reveals Roles for Candidate Phyla and Other Microbial Community Members in Biogeochemical Transformations in Oil Reservoirs
Abstract
ABSTRACT Oil reservoirs are major sites of methane production and carbon turnover, processes with significant impacts on energy resources and global biogeochemical cycles. We applied a cultivation-independent genomic approach to define microbial community membership and predict roles for specific organisms in biogeochemical transformations in Alaska North Slope oil fields. Produced water samples were collected from six locations between 1,128 m (24 to 27°C) and 2,743 m (80 to 83°C) below the surface. Microbial community complexity decreased with increasing temperature, and the potential to degrade hydrocarbon compounds was most prevalent in the lower-temperature reservoirs. Sulfate availability, rather than sulfate reduction potential, seems to be the limiting factor for sulfide production in some of the reservoirs under investigation. Most microorganisms in the intermediate- and higher-temperature samples were related to previously studied methanogenic and nonmethanogenic archaea and thermophilic bacteria, but one candidate phylum bacterium, a member of theAcetothermia(OP1), was present in Kuparuk sample K3. The greatest numbers of candidate phyla were recovered from the mesothermic reservoir samples SB1 and SB2. We reconstructed a nearly complete genome for an organism from the candidate phylumParcubacteria(OD1) that was abundant in sample SB1. Consistent with prior findings for members of this lineage, the OD1 genome is small, and metabolicmore »
- Authors:
-
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Dept. of Ecology, Climate and Ecosystem Sciences Division
- Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Sciences
- Univ. of Texas, Austin, Port Aransas, TX (United States). Dept. of Marine Science, Marine Science Institute
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1256078
- Alternate Identifier(s):
- OSTI ID: 1379039
- Grant/Contract Number:
- AC02- 05CH11231; SC0004918; AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Hu, Ping, Tom, Lauren, Singh, Andrea, Thomas, Brian C., Baker, Brett J., Piceno, Yvette M., Andersen, Gary L., and Banfield, Jillian F. Genome-Resolved Metagenomic Analysis Reveals Roles for Candidate Phyla and Other Microbial Community Members in Biogeochemical Transformations in Oil Reservoirs. United States: N. p., 2016.
Web. doi:10.1128/mbio.01669-15.
Hu, Ping, Tom, Lauren, Singh, Andrea, Thomas, Brian C., Baker, Brett J., Piceno, Yvette M., Andersen, Gary L., & Banfield, Jillian F. Genome-Resolved Metagenomic Analysis Reveals Roles for Candidate Phyla and Other Microbial Community Members in Biogeochemical Transformations in Oil Reservoirs. United States. https://doi.org/10.1128/mbio.01669-15
Hu, Ping, Tom, Lauren, Singh, Andrea, Thomas, Brian C., Baker, Brett J., Piceno, Yvette M., Andersen, Gary L., and Banfield, Jillian F. Tue .
"Genome-Resolved Metagenomic Analysis Reveals Roles for Candidate Phyla and Other Microbial Community Members in Biogeochemical Transformations in Oil Reservoirs". United States. https://doi.org/10.1128/mbio.01669-15. https://www.osti.gov/servlets/purl/1256078.
@article{osti_1256078,
title = {Genome-Resolved Metagenomic Analysis Reveals Roles for Candidate Phyla and Other Microbial Community Members in Biogeochemical Transformations in Oil Reservoirs},
author = {Hu, Ping and Tom, Lauren and Singh, Andrea and Thomas, Brian C. and Baker, Brett J. and Piceno, Yvette M. and Andersen, Gary L. and Banfield, Jillian F.},
abstractNote = {ABSTRACT Oil reservoirs are major sites of methane production and carbon turnover, processes with significant impacts on energy resources and global biogeochemical cycles. We applied a cultivation-independent genomic approach to define microbial community membership and predict roles for specific organisms in biogeochemical transformations in Alaska North Slope oil fields. Produced water samples were collected from six locations between 1,128 m (24 to 27°C) and 2,743 m (80 to 83°C) below the surface. Microbial community complexity decreased with increasing temperature, and the potential to degrade hydrocarbon compounds was most prevalent in the lower-temperature reservoirs. Sulfate availability, rather than sulfate reduction potential, seems to be the limiting factor for sulfide production in some of the reservoirs under investigation. Most microorganisms in the intermediate- and higher-temperature samples were related to previously studied methanogenic and nonmethanogenic archaea and thermophilic bacteria, but one candidate phylum bacterium, a member of theAcetothermia(OP1), was present in Kuparuk sample K3. The greatest numbers of candidate phyla were recovered from the mesothermic reservoir samples SB1 and SB2. We reconstructed a nearly complete genome for an organism from the candidate phylumParcubacteria(OD1) that was abundant in sample SB1. Consistent with prior findings for members of this lineage, the OD1 genome is small, and metabolic predictions support an obligately anaerobic, fermentation-based lifestyle. At moderate abundance in samples SB1 and SB2 were members of bacteria from other candidate phyla, includingMicrogenomates(OP11),Atribacteria(OP9), candidate phyla TA06 and WS6, andMarinimicrobia(SAR406). The results presented here elucidate potential roles of organisms in oil reservoir biological processes. IMPORTANCEThe activities of microorganisms in oil reservoirs impact petroleum resource quality and the global carbon cycle. We show that bacteria belonging to candidate phyla are present in some oil reservoirs and provide the first insights into their potential roles in biogeochemical processes based on several nearly complete genomes.},
doi = {10.1128/mbio.01669-15},
journal = {mBio (Online)},
number = 1,
volume = 7,
place = {United States},
year = {Tue Jan 19 00:00:00 EST 2016},
month = {Tue Jan 19 00:00:00 EST 2016}
}
Web of Science
Figures / Tables:
Works referenced in this record:
Characterization of 16S rRNA genes from oil field microbial communities indicates the presence of a variety of sulfate-reducing, fermentative, and sulfide-oxidizing bacteria.
journal, January 1996
- Voordouw, G.; Armstrong, S. M.; Reimer, M. F.
- Applied and environmental microbiology, Vol. 62, Issue 5
Prokaryotes: The unseen majority
journal, June 1998
- Whitman, W. B.; Coleman, D. C.; Wiebe, W. J.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
Evolution of Acetoclastic Methanogenesis in Methanosarcina via Horizontal Gene Transfer from Cellulolytic Clostridia
journal, November 2007
- Fournier, G. P.; Gogarten, J. P.
- Journal of Bacteriology, Vol. 190, Issue 3
The monosaccharide spectra of natural waters
journal, October 1980
- Mopper, Kenneth; Dawson, Rodger; Liebezeit, Gerd
- Marine Chemistry, Vol. 10, Issue 1
The Impact of Microbial Metabolism on Marine Dissolved Organic Matter
journal, January 2011
- Kujawinski, Elizabeth B.
- Annual Review of Marine Science, Vol. 3, Issue 1
Gene and translation initiation site prediction in metagenomic sequences
journal, July 2012
- Hyatt, Doug; LoCascio, Philip F.; Hauser, Loren J.
- Bioinformatics, Vol. 28, Issue 17
Thermacetogenium phaeum gen. nov., sp. nov., a strictly anaerobic, thermophilic, syntrophic acetate-oxidizing bacterium
journal, July 2000
- Hattori, S.; Kamagata, Y.; Hanada, S.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 50, Issue 4
KEGG for integration and interpretation of large-scale molecular data sets
journal, November 2011
- Kanehisa, M.; Goto, S.; Sato, Y.
- Nucleic Acids Research, Vol. 40, Issue D1
Xylan of Siphonaceous Green Algae
journal, July 1960
- Iriki, Yoshihiko; Suzuki, Takeo; Nisizawa, Kazutosi
- Nature, Vol. 187, Issue 4731
KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 1999
- Ogata, H.; Goto, S.; Sato, K.
- Nucleic Acids Research, Vol. 27, Issue 1
Biological activity in the deep subsurface and the origin of heavy oil
journal, November 2003
- Head, Ian M.; Jones, D. Martin; Larter, Steve R.
- Nature, Vol. 426, Issue 6964
Anaerobic oxidation of long-chain n-alkanes by the hyperthermophilic sulfate-reducing archaeon, Archaeoglobus fulgidus
journal, April 2014
- Khelifi, Nadia; Amin Ali, Oulfat; Roche, Philippe
- The ISME Journal, Vol. 8, Issue 11
Desulfonauticus autotrophicus sp. nov., a novel thermophilic sulfate-reducing bacterium isolated from oil-production water and emended description of the genus Desulfonauticus
journal, December 2008
- Mayilraj, Shanmugam; Kaksonen, Anna H.; Cord-Ruwisch, Ralf
- Extremophiles, Vol. 13, Issue 2
ARB: a software environment for sequence data
journal, February 2004
- Ludwig, W.
- Nucleic Acids Research, Vol. 32, Issue 4
Functional differences between Arctic seawater and sedimentary microbial communities: contrasts in microbial hydrolysis of complex substrates: Functional differences in Arctic microbial communities
journal, November 2008
- Arnosti, Carol
- FEMS Microbiology Ecology, Vol. 66, Issue 2
Hydrocarbon Degradation in Petroleum Reservoirs
book, January 2010
- Head, I. M.; Larter, S. R.; Gray, N. D.
- Handbook of Hydrocarbon and Lipid Microbiology
Unusual biology across a group comprising more than 15% of domain Bacteria
journal, June 2015
- Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C.
- Nature, Vol. 523, Issue 7559
Community Genomics Among Stratified Microbial Assemblages in the Ocean's Interior
journal, January 2006
- DeLong, E. F.
- Science, Vol. 311, Issue 5760
Hydrogen metabolism in the extreme thermophile Thermotoga neapolitana
journal, March 2010
- d'Ippolito, Giuliana; Dipasquale, Laura; Vella, Filomena Monica
- International Journal of Hydrogen Energy, Vol. 35, Issue 6
Substrate specificity in polysaccharide hydrolysis: Contrasts between bottom water and sediments
journal, July 2000
- Arnosti, C.
- Limnology and Oceanography, Vol. 45, Issue 5
Evaluation and Optimization of DNA Extraction and Purification Procedures for Soil and Sediment Samples
journal, November 1999
- Miller, D. N.; Bryant, J. E.; Madsen, E. L.
- Applied and Environmental Microbiology, Vol. 65, Issue 11
The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus
journal, November 1997
- Klenk, Hans-Peter; Clayton, Rebecca A.; Tomb, Jean-Francois
- Nature, Vol. 390, Issue 6658
Roles of thermophilic thiosulfate-reducing bacteria and methanogenic archaea in the biocorrosion of oil pipelines
journal, March 2014
- Liang, Renxing; Grizzle, Robert S.; Duncan, Kathleen E.
- Frontiers in Microbiology, Vol. 5
Deep subseafloor microbial cells on physiological standby
journal, October 2011
- Jorgensen, B. B.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 45
Temperature and injection water source influence microbial community structure in four Alaskan North Slope hydrocarbon reservoirs
journal, August 2014
- Piceno, Yvette M.; Reid, Francine C.; Tom, Lauren M.
- Frontiers in Microbiology, Vol. 5
The Eastern and Western branches of the Wood/Ljungdahl pathway: how the East and West were won
journal, January 1997
- Ragsdale, Stephen W.
- BioFactors, Vol. 6, Issue 1
Draft Genome Sequence of the Xylan-Degrading Marine Bacterium Strain S124, Representing a Novel Species of the Genus Oceanicola
journal, October 2012
- Kwon, Y. -K.; Kim, J. J.; Kim, J. H.
- Journal of Bacteriology, Vol. 194, Issue 22
UniRef: comprehensive and non-redundant UniProt reference clusters
journal, March 2007
- Suzek, B. E.; Huang, H.; McGarvey, P.
- Bioinformatics, Vol. 23, Issue 10
Metabolic Activity of Subsurface Life in Deep-Sea Sediments
journal, March 2002
- D'Hondt, S.
- Science, Vol. 295, Issue 5562
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006
- Stamatakis, Alexandros
- Bioinformatics, Vol. 22, Issue 21
Methanogenesis, sulfate reduction and crude oil biodegradation in hot Alaskan oilfields: Methanogenic crude oil biodegradation in hot oilfields
journal, November 2010
- Gieg, Lisa M.; Davidova, Irene A.; Duncan, Kathleen E.
- Environmental Microbiology, Vol. 12, Issue 11
Key players and team play: anaerobic microbial communities in hydrocarbon-contaminated aquifers
journal, April 2012
- Kleinsteuber, Sabine; Schleinitz, Kathleen M.; Vogt, Carsten
- Applied Microbiology and Biotechnology, Vol. 94, Issue 4
The genome of S yntrophorhabdus aromaticivorans strain UI provides new insights for syntrophic aromatic compound metabolism and electron flow
journal, March 2014
- Nobu, Masaru K.; Narihiro, Takashi; Hideyuki, Tamaki
- Environmental Microbiology, Vol. 17, Issue 12
Archaeoglobus fulgidus and Thermotoga elfii , Thermophilic Isolates from Deep Geothermal Water of the Paris Basin
journal, February 2009
- Fardeau, Marie-Laure; Goulhen, Florence; Bruschi, Mireille
- Geomicrobiology Journal, Vol. 26, Issue 2
Global distribution of microbial abundance and biomass in subseafloor sediment
journal, August 2012
- Kallmeyer, J.; Pockalny, R.; Adhikari, R. R.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 40
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012
- Peng, Y.; Leung, H. C. M.; Yiu, S. M.
- Bioinformatics, Vol. 28, Issue 11
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012
- Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
- Nucleic Acids Research, Vol. 41, Issue D1
Characterizing microbial diversity in production water from an Alaskan mesothermic petroleum reservoir with two independent molecular methods
journal, January 2009
- Pham, Vinh D.; Hnatow, Linda L.; Zhang, Shiping
- Environmental Microbiology, Vol. 11, Issue 1
New Hydrocarbon Degradation Pathways in the Microbial Metagenome from Brazilian Petroleum Reservoirs
journal, February 2014
- Sierra-García, Isabel Natalia; Correa Alvarez, Javier; Pantaroto de Vasconcellos, Suzan
- PLoS ONE, Vol. 9, Issue 2
Polysaccharide hydrolysis in aggregates and free enzyme activity in aggregate-free seawater from the north-eastern Gulf of Mexico
journal, February 2008
- Ziervogel, Kai; Arnosti, Carol
- Environmental Microbiology, Vol. 10, Issue 2
Biodegradation of Crude Oils in Reservoirs
book, January 1984
- Connan, Jacques
- Advances in Petroleum Geochemistry
Desulfotomaculum thermocisternum sp. nov., a Sulfate Reducer Isolated from a Hot North Sea Oil Reservoir
journal, April 1996
- Nilsen, R. K.; Torsvik, T.; Lien, T.
- International Journal of Systematic Bacteriology, Vol. 46, Issue 2
Biological souring and mitigation in oil reservoirs
journal, August 2011
- Gieg, Lisa M.; Jack, Tom R.; Foght, Julia M.
- Applied Microbiology and Biotechnology, Vol. 92, Issue 2
The microbial communities in two apparently physically separated deep subsurface oil reservoirs show extensive DNA sequence similarities: Comparative metagenomics of two oil reservoirs using high-throughput sequencing
journal, July 2013
- Lewin, Anna; Johansen, Jostein; Wentzel, Alexander
- Environmental Microbiology, Vol. 16, Issue 2
A Deeply Branching Thermophilic Bacterium with an Ancient Acetyl-CoA Pathway Dominates a Subsurface Ecosystem
journal, January 2012
- Takami, Hideto; Noguchi, Hideki; Takaki, Yoshihiro
- PLoS ONE, Vol. 7, Issue 1
Hyperthermophilic archaea are thriving in deep North Sea and Alaskan oil reservoirs
journal, October 1993
- Stetter, K. O.; Huber, R.; Blöchl, E.
- Nature, Vol. 365, Issue 6448
Dissolved carbohydrates in the new york bight and the variability of marine organic matter
journal, April 1983
- Harvey, George R.
- Marine Chemistry, Vol. 12, Issue 4
Characterization of thermophilic consortia from two souring oil reservoirs.
journal, January 1996
- Mueller, R. F.; Nielsen, P. H.
- Applied and environmental microbiology, Vol. 62, Issue 9
Distribution of thermophilic marine sulfate reducers in north sea oil field waters and oil reservoirs.
journal, January 1996
- Nilsen, R. K.; Beeder, J.; Thorstenson, T.
- Applied and environmental microbiology, Vol. 62, Issue 5
Archaeoglobus fulgidus Isolated from Hot North Sea Oil Field Waters
journal, January 1994
- Beeder, Janiche; Nilsen, Roald Kåre; Rosnes, Jan Thomas
- Applied and Environmental Microbiology, Vol. 60, Issue 4
Works referencing / citing this record:
Thermophilic endospores associated with migrated thermogenic hydrocarbons in deep Gulf of Mexico marine sediments
journal, March 2018
- Chakraborty, Anirban; Ellefson, Emily; Li, Carmen
- The ISME Journal, Vol. 12, Issue 8
Microbial community analyses of produced waters from high-temperature oil reservoirs reveal unexpected similarity between geographically distant oil reservoirs
journal, May 2018
- Kim, Daehyun D.; O'Farrell, Corynne; Toth, Courtney R. A.
- Microbial Biotechnology, Vol. 11, Issue 4
Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO 2 concentrations : Genomic resolution of a high-CO
journal, July 2016
- Probst, Alexander J.; Castelle, Cindy J.; Singh, Andrea
- Environmental Microbiology, Vol. 19, Issue 2
The Wood–Ljungdahl pathway as a key component of metabolic versatility in candidate phylum Bipolaricaulota (Acetothermia, OP1)
journal, April 2019
- Youssef, Noha H.; Farag, Ibrahim F.; Rudy, Sydney
- Environmental Microbiology Reports, Vol. 11, Issue 4
Anaerobic Biodegradation of Hydrocarbons: Metagenomics and Metabolomics
book, January 2016
- Gieg, Lisa M.; Toth, Courtney R. A.
- Consequences of Microbial Interactions with Hydrocarbons, Oils, and Lipids: Biodegradation and Bioremediation
Mineralizing Filamentous Bacteria from the Prony Bay Hydrothermal Field Give New Insights into the Functioning of Serpentinization-Based Subseafloor Ecosystems
journal, January 2017
- Pisapia, Céline; Gérard, Emmanuelle; Gérard, Martine
- Frontiers in Microbiology, Vol. 8
Discovered by genomics: putative reductive dehalogenases with N-terminus transmembrane helixes
journal, April 2019
- Atashgahi, Siavash
- FEMS Microbiology Ecology, Vol. 95, Issue 5
Genomic analysis of the mesophilic Thermotogae genus Mesotoga reveals phylogeographic structure and genomic determinants of its distinct metabolism: Comparative genomic analysis of Mesotoga
journal, December 2018
- Nesbø, Camilla L.; Charchuk, Rhianna; Pollo, Stephen M. J.
- Environmental Microbiology, Vol. 21, Issue 1
Parallel Evolution of Genome Streamlining and Cellular Bioenergetics across the Marine Radiation of a Bacterial Phylum
journal, September 2018
- Getz, Eric W.; Tithi, Saima Sultana; Zhang, Liqing
- mBio, Vol. 9, Issue 5
Spatio‐temporal insights into microbiology of the freshwater‐to‐hypersaline, oxic‐hypoxic‐euxinic waters of Ursu Lake
journal, January 2020
- Baricz, Andreea; Chiriac, Cecilia Maria; Andrei, Adrian‐Ștefan
- Environmental Microbiology
Current Status and Potential Applications of Underexplored Prokaryotes
journal, October 2019
- Goh, Kian Mau; Shahar, Saleha; Chan, Kok-Gan
- Microorganisms, Vol. 7, Issue 10
Genomic analysis of the mesophilic Thermotogae genus Mesotoga reveals phylogeographic structure and genomic determinants of its distinct metabolism
posted_content, October 2018
- Nesbø, Camilla L.; Charchuk, Rhianna; Pollo, Stephen M. J.
- bioRxiv
Time Course-Dependent Methanogenic Crude Oil Biodegradation: Dynamics of Fumarate Addition Metabolites, Biodegradative Genes, and Microbial Community Composition
journal, January 2018
- Toth, Courtney R. A.; Gieg, Lisa M.
- Frontiers in Microbiology, Vol. 8
Metagenomic identification of active methanogens and methanotrophs in serpentinite springs of the Voltri Massif, Italy
journal, January 2017
- Brazelton, William J.; Thornton, Christopher N.; Hyer, Alex
- PeerJ, Vol. 5
Microbial metabolism and adaptations in Atribacteria-dominated methane hydrate sediments
journal, June 2021
- Glass, Jennifer B.; Ranjan, Piyush; Kretz, Cecilia B.
- Environmental Microbiology
New Biological Insights Into How Deforestation in Amazonia Affects Soil Microbial Communities Using Metagenomics and Metagenome-Assembled Genomes
journal, July 2018
- Kroeger, Marie E.; Delmont, Tom O.; Eren, A. M.
- Frontiers in Microbiology, Vol. 9
Exploring neighborhoods in large metagenome assembly graphs using spacegraphcats reveals hidden sequence diversity
journal, July 2020
- Brown, C. Titus; Moritz, Dominik; O’Brien, Michael P.
- Genome Biology, Vol. 21, Issue 1
Simulation of Deepwater Horizon oil plume reveals substrate specialization within a complex community of hydrocarbon degraders
journal, June 2017
- Hu, Ping; Dubinsky, Eric A.; Probst, Alexander J.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 28
Figures / Tables found in this record: