Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales

Borton, Mikayla A.; Hoyt, David W.; Roux, Simon; Daly, Rebecca A.; Welch, Susan A.; Nicora, Carrie D.; Purvine, Samuel; Eder, Elizabeth K.; Hanson, Andrea J.; Sheets, Julie M.; Morgan, David M.; Wolfe, Richard A.; Sharma, Shikha; Carr, Timothy R.; Cole, David R.; Mouser, Paula J.; Lipton, Mary S.; Wilkins, Michael J.; Wrighton, Kelly C.

doi:10.1073/pnas.1800155115

Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales

Journal Article · 25 June 2018 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1800155115· OSTI ID:1503494

Borton, Mikayla A.; ; ; Daly, Rebecca A.; Welch, Susan A.; Nicora, Carrie D.; Purvine, Samuel; Eder, Elizabeth K.; Hanson, Andrea J.; Sheets, Julie M.; Morgan, David M.; Wolfe, Richard A.; Sharma, Shikha; Carr, Timothy R.; ; Mouser, Paula J.; Lipton, Mary S.; Wilkins, Michael J.; Wrighton, Kelly C.

Hydraulic fracturing is one of the industrial processes behind the surging natural gas output in the United States. This technology inadvertently creates an engineered microbial ecosystem thousands of meters below Earth’s surface. Here, we used laboratory reactors to perform manipulations of persisting shale microbial communities that are currently not feasible in field scenarios. Metaproteomic and metabolite findings from the laboratory were then corroborated using regression based modeling performed on metagenomic and metabolite data from more than 40 produced fluids from five hydraulically fractured shale wells. Collectively, our findings show that Halanaerobium, Geotoga, and Methanohalophilius strain abundances predict a significant fraction of nitrogen and carbon metabolites in the field. Our laboratory findings also exposed cryptic predatory, cooperative, and competitive interactions that impact microorganisms across fractured shales. Scaling these results from the laboratory to the field identified mechanisms underpinning biogeochemical reactions, yielding knowledge that can be harnessed to potentially increase energy yields and inform management practices in hydraulically fractured shales.

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

DOE Contract Number:: AC05-76RL01830

OSTI ID:: 1503494

Report Number(s):: PNNL-SA-134972

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, Issue 28; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)

Country of Publication:: United States

Language:: English

References (66)

Analysis of immune, microbiota and metabolome maturation in infants in a clinical trial of Lactobacillus paracasei CBA L74-fermented formula No authors listed Nature Communications https://doi.org/10.1038/s41467-020-16582-1		June 2020
New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11 No authors listed The ISME Journal https://doi.org/10.1038/ismej.2016.150		December 2016
Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2 No authors listed Bioinformatics https://doi.org/10.1093/bioinformatics/bts079		February 2012
Bioenergetic Aspects of Halophilism No authors listed Microbiology and Molecular Biology Reviews https://doi.org/10.1128/MMBR.63.2.334-348.1999		June 1999
Methanohalophilus mahii gen. nov., sp. nov., a Methylotrophic Halophilic Methanogen No authors listed International Journal of Systematic Bacteriology https://doi.org/10.1099/00207713-38-1-122		January 1988
Choline and N , N -Dimethylethanolamine as Direct Substrates for Methanogens No authors listed Applied and Environmental Microbiology https://doi.org/10.1128/AEM.01941-12		September 2012
Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry No authors listed Nature Methods https://doi.org/10.1038/nmeth1019		February 2007
Performance of some variable selection methods when multicollinearity is present No authors listed Chemometrics and Intelligent Laboratory Systems https://doi.org/10.1016/j.chemolab.2004.12.011		July 2005
Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea No authors listed Nature Biotechnology https://doi.org/10.1038/nbt.3893		August 2017
InterProScan: protein domains identifier No authors listed Nucleic Acids Research https://doi.org/10.1093/nar/gki442		July 2005
Gene and translation initiation site prediction in metagenomic sequences No authors listed Bioinformatics https://doi.org/10.1093/bioinformatics/bts429		July 2012
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla No authors listed Science https://doi.org/10.1126/science.1224041		September 2012
Bacterial Communities Associated with Production Facilities of Two Newly Drilled Thermogenic Natural Gas Wells in the Barnett Shale (Texas, USA) No authors listed Microbial Ecology https://doi.org/10.1007/s00248-012-0073-3		May 2012
Classifying the uncultivated microbial majority: A place for metagenomic data in the Candidatus proposal No authors listed Systematic and Applied Microbiology https://doi.org/10.1016/j.syapm.2015.01.001		June 2015
Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales No authors listed Nature Microbiology https://doi.org/10.1038/nmicrobiol.2016.146		September 2016
A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase No authors listed Proceedings of the National Academy of Sciences https://doi.org/10.1073/pnas.1409642111		October 2014
Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions No authors listed Nature Communications https://doi.org/10.1038/s41467-017-01753-4		November 2017
EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data No authors listed Genome Biology https://doi.org/10.1186/gb-2011-12-5-r44		May 2011
Methanohalophilus zhilinae sp. nov., an Alkaliphilic, Halophilic, Methylotrophic Methanogen No authors listed International Journal of Systematic Bacteriology https://doi.org/10.1099/00207713-38-2-139		April 1988
New amino acids, and heterocyclic compounds participating in the stickland reaction of Clostridium sticklandii No authors listed Archiv f�r Mikrobiologie https://doi.org/10.1007/BF00412026		January 1973
The Functional Potential of Microbial Communities in Hydraulic Fracturing Source Water and Produced Water from Natural Gas Extraction Characterized by Metagenomic Sequencing No authors listed PLoS ONE https://doi.org/10.1371/journal.pone.0107682		October 2014
VirSorter: mining viral signal from microbial genomic data No authors listed PeerJ https://doi.org/10.7717/peerj.985		January 2015
Glycine metabolism in anaerobes No authors listed Antonie van Leeuwenhoek https://doi.org/10.1007/BF00871641		January 1994
Predominance and Metabolic Potential of Halanaerobium spp. in Produced Water from Hydraulically Fractured Marcellus Shale Wells No authors listed Applied and Environmental Microbiology https://doi.org/10.1128/AEM.02659-16		February 2017
Draft Genome Sequence of Methanohalophilus mahii Strain DAL1 Reconstructed from a Hydraulic Fracturing-Produced Water Metagenome No authors listed Genome Announcements https://doi.org/10.1128/genomeA.00899-16		September 2016
Thermodynamic limits to microbial life at high salt concentrations: Thermodynamic limits to halophilic life No authors listed Environmental Microbiology https://doi.org/10.1111/j.1462-2920.2010.02365.x		November 2010
Temporal Changes in Microbial Ecology and Geochemistry in Produced Water from Hydraulically Fractured Marcellus Shale Gas Wells No authors listed Environmental Science & Technology https://doi.org/10.1021/es501173p		May 2014
Eating For Two: How Metabolism Establishes Interspecies Interactions in the Gut No authors listed Cell Host & Microbe https://doi.org/10.1016/j.chom.2011.10.002		October 2011
Search and clustering orders of magnitude faster than BLAST No authors listed Bioinformatics https://doi.org/10.1093/bioinformatics/btq461		August 2010
Methanohalophilus zhilinae sp. nov., an Alkaliphilic, Halophilic, Methylotrophic Methanogen No authors listed International Journal of Systematic Bacteriology https://doi.org/10.1099/00207713-38-3-333a		July 1988
Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme No authors listed Proceedings of the National Academy of Sciences https://doi.org/10.1073/pnas.1215689109		November 2012
Hydraulic fracturing offers view of microbial life in the deep terrestrial subsurface No authors listed FEMS Microbiology Ecology https://doi.org/10.1093/femsec/fiw166		August 2016
Eubacterium acidaminophilum sp. nov., a versatile amino acid-degrading anaerobe producing or utilizing H2 or formate: Description and enzymatic studies No authors listed Archives of Microbiology https://doi.org/10.1007/BF00407789		July 1988
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools No authors listed Nucleic Acids Research https://doi.org/10.1093/nar/gks1219		November 2012
Evolution and classification of the CRISPR–Cas systems No authors listed Nature Reviews Microbiology https://doi.org/10.1038/nrmicro2577		May 2011
Metagenomic biomarker discovery and explanation No authors listed Genome Biology https://doi.org/10.1186/gb-2011-12-6-r60		January 2011
Clostridium sticklandii, a specialist in amino acid degradation:revisiting its metabolism through its genome sequence No authors listed BMC Genomics https://doi.org/10.1186/1471-2164-11-555		January 2010
Microbial Community Changes in Hydraulic Fracturing Fluids and Produced Water from Shale Gas Extraction No authors listed Environmental Science & Technology https://doi.org/10.1021/es402928b		October 2013
Targeted Profiling: Quantitative Analysis of ¹ H NMR Metabolomics Data No authors listed Analytical Chemistry https://doi.org/10.1021/ac060209g		July 2006
Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics No authors listed Nature Communications https://doi.org/10.1038/s41467-017-01086-2		October 2017
Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome No authors listed Microbiome https://doi.org/10.1186/s40168-017-0264-8		April 2017
Fast gapped-read alignment with Bowtie 2 No authors listed Nature Methods https://doi.org/10.1038/nmeth.1923		March 2012
Sulfide Generation by Dominant Halanaerobium Microorganisms in Hydraulically Fractured Shales No authors listed mSphere https://doi.org/10.1128/mSphereDirect.00257-17		July 2017
Biogenic methane production from coal: A review on recent research and development on microbially enhanced coalbed methane (MECBM) No authors listed Fuel https://doi.org/10.1016/j.fuel.2015.10.121		February 2016
Sparse principal component analysis via regularized low rank matrix approximation No authors listed Journal of Multivariate Analysis https://doi.org/10.1016/j.jmva.2007.06.007		July 2008
New gas material balance to quantify biogenic gas generation rates from shallow organic-matter-rich shales No authors listed Fuel https://doi.org/10.1016/j.fuel.2012.06.054		February 2013
Bringing your tools to CyVerse Discovery Environment using Docker No authors listed F1000Research https://doi.org/10.12688/f1000research.8935.3		January 2016
Microbial distribution and variation in produced water from separators to storage tanks of shale gas wells in Sichuan Basin, China No authors listed Environmental Science: Water Research & Technology https://doi.org/10.1039/C6EW00286B		January 2017
Bringing your tools to CyVerse Discovery Environment using Docker No authors listed F1000Research https://doi.org/10.12688/f1000research.8935.1		January 2016
Amino Acid Degradation by Anaerobic Bacteria No authors listed Annual Review of Biochemistry https://doi.org/10.1146/annurev.bi.50.070181.000323		June 1981
Bringing your tools to CyVerse Discovery Environment using Docker No authors listed F1000Research https://doi.org/10.12688/f1000research.8935.2		January 2016
Sparse principal component analysis via regularized low rank matrix approximation No authors listed The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/sn3b-9005		January 2008
Organic and inorganic composition and microbiology of produced waters from Pennsylvania shale gas wells No authors listed Applied Geochemistry https://doi.org/10.1016/j.apgeochem.2015.04.011		September 2015
Metabolic Capability of a Predominant Halanaerobium sp. in Hydraulically Fractured Gas Wells and Its Implication in Pipeline Corrosion No authors listed Frontiers in Microbiology https://doi.org/10.3389/fmicb.2016.00988		June 2016
Predominant archaea in marine sediments degrade detrital proteins No authors listed Nature https://doi.org/10.1038/nature12033		March 2013
Plankton networks driving carbon export in the oligotrophic ocean No authors listed Nature https://doi.org/10.1038/nature16942		February 2016
Alignment-free $d_2^*$ oligonucleotide frequency dissimilarity measure improves prediction of hosts from metagenomically-derived viral sequences No authors listed Nucleic Acids Research https://doi.org/10.1093/nar/gkw1002		November 2016
MS-GF+ makes progress towards a universal database search tool for proteomics No authors listed Nature Communications https://doi.org/10.1038/ncomms6277		October 2014
A Sparse PLS for Variable Selection when Integrating Omics Data No authors listed Statistical Applications in Genetics and Molecular Biology https://doi.org/10.2202/1544-6115.1390		January 2008
Glycine reductase mechanism No authors listed Current Opinion in Chemical Biology https://doi.org/10.1016/j.cbpa.2004.08.002		October 2004
Tracer Studies on Ornithine, Lysine, and Formate Metabolism in an Amino acid Fermenting Clostridium No authors listed Journal of Bacteriology https://doi.org/10.1128/jb.67.6.651-657.1954		January 1954
Erratum: Corrigendum: Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea No authors listed Nature Biotechnology https://doi.org/10.1038/nbt0718-660a		July 2018
Deep-sea striving No authors listed Nature Reviews Microbiology https://doi.org/10.1038/nrmicro3037		May 2013
Converging on a mechanism for choline degradation No authors listed Proceedings of the National Academy of Sciences https://doi.org/10.1073/pnas.1219534110		December 2012
Naturally Occurring Asbestos in Valmalenco (Central Alps, Northern Italy): From Quarries and Mines to Stream Sediments No authors listed Environmental and Engineering Geoscience https://doi.org/10.2113/eeg-2270		February 2020
of EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data No authors listed figshare https://doi.org/10.6084/m9.figshare.10040330.v1		January 2019

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A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments No authors listed Microbiome https://doi.org/10.1186/s40168-019-0732-4		August 2019
Members of Marinobacter and Arcobacter Influence System Biogeochemistry During Early Production of Hydraulically Fractured Natural Gas Wells in the Appalachian Basin No authors listed Frontiers in Microbiology https://doi.org/10.3389/fmicb.2018.02646		November 2018
Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface No authors listed mSphere https://doi.org/10.1128/msphere.00613-19		December 2019
Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils No authors listed mSystems https://doi.org/10.1128/msystems.00320-19		December 2019
Comparative genomics and physiology of the genus Methanohalophilus , a prevalent methanogen in hydraulically fractured shale No authors listed Environmental Microbiology https://doi.org/10.1111/1462-2920.14467		December 2018
In situ transformation of ethoxylate and glycol surfactants by shale-colonizing microorganisms during hydraulic fracturing No authors listed The ISME Journal https://doi.org/10.1038/s41396-019-0466-0		June 2019
Bacterial microcompartments: catalysis-enhancing metabolic modules for next generation metabolic and biomedical engineering No authors listed BMC Biology https://doi.org/10.1186/s12915-019-0691-z		October 2019
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