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

Abstract

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.

Authors:
; ORCiD logo; ORCiD logo; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1503494
Report Number(s):
PNNL-SA-134972
Journal ID: ISSN 0027-8424
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 115; Journal Issue: 28; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
hydraulic fracturing, metaproteomics, methanogenesis, Stickland reaction, metagenomics

Citation Formats

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., and Wrighton, Kelly C. Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales. United States: N. p., 2018. Web. doi:10.1073/pnas.1800155115.
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. Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales. United States. https://doi.org/10.1073/pnas.1800155115
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., and Wrighton, Kelly C. Mon . "Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales". United States. https://doi.org/10.1073/pnas.1800155115.
@article{osti_1503494,
title = {Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales},
author = {Borton, Mikayla A. and Hoyt, David W. and Roux, Simon and Daly, Rebecca A. and Welch, Susan A. and Nicora, Carrie D. and Purvine, Samuel and Eder, Elizabeth K. and Hanson, Andrea J. and Sheets, Julie M. and Morgan, David M. and Wolfe, Richard A. and Sharma, Shikha and Carr, Timothy R. and Cole, David R. and Mouser, Paula J. and Lipton, Mary S. and Wilkins, Michael J. and Wrighton, Kelly C.},
abstractNote = {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.},
doi = {10.1073/pnas.1800155115},
url = {https://www.osti.gov/biblio/1503494}, journal = {Proceedings of the National Academy of Sciences of the United States of America},
issn = {0027-8424},
number = 28,
volume = 115,
place = {United States},
year = {2018},
month = {6}
}

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journal, January 1988


Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea
journal, August 2017


Gene and translation initiation site prediction in metagenomic sequences
journal, July 2012


Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012


Classifying the uncultivated microbial majority: A place for metagenomic data in the Candidatus proposal
journal, June 2015


Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions
journal, November 2017


EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data
journal, May 2011


VirSorter: mining viral signal from microbial genomic data
journal, January 2015


Glycine metabolism in anaerobes
journal, January 1994


Temporal Changes in Microbial Ecology and Geochemistry in Produced Water from Hydraulically Fractured Marcellus Shale Gas Wells
journal, May 2014


Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme
journal, November 2012


Hydraulic fracturing offers view of microbial life in the deep terrestrial subsurface
journal, August 2016


Clostridium sticklandii, a specialist in amino acid degradation:revisiting its metabolism through its genome sequence
journal, January 2010


Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics
journal, October 2017


Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome
journal, April 2017


Plankton networks driving carbon export in the oligotrophic ocean
journal, February 2016


A Sparse PLS for Variable Selection when Integrating Omics Data
journal, January 2008


Glycine reductase mechanism
journal, October 2004


Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2
journal, February 2012


Choline and N , N -Dimethylethanolamine as Direct Substrates for Methanogens
journal, September 2012


Performance of some variable selection methods when multicollinearity is present
journal, July 2005


InterProScan: protein domains identifier
journal, July 2005


Bacterial Communities Associated with Production Facilities of Two Newly Drilled Thermogenic Natural Gas Wells in the Barnett Shale (Texas, USA)
journal, May 2012


Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales
journal, September 2016


A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase
journal, October 2014


Methanohalophilus zhilinae sp. nov., an Alkaliphilic, Halophilic, Methylotrophic Methanogen
journal, April 1988


New amino acids, and heterocyclic compounds participating in the stickland reaction of Clostridium sticklandii
journal, January 1973


Predominance and Metabolic Potential of Halanaerobium spp. in Produced Water from Hydraulically Fractured Marcellus Shale Wells
journal, February 2017


Eating For Two: How Metabolism Establishes Interspecies Interactions in the Gut
journal, October 2011


Search and clustering orders of magnitude faster than BLAST
journal, August 2010


The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012


Evolution and classification of the CRISPR–Cas systems
journal, May 2011


Metagenomic biomarker discovery and explanation
journal, January 2011


Microbial Community Changes in Hydraulic Fracturing Fluids and Produced Water from Shale Gas Extraction
journal, October 2013


Targeted Profiling:  Quantitative Analysis of 1 H NMR Metabolomics Data
journal, July 2006


Fast gapped-read alignment with Bowtie 2
journal, March 2012


Sulfide Generation by Dominant Halanaerobium Microorganisms in Hydraulically Fractured Shales
journal, July 2017


Sparse principal component analysis via regularized low rank matrix approximation
journal, July 2008


Bringing your tools to CyVerse Discovery Environment using Docker
journal, January 2016


Microbial distribution and variation in produced water from separators to storage tanks of shale gas wells in Sichuan Basin, China
journal, January 2017


Bringing your tools to CyVerse Discovery Environment using Docker
journal, January 2016


Amino Acid Degradation by Anaerobic Bacteria
journal, June 1981


Organic and inorganic composition and microbiology of produced waters from Pennsylvania shale gas wells
journal, September 2015


Predominant archaea in marine sediments degrade detrital proteins
journal, March 2013


MS-GF+ makes progress towards a universal database search tool for proteomics
journal, October 2014


Bioenergetic Aspects of Halophilism
journal, June 1999


Tracer Studies on Ornithine, Lysine, and Formate Metabolism in an Amino acid Fermenting Clostridium
journal, January 1954


    Works referencing / citing this record:

    Search and clustering orders of magnitude faster than BLAST
    journal, August 2010


    Methanohalophilus zhilinae sp. nov., an Alkaliphilic, Halophilic, Methylotrophic Methanogen
    journal, April 1988


    New amino acids, and heterocyclic compounds participating in the stickland reaction of Clostridium sticklandii
    journal, January 1973


    Eating For Two: How Metabolism Establishes Interspecies Interactions in the Gut
    journal, October 2011


    Performance of some variable selection methods when multicollinearity is present
    journal, July 2005


    Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2
    journal, February 2012


    Clostridium sticklandii, a specialist in amino acid degradation:revisiting its metabolism through its genome sequence
    journal, January 2010


    Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales
    journal, September 2016


    MS-GF+ makes progress towards a universal database search tool for proteomics
    journal, October 2014


    Microbial distribution and variation in produced water from separators to storage tanks of shale gas wells in Sichuan Basin, China
    journal, January 2017


    Predominance and Metabolic Potential of Halanaerobium spp. in Produced Water from Hydraulically Fractured Marcellus Shale Wells
    journal, February 2017


    Predominant archaea in marine sediments degrade detrital proteins
    journal, March 2013


    Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme
    journal, November 2012


    VirSorter: mining viral signal from microbial genomic data
    journal, January 2015


    Choline and N , N -Dimethylethanolamine as Direct Substrates for Methanogens
    journal, September 2012


    Classifying the uncultivated microbial majority: A place for metagenomic data in the Candidatus proposal
    journal, June 2015


    Temporal Changes in Microbial Ecology and Geochemistry in Produced Water from Hydraulically Fractured Marcellus Shale Gas Wells
    journal, May 2014


    InterProScan: protein domains identifier
    journal, July 2005


    Sulfide Generation by Dominant Halanaerobium Microorganisms in Hydraulically Fractured Shales
    journal, July 2017


    Metagenomic biomarker discovery and explanation
    journal, January 2011


    Microbial Community Changes in Hydraulic Fracturing Fluids and Produced Water from Shale Gas Extraction
    journal, October 2013


    The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
    journal, November 2012


    Deep-Subsurface Pressure Stimulates Metabolic Plasticity in Shale-Colonizing Halanaerobium spp.
    journal, April 2019


    Fast gapped-read alignment with Bowtie 2
    journal, March 2012


    Comparative genomics and physiology of the genus Methanohalophilus , a prevalent methanogen in hydraulically fractured shale
    journal, December 2018


    Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
    journal, September 2012


    Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics
    journal, October 2017


    Amino Acid Degradation by Anaerobic Bacteria
    journal, June 1981


    Sparse principal component analysis via regularized low rank matrix approximation
    journal, July 2008


    EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data
    journal, May 2011


    Glycine reductase mechanism
    journal, October 2004


    Hydraulic fracturing offers view of microbial life in the deep terrestrial subsurface
    journal, August 2016


    Organic and inorganic composition and microbiology of produced waters from Pennsylvania shale gas wells
    journal, September 2015


    Evolution and classification of the CRISPR–Cas systems
    journal, May 2011


    Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea
    journal, August 2017


    Glycine metabolism in anaerobes
    journal, January 1994


    Bringing your tools to CyVerse Discovery Environment using Docker
    journal, January 2016


    Gene and translation initiation site prediction in metagenomic sequences
    journal, July 2012


    Targeted Profiling:  Quantitative Analysis of 1 H NMR Metabolomics Data
    journal, July 2006


    Methanohalophilus mahii gen. nov., sp. nov., a Methylotrophic Halophilic Methanogen
    journal, January 1988


    Bacterial Communities Associated with Production Facilities of Two Newly Drilled Thermogenic Natural Gas Wells in the Barnett Shale (Texas, USA)
    journal, May 2012


    A Sparse PLS for Variable Selection when Integrating Omics Data
    journal, January 2008


    Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions
    journal, November 2017


    Plankton networks driving carbon export in the oligotrophic ocean
    journal, February 2016


    Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils
    journal, December 2019


    New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11
    journal, December 2016


    A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase
    journal, October 2014


    Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome
    journal, April 2017


    In situ transformation of ethoxylate and glycol surfactants by shale-colonizing microorganisms during hydraulic fracturing
    journal, June 2019