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Title: Deep-Subsurface Pressure Stimulates Metabolic Plasticity in Shale-Colonizing Halanaerobium spp.

Abstract

Bacterial Halanaerobium strains become the dominant persisting microbial community member in produced fluids across geographically distinct hydraulically fractured shales. Halanaerobium is believed to be inadvertently introduced into this environment during the drilling and fracturing process and must therefore tolerate large changes in pressure, temperature, and salinity. Here, we used a Halanaerobium strain isolated from a natural gas well in the Utica Point Pleasant formation to investigate metabolic and physiological responses to growth under high-pressure subsurface conditions. Laboratory incubations confirmed the ability of Halanaerobium congolense strain WG8 to grow under pressures representative of deep shale formations (21 to 48 MPa). Under these conditions, broad metabolic and physiological shifts were identified, including higher abundances of proteins associated with the production of extracellular polymeric substances. Confocal laser scanning microscopy indicated that extracellular polymeric substance (EPS) production was associated with greater cell aggregation when biomass was cultured at high pressure.

Authors:
 [1];  [2];  [1];  [2];  [2];  [2];  [1];  [3];  [3];  [4];  [2]; ORCiD logo [5];  [6];  [6];  [7]
  1. The Ohio State Univ., Columbus, OH (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. DowDuPont Industrial Biosciences, Wilmington, DE (United States)
  4. Univ. of Tennessee, Knoxville, TN (United States)
  5. Univ. of New Hampshire, Durham, NH (United States)
  6. Colorado State Univ., Fort Collins, CO (United States)
  7. Chinese Academy of Sciences (CAS), Beijing (China)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1567051
Report Number(s):
PNNL-SA-144542
Journal ID: ISSN 0099-2240
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 85; Journal Issue: 12; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Halanaerobium; Shale; Biofilms; High Pressure; Hydraulic fracturing; Metabolomics

Citation Formats

Booker, Anne E., Hoyt, David W., Meulia, Tea, Eder, Elizabeth, Nicora, Carrie D., Purvine, Samuel O., Daly, Rebecca A., Moore, Joseph D., Wunch, Kenneth, Pfiffner, Susan M., Lipton, Mary S., Mouser, Paula J., Wrighton, Kelly C., Wilkins, Michael J., and Liu, Shuang-Jiang. Deep-Subsurface Pressure Stimulates Metabolic Plasticity in Shale-Colonizing Halanaerobium spp.. United States: N. p., 2019. Web. doi:10.1128/AEM.00018-19.
Booker, Anne E., Hoyt, David W., Meulia, Tea, Eder, Elizabeth, Nicora, Carrie D., Purvine, Samuel O., Daly, Rebecca A., Moore, Joseph D., Wunch, Kenneth, Pfiffner, Susan M., Lipton, Mary S., Mouser, Paula J., Wrighton, Kelly C., Wilkins, Michael J., & Liu, Shuang-Jiang. Deep-Subsurface Pressure Stimulates Metabolic Plasticity in Shale-Colonizing Halanaerobium spp.. United States. doi:10.1128/AEM.00018-19.
Booker, Anne E., Hoyt, David W., Meulia, Tea, Eder, Elizabeth, Nicora, Carrie D., Purvine, Samuel O., Daly, Rebecca A., Moore, Joseph D., Wunch, Kenneth, Pfiffner, Susan M., Lipton, Mary S., Mouser, Paula J., Wrighton, Kelly C., Wilkins, Michael J., and Liu, Shuang-Jiang. Fri . "Deep-Subsurface Pressure Stimulates Metabolic Plasticity in Shale-Colonizing Halanaerobium spp.". United States. doi:10.1128/AEM.00018-19. https://www.osti.gov/servlets/purl/1567051.
@article{osti_1567051,
title = {Deep-Subsurface Pressure Stimulates Metabolic Plasticity in Shale-Colonizing Halanaerobium spp.},
author = {Booker, Anne E. and Hoyt, David W. and Meulia, Tea and Eder, Elizabeth and Nicora, Carrie D. and Purvine, Samuel O. and Daly, Rebecca A. and Moore, Joseph D. and Wunch, Kenneth and Pfiffner, Susan M. and Lipton, Mary S. and Mouser, Paula J. and Wrighton, Kelly C. and Wilkins, Michael J. and Liu, Shuang-Jiang},
abstractNote = {Bacterial Halanaerobium strains become the dominant persisting microbial community member in produced fluids across geographically distinct hydraulically fractured shales. Halanaerobium is believed to be inadvertently introduced into this environment during the drilling and fracturing process and must therefore tolerate large changes in pressure, temperature, and salinity. Here, we used a Halanaerobium strain isolated from a natural gas well in the Utica Point Pleasant formation to investigate metabolic and physiological responses to growth under high-pressure subsurface conditions. Laboratory incubations confirmed the ability of Halanaerobium congolense strain WG8 to grow under pressures representative of deep shale formations (21 to 48 MPa). Under these conditions, broad metabolic and physiological shifts were identified, including higher abundances of proteins associated with the production of extracellular polymeric substances. Confocal laser scanning microscopy indicated that extracellular polymeric substance (EPS) production was associated with greater cell aggregation when biomass was cultured at high pressure.},
doi = {10.1128/AEM.00018-19},
journal = {Applied and Environmental Microbiology},
number = 12,
volume = 85,
place = {United States},
year = {2019},
month = {4}
}

Journal Article:
Free Publicly Available Full Text
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Cited by: 3 works
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Figures / Tables:

FIG 1 FIG 1: H. congolense WG8 growth at high pressure. Growth rates (red) and corresponding cell densities (gray) across a pressure gradient (0.1 to 48 MPa) are shown. Growth rate and cell densities decreased as incubation pressure increased.

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Works referenced in this record:

TonB-Dependent Transporters: Regulation, Structure, and Function
journal, October 2010


Pressure effects on in vivo microbial processes
journal, March 2002

  • Bartlett, D. H.
  • Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1595, Issue 1-2
  • DOI: 10.1016/S0167-4838(01)00357-0

Biofilm formation by a Bacillus subtilis strain that produces  -polyglutamate
journal, September 2006


Improved measurement of microbial activity in deep-sea sediments at in situ pressure and methane concentration: Measuring activity in deep-sea sediments
journal, October 2011

  • Bowles, Marshall W.; Samarkin, Vladimir A.; Joye, Samantha B.
  • Limnology and Oceanography: Methods, Vol. 9, Issue 10
  • DOI: 10.4319/lom.2011.9.499

Stress response of Escherichia coli to elevated hydrostatic pressure.
journal, November 1993


Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria
journal, November 2014

  • Schuchmann, Kai; Müller, Volker
  • Nature Reviews Microbiology, Vol. 12, Issue 12
  • DOI: 10.1038/nrmicro3365

Biofilm-Related Diseases and Omics: Global Transcriptional Profiling of Enterococcus faecium Reveals Different Gene Expression Patterns in the Biofilm and Planktonic Cells
journal, October 2017

  • Lim, Shu Yong; Teh, Cindy Shuan Ju; Thong, Kwai Lin
  • OMICS: A Journal of Integrative Biology, Vol. 21, Issue 10
  • DOI: 10.1089/omi.2017.0119

Bacterial biofilm shows persistent resistance to liquid wetting and gas penetration
journal, December 2010

  • Epstein, A. K.; Pokroy, B.; Seminara, A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 3
  • DOI: 10.1073/pnas.1011033108

Current developments in marine microbiology: high-pressure biotechnology and the genetic engineering of piezophiles
journal, June 2015


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

  • Davis, James P.; Struchtemeyer, Christopher G.; Elshahed, Mostafa S.
  • Microbial Ecology, Vol. 64, Issue 4
  • DOI: 10.1007/s00248-012-0073-3

Resilience of planktonic and biofilm cultures to supercritical CO2
journal, December 2008

  • Mitchell, Andrew C.; Phillips, Adrienne J.; Hamilton, Marty A.
  • The Journal of Supercritical Fluids, Vol. 47, Issue 2
  • DOI: 10.1016/j.supflu.2008.07.005

Pyruvate Ferredoxin Oxidoreductase and Its Radical Intermediate
journal, June 2003


Ethylene Glycol Metabolism in the Acetogen Acetobacterium woodii
journal, January 2016

  • Trifunović, Dragan; Schuchmann, Kai; Müller, Volker
  • Journal of Bacteriology, Vol. 198, Issue 7
  • DOI: 10.1128/JB.00942-15

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


Influence of Anaerobiosis and Low Temperature on Bacillus cereus Growth, Metabolism, and Membrane Properties
journal, January 2012

  • de Sarrau, Benoît; Clavel, Thierry; Clerté, Caroline
  • Applied and Environmental Microbiology, Vol. 78, Issue 6
  • DOI: 10.1128/AEM.06410-11

A role for TonB1 in biofilm formation and quorum sensing in Pseudomonas aeruginosa
journal, September 2007


Polyhedral organelles compartmenting bacterial metabolic processes
journal, March 2006


Heat Stress Dictates Microbial Lipid Composition along a Thermal Gradient in Marine Sediments
journal, August 2017

  • Sollich, Miriam; Yoshinaga, Marcos Y.; Häusler, Stefan
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.01550

Spermidine promotes Bacillus subtilis biofilm formation by activating expression of the matrix regulator slrR
journal, May 2017

  • Hobley, Laura; Li, Bin; Wood, Jennifer L.
  • Journal of Biological Chemistry, Vol. 292, Issue 29
  • DOI: 10.1074/jbc.M117.789644

Acetate-Enhanced Corrosion of Carbon Steel—Further Factors in Oilfield Environments
journal, March 2007

  • Pletcher, D.; Sidorin, D.; Hedges, B.
  • CORROSION, Vol. 63, Issue 3
  • DOI: 10.5006/1.3278356

Absence of TolC Impairs Biofilm Formation in Actinobacillus pleuropneumoniae by Reducing Initial Attachment
journal, September 2016


Morphological and proteomic analysis of biofilms from the Antarctic archaeon, Halorubrum lacusprofundi
journal, November 2016

  • Liao, Y.; Williams, T. J.; Ye, J.
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep37454

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

  • Lipus, Daniel; Vikram, Amit; Ross, Daniel
  • Applied and Environmental Microbiology, Vol. 83, Issue 8
  • DOI: 10.1128/AEM.02659-16

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

  • Cluff, Maryam A.; Hartsock, Angela; MacRae, Jean D.
  • Environmental Science & Technology, Vol. 48, Issue 11
  • DOI: 10.1021/es501173p

High-pressure tolerance in Halobacterium salinarum NRC-1 and other non-piezophilic prokaryotes
journal, January 2012


Biomass, bioactivity and biodiversity: microbial ecology of the deep subsurface: analysis of ester-linked phospholipid fatty acids
journal, July 1997


Simultaneous production of isopropanol, butanol, ethanol and 2,3-butanediol by Clostridium acetobutylicum ATCC 824 engineered strains
journal, January 2012


Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors
journal, November 2006

  • Paoletti, A. C.; Parmely, T. J.; Tomomori-Sato, C.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 50
  • DOI: 10.1073/pnas.0606379103

Mechanisms of biofilm resistance to antimicrobial agents
journal, January 2001


Classic Spotlight: Hfq, from a Specific Host Factor for Phage Replication to a Global Player in Riboregulation
journal, August 2016


Role and Regulation of Fatty Acid Biosynthesis in the Response of Shewanella piezotolerans WP3 to Different Temperatures and Pressures
journal, February 2009

  • Wang, F.; Xiao, X.; Ou, H. -Y.
  • Journal of Bacteriology, Vol. 191, Issue 8
  • DOI: 10.1128/JB.00498-08

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

  • Mouser, Paula J.; Borton, Mikayla; Darrah, Thomas H.
  • FEMS Microbiology Ecology, Vol. 92, Issue 11
  • DOI: 10.1093/femsec/fiw166

Discovery of an archetypal protein transport system in bacterial outer membranes
journal, April 2012

  • Selkrig, Joel; Mosbahi, Khedidja; Webb, Chaille T.
  • Nature Structural & Molecular Biology, Vol. 19, Issue 5
  • DOI: 10.1038/nsmb.2261

Differential Gene Expression Profiling of Staphylococcus aureus Cultivated under Biofilm and Planktonic Conditions
journal, May 2005


High pressure effects on the activity of glycolytic enzymes
journal, February 1975


Pullulanase: Role in Starch Hydrolysis and Potential Industrial Applications
journal, January 2012

  • Hii, Siew Ling; Tan, Joo Shun; Ling, Tau Chuan
  • Enzyme Research, Vol. 2012
  • DOI: 10.1155/2012/921362

Transcriptional Analysis of Biofilm Formation Processes in the Anaerobic, Hyperthermophilic Bacterium Thermotoga maritima
journal, October 2004


Involvement of Iron in Biofilm Formation by Staphylococcus aureus
journal, March 2012


Pores in Marcellus Shale: A Neutron Scattering and FIB-SEM Study
journal, February 2015


Pseudomonas aeruginosa Displays Multiple Phenotypes during Development as a Biofilm
journal, February 2002


Microbial diversity and methanogenic activity of Antrim Shale formation waters from recently fractured wells
journal, January 2013


Biochemistry of coenzyme B12-dependent glycerol and diol dehydratases and organization of the encoding genes
journal, December 1998


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

  • Murali Mohan, Arvind; Hartsock, Angela; Bibby, Kyle J.
  • Environmental Science & Technology, Vol. 47, Issue 22
  • DOI: 10.1021/es402928b

Micro/Nano-pore Network Analysis of Gas Flow in Shale Matrix
journal, August 2015

  • Zhang, Pengwei; Hu, Liming; Meegoda, Jay N.
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep13501

Understanding the Mechanism of B 12 -Dependent Diol Dehydratase:  A Synergistic Retro-Push−Pull Proposal
journal, February 2001

  • Smith, David M.; Golding, Bernard T.; Radom, Leo
  • Journal of the American Chemical Society, Vol. 123, Issue 8
  • DOI: 10.1021/ja001454z

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

  • Weljie, Aalim M.; Newton, Jack; Mercier, Pascal
  • Analytical Chemistry, Vol. 78, Issue 13
  • DOI: 10.1021/ac060209g

Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales
journal, June 2018

  • Borton, Mikayla A.; Hoyt, David W.; Roux, Simon
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 28
  • DOI: 10.1073/pnas.1800155115

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


Elimination of hydrogenase active site assembly blocks H2 production and increases ethanol yield in Clostridium thermocellum
journal, January 2015

  • Biswas, Ranjita; Zheng, Tianyong; Olson, Daniel G.
  • Biotechnology for Biofuels, Vol. 8, Issue 1
  • DOI: 10.1186/s13068-015-0204-4

Enhancing the Adaptability of the Deep-Sea Bacterium Shewanella piezotolerans WP3 to High Pressure and Low Temperature by Experimental Evolution under H 2 O 2 Stress
journal, December 2017

  • Xie, Zhe; Jian, Huahua; Jin, Zheng
  • Applied and Environmental Microbiology, Vol. 84, Issue 5
  • DOI: 10.1128/AEM.02342-17

Biofilm Matrix and Its Regulation in Pseudomonas aeruginosa
journal, October 2013

  • Wei, Qing; Ma, Luyan
  • International Journal of Molecular Sciences, Vol. 14, Issue 10
  • DOI: 10.3390/ijms141020983

High hydrostatic pressure adaptive strategies in an obligate piezophile Pyrococcus yayanosii
journal, June 2016

  • Michoud, Grégoire; Jebbar, Mohamed
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep27289

Growth Rates Made Easy
journal, October 2013

  • Hall, B. G.; Acar, H.; Nandipati, A.
  • Molecular Biology and Evolution, Vol. 31, Issue 1
  • DOI: 10.1093/molbev/mst187

Identification of Poly- N- acetylglucosamine as a Major Polysaccharide Component of the Bacillus subtilis Biofilm Matrix
journal, June 2015

  • Roux, Damien; Cywes-Bentley, Colette; Zhang, Yi-Fan
  • Journal of Biological Chemistry, Vol. 290, Issue 31
  • DOI: 10.1074/jbc.M115.648709

Self-induced mechanical stress can trigger biofilm formation in uropathogenic Escherichia coli
journal, October 2018


Protein Expression by Streptococcus mutans during Initial Stage of Biofilm Formation
journal, June 2004


Metabolic Capability of a Predominant Halanaerobium sp. in Hydraulically Fractured Gas Wells and Its Implication in Pipeline Corrosion
journal, June 2016

  • Liang, Renxing; Davidova, Irene A.; Marks, Christopher R.
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00988

The relationship between glycogen synthesis, biofilm formation and virulence in Salmonella enteritidis
journal, October 2000


The Phosphoenolpyruvate Phosphotransferase System Regulates Vibrio cholerae Biofilm Formation through Multiple Independent Pathways
journal, April 2010

  • Houot, L.; Chang, S.; Pickering, B. S.
  • Journal of Bacteriology, Vol. 192, Issue 12
  • DOI: 10.1128/JB.00213-10

Bacterial diguanylate cyclases: Structure, function and mechanism in exopolysaccharide biofilm development
journal, January 2015


Pressure as an environmental parameter for microbial life — A review
journal, December 2013


Biofilm Matrix Exoproteins Induce a Protective Immune Response against Staphylococcus aureus Biofilm Infection
journal, December 2013

  • Gil, Carmen; Solano, Cristina; Burgui, Saioa
  • Infection and Immunity, Vol. 82, Issue 3
  • DOI: 10.1128/IAI.01419-13

Vibrio fischeri  54 Controls Motility, Biofilm Formation, Luminescence, and Colonization
journal, April 2004


A Rapid Method of Total Lipid Extraction and Purification
journal, August 1959

  • Bligh, E. G.; Dyer, W. J.
  • Canadian Journal of Biochemistry and Physiology, Vol. 37, Issue 8
  • DOI: 10.1139/o59-099

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    In situ transformation of ethoxylate and glycol surfactants by shale-colonizing microorganisms during hydraulic fracturing
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      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.