Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Surface Water Microbial Community Response to the Biocide 2,2-Dibromo-3-Nitrilopropionamide, Used in Unconventional Oil and Gas Extraction

Abstract

Production of unconventional oil and gas continues to rise, but the effects of high-density hydraulic fracturing (HF) activity near aquatic ecosystems are not fully understood. A commonly used biocide in HF, 2,2-dibromo-3-nitrilopropionamide (DBNPA), was studied in microcosms of HF-impacted (HF+) versus HF-unimpacted (HF-) surface water streams to (i) compare the microbial community response, (ii) investigate DBNPA degradation products based on past HF exposure, and (iii) compare the microbial community response differences and similarities between the HF biocides DBNPA and glutaraldehyde. The microbial community responded to DBNPA differently in HF-impacted versus HF-unimpacted microcosms in terms of the number of 16S rRNA gene copies quantified, alpha and beta diversity, and differential abundance analyses of microbial community composition through time. The differences in microbial community changes affected degradation dynamics. HF-impacted microbial communities were more sensitive to DBNPA, causing the biocide and by-products of the degradation to persist for longer than in HF-unimpacted microcosms. A total of 17 DBNPA by-products were detected, many of them not widely known as DBNPA by-products. Many of the brominated by-products detected that are believed to be uncharacterized may pose environmental and health impacts. Similar taxa were able to tolerate glutaraldehyde and DBNPA; however, DBNPA was not as effectivemore » for microbial control, as indicated by a smaller overall decrease of 16S rRNA gene copies/ml after exposure to the biocide, and a more diverse set of taxa was able to tolerate it. These findings suggest that past HF activity in streams can affect the microbial community response to environmental perturbation such as that caused by the biocide DBNPA.« less

Authors:
 [1]; ORCiD logo [2];  [1];  [3];  [4];  [4];  [4];  [5];  [5];  [1];  [5]; ORCiD logo [6]
+ Show Author Affiliations
  1. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Michigan Technological Univ., Houghton, MI (United States)
  3. Chinese Academy of Sciences (CAS), Liaoning, Shenyang (China). Key Lab. of Pollution Ecology and Environmental Engineering, Inst. of Applied Ecology; Univ. of Tennessee, Knoxville, TN (United States)
  4. Univ. of Tennessee, Knoxville, TN (United States)
  5. Juniata College, Huntingdon, PA (United States)
  6. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Inst. for a Secure and Sustainable Environment, Knoxville, TN (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF); Methane Center in the Institute for a Secure and Sustainable Environment
OSTI Identifier:
1580966
Alternate Identifier(s):
OSTI ID: 1608200
Grant/Contract Number:  
AC02-05CH11231; AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 85; Journal Issue: 21; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Campa, Maria Fernanda, Techtmann, Stephen M., Ladd, Mallory P., Yan, Jun, Patterson, Megan, Garcia de Matos Amaral, Amanda, Carter, Kimberly E., Ulrich, Nikea, Grant, Christopher J., Hettich, Robert L., Lamendella, Regina, and Hazen, Terry C. Surface Water Microbial Community Response to the Biocide 2,2-Dibromo-3-Nitrilopropionamide, Used in Unconventional Oil and Gas Extraction. United States: N. p., 2019. Web. doi:10.1128/AEM.01336-19.
Copy to clipboard
Campa, Maria Fernanda, Techtmann, Stephen M., Ladd, Mallory P., Yan, Jun, Patterson, Megan, Garcia de Matos Amaral, Amanda, Carter, Kimberly E., Ulrich, Nikea, Grant, Christopher J., Hettich, Robert L., Lamendella, Regina, & Hazen, Terry C. Surface Water Microbial Community Response to the Biocide 2,2-Dibromo-3-Nitrilopropionamide, Used in Unconventional Oil and Gas Extraction. United States. https://doi.org/10.1128/AEM.01336-19
Copy to clipboard
Campa, Maria Fernanda, Techtmann, Stephen M., Ladd, Mallory P., Yan, Jun, Patterson, Megan, Garcia de Matos Amaral, Amanda, Carter, Kimberly E., Ulrich, Nikea, Grant, Christopher J., Hettich, Robert L., Lamendella, Regina, and Hazen, Terry C. Fri . "Surface Water Microbial Community Response to the Biocide 2,2-Dibromo-3-Nitrilopropionamide, Used in Unconventional Oil and Gas Extraction". United States. https://doi.org/10.1128/AEM.01336-19. https://www.osti.gov/servlets/purl/1580966.
Copy to clipboard
@article{osti_1580966,
title = {Surface Water Microbial Community Response to the Biocide 2,2-Dibromo-3-Nitrilopropionamide, Used in Unconventional Oil and Gas Extraction},
author = {Campa, Maria Fernanda and Techtmann, Stephen M. and Ladd, Mallory P. and Yan, Jun and Patterson, Megan and Garcia de Matos Amaral, Amanda and Carter, Kimberly E. and Ulrich, Nikea and Grant, Christopher J. and Hettich, Robert L. and Lamendella, Regina and Hazen, Terry C.},
abstractNote = {Production of unconventional oil and gas continues to rise, but the effects of high-density hydraulic fracturing (HF) activity near aquatic ecosystems are not fully understood. A commonly used biocide in HF, 2,2-dibromo-3-nitrilopropionamide (DBNPA), was studied in microcosms of HF-impacted (HF+) versus HF-unimpacted (HF-) surface water streams to (i) compare the microbial community response, (ii) investigate DBNPA degradation products based on past HF exposure, and (iii) compare the microbial community response differences and similarities between the HF biocides DBNPA and glutaraldehyde. The microbial community responded to DBNPA differently in HF-impacted versus HF-unimpacted microcosms in terms of the number of 16S rRNA gene copies quantified, alpha and beta diversity, and differential abundance analyses of microbial community composition through time. The differences in microbial community changes affected degradation dynamics. HF-impacted microbial communities were more sensitive to DBNPA, causing the biocide and by-products of the degradation to persist for longer than in HF-unimpacted microcosms. A total of 17 DBNPA by-products were detected, many of them not widely known as DBNPA by-products. Many of the brominated by-products detected that are believed to be uncharacterized may pose environmental and health impacts. Similar taxa were able to tolerate glutaraldehyde and DBNPA; however, DBNPA was not as effective for microbial control, as indicated by a smaller overall decrease of 16S rRNA gene copies/ml after exposure to the biocide, and a more diverse set of taxa was able to tolerate it. These findings suggest that past HF activity in streams can affect the microbial community response to environmental perturbation such as that caused by the biocide DBNPA.},
doi = {10.1128/AEM.01336-19},
journal = {Applied and Environmental Microbiology},
number = 21,
volume = 85,
place = {United States},
year = {2019},
month = {8}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/AEM.01336-19
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 1 work
Citation information provided by
Web of Science
Save / Share:
Export Metadata
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.

Works referenced in this record:

Physical, chemical, and biological characteristics of compounds used in hydraulic fracturing
journal, June 2014

UCHIME improves sensitivity and speed of chimera detection
journal, June 2011

Active efflux, a common mechanism for biocide and antibiotic resistance
journal, May 2002

Bacterial Biomarkers of Marcellus Shale Activity in Pennsylvania
journal, August 2018

  • Chen See, Jeremy R.; Ulrich, Nikea; Nwanosike, Hephzibah
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.01697

Downhole Transformation of the Hydraulic Fracturing Fluid Biocide Glutaraldehyde: Implications for Flowback and Produced Water Quality
journal, September 2016

  • Kahrilas, Genevieve A.; Blotevogel, Jens; Corrin, Edward R.
  • Environmental Science & Technology, Vol. 50, Issue 20
  • DOI: 10.1021/acs.est.6b02881

Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
journal, July 2006

  • DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.
  • Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072
  • DOI: 10.1128/AEM.03006-05

Fundamentals of Microbial Community Resistance and Resilience
journal, January 2012

PyNAST: a flexible tool for aligning sequences to a template alignment
journal, November 2009

Microbial dehalogenation
journal, September 1995

  • Slater, J. Howard; Bull, Alan T.; Hardman, David J.
  • Biodegradation, Vol. 6, Issue 3
  • DOI: 10.1007/bf00700456

Mechanisms of bacterial insusceptibility to biocides
journal, August 2001

VEGAN, a package of R functions for community ecology
journal, January 2003

Hydrocarbon-Degrading Bacteria and the Bacterial Community Response in Gulf of Mexico Beach Sands Impacted by the Deepwater Horizon Oil Spill
journal, September 2011

  • Kostka, Joel E.; Prakash, Om; Overholt, Will A.
  • Applied and Environmental Microbiology, Vol. 77, Issue 22
  • DOI: 10.1128/AEM.05402-11

Metatranscriptome analysis of active microbial communities in produced water samples from the Marcellus Shale
journal, July 2016

2,2-Dibromo-3-nitrilopropionamide (DBNPA) chemical degradation in natural waters: Experimental evaluation and modeling of competitive pathways
journal, July 1987

Drinking Water Disinfection Byproducts (DBPs) and Human Health Effects: Multidisciplinary Challenges and Opportunities
journal, January 2018

  • Li, Xing-Fang; Mitch, William A.
  • Environmental Science & Technology, Vol. 52, Issue 4
  • DOI: 10.1021/acs.est.7b05440

Wastewater Disposal from Unconventional Oil and Gas Development Degrades Stream Quality at a West Virginia Injection Facility
journal, May 2016

  • Akob, Denise M.; Mumford, Adam C.; Orem, William
  • Environmental Science & Technology, Vol. 50, Issue 11
  • DOI: 10.1021/acs.est.6b00428

Can marine bacteria be recruited from freshwater sources and the air?
journal, June 2014

  • Comte, Jérôme; Lindström, Eva S.; Eiler, Alexander
  • The ISME Journal, Vol. 8, Issue 12
  • DOI: 10.1038/ismej.2014.89

Sustained persulfate activation using solid iron: Kinetics and application to ciprofloxacin degradation
journal, January 2017

Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007

  • Wang, Q.; Garrity, G. M.; Tiedje, J. M.
  • Applied and Environmental Microbiology, Vol. 73, Issue 16
  • DOI: 10.1128/AEM.00062-07

Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible
journal, April 2014

Rates and products of decomposition of 2,2-dibromo-3-nitrilopropionamide
journal, May 1973

  • Exner, Jurgen H.; Burk, George A.; Kyriacou, Demetrios
  • Journal of Agricultural and Food Chemistry, Vol. 21, Issue 5
  • DOI: 10.1021/jf60189a012

UniFrac: an effective distance metric for microbial community comparison
journal, September 2010

  • Lozupone, Catherine; Lladser, Manuel E.; Knights, Dan
  • The ISME Journal, Vol. 5, Issue 2
  • DOI: 10.1038/ismej.2010.133

Efflux as a Glutaraldehyde Resistance Mechanism in Pseudomonas fluorescens and Pseudomonas aeruginosa Biofilms
journal, March 2015

  • Vikram, Amit; Bomberger, Jennifer M.; Bibby, Kyle J.
  • Antimicrobial Agents and Chemotherapy, Vol. 59, Issue 6
  • DOI: 10.1128/AAC.05152-14

Antiseptics and Disinfectants: Activity, Action, and Resistance
journal, January 1999

  • McDonnell, Gerald; Russell, A. Denver
  • Clinical Microbiology Reviews, Vol. 12, Issue 1
  • DOI: 10.1128/CMR.12.1.147

Microbial dehalogenation
journal, June 2001

  • Janssen, Dick B.; Oppentocht, Jantien E.; Poelarends, Gerrit J.
  • Current Opinion in Biotechnology, Vol. 12, Issue 3
  • DOI: 10.1016/S0958-1669(00)00208-1

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

Discharges of produced waters from oil and gas extraction via wastewater treatment plants are sources of disinfection by-products to receiving streams
journal, January 2014

phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013

Antibiotic resistance genes in water environment
journal, March 2009

  • Zhang, Xu-Xiang; Zhang, Tong; Fang, Herbert H. P.
  • Applied Microbiology and Biotechnology, Vol. 82, Issue 3
  • DOI: 10.1007/s00253-008-1829-z

Marcellus and mercury: Assessing potential impacts of unconventional natural gas extraction on aquatic ecosystems in northwestern Pennsylvania
journal, March 2015

  • Grant, Christopher J.; Weimer, Alexander B.; Marks, Nicole K.
  • Journal of Environmental Science and Health, Part A, Vol. 50, Issue 5
  • DOI: 10.1080/10934529.2015.992670

Produced Water Exposure Alters Bacterial Response to Biocides
journal, October 2014

  • Vikram, Amit; Lipus, Daniel; Bibby, Kyle
  • Environmental Science & Technology, Vol. 48, Issue 21
  • DOI: 10.1021/es5036915

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

Organic geochemistry and toxicology of a stream impacted by unconventional oil and gas wastewater disposal operations
journal, May 2017

Spills of Hydraulic Fracturing Chemicals on Agricultural Topsoil: Biodegradation, Sorption, and Co-contaminant Interactions
journal, May 2016

  • McLaughlin, Molly C.; Borch, Thomas; Blotevogel, Jens
  • Environmental Science & Technology, Vol. 50, Issue 11
  • DOI: 10.1021/acs.est.6b00240

Bacterial communities associated with hydraulic fracturing fluids in thermogenic natural gas wells in North Central Texas, USA
journal, November 2011

Response of Aquatic Bacterial Communities to Hydraulic Fracturing in Northwestern Pennsylvania: A Five-Year Study
journal, April 2018

Natural Bacterial Communities Serve as Quantitative Geochemical Biosensors
journal, May 2015

Efflux pumps as antimicrobial resistance mechanisms
journal, January 2007

Analysis of BTEX groundwater concentrations from surface spills associated with hydraulic fracturing operations
journal, January 2013

  • Gross, Sherilyn A.; Avens, Heather J.; Banducci, Amber M.
  • Journal of the Air & Waste Management Association, Vol. 63, Issue 4
  • DOI: 10.1080/10962247.2012.759166

A Comprehensive Analysis of Groundwater Quality in The Barnett Shale Region
journal, June 2015

  • Hildenbrand, Zacariah L.; Carlton, Doug D.; Fontenot, Brian E.
  • Environmental Science & Technology, Vol. 49, Issue 13
  • DOI: 10.1021/acs.est.5b01526

Inhibition of Biodegradation of Hydraulic Fracturing Compounds by Glutaraldehyde: Groundwater Column and Microcosm Experiments
journal, August 2017

  • Rogers, Jessica D.; Ferrer, Imma; Tummings, Shantal S.
  • Environmental Science & Technology, Vol. 51, Issue 17
  • DOI: 10.1021/acs.est.7b02316

Fracked ecology: Response of aquatic trophic structure and mercury biomagnification dynamics in the Marcellus Shale Formation
journal, October 2016

  • Grant, Christopher James; Lutz, Allison K.; Kulig, Aaron D.
  • Ecotoxicology, Vol. 25, Issue 10
  • DOI: 10.1007/s10646-016-1717-8

Characterization and biological removal of organic compounds from hydraulic fracturing produced water
journal, January 2019

  • Akyon, Benay; McLaughlin, Molly; Hernández, Felipe
  • Environmental Science: Processes & Impacts, Vol. 21, Issue 2
  • DOI: 10.1039/C8EM00354H

A comparison of DNA- and RNA-based clone libraries from the same marine bacterioplankton community
journal, February 2005

  • Moeseneder, Markus M.; Arrieta, Jesus M.; Herndl, Gerhard J.
  • FEMS Microbiology Ecology, Vol. 51, Issue 3
  • DOI: 10.1016/j.femsec.2004.09.012

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Differential abundance analysis for microbial marker-gene surveys
journal, September 2013

  • Paulson, Joseph N.; Stine, O. Colin; Bravo, Héctor Corrada
  • Nature Methods, Vol. 10, Issue 12
  • DOI: 10.1038/nmeth.2658

VEGAN, a package of R functions for community ecology
journal, April 2003

Isolation and Identification of Methylobacterium Species from the Tap Water in Hospitals in Japan and Their Antibiotic Susceptibility
journal, January 2006

The ecology and biotechnology of sulphate-reducing bacteria
journal, May 2008

  • Muyzer, Gerard; Stams, Alfons J. M.
  • Nature Reviews Microbiology, Vol. 6, Issue 6
  • DOI: 10.1038/nrmicro1892

Common Hydraulic Fracturing Fluid Additives Alter the Structure and Function of Anaerobic Microbial Communities
journal, February 2018

  • Mumford, Adam C.; Akob, Denise M.; Klinges, J. Grace
  • Applied and Environmental Microbiology, Vol. 84, Issue 8
  • DOI: 10.1128/AEM.02729-17

Biocides in Hydraulic Fracturing Fluids: A Critical Review of Their Usage, Mobility, Degradation, and Toxicity
journal, December 2014

  • Kahrilas, Genevieve A.; Blotevogel, Jens; Stewart, Philip S.
  • Environmental Science & Technology, Vol. 49, Issue 1
  • DOI: 10.1021/es503724k

Impacts of Glutaraldehyde on Microbial Community Structure and Degradation Potential in Streams Impacted by Hydraulic Fracturing
journal, April 2018

  • Campa, Maria Fernanda; Techtmann, Stephen M.; Gibson, Caleb M.
  • Environmental Science & Technology, Vol. 52, Issue 10
  • DOI: 10.1021/acs.est.8b00239

Potential for Chemolithoautotrophy Among Ubiquitous Bacteria Lineages in the Dark Ocean
journal, September 2011

Stream microbial ecology
journal, March 2010

  • Findlay, Stuart
  • Journal of the North American Benthological Society, Vol. 29, Issue 1
  • DOI: 10.1899/09-023.1

EMPeror: a tool for visualizing high-throughput microbial community data
journal, November 2013

  • Vázquez-Baeza, Yoshiki; Pirrung, Meg; Gonzalez, Antonio
  • GigaScience, Vol. 2, Issue 1
  • DOI: 10.1186/2047-217X-2-16

Elevated levels of diesel range organic compounds in groundwater near Marcellus gas operations are derived from surface activities
journal, October 2015

  • Drollette, Brian D.; Hoelzer, Kathrin; Warner, Nathaniel R.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 43
  • DOI: 10.1073/pnas.1511474112

Assessing impacts of unconventional natural gas extraction on microbial communities in headwater stream ecosystems in Northwestern Pennsylvania
journal, November 2014

Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals
journal, September 2006

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014

Disinfection by-products and other emerging contaminants in drinking water
journal, November 2003

Overview of Disinfection By-products and Associated Health Effects
journal, January 2015

  • Villanueva, Cristina M.; Cordier, Sylvaine; Font-Ribera, Laia
  • Current Environmental Health Reports, Vol. 2, Issue 1
  • DOI: 10.1007/s40572-014-0032-x

2,2-Dibromo-3-Nitrilopropionamide, a Compound with Slimicidal Activity
journal, October 1972

Microbial reductive dehalogenation
journal, September 1992

Bacterial dehalogenases: biochemistry, genetics, and biotechnological applications
journal, December 1994

Microbial community structure and functional properties in permanently and seasonally flooded areas in Poyang Lake
journal, March 2020

Microbial Dysbiosis During Simian Immunodeficiency Virus Infection is Partially Reverted with Combination Anti-retroviral Therapy
journal, April 2020

  • Blum, Faith C.; Hardy, Britney L.; Bishop-Lilly, Kimberly A.
  • Scientific Reports, Vol. 10, Issue 1
  • DOI: 10.1038/s41598-020-63196-0

The Gut Microbiome in Autism: Study-Site Effects and Longitudinal Analysis of Behavior Change
journal, April 2021

Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
journal, March 2021

Antiseptics and Disinfectants: Activity, Action, and Resistance
journal, January 2001

Common hydraulic fracturing fluid additives alter the structure and function of anaerobic microbial communities
dataset, January 2018

  • [0000-0002-5123-1007], Adam C. Mumford [0000-0002-8082-8910], Denise M. Akob [0000-0003-1534-3025], J. Grace Klinges, And Isabelle M. Cozzarelli
  • U.S. Geological Survey
  • DOI: 10.5066/f73n229q

Waste Not, Want Not: Why Rarefying Microbiome Data is Inadmissible
text, January 2013

    Sort by:
    [ × clear filter / sort ]

    Similar Records in DOE PAGES and OSTI.GOV collections: