skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Viral and bacterial community responses to stimulated Fe(III)–bioreduction during simulated subsurface bioremediation

Abstract

The delivery of fermentable substrate(s) to subsurface environments stimulates Fe(III)–bioreduction and achieves detoxification of organic/inorganic contaminants. Although, much research has been conducted on the microbiology of such engineered systems at lab and field scales, little attention has been given to the phage–host interactions and virus community dynamics in these environments. The objective was to determine the responses of soil bacterial communities and viral assemblages to stimulated anaerobic Fe(III)–bioreduction following electron donor (e.g. acetate) addition. Microbial communities, including viral assemblages, were investigated after 60 days of Fe(III)–bioreduction in laboratory–scale columns continuously fed with acetate–amended artificial groundwater. Viral abundances were greatest in the influent section and decreased along the flow path. Acetate availability was important in influencing bacterial diversity, microbial interactions and viral abundance and community composition. The impact of acetate addition was most evident in the influent section of the columns. The increased relative abundance of Fe(III)–reducing bacteria coincided with an increase in viral abundance in areas of the columns exhibiting the most Fe(III) reduction. In conclusion, the genetic composition of viruses in these column sections also differed from the control column and distal sections of acetate–treated columns suggesting viral communities responded to biostimulated Fe(III)–bioreduction.

Authors:
ORCiD logo [1];  [1]; ORCiD logo [2];  [1];  [1]; ORCiD logo [1];  [1];  [1]
  1. The Univ. of Tennessee, Knoxville, TN (United States)
  2. The Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1558476
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 21; Journal Issue: 6; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Liang, Xiaolong, Zhuang, Jie, Löffler, Frank E., Zhang, Yingyue, DeBruyn, Jennifer M., Wilhelm, Steven W., Schaeffer, Sean M., and Radosevich, Mark. Viral and bacterial community responses to stimulated Fe(III)–bioreduction during simulated subsurface bioremediation. United States: N. p., 2019. Web. doi:10.1111/1462-2920.14566.
Liang, Xiaolong, Zhuang, Jie, Löffler, Frank E., Zhang, Yingyue, DeBruyn, Jennifer M., Wilhelm, Steven W., Schaeffer, Sean M., & Radosevich, Mark. Viral and bacterial community responses to stimulated Fe(III)–bioreduction during simulated subsurface bioremediation. United States. doi:10.1111/1462-2920.14566.
Liang, Xiaolong, Zhuang, Jie, Löffler, Frank E., Zhang, Yingyue, DeBruyn, Jennifer M., Wilhelm, Steven W., Schaeffer, Sean M., and Radosevich, Mark. Sun . "Viral and bacterial community responses to stimulated Fe(III)–bioreduction during simulated subsurface bioremediation". United States. doi:10.1111/1462-2920.14566. https://www.osti.gov/servlets/purl/1558476.
@article{osti_1558476,
title = {Viral and bacterial community responses to stimulated Fe(III)–bioreduction during simulated subsurface bioremediation},
author = {Liang, Xiaolong and Zhuang, Jie and Löffler, Frank E. and Zhang, Yingyue and DeBruyn, Jennifer M. and Wilhelm, Steven W. and Schaeffer, Sean M. and Radosevich, Mark},
abstractNote = {The delivery of fermentable substrate(s) to subsurface environments stimulates Fe(III)–bioreduction and achieves detoxification of organic/inorganic contaminants. Although, much research has been conducted on the microbiology of such engineered systems at lab and field scales, little attention has been given to the phage–host interactions and virus community dynamics in these environments. The objective was to determine the responses of soil bacterial communities and viral assemblages to stimulated anaerobic Fe(III)–bioreduction following electron donor (e.g. acetate) addition. Microbial communities, including viral assemblages, were investigated after 60 days of Fe(III)–bioreduction in laboratory–scale columns continuously fed with acetate–amended artificial groundwater. Viral abundances were greatest in the influent section and decreased along the flow path. Acetate availability was important in influencing bacterial diversity, microbial interactions and viral abundance and community composition. The impact of acetate addition was most evident in the influent section of the columns. The increased relative abundance of Fe(III)–reducing bacteria coincided with an increase in viral abundance in areas of the columns exhibiting the most Fe(III) reduction. In conclusion, the genetic composition of viruses in these column sections also differed from the control column and distal sections of acetate–treated columns suggesting viral communities responded to biostimulated Fe(III)–bioreduction.},
doi = {10.1111/1462-2920.14566},
journal = {Environmental Microbiology},
number = 6,
volume = 21,
place = {United States},
year = {2019},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 3 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Bioremediation of uranium-contaminated groundwater: a systems approach to subsurface biogeochemistry
journal, June 2013

  • Williams, Kenneth H.; Bargar, John R.; Lloyd, Jonathan R.
  • Current Opinion in Biotechnology, Vol. 24, Issue 3
  • DOI: 10.1016/j.copbio.2012.10.008

Stimulating the In Situ Activity of Geobacter Species To Remove Uranium from the Groundwater of a Uranium-Contaminated Aquifer
journal, October 2003


Combination of aquifer thermal energy storage and enhanced bioremediation: Biological and chemical clogging
journal, February 2018


Viruses in soil: Nano-scale undead drivers of microbial life, biogeochemical turnover and ecosystem functions
journal, December 2018


Host-linked soil viral ecology along a permafrost thaw gradient
journal, July 2018


A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes
journal, January 2015

  • Weitz, Joshua S.; Stock, Charles A.; Wilhelm, Steven W.
  • The ISME Journal, Vol. 9, Issue 6
  • DOI: 10.1038/ismej.2014.220

Nutrients and Other Environmental Factors Influence Virus Abundances across Oxic and Hypoxic Marine Environments
journal, June 2017

  • Finke, Jan; Hunt, Brian; Winter, Christian
  • Viruses, Vol. 9, Issue 6
  • DOI: 10.3390/v9060152

Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing
journal, October 2018


Phage puppet masters of the marine microbial realm
journal, June 2018


Distribution of Organohalide-Respiring Bacteria between Solid and Aqueous Phases
journal, August 2014

  • Cápiro, Natalie L.; Wang, Yonggang; Hatt, Janet K.
  • Environmental Science & Technology, Vol. 48, Issue 18
  • DOI: 10.1021/es501320h

Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform
journal, June 2013

  • Kozich, James J.; Westcott, Sarah L.; Baxter, Nielson T.
  • Applied and Environmental Microbiology, Vol. 79, Issue 17
  • DOI: 10.1128/AEM.01043-13

Keystone taxa as drivers of microbiome structure and functioning
journal, May 2018

  • Banerjee, Samiran; Schlaeppi, Klaus; van der Heijden, Marcel G. A.
  • Nature Reviews Microbiology, Vol. 16, Issue 9
  • DOI: 10.1038/s41579-018-0024-1

Dominance of sulfur-fueled iron oxide reduction in low-sulfate freshwater sediments
journal, April 2015

  • Hansel, Colleen M.; Lentini, Chris J.; Tang, Yuanzhi
  • The ISME Journal, Vol. 9, Issue 11
  • DOI: 10.1038/ismej.2015.50

Changes in Bacterial and Archaeal Community Structure and Functional Diversity along a Geochemically Variable Soil Profile
journal, January 2008

  • Hansel, C. M.; Fendorf, S.; Jardine, P. M.
  • Applied and Environmental Microbiology, Vol. 74, Issue 5
  • DOI: 10.1128/AEM.01787-07

Impact of Organic Carbon Electron Donors on Microbial Community Development under Iron- and Sulfate-Reducing Conditions
journal, January 2016


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


Abundance and Distribution of Microbial Cells and Viruses in an Alluvial Aquifer
journal, July 2017


The ‘Neglected’ Soil Virome – Potential Role and Impact
journal, August 2018


Marine viruses — major players in the global ecosystem
journal, October 2007


Deciphering the virus-to-prokaryote ratio (VPR): insights into virus-host relationships in a variety of ecosystems: Deciphering the virus-to-prokaryote ratio
journal, April 2016

  • Parikka, Kaarle J.; Le Romancer, Marc; Wauters, Nina
  • Biological Reviews, Vol. 92, Issue 2
  • DOI: 10.1111/brv.12271

Inferring Correlation Networks from Genomic Survey Data
journal, September 2012


Belowground biodiversity and ecosystem functioning
journal, November 2014

  • Bardgett, Richard D.; van der Putten, Wim H.
  • Nature, Vol. 515, Issue 7528
  • DOI: 10.1038/nature13855

A Host-Produced Quorum-Sensing Autoinducer Controls a Phage Lysis-Lysogeny Decision
journal, January 2019


Redox cycling of Fe(II) and Fe(III) in magnetite by Fe-metabolizing bacteria
journal, March 2015


Anaerobic Benzene Oxidation via Phenol in Geobacter metallireducens
journal, October 2013

  • Zhang, Tian; Tremblay, Pier-Luc; Chaurasia, Akhilesh Kumar
  • Applied and Environmental Microbiology, Vol. 79, Issue 24
  • DOI: 10.1128/AEM.03134-13

Soil aggregation: Influence on microbial biomass and implications for biological processes
journal, January 2015


Comparative Analysis of Bacteriophages and Bacteria Removal in Soils and Pyrophyllite-Amended Soils: Column Experiments
journal, February 2017

  • Park, Jeong-Ann; Kang, Jin-Kyu; Kim, Song-Bae
  • Water, Air, & Soil Pollution, Vol. 228, Issue 3
  • DOI: 10.1007/s11270-017-3288-6

Cultivation-Based Assessment of Lysogeny Among Soil Bacteria
journal, March 2008

  • Williamson, Kurt E.; Schnitker, Jennifer B.; Radosevich, Mark
  • Microbial Ecology, Vol. 56, Issue 3
  • DOI: 10.1007/s00248-008-9362-2

Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain
journal, February 2013


Embracing the unknown: disentangling the complexities of the soil microbiome
journal, August 2017


Environmental influences on virus-host interactions in an Australian subtropical reservoir: Virus-host interactions in the sub-tropics
journal, November 2011


Patterns and Processes of Microbial Community Assembly
journal, September 2013

  • Nemergut, D. R.; Schmidt, S. K.; Fukami, T.
  • Microbiology and Molecular Biology Reviews, Vol. 77, Issue 3
  • DOI: 10.1128/MMBR.00051-12

In situ vadose zone bioremediation
journal, June 2014


Kinetics of calcite precipitation induced by ureolytic bacteria at 10 to 20°C in artificial groundwater
journal, April 2004


Effects of Nitrate on the Stability of Uranium in a Bioreduced Region of the Subsurface
journal, July 2010

  • Wu, Wei-Min; Carley, Jack; Green, Stefan J.
  • Environmental Science & Technology, Vol. 44, Issue 13
  • DOI: 10.1021/es1000837

Bacteriophage–prokaryote dynamics and interaction within anaerobic digestion processes across time and space
journal, May 2017


Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists
journal, November 2013

  • Chow, Cheryl-Emiliane T.; Kim, Diane Y.; Sachdeva, Rohan
  • The ISME Journal, Vol. 8, Issue 4
  • DOI: 10.1038/ismej.2013.199

In Situ Chemical Oxidation of Contaminated Groundwater by Persulfate: Decomposition by Fe(III)- and Mn(IV)-Containing Oxides and Aquifer Materials
journal, August 2014

  • Liu, Haizhou; Bruton, Thomas A.; Doyle, Fiona M.
  • Environmental Science & Technology, Vol. 48, Issue 17
  • DOI: 10.1021/es502056d

Iron oxide nanoparticles in geomicrobiology: from biogeochemistry to bioremediation
journal, September 2013

  • Braunschweig, Juliane; Bosch, Julian; Meckenstock, Rainer U.
  • New Biotechnology, Vol. 30, Issue 6
  • DOI: 10.1016/j.nbt.2013.03.008

Viral ecology comes of age: Crystal ball
journal, February 2017

  • Sullivan, Matthew B.; Weitz, Joshua S.; Wilhelm, Steven
  • Environmental Microbiology Reports, Vol. 9, Issue 1
  • DOI: 10.1111/1758-2229.12504

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
  • DOI: 10.1093/nar/gks1219

Abundance and Diversity of Viruses in Six Delaware Soils
journal, June 2005


The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle
journal, October 2014

  • Melton, Emily D.; Swanner, Elizabeth D.; Behrens, Sebastian
  • Nature Reviews Microbiology, Vol. 12, Issue 12
  • DOI: 10.1038/nrmicro3347

Direct Assessment of Viral Diversity in Soils by Random PCR Amplification of Polymorphic DNA
journal, June 2013

  • Srinivasiah, Sharath; Lovett, Jacqueline; Polson, Shawn
  • Applied and Environmental Microbiology, Vol. 79, Issue 18
  • DOI: 10.1128/AEM.00268-13

Evidence of Geobacter-associated phage in a uranium-contaminated aquifer
journal, August 2014

  • Holmes, Dawn E.; Giloteaux, Ludovic; Chaurasia, Akhilesh K.
  • The ISME Journal, Vol. 9, Issue 2
  • DOI: 10.1038/ismej.2014.128

Incidence of lysogeny within temperate and extreme soil environments
journal, October 2007


Size-Driven Structural and Thermodynamic Complexity in Iron Oxides
journal, March 2008


Biogeochemical Redox Processes and their Impact on Contaminant Dynamics
journal, January 2010

  • Borch, Thomas; Kretzschmar, Ruben; Kappler, Andreas
  • Environmental Science & Technology, Vol. 44, Issue 1
  • DOI: 10.1021/es9026248

Anaerobic lipopeptide biosurfactant production by an engineered bacterial strain for in situ microbial enhanced oil recovery
journal, January 2017

  • Liang, Xiaolong; Shi, Rongjiu; Radosevich, Mark
  • RSC Advances, Vol. 7, Issue 33
  • DOI: 10.1039/C7RA02453C

Viruses control dominant bacteria colonizing the terrestrial deep biosphere after hydraulic fracturing
journal, December 2018


Spatial organization of bacterial populations in response to oxygen and carbon counter-gradients in pore networks
journal, February 2018


Viruses and Nutrient Cycles in the Sea
journal, October 1999

  • Wilhelm, Steven W.; Suttle, Curtis A.
  • BioScience, Vol. 49, Issue 10
  • DOI: 10.2307/1313569

Viruses in Soil Ecosystems: An Unknown Quantity Within an Unexplored Territory
journal, September 2017


Compact graphical representation of phylogenetic data and metadata with GraPhlAn
journal, January 2015

  • Asnicar, Francesco; Weingart, George; Tickle, Timothy L.
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.1029

Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction
journal, October 2006

  • Weber, Karrie A.; Achenbach, Laurie A.; Coates, John D.
  • Nature Reviews Microbiology, Vol. 4, Issue 10, p. 752-764
  • DOI: 10.1038/nrmicro1490

Viral release of iron and its bioavailability to marine plankton
journal, September 2004

  • Poorvin, Leo; Rinta-Kanto, Johanna M.; Hutchins, David A.
  • Limnology and Oceanography, Vol. 49, Issue 5
  • DOI: 10.4319/lo.2004.49.5.1734

Numerical Modeling of Arsenic Mobility during Reductive Iron-Mineral Transformations
journal, February 2016

  • Rawson, Joey; Prommer, Henning; Siade, Adam
  • Environmental Science & Technology, Vol. 50, Issue 5
  • DOI: 10.1021/acs.est.5b05956

Acyl-Homoserine Lactones Can Induce Virus Production in Lysogenic Bacteria: an Alternative Paradigm for Prophage Induction
journal, September 2009

  • Ghosh, D.; Roy, K.; Williamson, K. E.
  • Applied and Environmental Microbiology, Vol. 75, Issue 22
  • DOI: 10.1128/AEM.00950-09

Extracellular electron transfer mechanisms between microorganisms and minerals
journal, August 2016

  • Shi, Liang; Dong, Hailiang; Reguera, Gemma
  • Nature Reviews Microbiology, Vol. 14, Issue 10
  • DOI: 10.1038/nrmicro.2016.93

Linking internal and external bacterial community control gives mechanistic framework for pelagic virus-to-bacteria ratios: Framework for VBR
journal, July 2016

  • Våge, Selina; Pree, Bernadette; Thingstad, T. Frede
  • Environmental Microbiology, Vol. 18, Issue 11
  • DOI: 10.1111/1462-2920.13391

Bacteria-Phage Antagonistic Coevolution in Soil
journal, March 2011


Re-examination of the relationship between marine virus and microbial cell abundances
journal, January 2016

  • Wigington, Charles H.; Sonderegger, Derek; Brussaard, Corina P. D.
  • Nature Microbiology, Vol. 1, Issue 3
  • DOI: 10.1038/nmicrobiol.2015.24

Microbial Communities in Contaminated Sediments, Associated with Bioremediation of Uranium to Submicromolar Levels
journal, May 2008

  • Cardenas, E.; Wu, W. -M.; Leigh, M. B.
  • Applied and Environmental Microbiology, Vol. 74, Issue 12
  • DOI: 10.1128/AEM.02308-07

Microbial community structure and its functional implications
journal, May 2009


Bacteria–phage coevolution as a driver of ecological and evolutionary processes in microbial communities
journal, September 2014


Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient
journal, August 2012


Bacteria–Bacteriophage Coevolution in the Human Gut: Implications for Microbial Diversity and Functionality
journal, August 2017


Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics
journal, August 2015

  • Brum, Jennifer R.; Hurwitz, Bonnie L.; Schofield, Oscar
  • The ISME Journal, Vol. 10, Issue 2
  • DOI: 10.1038/ismej.2015.125

Toward an Ecological Classification of soil Bacteria
journal, June 2007

  • Fierer, Noah; Bradford, Mark A.; Jackson, Robert B.
  • Ecology, Vol. 88, Issue 6
  • DOI: 10.1890/05-1839