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

Title: Impact of Organic Carbon Electron Donors on Microbial Community Development under Iron- and Sulfate-Reducing Conditions

Abstract

Although iron- and sulfate-reducing bacteria in subsurface environments have crucial roles in biogeochemical cycling of C, Fe, and S, how specific electron donors impact the compositional structure and activity of native iron- and/or sulfate-reducing communities is largely unknown. To understand this better, we created bicarbonate-buffered batch systems in duplicate with three different electron donors (acetate, lactate, or glucose) paired with ferrihydrite and sulfate as the electron acceptors and inoculated them with subsurface sediment as the microbial inoculum. Sulfate and ferrihydrite reduction occurred simultaneously and were faster with lactate than with acetate. 16S rRNA-based sequence analysis of the communities over time revealed that Desulfotomaculum was the major driver for sulfate reduction coupled with propionate oxidation in lactate-amended incubations. The reduction of sulfate resulted in sulfide production and subsequent abiotic reduction of ferrihydrite. In contrast, glucose promoted faster reduction of ferrihydrite, but without reduction of sulfate. Interestingly, the glucose-amended incubations led to two different biogeochemical trajectories among replicate bottles that resulted in distinct coloration (white and brown). The two outcomes in geochemical evolution might be due to the stochastic evolution of the microbial communities or subtle differences in the initial composition of the fermenting microbial community and its development via the usemore » of different glucose fermentation pathways available within the community. Synchrotron-based x-ray analysis indicated that siderite and amorphous Fe(II) were formed in the replicate bottles with glucose, while ferrous sulfide and vivianite were formed with lactate or acetate. As a result, these data sets reveal that use of different C utilization pathways projects significant changes in microbial community composition over time that uniquely impact both the geochemistry and mineralogy of subsurface environments.« less

Authors:
 [1];  [2];  [2];  [2];  [2];  [2];  [2];  [3]
  1. Argonne National Lab. (ANL), Argonne, IL (United States); Korea Institute of Science and Technology (KIST) - Gangneung Institute, Gangneung (South Korea)
  2. Argonne National Lab. (ANL), Argonne, IL (United States)
  3. Univ. of Akron, Akron, OH (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Subsurface Biogeochemical Research
OSTI Identifier:
1399243
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; electron donor; iron reduction; microbial community development; sulfate reduction; sulfates; glucose; sulfides; glucose metabolism; sediment; fermentation; oxidation

Citation Formats

Kwon, Man Jae, O’Loughlin, Edward J., Boyanov, Maxim I., Brulc, Jennifer M., Johnston, Eric R., Kemner, Kenneth M., Antonopoulos, Dionysios A., and Senko, John M. Impact of Organic Carbon Electron Donors on Microbial Community Development under Iron- and Sulfate-Reducing Conditions. United States: N. p., 2016. Web. doi:10.1371/journal.pone.0146689.
Kwon, Man Jae, O’Loughlin, Edward J., Boyanov, Maxim I., Brulc, Jennifer M., Johnston, Eric R., Kemner, Kenneth M., Antonopoulos, Dionysios A., & Senko, John M. Impact of Organic Carbon Electron Donors on Microbial Community Development under Iron- and Sulfate-Reducing Conditions. United States. doi:10.1371/journal.pone.0146689.
Kwon, Man Jae, O’Loughlin, Edward J., Boyanov, Maxim I., Brulc, Jennifer M., Johnston, Eric R., Kemner, Kenneth M., Antonopoulos, Dionysios A., and Senko, John M. Fri . "Impact of Organic Carbon Electron Donors on Microbial Community Development under Iron- and Sulfate-Reducing Conditions". United States. doi:10.1371/journal.pone.0146689. https://www.osti.gov/servlets/purl/1399243.
@article{osti_1399243,
title = {Impact of Organic Carbon Electron Donors on Microbial Community Development under Iron- and Sulfate-Reducing Conditions},
author = {Kwon, Man Jae and O’Loughlin, Edward J. and Boyanov, Maxim I. and Brulc, Jennifer M. and Johnston, Eric R. and Kemner, Kenneth M. and Antonopoulos, Dionysios A. and Senko, John M.},
abstractNote = {Although iron- and sulfate-reducing bacteria in subsurface environments have crucial roles in biogeochemical cycling of C, Fe, and S, how specific electron donors impact the compositional structure and activity of native iron- and/or sulfate-reducing communities is largely unknown. To understand this better, we created bicarbonate-buffered batch systems in duplicate with three different electron donors (acetate, lactate, or glucose) paired with ferrihydrite and sulfate as the electron acceptors and inoculated them with subsurface sediment as the microbial inoculum. Sulfate and ferrihydrite reduction occurred simultaneously and were faster with lactate than with acetate. 16S rRNA-based sequence analysis of the communities over time revealed that Desulfotomaculum was the major driver for sulfate reduction coupled with propionate oxidation in lactate-amended incubations. The reduction of sulfate resulted in sulfide production and subsequent abiotic reduction of ferrihydrite. In contrast, glucose promoted faster reduction of ferrihydrite, but without reduction of sulfate. Interestingly, the glucose-amended incubations led to two different biogeochemical trajectories among replicate bottles that resulted in distinct coloration (white and brown). The two outcomes in geochemical evolution might be due to the stochastic evolution of the microbial communities or subtle differences in the initial composition of the fermenting microbial community and its development via the use of different glucose fermentation pathways available within the community. Synchrotron-based x-ray analysis indicated that siderite and amorphous Fe(II) were formed in the replicate bottles with glucose, while ferrous sulfide and vivianite were formed with lactate or acetate. As a result, these data sets reveal that use of different C utilization pathways projects significant changes in microbial community composition over time that uniquely impact both the geochemistry and mineralogy of subsurface environments.},
doi = {10.1371/journal.pone.0146689},
journal = {PLoS ONE},
number = 1,
volume = 11,
place = {United States},
year = {2016},
month = {1}
}

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

Citation Metrics:
Cited by: 9 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Genome-Wide Gene Expression Patterns and Growth Requirements Suggest that Pelobacter carbinolicus Reduces Fe(III) Indirectly via Sulfide Production
journal, May 2008

  • Haveman, S. A.; DiDonato, R. J.; Villanueva, L.
  • Applied and Environmental Microbiology, Vol. 74, Issue 14
  • DOI: 10.1128/AEM.02901-07

Enumeration and Characterization of Iron(III)-Reducing Microbial Communities from Acidic Subsurface Sediments Contaminated with Uranium(VI)
journal, December 2003


ATHENA , ARTEMIS , HEPHAESTUS : data analysis for X-ray absorption spectroscopy using IFEFFIT
journal, June 2005


Organic matter mineralization with the reduction of ferric iron: A review
journal, January 1987


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


Characterization of Fe(III) Reduction by Chlororespiring Anaeromxyobacter dehalogenans
journal, May 2003


Impact of Biostimulated Redox Processes on Metal Dynamics in an Iron-Rich Creek Soil of a Former Uranium Mining Area
journal, January 2010

  • Burkhardt, Eva-Maria; Akob, Denise M.; Bischoff, Sebastian
  • Environmental Science & Technology, Vol. 44, Issue 1
  • DOI: 10.1021/es902038e

Molecular analysis of phosphate limitation in Geobacteraceae during the bioremediation of a uranium-contaminated aquifer
journal, December 2009

  • N'Guessan, A. Lucie; Elifantz, Hila; Nevin, Kelly P.
  • The ISME Journal, Vol. 4, Issue 2
  • DOI: 10.1038/ismej.2009.115

Ferrozine---a new spectrophotometric reagent for iron
journal, June 1970

  • Stookey, Lawrence L.
  • Analytical Chemistry, Vol. 42, Issue 7, p. 779-781
  • DOI: 10.1021/ac60289a016

Redox zoning, rates of sulfate reduction and interactions with Fe-reduction and methanogenesis in a shallow sandy aquifer, Rømø, Denmark
journal, January 1999


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


Uranium reduction and microbial community development in response to stimulation with different electron donors
journal, January 2012


Biostimulation of iron reduction and subsequent oxidation of sediment containing Fe-silicates and Fe-oxides: Effect of redox cycling on Fe(III) bioreduction
journal, July 2007


Contribution of Anionic vs. Neutral Polymers to the Formation of Green Rust 1 from γ-FeOOH Bioreduction
journal, August 2013


Effects of dissimilatory sulfate reduction on FeIII (hydr)oxide reduction and microbial community development
journal, March 2014

  • Kwon, Man Jae; Boyanov, Maxim I.; Antonopoulos, Dionysios A.
  • Geochimica et Cosmochimica Acta, Vol. 129
  • DOI: 10.1016/j.gca.2013.09.037

Bacterial sulfate reduction limits natural arsenic contamination in groundwater
journal, January 2004

  • Kirk, Matthew F.; Holm, Thomas R.; Park, Jungho
  • Geology, Vol. 32, Issue 11
  • DOI: 10.1130/G20842.1

Reductive dissolution of iron(III) (hydr)oxides by hydrogen sulfide
journal, June 1992


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

Enriched Iron(III)-Reducing Bacterial Communities are Shaped by Carbon Substrate and Iron Oxide Mineralogy
journal, January 2012

  • Lentini, Christopher J.; Wankel, Scott D.; Hansel, Colleen M.
  • Frontiers in Microbiology, Vol. 3
  • DOI: 10.3389/fmicb.2012.00404

Analysis of Biostimulated Microbial Communities from Two Field Experiments Reveals Temporal and Spatial Differences in Proteome Profiles
journal, December 2010

  • Callister, Stephen J.; Wilkins, Michael J.; Nicora, Carrie D.
  • Environmental Science & Technology, Vol. 44, Issue 23
  • DOI: 10.1021/es101029f

Ferrihydrite-Dependent Growth of Sulfurospirillum deleyianum through Electron Transfer via Sulfur Cycling
journal, October 2004


Potential for Nonenzymatic Reduction of Fe(III) via Electron Shuttling in Subsurface Sediments
journal, June 2000

  • Nevin, Kelly P.; Lovley, Derek R.
  • Environmental Science & Technology, Vol. 34, Issue 12
  • DOI: 10.1021/es991181b

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


Effects of Si-bearing minerals on the nature of secondary iron mineral products from lepidocrocite bioreduction
journal, October 2011


The formation of green rust induced by tropical river biofilm components
journal, June 2011


The Ribosomal Database Project: improved alignments and new tools for rRNA analysis
journal, January 2009

  • Cole, J. R.; Wang, Q.; Cardenas, E.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn879

Microorganisms Associated with Uranium Bioremediation in a High-Salinity Subsurface Sediment
journal, June 2003


Iron sulfides and sulfur species produced at hematite surfaces in the presence of sulfate-reducing bacteria
journal, January 2001

  • Neal, Andrew L.; Techkarnjanaruk, Somkiet; Dohnalkova, Alice
  • Geochimica et Cosmochimica Acta, Vol. 65, Issue 2
  • DOI: 10.1016/S0016-7037(00)00537-8

Acetate Availability and its Influence on Sustainable Bioremediation of Uranium-Contaminated Groundwater
journal, June 2011


Energetics and kinetics of lactate fermentation to acetate and propionate via methylmalonyl-CoA or acrylyl-CoA
journal, May 2002


Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium
journal, October 1998

  • Fredrickson, James K.; Zachara, John M.; Kennedy, David W.
  • Geochimica et Cosmochimica Acta, Vol. 62, Issue 19-20
  • DOI: 10.1016/S0016-7037(98)00243-9

Desulfotomaculum geothermicum sp. nov., a thermophilic, fatty acid-degrading, sulfate-reducing bacterium isolated with H2 from geothermal ground water
journal, January 1988

  • Daumas, S.; Cord-Ruwisch, R.; Garcia, J. L.
  • Antonie van Leeuwenhoek, Vol. 54, Issue 2
  • DOI: 10.1007/BF00419203

Effects of Bound Phosphate on the Bioreduction of Lepidocrocite (γ-FeOOH) and Maghemite (γ-Fe 2 O 3 ) and Formation of Secondary Minerals
journal, August 2013

  • O’Loughlin, Edward J.; Boyanov, Maxim I.; Flynn, Theodore M.
  • Environmental Science & Technology, Vol. 47, Issue 16
  • DOI: 10.1021/es400627j

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

Effects of Oxyanions, Natural Organic Matter, and Bacterial Cell Numbers on the Bioreduction of Lepidocrocite (γ-FeOOH) and the Formation of Secondary Mineralization Products
journal, June 2010

  • O’Loughlin, Edward J.; Gorski, Christopher A.; Scherer, Michelle M.
  • Environmental Science & Technology, Vol. 44, Issue 12
  • DOI: 10.1021/es100294w

Surface chemistry and morphology of poorly crystalline iron sulfides precipitated in media containing sulfate-reducing bacteria
journal, January 1998


Fluctuations in Species-Level Protein Expression Occur during Element and Nutrient Cycling in the Subsurface
journal, March 2013


FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
journal, April 2009

  • Price, M. N.; Dehal, P. S.; Arkin, A. P.
  • Molecular Biology and Evolution, Vol. 26, Issue 7
  • DOI: 10.1093/molbev/msp077

A new anaerobic, sporing, acetate-oxidizing, sulfate-reducing bacterium, Desulfotomaculum (emend.) acetoxidans
journal, January 1977

  • Widdel, Friedrich; Pfennig, Norbert
  • Archives of Microbiology, Vol. 112, Issue 1
  • DOI: 10.1007/BF00446665

Functional Diversity and Electron Donor Dependence of Microbial Populations Capable of U(VI) Reduction in Radionuclide-Contaminated Subsurface Sediments
journal, March 2008

  • Akob, D. M.; Mills, H. J.; Gihring, T. M.
  • Applied and Environmental Microbiology, Vol. 74, Issue 10
  • DOI: 10.1128/AEM.02881-07

Phosphate Imposed Limitations on Biological Reduction and Alteration of Ferrihydrite
journal, January 2007

  • Borch, Thomas; Masue, Yoko; Kukkadapu, Ravi K.
  • Environmental Science & Technology, Vol. 41, Issue 1
  • DOI: 10.1021/es060695p

Disturbed subsurface microbial communities follow equivalent trajectories despite different structural starting points: Microbial community succession and disturbance
journal, April 2014

  • Handley, Kim M.; Wrighton, Kelly C.; Miller, Christopher S.
  • Environmental Microbiology, Vol. 17, Issue 3
  • DOI: 10.1111/1462-2920.12467