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Title: Electron Donor Utilization and Secondary Mineral Formation during the Bioreduction of Lepidocrocite by Shewanella putrefaciens CN32

Abstract

The bioreduction of Fe(III) oxides by dissimilatory iron reducing bacteria (DIRB) may result in the production of a suite of Fe(II)-bearing secondary minerals, including magnetite, siderite, vivianite, green rusts, and chukanovite; the formation of specific phases controlled by the interaction of various physiological and geochemical factors. In an effort to better understand the effects of individual electron donors on the formation of specific Fe(II)-bearing secondary minerals, we examined the effects of a series of potential electron donors on the bioreduction of lepidocrocite ($γ$-FeOOH) by Shewanella putrefaciens CN32. Biomineralization products were identified by X-ray diffraction, Mössbauer spectroscopy, and scanning electron microscopy. Acetate, citrate, ethanol, glucose, glutamate, glycerol, malate, and succinate were not effectively utilized for the bioreduction of lepidocrocite by S. putrefaciens CN32; however, substantial Fe(II) production was observed when formate, lactate, H2, pyruvate, serine, or N acetylglucosamine (NAG) was provided as an electron donor. Carbonate or sulfate green rust was the dominant Fe(II)-bearing secondary mineral when formate, H2, lactate, or NAG was provided, however, siderite formed with pyruvate or serine. Geochemical modeling indicated that pH and carbonate concentration are the key factors determining the prevalence of carbonate green rust verses siderite.

Authors:
 [1]; ORCiD logo [2]; ORCiD logo [3];  [4]
  1. Argonne National Lab. (ANL), Argonne, IL (United States). Biosciences Div.
  2. Univ. of Iowa, Iowa City, IA (United States). Dept. of Civil and Environmental Engineering; Pennsylvania State Univ., University Park, PA (United States). Dept. of Civil and Environmental Engineering
  3. Argonne National Lab. (ANL), Argonne, IL (United States). Biosciences Div.; California Dept. of Water Resources, Sacramento, CA (United States)
  4. Univ. of Iowa, Iowa City, IA (United States). Dept. of Civil and Environmental Engineering
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science - Office of Biological and Environmental Research - Subsurface Biogeochemical Research
OSTI Identifier:
1560537
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Minerals
Additional Journal Information:
Journal Volume: 9; Journal Issue: 7; Journal ID: ISSN 2075-163X
Publisher:
MDPI
Country of Publication:
United States
Language:
English
Subject:
58 GEOSCIENCES; dissimilatory iron reduction; green rust; iron oxide; siderite

Citation Formats

O’Loughlin, Edward J., Gorski, Christopher A., Flynn, Theodore M., and Scherer, Michelle M. Electron Donor Utilization and Secondary Mineral Formation during the Bioreduction of Lepidocrocite by Shewanella putrefaciens CN32. United States: N. p., 2019. Web. doi:10.3390/min9070434.
O’Loughlin, Edward J., Gorski, Christopher A., Flynn, Theodore M., & Scherer, Michelle M. Electron Donor Utilization and Secondary Mineral Formation during the Bioreduction of Lepidocrocite by Shewanella putrefaciens CN32. United States. doi:10.3390/min9070434.
O’Loughlin, Edward J., Gorski, Christopher A., Flynn, Theodore M., and Scherer, Michelle M. Sun . "Electron Donor Utilization and Secondary Mineral Formation during the Bioreduction of Lepidocrocite by Shewanella putrefaciens CN32". United States. doi:10.3390/min9070434. https://www.osti.gov/servlets/purl/1560537.
@article{osti_1560537,
title = {Electron Donor Utilization and Secondary Mineral Formation during the Bioreduction of Lepidocrocite by Shewanella putrefaciens CN32},
author = {O’Loughlin, Edward J. and Gorski, Christopher A. and Flynn, Theodore M. and Scherer, Michelle M.},
abstractNote = {The bioreduction of Fe(III) oxides by dissimilatory iron reducing bacteria (DIRB) may result in the production of a suite of Fe(II)-bearing secondary minerals, including magnetite, siderite, vivianite, green rusts, and chukanovite; the formation of specific phases controlled by the interaction of various physiological and geochemical factors. In an effort to better understand the effects of individual electron donors on the formation of specific Fe(II)-bearing secondary minerals, we examined the effects of a series of potential electron donors on the bioreduction of lepidocrocite ($γ$-FeOOH) by Shewanella putrefaciens CN32. Biomineralization products were identified by X-ray diffraction, Mössbauer spectroscopy, and scanning electron microscopy. Acetate, citrate, ethanol, glucose, glutamate, glycerol, malate, and succinate were not effectively utilized for the bioreduction of lepidocrocite by S. putrefaciens CN32; however, substantial Fe(II) production was observed when formate, lactate, H2, pyruvate, serine, or N acetylglucosamine (NAG) was provided as an electron donor. Carbonate or sulfate green rust was the dominant Fe(II)-bearing secondary mineral when formate, H2, lactate, or NAG was provided, however, siderite formed with pyruvate or serine. Geochemical modeling indicated that pH and carbonate concentration are the key factors determining the prevalence of carbonate green rust verses siderite.},
doi = {10.3390/min9070434},
journal = {Minerals},
number = 7,
volume = 9,
place = {United States},
year = {2019},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
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Figures / Tables:

Figure 1 Figure 1: Fe(II) production during the bioreduction of lepidocrocite by S. putrefaciens CN32 as a function of available electron donor.

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  • Fredrickson, James K.; Romine, Margaret F.; Beliaev, Alexander S.
  • Nature Reviews Microbiology, Vol. 6, Issue 8
  • DOI: 10.1038/nrmicro1947

N -acetylglucosamine dynamics in freshwater environments: Concentration of amino sugars, extracellular enzyme activities, and microbial uptake
journal, July 1994


Reduction of SeO 4 2 - Anions and Anoxic Formation of Iron(II)−Iron(III) Hydroxy-Selenate Green Rust
journal, March 2000

  • Refait, Philippe; Simon, Lilian; Génin, Jean-Marie R.
  • Environmental Science & Technology, Vol. 34, Issue 5
  • DOI: 10.1021/es990376g

Shewanella frigidimarina and Shewanella livingstonensis sp. nov. isolated from Antarctic coastal areas.
journal, January 2002

  • Tudela, Encarna; Montes, M. Jesús; Jiménez, Francisco
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 52, Issue 1
  • DOI: 10.1099/00207713-52-1-195

The mechanisms of reduction of hexavalent chromium by green rust sodium sulphate: Formation of Cr-goethite
journal, July 2006

  • Skovbjerg, L. L.; Stipp, S. L. S.; Utsunomiya, S.
  • Geochimica et Cosmochimica Acta, Vol. 70, Issue 14
  • DOI: 10.1016/j.gca.2006.02.017

X-ray absorption and photoelectron spectroscopy investigation of selenite reduction by FeII-bearing minerals
journal, December 2008

  • Scheinost, Andreas C.; Kirsch, Regina; Banerjee, Dipanjan
  • Journal of Contaminant Hydrology, Vol. 102, Issue 3-4
  • DOI: 10.1016/j.jconhyd.2008.09.018

Fougerite, a new mineral of the pyroaurite-iowaite group: description and crystal structure
journal, June 2007

  • Trolard, Fabienne; Bourrié, Guilhem; Abdelmoula, Mustapha
  • Clays and Clay Minerals, Vol. 55, Issue 3
  • DOI: 10.1346/CCMN.2007.0550308

Mössbauerite, Fe 6 3+ O 4 (OH) 8 [CO 3 ]·3H 2 O, the fully oxidized ‘green rust’ mineral from Mont Saint-Michel Bay, France
journal, April 2014


Reduction of Uranium(VI) by Mixed Iron(II)/Iron(III) Hydroxide (Green Rust):  Formation of UO 2 Nanoparticles
journal, February 2003

  • O'Loughlin, Edward J.; Kelly, Shelly D.; Cook, Russell E.
  • Environmental Science & Technology, Vol. 37, Issue 4
  • DOI: 10.1021/es0208409

Biotransformation of two-line silica-ferrihydrite by a dissimilatory Fe(III)-reducing bacterium: formation of carbonate green rust in the presence of phosphate
journal, July 2004

  • Kukkadapu, Ravi K.; Zachara, John M.; Fredrickson, James K.
  • Geochimica et Cosmochimica Acta, Vol. 68, Issue 13
  • DOI: 10.1016/j.gca.2003.12.024

BIOGEOCHEMICAL AND ENVIRONMENTAL FACTORS IN Fe BIOMINERALIZATION: MAGNETITE AND SIDERITE FORMATION
journal, February 2003


Biotransformation of lepidocrocite in the presence of quinones and flavins
journal, August 2013


Fe(II)/Fe(III) ‘green rust’ developed within ochreous coal mine drainage sediment in South Wales, UK
journal, December 2006


Microbial and plant uptake of free amino sugars in grassland soils
journal, June 2012


Observations and assessment of iron oxide and green rust nanoparticles in metal-polluted mine drainage within a steep redox gradient
journal, January 2014

  • Johnson, Carol A.; Freyer, Gina; Fabisch, Maria
  • Environmental Chemistry, Vol. 11, Issue 4
  • DOI: 10.1071/EN13184

Microbial Fe(III) reduction in subsurface environments
journal, July 1997


Neptunyl (Np) interaction with green rust,
journal, March 2011

  • Christiansen, B. C.; Geckeis, H.; Marquardt, C. M.
  • Geochimica et Cosmochimica Acta, Vol. 75, Issue 5
  • DOI: 10.1016/j.gca.2010.12.003

Iron and Manganese in Anaerobic Respiration: Environmental Significance, Physiology, and Regulation
journal, October 1994


Arsenic sequestration by sorption processes in high-iron sediments
journal, December 2007

  • Root, Robert A.; Dixit, Suvasis; Campbell, Kate M.
  • Geochimica et Cosmochimica Acta, Vol. 71, Issue 23
  • DOI: 10.1016/j.gca.2007.04.038

Characterization of Predominant Reductants in an Anaerobic Leachate-Contaminated Aquifer by Nitroaromatic Probe Compounds
journal, January 1998

  • Rügge, Kirsten; Hofstetter, Thomas B.; Haderlein, Stefan B.
  • Environmental Science & Technology, Vol. 32, Issue 1
  • DOI: 10.1021/es970249p

Kinetics of Cr(VI) Reduction by Carbonate Green Rust
journal, September 2001

  • Williams, Aaron G. B.; Scherer, Michelle M.
  • Environmental Science & Technology, Vol. 35, Issue 17
  • DOI: 10.1021/es010579g

Thermoterrabacterium ferrireducens gen. nov., sp. nov., a Thermophilic Anaerobic Dissimilatory Fe(III)-Reducing Bacterium from a Continental Hot Spring
journal, April 1997

  • Slobodkin, A.; Reysenbach, A. -L.; Strutz, N.
  • International Journal of Systematic Bacteriology, Vol. 47, Issue 2
  • DOI: 10.1099/00207713-47-2-541

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

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