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Title: Orenia metallireducens sp. nov. strain Z6, a Novel Metal-reducing [member of the Phylum] Firmicute from the Deep Subsurface

Abstract

A novel halophilic and metal-reducing bacterium, Orenia metallireducens strain Z6, was isolated from briny groundwater extracted from a 2.02 km-deep borehole in the Illinois Basin, IL. This organism shared 96% 16S rRNA gene similarity with Orenia marismortui but demonstrated physiological properties previously unknown for this genus. In addition to exhibiting a fermentative metabolism typical of the genus Orenia, strain Z6 reduces various metal oxides [Fe(III), Mn(IV), Co(III), and Cr(VI)], using H2 as the electron donor. Strain Z6 actively reduced ferrihydrite over broad ranges of pH (6 to 9.6), salinity (0.4 to 3.5 M NaCl), and temperature (20 to 60°C). At pH 6.5, strain Z6 also reduced more crystalline iron oxides, such as lepidocrocite (γ-FeOOH), goethite (α-FeOOH), and hematite (α-Fe2O3). Analysis of X-ray absorption fine structure (XAFS) following Fe(III) reduction by strain Z6 revealed spectra from ferrous secondary mineral phases consistent with the precipitation of vivianite [Fe3(PO4)2] and siderite (FeCO3). The draft genome assembled for strain Z6 is 3.47 Mb in size and contains 3,269 protein-coding genes. Unlike the well-understood iron-reducing Shewanella and Geobacter species, this organism lacks the c-type cytochromes for typical Fe(III) reduction. Strain Z6 represents the first bacterial species in the genus Orenia (order Halanaerobiales) reported to reducemore » ferric iron minerals and other metal oxides. This microbe expands both the phylogenetic and physiological scopes of iron-reducing microorganisms known to inhabit the deep subsurface and suggests new mechanisms for microbial iron reduction. In conclusion, these distinctions from other Orenia spp. support the designation of strain Z6 as a new species, Orenia metallireducens sp. nov.« less

Authors:
 [1];  [1];  [2];  [3];  [2];  [2];  [2];  [1];  [4];  [1];  [1];  [1];  [1];  [1];  [1]
  1. Univ. of Illinois, Urbana-Champaign, Urbana, IL (United States)
  2. Argonne National Lab. (ANL), Lemont, IL (United States)
  3. (Bulgaria)
  4. (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Subsurface Biogeochemical Research; National Aeronautics and Space Administration (NASA)
OSTI Identifier:
1330336
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 82; 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

Dong, Yiran, Sanford, Robert A., Boyanov, Maxim I., Bulgarian Academy of Sciences, Sofia, Kemner, Kenneth M., Flynn, Theodore M., O'Loughlin, Edward J., Chang, Yun-juan, Rutgers Univ., New Brunswick, NJ, Locke, Jr., Randall A., Weber, Joseph R., Egan, Sheila M., Mackie, Roderick I., Cann, Isaac, and Fouke, Bruce W. Orenia metallireducens sp. nov. strain Z6, a Novel Metal-reducing [member of the Phylum] Firmicute from the Deep Subsurface. United States: N. p., 2016. Web. doi:10.1128/AEM.02382-16.
Dong, Yiran, Sanford, Robert A., Boyanov, Maxim I., Bulgarian Academy of Sciences, Sofia, Kemner, Kenneth M., Flynn, Theodore M., O'Loughlin, Edward J., Chang, Yun-juan, Rutgers Univ., New Brunswick, NJ, Locke, Jr., Randall A., Weber, Joseph R., Egan, Sheila M., Mackie, Roderick I., Cann, Isaac, & Fouke, Bruce W. Orenia metallireducens sp. nov. strain Z6, a Novel Metal-reducing [member of the Phylum] Firmicute from the Deep Subsurface. United States. https://doi.org/10.1128/AEM.02382-16
Dong, Yiran, Sanford, Robert A., Boyanov, Maxim I., Bulgarian Academy of Sciences, Sofia, Kemner, Kenneth M., Flynn, Theodore M., O'Loughlin, Edward J., Chang, Yun-juan, Rutgers Univ., New Brunswick, NJ, Locke, Jr., Randall A., Weber, Joseph R., Egan, Sheila M., Mackie, Roderick I., Cann, Isaac, and Fouke, Bruce W. Fri . "Orenia metallireducens sp. nov. strain Z6, a Novel Metal-reducing [member of the Phylum] Firmicute from the Deep Subsurface". United States. https://doi.org/10.1128/AEM.02382-16. https://www.osti.gov/servlets/purl/1330336.
@article{osti_1330336,
title = {Orenia metallireducens sp. nov. strain Z6, a Novel Metal-reducing [member of the Phylum] Firmicute from the Deep Subsurface},
author = {Dong, Yiran and Sanford, Robert A. and Boyanov, Maxim I. and Bulgarian Academy of Sciences, Sofia and Kemner, Kenneth M. and Flynn, Theodore M. and O'Loughlin, Edward J. and Chang, Yun-juan and Rutgers Univ., New Brunswick, NJ and Locke, Jr., Randall A. and Weber, Joseph R. and Egan, Sheila M. and Mackie, Roderick I. and Cann, Isaac and Fouke, Bruce W.},
abstractNote = {A novel halophilic and metal-reducing bacterium, Orenia metallireducens strain Z6, was isolated from briny groundwater extracted from a 2.02 km-deep borehole in the Illinois Basin, IL. This organism shared 96% 16S rRNA gene similarity with Orenia marismortui but demonstrated physiological properties previously unknown for this genus. In addition to exhibiting a fermentative metabolism typical of the genus Orenia, strain Z6 reduces various metal oxides [Fe(III), Mn(IV), Co(III), and Cr(VI)], using H2 as the electron donor. Strain Z6 actively reduced ferrihydrite over broad ranges of pH (6 to 9.6), salinity (0.4 to 3.5 M NaCl), and temperature (20 to 60°C). At pH 6.5, strain Z6 also reduced more crystalline iron oxides, such as lepidocrocite (γ-FeOOH), goethite (α-FeOOH), and hematite (α-Fe2O3). Analysis of X-ray absorption fine structure (XAFS) following Fe(III) reduction by strain Z6 revealed spectra from ferrous secondary mineral phases consistent with the precipitation of vivianite [Fe3(PO4)2] and siderite (FeCO3). The draft genome assembled for strain Z6 is 3.47 Mb in size and contains 3,269 protein-coding genes. Unlike the well-understood iron-reducing Shewanella and Geobacter species, this organism lacks the c-type cytochromes for typical Fe(III) reduction. Strain Z6 represents the first bacterial species in the genus Orenia (order Halanaerobiales) reported to reduce ferric iron minerals and other metal oxides. This microbe expands both the phylogenetic and physiological scopes of iron-reducing microorganisms known to inhabit the deep subsurface and suggests new mechanisms for microbial iron reduction. In conclusion, these distinctions from other Orenia spp. support the designation of strain Z6 as a new species, Orenia metallireducens sp. nov.},
doi = {10.1128/AEM.02382-16},
journal = {Applied and Environmental Microbiology},
number = 21,
volume = 82,
place = {United States},
year = {Fri Aug 26 00:00:00 EDT 2016},
month = {Fri Aug 26 00:00:00 EDT 2016}
}

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Works referenced in this record:

Dissimilatory Reduction of Fe(III) and Other Electron Acceptors by a Thermus Isolate
journal, March 1999


Fervidicella metallireducens gen. nov., sp. nov., a thermophilic, anaerobic bacterium from geothermal waters
journal, August 2009

  • Ogg, C. D.; Patel, B. K. C.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 60, Issue 6
  • DOI: 10.1099/ijs.0.014670-0

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


Prokaryotes: The unseen majority
journal, June 1998

  • Whitman, W. B.; Coleman, D. C.; Wiebe, W. J.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
  • DOI: 10.1073/pnas.95.12.6578

Dissimilatory Reduction of Fe(III) by Thermophilic Bacteria and Archaea in Deep Subsurface Petroleum Reservoirs of Western Siberia
journal, August 1999

  • Slobodkin, Alexander I.; Jeanthon, Christian; L'Haridon, Stéphane
  • Current Microbiology, Vol. 39, Issue 2
  • DOI: 10.1007/s002849900426

Secondary mineralization pathways induced by dissimilatory iron reduction of ferrihydrite under advective flow
journal, August 2003


Microbiological evidence for Fe(III) reduction on early Earth
journal, September 1998

  • Vargas, Madeline; Kashefi, Kazem; Blunt-Harris, Elizabeth L.
  • Nature, Vol. 395, Issue 6697
  • DOI: 10.1038/25720

Ferric Iron Reduction by Fermentative Strain BS2 Isolated From an Iron-Rich Anoxic Environment (Lake Pavin, France)
journal, October 2010

  • Lehours, Anne-Catherine; Rabiet, Marion; Morel-Desrosiers, Nicole
  • Geomicrobiology Journal, Vol. 27, Issue 8
  • DOI: 10.1080/01490451003597663

The RDP-II (Ribosomal Database Project)
journal, January 2001


Analysis of multiple-scattering XAFS data using theoretical standards
journal, March 1995


Exploration of deep intraterrestrial microbial life: current perspectives
journal, April 2000


Alkaline iron(III) reduction by a novel alkaliphilic, halotolerant, Bacillus sp. isolated from salt flat sediments of Soap Lake
journal, October 2007

  • Pollock, Jarrod; Weber, Karrie A.; Lack, Joe
  • Applied Microbiology and Biotechnology, Vol. 77, Issue 4
  • DOI: 10.1007/s00253-007-1220-5

Dissimilatory Fe(III) and Mn(IV) reduction.
journal, January 1991


Thermodynamic Evaluation on H 2 Production in Glucose Fermentation
journal, April 2008

  • Lee, Hyung-Sool; Salerno, Michael B.; Rittmann, Bruce E.
  • Environmental Science & Technology, Vol. 42, Issue 7
  • DOI: 10.1021/es702610v

Nanosized Iron Oxide Colloids Strongly Enhance Microbial Iron Reduction
journal, November 2009

  • Bosch, Julian; Heister, Katja; Hofmann, Thilo
  • Applied and Environmental Microbiology, Vol. 76, Issue 1
  • DOI: 10.1128/AEM.00417-09

Characterization of iron-reducing Alteromonas putrefaciens strains from oil field fluids
journal, May 1987

  • Semple, K. M.; Westlake, D. W. S.
  • Canadian Journal of Microbiology, Vol. 33, Issue 5
  • DOI: 10.1139/m87-064

IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011

  • Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1044

Solubility and dissimilatory reduction kinetics of iron(III) oxyhydroxides: A linear free energy relationship
journal, September 2009

  • Bonneville, Steeve; Behrends, Thilo; Van Cappellen, Philippe
  • Geochimica et Cosmochimica Acta, Vol. 73, Issue 18
  • DOI: 10.1016/j.gca.2009.06.006

RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006


Adsorption of Fe(II) and U(VI) to carboxyl-functionalized microspheres: The influence of speciation on uranyl reduction studied by titration and XAFS
journal, April 2007

  • Boyanov, Maxim I.; O’Loughlin, Edward J.; Roden, Eric E.
  • Geochimica et Cosmochimica Acta, Vol. 71, Issue 8
  • DOI: 10.1016/j.gca.2007.01.025

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology
journal, June 2010


Kinetic Analysis of the Bacterial Reduction of Goethite
journal, June 2001

  • Liu, Chongxuan; Kota, Sreenivas; Zachara, John M.
  • Environmental Science & Technology, Vol. 35, Issue 12
  • DOI: 10.1021/es001956c

Syntrophy in anaerobic global carbon cycles
journal, December 2009

  • McInerney, Michael J.; Sieber, Jessica R.; Gunsalus, Robert P.
  • Current Opinion in Biotechnology, Vol. 20, Issue 6
  • DOI: 10.1016/j.copbio.2009.10.001

The Microbial Ferrous Wheel in a Neutral pH Groundwater Seep
journal, January 2012


Deep subsurface microbial processes
journal, January 1995

  • Lovley, Derek R.; Chapelle, Francis H.
  • Reviews of Geophysics, Vol. 33, Issue 3
  • DOI: 10.1029/95RG01305

Recrystallization Processes Involving Iron Oxides in Natural Environments and In Vitro
book, February 2013

  • Taitel-Goldman, Nurit
  • Recent Developments in the Study of Recrystallization
  • DOI: 10.5772/53735

Molecular Underpinnings of Fe(III) Oxide Reduction by Shewanella Oneidensis MR-1
journal, January 2012


Geoalkalibacter subterraneus sp. nov., an anaerobic Fe(III)- and Mn(IV)-reducing bacterium from a petroleum reservoir, and emended descriptions of the family Desulfuromonadaceae and the genus Geoalkalibacter
journal, April 2009

  • Greene, A. C.; Patel, B. K. C.; Yacob, S.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 4
  • DOI: 10.1099/ijs.0.001537-0

Influence of Biogenic Fe(II) on Bacterial Crystalline Fe(III) Oxide Reduction
journal, March 2002


Reductive dissolution of fe(III) oxides byPseudomonas sp. 200
journal, October 1988

  • Arnold, Robert G.; DiChristina, Thomas J.; Hoffmann, Michael R.
  • Biotechnology and Bioengineering, Vol. 32, Issue 9
  • DOI: 10.1002/bit.260320902

Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA.
journal, January 1997


The surprising diversity of clostridial hydrogenases: a comparative genomic perspective
journal, April 2010


Description of Two New Thermophilic Desulfotomaculum spp., Desulfotomaculum putei sp. nov., from a Deep Terrestrial Subsurface, and Desulfotomaculum luciae sp. nov., from a Hot Spring
journal, July 1997

  • Liu, Yitai; Karnauchow, Tim M.; Jarrell, Ken F.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 47, Issue 3
  • DOI: 10.1099/00207713-47-3-615

The thermodynamic ladder in geomicrobiology
journal, March 2011

  • Bethke, C. M.; Sanford, R. A.; Kirk, M. F.
  • American Journal of Science, Vol. 311, Issue 3
  • DOI: 10.2475/03.2011.01

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


c-Type Cytochromes in Pelobacter carbinolicus
journal, August 2006

  • Haveman, Shelley A. ; Holmes, Dawn E.; Ding, Yan-Huai R.
  • Applied and Environmental Microbiology, Vol. 72, Issue 11
  • DOI: 10.1128/AEM.01128-06

Iron metabolism in anoxic environments at near neutral pH
journal, January 2001


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

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

Bacterial chitin utilization at halophilic conditions
journal, December 2013


Pore‐size constraints on the activity and survival of subsurface bacteria in a late cretaceous shale‐sandstone sequence, northwestern New Mexico
journal, July 1997

  • Fredrickson, J. K.; McKinley, J. P.; Bjornstad, B. N.
  • Geomicrobiology Journal, Vol. 14, Issue 3
  • DOI: 10.1080/01490459709378043

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

Caloramator australicus sp. nov., a thermophilic, anaerobic bacterium from the Great Artesian Basin of Australia
journal, January 2009

  • Ogg, C. D.; Patel, B. K. C.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 1
  • DOI: 10.1099/ijs.0.000802-0

Agar Shake Tube Technique for Simultaneous Determination of Aerobic and Anaerobic Susceptibility to Antibiotics
journal, October 1977

  • Evans, J. B.; Harrell, L. J.
  • Antimicrobial Agents and Chemotherapy, Vol. 12, Issue 4
  • DOI: 10.1128/AAC.12.4.534

Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation
journal, February 2013

  • Buckel, Wolfgang; Thauer, Rudolf K.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2
  • DOI: 10.1016/j.bbabio.2012.07.002

Thermophilic Fe(III)-Reducing Bacteria from the Deep Subsurface: The Evolutionary Implications
journal, August 1997


SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler
journal, December 2012


Transformation of Two-Line Ferrihydrite to Goethite and Hematite as a Function of pH and Temperature
journal, January 2011

  • Das, Soumya; Hendry, M. Jim; Essilfie-Dughan, Joseph
  • Environmental Science & Technology, Vol. 45, Issue 1
  • DOI: 10.1021/es101903y

Fe, C, and O isotope compositions of banded iron formation carbonates demonstrate a major role for dissimilatory iron reduction in ~2.5Ga marine environments
journal, May 2010

  • Heimann, Adriana; Johnson, Clark M.; Beard, Brian L.
  • Earth and Planetary Science Letters, Vol. 294, Issue 1-2
  • DOI: 10.1016/j.epsl.2010.02.015

Organic Matter Mineralization with Reduction of Ferric Iron in Anaerobic Sediments
journal, January 1986


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


Microbial Reduction of Crystalline Iron(III) Oxides:  Influence of Oxide Surface Area and Potential for Cell Growth
journal, January 1996

  • Roden, Eric E.; Zachara, John M.
  • Environmental Science & Technology, Vol. 30, Issue 5
  • DOI: 10.1021/es9506216

Deferribacter thermophilus gen. nov., sp. nov., a Novel Thermophilic Manganese- and Iron-Reducing Bacterium Isolated from a Petroleum Reservoir
journal, April 1997

  • Greene, A. C.; Patel, B. K. C.; Sheehy, A. J.
  • International Journal of Systematic Bacteriology, Vol. 47, Issue 2
  • DOI: 10.1099/00207713-47-2-505

Microbial reduction of metals and radionuclides
journal, June 2003


An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors
journal, November 2014


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

Orenia salinaria sp. nov., a fermentative bacterium isolated from anaerobic sediments of Mediterranean salterns.
journal, March 2000

  • Mouné, S.; Eatock, C.; Matheron, R.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 50, Issue 2
  • DOI: 10.1099/00207713-50-2-721

Sulfur-mediated electron shuttling during bacterial iron reduction
journal, May 2014


Microbial community structure analysis of produced water from a high-temperature North Sea oil-field
journal, June 2007


Reduction of Technetium(VII) byDesulfovibrio fructosovorans Is Mediated by the Nickel-Iron Hydrogenase
journal, October 2001


Extracellular Electron Transport-Mediated Fe(III) Reduction by a Community of Alkaliphilic Bacteria That Use Flavins as Electron Shuttles
journal, October 2013

  • Fuller, Samuel J.; McMillan, Duncan G. G.; Renz, Marc B.
  • Applied and Environmental Microbiology, Vol. 80, Issue 1
  • DOI: 10.1128/AEM.02282-13

Bacillus infernus sp. nov., an Fe(III)- and Mn(IV)-Reducing Anaerobe from the Deep Terrestrial Subsurface
journal, July 1995

  • Boone, D. R.; Liu, Y.; Zhao, Z. -J.
  • International Journal of Systematic Bacteriology, Vol. 45, Issue 3
  • DOI: 10.1099/00207713-45-3-441

Structure and mechanism of iron-only hydrogenases
journal, December 1999


Depositional and diagenetic variability within the Cambrian Mount Simon Sandstone: Implications for carbon dioxide sequestration
journal, June 2011

  • Bowen, Brenda B.; Ochoa, Raul I.; Wilkens, Nathan D.
  • Environmental Geosciences, Vol. 18, Issue 2
  • DOI: 10.1306/eg.07271010012

The Prokaryotes Vol. 4: Bacteria: Firmicutes, Cyanobacteria
reference-book, January 2006


Iron Oxides in the Laboratary
book, April 2000


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