Temperature dependence of nitrate-reducing Fe(II) oxidation by Acidovorax strain BoFeN1 – evaluating the role of enzymatic vs. abiotic Fe(II) oxidation by nitrite

Dopffel, Nicole; Jamieson, James; Bryce, Casey; Joshi, Prachi; Mansor, Muammar; Siade, Adam; Prommer, Henning; Kappler, Andreas

doi:10.1093/femsec/fiab155

Temperature dependence of nitrate-reducing Fe(II) oxidation by Acidovorax strain BoFeN1 – evaluating the role of enzymatic vs. abiotic Fe(II) oxidation by nitrite

Journal Article · 26 November 2021 · FEMS Microbiology Ecology (Online)

DOI:https://doi.org/10.1093/femsec/fiab155· OSTI ID:1979485

Dopffel, Nicole; ; Bryce, Casey; Joshi, Prachi; Mansor, Muammar; Siade, Adam; Prommer, Henning; Kappler, Andreas

ABSTRACT

Fe(II) oxidation coupled to nitrate reduction is a widely observed metabolism. However, to what extent the observed Fe(II) oxidation is driven enzymatically or abiotically by metabolically produced nitrite remains puzzling. To distinguish between biotic and abiotic reactions, we cultivated the mixotrophic nitrate-reducing Fe(II)-oxidizing Acidovorax strain BoFeN1 over a wide range of temperatures and compared it to abiotic Fe(II) oxidation by nitrite at temperatures up to 60°C. The collected experimental data were subsequently analyzed through biogeochemical modeling. At 5°C, BoFeN1 cultures consumed acetate and reduced nitrate but did not significantly oxidize Fe(II). Abiotic Fe(II) oxidation by nitrite at different temperatures showed an Arrhenius-type behavior with an activation energy of 80±7 kJ/mol. Above 40°C, the kinetics of Fe(II) oxidation were abiotically driven, whereas at 30°C, where BoFeN1 can actively metabolize, the model-based interpretation strongly suggested that an enzymatic pathway was responsible for a large fraction (ca. 62%) of the oxidation. This result was reproduced even when no additional carbon source was present. Our results show that at below 30°C, i.e. at temperatures representing most natural environments, biological Fe(II) oxidation was largely responsible for overall Fe(II) oxidation, while abiotic Fe(II) oxidation by nitrite played a less important role.

Research Organization:: Columbia Univ., New York, NY (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE)

DOE Contract Number:: EE0009506

OSTI ID:: 1979485

Journal Information:: FEMS Microbiology Ecology (Online), Vol. 97, Issue 12; ISSN 1574-6941

Publisher:: Federation of European Microbiological Societies

Country of Publication:: United States

Language:: English

References (60)

Microbiological Oxidation of Ferrous Iron at Low Temperatures Ahonen, Lasse; Tuovinen, Olli H. Applied and Environmental Microbiology, Vol. 55, Issue 2 https://doi.org/10.1128/aem.55.2.312-316.1989	journal	February 1989
Adaptation of Microorganisms to Cold Temperatures, Weak Acid Preservatives, Low pH, and Osmotic Stress: A Review Beales, N. Comprehensive Reviews in Food Science and Food Safety, Vol. 3, Issue 1 https://doi.org/10.1111/j.1541-4337.2004.tb00057.x	journal	January 2004
" Genome-enabled studies of anaerobic, nitrate-dependent iron oxidation in the chemolithoautotrophic bacterium Thiobacillus denitrificans" Beller, Harry R.; Zhou, Peng; Legler, Tina C. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00249	journal	January 2013
Anaerobic and aerobic oxidation of ferrous iron at neutral pH by chemoheterotrophic nitrate-reducing bacteria Benz, M.; Brune, Andreas; Schink, Bernhard Archives of Microbiology, Vol. 169, Issue 2 https://doi.org/10.1007/s002030050555	journal	February 1998
Iron and Copper Act Synergistically To Delay Anaerobic Growth of Bacteria Bird, Lina J.; Coleman, Maureen L.; Newman, Dianne K. Applied and Environmental Microbiology, Vol. 79, Issue 12 https://doi.org/10.1128/AEM.03944-12	journal	April 2013
Composition and Activity of an Autotrophic Fe(II)-Oxidizing, Nitrate-Reducing Enrichment Culture Blothe, M.; Roden, E. E. Applied and Environmental Microbiology, Vol. 75, Issue 21 https://doi.org/10.1128/AEM.01742-09	journal	September 2009
Aqueous nitrosyliron(II) chemistry. 1. Reduction of nitrite and nitric oxide by iron(II) and (trioxodinitrato)iron(II) in acetate buffer. Intermediacy of nitrosyl hydride Bonner, Francis T.; Pearsall, Kenneth A. Inorganic Chemistry, Vol. 21, Issue 5 https://doi.org/10.1021/ic00135a053	journal	May 1982
Biogeochemical Redox Processes and their Impact on Contaminant Dynamics Borch, Thomas; Kretzschmar, Ruben; Kappler, Andreas Environmental Science & Technology, Vol. 44, Issue 1 https://doi.org/10.1021/es9026248	journal	January 2010
Microbial anaerobic Fe(II) oxidation - Ecology, mechanisms and environmental implications: Microbial anaerobic Fe(II) oxidation Bryce, Casey; Blackwell, Nia; Schmidt, Caroline Environmental Microbiology, Vol. 20, Issue 10 https://doi.org/10.1111/1462-2920.14328	journal	October 2018
Fe(II) Oxidation Is an Innate Capability of Nitrate-Reducing Bacteria That Involves Abiotic and Biotic Reactions Carlson, H. K.; Clark, I. C.; Blazewicz, S. J. Journal of Bacteriology, Vol. 195, Issue 14 https://doi.org/10.1128/JB.00058-13	journal	May 2013
Induction of Nitrate-Dependent Fe(II) Oxidation by Fe(II) in Dechloromonas sp. Strain UWNR4 and Acidovorax sp. Strain 2AN Chakraborty, Anirban; Picardal, Flynn Applied and Environmental Microbiology, Vol. 79, Issue 2 https://doi.org/10.1128/AEM.02709-12	journal	January 2013
Inhibition of NO3- and NO2- Reduction by Microbial Fe(III) Reduction: Evidence of a Reaction between NO2- and Cell Surface-Bound Fe2+ Coby, A. J.; Picardal, F. W. Applied and Environmental Microbiology, Vol. 71, Issue 9 https://doi.org/10.1128/AEM.71.9.5267-5274.2005	journal	September 2005
Following the Kinetics: Iron-Oxidizing Microbial Mats in Cold Icelandic Volcanic Habitats and Their Rock-Associated Carbonaceous Signature Cockell, Charles S.; Kelly, Laura C.; Summers, Stephen Astrobiology, Vol. 11, Issue 7 https://doi.org/10.1089/ast.2011.0606	journal	September 2011
Denitrification and ammonification at low soil temperatures Dorland, S.; Beauchamp, E. G. Canadian Journal of Soil Science, Vol. 71, Issue 3 https://doi.org/10.4141/cjss91-029	journal	August 1991
Abiotic Process for Fe(II) Oxidation and Green Rust Mineralization Driven by a Heterotrophic Nitrate Reducing Bacteria ( Klebsiella mobilis ) Etique, Marjorie; Jorand, Frédéric P. A.; Zegeye, Asfaw Environmental Science & Technology, Vol. 48, Issue 7 https://doi.org/10.1021/es403358v	journal	March 2014
Isolation and temperature characterization of psychrotrophic strains of Thiobacillus ferrooxidans from the environment of a uranium mine. Ferroni, G. D.; Leduc, L. G.; Todd, M. The Journal of General and Applied Microbiology, Vol. 32, Issue 3 https://doi.org/10.2323/jgam.32.169	journal	January 1986
Precipitation and dissolution kinetics and equilibria of aqueous ferrous carbonate vs temperature Greenberg, Janet; Tomson, Mason Applied Geochemistry, Vol. 7, Issue 2 https://doi.org/10.1016/0883-2927(92)90036-3	journal	March 1992
Reduction of nitrate to ammonium by sulphate green rust: activation energy and reaction mechanism Hansen, H. C. B.; Bender Koch, C. Clay Minerals, Vol. 33, Issue 1 https://doi.org/10.1180/000985598545453	journal	March 1998
Evaluation of the free energy of formation of Fe(II)-Fe(III) hydroxide-sulphate (green rust) and its reduction of nitrite Hansen, Hans Christian Bruun; Borggaard, Ole Kragholm; Sørensen, Jan Geochimica et Cosmochimica Acta, Vol. 58, Issue 12 https://doi.org/10.1016/0016-7037(94)90131-7	journal	June 1994
Abiotic Nitrate Reduction to Ammonium: Key Role of Green Rust Hansen, Hans Chr. B.; Koch, Christian B.; Nancke-Krogh, Hanne Environmental Science & Technology, Vol. 30, Issue 6, p. 2053-2056 https://doi.org/10.1021/es950844w	journal	January 1996
Metagenomic Analyses of the Autotrophic Fe(II)-Oxidizing, Nitrate-Reducing Enrichment Culture KS He, Shaomei; Tominski, Claudia; Kappler, Andreas Applied and Environmental Microbiology, Vol. 82, Issue 9 https://doi.org/10.1128/AEM.03493-15	journal	February 2016
The iron-oxidizing proteobacteria Hedrich, Sabrina; Schlömann, Michael; Johnson, D. Barrie Microbiology, Vol. 157, Issue 6 https://doi.org/10.1099/mic.0.045344-0	journal	June 2011
Does a low-pH microenvironment around phototrophic FeII-oxidizing bacteria prevent cell encrustation by FeIII minerals?: Low-pH microenvironment prevents cell encrustation Hegler, Florian; Schmidt, Caroline; Schwarz, Heinz FEMS Microbiology Ecology, Vol. 74, Issue 3 https://doi.org/10.1111/j.1574-6941.2010.00975.x	journal	October 2010
Interaction of Fe(II) with phosphate and sulfate on iron oxide surfaces Hinkle, Margaret A. G.; Wang, Zimeng; Giammar, Daniel E. Geochimica et Cosmochimica Acta, Vol. 158 https://doi.org/10.1016/j.gca.2015.02.030	journal	June 2015
Anaerobic Fe(II)-Oxidizing Bacteria Show As Resistance and Immobilize As during Fe(III) Mineral Precipitation Hohmann, Claudia; Winkler, Eva; Morin, Guillaume Environmental Science & Technology, Vol. 44, Issue 1 https://doi.org/10.1021/es900708s	journal	January 2010
A Novel Enrichment Culture Highlights Core Features of Microbial Networks Contributing to Autotrophic Fe(II) Oxidation Coupled to Nitrate Reduction Huang, Yu-Ming; Straub, Daniel; Kappler, Andreas Microbial Physiology, Vol. 31, Issue 3 https://doi.org/10.1159/000517083	journal	January 2021
Nitrate Removal by a Novel Lithoautotrophic Nitrate-Reducing, Iron(II)-Oxidizing Culture Enriched from a Pyrite-Rich Limestone Aquifer Jakus, Natalia; Blackwell, Nia; Osenbrück, Karsten Applied and Environmental Microbiology, Vol. 87, Issue 16 https://doi.org/10.1128/AEM.00460-21	journal	July 2021
Identifying and Quantifying the Intermediate Processes during Nitrate-Dependent Iron(II) Oxidation Jamieson, James; Prommer, Henning; Kaksonen, Anna H. Environmental Science & Technology, Vol. 52, Issue 10 https://doi.org/10.1021/acs.est.8b01122	journal	April 2018
Growth kinetics of siderite at 298.15 K and 1 bar Jiang, Clancy Zhijian; Tosca, Nicholas J. Geochimica et Cosmochimica Acta, Vol. 274 https://doi.org/10.1016/j.gca.2020.01.047	journal	April 2020
A New Rate Law Describing Microbial Respiration Jin, Q.; Bethke, C. M. Applied and Environmental Microbiology, Vol. 69, Issue 4 https://doi.org/10.1128/AEM.69.4.2340-2348.2003	journal	April 2003
Stable Isotopes and Iron Oxide Mineral Products as Markers of Chemodenitrification. Jones, L. Camille; Peters, Brian; Lezama Pacheco, Juan S. Environmental Science & Technology, Vol. 49, Issue 6 https://doi.org/10.1021/es504862x	journal	February 2015
Reduced iron induced nitric oxide and nitrous oxide emission Kampschreur, Marlies J.; Kleerebezem, Robbert; de Vet, Weren W. J. M. Water Research, Vol. 45, Issue 18 https://doi.org/10.1016/j.watres.2011.08.056	journal	November 2011
Formation of Fe(III)-minerals by Fe(II)-oxidizing photoautotrophic bacteria 1 1Associate editor: L. G. Benning Kappler, Andreas; Newman, Dianne K. Geochimica et Cosmochimica Acta, Vol. 68, Issue 6 https://doi.org/10.1016/j.gca.2003.09.006	journal	March 2004
Fe(III) mineral formation and cell encrustation by the nitrate-dependent Fe(II)-oxidizer strain BoFeN1 Kappler, A.; Schink, B.; Newman, D. K. Geobiology, Vol. 3, Issue 4 https://doi.org/10.1111/j.1472-4669.2006.00056.x	journal	October 2005
Abiotic oxidation of Fe(II) by reactive nitrogen species in cultures of the nitrate-reducing Fe(II) oxidizer Acidovorax sp. BoFeN1 - questioning the existence of enzymatic Fe(II) oxidation Klueglein, N.; Kappler, A. Geobiology, Vol. 11, Issue 2 https://doi.org/10.1111/gbi.12019	journal	December 2012
Ligand-Enhanced Abiotic Iron Oxidation and the Effects of Chemical versus Biological Iron Cycling in Anoxic Environments Kopf, Sebastian H.; Henny, Cynthia; Newman, Dianne K. Environmental Science & Technology, Vol. 47, Issue 6 https://doi.org/10.1021/es3049459	journal	February 2013
The development of the Arrhenius equation Laidler, Keith J. Journal of Chemical Education, Vol. 61, Issue 6 https://doi.org/10.1021/ed061p494	journal	June 1984
Evidence for the Existence of Autotrophic Nitrate-Reducing Fe(II)-Oxidizing Bacteria in Marine Coastal Sediment Laufer, Katja; Røy, Hans; Jørgensen, Bo Barker Applied and Environmental Microbiology, Vol. 82, Issue 20 https://doi.org/10.1128/AEM.01570-16	journal	October 2016
Microbially mediated nitrate-reducing Fe(II) oxidation: Quantification of chemodenitrification and biological reactions Liu, Tongxu; Chen, Dandan; Luo, Xiaobo Geochimica et Cosmochimica Acta, Vol. 256 https://doi.org/10.1016/j.gca.2018.06.040	journal	July 2019
Crystal structure of green rust formed by corrosion of cast iron McGILL, I. R.; McENANEY, B.; Smith, D. C. Nature, Vol. 259, Issue 5540 https://doi.org/10.1038/259200a0	journal	January 1976
Preservation of protein globules and peptidoglycan in the mineralized cell wall of nitrate-reducing, iron(II)-oxidizing bacteria: a cryo-electron microscopy study: Persistence of organics in mineralized Fe-oxidizing bacteria Miot, J.; Maclellan, K.; Benzerara, K. Geobiology, Vol. 9, Issue 6 https://doi.org/10.1111/j.1472-4669.2011.00298.x	journal	September 2011
Ecophysiology and the energetic benefit of mixotrophic Fe(II) oxidation by various strains of nitrate-reducing bacteria Muehe, Eva Marie; Gerhardt, Simone; Schink, Bernhard FEMS Microbiology Ecology, Vol. 70, Issue 3 https://doi.org/10.1111/j.1574-6941.2009.00755.x	journal	December 2009
Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature Nedwell, D. B. FEMS Microbiology Ecology, Vol. 30, Issue 2 https://doi.org/10.1111/j.1574-6941.1999.tb00639.x	journal	October 1999
Mineral Defects Enhance Bioavailability of Goethite toward Microbial Fe(III) Reduction Notini, Luiza; Byrne, James M.; Tomaszewski, Elizabeth J. Environmental Science & Technology, Vol. 53, Issue 15 https://doi.org/10.1021/acs.est.9b03208	journal	July 2019
Cold Stress Responses in Mesophilic Bacteria Panoff, Jean-Michel; Thammavongs, Bouachanh; Guéguen, Micheline Cryobiology, Vol. 36, Issue 2 https://doi.org/10.1006/cryo.1997.2069	journal	March 1998
Green Rust Formation during Fe(II) Oxidation by the Nitrate-Reducing Acidovorax sp. Strain BoFeN1 Pantke, Claudia; Obst, Martin; Benzerara, Karim Environmental Science & Technology, Vol. 46, Issue 3 https://doi.org/10.1021/es2016457	journal	January 2012
Surface Chemistry and Dissolution Kinetics of Divalent Metal Carbonates Pokrovsky, O. S.; Schott, J. Environmental Science & Technology, Vol. 36, Issue 3 https://doi.org/10.1021/es010925u	journal	February 2002
Nitrite Reduction by Siderite Rakshit, Sudipta; Matocha, Christopher J.; Coyne, Mark S. Soil Science Society of America Journal, Vol. 72, Issue 4 https://doi.org/10.2136/sssaj2007.0296	journal	July 2008
Relationship between temperature and growth rate of bacterial cultures. Ratkowsky, D. A.; Olley, J.; McMeekin, T. A. Journal of Bacteriology, Vol. 149, Issue 1 https://doi.org/10.1128/jb.149.1.1-5.1982	journal	January 1982
Effect of pH and Temperature on Denitrification Gene Expression and Activity in Pseudomonas mandelii Saleh-Lakha, Saleema; Shannon, Kelly E.; Henderson, Sherri L. Applied and Environmental Microbiology, Vol. 75, Issue 12 https://doi.org/10.1128/AEM.00080-09	journal	June 2009
A Revised Iron Extraction Protocol for Environmental Samples Rich in Nitrite and Carbonate Schaedler, Franziska; Kappler, Andreas; Schmidt, Caroline Geomicrobiology Journal, Vol. 35, Issue 1 https://doi.org/10.1080/01490451.2017.1303554	journal	May 2017
Isolation of a High-Affinity Functional Protein Complex between OmcA and MtrC: Two Outer Membrane Decaheme c-Type Cytochromes of Shewanella oneidensis MR-1 Shi, L.; Chen, B.; Wang, Z. Journal of Bacteriology, Vol. 188, Issue 13 https://doi.org/10.1128/JB.01966-05	journal	June 2006
Stimulation by lepidocrocite (7-FeOOH) of Fe(II)-dependent nitrite reduction Sørensen, Jan; Thorling, Lærke Geochimica et Cosmochimica Acta, Vol. 55, Issue 5 https://doi.org/10.1016/0016-7037(91)90307-Q	journal	May 1991
Kinetics of Corrosion Layer Formation: Part 1—Iron Carbonate Layers in Carbon Dioxide Corrosion Sun, W.; Nešić, S. CORROSION, Vol. 64, Issue 4 https://doi.org/10.5006/1.3278477	journal	April 2008
Nitrite reduction with hydrous ferric oxide and Fe(II): Stoichiometry, rate, and mechanism Tai, Yuan-Liang; Dempsey, Brian A. Water Research, Vol. 43, Issue 2 https://doi.org/10.1016/j.watres.2008.10.055	journal	February 2009
A surface complexation model of the carbonate mineral-aqueous solution interface Van Cappellen, Philippe; Charlet, Laurent; Stumm, Werner Geochimica et Cosmochimica Acta, Vol. 57, Issue 15, p. 3505-3518 https://doi.org/10.1016/0016-7037(93)90135-J	journal	August 1993
Nitrite stability influenced by iron compounds Van Cleemput, O.; Baert, L. Soil Biology and Biochemistry, Vol. 15, Issue 2 https://doi.org/10.1016/0038-0717(83)90093-7	journal	January 1983
Effects of temperature on rates and mineral products of microbial Fe(II) oxidation by Leptothrix cholodnii at microaerobic conditions Vollrath, Susann; Behrends, Thilo; Koch, Christian Bender Geochimica et Cosmochimica Acta, Vol. 108 https://doi.org/10.1016/j.gca.2013.01.019	journal	May 2013
Microbially Catalyzed Nitrate-Dependent Oxidation of Biogenic Solid-Phase Fe(II) Compounds Weber, Karrie A.; Picardal, Flynn W.; Roden, Eric E. Environmental Science & Technology, Vol. 35, Issue 8, p. 1644-1650 https://doi.org/10.1021/es0016598	journal	April 2001
Anaerobic Nitrate-Dependent Iron(II) Bio-Oxidation by a Novel Lithoautotrophic Betaproteobacterium, Strain 2002 Weber, K. A.; Pollock, J.; Cole, K. A. Applied and Environmental Microbiology, Vol. 72, Issue 1 https://doi.org/10.1128/AEM.72.1.686-694.2006	journal	January 2006

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