Fe(III) (oxyhydr)oxide reduction by the thermophilic iron-reducing bacterium Desulfovulcanus ferrireducens

Some thermophilic bacteria from deep-sea hydrothermal vents grow by dissimilatory iron reduction, but our understanding of their biogenic mineral transformations is nascent. Mineral transformations catalyzed by the thermophilic iron-reducing bacterium Desulfovulcanus ferrireducens during growth at 55°C were examined using synthetic nanophase ferrihydrite, akaganeite, and lepidocrocite separately as terminal electron acceptors. Spectral analyses using visible-near infrared (VNIR), Fourier-transform infrared attenuated total reflectance (FTIR-ATR), and Mössbauer spectroscopies were complemented with x-ray diffraction (XRD) and transmission electron microscopy (TEM) using selected area electron diffraction (SAED) and energy dispersive X-ray (EDX) analyses. The most extensive biogenic mineral transformation occurred with ferrihydrite, which produced a magnetic, visibly dark mineral with spectral features matching cation-deficient magnetite. Desulfovulcanus ferrireducens also grew on akaganeite and lepidocrocite and produced non-magnetic, visibly dark minerals that were poorly soluble in the oxalate solution. Bioreduced mineral products from akaganeite and lepidocrocite reduction were almost entirely absorbed in the VNIR spectroscopy in contrast to both parent minerals and the abiotic controls. However, FTIR-ATR and Mössbauer spectra and XRD analyses of both biogenic minerals were almost identical to the parent and control minerals. The TEM of these biogenic minerals showed the presence of poorly crystalline iron nanospheres (50–200 nm in diameter) of unknown mineralogy that were likely coating the larger parent minerals and were absent from the controls. The study demonstrated that thermophilic bacteria transform different types of Fe(III) (oxyhydr)oxide minerals for growth with varying mineral products. These mineral products are likely formed through dissolution-reprecipitation reactions but are not easily predictable through chemical equilibrium reactions alone.

[1]  M. Dyar,et al.  Spectral Detection of Nanophase Iron Minerals Produced by Fe(III)-Reducing Hyperthermophilic Crenarchaea , 2022, Astrobiology.

[2]  K. Livi,et al.  A Multi-Technique Analysis of Surface Materials From Blood Falls, Antarctica , 2022, Frontiers in Astronomy and Space Sciences.

[3]  J. Holden,et al.  Desulfovulcanus ferrireducens gen. nov., sp. nov., a thermophilic autotrophic iron and sulfate-reducing bacterium from subseafloor basalt that grows on akaganéite and lepidocrocite minerals , 2022, Extremophiles : life under extreme conditions.

[4]  E. Swanner,et al.  An evolving view on biogeochemical cycling of iron , 2021, Nature Reviews Microbiology.

[5]  M. Tomczyk,et al.  The FT-IR and Raman Spectroscopies as Tools for Biofilm Characterization Created by Cariogenic Streptococci , 2020, International journal of molecular sciences.

[6]  M. Dyar,et al.  Reduction and Morphological Transformation of Synthetic Nanophase Iron Oxide Minerals by Hyperthermophilic Archaea , 2018, Front. Microbiol..

[7]  F. Rull,et al.  Abiotic versus biotic iron mineral transformation studied by a miniaturized backscattering Mössbauer spectrometer (MIMOS II), X-ray diffraction and Raman spectroscopy , 2017 .

[8]  J. Holden,et al.  Pyrodictium delaneyi sp. nov., a hyperthermophilic autotrophic archaeon that reduces Fe(III) oxide and nitrate. , 2016, International journal of systematic and evolutionary microbiology.

[9]  K. Edwards,et al.  Iron Transformation Pathways and Redox Micro-Environments in Seafloor Sulfide-Mineral Deposits: Spatially Resolved Fe XAS and δ57/54Fe Observations , 2016, Front. Microbiol..

[10]  M. Lilley,et al.  Linkages between mineralogy, fluid chemistry, and microbial communities within hydrothermal chimneys from the Endeavour Segment, Juan de Fuca Ridge , 2016, Geochemistry Geophysics Geosystems.

[11]  M. Dyar,et al.  Magnetite formation from ferrihydrite by hyperthermophilic archaea from Endeavour Segment, Juan de Fuca Ridge hydrothermal vent chimneys , 2014, Geobiology.

[12]  J. Bosch,et al.  Iron oxide nanoparticles in geomicrobiology: from biogeochemistry to bioremediation. , 2013, New biotechnology.

[13]  T. Prozorov,et al.  Chemical Purity of Shewanella oneidensis-Induced Magnetites , 2013 .

[14]  J. Huber,et al.  Modeling the Impact of Diffuse Vent Microorganisms Along Mid‐Ocean Ridges and Flanks , 2013 .

[15]  E. Bonch‐Osmolovskaya,et al.  Deferrisoma camini gen. nov., sp. nov., a moderately thermophilic, dissimilatory iron(III)-reducing bacterium from a deep-sea hydrothermal vent that forms a distinct phylogenetic branch in the Deltaproteobacteria. , 2012, International journal of systematic and evolutionary microbiology.

[16]  C. Vetriani,et al.  Chemoautotrophy at deep-sea vents : past, present, and future , 2012 .

[17]  M. Schulte,et al.  Biogeochemical processes at hydrothermal vents : microbes and minerals, bioenergetics, and carbon fluxes , 2012 .

[18]  C. Romanek,et al.  Magnetite as a prokaryotic biomarker: A review , 2010 .

[19]  Enrique Iañez-Pareja,et al.  Magnetite biomineralization induced by Shewanella oneidensis , 2010 .

[20]  E. Bonch‐Osmolovskaya,et al.  Geoglobus acetivorans sp. nov., an iron(III)-reducing archaeon from a deep-sea hydrothermal vent. , 2009, International journal of systematic and evolutionary microbiology.

[21]  J. Lloyd,et al.  Mineralogical and morphological constraints on the reduction of Fe(III) minerals by Geobacter sulfurreducens , 2009 .

[22]  E. Bonch‐Osmolovskaya,et al.  Deferribacter autotrophicus sp. nov., an iron(III)-reducing bacterium from a deep-sea hydrothermal vent. , 2009, International journal of systematic and evolutionary microbiology.

[23]  M. Dyar,et al.  Degeneration of biogenic superparamagnetic magnetite , 2009, Geobiology.

[24]  G. Waychunas,et al.  Structure, chemistry, and properties of mineral nanoparticles , 2008 .

[25]  D. Kelley,et al.  Abundances of Hyperthermophilic Autotrophic Fe(III) Oxide Reducers and Heterotrophs in Hydrothermal Sulfide Chimneys of the Northeastern Pacific Ocean , 2008, Applied and Environmental Microbiology.

[26]  L. Legrand,et al.  Carbonate and sulphate green rusts—Mechanisms of oxidation and reduction , 2008 .

[27]  D. Lovley,et al.  Characterization of extracellular minerals produced during dissimilatory Fe(III) and U(VI) reduction at 100 °C by Pyrobaculum islandicum , 2008, Geobiology.

[28]  M. Hannington,et al.  Growth history of a diffusely venting sulfide structure from the Juan de Fuca Ridge: A petrological and geochemical study , 2006 .

[29]  Jizhong Zhou,et al.  Metal Reduction and Iron Biomineralization by a Psychrotolerant Fe(III)-Reducing Bacterium, Shewanella sp. Strain PV-4 , 2006, Applied and Environmental Microbiology.

[30]  J. Kirschvink,et al.  Formation of tabular single-domain magnetite induced by Geobacter metallireducens GS-15. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[31]  P. Nico,et al.  Structural constraints of ferric (hydr)oxides on dissimilatory iron reduction and the fate of Fe(II) , 2004 .

[32]  V. Barrón,et al.  Potential Pathways to Maghemite in Mars Soils: The Key Role of Phosphate , 2004 .

[33]  V. Barrón,et al.  Hydromaghemite, an intermediate in the hydrothermal transformation of 2-line ferrihydrite into hematite , 2003 .

[34]  U. Schwertmann,et al.  The Iron Oxides: Structure, Properties, Reactions, Occurrences and Uses , 2003 .

[35]  S. Spring,et al.  Deferribacter abyssi sp. nov., an anaerobic thermophile from deep-sea hydrothermal vents of the Mid-Atlantic Ridge. , 2003, International journal of systematic and evolutionary microbiology.

[36]  V. Barrón,et al.  Can the presence of structural phosphorus help to discriminate between abiogenic and biogenic magnetites? , 2003, JBIC Journal of Biological Inorganic Chemistry.

[37]  R. Kukkadapu,et al.  Secondary Mineralization Pathways Induced by Dissimilatory Iron Reduction of Ferrihydrite Under Advective Flow , 2003 .

[38]  U. Schwertmann,et al.  Iron Oxides , 2003, SSSA Book Series.

[39]  D. Lovley,et al.  Thermophily in the Geobacteraceae: Geothermobacter ehrlichii gen. nov., sp. nov., a Novel Thermophilic Member of the Geobacteraceae from the “Bag City” Hydrothermal Vent , 2003, Applied and Environmental Microbiology.

[40]  D. Lovley,et al.  Geoglobus ahangari gen. nov., sp. nov., a novel hyperthermophilic archaeon capable of oxidizing organic acids and growing autotrophically on hydrogen with Fe(III) serving as the sole electron acceptor. , 2002, International journal of systematic and evolutionary microbiology.

[41]  Steven C. Smith,et al.  Biomineralization of Poorly Crystalline Fe(III) Oxides by Dissimilatory Metal Reducing Bacteria (DMRB) , 2002 .

[42]  D. Sparks,et al.  ATR-FTIR Spectroscopic Investigation on Phosphate Adsorption Mechanisms at the Ferrihydrite-Water Interface , 2001 .

[43]  R. Messina,et al.  A Raman and infrared study of a new carbonate green rust obtained by electrochemical way , 2001 .

[44]  E. Bonch‐Osmolovskaya,et al.  Evidence for the presence of thermophilic Fe(III)-reducing microorganisms in deep-sea hydrothermal vents at 13 degrees N (East Pacific Rise). , 2001, FEMS microbiology ecology.

[45]  D. Lovley,et al.  Anaerobic degradation of aromatic compounds coupled to Fe(III) reduction by Ferroglobus placidus. , 2001, Environmental microbiology.

[46]  U. Schwertmann,et al.  Iron Oxides in the Laboratary , 2000 .

[47]  Sigg,et al.  Reductive Dissolution of Fe(III) (Hydr)oxides by Cysteine: Kinetics and Mechanism , 1997, Journal of colloid and interface science.

[48]  R. Keller,et al.  Electron microscopy and 57Fe Mössbauer spectra of 10 nm particles, intermediate in composition between Fe3O4and γ‐Fe2O3, produced by bacteria , 1996 .

[49]  R. Vandenberghe,et al.  On the methodology of the analysis of Mössbauer spectra , 1994 .

[50]  U. Schwertmann,et al.  The Formation of Green Rust and Its Transformation to Lepidocrocite , 1994, Clay Minerals.

[51]  D. Lovley Dissimilatory Fe(III) and Mn(IV) reduction , 1991, Microbiological reviews.

[52]  R. Frankel,et al.  Structure and morphology of magnetite anaerobically-produced by a marine magnetotactic bacterium and a dissimilatory iron-reducing bacterium , 1990 .

[53]  R. M. Cornell,et al.  Effect of Cysteine and Manganese on the Crystallization of Noncrystalline Iron(III) Hydroxide at pH 8 , 1990 .

[54]  Derek R. Lovley,et al.  Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism , 1987, Nature.

[55]  D. Lovley,et al.  Determination of Fe(III) and Fe(II) in oxalate extracts of sediment , 1987 .

[56]  J. Hobbie,et al.  Use of nuclepore filters for counting bacteria by fluorescence microscopy , 1977, Applied and environmental microbiology.

[57]  T. Misawa,et al.  Infrared Absorption Spectra and Oxidation of Iron(II) Hydroxide and Green Rust I , 1969 .

[58]  M. Dyar,et al.  Spectral and morphological characteristics of synthetic nanophase iron (oxyhydr)oxides , 2017, Physics and Chemistry of Minerals.