Hostname: page-component-848d4c4894-ttngx Total loading time: 0 Render date: 2024-06-11T10:19:26.141Z Has data issue: false hasContentIssue false
  • English
  • Français

Bacterial production of vanadium ferrite spinel (Fe,V)3O4 nanoparticles

Published online by Cambridge University Press:  01 July 2020

Victoria S Coker ,
Gerrit van der Laan ,
Neil D Telling ,
Jonathan R Lloyd ,
James M Byrne ,
Elke Arenholz  and
Richard AD Pattrick Open the ORCID record for Richard AD Pattrick [Opens in a new window]
Victoria S Coker*
Affiliation:
School of Earth & Environmental Sciences, University of Manchester, ManchesterM13 9PL, UK
Gerrit van der Laan
Affiliation:
School of Earth & Environmental Sciences, University of Manchester, ManchesterM13 9PL, UK Magnetic Spectroscopy Group, Diamond Light Source, Didcot, OxfordshireOX11 0DE, UK
Neil D Telling
Affiliation:
Institute for Science and Technology in Medicine, Keele University, Thornburrow Drive, Hartshill, Stoke-on-TrentST4 7QB, UK
Jonathan R Lloyd
Affiliation:
School of Earth & Environmental Sciences, University of Manchester, ManchesterM13 9PL, UK
James M Byrne
Affiliation:
School of Earth Sciences, Wills Memorial Building, Queens Road, Clifton, BristolBS8 1R, UK
Elke Arenholz
Affiliation:
Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA
Richard AD Pattrick
Affiliation:
School of Earth & Environmental Sciences, University of Manchester, ManchesterM13 9PL, UK
*
*Author for correspondence: Victoria S Coker, Email: vicky.coker@manchester.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Biogenic nanoscale vanadium magnetite is produced by converting V(V)-bearing ferrihydrites through reductive transformation using the metal-reducing bacterium Geobacter sulfurreducens. With increasing vanadium in the ferrihydrite, the amount of V-doped magnetite produced decreased due to V-toxicity which interrupted the reduction pathway ferrihydrite–magnetite, resulting in siderite or goethite formation. Fe L2,3 and V L2,3 X-ray absorption spectra and data from X-ray magnetic circular dichroism analysis revealed the magnetite to contain the V in the Fe(III) Oh site, predominately as V(III) but always with a component of V(VI), present a consistent V(IV)/V(III) ratio in the range 0.28 to 0.33. The bacteriogenic production of V-doped magnetite nanoparticles from V-doped ferrihydrite is confirmed and the work reveals that microbial reduction of contaminant V(V) to V(III)/V(IV) in the environment will occur below the Fe-redox boundary where it will be immobilised in biomagnetite nanoparticles.

Keywords

vanadiumbiomagnetiteGeobacter sulfurreducensL2,3-edge XASXMCD
Type
Article
Information
Mineralogical Magazine , Volume 84 , Issue 4 , August 2020 , pp. 554 - 562
Copyright
Copyright © The Mineralogical Society of Great Britain and Ireland, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Current address: CHESS/Wilson Lab, 161 Synchrotron Drive, Ithica, NY 14853, 607-255-7163, USA.

Associate Editor: Janice Kenney

References

Arenholz, E. and Prestemon, S.O. (2005) Design and performance of an eight-pole resistive magnet for soft X-ray magnetic dichroism measurements. Reviews of Scieintific Instruments, 76, 083908/083901-083908.Google Scholar
Balan, E., De Villiers, J.P.R., Eeckhout, S.G., Glatzel, P., Toplis, M.J., Fritsch, E., Allard, T., Galoisy, L. and Calas, G. (2006) The oxidation state of vanadium in titanomagnetite from layered basic intrusions. American Mineralogist, 91, 953–956.CrossRefGoogle Scholar
Bordage, A., Balan, E., Villiers, J.R., Cromarty, R., Juhin, A.l., Carvallo, C., Calas, G., Sunder Raju, P.V. and Glatzel, P. (2011) V oxidation state in Fe-Ti oxides by high-energy resolution fluorescence-detected X-ray absorption spectroscopy. Physics and Chemistry of Minerals, 38, 449–458.CrossRefGoogle Scholar
Bredberg, K., Karlsson, H.T. and Holst, O. (2004) Reduction of vanadium(V) with Acidithiobacillus ferrooxidans and Acidithiobacillus thiooxidans. Bioresource Technology, 92, 93–96.CrossRefGoogle ScholarPubMed
Brik, M.G., Ogasawara, K., Ikeno, H. and Tanaka, I. (2006) Fully relativistic calculations of the L 2,3-edge XANES spectra for vanadium oxides. European Physics Journal B, 51, 345–355.CrossRefGoogle Scholar
Byrne, J.M., Telling, N.D., Coker, V.S., Pattrick, R.A.D., van der Laan, G., Arenholz, E., Tuna, F. and Lloyd, J.R. (2011) Control of nanoparticle size, reactivity and magnetic properties during the bioproduction of magnetite by Geobacter sulfurreducens. Nanotechnology, 22, 455709.CrossRefGoogle ScholarPubMed
Byrne, J.M., Coker, V.S., Moise, S., Wincott, P.L., Vaughan, D.J., Tuna, F., Arenholz, E., van der Laan, G., Pattrick, R.A.D., Lloyd, J.R. and Telling, N.D. (2013) Controlled cobalt doping in biogenic magnetite nanoparticles. Journal of the Royal Society Interface, 10, 20130134.CrossRefGoogle ScholarPubMed
Caccavo, F. Jr, Lonergan, D.J., Lovley, D.R., Davis, M., Stolz, J.F. and McInerney, M.J. (1994) Geobacter sulfurreducens sp. nov., a hydrogen and acetate-oxidizing dissimilatory metal reducing bacterium. Applied & Environmental Microbiology, 60, 3752–3759.CrossRefGoogle Scholar
Carpentier, W., Sandra, K., De Smet, I., Brige, A., De Smet, L. and Van Beeumen, J. (2003) Microbial reduction and precipitation of vanadium by Shewanella oneidensis. Applied and Environmental Microbiology, 69, 3636–3639.CrossRefGoogle ScholarPubMed
Cawthorn, R. and Molyneaux, T. (1986) Vanadiferous magnetite deposits of the Bushveld Complex. Pp. 1251–1266 in: Mineral Deposits of South Africa (Anhaeusser, C. and Maske, S., editors). Geological Society of Africa, Johannesburg.Google Scholar
Coker, V.S., Pearce, C.I., Lang, C., van der Laan, G., Pattrick, R.A.D., Telling, N.D., Schüler, D, Arenholz, E. and Lloyd, J.R. (2007). Cation site occupancy of biogenic magnetite compared to polygenic ferrite spinels determined by X-ray magnetic circular dichroism. European Journal of Mineralogy, 19, 707–716.CrossRefGoogle Scholar
Coker, V.S., Pearce, C.I., Pattrick, R.A.D., van der Laan, G., Telling, N.D., Charnock, J.M., Arenholz, E. and Lloyd, J.R. (2008a) Probing the site occupancies of Co, Ni and Mn substituted biogenic magnetite using XAS and XMCD. American Mineralogist, 93, 1119–1132.CrossRefGoogle Scholar
Coker, V.S., Bell, A.M.T., Pearce, C.I., Pattrick, R.A.D., van der Laan, G. and Lloyd, J.R. (2008 b) Time-resolved synchrotron X-ray powder diffraction study of magnetite formation by the Fe(III)-reducing bacterium, Geobacter sulfurreducens. American Mineralogist, 93, 540–547.CrossRefGoogle Scholar
Coker, V.S., Telling, N.D., van der Laan, G., Pattrick, R.A.D., Pearce, C.I., Arenholz, E., Tuna, F., Winpenny, R.E.P. and Lloyd, J.R. (2009) Harnessing the extracellular bacterial production of nanoscale cobalt ferrite with exploitable magnetic properties. ACS Nano, 3, 1922–1928.CrossRefGoogle ScholarPubMed
Cornell, R.M. and Schwertmann, U. (2003) The Iron Oxides: Structure, Properties, Reactions, Occurrences and Uses, pp 186, Wiley-VCH, Germany.CrossRefGoogle Scholar
Cutting, R.S, Coker, V.S., Fellowes, J.W., Lloyd, J.R., Vaughan, D.J. (2009) Mineralogical and morphological constraints on the reduction of Fe(III) minerals by Geobacter sulfurreducens. Geochimica et Cosmochimica Acta, 73, 4004–4022.CrossRefGoogle Scholar
Duffy, L.B., Figueroa, A.I., van der Laan, G. and Hesjedal, T. (2017) Co-doping of SbxTe3 thin films with V and Cr. Physical Review Materials, 1, 064409.CrossRefGoogle Scholar
Ehrenreich, A. and Widdel, F. (1994) Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Applied and Environmental Microbiology, 60, 4517–4526.CrossRefGoogle ScholarPubMed
Evans, L.J. and Barabash, S.J. (2010) Molybdenum, silver, thallium and vanadium. Pp. 515–549 in: Trace Elements in Soils, John Wiley & Sons, Ltd.CrossRefGoogle Scholar
French, S., Fakra, S.C., Trevors, J.T. and Glasauer, S. (2012) Changes in Shewanella putrefaciens CN32 membrane stability upon growth in the presence of soluble Mn(II), V(IV), and U(VI). Geomicrobiology Journal, 30, 245–254.CrossRefGoogle Scholar
Hansel, C.M., Benner, S.G., Neiss, J., Dohnalkova, A., Kukkadapu, R.K. and Fendorf, S. (2003) Secondary mineralization pathways induced by dissimilatory iron reduction of ferrihydrite under advective flow. Geochimica et Cosmochimica Acta, 67, 2977–2992.CrossRefGoogle Scholar
Hansel, C.M., Benner, S.G. and Fendorf, S. (2005) Competing Fe(II)-induced mineralization pathways of ferrihydrite. Environmental Science & Technology, 39, 7147–7153.CrossRefGoogle ScholarPubMed
Heiba, Z.K., Mohamed, B.K., Wahba, A.M. and Almalowi, M.I. (2018). Effect of vanadium doping on structural and magnetic properties of defective nano-nickel ferrite. Applied Physics A, 124, 10.1007/s00339-018-1721-3.CrossRefGoogle Scholar
Israel, Y. and Meites, L. (1985) Vanadium. In: Standard Electrode Potentials in Aqueous Solution. Monographs in Electroanalytical Chemistry and Electrochemistry. (Bard, A.J. A.J., Parsons, R. R. and Jordan, J., editors), Marcel Dekker, Inc, New York.Google Scholar
Jolivet, J.-P., Tronc, E. and Chaneac, C. (2002) Synthesis of iron oxide-based magnetic nanomaterials and composites. Comptes Rendus Chimie, 5, 659–664.CrossRefGoogle Scholar
Kamika, I. and Momba, M.N.B. (2012) Comparing the Tolerance Limits of Selected Bacterial and Protozoan Species to Vanadium in Wastewater Systems. Water, Air and Soil Pollution, 223, 2525–2539.CrossRefGoogle Scholar
Kang, J.-S., Hwang, J., Kim, D.H., Lee, E., Kim, W.C., Kim, C.S., Kwon, S., Lee, S., Kim, J.-Y., Ueno, T., Sawada, M., Kim, B., Kim, B.H. and Min, B.I. (2012) Valence states and spin structure of spinel FeV2O4 with different orbital degrees of freedom. Physical Review B, 85, 165136CrossRefGoogle Scholar
Kaur, N, Singh, B.J., Kennedy, B. and Gräfe, M. (2009). The preparation and characterization of vanadium-substituted goethite: The importance of temperature. Geochimica et Cosmochimica Acta, 73, 582–593.CrossRefGoogle Scholar
Kim, K.J., Choi, S.-l., Lee, H.J., Lee, J.H. and Park, J.Y. (2007a) Evolution of structural and optical-absorption properties in VxFe3−xO4. Solid State Communications, 143, 285–288.CrossRefGoogle Scholar
Kim, K.J., Choi, S.-l., Park, Y.R., Lee, J.H., Park, J.Y. and Kim, S.J. (2007b) Magnetic and electronic properties of vanadium-substituted magnetite VxFe3xO4 thin films. Journal of Magnetism and Magnetic Materials, 310, e876–e877.CrossRefGoogle Scholar
Klemm, D., Henckel, J., Dehm, R. M. and Von Gruenewald, G. (1985) The geochemistry of titanomagnetite in magnetite layers and their host rocks of the eastern Bushveld Complex. Economic Geology, 80, 1075–88.CrossRefGoogle Scholar
Larsson, M., Hadialhejazi, G. and Gustafsson, J. (2017) Vanadium sorption by mineral soils: Development of a predictive model. Chemosphere, 168, 925–932.CrossRefGoogle ScholarPubMed
Liang, X.L., Zhu, S.Y., Zhong, Y.H., Zhu, J.X., Yuan, P., He, H.P. and Zhang, J. (2010) The remarkable effect of vanadium doping on the adsorption and catalytic activity of magnetite in the decolorization of methylene blue. Applied Catalysis B-Environmental, 97, 151–159.CrossRefGoogle Scholar
Lloyd, J.R. (2003) Microbial reduction of metals and radionuclides. FEMS Microbiology Reviews, 27, 411–425.CrossRefGoogle ScholarPubMed
Lloyd, J.R., Leang, C., Hodges Myerson, A.L., Coppi, M.V., Cuifo, S., Methe, B., Sandler, S.J. and Lovley, D.R. (2003) Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. Biochemistry Journal, 369, 153–161.CrossRefGoogle ScholarPubMed
Lovley, D.R. (1993) Dissimilatory metal reduction. Annual Reviews in Microbiology, 47, 263–290.CrossRefGoogle ScholarPubMed
Lovley, D.R. and Phillips, E.J.P. (1986) Organic material mineralization with reduction of ferric iron in anaerobic sediments. Applied & Environmental Microbiology, 51, 683–689.CrossRefGoogle Scholar
Maganas, D., Roemelt, M., Weyhermuller, T., Blume, R., Havecker, M., Knop-Gericke, A., DeBeer, S., Schlogl, R. and Neese, F. (2014) L-edge X-ray absorption study of mononuclear vanadium complexes and spectral predictions using a restricted open shell configuration interaction Ansatz. Physical Chemistry Chemical Physics, 16, 264–276.CrossRefGoogle ScholarPubMed
Matsuura, K., Sagayama, H., Nii, Y., Khanh, N.D., Abe, N. and Arima, T. (2015) X-ray magnetic circular dichroism study of an orbital ordered state in the spinel-type vanadium oxide AV2O4 (A = Mn, Fe). Physical Review B, 92, 035133.CrossRefGoogle Scholar
Michelin, A., Drouet, E., Foy, E, Dynes, J.J., Neff, D. and Dillmann, P. (2013). Investigation at the nanometre scale on the corrosion mechanisms of archaeological ferrous artefacts by STXM. Journal of Analytical and Atomic Spectrometry, 28, 59–66.CrossRefGoogle Scholar
Moon, J.-W., Yeary, L.W., Rondinone, A.J., Rawn, C.J., Kirkham, M.J., Roh, Y., Love, L.J. and Phelps, T.J. (2007) Magnetic response of microbially synthesized transition metal- and lanthanide-substituted nanosized magnetites. Journal of Magnetism and Magnetic Materials, 313, 283–292.CrossRefGoogle Scholar
Nivoix, V. and Gillot, B. (2000) Synthesis and stability region of stoichiometric nanocrystalline vanadium−iron spinel powders. Chemical Materials, 12, 2971–2976.CrossRefGoogle Scholar
Nohair, M., Aymes, D., Perriat, P. and Gillot, B. (1995) Infrared spectra-structure correlation study of vanadium-iron spinels and of their oxidation products. Vibrational spectroscopy, 9, 181–190.CrossRefGoogle Scholar
Okabayashi, J., Miyasaka, S., Hemni, K., Tanaka, K., Tajima, S., Wadati, H., Tanaka, A., Takagi, Y. and Yokoyama, T. (2015) Investigating orbital magnetic moments in spinel-type MnV2O4 using X-ray magnetic circular dichroism. Journal of the Physical Society of Japan, 84, 104703.CrossRefGoogle Scholar
Ortiz-Bernad, I., Anderson, R.T., Vrionis, H.A. and Lovley, D.R. (2004) Vanadium respiration by Geobacter metalireducens: Novel strategy for in situ removal of vanadium from groundwater. Applied and Environmental Microbiology, 70, 3091–3095.CrossRefGoogle ScholarPubMed
Pattrick, R.A.D., van der Laan, G., Henderson, C.M.B., Kuiper, P., Dudzik, E. and Vaughan, D.J. (2002) Cation site occupancy in spinel ferrites studied by X-ray magnetic circular dichroism: Developing a method for mineralogists. European Journal of Mineralogy, 14, 1095–1102.CrossRefGoogle Scholar
Peacock, C. and Sherman, D (2004). Vanadium(V) adsorption onto goethite (α-FeOOH) at pH 1.5 to 12: A surface complexation model based on ab initio molecular geometries and EXAFS spectroscopy. Geochimica et Cosmochimica Acta, 68, 1723–1733.CrossRefGoogle Scholar
Pearce, C.I., Henderson, C.M.B., Telling, N.D., Pattrick, R.A.D., Charnock, J.M., Coker, V.S., Arenholz, E., Tuna, F. and van der Laan, G. (2010) Fe site occupancy in magnetite–ulvospinel solid solutions: A new approach using X-ray magnetic circular dichroism. American Mineralogist, 95, 425–439.CrossRefGoogle Scholar
Safarik, I. and Safarikova, M. (2002) Magnetic nanoparticles and biosciences. Monatshefte für Chemie, 133, 737–759.Google Scholar
Scherrer, P. (1918) Estimation of size and internal structure of colloidal particles by means of Rontgen rays. Nachr Ges Wiss Gottingen, 96–100.Google Scholar
Stookey, L.L. (1970) Ferrozine – A new spectrophotometric reagent for iron. Analytical Chemistry, 42, 779–781.CrossRefGoogle Scholar
Taylor, J., Keith, S., Cseh, L.I., Chappell, L., Rhoades, J. and Hueber, A. (2012) Toxicological Profile for Vanadium, US. Department of Health and Human Services Public Health Service Agency for Toxic Substances and Disease Registry, Atlanta, USA. pp 255.Google Scholar
White, A.F. and Peterson, M.L. (1996) Reduction of aqueous transition metal species on the surfaces of Fe(II)-containing oxides. Geochimica Cosmochimica Acta, 60, 3799–3814.CrossRefGoogle Scholar
van der Laan, G. and Figueroa, A.I. (2014) X-ray magnetic circular dichroism – a versatile tool to study magnetism. Coordination Chemistry Reviews, 277–278, 95–129.CrossRefGoogle Scholar
van der Laan, G. and Kirkman, I.W (1992) The 2p absorption spectra of 3d transition metal compounds in tetrahedral and octahedral symmetry. Journal of Physics: Condensed Matter, 4, 4189–4204.Google Scholar
van der Laan, G. and Thole, B.T. (1991) Strong magnetic X-ray dichroism in 2p absorption spectra of 3d transition metal ions. Physical Review B, 43, 13401–13411.CrossRefGoogle ScholarPubMed
Yurkova, N.A. and Lyalikova, N.N. (1991) New vanadate-reducing facultative chemolithotrophic bacteria. Microbiology, 59, 672–677.Google Scholar
Zhang, B., Hao, L., Tian, C., Tuan, S., Feng, C., Ni, J. and Borthwick, A.G.L. (2015) Microbial reduction and precipitation of vanadium (V) in groundwater by immbolized mixed anaerobic culture. Bioresource Technology, 192, 410–417.CrossRefGoogle Scholar
Zhou, M.-F., Robinson, P.T., Lesher, C.M., Keays, R.R., Zhang, C.-J. and Malpas, J. (2005) Geochemistry, Petrogenesis and Metallogenesis of the Panzhihua Gabbroic Layered Intrusion and Associated Fe–Ti–V Oxide Deposits, Sichuan Province, SW China. Journal of Petrology, 46, 2253–2280.CrossRefGoogle Scholar