Mossbauer spectroscopic and magnetic studies of magnetoferritin
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1 Mossbauer spectroscopic and magnetic studies of magnetoferritin Q.A. Pankhurst, S. Betteridge, D.P.E. Dickson Department of Physics, University of Liverpool, Liverpool L693BX, UK T. Douglas, S. Mann School of Chemistry, University of Bath, Bath BA2 7AY, UK and R.B. Frankel Physics Department, California Polytechnic State University, San Luis Obispo, CA 93407, USA Mossbauer spectroscopic and magnetic measurements have been made on a novel magnetic protein produced by the controlled reconstitution of ferritin. The data indicate that the predominant mineral form in the iron-containing cores is maghemite (y-fe203) rather than magnetite (Fe304)' 1. Introduction The iron-storage protein ferritin consists of a spherical protein shell of external diameter 12 nm, with an inner cavity of approximately 8 nm diameter [I]. Iron is stored within this cavity as a particle of the hydrated iron oxide mineral ferrihydrite (5Fe203. 9H20). Channels through the protein shell enable iron to be taken up and released. The accumulation and mineralisation of iron appears to involve active sites within the channels and on the inner surface of the protein [2]. It has recently been shown that following removal of the ferrihydrite core from native horse spleen ferritin, it is possible to reconstitute the empty protein shell under controlled oxidative conditions, tailored to the synthesis of magnetite rather than ferrihydrite [3]. This process is illustrated in fig. 1. The material produced, which has been named magnetoferritin, was characterised by electron diffraction, which indicated that the mineral form was either magnetite (Fe304) or maghemite (y-fe203)' The black colour and the restricted oxidation conditions used in the preparation suggested that magnetite was the more likely possibility.
2 Native ferritin Apoferritin Magnetoferdtin Fig. I. Schematic diagram of the process used to produce magnetoferritin. Step I involves the removal of the ferrihydrite cores from native ferritin, while step II involves the reconstitution of apoferritin with Fe(II) under controlled oxidative conditions. Irrespective of whether it contains magnetite or maghemite, magnetoferritin may have considerable importance as a biocompatible ferrofluid, with many possible biomedical and industrial applications based on its magnetic properties. The purpose of the present work is to investigate magnetoferritin by Mfssbauer spectroscopy and magnetization measurements in order to provide additional characterisation of this novel material. 2. Experimental 57Fe M6ssbauer spectra were recorded using a conventional constant acceleration spectrometer, and were calibrated against t~-fe at room temperature. A triangular drive waveform was used, and the resultant spectra were folded to remove any baseline curvature. Spectra were recorded at 100 and 4.2 K using liquid helium flow and bath cryostats. A transverse field of 9 T was applied perpendicular to the direction of the "/-ray beam using a split-pair superconducting solenoid. 3. Results and discussion 3.1. ZERO-FIELD MOSSBAUER SPECTRA The M6ssbauer spectra of the magnetoferritin samples obtained at 100 and 4.2 K are shown in fig. 2. The 100 K spectrum is very different from that of the native ferritin at this temperature, which is a single quadrupole-split doublet due to fast superparamagnetic relaxation. The Fe3 doublet component indicates that some of the reconstituted mineral may be ferrihydrite-like or that there is some superparamagnetic relaxation of the magntoferritin cores. The magnetic sextet component of the 100 K spectrum and the sextet observed at 4.2 K have broad asymmetric lines, presumably due to the heterogeneity of iron sites, which might be expected in a material such as this. The lines do not show the degree of structure observed in the spectra of magnetite at these temperatures, but are consistent with the line shapes observed in the spectra of maghemite. However, the line broadening smears out the differences between the spectra of magnetite and maghemite, and
3 Magnetoferritin 9,, ", 9,, :-, 100 K 4.2 K K, 9.0 T 7-.rays 0.75 I I I -lo'o -6.o '.o o.o Velocity (rnrnls) Fig. 2. M~ssbauer spectra of magnetoferritin at 100 K, and at 4.2 K in zero field and with a magnetic field of 9 T applied perpendicular to the direction of the 7-ray beam. prevents any clear distinction on the basis of the zero-field spectra. The mean value of the hyperfine field, 50 T at 4.2 K, is consistent with those observed in both magnetite and maghemite. 3.2, APPLIED-FIELD MOSSBAUER SPECTRA Considerable information concerning magnetic structure and microscopic magnetic parameters (e.g. exchange field, anisotropy field, spin ratio) can be obtained from the M6ssbauer spectra of polycrystalline samples in large applied magnetic fields [4]. Such applied field spectra can provide more possibilities for discriminating between the different mineral forms of the iron oxides than the zero-field spectra. The M6ssbauer spectrum of magnetoferritin at 4.2 K in a field of 9 T applied perpendicular to the 7-ray beam is shown in fig. 2. (Although the preferred geometry for such an experiment is for the 7-rays to be parallel to the applied field, our longitudinal drive apparatus was malfunctioning during the short time that we had access to the magnetoferritin sample.) It is immediately apparent from the linesplitting and the structure in the spectrum in fig. 2 that the sample is ferrimagnetic. The spectrum comprises two six-line subspectra, one with relatively sharp lines and the other with broader lines. In the subspectrum with the sharper lines, the ratio of the areas of the outer: middle :inner pairs of lines is close to 3 : 4: 1, implying that the magnetic moments are lying in the plane perpendicular to the 3'-ray beam. The
4 magnetic splitting of this subspectrum, which corresponds to the vector addition of the applied and hyperfine field at the nucleus, is T. Since the hyperfine field of an Fe 3+ ion lies antiparallel to its atomic moment, and since the magnitude of the hyperfine field is insensitive to the applied field and will therefore remain ~ 50 T, we conclude that this subspectrum corresponds to moments that are fully collinear with the applied field, and directed antiparallel to it. The subspectrum with the broader lines has a magnetic splitting T and line area ratios of order 3 : 3.3 : 1. Both these factors points to the moments associated with this subspectrum being not fully collinear with the applied field. The reduced magnetic splitting indicates that the moments are inclined towards the applied field. The relative areas of the two subspectra are approximately 31% for the sharp sextet and 69% for the broad sextet. In order that we may identify the material or materials which give rise to this spectrum, it is useful to refer to the spectra associated with the possible constituents of the magnetoferritin cores. In fig. 3, the spectra of well-crystallised "six-line" ferrihydrite [5], poorly crystallised "two-line" ferrihydrite [5], magnetite [6] and maghemite [6] obtained at 4.2 K in 9 T applied fields are shown. The 9 T spectrum of native horse-spleen ferritin is almost identical to that of "six-line" ferrihydrite [7]. 'Six-line' Ferrihydrite 4.2 K, 9.0 T U y-rays o.oo "~ r~ ~'' ~ ~" ~ 4.00 ** z v I,..,r v *Two-line' Fen-ihydri~ 0.00.~'~.r~ e.':% ~ -'"~".~"~"'~'~" e- Magnetite o.oo ~ ~ t.-~, ~ ~ r-,,"--' ~' 9 ~ ~;.. Maghemitc o.oo "-",~.F---~\~:.,--~.~,..,--!J E! ~; ::.. " ":.. v '~ V :" I I I -;o'.o -6.o s zo 8'.o ~o.o Velocity (mm/s) Fig. 3. M0ssbauer spectra of well-crystallised "six-line" ferrihydritc, poorly crysta lised "two-line" ferrihydrite, magnetite and maghemite, recorded at 4.2 K in a magnetic field of 9 T applied parallel to the direction of the 7-ray beam.
5 (The nomenclature "six-line" and "two-line" refers to the number of peaks discernable in the X-ray diffraction scans of the ferrihydrite specimens.) In these spectra, the field was applied parallel to the T-ray beam. This different experimental geometry affects the relative intensities of the second and fifth lines of any constituent sextet. Although spectra obtained in the two geometries are not directly comparable, some conclusions may be drawn by restricting attention to the outermost lines of the spectra in figs. 2 and 3. The magnetoferritin spectrum most closely resembles that of maghemite. This is particularly evident in the relative intensities of the two right-hand-most lines of the magnetoferritin spectrum, where despite its broadening the lower velocity line still has a bigger absorption than the higher velocity line. This characteristic is apparent in the spectrum of maghemite, and is the opposite of the intensity ratio in the corresponding lines of the magnetite spectrum. In addition, the relative areas of the two subspectra in the maghemite spectrum are 37.5% and 62.5%, which is close to that observed in magnetoferritin. We conclude that it appears that the magnetoferritin cores predominantly contain maghemite MAGNETIZATION MEASUREMENTS Room temperature magnetization measurements show Langevin function behaviour, characteristic of ferrimagnetically ordered small particles. There is no evidence for any hysteresis and the magnetic moment per particle is consistent with either magnetite or maghemite particles, with sizes typical of those of ferritin cores. 4. Conclusions The M6ssbauer spectroscopy and magnetization data presented above confirm that magnetoferritin represents a new magnetic protein, which is clearly different from the starting material of native horse-spleen ferritin. The M6ssbauer data indicate that the mineral form of the cores corresponds to maghemite rather than magnetite. This result has implications regarding the understanding of the oxidation processes involved during the reconstitution of this material. References [1] G.C. Ford, P.M. Harrison, D.N. Rice, J.M.A. Smith, A. Treffry, J.L. White and J. Yariv, Phil. Trans. Roy. Soc. London B304(1984)551. [2] P.M. Harrison, P.J. Artymiuk, G.C. Ford, D.M. Lawson, J.M.A. Smith, A. Treffry and J.L. White, in: Biomineralization: Chemicaland Biochemical Perspectives,eds. S. Mann, J. Webb and R.J.P. Williams (VCH, Weinheim, 1989) pp [3] F.C. Meldrum, B.R. Heywood and S. Mann, Science 257(1992)522. [4] Q.A. Pankhurst and R.J. Pollard, J. Phys. C.M. 2(1992)7329. [5] Q.A. Pankhurst and R.J. Pollard, Clays Clay Miner. 40(1992)268. [6] R.J. Pollard, MOssbauer spectra of iron oxides and oxyhydroxides in applied magnetic fields, Internal Report, Department of Physics, Monash University (1992), available upon request. [7] C. Hunt, Q.A. Pankhurst and D.P.E. Dickson, these Proceedings, Hyp. Int.
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