Controlled cobalt doping in the spinel structure of magnetosome magnetite: new evidences from element- and site-specific X-ray magnetic circular dichroism analyses

Abstract

The biomineralization of magnetite nanocrystals (called magnetosomes) by magnetotactic bacteria (MTB) has attracted intense interest in biology, geology and materials science due to the precise morphology of the particles, the chain-like assembly and their unique magnetic properties. Great efforts have been recently made in producing transition metal-doped magnetosomes with modified magnetic properties for a range of applications. Despite some successful outcomes, the coordination chemistry and magnetism of such metal-doped magnetosomes still remain largely unknown. Here, we present new evidences from X-ray magnetic circular dichroism (XMCD) for element- and site-specific magnetic analyses that cobalt is incorporated in the spinel structure of the magnetosomes within Magnetospirillum magneticum AMB-1 through the replacement of Fe(2+) ions by Co(2+) ions in octahedral (Oh) sites of magnetite. Both XMCD at Fe and Co L2,3 edges, and energy-dispersive X-ray spectroscopy on transmission electron microscopy analyses reveal a heterogeneous distribution of cobalt occurring either in different particles or inside individual particles. Compared with non-doped one, cobalt-doped magnetosome sample has lower Verwey transition temperature and larger magnetic coercivity, related to the amount of doped cobalt. This study also demonstrates that the addition of trace cobalt in the growth medium can significantly improve both the cell growth and the magnetosome formation within M. magneticum AMB-1. Together with the cobalt occupancy within the spinel structure of magnetosomes, this study indicates that MTB may provide a promising biomimetic system for producing chains of metal-doped single-domain magnetite with an appropriate tuning of the magnetic properties for technological and biomedical applications.

Keywords: X-ray magnetic circular dichroism; biomineralization; cobalt-doped magnetite; coordination chemistry; magnetic alteration; magnetotactic bacteria.

Figure 1.

Characterization of magnetosomes produced by AMB-1 cells within the Co(0) (a,b), Co(2.1) (c,d) and Co(12.1) (e,f) cultures. (a,c,e) HAADF-STEM images of AMB-1 cells and magnetosomes, while (b,d,f) indicate the corresponding grain size distributions (values of mean size (standard deviation), distribution skewness and statistics number are shown in each panel).

Figure 2.

Magnetic properties of magnetosomes produced by AMB-1 cells within the Co(0) (a–c), Co(2.1) (d–f) and Co(12.1) (g–i) cultures. (a,d,g) Room-temperature, first-order reversal curves (FORCs) diagrams; (b,e,h) thermal decays of saturation remanence magnetization imparted at 2.5 T at 10 K after cooling the sample from 300 to 10 K in a 2.5 T field (FC) and zero field (ZFC); (c,f,i) hysteresis loop measured at temperatures 5, 100, 200 and 300 K. Note that the x-axes scales of (c), (f) and (i) are different.

Figure 3.

XMCD spectra measured at Fe L_2,3 edges on the Co(0) magnetosomes (a,b) and on the Co(12.1) magnetosomes (c,d). The experimental XMCD signals are plotted in black dots and compared with the result of the best linear combination (red line) of maghemite and magnetite reference samples (see Methods). The arrow in (d) indicates the missing fraction of Fe²⁺ in O_h site that is interpreted as resulting from Co²⁺ substitution.

Figure 4.

(a) Experimental XAS spectra at the Fe and Co L_2,3 edges on the Co(12.1) magnetosomes for right and left polarized X-rays in a 0.6 T magnetic field at 4 K. The baseline difference prior to the Co L_2,3 edges is due to magnetic XAFS from Fe L_2,3 edges. (b) Experimental XMCD signal (black dots) at the Co L_2,3 edges compared with the ligand field multiple calculated spectrum (red line) for octahedral Co²⁺ ion. The two peaks around 780 and 795 eV in (a) arise from the M_4,5 edges of Ba impurities in the Si wafer on which the sample was deposited (electronic supplementary material, figure S5).

Figure 5.

Element-specific magnetization curves detected at 3 K by XMCD at the Fe (black line) and Co (red line) L₃ edges in the Co(0) magnetosomes (a) and Co(12.1) magnetosomes (b). Note that the x-axis is different for the two types of magnetosomes.

Figure 6.

EDXS measurements performed on individual magnetosome particles. (a) TEM image of one magnetosome chain within one same cell which was analysed by EDXS in TEM mode. (b,c) EDX spectra of six individual particles as indicated by the numbers in (a). For each particle, the EDX spectrum was recorded with a counting time of 4 min and an electron probe of several nanometres to optimize a good signal to noise ratio and to minimize the induced irradiation damage of the particles. All the EDX spectra were normalized by their own Fe-Kα peak, and therefore the degree of asymmetry of Fe-Kβ peak (approx. 7.05 keV) and the intensity of Co-Kβ peak (approx. 6.92 keV) could be compared among the six individual particles and closely related to their cobalt amounts. Clearly, those cobalt-doped magnetosomes are characterized by an obviously asymmetric Fe-Kβ peak (approx. 7.05 keV) with a small shoulder at approximately 6.92 keV (i.e. Co-Kα peak) along with a small Co-Kβ peak at approximately 7.65 keV, i.e. particles 1–3 may contain more cobalt than particles 4–6.