A strong angular dependence of magnetic properties of...

A strong angular dependence of magneticproperties of magnetosome chains: Implicationsfor rock magnetism and paleomagnetism

Jinhua Li, Kunpeng Ge, and Yongxin PanPaleomagnetism and Geochronology Laboratory, Key Laboratory of Earth’s Deep Interior, Institute of Geologyand Geophysics, Chinese Academy of Sciences, Beijing, China ([email protected])

China-France Biomineralization and Nano-Structure Laboratory, Chinese Academy of Sciences, Beijing, China

Wyn WilliamsGrant Institute of Earth Science, University of Edinburgh, Edinburgh, UK

Qingsong Liu and Huafeng QinPaleomagnetism and Geochronology Laboratory, Institute of Geology and Geophysics, Chinese Academy of Sci-ences, Beijing, China

[1] Single-domain magnetite particles produced by magnetotactic bacteria (magnetosomes) and alignedin chains are of great interest in the biosciences and geosciences. Here, we investigated angular variationof magnetic properties of aligned Magnetospirillum magneticum AMB-1 cells, each of which containsone single fragmental chain of magnetosomes. With measurements at increasing angles from the chaindirection, we observed that (i) the hysteresis loop gradually changes from nearly rectangular to a ramp-like shape (e.g., Bc and remanence decrease), (ii) the acquisition and demagnetization curves of IRM shifttoward higher fields (e.g., Bcr increases), and (iii) the FORC diagram shifts toward higher coercivity fields(e.g., Bc,FORC increases). For low-temperature results, compared to unoriented samples, the samplescontaining aligned chains have a much lower remanence loss of field-cooled (�FC) and zero-field-cooled(�ZFC) remanence upon warming through the Verwey transition, higher �-ratio (�¼ �FC/�ZFC) for themeasurement parallel to the chain direction, and lower �-ratio, larger �FC and �ZFC values for theperpendicular measurement. Micromagnetic simulations confirm the experimental observations andreveal that the magnetization reversal of magnetosome chain appears to be noncoherent at low angles andcoherent at high angles. The simulations also demonstrate that the angular dependence of magneticproperties is related to the dispersion degree of individual chains, indicating that effects of anisotropyneed to be accounted for when using rock magnetism to identify magnetosomes or magnetofossils oncethey have been preserved in aligned chains. Additionally, this study experimentally demonstrates anempirical correspondence of the parameter Bc,FORC to Bcr rather than Bc, at least for magnetite chainswith strong shape anisotropy. This suggests FORC analysis is a good discriminant of magnetofossils insediments and rocks.

Components: 12,636 words, 11 figures, 1 table.

Keywords: magnetosome chain; magnetic property; angular dependence; magnetic anisotropy; rock magnetism;paleomagnetism.

Index Terms: 1505 Biogenic magnetic minerals: Geomagnetism and Paleomagnetism; 1540 Rock and mineral magne-tism: Geomagnetism and Paleomagnetism; 1512 Environmental magnetism: Geomagnetism and Paleomagnetism; 0416Biogeophysics: Biogeosciences; 0419 Biomineralization: Biogeosciences.

© 2013. American Geophysical Union. All Rights Reserved. 1

Article

Volume 00, Number 00

0 MONTH 2012

doi: 10.1002/ggge.20228

ISSN: 1525-2027

Received 22 April 2013; Revised 1 July 2013; Accepted 19 July 2013; Published 00 Month 2013.

Li, J., K. Ge, Y. Pan, W. Williams, Q. Liu, and H. Qin (2013), A strong angular dependence of magnetic properties of mag-netosome chains: Implications for rock magnetism and paleomagnetism, Geochem. Geophys. Geosyst., 14, doi:10.1002/ggge.20228.

1. Introduction

[2] Single-domain (SD) magnetite particles syn-thesized by magnetotactic bacteria (MTB) withinintracellular membrane organelles, termed mag-netosomes, are of great interest to a wide varietyof disciplines ranging from the study of biologi-cally controlled mineralization and magnetore-ception in higher organisms to geologicalapplications of paleomagnetic and paleoenviron-mental studies [Faivre and Sch€uler, 2008; Koppand Kirschvink, 2008; Komeili, 2012]. WithinMTB, magnetosomes are formed under strictlybiological control and are often assembled intochain(s), which facilitates navigation of cellsalong the geomagnetic field lines to fast arrive attheir growth-favoring positions within aquaticenvironments, a process known as magnetotaxis[Bazylinski and Frankel, 2004]. The chain con-figuration of magnetosome is physically favor-able for MTB magnetotaxis because it canmaximize the magnetic energy to overcome thethermal energy when the cells are swimming[Bazylinski and Frankel, 2004; Kopp andKirschvink, 2008].

[3] After MTB die, magnetosomes can be pre-served in sediments or sedimentary rocks tobecome magnetofossils [Kopp and Kirschvink,2008]. Magnetofossils potentially contribute to thenatural remanent magnetization (NRM) since theymight have been aligned by the geomagnetic fieldas they fell through the water column and settledin the sediment. Magnetofossils in certain types ofsediments therefore have potential for reconstruct-ing paleomagnetic information [Tarduno et al.,1998; Snowball and Sandgren, 2004; Winklhoferand Petersen, 2007]. Since also MTB commun-ities and their synthesized magnetites are sensitiveto environmental factors such as oxygen and ironsource [Flies et al., 2005; Faivre et al., 2008; Liand Pan, 2012], magnetofossils in natural systemscould bear useful paleoecological and paleoenvir-onmental information [Hesse, 1994; Yamazaki

and Kawahata, 1998; Schumann et al., 2008;Roberts et al., 2011]. Magnetofossils have beenwidely found in a variety of Cenozoic environ-ments in many sediment types, ranging from bio-genic pelagic carbonates to lithogenic sediments,including marine and lacustrine clays, and possi-bly glaci-marine sediments [Kopp and Kirschvink,2008; Roberts et al., 2012].

[4] The study of magnetic properties of magneto-some chains is particularly important not only forbetter understanding the mechanism of MTB bio-mineralization and magnetotaxis but also for iden-tifying magnetofossils from sediments orsedimentary rocks. Magnetic properties of magne-tosomes have been extensively studied both inbulk samples [Moskowitz et al., 1988, 1993; Panet al., 2005; Fischer et al., 2008; Li et al., 2010a,2010b; Gehring et al., 2011a] and in individualcells or chains [Dunin-Borkowski et al., 1998;Hanzlik et al., 2002; P�osfai et al., 2007]. Previousexperimental and theoretical studies have shownthat magnetosomes in chain configuration can beconsidered as an ideal uniaxial SD (USD) particle[Moskowitz et al., 1993; Charilaou et al., 2011].Such USD-like behavior induces a series of dis-tinctive magnetic properties for magnetosomalmagnetites. For instance, intact MTB cells andwell-dispersed magnetosome chains are generallycharacterized by strong magnetic anisotropy andrather weak or no interchain interactions [Mosko-witz et al., 1993; Pan et al., 2005; Chen et al.,2007; Li et al., 2010a, 2012]. The combination ofthese investigations have been used to detect mag-netofossils in geological materials [Kopp et al.,2006, 2009; Egli et al., 2010; Gehring et al.,2011b; Kind et al., 2011; Roberts et al., 2011,2012; Larrasoa~na et al., 2012].

[5] The pronounced magnetic anisotropy of magne-tosome chain originates both from the interparticleinteractions along the linear chains (i.e.,interaction-induced anisotropy) and from the shapeanisotropy of individual particles (i.e., elongation-induced anisotropy) [Muxworthy and Williams,

LI ET AL. : MAGNETISM OF MAGNETOSOME CHAINS 10.1002/ggge.20228

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2006a; P�osfai et al., 2007; Muxworthy and Wil-liams, 2009; Newell, 2009; Li et al., 2010b]. Com-paring simulations with the experimentallyobserved ferromagentic resonance (FMR) spectra,Charilaou et al. [2011] proposed that magnetosomechain can be treated as a Stoner-Wohlfarth-type(SW-type) rotation ellipsoid [e.g., Stoner and Wohl-farth, 1948; Hanzlik et al., 2002].

[6] In the present study, we have performed rockmagnetic measurements and micromagnetic simu-lations on aligned magnetosome chain(s) at vari-ous angles of the given magnetic field relative tothe chain direction in order to further understandthe anisotropy of magnetosome chain and its mag-netic effects.

2. Experimental Measurements

2.1. Sample Preparation

[7] Magnetospirillum magneticum AMB-1(ATCC strain 700264) was cultured anaerobicallyat 26�C in modified ATCC-recommended liquidmedium with addition of 60 mM ferric quinate, asdescribed by Li and Pan [2012]. Cells grown for64 h (i.e., the stationary phase of cell growth) wereharvested by centrifugation at 10,000 rpm for 10min at 4�C. Two types of samples were made, inthe first type the magnetosome chains were ran-domly oriented and in the second the chains wereoriented parallel to each other. The unorientedsample was made directly from the cell pelletformed by centrifugation. For the oriented sample,about 100 ml of cell suspension containing concen-trated living cells (�1010 cells/ml) were depositedand dried on the surface of a small piece of non-magnetic cover slide (�0.3 � �0.3 cm) under thepresence of a strong magnetic field (�1 T, pro-duced by a pair of disk magnets). However, asshown in Figures 1a–1c, the intact AMB-1 cellsare not perfectly aligned. There is a certain degreeof dispersion of individual chains. Statistically, thedispersion angles are in accordance with a circularnormal distribution with mean and standard devia-tion (�) being �0� and �21� (Figure 1d). The mis-alignment of some cells possibly resulted fromthermal and mechanical disturbance during bacte-ria deposition and water evaporation.

[8] To avoid postoxidization, both the orientedand unoriented samples were dried in an anaerobicchamber (Coy Labs, USA, [O2]< 300 ppm). Allsamples were maintained in pure nitrogen atmos-

phere in a refrigerator at �20�C prior to magneticmeasurements.

2.2. Electron Microscopy

[9] Transmission electron microscopy (TEM)observations were carried out on a JEOL JEM-2100F microscope with an accelerating voltage of200 kV. Crystal length (L) and width (W) of mag-netosome, distance between adjacent subchainswithin cells (dsc), and center-to-center distancebetween adjacent particles within subchains (dcc)were measured with the software package ImageJ1.44 (Figure 2 and supporting information FigureS1) [Li et al., 2009]. The grain size (S) and shapefactor of magnetosome are defined as (LþW)/2and W/L, respectively. To determine the crystalhabit and orientation of magnetosomes, high-resolution TEM (HRTEM) lattice images wererecorded with a Gatan UltraScan 4000 4 k � 4 kCCD camera and processed to obtain Fast Fouriertransform (FFT) patterns using the ImageJ 1.44software. Based on HRTEM and the correspond-ing FFT images of individual magnetite (fcc) par-ticles [Faivre et al., 2008], the ideal crystalmorphology of magnetosomes was reconstructed(supporting information Figure S2).

[10] Scanning electron microscopy (SEM) obser-vations were performed on a Zeiss Supra 55microscope. The cover slide hosting orientedAMB-1 cells was mounted on an aluminum SEMstub with high-conductivity copper tape and thencoated with carbon or gold. The microscope wasoperated at 10 kV with a working distance of �7mm, and both in-Lens and Angle selective Back-scattered (AsB) detectors were used to study theorientation of cells and magnetosome chains.

2.3. Room-Temperature MagneticMeasurements

[11] Room-temperature magnetic measurementswere carried out on a Model 3900 vibrating sam-ple magnetometer (Princeton Measurements Cor-poration VSM 3900, sensitivity¼ 5.0 � 10�10

Am2) equipped with a horizontal rotation stage,which allows a sample to be rotated along Z-axisat a minimum step of 1� under computer or manualcontrol. The cover slide carrying oriented cellswas mounted on a Plexiglas holder with double-sided copper tape and horizontally fitted betweenthe pole pieces of the magnet. By rotating the sam-ple stage manually, hysteresis loop, acquisitionand demagnetization of isothermal remanent mag-netization (IRM) curves, and first-order reversal


3

curves (FORCs) at a given field angle were meas-ured. The field angle , which is defined as theangle of the given magnetic field relative to themagnetosome chain direction, was stepwiseincreased from 0� to 360� with 5� intervals.

[12] Hysteresis loops were measured between6500 mT and hysteresis parameters, includingsaturation magnetization (Ms), saturation rema-nence (Mrs), and coercivity (Bc), were determinedafter applying the high-field (350–500 mT) slopecorrections for linear contributions from the dia-magnetic and paramagnetic phases. Static IRM ac-quisition and DC demagnetization curves weremeasured up to 200 mT in a 5 mT increment onpreviously demagnetized samples. Remanencecoercivity (Bcr) was determined from DC demag-

netization curve of saturation IRM (SIRM).FORCs [Pike et al., 1999] were measured follow-ing the protocol as described by Roberts et al.[2000]. For each sample, a total of 120 FORCswere measured with a positive saturation field of500 mT, an increasing field step (�H) of 1.87 mT,and an averaging time of 200 ms. The FORC dia-grams were calculated using the FORCinel version1.22 software with a smoothing factor of 3 [Harri-son and Feinberg, 2008]. The FORC characteristiccoercivity (Bc,FORC) is given by the median coer-civity of the marginal coercivity distribution [Har-rison and Feinberg, 2008].

[13] Recently, Egli et al. [2010] have developed anew protocol for measuring high-resolution

Figure 1. (a–c) SEM images of oriented AMB-1 cells and their intracellular magnetosome chains. Figure 1awas recorded from gold-coated sample, while Figures 1b and 1c are from carbon-coated sample. The arrowslabeled B in Figures 1a–1c indicate the direction of magnetic field which was applied to orient the AMB-1cells. (d) Histogram of dispersion angles of individual magnetosome chains. SEM analyses reveal that intactAMB-1 cells were mounted on the surface of the cover slide and roughly aligned by the external applied mag-netic field with a certain degree of individual dispersions. Statistically, the mean value and standard deviationof individual chain angles in relative to the external applied magnetic field are 0� and 21�, respectively.


4

FORCs, where the minor vertical spreading of theFORC distribution associated with the discrete na-ture of measurements and smoothing is mini-mized. Our previous study has shown that theresolution of FORC measurement had no signifi-cant effects on the Bc,FORC values of magnetosomesamples, although it strongly affects the verticalspreading of the FORC distributions [Li et al.,2012]. Therefore, the lack of resolution of FORCmeasurement in this study is not significantbecause our samples only contain well-dispersedintact magnetosome chains and the data analysisfocuses on the marginal coercivity distribution.

2.4. Low-Temperature MagneticMeasurements

[14] Low-temperature magnetic measurementswere performed with a quantum design magneticproperty measurement system (MPMS XP-5,sensitivity¼ 5.0 � 10�10 Am2). For the orientedsamples, the cover slide was vertically fixed in agelatin capsule respectively at two orientations,which allowed sample to be measured either per-pendicular or parallel to the chain direction. Thechain orientation was first confirmed from their cor-responding 300 K hysteresis loops, i.e., rectangular-

Figure 2. (a) TEM image of one intact AMB-1 cell. Magnetosomes are formed and arranged into one singlefragmental chain, which consists of four subchains separated with large gap but all linearly aligned along thelong axis of the cell. The dsc indicates the distance between adjacent subchains within cell. (b) Close-up onthe area indicated in Figure 2a by the black continuous square. Within subchain, magnetosomes are closelyassembled with long axis of individual particles parallel to the chain direction. The dcc indicates the center-to-center distance between adjacent particles within subchain. HRTEM images of two magnetosomes recordedalong (c) [011] and (d) [112] zone axis of magnetite crystal. The corresponding FFT pattern is indexed andshown at top right-hand corner of the image. TEM and HRTEM observations reveal that AMB-1 magneto-somes are elongated and aligned along [111] crystal direction of magnetite.


5

like and ramp-like loop for the parallel and perpen-dicular measurement, respectively (supporting in-formation Figure S3). Zero-field-cooled (ZFC) andfield-cooled (FC) curves were obtained by coolingsamples from 300 to 10 K in zero field and in a 2.5T field, respectively, followed by imparting a SIRMin a 2.5 T field (hereafter termed as SIRM10K_2.5T),and then measuring the remanence in zero field dur-ing warming to 300 K. Low-temperature cycling(LTC) of SIRM, which acquired at a 2.5 T field at300 K (hereafter termed SIRM300K_2.5T), was meas-ured in zero field during a cooling-warming cycling(300! 10 ! 300 K). The Verwey transition tem-perature (Tv) is defined as the temperature of themaximum in the first-order derivative of the FCcurve. The Verwey transition signature of magneto-some chains is characterized by the �-ratio(�¼ �FC/�ZFC), in which �FC and �ZFC are calcu-lated as �¼ (M80K�M150K)/M80K, where M80K

and M150K are the remanences measured at 80 and150 K, respectively [Moskowitz et al., 1993].

3. Micromagnetic Modeling

[15] For micromagnetic simulations, the particleswithin chain are first meshed into tetrahedral ele-ments according to finite element method (FEM)using the CUBIT (cubit.sandia.gov) softwarepackage [Parthasarathy et al., 1994; Knupp,2000a, 2000b]. For each assembly of magneto-somes, the free magnetic energy (Etotal) can beexpressed in terms of its four components as:

Etotal ¼ Ee þ Ea þ Ed þ Eh ð1Þ

where Ee, Ea, Ed, and Eh are the exchange, crystal-line anisotropy, demagnetizing, and external fieldenergy, respectively [Dunlop and €Ozdemir, 1997].

[16] A hybrid approach to finding equilibriummagnetization states is taken. A fast initial solutionis obtained by minimizing the free energy usingthe conjugate gradient (CG) method [Williams andDunlop, 1989; Williams et al., 2010]. The finalequilibrium state is then obtained by minimizingthe torque on each discretized magnetic momentaccording to the Landau–Lifshitz–Gilbert (LLG)equation [Williams et al., 2011]:

dM

dt¼� �

1þ�2M�Heffþ

��

1þ�2ð ÞMSM� M�Heffð Þ ð2Þ

where M is the unit vector along the magnetizationdirection, � is the gyromagnetic ratio, � is a damp-

ing parameter, and Heff is the effective field actingon the vector at each node of the finite elementmesh defined as:

Heff ¼dEtotal

dMð3Þ

[17] Room-temperature parameters for magnetitewere used: saturation magnetization, Ms¼ 4.8 �105 Am�1, exchange constant, A¼ 1.34 � 1011

Jm�1 [Heider and Williams, 1988], and magneto-crystalline anisotropy, K1¼�1.24 � 104 Jm�3

[Fletcher and O’Reilly, 1974]. The hysteresis loop isacquired between 6200 mT with a 1 mT increment.

3.1. Single Chain

[18] For single chain, the angular variation of hys-teresis loops was obtained by changing the angle of the given magnetic field relative to the chaindirection from 0� to 90� with a step of 5� and thensolving for an equilibrium magnetization state bythe micromagnetic modeling method. From these19 simulated hysteresis loops, the parameters Mrs/Ms and Bc with angle were calculated.

3.2. 2-D and 3-D Oriented Assemblages ofChains

[19] To test the effects of angular dispersion of indi-vidual chains within a bulk sample, the hysteresisloops of 10,000 chains were statistically simulatedaccording to a circular normal and a Fisher continu-ous distribution of dispersion angles (�) for 2-D and3-D assemblages, respectively. Here, we assume thedistances between chains are large enough to be non-interacting. There are two reasons for modeling suchdistributions besides the need of simplifying the cal-culation. The first is that the interactions betweenchains within our experimental samples are ratherweak or negligible due to large gap between adja-cent chains and well separated by cytoplasm (seeFigures 1 and 2). The second is that experimentalobservations of previous studies [Egli et al., 2010;Roberts et al., 2012] demonstrate that magnetosomechains preserved in sediments or rocks (magnetofos-sils) generally interact weakly, possibly due to theirlow concentration and strong magnetic anisotropy.

[20] Within 2-D and 3-D assemblages, the magnet-ization of each chain at a given magnetic field(random angle of the given magnetic field relativeto the magnetosome chain direction from 0� to90�) was obtained by a seven-order polynomial fit-ting of the angular variation of magnetizationcurve, which was in turn calculated from the 19


6

simulated loops. The magnetization of the bulksamples at a given magnetic field was statisticallycalculated according the circular normal (2-D) orFisher distribution (3-D) of �.

[21] For 2-D assemblage, the probability densityfunction f(�) for a specific direction � is given by:

f �j�; �ð Þ¼ 1

2I0 �ð Þexp �cos �� ð Þð Þ ð4Þ

where I0(�) is the modified Bessel function oforder 0, � is a measure of location (the distributionis clustered around �, so is equal to 0 here), and �is a measure of concentration (a reciprocal mea-sure of dispersion, so 1/� is analogous to �2 in thenormal distribution).

[22] For 3-D assemblage, the probability (Pd�(�))of finding a direction within a band of width d�between � and � þd� is given by:

Pd� �ð Þ¼�

2sinh �ð Þ exp �cos�ð Þsin �d� ð5Þ

where � is the precision parameter [Butler, 1992].

[23] For each assemblage of chains, the angular-varied hysteresis loops were obtained by changingthe angle of the given magnetic field relative to thedistribution of the chain direction range from 0� to90�. Finally, the angular variations of Bc and Mrs/Ms with dispersion degrees (i.e., �) were obtained.Bcr was estimated directly from the hysteresisloops [Tauxe et al., 1996].

3.3. 2-D and 3-D Random Assemblages ofChains

[24] We also simulated the angular variation ofhysteresis loops of chains with a random distribu-tion of � to constrain the maximum dispersion ofindividual chains within bulk sample.

[25] Specially for 2-D assemblage with a randomdistribution of �, the probability density functionf(�) is given by:

f �ð Þ¼ 1

2ð6Þ

[26] And for 3-D assemblage with a random distri-bution of �, the probability (Pd�(�)) in the band ofwidth d � is given by:

Pd� �ð Þ¼1

2sin �d� ð7Þ

4. Experimental Results

4.1. Characteristics of MagnetosomeChains in AMB-1

[27] AMB-1 spirillum has an average cell lengthof �3.0 �m and a diameter of �0.5 �m (Figure2a). Grown under anaerobic condition used here,AMB-1 synthesized an average per cell of 26 mag-netosomes with mean crystal length, width andshape factor of 49.3 nm, 41.0 nm, and 0.83,respectively. A majority of cells (>90%) formed afragmental chain of magnetosomes linearlyaligned along the long axis of the cell. Each frag-mental chain is composed of several well-separated subchains [Li et al., 2009]. Statistically,the median values of subchain number per cell andintersubchain distance (dsc) are 4 and 164 nm withthe corresponding interquartile ranges being 2 and151 nm, respectively. Each subchain contains av-erage six close-packed magnetosomes with meandcc of 54.3 nm (supporting information Figure S1).Smaller particles often occur at the ends of sub-chain (Figure 2b).

[28] Based on HRTEM observations and morphol-ogy modeling, the AMB-1 synthesized magneto-somes can be recognized as truncated octahedronmagnetites with both elongation direction of indi-vidual particles and chain axis approximately par-allel to [111] crystal direction of magnetite (Figure2 and supporting information Figure S2).

4.2. Angular Variation of HysteresisParameters

[29] As expected, the unoriented sample of AMB-1 cells displays a typical magnetic behavior of ran-domly oriented noninteracting SD particles forMTB magnetite [Moskowitz et al., 1993], i.e., SW-type hysteresis loop with Mrs/Ms being equal to 0.5[Stoner and Wohlfarth, 1948], symmetric normal-ized IRM acquisition and demagnetization curveswith the crossing value R (i.e., the Wohlfarth-Cisowski test) being close to 0.5 [Cisowski, 1981].However, the hysteresis loop and IRM acquisitionand demagnetization magnetization curves of theoriented sample are strongly angle dependent.With the field angle increasing from 0� (parallelto the chain direction) to 90� (perpendicular to thechain direction), the hysteresis loop becomes fromnearly rectangular to ramp-like shape (Figure 3a),


7

and both the normalized IRM acquisition anddemagnetization curves shift toward higher fieldswith higher coercivity tails becoming moreobvious (Figure 3b). The hysteresis loop and IRMacquisition and demagnetization curves of theunoriented sample are more or less similar inshapes to those for the oriented sample measuredat around 60�. Its hysteresis parameters Mrs/Ms,Bcr, Bc, and Bcr/Bc are also comparable to those forthe oriented sample measured at ¼ 60� (Figure4). For the oriented sample, with increasingfrom 0� to 90�, it is observed that Mrs and Mrs/Ms

gradually decrease, Bcr and Bcr/Bc increase, whileMs keeps nearly constant. Bc keeps almost constantbetween 0� and 50� and then decreases rapidly to90�. From 90� to 180� (antiparallel to the chaindirection), samples exhibit a mirror angular rela-tionship compared to the case with decreasingfrom 90� to 0�. The variations from 180� to 360�

are similar to those from 0� to 180� (Figures 3 and4). A small fluctuation in Ms can be observed dur-ing the rotating measurements (Figure 4a). Thismay be related to some artificial effects, e.g., a

nonsaturating behavior and/or slightly shifting ofsample position. Additionally, we noted that theoriented sample could not be fully demagnetizedbefore the IRM measurements. The demagnetiza-tion becomes harder at higher field angles. Thisbehavior, which is different from the unorientedsample, may be related to prominent shape anisot-ropy of the oriented sample.

[30] Mrs, Mrs/Ms, and Bc of the oriented samplemaximize for measurements parallel to the chaindirection, e.g., Mrs¼ 4.57 � 10�7 Am2, Mrs/Ms¼ 0.84, and Bc¼ 32.0 mT at ¼ 0�, and mini-mize at the perpendicular direction to the chain,e.g., Mrs¼ 1.36 � 10�7 Am2, Mrs/Ms¼ 0.24, andBc¼ 20.5 mT at ¼ 90�. In contrast, Bcr and Bcr/Bc minimize at the chain direction, e.g., Bcr¼ 32.5mT and Bcr/Bc¼ 1.02 at ¼ 0�, and maximize atthe perpendicular direction to the chain, e.g.,Bcr¼ 45.1 mT and Bcr/Bc¼ 2.20 at ¼ 90�. De-spite the above systematic changes of hysteresisparameters with the field angle , each pair of nor-malized IRM acquisition and demagnetization

Figure 3. Normalized hysteresis loops (left) and IRM acquisition and demagnetization curves (right) forunoriented (dash-lined curves) and oriented sample (solid-lined curves) of AMB-1 cells measured at variousangles (showing in different colors) with respect to the magnetosome chain direction. (a and b) The field anglevaries from 0� to 90�. (c and d) The field angle varies from 90� to 180�.


8

curves is nearly symmetric and the R-values of theWohlfarth-Cisowski test are close to 0.5 (Figures3b and 3d), which indicates, as expected, no inter-actions among chains for the whole-cell sample[Cisowski, 1981; Moskowitz et al., 1988; Li et al.,2010a]. Therefore, the systematic variations ofhysteresis parameters mentioned above should bederived from the magnetic anisotropy of magneto-some chains.

4.3. Angular Variation of FORC Diagram

[31] FORC diagrams for unoriented and orientedsamples of AMB-1 cells are shown in Figure 5.All samples have FORC diagrams characteristic ofa pair of positive peak at a specific Bc and negativepeak near the Bb axis, as well as a narrow verticaldistribution (Figures 5a–5h). These features,which are indicative of noninteracting USDassemblages [Pike et al., 1999; Roberts et al.,2000; Newell, 2005], can also be regarded as a so-called central ridge in high-resolution FORCmeasurements [Egli et al., 2010; Li et al., 2012;Roberts et al., 2012].

[32] Compared with the unoriented counterpart, theoriented sample has a narrower horizontal (coerciv-ity) distribution of FORC when the measurement iscloser to ¼ 0�, while more extended when closerto ¼ 90�. Furthermore, the FORC distribution ofthe oriented sample shifts horizontally towardhigher coercivity fields with the field angle increasing from 0� to 90� and from 180� to 270�

and toward lower coercivity fields from 90� to 180�

and from 270� to 360� (e.g., Figures 5a–5h). Thisvariation is also evident in the horizontal profile ofFORC distribution at Bb¼ 0 mT, where it shifts to-ward higher coercivity fields and becomes broaderwith increasing from 0� to 90� (Figure 5i).

4.4. Low-Temperature MagneticProperties

[33] Low-temperature magnetic properties areshown in Figure 6. Compared with the unorientedsample, the oriented sample of AMB-1 cells meas-ured approximately parallel (�0�) to the magneto-some chain shows less difference between FC and

Figure 4. Angular variations of hysteresis parameters for oriented sample of AMB-1 cells. (a) Saturationmagnetization (Ms, solid squares) and saturation remanence (Mrs, open squares). (b) Remanence ratio (Mrs/Ms). (c) Coercivity (Bc, open circles) and remanence coercivity (Bcr, solid circles). (d) Bcr/Bc. The parametersfor unoriented sample are plotted in the corresponding figures.


9

ZFC curves below Tv, and more suppressed expres-sion of the Verwey transition on both FC and ZFCcurves. The DSIRM10K_2.5T (defined as (FC-SIRM10K_2.5T – ZFC-SIRM10K_2.5T)/FC-SIRM10K_2.5T), as well as �FC and �ZFC decreasefrom 36%, 0.27 and 0.056 for the former to 18%,0.095 and �0 for the latter (Table 1). When meas-ured approximately perpendicular (�90�) to themagnetosome chain, the oriented sample exhibits asignificantly enhanced Verwey transition comparedwith the above two measurements, having valuesof DSIRM10K_2.5T, �FC and �ZFC of 39%, 0.36 and0.20, respectively (Table 1).

[34] Curiously, the oriented sample measured par-allel to the chain direction experiences a slightincrease in remanence on ZFC curve from �104 K(i.e., Tv) to �134 K (�0.7% increasing in inten-sity) rather than the gradual decrease seen in theperpendicular measurement and the unorientedsample (see inset figures in Figure 6). To exactlyestimate the magnitude of remanence loss inducedby the Verwey transition, the � for the parallel

measurement of the oriented sample is recalcu-lated as �0 ¼ (M80K�M104K)/M80K. The new val-ues of �FC, �ZFC, and �0-ratio are 0.072, 0.0055,and 13.0, respectively.

[35] Additionally, unlike reversible cooling-warming cycling curves of SIRM300K_2.5T for theunoriented sample and the parallel measurementof the oriented sample, the warming curve of theoriented sample measured perpendicular to thechain direction shows only a small recover of rem-anence through the Verwey transition, and then anobviously thermal decay up to 300 K, resulting ina �7% loss of remanence after the low-temperature cycling (Figure 6 and Table 1).

5. Simulation Results

[36] On the basis of TEM observations and mor-phology modeling (Figure 2 and supporting infor-mation Figure S2), we created a subchaingeometry of magnetosomes for micromagnetic

Figure 5. FORC diagrams for (a) unoriented sample and oriented sample of AMB-1 cells measured at (b)0� (parallel to the magnetosome chain direction), (c) 15�, (d) 30�, (e) 45�, (f) 60�, (g) 75�, and (h) 90� (perpen-dicular to the magnetosome chain direction). (i) Horizontal profiles at Bb¼ 0 mT of FORC distributions.


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A strong angular dependence of magnetic properties of...

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