- Frontier letter
- Open Access
Constraining the magnetic properties of ultrafine- and fine-grained biogenic magnetite
© The Author(s) 2018
- Received: 2 September 2018
- Accepted: 14 December 2018
- Published: 24 December 2018
- Superparamagnetism (SP)
- Magnetosome magnetite
- Low-temperature measurements
- Biogenic magnetite
Superparamagnetic (SP) magnetite has been found in numerous geological samples, e.g., soils, pelagic sediments, tuffs and ice sheets, usually with some distinct magnetic properties; therefore, they are of great interests in rock magnetism, environmental magnetism and paleomagnetism. While progress has been made in identifying the SP magnetite in nature samples (Bedanta and Kleemann 2009; Creer 1961; Dunlop 1973; Lanci and Kent 2006; Liu et al. 2010; Maher 2016; Oldfield et al. 1981; Smirnov and Tarduno 2001; Tarduno 1995; Tauxe and Wu 1990; van de Moortele et al. 2007; Worm and Jackson 1999), some ambiguities in measurement interpretation remain, partially because of uncertainties in size distribution and particle magnetostatic interaction.
Worm and Jackson (1999) studied the magnetite in the Yucca Mountain tuff samples through measurement of hysteresis loops, isothermal remanent magnetization acquisition, thermal demagnetization and frequency and temperature dependence of susceptibility. They noted deviations exist between modeled and measured susceptibility, which was associated with size-dependent anisotropy, non-uniform magnetization and also uncertainties in the pre-exponential time (Worm and Jackson 1999). The pre-exponential time of magnetite was thought to be size-dependent and sensitive to particle interaction (Cao et al. 2010; Moskowitz et al. 1997).
Although SP magnetite grains are unable to retain a remanence at room temperature, numerical simulations and experimental measurements indicate that SP magnetite in sediments is abundant evidenced by their contribution to hysteresis loops (Tauxe et al. 1996). Their presence is indicative of magnetite reduction diagenesis at the Fe-redox boundary in pelagic sediments (Roberts et al. 2013; Tarduno 1995) and can reflect climate-associated pedogenesis in loess and soils (Maher 2016).
Stoichiometric SP magnetite with very narrow size distribution and good biocompatibility is also of great interest in magnetic nanomaterial production and related medical applications, e.g., contrast agents of magnetic resonance imaging (Bonnemain 1998; Hergt et al. 1998; Roch et al. 1999; Thorat et al. 2016; Tromsdorf et al. 2007; Wang et al. 2001), hyperthermia treatments of tumors (Hergt et al. 2008; Jordan et al. 1999), biomedical application (Fan et al. 2012; Gao et al. 2017; Schaefer et al. 2007; Thorek et al. 2006) and nanometric biomaterials (Amstad et al. 2011; Cao et al. 2014; Zhang et al. 2017).
Ferritin is a widely existing iron-storage protein in many living organisms throughout animals, plants and bacterias. It is a cage-like protein with an external diameter of 12 nm and an inner diameter of 8 nm, an ideal versatile platform for synthesis of size-controllable nanometer-scale ferrimagnetic particles. The structure of mature mammalian ferritin consists of a 24-subunit protein, composed of heavy subunits (H) and light subunits (L). Cao et al. (2010) used the recombinant human H-chain ferritin (HFn) and successfully synthesized mono-dispersed, non-interacting ferrimagnetic magnetoferritin (M-HFn) nanoparticles, which have magnetite cores with average diameters of a few nanometers (Cai et al. 2015; Cao et al. 2010). These biomimetic synthesized ferrimagnetic cores have extremely narrow size distribution and high crystallinity, are superparamagnetic at ambient temperature and due to their intact protein shell separation, have nearly no magnetostatic interactions (Cao et al. 2010; Walls et al. 2013).
Magnetotactic bacteria (MTB) intracellularly produce nanosized single-domain (SD) magnetite magnetosomes (30–120 nm), usually arranged in chains, allowing the microbes orientate in the ambient magnetic field (Blakemore 1975; Bazylinski and Frankel 2004), which is a model microorganism for biogeomagnetism study. MTB play important roles in sedimentary magnetism and iron cycling and have application in paleoenvironmental studies (Lin et al. 2014). Over the past decades, MTB have been found in a diverse range of aquatic environments, such as freshwater lakes, rivers, ponds, estuaries, lagoons, mangrove swamps, intertidal zones, deep-sea sediments, marine oxygen minimum zones, saline–alkaline lakes and hot springs, and appear to be important in the geochemical cycling of Fe, S, N and C and so forth (Bazylinski and Frankel 2004; Faivre and Schuler 2008; Kirschvink 1980; Kopp and Kirschvink 2008; Lin et al. 2014; Pan et al. 2005a; Schuler and Frankel 1999; Simmons and Edwards 2007; Zhou et al. 2012). Fossil magnetosomes (magnetofossils) have been widely identified in numerous of sediments, and they are important magnetic carriers (Chang et al. 2014; Channell et al. 2013a, b; Kopp et al. 2007; Li et al. 2013; Liu et al. 2015; Mao et al. 2014; Moskowitz et al. 1993, 2008; Pan et al. 2005b; Petersen et al. 1986; Yamazaki and Shimono 2012; Zhao et al. 2016).
In this study, we characterized the ultrafine-grained magnetite of M-HFn and fine-grained SD magnetosome magnetite by both room- and low- temperature magnetic measurements. The magnetoferritin, Magnetospirillum gryphiswaldense MSR-1 whole cells and two mixed samples with different concentrations of magnetoferritins were analyzed. The objective of this study is to examine magnetic properties of these two types of biogenic magnetites, in particular the traits of ultrafine-grained superparamagnetic magnetite. Applications of ultrafine- and fine-grained magnetite in rock magnetism, biomagnetic and biomedicine are also discussed.
Preparation of samples
The M-HFn nanoparticles were synthesized by the recombinant ferritin cage using the method of Cao et al. (2010) with minor modifications. Fe(II) (25 mM (NH4)2Fe(SO4)2·6H2O) was added in a rate of 80 Fe/protein/minute. Simultaneously, freshly prepared H2O2 (8.33 mM) was added as an oxidant in accordance with stoichiometric equivalents (1:3, H2O2/Fe2+). Then a theoretical 7000 atoms of Fe per protein cage was added to the reaction vessel and allowed to react for another 10 min. Then, 200 μl of 300 mM sodium citrate was added to each sample to chelate any free metal ions. Finally, purification was performed through size exclusion chromatography (Sepharose 6B, GE Healthcare) after centrifugation at 10,000 rpm for 30 min at 4 °C.
Magnetospirillum gryphiswaldense strain MSR-1 was cultured in a sodium lactate medium (SLM) at 30 °C while spinning at 100 rpm (Ding et al. 2010; Jogler and Schuler 2009); sterile ferric citrate was added as iron source. Fresh whole cells were collected by centrifugation at 8000 rpm for 10 min at 4 ◦C after culturing for 24 h.
In this study, four samples (M1, M2, M3 and M4) were prepared and used for magnetic measurements, namely M1, pure M-HFn nanoparticles, dry weight 3.1 mg; M2, a mixture of M-HFn nanoparticles (39.4 wt%) and MSR-1 whole cells (60.6 wt%), dry weight 15.5 mg; M3, a mixture of M-HFn (14.0 wt%) and MSR-1 whole cells (86.0 wt%), dry weight 22.5 mg; and M4, pure MSR-1 whole cells, dry weight 12.8 mg. Note that the magnetization and remanence values of this paper were calculated using the sample’s dry weight. Samples were transferred into non-magnetic capsules and stored in anoxic chamber before magnetic measurements.
Transmission electronic microscopy analysis
Magnetite cores within M-HFn nanoparticles and magnetosome magnetite in MSR-1 whole cells were examined by transmission electronic microscopy (TEM, JEOL JEM2100) operating at 200 kV. The sizes of magnetoferritin and magnetosome were analyzed using standard analytical software. The major and minor axes of magnetite were used as the length (L) and width (W) of the crystal, respectively. The grain size was defined as (L + W)/2.
Room-temperature hysteresis, first-order reversal curve (FORC) and saturation isothermal remanent magnetization (SIRM) measurements
Room-temperature hysteresis loops, FORCs and SIRMs were measured using a VSM3900 magnetometer (Princeton Measurements Corporation, USA, sensitivity 5.0 × 10−10 Am2). A total 120 curves were measured in FORCs using an increasing field step of 0.721 mT with an averaging time of 500 ms. The FORC diagrams were processed using FORCinel version 1.18 software (Harrison and Feinberg 2008) with a smooth factor of 3.
Low-temperature magnetic measurements
Low-temperature magnetic measurements were taken with a Quantum Design MPMS XP-5 SQUID magnetometer (sensitivity 5.0 × 10−10 Am2). Hysteresis loops were measured at temperatures 5 K, 10 K and 20 K. Low-field magnetization curves were measured between 5 and 300 K in a field of 1 mT field after the sample was cooled from 300 to 5 K in zero-field (zero-field cooling, ZFC) and 1 mT field (field cooling, FC), respectively. The thermal decay of saturation isothermal remanence (acquired in 2.5T at 5 K) was measured between 5 and 300 K after the sample was cooled in ZFC and FC (in a 2.5-T field) from 300 to 5 K, respectively. The AC susceptibility measurements were taken between 5 and 300 K at frequencies of 1, 5, 10, 50, 100, 200, 500 and 1000 Hz in a peak AC field of 0.4 mT.
Grain size and mass of magnetites in samples
Figure 1h–i shows the M-HFn nanoparticles adhered to MSR-1 cell surface in the mixed sample M2. Magnetite nanoparticles are separated by cell membrane and protein shell. Figure 1j shows the X-ray diffraction of the magnetite of M-HFn nanoparticles of Fig. 1i, confirming the crystalline ultrafine-grained magnetite in the M-HFn nanoparticles.
Hysteresis parameters obtained from room-temperature measurements
Magnetite in M-HFn (mg)
Magnetite in MSR-1 (mg)
FORCs diagram and magnetic interaction analysis
Hysteresis parameters obtained from low-temperature measurements
Low-temperature magnetic variation, blocking temperature and Verwey transition
Frequency dependence of AC susceptibility
Sample M4 containing only MTB cells has a totally different behavior in the χ′ -T and χ′′-T curves. Both χ′ and χ′′ increased slightly up to 85 K and then increased much more rapidly between 85 and 135 K, corresponding to the Verwey transition of magnetite. Above 130 K, χ′ continuously increased up to 300 K, while χ′′ decreased slightly. M4’s χ′ shows frequency dependence, and the values of χ′ decrease with increasing frequencies.
Magnetic signature of SP magnetite
Ferritin-based ultrafine-grained magnetites can be taken as ideal sample for superparamagnetism study, because of (1) controllable and uniform grain size, (2) mono-dispersed, (3) lack of magnetic interaction, (4) good availability and (5) “ideal” SP behaviors at room temperature. Hysteresis loop confirmed that the ultrafine-grained magnetites in sample M1 with a mean size of 5.3 ± 1.2 nm are superparamagnetic at room temperature (Fig. 3), which corresponds to a Tb of 35 K (Fig. 5); at T < Tb, they can carry remanence (Fig. 6). Their frequency dependences of AC magnetic susceptibility are significant, e.g., peak temperature and value of AC susceptibilities decrease with frequency from 1 Hz to 1 kHz (Fig. 7). Cao et al. (2010) previously determined the value of pre-exponential factor f0 in the Néel–Arrhenius equation from AC susceptibility data of M-HFn nanoparticles with a mean grain size of 3.9 ± 1.2 nm: (9.2 ± 7.9) × 1010 Hz and the extrapolated value of Mrs/Ms = 0.5 and Bcr/Bc = 1.12 at 0 K, which suggests the ferrimagnetic M-HFn is dominated by uniaxial anisotropy.
Grain size effect of SP magnetite is an interesting subject to probe. In the combination of data of this study and available magnetic results of magnetoferritins (Cai et al. 2015; Yang et al. 2017; Zhang et al. 2017), it is noted that Ms, Tb, Hc and peroxidase-like activity enhance with grain sizes. Recently, Cai et al. found that the synthesized M-HFn containing Fe2O3 cores with a mean grain size of 2.2 nm has a high longitudinal relaxivity value of 0.94 mM−1 s−1 and they proposed it as a potential positive contrast agent for magnetic resonance angiography (Cai et al. 2018). Efficiency of hyperthermia using ultrafine-grained iron oxides is also related to grain size of magnetic minerals (Banobre-Lopez et al. 2013; Deatsch and Evans 2014). Therefore, grain size effects of SP magnetites on mineral magnetism and related applications for biomedical detection and therapy need investigations.
Magnetic signature of bacterial SD magnetite
Over the past several decades, there are few studies on their magnetic properties of MTB samples (Ding et al. 2010; Li et al. 2009, 2010; Moskowitz et al. 1993; Prozorov et al. 2007; Weiss et al. 2004; Wang et al. 2015). The cultivated MSR-1 cells used in current study (M4 sample) contain in average 10–15 magnetite magnetosomes with a mean size of 29.6 ± 7.6 nm, arranged in single chains (Fig. 1d–g); the size of magnetosome magnetite in MSR-1 is slightly smaller than 38 nm of the wild-type MSR-1 (Ding et al. 2010), 44 nm of Magnetospirillum strain XM-1 (Wang et al. 2015) and 42 nm of Magnetospirillum magneticum AMB-1 (Li et al. 2009), probably, due to the strain degradation in cultivation. Strain degradation of MSR-1 may be caused by genetic instability (Ullrich et al. 2005), which is a common cause of strain degradation in industrial production (Gravius et al. 1993). The FORC diagram is nicely characterized by a rather narrow distribution around Hc,FORC ~ 13.8 mT along the horizontal axis, the so-called central ridge distribution (Egli et al. 2010) and a negative area in lower left region (Fig. 3). The Tv of 100 K is comparable to other cultivated MTB and uncultivated MTB (Li et al. 2010; Ding et al. 2010; Pan et al. 2005b; Moskowitz et al. 1993; Wang et al. 2015), confirming the lower Tv as a good indicative of MTB-produced magnetites.
Analysis of SP contribution in mixed samples
In this study two mixed samples with different portions of SP and SD magnetite were magnetically characterized. As mentioned previously, SP magnetite and SD magnetite in measured samples are well separated by protein and membranes; it led to magnetic interaction ignorable. With the known composition and grain size distribution, results of samples M2 (containing 84 wt% SP magnetite and 16 wt% SD magnetite) and M3 (containing 57 wt% SP magnetite and 43 wt% SD magnetite) provide us unambiguous constraints on contributions of either SP or SD component.
The room-temperature FORC diagrams for M2 and M3 are similar to that of M4 (Fig. 3), which is clearly signal of chain-arranged SD magnetosome magnetites. In contrast, the bulk magnetic properties, e.g., Hc, Ms and Mrs, χ′ and χ′′, measured at low temperatures of sample M2 and M3 (Table 2; Figs. 4, 5, 6, 7) are controlled by the SP magnetite. Comparing samples M1 to M3, at T ≤ 20 K, Mrs values decay rapidly with both temperature and SP concentrations; the Ms decay with SP concentrations but not with temperatures (Table 2); it suggests that the decay rates of Mrs and Ms at T < 20 K may be useful in estimating SP component in samples.
At room temperature, as expected, Mrs/Ms of samples M4 and M2 decrease from 0.37 to 0.02 while their Hrs/Hc increase from 1.58 to 8.72, respectively, reflecting significant influence of SP component to the hysteresis (Tauxe et al. 1996; Dunlop 2002). However, it should be aware that the measured mixed samples contained only non-interacting SP and SD magnetite. More measurements on samples with different concentrations and compositions are needed.
Identification of fossil magnetite in sediments
Although it has been found that present-day magnetotactic bacteria are ubiquitous in a diverse range of aquatic environments, identification of fossil magnetite from sediments as well as deciphering their paleoenvironmental and paleomagnetic records is somehow not straightway, because of relatively low concentrations of magnetofossils in sediments and mixtures with abundant detrital origin single- and multi-domain magnetites. This study confirms the magnetosome magnetite in MSR-1 does have a Tv around 100 K and central ridge behavior in FORCs. Through extensive investigation on both uncultivated and cultivated MTBs over past decades, it has been well demonstrated that magnetofossils can be identified through measurement of combination of the delta ratio (Moskowitz et al. 1993), FORCs (Egli et al. 2010), identification of lower Tv temperatures (Chang et al. 2014; Pan et al. 2005b), ferromagnetic resonance (Weiss et al. 2004), unique chemical signatures (Amor et al. 2015), Fe isotope signature (Amor et al. 2016), as well as TEM examinations. Recently, Lin et al. found through genetic and genomic analyses that magnetotactic bacteria may appear in Archean time, indicative of an Archean geomagnetic field and a small amount of oxygen in oceanic habitats (Lin et al. 2017). To uncover potential paleoenvironmental and paleomagnetic records carried by magnetofossils in sediments over geological time is desired.
YXP designed this work. TWZ carried out the experiments. YXP and TWZ analyzed data and wrote the manuscript. Both authors read and approved the final manuscript.
TWZ is now a research associate of Biogeomagnetism Laboratory at Institute of Geology and Geophysics, Chinese Academy of Sciences. He obtained bachelor degree of biotechnology at Anhui University and master degree of microbiology at China Agriculture University under the supervision of Prof. Ying Li. He joined the Biogeomagnetism Laboratory at Institute of Geology and Geophysics in 2012. His current main research interests include biomineralization of iron oxides and medical magnetic nanomaterials. YXP is now a research professor at Institute of Geology and Geophysics, Chinese Academy of Sciences (IGGCAS). He obtained bachelor and master degrees of geology at the China University of Geosciences under the supervision of Prof. Naihe Huang, a Ph.D. degree of geophysics under the supervision of Prof. Rixang Zhu. He joined the Paleomagnetism and Geochronology Laboratory at Institute of Geology and Geophysics in 1998. He visited the University of Liverpool in 2000 as a RS Royal Fellowship where he worked with Prof. John Shaw on paleointensity study and Munich University in 2003–2004 as an AvH Fellowship where he worked with Prof. Nikolai Petersen on biogeomagnetism. He is the founder director of the Biogeomagnetism Laboratory at IGGCAS. His current main research interests include rock magnetism, paleointensity, biogeomagnetism, biomineralization and planetary magnetism.
We thank Tang Xu and Gu Lixin at IGGCAS for TEM analysis. We appreciate John Tarduno, Adrian Muxworthy and two anonymous reviews for their very constructive comments that significantly improve this manuscript.
The authors declare that they have no competing interests.
Availability of data and materials
Data are present in supporting files. Other data are also available by requesting to YXP and TWZ.
This work was supported by the Frontier Science Key Project of CAS and NSFC grants (41621004).
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