Physiological origin of biogenic magnetic nanoparticles in health and disease: from bacteria to humans

Figures & data

Table 1 Properties of BMNPs in different organisms

Organism	Mineral/amorphous material	Size (nm)	Shape-controlled (+), other (−)	Domain structure	Localization			References
					Intracellular (+), extracellular (−)	In chain (+), other (−)	Membrane-bound (+), other (−)
Magnetotactic bacteria	Magnetite and/or greigite	10–40, 35–120*	+	SD	+	+	+	^Citation4, ^Citation5, ^Citation9, ^Citation26, ^Citation27, ^Citation69^–^Citation71
Bacteria with MSIs	Magnetite, greigite, lepidocrocite, or amorphous materials	−	−	SD, SPM	+, −	+, −	+, −	^Citation39
Archaea	Magnetite	~100*	−	SPM	+	−	−	^Citation39
Algae protists	Magnetite			SD				^Citation41
Worms	Magnetite	~20		SPM				^Citation35
Mollusks	Magnetite			SD				^Citation9, ^Citation72
Armored snails	Greigite			SD				^Citation42
Honeybees, butterflies, ants	Magnetite	500*–1,000*	−	SD	+	−		^Citation33, ^Citation44, ^Citation45
Termites	Magnetite	~10	−	SD, SPM		−		^Citation34
Lobster	Magnetite?			SD				^Citation46
Newts	Magnetite			SD				^Citation47
Fish	Magnetite	25–60	−	SD		+		^Citation36, ^Citation48^–^Citation53, ^Citation73
Sea turtles	Magnetite?			?				^Citation54
Birds	Magnetite, maghemite	~1,000*	+, −	SPM, SD	+	+, −	+	^Citation38, ^Citation55, ^Citation74, ^Citation75
Bats	Magnetite?			SD				^Citation59
Dolphins, whales	Magnetite			SPM, SD, MD				^Citation60
Humans	Magnetite, maghemite hematite	<1,000	−	SPM, SD, MD	+	+	+	^Citation61^–^Citation63, ^Citation76

Note:

* Size of BMNP clump, not single NP.

Abbreviations: BMNPs, biogenic magnetic nanoparticles; MSIs, magnet-sensitive inclusions; SD, single-domain; SPM, superparamagnetic; MD, multidomain.

Table 2 Magnetic iron minerals found in BMNPs

Oxide	Chemical structure	Magnetic character	TC (K)	Saturation magnetization (A^2·m kg^−1)	References
Magnetite	Fe3O4	Ferrimagnetic	850	92–100	^Citation77
Maghemite	γ-Fe2O3	Ferrimagnetic	820	60–80, 56–74	^Citation81
Hematite	α-Fe2O3	Ferrimagnetic	956	0.3–0.4	^Citation82
Ferrihydrite	Fe5HO8·4H2O	Antiferromagnetic	~350a–c	0.1–1	^Citation83, ^Citation84
Wüstite	FeO	Antiferromagnetic	~203a	–	^Citation84
Greigite	Fe3S4	Ferrimagnetic	<625	59	^Citation85
Goethite	α-FeOOH	Antiferromagnetic	400a	0.01–1	^Citation9, ^Citation84

Notes:

a T_N, Néel temperature, which describes transition from paramagnetic to antiferromagnetic phase;

b two-line, X-ray diffractometry of ferrihydrite crystals usually shows two or six lines;⁸⁴

c at 300 K.

Abbreviations: BMNPs, biogenic magnetic nanoparticles; T_C, Curie temperature.

Figure 1 (A) TEM of magnetotactic bacterium (Magnetospirillum strain AMB1); (B) BMNP chain in a magnetotactic bacterium; (C) zoomed BMNP chain, showing several hexagonal grains (TEM courtesy of B Leszczyński); (D) schematic representation of BMNPs in a magnetosome vesicle. BMNPs of typical shapes observed in magnetotactic bacteria, each surrounded by lipid bilayers.

Abbreviations: TEM, transmission electron microscopy; BMNP, biogenic magnetic nanoparticle.

Figure 2 Taxa in which BMNPs have been observed experimentally.

Notes: Red boxes, BMNPs found in representatives of the given taxa; black rectangle, reported presence of biogenic magnetite in an unclear form (either phytoferritin or botanic BMNPs).

Abbreviation: BMNPs, biogenic magnetic nanoparticles.

Figure 3 Ehrlich carcinoma cell.

Notes: AFM (left), MFM (right). Data from Chekchun et al.²¹ MFM shows BMNPs in the form of dark spots arranged in chains (arrow).

Abbreviations: AFM, atomic force microscopy; MFM, magnetic force microscopy; BMNPs, biogenic magnetic nanoparticles.

Figure 4 Fragment of an atherosclerotic plaque of mixed composition.

Notes: AFM (left), MFM (right). MFM shows BMNPs in the form of dark spots arranged in chains (arrow). There were no bacteria-like magnetosome BMNPs, but alignment of the BMNPs is visible along the plaque surface. Samples of atherosclerotic vessels were extracted from iliac artery during shunting surgery.

Abbreviations: AFM, atomic force microscopy; MFM, magnetic force microscopy; BMNPs, biogenic magnetic nanoparticles.

Table 3 Functional classes of proteins encoded by genes in the magnetosome island^{26,30,107,109–113}

Functions of proteins in biomineralization of BMNPs	Proteins of the magnetosome island	References
Proteins indispensable for biomineralization of BMNPs	MamB, MamM, MamA, MamE, MamO, MamN	^Citation11, ^Citation107, ^Citation109^–^Citation113
Regulatory proteins responsible for		^Citation11, ^Citation107, ^Citation109^–^Citation113
• vesicle formation	MamQ, MamL	^Citation11, ^Citation107, ^Citation109^–^Citation113
• magnetosome-chain formation	MamJ, MamK	^Citation11, ^Citation107, ^Citation109^–^Citation113
• quantity, shape and size of Fe3O4 particles	MamF, MamD, MamT, MamP, MamR, MamS, Mms6	^Citation30, ^Citation11
Proteins with unknown functions or of no effect on BMNP biomineralization	MamH, MamX, MamY, MamZ, MamC, MamG	^Citation11, ^Citation113

Abbreviation: BMNPs, biogenic magnetic nanoparticles.

Figure 5 Schematic representation of BMNP biomineralization in magnetotactic bacteria.

Note: Black hexagonal symbols represent magnetic crystal growth inside magnetosome vesicles.

Abbreviation: BMNP, biogenic magnetic nanoparticle.

Table 4 Statistically significant alignment of MTB proteins with human proteins based on BLAST standard parameters²³

MTB protein	MamA	MamB	MamM	MamN	MamE	MamO
Human homologue	PEX5 proteins	ZnT9 ZnT10	ZnT9 ZnT4	Permease P	HtrA1 HtrA2 HtrA3 HtrA4	HtrA1 HtrA2

Abbreviations: MTB, magnetotactic bacteria; BLAST, Basic Local Alignment Search Tool.

Table 5 Comparative table of functions of MTB proteins and their human homologues^23,116

MTB protein	MTB-protein functions	Name and functions of human homologue
MamB	Cation (Co^2+, Zn^2+, Cd^2+, Fe^2+) transporter	ZnT9, ZnT10: Zn-cation transporters; changes in these proteins in brain regions are associated with Alzheimer’s disease (AD); disturbance of zinc homeostasis plays a role in the pathogenesis of AD
MamE	Serine protease; the PDZ domain of this trypsin-like serine protease is involved in response to heat shock, chaperone function and apoptosis, and may be responsible for substrate recognition and/or binding	HtrA serine proteases, involved in important physiological processes including regulation of mitochondrial homeostasis, apoptosis and transmission of cell signals involved in the development of pathological processes such as cancer and neurodegenerative diseases, including AD
MamA	TPR domain-containing protein; based around a defined consensus sequence and identified in a variety of organisms, including bacteria, cyanobacteria, yeast, and fungi, TPR domains are involved in a variety of functions, which include protein-protein interactions, chaperone functions, the cell cycle, transcription, and protein transport	Pex5: peroxisome receptor, a TPR domain-containing protein; peroxisome is a widespread cell organelle surrounded by a membrane with a large variety of metabolic functions, such as destruction of toxic compounds and construction of the myelin sheath of nerve fibers
MamN	Permease P: the exact function of this protein is unknown, but it is believed to be involved in pH adjustment, together with the ATP-driven proton pump	Human permease P: the exact function of this protein is unknown, but it is believed to be involved in pH adjustment, together with the ATP-driven proton pump
MamO	Serine protease	HtrA2 serine protease
MamM	Cation (Co^2+, Zn^2+, Cd^2+) transporter	ZnT4, ZnT9: Zn-cation transporters

Abbreviations: MTB, magnetotactic bacteria; TPR, tetratricopeptide repeat.

Figure 6 Predicted biomineralization of intracellular BMNPs in eukaryotes, nonmagnetotactic prokaryotes, and archaea.

Note: Black shapes represent the magnetic crystals inside some organic material.

Abbreviation: BMNPs, biogenic magnetic nanoparticles.

Figure 7 Saccharomyces cerevisiae yeast cells with magnetic nanoparticles.

Note: AFM (left) and MFM image (right), showing chains (arrow) of artificial magnetic nanoparticles formed at the biomembranes of the cells, due to magnetic dipole–dipole interaction among the magnetic nanoparticles.

Abbreviations: AFM, atomic force microscopy; MFM, magnetic force microscopy.

Table 6 Properties of proteins of the ferritin family

Protein	Symmetry	Number of subunits	Outer/inner diameter (nm)	Iron content, atoms	References
Human ferritin	432	24	7–8/12	Up to 4,500	^Citation126, ^Citation129
Animal ferritin	432	24	8/12	Up to 4,500	^Citation128, ^Citation130
Bacterial ferritin	432	24	8/12.5	~1,600	^Citation128
Bacterioferritin (contains heme)	432	24	8/12.5	Up to 2,700	^Citation128
Phytoferritin (plant ferritin)	432	24		~2,000	^Citation131
Dps	23	12	5/9	500	^Citation132
Frataxin	?	48	?	~2,400	^Citation133

Figure 8 Schematic representation of ferritin molecule with twofold-, threefold-, and fourfold-symmetry axes.

Notes: Dps, PDB – 4DYU (top left); structure of human ferritin L-chain, PDB – 2FG8 (top center); structure of human ferritin L-chain, PDB – 2FFX (top right) (NCBI). The protein-shell diameter is 12 nm, and the core diameter 7–8 nm (right).

Abbreviations: PDB, Protein Data Bank; NCBI, National Center for Biotechnology Information.

Figure 9 (A) Ferritin TEM (HSF), the white stripes inside the black box indicate the scale bar 100 nm; (B) particle-size distribution based on TEM.

Abbreviations: TEM, transmission electron microscopy; HSF, horse-spleen ferritin; SD, standard deviation.

Table 7 Methods for study of magnetic properties of biogenic and synthetic ferritin and BMNPs

Method	Properties studied	Resolution	References
Mössbauer spectroscopy	Fe valence	≈0.2 nm	^Citation142^–^Citation145
SQUID magnetometry	Magnetization	~10 nm	^Citation19, ^Citation146
Transmission electron microscopy	Electron density, phase, and periodicity	≈50 pm	^Citation61, ^Citation62, ^Citation147, ^Citation148
Nuclear magnetic resonance	Molecule structure, dynamics, reaction state, and chemical environment	50–100 nm	^Citation149
Magnetic force microscopy	Magnetic interactions	10–30 nm	^Citation21, ^Citation92, ^Citation150, ^Citation151
X-ray absorption near-edge structure	Valence, interatomic distances, and bond angles	0.1–0.5 nm	^Citation152, ^Citation153
Small-angle X-ray scattering	Shape, size, characteristic distances of partially ordered materials, pore size	5–25 nm	^Citation154, ^Citation155
Magneto-optical spectroscopy	Type of mineral	2–30 nm	^Citation139, ^Citation156^–^Citation160
Electron energy-loss spectroscopy	Interatomic distances and coordination	~0.1 nm	^Citation154
Electron paramagnetic resonance	Valence		^Citation161, ^Citation162

Abbreviations: BMNPs, biogenic magnetic nanoparticles; SQUID, superconducting quantum-interference device.

Figure 10 Schematic representation of synthetic pathway.

Note: Using apoferritin in vitro as a bioreactor for producing monodisperse metal (eg, Ag or Au), semiconductor (eg, CdS), or metal oxide (eg, Fe₃O₄) particles for applications in electronics or biomedicine.

Abbreviation: Fh, ferrihydrite.

Figure 11 Schematic representation of discrimination.

Notes: Based on differences in magnetic linear birefringence and MORD spectra between ferrite (magnetically strong) materials, such as magnetite/maghemite, and antiferromagnetic (magnetically weak) materials, such as ferrihydrite or akaganeite. For details of magnetically strong MORD data, see Figure 13 and Koralewski et al.¹⁵⁹ Magnetically weak MORD data were obtained for akaganeite-type materials, the same as were studied in Koralewski et al.¹⁶⁰

Abbreviations: MORD, magnetic optical rotatory dispersion; C^CM, Cotton-Mouton constant; V, Verdet constant; D, particle diameter.

Figure 12 Reduced linear magnetic birefringence.

Notes: HSF, synthetic magnetoferritin (loading factor 1,250), magnetite, and a mixture of HSF and magnetite (Fe weight proportion 23:1) versus the square of the applied magnetic field – H². Dashed line indicates the low-field region in which the Cotton–Mouton (C^CM) constant was determined (ie, Δn=C^CMλH^2, where λ is light wavelength and H magnetic field intensity); solid line represents the best fit for the Langevin function. Reprinted from J Magn Magn Mater. Vol 323. Koralewski M, Pochylski M, Mitroova Z, Timko M, Kopcansky P, Melnıkova L. Magnetic birefringence of natural and synthetic ferritin. Pages 2413–2417. Copyright 2011, with permission from Elsevier.¹³⁹

Abbreviation: HSF, horse-spleen ferritin.

Figure 13 Wavelength dependence.

Notes: Faraday rotation (MORD) for HSF, synthetic magnetoferritin with different loading factors (loading factor 1,250 and 3,280), Fe₂O₃, and magnetite suspensions. Reprinted from Koralewski M, Kłos JW, Baranowski M, et al. The Faraday effect of natural and artificial ferritins. Nanotechnology. 2012;23:355704.¹⁵⁹ Copyright 2012. IOP Publishing Ltd.

Abbreviations: MORD, magnetic optical rotatory dispersion; HSF, horse-spleen ferritin; LF, loading factor.

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