Anisotropy of Bullet-Shaped Magnetite Nanoparticles in the Magnetotactic Bacteria Desulfovibrio magneticus sp. Strain RS-1

Abstract

Magnetotactic bacteria (MTB) build magnetic nanoparticles in chain configuration to generate a permanent dipole in their cells as a tool to sense the Earth's magnetic field for navigation toward favorable habitats. The majority of known MTB align their nanoparticles along the magnetic easy axes so that the directions of the uniaxial symmetry and of the magnetocrystalline anisotropy coincide. Desulfovibrio magneticus sp. strain RS-1 forms bullet-shaped magnetite nanoparticles aligned along their (100) magnetocrystalline hard axis, a configuration energetically unfavorable for formation of strong dipoles. We used ferromagnetic resonance spectroscopy to quantitatively determine the magnetocrystalline and uniaxial anisotropy fields of the magnetic assemblies as indicators for a cellular dipole with stable direction in strain RS-1. Experimental and simulated ferromagnetic resonance spectral data indicate that the negative effect of the configuration is balanced by the bullet-shaped morphology of the nanoparticles, which generates a pronounced uniaxial anisotropy field in each magnetosome. The quantitative comparison with anisotropy fields of Magnetospirillum gryphiswaldense, a model MTB with equidimensional magnetite particles aligned along their (111) magnetic easy axes in well-organized chain assemblies, shows that the effectiveness of the dipole is similar to that in RS-1. From a physical perspective, this could be a reason for the persistency of bullet-shaped magnetosomes during the evolutionary development of magnetotaxis in MTB.

Competitive and cooperative anisotropy in magnetic nanocrystal chains of magnetotactic bacteria

“…The magnetite nanocrystallites exhibit irregular bullet-shaped morphology characteristic of the strain RS-1. 27,34 As previously reported, 31 the average length of the nanocrystallites in our cultured RS-1 strain is 53.8 6 14.2 nm, which is above the threshold for non-interacting stable singledomain (SSD) magnetite. 37,38 In addition to the SSD nanocrystallites, smaller spherical particles of about 20 nm in size occur at the ends of the chains [ Figure 1(b)].…”

“…Considering the RS-1 strain, the intracellular chains, consisting of less than ten magnetite crystallites generally organized along the [100] hard axis, can in their entirety be modeled by prolate ellipsoids. 30,41 An average length-towidth aspect ratio of 1.8 6 0.4, previously determined for our cultured RS-1 strain, 31 is equivalent to an effective demagnetizing factor of N eff ¼ 0.215 6 0.085. This corresponds to a uniaxial shape anisotropy field of 1.235 6 0.460 kOe, based on Eq.…”

“…1(c)), which, nonetheless, also results in an intra-cellular magnetic dipole aligned with the long axis of the chain, specifically due to the elongation of the crystallites along the [100] axis. 30,31 The separation and quantification of the different anisotropy contributions and their change during a shift from a competitive to a cooperative system and vice versa are of fundamental interest to understand magnetotaxis in living organisms and to build bio-inspired magnetic nanocomposites with tunable anisotropy properties. The ideal candidates to explore this shift are MTB with magnetite crystallites arranged along the [001] hard axes, because pure magnetite undergoes a low-temperature transition, known as Verwey transition with T v % 120 K. In this case, the crystallographic structure changes from cubic to monoclinic and the magnetic easy axis switches from [111] to [001] upon cooling, 32,33 i.e., the anisotropy system transforms from competitive above T v to cooperative below T v .…”

The role of faceting and elongation on the magnetic anisotropy of magnetite Fe3O4 nanocrystals

“…In most of these studies however the effects of particle shape and elongation have been largely ignored due to the computational complexity. Recent experimental measurements of particle size distributions 13 have suggested that shape anisotropy is likely to play an important role in the magnetic anisotropy of magnetite samples, particularly at small sizes, and is also a feature of crystals in magnetotactic bacteria 14 .…”

Investigation of Magnetotaxis of Reconfigurable Micro‐Origami Swimmers with Competitive and Cooperative Anisotropy

“…In nature, magnetotactic bacteria solve this problem by building MNPs in chain configurations to create a permanent dipole moment (PDM) in their cells. This is essentially a tool to sense the Earth's magnetic field, acting as a compass for navigation toward favorable habitats regardless of variation in bacterial morphologies …”