Influence of Crystal Shape and Orientation on the Magnetic Microstructure of Bullet-Shaped Magnetosomes Synthesized by Magnetotactic Bacteria

Nanoscience Chemistry Inorganic Chemistry Materials Chemistry Materials Science Life Sciences Microbiology
Magnetotactic bacteria Magnetosomes Crystal shape Magnetic anisotropy Off-axis electron holography Magnetite Nanocrystals

Magnetotactic Bacteria (MTB) are a group of microorganisms capable of biomineralizing magnetosomes. Magnetosomes are membrane-bound magnetic nanocrystals primarily composed of magnetite (Fe₃O₄) or greigite (Fe₃S₄). These magnetosomes are arranged in chains or specific orientations within bacterial cells, endowing the bacteria with a magnetic dipole moment that enables them to orient and move along the Earth’s magnetic field lines, a phenomenon known as magnetotaxis. Magnetotaxis helps bacteria locate and maintain their optimal position in vertical chemical concentration gradients, typically oxygen gradients.

The magnetic properties of magnetosomes are determined by their size, shape, crystallographic orientation, and spatial arrangement, making them ideal models for studying the magnetism of nanoparticles. However, magnetosomes from different bacterial strains exhibit varying crystal morphologies and orientations, particularly bullet-shaped magnetosomes, whose crystal morphology significantly deviates from the equilibrium shape of magnetite, and whose elongation axis does not necessarily align with the magnetocrystalline easy axis (<111> direction). Therefore, studying the magnetic microstructure of bullet-shaped magnetosomes and their relationship with crystal shape and orientation is crucial for understanding the magnetic behavior of nanoparticles and the evolution of magnetotaxis.

Source of the Paper

This paper was collaboratively authored by András Kovács and other scholars from multiple research institutions, including the Ernst Ruska-Centre for Microscopy and Spectroscopy with Electrons, University of Pannonia, Guangxi University, Aix-Marseille Université, University of Nevada at Las Vegas, and California Polytechnic State University. The paper was published on March 4, 2024, in the journal Geo-Bio Interfaces, titled Influence of Crystal Shape and Orientation on the Magnetic Microstructure of Bullet-Shaped Magnetosomes Synthesized by Magnetotactic Bacteria.

Research Process and Results

1. Research Objectives and Experimental Design

This study aimed to analyze the magnetic properties of bullet-shaped magnetite magnetosomes, particularly the influence of crystal shape and orientation on their magnetic microstructure. The research focused on three MTB strains: Desulfovibrio magneticus RS-1, Candidatus Magnetoovum mohavensis LO-1, and Candidatus Thermomagnetovibrio paiutensis HSMV-1. These strains biomineralize magnetite crystals with elongation axes parallel to <100> (RS-1 and LO-1) or <110> (HSMV-1).

2. Experimental Methods

The study employed various advanced techniques, including Transmission Electron Microscopy (TEM), Off-Axis Electron Holography (EH), Electron Diffraction, and Electron Tomography. Off-axis electron holography was used to measure the magnetic phase shift of magnetosomes, thereby obtaining quantitative data on magnetic induction distributions and magnetic dipole moments.

a) Sample Preparation

  • RS-1 strain: Cultivated in a 6-liter bioreactor using modified DSMZ medium. Magnetosomes were purified through centrifugation and magnetic separation, and finally deposited onto TEM grids.
  • LO-1 and HSMV-1 strains: Magnetosomes were extracted from environmental samples and directly deposited onto TEM grids to preserve their original arrangement within cells.

b) Structural Characterization

  • TEM imaging: High-Angle Annular Dark-Field Scanning Transmission Electron Microscopy (HAADF-STEM) images were recorded using an FEI Titan ChemiSTEM instrument to obtain information on the morphology and crystal structure of magnetosomes.
  • Electron diffraction: Used to confirm the elongation axis of the crystals.
  • Electron tomography: Three-dimensional reconstructions were performed from tilt series images to obtain the three-dimensional shapes and crystal facets of magnetosomes.

c) Magnetic Characterization

  • Off-axis electron holography: Conducted in an FEI Titan 60-300 TEM, where the magnetization direction of the sample was reversed, and holograms were recorded to separate the magnetic phase shift from the mean inner potential contribution. Magnetic induction distributions were generated from magnetic phase shift images.

3. Key Results

a) Crystal Morphology and Structure

  • RS-1 and LO-1 strains: Magnetosome crystals have elongation axes parallel to <100>, with the base of the crystals typically exhibiting well-developed octahedral {111} facets.
  • HSMV-1 strain: Magnetosome crystals have elongation axes parallel to <110>, with an irregular base perpendicular to the long axis.
  • Crystal bending: Some crystals exhibited bending, which was not accounted for in the models.

b) Magnetic Properties

  • Single-domain state: All magnetosome crystals exhibited single-domain states, with magnetic induction lines primarily parallel to the elongation axis and chain direction.
  • Magnetic dipole moment measurements: Both model-independent and model-dependent methods were used to measure the magnetic dipole moments and magnetization of magnetosomes. For example, a magnetosome from the LO-1 strain had a magnetic dipole moment of 4.07 × 10⁶ μB, with an average saturation magnetic induction of 0.52 ± 0.04 T, slightly lower than the expected value for pure magnetite (0.6 T).
  • Magnetic interactions: In disordered chains, magnetostatic interactions between adjacent crystals significantly influenced the direction of magnetic induction lines, causing deviations from the elongation axis.

4. Conclusions and Significance

This study, through quantitative magnetic imaging and measurements, revealed the magnetic properties of bullet-shaped magnetite magnetosomes. The results indicate that the elongated shape of magnetosomes and magnetostatic interactions between crystals are the primary factors determining their magnetic behavior, while magnetocrystalline anisotropy has a relatively minor influence. This finding not only deepens the understanding of nanoparticle magnetism but also provides new insights into the evolution of magnetotaxis.

Additionally, the study raised questions about the genetic control of magnetosome crystal morphology. Although it is known that magnetosome synthesis is controlled by specific gene clusters (e.g., mam and mms genes), the genetic mechanisms underlying the different elongation axes of bullet-shaped magnetosomes remain unclear. Future genomic analyses may provide clues to address this issue.

5. Research Highlights

  • Novel magnetic imaging techniques: Off-axis electron holography provided the highest spatial resolution images of magnetic microstructures to date.
  • Unique properties of bullet-shaped magnetosomes: The study provided the first in-depth analysis of the magnetic behavior of bullet-shaped magnetosomes with <100> and <110> elongation axes, filling a gap in this field.
  • Evolutionary significance: The study hypothesized that bullet-shaped magnetosomes may represent an early form of magnetotaxis, offering important clues for further research into the origin and evolution of magnetotaxis.

Other Valuable Information

The study also explored the potential of bullet-shaped magnetosomes as biomarkers. Since bullet-shaped magnetosomes are considered products of ancient evolutionary lineages, their presence in rocks may indicate the activity of ancient bacteria under specific environmental conditions. However, the dissolution of magnetite in sediments may affect their reliability as biomarkers, necessitating further research into magnetite diagenesis.

This study not only provided new experimental methods and theoretical support for nanoparticle magnetism research but also opened new directions for the study of magnetotaxis evolution and paleoenvironments.