Chain organization of dimple-ended magnetite magnetosomes supports field-dependent cell linking in unicellular magnetotactic bacteria

Magnetotactic bacteria (MTB) are generally thought to navigate as individual cells by using intracellular magnetosome chains that provide a stable magnetic moment for orientation along magnetic field lines. Whether nonclassical magnetosome geometries and particle-scale magnetic states can support robust chain-level magnetic function, and potentially mediate interactions between cells, remains unresolved. Here, to we report a unicellular magnetotactic bacterium, strain WYHV-1, that biomineralizes comparatively large prismatic magnetite magnetosomes with distinctive dimples at both crystal ends and organizes them into a single tightly packed intracellular chain. Off-axis electron holography reveals that individual dimple-ended particles commonly exhibit single-vortex behavior rather than a canonical uniformly magnetized single-domain (SD) state. Micromagnetic simulations indicate a size-dependent transition from SD to single-vortex behavior in dimple-ended particles and that tight intrachain coupling suppresses particle-scale nonuniformity, producing a predominantly SD-like magnetization within the chain and a strong chain-parallel remanent moment. Further simulations indicate that chain-generated stray fields concentrated at chain ends can generate intercellular magnetic attraction strong enough to promote head-to-tail linking between neighboring cells over subcellular distances. These results provide a physical explanation for field-dependent multicell-like assemblies observed in hanging-drop experiments and indicate that magnetic performance in WYHV-1 is governed primarily by chain-level organization rather than by the magnetic state of idealized isolated particles. Our findings expand the known structural and magnetic diversity of biogenic magnetite and reveal a cross-scale mechanism by which magnetosome chains support cellular orientation, and under field-aligned experimental conditions, mediate intercellular magnetic organization.

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Journal
Proceedings of the National Academy of Sciences
Published
2026-09-29
DOI
https://doi.org/10.1073/pnas.2615054123
Primary Topic
Geomagnetism and Paleomagnetism Studies
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article
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article

Chain organization of dimple-ended magnetite magnetosomes supports field-dependent cell linking in unicellular magnetotactic bacteria

Nicolas Menguy, Éric Leroy, Yongxin Pan, Qianqian Lan et al.
Proceedings of the National Academy of Sciences
Geomagnetism and Paleomagnetism Studies
article

Chain organization of dimple-ended magnetite magnetosomes supports field-dependent cell linking in unicellular magnetotactic bacteria

Nicolas Menguy, Éric Leroy, Yongxin Pan, Qianqian Lan, Wyn Williams, Yuqin Wang, Rafal E. Dunin–Borkowski, Xiang Zhao, Jinhua Li, Jiawei Liu, Jian Wang, Andrew P. Roberts, Liu Peiyu, Rixiang Zhu
article en

Abstract

Magnetotactic bacteria (MTB) are generally thought to navigate as individual cells by using intracellular magnetosome chains that provide a stable magnetic moment for orientation along magnetic field lines. Whether nonclassical magnetosome geometries and particle-scale magnetic states can support robust chain-level magnetic function, and potentially mediate interactions between cells, remains unresolved. Here, to we report a unicellular magnetotactic bacterium, strain WYHV-1, that biomineralizes comparatively large prismatic magnetite magnetosomes with distinctive dimples at both crystal ends and organizes them into a single tightly packed intracellular chain. Off-axis electron holography reveals that individual dimple-ended particles commonly exhibit single-vortex behavior rather than a canonical uniformly magnetized single-domain (SD) state. Micromagnetic simulations indicate a size-dependent transition from SD to single-vortex behavior in dimple-ended particles and that tight intrachain coupling suppresses particle-scale nonuniformity, producing a predominantly SD-like magnetization within the chain and a strong chain-parallel remanent moment. Further simulations indicate that chain-generated stray fields concentrated at chain ends can generate intercellular magnetic attraction strong enough to promote head-to-tail linking between neighboring cells over subcellular distances. These results provide a physical explanation for field-dependent multicell-like assemblies observed in hanging-drop experiments and indicate that magnetic performance in WYHV-1 is governed primarily by chain-level organization rather than by the magnetic state of idealized isolated particles. Our findings expand the known structural and magnetic diversity of biogenic magnetite and reveal a cross-scale mechanism by which magnetosome chains support cellular orientation, and under field-aligned experimental conditions, mediate intercellular magnetic organization.

Proceedings of the National Academy of SciencesVol. 123(40)
Australian National University (AU), Centre National de la Recherche Scientifique (FR), Chinese Academy of Sciences (CN), Ernst Ruska Centre (DE), University of Saskatchewan (CA), Sorbonne Université (FR), Institute of Geology and Geophysics (AZ), Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (CN), Qingdao National Laboratory for Marine Science and Technology (CN), Institute of Geology and Geophysics (CN), Institut de Chimie et des Matériaux Paris-Est (FR), Institut de minéralogie, de physique des matériaux et de cosmochimie (FR), University of Chinese Academy of Sciences (CN), Canadian Light Source (Canada) (CA), University of Edinburgh (GB)
Openalex Percentile: Top 19%
Geomagnetism and Paleomagnetism Studies
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