DOI: 10.1073/pnas.2615054123 ISSN: 0027-8424

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

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

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.