Collective magnetotaxis of microbial holobionts is optimized by the three-dimensional organization and magnetic properties of ectosymbionts

Significance Symbiosis between a motile microeukaryotic host and dozens of nonmotile, surface-attached magnetic bacterial symbionts was recently discovered, where the host acquires geomagnetic field-guided navigation thanks to chains of ferrimagnetic nanoparticles (within organelles called magnetosomes) produced by the bacteria. Our findings reveal magnetic dipoles of each magnetosome chain consistently align and efficiently confer a large magnetic moment to the host. Remarkably, the calculated magnetic moment is greatly in excess of that required to gain a magnetotactic advantage. These results not only show an optimization of collective magnetotaxis during the course of evolution owing to the three-dimensional organization and magnetic properties of bacteria but also raise the question on the magnetosome’s function beyond magnetic field guidance since they abundantly cover the host.