Angle sensing in magnetotaxis of Magnetospirillum magneticum AMB-1

Abstract

The mechanism of how magnetotactic bacteria navigate along the magnetic field has been a puzzle. Two main models disagree on whether the magnetotactic behavior results from passive alignment with the magnetic field or active sensing of the magnetic force. Here, we quantitatively studied the swimming patterns of Magnetospirillum magneticum AMB-1 cells to understand the origin of their magnetotactic behaviors. Single-cell tracking and swimming pattern analysis showed that the cells follow a mixed run–reverse–tumble pattern. The average run time decreased with the angle between the cell's moving velocity and the external magnetic field. For mutant cells without the methyl-accepting chemotaxis protein (MCP) Amb0994, such dependence disappeared and bacteria failed to align with magnetic field lines. This dysfunction was recovered by complementary Amb0994 on a plasmid. At high magnetic field (>5 mT), all strains with intact magnetosome chains (including the Δamb0994–0995 strains) showed alignment with the external magnetic field. These results suggested that the mechanism for magnetotaxis is magnetic field dependent. Due to the magnetic dipole moment of the cell, the external magnetic field exerts a torque on the cell. In high magnetic fields, this torque is large enough to overcome the random re-orientation of the cell, and the cells align passively with the external magnetic field, much like a compass. In smaller (and biologically more relevant) external fields, the external force alone is not strong enough to align the cell mechanically. However, magnetotactic behaviors persist due to an active sensing mechanism in which the cell senses the torque by Amb0994 and actively regulates the flagella bias accordingly to align its orientation with the external magnetic field. Our results reconciled the two putative models for magnetotaxis and revealed a key molecular component in the underlying magneto-sensing pathway.