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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 ?amb0994-0995 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.

SUBMITTER: Zhu X

PROVIDER: S-EPMC4134682 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Angle sensing in magnetotaxis of Magnetospirillum magneticum AMB-1.

Zhu Xuejun X Ge Xin X Li Ning N Wu Long-Fei LF Luo Chunxiong C Ouyang Qi Q Tu Yuhai Y Chen Guanjun G

Integrative biology : quantitative biosciences from nano to macro 20140530 7

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 ...[more]

PMID: 24877161

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Project description:Magnetotactic bacteria are a unique group of bacteria that synthesize a magnetic organelle termed the magnetosome, which they use to assist with their magnetic navigation in a specific type of bacterial motility called magneto-aerotaxis. Cytoskeletal filaments consisting of the actin-like protein MamK are associated with the magnetosome chain. Previously, the function of MamK was thought to be in positioning magnetosome organelles; this was proposed based on observations via electron microscopy still images. Here, we conducted live-cell time-lapse fluorescence imaging analyses employing highly inclined and laminated optical sheet microscopy, and these methods enabled us to visualize detailed dynamic movement of magnetosomes in growing cells during the entire cell cycle with high-temporal resolution and a high signal/noise ratio. We found that the MamK cytoskeleton anchors magnetosomes through a mechanism that requires MamK-ATPase activity throughout the cell cycle to prevent simple diffusion of magnetosomes within the cell. We concluded that the static chain-like arrangement of the magnetosomes is required to precisely and consistently segregate the magnetosomes to daughter cells. Thus, the daughter cells inherit a functional magnetic sensor that mediates magneto-reception.IMPORTANCE Half a century ago, bacterial cells were considered a simple "bag of enzymes"; only recently have they been shown to comprise ordered complexes of macromolecular structures, such as bacterial organelles and cytoskeletons, similar to their eukaryotic counterparts. In eukaryotic cells, the positioning of organelles is regulated by cytoskeletal elements. However, the role of cytoskeletal elements in the positioning of bacterial organelles, such as magnetosomes, remains unclear. Magnetosomes are associated with cytoskeletal filaments that consist of the actin-like protein MamK. In this study, we focused on how the MamK cytoskeleton regulates the dynamic movement of magnetosome organelles in living magnetotactic bacterial cells. Here, we used fluorescence imaging to visualize the dynamics of magnetosomes throughout the cell cycle in living magnetotactic bacterial cells to understand how they use the actin-like cytoskeleton to maintain and to make functional their nano-sized magnetic organelles.

Dataset Information

Angle sensing in magnetotaxis of Magnetospirillum magneticum AMB-1.

Publications

Angle sensing in magnetotaxis of Magnetospirillum magneticum AMB-1.

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