An MCP-like protein interacts with the MamK cytoskeleton and is involved in magnetotaxis in Magnetospirillum magneticum AMB-1

J Mol Biol. 2010 Jul 16;400(3):309-22. doi: 10.1016/j.jmb.2010.05.011. Epub 2010 May 13.

Abstract

Magnetotactic bacteria have the unique capacity of aligning and swimming along geomagnetic field lines, a behavior called magnetotaxis. Although this behavior has been observed for 40 years, little is known about its mechanism. Magnetotactic bacteria synthesize unique organelles, magnetosomes, which are magnetic crystals enveloped by membrane. They form chains with the help of the filamentous cytoskeletal protein MamK and impart a net magnetic-dipole moment to the bacterium. The current model proposes that magnetotaxis comprises passive magnetic orientation and active swimming due to flagellar rotation. We thought that magnetic sensing, via the widely used chemotaxis mechanism, might be actively involved in magnetotaxis. We found that the methyl-accepting chemotaxis protein Amb0994 of Magnetospirillum magneticum AMB-1 was capable of carrying out such a function. Amb0994 is encoded by a gene in the magnetosome island, in which genes essential for magnetosome biosynthesis and magnetotaxis are concentrated. Amb0994 lacks periplasmic sensing domain, which is generally involved in sensing stimuli from outside of cells. By constructing fusions with a derivative of yellow-fluorescent-protein, we showed that Amb0994 localizes to the cell poles, where methyl-accepting chemotaxis proteins are usually clustered. We then showed that Amb0994 specifically interacts, via its C-terminal domain, with MamK, using a bimolecular fluorescence complementation assay. Moreover, overproduction of Amb0994 slowed down the response of the bacterium to changes in the direction of the magnetic field. Most importantly, the C-terminal domain of Amb0994, which interacts with MamK, is responsible for this phenotype, suggesting that the interaction between Amb0994 and MamK plays a key role in magnetotaxis. These results lead to a novel explanation for magnetotaxis at the molecular level.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / metabolism*
  • Cytoskeletal Proteins / metabolism*
  • Genes, Reporter
  • Locomotion*
  • Magnetics*
  • Magnetospirillum / physiology*
  • Protein Interaction Mapping

Substances

  • Bacterial Proteins
  • Cytoskeletal Proteins