Magnetochrome-catalyzed oxidation of ferrous iron by MamP enables magnetite crystal growth in the magnetotactic bacterium AMB-1

Proc Natl Acad Sci U S A. 2024 Dec 10;121(50):e2410245121. doi: 10.1073/pnas.2410245121. Epub 2024 Dec 2.

Abstract

Magnetotactic bacteria have evolved the remarkable capacity to biomineralize chains of magnetite [Fe(II)Fe(III)2O4] nanoparticles that align along the geomagnetic field and optimize their navigation in the environment. Mechanisms enabling magnetite formation require the complex action of numerous proteins for iron acquisition, sequestration in dedicated magnetosome organelles, and precipitation into magnetite. The MamP protein contains c-type cytochromes called magnetochrome domains that are found exclusively in magnetotactic bacteria. Ablation of magnetochromes in MamP prevents bacteria from aligning with external magnetic fields, showing their importance to maintain this biological function. MamP has been proposed, mostly from in vitro experimentations, to regulate iron redox state and maintain an Fe(II)/Fe(III) balance compatible with magnetite formation via the iron oxidase activity of magnetochromes. To test the proposed function for MamP in vivo in the magnetotactic strain Magnetospirillum magneticum (AMB)-1, we characterized the iron species in chemical MamP-mediated magnetite syntheses as well as in bacteria unable to produce MamP using a combination of physicochemical methodologies. We show that MamP has no apparent control on the speciation and oxidation state of intracellular iron or on the Fe(II)/Fe(III) balance in magnetite. We propose that MamP promotes magnetite growth by incorporating Fe(III) into preexisting magnetite seeds and that magnetite structure and stoichiometry is maintained by further equilibration with dissolved Fe(II) in magnetosome organelles.

Keywords: cytochromes; magnetite biomineralization; magnetotactic bacteria; magnetotaxis.

MeSH terms

  • Bacterial Proteins* / metabolism
  • Crystallization
  • Cytochromes / metabolism
  • Ferrosoferric Oxide* / chemistry
  • Ferrosoferric Oxide* / metabolism
  • Ferrous Compounds / metabolism
  • Iron* / metabolism
  • Magnetosomes / metabolism
  • Magnetospirillum* / metabolism
  • Oxidation-Reduction*

Substances

  • Ferrosoferric Oxide
  • Bacterial Proteins
  • Iron
  • Cytochromes
  • Ferrous Compounds

Supplementary concepts

  • Magnetospirillum magneticum