Genetic and biochemical investigations of the role of MamP in redox control of iron biomineralization in Magnetospirillum magneticum

Stephanie R. Jones, Tiffany D. Wilson, Margaret E. Brown, Lilah Rahn-Lee, Yi Yu, Laura L. Fredriksen, Ertan Ozyamak, Arash Komeili, Michelle C.Y. Chang, Harry B. Gray

Research output: Contribution to journalArticlepeer-review

47 Scopus citations

Abstract

Magnetotactic bacteria have evolved complex subcellularmachinery to construct linear chains of magnetite nanocrystals that allow the host cell to sense direction. Each mixed-valent iron nanoparticle is mineralized from soluble iron within a membrane-encapsulated vesicle termed the magnetosome, which serves as a specialized compartment that regulates the iron, redox, and pH environment of the growing mineral. To dissect the biological components that control this process, we have carried out a genetic and biochemical study of proteins proposed to function in iron mineralization. In this study, we show that the redox sites of c-type cytochromes of the Magnetospirillum magneticum AMB-1 magnetosome island, MamP and MamT, are essential to their physiological function and that ablation of one or both heme motifs leads to loss of function, suggesting that their ability to carry out redox chemistry in vivo is important. We also develop a method to heterologously express fully heme-loaded MamP from AMB-1 for in vitro biochemical studies, which show that its Fe(III)-Fe(II) redox couple is set at an unusual potential (-89 ± 11 mV) compared with other related cytochromes involved in iron reduction or oxidation. Despite its low reduction potential, it remains competent to oxidize Fe(II) to Fe(III) and mineralize iron to produce mixed-valent iron oxides. Finally, in vitro mineralization experiments suggest that Mms mineral- templating peptides from AMB-1 can modulate the iron redox chemistry of MamP.

Original languageEnglish (US)
Pages (from-to)3904-3909
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number13
DOIs
StatePublished - Mar 31 2015
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • General

Keywords

  • Biomineralization
  • Cytochrome
  • Iron
  • Magnetosome
  • MamP

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