Abstract

Formation of magnetite nanocrystals by magnetotactic bacteria is controlled by specific proteins which regulate the particles’ nucleation and growth. One such protein is Mms6. This small, amphiphilic protein can self‐assemble and bind ferric ions to aid in magnetite formation. To understand the role of Mms6 during in vitro iron oxide precipitation we have performed in situ pH titrations. We find Mms6 has little effect during ferric salt precipitation, but exerts greatest influence during the incorporation of ferrous ions and conversion of this salt to mixed‐valence iron minerals, suggesting Mms6 has a hitherto unrecorded ferrous iron interacting property which promotes the formation of magnetite in ferrous‐rich solutions. We show ferrous binding to the DEEVE motif within the C‐terminal region of Mms6 by NMR spectroscopy, and model these binding events using molecular simulations. We conclude that Mms6 functions as a magnetite nucleating protein under conditions where ferrous ions predominate.

Highlights

  • Essential to many organisms, iron is an important component of many biological processes.[1]

  • Many proteins have evolved to utilise, control and harness the useful capabilities of iron whilst minimizing any potentially damaging side effects.[1a,b] In the case of magnetotactic bacteria (MTB), they have evolved to take advantage of the magnetic characteristics of certain iron oxides by producing biogenic magnetic nanoparticles[3] within internal lipid vesicles termed magnetosomes.[4]. These vesicles are in effect a nanoreactor for the precise synthesis of, most commonly, the iron oxide magnetite (Fe3O4).[3c,5] The formation of nanocrystalline magnetite is tightly controlled by a suite of biomineralisation proteins which are present within the lipid membrane of the magnetosome.[6]

  • There are a number of reactions present in this system[19b] that can lead to several iron oxide and iron oxyhydroxide products or intermediates, namely the mixed ferric/ferrous minerals magnetite (Fe2+Fe3+2O4) [Eq (3)] and green rusts ([Fe2+4Fe3+2(OH)12] [SO4]·x H2O [Eq (2)] as well as the pure ferrous mineral ferrous hydroxide (Fe2+(OH)2) [Eq (1)] and pure ferric minerals schwertmannite ([Fe3+8O8(OH)6] [SO4]·x H2O [Eq (5)] and goethite (Fe3+O(OH)) [Eq (4)] at the extremes of the oxidation states, see Equations (1)–(5), from pure ferrous to pure ferric minerals : Fe2þ þ 2 OHÀ ! FeðOHÞ2

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Summary

Introduction

Iron is an important component of many biological processes.[1] Due to the inherent redox activity and pH sensitivity of this transition metal its presence in cells must be carefully controlled to prevent potentially harmful effects from reactive oxygen species[1c] or iron precipitation.[2] Many proteins have evolved to utilise, control and harness the useful capabilities of iron whilst minimizing any potentially damaging side effects.[1a,b] In the case of magnetotactic bacteria (MTB), they have evolved to take advantage of the magnetic characteristics of certain iron oxides by producing biogenic magnetic nanoparticles[3] within internal lipid vesicles termed magnetosomes.[4] These vesicles are in effect a nanoreactor for the precise synthesis of, most commonly, the iron oxide magnetite (Fe3O4).[3c,5] The formation of nanocrystalline magnetite is tightly controlled by a suite of biomineralisation proteins which are present within the lipid membrane of the magnetosome.[6] The nucleation, crystal growth and regulation of the final size and shape of the particle are strictly regulated by these proteins. Research is currently focusing on identifying and characterising these biomineralisation Mms (magnetosome membrane specific) proteins in order to elucidate a detailed understanding of iron oxide biomineralisation

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