Modes of Biomineralization of Magnetite by Microbes

Abstract

Biomineralization processes have traditionally been grouped into two distinct modes; biologically induced mineralization (BIM) and biologically controlled mineralization (BCM). In BIM, microbes cause mineral formation by sorbing solutes onto their cell surfaces or extruded organic polymers and/or releasing reactive metabolites which alter the saturation state of the solution proximal to the cell or polymer surface. Such mineral products appear to have no specific recognized functions. On the other hand, in BCM microbes exert a great degree of chemical and genetic control over the nucleation and growth of mineral particles, presumably because the biominerals produced serve some physiological function. Interestingly, there are examples where the same biomineral is produced by both modes in the same sedimentary environment. For example, the magnetic mineral magnetite (Fe ₃ O ₄ ) is generated extracellularly in the bulk pore waters of sediments by various Fe(III)-reducing bacteria under anaerobic conditions, while some other anaerobic and microaerophilic bacteria and possibly protists form magnetite intracellularly within preformed vesicles. Differences in precipitation mechanisms might be caused by enzymatic activity at specific sites on the surface of the cell. Whereas one type of microbe might facilitate the transport of dissolved Fe(III) into the cell, another type will express its reductive enzymes and cause the reduction of Fe(III) external to the cell. Still other microbes might induce magnetite formation indirectly through the oxidation of Fe(II), followed by the reaction of dissolved Fe(II) with hydrolyzed Fe(III). The biomineralization of magnetite has significant effect on environmental iron cycling, the magnetization of sediments and thus the geologic record, and on the use of biomarkers as microbial fossils.

Keywords:

• biomineralization
• iron oxides
• magnetite
• magnetotactic bacteria
• Fe(III)-reducing bacteria

Acknowledgments

We thank K. J. Edwards, B. M. Moskowitz, D. Schüler, and S. Simmons for valuable discussions; S. Glasauer for Figure 4; and two anonymous reviewers for significantly helpful comments. DAB is grateful for support from US National Science Foundation grant EAR-0311950 and National Aeronautics and Space Administration (NASA) Johnson Space Center grant NAG 9-1115. KK was supported by a Natural Sciences and Engineering Research Council award (249565-2002).