Rapid magnetosome formation shown by real-time x-ray magnetic circular dichroism

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 104; no. 49; pp. 19524 - 19528
• Main Authors: Staniland, Sarah, Ward, Bruce, Harrison, Andrew, van der Laan, Gerrit, Telling, Neil
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 04-12-2007; National Acad Sciences
• Subjects: Absorption spectroscopy; Bacteria; Biological Sciences; Biomineralogy; Catalysis; Chemical precipitation; Circular Dichroism - methods; Crystals; Ferrosoferric Oxide - analysis; Ferrosoferric Oxide - metabolism; Genetics; High temperature; Inclusion Bodies - chemistry; Inclusion Bodies - metabolism; Inductive reasoning; Iron oxides; Magnetic fields; Magnetics; Magnetite; Magnetization; Magnetosomes; Magnetospirillum; Magnetospirillum - growth & development; Magnetospirillum - metabolism; Magnetospirillum - ultrastructure; Microscopy, Electron, Transmission; Mineralization; Minerals; Nanoparticles; Nanoparticles - analysis; Proteomics; Spectrum analysis; X-Rays
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.0704879104

Magnetosomes are magnetite nanoparticles formed by biomineralization within magnetotactic bacteria. Although there have been numerous genetic and proteomic studies of the magnetosome-formation process, there have been only limited and inconclusive studies of mineral-phase evolution during the formation process, and no real-time studies of such processes have yet been performed. Thus, suggested formation mechanisms still need substantiating with data. Here we report the examination of the magnetosome material throughout the formation process in a real-time in vivo study of Magnetospirillum gryphiswaldense, strain MSR-1. Transmission EM and x-ray absorption spectroscopy studies reveal that full-sized magnetosomes are seen 15 min after formation is initiated. These immature magnetosomes contain a surface layer of the nonmagnetic iron oxide-phase hematite. Mature magnetite is found after another 15 min, concurrent with a dramatic increase in magnetization. This rapid formation result is contrary to previously reported studies and discounts the previously proposed slow, multistep formation mechanisms. Thus, we conclude that the biomineralization of magnetite occurs rapidly in magnetotactic bacteria on a similar time scale to high-temperature chemical precipitation reactions, and we suggest that this finding is caused by a biological catalysis of the process.