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

Abstract

Magnetosomes are magnetite nanoparticles formed by biomineralization within magnetotactic bacteria. Although there have been numerous genetic and proteomic studies of the magnetosomeformation 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.biomineralization ͉ magnetotactic bacteria ͉ biogenic magnetite ͉ ␣-hematite precursor

Ecology, Diversity, and Evolution of Magnetotactic Bacteria

“…However, when cells of Ms. gryphiswaldense were shifted from iron-limited to iron-sufficient conditions, they showed no delay in magnetite production (100), suggesting that no mineral precursors to magnetite are formed during biomineralization or that they are unstable and convert to magnetite extremely quickly. A time period of 15 min is sufficient for full-sized, mature magnetosomes after the addition of iron to iron-limited cells (185). In one study, immature magnetite magnetosome crystals were shown to contain a surface layer of nonmagnetic iron oxide-phase hematite (185).…”

Measuring spectroscopy and magnetism of extracted and intracellular magnetosomes using soft X-ray ptychography

“…4A). The α-Fe 2 O 3 may be considered as an intermediate phase before Fe 3 O 4 formation, as reported by Staniland et al (11). Based on these observations, we propose that the pathway of magnetosome biomineralization for M. blakemorei strain MV-1 is as follows: i) Iron is taken up from the environment as Fe(II) or Fe(III).…”

“…In our previous study, we showed that these immature magnetosomes are nonmagnetic because they have zero XMCD signals (23). In a real-time XMCD study of Magnetospirillum gryphiswaldense strain MSR-1, Staniland et al (11) reported the presence of a surface layer of a nonmagnetic phase, hematite (α-Fe 2 O 3 ), in immature magnetosomes that is rapidly converted to magnetite in a very short time. the magnetosome magnetization.…”

“…Ferromagnetic particles have also been found in other organisms, such as algae (6), fish (7), insects (8), birds (9), and even humans (10). As one of the simplest biomineralizing microorganisms, MTB serve as a useful model for understanding the evolution and mechanism of biomineralization (4,5,11,12). In addition, they provide an easily accessible system to study the significance of biomagnetism for detection and use of the local Earth's magnetic field in other living organisms.…”

Amino Acids in Iron Oxide Mineralization: (Incomplete) Crystal Phase Selection Is Achieved Even with Single Amino Acids

“…[4][5][6][7][8] Despite the successful implementation in several branches of technology, the details of iron oxide mineralization both in vivo and in vitro are a subject of ongoing research. [9][10][11][12][13][14][15][16][17][18][19][20][21][22] For example, Mann et al have studied the formation of iron oxides and oxyhydroxides using phospholipid vesicles as a model system. 9 Banfield and coworkers have studied the mineralization of iron oxides on a polymer-based scaffold and have suggested reasons why some microbes release polysaccharide-templated iron oxohydroxides.…”