Quantum Magnetic Imaging of Iron Biomineralization in Teeth of the Chiton Acanthopleura hirtosa

Abstract

Iron is critical for life. Nature capitalizes on the physical attributes of iron biominerals for functional, structural, and sensory applications. Iron biomineralization is well exemplified by the magnetite‐bearing radula of chitons, the hardest known biomineral of any animal. Although magnetism is an integral property of iron biominerals, limited information exists on the magnetic state, structure, and orientation of these nanoscale materials during mineralization. The advent of quantum‐based magnetic microscopy provides a new avenue to probe these biological systems directly, providing detailed magnetic information of the iron oxide structures. Here two complementary quantum magnetic microscopy methods are applied, based on nitrogen‐vacancy centers in diamond, to spatially map the mineral phases ferrihydrite and magnetite in the developing teeth of the chiton Acanthopleura hirtosa. The images reveal previously undiscovered long‐range magnetic order, established at the onset of magnetite mineralization. This is in contrast to electron microscopy studies that show no strong common crystallographic orientation. The implications of these results are important, not just for the insights gained in biomineralization of the target organism, but also for the study of a broad range of iron minerals in the physical and biological sciences.

Principles and techniques of the quantum diamond microscope

“…Synthetic diamond chips used in QDMs are available in several cuts. The most common are diamonds with the top face along the [100 ] plane and the sides along the [100 ] or [110 ] planes (Fig. 14A).…”

“…The NVs in these diamonds point roughly 35 • out of the plane. Less common diamond cuts include [110 ] and [111 ] top faces. The former has two NV orientations in-plane, while the latter has one NV orientation pointing normal to the face.…”

“…This approach allows reconstruction of vector magnetic field information from the eight NV resonance frequencies. B 0 can also be aligned with the crystallographic [100] or [110] directions, such that the resonance frequencies for different NV orientations are degenerate, leading to improved contrast. If B 0 is aligned along the [100] direction with a diamond cut along [100], the magnetic field projection direction is normal to the chip, though the Zeeman shift is √ 3 times weaker than for B 0 along the [111] direction direction, such that each NV orientation has the same Zeeman interaction.…”

“…Panel F reprinted with permission from Ref [1]. (G) Imaging magnetic field from iron mineralization in chiton teeth [110] (H) Visualization of trafficking of magnetite particles in biological tissue [111] Magnetic field imaging for determining current flow along circuit traces was one of the first demonstrations [112] of imaging the vector component from a nontrivial current distribution. However, the sensitivity of the system was not optimized and nontrivial temporal dynamics of current flow were not investigated.…”

“…15D. Other work has been performed to look at the intrinsic magnetite in chiton teeth to study iron mineralization [110] (see Fig. 15G) and malarial hemozoin nanocrystals [100].…”