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      Quantum magnetic imaging of iron biomineralisation in teeth of the chiton Acanthopleura hirtosa

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          Abstract

          Iron biomineralisation is critical for life. Nature capitalises on the physical attributes of iron biominerals for a variety of functional, structural and sensory applications. Although magnetism is an integral property of iron biominerals, the role it plays in their nano-assembly remains a fundamental, unanswered question. This is well exemplified by the magnetite-bearing radula of chitons. Chitons, a class of marine mollusc, create the hardest biomineral of any animal in their abrasion-resistant, self-sharpening teeth4. Despite this system being subjected to a range of high resolution imaging studies, the mechanisms that drive mineral assembly remain unresolved. However, the advent of quantum imaging technology provides a new avenue to probe magnetic structures directly. Here we use quantum magnetic microscopy, based on nitrogen-vacancy centres in diamond, to attain the first subcellular magnetic profiling of a eukaryotic system. Using complementary magnetic imaging protocols, we spatially map the principal mineral phases (ferrihydrite and magnetite) in the developing teeth of Acanthopleura hirtosa with submicron resolution. The images reveal previously undiscovered long-range magnetic order, established at the onset of magnetite mineralisation. This is in contrast to electron microscopy studies that show no strong common crystallographic orientation. The quantum-based magnetic profiling techniques presented in this work have broad application in biology, earth science, chemistry and materials engineering and can be applied across the range of systems for which iron is vital.

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          Magnetic spin imaging under ambient conditions with sub-cellular resolution

          The detection of small numbers of magnetic spins is a significant challenge in the life, physical and chemical sciences, especially when room temperature operation is required. Here we show that a proximal nitrogen-vacancy spin ensemble serves as a high precision sensing and imaging array. Monitoring its longitudinal relaxation enables sensing of freely diffusing, unperturbed magnetic ions and molecules in a microfluidic device without applying external magnetic fields. Multiplexed charge-coupled device acquisition and an optimized detection scheme permits direct spin noise imaging of magnetically labelled cellular structures under ambient conditions. Within 20 s we achieve spatial resolutions below 500 nm and experimental sensitivities down to 1,000 statistically polarized spins, of which only 32 ions contribute to a net magnetization. The results mark a major step towards versatile sub-cellular magnetic imaging and real-time spin sensing under physiological conditions providing a minimally invasive tool to monitor ion channels or haemoglobin trafficking inside live cells.
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            Nanoscale chemical tomography of buried organic-inorganic interfaces in the chiton tooth.

            Biological organisms possess an unparalleled ability to control the structure and properties of mineralized tissues. They are able, for example, to guide the formation of smoothly curving single crystals or tough, lightweight, self-repairing skeletal elements. In many biominerals, an organic matrix interacts with the mineral as it forms, controls its morphology and polymorph, and is occluded during mineralization. The remarkable functional properties of the resulting composites-such as outstanding fracture toughness and wear resistance-can be attributed to buried organic-inorganic interfaces at multiple hierarchical levels. Analysing and controlling such interfaces at the nanometre length scale is critical also in emerging organic electronic and photovoltaic hybrid materials. However, elucidating the structural and chemical complexity of buried organic-inorganic interfaces presents a challenge to state-of-the-art imaging techniques. Here we show that pulsed-laser atom-probe tomography reveals three-dimensional chemical maps of organic fibres with a diameter of 5-10 nm in the surrounding nano-crystalline magnetite (Fe(3)O(4)) mineral in the tooth of a marine mollusc, the chiton Chaetopleura apiculata. Remarkably, most fibres co-localize with either sodium or magnesium. Furthermore, clustering of these cations in the fibre indicates a structural level of hierarchy previously undetected. Our results demonstrate that in the chiton tooth, individual organic fibres have different chemical compositions, and therefore probably different functional roles in controlling fibre formation and matrix-mineral interactions. Atom-probe tomography is able to detect this chemical/structural heterogeneity by virtue of its high three-dimensional spatial resolution and sensitivity across the periodic table. We anticipate that the quantitative analysis and visualization of nanometre-scale interfaces by laser-pulsed atom-probe tomography will contribute greatly to our understanding not only of biominerals (such as bone, dentine and enamel), but also of synthetic organic-inorganic composites.
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              Mineralization and magnetization of chiton teeth: paleomagnetic, sedimentologic, and biologic implications of organic magnetite

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                Author and article information

                Journal
                14 February 2019
                Article
                1902.09637
                3b011b89-47bf-425d-88e5-d4480410b818

                http://arxiv.org/licenses/nonexclusive-distrib/1.0/

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                Custom metadata
                physics.bio-ph

                Biophysics
                Biophysics

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