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. 2019 Oct 1;14(10):e0222401.
doi: 10.1371/journal.pone.0222401. eCollection 2019.

The Rotating Magnetocaloric Effect as a Potential Mechanism for Natural Magnetic Senses

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Free PMC article

The Rotating Magnetocaloric Effect as a Potential Mechanism for Natural Magnetic Senses

A Martin Bell et al. PLoS One. .
Free PMC article

Abstract

Many animals are able to sense the earth's magnetic field, including varieties of arthropods and members of all major vertebrate groups. While the existence of this magnetic sense is widely accepted, the mechanism of action remains unknown. Building from recent work on synthetic magnetoreceptors, we propose a new model for natural magnetosensation based on the rotating magnetocaloric effect (RME), which predicts that heat generated by magnetic nanoparticles may allow animals to detect features of the earth's magnetic field. Using this model, we identify the conditions for the RME to produce physiological signals in response to the earth's magnetic field and suggest experiments to distinguish between candidate mechanisms of magnetoreception.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Concept for how the rotating magnetocaloric effect could provide a mechanism for natural magnetosensation.
(A) Schematic of a RME-receptor: a magnetically anisotropic particle is bound to a temperature sensitive ion channel. This particle will release or absorb heat energy under rotation in a magnetic field, and this energy could influence the gating of the associated channel. (B) The magnetization of a magnetic nanoparticle is a function of the angle between the easy axis of the particle and the direction of the applied field as shown in the radar plot. Thus rotation will cause the particle magnetization to change, despite no change in the strength of the applied field. For most materials, the easy and hard axis magnetizations are approximately linear for geomagnetic field amplitudes (25-65 μT). As a result, we can calculate the maximum change in magnetization ΔM as this difference between the magnetization when the field is along the easy axis (solid line) and hard axis (dotted line). These values are calculated based on 10 nm radius magnetite particles. The gray shaded region shows ΔM ∼ 0.4 × 10−20 Am2 for rotation in an Earth-strength magnetic field.
Fig 2
Fig 2. Arrangements of RME-receptors that could produce cells that respond to specific field directions.
(A) Two potential arrangements of RME-receptors that would produce a change in average particle magnetization under cell rotation: a high cell aspect ratio with uniformly (or randomly) distributed RME-receptor channels, or a cell of any shape in which the RME-receptor channels cluster together. Either configuration will result in larger numbers of channels oriented along specific axes (along angles ψ=π2 in this example), and fewer along others (angles ψ = 0, π in this example). As a result, the average particle magnetization changes when the cell rotates, which generates or absorbs heat (assuming the easy axis is consistently aligned with the channel pore). Plot shows average magnetization of particles in RME-receptors for prolate spheroidal cells rotating in an Earth-strength magnetic field (with aspect ratios of 1, 2, and 10). Cells with larger aspect ratios will produce greater changes in average particle magnetization under rotation. (B) The maximal change in average channel magnetization is shown as a function of cell aspect ratio for randomly distributed channels with orientation-locked particles. The change in average particle magnetization (which corresponds to the average heat generated or absorbed per particle) increases asymptotically with cell aspect ratio. Cells with aspect ratios greater than ∼ 20 are expected to show near-maximal average magnetocaloric heat generation. Many sensory cells show aspect ratios near or above this number, and thus could be candidate RME-receptive cells. Calculations of magnetization are based on 10 nm radius magnetite particles.
Fig 3
Fig 3. Experimentally observed biogenic magnetic particles include good candidates for magnetocaloric heat changes.
(A) Rows show materials found to be present in biogenic nanoparticles. Grey bars indicate sizes found in literature [10, 12, 15, 39–41], with lighter gray representing uncertainty about limits (for example, goethite particles are found in Columba livia pigeons, but the particle size is unconfirmed). Black dashed lines represent the boundary (critical diameter) between the superparamagnetic and non-superparamagnetic domains for spherical particles at 300K according to Néel relaxation theory. Grey circles indicate that nanoparticles of the materials indicated on the left have been identified in one or more members of the order indicated. Animal orders shown are: Hymenoptera, Lepidoptera, Salmoniformes, Columbiformes and Passeriformes, Rodentia, Caudata, Decapoda, Testudines, Panpulmonata, and Patellogastropoda. (B) The Néel relaxation rate of a particle can be predicted via Néel relaxation theory using the magnetic moment and anisotropy constant of the particle. Contour lines show consistent Néel relaxation times as a function of magnetic moment and anisotropy energies. Contours range from 100 microseconds to 100 seconds. Assuming the Néel relaxation must be faster than the time of animal reorientation constrains the parameter space of allowed superparamagnetic nanoparticles. For particles with magnetic moments < 0.1fAm2 a 1,000,000x increase in the choice of relaxation time threshold results in an increase in maximum particle anisotropy of <10x. (C) Maximum heat generated under rotation as a function of magnetic moment and particle anisotropy energy, for particles with relaxation values below 100 milliseconds. The white line shows the threshold for particles that are expected to produce at least as much heat under rotation (≥ 6 J/mol) as is expected from the synthetic magnetosensor Magneto 2.0 under application of a 275 mT field. Black icons represent particles of materials whose presence has been established in animals with magnetic senses. Of these, hematite (black star) has been found in sizes capable of generating greater than 6 J/mol. Black circles show other magnetic materials found in animals with magnetosensory abilities, but whose material properties and size distributions are less suited for use in RME-receptors. Materials: i) 8 nm radius magnetite, ii) 12 nm magnetite, iii) 20 nm maghemite, iv) 120 nm hematite, v) 8 nm ferrihydrite, vi) 1.25 nm wüstite, vii) 10 nm greigite, viii) 60 nm goethite. Heat generation values assume 25 μT field, near the lower limit for the range of observed GMF field strengths and use published values of material saturation magnetization strengths and anisotropy constants, and a rotation from aligned with the hard axis to aligned with the easy axis [47–59]. *[39, 60–62] ¤[39].

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Grant support

JTR received the NeuroNex Innovation Award 1707562 from the National Science Foundation. JTR received the Welch Foundation Award C-1963-20180324. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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