Mechanisms of Magnetoreception of Hypomagnetic Fields: Comparison
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The Earth’s magnetic field is one of the basic abiotic factors in all environments, and organisms had to adapt to it during evolution. On some occasions, organisms can be confronted with a significant reduction in a magnetic field, termed a “hypomagnetic field—HMF”, for example, in buildings with steel reinforcement or during interplanetary flight. HMFs can modify cell signalling by affecting the contents of ions (e.g., calcium) or the reactive oxygen species (ROS) level, which participate in cell signal transduction. Additionally, HMFs have different effects on the growth or functions of organ systems in different organisms, but negative effects on embryonal development have been shown. Embryonal development is strictly regulated to avoid developmental abnormalities, which have often been observed when exposed to a HMF. Only a few studies have addressed the effects of HMFs on the survival of microorganisms. Studying the magnetoreception of microorganisms could be useful to understand the physical aspects of the magnetoreception of the HMF.

  • hypomagnetic field
  • magnetic zero
  • magnetoreception

1. Introduction

Every living organism on Earth has adapted to the geomagnetic field during an evolutionary process lasting billions of years. The presence of a geomagnetic field (approximately 50 uT) is natural to each cell [1]. However, in a few circumstances, organisms can face the absence of magnetic fields. Understanding its effect can enhance the knowledge of magnetoreception mechanisms, with applications in space research, biotechnology or medicine. The terms “hypomagnetic”, “conditionally zero magnetic field” or “magnetic vacuum” generally refer to fields with a magnetic flux density (B) below 100 nT [2], but according to some authors, it can be spoke of a magnetic field weaker than 5 µT as being hypomagnetic [3].
Hypomagnetic fields (HMFs) commonly occur in the interplanetary space of the solar system and fluctuate in the range of several nanoteslas (nT). For example, the lunar magnetic field is less than 300 nT, and the magnetic field on Mars is approximately 1 µT [3]. The planetary magnetic field of Mars is extremely small, and the planetary magnetic field of Venus is practically non-existing [4] (Figure 1).
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Figure 1. Presence of hypomagnetic field in the solar system [3].
New technologies are currently being developed to enable space exploration and interplanetary flights. In the future, organisms will be exposed to a HMF during space travels, which is significantly weaker than the geomagnetic field (GMF) and expected to have diverse biological effects. During these travels, organisms will be exposed to tedious periods of a HMF that is approximately 10,000 times weaker than the Earth’s magnetic field, ranging from 0.1 to 1 nT [5]. However, attenuation of the Earth’s magnetic field is not limited to staying in space but occurs in daily life, for example, in buildings with steel walls or steel reinforcement [2]. Building walls are a natural shield against low- and high-frequency electromagnetic fields. However, a magnetic field (such as a geomagnetic field) is more difficult to shield. In contrast to radiofrequency and low-frequency electric fields, thin sheets of metal have no effect on magnetic fields [6]. However, there is evidence that buildings with steel in their construction magnetise and deform the natural geomagnetic field [5], causing an even 50-fold magnetic field attenuation according to the building size and the complexity of the steel [7].
Hypomagnetic fields can have various effects on organisms, although the underlying mechanisms remain unknown. Erdman et al. [8] suggest that the magnetoreception of the HMF differs among different organisms. The authors assume that the magnetoreception of the HMF is a nonspecific mechanism and manifests in highly different biological systems as mostly random reactions as a result of magnetic interaction with magnetic moments at a physical level. This moment, which is present in each molecule, could transfer the magnetic signal at the level of downstream biochemical events [2].

2. Mechanisms of Magnetoreception of HMFs

Magnetoreception is the universal ability of a biological system to detect magnetic and electromagnetic fields, although it may manifest itself differently in different organisms. Any changes in magnetic field intensity may affect the organisms in many ways, including the basic metabolism of prokaryotic and eukaryotic cells [8]. Magnetoreception relates not only to geomagnetic fields and higher magnetic and electromagnetic fields, but it also explains the perception of HMFs. The hypothesis of nonspecific nonthermal magnetoreception on the physical level has not been studied since none of those has yet been identified experimentally. Typical for hypomagnetic magnetoreception experiments is a high sensitivity to the physical, chemical and physiological conditions, as well as a low reproducibility [2] and a great variety of effects in different organisms. It has not yet been possible to establish any common conditions controlling the magnetic effects in different organisms or populations rather than in their individual forms [9]. Several mechanisms have been described that could explain the mechanism of magnetoreception, such as the cyclotron resonance model, macroscopic charged vortices in the cytoplasm and the parametric resonance model, among others [10]. The most likely physical mechanisms with expected biological responses are: (i) the radical pair mechanism, (ii) the universal physical mechanism and (iii) the molecular gyroscope mechanism. However, according to Binhi and Prato [2], the radical pair mechanism is unlikely to explain all HMF effects on living organisms. The authors assume that the universal physical mechanism and the molecular gyroscope mechanism are more accurate. These primary physical mechanisms can lead to secondary biophysical responses, which can include changes in ROS concentrations, Ca2+ ion homeostasis or influence enzymes that are involved in the electron transport chain in mitochondria or in cell cycle promotion.
1.
Radical pair mechanism
Traditionally, radicals (for example, reactive oxygen species (ROS) are considered harmful because they can cause cell death via oxidative intracellular damage in the metabolism of sugars, fats and nucleic acids. Several studies have also shown the importance of ROS in intracellular signalling cascades such as apoptosis initiation [11][12][13]. Radicals are magnetic because an electron (along with a proton and a neutron) has a property known as spin or, more precisely, a spin momentum [14]. The radical pair consists of two radicals that have been formed simultaneously, usually by a chemical reaction. The spins of two unpaired electrons can be either parallel to each other (↑↑ which gives S = 1) or anti-parallel (↑↓, which gives S = 0, where S is the spin quantum number). The two forms of the electron pair are therefore known as triplet (S = 1) and singlet (S = 0) [15]. Influencing either singlet or triplet formations of electron pairs could be associated with the presence of an external magnetic field and leads to a longer life of the radical pairs (triplet states) [16]. This mechanism can cause a difference in the stability of radical pairs and affects the shift of the chemical reaction equilibrium. Thus, during the formation of radical pairs, external magnetic fields change the recombination rate of these radical pairs, which in turn changes the concentration of radicals such as O2 • and molecules such as H2O2 [17]. In general, the coupling between unpaired electrons and nuclei in each fragment of a radical pair can be achieved by magnetic fields in the range of 10 μT–3 mT [18]. Magnetic fields could interact with the magnetic moments of radical pairs at physical levels, which are ubiquitous in macromolecules with unpaired electrons, protons, paramagnetic ions or other magnetic nuclei in biological cells, and then transmit the magnetic signal to subsequent biochemical events such as cell oxidative stress reactions. This procedure would therefore lead to highly different biological observables and mostly random reactions [19]. This mechanism does not have frequency selectivity because the development of a magnetosensitive spin state occurs over an extremely short life of the radical pair, usually in the order of 10−9–10−7 s [20]. Many authors explain the observed results by this mechanism [21][22][23].
2.
Universal physical mechanism
The rotation of magnetic moments in a magnetic field precedes any biophysical or biochemical mechanism of magnetoreception and largely determines the spectral and nonlinear characteristics of the biological effect of the field. The mechanism is based on the external magnetic field, which influences the magnetic moment of the molecules and leads to the terminal relaxation of the magnetic moment [19]. Magnetic relaxation is known as the approach to equilibrium after a magnetic system was exposed to magnetic field change. Relaxation processes allow nuclear spins to return to equilibrium following a magnetic disturbance [24]. The biological effect is observed only when changes in the magnetic momentum dynamics go through the stages of transformation at the biochemical, physiological and biological levels of the system. A special characteristic of this mechanism is that it predicts the effects of weak magnetic fields but also those of electromagnetic fields induced by alternating electric currents (ACs) in the same biological system [2].
3.
Molecular gyroscope mechanism
The molecular gyroscope mechanism can be explained as the rotation of large fragments of macromolecules or amino acid residues with a distributed electric charge. This movement can be influenced by a magnetic field. In some stages of protein assembly, in the final stage of their synthesis, virtual cavities without water molecules, of the order of 1 nm or less, may occur in the protein [25]. In these cavities, amino acid residues (molecular gyroscopes) rotate over milliseconds, searching for the best position. As a result of such rotation, a magnetic moment interacts with an external magnetic field [2]. The magnetic field affects these rotations, which results in possible changes in protein folding. The folding of protein chains is an evolutionarily conserved process, and improper folding can prevent a protein from performing its specific function [26]. Mostly, random changes in the proteome of the cell can explain various biological responses after HMF exposure.

References

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