Abstract
Static magnetic field (SMF) exists in nature widely and plays an essential role in the biological evolution. Due to the rapid development of superconducting technology, the intensities of SMFs used for medical and academic research purposes have steadily increased in recent years. This chapter presents an overview on the biological effects induced by SMFs with intensities ranging from mT to several Teslas (T). The effects of SMFs on microorganisms are divided into six sections, including cellular growth and viability, morphological and biochemical modifications, genotoxicity, gene and protein expression, magnetosome formation sensing magnetic field, and application of SMFs on antibiotic resistance, fermentation, and wastewater treatment. The effects of SMFs on plants are divided into six sections, including germination, growth, gravitropism, photosynthesis, redox status, and cryptochromes (CRYs) sensing magnetic field. The effects of SMFs on animals are divided into seven sections, including Caenorhabditis elegans, insects, Helix pomatia, aquatic animals, Xenopus laevis, mice and rats, and magnetic sensing protein in animals. This chapter will be very helpful for better understanding the biological responses to SMFs in different species and their underlying mechanisms.
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7.1 Introduction
Static magnetic field (SMF) is a ubiquitous environmental factor for all living organisms during the evolution process. A variety of organisms including bacteria, algae, snails, planaria, honeybee, salmon, lobsters, salamanders, homing pigeons, robins, mice, and possibly humans have been demonstrated the ability to sense magnetic fields (MFs) for orientation in navigation, migration, homing, escaping, and nest building (Qin et al. 2016). Although the biophysical mechanisms of magnetoreception are poorly understood, three main hypothesis for magnetosensing have been proposed: (1) magnetic induction, which can only be applied to marine creatures, owing to the high conductivity of salt water; (2) the magnetite hypothesis that proposes a process mediated by crystals of permanently magnetic material (magnetite) with an evolutionary genetics hypothesis for magnetite formation; (3) the radical pair mechanism (RPM) which relies on a chemical reaction involving specialized photoreceptors (Fedele et al. 2014; Bellinger et al. 2022). However, the recently proposed MagR/Cry-based biocompass model combines the concepts of ferrimagnetism and the involvement of Cry in magnetoreception, which have also attracted a lot of attention (Qin et al. 2016).
Since the Industrial Revolution in the 1850s, human-made sources of SMFs have become inevitable environmental factors for organisms on Earth. In particular, the development of electromagnets in the nineteenth century and superconducting magnets in the mid-twentieth century has greatly increased the risk of the exposure of organisms to higher magnetic fields. Acute and chronic exposure of organisms to SMFs, which are often ten and more times greater than geomagnetic fields, have been investigated for decades. However, the exact mechanisms underlying the influence of SMFs on living systems are still largely unknown, and until now there is no unique theory about magnetic field–organism interaction. In this review, we limit our discussion on the evidence of the biological response of SMFs with the intensities ranging from a few mT to several Teslas (T) on microorganisms, plants, and animals and explore recent results on the investigation of magnetoreception in these organisms.
7.2 SMFs on Microorganisms
7.2.1 SMFs on Cellular Growth and Viability
The influence of magnetic fields with various flux densities on the growth rate and viability of microbes has been investigated in bacteria, yeast, and plant pathogenic fungi. Under low and moderate magnetic fields, the inhibition on the growth of microorganisms has been reported in various bacteria species. Bajpai et al. (2012) showed that a SMF of 100 mT suppressed the growth of both gram-positive (S. epidermidis) and gram-negative bacteria (Escherichia coli, E. coli), which was related to the cellular membrane damage. Fan et al. (2018) discussed the effect of long-term exposure to a moderate SMF on Enterococcus faecalis and showed that the cellular proliferation of Enterococcus faecalis (E. faecalis) was inhibited by a SMF of 170 mT with 120 h exposure. The moderate SMFs in the range from 50 to 500 mT on the growth of Streptococcus pyogenes (S. pyogenes) was investigated by Morrow et al. (2007) and was found that the growth inhibition was observed up to 300 mT, but an increase in growth rate when cells were exposed to 500 mT. Although a SMF of 300 mT had no influence on the growth of E. coli in nutrient rich Luria Bertani (LB) medium, it increased bacterial cell culture density during late growth in diluted LB (Potenza et al. 2004). El May et al. (2009) also reported that a SMF of 200 mT failed to alter cellular growth but induced a decrease of colony-forming units (CFU) between 3 and 6 h followed by an increase from 6 to 9 h. Ben Mouhoub et al. (2018) showed that 57 mT SMF improved the viability of Salmonella Hadar compared with the control group. Under high magnetic fields, Kazuhiro et al. (1997) reported that the cellular growth of Bacillus subtilis MI113 and genetically transformed B. subtilis MI113 (pC112) was significantly increased by exposure to homogeneous 7 T and inhomogeneous 5.2–6.1 T magnetic fields. Moreover, a SMF of 5.2–6.1 T promoted survival rate of E. coli B cells of stationary phase, which the CFU number and the amount of S factor encoded by the rpoS gene were much higher than that under a geomagnetic field (Horiuchi et al. 2001). These observations suggest that SMFs are not always negative to the growth of microorganism, which are closely related to the intensities of SMFs, types of bacteria, and exposure manners.
The combined effects of SMF and other environmental factors on the growth of microorganisms are largely unknown. Ji et al. (2009) showed that a SMF of 450 mT inhibited the growth and even killed E. coli, in which the inhibitory effect was increased with temperature. Masahiro et al. (2000) compared the effect of SMF exposure up to 100 mT on the culture of Streptococcus mutans (S. aureus) and E. coli grown in aerobic and anaerobic conditions. They found that the bacterial growth was inhibited by the SMF in anaerobic conditions, but remained unaffected when the SMF was applied in aerobic conditions, indicating that oxygen played an inhibitory effect for the magnetic field. Letuta and Berdinskiy (2019) found that the concurrent treatment of isotope 67Zn and 25–35 mT SMF increased the colony formation ability and growth rate constant of E. coli by 2–4 times compared with non-magnetic zinc isotopes 64,66Zn.
There are few studies on the growth and sporulation of phytopathogenic microscopic fungi under the static magnetic fields. Nagy and Fischl (2004) showed that the applied magnetic fields with flux intensities ranging from 0.1 to 1 mT decreased the growth of phytopathogenic fungi colonies and the number of Fusarium oxysporum conidia, while the number of the developed conidia of Alternaria alternata and Curvularia inaequalis was increased. Maria Cristina et al. (2003) and Jan et al. (2007) provided further evidence on the growth depression of fungi exposed to SMF. A 1.5–2 times faster growth rate was found in Aspergillus niger exposed to a static B-field varying from 40 to 80 T than in sham controls and the B-field exposure could have an effect on the biodegradability of materials by enhancing the growth rate and the aggressiveness of the fungus. However, Ruiz-Gómez et al. (2004) reported that magnetic fields had no effect on fungal growth.
In yeast, Lucielen Oliveira et al. (2010) showed that a SMF of 25 mT resulted in an increase of glutathione content and biomass in Saccharomyces cerevisiae (S. cerevisiae). Muniz et al. (2007) reported that the biomass (g/L) increment of S. cerevisiae DAUFPE-1012 was 2.5 times greater in cultures exposed to 220 mT SMF as compared with non-exposed cultures. Kthiri et al. (2019) furtherly reported that under the treatment of 250 mT SMF, the growth and viability of Saccharomyces cerevisiae and colony formation decreased significantly after 6 h, but increased from 6 to 9 h. In contrast, Malko et al. (1994) reported that yeast cells subjected to a static MF of 1.5 T over the course of seven cell divisions displayed growth rates similar to unexposed cells, indicating that moderate SMF had minimal effect on the growth of yeast. With the intensity increase of SMFs, Masakazu et al. (2004) found that gradient magnetic fields of 14 T exhibited the decelerated growth in a liquid–gas mixture system.
7.2.2 SMF on Morphological and Biochemical Modifications
The morphological study of SMF treated cells using transmission electron microscope (TEM) revealed that bacterial cell wall was ruptured by SMF exposure (Ji et al. 2009). Quiñones-Peña et al. (2017) reported that the prototype of E. coli: strain-EPEC E2348/69 exposed to 107 mT SMF reduced its aggregation and altered the adhesion pattern, which was related to the expression of its BFP cilia. A SMF of 200 mT significantly altered the phospholipid proportions in Salmonella typhimurium (S. typhimurium) wild type and dam mutant strain, which the most affected were those of the acidic phospholipids, cardiolipins (CL) (Mouadh et al. 2012). Egami et al. (2010) investigated the effect of SMFs on the budding of S. typhimurium and found that the size of budding yeast cells and the budding angle were affected by a SMF of 2.93 T. In homogeneous magnetic field, the budding direction of daughter yeast cells was mainly oriented in the direction of magnetic field B; in contrast, in inhomogeneous magnetic field, the daughter yeast cells tended to bud along the axis of capillary flow in regions where the magnetic gradient was high.
Microorganisms as models for analyzing fundamental metabolic responses to magnetic fields have great advantages, as they represent simple unicellular organisms. Letuta (2020) found that the maximum concentration of ATP was generated under the action of the magnetic isotope 25Mg and an electro SMF of 70–90 mT. The composition of membrane lipids in S. typhimurium was disturbed by 200 mT SMF, which the bacteria tried to change SFA, UFA, and CFA, and hydroxyl FA levels to maintain membrane fluidity, while the UFAs/SFAs ratio of Salmonella reached equilibrium after 9 h of exposure (Ramla et al. 2017). Similarly, Mihoub et al. (2012) showed that a SMF of 200 mT significantly affected the lipid proportions in membrane, leading to an unusual accumulation of the acidic phospholipids cardiolipins, with a significant increase of membrane cyclic fatty acids and a meaningful increase of the total unsaturated fatty acids to total saturated fatty acids ratios of the exposed cells. Tang et al. (2019) exposed Flavobacterium m1–14 to 100 mT SMF for 0, 24, 48, 72, or 120 h, respectively, and found that the length of the cells increased significantly by SMF treatment. Compared with the control group, after 24 h, 48 h, 72 h, and 120 h of 100 mT SMF treatment, the length of the cell increased by 123%, 258%, 70.1%, and 31.2%, respectively; among them, the cells treated by the magnetic field for 48 h were more elongated (Fig. 7.1). The inhibition of mycelia growth by a SMF of 300 mT was accompanied by morphological and biochemical changes, and Ca2+-dependent signal transduction pathways were involved in conidia germination (Maria Cristina et al. 2003). The patterns of metabolites released from S. pyogenes exposed to different magnetic flux intensities ranging from 50 to 500 mT were significantly altered (Morrow et al. 2007). A SMF of 250–300 mT elicited the maximal release of the majority of metabolites. Hu et al. (2009) reported that the composition and conformation of nucleic acid, protein, and fatty acid of E. coli were altered by 10 T SMF, which were reflected by the changes of spectral region of Fourier-transform infrared (FTIR) spectroscopy combined with cluster analysis. She et al. (2009) further found that 3.46–9.92% of the disorder coils in the secondary structures of protein were altered into α-helices by 10 T SMF; in contrast, 10 T SMF had little influence on Staphylococcus aureus (S. aureus).
7.2.3 SMF on Genotoxicity
In living organisms, the production of free radicals has the potential to interact with DNA and plays an important role both in the aging process and environmental stress related adverse effects. Exposure of cells to 300 mT SMF significantly reduced the yield of 8-hydroxyguanine in extracted DNA compared to controls, suggesting some possible antioxidant protection to S. pyogenes at this field strength (Morrow et al. 2007). Carlioz and Touati (1986) showed an induction of the expression of a soxS::lacZ fusion gene following strong SMF exposure. Fan et al. (2018) confirmed that Enterococcus faecalis (E. faecalis) could induce a stress response by upregulating the expression of dnaK gene and the expression of virulence genes efaA and ace under the treatment of SMF. Righi et al. (2020) exposed irradiated Deinococcus radiodurans (D. radiodurans) cells to SMF and found that their cell viability was improved, which might be due to the improvement of the efficiency of DNA fragment recombination by SMF exposure.
The direct evidence on the genotoxicity of SMFs is limited and controversial. Mahdi et al. (1994) exposed various mutant strains of E. coli to a homogeneous SMF of either 500 mT or 3 T. No evidence of increased DNA damage was detected in SMF-sexposed E. coli, even with bacterial strains disabled for DNA repair. Masateru et al. (1999) performed a bacterial mutation assay to determine the mutagenic potential of SMF. No mutagenic effects were detected in four uvrB strains of S. typhimurium (TA98, TA100, TA1535 and TA1537) and E. coli WP2uvrA. Schreiber et al. (2001) also reported that exposures to a SMF of 7.2 T did not show any alteration in the number of His+ revertants in Salmonella mutagenicity test. Yoshie et al. (2012) reported that no statistically significant differences in the mutation frequency in thymine synthesis genes were observed between SMF-exposed cells and unexposed cells at any of the applied magnetic flux intensities. SMFs up to 13 T caused neither mutagenicity nor co-mutagenicity in the superoxide dismutase (SOD)-deficient E. coli strain QC774 or in its parental strain GC4468, suggesting that exposure to high SMFs did not affect the behavior of superoxide in these microorganisms. However, the modification of chromatin conformation was reported in E. coli cells by Belyaev et al. (1994). Zhang et al. (2003) showed a dose–response relationship between the magnetic flux intensity (5 and 9 T SMF) and an increase in mutation frequency in the SOD-deficient E. coli strain QC774.
7.2.4 SMF on Gene and Protein Expression
Differential gene expression is a critical event, common to all biological systems, allowing the accurate response under normal conditions and adaptation to various environmental stresses including magnetic fields. Tsuchiya et al. (1999) reported that inhomogeneous magnetic fields ranging from 5.2 to 6.1 T enhanced the transcription of the rpoS gene in E. coli. Three cDNAs were found to be expressed only in E. coli exposed to 300 mT SMF, whereas one cDNA was more expressed in the controls (Potenza et al. 2004). El May et al. (2009) found that the expression level of the 16S rRNA mRNA in Salmonella Hadar (S. Hadar) remained stable during the exposure of 200 mT SMF, while mRNAs of rpoA, katN, and dnaK genes were over-expressed following 10 h of SMF exposure. Ikehata et al. (2003) reported that a slight decrease in the expression of genes related to respiration was observed in the budding yeast, Saccharomyces cerevisiae (S. cerevisiae), exposed to 14 T SMF, whereas no changes were observed with field strengths <5 T. Although 14.1 T SMF caused little effects on cell growth of Shewanella oneidensis (S. onedensis) MR-1, apparent changes at transcriptional levels were detected in exposed cells, in which 21 genes were upregulated while other 44 genes were downregulated (Gao et al. 2005). In contrast, Potenza et al. (2012) reported that no differences were observed in gene expression in Tuber borchii mycelium after exposure to SMF, and only the activities of glucose 6-phosphate dehydrogenase and hexokinase were increased. These results indicated that the effects of the magnetic fields on the expression of genes are variable and dependent on parameters applied as well as the cell type.
Protein is the essential unit for biological activities in cells and their functions are determined by the sequence of amino acid including primary and tertiary structures of protein. Snoussi et al. (2012) investigated the effect of 200 mT SMF on the outer membrane protein pattern in S. Hadar. They found that a total of 11 proteins displaying more than a twofold change were differentially expressed in exposed cells, among which 7 were upregulated and 4 downregulated. The proteomic analysis provided a further overview of potentially important cytosolic proteins, in which a total of 35 proteins displaying more than a twofold change were differentially expressed in exposed cells, among which 25 were upregulated and 10 were downregulated. The stress response to a SMF of 200 mT was essentially set up to avoid oxidative damages, with the overexpression of proteins directly involved in oxidative stress response and metabolic switches to counteract oxidative stress (Snoussi et al. 2016).
7.2.5 Magnetosome Formation Sensing Magnetic Fields
Microbial magnetosomes represent a special category of intracellular organelles that are synthesized by magnetotactic bacteria (MTB). As a group of Gram-negative aquatic prokaryotes, MTB had a broad range of morphological types, including vibrioid, coccoid, rod, and spirillum. They used the magnetosomes to sense and modify their orientation according to the magnetic field (Moisescu et al. 2014). Magnetosomes comprised magnetic iron-bearing inorganic crystals enveloped by an organic membrane (Staniland et al. 2007). The membrane of magnetosomes contained a unique set of proteins that were thought to direct the biomineralization of magnetite crystals and magnetosome chain formation and regulation (Komeili et al. 2004). Forty-eight proteins were identified as magnetosome-specific proteins in Magnetospirillum magneticum (M. magneticum) AMB-1, and at least 13 proteins were potentially involved in the formation of magnetosomes, which were encoded by the mam and mms genes (Matsunaga et al. 2005). Among the genes known to be essential for magnetosome formation, magA, mms6, mamA, and mms13 were involved in iron uptake (Chikashi et al. 1995; Grünberg et al. 2001), synthesis of magnetite crystals of a uniform size and narrow size distribution with a cubo-octahedral morphology (Amemiya et al. 2007), magnetosome assembly (Komeili et al. 2004), and formation of magnetosomes, respectively. The superior crystalline and magnetic properties of magnetosomes have been attracting much interest in studying biomineralization and medical applications such as drug delivery, magnetic resonance imaging, and array-based assaying (Yoshino and Matsunaga 2006; Matsunaga et al. 2007; Barber-Zucker et al. 2016).
Wang et al. (2008) found that exposure to hypomagnetic field less than 500 nT restrained the growth of M. magneticum strain AMB-1 during the stationary phase, but increased the percentage of bacteria that contained mature SD magnetosomes in their exponential growth phase. The average size of magnetic particles in cells exposed to hypomagnetic field was larger (>50 nm) and they contained a larger proportion (57%) of SD particles compared to those grown in the geomagnetic field only. 200 mT SMF could impair the cellular growth and raise Cmag values of the cultures (Wang et al. 2009). The number of magnetic particles per cell and the linearity of magnetosome chain were affected by SMF exposure. Moreover, the expression of mamA, mms13, magA genes was upregulated by SMF. Blondeau et al. (2018) explored the effect of magnetotactic bacterium AMB-1 magnetosome chain alignment under conditions of limited external magnetic field. The bacteria were under a silica matrix, and some bacteria exposed to a field of 80 mT exhibited several magnetic lines. The chains of magnetosomes were arranged parallel to each other but offset relative to the longitudinal axis of the bacteria as shown in Fig. 7.2.
7.2.6 Application of Static Magnetic Fields on Antibiotic Resistance, Fermentation, and Wastewater Treatment
The application of SMF of 0.5 ± 2 mT significantly enhanced the activity of the antibiotic gentamicin against Pseudomonas aeruginosa (Benson et al. 1994). Stansell et al. (2001) found that exposure of E. coli to SMF of 4.5 mT significantly increased its antibiotic resistance. Tagourti et al. (2010) showed that exposure to a 200 mT SMF increased the efficiency of gentamicin against S. Hadar, but did not affect the diameter of the inhibition zone of some other antibiotics actives on Enterobacteria: penicillin, oxacillin, cephalotin, neomycin, amikacin, tetracycline, erythromycin, spiramycin, chloramphenicol, nalidixic acid, and vancomycin. However, Grosman et al. (1992) reported that a SMF of 0.5 ± 4.0 T had no significant influence on the growth of two strains of E. coli or S. aureus after exposure time of 30 ± 120 min, nor were there any effects on sensitivity to several antibiotics.
The influence of SMF on fermentation process has been investigated in biomass, and enzyme activity (Motta et al. 2001). da Motta et al. (2004) showed that exposure to 220 mT SMF significantly increased the biomass (g/L) of S. cerevisiae strain by 2.5-fold and the concentration of ethanol by 3.4-fold as compared with SMF non-exposed cultures. Glucose consumption was higher in magnetized cultures, which was correlated to the ethanol yield. Invertase is an enzyme (b-fructofuranosidase, EC 3.2.1.26) used to produce noncrystallizable sugar syrup from sucrose. Taskin et al. (2013) showed that the maximum invertase activity and biomass concentration were achieved with the spores exposed to 5 mT SMF.
Enhancement of biochemical processes by SMF has been applied in biological wastewater treatment. SMF had a positive effect on activated sludge biomass growth and dehydrogenase activity, which was similar to the observation in p-nitroaniline removal with activated sludge (Niu et al. 2014). Low and moderate SFMs could enhance the activities and growth of nitrite-oxidizing bacteria, increasing the removal of organic pollutants from wastewater (Jia et al. 2018). The effect of SMF exposure on the biodegradation rate of a mixture of pollutants was investigated by three strains including Pseudomonas stutzeri LBR (KC157911), Cupriavidus metallidurans LBJ (KU659610), and Rhodococcus equi LBB (KU743870) isolated and identified near Bizerte, Tunisia. Mansouri et al. (2019) applied 200 mT to these three strains and found there was an increase by 20% in the growth of the exposed bacterial population compared to controls, and 98% of biodegradation of DDT and 90% for BaP after 30 days of follow-up. The efficiency of phenol biodegradation was greatly increased by 30% under moderate SMFs (Kriklavova et al. 2014). Krzemieniewski et al. (2003) reported that a SMF of 400–600 mT stimulated the conditioning of wastewater sludge. A significant 30% increase in maximum nitrogen removal rate and an approximate 1/4 saving in cultivation time were achieved by using a SMF of 60 mT, indicating that the magnetic field was useful and reliable for fast start-up of anammox process (Liu et al. 2008). In algal-bacterial symbiotic system, Tu et al. (2015) reported that SMF stimulated both algal growth and oxygen production, suggesting that magnetic field could reduce the energy consumption required for aeration during the degradation of organic matter in municipal wastewater. Although SMFs have shown interesting potential in biodegradation of wastewater, there are some negative results. Mateescu et al. (2011) showed that SMFs of 500 and 620 mT produced an atypical growth in the fungus that was characterized by less and swollen, bombastic colonies which did not spread on the entire surface of the culture medium. Jasmina et al. (2012) reported that SMF (B = 17 mT) negatively influenced the growth of E. coli and Pseudomonas putida that were commonly found in wastewater treatment plants, but positively influenced enzymatic activity.
In addition to the application in wastewater biological treatment, SMFs also have broad application prospects for decolorization and de-oiling. In terms of decolorization reactions, Shao et al. (2019) studied the decolorization effect of marine microbial communities on azo dyes under SMF and found that the decolorization, chemical oxygen demand (COD) removal, and detoxification efficiency were higher at 45.3 mT SMF. Tan et al. (2020) found that the SMF and the salt-tolerant yeast Candida tropicalis SYF-1 co-enhanced SBR (named MSF-SBR) had higher and more stable ARB (acidity) under high salt and continuous operating conditions Red B processing efficiency (Shao et al. 2019). Ren et al. (2018) studied the effect of SMF on the high-efficiency oil-removing bacteria Acinetobacter B11, and the results showed that under a low-intensity magnetic field of 15–35 mT, the permeability of the cell membrane was increased and superoxide disproportionation was improved. Enzyme (SOD) activity effectively enhanced the lipid degradation performance of bacteria.
7.3 SMF on Plants
7.3.1 SMF on Germination
Magnetic seed treatment is one of the physical presowing seed treatments that have been reported to enhance the germination of crop plants. The rate and percentage of germination were increased by low and moderate SMFs in barley seed, rice (Oryza sativa L.) seeds, chickpea (Cicer arietinum L.) seeds, sunflower seeds, bean seeds, wheat seeds, okra (Abelmoschus esculentus cv. Sapz pari), garden pea (Pisum sativum L. cv. climax), mung beans seeds, onion seeds (c.v. Giza Red), and cumin seeds. However, there are few reports on negative results of germination stimulated by moderate SMFs. The effects of SMFs at various intensities and exposure periods on the germination of different plants were summarized in Table 7.1.
The coeffects of SMFs with other factors on germination have been investigated to obtain higher germination. Poinapen et al. (2013) investigated the magnetic flux intensity, together with exposure time, seed orientation (North and South polarity), and relative humidity (RH) in tomato (Solanum lycopersicum L.) var. MST/32 seeds. They found that higher germination (∼11.0%) was observed in magnetically exposed seeds than in non-exposed ones, suggesting a significant effect of non-uniform SMFs on seed performance with respect to RH, and more pronounced effects were observed during seed imbibition rather than during later developmental stages. Jovicic-Petrovic et al. (2021) found that the synergistic effect of B. amyloliquefaciens D5 ARV and 90 mT exposure increased the germination rate of white mustard (Sinapis alba L.) by 53.20%.
The mechanism of SMF on germination is not very clear. Bahadir et al. (2018) reported that 125 mT SMF treatment improved the germination of Lathyrus chrysanthus Boiss by breaking dormancy. Raipuria et al. (2021) showed that 200 mT SMF promoted nitric oxide via nitric oxide synthase to ameliorate the UV-B stress during germination of soybean seedlings. Kataria et al. (2020) reported the role of nitric oxide (NO) at 200 mT SMF induced seed germination and early growth characteristics of soybean (Glycine max) seedlings under salt stress and found that pretreatment of seeds with 200 mT SMF positively stimulated the germination and then promoted the seedling growth.
7.3.2 SMF on Growth
The effects of SMFs on growth have been well studied in various seeds of crop, vegetable, and fruit. Extremely low magnetic field at 47 ± 5 μT promoted the maize seedling growth (Hajnorouzi et al. 2011). Besides, Vashisth and Nagarajan (2010) found that under the same conditions, seedlings of sunflower showed higher seedling dry weight, root length, root surface area, and root volume; moreover, in germinating seeds, enzyme activities of amylase, dehydrogenase, and protease were significantly higher in treated seeds than controls as shown in Fig. 7.3. The beneficial effects of low SMFs on the growth have been well investigated in potato plantlets, barley seeds, soybean, corn, Zea mays, pea, and radish seedlings as shown in Table 7.2.
7.3.3 SMF on Gravitropism
Gravitropism is the most conspicuous response to the gravitational force in plants, which plays an essential role in maintaining the spatial orientation of seedlings and stable balance of massive plants. The ability of plants to sense gravity is largely attributed to starch-filled amyloplasts, which is a long-lived response throughout the entire life. Kuznetsov and Hasenstein (1996) reported that high-gradient magnetic fields (HGMFs) induced intracellular magnetophoresis of amyloplasts. The shoots of lazy-2 mutant of tomato (Lycopersicon esculentum Mill., cv. Ailsa Craig) exhibited negative gravitropism in the dark, but responded positively gravitropically in red light. The induced magnetophoretic curvature showed that lazy-2 mutants perceived the displacement of amyloplasts in a similar manner than wild type and the high MF did not affect the graviresponse mechanism (Hasenstein and Kuznetsov 1999). Weise et al. (2000) reported that Arabidopsis stems positioned in a high-gradient magnetic field (HGMF) on a rotating clinostat showed the lack of apical curvature after basal amyloplast displacement, indicating that gravity perception in the base was not transmitted to the apex. Jin et al. (2019) reported that root growth was significantly enhanced by SMFs in an intensity and magnetic direction dependent way, which was mediated by CRY and auxin signaling pathways in Arabidopsis. Hasenstein et al. (2013) examined the movement of starch grains of corn, wheat, and potato (Solanum tuberosum) in suspension during parabolic flights and found that magnetic gradients were able to move diamagnetic compounds under weightless or microgravity conditions and serve as directional stimulus during seed germination in low-gravity environments. Yano et al. (2001) reported that the primary roots of radish (Raphanus sativus L.) seedlings responded tropically to the 13–68 mT SMF with the tropism appearing to be negative and the roots responded significantly to the south pole of the magnet.
7.3.4 SMF on Photosynthesis
The effects of SMF on the photosynthesis have been investigated in various plants including soybean, corn, Lemna minor, and lettuce. Shine et al. (2011) reported that presowing magnetic treatment could improve biomass accumulation in soybean. Polyphasic chlorophyll a fluorescence transient from magnetically treated soybean plants gave a higher fluorescence yield. Baghel et al. (2016) provided further evidence that polyphasic chlorophyll a fluorescence (OJIP) transient from magnetically treated plants gave a higher fluorescence yield at J–I–P phase. Moreover, nitrate reductase activity, PIABS, photosynthetic pigments, and net rate of photosynthesis were also higher in plants that emerged from soybean seeds exposed to 200 mT SMF. In corn plants, Anand et al. (2012) reported that SMFs of 100 and 200 mT increased the photosynthesis, stomatal conductance, and chlorophyll content. The pretreatment of seeds of two corn cultivars with different magnetic treatments significantly alleviated the drought-induced adverse effects on growth by improving chlorophyll, photochemical quenching, and non-photochemical quenching (Javed et al. 2011). Jan et al. (2015) found that the reduced geomagnetic field (GMF) significantly stimulated growth rate of the total frond area in the magnetically treated Lemna minor plants, while the enhanced GMF pointed toward inhibition of growth rate in exposed plants in comparison to control, but the difference was not statistically significant. All photosynthetic pigments in lettuce seeds (Lactuca sativa var. capitata L.) were induced markedly under 0.44 T, 0.77 T, and 1 T SMF, especially chlorophyll a (Latef et al. 2020).
There are few studies on the coeffects of SMFs and other environmental factors on photosynthesis. Kataria et al. (2021) reported that 200 mT SMF pretreatment enhanced photosynthetic performance in soybean under supplemental ultraviolet-B radiation. Fatima et al. (2021a) found that 200 mT SMF pretreatment caused enhancement of leaf growth along with photosynthesis even under the presence of ambient UV-B stress. Moreover, pretreatment with 50–300 mT SMF increased water uptake by the midrib of soybean (Glycine max, variety JS-335), which in turn led to an increase in photosynthesis and stomatal conductance (Fatima et al. 2017). In addition, Jovanić and Sarvan (2004) reported that SMF induced significant changes in bean leaf fluorescence spectra and temperature, which the fluorescence intensity ratio (FIR) and change of leaf temperature βT were increased with the increase of MF intensity.
7.3.5 SMF on Redox Status
The uncoupling of free radicals including reactive oxygen/nitrogen species (ROS/RNS) is involved in the underlying mechanism of SMF induced oxidative stress in plants. The activities of free radical scavenging enzymes, including catalase (CAT), superoxide dismutase (SOD), glutathione reductase (GR), glutathione transferase (GT), peroxidase (POD), ascorbate peroxidase (APX), and polyphenol oxidase (POP), have been well documented to be altered by SMF exposure in various plants, including pea, radish (Raphanus sativus), Leymus chinensis, soybean, cucumber (Cucumis sativus), broad bean, corn, parsley (Petroselinum crispum), and wheat (Regoli et al. 2005; Baby et al. 2011; Jouni et al. 2012). Mohammadi et al. (2018) found that 0.2 mT SMF increased the contents of nitric oxide (NO), hydrogen peroxide (HO), and salicylic acid (SA) in tobacco cells (Nicotiana tabacum cv. Barley 21), and suggested that a signaling pathway activated by SMF starting from accumulation of NO and HO, then increased the cyclic nucleotides and subsequent decreased the cyclin-dependent kinases A (CDKA) and D-type cyclin (CycD). Cakmak et al. (2012) reported that SMF of 7 mT increased lipid peroxidation and H2O2 levels in shallot (Allium ascalonicum) leaves. Jouni et al. (2012) found that treatment of plants with 15 mT SMF caused accumulation of reactive oxygen species (ROS), lowered the antioxidant defense system, and increased the peroxidation of membrane lipids in broad bean (Vicia faba L.). Shokrollahi et al. (2018) found that 20 mT SMF decreased ferrous and HO contents, content and activity of ferritin and catalase in soybean plants, but the opposite responses were observed under 30 mT treatments. Shine et al. (2012) showed that SMFs of 150 and 200 mT enhanced production of ROS mediated by cell wall peroxidase, while the increase in the cytosolic peroxidase activity indicated that this antioxidant enzyme had a vital role in scavenging the increased H2O2 produced in seedlings from the magnetically treated soybean seeds. In mung bean seedlings treated with 600 mT SMF followed by cadmium stress, Chen et al. (2011) found that the concentration of malondialdehyde, H2O2, and O− were decreased, while the NO concentration and NOS activity were increased compared to cadmium stress alone, indicating that MF compensates for the toxicological effects of cadmium exposure were related to NO signal.
7.3.6 Cryptochromes Sensing Magnetic Field
Cryptochromes (CRYs) are flavoproteins that direct a diverse array of developmental processes in response to blue light in plants (Yu et al. 2010). CRY has been suggested to be a potential magnetoreceptor for light-initiated electron transfer chemistry which might be magnetically sensitive to virtue of the radical pair mechanism (Evans and Davidson 2013; Hore and Mouritsen 2016). Geomagnetic field (GMF) has been hypothesized to affect the redox balance of cryptochromes and the related signaling state (Vanderstraeten et al. 2015); however, the influence of strong SMF on the function of CRYs is still largely unexplored.
Three CRYs, CRY1, CRY2, and CRY3 are encoded in Arabidopsis genome (Lin and Todo 2005). CRY1 and CRY2 function as major blue light receptors regulating blue light induced de-etiolation, photoperiodic flowering, and circadian clock (Liu et al. 2016). Xu et al. (2014) found SMF of 500 μT modified the function of CRYs. The blue light-dependent phosphorylations of CRY1 and CRY2 were enhanced in Arabidopsis seedlings grown in a 500 μT MF, whereas the near-null MF weakened the blue light-dependent phosphorylation of CRY2 but not CRY1; in the darkness, dephosphorylations of CRY1 and CRY2 were slowed down in the 500 μT MF, whereas dephosphorylations of CRY1 and CRY2 were accelerated in the near-null MF. According to the calculation of radical pair mechanism in a relatively realistic model of the radical pair system in Arabidopsis CRY1, Solov’yov et al. (2007) showed that 500 μT MF could increase the signaling activity of cryptochrome by up to 10%, suggesting that the function of CRYs was affected by magnetic field. Pooam et al. (2019) investigated the response of Arabidopsis CRY1 in vivo to 500 μT SMF using both plant growth and light-dependent phosphorylation as an assay, then they found that the magnetically sensitive reaction step in the cryptochrome photocycle must occur during flavin reoxidation, and likely involved the formation of ROS. Ahmad et al. (2007) reported that 500 μT MF enhanced the blue light-dependent inhibition of hypocotyl growth of Arabidopsis. Hypocotyl growth of Arabidopsis mutants lacking CRYs was unaffected by the increase of magnetic intensity, while cryptochrome-dependent responses, such as blue light-dependent anthocyanin accumulation and blue light-dependent degradation of CRY2 protein, were enhanced at the higher magnetic intensity. However, with experimental conditions chosen to match Ahmad’s study, Harris et al. (2009) found that in no case consistent, statistically significant MF responses were detected.
CRYs evolved from photolyases are conserved across many different species. In addition to plants, the expression of CRYs has been detected in migratory birds and the eyes of mammals, which were putative sites for magnetoreceptors in vertebrates, and there was no evidence for intracellular magnetite in putative vertebrate magnetoreceptors identified by magnetic screening (Möller et al. 2004; Nießner et al. 2013; Edelman et al. 2015). In animals, CRYs also functioned as circadian photoreceptors in the Drosophila brain, mediating the light resetting of the 24 h clock; but in vertebrates, the CRYs acted as the main negative regulators for the circadian feedback loop, due to the difference in light sensing (Yoshii et al. 2009; Fedele et al. 2014). Non-Drosophila insects can also encode CRY1 and CRY2, but CRY1 retain their light-sensing properties, whereas the CRY2s act as vertebrate-like negative regulators. Marley et al. (2014) reported that MF exposure coupled with CRY photoactivation during embryogenesis was sufficient to produce heightened seizure susceptibility in resultant Drosophila third instar (L3) larvae. Giachello et al. (2016) provided evidence that exposure to a MF of 100 mT was sufficient to potentiate the ability of light-activated cryptochrome to increase neuronal action potential firing, indicating that the activity of cryptochrome was sensitive to an external MF that was capable of modifying animal behavior.
7.4 SMF on Animals
7.4.1 SMF on Caenorhabditis elegans
Caenorhabditis elegans (C. elegans) is a small free-living nematode that has been widely utilized to address fundamental questions of developmental biology, neurobiology, and behavioral biology. C. elegans is similar to higher eukaryotes in many molecular and cellular pathways (Kaletta and Hengartner 2006) and offers unique advantages, including the ease of maintenance, small size, short life cycle, genetic manipulability, stereotypical development, and high-throughput capability. As about 50% of its genes have human homologs, C. elegans based assays are increasingly used to evaluate potential toxicity of different stressors in humans and mechanisms of toxicity by physical and chemical exposures (Kazazian Jr. 2004; Dengg and van Meel 2004; Rajini et al. 2008; Sprando et al. 2009; Boyd et al. 2010).
Recent evidence has shown that the C. elegans oriented to the earth’s magnetic field during vertical burrowing migrations neuron pair (Vidal-Gadea et al. 2015). A pair of neurons called the AFD neurons, which carry information about temperature and chemical stimuli from the environment, were critical for magnetic navigation in C. elegans. The further investigation showed the unique spatiotemporal trajectories of magnetotactic processes in C. elegans under different external conditions including temporal, spatial, and environmental factors. They found that the magnetic orientation of these “small worm” might be stronger under dry conditions (<50% RH) (Bainbridge et al. 2020). Using worms with mutations at some of the genes expressed in the AFD neurons and a calcium sensitive protein, it was found that the tax-4 gene, which encoded an ion channel protein similar to a photoreceptor found in the retina of human eyes, was required for magnetotaxis (Rankin and Lin 2015). These data represented a significant advance in our understanding of the neurobiology underlying how organisms navigate using the Earth’s magnetic field. Recently, Cheng et al. (2022) found that exposure C. elegans to 0.5 T and 1 T SMFs greatly decreased the avoidance behavior of the pathogenic Pseudomonas aeruginosa. The total serotonin level was significantly increased by exposure to 0.5 T and 1 T SMF; in contrast, SMFs had few effects on other three neurotransmitters including choline, γ-aminobutyric acid (GABA), dopamine as shown in Fig. 7.4. These data indicated that moderate-intensity SMFs induced neurobehavioral disorder might be modulated by serotonin in C. elegans.
The biological effects of SMFs on C. elegans have been focused on the development, aging process, behavior, and global gene expression. Hung et al. (2010) reported that treatment with 200 mT SMF reduced the development time from the L2 to the L3 stage by 20%, from L3 to L4 by 23%, and from L4 to young adult by 31%. With SMF treatment, the average lifespan was reduced from 31 to 24 days in wild-type nematodes. The upregulation of lim-7, clk-1, daf-2, unc-3, and age-1 by SMF treatment was verified by quantitative real-time PCR; in contrast, lifespan analyses showed that SMF treatment had no effect on let-7, unc-3, and age-1 mutants, indicating that the induction of gene expression by SMFs was selective and dose-dependent. Lee et al. (2012) showed that long-term and low-dosage exposure to 200 mT SMF was capable of inducing an apoptosis-mediated behavioral decline in nematodes. 26 differentially expressed genes including apoptosis, oxidative stress, and cancer-related genes were identified, indicating that a global molecular response to SMF exposure occurred. Mutations in genes involved in major apoptotic pathways, that is, ced-3, ced-4, and ced-9, abolished this SMF-induced behavioral decline. Kimura et al. (2008) reported that genes involved in motor activity, actin binding, cell adhesion, and cuticles were transiently and specifically induced by 3 or 5 T SMF exposure in C. elegans. Several genes encoding apoptotic cell-death activators and secreted surface proteins were upregulated by ionizing radiation, instead of SMFs. Exposure to 3 or 5 T SMFs did not induce DNA double-strand breaks or germline cell apoptosis during meiosis. However, we found that 8.5 T SMFs resulted in a time-dependent lifespan decrease and alteration of development rate and stages in C. elegans. Germ cell apoptosis dramatically increased upon exposure to 8.5 T SMF in worms via core apoptotic machinery, which could be prevented by concurrent treatment with a free radical scavenger, dimethyl sulfoxide (Wang et al. 2015). Yang et al. (2022) further explored the biological effects of 10 T SMF on sperms and their offspring in him-5 male mutants of C. elegans and found that sperms were sensitive targets of high SMFs as shown in Figs. 7.5 and 7.6. Although 10 T SMF had little effect on the morphology of sperms, the size of unactivated sperms and the function of sperms were modified by SMF exposure, leading to diminish the reproductive capacity of him-5 male worms. These observations provided interesting information regarding the adverse effects of high SMFs on the reproductive function of C. elegans and their offspring, which could improve our understanding of the fundamental aspects of high SMFs on biological system.
7.4.2 SMF on Insects
Magnetic fields have been shown to affect the orientation, oviposition development, fecundity, and behaviors for a wide variety of insects. The insect eggs have advantages in magnetic exposure for a large number of eggs which can be placed into the magnet at the same time. The SMF at 4.5 mT had no effect on egg lying, but increased mortality of eggs, larvae, and pupa, and diminished adult viability in Drosophila (Ramirez et al. 1983). Decreased hatching rate after exposure to a weak SMF during early embryogenesis was also obtained in D. melanogaster and Heliothis virescens (tobacco budworm) (Ho et al. 1992; Pan 1996). A significant increase of Hylotrupes bajulus viability and larval mass was reported after exposure to a SMF of 98 mT (Rauš Balind et al. 2009). The SMF of 60 mT reduced the embryonic and post-embryonic development and induced weaker viability in two different species, Drosophila melanogaster and Drosophila hydei (Savić et al. 2011). Todorovic et al. (2019) found that chronic exposure to 110 mT SMF significantly decreased the gut mass and the activity of glutathione reductase (GR) and glutathione S-transferase (GST) as compared to the control in Blaptica dubia (B. dubia). They further reported that 110 mT SMF decreased nymph body mass and glycogen content in the fat body but increased all examined parameters of locomotion, indicating that B. dubia nymphs were sensitive to SMF exposure (Todorovic et al. 2020). Oak and beech populations of Drosophila subobscura had longer development time, and lower viability was observed in N and S groups of 2.4 T SMF, which was mediated by oxidative stress (Todorović et al. 2015). Apparent hatching delay of strong magnetic fields was observed in mosquito eggs in the center of 9.4 and 14.1 T magnets (Pan and Liu 2004).
In insects, the neuroendocrine system is a main regulator of all aspects of life processes, such as development and behavior, and the detection and activity of an external magnetic field may be transmitted by the neuroendocrine system (Blanchard and Blackman 1994; Gilbert et al. 1996). A SMF of 375 mT caused the disturbance of development and survival of pupae of the honeybee and Tenebrio molitor, yellow mealworm (Prolic and Jovanovic 1986; Prolić and Nenadović 1995). The morphometric parameters of the A1 and A2′ neurosecretory neurons of the protocerebrum as well as the morphometric parameters of the corpora allata were changed by a SMF of 320 mT (Perić-Mataruga et al. 2008). However, SMF of 50 mT did not effect on pupa-adult development dynamic of two examine Tenebrio species, but modulated their motor behavior (Todorović et al. 2013).
The antennal lobe of Drosophila provides an ideal intact neural network model to investigate neural circuit function (Ng et al. 2002). Yang et al. (2011) found that a SMF of 3.0 T modilated the rhythmic spontaneous activities of large LNs and correlated activity of ipsilateral pairs of large LN/LN in Drosophila antennal lobe, indicating that Drosophila could be an ideal intact neural circuit model to evaluate the effects of magnetic field stimulations.
Mutagenic effects of a static magnetic field were investigated by increasing mutation rate in population of Drosophila exposed to magnetic field 10–12 times greater than geomagnetic one (Giorgi et al. 1992). Exposure to 2, 5, or 14 T fields caused a statistically significant enhancement in somatic recombination frequency in the postreplication repair-deficient flies, whereas the frequency of somatic recombination remained unchanged in the nucleotide excision repair-deficient flies and in DNA repair-proficient flies after exposure (Takashima et al. 2004).
7.4.3 SMF on Helix pomatia
Helix pomatia possesses simple nerve system and displays simple behavioral repertoire. Single identified neurons have been documented as a good experimental model for the relatively large size, easy manipulation, consistent position on the surface of the ganglia, and consistent type of synaptic connections. Nikolić et al. (2008) reported that the magnetic field of 2.7 mT intensity caused changes in the amplitude and duration of action potential of the Br neuron in subesophageal ganglia of the garden snail Helix pomatia, whereas the 10 mT magnetic field changed the resting potential, amplitude spike, firing frequency, and duration of action potential of the Br neuron. Moreover, significant increase of the activity of Na+/K+-ATPase and the expression of its α-subunit in nervous system were observed in Helix pomatia exposed to 10 mT SMF (Nikolić et al. 2013). With single, 30-min long, and whole body exposed to 147 mT, Hernádi and László (2014) reported that SMF exposure mediated peripheral thermal nociceptive threshold by affecting the serotonerg as well as the opioiderg system.
7.4.4 SMF on Aquatic Animals
Sea urchins are the only invertebrates with the same development patterns as mammals. Moreover, the gametes of sea urchins can be obtained easily, the eggs and early embryos are transparent, and the early development of embryos is highly synchronous. A SMF of 30 mT delayed the onset of mitosis in two species of sea urchins, Lytechinus pictus and Strongylocentrotus purpuratus. There was an eightfold increase in the incidence of exogastrulation in Lytechinus pictus embryos exposed to SMFs, while magnetic fields had no effects on species Strongylocentrotus purpuratus embryos (Levin and Ernst 1997). Exposure of fertilized eggs of Echinometra mathaei to 30, 40, and 50 mT of magnetic fields delayed the onset of early cleavage division and significantly decreased the cleaved cells for exposed embryos. As the increase of intensity of the magnetic fields, earlier appearances of abnormalities were observed (Sakhnini and Dairi 2004).
The interaction among neurons in escape circuit of crayfish has been well studied. As the lateral giant (LG) neuron was easy to access for electrophysiological study, Ye et al. (2004) found that exposure to SMF at 4.74–43.45 mT increased the amplitude of action potential (AP) in LG depending upon both the intensity of field and duration of field exposure, which was mediated by the increasing level of intracellular Ca2+ in the LG. The excitatory postsynaptic potential (EPSP) produced via electrical and chemical synapses in the lateral giant neuron was enhanced after 30 min of SMF exposure (8.08 mT). Perfusion of field-exposed crayfish bath solution or preloading of Ca2+ chelator and intracellular Ca2+ release blocker failed to observe the SMF-induced enhancement on EPSP (Yeh et al. 2008).
As an increasingly important model species in genetic and neurobehavioral studies, zebrafish (Danio rerio) is an excellent organism for better understanding the biological mechanism of SMFs. Using a fast, fully automated assay system relying on negative reinforcement, Shcherbakov et al. (2005) recorded statistically highly significant reactions to weak magnetic field changes in Mozambique tilapia, a fish migrating regularly between freshwater and the sea, and non-migratory zebrafish. Takebe et al. (2012) found that zebrafish responded to a magnetic field as weak as the geomagnetic field by bidirectional orientation with group-specific preferences regardless of close kinships. SMFs with density from 4.7 to 11.7 T profoundly disturbed the orientation and locomotion behaviors of adult zebrafish, and the independence of these effects from other sensory modalities suggested that they were mediated by the vestibular system as shown in Fig. 7.7 (Ward et al. 2014). In addition, the SMFs could be disrupting metabolism and immunity of the Caspian kutum fry during acute and subacute exposures (Loghmannia et al. 2015). Ge et al. (2019) showed that 9.0 T SMF exposure had no effect on the survival and overall development of zebrafish embryos, but slowed down the development speed of the whole animal. They surmised that microtubule and spindle positioning were perturbed under such high SMF.
7.4.5 SMF on Xenopus laevis
Xenopus embryos are thought to be a useful tool for studying vertebrate development, and gene expression for their embryogenesis is rapid and completed outside of the female. The hatching rate of embryos of the frog Rana pipiens subjected to the field of a 1 T permanent magnet was found to be reduced (Neurath 1968). Ueno et al. (1984) investigated embryos of African clawed toads exposed to 1 T magnetic field and found that the magnetic field exerted no harmful or modifying effects on gastrulation and neurulation; however, exposed embryos occasionally developed into tadpoles with reduced pigmentation, axial anomalies, or microcephaly. Compared to the first and the second cleavage, the third cleavage was the most susceptible to reorientation in strong SMFs. Exposure to SMF at 16.7 T altered the direction of the third cleavage furrow from its normal horizontal type to the perpendicular type, which was confirmed by embryos exposed to 8 T (Denegre et al. 1998; Eguchi et al. 2006). These results indicated that SMFs might act directly on the microtubules of the mitotic apparatus to cause distortion of the third cleavage furrow. Kawakami et al. (2006) found that a SMF of 11–15 T significantly retarded normal development and induced microcephaly, two heads, abnormal cement glands, and multiple malformations. Moreover, the gene expression of Xotx2 (an important regulator of fore and midbrain morphogenesis) and Xag1 (essential for cement gland formation) was greatly suppressed by strong SMF. Mietchen et al. (2005) investigated the morphology of fertilizable Xenopus laevis eggs with and without jelly coat that were subjected to a SMF of up to 9.4 T and found that no effect was observed when the jelly layers of the eggs were left intact, indicating the action of magnetic fields might involve cortical pigments or associated cytoskeletal structures normally held in place by the jelly layers.
The effects of SMF exposure on nerve conduction were investigated in frog sciatic nerves. A significant increase in the nerve conduction velocity (NCV) of compound action potentials (CAP) in sciatic nerves was observed by exposure to a uniform SMF of 1.16 T. Edelman et al. (1979) observed a significant increase in the amplitude of CAP in frog sciatic nerves when a uniform SMF of 385 or 600 mT was applied perpendicular to the axis of the nerve fibers. Although NCV of CAP was not affected by the 8 T SMF, Eguchi et al. (2003) reported that under SMF exposure an optimal time interval existed in the relative refractory period (1.0–1.1 ms) during which some ions move dynamically through specific ion channels. Satow et al. (2001) found that 0.65 T SMF increased excitability in bullfrog sartorius muscle during the recovery period in a conditioning-test stimulation paradigm. With the exposure of in vitro frog sciatic nerve fibers to moderate-intensity gradient SMF up to 0.7 T, Okano et al. (2012) found the values of the nerve conduction velocity of C fibers were significantly reduced by Bmax of 0.7 T SMF but not by 0.21 T SMF, relative to the unexposed control. Although the mechanistic reasons for this decrease have yet to be clarified, SMF could affect the behavior of some types of ion channels associated with C fibers.
7.4.6 SMF on Mice and Rats
7.4.6.1 SMF on Bone Growth, Healing, and Loss
SMF has been considered as a physical therapy on bone health maintenance and bone disorders treatment for it can enhance bone fracture healing and bone formation by osteoblast both in vivo and in vitro (Trock 2000; Miyakoshi 2005; Saunders 2005; Wang et al. 2011). Zhang et al. (2018a) found that 4 mT SMF could inhibit the structural deterioration of trabecular and cortical bone and reduce mechanical strength in T1DM rats. They compared the microstructure and mechanical properties of mouse bone under either hypomagnetic field (HyMF, 500 nT) or moderate SMF (MMF, 0.2 T) and found that exposure to MMF for 4 weeks had a significant effect on bone biology mechanical properties but bone microarchitecture was not affected, whereas HyMF significantly inhibited mouse growth and bone elasticity (Zhang et al. 2018b). Shan et al. (2021) reported that the tooth movement speed was significantly faster and the periodontal ligament (PDL) width was significantly increased under a SMF of 20–204 mT. 2–4 T SMFs improved bone microstructure and strength by stimulating bone formation and inhibiting bone resorption (Yang et al. 2021).
With implantation of magnetized rods into the middle diaphysis of rat femurs to generate SMF, Yan et al. (1998) found that the femurs adjacent to magnetized specimens had significantly higher bone mineral density (BMD) and calcium content than those adjacent to the unmagnetized specimen. The significantly reduced BMD in this ischemic bone model could be prevented by long-term SMF exposure of 3 weeks (Xu et al. 2001). The SMF accelerated not only the bone neoformation but also the integration of the bone grafts (Puricelli et al. 2009; Leesungbok et al. 2013). Kotani et al. (2002) showed that high SMF of 8 T stimulated ectopic bone formation in and around subcutaneously implanted bone morphogenetic protein (BMP) 2-containing pellets in mice, in which the orientation of bone formation was parallel to the magnetic field. Using ovariectomized (OVX) rat model to represent the clinical features of bone loss, Xu et al. (2010) observed that SMF significantly increased the BMD of osteoporotic lumbar vertebrate without affecting the E2 (17-b-estradiol) levels of serum compared with sham control. Taniguchi et al. (2004) examined the effect of the whole-body exposure to SMF on bone formation and found that SMF could contribute to the relief of pain induced by adjuvant arthritis and BMD was also accelerated significantly. However, with the same SMF exposure device, Taniguchi and Kanai (2007) reported that SMF did inhibit the bone loss of tibia in OVX rats to some extent, but its BMD was still much lower than normal rats, which might be due to the enhanced locomotor activity.
7.4.6.2 SMF on Cardiovascular System
7.4.6.2.1 Blood Pressure and Blood Flow
SMF in the mT range has been reported to modulate circulatory hemodynamics and/or arterial blood pressure (BP) and baroreflex sensitivity (BRS). Okano and Ohkubo (2003, 2005, 2006) found that whole-body exposure to SMF suppressed spontaneously hypertensive rats (SHR), which was mediated by nitric oxide (NO) pathway, Ca2+ channel, and hormonal regulatory systems. With the calculation of the hematological characteristics, Tasic et al. (2021) found that SMFs with different orientations had adverse effects on the hematological indicators of spontaneously hypertensive rats, but their cardiac and renal morphological features were not affected. Li et al. (2020) found that 20–150 mT SMF had antithrombotic effects in constructed rat and mouse thrombosis models, indicating a non-invasive prevention and treatment way for clot-related diseases.
It is well known that surface temperature and cutaneous blood flow are closely parallel to each other. Ichioka et al. (2003) reported that the whole body of anesthetized rats exposed to 8 T SMF was associated with reduced skin blood flow and temperature, which could be recovered after removal of the animal from the magnet. Both increases and decreases in skin and rectal temperatures were observed in mice exposed to SMFs with intensities ranging from 0.4 to 8 T. In contrast to these observations, no evidence was found for a change in body temperature of rodents exposed to strong homogeneous or gradient magnetic fields (Tenforde 1986).
7.4.6.2.2 Cardiac Function
Blood flow in an applied magnetic field gives rise to induce voltages in the aorta and other major arteries of the central circulatory system that can be observed as superimposed electrical signals in the electrocardiogram (ECG). The largest magnetically induced voltage occurs during pulsatile blood flow into the aorta and results in an increased signal at the location of the T-wave in the ECG. A marked increased T-wave in the ECG records was observed in squirrel monkeys during the exposure to stationary fields of 2–7 T and rabbits exposed to 1 T SMF (Beischer and Knepton Jr. 1964; Togawa et al. 1967). Similar observation was reported by Gaffey and Tenforde (1981) that a field strength dependent increase in the amplitude of the T-wave signal in the rat ECG was revealed during exposure to homogeneous stationary magnetic fields of 2 T, which might be due to a superimposed electrical potential generated by aortic blood flow in the presence of a stationary magnetic field. The exposure of rats to a SMF of 128 mT decreased the activities of glutathione peroxidase (GPx) and the CuZn superoxide dismutase (CuZn-SOD) in rat cardiac muscle (Amara et al. 2009).
7.4.6.2.3 Hematological Parameters
The effects of SMFs on hematological parameters have been studied in rats at the intensity of 128 mT. Amara et al. (2006b) reported that a SMF of 128 mT significantly decreased the growth rates, but increased the plasmatic total protein levels, hemoglobin, red blood cells, white blood cells, platelet number, and the activities of lactate dehydrogenase (LDH), aspartate aminotransferase (AST), and alanine aminotransferase (ALT) in male Wistar rats; in contrast, the glucose concentration was unaffected. Milovanovich et al. (2016) showed that both upward- and downward-oriented SMF of 128 mT caused a reduction in the amount of total white blood cells (WBC). Chater et al. (2006) found that subacute exposure to a SMF of 128 mT stimulated biosynthesis of plasma corticosterone and metallothionein activities in female rats, while increased blood glucose and decreased insulin release, leading to a diabetic-like state in pregnant rats. Elferchichi et al. (2016) showed an impaired glucose homeostasis and a deregulated lipid metabolism after SMF exposure in adult rats. But, they noticed that a SMF of 128 mT induced a pseudoanemia status with increased monocarboxylate transporters (MCT4) and glucose transporter 4 (Glut4). Atef et al. (1995) investigated changes of hemoglobin (Hb)’s characteristics in Swiss mice using hundreds of mT for 10 min and found that the rate of Hb oxidative reaction was declined by 350–400 mT. However, Djordjevich et al. (2012) found that differently oriented SMF of 16 mT did not alter hemoglobin and hematocrit, although the upward and downward fields caused statistically significant higher levels of serum transferrin.
In addition, the supplementation with vitamin D corrected and restored glycemia and insulinemia in SMF-exposed rats (Lahbib et al. 2015). Selenium (Se) improved adverse oxidative stress in blood induced by SMF, whereas zinc supplementation could prevent toxic effects of SMFs probably by its antioxidant proprieties (Ghodbane et al. 2011).
7.4.6.3 SMF on Digestive System
The effects of SMFs on digestive system are largely unknown and most of studies mainly focus on the intensity of 128 mT. A SMF of 128 mT increased total GSH levels and the activity of superoxide dismutase (SOD) and catalase (CAT) in rat liver and hepatocyte apoptosis through a caspase-independent pathway involving mitochondrial apoptosis-inducing factor (AIF), which was restored by Se and vitamin E supplementations (Ghodbane et al. 2015). Amara et al. (2009) found that exposure of rats to a SMF of 128 mT increased the 8-oxo-7,8-dihydro-2′-deoxyguanosine (8-oxodGuo) concentration in kidney.
7.4.6.4 SMF on Endocrine System
The influence of SMFs on endocrine system has been linked to their function, such as insulin, pineal gland, and testis. Jing et al. (2010) found that 180 mT SMF exposure could significantly accelerate the diabetic wound (DW) closure process and enhance the wound tensile strength (TS); however, 180 mT local SMF exposure had slight effect on insulin secretion or pancreatic cells of diabetic rats (Rosmalen et al. 2002). Under the neodymium permanent magnets, Feng et al. (2022) found that SMFs promoted diabetic mice wound healing by suppressing oxidative stress. Elferchichi et al. (2011) showed that the metabolic alterations following exposure to a SMF of moderate intensity could trigger the development of a pre-diabetic state. Exposure to a SMF of 128 mT induced an increase in plasma glucose level and a decrease in plasma insulin concentration in rats, which could be corrected by vitamin D supplementation (Lahbib et al. 2010, 2015). Moreover, β cell insulin content, the expression of glucose transporter GLUT2 and islet area were lower in SMF-exposed group compared to control. Tang et al. (2021) found that moderate-intensity SMFs could cause the abnormalities of glucose metabolism in rats’ brain in an intensity-dependent way, which was closely related to anxiety behavior as shown in Fig. 7.8. However, László et al. (2011) showed that daily SMF exposure repeated for several weeks was protective against the development of high blood glucose level in diabetic mice. Li et al. (2020) also reported that moderate intensity of SMFs, 400 mT and 600 mT, had the protective effects on diabetic mice. Yu et al. (2021) further found that downward 100 mT SMF could reduce the occurrence of hyperglycemia, fatty liver, weight gain, and tissue damage effectively, while upward SMF cannot. Both weak static fields (800 G) for periods between 12 h and 8 days and a 7-Tesla MRI magnet for 45 min had slight effect on nighttime pineal, serum melatonin levels, 5-hydroxytryptamine (5-HT), and 5-hydroxyindole acetic acid (5-HIAA) in exposed rats (Kroeker et al. 1996). Abdelmelek et al. (2006) reported that a SMF of 128 mT induced an increase in norepinephrine content in rat gastrocnemius muscle.
7.4.6.5 SMF on Lymphatic System
Bellossi (1986) showed that the lifetime was prolonged significantly by uniform SMFs of 600 or 800 mT in female AKR mice, which developed spontaneous lymphoblastic leukemia. Yang et al. (2009) observed that SMFs of 200–400 mT prolonged the average lifetime of mice bearing L1210 leukemia cells and increased the spleen and thymus index in normal mice. Milovanovich et al. (2016) reported that a SMF of 128 mT caused a reduction in the amount of lymphocytes in serum and a decrease of granulocytes in the spleen, kidney inflammation, a specific redistribution of pro-inflammatory cells in blood and various organs. De Luka et al. (2016) showed that a SMF of 1 mT reduced the content of zinc in mouse spleen, while copper amount remained unchanged.
7.4.6.6 SMF on Nervous System
The nervous system, including brain, spiral cord, and neurons, is important target of magnetic fields. SMF exposure had a strong modulation effect on cellular hydration in different tissues of rats including brain tissue. Krištofiková et al. (2005) showed functional teratogenic risks of the alterations in the orientation of 140 mT SMF for postnatal brain development and functional specialization of both hippocampi in rats. The whole-body SMF exposure and local SMF exposure on the spine resulted in practically identical ear thicknesses and significant effects of the SMF might involve a lower spinal response to the SMF exposure, and showed that local SMF exposure on the spine affected ear thickness, indicating that the place of local SMF action may be in the lower spinal region (Kiss et al. 2015). Dincic et al. (2018) reported increased synaptosome ATPase activities in rat synaptosomes exposed to 1 mT SMF. Veliks et al. (2004) investigated the influence of 100 mT SMF on autonomic nervous system in rat brain by evaluating heart rate and rhythmicity and found that the effectiveness of SMF in large measure depended on both functional peculiarities and functional activities of brain autonomic centers. Yakir-Blumkin et al. (2020) implanted a small magnetic sheet into the rat skull, which an average magnetic field intensity of 4.3 mT in the subventricular zone (SVZ) and 12.9 mT in the endothelial layer, and found that low-intensity SMF exposure enhanced the proliferation of SVZ cells in young adult rats and DCX-expressing new cells in the neocortical area.
Behavioral effects are essential response of nervous system function. Exposure to 128 mT SMF not only altered emotional behavior of rats in the plus maze and long-term spatial memory, but also led to cognitive impairments or at least to substantial attention disorders in the Morris water maze (Ammari et al. 2008). Saeedi Goraghani et al. (2019) found that simultaneous exposure to 5 mT SMF increased the neurobehavioral effects of MK-801, N-methyl d-aspartate (NMDA) receptor blocker, in male Wistar rats. Maaroufi et al. (2013) showed that SMF exposure had no massive effect but affected long-term spatial memory. Weiss et al. (1992) confirmed that acute behavioral and neural effects on rats became apparent at 4 T in a simple T-maze study. A 30 min exposure of rats to a 9.4 T superconducting magnet induced tight circling locomotor activity, conditioned taste aversion (CTA), and the express of c-Fos in specific vestibular and visceral nuclei within the brainstem (Nolte et al. 1998; Snyder et al. 2000). They extended the studies on the relationship of rat behavior and SMF of 7 or 14 T and found that depressed drinking, more circling, and less rearing actions were observed in SMF-exposed group, while CTA was acquired in a short time, and the direction of circling was dependent on the orientation of SMF to rats as shown in Fig. 7.9 (Houpt et al. 2007, 2012). The behavior response of magnetic field exposure was abolished by chemical labyrinthectomy, suggesting that the vestibular apparatus of the intact inner ear is the locus of magnetic field interaction (Houpt et al. 2007; Cason et al. 2009). Tkac et al. (2021) found that 16.4 T SMF induced long-term impairment of the vestibular system in mice, while 10.5 T SMF exposure had no effect.
Magnetic therapy as a non-contact, non-invasive, and cheap physiotherapeutic method has been used for analgesic modulation. Gyires et al. (2008) reported that acute exposure of mice to 2–754 mT SMF resulted in an opioid-mediated analgesic action in the writhing test in the mouse. Exposure of mice to both inhomogeneous (3–477 mT) and homogeneous (145 mT) SMF generated an analgesic effect toward visceral pain elicited by chemically induced pain (Kiss et al. 2013). Zhu et al. (2017) found that the orofacial pain levels of mice in the environment of 20–204 mT SMF could be reduced and significantly downregulated P2X3 receptors of trigeminal ganglion (TG) in mice during experimental tooth movement.
Using EEG detection, Rivadulla et al. (2018) found that 0.5 T SMF treatment for 1–2 h could reduce epileptiform activity in anesthetized rats and monkeys. Antal and László (2009) found that inhomogeneous subchronic SMF could prohibit the increased sensitivity of mice to mechanical stimuli in neuralgia in mice, which was in consistent with the pain suppression by SMF of clinical magnetic resonance order. With rat model of Huntington disease, the static magnetic field north and south promoted a distinct behavioral profile and morphological preservation after 7 days of lesion with quinolinic acid associated with apomorphine (APO) (Giorgetto et al. 2015). Lv et al. (2022) found that 7 T SMF exposure for 8 h attenuated the depressive state of depressed mice, including reducing the immobility time of the tail suspension test and increasing sucrose preference. Brain tissue analysis showed that 11.1–33.0 T and 7 T SMF can increase oxytocin by 164.65% and 36.03%, respectively, promoting the increase of c-Fos level in the hippocampus by 14.79%. However, Sekino et al. (2006) reported that a SMF of 8 T upregulated the action potentials of nerve C fiber, which enhanced pain feeling in rats for the C fiber is functioned as pain transmitter.
7.4.6.7 SMF on Reproduction and Development
The adverse effects of SMF on aspects of spermatogenesis, organogenesis, or even ontogenesis in humans have cause great concern in recent years. Embryonic development is a highly sensitive process to SMFs. Many researchers have explored the biological effects of SMF exposure with different magnetic field intensities and different exposure methods on mice and their embryos. The exposure modes were mainly intermittent short-term and continuous long-term exposure, and studies found that different steady-state magnetic field parameters and exposure methods have different effects on the organism as shown in Table 7.3.
7.4.7 Magnetic Sensing Protein in Animals
Many animals have evolved to sense the direction of the geomagnetic field for orientation, navigation, and migration over long distances. The blue light receptor CRYs that could form radical pairs after exposure to blue light were suggested to be a magnetoreceptor based on the proposition that radical pairs were involved in the magnetoreception. CRYs are expressed not only in plant, but also in newts, fruit flies, birds, and the eyes of mammals (Möller et al. 2004; Nießner et al. 2013). Gegear et al. (2008) reported that cry mutants of Drosophila melanogaster showed neither naive nor a magnetic field, while the wild-type flies showed significant naive and trained responses to the magnetic field. Expression of monarch butterfly (Danaus plexippus) cryptochrome gene in Drosophila cry mutants rescued the responses to the magnetic field (Gegear et al. 2010). Marley et al. (2014) reported that MF exposure coupled with CRY photoactivation during embryogenesis was sufficient to produce heightened seizure susceptibility in resultant Drosophila third instar (L3) larvae. Giachello et al. (2016) provided new evidence that exposure to MF of 100 mT was sufficient to potentiate the ability of light-activated CRY to increase neuronal action potential firing, indicating that the activity of CRY was sensitive to an external MF that was capable of modifying animal behavior. CRYs also function as circadian photoreceptors in the Drosophila brain, mediating the light resetting of the 24 h clock, but in vertebrates, the CRYs act as the main negative regulators for the circadian feedback loop, due to the difference in light sensing (Yoshii et al. 2009; Fedele et al. 2014). Non-Drosophila insects encode CRY1 and CRY2, but CRY1 retains their light-sensing properties, whereas the CRY2s act as vertebrate-like negative regulators.
In order to investigate a possible interaction between CRY4 and the iron-sulfur-containing assembly protein (ISCA1) from European robin (Erithacus rubecula), CRY4 has recently been proposed to be relevant for magnetic field sensing. Kimø et al. (2018) reported that the ISCA1 complex and CRY4 were capable of binding; however, the peculiarities of this binding argue strongly against ISCA1 as relevant for magnetoreception. In the fruit fly, CRY plays a light-independent role as “assembling” protein in the rhabdomeres of the compound eyes (Schlichting et al. 2018). Schleicher et al. (2017) demonstrated that photo-induced electron transfer reactions in Drosophila melanogaster cryptochrome were indeed influenced by magnetic fields of a few millitesla. Günther et al. (2018) sequenced night-migratory European robin (Erithacus rubecula) Cry4 from the retina and predicted the currently unresolved structure of the erCry4 protein, which suggested that erCry4 should bind Flavin. They also found that Cry1a, Cry1b, and Cry2 mRNA displayed robust circadian oscillation patterns, whereas Cry4 showed only a weak circadian oscillation. CRYs are sensing magnetic fields in insects as well as in humans. Nohr et al. (2017) presented compelling evidence for an extended electron transfer cascade in the Drosophila cryptochrome and identified W394 as a key residue for flavin photoreduction and formation of a spin-correlated radical pair with a sufficient lifetime for high-sensitivity magnetic field sensing. Xu et al. (2021) found that the photochemistry of cryptochrome 4 (CRY4) from the night-migratory European robin (Erithacus rubecula) was magnetically sensitive in vitro, and more so than CRY4 from two non-migratory bird species, chicken (Gallus gallus) and pigeon (Columba livia). Site-specific mutations of ErCRY4 revealed the roles of four successive flavin-tryptophan radical pairs in generating magnetic field effects and in stabilizing potential signaling states in a way that could enable sensing and signaling functions to be independently optimized in night-migratory birds. Wan et al. (2021) reported that monarchs responded to a reversal of the inclination of the Earth’s magnetic field in an UV-A/blue light and CRY1, but not CRY2, dependent manner, and further demonstrated that both antennae and eyes, which expressed CRY1, were magnetosensory organs.
7.5 Conclusion and Perspectives
SMFs are constant fields, which do not change in intensity or direction over time. There are four SMF parameters relevant for the interaction with a biological system: target tissue(s), magnet characteristics, magnet support device, and dosing regimen. Although the interaction of SMFs with living organisms is a rapidly growing field of investigation, many inconsistencies and seemingly contradictory observations exist. These inconsistencies in the literature are linked to the lack of appropriate systematic approaches to isolate the bioeffects of the treatment relative to other factors including geomagnetic field, the use of different exposure systems, different biological model systems, and the lack of uniformity in culture conditions.
With rapid development of superconducting technology, the magnetic flux density of SMFs used for medical and academic research purposes has steadily increased. Exposure to several Tesla (T) or higher from magnetic resonance imaging (MRI) and magnetic resonance spectroscopy (MRS) instruments has become common in pursuit of higher resolution and sensitivity, and human and animal studies have been performed at up to 9.4 and 21.1 T, respectively. In the meanwhile, strong SMFs may also be generated by thermonuclear reactors, magnetohydrodynamic systems, and superconducting generators. The facilities equipped with bubble chambers, particle accelerators, superconducting spectrometers, and isotope devices with high magnetic flux density separation units may have areas around these. However, data on living organisms from exposure to strong SMFs have not been sufficient to evaluate these potential ecosystem risks and explore the function of magnetoreception.
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Yang, B., Cheng, L., Liu, Z., Zhao, Y., Xu, A. (2023). Impact of SMFs on Microorganisms, Plants, and Animals. In: Zhang, X. (eds) Biological Effects of Static Magnetic Fields. Springer, Singapore. https://doi.org/10.1007/978-981-19-8869-1_7
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