Article pubs.acs.org/Langmuir
Light Reflection Control in Biogenic Micro-Mirror by Diamagnetic Orientation Masakazu Iwasaka*,†,‡ and Yuri Mizukawa† †
Chiba University, 1-33 Yayoicho, Inage-ku, Chiba, 263-8522, Japan Japan Science and Technology Agency, PRESTO, 4-1-8 Honcho, Kawaguchi, Saitama, 332-0012, Japan
‡
ABSTRACT: As has become known, most materials, such as proteins and DNA, show orientation under strong magnetic fields. However, the critical threshold for the magnetic field of the magnetomechanical phenomena is still unknown. We demonstrate that a thin micro-mirror from a fish scale with high reflectivity exhibits a distinct magnetic response at 100 mT. A dramatic event under a magnetic field is the decrease of light scattering from guanine crystals as well as rapid rotation against the applied magnetic field. Enhancement of light scattering intensity is also observed when the three vectors of light incidence, magnetic field, and observation are orthogonally directed. The results indicate that biogenic guanine crystals have a large diamagnetic anisotropy along the surface parallel and normal directions. The micrometer to submicrometer scale of thin biogenic plates can act as a noninvasively, magnetically controlled micro-mirror for light irradiation control in the micrometer-scale region.
1. INTRODUCTION Compared to distinct magnetisms such as paramagnetism and strong magnetism, diamagnetism is considered to have little connection to observable magnetic phenomena, although it is a kind of universal magnetic property of materials with electrons. However, diamagnetism in all materials shows a remarkable behavior under strong static magnetic fields of Tesla order1−10 because the magnetic energy of the weak magnetism becomes comparable to the thermal energy at room temperature in a diamagnetic material of large size with aligned diamagnetic moments in molecular orbits. Past studies on magnetic orientations of macromolecules, which are made of amino acids, nucleic acids, lipids, and so forth, revealed that fibers such as fibrin,1 collagen,2 and DNA3 oriented versus applied external magnetic fields of several tesla (T). The key to the quick magnetic orientation response should be a distinct anisotropy in diamagnetic susceptibility. In general, diamagnetic susceptibility is proportional to the material’s density. Therefore, we conjectured that crystallized materials may show a clear magnetic orientation even in living systems.9 The biomineralization process is a candidate for the source of high sensitivity to external magnetic fields when they have a large diamagnetic anisotropy between crystal directions. In the field of biomineralization, one of the typical living creatures sensing the Earth’s magnetic field is magnetotactic bacteria. The bacteria utilize magnetite, which shows strong magnetism.10−15 In contrast, recent topics on magnetoreception have focused on paramagnetism in electron and radical-pairs.16−22 The present study focuses on the guanine crystals in fish scales that are an organic diamagnetic material. The crystals as a condensed diamagnetic material seem to have relatively large diamagnet© XXXX American Chemical Society
ism, so the crystallized nucleic acid base with negative magnetic susceptibility can obtain enough magnetic energy for behavior like a paramagnetic material. If the organic diamagnetic crystals have distinct differences in magnetic susceptibility along their morphological axes, magnetic rotation versus the applied external magnetic field should be observable, even at room temperature. In addition, the guanine crystals as biogenic photonic crystals in fish scales have as good an ability to produce structural colors as other biogenic periodically aligned structures in organic or inorganic tissue, such as bird feathers, on the surface of living creatures.23−31 The detailed structure of guanine crystals from carp and their shining mechanism were reported.29,30 The previous works reported that the refractive index of guanine crystals was ∼1.83 and discussed the shining in fish.24−31 Interestingly, the stack of guanine crystals was found to have a nonpolarized light scattering in a recent work.31 We previously investigated the dynamic behavior of guanine crystals under static magnetic fields of up to 5 T. Remarkably, the decrease of light scattering in the guanine crystals of goldfish Carassius auratus occurred at relatively low magnetic fields, as low as 0.26 T.9 We speculated that the decrease of light scattering in the guanine crystals was correlated with the possible magnetic orientation of guanine crystals. The present study gives evidence that the guanine crystals of goldfish and their suspension show light scattering anisotropy when the crystals oriented under magnetic fields. Received: January 6, 2013 Revised: March 1, 2013
A
dx.doi.org/10.1021/la400046a | Langmuir XXXX, XXX, XXX−XXX
Langmuir
Article
2. EXPERIMENTAL SECTION 2.1. Materials. The guanine crystals in fish scales were obtained from goldfish, Carassius auratus, under anesthesia following the proposed experimental plan accepted by the bioethics committee at Chiba University to use the goldfish. The observation of goldfish’s guanine crystals under magnetic field was carried out in situ by a high amplification CCD microscope whose lens was inserted into the magnetic field exposure space in the magnet. The scales from the goldfish were collected in a 12-mL centrifuge tube (Corning 430052) and washed three or four times with distilled water. The number of scales in the tube was between about 20 and 50 pieces. Pipetting with a 3-mL pipet (BD Falcon, 357575) separated the scales and contaminated skin. After the scales sank to the bottom of the tube, the supernatant was removed. This cleaning process was repeated three or four times. Next, 1 to 2 mL of distilled water was added to the scale sediment. We poked the scale sediment with a bamboo skewer for 10 min until the chromatophore (iridophore) and guanine crystals detached from the scales, when the scales became relatively transparent. Then the tube was set in a centrifuge (Hitachi co Ltd., Himac-CT4), and right after centrifugation for 5 s at 1500 rpm, the supernatant suspension that contained condensed guanine crystals was moved to a brand-new centrifuge tube of the same type. This guanine condensation treatment was performed two times for the same scales, and about 3 mL of condensed guanine suspension was obtained. The magnetic response experiments were carried out while the guanine suspension was fresh and under a low bacterial concentration. As a result, the above-mentioned preparation protocols allowed the guanine suspension consisting of both guanine crystal’s stacks and individual guanine crystal crystals, and cellular elements of choromatophore cells, such as residual lipid membranes. 2.2. Methods. Figure 1 shows the experimental configurations of the sample cell, camera, light source, and the direction of observation. The collected guanine crystals were contained in a closed thin glass chamber, and guanine crystals were placed statically and horizontally at the bottom before being exposed to magnetic fields in the vertical direction in the cases with microscope of 500× to 2000× magnifications, as shown in Figure 1A. Two kinds of CCD microscopes (Keyence VH-5000 and VHX2000) were utilized. The utilized light source was a halogen lamp which provided a continuous light. The macroscopic view of the aqueous suspension containing the floating guanine crystals was obtained by a low amplification CCD camera (ELMO Co. Ltd., CC421). A chamber with a 25 μL capacity (frame seal chamber; BIO-RAD SLF-0201) was utilized in experiments with a high-amplification microscope. On the other hand, a cylindrical glass tube was used as the container for the suspension of the guanine crystals in low-amplification CCD observation (Figure 1B). The magnetic field generator for this study was a superconducting magnet (Oxford Ltd., 5Tr90) with a maximum field of 5 T. The inner surface of the cylindrical bore was covered with a water-circulating jacket for temperature stabilization at 23 °C. In this space, the sample chamber containing the guanine crystals was set in front of the lens of a CCD microscope (Figure 1A and B). The rate of the magnetic field changing in the superconducting magnets was 1000 mT/min. An additional measurement of scattered light in the same configuration as Figure 1A was carried out in the fiberoptic measurement system, as shown in Figure 1C. In the case of the fiberoptic measurement, a superconducting magnet with a horizontal bore (Oxford Ltd., 14Tr70) was utilized. In the case of the X-ray diffraction pattern measurements, the condensed guanine crystal suspension was centrifuged again at 2000 rpm for 5 min, and after removing the supernatant solution, about 300 mL of acetone was added to the sedimentation. The collected guanine containing paste was dried by a heater and then kept in a desiccator for more than 3 h, and the X-ray diffraction measurements were carried out on both the flakes of crystals and powders which were ground in mortar. The diffraction patterns of goldfish guanine crystals were measured by utilizing a powder diffractometer (D8 Advance, Buruker). The detailed parameters for the X-ray diffraction measurements were
Figure 1. Experimental configurations of the sample cell, camera, light source, and the direction of observation. (A) Configuration for highamplification microscope observation for “light scattering inhibition” with a cylindrical type of CCD microscope (Keyence, VH-5000 with VHS501 lens). (B) Configuration for low-amplification CCD microscope in the cases with “light scattering enhancement” where the vectors of three parameters were orthogonal to each other. (C) Configuration for measurement of scattered light in the same configuration as (A). as follows: range of 2θ, 5−55°; exposure time, 4 s; capture step, 0.02°; divergence slit, 0.3°; generator voltage, 40 kV.
3. RESULTS AND DISCUSSION Figure 2 shows a case where the direction of the magnetic is parallel to the observation, and the light incidence comes from the side. The guanine crystals were twinkling frequently because of Brownian motion, and they darkened as shown in Figure 2A after being set in a magnetic field of more than 100 mT. Most of the twinkling guanine crystals darkened after being set in a magnetic field of 200 mT for 10 s. Bright field observation of the guanine crystals with and without magnetic fields provided us with information, as shown B
dx.doi.org/10.1021/la400046a | Langmuir XXXX, XXX, XXX−XXX
Langmuir
Article
Figure 2. Magnetically induced inhibition of light scattering in guanine crystals. (A) Time course of light scattering inhibition of guanine crystals during a magnetic field sweep up to 200 mT. The images were obtained under dark field illumination. Bar, 20 μm. The ⊗ symbol represents the direction of the applied magnetic field. (B) Bright field images of guanine crystals with and without the magnetic field of 200 mT. Bar (black), 20 μm. Light incidences were added from both the front and side. The white matter is the scattered light of the guanine crystals from the side. (C) Diamagnetically induced rotation of a guanine crystal around its b-axis or length of the (102) plane. Bar, 5 μm. (D) Change in the width of the observed shape of a guanine crystal during the magnetic field increment from 0 to 500 mT (n = 14). The rate of magnetic field change was 1000 mT per minute. Each of the black lines shows an individual rotation, and the red line is their average. In the inset-bar, b means the width of the (102) plane, and θ is the angle between the width of the (102) plane and horizontal plane. The width of the observed shape of a guanine crystal corresponds to b cos θ. MF, magnetic fields. (E) Light scattering inhibition in guanine crystals immediately after being set in constant magnetic fields of 50, 100, and 200 mT (n = 8 per group). The mean value of a count every 3 s and the ± standard deviation are shown. The number of shining guanine crystals with a length of more than 10 μm was counted in the observed area of 610 μm × 460 μm. (F) Time courses of scattered light intensity in the suspension containing guanine crystals. The light incidence direction was perpendicular to both the magnetic field and the observation (detection). The vertical axis shows the relative change in the normalized light intensity since the magnetic field was turned on. The intensity at the turning on was set to 100% and the relative change was calculated. The data of 0 mT were obtained by a random sampling.
in Figure 2B, about the correlation between the magnetic orientation of guanine crystals and their light-scattering properties when the guanine crystals were exposed to light from both the front and side directions. In addition, utilizing a high-resolution optical microscope lens, real-time observation of the guanine crystals as the magnetic field changed revealed that the guanine crystals oriented their (102) planes parallel to the applied magnetic field (Figure 2C, D). It also showed that the light scattering decrease in the guanine crystals was caused by the rotation of a majority of the crystals, which was due to induced diamagnetic moments in the guanine crystal structure.32,33 In the photos in Figure 2C, decreases were observed in the width of the white object under magnetic fields of 400 to 501 mT. This
phenomenon means that the guanine crystals stood by directing its (102) planes to the applied magnetic field direction, which was parallel to Earth’s gravity, and the width of the white object decreased as shown in Figure 2D. The averaged data (red line) in Figure 2D shows a threshold of between 200 and 300 mT for the magnetic orientation of the guanine crystals. The behavior is consistent with the previous finding that the minimum magnetic field for obtaining light scattering inhibition in goldfish guanine crystal arrays is 260 mT.9 The new finding in the present study is a response over a long period to a magnetic field. The magnetic orientation of the guanine crystals apparently occurred when the magnetic field was kept steady at 100 mT, which is the minimum threshold for C
dx.doi.org/10.1021/la400046a | Langmuir XXXX, XXX, XXX−XXX
Langmuir
Article
crystals.29 However, the appeared peaks of the (110) plane on the left side of Figure 3A suggested that the utilized goldfish guanine crystals accompanied monohydrated crystals. A recently reported paper shows that the anhydrous guanine crystals from Japanese carp are adjacent to an amorphous region containing monohydrated guanine crystals.36 Possibly the goldfish guanine crystals are speculated to have a similar structure, having contact with monohydrated guanine crystals. In this study’s experiments, the prepared guanine crystals from goldfish seem to keep the stack with cytoplasm spacing because an optical microscopy observation of the thickness of guanine crystals revealed that the thickness was approximately 500− 1000 nm. The SEM image in Figure 4 provides evidence that there were very thin guanine crystal plates. The gauzy plates in Figure
detecting the magnetic orientation of goldfish guanine crystals. The shining guanine crystals gradually darkened within 10 s in a magnetic field ranging from 100 to 200 mT, as shown in Figure 2E. This finding was confirmed by measuring the scattered light from the suspension of floating guanine crystals (Figure 2F). The arrangement of magnetic field, light irradiation and observation was the same as Figure 2E. The scattered light intensity was continuously measured from the direction of observation, and the results show that the scattered light clearly decreased under magnetic fields at 100 mT, while no significant change occurred at 0−50 mT (Figure 2F). We carried out X-ray powder diffraction pattern measurements on our samples of goldfish, as shown in Figure 3, and compared them to previously reported data of both anhydrous34 and monohydrated guanine crystals.35 The X-ray diffraction patterns of goldfish guanine crystals resembled to the diffraction pattern of anhydrous guanine crystals in Japanese carp,29,30 particularly having the same peak of the (012) plane which appeared only in the data of anhydrous
Figure 4. SEM images of guanine crystals. (A) Two accumulated guanine crystals with very thin thicknesses. (B) Overlapping multilamellar layers of guanine crystals. (C) Defects on the surfaces of the crystal.
4A were so thin that it looked nearly transparent for the irradiated electron beam. The guanine crystals, derived from goldfish scales, have smooth planes, partially forming defects, localized terraces, or holes (Figure 4B,C). According to previous works,29,30 the broadest surface of the plates corresponds to the (102) plane of the guanine crystal. One of the edges in the plate shown in Figure 4B has a saw-like structure, which was formed by many overlapping thin plates. Recognizable in the photograph shown in Figure 4B, stacked guanine crystal plates had been found at the edge. The mechanism of the magnetic orientation of the biogenic guanine crystals is explained as follows. The applied external magnetic field induces a maximum diamagnetic moment in the normal direction of the (102) plane of the guanine molecules. As a result, the guanine crystals direct their (102) plane surface parallel to the magnetic fields in order to minimize the diamagnetic moment which is perpendicular to the surface. Figure 5A illustrates a model for the magnetic orientation of guanine crystals of a goldfish scale. The ring structures in a guanine molecule induce maximum diamagnetic moments in the center of the rings. Previous studies on the molecular assembly structures of guanine have reported that guanine molecules have strong hydrogen bonds between them, and form a specific structure, such as guanine tetraplex.32,33 The
Figure 3. X-ray diffraction patterns of guanine crystals. (A) Powder diffraction pattern of the guanine crystals from goldfish. (B) Diffraction pattern of anhydrous guanine crystals in the database.34 (C) Diffraction pattern of monohydrated guanine crystals in the database.35 M, monohydrate. A, anhydrous. D
dx.doi.org/10.1021/la400046a | Langmuir XXXX, XXX, XXX−XXX
Langmuir
Article
Figure 5. (A) Model for the magnetic orientation of the guanine crystals of goldfish scales. (B) Guanine crystals which were separated from the chromatophore of a goldfish and were scattered on the surface of the scale. (C) High amplification optical image of guanine crystals in an aqueous medium. Two cross-stacked guanine crystals showed dynamic structural color changes and striped patterns which were produced by the optical interference between guanine crystals. Bar, 10 μm.
Figure 6. Light-reflecting guanine crystal particles which were floating in water. The directions of three kinds of vectors (magnetic field, light incidence, and observation direction) were normal to each other. (A) Light scattering in ambient geomagnetic magnetic fields became brighter in 330 mT. Bar, 1 mm. (B) Time series of photos showing the brightening of light scattering in floating guanine crystals before, during, and after magnetic field exposure of up to 500 mT. The ⊗ symbol represents the direction of observation. B, magnetic fields. L, light incidence. Bar, 2 mm.
hydrogen-bonded guanine molecules obtained enough diamagnetic energy to align their broadest surface, the (102) plane, parallel to the external magnetic fields, while the crystals showed random orientation under no magnetic field exposure. Additionally, the biogenic guanine crystal has a relatively large reflective index of ∼1.83 and shows strong light scattering on the surface of the crystals.24−31 In the case of the goldfish scale, isolated guanine crystals shining under dark field illumination can be observed on the scale surface. The guanine crystals that are generated in the chromatophore of the goldfish show a twinkle shining, as shown in Figure 5B. Therefore, the refractivity of guanine crystals from goldfish was speculated to be ∼1.83. The photographs in Figure 5C were from an optical microscope without magnetic field exposure under dark field illumination. There were overlapping guanine crystals lying near the bottom, and they induced an iridescence by light interference. The four images in Figure 5C show two crystals changing their angle of crossing. Notably, an optical dispersion occurred in the two images on the left, which show separation of red and green colors, while the two images on the right show a stripe pattern. The multilayer structure in the guanine crystals caused the optical interference when the two crystals overlapped by crossing angles. It is possible to additionally comment that the magnetic orientation of guanine crystals can be applied to control the light interference between crystals. For the purpose of checking the relevance of the guanine crystal orientation, a suspension of the guanine crystals was observed with the magnetic field orthogonal to the observation. Figure 6A shows that the light scattering from the guanine crystals consistently floating in water became brighter under magnetic fields at 330 mT. Compared to the case with the magnetic field parallel to the observation, the condition of Figure 6A demonstrates a dramatic enhancement of light scattering in guanine crystals. The presence of disassembled cellular elements including lipid membranes increased the buoyancy of the guanine crystal arrays, and consequently, the
guanine crystals were consistently floating in the suspension. The phenomenon of brightening of guanine crystals occurred at several hundred mT, which is the same level as the magnetic fields in the cases of light scattering inhibition. In the images in Figure 6B, the floating guanine crystals were exposed to light irradiation in the horizontal direction from the right to left. The distribution of star-like twinkling patterns was uniform when the magnetic field was at the ambient geomagnetic field. In contrast, a light beam pattern formed in magnetic fields of more than 200 mT, as shown in Figure 6B. The edge of the area with bright guanine crystals and dark area outside can be clearly seen in the photos. Strong light scattering occurred in the bright region, but light was less propagated to the dark region. It looks like the scattered light from the guanine crystals did not diffuse parallel to the applied magnetic fields. The magnetically oriented guanine crystals directing their (102) planes parallel to the applied magnetic fields might exhibit an induced anisotropy in light scattering. It has been reported that the guanine crystals in fish have a distinct refractive anisotropy,28,30,31 as well as the guanine sheet on silicon.37 According to these previous reports, the light incidence to the broadest surface of crystal, i.e., the (102) plane of anhydrous guanine crystal, is refracted more strongly than the incidence normal to the plane. This study’s finding of light scattering enhancement under magnetic fields seems to be concerned with this refractive anisotropy in the guanine crystals. The magnetic orientation increased the number of crystals directing their (102) plane parallel to the magnetic field, and consequently, the scattered light reached the observer easily. The magnetic orientation allowed guanine crystals the free rotation around the b-axis, enhancing the flickering light scattering which can be explained by this rotation. In addition to the magnetic orientation, modulation of the structural colors of guanine crystals by the magnetic field was E
dx.doi.org/10.1021/la400046a | Langmuir XXXX, XXX, XXX−XXX
Langmuir
■
ACKNOWLEDGMENTS This study was supported by JST, PRESTO, “Creation of Basic Technology for Improved Bioenergy Production through Functional Analysis and Regulation of Algae and Other Aquatic Microorganisms.” We wish to acknowledge Dr. H. Masu for supporting X-ray diffraction pattern measurements. We also thank Mr. Y. Miyashita for his support in data analyses.
observed, because the oriented guanine crystals increased the chance to align their (102) plane in a parallel direction. Our previous study clarified the existence of structural color changes in guanine crystal arrays under strong magnetic fields of up to 10 T.38 The photos in Figure 6A show an enhancement of iridescence in colors under the magnetic field at 330 mT. The optical interference increment due to the light scattering enhancement produced such structural color changes. There have been other works concerning nonbiogenic monohydrated guanine crystals, which have been investigated for the purpose of exploring new electronic materials.39,40 It will be interesting to compare the magnetic responses of anhydrous and monohydrated guanine crystals in future study. Also, it should be important to check the possible role of an aqueous solution in the spacing of guanine crystal arrays on the light scattering properties, because the twinkling of light scattering stopped when the medium surrounding guanine crystals was changed from water to acetone. As mentioned in the previous report, the possible existence of a liquid crystalline state inside the guanine crystals allows a magnetic orientation inside the guanine crystal stacks.38 The recent report by Gur et al.36 shows that the guanine crystal stacks from Japanese carp have amorphous structures which reversibly absorb water. It is conjectured that the existence of water inside the guanine crystal stacks have an important role in the observed flickering light scattering. As well as the thermal agitation of water surrounding guanine crystals, the possible effects of the dynamic motion of the water in the amorphous region on the flickering light scattering must be tested in future study. The magnetic orientation of the guanine crystal occurred due to the diamagnetic rotation of the whole body of a guanine crystal stack. Clarifying the diamagnetic property of amorphous structures may bring a magnetically controlled nanoscale mirror.
■
REFERENCES
(1) Torbet, J.; Freyssinet, J. M.; Hudry-Clergeon, G. Oriented fibrin gels formed by polymerization in strong magnetic fields. Nature 1981, 289, 91−93. (2) Torbet, J.; Ronziere, M. C. Magnetic alignment of collagen during self-assembly. Biochem. J. 1984, 219, 1057−1059. (3) Torbet, J. Solution behavior of DNA studied with magnetically induced birefringence. Methods Enzymol. 1992, 211, 518−532. (4) Higashi, T.; Yamagishi, A.; Takeuchi, T.; Kawaguchi, N.; Sagawa, S.; Onishi, S.; Date, M. Orientation of erythrocytes in a strong static magnetic field. Blood 1993, 82, 1328−1334. (5) Torbet, J.; Malbouyres, M.; Builles, N.; Justin, V.; Roulet, M.; Damour, O.; Oldberg, A.; Ruggiero, F.; Hulmes, D. J. S. Orthogonal scaffold of magnetically aligned collagen lamellae for corneal stroma reconstruction. Biomaterials 2007, 28, 4268−4276. (6) Suzuki, K.; Toyota, T.; Sato, K.; Iwasaka, M.; Ueno, S.; Sugawara, T. Characteristic curved structure derived from collagen-containing tubular giant vesicles under static magnetic field. Chem. Phys. Lett. 2007, 440, 286−290. (7) Chabre, M. Diamagnetic anisotropy and orientation of α helix in frog rhodopsin and meta II intermediate. Proc. Natl. Acad. Sci. U.S.A. 1978, 75, 5471−5474. (8) Nakaoka, Y.; Takeda, R.; Shimizu, K. Orientation of Paramecium swimming in a DC magnetic field. Bioelectromagnetics 2002, 23, 607− 613. (9) Iwasaka, M. Effects of static magnetic fields on light scattering in red chromatophore of goldfish scale. J. Appl. Phys. 2010, 107, 09B314(1−3). (10) Gohain Barua, A.; Iwasaka, M.; Miyashita, Y.; Kurita, S.; Owada, N. Firefly flashing under strong static magnetic fields. Photchem. Photobiol. Sci. 2012, 11, 345−350. (11) Sakaguchi, T.; Burgess, J. G.; Matsunaga, T. Magnetite formation by a sulphate-reducing bacterium. Nature 1993, 365, 47−49. (12) Kirschvink, J. L.; Walker, M. M.; Diebel, C. E. Magnetite-based magnetoreception. Curr. Opin. Neurobiol. 2001, 11, 462−467. (13) Kirschvink, J. L.; Gould, J. L. Biogenic magnetite as a basis for magnetic field detection in animals. BioSystems 1981, 13, 181−201. (14) Matsunaga, T.; Sakaguchi, T.; Tadokoro, F. Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl. Microb. Biotechnol. 1991, 35, 651−655. (15) Blakemore, R. Magnetotactic bacteria. Science 1975, 190, 377− 379. (16) Maeda, K.; Robinson, A. J.; Henbest, K. B.; Hogben, H. J.; Biskup, T.; Ahmad, M.; Schleicher, E.; Weber, S.; Timmer, C. R.; Hore, P. J. Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 4774−4779. (17) Efimova, O.; Hore, P. J. Role of exchange and dipolar interactions in the radical pair model of the avian magnetic compass. Biophys. J. 2008, 94, 1565−1574. (18) Wiltschko, W.; Wiltschko, R. Magnetic orientation and magnetoreception in birds and other animals. J. Comp. Physiol. A 2005, 191, 675−693. (19) Wiltschko, W.; Wiltschko, R. Magnetic compass of European robins. Science 1972, 176, 62−64. (20) Ritz, T.; Adem, S.; Schulten, K. A model for photoreceptorbased magnetoreception in birds. Biophys. J. 2000, 78, 707−718. (21) Lohmann, K. J. Q&A: Animal behaviour: Magnetic-field perception. Nature 2010, 464, 11401142.
4. CONCLUSIONS In summary, this work points out that very thin biogenic guanine crystals with high optical refractivity behave like microscale mirrors, and their diamagnetic rotation modulates light scattering in micro-mirrors in a noncontact and remote control manner. In the cases of the observation parallel to magnetic field direction, the magnetic orientation of guanine crystals reduces the scattering of the light incidence from the side. The light scattering inhibition also occurs in the suspension of guanine crystals. In the cases of the observation perpendicular to magnetic field direction, a light scattering enhancement occurs in the suspension of guanine crystals when the light incidence is perpendicular to both the magnetic field and observation. The noncontact control possible with such guanine micro mirrors can be available in in situ microspectroscopy for cellular analysis.
■
Article
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Notes
The authors declare no competing financial interest. F
dx.doi.org/10.1021/la400046a | Langmuir XXXX, XXX, XXX−XXX
Langmuir
Article
(22) Maeda, K.; Henbest, K. B.; Cintolesi, F.; Kuprov, I.; Rodgers, C. T.; Liddell, P. A.; Gust, D.; Timmel, C. R.; Hore, P. J. Chemical compass model of avian magnetoreception. Nature 2008, 453, 387− 390. (23) Mason, C. W. Structural colors in insects. II. J. Phys. Chem. 1927, 31, 321−354. (24) Yoshioka, S.; Matsuhana, B.; Tanaka, S.; Inouye, Y.; Oshima, N.; Kinoshita, S. Mechanism of variable structural color in the neon tetra: quantitative evaluation of the Venetian blind model. J. R. Soc. Interface 2011, 8, 56−66. (25) Nagaishi, H.; Oshima, N.; Fujii, R. Light-reflecting properties of the iridophores of the neon tetra Paracheirodon innesi. Comp. Biochem. Physiol. 1990, 95A, 337−341. (26) Herring, P. J. Reflective systems in aquatic animals. Comp. Biochem. Physiol. 1994, 109A, 513−546. (27) Lyngsum, J. N.; Shand, J. Changes in spectral reflexions from the iridophores of the Neon tetra. J. Physiol. 1982, 325, 23−34. (28) Denton, E. J. Review Lecture: On the organization of reflecting surfaces in some marine animals. Philos. Trans. R. Soc. London, Ser. B 1970, 258, 285−313. (29) Levy-Lior, A.; Pokroy, B.; Levavi-Sivan, B.; Leiserowitz, L.; Weiner, S.; Addadi, L. Biogenic Guanine Crystals from the Skin of Fish May Be Designed to Enhance Light Reflectance. Cryst. Growth Des. 2008, 8, 507−511. (30) Levy-Lior, A.; Shimoni, E.; Schwartz, O.; Gavish-Regev, E.; Oron, D.; Oxford, G.; Weiner, S.; Addadi, L. Guanine-Based Biogenic Photonic-Crystal Arrays in Fish and Spiders. Adv. Funct. Mater. 2010, 20, 320−329. (31) Jordan, T. M.; Partridge, J. C.; Roberts, N. W. Non-polarizing broadband multilayer reflectors in fish. Nat. Photonics 2012, 260, 759− 763. (32) Laughlan, G.; Murchie, A. I. H.; Norman, D. G.; Moore, M. H.; Moody, P. C. E.; Lilley, D. M. J.; Luisi, B. The high-resolution crystal structure of a parallel-stranded guanine tetraplex. Science 1994, 265, 520−524. (33) Phillips, K.; Dauter, Z.; Murchie, A. I. H.; Lilley, D. M. J.; Luisi, B. The crystal structure of a parallel-stranded guanine tetraplex at 0.95Å resolution. J. Mol. Biol. 1997, 273, 171−182. (34) Guille, K.; Clegg, W. Anhydrous guanine: a synchrotron study. Acta Crystallogr., Sect. C 2006, 62, O515−517. (35) Thewalt, U.; Bugg, C. E.; Marsh, R. E. The crystal structure of guanine monohydrate. Acta Crystallogr., Sect. B 1971, B27, 2358−2363. (36) Gur, D.; Politi, Y.; Sivan, B.; Fratzl, P.; Weiner, S.; Addadi, L. Guanine-based photonic crystals in fish scales form from an amorphous precursor. Angew. Chem., Int. Ed. 2013, 52, 388−391. (37) Hinrichs, K.; Silaghi, S. D.; Cobet, C.; Esser, N.; Zahn, D. R. T. Ellipsometry from infrared to vacuum ultraviolet: Structural properties of thin anisotropic guanine films on silicon. Phys. Status Solidi 2005, 242, 2681−2687. (38) Iwasaka, M.; Miyashita, Y.; Kudo, M.; Kurita, S.; Owada, N. Effect of 10-T magnetic fields on structural colors in guanine crystals of fish scales. J. Appl. Phys. 2012, 111, 07B316(1−3). (39) Ortmann, F.; Hannewald, K.; Bechstedt, F. Guanine crystals: A first principles study. J. Phys. Chem. B 2008, 112, 1540−1548. (40) Otero, R.; Schö ck, M.; Molina, L. M.; Lœgsgaard, E.; Stensgaard, I.; Hammer, B.; Besenbacher, F. Guanine quartet networks stabilized by cooperative hydrogen bonds. Angew. Chem. 2005, 44, 2270−2275.
G
dx.doi.org/10.1021/la400046a | Langmuir XXXX, XXX, XXX−XXX
