A highly reflective biogenic photonic material from core–shell birefringent nanoparticles

Abstract

Spectacular natural optical phenomena are produced by highly reflective assemblies of organic crystals. Here we show how the tapetum reflector in a shrimp eye is constructed from arrays of spherical isoxanthopterin nanoparticles and relate the particle properties to their optical function. The nanoparticles are composed of single-crystal isoxanthopterin nanoplates arranged in concentric lamellae around a hollow core. The spherulitic birefringence of the nanoparticles, which originates from the radial alignment of the plates, results in a significant enhancement of the back-scattering. This enables the organism to maximize the reflectivity of the ultrathin tapetum, which functions to increase the eye’s sensitivity and preserve visual acuity. The particle size, core/shell ratio and packing are also controlled to optimize the intensity and spectral properties of the tapetum back-scattering. This system offers inspiration for the design of photonic crystals constructed from spherically symmetric birefringent particles for use in ultrathin reflectors and as non-iridescent pigments.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Schematic of the eye and in situ images of isoxanthopterin nanoparticles.
Fig. 2: The structural properties of the nanoparticles.
Fig. 3: Close-packing of isoxanthopterin nanoparticles into compartments and their arrangement within the retina.
Fig. 4: The microstructure and optical properties of the tapetum.
Fig. 5: Scattering from isolated nanoparticles.
Fig. 6: Reflectivity from arrays of nanospheres.

Data availability

The data that support the findings of this study are available from the corresponding authors upon reasonable request.

References

  1. 1.

    Kinoshita, S., Yoshioka, S. & Miyazaki, J. The physics of structural colors. Rep. Prog. Phys.71, 2–30 (2008).

    Google Scholar 

  2. 2.

    Parker, A. R. 515 million years of structural colour. J. Opt. A2, R15 (2000).

    Google Scholar 

  3. 3.

    Vukusic, P. & Sambles, J. R. Photonic structures in biology. Nature424, 852–855 (2003).

    CAS  Google Scholar 

  4. 4.

    Ling, L. et al. A highly conspicuous mineralized composite photonic architecture in the translucent shell of the blue-rayed limpet. Nat. Commun.6, 6322 (2015).

    Google Scholar 

  5. 5.

    Noh, H. et al. How noniridescent colors are generated by quasi-ordered structures of bird feathers. Adv. Mater.22, 2871–2880 (2010).

    CAS  Google Scholar 

  6. 6.

    Vukusic, P., Hallam, B. & Noyles, J. Brilliant whiteness in ultrathin beetle scales. Science315, 348 (2007).

    CAS  Google Scholar 

  7. 7.

    Vignolini, S. et al. Pointillist structural color in Pollia fruit. Proc. Natl Acad. Sci. USA109, 15712–15715 (2012).

    CAS  Google Scholar 

  8. 8.

    Harun-Ur-Rashid, M. et al. Angle-independent structural color in colloidal amorphous arrays. ChemPhysChem11, 579–583 (2010).

    CAS  Google Scholar 

  9. 9.

    Forster, J. D. et al. Biomimetic isotropic nanostructures for structural coloration. Adv. Mater.22, 2939–2944 (2010).

    CAS  Google Scholar 

  10. 10.

    Saranathan, V. et al. Structure and optical function of amorphous photonic nanostructures from avian feather barbs: a comparative small angle X-ray scattering (SAXS) analysis of 230 bird species. J. R. Soc. Interface9, 2563–2580 (2012).

    Google Scholar 

  11. 11.

    Burresi, M. et al. Bright-white beetle scales optimise multiple scattering of light. Sci. Rep.4, 6075 (2014).

    CAS  Google Scholar 

  12. 12.

    Mäthger, L. M. et al. Bright white scattering from protein spheres in color changing, flexible cuttlefish skin. Adv. Func. Mater.23, 3980–3989 (2013).

    Google Scholar 

  13. 13.

    Denton, E. J. & Land, M. F. Mechanism of reflexion in silvery layers of fish and cephalopods. Proc. R. Soc. Lond. B178, 43–61 (1971).

    CAS  Google Scholar 

  14. 14.

    Gur, D., Palmer, B. A., Weiner, S. & Addadi, L. Light manipulation by guanine crystals in organisms: biogenic scatterers, mirrors, multilayer reflectors and photonic crystals. Adv. Func. Mater.27, 1603514 (2017).

    Google Scholar 

  15. 15.

    Jordan, T. M., Partridge, J. C. & Roberts, N. W. Non-polarizing broadband multilayer reflectors in fish. Nat. Photon.6, 759–763 (2012).

    CAS  Google Scholar 

  16. 16.

    Gur, D. et al. The mechanism of color change in the neon tetra fish: a light-induced tunable photonic crystal array. Angew. Chem. Int. Ed.54, 12426–12430 (2015).

    CAS  Google Scholar 

  17. 17.

    Gur, D. et al. Structural basis for the brilliant colors of the Sapphirinid copepods. J. Am. Chem. Soc.137, 8408–8411 (2015).

    CAS  Google Scholar 

  18. 18.

    Teyssier, J., Saenko, S. V., van der Marel, D. & Milinkovitch, M. C. Photonic crystals cause active colour change in chameleons. Nat. Commun.6, 6368–6375 (2015).

    CAS  Google Scholar 

  19. 19.

    Palmer, B. A. et al. The image-forming mirror in the eye of the scallop. Science358, 1172–1175 (2017).

    CAS  Google Scholar 

  20. 20.

    Palmer, B. A., Gur, D., Weiner, S., Addadi, L. & Oron, D. The organic crystalline materials of vision: structure–function considerations from the nanometer to the millimeter scale. Adv. Mater.30, 1800006 (2018).

    Google Scholar 

  21. 21.

    Hirsch, A. et al. Biologically controlled morphology and twinning in guanine crystals. Angew. Chem. Int. Ed.56, 9420–9424 (2017).

    CAS  Google Scholar 

  22. 22.

    Hirsch, A. et al. ‘Guanigma’: the revised structure of biogenic anhydrous guanine. Chem. Mat.27, 8289–8297 (2015).

    CAS  Google Scholar 

  23. 23.

    Huxley, A. F. High-power interference microscope. J. Physiol. (Lond.)125, 11–13 (1954).

    CAS  Google Scholar 

  24. 24.

    Bohm, A. & Pass, G. The ocelli of Archaeognatha (Hexapoda): functional morphology, pigment migration and chemical nature of the reflective tapetum. J. Exp. Biol.219, 3039–3048 (2016).

    Google Scholar 

  25. 25.

    Pirie, A. Crystals of riboflavin making up the tapetum lucidum in the eye of a lemur. Nature183, 985–986 (1959).

    CAS  Google Scholar 

  26. 26.

    Caveney, S. Cuticle reflectivity and optical activity in scarab beetles: the role of uric acid. Proc. R. Soc. Lond. B201, 179–189 (1971).

    Google Scholar 

  27. 27.

    Palmer, B. A. et al. Optically functional isoxanthopterin crystals in the mirrored eyes of decapod crustaceans. Proc. Natl Acad. Sci. USA115, 2299–2304 (2018).

    CAS  Google Scholar 

  28. 28.

    Vogt, K. Zur Optik des Flusskrebsauges. Z. Naturforsch.30c, 691 (1975).

    Google Scholar 

  29. 29.

    Hirsch, A. et al. Structure and morphology of light-reflecting synthetic and biogenic polymorphs of isoxanthopterin: a comparison. Chem. Mater.31, 4479–4489 (2019).

    CAS  Google Scholar 

  30. 30.

    Roth, J. & Dignam, M. J. Scattering and extinction cross sections for a spherical particle coated with an oriented molecular layer. J. Opt. Soc. Am.63, 308–311 (1973).

    Google Scholar 

  31. 31.

    Hahn, D. K. & Aragón, S. R. MIE scattering from anisotropic thick spherical shells. J. Chem. Phys.101, 8409–8417 (1994).

    CAS  Google Scholar 

  32. 32.

    Qiu, C. W., Gao, L., Joannopoulos, J. D. & Soljačić, M. Light scattering from anisotropic particles: propagation, localization, and nonlinearity. Laser Photonics Rev.4, 268–282 (2010).

    CAS  Google Scholar 

  33. 33.

    Bohren, C. F. & Huffman, D. R. Absorption and Scattering of Light by Small Particles (John Wiley & Sons, 2008).

  34. 34.

    Joannopoulos, J. D., Johnson, S. G., Winn, J. N. & Meade, R. D. Photonic Crystals: Molding the Flow of Light 2nd edn (Princeton Univ. Press, 2011).

  35. 35.

    Schroden, R. C., Al-Daous, M., Blanford, C. F. & Stein, A. Optical properties of inverse opal photonic crystals. Chem. Mater.15, 3305–3315 (2002).

    Google Scholar 

  36. 36.

    Naraghi, R. R., Sukhov, S. & Dogariu, A. Directional control of scattering by all-dielectric core–shell spheres. Opt. Lett.40, 585–588 (2015).

    Google Scholar 

  37. 37.

    Balestreri, A., Andreani, L. C. & Agio, M. Optical properties and diffraction effects in opal photonic crystals. Phys. Rev. E74, 036603 (2006).

    Google Scholar 

  38. 38.

    Astratov, V. N. et al. Interplay of order and disorder in the optical properties of opal photonic crystals. Phys. Rev. B66, 13 (2002).

    Google Scholar 

  39. 39.

    Yallapragada, V. J. & Oron, D. Optical properties of spherulite opals. Opt. Lett.44, 5860–5863 (2019).

    Google Scholar 

  40. 40.

    Warrant, E. J. & McIntyre, P. D. Strategies for retinal design in arthropod eyes of low F-number. J. Comp. Physiol. A168, 499–512 (1991).

    Google Scholar 

  41. 41.

    Bryceson, K. P. & McIntyre, P. Image quality and acceptance angle in a reflecting superposition eye. J. Comp. Physiol. A151, 367–380 (1983).

    Google Scholar 

  42. 42.

    Holthuis, L. B. Shrimps and Prawns of the World. An Annotated Catalogue of Species of Interest to Fisheries Vol. 1 (FAO, 1980).

  43. 43.

    Matsuda, K. & Wilder, M. N. Difference in light perception capability and spectral response between juveniles and sub-adults of the whiteleg shrimp Litopenaeus vannamei as determined by electroretinogram. Fish. Sci.76, 633–641 (2010).

    CAS  Google Scholar 

  44. 44.

    Zabel, I. H. H. & Stroud, D. Photonic band structures of optically anisotropic periodic arrays. Phys. Rev. B48, 5004–5012 (1993).

    CAS  Google Scholar 

  45. 45.

    Zhi-Yuan, L., Wang, J. & Gu, B.-Y. Creation of partial band gaps in anisotropic photonic-band-gap structures. Phys. Rev. B58, 3721–3729 (1998).

    Google Scholar 

  46. 46.

    Park, J. et al. Full-spectrum photonic pigments with non-iridescent structural colors through colloidal assembly. Angew. Chem. Int. Ed.53, 2899–2903 (2014).

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Israel Science Foundation Grants 354/18 and 583/17, the Crown Center of Photonics and the ICORE: The Israeli Center of Research Excellence ‘Circle of Light.’ L.A. is the incumbent of the Dorothy and Patrick Gorman Professorial Chair of Biological Ultrastructure. D.O. is the incumbent of the Harry Weinrebe Professorial Chair of laser physics. B.A.P. is the recipient of the 2019 Azrieli Faculty Fellowship.

Author information

Affiliations

Authors

Contributions

B.A.P., S.W., L.A. and D.O. designed and directed the study. V.J.Y. carried out the scattering and reflectivity calculations and performed reflectivity measurements. N.S. and E.M.W. prepared the samples for cryo-SEM and TEM, and performed image analysis and optical microscopy measurements. B.A.P. performed cryo-SEM and optical microscopy measurements. N.E. performed the TEM measurements and TEM tomography analysis. A.S. and E.D.A. provided the specimens and knowledge of shrimp biology. B.A.P., V.J.Y., S.W., L.A. and D.O. wrote the manuscript with contributions from all the authors.

Corresponding authors

Correspondence to Benjamin A. Palmer or Dan Oron.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–5, Materials and Methods and refs. 1–7.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Palmer, B.A., Yallapragada, V.J., Schiffmann, N. et al. A highly reflective biogenic photonic material from core–shell birefringent nanoparticles. Nat. Nanotechnol. 15, 138–144 (2020). https://doi.org/10.1038/s41565-019-0609-5

Download citation

Further reading

Search

Find nanotechnology articles, nanomaterial data and patents all in one place. Visit Nano by Nature Research