Optically-Functional Organic Bio-Crystals
Many optical phenomena in organisms are produced by the interaction of light with assemblies of highly reflective organic crystals. However, despite their widespread distribution in animals little is known about the structure and properties of these materials. Now, the study of biologically-formed organic crystalline materials (‘Organic Biomineralization’) is emerging as an exciting new discipline alongside the parent field of Biomineralization.
It is well-established that high refractive index guanine crystals produce iridescent structural colors in animals such as fish, spiders and crustaceans. Crystalline guanine is also utilized to construct mirrors in animal eyes used for image-formation (Fig. 1) and enhancing photon-capture (Fig. 2). A common motif for guanine-based reflectors is that of multilayer stacks of plate-like crystals interspersed with cytoplasm in the form a Bragg reflector. Reflectivity is produced by constructive interference of light reflected from the high/low refractive index interfaces.
Fig 1. (Upper) Photograph of the eyes of the scallop P. maximus courtesy of Prof. Dan-Eric Nilsson, Lund University. (Lower) Cryo-SEM micrograph of the image-forming mirror in the eye of a scallop, composed of a tesselated network of square guanine crystal-tiles. (from Palmer et. al., Science 2017, 358, 1172-1175.)
Fig 2. (A) X-ray CT micrograph of a shrimp eye. (B) Cryo-SEM image of assemblies of densely-packed isoxanthopterin crystalline nanoparticles surrounding the retina. (C) High-magnification cryo-SEM images of the core-shell polycrystalline nanoparticles. (from Palmer et. al., Nat. Nano., 2020, https://doi.org/10.1038/s41565-019-0609-5)
To date guanine crystals have been found in at least 7 animal and plant phyla. However, aside from guanine, few other functional biogenic organic crystals have been reported, and those that have been are often poorly characterized (Fig. 3). In recent years, two 'new' biogenic crystals, isoxanthopterin and 7,8-dihydroxanthopterin were reported in reflective structures in the eyes of shrimp and fish. These molecules belong to the pteridine family, which previously were thought to act exclusively as absorbing pigments in nature. These findings, together with other evidence in the literature suggest that there are many more organic bio-crystals 'out there' to be discovered.
Fig 3. The currently-identified organic crystal components of biological reflectors and their molecular structures.
This part of the group studies the materials chemistry of unexplored photonic structures in animals, where the identity and properties of the underlying optical materials are not known. We use in situ synchrotron X-ray diffraction, electron diffraction and electron microscopy to characterize the structural and optical properties (e.g., crystal structure, crystal habit) of the component materials in these systems. By coupling this information with optical calculations and measurements (e.g., refractive index and reflectivity) carried out in collaboration with Prof. Dan Oron, Weizmann Institute of Science, we can rationalize the amazing optical properties of these biological photonic systems.
As well as being of fundamental interest, biogenic organic crystalline materials have the potential to inspire a new generation of bio-inspired and bio-friendly organic optical materials such as non-fading pigments, photonic paints and digital display materials.
Biological Crystallization Mechanisms
By controlling the structure, morphology (Fig. 4) and organization of organic crystals, animals produce a raft of different optical 'devices' including broadband and narrowband reflectors, diffuse scatterers, tunable photonic crystals, and image‐forming mirrors.
Fig. 4. Biogenic organic crystals formed by different organisms with radically different habits. (A) Plate-like hexagonal guanine from a copepod crustacean (from Hirsch et. al., Angew. Chem. 2017, 56, 9420-9424) (B) Asymmetric hexagonal guanine crystals from fish. (C) Prismatic guanine crystals from the cuticle of L. pallidus (courtesy of Prof. Lia Addadi, Weizmann Institute). (D) Square platelet guanine crysals from the eye of the Pecten scallop. (from Palmer et. al., Science 2017, 358, 1172-1175) (E) Core-shell spherical nanoparticles of crystalline isoxanthopterin. Each particle is constructed from an assembly of single crystal plates arranged in concentric lamellae around an aqueous core. (from Palmer et. al., Nat. Nano., 2020, https://doi.org/10.1038/s41565-019-0609-5 (F) Prismatic guanine crystals from the spider L. pallidus (from Levy-Lior et. al., Adv. Funct. Mater., 2010, 20, 320–329).
A key question is: how do organisms so exquisitely control the crystallization of the component organic molecules? We aim to unveil biology’s crystallization tricks which are far superior to state of the art methods in solid state chemistry. To explore this question, we follow crystal formation processes in a range of model organisms undergoing development or regeneration. We study changes in crystal morphology and organization using cryogenic electron microscopy techniques, observing the biological tissues in their fully-hydrated, native state. In situ diffraction and spectroscopic tools are used to determine changes in the physical and chemical properties of the crystals during growth. Information from these approaches are then synthesized to gain insights on biological crystallization mechanisms. Our ultimate objective is to understand the underlying biological control behind these crystallization processes. Thus, we utilize genetic molecules to correlate gene expression with specific crystallization events during formation. We aim to reveal the key proteins and enzymes involved in initiating nucleation and directing crystal growth.
Bio-inspired Optical Materials
A major challenge in the field of organic materials is to be able to control the structural properties of the component crystalline materials such as crystal habit, polymorph and crystal coherence-length. These parameters often dictate the efficiency of organic electronic and opto-electronic materials. Could biology’s crystallization strategies be applied or mimicked to control the formation of non-natural organic materials? One of the long-term objectives of the group is to apply nature’s crystallization tricks to make novel optical materials which have superior properties to those formed biologically. These strategies include confined-space crystallization, using dopants to control crystal habit and lipid-based templates for controlling nucleation sites and crystal growth directions. Our intention is to be genuinely biology-led, so before this applied work starts in earnest, we must first obtain a much deeper understanding of biologically-controlled crystallization pathways!