Bio-Inspired Photonics Comes Full Circle

VALERIE C. COFFEY, SCIENCE WRITER, stellaredit@gmail.com

Nothing compares with nature’s ability to design complex biological organisms and structures, refined by eons of evolution. Natural design has inspired scientists for centuries to try to imitate natural phenomena such as the sticky grip of a gecko, the camouflage of an octopus or the flight of a bird. Similarly, bio-inspired photonics extracts inspiration from the way organisms interact with light, applying it to photonics technology and manmade systems, perhaps using different materials, architectures or configurations.

In the early 1800s, the invention of the microscope inspired professionals and interested members of the public to purchase the tool to explore the diverse beauty of the microscopic world. As exploring aspects of the microcosm grew into a fad, the demand increased for slides mounted with tiny objects. One of the first minute targets depicted in mounted slides were beautiful arrangements of marine diatoms — the silicon exoskeletons of single-celled algae (Figure 1).

Figure 1. Intricate slide mounts featuring tiny diatoms frozen in kaleidoscopic displays were a Victorian era fad that has sparked bio-inspired photonics research today. Modern slide-mount hobbyist Klaus Kemp created this rosette of diatoms, photographed with a dark ground technique (a). Over 100,000 species of diatom, single-cell algae that create complex glass shells around themselves, form an astounding array of structures that when artfully arranged are only visible in a microscope (by Eduard Thum, c. 1880s) (b). Both arrangements are the size of a period in news print. Courtesy of K. Kemp/H. Lynk.

“Diatoms do an amazing thing,” said Robert Norwood, professor of optical sciences at the University of Arizona, Tucson. “They create frustules — exoskeletons out of fused silica like that in optical fiber.”

The miniature, three-dimensional glass shells are elaborate and highly variable in shape: criss-crossing bars, barrels, stars, triangles, saucers. Inspired by complex arrangements of hundreds of thousands of shapes of frustules from hundreds of thousands of species of diatoms, Norwood and his colleagues started manipulating diatoms and growing them, building on previous work that used them as lenses because of their periodic structure and curved nature.

They found that by directing a broadband (400- to 1700-nm) supercontinuum laser focused to a 20-µm-diameter spot through the central valve of a frustule no bigger than 100 µm, the light is diffracted¹. Furthermore, as they changed the angle of incidence of the beam, they found that the photonic bandgap wavelengths are directly correlated to the periodicity of the pore pattern in the valve. In other words, the diatom acted like a tunable filter (Figure 2).

Figure 2. A supercontinuum laser shines a single circular white spot approximately 20 µm in size with a clear beam path (a). The laser shines through the hexagonal valve (130 µm in diameter) of a single diatom frustule, exhibiting diffraction and hexagonal scattering patterns. The central spot of the tightly focused optical beam changes color over a range of incidence angles, acting like a tunable filter with potential in metrology and optical biosensing (b, c, d). Courtesy of R. Norwood/University of Arizona.

“The interesting follow-on is that this is reproducible via genetic engineering,” Norwood said. “We can grow a micro- or nano-device tailored with a periodic pore structure like that of multiple species of diatom frustules to fit the needs of various applications.”

When working with optical biosensors, for example, the frustules can be chemically modified to bind to a specific bioprobe that can work as an antibody. These modified diatom frustules emit photoluminescence that reveal how much interaction occurs between antibody and ligand, a molecule that binds to another (usually larger) molecule. They can also be useful in lab-on-a-chip applications.

“We’ve now found a way to make diatoms be a true photonic crystal,” Norwood said.

In another study, the researchers found that the quasi-periodic structures of the light output through different frustules are unusual and unique. Mapping of their periodicity predicted how the diatoms interact with light. For example, the different periodic structures of two specific species of diatoms — Coscinodiscus wailesii and Melosira variance — preferentially diffract blue and blue-green light, respectively, making them potentially useful as inexpensive, biocompatible tunable filters or as short light guides when coupled to optical fiber.

Research is still in its early stages, but Norwood hopes the frustules could also be useful as water quality gauges, imaging contrast agents, or in enhancing numerous types of optics-based therapies. Because diatoms are cheap, abundant and biologically reproducible, the idea of using them in biomedical imaging, guiding, and light therapies is compelling.

Nature has evolved an impressive opus of biological vision systems that “see” by way of stimuli-responsive liquid and soft tissues that can generate, regenerate and dynamically reconfigure in complex ways. At the Massachusetts Institute of Technology, assistant professor Mathias Kolle at the Laboratory for Biologically Inspired Photonic Engineering, is hoping to emulate nature’s biological optics by designing new optical components using soft solids and fluids. His work is a bio-inspired perspective on a relatively new field of study called “soft photonics².”

Intrigued by the efficiency of retinas of nocturnal mammals, one of Kolle’s projects is based on the animal’s ability to retain image acuity even though they are collecting fewer photons in dark environments. The nuclei of their photoreceptors possess a unique architecture — a low refractive index shell and high index core — that works like a chain of microlenses in each rod, channeling light more efficiently toward the cell’s light-sensitive regions. With this in mind, Kolle and collaborators designed arrays of tunable microlenses that can enhance the capabilities of optical systems³ (Figure 3). The lenses, each of which measure approximately 100 µm in diameter and achieve a resolution of 3.7 µm, are made of liquid droplets of hydrocarbon and fluorocarbon.

Figure 3. White light illuminates a dust molecule through an array of liquid bi-phase droplets 100 µm in diameter that act as tunable compound microlenses (a). Four microlenses image a grid positioned above the droplets (b). Courtesy S. Nagelberg/MIT.

One useful application for these liquid lenses is as micro-imagers. Kolle hopes to build an imaging system with these lenses that allows visualization of microscopic objects in 3D with a device the size of a cellphone. Such miniaturized integral imaging devices could provide an alternative for expensive, bulky equipment, including confocal microscopes. While such microscale integral imaging devices cannot achieve the same resolution as a confocal microscope, they can offer a larger field of view and can be implemented with significantly smaller form factor at much lower cost.

“We anticipate that the ability to image in 3D with marker-free, high-throughput, miniaturized devices that rely on integral imaging and computational image reconstruction could have tremendous benefits for medical diagnostics and biological applications in health monitoring,” Kolle said, “which could be used in point-of-care diagnostics and early detection of infectious diseases, cancer and bacterial pathogens, and the diagnosis of sickle cell disease.”

Kolle and Norwood add a caveat: These bio-inspired photonics studies are in the early stages with a long path ahead for commercialization to make them scalable and inexpensive to manufacture. It’s not enough to mimic nature — scientists have to improve upon it, affordably. “The missing link in bio-inspired photonics is still to form these inventions cheaply,” Kolle said. “If anyone finds a way to cheaply recreate the beautiful scale structures in butterflies or the silicon and calcite shells of marine animals at industrial scales, it would be a great break for the field.”

At GE Global Research in Niskayuna, N.Y., principal scientist Radislav Potyrailo and his team have made great strides toward commercializing an affordable technology that was inspired by the bright-blue iridescent wings of the Morpho butterfly. The scales of the Morpho with their Christmas-tree-like 3D structure have launched numerous studies of bio-inspired designs for sensing. The intricate ridges and lamella of the scales have an open-air architecture that combines diffraction and optical interference effects, making the butterfly stand out in bright light. The researchers realized it could also facilitate detection of molecules in complex environments such as in gas or liquid monitoring — an ideal basis for bio-optical sensors with broad application in the life sciences^4,5.

For these bio-optical sensors to succeed, they must have a clear advantage over commercially available sensors. For example, using conventional photolithography and chemical etching, Potyrailo’s team fabricated nanostructures that improved the gas-sensing performance over that of natural Morpho nanostructures. The team then incorporated machine learning to reject unwanted interference such as humidity and other chemicals. These advances significantly improved the accuracy and reliability over that of existing commercial sensors.

The gas biosensor element, which the group estimates will cost less than 50 cents each, or 10× less than commercial sensors today, can detect trace concentrations of gases and volatiles important to wellness and health. Examples of such chemicals include carcinogens (benzene) and metabolic products (CO>SUB>2) in complex backgrounds. Furthermore, the new bio-inspired inorganic nanostructure material is more rugged and thermally stable compared to chitin, a common polysaccharide in the Morpho’s wing with a structure comparable to the cellulose found in plant fiber.

“We’re taking things from nature and making them better than nature can,” Potyrailo said.

The sensors can detect metabolic volatile products of bacteria and cells in biomedical and biopharmaceutical applications. Potyrailo’s group is working on making the sensors practical for commercial use, including testing the sensors for many applications. This may eventually include medical diagnostics and wearable devices for monitoring the health of medical patients, chronically ill individuals and athletes. The sensors could be used to monitor wound healing, where the sensor would provide valuable information about the specific biochemical pattern related to the numerous phases of healing, related to the type of biological organism and their concentration. Furthermore, the bio-inspired sensors can detect different chemical or biological moieties in liquids, which could have applications in flow cytometry and in vivo brain activity monitoring.

Researchers in Europe are also taking inspiration from a variety of nature’s photonic nanostructures. Silvia Vignolini, professor in the department of Chemistry of Biomaterials at the University of Cambridge in England, and an international group of colleagues are aiming to produce biocompatible composite materials for numerous applications inspired by the iridescent shells of beetles and berries^6,7.

The widespread iridescence found in the wings of butterflies and exoskeletons of insects is a structural coloration arising from optical effects in multiple layers of semitransparent materials such as chitin. Similarly, the iridescent berry hulls of Pollia condensta and Margarita nobilis are based on helicoidal cellulose structures in the cell walls.

Based on studies of these underlying structures, Vignolini and colleagues are working on perfecting the fabrication of cellulose nanocrystal (CNC) films with vivid metallic appearances. The aqueous suspensions of these CNC films are tough, cohesive and can be applied to almost any surface, or mixed into substances to create iridescence and other optical effects.

Using steered self-assembly, Vignolini’s team created chiral structures in the CNCs so they reflect circularly polarized light. Controlling the surface design in other ways also enables the possibility of flexible tuning via the spacing of features, phase of reflectance and other optical response properties. The films are also biocompatible, edible and biodegradable, as well as low cost and scalable.

While the research is still ongoing, the CNC films could be used for aesthetic effect in food and cosmetics, and even in tissue engineering, where their mechanical properties and aesthetics could give skin a more lifelike appearance.

Beyond the aesthetic, the strong sensitivity of the films to very slight changes in scale or shape makes them good candidates for biomolecular sensors. For example, because the underlying nanostructure defines the reflected color, the iridescent films could be designed to structurally swell in response to an external stimulus, enabling them to potentially replace expensive environmentally hazardous molecular biosensors with cheap, biodegradable ones.

While the research is still in early stages, the group is working on scaling up in fabrication to attract commercial partners. “We’re really excited about developing new bio-inspired structures,” Vignolini said. “It’s fitting that technology inspired by nature can come full circle to enhance our lives.”

References

1. K. Kieu et al. (June 2014). Structure-based optical filtering by the silica microshell of the centric marine diatom Coscinodiscus wailesii. Opt Expr, Vol. 22, No. 13, p. 15992 (DOI:10.1364/OE.22.015992).

2. M. Kolle and S. Lee (Oct. 2017). Progress and opportunities in soft photonics and biologically inspired optics. Adv Mater, 1702669 (DOI.org/10.1002/adma.201702669).

3. S. Nagelberg et al. (March 2017). Reconfigurable and responsive droplet-based compound micro-lenses. Nat Comm, Vol. 8, 14673 (DOI: 10.1038/ncomms14673).

4. R.A. Potyrailo et al. (Sept. 2015). Towards outperforming conventional sensor arrays with fabricated individual photonic vapour sensors inspired by Morpho butterflies. Nat Comm, Vol. 6, No. 7959 (DOI:10.1038/ncomms8959).

5. R.A. Potyrailo (Aug. 2017). Toward high value sensing: Monolayer-protected metal nanoparticles in multivariable gas and vapor sensors. Chem Soc Rev, Vol. 46, No. 17, pp. 5311-5346 (DOI: 10.1039/C7CS00007C).

6. G. Guidetti et al. (Dec. 2016). Flexible photonic cellulose nanocrystal films. Adv Mater, Vol. 28, No 45, pp. 10042-10047 (DOI: 10.1002/adma.201603386).

7. S. Vignolini et al. (Nov. 2016). Structural colour from helicoidal cell-wall architecture in fruits of Margaritaria nobilis. J R Soc Interface, Vol. 13, No. 20160645 (DOI: 10.1098/rsif.2016.0645).