Quo vadis biophotonics? Wearing serendipity and slow science as a badge of pride, and embracing biology

TL;DR

This perspective centers on the single gyroid $I4_132$ photonic network found in green butterflies and its bicontinuous relatives such as the double gyroid $Ia\overline{3}d$, highlighting how these geometries illuminate the interface between biology and materials science. It argues that despite substantial progress in characterizing optical properties and self-assembly, understanding the biological formation and evolutionary function remains limited. The author calls for embracing serendipity and slow science, and for closer collaboration with living tissue studies to address functional biology rather than purely materials-science questions. Together, these themes frame a roadmap where deeper biological insight underpins durable advances in biophotonics.

Abstract

This article is a reflection on the themes of the Faraday Discussion meeting on "Biological and bio-inspired optics" held from 20 to 22 July 2020. It is a personal perspective on the nature of this field as a broad and interdisciplinary field that has led to a sound understanding of the material properties of biological nanostructured and optical materials. The article describes how the nature of the field and the themes of the conference are reflected in particular in work on the 3D bicontinuous biophotonic nanostructures known as single gyroids and in bicontinuous structures more broadly. Such single gyroid materials are found for example in the butterfly Thecla opisena, where the questions of biophotonic response, of bio-inspired optics, of the relationship between structure and function, and of the relationship between natural and synthetic realisations are closely interlinked. This multitude of facets of research on single gyroid structures reflects the beauty of the broader field of biophotonics, namely as a field that lives through embracing the serendipitous discovery of the biophotonic marvels that nature offers to us as seeds for in-depth analysis and understanding. The meandering nature of its discoveries, and the need to accept the slowness that comes from exploration of intellectually new or foreign territory, mean that the field shares some traits with biological evolution itself. Looking into the future, I consider that a closer engagement with living tissue and with the biological questions of function and formation, rather than with the materials science of biological materials, will help ensure the continuing great success of this field.

Figures (5)

• Figure 1: The Eupholus magnificus beetle, as described by Pouya et al.Pouya:11 remains a magnificent example of photonic materials with varying degrees of order. The yellow part of the cuticle has an ordered Diamond nanostructure, whereas the blue part only shows quasi-order. Scale bars are 2 microns. (Images reproduced in adapted form from Pouya et al.Pouya:11)
• Figure 2: Optics & Photonics in Nature: The green speckled appearance of the wing-scales of Thecla opisena is due to crystallites with an internal three-dimensional nanostructure that can be modelled by the single gyroid geometry. (Data and images from the same samples and specimen as used in Wiltse1603119.)
• Figure 3: Natural and synthetic materials: The single gyroid structure has been generated both as a synthetic material and as a natural material, using a variety of different processes and covering length scales from $nm$ to $cm$. (Left) Copolymer-templated silver nanostructurewiltscircularsilver2020; (Middle) Chitin single Gyroid in the green butterfly Thecla opisenaWiltse1603119; and (right) nanofabricated single gyroid as an optical device prototype TurnerSabaZhangCummingSchroederTurkGu:2013. (Images reproduced from publications wiltscircularsilver2020Wiltse1603119TurnerSabaZhangCummingSchroederTurkGu:2013 with permission of the authors)
• Figure 4: Towards in-vivo imaging of butterfly nanostructural development: Understanding the growth mechanism of single gyroids in green butterflies will be likely achieved through a combination of advances in structural and developmental cell biology, biochemistry, materials science and nanostructural microscopy. We will have to see how the gyroid crystallites found by Wilts et al.Wiltse1603119 will relate to Helen Ghiradella's model based on membranes in the endoplasmic reticulumdoi:10.1002/jmor.1052020106 and to Tomas Landh's invagination modeldoi:10.1016/0014-5793(95)00660-2. Images reproduced in adapted form from Wilts et alWiltse1603119 (top), Landhdoi:10.1016/0014-5793(95)00660-2 (middle) and Ghiradelladoi:10.1002/jmor.1052020106 (bottom).
• Figure 5: Is the next rose the runner bean?: The runner bean Phaseolus coccineus is one of the many plants that, when grown in darkness, adopts a curious bicontinuous membrane structure in the chloroplast precursor, called the pro-lamellar body (curiously, often with the symmetry of the single diamond; that is, it is unbalanced). Nanostructural and light-related effects in plants, such as this and others, might lend themselves more easily to close collaborations between materials science, physics and biology, in particular given advances in imaging such materialsKowalewska875doi:10.1080/23818107.2019.161919510.1093/jxb/erz496. (Microscopy, photography and image composition by Lucja Kowalewska and Dainius Jakubauskas. Image adapted from Mezzenga et al.doi:10.1002/adma.201900818)