Wavelength-specific forward scattering of light by Bragg-reflective iridocytes in giant clams

Abstract

A surprising recent discovery revealed that the brightly reflective cells ('iridocytes') in the epithelia of giant clams actually send the majority of incident photons 'forward' into the tissue. While the intracellular Bragg reflectors in these cells are responsible for their colourful back reflection, Mie scattering produces the forward scattering, thus illuminating a dense population of endosymbiotic, photosynthetic microalgae. We now present a detailed micro-spectrophotometric characterization of the Bragg stacks in the iridocytes in live tissue to obtain the refractive index of the high-index layers (1.39 to 1.58, average 1.44 + 0.04), the thicknesses of the high-and low-index layers (50-150 nm), and the numbers of pairs of layers (2-11) that participate in the observed spectral reflection. Based on these measurements, we performed electromagnetic simulations to better understand the optical behaviour of the iridocytes. The results open a deeper understanding of the optical behaviour of these cells, with the counterintuitive discovery that specific combinations of iridocyte diameter and Bragg-lamellar spacing can produce back reflection of the same colour that is also scattered forward, in preference to other wavelengths that are scattered at higher angles. We find for all values of size and wavelength investigated that more than 90% of the incident energy is carried by the photons that are scattered in the forward direction; while this forward scattering from each iridocyte shows very narrow angular dispersion (ca +68), the multiplicative scattering from a layer of ca 20 iridocytes broadens this dispersion to a cone of approximately +908. This understanding of the complex biophotonic dynamics enhances our comprehension of the physiologically, ecologically and evolutionarily significant light environment inside the giant clam, which is diffuse and nearly white at small tissue depths and downwelling, relatively monochromatic, and can be the same colour as the back-reflected light at greater depths in the tissue. Originally thought to be unique, cells of similar structure and photonic activity are now recognized in other species, where they serve other functions. The behaviour of the iridocytes opens possible new considerations for conservation and management of the valuable giant clam resource and new avenues for biologically inspired photonic applications.

Light-Dependent Phenomena and Related Molecular Mechanisms in Giant Clam-Dinoflagellate Associations: A Review

“…Iridocytes contain stacks of tiny reflective platelets (Griffiths et al, 1992) that can scatter light of photosynthetically conducive wavelengths to the tertiary tubules and enhance the quantum of usable light reaching the symbionts by fivefold (Holt et al, 2014). They also back-reflect light of non-productive wavelengths, contributing in part to the distinctive coloration and pattern of the outer mantle of individual giant clams (Holt et al, 2014;Ghoshal et al, 2016). Iridocytes can also protect the symbionts against harmful short wavelength UV radiation by absorbing it and re-emitting radiation of longer wavelengths that are conducive for photosynthesis (Rossbach et al, 2020).…”

Marine-Derived Polymeric Materials and Biomimetics: An Overview

“…Much comes from inherently coloured molecules that absorb light (i.e., chlorophyll) or compounds that luminesce (i.e., luciferin). However, a myriad of deep structural colours (iridescence) in the marine environment come from the nanostructuration of the material and has evolved independently across many phyla [228], including crustaceans [229][230][231], fish [232][233][234][235], bivalves [236,237], cephalopods [238], algae [239][240][241][242], diatoms [243], bacteria [244], etc. In the animal world, this type of colouration has been linked to camouflage, predation, signal communication and sex choice [245].…”

“…The iridocytes are distributed in such a manner photosynthetically productive wavelengths scattered laterally and forward and non-productive wavelengths are reflected backwards [236]. The spectral and angular scattering behaviour of an iridocyte depend on, and can be controlled by cell diameter, thicknesses of the high and low refractive index Bragg lamellae and their refractive indices [237]. Using these findings, Su et al [254] designed synthetic iridocytes using silica nanoparticles in microspheres embedded in gelatin for use in optimal harvesting of solar energy.…”

Functional nanomaterials to augment photosynthesis: evidence and considerations for their responsible use in agricultural applications

“…To overcome this the coral has evolved fluorescent light-harvesting mechanisms to provide additional light for its symbiont algae [33][34][35][36][37][38]. A similar system is present in giant clams, Tridacna crocea, which have developed highly reflective cells named iridocytes which do not produce colour using chemical pigments but instead use structural colour caused by physical photonic structures at the nanoscale that act as Bragg reflectors and illuminate the symbiotic algae present in the clam [39][40][41]. These observations suggest that it is possible that other forms of structural colour produced in planta have evolved to enhance photosynthesis or photoprotection in specific lighting environments.…”