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Melanin-based structural coloration of birds and its biomimetic applications

Melanin-based structural coloration of birds and its biomimetic applications Melanin has been a widely researched pigment by scientists for decades as it is undoubtedly the most ubiquitous and ancient pigment found in nature. Melanin plays very significant roles in structural plumage colors in birds: it has vis‑ ible light‑absorbing capabilities, and nanoscale structures can be formed by self‑assembling melanin granules. Herein, we review recent progress on melanin‑based structural coloration research. We hope that this review will provide current understanding of melanin’s structural and optical properties, natural coloration mechanisms, and biomimetic methods to implement artificial melanin‑based structural colors. Keywords: Melanin, Structural color, Pigment, Biomimetics chemical molecules that absorb specific wavelengths. Introduction Second, unlike pigment-based colors, structure makes Most animals survive by obtaining information from color by selectively reflecting light of certain wavelengths colors. Colors can be used for communication between from nanostructures. Melanin is a type of pigment that conspecifics, and colors can also be used to convey sub - contributes to the coloration of both pigment-based and ordination signals, nutritional conditions, health quality, structural colors of feathers (Hill and McGraw 2006; Rie- and even genetic conditions. Particularly, birds are rep- dler et  al. 2014). In fact, melanin itself can function as a resentative animals that display vivid, bright, and colorful pigment that absorbs visible light and simultaneously colors. Over 10,000 species of birds possess and utilize produce structural color. Overall, melanin plays a signifi - an amazing diversity of colors in their feathers (Brusatte cant role in the production of bird coloration, thus serv- et  al. 2015; Hart and Vorobyev 2005; Jetz et  al. 2012; ing as a major component. Lovette 2014; Hill and McGraw 2006; Tedore and Nilsson Melanin has been a widely studied pigment by scien- 2019). As birds are tetrachromats, birds are more sensi- tists for decades because it is undoubtedly the most ubiq- tive to a wider range of color spectrum in comparison to uitous and ancient pigment found in nature (d’Ischia humans. Humans have three types of cones or photore- et  al. 2014; d’Ischia et  al. 2020; Simon and Peles 2010). ceptor cells (peaks at 424, 530, and 560 nm). In contrast, Traditional and more recent technologies, such as scan- birds have four types of cones (peaks at 370, 445, 508, ning electron microscopy (SEM), transmission electron and 565 nm). Because of these advantages, research on microscopy (TEM), atomic force microscopy (AFM), birds’ plumage colors has attracted increasing scientific electron energy loss spectroscopy (EELS), and energy- attention. dispersive spectroscopy (EDS) have enabled huge In birds’ plumage, pigments and structures are two advances in understanding the molecular structures, main sources that generate color (Auber 1957; Hill and optical properties, and coloration mechanisms in the McGraw 2006). First, pigments make color by using last few decades (Galeb et al. 2021). Over the last decade, several papers have reviewed melanin chemistry, opti- *Correspondence: jongsoukyeo@yonsei.ac.kr cal functions of melanin, melanosome morphology, and Yonsei Institute of Convergence Technology, Yonsei University, 85 Songdogwahak‑ro, Yeonsu‑gu, Incheon 21983, Republic of Korea biomimetic structural coloration (D’Alba and Shawkey Full list of author information is available at the end of the article © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Jeon et al. Appl. Microsc. (2021) 51:14 Page 2 of 11 2019; Kohri 2019, 2020; Sun et al. 2013; Xiao et al. 2020). multi-film interference, coherent scattering, incoher - However, there is a lack of a comprehensive review focus- ent scattering, photonic band gap formation by photonic ing on how optical and structural properties of melanin nanostructures. are related to biomimetic applications. In this review, Thin-film interference is a phenomenon frequently we cover current issues of melanin-based colors of birds observed in nature. A simple example of structural colors and briefly summarize biomimetic optical applications caused by thin-film interference is a rainbow iridescent inspired by natural melanin-based colors. colors of a thin-film of oil on water. As shown in Fig.  1(a), a thin-film material surrounded by other materials con - Physical mechanisms of structural colors in birds sisting of different refractive indices can cause thin-film Structural colors in birds are generally observed on barbs interference. Light reflected from both top and bottom or barbules of feathers. β-keratin nanostructures and interfaces of a thin-film can be cancelled out or rein - melanin are the major factors affecting colors in barb- forced (Pancharatnam 1956; Parker 2000). Reflected light based structural colors, whereas β-keratin cortex and waves that are out of phase will destructively interfere, melanin are the major factors in barbule-based struc- whereas reflected light waves that are in phase will con - tural colors. β-keratin nanostructures and cortex are fac- structively interfere. Peak wavelength of structural colors tors that only affect the reflection of certain wavelengths, caused by thin-film interference can be defined as whereas melanin affects the reflection and absorption. 2n dcosθ Simultaneously, melanin plays a role in not only absorb- ers of broadband UV to visible light but also building blocks for photonic nanostructures. Structural colors where λ is the peak wavelength, n is a refractive index of are generated by complex interactions between inci- thin-film material, d is a film thickness, θ is an angle of dent light and optical components, especially melanin refraction, and m is an arbitrary natural number. Multi- and β-keratin in feathers. Structural colors in birds can film interference can be simply understood in terms be classified into five categories: thin-film interference, of thin-film interference with multilayer arrangement. Fig. 1 (a‑c) Basic physical mechanisms of structural coloration in birds. Structural colors appeared in barbs or barbules are based on (a) Thin‑film interference, (b) Incoherent scattering, (c) Coherent scattering, (d‑e) Representative melanin‑based photonic nanostructures, (d) Crystalline nanostructures generate iridescent colors, and (e) Amorphous nanostructures generate non‑iridescent colors Jeon  et al. Appl. Microsc. (2021) 51:14 Page 3 of 11 In birds, structural colors from thin-film interference biopolymers (King 2007). Melanin is produced by vari- are observed in the barbule-based structural colors. ous organisms including bacteria, fungi, plants, animals, β-keratin cortex of barbule can act as a thin-film mate - birds, and humans (Cordero and Casadevall 2020; D’Alba rial. Multilayered thin-film structures make light waves and Shawkey 2019). Structural and optical properties of reflect multiple times at the interfaces. Structural colors melanin are highly dependent on chemical and hierar- from multi-film interference often appear to be highly chical structure of melanin (D’Alba and Shawkey 2019). saturated, vivid, and bright when compared to thin-film Therefore, the understanding on melanin chemistry, interference (Sun et  al. 2013). Birds’ multilayered mela- melanosome morphology, and organization is highly nosomes can produce structural colors from multi-film demanded. interference. There are four general types of melanin: eumelanin, Light scattering means light-matter interactions with pheomelanin, neuromelanin, and allomelanin (Nico- scattering objects such as elementary particles (Skip- laus 1968; G. Prota 1988; Singh et  al. 2013). Eumelanin etrov and Sokolov 2014). In conventional use, scattering and pheomelanin are most commonly found in birds and includes constructive or destructive interferences of light other animals including humans (D’Alba and Shawkey waves reflected by light scattering objects (Prum et  al. 2019). Neuromelanin is a dark pigment found in the 2006). In addition, light scattering for structural colors in brain. Neuromelanin assists navigation with electromag- birds can be simply classified into two categories: inco - netic tracking (Bolzoni et  al. 2002; Sakurai et  al. 2004), herent scattering and coherent scattering. Incoherent and reduces oxidative stress in the brain (Xiao et  al. and coherent scatterings differ in the dependency of the 2020). Allomelanin is a heterogeneous group of nitro- phase relationships (Prum and Torres 2003). In incoher- gen-free polymers found in bacteria, fungi, and plants ent scattering, there is no phase relationship of scattered (Nosanchuk and Casadevall 2003). This review focuses light waves as shown in Fig.  1(b). In contrast, there is a on eumelanin and pheomelanin because these are the phase relationship of scattered light waves in coherent two main pigments in birds’ plumage coloration. scattering, because coherent scattering occurs when scat- In biosynthetic systems, types of melanin are pro- tering objects have uniform arrangement as shown in duced by following oxidative processes that involve Fig.  1(c). In birds, β-keratin nanostructures and melano- enzymes such as oxidases. For example, eumelanin somes can act as scattering objects. and pheomelanin are produced within melanocytes by Optical properties of structural colors in birds are the biosynthetic pathway that includes the tyrosinase- also dependent on the crystallinity of photonic nano- involved oxidation of tyrosine (Fig.  2). Eumelanin and structures. As shown in Fig.  1(d, e), crystalline photonic pheomelanin could be conventionally classified based nanostructures (photonic crystals, PhCs) that have a on differences in their optical properties: eumelanin long-range order produce angle-dependent iridescent shows black to brown while pheomelanin shows yel- colors, whereas amorphous photonic nanostructures low to reddish colors (Prota 1992; Simon and Peles (photonic glasses, PhGs) that have a lack of long-range 2010). Recent studies found that eumelanin is com- order produce angle-independent non-iridescent colors. posed of two molecules: 5, 6-dihydroxyl indole (DHI) There is the trade-off relationship between color satu - and 5, 6-dihydroxyindole-2-carboxylic acid (DHICA) ration and angle-dependency. Therefore, compared to (Miserez et  al. 2008). Based on advances in X-ray and PhCs, PhGs display less saturated structural colors. Tradi- high-resolution TEM techniques, these two eumelanin tionally, it was known that only long-range ordered PhCs protomolecules are shown in planar structures by π-π can form photonic band gap (PBG), but the recent study stacking (Cheng et  al. 1994; d’Ischia et  al. 2013; Watt support that short-range ordered PhGs can also form et  al. 2009; Xiao et  al. 2018). Pheomelanin is assumed PBG  (Miyazaki et  al. 2003). In birds, natural photonic to be composed of benzothiazine intermediates (Simon nanostructures are composed of β-keratin nanostruc- et  al. 2009). There is, however, still inadequate under - tures in barbs or melanosomes in barbules. Particularly, standing of pheomelanin’s chemical structure, there- in PhGs-type melanosomes, melanin’s strong absorption fore requiring further studies on melanin oligomers’ properties help to achieve saturated and bright structural chemical structures and synthetic processes based colors by suppressing incoherent scattering of light. on intramolecular interactions. Additionally, in birds and mammals, one significant problem in research on Structural and optical properties of melanin melanin is that eumelanin and pheomelanin are often Melanin is a pigment most commonly produced by observed in a combined form. Most melanin-based melanocytes within intracellular melanin granules colors are generated from a combination of eumelanin (melanosomes) (Simon and Peles 2010). Melanin has and pheomelanin in varying concentrations. Quite a an aggregation of monomer building blocks that form few of papers have reported melanosomes containing Jeon et al. Appl. Microsc. (2021) 51:14 Page 4 of 11 Fig. 2 Biosynthetic pathways of three different types of natural melanin in birds pure eumelanin or pheomelanin (Ito and Wakamatsu Melanin has a unique and distinguishing feature on the 2003; Hill and McGraw 2006; Micillo et  al. 2017; Nay- broadband absorbance spectrum as shown in Fig.  3(b): smith et al. 2004; Simon et al. 2008). The difficulty sep - eumelanin and pheomelanin absorb visible light, eumela- arating types of melanin makes it difficult to interpret nin absorbs more than pheomelanin for longer wave- optical functions of melanin-based colors. lengths (> 500 nm), and eumelanin and pheomelanin Melanosomes can be in spherical, rod, hollow-rod, or absorption spectra do not have peaks (Stavenga et  al. hollow-platelet shapes as shown in Fig.  3(a). Based on 2012). While most biological pigments show distinct previous findings about melanin coloration, larger per - peaks, this monotonic absorption spectrum differs from centages of eumelanin can form spherical, rod, hollow- other biological pigments (Xiao et  al. 2020). The mono - rod, and hollow-platelet melanosomes, but nearly pure tonic absorption of melanin differs also from broadband pheomelanin can only form spherical-shaped melano- absorbers such as carbon black. Melanin absorbs more somes (Durrer 1986; Liu et  al. 2005; Maia et  al. 2013). ultraviolet (UV) and blue light than longer wavelengths. Various melanosome morphologies may be associated There are several studies that have contributed to the with the chemical structure of melanin, and there are cause of this monotonic absorption of melanin (Chen many efforts to investigate melanin and melanosomes. et al. 2014; McGinness et al. 1974; McGinness 1972; Mer- However, scientists encounter significant technical limi - edith et al. 2006; Tran et al. 2006). For instance, Meredith tations to accurately characterize individual melano- et al. suggested that the large broadband absorption spec- somes. More research on investigating the chemistry of trum was caused by the superposition of absorption of all melanin and melanosomes may further clarify the cor- spectra at different wavelengths (Meredith et  al. 2006). relation between the chemical structure of melanin and Chen et  al. found that the interplay of geometric order melanosome morphologies. and disorder of eumelanin aggregate structures could broaden the absorption spectrum (Chen et al. 2014). The Jeon  et al. Appl. Microsc. (2021) 51:14 Page 5 of 11 Fig. 3 Structural and optical properties of melanin. (a) Melanosomes in birds have four main structures: nanoparticles (purple), nanorods (red), hollow nanorods (blue), and hollow platelets (green). (Scale bars: 500 nm). Reproduced with permission (Maia et al. 2013). Copyright 2013, The Authors. Published by National Academy of Sciences. (b) Extinction coefficients of eumelanin and pheomelanin in the visible range. Reproduced under the terms of the Creative Commons CC BY license (Stavenga et al. 2012). Copyright 2012, The Authors. Published by the Public Library of Science complexity of melanin structure is the main cause of our cortex’s thickness also affects the glossiness of feathers understanding on the monotonic absorption properties (Maia et al. 2011). In their study of a comparison between of melanin. California quail and common raven feathers indicated that the glossiness decreased as the keratin cortex’s thick- Melanin‑based structural coloration in nature ness, the melanin layer’s discontinuity, and the number of Melanin is the most ubiquitous pigment in that its abil- gaps in the melanin layer increased. ity for broadband absorption of UV to visible light can Melanin not only acts as an absorbing material of generate pigmentary colors and patterns in many organ- broadband visible wavelengths for coloration, but mela- isms. In addition to pigment-based coloration, melanin nin granules also produce iridescent structural colors can produce bright and vivid structural colors if mela- when they are arranged with high crystallinity. Highly nosomes are arranged into uniform nanostructures. crystalline melanosomes produce constructively scat- The colors produced here are iridescent, meaning that tered light, and the wavelengths depend on structural they change according to the viewing angle. Conversely, parameters of melanosome arrays. Materials (keratin or non-iridescent colors, colors that do not change with the air) surrounding melanosomes also affect the structural viewing angle, are often observed in structural colors colors because the effective refractive index changes produced by keratin, not melanin. Melanin acts as an with keratin and air having different refractive indi - absorbing material of broadband visible wavelengths ces (Kinoshita 2008). Melanosomes have solid/hollow for coloration. For example, amorphous melanosomes shapes, including spherical, rod, and platelet shapes, and in the blue barb in Steller’s jay indirectly affect non-iri - their arrangements ranging from a single layer to multi- descent colors as shown in Fig.  4(a) (Shawkey and Hill layers (Maia et al. 2013). 2006). Amorphous melanosomes in the barb can absorb In melanin-based structural colors, thin film interfer - incoherent scattering from β-keratin spongy layers and ence by stacked melanosomes and keratin is the most improve the color saturation. The barbule of the rock basic coloration model (Kinoshita et al. 2008; Kolle et al. dove (domestic pigeon) is an example of thin-film inter - 2010; Sun et al. 2013). In birds, established findings dem - ference-based structural coloration because the keratin onstrate that multilayer thin film interference can occur cortex that is on top of the melanosomes is thick enough due to layers of keratin and melanosomes, which pro- to produce constructive interference from the air/kera- duce iridescent colors (Durrer, and Villiger, W. J. Z. f. Z. tin cortex and keratin/melanosome interfaces (Yoshioka u. m. A. 1970; Greenewalt et  al. 1960; Hill and McGraw et  al. 2007). Melanosomes in the barbule of rock dove 2006; Land 1972; Zi et al. 2003). Among the basic multi- provide enough refractive index contrast (melanin ~ 1.8 layer thin films composed of melanosomes, one fascinat - and keratin 1.54) to produce thin-film interference. Mela - ing example is the male Lawes’ parotia’s breast feathers nosomes also absorb broadband visible light other than as shown in Fig.  5(a) (Stavenga et  al. 2011). They have constructive interference and contribute to color as a angular-dependent spectral shifts of reflected light rang - dark background. R. Maia et  al. found that the keratin ing from yellow to blue. These unique optical properties Jeon et al. Appl. Microsc. (2021) 51:14 Page 6 of 11 Fig. 4 Melanin as an absorbing material of broadband visible wavelengths for coloration. (a) Amorphous melanosomes in the blue barb of the Steller’s jay and the barbule of the rock dove’s (domestic pigeon) feathers. (Scale bars: 2 μm). Steller’s Jay, image reproduced under CC BY license. Photograph by Noel Reynolds. Feather microstructure of a blue Steller’s Jay feather, image reproduced with permission (Shawkey and Hill 2006). Copyright 2006, The Company of Biologists Ltd. Rock Dove, image reproduced under CC BY license. Photograph by Diego Delso. Feather microstructure of a Rock Dove feather, image reproduced under CC BY license (Yoshioka et al. 2007). Copyright 2007, The Authors. Published by The Physical Society of Japan. (b) Matte black color from the barbule of the California quail’s feather and glossy black color from the barbule of the common raven. (Scale bars: 2 μm). Reproduced with permission (Maia et al. 2011). Copyright 2010, The Royal Society are derived from stacked rod-shaped melanosomes sur- in the wing feather of the green-winged teal (Xiao et  al. rounded by keratin layers, and the melanosomes are 2017). arranged along boomerang-like barbules. Some birds have hollow melanosome structures that The most frequently observed melanin-based struc - increase the intensity of the colors shown on the feathers tural colors are rod-shaped melanosomes arranged along (Eliason et  al. 2013; Maia et  al. 2013). The mechanisms barbules (Li et al. 2010; Liu et al. 2005). Structural param- for how hollow melanosomes are formed have not yet eters that affect the color are mainly classified into four been determined. However, several studies report that parts: melanosome diameter, pitch (distance between hollow melanosomes could be formed after nanostruc- melanosomes), packing density, and orientation. The tural self-assembly of solid melanosomes in developing aspect ratio of eumelanin-dominant melanosome, which barbules (D’Alba et  al. 2021; Shawkey et  al. 2015). This in most rod shapes approaches 1:3.7, is also expected to evidence suggests selective loss of the core material in affect color because it affects stacking through deple - solid melanosomes, possibly due to the disintegration tion attraction of melanosomes (Li et  al. 2012; Maia of pheomelanin. Pheomelanin is more soluble in basic et  al. 2012; Piech and Walz 2000). However, the afore- solutions, and has less chemical stability than eumela- mentioned factors have a greater impact, thus we do nin (Simon and Peles 2010). Based on this evidence, not describe the aspect ratio in this review. Based on the Shawkey et al. discussed that solid melanosomes with the transverse direction of the barbule, melanosomes can pheomelanin-core and eumelanin-shell can be the ori- arrange from 2D hexagonal close packing to loose pack- gin of hollow melanosomes and human eyes also contain ing. Fig.  5(b) represents loosely packed melanosomes pheomelanin-eumelanin core-shell melanosomes (D’Alba and Shawkey 2019; Shawkey et al. 2015; Simon and Peles Jeon  et al. Appl. Microsc. (2021) 51:14 Page 7 of 11 Fig. 5 Melanin as a main structural component of structural coloration. (a) Multilayer thin films composed of melanosomes in the male Lawes’ parotia’s breast feathers. (Scale bar: 5 μm). Reproduced with permission (Stavenga et al. 2011). Copyright 2011, The Royal Society. (b) Non‑ close packed melanosomes in the wing feathers of the green‑ winged teal. (Scale bar: 500 nm). Reproduced under the terms of CC BY license (Xiao et al. 2017). Copyright 2017, The Authors. Published by The American Association for the Advancement of Science. (c) Close packed hollow melanosomes in the feather barbules of the violet‑backed starling. (Scale bar: 500 nm). Reproduced with permission (Eliason et al. 2013). Copyright 2013, The Authors. Published by The Royal Society. (d) Layered hollow platelet‑shaped melanosomes in the gorget feathers of the white ‑booted racket ‑tail hummingbird. (Scale bar: 500 nm). Reproduced with permission (Eliason et al. 2020). Copyright 2020, Wiley 2010). If we can determine the biological components or scattering. Biomimetic structural colors have often dis- conditions that make pheomelanin cores stable in eyes played low-saturation colors due to the incoherent scat- but not in feathers, we will be a step closer to understand tering of light. To suppress the incoherent scattering, the hollow melanosome development process. Eliason absorbing materials such as carbon black have been used et  al. suggest that hollow melanosomes allow birds to conventionally. However, artificial melanin-based struc - produce distinct colors compared to solid melanosomes tural colors do not need to add extra absorbing materi- (Eliason et  al. 2013), and the increased structural com- als, because artificial melanin can absorb broadband light plexity of feather tissues is associated with greater vari- and form nanostructures. As PDA can be synthesized ations in morphology and iridescent coloration (Eliason in various forms from thin films to core-shell particles, et  al. 2015). They also showed that hollow melanosomes many researchers have used PDA to produce structural may increase the whole reflectance based on hollow rod- colors (Kohri 2019, 2020; Xiao et al. 2020). Self-assembly shaped melanosomes of the wild turkey and magpie as of colloidal nanoparticles is one of the important and shown in Fig. 5(c) (Eliason et al. 2013), and hollow plate- effective methods to produce structural colors. From pre - let-shaped melanosomes of the hummingbird as shown vious studies, implemented structural colors depend on in Fig. 5(d) (Eliason et al. 2020). five parameters: (i) size of nanoparticles (Ge et  al. 2014; Kim et  al. 2017; Li et  al. 2017) and pitch of nanoparti- Biomimetic optical applications using artificial cles (Fudouzi and Sawada 2006; Fudouzi and Xia 2003), melanin (ii) refractive index of nanoparticles (Huang et  al. 2014; In recent years, materials for producing structural colors Zulian et  al. 2012), (iii) arrangement of nanoparticles have attracted considerable attention for their use in bio- (Katagiri et al. 2018; Takeoka 2012; Yoshioka and Takeoka mimetic optical applications. Polydopamine (PDA), an 2014), (iv) absorbance of nanoparticles and substrates artificial melanin, is the most widely used material for (Forster et  al. 2010; Takeoka 2018; Takeoka et  al. 2013), artificially implementing structural colors. Similar to (v) shape of nanoparticles (Kohri et  al. 2019). These five natural melanin in birds, artificial melanin’s broadband parameters affect the overall optical properties from hue absorption of UV to visible light helps to increase color to angle-dependency. Because this review focuses on saturation of structural colors by suppressing incoherent structural coloration using PDA-based artificial melanin, Jeon et al. Appl. Microsc. (2021) 51:14 Page 8 of 11 we will discuss representative examples of how structural et  al. 2015). In 2015, Xiao et  al. reported highly satu- parameters (size, arrangement, and shape) affect struc - rated structural colors with thin film structures contain - tural colors. ing assembled PDA nanoparticles as shown in Fig.  6(b) As described earlier, PDA has been synthesized in (Xiao et al. 2015). Xiao et al. also demonstrated full-spec- the form of thin films to core-shell particles. The most trum non-iridescent colors by supraball ink composed representative study in thin film-based structural col - of PDA core and silica shell nanoparticles as shown in oration is shown in Fig.  6(a). Zhang et  al. reported a Fig.  6(c) (Xiao et  al. 2017). Although many researchers simple method that achieves angle-independent struc- have reported bright structural colors using PDA-based tural colors using a PDA thin film coating on a silicon artificial melanin, the effect from the shape of nanopar - wafer (Zhang et al. 2017). Most of the studies have used ticles is still poorly understood. In nature, rod-shaped spherical-shaped nanoparticles. For instance, Kohri et al. anisotropic melanosomes play a significant role for struc - reported that bright structural colors are achieved by tural coloration, however, there are only a few exam- core-shell-type artificial melanin nanoparticles (Kohri ples for artificially implementing structural colors using Fig. 6 PDA‑based artificial melanin for producing structural colors. (a) Structural colors using a PDA coating on a silicon wafer. (Scale bar: 1 cm). Reproduced with permission (Zhang et al. 2017). Copyright 2017, Royal Society of Chemistry. (b) Structural colors by thin‑film interference of PDA nanoparticles. (Scale bar: 500 nm). Reproduced with permission (Xiao et al. 2015). Copyright 2015, American Chemical Society. (c) Supraball‑type photonic ink from a PDA core and silica shell nanoparticles. (Scale bar: 500 nm). Reproduced under the terms of CC BY license (Xiao et al. 2017). Copyright 2017, The Authors. Published by The American Association for the Advancement of Science. (d) Nanoparticles’ aspect ratio dependent structural coloration. Reproduced with permission (Kohri et al. 2019). Copyright 2019, American Chemical Society Jeon  et al. Appl. Microsc. (2021) 51:14 Page 9 of 11 Acknowledgments non-spherical nanoparticles. Kohri et  al. reported ellip- N/A soidal artificial melanin nanoparticles for structural col - oration (Kohri et al. 2019). The anisotropic nanoparticles Authors’ contributions Deok‑ Jin Jeon, Suejeong Paik, and Seungmuk Ji conceived the rationale and can be achieved by stretching asymmetrically of polysty- designed the review. Deok‑ Jin Jeon, Suejeong Paik, and Jong‑Souk Yeo wrote rene core and PDA shell spherical-shaped nanoparticles. the manuscript. Suejeong Paik initially drafted this review as a lab intern In addition to color production, biomimetic applications working full time during the summer and contributed specifically on writing the optical properties of melanin and melanosome morphology. Deok‑ Jin inspired by structural colors in nature have a consider- Jeon, Seungmuk Ji, and Jong‑Souk Yeo performed analysis and discussion. ably wide range of applications, ranging from humidity Jong‑Souk Yeo supervised the overall process. All the authors have read and sensor (Xiao et  al. 2016) to strain-sensor (Wang et  al. approved the final manuscript. 2020), and the range of biomimetic applications is still Funding expanding rapidly. As PDA-based artificial melanin has This work was funded by the National Institute of Ecology through the grant various functionalities ranging from producing structural number NIE‑ C‑2021‑18, and also supported by Human Frontier Science Program through the grant number (RGP0047/2019). colors to UV shields, PDA will play a more significant role in future biomimetic optical applications. Availability of data and materials N/A Conclusion In this review, we broadly summarized melanin’s struc- Declarations tural and optical properties, current understanding of Competing interests melanin-based structural coloration, and fabrication figThe authors declare that they have no competing interests. methods to implement structural colors using syn- Author details thetic melanin. Information on chemical structures of School of Integrated Technology, Yonsei University, 85 Songdogwahak‑ro, pheomelanin is less understood than eumelanin. Mela- Yeonsu‑gu, Incheon 21983, Republic of Korea. Yonsei Institute of Conver‑ nosomes’ shapes vary from spherical, rod, and hollow gence Technology, Yonsei University, 85 Songdogwahak‑ro, Yeonsu‑gu, Incheon 21983, Republic of Korea. 39 Yeonhui‑ro 22‑ gil, Seodaemun‑gu, rod to hollow platelets. Melanosome morphologies may Seoul 03723, Republic of Korea. depend on the chemical structures of melanin. We also discussed the optical properties of melanin. Eumela- Received: 1 July 2021 Accepted: 24 September 2021 nin and pheomelanin absorb visible light, and eumela- nin absorbs UV to blue light more than pheomelanin. Eumelanin and pheomelanin’s absorption spectra do References not have peaks. Their monotonic absorption spectra are L.J.I. Auber, The distribution of structural colours and unusual pigments in the unusual compared to other biological pigments. Not class. Aves. 99(3), 463–476 (1957) only melanin acts in pigment as an absorbing material F. Bolzoni, S. Giraudo, L. Lopiano, B. Bergamasco, M. Fasano, P.R. 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Melanin-based structural coloration of birds and its biomimetic applications

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Abstract

Melanin has been a widely researched pigment by scientists for decades as it is undoubtedly the most ubiquitous and ancient pigment found in nature. Melanin plays very significant roles in structural plumage colors in birds: it has vis‑ ible light‑absorbing capabilities, and nanoscale structures can be formed by self‑assembling melanin granules. Herein, we review recent progress on melanin‑based structural coloration research. We hope that this review will provide current understanding of melanin’s structural and optical properties, natural coloration mechanisms, and biomimetic methods to implement artificial melanin‑based structural colors. Keywords: Melanin, Structural color, Pigment, Biomimetics chemical molecules that absorb specific wavelengths. Introduction Second, unlike pigment-based colors, structure makes Most animals survive by obtaining information from color by selectively reflecting light of certain wavelengths colors. Colors can be used for communication between from nanostructures. Melanin is a type of pigment that conspecifics, and colors can also be used to convey sub - contributes to the coloration of both pigment-based and ordination signals, nutritional conditions, health quality, structural colors of feathers (Hill and McGraw 2006; Rie- and even genetic conditions. Particularly, birds are rep- dler et  al. 2014). In fact, melanin itself can function as a resentative animals that display vivid, bright, and colorful pigment that absorbs visible light and simultaneously colors. Over 10,000 species of birds possess and utilize produce structural color. Overall, melanin plays a signifi - an amazing diversity of colors in their feathers (Brusatte cant role in the production of bird coloration, thus serv- et  al. 2015; Hart and Vorobyev 2005; Jetz et  al. 2012; ing as a major component. Lovette 2014; Hill and McGraw 2006; Tedore and Nilsson Melanin has been a widely studied pigment by scien- 2019). As birds are tetrachromats, birds are more sensi- tists for decades because it is undoubtedly the most ubiq- tive to a wider range of color spectrum in comparison to uitous and ancient pigment found in nature (d’Ischia humans. Humans have three types of cones or photore- et  al. 2014; d’Ischia et  al. 2020; Simon and Peles 2010). ceptor cells (peaks at 424, 530, and 560 nm). In contrast, Traditional and more recent technologies, such as scan- birds have four types of cones (peaks at 370, 445, 508, ning electron microscopy (SEM), transmission electron and 565 nm). Because of these advantages, research on microscopy (TEM), atomic force microscopy (AFM), birds’ plumage colors has attracted increasing scientific electron energy loss spectroscopy (EELS), and energy- attention. dispersive spectroscopy (EDS) have enabled huge In birds’ plumage, pigments and structures are two advances in understanding the molecular structures, main sources that generate color (Auber 1957; Hill and optical properties, and coloration mechanisms in the McGraw 2006). First, pigments make color by using last few decades (Galeb et al. 2021). Over the last decade, several papers have reviewed melanin chemistry, opti- *Correspondence: jongsoukyeo@yonsei.ac.kr cal functions of melanin, melanosome morphology, and Yonsei Institute of Convergence Technology, Yonsei University, 85 Songdogwahak‑ro, Yeonsu‑gu, Incheon 21983, Republic of Korea biomimetic structural coloration (D’Alba and Shawkey Full list of author information is available at the end of the article © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Jeon et al. Appl. Microsc. (2021) 51:14 Page 2 of 11 2019; Kohri 2019, 2020; Sun et al. 2013; Xiao et al. 2020). multi-film interference, coherent scattering, incoher - However, there is a lack of a comprehensive review focus- ent scattering, photonic band gap formation by photonic ing on how optical and structural properties of melanin nanostructures. are related to biomimetic applications. In this review, Thin-film interference is a phenomenon frequently we cover current issues of melanin-based colors of birds observed in nature. A simple example of structural colors and briefly summarize biomimetic optical applications caused by thin-film interference is a rainbow iridescent inspired by natural melanin-based colors. colors of a thin-film of oil on water. As shown in Fig.  1(a), a thin-film material surrounded by other materials con - Physical mechanisms of structural colors in birds sisting of different refractive indices can cause thin-film Structural colors in birds are generally observed on barbs interference. Light reflected from both top and bottom or barbules of feathers. β-keratin nanostructures and interfaces of a thin-film can be cancelled out or rein - melanin are the major factors affecting colors in barb- forced (Pancharatnam 1956; Parker 2000). Reflected light based structural colors, whereas β-keratin cortex and waves that are out of phase will destructively interfere, melanin are the major factors in barbule-based struc- whereas reflected light waves that are in phase will con - tural colors. β-keratin nanostructures and cortex are fac- structively interfere. Peak wavelength of structural colors tors that only affect the reflection of certain wavelengths, caused by thin-film interference can be defined as whereas melanin affects the reflection and absorption. 2n dcosθ Simultaneously, melanin plays a role in not only absorb- ers of broadband UV to visible light but also building blocks for photonic nanostructures. Structural colors where λ is the peak wavelength, n is a refractive index of are generated by complex interactions between inci- thin-film material, d is a film thickness, θ is an angle of dent light and optical components, especially melanin refraction, and m is an arbitrary natural number. Multi- and β-keratin in feathers. Structural colors in birds can film interference can be simply understood in terms be classified into five categories: thin-film interference, of thin-film interference with multilayer arrangement. Fig. 1 (a‑c) Basic physical mechanisms of structural coloration in birds. Structural colors appeared in barbs or barbules are based on (a) Thin‑film interference, (b) Incoherent scattering, (c) Coherent scattering, (d‑e) Representative melanin‑based photonic nanostructures, (d) Crystalline nanostructures generate iridescent colors, and (e) Amorphous nanostructures generate non‑iridescent colors Jeon  et al. Appl. Microsc. (2021) 51:14 Page 3 of 11 In birds, structural colors from thin-film interference biopolymers (King 2007). Melanin is produced by vari- are observed in the barbule-based structural colors. ous organisms including bacteria, fungi, plants, animals, β-keratin cortex of barbule can act as a thin-film mate - birds, and humans (Cordero and Casadevall 2020; D’Alba rial. Multilayered thin-film structures make light waves and Shawkey 2019). Structural and optical properties of reflect multiple times at the interfaces. Structural colors melanin are highly dependent on chemical and hierar- from multi-film interference often appear to be highly chical structure of melanin (D’Alba and Shawkey 2019). saturated, vivid, and bright when compared to thin-film Therefore, the understanding on melanin chemistry, interference (Sun et  al. 2013). Birds’ multilayered mela- melanosome morphology, and organization is highly nosomes can produce structural colors from multi-film demanded. interference. There are four general types of melanin: eumelanin, Light scattering means light-matter interactions with pheomelanin, neuromelanin, and allomelanin (Nico- scattering objects such as elementary particles (Skip- laus 1968; G. Prota 1988; Singh et  al. 2013). Eumelanin etrov and Sokolov 2014). In conventional use, scattering and pheomelanin are most commonly found in birds and includes constructive or destructive interferences of light other animals including humans (D’Alba and Shawkey waves reflected by light scattering objects (Prum et  al. 2019). Neuromelanin is a dark pigment found in the 2006). In addition, light scattering for structural colors in brain. Neuromelanin assists navigation with electromag- birds can be simply classified into two categories: inco - netic tracking (Bolzoni et  al. 2002; Sakurai et  al. 2004), herent scattering and coherent scattering. Incoherent and reduces oxidative stress in the brain (Xiao et  al. and coherent scatterings differ in the dependency of the 2020). Allomelanin is a heterogeneous group of nitro- phase relationships (Prum and Torres 2003). In incoher- gen-free polymers found in bacteria, fungi, and plants ent scattering, there is no phase relationship of scattered (Nosanchuk and Casadevall 2003). This review focuses light waves as shown in Fig.  1(b). In contrast, there is a on eumelanin and pheomelanin because these are the phase relationship of scattered light waves in coherent two main pigments in birds’ plumage coloration. scattering, because coherent scattering occurs when scat- In biosynthetic systems, types of melanin are pro- tering objects have uniform arrangement as shown in duced by following oxidative processes that involve Fig.  1(c). In birds, β-keratin nanostructures and melano- enzymes such as oxidases. For example, eumelanin somes can act as scattering objects. and pheomelanin are produced within melanocytes by Optical properties of structural colors in birds are the biosynthetic pathway that includes the tyrosinase- also dependent on the crystallinity of photonic nano- involved oxidation of tyrosine (Fig.  2). Eumelanin and structures. As shown in Fig.  1(d, e), crystalline photonic pheomelanin could be conventionally classified based nanostructures (photonic crystals, PhCs) that have a on differences in their optical properties: eumelanin long-range order produce angle-dependent iridescent shows black to brown while pheomelanin shows yel- colors, whereas amorphous photonic nanostructures low to reddish colors (Prota 1992; Simon and Peles (photonic glasses, PhGs) that have a lack of long-range 2010). Recent studies found that eumelanin is com- order produce angle-independent non-iridescent colors. posed of two molecules: 5, 6-dihydroxyl indole (DHI) There is the trade-off relationship between color satu - and 5, 6-dihydroxyindole-2-carboxylic acid (DHICA) ration and angle-dependency. Therefore, compared to (Miserez et  al. 2008). Based on advances in X-ray and PhCs, PhGs display less saturated structural colors. Tradi- high-resolution TEM techniques, these two eumelanin tionally, it was known that only long-range ordered PhCs protomolecules are shown in planar structures by π-π can form photonic band gap (PBG), but the recent study stacking (Cheng et  al. 1994; d’Ischia et  al. 2013; Watt support that short-range ordered PhGs can also form et  al. 2009; Xiao et  al. 2018). Pheomelanin is assumed PBG  (Miyazaki et  al. 2003). In birds, natural photonic to be composed of benzothiazine intermediates (Simon nanostructures are composed of β-keratin nanostruc- et  al. 2009). There is, however, still inadequate under - tures in barbs or melanosomes in barbules. Particularly, standing of pheomelanin’s chemical structure, there- in PhGs-type melanosomes, melanin’s strong absorption fore requiring further studies on melanin oligomers’ properties help to achieve saturated and bright structural chemical structures and synthetic processes based colors by suppressing incoherent scattering of light. on intramolecular interactions. Additionally, in birds and mammals, one significant problem in research on Structural and optical properties of melanin melanin is that eumelanin and pheomelanin are often Melanin is a pigment most commonly produced by observed in a combined form. Most melanin-based melanocytes within intracellular melanin granules colors are generated from a combination of eumelanin (melanosomes) (Simon and Peles 2010). Melanin has and pheomelanin in varying concentrations. Quite a an aggregation of monomer building blocks that form few of papers have reported melanosomes containing Jeon et al. Appl. Microsc. (2021) 51:14 Page 4 of 11 Fig. 2 Biosynthetic pathways of three different types of natural melanin in birds pure eumelanin or pheomelanin (Ito and Wakamatsu Melanin has a unique and distinguishing feature on the 2003; Hill and McGraw 2006; Micillo et  al. 2017; Nay- broadband absorbance spectrum as shown in Fig.  3(b): smith et al. 2004; Simon et al. 2008). The difficulty sep - eumelanin and pheomelanin absorb visible light, eumela- arating types of melanin makes it difficult to interpret nin absorbs more than pheomelanin for longer wave- optical functions of melanin-based colors. lengths (> 500 nm), and eumelanin and pheomelanin Melanosomes can be in spherical, rod, hollow-rod, or absorption spectra do not have peaks (Stavenga et  al. hollow-platelet shapes as shown in Fig.  3(a). Based on 2012). While most biological pigments show distinct previous findings about melanin coloration, larger per - peaks, this monotonic absorption spectrum differs from centages of eumelanin can form spherical, rod, hollow- other biological pigments (Xiao et  al. 2020). The mono - rod, and hollow-platelet melanosomes, but nearly pure tonic absorption of melanin differs also from broadband pheomelanin can only form spherical-shaped melano- absorbers such as carbon black. Melanin absorbs more somes (Durrer 1986; Liu et  al. 2005; Maia et  al. 2013). ultraviolet (UV) and blue light than longer wavelengths. Various melanosome morphologies may be associated There are several studies that have contributed to the with the chemical structure of melanin, and there are cause of this monotonic absorption of melanin (Chen many efforts to investigate melanin and melanosomes. et al. 2014; McGinness et al. 1974; McGinness 1972; Mer- However, scientists encounter significant technical limi - edith et al. 2006; Tran et al. 2006). For instance, Meredith tations to accurately characterize individual melano- et al. suggested that the large broadband absorption spec- somes. More research on investigating the chemistry of trum was caused by the superposition of absorption of all melanin and melanosomes may further clarify the cor- spectra at different wavelengths (Meredith et  al. 2006). relation between the chemical structure of melanin and Chen et  al. found that the interplay of geometric order melanosome morphologies. and disorder of eumelanin aggregate structures could broaden the absorption spectrum (Chen et al. 2014). The Jeon  et al. Appl. Microsc. (2021) 51:14 Page 5 of 11 Fig. 3 Structural and optical properties of melanin. (a) Melanosomes in birds have four main structures: nanoparticles (purple), nanorods (red), hollow nanorods (blue), and hollow platelets (green). (Scale bars: 500 nm). Reproduced with permission (Maia et al. 2013). Copyright 2013, The Authors. Published by National Academy of Sciences. (b) Extinction coefficients of eumelanin and pheomelanin in the visible range. Reproduced under the terms of the Creative Commons CC BY license (Stavenga et al. 2012). Copyright 2012, The Authors. Published by the Public Library of Science complexity of melanin structure is the main cause of our cortex’s thickness also affects the glossiness of feathers understanding on the monotonic absorption properties (Maia et al. 2011). In their study of a comparison between of melanin. California quail and common raven feathers indicated that the glossiness decreased as the keratin cortex’s thick- Melanin‑based structural coloration in nature ness, the melanin layer’s discontinuity, and the number of Melanin is the most ubiquitous pigment in that its abil- gaps in the melanin layer increased. ity for broadband absorption of UV to visible light can Melanin not only acts as an absorbing material of generate pigmentary colors and patterns in many organ- broadband visible wavelengths for coloration, but mela- isms. In addition to pigment-based coloration, melanin nin granules also produce iridescent structural colors can produce bright and vivid structural colors if mela- when they are arranged with high crystallinity. Highly nosomes are arranged into uniform nanostructures. crystalline melanosomes produce constructively scat- The colors produced here are iridescent, meaning that tered light, and the wavelengths depend on structural they change according to the viewing angle. Conversely, parameters of melanosome arrays. Materials (keratin or non-iridescent colors, colors that do not change with the air) surrounding melanosomes also affect the structural viewing angle, are often observed in structural colors colors because the effective refractive index changes produced by keratin, not melanin. Melanin acts as an with keratin and air having different refractive indi - absorbing material of broadband visible wavelengths ces (Kinoshita 2008). Melanosomes have solid/hollow for coloration. For example, amorphous melanosomes shapes, including spherical, rod, and platelet shapes, and in the blue barb in Steller’s jay indirectly affect non-iri - their arrangements ranging from a single layer to multi- descent colors as shown in Fig.  4(a) (Shawkey and Hill layers (Maia et al. 2013). 2006). Amorphous melanosomes in the barb can absorb In melanin-based structural colors, thin film interfer - incoherent scattering from β-keratin spongy layers and ence by stacked melanosomes and keratin is the most improve the color saturation. The barbule of the rock basic coloration model (Kinoshita et al. 2008; Kolle et al. dove (domestic pigeon) is an example of thin-film inter - 2010; Sun et al. 2013). In birds, established findings dem - ference-based structural coloration because the keratin onstrate that multilayer thin film interference can occur cortex that is on top of the melanosomes is thick enough due to layers of keratin and melanosomes, which pro- to produce constructive interference from the air/kera- duce iridescent colors (Durrer, and Villiger, W. J. Z. f. Z. tin cortex and keratin/melanosome interfaces (Yoshioka u. m. A. 1970; Greenewalt et  al. 1960; Hill and McGraw et  al. 2007). Melanosomes in the barbule of rock dove 2006; Land 1972; Zi et al. 2003). Among the basic multi- provide enough refractive index contrast (melanin ~ 1.8 layer thin films composed of melanosomes, one fascinat - and keratin 1.54) to produce thin-film interference. Mela - ing example is the male Lawes’ parotia’s breast feathers nosomes also absorb broadband visible light other than as shown in Fig.  5(a) (Stavenga et  al. 2011). They have constructive interference and contribute to color as a angular-dependent spectral shifts of reflected light rang - dark background. R. Maia et  al. found that the keratin ing from yellow to blue. These unique optical properties Jeon et al. Appl. Microsc. (2021) 51:14 Page 6 of 11 Fig. 4 Melanin as an absorbing material of broadband visible wavelengths for coloration. (a) Amorphous melanosomes in the blue barb of the Steller’s jay and the barbule of the rock dove’s (domestic pigeon) feathers. (Scale bars: 2 μm). Steller’s Jay, image reproduced under CC BY license. Photograph by Noel Reynolds. Feather microstructure of a blue Steller’s Jay feather, image reproduced with permission (Shawkey and Hill 2006). Copyright 2006, The Company of Biologists Ltd. Rock Dove, image reproduced under CC BY license. Photograph by Diego Delso. Feather microstructure of a Rock Dove feather, image reproduced under CC BY license (Yoshioka et al. 2007). Copyright 2007, The Authors. Published by The Physical Society of Japan. (b) Matte black color from the barbule of the California quail’s feather and glossy black color from the barbule of the common raven. (Scale bars: 2 μm). Reproduced with permission (Maia et al. 2011). Copyright 2010, The Royal Society are derived from stacked rod-shaped melanosomes sur- in the wing feather of the green-winged teal (Xiao et  al. rounded by keratin layers, and the melanosomes are 2017). arranged along boomerang-like barbules. Some birds have hollow melanosome structures that The most frequently observed melanin-based struc - increase the intensity of the colors shown on the feathers tural colors are rod-shaped melanosomes arranged along (Eliason et  al. 2013; Maia et  al. 2013). The mechanisms barbules (Li et al. 2010; Liu et al. 2005). Structural param- for how hollow melanosomes are formed have not yet eters that affect the color are mainly classified into four been determined. However, several studies report that parts: melanosome diameter, pitch (distance between hollow melanosomes could be formed after nanostruc- melanosomes), packing density, and orientation. The tural self-assembly of solid melanosomes in developing aspect ratio of eumelanin-dominant melanosome, which barbules (D’Alba et  al. 2021; Shawkey et  al. 2015). This in most rod shapes approaches 1:3.7, is also expected to evidence suggests selective loss of the core material in affect color because it affects stacking through deple - solid melanosomes, possibly due to the disintegration tion attraction of melanosomes (Li et  al. 2012; Maia of pheomelanin. Pheomelanin is more soluble in basic et  al. 2012; Piech and Walz 2000). However, the afore- solutions, and has less chemical stability than eumela- mentioned factors have a greater impact, thus we do nin (Simon and Peles 2010). Based on this evidence, not describe the aspect ratio in this review. Based on the Shawkey et al. discussed that solid melanosomes with the transverse direction of the barbule, melanosomes can pheomelanin-core and eumelanin-shell can be the ori- arrange from 2D hexagonal close packing to loose pack- gin of hollow melanosomes and human eyes also contain ing. Fig.  5(b) represents loosely packed melanosomes pheomelanin-eumelanin core-shell melanosomes (D’Alba and Shawkey 2019; Shawkey et al. 2015; Simon and Peles Jeon  et al. Appl. Microsc. (2021) 51:14 Page 7 of 11 Fig. 5 Melanin as a main structural component of structural coloration. (a) Multilayer thin films composed of melanosomes in the male Lawes’ parotia’s breast feathers. (Scale bar: 5 μm). Reproduced with permission (Stavenga et al. 2011). Copyright 2011, The Royal Society. (b) Non‑ close packed melanosomes in the wing feathers of the green‑ winged teal. (Scale bar: 500 nm). Reproduced under the terms of CC BY license (Xiao et al. 2017). Copyright 2017, The Authors. Published by The American Association for the Advancement of Science. (c) Close packed hollow melanosomes in the feather barbules of the violet‑backed starling. (Scale bar: 500 nm). Reproduced with permission (Eliason et al. 2013). Copyright 2013, The Authors. Published by The Royal Society. (d) Layered hollow platelet‑shaped melanosomes in the gorget feathers of the white ‑booted racket ‑tail hummingbird. (Scale bar: 500 nm). Reproduced with permission (Eliason et al. 2020). Copyright 2020, Wiley 2010). If we can determine the biological components or scattering. Biomimetic structural colors have often dis- conditions that make pheomelanin cores stable in eyes played low-saturation colors due to the incoherent scat- but not in feathers, we will be a step closer to understand tering of light. To suppress the incoherent scattering, the hollow melanosome development process. Eliason absorbing materials such as carbon black have been used et  al. suggest that hollow melanosomes allow birds to conventionally. However, artificial melanin-based struc - produce distinct colors compared to solid melanosomes tural colors do not need to add extra absorbing materi- (Eliason et  al. 2013), and the increased structural com- als, because artificial melanin can absorb broadband light plexity of feather tissues is associated with greater vari- and form nanostructures. As PDA can be synthesized ations in morphology and iridescent coloration (Eliason in various forms from thin films to core-shell particles, et  al. 2015). They also showed that hollow melanosomes many researchers have used PDA to produce structural may increase the whole reflectance based on hollow rod- colors (Kohri 2019, 2020; Xiao et al. 2020). Self-assembly shaped melanosomes of the wild turkey and magpie as of colloidal nanoparticles is one of the important and shown in Fig. 5(c) (Eliason et al. 2013), and hollow plate- effective methods to produce structural colors. From pre - let-shaped melanosomes of the hummingbird as shown vious studies, implemented structural colors depend on in Fig. 5(d) (Eliason et al. 2020). five parameters: (i) size of nanoparticles (Ge et  al. 2014; Kim et  al. 2017; Li et  al. 2017) and pitch of nanoparti- Biomimetic optical applications using artificial cles (Fudouzi and Sawada 2006; Fudouzi and Xia 2003), melanin (ii) refractive index of nanoparticles (Huang et  al. 2014; In recent years, materials for producing structural colors Zulian et  al. 2012), (iii) arrangement of nanoparticles have attracted considerable attention for their use in bio- (Katagiri et al. 2018; Takeoka 2012; Yoshioka and Takeoka mimetic optical applications. Polydopamine (PDA), an 2014), (iv) absorbance of nanoparticles and substrates artificial melanin, is the most widely used material for (Forster et  al. 2010; Takeoka 2018; Takeoka et  al. 2013), artificially implementing structural colors. Similar to (v) shape of nanoparticles (Kohri et  al. 2019). These five natural melanin in birds, artificial melanin’s broadband parameters affect the overall optical properties from hue absorption of UV to visible light helps to increase color to angle-dependency. Because this review focuses on saturation of structural colors by suppressing incoherent structural coloration using PDA-based artificial melanin, Jeon et al. Appl. Microsc. (2021) 51:14 Page 8 of 11 we will discuss representative examples of how structural et  al. 2015). In 2015, Xiao et  al. reported highly satu- parameters (size, arrangement, and shape) affect struc - rated structural colors with thin film structures contain - tural colors. ing assembled PDA nanoparticles as shown in Fig.  6(b) As described earlier, PDA has been synthesized in (Xiao et al. 2015). Xiao et al. also demonstrated full-spec- the form of thin films to core-shell particles. The most trum non-iridescent colors by supraball ink composed representative study in thin film-based structural col - of PDA core and silica shell nanoparticles as shown in oration is shown in Fig.  6(a). Zhang et  al. reported a Fig.  6(c) (Xiao et  al. 2017). Although many researchers simple method that achieves angle-independent struc- have reported bright structural colors using PDA-based tural colors using a PDA thin film coating on a silicon artificial melanin, the effect from the shape of nanopar - wafer (Zhang et al. 2017). Most of the studies have used ticles is still poorly understood. In nature, rod-shaped spherical-shaped nanoparticles. For instance, Kohri et al. anisotropic melanosomes play a significant role for struc - reported that bright structural colors are achieved by tural coloration, however, there are only a few exam- core-shell-type artificial melanin nanoparticles (Kohri ples for artificially implementing structural colors using Fig. 6 PDA‑based artificial melanin for producing structural colors. (a) Structural colors using a PDA coating on a silicon wafer. (Scale bar: 1 cm). Reproduced with permission (Zhang et al. 2017). Copyright 2017, Royal Society of Chemistry. (b) Structural colors by thin‑film interference of PDA nanoparticles. (Scale bar: 500 nm). Reproduced with permission (Xiao et al. 2015). Copyright 2015, American Chemical Society. (c) Supraball‑type photonic ink from a PDA core and silica shell nanoparticles. (Scale bar: 500 nm). Reproduced under the terms of CC BY license (Xiao et al. 2017). Copyright 2017, The Authors. Published by The American Association for the Advancement of Science. (d) Nanoparticles’ aspect ratio dependent structural coloration. Reproduced with permission (Kohri et al. 2019). Copyright 2019, American Chemical Society Jeon  et al. Appl. Microsc. (2021) 51:14 Page 9 of 11 Acknowledgments non-spherical nanoparticles. Kohri et  al. reported ellip- N/A soidal artificial melanin nanoparticles for structural col - oration (Kohri et al. 2019). The anisotropic nanoparticles Authors’ contributions Deok‑ Jin Jeon, Suejeong Paik, and Seungmuk Ji conceived the rationale and can be achieved by stretching asymmetrically of polysty- designed the review. Deok‑ Jin Jeon, Suejeong Paik, and Jong‑Souk Yeo wrote rene core and PDA shell spherical-shaped nanoparticles. the manuscript. Suejeong Paik initially drafted this review as a lab intern In addition to color production, biomimetic applications working full time during the summer and contributed specifically on writing the optical properties of melanin and melanosome morphology. Deok‑ Jin inspired by structural colors in nature have a consider- Jeon, Seungmuk Ji, and Jong‑Souk Yeo performed analysis and discussion. ably wide range of applications, ranging from humidity Jong‑Souk Yeo supervised the overall process. All the authors have read and sensor (Xiao et  al. 2016) to strain-sensor (Wang et  al. approved the final manuscript. 2020), and the range of biomimetic applications is still Funding expanding rapidly. As PDA-based artificial melanin has This work was funded by the National Institute of Ecology through the grant various functionalities ranging from producing structural number NIE‑ C‑2021‑18, and also supported by Human Frontier Science Program through the grant number (RGP0047/2019). colors to UV shields, PDA will play a more significant role in future biomimetic optical applications. Availability of data and materials N/A Conclusion In this review, we broadly summarized melanin’s struc- Declarations tural and optical properties, current understanding of Competing interests melanin-based structural coloration, and fabrication figThe authors declare that they have no competing interests. methods to implement structural colors using syn- Author details thetic melanin. Information on chemical structures of School of Integrated Technology, Yonsei University, 85 Songdogwahak‑ro, pheomelanin is less understood than eumelanin. Mela- Yeonsu‑gu, Incheon 21983, Republic of Korea. Yonsei Institute of Conver‑ nosomes’ shapes vary from spherical, rod, and hollow gence Technology, Yonsei University, 85 Songdogwahak‑ro, Yeonsu‑gu, Incheon 21983, Republic of Korea. 39 Yeonhui‑ro 22‑ gil, Seodaemun‑gu, rod to hollow platelets. Melanosome morphologies may Seoul 03723, Republic of Korea. depend on the chemical structures of melanin. We also discussed the optical properties of melanin. Eumela- Received: 1 July 2021 Accepted: 24 September 2021 nin and pheomelanin absorb visible light, and eumela- nin absorbs UV to blue light more than pheomelanin. Eumelanin and pheomelanin’s absorption spectra do References not have peaks. Their monotonic absorption spectra are L.J.I. Auber, The distribution of structural colours and unusual pigments in the unusual compared to other biological pigments. Not class. Aves. 99(3), 463–476 (1957) only melanin acts in pigment as an absorbing material F. Bolzoni, S. Giraudo, L. Lopiano, B. Bergamasco, M. Fasano, P.R. Crippa, Mag‑ netic investigations of human mesencephalic neuromelanin. Biochimica of broadband visible wavelengths for coloration, but Et Biophysica Acta‑Molecular Basis of Disease 1586(2), 210–218 (2002). melanin granules also produce iridescent structural https:// doi. org/ 10. 1016/ S0925‑ 4439(01) 00099‑0 colors when they are arranged with high crystallinity. S.L. Brusatte, J.K. O’Connor, E.D. Jarvis, The origin and diversification of birds. Curr. Biol. 25(19), R888–R898 (2015). https:// doi. org/ 10. 1016/j. cub. 2015. We introduced a few studies on the optical advantages 08. 003 of hollow melanosomes, and briefly addressed the need C.T. Chen, C. Chuang, J.S. Cao, V. Ball, D. Ruch, M.J. Buehler, Excitonic effects for future research on the biosynthetic mechanisms of from geometric order and disorder explain broadband optical absorp‑ tion in eumelanin. Nat. Commun. 5 (2014). https:// doi. org/ 10. 1038/ hollow melanosomes. 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Journal

Applied MicroscopySpringer Journals

Published: Oct 11, 2021

Keywords: Melanin; Structural color; Pigment; Biomimetics

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