Blumer Michael J, Surapaneni Venkata A, Ciecierska-Holmes Jana, Redl Stefan, Pechriggl Elisabeth J, Mollen Frederik H, Dean Mason N
Institute of Clinical and Functional Anatomy, Medical University Innsbruck, Innsbruck, Austria.
Department of Infectious Diseases and Public Health, City University of Hong Kong, Kowloon, Hong Kong SAR, China.
Front Cell Dev Biol. 2024 Jul 10;12:1393237. doi: 10.3389/fcell.2024.1393237. eCollection 2024.
In animals, pigments but also nanostructures determine skin coloration, and many shades are produced by combining both mechanisms. Recently, we discovered a new mechanism for blue coloration in the ribbontail stingray , a species with electric blue spots on its yellow-brown skin. Here, we characterize finescale differences in cell composition and architecture distinguishing blue from non-blue regions, the first description of elasmobranch chromatophores and the nanostructures responsible for the stingray's novel structural blue, contrasting with other known mechanisms for making nature's rarest color. In blue regions, the upper dermis comprised a layer of chromatophore units -iridophores and melanophores entwined in compact clusters framed by collagen bundles- this structural stability perhaps the root of the skin color's robustness. Stingray iridophores were notably different from other vertebrate light-reflecting cells in having numerous fingerlike processes, which surrounded nearby melanophores like fists clenching a black stone. Iridophores contained spherical iridosomes enclosing guanine nanocrystals, suspended in a 3D quasi-order, linked by a cytoskeleton of intermediate filaments. We argue that intermediate filaments form a structural scaffold with a distinct optical role, providing the iridosome spacing critical to produce the blue color. In contrast, black-pigmented melanosomes within melanophores showed space-efficient packing, consistent with their hypothesized role as broadband-absorbers for enhancing blue color saturation. The chromatophore layer's ultrastructure was similar in juvenile and adult animals, indicating that skin color and perhaps its ecological role are likely consistent through ontogeny. In non-blue areas, iridophores were replaced by pale cells, resembling iridophores in some morphological and nanoscale features, but lacking guanine crystals, suggesting that the cell types arise from a common progenitor cell. The particular cellular associations and structural interactions we demonstrate in stingray skin suggest that pigment cells induce differentiation in the progenitor cells of iridophores, and that some features driving color production may be shared with bony fishes, although the lineages diverged hundreds of millions of years ago and the iridophores themselves differ drastically.
在动物中，色素以及纳米结构决定了皮肤的颜色，许多色调是通过这两种机制共同作用产生的。最近，我们在带状尾魟中发现了一种产生蓝色的新机制，这种物种的黄棕色皮肤上有电蓝色斑点。在此，我们描述了区分蓝色区域和非蓝色区域的细胞组成和结构的细微差异，首次描述了板鳃亚纲动物的色素细胞以及产生魟独特结构蓝色的纳米结构，这与制造自然界最稀有颜色的其他已知机制形成对比。在蓝色区域，上层真皮由一层色素细胞单元组成——虹彩细胞和黑素细胞紧密缠绕成簇，由胶原束构成框架——这种结构稳定性或许是皮肤颜色稳定性的根源。魟的虹彩细胞与其他脊椎动物的反光细胞明显不同，它有许多指状突起，像握紧黑色石头的拳头一样围绕着附近的黑素细胞。虹彩细胞含有包裹着鸟嘌呤纳米晶体的球形虹彩体，以三维准有序状态悬浮，由中间丝的细胞骨架连接。我们认为中间丝形成了一个具有独特光学作用的结构支架，为产生蓝色提供了关键的虹彩体间距。相比之下，黑素细胞内黑色的黑素体排列紧凑，与其作为增强蓝色饱和度的宽带吸收体的假设作用一致。幼年和成年动物的色素细胞层超微结构相似，表明皮肤颜色及其生态作用在个体发育过程中可能是一致的。在非蓝色区域，虹彩细胞被浅色细胞取代，这些浅色细胞在一些形态和纳米尺度特征上与虹彩细胞相似，但缺乏鸟嘌呤晶体，这表明这些细胞类型起源于共同的祖细胞。我们在魟皮肤中展示的特定细胞关联和结构相互作用表明，色素细胞诱导虹彩细胞祖细胞的分化，尽管这两个谱系在数亿年前就已分化，且虹彩细胞本身也有很大差异，但一些驱动颜色产生的特征可能与硬骨鱼相同。
