Structural color in the bacterial domain: the ecogenomics of a 2-dimensional optical phenotype

Structural colour is an optical phenomenon resulting from light interacting with nanostructured materials. Although structural colour is widespread in the tree of life, the underlying genetics and genomics are not well understood. Here we collected and sequenced a set of 87 structurally coloured bacterial isolates, and 30 related strains lacking SC. Optical analysis of colonies indicated that diverse bacteria from at least two different phyla (Bacteroidetes and Proteobacteria) can create two dimensional packing capable of producing SC. Pan-genome-wide association approaches were used to identify genes associated with structural colour. The biosynthesis of uroporphyrin and pterins, as well as carbohydrate utilisation and metabolism, were found to be involved. Using this information, we constructed a classifier to predict structural colour directly from bacterial genome sequences, validated it by scoring 100 strains that were not involved in creating the structural colour classifier, and predicted that photonic structures are widely distributed within Gram-negative bacteria. Analysis of over 13 thousand assembled metagenomes predicted that SC is nearly absent from most habitats associated with multicellular organisms except macroalgae and is abundant in marine waters and surface/air interfaces. This work provides the first large-scale ecogenomics view of structural colour in bacteria and identifies microbial pathways and evolutionary relationships that underlie this optical phenomenon.

结构色（Structural colour）是一种光与纳米结构材料相互作用产生的光学现象。尽管结构色在生命之树中广泛存在，但其背后的遗传学与基因组学机制尚未得到充分阐明。本研究收集并测序了87株产结构色的细菌分离株，以及30株不具备结构色（SC）的相关菌株。对菌落的光学分析表明，来自至少两个不同门类——拟杆菌门（Bacteroidetes）与变形菌门（Proteobacteria）的多种细菌，可形成能够产生结构色的二维组装结构。本研究采用泛基因组全关联分析方法，筛选与结构色形成相关的基因，结果发现尿卟啉与蝶啶的生物合成途径，以及碳水化合物利用与代谢过程均参与其中。基于上述信息，我们构建了一个可直接通过细菌基因组序列预测结构色的分类器，并通过对100株未参与该分类器构建的菌株进行验证，最终预测光子结构在革兰氏阴性菌中广泛分布。通过对超过1.3万条组装后的宏基因组（metagenomes）序列进行分析后发现，除大型藻类（macroalgae）之外，与多细胞生物相关的多数生境中几乎不存在结构色，而其在海水及地表/空气界面生境中则大量存在。本研究首次从生态基因组学视角，系统解析了细菌结构色的大规模分布特征，并揭示了支撑该光学现象背后的微生物代谢途径与演化关联。