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.

结构色是一种由光与纳米结构材料相互作用而产生的光学现象。尽管结构色在生命之树上普遍存在，但其背后的遗传学和基因组学尚未得到充分理解。本研究收集并测序了87种结构色细菌分离株以及30种缺乏结构色的相关菌株。对菌落的光学分析表明，至少来自两个不同的门（拟杆菌门和Bacteroidetes）的多种细菌能够形成二维堆积，从而产生结构色。通过全基因组关联方法，我们识别了与结构色相关的基因。研究发现，尿卟啉和卟啉的生物合成、碳水化合物利用和代谢过程均与此现象相关。基于此信息，我们构建了一个分类器，可直接从细菌基因组序列中预测结构色，并通过对100个未参与构建结构色分类器的菌株进行评分来验证其有效性，预测光子结构在革兰氏阴性菌中广泛分布。对超过13,000个组装的宏基因组进行分析，预测结构色在大多数与多细胞生物相关的生境中几乎不存在，除了大型海藻，而在海洋水和表面/空气界面中丰富。本研究为细菌中结构色的首次大规模生态基因组学研究提供了视角，并确定了支撑这一光学现象的微生物途径和进化关系。