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

Author:

Zomer Aldert1ORCID,Ingham Colin J.2ORCID,von Meijenfeldt F. A. Bastiaan34ORCID,Escobar Doncel Álvaro2ORCID,van de Kerkhof Gea T.5ORCID,Hamidjaja Raditijo2ORCID,Schouten Sanne2,Schertel Lukas56,Müller Karin H.7ORCID,Catón Laura25ORCID,Hahnke Richard L.8ORCID,Bolhuis Henk4ORCID,Vignolini Silvia59,Dutilh Bas E.310ORCID

Affiliation:

1. Division of Infectious Diseases and Immunology, Utrecht University, Utrecht 3584 CL, the Netherlands

2. Hoekmine Besloten Vennootschap, Utrecht 3515 GJ, the Netherlands

3. Theoretical Biology and Bioinformatics, Department of Biology, Science for Life, Utrecht University, Utrecht 3584 CH, the Netherlands

4. Department of Marine Microbiology & Biogeochemistry, Royal Netherlands Institute for Sea Research, ‘t Horntje 1797 SZ, The Netherlands

5. Yusuf Hamied Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom

6. Department of Physics, University of Fribourg, Fribourg CH-1700, Switzerland

7. Department of Physiology, Development and Neuroscience, Cambridge Advanced Imaging Centre, University of Cambridge, Cambridge CB2 3DY, United Kingdom

8. Leibniz Institute, German Collection of Microorganisms and Cell Cultures, Braunschweig 38124, Germany

9. Sustainable and Bio-inspired Materials, Max Planck Institute of Colloids and Interfaces, Potsdam 14476, Germany

10. Institute of Biodiversity, Faculty of Biological Sciences, Cluster of Excellence Balance of the Microverse, Friedrich Schiller University Jena, Jena 07743, Germany

Abstract

Structural color is an optical phenomenon resulting from light interacting with nanostructured materials. Although structural color (SC) 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 colored 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 of cells capable of producing SC. A pan-genome-wide association approach was used to identify genes associated with SC. The biosynthesis of uroporphyrin and pterins, as well as carbohydrate utilization and metabolism, was found to be involved. Using this information, we constructed a classifier to predict SC directly from bacterial genome sequences and validated it by cultivating and scoring 100 strains that were not part of the training set. We predicted that SCr is widely distributed within gram-negative bacteria. Analysis of over 13,000 assembled metagenomes suggested 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 a large-scale ecogenomics view of SC in bacteria and identifies microbial pathways and evolutionary relationships that underlie this optical phenomenon.

Funder

ZonMw

EC | HORIZON EUROPE Framework Programme

UKRI | Biotechnology and Biological Sciences Research Council

Swiss National Science Foundation

Isaac Newton Trust

EC | European Research Council

Deutsche Forschungsgemeinschaft

Publisher

Proceedings of the National Academy of Sciences

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