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.
| Original language | English |
|---|---|
| Article number | e2309757121 |
| Number of pages | 11 |
| Journal | Proceedings of the National Academy of Sciences of the United States of America |
| Volume | 121 |
| Issue number | 29 |
| DOIs | |
| Publication status | Published - 11 Jul 2024 |
Bibliographical note
Publisher Copyright:© 2024 the Author(s). Published by PNAS.
Funding
ACKNOWLEDGMENTS. We thank Jens Harder, Anne Olsen, J-P Bernadet, Eric Duchaud, Francois Thomas, Gurvan Michel, Jeffrey Gralnick, and Lars Jelsbak for strains and information on phenotyping. We also thank the MBA Lab, Plymouth (UK), and CNRS Roscoff (FR) for access to sampling facilities via the ASSEMBLE Plus program of the EU and the iLAB, Utrecht, for access to lab facilities (Hoekmine).This project has received funding from the European Union\u2019s Horizon 2020 research and innovation program under Marie Sk\u0142odowska-Curie grant agreement No 860125 (C.J.I., A.E.D., and S.V.), ZonMW Enabling Technologies Hotels grant 40-43500-98-4102/435004516 (H.B.),BBSRC UKiCASE fellowship 2110570 (L.C.), the EU\u2019s Horizon 2020 Research and Innovation program under Marie Sk\u0142odowska-Curie grant agreement No. 722842 (ITN Plant-inspired and Surfaces\u2013PlaMatSu) (G.T.v.d.K.), the Swiss NSF under project P2ZHP2_183998 (L.S.), the Isaac Newton Trust (grant SNSF3) (L.S.), the Swiss NSF SNSF 40B1-0_198708 (L.S.), the European Research Council (ERC) Consolidator grant 865694: DiversiPHI (BED), the (ERC) Consolidator grant 101001637: BiTe (L.C.and S.V.),the BBSRC grant BB/V00364X/1 (L.C.and S.V.),the Alexander von Humboldt Foundation in the context of an Alexander von Humboldt-Professorship founded by German Federal Ministry of Education and Research (BED),and the Deutsche Forschungsgemeinschaft (DFG,German Research Foundation) under Germany\u2019s Excellence Strategy\u2014EXC 2051\u2014Project-ID 390713860. This material reflects only the author\u2019s views,and the European Union is not liable for any use that may be made of the information contained therein. We thank Jens Harder, Anne Olsen, J-P Bernadet, Eric Duchaud, Francois Thomas, Gurvan Michel, Jeffrey Gralnick, and Lars Jelsbak for strains and information on phenotyping. We also thank the MBA Lab, Plymouth (UK), and CNRS Roscoff (FR) for access to sampling facilities via the ASSEMBLE Plus program of the EU and the iLAB, Utrecht, for access to lab facilities (Hoekmine). This project has received funding from the European Union\u2019s Horizon 2020 research and innovation program under Marie Sk\u0142odowska-Curie grant agreement No 860125 (C.J.I., A.E.D., and S.V.), ZonMW Enabling Technologies Hotels grant 40-43500-98-4102/435004516 (H.B.), BBSRC UK iCASE fellowship 2110570 (L.C.), the EU\u2019s Horizon 2020 Research and Innovation program under Marie Sk\u0142odowska-Curie grant agreement No. 722842 (ITN Plant-inspired and Surfaces\u2013PlaMatSu) (G.T.v.d.K.), the Swiss NSF under project P2ZHP2_183998 (L.S.), the Isaac Newton Trust (grant SNSF3) (L.S.), the Swiss NSF SNSF 40B1-0_198708 (L.S.), the European Research Council (ERC) Consolidator grant 865694: DiversiPHI (BED), the (ERC) Consolidator grant 101001637: BiTe (L.C. and S.V.), the BBSRC grant BB/V00364X/1 (L.C. and S.V.), the Alexander von Humboldt Foundation in the context of an Alexander von Humboldt-Professorship founded by German Federal Ministry of Education and Research (BED), and the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany\u2019s Excellence Strategy\u2014EXC 2051\u2014Project-ID 390713860. This material reflects only the author\u2019s views, and the European Union is not liable for any use that may be made of the information contained therein.
| Funders | Funder number |
|---|---|
| BED | |
| Centre National de la Recherche Scientifique | |
| Bundesministerium für Bildung und Forschung | |
| European Commission | |
| Isaac Newton Trust | |
| Alexander von Humboldt-Stiftung | |
| Swiss NSF SNSF | 40B1-0_198708 |
| European Research Council | BB/V00364X/1, 865694, 101001637 |
| Biotechnology and Biological Sciences Research Council | 2110570 |
| Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung | P2ZHP2_183998 |
| Horizon 2020 Framework Programme | 860125 |
| EU’s Horizon 2020 Research and Innovation program | 722842 |
| ZonMW Enabling Technologies Hotels | 40-43500-98-4102/435004516 |
| Deutsche Forschungsgemeinschaft | 390713860 |
Keywords
- Bacteria/genetics
- Bacteroidetes/genetics
- Color
- Genome, Bacterial
- Genome-Wide Association Study
- Metagenome
- Phenotype
- Phylogeny
- Proteobacteria/genetics