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Research Article

Genetic manipulation of structural color in bacterial colonies

View ORCID ProfileVillads Egede Johansen, View ORCID ProfileLaura Catón, View ORCID ProfileRaditijo Hamidjaja, Els Oosterink, View ORCID ProfileBodo D. Wilts, View ORCID ProfileTorben Sølbeck Rasmussen, Michael Mario Sherlock, Colin J. Ingham, and View ORCID ProfileSilvia Vignolini
PNAS March 13, 2018 115 (11) 2652-2657; first published February 22, 2018; https://doi.org/10.1073/pnas.1716214115
Villads Egede Johansen
aDepartment of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom;
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  • ORCID record for Villads Egede Johansen
Laura Catón
bHoekmine Besloten Vennootschap, Kenniscentrum Technologie en Innovatie, Hogeschool Utrecht, 3584 CS, Utrecht, The Netherlands;
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  • ORCID record for Laura Catón
Raditijo Hamidjaja
bHoekmine Besloten Vennootschap, Kenniscentrum Technologie en Innovatie, Hogeschool Utrecht, 3584 CS, Utrecht, The Netherlands;
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  • ORCID record for Raditijo Hamidjaja
Els Oosterink
cWageningen Food & Biobased Research, 6708 WG, Wageningen, The Netherlands;
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Bodo D. Wilts
dDepartment of Physics, University of Cambridge, Cambridge CB3 0HE, United Kingdom;
eAdolphe Merkle Institute, University of Fribourg, CH-1700 Fribourg, Switzerland;
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  • ORCID record for Bodo D. Wilts
Torben Sølbeck Rasmussen
fDepartment of Biotechnology and Biomedicine–Infection Microbiology, Technical University of Denmark, 2800 Kongens Lyngby, Denmark
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  • ORCID record for Torben Sølbeck Rasmussen
Michael Mario Sherlock
aDepartment of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom;
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Colin J. Ingham
bHoekmine Besloten Vennootschap, Kenniscentrum Technologie en Innovatie, Hogeschool Utrecht, 3584 CS, Utrecht, The Netherlands;
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  • For correspondence: sv319@cam.ac.uk colinutrecht@gmail.com
Silvia Vignolini
aDepartment of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom;
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  • ORCID record for Silvia Vignolini
  • For correspondence: sv319@cam.ac.uk colinutrecht@gmail.com
  1. Edited by David A. Weitz, Harvard University, Cambridge, MA, and approved January 17, 2018 (received for review September 25, 2017)

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Significance

We demonstrate the genetic modification of structural color in a living system by using bacteria Iridescent 1 (IR1) as a model system. IR1 colonies consist of rod-shaped bacteria that pack in a dense hexagonal arrangement through gliding and growth, thus interfering with light to give a bright, green, and glittering appearance. By generating IR1 mutants and mapping their optical properties, we show that genetic alterations can change colony organization and thus their visual appearance. The findings provide insight into the genes controlling structural color, which is important for evolutionary studies and for understanding biological formation at the nanoscale. At the same time, it is an important step toward directed engineering of photonic systems from living organisms.

Abstract

Naturally occurring photonic structures are responsible for the bright and vivid coloration in a large variety of living organisms. Despite efforts to understand their biological functions, development, and complex optical response, little is known of the underlying genes involved in the development of these nanostructures in any domain of life. Here, we used Flavobacterium colonies as a model system to demonstrate that genes responsible for gliding motility, cell shape, the stringent response, and tRNA modification contribute to the optical appearance of the colony. By structural and optical analysis, we obtained a detailed correlation of how genetic modifications alter structural color in bacterial colonies. Understanding of genotype and phenotype relations in this system opens the way to genetic engineering of on-demand living optical materials, for use as paints and living sensors.

  • genetics
  • structural color
  • Flavobacteria
  • self-organization
  • disorder

Footnotes

  • ↵1V.E.J. and L.C. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: sv319{at}cam.ac.uk or colinutrecht{at}gmail.com.
  • Author contributions: V.E.J., L.C., C.J.I., and S.V. designed research; V.E.J., L.C., R.H., E.O., B.D.W., T.S.R., M.M.S., C.J.I., and S.V. performed research; V.E.J., L.C., R.H., E.O., B.D.W., T.S.R., M.M.S., C.J.I., and S.V. analyzed data; V.E.J., L.C., C.J.I., and S.V. wrote the paper; V.E.J. planned experiments, cultivated bacteria, performed goniometry and SEM, and processed and analyzed optical/SEM data; L.C. planned and executed genetics and genomics and contributed to conclusions and writing; R.H. cultivated bacteria and performed experiments related to volatiles; B.D.W. performed optical analysis and SEM; E.O. isolated and characterized IR1; T.S.R. cultivated bacteria, fixed samples, and processed SEM images; M.M.S. cultivated bacteria and performed goniometry and subsequent analysis; S.V. performed data processing and analysis; C.J.I. performed transposon mutagenesis, fixation for SEM, SEM, genetic analysis, experimental design, and data analysis; V.E.J., L.C., C.J.I., and S.V. led the writing of the paper; and V.E.J., L.C., R.H., E.O., B.D.W., T.S.R., M.M.S., C.J.I., and S.V. discussed results and commented on the manuscript.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequence reported in this paper has been deposited in the GenBank database (accession no. NQOT00000000). Additional data related to this publication are available at the University of Cambridge data repository (doi.org/10.17863/CAM.16794).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1716214115/-/DCSupplemental.

Published under the PNAS license.

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Genetic manipulation of living bacterial color
Villads Egede Johansen, Laura Catón, Raditijo Hamidjaja, Els Oosterink, Bodo D. Wilts, Torben Sølbeck Rasmussen, Michael Mario Sherlock, Colin J. Ingham, Silvia Vignolini
Proceedings of the National Academy of Sciences Mar 2018, 115 (11) 2652-2657; DOI: 10.1073/pnas.1716214115

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Genetic manipulation of living bacterial color
Villads Egede Johansen, Laura Catón, Raditijo Hamidjaja, Els Oosterink, Bodo D. Wilts, Torben Sølbeck Rasmussen, Michael Mario Sherlock, Colin J. Ingham, Silvia Vignolini
Proceedings of the National Academy of Sciences Mar 2018, 115 (11) 2652-2657; DOI: 10.1073/pnas.1716214115
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Proceedings of the National Academy of Sciences: 115 (11)
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Article Classifications

  • Physical Sciences
  • Applied Physical Sciences
  • Biological Sciences
  • Microbiology

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  • Article
    • Abstract
    • Overview of Flavobacterium Strain and Mutants
    • Differences in Organizational Capacity Are Revealed by Electron Microscopy
    • Photonic Responses of Colonies Are Closely Related to Local Colony Organization
    • Analysis of Transposon Insertion Mutants Confirms Relation Between Motility and Structural Color
    • Not Only Motility Genes Affect Structural Coloration
    • Presence of Macroalgae Influences the Growth of Bacteria
    • Discussion
    • Materials and Methods
    • Acknowledgments
    • Footnotes
    • References
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