A unique self-organization of bacterial sub-communities creates iridescence in Cellulophaga lytica colony biofilms

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Kientz, Betty ^a   Luke, Stephen ^b   Vukusic, Peter ^b   Péteri, Renaud ^a   Beaudry, Cyrille ^a   Renault, Tristan ^c   Simon, David ^a   Mignot, Tâm ^d   Rosenfeld, Eric ^a  

^a UNIVERSITÉ DE LA ROCHELLE   (France)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c IFREMER   (France)

^d AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFILM; CELL POPULATION; CELLULOPHAGA; IRIDESCENCE; MICROBIOLOGY; MODEL; PERIODICITY; COLOR; FLAVOBACTERIACEAE; LIGHT; PHYSIOLOGY; ULTRASTRUCTURE;

BIOFILMS; COLOR; FLAVOBACTERIACEAE; IRIDESCENCE; LIGHT;

EID: 84964309684     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep19906     Document Type: Article

References (48)

1. Barott, K. et al. Hyperspectral and Physiological Analyses of Coral-Algal Interactions. Plos One 4, e8043 (2009).
2. Wiedenmann, J., Oswald, F. & Nienhaus, G. U. Fluorescent proteins for live cell imaging: opportunities, limitations, and challenges. IUBMB Life 61, 1029-1042 (2009).
3. Widder, E. A. Bioluminescence in the ocean: origins of biological, chemical, and ecological diversity. Science 328, 704-708 (2010).
4. Doucet, S. M. & Meadows, M. G. Iridescence: a functional perspective. J. R. Soc. Interface 6, 115-132 (2009).
5. Vukusic, P. Materials science. Evolutionary photonics with a twist. Science 325, 398-399 (2009).
6. Vukusic, P. & Sambles, J. R. Photonic structures in biology. Nature 424, 852-855 (2003).
7. Parker, A. R. The diversity and implications of animal structural colours. J. Exp. Biol. 201, 2343-2347 (1998).
8. Welch, V., Vigneron, J. P., Lousse, V. & Parker, A. Optical properties of the iridescent organ of the comb-jellyfish Beroë cucumis (Ctenophora). Phys. Rev. E. Stat. Nonlin. Soft Matter Phys. 73, 041916 (2006).
9. Levy-Lior, A. et al. Guanine-Based Biogenic Photonic-Crystal Arrays in Fish and Spiders. Adv. Funct. Mater., 20, 320-329, doi: 10.1002/adfm.200901437 (2010).
10. Jordan, T. M., Partridge, J. C. & Roberts, N. W. Non-polarizing broadband multilayer reflectors in fish. Nat. Photonics. 6, 759-763, doi: 10.1038/nphoton.2012.260 (2012).
11. Brady, P. C., Travis, K. A., Maginnis, T. & Cummings, M. E. Polaro-cryptic mirror of the lookdown as a biological model for open ocean camouflage. Proc. Natl. Acad. Sci. USA. 110, 9764-9769, doi: 10.1073/pnas.1222125110 (2013).
12. Holt, A. L., Vahidinia, S., Gagnon, Y. L., Morse, D. E. & Sweeney, A. M. Photosymbiotic giant clams are transformers of solar flux. J. R. Soc. Interface. 11, 20140678 (2014).
13. Li, L. et al. A highly conspicuous mineralized composite photonic architecture in the translucent shell of the blue-rayed limpet. Nat. Commun. 6, 6322, doi: 10.1038/ncomms7322 (2015).
14. Gerwick, W. H. & Lang, N. J. Structural, chemical and ecological studies on iridescence in Iridaea (Rhodophyta). J. Phycol. 13, 121-127 (1977).
15. Craigie, J. S., Correa, J. A. & Gordon, M. E. Cuticles from Chondrus crispus (Rhodophyta). J. Phycol. 28, 777-786 (1992).
16. Noyes, J., Sumper, M. & Vukusic, P. Light manipulation in a marine diatom. J. Mater. Res. 23, 3229-3232 (2008).
17. Gordon, R., Losic, D., Tiffany, M. A., Nagy, S. S. & Sterrenburg, F. A. S. The glass menagerie: diatoms for novel applications in nanotechnology. Trends Biotechnol. 27, 116-127 (2009).
18. Williams, R. C. & Smith, K. M. The polyhedral form of the Tipula iridescent virus. Biochim. Biophys. Acta 28, 464-469 (1958).
19. Kientz, B., Vukusic, P., Luke, S. & Rosenfeld, E. Iridescence of a marine bacterium and classification of prokaryotic structural colors. Appl. Environ. Microbiol. 78, 2092-2099 (2012).
20. Pijper, A. Diffraction phenomena in cultures of microorganisms. Med. J. S. Afr. 14, 211-218 (1918).
21. Pijper, A. Diffraction in biological structures. I. The structure of colonies of the Coli-Typhoid group. S. Afr. Med. Rec. 17, 243-248 (1923).
22. Pijper, A. Diffraction in biological structures. III. The relative diameters of members of the Coli-Typhoid group. S. Afr. Med. Rec. 23, 453-462 (1925).
23. Ponder, E. Diffraction patterns produced by bacteria. J. Exp. Biol. 11, 54-57 (1934).
24. Guillot, M. Relation entre certaines propriétés optiques des bactéries et leur forme géométrique vraie. Diffraction de la lumière par les cultures et symétrie de la bactérie. C. R. Acad. Sci. 1100-1103 (1941).
25. Guillot, M. Critères physiques d'homogénéité d'une culture de microbes vivants. C. R. Soc. Biol. 720-721 (1942).
26. Engboek, H. C. The phenomenon of iridescence in bacterial cultures, with particular reference to Pfeiffer's bacillus. Acta Path. Micro. 27, 388-393 (1950).
27. Nogrady, G. & Guérault, A. Conditions favorisant l'iridescence bactérienne et l'observation du phénomène. Rev. Can. Biol. 23, 367-373 (1964).
28. Wensinck, F., van Dalen, A. & Wedema, M. Iridescent material and the effect of iron on its production by Pseudomonas aeruginosa. Antonie van Leeuwenhoek 33, 73-86 (1967).
29. D'Argenio, D. A. et al. Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol. Microbiol. 64, 512-533 (2007).
30. Schafhauser, J. et al. The stringent response modulates 4-hydroxy-2-alkylquinoline biosynthesis and quorum-sensing hierarchy in Pseudomonas aeruginosa. J. Bacteriol. 196, 1641-1650 (2014).
31. Vignolini, S. et al. Pointillist structural color in Pollia fruit. Proc. Natl. Acad. Sci. USA. 109, 15712-15715, doi: 10.1073/pnas.1210105109 (2012).
32. Kientz, B., Marié, P. & Rosenfeld, E. Effect of abiotic factors on the unique glitter-like iridescence of Cellulophaga lytica. FEMS Microbiol. Lett. 333, 101-108 (2012).
33. Kientz, B. et al. Glitter-like iridescence within the bacteroidetes especially Cellulophaga spp.: optical properties and correlation with gliding motility. Plos One 7, e52900 (2012).
34. Kientz, B., Agogué, H., Lavergne, C., Marié, P. & Rosenfeld, E. Isolation and distribution of iridescent Cellulophaga and other iridescent marine bacteria from the Charente-Maritime coast, French Atlantic. Syst. Appl. Microbiol. 36, 244-251(2013).
35. Pati, A. et al. Complete genome sequence of Cellulophaga lytica type strain (LIM-21). Stand. Genomic Sci. 4, 221-232 (2011).
36. Petroff, A. P., Wu, X. L. & Libchaber, A. Fast-moving bacteria self-organize into active two-dimensional crystals of rotating cells. Phys. Rev. Lett. 114, 158102 (2015).
37. Lewin, R. A. & Lounsbery, D. M. Isolation, cultivation and characterization of flexibacteria. Microbiology 58, 145-170 (1969).
38. Johansen, J. E., Nielsen, P. & Sjøholm, C. Description of Cellulophaga baltica gen. nov., sp. nov. and Cellulophaga fucicola gen. nov., sp. nov. and reclassification of [Cytophaga] lytica to Cellulophaga lytica gen. nov., comb. nov. Int. J. Syst. Evol. Micr. 49, 1231-1240 (1999).
39. Jensen, P. R., Kauffman, C. A. & Fenical, W. High recovery of culturable bacteria from the surfaces of marine algae. Mar. Biol. 126, 1-7 (1996).
40. Renault, T., Le Deuff R.-M., Cochennec, N. & Maffart, P. Herpes viruses associated with mortalities among Pacific oyster, Crassostrea gigas, in France - Comparative study. Revue Méd. Vét. 145, 735-742 (1994).
41. Gonzalez, R. C., Woods, R. E. & Eddins, S. L. In Digital Image Processing Using MATLAB. Prentice-Hall, Inc., Upper Saddle River, NJ, USA (2003).
42. Serra, J. P. & Soille, P. 1994. In Mathematical Morphology And Its Applications To Image Processing (Kluwer Academic Publishers, 1994).
43. Otsu, N. A threshold selection method from gray-level histograms. IEEE Trans. Sys. Man. Cyber. 9, 62-66, doi: 10.1109/TSMC.1979.4310076 (1979).
44. Duda, R. O. & Hart, P. E. Use of the Hough Transformation to Detect Lines and Curves in Pictures. Comm. ACM 15, 11-15 (1972).
45. Lee, T.-M. et al. Optical Characterization of Contrast Agents for Optical Coherence Tomography. Proc. of SPIE 4967, 129-134 (2003).
46. Leis, A. P., Schlicher, S., Franke, H. & Strathmann, M. Optically transparent porous medium for nondestructive studies of microbial biofilm architecture and transport dynamics. Appl. Environ. Microbiol. 71, 4801-4808 (2005).
47. Valkenburg, J. A. & Woldringh, C. L. Phase separation between nucleoid and cytoplasm in Escherichia coli as defined by immersive refractometry. J. Bacteriol. 160, 1151-1157 (1984).
48. Ross, K. F. A. & Billing, E. The water and Solid Content of Bacterial Spores and Vegetative Cells as Indicated by Refractive Index Measurements. J. Gen. Microbiol. 16, 418-425 (1957).