1887

Abstract

Iridescence is an original type of colouration that is relatively widespread in nature but has been either incompletely described or entirely neglected in prokaryotes. Recently, we reported a brilliant ‘pointillistic’ iridescence in agar-grown colony biofilms of and some other marine Flavobacteria that exhibit gliding motility. Bacterial iridescence is created by a unique self-organization of sub-communities of cells, but the mechanisms underlying such living photonic crystals are unknown. In this study, we used Petri dish assays to screen a large panel of potential activators or inhibitors of ’s iridescence. Derivatives potentially interfering with quorum-sensing and other communication or biofilm formation processes were tested, as well as metabolic poisons or algal exoproducts. We identified an indole derivative, 5-hydroxyindole (5HI, 250 µM) which inhibited both gliding and iridescence at the colonial level. 5HI did not affect growth or cell respiration. At the microscopic level, phase-contrast imaging confirmed that 5HI inhibits the gliding motility of cells. Moreover, the lack of iridescence correlated with a perturbation of self-organization of the cell sub-communities in both the WT and a gliding-negative mutant. This effect was proved using recent advances in machine learning (deep neuronal networks). In addition to its effect on colony biofilms, 5HI was found to stimulate biofilm formation in microplates. Our data are compatible with possible roles of 5HI or marine analogues in the eco-biology of iridescent bacteria.

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2018-03-01
2024-03-28
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References

  1. Parker AR. The diversity and implications of animal structural colours. J Exp Biol 1998; 201:2343–2347[PubMed]
    [Google Scholar]
  2. Welch V, Vigneron JP, 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 2006; 73:041916 [View Article][PubMed]
    [Google Scholar]
  3. Noyes J, Sumper M, Vukusic P. Light manipulation in a marine diatom. J Mater Res 2008; 23:3229–3235 [View Article]
    [Google Scholar]
  4. Gordon R, Losic D, Tiffany MA, Nagy SS, Sterrenburg FA. The glass menagerie: diatoms for novel applications in nanotechnology. Trends Biotechnol 2009; 27:116–127 [View Article][PubMed]
    [Google Scholar]
  5. Doucet SM, Meadows MG. Iridescence: a functional perspective. J R Soc Interface 2009; 6:S115–S132 [View Article][PubMed]
    [Google Scholar]
  6. Vukusic P, Science M. Evolutionary photonics with a twist. Science 2009; 325:398–399 [View Article]
    [Google Scholar]
  7. Vukusic P, Sambles JR. Photonic structures in biology. Nature 2003; 424:852–855 [View Article][PubMed]
    [Google Scholar]
  8. Pati A, Abt B, Teshima H, Nolan M, Lapidus A et al. Complete genome sequence of Cellulophaga lytica type strain (LIM-21). Stand Genomic Sci 2011; 4:221–232 [View Article][PubMed]
    [Google Scholar]
  9. Asahina AY, Hadfield MG. Complete genome sequence of Cellulophaga lytica HI1 using PacBio single-molecule real-time sequencing. Genome Announc 2014; 2:e01148-14 [View Article][PubMed]
    [Google Scholar]
  10. Chapelais-Baron M, Goubet I, Duchaud E, Rosenfeld E. Draft genome sequence of the iridescent marine bacterium Cellulophaga lytica CECT 8139. Genome Announc 2017; 5:e00811-17 [View Article][PubMed]
    [Google Scholar]
  11. Zhu Y, McBride MJ. Comparative Analysis of Cellulophaga algicola and Flavobacterium johnsoniae Gliding Motility. J Bacteriol 2016; 198:1743–1754 [View Article][PubMed]
    [Google Scholar]
  12. Johnston JJ, Shrivastava A, McBride MJ. Untangling Flavobacterium johnsoniae gliding motility and protein secretion. J Bacteriol 2018; 200:JB.00362-17e00362-17 [View Article][PubMed]
    [Google Scholar]
  13. Kientz B, Vukusic P, Luke S, Rosenfeld E. Iridescence of a marine bacterium and classification of prokaryotic structural colors. Appl Environ Microbiol 2012; 78:2092–2099 [View Article][PubMed]
    [Google Scholar]
  14. Kientz B, Marié P, Rosenfeld E. Effect of abiotic factors on the unique glitter-like iridescence of Cellulophaga lytica. FEMS Microbiol Lett 2012; 333:101–108 [View Article][PubMed]
    [Google Scholar]
  15. Kientz B, Ducret A, Luke S, Vukusic P, Mignot T et al. Glitter-like iridescence within the bacteroidetes especially Cellulophaga spp.: optical properties and correlation with gliding motility. PLoS One 2012; 7:e52900 [View Article][PubMed]
    [Google Scholar]
  16. 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 2013; 36:244–251 [View Article][PubMed]
    [Google Scholar]
  17. Kientz B, Luke S, Vukusic P, Péteri R, Beaudry C et al. A unique self-organization of bacterial sub-communities creates iridescence in Cellulophaga lytica colony biofilms. Sci Rep 2016; 6:19906 [View Article][PubMed]
    [Google Scholar]
  18. Ducret A, Maisonneuve E, Notareschi P, Grossi A, Mignot T et al. A microscope automated fluidic system to study bacterial processes in real time. PLoS One 2009; 4:e7282 [View Article][PubMed]
    [Google Scholar]
  19. Rasband WS. 1997–2016; ImageJ, U.S. National Institutes of Health, Bethesda, Maryland, USA. https://imagej.nih.gov/ij/
  20. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012; 9:676–682 [View Article][PubMed]
    [Google Scholar]
  21. Shrivastava A, Rhodes RG, Pochiraju S, Nakane D, McBride MJ. Flavobacterium johnsoniae RemA is a mobile cell surface lectin involved in gliding. J Bacteriol 2012; 194:3678–3688 [View Article][PubMed]
    [Google Scholar]
  22. Dufour V, Li J, Flint A, Rosenfeld E, Rivoal K et al. Inactivation of the LysR regulator Cj1000 of Campylobacter jejuni affects host colonization and respiration. Microbiology 2013; 159:1165–1178 [View Article][PubMed]
    [Google Scholar]
  23. Hütter E, Unterluggauer H, Garedew A, Jansen-Dürr P, Gnaiger E. High-resolution respirometry-a modern tool in aging research. Exp Gerontol 2006; 41:103–109 [View Article][PubMed]
    [Google Scholar]
  24. Lecun Y, Bengio Y, Hinton G. Deep learning. Nature 2015; 521:436–444 [View Article][PubMed]
    [Google Scholar]
  25. Krizhevsky A, Sutskever I, Hinton GE. ImageNet classification with deep convolutional neural networks. Neural Information Processing Systems (NIPS) vol. 25 2012
    [Google Scholar]
  26. Deng J, Dong W, Socher R, Lj L, Li K et al. Imagenet: a large-scale hierarchical image database. IEEE Conference on Computer Vision and Pattern Recognition 2009
    [Google Scholar]
  27. Szegedy C, Vanhoucke V, Ioffe S, Shlens J, Wojna Z. Rethinking the inception architecture for computer vision. Proceedings of IEEE Conference on Computer Vision and Pattern Recognition 20162818–2826
    [Google Scholar]
  28. Ridgway HF. Source of energy for gliding motility in Flexibacter polymorphus: effects of metabolic and respiratory inhibitors on gliding movement. J Bacteriol 1977; 131:544–556[PubMed]
    [Google Scholar]
  29. Lee JH, Wood TK, Lee J. Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol 2015; 23:707–718 [View Article][PubMed]
    [Google Scholar]
  30. Pandley R, Swamy KV, Khetmalas MB. Indole: a novel signaling molecule and its applications. Indian J Biotechnol 2013; 12:297–310
    [Google Scholar]
  31. Majumdar P, Lee E, Patel N, Ward K, Stafslien SJ et al. Combinatorial materials research applied to the development of new surface coatings IX: an investigation of novel antifouling/fouling-release coatings containing quaternary ammonium salt groups. Biofouling 2008; 24:185–200 [View Article][PubMed]
    [Google Scholar]
  32. Sokolova A, Cilz N, Daniels J, Stafslien SJ, Brewer LH et al. A comparison of the antifouling/foul-release characteristics of non-biocidal xerogel and commercial coatings toward micro- and macrofouling organisms. Biofouling 2012; 28:511–523 [View Article][PubMed]
    [Google Scholar]
  33. Thomas TR, Kavlekar DP, Lokabharathi PA. Marine drugs from sponge-microbe association-a review. Mar Drugs 2010; 8:1417–1468 [View Article][PubMed]
    [Google Scholar]
  34. Zhang W, Che Q, Tan H, Qi X, Li J et al. Marine Streptomyces sp. derived antimycin analogues suppress HeLa cells via depletion HPV E6/E7 mediated by ROS-dependent ubiquitin-proteasome system. Sci Rep 2017; 7:42180 [View Article][PubMed]
    [Google Scholar]
  35. Knowles CJ. Microorganisms and cyanide. Bacteriol Rev 1976; 40:652–680[PubMed]
    [Google Scholar]
  36. Askeland RA, Morrison SM. Cyanide production by Pseudomonas fluorescens and Pseudomonas aeruginosa. Appl Environ Microbiol 1983; 45:1802–1807[PubMed]
    [Google Scholar]
  37. Rane MR, Sarode PD, Chaudhari BL, Chincholkar SB. Exploring antagonistic metabolites of established biocontrol agent of marine origin. Appl Biochem Biotechnol 2008; 151:665–675 [View Article][PubMed]
    [Google Scholar]
  38. Guo J, Jing X, Peng WL, Nie Q, Zhai Y et al. Comparative genomic and functional analyses: unearthing the diversity and specificity of nematicidal factors in Pseudomonas putida strain 1A00316. Sci Rep 2016; 6:29211 [View Article][PubMed]
    [Google Scholar]
  39. Cugini C, Morales DK, Hogan DA. Candida albicans-produced farnesol stimulates Pseudomonas quinolone signal production in LasR-defective Pseudomonas aeruginosa strains. Microbiology 2010; 156:3096–3107 [View Article][PubMed]
    [Google Scholar]
  40. Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB et al. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 2002; 148:87–102 [View Article][PubMed]
    [Google Scholar]
  41. González JF, Venturi V. A novel widespread interkingdom signaling circuit. Trends Plant Sci 2013; 18:167–174 [View Article][PubMed]
    [Google Scholar]
  42. Patel HK, Suárez-Moreno ZR, Degrassi G, Subramoni S, González JF et al. Bacterial LuxR solos have evolved to respond to different molecules including signals from plants. Front Plant Sci 2013; 4:447 [View Article][PubMed]
    [Google Scholar]
  43. Martino PD, Fursy R, Bret L, Sundararaju B, Phillips RS. Indole can act as an extracellular signal to regulate biofilm formation of Escherichia coli and other indole-producing bacteria. Can J Microbiol 2003; 49:443–449 [View Article][PubMed]
    [Google Scholar]
  44. Lee J, Jayaraman A, Wood TK. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 2007; 7:42 [View Article][PubMed]
    [Google Scholar]
  45. Biswas NN, Kutty SK, Barraud N, Iskander GM, Griffith R et al. Indole-based novel small molecules for the modulation of bacterial signalling pathways. Org Biomol Chem 2015; 13:925–937 [View Article][PubMed]
    [Google Scholar]
  46. Bunders CA, Minvielle MJ, Worthington RJ, Ortiz M, Cavanagh J et al. Intercepting bacterial indole signaling with flustramine derivatives. J Am Chem Soc 2011; 133:20160–20163 [View Article][PubMed]
    [Google Scholar]
  47. Sabag-Daigle A, Soares JA, Smith JN, Elmasry ME, Ahmer BM. The acyl homoserine lactone receptor, SdiA, of Escherichia coli and Salmonella enterica serovar Typhimurium does not respond to indole. Appl Environ Microbiol 2012; 78:5424–5431 [View Article][PubMed]
    [Google Scholar]
  48. Kim YG, Lee JH, Cho MH, Lee J. Indole and 3-indolylacetonitrile inhibit spore maturation in Paenibacillus alvei. BMC Microbiol 2011; 11:119 [View Article][PubMed]
    [Google Scholar]
  49. Sugimori D, Sekiguchi T, Hasumi F, Kubo M, Shirasaka N et al. Microbial hydroxylation of indole to 7-hydroxyindole by Acinetobacter calcoaceticus strain 4-1-5. Biosci Biotechnol Biochem 2004; 68:1167–1169 [View Article][PubMed]
    [Google Scholar]
  50. Salamanca D, Engesser KH. Isolation and characterization of two novel strains capable of using cyclohexane as carbon source. Environ Sci Pollut Res Int 2014; 21:12757–12766 [View Article][PubMed]
    [Google Scholar]
  51. Lee J, Attila C, Cirillo SL, Cirillo JD, Wood TK. Indole and 7-hydroxyindole diminish Pseudomonas aeruginosa virulence. Microb Biotechnol 2009; 2:75–90 [View Article][PubMed]
    [Google Scholar]
  52. Lee JH, Lee J. Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 2010; 34:426–444 [View Article][PubMed]
    [Google Scholar]
  53. Lee J, Bansal T, Jayaraman A, Bentley WE, Wood TK. Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl Environ Microbiol 2007; 73:4100–4109 [View Article][PubMed]
    [Google Scholar]
  54. Treuner-Lange A, Macia E, Guzzo M, Hot E, Faure LM et al. The small G-protein MglA connects to the MreB actin cytoskeleton at bacterial focal adhesions. J Cell Biol 2015; 210:243–256 [View Article][PubMed]
    [Google Scholar]
  55. Lee Y, Yeom J, Kim J, Jung J, Jeon CO et al. Phenotypic and physiological alterations by heterologous acylhomoserine lactone synthase expression in Pseudomonas putida. Microbiology 2010; 156:3762–3772 [View Article][PubMed]
    [Google Scholar]
  56. McShan AC, Anbanandam A, Patnaik S, de Guzman RN. Characterization of the binding of hydroxyindole, indoleacetic acid, and morpholinoaniline to the salmonella type III secretion system proteins SipD and SipB. ChemMedChem 2016; 11:963–971 [View Article][PubMed]
    [Google Scholar]
  57. Netz N, Opatz T. Marine Indole Alkaloids. Mar Drugs 2015; 13:4814–4915 [View Article][PubMed]
    [Google Scholar]
  58. França PH, Barbosa DP, da Silva DL, Ribeiro ÊA, Santana AE et al. Indole alkaloids from marine sources as potential leads against infectious diseases. Biomed Res Int 2014; 2014:1–12 [View Article][PubMed]
    [Google Scholar]
  59. Lee Y-J, Lee D-G, Rho HS, Krasokhin VB, Shin HJ et al. Cytotoxic 5-Hydroxyindole Alkaloids from the Marine Sponge Scalarispongia sp. J Heterocycl Chem 2013; 50:1400–1404 [View Article]
    [Google Scholar]
  60. Lee HS, Yoon KM, Han YR, Lee KJ, Chung SC et al. 5-Hydroxyindole-type alkaloids, as Candida albicans isocitrate lyase inhibitors, from the tropical sponge Hyrtios sp. Bioorg Med Chem Lett 2009; 19:1051–1053 [View Article][PubMed]
    [Google Scholar]
  61. Mazzanti G, Piccinelli D. The occurrence of indole and imidazole compounds in marine worms and sea anemones from South Africa. Comp Biochem Physiol 1979; 63:215–219 [View Article]
    [Google Scholar]
  62. Yang Q, Pande GSJ, Wang Z, Lin B, Rubin RA et al. Indole signalling and (micro)algal auxins decrease the virulence of Vibrio campbellii, a major pathogen of aquatic organisms. Environ Microbiol 2017; 19:1987–2004 [View Article][PubMed]
    [Google Scholar]
  63. Gutierrez CK, Matsui GY, Lincoln DE, Lovell CR. Production of the phytohormone indole-3-acetic acid by estuarine species of the genus Vibrio. Appl Environ Microbiol 2009; 75:2253–2258 [View Article][PubMed]
    [Google Scholar]
  64. Dang H, Lovell CR. Microbial surface colonization and biofilm development in marine environments. Microbiol Mol Biol Rev 2016; 80:91–138 [View Article][PubMed]
    [Google Scholar]
  65. Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 2015; 522:98–101 [View Article][PubMed]
    [Google Scholar]
  66. Maruyama A, Maeda M, Simidu U. Microbial production of auxin indole-3-acetic acid in marine sediments. Mar Ecol Prog Ser 1989; 58:69–75 [View Article]
    [Google Scholar]
  67. Wang Y, Li H, Cui X, Zhang XH. A novel stress response mechanism, triggered by indole, involved in quorum quenching enzyme MomL and iron-sulfur cluster in Muricauda olearia Th120. Sci Rep 2017; 7:4252 doi [View Article][PubMed]
    [Google Scholar]
  68. Yu X, Jiang J, Liang C, Zhang X, Wang J et al. Indole affects the formation of multicellular aggregate structures in Pantoea agglomerans YS19. J Gen Appl Microbiol 2016; 62:31–37 [View Article][PubMed]
    [Google Scholar]
  69. Jaques S, Kim YK, McCarter LL. Mutations conferring resistance to phenamil and amiloride, inhibitors of sodium-driven motility of Vibrio parahaemolyticus. Proc Natl Acad Sci USA 1999; 96:5740–5745 [View Article][PubMed]
    [Google Scholar]
  70. Jaffe JD, Stange-Thomann N, Smith C, Decaprio D, Fisher S et al. The complete genome and proteome of Mycoplasma mobile. Genome Res 2004; 14:1447–1461 [View Article][PubMed]
    [Google Scholar]
  71. Hagen SJ, Son M, Weiss JT, Young JH. Bacterium in a box: sensing of quorum and environment by the LuxI/LuxR gene regulatory circuit. J Biol Phys 2010; 36:317–327 [View Article][PubMed]
    [Google Scholar]
  72. Defoirdt T, Crab R, Wood TK, Sorgeloos P, Verstraete W et al. Quorum sensing-disrupting brominated furanones protect the gnotobiotic brine shrimp Artemia franciscana from pathogenic Vibrio harveyi, Vibrio campbellii, and Vibrio parahaemolyticus isolates. Appl Environ Microbiol 2006; 72:6419–6423 [View Article][PubMed]
    [Google Scholar]
  73. Brameyer S, Kresovic D, Bode HB, Heermann R. Dialkylresorcinols as bacterial signaling molecules. Proc Natl Acad Sci USA 2015; 112:572–577 [View Article][PubMed]
    [Google Scholar]
  74. Mart'ianov SV, Zhurina MV, Él'-Registan GI, Plakunov VK. [Activation of formation of bacterial biofilms by azithromycin and prevention of this effect]. Mikrobiologiia 2015; 84:27–36[PubMed]
    [Google Scholar]
  75. Scoffone VC, Chiarelli LR, Makarov V, Brackman G, Israyilova A et al. Discovery of new diketopiperazines inhibiting Burkholderia cenocepacia quorum sensing in vitro and in vivo. Sci Rep 2016; 6:32487 [View Article][PubMed]
    [Google Scholar]
  76. Rajput A, Kaur K, Kumar M. SigMol: repertoire of quorum sensing signaling molecules in prokaryotes. Nucleic Acids Res 2016; 44:D634-9D634–D639 [View Article][PubMed]
    [Google Scholar]
  77. Dagorn A, Hillion M, Chapalain A, Lesouhaitier O, Duclairoir Poc C et al. Gamma-aminobutyric acid acts as a specific virulence regulator in Pseudomonas aeruginosa. Microbiology 2013; 159:339–351 [View Article][PubMed]
    [Google Scholar]
  78. Ojima Y, Nunogami S, Taya M. Antibiofilm effect of warfarin on biofilm formation of Escherichia coli promoted by antimicrobial treatment. J Glob Antimicrob Resist 2016; 7:102–105 [View Article][PubMed]
    [Google Scholar]
  79. Jang IA, Kim J, Park W. Endogenous hydrogen peroxide increases biofilm formation by inducing exopolysaccharide production in Acinetobacter oleivorans DR1. Sci Rep 2016; 6:21121 [View Article][PubMed]
    [Google Scholar]
  80. Gerwick WH, Lang NJ. Structural, chemical and ecological studies on iridescence in iridaea (Rhodophyta). J Phycol 1977; 13:121–127 [View Article]
    [Google Scholar]
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