Detection and imaging of quorum sensing in Pseudomonas aeruginosa biofilm communities by surface-enhanced resonance Raman scattering

Nature Materials

Volumn 15, Issue 11, 2016, Pages 1203-1211

  Bodelón, Gustavo ^a   Montes García, Verónica ^a   López Puente, Vanesa ^a   Hill, Eric H ^b   Hamon, Cyrille ^b   Sanz Ortiz, Marta N ^b   Rodal Cedeira, Sergio ^a   Costas, Celina ^a   Celiksoy, Sirin ^a   Pérez Juste, Ignacio ^a   Scarabelli, Leonardo ^b   La Porta, Andrea ^b   Pérez Juste, Jorge ^a   Pastoriza Santos, Isabel ^a   Liz Marzán, Luis M ^a,c,d  

^a UNIVERSITY OF VIGO   (Spain)

^b CIC BIOMAGUNE   (Spain)

^c BASQUE FOUNDATION FOR SCIENCE   (Spain)

^d BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOFILMS; CELL SIGNALING; PLASMONS; RAMAN SCATTERING;

ANALYTICAL APPROACH; BACTERIAL POPULATION; CELL-TO-CELL COMMUNICATION; INTERCELLULAR COMMUNICATIONS; INTERCELLULAR SIGNALLING; LABEL-FREE DETECTION; PSEUDOMONAS AERUGINOSA; SURFACE-ENHANCED RESONANCE RAMAN SCATTERING;

SURFACE SCATTERING;

BIOFILM; CYTOLOGY; MOLECULAR IMAGING; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; RAMAN SPECTROMETRY;

BIOFILMS; MOLECULAR IMAGING; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; SPECTRUM ANALYSIS, RAMAN;

EID: 84981187589     PISSN: 14761122     EISSN: 14764660     Source Type: Journal    
DOI: 10.1038/nmat4720     Document Type: Article

References (65)

1. Waters, C. M. & Bassler, B. L. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319-346 (2005).
2. Lazdunski, A. M., Ventre, I. & Sturgis, J. N. Regulatory circuits and communication in gram-negative bacteria. Nature Rev. Microbiol. 2, 581-592 (2004).
3. Rutherford, S. T. & Bassler, B. L. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2, a012427 (2012).
4. LaSarre, B. & Federle, M. J. Exploiting quorum sensing to confuse bacterial pathogens. Microbiol. Mol. Biol. Rev. 77, 73-111 (2013).
5. Hall-Stoodley, L., Costerton, J. W. & Stoodley, P. Bacterial biofilms: from the natural environment to infectious diseases. Nature Rev. Microbiol. 2, 95-108 (2004).
6. Davey, M. E. & O'toole, G. A. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64, 847-867 (2000).
7. Li, Y. H. & Tian, X. L. Quorum sensing and bacterial social interactions in biofilms. Sensors 12, 2519-2538 (2012).
8. Parsek, M. R. & Greenberg, E. P. Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol. 13, 27-33 (2005).
9. Rybtke, M., Hultqvist, L. D., Givskov, M. & Tolker-Nielsen, T. Pseudomonas aeruginosa biofilm infections: community structure, antimicrobial tolerance and immune response. J. Mol. Biol. 427, 3628-3645 (2015).
10. Jimenez, P. N. et al. The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev. 76, 46-65 (2012).
11. Castillo-Juarez, I. et al. Role of quorum sensing in bacterial infections. World J. Clin. Cases 3, 575-598 (2015).
12. Decho, A. W., Norman, R. S. & Visscher, P. T. Quorum sensing in natural environments: emerging views from microbial mats. Trends Microbiol. 18, 73-80 (2010).
13. Steindler, L. & Venturi, V. Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiol. Lett. 266, 1-9 (2007).
14. Jansson, J. K. Marker and reporter genes: illuminating tools for environmental microbiologists. Curr. Opin. Microbiol. 6, 310-316 (2003).
15. Moskovits, M. Surface-enhanced Raman spectroscopy: A brief retrospective. J. Raman Spectrosc. 36, 485-496 (2005).
16. Stiles, P. L., Dieringer, J. A., Shah, N. C. & Van Duyne, R. R. Surface-enhanced Raman spectroscopy. Annu. Rev. Anal. Chem. 1, 601-626 (2008).
17. Schlucker, S. Surface-enhanced Raman spectroscopy: concepts and chemical applications. Angew. Chem. Int. Ed. 53, 4756-4795 (2014).
18. Anker, J. N. et al. Biosensing with plasmonic nanosensors. Nature Mater. 7, 442-453 (2008).
19. Bantz, K. C. et al. Recent progress in SERS biosensing. Phys. Chem. Chem. Phys. 13, 11551-11567 (2011).
20. Abalde-Cela, S. et al. Surface-enhanced Raman scattering biomedical applications of plasmonic colloidal particles. J. R. Soc. Interface 7, S435-S450 (2010).
21. Alvarez-Puebla, R. A. & Liz-Marzan, L. M. SERS-based diagnosis and biodetection. Small 6, 604-610 (2010).
22. Howes, P. D., Chandrawati, R. & Stevens, M. M. Colloidal nanoparticles as advanced biological sensors. Science 346, 1247390 (2014).
23. Zeng, S. W., Baillargeat, D., Ho, H. P. & Yong, K. T. Nanomaterials enhanced surface plasmon resonance for biological and chemical sensing applications. Chem. Soc. Rev. 43, 3426-3452 (2014).
24. Pierson, L. S. & Pierson, E. A. Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl. Microbiol. Biotechnol. 86, 1659-1670 (2010).
25. Mavrodi, D. V. et al. Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J. Bacteriol. 183, 6454-6465 (2001).
26. Dietrich, L. E. P. et al. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61, 1308-1321 (2006).
27. Dietrich, L. E. P., Teal, T. K., Price-Whelan, A. & Newman, D. K. Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321, 1203-1206 (2008).
28. Ramos, I., Dietrich, L. E. P., Price-Whelan, A. & Newman, D. K. Phenazines a-ect biofilm formation by Pseudomonas aeruginosa in similar ways at various scales. Res. Microbiol. 161, 187-191 (2010).
29. Dietrich, L. E. P. et al. Bacterial community morphogenesis is intimately linked to the intracellular redox state. J. Bacteriol. 195, 1371-1380 (2013).
30. Price-Whelan, A., Dietrich, L. E. & Newman, D. K. Rethinking secondary' metabolism: physiological roles for phenazine antibiotics. Nature Chem. Biol. 2, 71-78 (2006).
31. Lee, J. & Zhang, L. H. The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6, 26-41 (2015).
32. Wu, X. M. et al. Culture-free diagnostics of Pseudomonas aeruginosa infection by silver nanorod array based SERS from clinical sputum samples. Nanomedicine 10, 1863-1870 (2014).
33. Lopez-Puente, V. et al. Plasmonic mesoporous composites as molecular sieves for SERS detection. J. Phys. Chem. Lett. 4, 2715-2720 (2013).
34. Yang, S., Dai, X., Boschitsch Stogin, B. &Wong, T. Ultrasensitive surface-enhanced Raman scattering detection in common fluids. Proc. Natl Acad. Sci. USA 113, 268-273 (2015).
35. Hamon, C. et al. Hierarchical self-assembly of gold nanoparticles into patterned plasmonic nanostructures. ACS Nano 8, 10694-10703 (2014).
36. Reszka, K. J. et al. Oxidation of pyocyanin, a cytotoxic product from Pseudomonas aeruginosa, by microperoxidase 11 and hydrogen peroxide. Free Radic. Biol. Med. 36, 1448-1459 (2004).
37. Lebeaux, D., Chauhan, A., Rendueles, O. & Beloin, C. From in vitro to in vivo models of bacterial biofilm-related infections. Pathogens 2, 288-356 (2013).
38. Coenye, T. & Nelis, H. J. In vitro and in vivo model systems to study microbial biofilm formation. J. Microbiol. Methods 83, 89-105 (2010).
39. Koley, D., Ramsey, M. M., Bard, A. J. &Whiteley, M. Discovery of a biofilm electrocline using real-time 3D metabolite analysis. Proc. Natl Acad. Sci. USA 108, 19996-20001 (2011).
40. Bellin, D. L. et al. Integrated circuit-based electrochemical sensor for spatially resolved detection of redox-active metabolites in biofilms. Nature Commun. 5, 3256 (2014).
41. Pedersen, S. S., Shand, G. H., Hansen, B. L. & Hansen, G. N. Induction of experimental chronic Pseudomonas-aeruginosa lung infection with Pseudomonas-aeruginosa entrapped in alginate microspheres. APMIS 98, 203-211 (1990).
42. Leevy, W. M., Serazin, N. & Smith, B. D. Optical imaging of bacterial infection models. Drug Discov. Today Dis. Models 4, 91-97 (2007).
43. Hunter, R. C. et al. Phenazine content in the cystic fibrosis respiratory tract negatively correlates with lung function and microbial complexity. Am. J. Respir. Cell Mol. Biol. 47, 738-745 (2012).
44. Reuter, K., Steinbach, A. & Helms, V. Interfering with bacterial quorum sensing. Perspect. Medicin. Chem. 8, 1-15 (2016).
45. O'Loughlin, C. T. et al. A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc. Natl Acad. Sci. USA 110, 17981-17986 (2013).
46. Welsh, M. A., Eibergen, N. R., Moore, J. D. & Blackwell, H. E. Small molecule disruption of quorum sensing cross-regulation in Pseudomonas aeruginosa causes major and unexpected alterations to virulence phenotypes. J. Am. Chem. Soc. 137, 1510-1519 (2015).
47. Dai, T. H. et al. Animal models of external traumatic wound infections. Virulence 2, 296-315 (2011).
48. Wessel, A. K., Hmelo, L., Parsek, M. R. &Whiteley, M. Going local: technologies for exploring bacterial microenvironments. Nature Rev. Microbiol. 11, 337-348 (2013).
49. Connell, J. L. et al. Real-time monitoring of quorum sensing in 3D-printed bacterial aggregates using scanning electrochemical microscopy. Proc. Natl Acad. Sci. USA 111, 18255-18260 (2014).
50. Buenger, D., Topuz, F. & Groll, J. Hydrogels in sensing applications. Prog. Polym. Sci. 37, 1678-1719 (2012).
51. Weibel, D. B., DiLuzio, W. R. &Whitesides, G. M. Microfabrication meets microbiology. Nature Rev. Microbiol. 5, 209-218 (2007).
52. Tian, L. et al. Plasmonic biofoam: A versatile optically active material. Nano Lett. 16, 609-616 (2016).
53. Hamon, C. et al. Hierarchical organization and molecular di-usion in gold nanorod/silica supercrystal nanocomposites. Nanoscale 8, 7914-7922 (2016).
54. Falconnet, D., Csucs, G., Grandin, H. M. & Textor, M. Surface engineering approaches to micropattern surfaces for cell-based assays. Biomaterials 27, 3044-3063 (2006).
55. Shao, Y. & Fu, J. P. Integrated micro/nanoengineered functional biomaterials for cell mechanics and mechanobiology: A materials perspective. Adv. Mater. 26, 1494-1533 (2014).
56. Mitragotri, S. & Lahann, J. Physical approaches to biomaterial design. Nature Mater. 8, 15-23 (2009).
57. Watrous, J. D. & Dorrestein, P. C. Imaging mass spectrometry in microbiology. Nature Rev. Microbiol. 9, 683-694 (2011).
58. Fang, J. S. & Dorrestein, P. C. Emerging mass spectrometry techniques for the direct analysis of microbial colonies. Curr. Opin. Microbiol. 19, 120-129 (2014).
59. Wang, C., Flynn, N. T. & Langer, R. Controlled structure and properties of thermoresponsive nanoparticle-hydrogel composites. Adv. Mater. 16, 1074-1079 (2004).
60. Scarabelli, L., Grzelczak, M. & Liz-Marzan, L. M. Tuning gold nanorod synthesis through prereduction with salicylic acid. Chem. Mater. 25, 4232-4238 (2013).
61. Crepaldi, E. L. et al. Controlled formation of highly organized mesoporous titania thin films: from mesostructured hybrids to mesoporous nanoanatase TiO2. J. Am. Chem. Soc. 125, 9770-9786 (2003).
62. Dong Qin, Y. X. &Whitesides, G. M. Soft lithography for micro-and nanoscale patterning. Nature Protoc. 5, 491-502 (2010).
63. McDonald, J. C. et al. Fabrication of microfluidic systems in poly(dimethylsiloxane). Electrophoresis 21, 27-40 (2000).
64. Alvarez-Puebla, R. A. et al. Au@pNIPAM colloids as molecular traps for surface-enhanced, spectroscopic, ultra-sensitive analysis. Angew. Chem. Int. Ed. 48, 138-143 (2009).
65. Kern, S. E. & Newman, D. K. Measurement of phenazines in bacterial cultures. Methods Mol. Biol. 1149, 303-310 (2014).