Nanoscale chemical imaging of bacillus subtilis spores by combining tip-enhanced raman scattering and advanced statistical tools

ACS Nano

Volumn 8, Issue 12, 2014, Pages 12300-12309

  Rusciano, Giulia ^a   Zito, Gianluigi ^a   Isticato, Rachele ^a   Sirec, Teja ^a   Ricca, Ezio ^a   Bailo, Elena ^b   Sasso, Antonio ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b WITec Wissenschaftliche Instrumente und Technologie GmbH   (Germany)

Author keywords

Bacillus subtilis; chemical imaging; principal component analysis (PCA); tip enhanced Raman scattering

Indexed keywords

BACTERIOLOGY; DATA HANDLING; DISPLAY DEVICES; DRUG DELIVERY; NANOTECHNOLOGY; PRINCIPAL COMPONENT ANALYSIS; RAMAN SCATTERING; STATISTICAL MECHANICS; SURFACE ANALYSIS;

BACILLUS SUBTILIS; BACILLUS SUBTILIS SPORES; CHEMICAL IMAGING; CHEMICAL INFORMATION; DRUG DELIVERY APPLICATIONS; HETEROGENEOUS ENVIRONMENTS; SPECTROSCOPIC TECHNIQUE; TIP-ENHANCED RAMAN SCATTERINGS;

CHEMICAL ANALYSIS;

BACILLUS SUBTILIS; BACTERIAL SPORE; NANOTECHNOLOGY; PRINCIPAL COMPONENT ANALYSIS; PROCEDURES; RAMAN SPECTROMETRY;

BACILLUS SUBTILIS; NANOTECHNOLOGY; PRINCIPAL COMPONENT ANALYSIS; SPECTRUM ANALYSIS, RAMAN; SPORES, BACTERIAL;

EID: 84919779816     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn504595k     Document Type: Article

References (68)

1. Nicholson, W. L.; Munakata, N.; Horneck, G.; Melosh, H. J.; Setlow, P. Resistance of Bacillus Endospores to Extreme Terrestrial and Extraterrestrial Environments Microbiol. Mol. Biol. Rev. 2000, 64, 548-572
2. Setlow, P. I. Will Survive: DNA Protection in Bacterial Spores Trends Microbiol. 2007, 15, 172-180
3. McKenney, P. T.; Driks, A.; Eichenberger, P. The Bacillus subtilis Spore: Assembly and Functions of the Multilayered Coat Nat. Rev. Microbiol. 2013, 11, 33-44
4. Watabe, K.; Imamura, D.; Kuwana, R.; Takamatsu, H.; Watabe, K. Proteins Involved in Formation of the Outermost Layer of Bacillus subtilis Spores J. Bacteriol. 2011, 193, 4075-4080
5. Warth, A. D.; Ohye, D. F.; Murrell, W. G. The Composition and Structure of Bacterial Spores J. Cell Biol. 1963, 16, 579-592
6. Driks, A. Bacillus subtilis Spore Coat Microbiol. Mol. Biol. Rev. 1999, 63, 1-20
7. Chen, X.; Mahadevan, L.; Driks, A.; Sahin, O. Bacillus Spores as Building Blocks for Stimuli Responsive Materials and Nanogenerators Nat. Nanotechnol. 2014, 9, 137-141
8. Hong, H. A.; Duc, L. H.; Cutting, S. M. The Use of Bacterial Spore Formers as Probiotics FEMS Microbiol. Rev. 2005, 29, 813-835
9. Stahl, S.; Uhlen, M. Bacterial Surface Display: Trends and Progresses Trends Biotechnol. 1997, 15, 185-192
10. Sirec, T.; Strazzulli, A.; Isticato, R.; De Felice, M.; Moracci, M.; Ricca, E. Adsorption of -galactosidase of Alicyclobacillus acidocaldarius on Wild Type and Mutants Spores of Bacillus subtilis Microb. Cell. Fact. 2012, 11, 100-110
11. Sirec, R.; Scotto Di Mase, D.; Mauriello, E. M. F.; De Felice, M.; Ricca, E. Amino Terminal Fusion of Heterologous Proteins to CotC Increases Display Efficiencies in the Bacillus subtilis Spore System BioTechniques 2007, 42, 151-156
12. Isticato, R.; Sirec, T.; Treppiccione, L.; Maurano, F.; De Felice, M.; Rossi, M.; Ricca, E. Non-recombinant Display of the B Subunit of the Heat Labile Toxin of Escherichia coli on Wild Type and Mutant Spores of Bacillus subtilis Microb. Cell. Fact. 2013, 12, 98-108
13. Kailas, L.; Terry, C.; Abbott, N.; Taylor, R.; Mullin, N.; Tzokov, S. B.; Todd, S. J.; Wallace, B. A.; Hobbs, J. K.; Moir, A. et al. Surface Architecture of Spores of the Bacillus Cereus/Anthracis/Thuringiensis Family at the Subnanometer Scale Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 16014-16019
14. 2) J. Appl. Microbiol. 2011, 111, 1057-1064
15. Plomp, M.; Leighton, T.; Wheeler, K. E.; Malkin, A. J. The High-Resolution Architecture and Structural Dynamics of Bacillus Spores Biophys. J. 2004, 88, 603-608
16. Yeo, B. S.; Stadler, J.; Schmid, T.; Zenobi, R.; Zhang, W. H. Tip-Enhanced Raman Spectroscopy-Its Status, Challenges and Future Directions Chem. Phys. Lett. 2009, 472, 1-13
17. Yeo, B. S.; Maedler, S.; Schmid, T.; Zhang, W. H.; Zenobi, R. Tip-Enhanced Raman Spectroscopy Can See More: The Case of Cytochrome c J. Phys. Chem. C 2008, 112, 4867-4873
18. Sonntag, M. D.; Klingsporn, J. M.; Garibay, L. K.; Roberts, J. M.; Dieringer, J. A.; Seideman, T.; Scheidt, K. A.; Jensen, L.; Schatz, G. C.; Van Duyne, R. P. Single-Molecule Tip-Enhanced Raman Spectroscopy J. Phys. Chem. C 2012, 116, 478-483
19. Stadler, J.; Schmid, T.; Zenobi, R. Nanoscale Chemical Imaging Using Top-Illumination Tip-Enhanced Raman Spectroscopy Nano Lett. 2010, 10, 4514-4520
20. Pozzi, E. A.; Sonntag, M. D.; Jiang, N.; Klingsporn, J. M.; Hersam, M. C.; Van Duyne, R. P. Tip-Enhanced Raman Imaging: An Emergent Tool for Probing Biology at the Nanoscale ACS Nano 2013, 7, 885-888
21. Treffer, R.; Bohme, R.; Deckert-Gaudig, T.; Lau, K.; Tiede, S.; Lin, X.; Deckert, V. Advances in TERS (Tip-Enhanced Raman Scattering) for Biochemical Applications Biochem. Soc. Trans. 2012, 40, 609-614
22. Sonntag, M. D.; Pozzi, E. A.; Jiang, N.; Hersam, M. C.; Van Duyne, R. V. Recent Advances in Tip-Enhanced Raman Spectroscopy J. Phys. Chem. Lett. 2014, 5, 3125-3130
23. Schmid, T.; Opilik, L.; Blum, C.; Zenobi, R. Nanoscale Chemical Imaging Using Tip-Enhanced Raman Spectroscopy: A Critical Review Angew. Chem., Int. Ed. 2013, 52, 5940-5954
24. Pahlow, S.; März, A.; Seise, B.; Hartmann, K.; Freitag, I.; Kämmer, E.; Böhme, R.; Deckert, V.; Weber, K.; Cialla, D. et al. Bioanalytical Application of Surface- and Tip-Enhanced Raman Spectroscopy Eng. Life Sci. 2012, 12, 131-143
25. Deckert-Gaudig, T.; Deckert, V. Nanoscale Structural Analysis Using Tip-Enhanced Raman Spectroscopy Curr. Opin. Chem. Biol. 2011, 15, 719-724
26. Bailo, E.; Deckert, V. Tip-Enhanced Raman Scattering Chem. Soc. Rev. 2008, 37, 921-930
27. Lipiec, E.; Sekine, R.; Bielecki, J.; Kwiatek, W. M.; Wood, R. B. Molecular Characterization of DNA Double Strand Breaks with Tip-Enhanced Raman Scattering Angew. Chem., Int. Ed. 2014, 53, 169-172
28. Ichimura, T.; Watanabe, H.; Morita, Y.; Verma, P.; Kawata, S.; Inouye, Y. Temporal Fluctuation of Tip-Enhanced Raman Spectra of Adenine Molecules J. Phys. Chem. C 2007, 111, 9460-9464
29. Treffer, R.; Lin, X.; Bailo, E.; Deckert-Gaudig, T.; Deckert, V. Distinction of Nucleobases-A Tip-Enhanced Raman Approach Beilstein J. Nanotechnol. 2011, 2, 628-637
30. Hennemann, L. E.; Meixner, A. J.; Zhang, D. Surface- and Tip Enhanced Raman Spectroscopy of DNA Spectroscopy 2010, 24, 119-124
31. Domke, K. F.; Zhang, D.; Pettinger, B. Tip-Enhanced Raman Scattering of Picomole Quantities of DNA Nucleobases at Au(1 1 1) J. Am. Chem. Soc. 2007, 129, 6708-6709
32. Rasmussen, A.; Deckert, V. Surface- and Tip-enhanced Raman Scattering of DNA Components J. Raman Spectrosc. 2006, 37, 311-317
33. Najjar, S.; Talaga, D.; Schue, L.; Coffinier, Y.; Szunerits, S.; Boukherroub, R.; Servant, L.; Rodriguez, L.; Bonhommeau, S. Tip-Enhanced Raman Spectroscopy of Combed Double-Stranded DNA Bundles J. Phys. Chem. C 2014, 118, 1174-1181
34. Zhang, D.; Domke, K.; Pettinger, B. Tip-Enhanced Raman Spectroscopic Studies of the Hydrogen Bonding Between Adenine and Thymine Adsorbed on Au(1 1 1) ChemPhysChem 2010, 11, 1662-1665
35. Kurouski, D.; Postiglione, T.; Deckert-Gaudig, T.; Deckert, V.; Lednev, I. K.; Amide, I. Vibrational Mode Suppression in Surface (SERS) and Tip (TERS) Enhanced Raman Spectra of Protein Specimens. Analyst 138, 6, 1665-1673.
36. Deckert-Gaudig, T.; Deckert, V. Tip-Enhanced Raman Scattering of Histidine on Novel Silver Substrates J. Raman. Spectrosc. 2009, 40, 1446-1451
37. Deckert-Gaudig, T.; Rauls, E.; Deckert, V. Aromatic Amino Acid Monolayers Sandwiched Between Gold and Silver: a Combined Tip-Enhanced Raman and Theoretical Approach J. Phys. Chem. C 2010, 114, 7412-7420
38. Deckert-Gaudig, T.; Kömmer, E.; Deckert, V. Tracking of Nanoscale Structural Variations on a Single Amyloid Fibril with Tip-Enhanced Raman Scattering J. Biophot. 2012, 5, 215-219
39. Schmid, T.; Messmer, A.; Yeo, B. S.; Zhang, W. H.; Zenobi, R. Towards Chemical Analysis of Nanostructures in Biofilms II: Tip-Enhanced Raman Spectroscopy of Alginates Anal. Bioanal. Chem. 2008, 391, 1907-1916
40. Kurouski, D.; Deckert-Gaudig, T.; Deckert, V.; Lednev, I. K. Surface Characterization of Insulin Protofilaments and Fibril Polymorphs Using Tip-Enhanced Raman Spectroscopy (TERS) Biophys. J. 2014, 106, 263-271
41. Cialla, D.; Deckert-Gaudig, T.; Budich, C.; Laue, M.; Möller, R.; Naumann, D.; Deckert, V.; Popp, J. Raman to the Limit: Tip-Enhanced Raman Spectroscopic Investigation of Sinlge Tobacco Mosaic Virus J. Raman. Spectrosc. 2009, 40, 240-243
42. Wood, B. R.; Bailo, E.; Khiavi, M. A.; Tilley, L.; Deed, S.; Deckert-Gaudig, T.; McNaughton, D.; Deckert, V. Tip-Enhanced Raman Scattering (TERS) from Hemozoin Crystals within a Sectioned Erythrocyte Nano Lett. 2011, 11, 1868-1873
43. Nakata, A.; Nomoto, T.; Toyota, T.; Fujinami, M. Tip-Enhanced Raman Spectroscopy of Lipid Bilayers in Water With an Alumina- and Silver-Coated Tungsten Tip Anal. Sci. 2013, 29, 865-869
44. Böhme, R.; Richter, M.; Cialla, D.; Rosch, P.; Deckert, V.; Popp, J. Towards a Specific Characterisation of Components on a Cell Surface-Combined TERS: Investigations of Lipids and Human Cells J. Raman Spectrosc. 2009, 40, 1452-1457
45. Deckert-Gaudig, T.; Böhme, R.; Freier, E.; Sebesta, A.; Merkendorf, T.; Popp, J.; Gerwert, K.; Deckert, V. Nanoscale Distinction of Membrane Patches-A TERS Study of Halobacterium Salinarum J. Biophotonics 2012, 5, 582-591
46. Neugebauer, U.; Rösch, P.; Schmitt, M.; Popp, J.; Julien, C.; Rasmussen, A.; Budich, C.; Deckert, V. On the Way to Nanometer-Sized Information of the Bacterial Surface by Tip-Enhanced Raman Spectroscopy ChemPhysChem 2006, 17, 1428-30
47. Budich, C.; Neugebauer, U.; Popp, J.; Deckert, V. Cell Wall Investigations Utilizing Tip-Enhanced Raman Scattering J. Microsc. 2008, 229, 533-539
48. Richter, M.; Hedegaard, M.; Deckert-Gaudig, T.; Lampen, P.; Deckert, V. Laterally Resolved and Direct Spectroscopic Evidence of Nanometer-Sized Lipid and Protein Domains on a Single Cell Small 2011, 7, 209-214
49. Ong, Y. H.; Lim, M.; Liu, Q. Comparison of Principal Component Analysis and Biochemical Component Analysis in Raman Spectroscopy for the Discrimination of Apoptosis and Necrosis in K562 Leukemia Cells Opt. Exp. 2012, 20, 22158-22171
50. Jolliffe, I. T. Principal Component Analysis; Springer Verlag: Berlin, 2002.
51. Rusciano, G. Experimental Analysis of Hb Oxy-Deoxy Transition in Single Optically Stretched Red Blood Cells Phys. Medica 2010, 26, 233-239
52. Sahin, O.; Yong, E. H.; Driks, A.; Mahadevan, L. Physical Basis for the Adaptive Flexibility of Bacillus Spore Coats J. R. Soc. Interface 2012, 9, 3156-3160
53. Martinez, L.; Tello, M.; Diaz, M.; Roman, E.; Garcia, R.; Huttel, Y. Aspect-Ratio and Lateral-Resolution Enhancement in Force Microscopy by Attaching Nanoclusters Generated by an Ion Cluster Source at the End of a Silicon Tip Rev. Sci. Instrum. 2011, 82, 023710/1-023710/7
54. Manzano, C. V.; Caballero-Calero, O.; Hormeno, S.; Penedo, M.; Luna, M.; Martin-Gonzalez, M. S. ZnO Morphology Control by Pulsed Electrodeposition J. Phys. Chem. C 2012, 117, 1502-1508
55. Hormeno, S.; Penedo, M.; Vicente, C.; Luna, M. Gold Nanoparticle Coated Silicon Tips for Kelvin Probe Force Microscopy in Air Nanotechnology 2013, 24, 395701-395701
56. Isticato, R.; Sirec, T.; Giglio, R.; Baccigalupi, L.; Rusciano, G.; Pesce, G.; Zito, G.; Sasso, A.; De Felice, M.; Ricca, E. Flexibility of the Prograamme of Spore Coat Formation in Bacillus subtilis: Bypass of CotE Requirement by Over-Production of CotH PLoS One 2013, 8, e74949-e74957
57. Moretti, M.; Zaccaria, R. P.; Descrovi, E.; Das, G.; Leoncini, M.; Liberale, C.; De Angelis, F.; Di Fabrizio, E. Reflection-mode TERS on Insulin Amyloid Fibrils with Top-Visual AFM Probes Plasmonics 2013, 33, 8-25
58. Novotny, L.; Hecht, B. Principles of Nano-Optics; Cambridge University Press: Cambridge, 2006.
59. Blum, C.; Opilik, L.; Metanis, N.; Weidmann, S.; Zenobi, R. Missing Amide I Mode in Tip-Enhanced Raman Spectra of Proteins J. Phys. Chem. C 2012, 116, 23061-23066
60. Blum, C.; Schmid, T.; Opilik, L.; Weidmann, S.; Fagerer, S. R.; Zenobi, R. Understanding Tip-Enhanced Raman Spectra of Biological Molecules: a Combined Raman, SERS and TERS Study J. Raman Spectrosc. 2012, 43, 1895-1904
61. Blum, C.; Opilik, L.; Atkin, J. M.; Braun, K.; Kämmer, S. B.; Kravtsov, V.; Kumar, N.; Lemeshko, S.; Li, J.; Luszcz, K. et al. Tip-Enhanced Raman Spectroscopy-An Interlaboratory Reproducibility and Comparison Study J. Raman Spectrosc. 2014, 45, 22-31
62. Waller, L. N.; Fox, N.; Fox, K. F.; Fox, A.; Price, R. L. Ruthenium Red Staining for Ultrastructural Visualization of a Glycoprotein Layer Surrounding the Spore of Bacillus anthracis and Bacillus subtilis J. Microbiol. Methods 2004, 58, 23-30
63. Alexander, T. A.; Pellegrino, P.; Gillespie, J. B. Near-Infrared Surface-Enhanced-Raman-Scattering-Mediated Detection of Single Optically Trapped Bacterial Spores Appl. Spectrosc. 2003, 57, 1340-1345
64. Chada, V. G. R.; Sanstad, E. A.; Wang, R.; Driks, A. Morphogenesis of Bacillus Spore Surfaces J. Bacteriol. 2003, 185, 6255-6261
65. Plomp, M.; McCaffery, J. M.; Cheong, I.; Huang, X.; Bettegowda, C.; Kinzler, K. W.; Zhou, S.; Vogelstein, B.; Malkin, A. J. Spore Coat Architecture of Clostridium Novyi NT Spores J. Bacteriol. 2007, 189, 6457-6468
66. Zolock, R. A.; Li, G.; Bleckmann, C.; Burggraf, L.; Fullerc, D. C. Atomic Force Microscopy of Bacillus Spore Surface Morphology Micron 2006, 9, 363-369
67. Rogers, J. L.; Nicewander, W. A. Thirteen Ways to Look at the Correlation Coefficient Am. Statist. 1995, 42, 59-66
68. www.witec.de, WITec GmbH, Ulm, Germany.