Abstract

Surface-enhanced-Raman-spectroscopy (SERS) can be made an attractive approach for the identification of Raman-active compounds and biological materials (i.e., toxins, viruses, or intact bacterial cells or spores) through development of reproducible, spatially uniform SERS-active substrates. Recently, reproducible (from substrate to substrate), spatially homogeneous (over large areas) SERS-active substrates have been commercialized and are now available in the marketplace. Scanning electron microscopy and high-resolution, tapping-mode atomic force microscopy have been used to analyze these novel plasmonic surfaces for topographical consistency. Additionally, we have assessed, by wavelength-tunable microreflectance spectrometry, the spatial distribution of the localized surface plasmon resonance (LSPR) across a single substrate surface as well as the LSPR λMAX variance from substrate to substrate. These analyses reveal that these surfaces are topologically uniform with small LSPR variance from substrate to substrate. Further, we have utilized these patterned surfaces to acquire SERS spectral signatures of four intact, genetically distinct Bacillus spore species cultivated under identical growth conditions. Salient spectral signature features make it possible to discriminate among these genetically distinct spores. Additionally, partial least squares, a multivariate calibration method, has been used to develop personal-computer-borne algorithms useful for classification of unknown spore samples based solely on SERS spectral signatures. To our knowledge, this is the first report detailing application of these commercially available SERS-active substrates to identification of intact Bacillus spores.

© 2007 Optical Society of America

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2006 (6)

J. K. Daniels, T. P. Caldwell, K. A. Christesen, and G. Chumanov, "Monitoring the kinetics of Bacillus subtilis endospore germination via surface-enhanced Raman scattering spectroscopy," Anal. Chem. 78, 1724-1729 (2006).
[CrossRef] [PubMed]

X. Zhang, J. Zhao, A. V. Whitney, J. W. Elam, and R. P. Van Duyne, "Ultrastable substrates for surface-enhanced Raman spectroscopy: Al2O3 overlayers fabricated by atomic layer deposition yield improved anthrax biomarker detection," J. Am. Chem. Soc. 128, 10304-10309 (2006).
[CrossRef] [PubMed]

D. D. Evanoff, Jr., J. Heckel, T. P. Caldwell, K. A. Christesen, and G. Chumanov, "Monitoring DPA release from a single germinating Bacillus subtilis endospore via surface-enhanced Raman scattering microscopy," J. Am. Chem. Soc. 128, 12618-12619 (2006).
[CrossRef] [PubMed]

T. Orzali, M. Casarin, G. Granozzi, M. Sambi, and A. Vittadini, "Bottom-up assembly of single-domain titania nanosheets on (1 × 2)-Pt(110)," Phys. Rev. Lett. 97, 156101 (2006).
[CrossRef] [PubMed]

N. M. B. Perney, J. J. Baumberg, M. E. Zoorob, M. D. B. Charlton, S. Mahnkopf, and C. M. Netti, "Tuning localized plasmons in nanostructured substrates for surface-enhanced Raman scattering," Opt. Express 14, 847-857 (2006).
[CrossRef] [PubMed]

S. P. Kuo, O. Tarasenko, S. Nourkbash, A. Bakhtina, and K. Levon, "Plasma effects on bacterial spores in a wet environment," New J. Phys. 8, 41-51 (2006).
[CrossRef]

2005 (7)

J. Grand, M. Lamy de la Chapelle, J.-L. Bijeon, P.-M. Adam, A. Vial, and P. Royer, "Role of localized surface plasmons in surface-enhanced Raman scattering of shape-controlled metallic particles in regular arrays," Phys. Rev. B 72, 033407 (2005).
[CrossRef]

M. Plomp, T. J. Leighton, K. E. Wheeler, and A. Malkin, "The high-resolution architectural and structural dynamics of Bacillus spores," Biophys. J. 88, 603-608 (2005).
[CrossRef]

M. B. Phillips, "Bioterrorism: a brief history," Northeast Fla. Med. 56, 32-35 (2005).

T. G. Abshire, J. E. Brown, and J. W. Ezzell, "Production and validation of the use of gamma phage for identification of Bacillus anthracis," J. Clin. Microbiol. 43, 4780-4788 (2005).
[CrossRef] [PubMed]

A. Sengupta, M. L. Laucks, and E. J. Davis, "Surface-enhanced Raman spectroscopy of bacteria and pollen," Appl. Spectrosc. 59, 1016-1023 (2005).
[CrossRef] [PubMed]

M. L. Laucks, A. Sengupta, K. Junge, E. J. Davis, and B. D. Swanson, "Comparison of psychro-active arctic marine bacteria and common mesophilic bacteria using surface-enhanced Raman spectroscopy," Appl. Spectrosc. 59, 1222-1228 (2005).
[CrossRef] [PubMed]

W. R. Premasiri, D. T. Moir, M. S. Klemper, N. Krieger, G. Jones II , and L. D. Ziegler, "Characterization of the surface enhanced Raman scattering (SERS) of bacteria," J. Phys. Chem. B 109, 312-320 (2005).
[CrossRef]

2004 (5)

P. J. Meehan, N. E. Rosenstein, M. Gillen, R. F. Meyer, M. J. Kiefer, S. Deitchman, R. E. Besser, R. L. Ehrenberg, K. M. Edwards, and K. F. Martinez for the Centers for Disease Control and Prevention, "Responding to detection of aerosolized Bacillus anthracis by autonomous detection systems in the workplace," MMWR Morb. Mortal. Wkly. Rep. 53, 1-11 (2004).

N. Nuraje, I. A. Banerjee, R. I. MacCuspie, L. Yu, and H. Matsui, "Biological bottom-up assembly of antibody nanotubes on patterned antigen arrays," J. Am. Chem. Soc. 126, 8088-8089 (2004).
[CrossRef] [PubMed]

N. Felidj, S. L. Truong, J. Aubard, G. Levi, J. R. Krenn, A. Hohenau, A. Leitner, and F. R. Aussenegg, "Gold particle interaction in regular arrays probed by surface enhanced Raman scattering," J. Chem. Phys. 120, 7141-7146 (2004).
[CrossRef] [PubMed]

R. M. Jarvis, A. Brooker, and R. Goodacre, "Surface-enhanced Raman spectroscopy for bacterial discrimination utilizing a scanning electron microscope with a Raman spectroscopy interface," Anal. Chem. 76, 5198-5202 (2004).
[CrossRef] [PubMed]

T. Kalkbrenner, U. Hakanson, and V. Sandoghdar, "Tomographic plasmon spectroscopy of a single gold nanoparticle," Nano. Lett. 4, 2309-2314 (2004).
[CrossRef]

2003 (4)

V. G. R. Chada, E. A. Sanstad, R. Wang, and A. Driks, "Morphogenesis of Bacillus spore surfaces," J. Bacteriol. 185, 6255-6261 (2003).
[CrossRef] [PubMed]

C. L. Haynes and R. P. Van Duyne, "Plasmon-sampled surface-enhanced Raman excitation spectroscopy," J. Phys. Chem. B 107, 7426-7433 (2003).
[CrossRef]

D. Whang, S. Jin, Y. Wu, and C. M. Lieber, "Large-scale hierarchical organization of nanowire arrays for integrated nanosystems," Nano. Lett. 3, 1255-1259 (2003).
[CrossRef]

T. A. Alexander, P. M. Pellegrino, and J. B. Gillespie, "Near-infrared surface-enhanced-Raman-scattering-mediated detection of single optically trapped bacterial spores," Appl. Spectrosc. 57, 1340-1345 (2003).
[CrossRef] [PubMed]

2002 (4)

B. K. De, S. L. Bragg, G. N. Sanden, K. E. Wilson, L. A. Diem, C. K. Marston, A. R. Hoffmaster, G. A. Barnett, R. S. Weyeant, T. G. Abshire, J. W. Ezzell, and T. Popovic, "Two-component direct fluorescent-antibody assay for rapid identification of Bacillus anthracis," Emerging Infect. Dis. 8, 1060-1065 (2002).
[PubMed]

T. V. Inglesby, T. O'Toole, D. A. Henderson, J. G. Bartlett, M. S. Ascher, E. Eitzen, A. M. Friedlander, J. Gerberding, J. Hauer, J. Hughes, J. E. McDade, M. T. Osterholm, G. Parker, T. M. Perl, P. K. Russell, and K. Tonat, "Anthrax as a biological weapon, 2002: updated recommendations for management," J. Am. Med. Assoc. 287, 2236-2252 (2002).
[CrossRef]

W. E. Doering and S. Nie, "Single-molecule and single-nanoparticle SERS: examining the roles of surface active sites and chemical enhancement," J. Phys. Chem. B 106, 311-317 (2002).
[CrossRef]

N. Felidj, J. Aubard, G. Levi, J. R. Krenn, G. Schider, A. Leitner, and F. R. Aussenegg, "Enhanced substrate-induced coupling in two-dimensional gold nanoparticle arrays," Phys. Rev. B 66, 245407 (2002).
[CrossRef]

2001 (3)

T. A. Alexander and C. D. Tran, "Near-infrared spectrometric determination of di- and tripeptides synthesized by a combinatorial solid-phase method," Anal. Chem. 73, 1062-1067 (2001).
[CrossRef] [PubMed]

D. T. Dennis, T. V. Inglesby, D. A. Henderson, J. G. Bartlett, M. S. Ascher, E. Eitzen, A. D. Fine, A. M. Friedlander, J. Hauer, M. Layton, S. R. Lillibridge, J. E. McDade, M. T. Osterholm, T. O'Toole, G. Parker, T. M. Perl, P. K. Russel, and K. Tonat, "Tularemia as a biological weapon: medical and public heath management," J. Am. Med. Assoc. 285, 2763-2773 (2001).
[CrossRef]

J. A. Jernigan, D. S. Stephens, D. A. Ashford, C. Omenaca, M. S. Topiel, M. Galbraith, M. Tapper, T. L. Fisk, S. Zaki, T. Popovic, R. F. Meyer, C. P. Quinn, S. A. Harper, S. K. Fridkin, J. J. Sejvar, C. W. Shephard, M. McConnell, J. Guarner, W. J. Sheih, J. M. Malecki, J. L. Berberding, J. M. Hughes, B. A. Perkins, and Members of the Anthrax Bioterrorism Investigation Team, "Bioterrorism-related inhalation anthrax: the first 10 cases reported in the United States," Emerging Infect. Dis. 7, 933-944 (2001).
[CrossRef] [PubMed]

2000 (4)

"A health warning on bioterrorism," Nature 406, 109 (2000).
[PubMed]

D. R. Walt and D. R. Franz, "Biological warfare detection," Anal. Chem. 72, 738A-746A (2000).
[PubMed]

C. Vieu, F. Carcenac, A. Pepin, Y. Chen, M. Mejias, A. Lebib, L. Manin-Ferlazzo, L. Couraud, and H. Launois, "Electron beam lithography: resolution limits and applications," Appl. Surf. Sci. 164, 111-117 (2000).
[CrossRef]

C. K. Mann and T. J. Vickers, "Chemical analysis with a low-resolution Raman spectrometer," Appl. Spectrosc. 54, 742-746 (2000).
[CrossRef]

1999 (4)

S. Christesen, B. MacIver, L. Procell, D. Sorrick, M. Carrabba, and J. Bello, "Nonintrusive analysis of chemical agent identification sets using a portable fiber-optic Raman spectrometer," Appl. Spectrosc. 53, 850-855 (1999).
[CrossRef]

J. B. Tucker, "Historical trends related to bioterrorism: an emperical analysis," Emerging Infect. Dis. 5, 498-504 (1999).
[CrossRef] [PubMed]

D. W. Siegrist, "The threat of biological attack: why concern now?" Emerging Infect. Dis. 5, 505-508 (1999).
[CrossRef] [PubMed]

J. Papaparaskevas, D. P. Houhoula, M. Papadimitriou, G. Saroglou, N. J. Legakis, and L. Zerva, "Ruling out Bacillus anthracis," Emerging Infect. Dis. 10, 732-735 (1999).

1998 (5)

A. Campion and P. Kambhampati, "Surface-enhanced Raman scattering," Chem. Soc. Rev. 27, 241-250 (1998).
[CrossRef]

M. Kahl, E. Voges, S. Kostrewa, C. Viets, and W. Hill, "Periodically structured metallic substrates for SERS," Sens. Actuators B 51, 285-291 (1998).
[CrossRef]

R. H. Clarke, S. Londhe, and M. E. Womble, "Low-resolution Raman spectroscopy as an analytical tool for organic liquids," Spectroscopy 13, 28-35 (1998).

K. Kneipp, H. Kneipp, G. Deinum, I. Itzkan, R. R. Dasari, and M. S. Feld, "Single-molecule detection of a cyanine dye in silver colloidal solution using near-infrared surface-enhanced Raman scattering," Appl. Spectrosc. 52, 175-178 (1998).
[CrossRef]

T. Baum and D. J. Schiffrin, "Mechanistic aspects on anisotropic dissolution of materials: etching of single-crystal silicon in alkaline solutions," J. Chem. Soc. Faraday Trans. 94, 691-694 (1998).
[CrossRef]

1997 (3)

J. Fruhauf and B. Hannemann, "Anisotropic multi-step etch processes of silicon," J. Micromech. Microeng. 7, 137-140 (1997).
[CrossRef]

A. G. Brolo, D. E. Irish, and J. Lipkowski, "Surface-enhanced Raman spectra of pyridine and pyrazine adsorbed on a Au(210) single-crystal electrode," J. Phys. Chem. B 101, 3906-3909 (1997).
[CrossRef]

X. Wang, H. Wen, T. He, J. Zuo, C. Xu, and L. Fan-Chen, "Enhancement mechanism of SERS from cyanine dyes adsorbed on Ag2O colloids," Spectrochim. Acta Part A 53, 2495-2504 (1997).
[CrossRef]

1985 (1)

M. Moskovits, "Surface-enhanced spectroscopy," Rev. Mod. Phys. 57, 783-826 (1985).
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Figures (9)

Fig. 1
Fig. 1

(Color online) Schematic diagram of wavelength-tunable microreflectance spectrometer.

Fig. 2
Fig. 2

A, Low-resolution (1,000× magnification) scanning electron micrograph of Au-coated, lithographically patterned substrate. B, High-resolution (10,000× magnification) scanning electron micrograph taken at a 20° angle of incidence clearly showing the inverted pyramidal motif utilized to fabricate the patterned substrate SERS-active region.

Fig. 3
Fig. 3

(Color online) A, Tapping-mode AFM cross-sectional depth profile of substrate patterned region. Pyramidal subunits begin as 1.47 μm (RSD = 1.96%) openings, which are monotonically tapered over the 1.00 μm (RSD = 3.77%) deep depression. B, Inverted AFM image of substrate, showing regularly spaced, C4v-symmetric pyramidal subunits arranged in square lattice configuration at a separation of 0.57 μm (RSD = 3.88%).

Fig. 4
Fig. 4

Representative reflectance spectra at 25 sites across a 3   mm × 3   mm area of substrate patterned surface.

Fig. 5
Fig. 5

A–C, Contour surface plot of reflectance detected at 785   nm   ( Δ ν = 0   cm 1 ) taken at 25 sites over three different substrates. D–F, Contour surface plot of reflectance detected at 898   nm   ( Δ ν = + 160 0   cm 1 ) taken at 25 sites over three different substrates.

Fig. 6
Fig. 6

NRS spectrum and SERS spectrum of 0.1 M aqueous pyridine acquired by using commercialized SERS substrate.

Fig. 7
Fig. 7

Possible orientations of a single, dry, exporium-free B. subtilis 168 spore relative to SERS substrate surface. A, Spore long axis parallel to substrate surface. B, Spore long axis perpendicular to substrate surface. Bacillus subtilis 168 spore dimensions used are 1.85 μ m × 0.71 μ m reported by Plomp et al. [53].

Fig. 8
Fig. 8

SERS spectral signatures of B. cereus (ATCC 11778), B. pumilus (ATCC 27142), B. subtilis (ATCC 6633), and B. thuringiensis (ATCC 29730) acquired by using commercialized SERS substrates.

Fig. 9
Fig. 9

A, Scores plot of normal PLS2 model, using first three calculated PCs. B, Classification of 12 unknown Bacillus spore samples, using normal PLS2 model based on seven PCs. C, Scores plot of derivatized PLS2 model using first three calculated PCs. D, Classification of 12 unknown Bacillus spore samples using derivatized PLS2 model based on 3 PCs.

Tables (1)

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Table 1 Statistical Analysis of Commercialized Substrate Based on Microreflectometry a

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