Silver, in the form of nanostructures, is widely employed as an antimicrobial agent. The origin of the biocidal mechanism has been elucidated in the last decades, originating from silver cation release due to oxidative dissolution followed by cellular uptake of silver ions, a process that causes a severe disruption of bacterial metabolism, leading to eradication. Despite the large body of work addressing the effects of nanosilver shape/size on the antibacterial mechanism and on the (bio)physical chemistry pathways that drive bacterial eradication, little effort has been devoted to the investigation of nanostructured silver plasmon response upon interaction with bacteria. We investigate the bacteria-induced changes of the plasmonic response of silver nanoplates after exposure to the bacterial model Escherichia coli. Ultrafast pump-probe measurements indicate that the dramatic changes on particle size/shape and crystallinity, which likely stem from a bacteria-induced oxidative dissolution process, translate into a clear modification of the plasmonic response. Specifically, exposure to bacteria causes a decrease in the electron–phonon coupling time and an increase in lattice-environment coupling time, effects explained by an increase in the free electron density and amorphization of the silver particles. Coherent oscillations that are observed in pristine silver are completely damped in contaminated samples, which can be attributed again to amorphization of the nanoplates at the surface and an increase in polydispersivity of particle geometries. This study opens innovative avenues in the biophysics of bio-responsive materials, with the aim of providing reliable biophysical signatures of the interaction of plasmonic materials with complex biological environments.
References
1.
S.
Chernousova
and M.
Epple
, “Silver as antibacterial agent: Ion, nanoparticle, and metal
,” Angew. Chem. Int. Ed. Engl.
52
, 1636
–1653
(2013
).2.
Z.-m.
Xiu
, Q.-b.
Zhang
, H. L.
Puppala
, V. L.
Colvin
, and P. J. J.
Alvarez
, “Negligible particle-specific antibacterial activity of silver nanoparticles
,” Nano Lett.
12
, 4271
–4275
(2012
).3.
B.
Le Ouay
and F.
Stellacci
, “Antibacterial activity of silver nanoparticles: A surface science insight
,” Nano Today
10
, 339
–354
(2015
).4.
Q. L.
Feng
, J.
Wu
, G. Q.
Chen
, F. Z.
Cui
, T. N.
Kim
, and J. O.
Kim
, “A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus
,” J. Biomed. Mater. Res.
52
, 662
–668
(2000
).5.
J. A.
Lemire
, J. J.
Harrison
, and R. J.
Turner
, “Antimicrobial activity of metals: Mechanisms, molecular targets and applications
,” Nat. Rev. Microbiol.
11
, 371
–384
(2013
).6.
L.
Rizzello
and P. P.
Pompa
, “Nanosilver-based antibacterial drugs and devices: Mechanisms, methodological drawbacks, and guidelines
,” Chem. Soc. Rev.
43
, 1501
–1518
(2014
).7.
M. A.
Cazalilla
, J. S.
Dolado
, A.
Rubio
, and P.
Echenique
, “Plasmonic excitations in noble metals: The case of Ag
,” Phys. Rev. B Condens. Matter Mater. Phys.
61
, 8033
–8042
(2000
).8.
K. B.
Mogensen
and K.
Kneipp
, “Size-dependent shifts of plasmon resonance in silver nanoparticle films using controlled dissolution: Monitoring the onset of surface screening effects
,” J. Phys. Chem. C
118
, 28075
–28083
(2014
).9.
G. M.
Paternò
, L.
Moscardi
, S.
Donini
, D.
Ariodanti
, I.
Kriegel
, M.
Zani
, E.
Parisini
, F.
Scotognella
, and G.
Lanzani
, “Hybrid one-dimensional plasmonic-photonic crystals for optical detection of bacterial contaminants
,” J. Phys. Chem. Lett.
10
, 4980
–4986
(2019
).10.
G. M.
Paternò
, L.
Moscardi
, S.
Donini
, A. M.
Ross
, S. M.
Pietralunga
, N.
Dalla Vedova
, S.
Normani
, I.
Kriegel
, G.
Lanzani
, and F.
Scotognella
, “Integration of bio-responsive silver in 1D photonic crystals: Towards the colorimetric detection of bacteria
,” Faraday Discuss.
223
, 125
–135
(2020
).11.
S.
Normani
, N. D.
Vedova
, G.
Lanzani
, F.
Scotognella
, and G. M.
Paternò
, “Design of 1D photonic crystals for colorimetric and ratiometric refractive index sensing
,” Opt. Mater.: X
8
, 100058
(2020
).12.
G. M.
Paternò
, G.
Manfredi
, F.
Scotognella
, and G.
Lanzani
, “Distributed Bragg reflectors for the colorimetric detection of bacterial contaminants and pollutants for food quality control
,” APL Photonics
5
, 080901
(2020
).13.
T. C.
Dakal
, A.
Kumar
, R. S.
Majumdar
, and V.
Yadav
, “Mechanistic basis of antimicrobial actions of silver nanoparticles
,” Front. Microbiol.
7
, 1831
(2016
).14.
A. M.
El Badawy
, R. G.
Silva
, B.
Morris
, K. G.
Scheckel
, M. T.
Suidan
, and T. M.
Tolaymat
, “Surface charge-dependent toxicity of silver nanoparticles
,” Environ. Sci. Technol.
45
, 283
–287
(2011
).15.
W. J.
Stark
, “Nanoparticles in biological systems
,” Angew. Chem. Int. Ed. Engl.
50
, 1242
–1258
(2011
).16.
M.
Rai
, A.
Yadav
, and A.
Gade
, “Silver nanoparticles as a new generation of antimicrobials
,” Biotechnol. Adv.
27
, 76
–83
(2009
), arXiv:NIHMS150003.17.
S.
Pal
, Y. K.
Tak
, and J. M.
Song
, “Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli
,” Appl. Environ. Microbiol.
73
, 1712
–1720
(2007
), arXiv:8.18.
R. D.
Kent
and P. J.
Vikesland
, “Controlled evaluation of silver nanoparticle dissolution using atomic force microscopy
,” Environ. Sci. Technol.
46
, 6977
–6984
(2012
).19.
X.
Zhang
, E. M.
Hicks
, J.
Zhao
, G. C.
Schatz
, and R. P.
Van Duyne
, “Electrochemical tuning of silver nanoparticles fabricated by nanosphere lithography
,” Nano Lett.
5
, 1503
–1507
(2005
).20.
J.
Limwongyut
, C.
Nie
, A. S.
Moreland
, and G. C.
Bazan
, “Molecular design of antimicrobial conjugated oligoelectrolytes with enhanced selectivity toward bacterial cells
,” Chem. Sci.
11
, 8138
(2020
).21.
A. J.
Kora
and L.
Rastogi
, “Enhancement of antibacterial activity of capped silver nanoparticles in combination with antibiotics, on model gram-negative and gram-positive bacteria
,” Bioinorg. Chem. Appl.
2013
, 1
–7
.22.
N.
Murthy
and H.
Minor
, “General procedure for evaluating amorphous scattering and crystallinity from X-ray diffraction scans of semicrystalline polymers
,” Polym.
31
, 996
–1002
(1990
).23.
J.
Liu
, D. A.
Sonshine
, S.
Shervani
, and R. H.
Hurt
, “Controlled release of biologically active silver from nanosilver surfaces
,” ACS Nano
4
, 6903
–6913
(2010
).24.
G. S.
Métraux
and C. A.
Mirkin
, “Rapid thermal synthesis of silver nanoprisms with chemically tailorable thickness
,” Adv. Mater.
17
, 412
–415
(2005
).25.
C.
Xue
and C. A.
Mirkin
, “pH-switchable silver nanoprism growth pathways
,” Angew. Chem. Int. Ed. Engl.
46
, 2036
–2038
(2007
).26.
Z.
Yi
, X.
Xu
, X.
Wu
, C.
Chen
, X.
Li
, B.
Luo
, J.
Luo
, X.
Jiang
, W.
Wu
, Y.
Yi
, and Y.
Tang
, “Silver nanoplates: Controlled preparation, self-assembly, and applications in surface-enhanced Raman scattering
,” Appl. Phys. A: Mater. Sci. Process.
110
, 335
–342
(2013
).27.
A.
Panáček
, L.
Kvítek
, M.
Smékalová
, R.
Večeřová
, M.
Kolář
, M.
Röderová
, F.
Dyčka
, M.
Šebela
, R.
Prucek
, O.
Tomanec
, and R.
Zbořil
, “Bacterial resistance to silver nanoparticles and how to overcome it
,” Nat. Nanotechnol.
13
, 65
–71
(2018
).28.
N. E.
Christensen
, “The band structure of silver and optical interband transitions
,” Phys. Status Solidi B
54
, 551
–563
(1972
).29.
R.
Rosei
, “Temperature modulation of the optical transitions involving the Fermi surface in Ag: Theory
,” Phys. Rev. B
10
, 474
–483
(1974
).30.
C.
Voisin
, N.
Del Fatti
, D.
Christofilos
, and F.
Vallée
, “Ultrafast electron dynamics and optical nonlinearities in metal nanoparticles
,” J. Phys. Chem. B
105
, 2264
–2280
(2001
).31.
R. H.
Groeneveld
, R.
Sprik
, and A.
Lagendijk
, “Femtosecond spectroscopy of electron–electron and electron-phonon energy relaxation in Ag and Au
,” Phys. Rev. B
51
, 11433
–11445
(1995
).32.
F.
Scotognella
, G.
Della Valle
, A. R.
Srimath Kandada
, M.
Zavelani-Rossi
, S.
Longhi
, G.
Lanzani
, and F.
Tassone
, “Plasmonics in heavily-doped semiconductor nanocrystals
,” Eur. Phys. J. B
86
, 154
(2013
).33.
L. T. M. I.
Kaganov
and I. M.
Lifshitz
, “Relaxation between electrons and the crystalline lattice
,” JEPT
4
, 173
(1957
).34.
C.-K.
Sun
, F.
Vallée
, L. H.
Acioli
, E. P.
Ippen
, and J. G.
Fujimoto
, “Femtosecond-tunable measurement of electron thermalization in gold
,” Phys. Rev. B
50
, 15337
–15348
(1994
).35.
G. D.
Valle
, M.
Conforti
, S.
Longhi
, G.
Cerullo
, and D.
Brida
, “Real-time optical mapping of the dynamics of nonthermal electrons in thin gold films
,” Phys. Rev. B Condens. Matter Mater. Phys.
86
, 1
–6
(2012
).36.
P. B.
Johnson
and R. W.
Christy
, “Optical constants of the noble metals
,” Phys. Rev. B
6
, 4370
–4379
(1972
).37.
Y.
Hamanaka
, A.
Nakamura
, S.
Omi
, N.
Del Fatti
, F.
Vallée
, and C.
Flytzanis
, “Ultrafast response of nonlinear refractive index of silver nanocrystals embedded in glass
,” Appl. Phys. Lett.
75
, 1712
–1714
(1999
).38.
A.
Henglein
, “Physicochemical properties of small metal particles in solution: ‘Microelectrode’ reactions, chemisorption, composite metal particles, and the atom-to-metal transition
,” J. Phys. Chem.
97
, 5457
–5471
(1993
).39.
N.
Del Fatti
, C.
Voisin
, D.
Christofilos
, F.
Vallée
, and C.
Flytzanis
, “Acoustic vibration of metal films and nanoparticles
,” J. Phys. Chem. A
104
, 4321
–4326
(2000
).40.
S.
Link
and M. A.
El-Sayed
, “Simulation of the optical absorption spectra of gold nanorods as a function of their aspect ratio and the effect of the medium dielectric constant
,” J. Phys. Chem. B
109
, 10531
–10532
(2005
).41.
C.-K.
Tsung
, X.
Kou
, Q.
Shi
, J.
Zhang
, M. H.
Yeung
, J.
Wang
, and G. D.
Stucky
, “Selective shortening of single-crystalline gold nanorods by mild oxidation
,” J. Am. Chem. Soc.
128
, 5352
–5353
(2006
).42.
K.-S.
Lee
and M. A.
El-Sayed
, “Gold and silver nanoparticles in sensing and imaging: sensitivity of plasmon response to size, shape, and metal composition
,” J. Phys. Chem. B
110
, 19220
–19225
(2006
).43.
G. V.
Hartland
, “Optical studies of dynamics in noble metal nanostructures
,” Chem. Rev.
111
, 3858
–3887
(2011
).44.
T.
Stoll
, P.
Maioli
, A.
Crut
, N. D.
Fatti
, and F.
Vallée
, “Advances in femto-nano-optics: Ultrafast nonlinearity of metal nanoparticles
,” Eur. Phys. J. B
87
, 260
(2014
).45.
C.
Catania
, A. W.
Thomas
, and G. C.
Bazan
, “Tuning cell surface charge in E. coli with conjugated oligoelectrolytes
,” Chem. Sci.
7
, 2023
–2029
(2016
).46.
T.
Qiu
and C.
Tien
, “Short-pulse laser heating on metals
,” Int. J. Heat Mass Transfer
35
, 719
–726
(1992
).47.
L.
Jiang
and H. L.
Tsai
, “Improved two-temperature model and its application in ultrashort laser heating of metal films
,” J. Heat Transfer
127
, 1167
–1173
(2005
).48.
R. H.
Groeneveld
, R.
Sprik
, and A.
Lagendijk
, “Ultrafast relaxation of electrons probed by surface plasmons at a thin silver film
,” Phys. Rev. Lett.
64
, 784
–787
(1990
).49.
S.
Link
and M. A.
El-Sayed
, “Spectral properties and relaxation dynamics of surface plasmon electronic oscillations in gold and silver nanodots and nanorods
,” J. Phys. Chem. B
103
, 8410
–8426
(1999
).50.
A.
Arbouet
, C.
Voisin
, D.
Christofilos
, P.
Langot
, N. D.
Fatti
, F.
Vallée
, J.
Lermé
, G.
Celep
, E.
Cottancin
, M.
Gaudry
, M.
Pellarin
, M.
Broyer
, M.
Maillard
, M. P.
Pileni
, and M.
Treguer
, “Electron-phonon scattering in metal clusters
,” Phys. Rev. Lett.
90
, 177401
(2003
).51.
G. V.
Hartland
, “Measurements of the material properties of metal nanoparticles by time-resolved spectroscopy
,” Phys. Chem. Chem. Phys.
6
, 5263
–5274
(2004
).52.
M. B.
Mohamed
, T. S.
Ahmadi
, S.
Link
, M.
Braun
, and M. A.
El-Sayed
, “Hot electron and phonon dynamics of gold nanoparticles embedded in a gel matrix
,” Chem. Phys. Lett.
343
, 55
–63
(2001
).53.
M.
Hu
and G. V.
Hartland
, “Heat dissipation for Au particles in aqueous solution: Relaxation time versus size
,” J. Phys. Chem. B
106
, 7029
–7033
(2002
).54.
M.
Nisoli
, S.
De Silvestri
, A.
Cavalleri
, A. M.
Malvezzi
, A.
Stella
, G.
Lanzani
, P.
Cheyssac
, and R.
Kofman
, “Coherent acoustic oscillations in metallic nanoparticles generated with femtosecond optical pulses
,” Phys. Rev. B
55
, R13424
–R13427
(1997
).55.
N.
Del Fatti
, C.
Voisin
, F.
Chevy
, F.
Vallée
, and C.
Flytzanis
, “Coherent acoustic mode oscillation and damping in silver nanoparticles
,” J. Chem. Phys.
110
, 11484
–11487
(1999
).56.
W.
Qian
, L.
Lin
, Y. J.
Deng
, Z. J.
Xia
, Y. H.
Zou
, and G. K. L.
Wong
, “Femtosecond studies of coherent acoustic phonons in gold nanoparticles embedded in TiO2 thin films
,” J. Appl. Phys.
87
, 612
–614
(2000
).57.
G. V.
Hartland
, “Coherent vibrational motion in metal particles: Determination of the vibrational amplitude and excitation mechanism
,” J. Chem. Phys.
116
, 8048
–8055
(2002
).58.
H.
Petrova
, C. H.
Lin
, S.
De Liejer
, M.
Hu
, J. M.
McLellan
, A. R.
Siekkinen
, B. J.
Wiley
, M.
Marquez
, Y.
Xia
, J. E.
Sader
, and G. V.
Hartland
, “Time-resolved spectroscopy of silver nanocubes: Observation and assignment of coherently excited vibrational modes
,” J. Chem. Phys.
126
, 094709
(2007
).© 2021 Author(s). Published under an exclusive license by AIP Publishing.
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