Photonic Crystals for Optical Detection of

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Biophysical Chemistry, Biomolecules, and Biomaterials; Surfactants and Membranes

Hybrid 1D Plasmonic/Photonic Crystals for Optical Detection of Bacterial Contaminants Giuseppe M. Paterno, Liliana Moscardi, Stefano Donini, Davide Ariodanti, Ilka Kriegel, Maurizio Zani, Emilio Parisini, Francesco Scotognella, and Guglielmo Lanzani J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.9b01612 • Publication Date (Web): 13 Aug 2019 Downloaded from pubs.acs.org on August 13, 2019

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The Journal of Physical Chemistry Letters

Hybrid 1D Plasmonic/Photonic Crystals for Optical Detection of Bacterial Contaminants Giuseppe Maria Paternò1†*, Liliana Moscardi1,2†, Stefano Donini1, Davide Ariodanti3, Ilka Kriegel4, Maurizio Zani2, Emilio Parisini1, Francesco Scotognella1,2 and Guglielmo Lanzani1,2* 1Center

for Nano Science and Technology@PoliMi, Istituto Italiano di Tecnologia, Via Giovanni Pascoli, 70/3, 20133 Milano,

Italy; 2Dipartimento

di Fisica, Politecnico di Milano, Piazza Leonardo da Vinci 32, 20133 Milano, Italy.

3Dipartimento

di Chimica, Materiali e Ingegneria Chimica "Giulio Natta", Piazza Leonardo da Vinci 32, 20133 Milano, Italy.

4Department †These

of Nanochemistry, Istituto Italiano di Tecnologia (IIT), via Morego, 30, 16163 Genova, Italy

authors contributed equally to this work

* Corresponding authors Keywords: Responsive Photonics; Plasmonics; Bacterial contaminants; Antibacterial; Silver

Abstract. Photonic crystal-based biosensors hold great promise as low-cost devices for real-time monitoring of a variety of bio-targets, i.e., bacterial contaminants in food. Here, we report the proof of concept for a new colorimetric sensor of bacterial contamination, which is based on a novel hybrid plasmonic/photonic device. Our system consists of a layer of silver, a plasmonic metal exhibiting a well known bio-activity, on top of a 1D photonic crystal. We attribute the bioresponsivity to the formation of polarization charges at the Ag/bacterium interface within a sort of “bio-doping” mechanism. Interestingly, this triggers a blue-shift in the photonic response. As an example, we assessed the validity of our approach by detecting one of the most hazardous contaminant, Escherichia coli. This work demonstrates that our device can be a low-cost and portable platform for the detection of common bacterial contaminants.

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The integration of sensing elements with photonic crystals (PhCs) allows a simple readout of the detection event, often based on color changing, fostering applications in portable, and cheap technologies.1–5 For instance, photonic sensing might be of particular interest for the detection of contaminants or pathogenic bacteria in food and water, as in this case the vast majority of the existing detection systems are relatively time- and money-consuming mostly due to complexity of the read-out.6,7 Briefly, the periodicity in the dielectric constant along 1, 2 or 3 spatial dimensions gives rise to a forbidden gap for photons (stop-band) of specific wavelengths that, in turns, confers structural reflection colors to the material.8 Focusing on the simplest case of one-dimensional photonic crystals (also known as Bragg stacks, BSs) in which the stop-band arises from the alternation of layers with high/low refractive index, the structural color can be easily tuned by varying either the dielectric contrast or the periodicity of the alternated layers (or both). This can be achieved by the introduction of a medium within the 1D structure,9,10 as enabled by porosity at the meso/nanoscale in the BSs.11–19 To further enhance selectivity and to detect large or complex analytes (i.e., bacteria and biomolecules) it is also possible to chemically functionalize the surface of porous BS,20–22 although such a step would hamper easy scalability of the process. To this end, the fabrication of photonic sensors from scalable and low-cost procedures allowing fast and reliable detection of contaminants (i.e. in food and water) is highly desirable.23 In this context, our recent work has been focused on the development of responsive BSs made of alternating layer of dielectric materials and electro-optical responsive plasmonic materials, which are fabricated from easy and low-cost solution-based processes. In particular, the integration of metal plasmonic systems in PhCs provides both high sensitivity to environmental changes as well peculiar sensing capabilities

24,25

due to the specific metal

interactions.26–28 Carrier density modulation results in the change of the refractive index that ultimately determines the photonic stop-band, thus offering a handle for easy optical detection. We have shown that such peculiar feature of plasmonic materials can be exploited to build-up electro-optical switches based on the photonic reflection shift upon photo-electro doping of indium tin oxide (ITO) nanoparticles (NPs) in SiO2/ITO and TiO2/ITO photonic crystals,29,30 and electro doping of silver NPs in TiO2/Ag crystals31. Furthermore, the specific interactions occurring at the metal surface in contact with the analytes can be exploited for label-free and 2 ACS Paragon Plus Environment

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low-cost (bio)sensing purposes.32,33 It is well known that silver films and NPs exhibit antibacterial properties.34–38 Although the exact antibacterial mechanism is still under debate39 (see the supporting information for a brief discussion on Ag bactericidal mechanism), many reports agree that electrostatic attraction between the bacterial cell wall is crucial for the Ag adhesion to the bacterial membrane and to the consequent bactericidal activity possibly mediated by transmembrane ion penetration.38,40–42 Interestingly, this might lead to a modification of Ag charge carriers density and plasmon resonance upon bacteria/Ag interaction, for example as a result of polarization 43 charges accumulating at the bacteria/Ag interface. Here, we show that a novel hybrid plasmonic/photonic device consisting of a thin layer of silver deposited on top of a solution processed BS is responsive to bacterial contamination. In particular, we assessed the validity of our approach by detecting one of the most hazardous Gram-negative bacterial contaminant in food and water, Escherichia coli. Our data suggest that the increase in the plasmon charge density likely originates from the formation of polarization charges at the bacterium/Ag interface, resulting in a blue-shift of the plasmon resonance. This, in turns, eventually determines a change in the overall photonic response (blue-shift) that translates the broad plasmonic effect into a more spectrally precise read-out, as determined by the photonic reflection color. These promising results indicate that hybrid plasmonic/photonic PhCs can represent a novel class of low-cost devices responsive to common contaminants in food and water. The multilayered 1D photonic structures show the expected structural color in reflection (5 × SiO2/TiO2 bilayers) as shown in figure 1a-b, while electron microscopy images are reported in figure S1. The BSs were fabricated via simple spin-coating deposition of the respective aqueous colloidal dispersions. This is a key point in the view to scale the process by means of large-area and low-cost deposition techniques, such as ink-jet printing and roll-to-roll. On top of the dielectric BS we deposited a thin layer of silver (8 nm, Fig. S1b for the electron microscopy image), to exploit both the plasmonic behaviour and the marked and well-documented bioactivity. The thin silver layer is in-fact a defective cap layer of the photonic crystal that affects the optical response of the BS through the silver free carrier density (Drude model).44 Therefore, the main idea here is to exploit the possible change in the silver complex dielectric function driven by Ag/bacteria interaction to modify the dielectric properties at the BS/metal 3 ACS Paragon Plus Environment


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interface and, thus, the BS optical read-out. To this end, we firstly selected the minimum Ag thickness achievable with our deposition apparatus to localize strongly the plasmonic response in close proximity to the BS interface. To observe both the plasmonic and the photonic contributions to the overall sample transmission and disentangle them, we carried out measurements as a function of incidence angle (Fig. 1c). These data show a blue-shift of the photonic band-gap (PBG, 586 nm at 0°) by increasing the angle in agreement with the BraggSnell law (inset Fig. 1c),24 while the plasmonic peak at 500 nm does not display any angular dependence.

Figure 1. Hybrid plasmonic/photonic devices. (A) Picture of the fabricated 1D photonic crystal with a 8 nm silver capping layer and (B) sketch of the multilayered structure. (C) Light transmission of the Ag/(SiO2/TiO2)5 photonic crystals as a function of the light incidence angle (inset Bragg-Snell equation). PBG stands for photonic band-gap

To evaluate the effect of bacteria on the optical properties of silver, we employed a standard agar disk test, in which we spread the bacterial suspension in the culture medium (Luria-Bertani broth, LB) on agar gel at one specific concentration (0.5 OD600 corresponding to 1.12x107 colony-forming unit/mL) and exposed our samples to such contaminated surface. Note that we selected a bacterial concentration usually employed for challenge studies on real food matrices.45 We first exposed Ag films to LB only (control experiment) and then to E. coli (Fig. 2a), as described in the experimental section. We observe that the sample exposed to LB undergoes a substantial red-shift (+ 60 nm) that is likely due to the infiltration of the aqueous culture medium across the silver grains, leading to an increase in the effective refractive index.46 On the other hand, when the Ag layer is contaminated with E. coli in LB medium (Fig. 2b) we note the concomitant increase (+25%) of the plasmonic absorption at the high energy side (330 440 nm) and an attenuated red-shift (+ 35 nm) with respect to LB only exposure. Taken together, 4 ACS Paragon Plus Environment

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these data indicate an overall blue-shift (-25 nm) in the Ag plasmonic response upon contamination with E. coli. Furthermore, to mimic exposure to contaminated liquid samples, we dipped them either in LB medium (control) or in an LB/E. coli mixture with increasing bacterial loading (0.1, 0.5 and 1.2 OD600nm corresponding to 1.4x106 cfu/mL, 1.12x107 cfu/mL and 3.7x107 cfu/mL, respectively) and measured their plasmonic response (Fig. S2). Here, we essentially observed an analogous effect, with an increased plasmonic blue-shift upon exposure to bacteria that, interestingly, can be already noticed at the lowest loading (-15 nm at 0.1 OD600nm). In this scenario, we hypothesize that the bacteria-induced blue-shift in the plasmon resonance could stem from the formation of polarization charges at the silver-bacterium interface, i.e. negative on bacterial membrane41 and positive charges on Ag surface respectively (see Fig. 2c), finally leading to an overall increase of the charge carrier density.29,31 By employing the Lorentz-Drude model (Fig. 2d), we estimated that the 25 nm blue-shift observed experimentally corresponds to a 15% increase in the charge carried density of Ag in LB medium.

Figure 2. Plasmonic response upon bacterial contamination. (A) Average optical absorption (with standard deviation) of Ag thin films (8 nm on glass) before (green) and after exposure to either LB (orange line) or to (B) LB/E. coli (blue line) on agar plate (12 samples, two replicas). (C) Pictorial representation of the hypothesized mechanism giving rise to the plasmonic blue-



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shift (polarization accumulation charge). (D) Calculated transmission of the Ag layer for the pristine and “bio-doped” Ag layer in LB medium obtained by using the Lorentz-Drude model.

After having investigated the Ag plasmonic response of metallic film alone upon contamination with E. coli, we proceeded to study how this is affecting the all optical read-out in presence of the photonic crystal (Fig. 3a,b). Qualitatively, both exposure to LB or E. coli + LB leads to the same behavior, namely decreased transmittance, resonance broadening (20 nm) and red-shift of the stop-band. Again, we have two physical phenomena concurring to these changes: i) infiltration of LB inside the porous BS architecture, leading to an enhanced effective refractive index and ii) the modulation of the plasmon resonance in the top metal layer. The magnitude of the PBG red-shift, however, results decreased in presence of E. coli in LB, featuring an average shift of 5 nm compared to LB alone with + 15 nm. Interestingly, this yields an overall PBG blueshift of -10 nm upon contamination. Although the photonic response does not amplify the plasmonic blue-shift, the photonic structure would be beneficial for the optical detection for two main reasons: i. it can permit to engineer spectrally the overall optical read-out as one can place the photonic reflection virtually in any spectral region; ii. the color purity of the photonic response, whose reflection band is narrower and better defined (FWHM = 130 nm) than the broadband absorption spectrum of Ag thin films (FWHM = 330 nm). We reckon that this are key parameters to consider in the view to exploit this concept for easy colorimetric detection of bacterial contaminants. The presence of a well-defined zone of inhibition matching the shape of our samples in conformal contact with the agar medium inoculated with E. coli confirms the anti-bacterial activity of our Ag layer (Fig. S3). Furthermore, this effect seems to be confined within the sample area, suggesting that silver does not appreciably detach from the surface and diffuse in all the agar plate as it occurs with silver NPs,47 which may be of importance when considering possible applications of these devices in food packaging as an on-off indicator of bacterial contamination.48 To study the optical response of Ag/PhCs in contact with contaminated liquid specimens, we also immersed our samples in LB medium or E. coli/LB (10 minutes) and measured their optical transmission (Fig. S4). Although in this case the effect might appear less evident due the massive and unavoidable LB infiltration throughout the porous structure, we can still observe a decreased red-shift for the contaminated samples when compared to the LB case, an effect that can be already noted at the lowest bacterial loading (-10 nm for 0.1 OD600nm) in 6 ACS Paragon Plus Environment

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analogy with the plasmonic response. Furthermore, as a control experiment, we repeated the same procedure in contaminated agar plate on identical 1D photonic crystals but without the top Ag layer, in order to further prove the role of the plasmonic material in the bio-responsivity of our device (Fig. 3c,d). Here, we could not discriminate any difference between the samples exposed to LB or to LB/E. coli, with the exception of the usual read-shift (average shift = + 6 nm) and broadening of the stop-band that are connected to liquid condensation and infiltration throughout the porous structure. This confirms that the upper plasmonic layer represents the responsivity element of our hybrid plasmonic/photonic device, as the modification of the dielectric properties at the Ag/BS interface, which in turns is brought about by Ag/bacteria interaction, and governs the total optical read-out. With the aim to evaluate preliminary the possible selectivity of our device, we exposed our hybrid photonic structure to a Gram-positive bacterium, namely Micrococcus luteus (Fig. S5). One of the main difference between Gramnegative (i.e., E. coli) and Gram-positive bacteria lies on the bacterial cell envelope. In particular, Gram-negative bacteria possess a complex outer membrane (OM) consisting of an inner phospholipidic leaflet, while the outer leaflet is predominantly composed of lipopolysaccharides.49,50 On the other hand, Gram-positive bacteria expose a thick layer of peptidoglycan to the extracellular medium.41 It has been demonstrated that Ag is more active against Gram-negative bacteria than the Gram-positive counterparts, an effect that likely stems from the electrostatic interaction between the negatively charged functional groups in the OM and the Ag+.51 Interestingly, we found that the samples exposed to Micrococcus luteus undergo only a differential -3 nm shift if compared to the devices treated with the culture medium only (tryptone soya broth, TSB), confirming the relatively less efficient bioactivity of Ag against Gram-negative bacteria. In general, these data suggest that the plasmonic/photonic shift does not simply relate to a change on the refractive index environment (i.e., n passing from ≈ 1.33 in the aqueous culture medium to n ≈ 1.39 of E. coli52 or to n ≈ 1.38 of common Gram-positive bacteria53), but most probably originates from a specific interaction between the plasmonic surface and the bacterium cell envelope. We are currently planning additional measurements on different bacterial strains to investigate further this potential bacterial selectivity of our devices,



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Figure 3. Hybrid plasmonic/photonic response of hybrid Ag (8 nm) /1D PhCs upon contamination with E. coli. (A) Average transmittance spectrum (with standard deviation) of Ag/1D PhC after exposure to the LB medium (red-line) and (B) E. coli (blue-line). (C) Average shift at the stop-band maximum for the LB and E. coli contaminated PhCs. Data were averaged over two sets of measurement (six samples per measurement). (D) Average transmittance spectrum (with standard deviation) of Silica/Titania 1D PhC after exposure to the LB medium (red-line) and E. coli (blue-line).


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Finally, to obtain insights into the mechanism underpinning the photonic shift, we calculated the transmission spectra as a function of the silver carrier density (Fig. 4a). For this, we combined the transfer matrix method to model the alternating refractive indexes of the periodic structure, with the Maxwell-Garnett effective medium approximation for the description of the effective refractive indexes of the SiO2/TiO2 layers soaked with LB (see experimental section and supplementary information). In addition, we made use of the Lorentz-Drude model to account for the plasmonic contribution to the overall dielectric response of the device. We then proceeded to the simulation of the transmission spectra for 𝑛 = 5.76 × 1028 𝑚3 and 6.76 × 1028 𝑚3, with the former charge carrier density accounting for pristine Ag and the latter for the “bio-doped” film in the LB infiltrated photonic structure. Indeed, while an increased carrier density induces a large blue-shift of the plasmon resonance (25 nm) as it has been shown in the previous section, the PBG exhibits a less obvious 5 nm blue-shift. Notably, such a behavior corroborates our experimental data, at least from the qualitative point of view. On the other hand, the quantitative discrepancy can be probably attributed to the contribution of a different effect that intensifies the proposed mechanism. For instance, the metal/dielectric interface can be regarded as a degenerate case of an asymmetric metal−dielectric cavity mode that might lead to strong field enhancement and confinement at the metal/dielectric interface upon normal incidence illumination (i.e., Tamm optical modes)54–58, whose occurrence cannot be captured by our model. To preliminary assess this possible scenario, we also studied the photonic response of our hybrid PhCs with a top Ag layer of 16 nm (Fig. 4b,c). In this case, we observe a more pronounced contribution of the Ag plasmon to the overall transmission of the hybrid structure due to its higher optical density than in the previous samples. Remarkably, despite the plasmon resonance still shows a total 10 nm blue-shift after contamination when compared with the LBexposed samples, the PBG shift is limited to -5 nm. This might imply the involvement of an enhancement mechanism when Ag thickness is kept at relatively low value, due to the confinement of the plasmonic excitation at the dielectric interface.54,55,59 Further experiments are needed to elucidate such a scenario.



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Figure 4. Lorentz-Drude model and plasmonic/photonic response of hybrid Ag (16 nm)/1D PhCs. (A) Calculated transmission spectrum for the Ag/BS structure in LB medium for 𝑛 = 5.76 × 1028 𝑚 ―3 and 6.76 × 1028 𝑚 ―3.(B) Average transmittance spectrum (with standard deviation) of Ag/1D PhC after exposure to the LB medium (red-line) and (C) E. coli (blueline). Data were averaged over two sets of measurement (six samples per measurement).

In conclusion, we have shown that a novel hybrid plasmonic/photonic device consisting of a thin layer of the plasmonic and biocidal silver on top of a 1D photonic crystal can be responsive to bacterial contamination. We have preliminary demonstrated this concept by detecting one of the most hazardous bacterial contaminant in food and water, Escherichia coli. Our data points towards a scenario in which the polarization charge at the Ag/bacterium interface causes an increase of the metal charge carrier density that leads to a plasmon blue-shift, within a sort of “bio-doping” mechanism. This, in turns, leads to a blue-shift of the photonic structural color (10 nm). At this stage such a relatively small shift does not allow for visual colorimetric detection of bacteria, however we are following several strategies to enhance the optical response, i.e., by micro-structuring the plasmon layer to physically trap the bacteria on the surface. In addition, the promising yet preliminary data about possible discrimination between Gram-negative and Gram-positive bacteria will be verified via further experiments with additional pathogenic bacteria. In general, this can represent a novel approach for low-cost and real-time monitoring of contaminants in food and water.

Associated Content Supporting Information. Experimental methods, discussion on the biocidal activity of silver; modeling of the optical response; scanning electron microscopy images of the silver film and cross-section of the 1D photonic crystal; UV-Vis absorption spectra of the silver films after dipping in liquid LB and E. coli/LB mixture; zone of inhibition in the agar plate inoculated with 10 ACS Paragon Plus Environment

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E. coli; UV-Vis transmission spectra of the Ag/BSs samples after dipping in liquid LB and E. coli/LB mixture. UV-Vis transmission spectra of the Ag/BSs samples after exposure to TSB and M. Luteus/TSB mixture in agar plate.

Author information Corresponding authors E-mail: [email protected] ; [email protected] Notes The authors declare no competing financial interest.

Acknowledgments This work has been supported by Fondazione Cariplo, grant no. 2018-0979. F.S. thanks the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No. [816313]). We thank Dr. Stefano Perissinotto for the scanning electron microscopy experiments on 1D PhCs cross section and Ag films.

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Figure 1. Hybrid plasmonic/photonic devices. (A) Picture of the fabricated 1D photonic crystal with a 8 nm silver capping layer and (B) sketch of the multilayered structure. (C) Light transmission of the Ag/(SiO2/TiO2)5 photonic crystals as a function of the light incidence angle (inset Bragg-Snell equation). PBG stands for photonic band-gap 361x116mm (150 x 150 DPI)

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Figure 2. Plasmonic response upon bacterial contamination. (A) Average optical absorption (with standard deviation) of Ag thin films (8 nm on glass) before (green) and after exposure to either LB (orange line) or to (B) LB/E. coli (blue line) on agar plate (12 samples, two replicas). (C) Pictorial representation of the hypothesized mechanism giving rise to the plasmonic blue-shift (polarization accumulation charge). (D) Calculated transmission of the Ag layer for the pristine and “bio-doped” Ag layer in LB medium obtained by using the Lorentz - Drude model. 372x266mm (150 x 150 DPI)



Figure 3. Hybrid plasmonic/photonic response of hybrid Ag (8 nm) /1D PhCs upon contamination with E. coli. (A) Average transmittance spectrum (with standard deviation) of Ag/1D PhC after exposure to the LB medium (red-line) and (B) E. coli (blue-line). (C) Average shift at the stop-band maximum for the LB and E. coli contaminated PhCs. Data were averaged over two sets of measurement (six samples per measurement). (D) Average transmittance spectrum (with standard deviation) of Silica/Titania 1D PhC after exposure to the LB medium (red-line) and E. coli (blue-line). 490x430mm (150 x 150 DPI)


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Figure 4. Lorentz-Drude + Transfer matrix model and plasmonic/photonic response of hybrid Ag (16 nm)/1D PhCs. (A) Calculated transmission spectrum for the Ag/BS structure in LB medium for n=5.76×〖10〗^28 〖 m〗^(-3) and 6.76×〖10〗^28 〖 m〗^(-3).(B) Average transmittance spectrum (with standard deviation) of Ag/1D PhC after exposure to the LB medium (red-line) and (C) E. coli (blue-line). Data were averaged over two sets of measurement (six samples per measurement). 705x216mm (150 x 150 DPI)


Photonic Crystals for Optical Detection of

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