Tannic acid-induced interfacial ligand-to-metal charge transfer and the phase transformation of Fe3O4 nanoparticles for the photothermal bacteria destruction
Introduction
The spread of drug-resistant bacteria is an increasing threat to human health and is becoming a serious clinical problem [1], [2], [3]. An increasing number of bacterial strains with resistance to multiple antibiotics not only harms the clinical management of infectious diseases but also impacts food- and aquaculture-related industries, causing large economic losses [4], [5], [6]. There is an urgent need now and in the near future to search for a green way to develop effective bactericidal materials without inducing drug resistance to treat these superbacteria [7], [8]. Nanomaterials that directly contact the bacterial surface and physically destroy the cell membrane tend to minimize the possibility of inducing drug resistance [9], [10], [11]. Recently, a considerable number of studies has been directed toward the application of nanoparticles [12], [13], enabling nanosystem defenses against harmful malignancy [14] and infectious disease [15] by using chemically modified nanomaterials, such as dopants [16], surface core–shell engineering [17], [18], and photosensitizer integration [19], [20]. Relying on the new physical and chemical properties of functionalized nanoparticles, the potential development of new antibacterial strategies with delicate nanoparticles has been reported, including directly stretching the cell membrane [10], offering intramolecular electron transfer [21], causing rapid oxidation of the cell membrane [18], or increasing the binding affinity and charge distribution of the bacterial biolayer [17].
Recently, the optical technologies of nanoparticles have been further applied to photothermal ablation and sterilization, which provide a noninvasive treatment that can prevent undesirable side effects in normal cells [22], [23], [24]. For example, urchin-like Bi2S3 nanoparticles provide rapid bactericidal ability to E. coli and S. aureus by a complicated loading of 1-tetradecanol and linalool into their hollow cavity for combined photothermal chemotherapy [24]. If the cumulative dose on the surface of the bacteria is enhanced, it is expected that the reaction time with bacteria can be further shortened, reducing the laser dose and achieving a powerful bactericidal effect. Unfortunately, in recent studies on sterilization by NIR photothermal nanomaterials, it is rarely verified that this technology can achieve a complete bactericidal effect in less than 30 min of administration [25], [26].
Compared with other biocompatible NIR inorganic nanoparticles (e.g., Bi2S3 [24], copper selenide [23], Au-based NPs [20], [27], graphene [28], [29], and carbon nanotubes [30]), iron oxide nanoparticle (IONP) composites are biodegradable materials with transferrin proteins to assist the delivery of dissolved iron ions in reticuloendothelial systems (RESs) [31]. Due to these characteristics, Fe3O4 is an FDA-approved material and is recommended for healthcare development in humans. It has been reported that the high crystallization of Fe3O4 improves photothermal conversion, photolyzing harmful organisms through intervalence charge transfer (NIR-II: 1050 nm to 1300 nm) and d-d transitions (NIR-I: 650 nm to 950 nm) [32], [33]. However, the primary absorption is not easy to control due to the precise adjustment of the ratio between Fe2+ and Fe3+ in the preparation of the pure Fe3O4 crystal [34], [35], [36]. Aqueous synthesis suffers from uncontrollable oxidization conditions, such as aerobic environments or hydrolytic condensation during the hydrolysis–condensation process [37]. Therefore, the reliable control of and improvement in optical characteristics of the IONPs have not been achieved until now.
Recently, a complex of Fe ligands has been shown to enhance the ligand-to-metal charge transfer (LMCT) absorption band [38], which provides a new way to evolve specific absorption regions from visible to NIR wavelengths [39]. The fabrication of metal–organic frameworks (MOFs), in which phenolic ligands bind metal ions, is the most facile method to synthesize cross-linked nanocapsules, films for deposition, and mimicking materials for various biomedical applications [40], [41], [42]. Nevertheless, it is still a challenge to synthesize Fe-ligand capping lasers over the surface of IONPs to evolve LMCT absorption combined with IONP-related absorption properties.
In previous works, highly biocompatible and inexpensive tannic acid (TNA) with inherent nontoxicity has been used in integrating NIR absorption in nanomaterials via LMCT [42], [43]. TNA is a natural polyphenol compound and widely exists in many plants, especially in fruits and tea [44]. The phenol groups of this phenolic molecule can endow a moderate decrease in power by donating electrons to metal ions [45], [46]. Recently, it has been reported that TNA shows anti-COVID-19 activity by inhibiting the infection efficiency of SARS-CoV-2 in human cells [47]. In addition, TNA has many hydroxyl groups that offer a large number of hydrogen bonds for follow-up surface modification to target microorganisms [48], [49]. Thus, we hypothesize that the coordination of tannic acid (TNA), a polyphenol with a large number of gallol groups, and the iron ions of Fe3O4 NPs can induce superior NIR absorption with controllable photothermal properties in comparison to only Fe3O4 NPs.
To prove the above concept, a γ-Fe2O3 nanopowder is utilized for a hydrothermal reaction in the presence of TNA molecules as a green precursor, leading to a phase conversion that forms Fe3O4 with gram-scale production. A thin TNA-Fe complex layer decorated on the surface of the Fe3O4 NPs, enables additional LMCT absorbance at visible-NIR wavelengths and promotes the nonradiative processes to release heat. Because of the similar lattice constant of the face-centered cubic crystals between Fe2O3 and Fe3O4, the Fe3+ reduced by TNA is rearranged in the spinel crystal of the initial Fe3O4. Since Fe3O4 is a thermodynamically unstable product, the chemical transformation from γ-Fe2O3 to Fe3O4 requires a harsh reduction at high temperature by H2 gas in the traditional solid-state reaction [50], [51], [52]. To avoid toxic molecules, a green synthesis method to massively produce optical Fe3O4 by using a γ-Fe2O3 nanocrystal precursor has not been developed or published. We prepared d-mannose-decorated IONP@TNA, referred to as IONP-TNA@MA, to recognize bacterial fimbriae (FimH) [53], [54], [55] on Gram negative bacterial surface and demonstrate the targeted delivery of a photothermal treatment against extended-spectrum β-lactamase (ESBL)-producing and O157:H7 serotype Escherichia coli (E. coli). Compared with direct heat sterilization by an autoclave at 121 °C for 15 min, IONP-TNA@MA not only provides bacterial adhesion but also heats the bacteria specifically to reduce heating time, showing a promising development in the management of emergent and troublesome infectious disease.
Section snippets
Chemicals
Iron(III) oxide (γ-Fe2O3) was bought from ALDRICH. Tannic acid (TNA) and D-mannose (MA) were purchased from Alfa Aesar. All chemicals were used as received without any further purification. All nanoparticles synthesis and solution preparation were done by using DI water with 18.2MΩ resistance.
Characterizations
Transmission electron microscopy (TEM, Hitachi H7500 TEM instrument at 80 kV) was utilized to determine the structures of the IONP. The absorption spectra of the IONP-related samples were measured by a
Results and discussion
Fig. 1a shows a TEM image of a commercial γ-Fe2O3 nanopowder (γ-IONP) with a polyhedral structure. After the TNA-assisted hydrothermal reaction, the brown solution of colloidal γ-IONPs changed to a black colloidal solution (Fig. 1b). A similar polyhedron shape was observed from the black IONP product, which was the appearance of lower contrast on the surface with respect to the light element coating (e.g., H, C, and O atoms). By counting over 100 particles in the TEM images, the sizes of both
Conclusions
In summary, the surface modification of the TNA-Fe complex into IONPs was developed, rendering the additional combination of electron transition through interfacial charge transfer with the crystal-related absorption of iron oxide nanostructures. The interfacial LMCT and d-d transitions facilitated the elevation of photon absorption flux in the visible-NIR wavelength region. On the basis of Raman analysis results, the TNA-assisted hydrothermal reaction successfully converted maghemite (γ-IONP)
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported in part by grants from the Ministry of Science and Technology, Taiwan (MOST 108-2113-M-006-012-MY3 and MOST 109-2327-B-009-001), the Taipei City Hospital (TCH) and the Department of Health, Taipei City Government (TCH no. 10901-62-001 and 11001-62-004). This work was financially supported by the Center of Applied Nanomedicine, National Cheng Kung University from the Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the
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