Mussel-Inspired Immobilization of Silver ... - ACS Publications

Subscriber access provided by READING UNIV

Article

Mussel-Inspired Immobilization of Silver Nanoparticles toward Antimicrobial Cellulose Paper Md Shafiqul Islam, Nahida Akter, Md. Mahbubur Rahman, Chen Shi, M. Tofazzal Islam, Hongbo Zeng, and Md. Shafiul Azam ACS Sustainable Chem. Eng., Just Accepted Manuscript • DOI: 10.1021/ acssuschemeng.8b01523 • Publication Date (Web): 26 May 2018 Downloaded from http://pubs.acs.org on May 26, 2018

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Sustainable Chemistry & Engineering

Mussel-Inspired Immobilization of Silver Nanoparticles toward Antimicrobial Cellulose Paper Md. Shafiqul Islam,† Nahida Akter, † Md. Mahbubur Rahman,‡ Chen Shi, § M. Tofazzal Islam,‡ Hongbo Zeng, §* and Md. Shafiul Azam†* †

Department of Chemistry, Bangladesh University of Engineering and Technology (BUET),

Dhaka 1000, Bangladesh ‡

Department of Biotechnology, Bangabandhu Sheikh Muzibur Rahman Agricultural University,

Gazipur 1706, Bangladesh §

Department of Chemical and Materials Engineering, University of Alberta, 9211 - 116 Street

NW, Edmonton AB, T6G 1H9, Canada

*Corresponding Authors: [email protected], [email protected] (M.S.A.) [email protected] (H.Z.)

ACS Paragon Plus Environment

1

ACS Sustainable Chemistry & Engineering 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 2 of 41

ABSTRACT

Paper and paper products are widely used without any antimicrobial efficacy in our everyday lives and thus can act as potential transporters of many diseases. Herein, we introduce antimicrobial activity to cellulose paper by presenting a tailored mussel-inspired strategy for the sustainable immobilization of silver nanoparticles (AgNPs), which are well-known for the effectiveness in preventing annexation and proliferation of microbes on materials surfaces. First, we functionalized the cellulose paper with succinic acid that eventually reacted with dopamine to give dopamine-modified paper. The dopamine molecules possess excellent adhesion and strong coordination with metal substrates through catechol groups offering a potentially robust interface between AgNPs and the organic structure of the paper. Next, AgNPs were deposited onto the paper by simply immersing dopamine-modified paper in a silver salt solution to accomplish the antimicrobial properties. Field emission scanning electron microscopy (FESEM) study of the synthesized antimicrobial papers confirmed that the loading of AgNPs was time-dependent and the average size of the nanoparticles was in the range of 50 to 60 nm after 8 h of deposition time. The paper decorated with AgNPs showed excellent antimicrobial activity against highly virulent and multiple antibiotic resistant Gram-positive and Gram-negative pathogenic bacteria as well as against some extremely virulent fungal phytopathogens.

KEYWORDS: Mussel-inspired, antimicrobial paper, dopamine, silver nanoparticles


2

Page 3 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


INTRODUCTION Paper and paper-based products are ubiquitous in our daily lives. Cellulose paper, owing to its low cost and easy availability, is widely used as packaging materials for foods, healthcare and personal care products. Other uses of cellulose paper involve books and magazines, office paper and folders, wallpaper, medical records, bank notes and many more. Circulation and distribution of these cellulose materials with no antimicrobial efficacy to multiple people, in various environments, can cause alarming rates of contamination and transmission of numerous infectious diseases.1,2 Moreover, this contamination can cause re-emergence of previously wellcontrolled infectious diseases as well as develop new strains of bacteria resistant to currently available antibiotics.3,4 Demand of cellulose papers that inhibit or prevent attachment, establishment, and proliferation of microbes on their surfaces is thus obvious. Consequently, numerous attempts have been made to address this need of antimicrobial papers by either preparing antimicrobial pulp for paper5 or by directly modifying the cellulose paper with antimicrobials.6 Materials that are loaded onto the cellulose paper or other surfaces to introduce antimicrobial properties include alcohols, antibiotics, metal ions, and quaternary ammonium compounds. Unfortunately, these materials often cause environmental pollution, or the microbes are resistant to them.7,8 In recent times, the antimicrobial properties of metallic nanoparticles such as copper,9 silver,10 gold,11 titanium oxide,12 manganese oxide,13 and zinc oxide14 have been exploited to address these concerns. Particularly, silver nanoparticles (AgNPs) have been well investigated because of their strong antimicrobial activity toward many different antibiotic resistant bacteria,15,16 fungi,17 and viruses18 in conjunction with the minimal toxicity to humans.19 The extremely small size of the nanoparticles results in improved cell penetration20 and generation of


3


Page 4 of 41

oxidative stress on biological systems21 leading to greater antimicrobial activity. However, silver nanoparticles due to the high surface energy and van der Waals forces tend to aggregate deteriorating their antimicrobial efficacy remarkably.22 This deterioration of the antimicrobial activity is attributed to the loss of the nano-size-related properties caused by the aggregation of the nanoparticles. One simple and effective way to prevent or inhibit this aggregation and to enhance the nanoparticle dispersion is to use polymers, surfactants or other adhesive surfaces to hold the nanoparticles into the scaffold.23 A recent study showed that the immobilized or entrapped silver nanoparticles exhibited greater antimicrobial efficacy than colloidal AgNPs. Moreover, immobilization of AgNPs promote reusability of the antimicrobial substrates and thus elevates cost effectiveness.24 Consequently, surface immobilized AgNPs have recently been extensively used in health and cosmetic products, food packaging containers and textiles25 as well as in many medical applications such as surgical devices, dental composites, wound and burn dressings, et cetera.26,27 Numerous approaches have been proposed for immobilizing AgNPs onto a wide range of surfaces including either polymers23 and supramolecular assemblies28 or flat substrates like glass,29 stainless steel,30 and cellulose materials.31-34 The immobilization mechanisms involved in these strategies mostly rely on the noncovalent interaction between the functional groups of the polymers and the charged surfaces of the nanoparticles that eventually lead to leaching the nanoparticles off of the surface. A few reports have recently been made where the scaffold is covalently bonded with the functionalized or capped nanoparticles, which are unfortunately less active compared to the bare nanoparticles.35 For instance, Khan et al.

observed that the

exopolysaccharides capped particles showed less toxicity to Escherichia coli, Staphylococcus aureus and Micrococcus luteus when compared with the uncapped ones.36 On the other hand, the


4

Page 5 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


formation of Ag nanoparticles onto the surface was usually achieved either by chemical reduction of silver salts with the help of an external reducing agent i.e., NaBH4 or by posttreatment of the nanoparticle precursor incorporated surface using ultrasonic radiation making the process complicated and environmentally unfriendly.37,38 In recent years, polydopamine has enticed huge research interest as a biomimetic polymer reflecting the inspiration from the unique adhesive nature of the marine mussel.39 The ability of the catechol groups in polydopamine towards the reduction of noble metallic salts into metallic nanoparticles40 and the subsequent immobilization of the nanoparticles onto the scaffold preventing aggregation and leaching has aroused it as an universal surface modification agent. Consequently, this modification strategy has been used for various materials with wide range of applications in biosensors, supercapacitors, drug delivery materials, catalysts, and adsorbents.41,42 A number of attempts have been thereafter reported on how dopamine or polydopamine modified materials can be exploited to immobilize silver nanoparticles for introducing catalytic43,44 and antimicrobial45 properties into the structure. Despite the widespread use of mussel-inspired surface chemistry, modification of cellulose paper with dopamine molecules and nanoparticles remains unexplored owing to the lack of suitable reactive sites on the paper surface. Many paper-based applications including catalysis, bio-sensing,

medical

diagnosis,

and

environmental

remediation

require

sustainable

functionalization of the nanoparticles on the paper surface.46 Herein, we report a facile and costeffective approach for the chemical functionalization of cellulose paper with dopamine molecules that eventually lead to a green and robust immobilization of AgNPs (Scheme 1). Although many reports have been made on the dopamine or more commonly polydopamine modified surface for immobilizing AgNPs from the aqueous silver ions, the effects of reaction


5


Page 6 of 41

time on the growth and morphology of the AgNPs were not explored. We report here that the morphology of the AgNPs formed on the dopamine modified paper greatly depends on the reaction time. In addition, the antimicrobial properties and mechanical strength of the resultant AgNPs loaded paper were investigated. Excellent antimicrobial properties against some antibiotic resistant pathogenic bacteria and fungus along with moderate mechanical strength make the as-synthesized paper a potential candidate for use as a packaging material.

EXPERIMENTAL Materials. Whatman qualitative filter paper (grade 5, pore size 2.5 µm) was used as the cellulose paper (CP) for all modifications. Succinic anhydride and dopamine hydrochloride were purchased from Sigma-Aldrich. Silver nitrate (AgNO3) was obtained from Fisher Scientific. All chemicals were used as received without further purification. Ultrapure water was obtained using a Millipore water purification system (MA, USA) and was used for all experiments. Succinylation of CP. Whatman grade 5 filter papers were cut into circular pieces using a paper puncher presenting a diameter close to 6 mm. 0.5 g of the paper pieces were immersed in an aqueous solution of 10 wt % NaOH (10 mL) for 18 h. The samples were then repeatedly washed with absolute ethanol until a solution was obtained around neutral pH. The paper pieces were used for further reactions after the sogginess of the paper was removed by air. Pretreated cellulose paper (0.5 g, 9.1 mmol of active –OH groups47) was reacted with succinic anhydride (2.5 g, 25 mmol) at 90 °C for 17 h in 10 mL of a mixed solvent of pyridine (10 mL) and toluene (35 mL) to yield succinylated cellulose paper (SA-CP) containing exposed carboxylic acid groups. The paper samples were then taken out of the reaction and washed with toluene at least 3 times and then with acetone at least 5 times before drying in air. The samples were then allowed


6

Page 7 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


to dry at 50 °C in an oven for 4 h and stored in a desiccator until further analysis or functionalization. Back titration method was employed to determine the degree of substitution (DS) of succinylated paper,48 which gave a good estimation of the SA functionalization of the paper. 0.2 g of the sample was first immersed into 100 mL of 0.02 M aqueous NaHCO3 solution followed by stirring for 2h at room temperature. The resulting mixture was filtered and excess NaHCO3 was back

titrated using pre-standardized 0.02 M HCl. The DS was calculated by using the following equation:

𝐷𝑆 =

162 × 𝑛!""# 𝑚 − 100×𝑛!""#

⋯

⋯

(1)

Where, 162 g mol−1 is the molar mass of an arbitrary glucose unit (AGU), 100 g mol−1 is the increased molar mass of AGU, m is the weight of the SA-CP sample analyzed and nCOOH is the number of moles of consumed acid per gram sample. The mass percent gain (mpg) was calculated according to

𝑚𝑝𝑔 % =

𝑚!" − 𝑚!"!!" ×100 𝑚!"

⋯

⋯

(2)

where, mCP and mSA-CP denote the mass of CP and SA-CP, respectively. Dopamine Modification of SA-CP. Dopamine modification of the succinylated paper was carried out by coupling the –COOH group of succinylated paper with –NH2 group of dopamine in presence of EDC (N-3-dimethylaminopropyl-N’-ethylcarbodiimide) coupling agent. PBS buffer (35 mL, pH 5.0), dopamine hydrochloride (0.25 mmol, 42.5 mg), and EDC (0.35 mmol,


7


Page 8 of 41

70 mg) were transferred into a reaction flask and made sure that the pH of the solution remained close to pH 5.0. Previously prepared SA-CP samples (0.5 g) were added to this mixture and stirred gently for 24 h at a shaker. Afterward, the as obtained Dopa-CP papers were washed with PBS buffer at least 3 times and then with deionized water at least 5 times. The samples were dried in air for about 2 h and used for the next reaction, or stored in a desiccator. Immobilization of AgNPs. Ammoniacal silver nitrate (Tollen’s reagent) was used as the source of silver for the immobilization of AgNPs on the Dopa-CP surfaces.43 The precursor solution was prepared by adding ammonium hydroxide (2 wt %) into AgNO3 (5 mg mL-1) solution until the initially formed brown precipitate just dissolved. The Dopa-CP samples were then immersed in the ammoniacal silver nitrate solution and the reaction flask was shaken in a rotary shaker (150 rpm) for a variable time from 15 m to 18 h at room temperature. The silver ammonia solution was then collected for UV-Vis spectroscopy analysis and the blackish-brown paper was washed with deionized water until the washing liquid appeared clear. The brown papers decorated with AgNPs were then dried in air and stored in a desiccator. Characterizations. FTIR spectra of the dried CP, SA-CP, Dopa-CP and Ag-Dopa-CP samples were recorded on a Shimadzu 8400 FTIR spectrometer in the region of 4000 – 400 cm-1. The surface morphologies of the synthesized Ag-Dopa-CP samples were accomplished using JEOL JSM-6400LA FESEM operated at an accelerating voltage of 5 kV. The elemental compositions of the synthesized paper samples were determined by an EDX spectrometer coupled with the FESEM. The surface morphologies of the as-fabricated papers were investigated by AFM imaging conducted using an Asylum MFP-3D AFM in tapping mode with commercially available Si cantilever tips (Olympus, 300 kHz frequency). XPS spectra were recorded using the


8

Page 9 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


Al Ka radiation on a Kratos Axis Ultra spectrometer operated at 12 mA and 14 kV. The peak fitting was performed by Igor Pro software. Antimicrobial Activity Test. In vitro antimicrobial activities of silver nanoparticles immobilized paper (AgNP-paper) against selected virulent fish and shrimp pathogenic bacteria were determined by the disk diffusion method. The bacterial strains used in this study were Vibrio parahaemolyticus strain 2A1 and 2A2, Enterococcus faecalis strain FF11 and F1B1, Serratia marcescens strain 4V3 and Proteus mirabilis strain NS34 which were previously isolated in the laboratory of the department of biotechnology at Bangabandhu Sheikh Mujibur Rahman Agricultural University and identified based on 16S rRNA gene sequence homology studies. Among these, E. faecalis strains were isolated from Enterococcal infection in fish, Vibrio parahaemolyticus strains were isolated from vibriosis disease in shrimp, and Serratia marcescens and Proteus mirabilis strains were isolated from Black spot disease infected shrimp. All of the bacterial strains were previously identified as highly virulent and resistant to multiple antibiotics.49 The antimicrobial activity was tested by taking 30 µL of fresh bacterial culture (ca. 1 × 109 cfu) and spread on the Iso-senseitest Agar plates. Then, the sterilized (autoclaved and dried) paper disks were aseptically placed onto the culture plate and incubated at 28 °C for 24 h in an incubator. The plates were examined for possible clear zones due to growth inhibition of the antimicrobial activity of AgNP-paper disks after incubation at 28 °C for 24 h. The presence of any clear zone that formed around the AgNP-paper was recorded as an indication of inhibition against the tested microbial species. The diameter of AgNP-paper disks and diameter of the zone of inhibitions were measured and the ratios between the two (diaZOI/diadisk) were calculated.50 For the antifungal test, the culture of fungal strain (i.e. Magnaporthe oryzae) was done using 12 mL of potato dextrose agar on potato dextrose agar (PDA) plate after 7 days of inoculation.51 For


9


Page 10 of 41

sensitivity test, the sterilized (autoclaved and dried) Ag-Dopa-CP disks were aseptically placed on the culture plate and incubated in dark at 28 °C for 7 days in an incubator. The plates were examined for possible clear zones after incubation. Loading and Robustness of the Immobilized AgNPs. The total loading and robustness of the immobilized AgNPs were investigated by employing flame atomic absorption spectroscopy (FAAS). The experiment was conducted using a Varian 240FS atomic absorption spectrometer with a slit width of 0.5 nm and the absorbance was measured at a fixed wavelength of 328.1 nm for silver. To determine the total silver loading we treated about 100 mg (with the measured surface area) of dried Ag-Dopa-CP samples with concentrated nitric acid (30 %, 5 mL). The paper samples were then boiled in the acid solution for 1 h first, cooled down to room temperature, and then re-boiled for another 30 m with an additional 1 mL of hydrogen peroxide (30 %). This extensive acid treatment converted all the silver particles to silver ions. After cooling again the supernatant solution was separated using a glass filter and the effluent was analyzed with the help of a FAAS after required dilution with ultrapure water. The experiment was repeated at least 3 times with different samples and the average was taken. The robustness of the immobilized AgNPs was also tested using FAAS spectroscopy. In a typical experiment, a 2 x 2 cm2 piece of dried Ag-Dopa-CP sample was immersed in 200 mL ultrapure water. A specific volume (5 mL) of effluent was taken out at desired time intervals during the acid digestion and was analyzed by FAAS.

RESULTS AND DISCUSSION Our mussel-inspired strategy, as depicted in Scheme 1, requires the attachment of the dopamine molecules onto the cellulose paper, which is composed of β-glucose units containing


10

Page 11 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


primary alcohol (–OH) groups. We exploited these –OH groups for functionalizing the paper surface by succinylation followed by dopamine modification. However, the –OH groups of the glucose units are not readily available for functionalization because most of them form intermolecular hydrogen bonds with adjacent –OH groups leaving only a few available for surface reaction.52 Prior to the succinylation, the cellulose paper was treated with 10 % aqueous solution of NaOH to disrupt the extensive hydrogen bonds between cellulose fibers by deprotonating the primary –OH groups of glucose units.53 To investigate the effect of this alkali treatment we analyzed the degree of substitution and mass percent gain after the succinylation of both alkali-treated and untreated filter papers. The succinylation of the samples was performed by treating them with succinic anhydride in toluene and pyridine mixed solvent at 90 °C for 17 h. The degree of succinylation (DS) was measured by determining the amount of –COOH groups introduced onto the surface in this step via back titration method. We observed two times greater DS value for the alkali treated paper (DS = 0.11 ± 0.01) than that of the untreated ones (DS = 0.053 ± 0.006) suggesting the prerequisite of this step for effective functionalization of the paper substrate. Moreover, the mass percent gain per gram of the paper after succinylation was measured 1.5% and 4.5% as calculated from eq. (2) for untreated and alkali treated paper, respectively. Critical information that we derived from the data was that the treatment of cellulose paper with alkali increased the accessibility or reactivity of the –OH groups of the cellulose fibers for functionalization. However, alkali treatment of paper samples for prolonged period of time or use of higher concentration of NaOH was avoided as they caused some visible damage to the cellulose fibers. Next, the –COOH groups of the succinylated paper were allowed to couple with the –NH2 groups of dopamine in presence of EDC at a room temperature for 24 h at pH 5.0.54 The DS value decreased from 0.11 ± 0.01 for succinylated paper to 0.030 ± 0.007


11


Page 12 of 41

for the dopamine functionalized paper indicating that around 73% of the –COOH groups were coupled with dopamine via amidation.

Scheme 1. Schematic illustration of the mussel-inspired immobilization of AgNPs on a cellulose paper surface

The functionalization of the filter paper was qualitatively assessed using a bromocresol green indicator. The indicator is blue under basic conditions but turns yellow in presence of carboxylic and stronger acids. When dipped in the indicator solution, the untreated paper appeared pale green and deprotonated paper was bright blue (Supporting Info, Figure S1). When both of these papers were exposed to solutions of succinic anhydride overnight, they both appeared yellow when dipped in the bromocresol green solution, indicating the presence of carboxylic acid groups. The yellow color, however, was stronger for the sample that had been previously treated with NaOH indicating greater succinylation. The dopamine modified paper turned the bromocresol green indicator greenish yellow indicating decreased acid nature of the paper due to the loss of –COOH groups in the process. The catechol functional groups of dopamine molecules attached to the paper surface show important redox activity in addition to their adhesive


12

Page 13 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


nature.40,55 This catecholic redox chemistry enabled our synthesized Dopa-CP to facilitate the onsurface formation of AgNPs from the silver nitrate solution at room temperature. On the other hand, the adhesive nature of the catechol groups let the AgNPs stay glued to the paper surface after the formation. A visible difference was observed in the appearance of the paper before and after AgNPs deposition. The color of dopamine coated paper, when treated with ammoniacal silver nitrate solution for 8 h, turned from white to brown indicating the formation of AgNPs on the paper surface (photographic images of Dopa-CP and Ag-Dopa-CP are shown in the supporting info, Figure S1). Average loading of silver on the paper surface was measured at 0.54 ± 0.09 mg/cm2 (85 ± 14 mg Ag/dry g paper), which was 16-fold higher than what was reported for the bactericidal paper synthesized by depositing AgNPs via the in situ reduction of silver nitrate on the cellulose paper.31 This is a remarkable improvement in terms of loading AgNPs on the cellulose paper that we achieved via the aforesaid mussel-inspired approach. This strategy would certainly be useful for the functionalization of cellulose paper with diverse materials, including noble metals, metal oxides, and carbon nanomaterials, to generate improved paper-based catalytic systems and biosensors.46 It is indeed of importance that the scientists from various fields have been using polydopamine or polydopamine-coated substrates for the immobilization of AgNPs or other nanoparticles requiring lots of dopamine,48-50 which is reasonably expensive. In the described process, although the immobilization of AgNPs on the paper proceeded in three steps, more importantly this method required the minimum amount of dopamine simply for functionalizing the paper surface and thus making it more economical (a typical lab scale cost analysis is provided in the supporting info, Table S1). We also attempted to decorate CP and SACP with AgNPs by the same procedure and found negligible amount of AgNPs deposited on the


13


Page 14 of 41

surface. This observation further demonstrated the importance of the dopamine modification step in the method reported in this work (Supporting Info, Figure S2). For comparison, we also used AgNO3 solution as the Ag source without adding ammonia for the deposition of AgNPs onto the Dopa-CP. This experiment led to a very low loading amount of the AgNPs on the paper surface indicating the need of basic condition in our approach (Supporting Info, Figure S3).

The AFM imaging results of the paper surface are shown in Figure 1. In spite of some roughness of the cellulose paper, it is clear that AgNPs are uniformly functionalized on the surface. No significant differences were observed for the fresh filter paper and dopamine modified paper indicating that the chemical treatment of the CP did not damage the texture of the paper or the cellulose fibers in the process of the preparation of Dopa-CP (Supporting Info, Figure S4). After the Dopa-CP was incubated in ammoniacal AgNO3 solution the AFM images of the papers showed a surface presenting granular textures with a sparsely populated layer of AgNPs. The particles were with an average diameter of 53 ± 20 nm and density of 68 ± 11 nanoparticles/µm2, which is consistent with a previous report for similar flat and rough surfaces.56 Cellulose topography of the paper was mostly buried under the predominant deposition of AgNPs, which was also in good agreement with higher relative atom percentage of silver in the XPS obtained for Ag-Dopa-CP. XPS survey of the CP showed the peaks for C 1s (~286 eV) and O 1s (~531 eV) only. Dopamine modification of the CP surface was reflected by the appearance of the N 1s (~400 eV) and then AgNPs deposition on the Dopa-CP was confirmed by the appearance of Ag 3d doublet near 370 eV, Ag 3p at 571.8 and 602.6 eV, and Ag 3s at 717.2 eV as depicted in Figure 1C. The Ag 3d core-level spectrum shown in Figure 1D is composed of two distinct peak components with binding energies of Ag 3d3/2 and Ag 3d5/2 at


14

Page 15 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


368.1 eV and 374.1 eV, respectively, both attributed to the Ag0 species (Figure 1D). Moreover, the 6 eV splitting of the 3d doublet due to the spin-orbit coupling confirmed the existence of Ag⁰ state on the paper surface.57,58

Figure 1. AFM images of the (A) unmodified cellulose filter paper (CP), and (B) AgNPs deposited dopamine modified cellulose paper (Ag-Dopa-CP); (C) XPS survey scans of CP (black), and Ag-Dopa-CP (red), (D) detailed scan of Ag 3d peaks.

Further characterization by XPS was performed to probe the surface functionalization of the paper as illustrated in Scheme 1. The high-resolution C1s spectra of CP, Dopa-CP, and AgDopa-CP are shown in Figure 2A, B, and D, respectively. The spectra were calibrated against the binding energy of the adventitious C1s at 285.1 eV. The deconvolution of C1s XPS spectra of CP exhibited four common peaks at 285.1 eV, 286.6 eV, 288.0 eV and 289.3 eV, which can be assigned to saturated C–C bonding of cellulose, the C–O groups, carbonyl groups (C=O), and carboxyl groups (COOH), respectively.59,60 As cellulose is a natural polymer, little oxidation


15


Page 16 of 41

occur readily at the surface which explains the carbonyl peak at 289.3 eV for CP.61 The dopamine modified paper gave significant changes at the peak position and the deconvolution of high-resolution C1s peak showed five components which were assigned to C-C (285.1 eV), C-N (285.7 eV), C-O (286.9 eV), C=O (288.4 eV) and O-C=O (289.6 eV).50,51 The new peak at 285.7 eV indicated the formation of C-N bonds because of the coupling reaction. We intended to couple the surface –COOH groups with the –NH2 groups of dopamine and maintained pH 5.0 during the reaction to avoid the polymerization of dopamine.62 The bond percentage of different bonds based on the C1s spectra for CP, Dopa-CP, and Ag-Dopa-CP are summarized in Table 1. We observed that the ratio of the chemical bonds C-O, which was originated mostly from cellulose structure, to COO, which was mostly from SA and Dopa modifications, increased by 7folds (please see the supporting info for C1s XPS spectra of SA-CP, Figure S5). This observation yet again confirmed that the dopamine modification was successfully accomplished via our strategy. Next, C1s XPS spectra of the Ag-Dopa-CP exhibited no major changes in the peak positions but instead produced a significant increase in peak intensities for COO and C-N originated mostly from succinic ester and amide groups, which occurred on the top part of the paper surface. This was probably because the Ag-Dopa-CP was covered with AgNPs burying the glucose units in the inner part of the cellulose paper and thus suppressed the relative peak intensities of C-O (mostly from glucose units) as detected by XPS, which probes approximately the top 10 nm of the surface.63 The high-resolution XPS spectra of N1s peak of Dopa-CP and Ag-Dopa-CP are shown in Figure 2C and 2E. Both spectra showed a common peak at 397.8 eV, which indicated the presence of CONH groups of the amide formed during the coupling reaction between dopamine and the succinic acid group.64 The peak at 399.6 eV revealed the binding energy peak of –NH2


16

Page 17 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


group,65 which can be attributed to a very small amount of dopamine oligomers formed on the cellulose surface even at this low pH. Due to the strong adhesive nature of dopamine,41 the oligomers remained on the surface even after extensive washings. However, the dopamine left the surface when the Dopa-CP was allowed to react with ammoniacal silver nitrate salt and accordingly we observed the –NH2 peak disappeared in the N1s spectrum of Ag-Dopa-CP. We hypothesized that the catechol groups of the dopamine oligomers reduced Ag+ to form Ag nanoparticles, which were eventually held by the catechol groups owing to their strong adhesive force. The dopamine-AgNP species, which were not covalently attached to the paper surface, then left the surface and got dispersed in the solution. Now, if this hypothesis is true, the polydopamine-AgNP moieties should appear in the solution where the paper substrates were dipped in. We, therefore, examined the uv-visible spectra of the solutions left after Ag-Dopa-CP samples were taken out at each time intervals to see if any dopamine transferred into the solution. We indeed observed a peak that appeared at 285 nm on the absorption spectra, which was attributed to the polyphenolic groups of dopamine, suggesting the parting of adsorbed dopamine (Supporting Info, Figure S6). The absorbance at 285 nm increased initially with deposition time and reached the equilibrium after 4 h. We also monitored the effect of deposition time on the morphology and loading of the AgNPs by performing the FESEM and EDX, respectively, and the results will be discussed in a later section.


17


Page 18 of 41

Figure 2. XPS regions (A) C 1s of CP, (B) C 1s of Dopa-CP, (C) N 1s of Dopa-CP, (E) C 1s of Ag-Dopa-CP, (E) N 1s of Ag-Dopa-CP Table 1. Percentages of the functional groups obtained from XPS C1s peak fitting for CP, Dopa-CP, and Ag-Dopa-CP. Materials

Bond Percentages (%) C-C

C-N

C-O

C=O

COO

CP

10.6

0

70.3

17.6

1.5

Dopa-CP

10.3

7.0

61.3

13.3

8.1

Ag-Dopa-CP

11.8

19.6

43.0

13.8

11.8

To confirm the structural changes of the cellulose paper after undergoing their successive reactions, infrared absorbance experiments were performed on untreated CP, SA-CP, Dopa-CP,


18

Page 19 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


and Ag-Dopa-CP. In all FTIR spectra, a broad absorption was observed from 3050 to 3600 cm-1 and attributed to water and H-bonded cellulose –OH. The peak at 1633 cm-1 was also due to the water absorbed from air by the cellulose materials.66 The cellulose-based paper exhibited a few characteristic peaks at 3440, 2902, 1428, 1371, 1166, 1059, 897 cm-1, which were for –OH stretching, –CH stretching, –CH2 bending, –CH bending, –OH bending, C–O stretching and C– O–C stretching, respectively.66 After succinylation of the CP, a new peak appeared at 1740 cm-1, characteristic of the carbonyl (C=O) stretch, confirmed the addition of succinic group into the paper matrix.48 No significant changes were observed after dopamine modification because the broad –OH absorption of cellulose suppressed both –NH (amide) and catechol –OH of the dopamine moiety. However, a new peak at 1570 cm-1 appeared after the immobilization of the silver nanoparticles onto the paper surface which was attributed to the formation of Ag-catechol ring between the silver nanoparticles and catechol –OH groups as consistent with previous observation.67 Hence, the FTIR spectra of the samples yet again confirmed the immobilization of AgNPs via dopamine functionalization on the paper surface.

Figure 3. FTIR spectra of CP (black), SA-CP (green), Dopa-CP (blue) and Ag-Dopa-CP (red).


19


Page 20 of 41

We employed FESEM to observe directly the morphologies of the Ag-Dopa-CP and to map the distribution of AgNPs on the paper surface (Figure 4). Analysis of the Ag-Dopa-CP after 8h of immersion in AgNO3 solution demonstrated that AgNPs were immobilized on the surface uniformly as also in accordance with our AFM observation. All AgNPs are present in a wellsegregated manner with a few nanoclusters formed randomly. Two important factors that should govern the morphology, loading amount and density of the AgNPs formed on the surface via this mussel-inspired strategy are the concentration of AgNO3 solution, and the deposition time. Interestingly, Xie et al. observed that the concentration of ammoniacal silver nitrate did not have any significant effects on the morphology of the AgNPs on the dopamine-modified surface.43 However, our literature survey could not find any detailed report on how the deposition time affects the growth behavior of AgNPs on this kind of mussel-inspired surfaces. To investigate the effects of immersion time on the surface morphologies of AgNPs the DopaCP samples were immersed in AgNO3 solution for variable times such as 15 min, 4 h, 8 h, 12 h and 18 h. On surface formation of AgNPs was attained in just 15 m although the population of the particles per unit area was relatively low. We observed a steady deposition of AgNPs onto the paper with immersion time until 12 h. The average particle size increased slightly with broad size distributions (particle size distributions were extracted and analyzed using MIPAR imaging software and represented in Supporting Info, Figure S7) within this time. However, the formation of some nanoclusters appeared on the FESEM images after 12 h and eventually most of the nanoparticles were turned into aggregated nanoclusters after 18 h. To shed some light on the formation of these big clusters, we looked at them more closely with high-resolution SEM image by zooming in on one particle (Supporting Info, Figure S8). We observed very small nanoparticles (~2 nm) coagulating around the already formed AgNPs, which probably led to the


20

Page 21 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


ultimate bigger clusters. The representative normalized EDX spectra of the Ag-Dopa-CP samples after 8 h and 18 h as shown in Figure 4G confirmed that both the paper surfaces contained silver along with carbon, nitrogen and oxygen elements. To figure out the time-dependent loading of silver we calculated the atomic ratio Ag/N from the EDX data and plotted them as a function of immersion time (Figure 4H). We observed that the overall Ag loading on the paper dramatically decreased after 12 h and was very low at 18 h. To further investigate the effects of immersion time, we also measured the amount of silver in mg/cm2 for the Ag-Dopa-CP at each deposition time from the atomic absorption spectroscopy data. The amount of silver loaded on paper dropped from 0.58 ± 0.11 mg/cm2 at 12 h to 0.40 ± 0.12 mg/cm2 at 18 h yet again supporting our EDX data. The loss of silver nanoparticles from the surface after a certain immersion time in silver salts was likely a result of the increased mass of the silver nanoclusters, which were too heavy for the dopamine molecules to hold. This is indeed a very important observation that has never been reported elsewhere for this kind of surfaces as far as we know. Therefore, the immersion time of the Dopa-CP in silver salts solution has imperative effects on the loading and sizes of the nanoparticles. This remark we are concluding here might be true for other kinds of dopamine-modified flat surfaces in general as well.


21


Page 22 of 41

Figure 4. FESEM images of Dopa-CP after immersing in ammoniacal AgNO3 solution for (A) 0 m, (B) 15 m, (C) 4 h, (D) 8 h, (E) 12 h, and (F) 18 h (the scale bars in the insets of each FESEM images represent 500 nm in length); (G) normalized EDX spectra of Ag-Dopa-CP shows decreased intensity of Ag peak for Ag-Dopa-Cp with immersion time 18 h (black) compared to that of the Ag-Dopa-Cp with immersion time 8 h (red); (H) plot of EDX elemental ratio of Ag/N (black solid line), and loading of AgNPs in mg/cm2 (red dashed line) vs the immersion time of Dopa-CP in AgNO3 solution.

To investigate the antibacterial activity of the AgNP decorated papers, we measured the zones of inhibition (ZOI), which represent the regions over which the bacterial growth is absent around the sample in the disk diffusion tests. Experiments were carried out with some Gram-positive and Gram-negative highly virulent fish and shrimp pathogenic bacterial strains such as Vibrio parahaemolyticus

2A1,

Vibrio

parahaemolyticus

2A2,

Enterococcus

faecalis

FF11,


22

Page 23 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


Enterococcus faecalis F1B1, Serratia marcescens 4V3, and Proteus mirabilis NS34. These bacterial strains are pathogenic to several fish and shrimps and are resistant to various antibiotics.49,68 The Ag-Dopa-CP samples showed excellent antibacterial activity against these strains and the representative results of the measured ZOI are presented in Figure 5. The images showed that the Ag-Dopa-CP papers not only prevent the growth of bacteria on the surfaces but also inhibit them in a zone surrounding the paper disks. Yet despite some debates on the details of the bactericidal modes of action, recent studies have suggested that the major contributions come from direct contact killing by immobilized AgNPs, contact killing by Ag released into the solution as colloids, and ion-mediated killing by Ag+ released from either immobilized silver or colloidal silver.24 Although contact killing is the predominant bactericidal mechanism for surface immobilized AgNPs,24,69 contributions from other mechanisms cannot be ruled out. We hypothesized that the inhibition zones around the Ag-Dopa-CP samples were probably caused by the dissolution of silver nanoparticles or ions. To shed some lights on this, we determined the amount of Ag leached, if any, during the disk diffusion assay by measuring the concentration of silver (both Ag0 and Ag+) at the agar plates by FAAS. The results suggested that approximately 0.21% of the total silver leached after 24 h of incubation indicating the dissolution of very small amount of Ag from the Ag-Dopa-CP samples. This low leaching of silver during the antibacterial assay would also allow reuse, lessen the environmental risks, and elevate cost effectiveness of as-prepared Ag-Dopa-CP paper. The ratios between the diameter of the zone of inhibition and the diameter of Ag-Dopa-CP disk (diaZOI/diadisk) were measured and listed in Table 2, where Ag-Dopa-CP8h and Ag-DopaCP15m represent the Ag-Dopa-CP samples obtained after 8 h and 15 m immersion in AgNO3 solution, respectively. Ag-Dopa-CP8h exhibited antimicrobial activity against all of the bacterial


23


Page 24 of 41

strains tested except the Proteus mirabilis strain NS34. The amount of silver leached (0.21 % of the total Ag) from the antibacterial paper after 24 hours of incubation was roughly 2.6 µg/mL within the 12 mm of ZOI. This concentration of silver is comparable to the previously reported values of the minimum inhibitory concentration (MIC), defined as the lowest concentration of an antibacterial material to inhibit the visible growth of a microorganism, for in vitro antibacterial studies employing silver nanoparticles. For instance, Zarei et al. found that the MIC value of commercially available AgNPs against Vibrio parahaemolyticus was 3.12 µg/mL,70 which matches with the concentration of the leached silver from as-prepared Ag-Dopa-CP within the ZOI in this work. However, our samples were inactive against Proteus mirabilis, indicating that the leached concentration of silver (2.6 µg/mL) might not be adequate for inhibiting this specific microbe. Interestingly, the MIC values reported for silver nanoparticles against Proteus mirabilis varied in the literature, ranging from 1.5 µg/mL71 to 50 µg/mL,72 which most likely depends on the evaluation method used. It is also noted that the MIC values of AgNPs obtained from different studies may not be directly compared, since the bactericidal activity varies with the microbial strain, initial bacterial concentration, composition of culture media, size and shape of nanoparticles, etc.73 In this work, the leached concentration of silver (2.6 µg/mL) is close to the relatively small MIC value reported previously, suggesting that the leached silver was not very active against Proteus mirabilis. Obviously, bare CP and Dopa-CP did not show any noticeable zone of inhibition against any of the bacteria examined (data not shown) demonstrating the antibacterial effects solely due to the immobilized AgNPs. We discussed already that the loading of AgNPs on the paper samples was time dependent and observed significantly different loading for Ag-Dopa-CP8h (0.54 ± 0.09 mg/cm2) and Ag-DopaCP15m (0.33 ± 0.08 mg/cm2). To investigate the effects of the AgNPs loading on the antibacterial


24

Page 25 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


activity we performed the antibacterial tests on both samples. Perceptibly, we observed increased inhibition for Ag-Dopa-CP8h that had higher silver content than Ag-Dopa-CP15m against all the strains except Enterococcus faecalis strain F1B1 for which the inhibition was almost the same. This observation is consistent with previous work performed on a AgNP decorated membrane.74 Moreover, the low loading of AgNPs on the Ag-Dopa-CP15m was responsible for the inactivity against two additional strains such as Serratia marcescens strain 4V3 and Proteus mirabilis strain NS34. We also tested our Ag-Dopa-CP samples against a devastating wheat blast fungus Magnaporthe oryzae Triticum pathotype. This fungus recently emerged in Bangladesh and poses a serious threat to wheat cultivation in the country. We found that both Ag-Dopa-CP samples showed excellent inhibition against the growth of the fungi as well (Figure 5B). In addition, when we tested the effects of the Ag-Dopa-CP samples on the germination of wheat and on the excised leaves of the wheat, barley, and maize, we found that they have no visible phytotoxic effects (Supporting Info, Figure S9).

Figure 5. Antimicrobial properties of as synthesized AgNPs anchored papers. (A) Antibacterial activity of Ag-Dopa-CP papers: optical photographs (cropped) of zone of inhibition (ZOI) of AgDopa-CP15m (left column) and Ag-Dopa-CP8h (right column) against Vibrio parahaemolyticus


25


Page 26 of 41

strain 2A1 (first row), Enterococcus faecalis strain F1B1 (second row), and Enterococcus faecalis strain FF11 (third row) after 24 h of incubation at 28 °C. (B) Growth of wheat blast fungus Magnaporthe oryzae Triticum pathotype without the Ag-Dopa-CP papers (top image), the growth is strongly inhibited by the Ag-Dopa-CP15m and Ag-Dopa-CP8h papers (bottom image). Table 2. Antibacterial activity in terms of diaZOI/diadisk of Ag-Dopa-CP15m and Ag-DopaCP8h against fish and shrimp pathogenic bacteria. Spectrum

Bacterial Strain

Gram (–) Vibrio parahaemolyticus strain 2A1 Gram (–) Vibrio parahaemolyticus strain 2A2 Gram (+) Enterococcus faecalis strain FF11 Gram (+) Enterococcus faecalis strain F1B1 Gram (–) Serratia marcescens strain 4V3 Gram (–) Proteus mirabilis strain NS34 *na means not active against the particular strain

diaZOI/diadisk Ag-Dopa-CP15m Ag-Dopa-CP8h 1.83 2.25 1.90 2.52 1.95 2.11 2.00 1.98 na 1.66 na na

Next, the robustness of the synthesized Ag-Dopa-CP samples was evaluated by investigating the release of silver from the papers. It is important to investigate the release of silver from AgNPs based antibacterial materials for two reasons. First, exposure of silver beyond a certain limit can cause some human health effects.75 Second, release of silver from nano-silver based composite materials reasonably causes the bactericidal efficacy to decrease gradually with time and thus restrict the repeated use of the same material. We employed FAAS to measure the total silver released after a certain time of immersion in water. The total amount of silver released after 60 m duration was less than 0.02 % and after 8 h it reached only 0.12 %. Both these values were exceedingly smaller compared to what Dankovich et al. reported for their AgNPs containing paper.31 This low leaching was expected for our Ag-Dopa-CP papers where the dopamine molecules glue the AgNPs to retain them on the surface. The loss of silver in this study is also very low compared to the leaching (~1.15% of total silver deposited) from AgNPs anchored glass substrate, which was generated by immobilizing AgNPs on an amine-


26

Page 27 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


functionalized silica surface.24 Hence, the comparison of our leaching data with that of other similar reports clearly displays that the mussel-inspired immobilization strategy described in this report is acutely effective for retaining the AgNPs on paper surface. We performed additional control experiments to evaluate the mechanical robustness of our synthesized antibacterial paper samples. Ultra-sonication of the Ag-Dopa-CP samples immersed in water was employed for 30 m to test the mechanical robustness of the paper. Atomic absorption spectroscopy analysis of the water sample indicated that the amount of silver lost in the sonication process was only 0.09%. Moreover, to test if the immobilized AgNPs can withstand any physical/mechanical deformation, we performed folding and unfolding, bending, twisting, and rubbing on a 2 x 2 cm2 piece of dried Ag-Dopa-CP sample at least for ten cycles and then measured the weight before and after the tests using a six decimal analytical balance. No significant change in weight of the samples indicated excellent mechanical sustainability of the antibacterial paper against physical deformation. In addition to sustainable immobilization of AgNPs onto the paper surface, it was also critical for the use of paper in packaging materials that the cellulose paper did not lose its mechanical strength after the modification. The mechanical strengths of the paper before and after the immobilization of AgNPs were measured and discussed in the supporting info (Supporting Info, Figure S10) of the manuscript.

Conclusion Inspired by the marine mussel, we developed a facile and highly effective strategy for the robust immobilization of AgNPs onto cellulose paper. This strategy explored a new way of functionalizing CP, which otherwise possesses a lack of functional groups on the surface providing not as much of specific chemical reactivity. We functionalized CP with succinic acid


27


Page 28 of 41

groups, which were further functionalized with dopamine via a coupling reaction to get the dopamine-modified paper. These two steps for covalently attaching the dopamine molecules to the paper surface were proven useful in utilizing the tethered catechol groups to effectively immobilize the AgNPs. The catechol groups reduced the silver salt and subsequently held the produced nanopartciles via strong adhesion. The loading of AgNPs onto the paper surface and consequently the corresponding antimicrobial properties strongly depended on the immersion time of the dopamine-modified cellulose paper in ammoniacal silver nitrate solution. Excellent antimicrobial properties along with exceedingly low leaching of AgNPs from the paper surface would obviously facilitate the use of the fabricated Ag-Dopa-CP as a packaging material. Moreover, owing to the high adhesion of the dopamine moiety to nearly all inorganic substances, this approach might be extendable to robust immobilization of any other metals and metal oxides nanoparticles onto cellulose paper to explore new applications in numerous paper-based chemical and biological sensors.46 ASSOCIATED CONTENT Supporting Information. The Supporting Information is available free of charge on the ACS Publications website http://pubs.acs.org. This file contains the details about the characterizations of the modified CP, and Ag-Dopa-CP. AUTHOR INFORMATION Corresponding Author [email protected], [email protected] (M.S.A.); [email protected] (H.Z.) Author Contributions


28

Page 29 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. ACKNOWLEDGMENTS The authors thank BUET, Ministry of Science and Technology (Government of the People's Republic of Bangladesh), and The World Academy of Sciences (TWAS) for the funding. H. Zeng acknowledges the support from the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Canada Research Chairs Program. We also acknowledge the collaboration with Dr. Julianne M. Gibbs (University of Alberta) for the XPS analyses and Mr. Atique Ullah (Atomic Energy Centre, Dhaka, Bangladesh) for assistance on a series of AAS tests.

REFERENCES (1)

Angelakis, E.; Azhar, E. I.; Bibi, F.; Yasir, M.; Al-Ghamdi, A. K.; Ashshi, A. M.;

Elshemi, A. G.; Raoult, D. Paper Money and Coins as Potential Vectors of Transmissible Disease. Future Microbiol. 2014, 9, 249-261, DOI 10.2217/fmb.13.161. (2)

Dong, C.; Cairney, J.; Sun, Q.; Maddan, O. L.; He, G.; Deng, Y. Investigation of

Mg(OH)2 Nanoparticles as an Antibacterial Agent. J. Nanopart. Res. 2010, 12, 2101-2109, DOI 10.1007/s11051-009-9769-9. (3)

Stover, C. K.; Pham, X. Q.; Erwin, A. L.; Mizoguchi, S. D.; Warrener, P.; Hickey,

M. J.; Brinkman, F. S.; Hufnagle, W. O.; Kowalik, D. J.; Lagrou, M.; Garber, R. L.; Goltry, L.; Tolentino, E.; Westbrock-Wadman, S.; Yuan, Y.; Brody, L. L.; Coulter, S. N.; Folger, K. R.; Kas, A.; Larbig, K.; Lim, R.; Smith, K.; Spencer, D.; Wong, G. K.; Wu, Z.; Paulsen, I. T.; Reizer, J.; Saier, M. H.; Hancock, R. E.; Lory, S.; Olson, M. V. Complete Genome Sequence of


29


Page 30 of 41

Pseudomonas aeruginosa PAO1, an Opportunistic Pathogen. Nature 2000, 406, 959-964, DOI 10.1038/35023079. (4)

Ma, D.; Cook, D. N.; Hearst, J. E.; Nikaido, H. Efflux Pumps and Drug

Resistance in Gram-Negative Bacteria. Trends Microbiol. 1994, 2, 489-493, DOI 10.1016/0966842X(94)90654-8. (5)

Amini, E.; Azadfallah, M.; Layeghi, M.; Talaei-Hassanlouei, R.: Silver-

Nanoparticle-Impregnated Cellulose Nanofiber Coating for Packaging Paper, 2016, 23, 557-570, DOI 10.1007/s10570-015-0846-1. (6)

Hu, W.; Peng, C.; Luo, W.; Lv, M.; Li, X.; Li, D.; Huang, Q.; Fan, C. Graphene-

Based Antibacterial Paper. ACS Nano 2010, 4, 4317-4323, DOI 10.1021/nn101097v. (7)

Echegoyen, Y.; Nerin, C. Nanoparticle Release from Nano-Silver Antimicrobial

Food Containers. Food Chem. Toxicol. 2013, 62, 16-22, DOI 10.1016/j.fct.2013.08.014. (8)

Stewart, P. S.; Costerton, J. W. Antibiotic Resistance of Bacteria in Biofilms.

Lancet 2001, 358, 135-138. (9)

Huang, X.; Hu, N.; Wang, X.; Zhang, Y. S.; Sun, R. Copper Sulfide

Nanoparticle/Cellulose Composite Paper: Room-Temperature Green Fabrication for NIR LaserInducible Ablation of Pathogenic Microorganisms. ACS Sustainable Chem. Eng. 2017, 5, 26482655, DOI 10.1021/acssuschemeng.6b03003. (10)

Kumar, A.; Vemula, P. K.; Ajayan, P. M.; John, G. Silver-Nanoparticle-

Embedded Antimicrobial Paints Based on Vegetable Oil. Nat. Mater. 2008, 7, 236, DOI 10.1038/nmat2099


30

Page 31 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(11)

Zhao, Y.; Tian, Y.; Cui, Y.; Liu, W.; Ma, W.; Jiang, X. Small Molecule-Capped

Gold Nanoparticles as Potent Antibacterial Agents That Target Gram-Negative Bacteria. J. Am. Chem. Soc. 2010, 132, 12349-12356, DOI 10.1021/ja1028843. (12)

Wei, C.; Lin, W. Y.; Zainal, Z.; Williams, N. E.; Zhu, K.; Kruzic, A. P.; Smith, R.

L.; Rajeshwar, K. Bactericidal Activity of TiO2 Photocatalyst in Aqueous Media: Toward a Solar-Assisted Water Disinfection System. Environ. Sci. Technol. 1994, 28, 934-938, DOI 10.1021/es00054a027. (13)

Chowdhury, A. N.; Azam, M. S.; Aktaruzzaman, M.; Rahim, A. Oxidative and

Antibacterial Activity of Mn3O4. J. Hazard. Mater. 2009, 172, 1229-1235, DOI 10.1016/j.jhazmat.2009.07.129. (14)

Raghupathi, K. R.; Koodali, R. T.; Manna, A. C. Size-Dependent Bacterial

Growth Inhibition and Mechanism of Antibacterial Activity of Zinc Oxide Nanoparticles. Langmuir 2011, 27, 4020-4028, DOI 10.1021/la104825u. (15)

Kahrilas, G. A.; Haggren, W.; Read, R. L.; Wally, L. M.; Fredrick, S. J.; Hiskey,

M.; Prieto, A. L.; Owens, J. E. Investigation of Antibacterial Activity by Silver Nanoparticles Prepared by Microwave-Assisted Green Syntheses with Soluble Starch, Dextrose, and Arabinose. ACS Sustainable Chem. Eng. 2014, 2, 590-598, DOI 10.1021/sc400487x. (16)

Ma, P.; Jiang, L.; Yu, M.; Dong, W.; Chen, M. Green Antibacterial

Nanocomposites from Poly(lactide)/Poly(butylene adipate-co-terephthalate)/Nanocrystal Cellulose–Silver Nanohybrids. ACS Sustainable Chem. Eng. 2016, 4, 6417-6426, DOI 10.1021/acssuschemeng.6b01106. (17)

Rodriguez-Gonzalez, V.; Dominguez-Espindola, R. B.; Casas-Flores, S.; Patron-

Soberano, O. A.; Camposeco-Solis, R.; Lee, S. W. Antifungal Nanocomposites Inspired by


31


Page 32 of 41

Titanate Nanotubes for Complete Inactivation of Botrytis cinerea Isolated from Tomato Infection. ACS Appl. Mater. Interfaces 2016, 8, 31625-31637, DOI 10.1021/acsami.6b10060. (18)

Lara, H. H.; Ayala-Nuñez, N. V.; Ixtepan-Turrent, L.; Rodriguez-Padilla, C.

Mode of Antiviral Action of Silver Nanoparticles against HIV-1. J. Nanobiotechnology 2010, 8, 1, DOI 10.1186/1477-3155-8-1. (19)

AshaRani, P. V.; Low Kah Mun, G.; Hande, M. P.; Valiyaveettil, S. Cytotoxicity

and Genotoxicity of Silver Nanoparticles in Human Cells. ACS Nano 2009, 3, 279-290, DOI 10.1021/nn800596w. (20)

Choi, O.; Hu, Z. Size Dependent and Reactive Oxygen Species Related

Nanosilver Toxicity to Nitrifying Bacteria. Environ. Sci. Technol. 2008, 42, 4583-4588, DOI 10.1021/es703238h. (21)

Quinteros, M. A.; Cano Aristizabal, V.; Dalmasso, P. R.; Paraje, M. G.; Paez, P.

L. Oxidative Stress Generation of Silver Nanoparticles in Three Bacterial Genera and its Relationship with the Antimicrobial Activity. Toxicol. In Vitro 2016, 36, 216-223, DOI 10.1016/j.tiv.2016.08.007. (22)

Bae, E.; Park, H. J.; Lee, J.; Kim, Y.; Yoon, J.; Park, K.; Choi, K.; Yi, J. Bacterial

Cytotoxicity of the Silver Nanoparticle Related to Physicochemical Metrics and Agglomeration Properties. Environ. Toxicol. Chem. 2010, 29, 2154-2160, DOI 10.1002/etc.278. (23)

Kvítek, L.; Panáček, A.; Soukupová, J.; Kolář, M.; Večeřová, R.; Prucek, R.;

Holecová, M.; Zbořil, R. Effect of Surfactants and Polymers on Stability and Antibacterial Activity of Silver Nanoparticles (NPs). J. Phys. Chem. C 2008, 112, 5825-5834, DOI 10.1021/jp711616v.


32

Page 33 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(24)

Agnihotri, S.; Mukherji, S.; Mukherji, S. Immobilized Silver Nanoparticles

Enhance Contact Killing and Show Highest Efficacy: Elucidation of the Mechanism of Bactericidal Action of Silver. Nanoscale 2013, 5, 7328-7340, DOI 10.1039/C3NR00024A. (25)

Wijnhoven, S. W. P.; Peijnenburg, W. J. G. M.; Herberts, C. A.; Hagens, W. I.;

Oomen, A. G.; Heugens, E. H. W.; Roszek, B.; Bisschops, J.; Gosens, I.; Van De Meent, D.; Dekkers, S.; De Jong, W. H.; van Zijverden, M.; Sips, A. J. A. M.; Geertsma, R. E. Nano-Silver – a Review of Available Data and Knowledge Gaps in Human and Environmental Risk Assessment. Nanotoxicology 2009, 3, 109-138, DOI 10.1080/17435390902725914. (26)

Chen, X.; Schluesener, H. J. Nanosilver: a Nanoproduct in Medical Application.

Toxicol. Lett. 2008, 176, 1-12, DOI 10.1016/j.toxlet.2007.10.004. (27)

Ding, X.; Shi, L.; Liu, C.; Sun, B. A Randomized Comparison Study of Aquacel

Ag and Alginate Silver as Skin Graft Donor Site Dressings. Burns 2013, 39, 1547-1550, DOI 10.1016/j.burns.2013.04.017. (28)

Zhou, R.; Srinivasan, M. P. In Situ Synthesis and Immobilization of Metallic

Nanoparticles on a Calixarene Monolayer. Langmuir 2013, 29, 13042-13049, DOI 10.1021/la401751d. (29)

Kent, R. D.; Vikesland, P. J. Controlled Evaluation of Silver Nanoparticle

Dissolution Using Atomic Force Microscopy. Environ. Sci. Technol. 2012, 46, 6977-6984, DOI 10.1021/es203475a. (30)

Charlot, A.; Sciannamea, V.; Lenoir, S.; Faure, E.; Jerome, R.; Jerome, C.; Van

De Weerdt, C.; Martial, J.; Archambeau, C.; Willet, N.; Duwez, A.-S.; Fustin, C.-A.; Detrembleur, C. All-in-One Strategy for the Fabrication of Antimicrobial Biomimetic Films on Stainless Steel. J. Mater. Chem. 2009, 19, 4117-4125, DOI 10.1039/B820832H.


33


(31)

Page 34 of 41

Dankovich, T. A.; Gray, D. G. Bactericidal Paper Impregnated with Silver

Nanoparticles for Point-of-Use Water Treatment. Environ. Sci. Technol. 2011, 45, 1992-1998, DOI 10.1021/es103302t. (32)

Drogat, N.; Granet, R.; Le Morvan, C.; Bégaud-Grimaud, G.; Krausz, P.; Sol, V.

Chlorin-PEI-Labeled Cellulose Nanocrystals: Synthesis, Characterization and Potential Application in PDT. Bioorg. Med. Chem. Lett. 2012, 22, 3648-3652, DOI 10.1016/j.bmcl.2012.04.044. (33)

Ringot, C.; Sol, V.; Barrière, M.; Saad, N.; Bressollier, P.; Granet, R.; Couleaud,

P.; Frochot, C.; Krausz, P. Triazinyl Porphyrin-Based Photoactive Cotton Fabrics: Preparation, Characterization, and Antibacterial Activity. Biomacromolecules 2011, 12, 1716-1723, DOI 10.1021/bm200082d. (34)

Carpenter, B. L.; Scholle, F.; Sadeghifar, H.; Francis, A. J.; Boltersdorf, J.;

Weare, W. W.; Argyropoulos, D. S.; Maggard, P. A.; Ghiladi, R. A. Synthesis, Characterization, and Antimicrobial Efficacy of Photomicrobicidal Cellulose Paper. Biomacromolecules 2015, 16, 2482-2492, DOI 10.1021/acs.biomac.5b00758. (35)

Taglietti, A.; Diaz Fernandez, Y. A.; Amato, E.; Cucca, L.; Dacarro, G.; Grisoli,

P.; Necchi, V.; Pallavicini, P.; Pasotti, L.; Patrini, M. Antibacterial Activity of GlutathioneCoated Silver Nanoparticles against Gram Positive and Gram Negative Bacteria. Langmuir 2012, 28, 8140-8148, DOI 10.1021/la3003838. (36)

Khan, S. S.; Kumar, E. B.; Mukherjee, A.; Chandrasekaran, N. Bacterial

Tolerance to Silver Nanoparticles (SNPs): Aeromonas punctata Isolated from Sewage Environment. J. Basic Microbiol. 2011, 51, 183-190, DOI doi:10.1002/jobm.201000067.


34

Page 35 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(37)

Kim, W.; Kim, Y.-H.; Park, H.-K.; Choi, S. Facile Fabrication of a Silver

Nanoparticle Immersed, Surface-Enhanced Raman Scattering Imposed Paper Platform through Successive Ionic Layer Absorption and Reaction for On-Site Bioassays. ACS Appl. Mater. Interfaces 2015, 7, 27910-27917, DOI 10.1021/acsami.5b09982. (38)

Lokanathan, A. R.; Uddin, K. M. A.; Rojas, O. J.; Laine, J. Cellulose

Nanocrystal-Mediated Synthesis of Silver Nanoparticles: Role of Sulfate Groups in Nucleation Phenomena. Biomacromolecules 2014, 15, 373-379, DOI 10.1021/bm401613h. (39)

Xu, Y.; You, F.; Sun, H.; Shao, L. Realizing Mussel-Inspired Polydopamine

Selective Layer with Strong Solvent Resistance in Nanofiltration toward Sustainable Reclamation. ACS Sustainable Chem. Eng. 2017, 5, 5520-5528, DOI 10.1021/acssuschemeng.7b00871. (40)

Marcelo, G.; Fernandez-Garcia, M. Direct Preparation of PNIPAM Coating Gold

Nanoparticles by Catechol Redox and Surface Adhesion Chemistry. RSC Adv. 2014, 4, 1174011749, DOI 10.1039/C3RA47880G. (41)

Liu, Y.; Ai, K.; Lu, L. Polydopamine and Its Derivative Materials: Synthesis and

Promising Applications in Energy, Environmental, and Biomedical Fields. Chem. Rev. 2014, 114, 5057-5115, DOI 10.1021/cr400407a. (42)

Liu, R.; Guo, Y.; Odusote, G.; Qu, F.; Priestley, R. D. Core–Shell Fe3O4

Polydopamine Nanoparticles Serve Multipurpose as Drug Carrier, Catalyst Support and Carbon Adsorbent. ACS Appl. Mater. Interfaces 2013, 5, 9167-9171, DOI 10.1021/am402585y. (43)

Xie, Y.; Yan, B.; Xu, H.; Chen, J.; Liu, Q.; Deng, Y.; Zeng, H. Highly

Regenerable Mussel-Inspired Fe3O4@Polydopamine-Ag Core–Shell Microspheres as Catalyst


35


Page 36 of 41

and Adsorbent for Methylene Blue Removal. ACS Appl. Mater. Interfaces 2014, 6, 8845-8852, DOI 10.1021/am501632f. (44)

Ma, A.; Xie, Y.; Xu, J.; Zeng, H.; Xu, H. The Significant Impact of Polydopamine

on the Catalytic Performance of the Carried Au Nanoparticles. Chem. Commun. 2015, 51, 14691471, DOI 10.1039/C4CC08489F. (45)

Sileika, T. S.; Kim, H.-D.; Maniak, P.; Messersmith, P. B. Antibacterial

Performance of Polydopamine-Modified Polymer Surfaces Containing Passive and Active Components. ACS Appl. Mater. Interfaces 2011, 3, 4602-4610, DOI 10.1021/am200978h. (46)

Ge, S.; Zhang, L.; Zhang, Y.; Lan, F.; Yan, M.; Yu, J. Nanomaterials-Modified

Cellulose Paper as a Platform for Biosensing Applications. Nanoscale 2017, 9, 4366-4382, DOI 10.1039/C6NR08846E. (47)

Roy, D.; Guthrie, J. T.; Perrier, S. Graft Polymerization: Grafting Poly(styrene)

from Cellulose via Reversible Addition−Fragmentation Chain Transfer (RAFT) Polymerization. Macromolecules 2005, 38, 10363-10372, DOI 10.1021/ma0515026. (48)

Belhalfaoui, B.; Aziz, A.; Elandaloussi el, H.; Ouali, M. S.; De Menorval, L. C.

Succinate-Bonded Cellulose: a Regenerable and Powerful Sorbent for Cadmium-Removal from Spiked High-Hardness Groundwater. J. Hazard. Mater. 2009, 169, 831-837, DOI 10.1016/j.jhazmat.2009.04.021. (49)

Rahman, M.; Rahman, M. M.; Deb, S. C.; Alam, M. S.; Alam, M. J.; Islam, M. T.

Molecular Identification of Multiple Antibiotic Resistant Fish Pathogenic Enterococcus faecalis and their Control by Medicinal Herbs. Sci. Rep. 2017, 7, 3747, DOI 10.1038/s41598-017-036731.


36

Page 37 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(50)

Hossain, N.; Rahman, M. M.: Antibiotic and Herbal Sensitivity of Some

Aeromonas sp. Isolates Collected from Diseased Carp Fishes. Progress. Agric. 2010, 21, 117129, DOI 10.3329/pa.v21i1-2.16758. (51)

Islam, M. T.; Croll, D.; Gladieux, P.; Soanes, D. M.; Persoons, A.; Bhattacharjee,

P.; Hossain, M. S.; Gupta, D. R.; Rahman, M. M.; Mahboob, M. G.; Cook, N.; Salam, M. U.; Surovy, M. Z.; Sancho, V. B.; Maciel, J. L. N.; NhaniJúnior, A.; Castroagudín, V. L.; Reges, J. T. d. A.; Ceresini, P. C.; Ravel, S.; Kellner, R.; Fournier, E.; Tharreau, D.; Lebrun, M.-H.; McDonald, B. A.; Stitt, T.; Swan, D.; Talbot, N. J.; Saunders, D. G. O.; Win, J.; Kamoun, S. Emergence of Wheat Blast in Bangladesh was Caused by a South American Lineage of Magnaporthe oryzae. BMC Biol. 2016, 14, 84, DOI 10.1186/s12915-016-0309-7. (52)

Lee, C. M.; Kubicki, J. D.; Fan, B.; Zhong, L.; Jarvis, M. C.; Kim, S. H.

Hydrogen-Bonding Network and OH Stretch Vibration of Cellulose: Comparison of Computational Modeling with Polarized IR and SFG Spectra. J. Phys. Chem. B 2015, 119, 15138-15149, DOI 10.1021/acs.jpcb.5b08015. (53)

Tankhiwale, R.; Bajpai, S. K. Graft Copolymerization onto Cellulose-Based Filter

Paper and Its Further Development as Silver Nanoparticles Loaded Antibacterial FoodPackaging Material. Colloids Surf. B: Biointerfaces 2009, 69, 164-168, DOI 10.1016/j.colsurfb.2008.11.004. (54)

Zhang, X.; Li, Z.; Yuan, X.; Cui, Z.; Yang, X. Fabrication of Dopamine-Modified

Hyaluronic Acid/Chitosan Multilayers on Titanium Alloy by Layer-by-Layer Self-Assembly for Promoting Osteoblast Growth. Appl. Surf. Sci. 2013, 284, 732-737, DOI 10.1016/j.apsusc.2013.08.002.


37


(55)

Page 38 of 41

Marcelo, G.; López-González, M.; Mendicuti, F.; Tarazona, M. P.; Valiente, M.

Poly(N-isopropylacrylamide)/Gold Hybrid Hydrogels Prepared by Catechol Redox Chemistry. Characterization and Smart Tunable Catalytic Activity. Macromolecules 2014, 47, 6028-6036, DOI 10.1021/ma501214k. (56)

Chen, J.; Li, Y.; Huang, K.; Wang, P.; He, L.; Carter, K. R.; Nugen, S. R.

Nanoimprinted Patterned Pillar Substrates for Surface-Enhanced Raman Scattering Applications. ACS Appl. Mater. Interfaces 2015, 7, 22106-22113, DOI 10.1021/acsami.5b07879. (57)

Murray, B. J.; Li, Q.; Newberg, J. T.; Menke, E. J.; Hemminger, J. C.; Penner, R.

M. Shape- and Size-Selective Electrochemical Synthesis of Dispersed Silver(I) Oxide Colloids. Nano Lett. 2005, 5, 2319-2324, DOI 10.1021/nl051834o. (58)

Hammond, J. S.; Gaarenstroom, S. W.; Winograd, N. X-ray Photoelectron

Spectroscopic Studies of Cadmium- and Silver-Oxygen Surfaces. Anal. Chem. 1975, 47, 21932199, DOI 10.1021/ac60363a019. (59)

Diaz, J.; Paolicelli, G.; Ferrer, S.; Comin, F. Separation of the sp3 and sp2

Components in the C1s Photoemission Spectra of Amorphous Carbon Films. Phys. Rev. B Condens. Matter 1996, 54, 8064-8069, DOI 10.1103/PhysRevB.54.8064. (60)

Goldmann, A. S.; Tischer, T.; Barner, L.; Bruns, M.; Barner-Kowollik, C. Mild

and Modular Surface Modification of Cellulose via Hetero Diels−Alder (HDA) Cycloaddition. Biomacromolecules 2011, 12, 1137-1145, DOI 10.1021/bm101461h. (61)

Stevens, J. S.; Schroeder, S. L. M. Quantitative Analysis of Saccharides by X-ray

Photoelectron Spectroscopy. Surf. Interface Anal. 2009, 41, 453-462, DOI doi:10.1002/sia.3047.


38

Page 39 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(62)

Ho, C. C.; Ding, S. J. The pH-Controlled Nanoparticles Size of Polydopamine for

Anti-Cancer Drug Delivery. J. Mater. Sci. Mater. Med. 2013, 24, 2381-2390, DOI 10.1007/s10856-013-4994-2. (63)

Gilbert, J. B.; Rubner, M. F.; Cohen, R. E. Depth-Profiling X-ray Photoelectron

Spectroscopy (XPS) Analysis of Interlayer Diffusion in Polyelectrolyte Multilayers. Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 6651-6656, DOI 10.1073/pnas.1222325110. (64)

Schwaner, A. L.; Pylant, E. D.; White, J. M. Electron: Induced Surface

Chemistry: Synthesis of NHx Fragments on Ag(111). J. Vac. Sci. Technol. A 1996, 14, 14531456, DOI 10.1116/1.579968. (65)

Laksono, E.; Galtayries, A.; Argile, C.; Marcus, P. Adsorption of NH3 on Oxygen

Pre-Treated Ni(111). Surf. Sci. 2003, 530, 37-54, DOI 10.1016/S0039-6028(03)00267-X. (66)

Ciolacu, D.; Ciolacu, F.; Popa, V. I. Amorphous Cellulose—Structure and

Characterization. Cellulose Chem. Technol. 2011, 45, 13-21. (67)

Zhou, S.; Xie, M.; Yuan, X.; Zeng, F.; Zou, W.; Yuan, D. Polyaniline/AgCl

Hybrid Materials for Selective Determination of Dopamine by Electrochemical Methods. Am. J. Analyt. Chem. 2012, 3, 385-391, DOI 10.4236/ajac.2012.35051. (68)

Stratev, D.; Odeyemi, O. A. Antimicrobial Resistance of Aeromonas hydrophila

Isolated from Different Food Sources: A Mini-Review. J. Infect. Public Health 2016, 9, 535-544, DOI 10.1016/j.jiph.2015.10.006. (69)

Lv, M.; Su, S.; He, Y.; Huang, Q.; Hu, W.; Li, D.; Fan, C.; Lee, S. T. Long-Term

Antimicrobial Effect of Silicon Nanowires Decorated with Silver Nanoparticles. Adv. Mater. 2010, 22, 5463-5467, DOI 10.1002/adma.201001934.


39


(70)

Page 40 of 41

Zarei, M.; Jamnejad, A.; Khajehali, E. Antibacterial Effect of Silver Nanoparticles

Against Four Foodborne Pathogens. Jundishapur J. Microbiol. 2014, 7, e8720, DOI 10.5812/jjm.8720. (71)

Disaanayake, D. M. B. T.; Faoagali, J.; Laroo, H.; Hancock, G.; Whitehouse, M.

Efficacy of Some Colloidal Silver Preparations and Silver Salts Against Proteus Bacteria, One Possible Cause of Rheumatoid Arthritis. Inflammopharmacol. 2014, 22, 73-77, DOI 10.1007/s10787-013-0198-0. (72)

Buszewski, B.; Railean-Plugaru, V.; Pomastowski, P.; Rafinska, K.; Szultka-

Mlynska, M.; Golinska, P.; Wypij, M.; Laskowski, D.; Dahm, H. Antimicrobial Activity of Biosilver Nanoparticles Produced by a Novel Streptacidiphilus durhamensis strain. J. Microbiol. Immunol. Infect. 2018, 51, 45-54, DOI 10.1016/j.jmii.2016.03.002. (73)

Mukherji, S.; Ruparelia, J.; Agnihotri, S.: Antimicrobial Activity of Silver and

Copper Nanoparticles: Variation in Sensitivity Across Various Strains of Bacteria and Fungi. In Nano-Antimicrobials: Progress and Prospects; Cioffi, N., Rai, M., Eds.; Springer Berlin Heidelberg: Berlin, Heidelberg, 2012, 225-251, DOI 10.1007/978-3-642-24428-5_8. (74)

Goei, R.; Lim, T. T. Ag-Decorated TiO2 Photocatalytic Membrane with

Hierarchical Architecture: Photocatalytic and Anti-Bacterial Activities. Water Res. 2014, 59, 207-218, DOI 10.1016/j.watres.2014.04.025. (75)

Drake, P. L.; Hazelwood, K. J. Exposure-Related Health Effects of Silver and

Silver Compounds: a Review. Ann. Occup. Hyg. 2005, 49, 575-585, DOI 10.1093/annhyg/mei019.


40

Page 41 of 41 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


For Table of Contents Use Only

Synopsis. A sustainable chemical process is reported for the immobilization of AgNPs onto cellulose paper via a modified mussel-inspired strategy to introduce antimicrobial properties.


41

Mussel-Inspired Immobilization of Silver ... - ACS Publications

Recommend Documents