Selective Adsorption toward Hg(II) and Inhibitory Effect on Bacterial

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Surfaces, Interfaces, and Applications

Selective Adsorption toward Hg(II) and Inhibitory Effect on Bacterial Growth Occurring on ThiosemicarbazideFunctionalized Chitosan Microsphere Surface Yan Wang, Qi Feng Dang, Chengsheng Liu, Dejun Yu, Xiaoying Pu, Qiongqiong Wang, Hong Gao, Bainian Zhang, and Dongsu Cha ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.8b14893 • Publication Date (Web): 26 Oct 2018 Downloaded from http://pubs.acs.org on October 27, 2018

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ACS Applied Materials & Interfaces

Selective Adsorption toward Hg(II) and Inhibitory Effect on Bacterial Growth Occurring on Thiosemicarbazide-Functionalized Chitosan Microsphere Surface

Yan Wang,† Qifeng Dang,† Chengsheng Liu,*,† Dejun Yu,‡ Xiaoying Pu,† Qiongqiong Wang,† Hong Gao,† Bainian Zhang,§ and Dongsu Cha⊥

†

College of Marine Life Sciences, Ocean University of China, 5 Yushan Road, Qingdao 266003,

PR China ‡

Qingdao Marine Biomedical Research Institute, 23 Hong Kong East Road, Qingdao 266071, PR

China §

Qingdao Aorun Biotechnology Co., Ltd., Room 602, Century Mansion, 39 Donghaixi Road,

Qingdao 266071, PR China ⊥

The Graduate School of Biotechnology, Korea University, Seoul 136-701, South Korea

KEYWORDS: chitosan, thiosemicarbazide, selective adsorption, Hg(II), adsorption mechanism, antibacterial activity 1

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ABSTRACT: Work presented here aims to fabricate dual-purpose adsorbent with adsorption selectivity for Hg(II) and antibacterial activity. TSC-PGMA-MACS microspheres were first constructed via esterification of malic acid (MA) with chitosan (CS), and through successively grafting glycidyl methacrylate (GMA) and thiosemicarbazide (TSC) onto MACS microsphere surfaces. FTIR, EA, EDX, XRD, DSC, TG, DTG, SEM and BET results provided ample evidence that new mesoporous adsorbent, with 35.340 m2 g−1 of specific surface area and abundant −NH2 and C=S, was successfully fabricated and had loose crystalline, thermodynamically stable and well-defined architectures, beneficial for Hg(II) adsorption and bacterial cell killing. Optimal adsorption parameters were determined via varying pH, time, concentrations and temperatures, and pH 6.0 was chosen as an optimal pH for Hg(II) adsorption. Adsorption behavior, described well by pseudo-second-order kinetic and Langmuir isotherm models, and thermodynamic parameters implied a chemical, monolayer, endothermic and spontaneous adsorption process, and the maximum adsorption capacity for Hg(II) was 242.7 mg g−1, higher than most of the available adsorbents. Competitive adsorption exhibited excellent adsorption selectivity for Hg(II) in binary-metal solutions. Besides, TSC-PGMA-MACS microspheres had outstanding reusability even after five-time recycles, with adsorption capability loss < 14%. Several potential adsorption sites and bonding modes were proposed. Notably, TSC-PGMA-MACS microspheres before and after adsorption were of high antibacterial activity against E. coli and S. aureus (MICs, 2 and 0.25 mg mL−1), superior to CS powders, and possible antibacterial mechanisms were also summarized. Altogether, dual-purpose TSC-PGMA-MACS microspheres might be promising adsorbent for contaminated water scavenging.

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1. INTRODUCTION Water contamination is mainly ascribed to various contaminants, including physical (e.g., suspended solid and thermal pollution), chemical (e.g., organic and inorganic compounds), biological (e.g., viruses, bacteria, fungi and planktons) and radiological substances. These notorious pollutants, especially heavy metal ions (HMIs) and pathogenic microorganisms, are often transferred directly or indirectly to the human body via food chains, causing actual bodily harm.1 Hg(II), one of the most toxic HMIs, is deemed the initiation of various symptoms such as neuronal disorders, renal dysfunction, hepatic injuries, and immune system damage.2 Also, pathogens in water, such as E. coli, V. cholerae, poliovirus and Hanta virus, tremendously impact human health, which are listed in Handbook on Water Security recommended by USEPA. Thus, the removal of pollutants from contaminated water is an urgent need for providing high-quality water to our society. To remove HMIs from polluted water, researchers have developed diverse materials as absorbents, e.g., activated carbon, grapheme oxide, cellulose, TiO2, silica, zeolite, chitosan (CS) and its derivatives.3–10 Among numerous absorbents, CS is considered a suitable candidate for fabricating adsorbents for HMI removal, owing to raw material sufficiency, low energy consumption, desirable adsorbability, and non-toxicity. Consequently, varieties of satisfactory CS-based adsorbents have been fabricated for HMI adsorption.10–14 For example, Zarghami et al. design CS-PAMAM dendrimer with the greatly enhanced capability of chelating with Pb(II);13 and Monier et al. prepare cross-linked magnetic CS-phenylthiourea resin with adsorption capacity of 135, 120 and 52 mg g−1 for Hg(II), Cd(II) and Zn(II).12 However, most CS-based absorbents are used for uptake of single or multiple HMI(s), and work on selective removal of HMIs, not using imprinting technology, is relatively rare. Also, much work employs conventional 3



cross-linkers to improve mechanical strength and chemical stability and unfortunately, these cross-linkers, e.g., formaldehyde,12 glutaraldehyde,10 glyoxal,11 and epichlorohydrin,9 are toxic and substantially compromise adsorption capacity, because of the occupation of adsorption sites by cross-linkers. Additionally, previous studies rarely focus on multipurpose CS-based absorbents capable of removing more than one class of pollutants from wastewater. Notably, several CS-based adsorbents for selective adsorption toward Hg(II) have been synthesized, using thiourea, phenylthiourea and thiocarbamoyl as modifiers,12,15–17 showing greater adsorption selectivity for Hg(II) and agreeing well with HSAB theory. But, to the best of our knowledge, the CS-based adsorbent for selective adsorption toward Hg(II) using thiosemicarbazide (TSC) as a modifier has not been reported. Generally, chemical disinfectants (CDs) (e.g., free chlorine, chloramines and ozone) are used to kill bacteria in contaminated water.18 Despite high efficiency, broad spectrum, quick and lasting efficacy, residual CDs may produce carcinogenic byproducts, causing secondary pollution. Therefore, new materials, e.g., Ag nanoparticles, TiO2, fullerol, carbon nanotubes, cellulose, CS and its derivatives,19–22 have been developed, instead of CDs. Recently, numerous studies focus on CS and its derivates, owing to desirable antibacterial activity, as well as to biocompatibility, non-toxicity and biodegradability.22–26 As for antibacterial mechanisms of CS and its derivatives, the most approved one is that protonated moieties (e.g., −NH+3) in solutions alter bacterial cytomembrane permeability via electrostatic interactions, causing the death of bacteria. Self-evidently, researchers are mainly committed to synthesizing soluble CS derivatives as antiseptics used in pharmaceutical, food, agricultural and cosmetic fields. To date, the application of insoluble antibacterial CS derivatives to the water treatment field can hardly be found. If adsorption selectivity for Hg(II) is related to N and S atoms, then grafting −NH2 and C=S 4


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onto CS-based adsorbent surfaces will endow adsorbents with adsorption selectivity for Hg(II); if antibacterial activity of insoluble CS-based adsorbents in solutions is related to the protonation of surface moieties, as well as the positive charge density on surfaces, then the introduction of −NH2 and C=S will enhance antibacterial activity. Taking multiple elements into consideration, a strategy to engineer CS-based microspheres with adsorption selectivity for Hg(II) and high antibacterial activity was here proposed. First, we prepared MACS microspheres by a reversed-phase emulsification method, via esterification between CS and malic acid (MA) that is a versatile dicarboxylic-acid compound. With such an achievement, multiple purposes can be achieved: (1) to obtain desirable microspheres of ~ 40 μm in diameter, facilitating manipulation, unlike nanoparticles or powders; (2) to enhance mechanical strength and stability via esterification of −OH on CS with two terminal −COOH on MA, instead of conventional cross-linkers, leading to net-like architectures and avoiding secondary pollution risk caused by conventional cross-linkers to organisms; (3) to provide a compensation for adsorption sites, due to the introduction of plenty of O atoms on MA. Second, we grafted glycidyl methacrylate (GMA) onto MACS microsphere surfaces to construct poly(GMA) MACS (PGMA-MACS) microspheres via graft copolymerization. This construction aims to (i) use the grafted GMA as an irreplaceable “bridge” to connect with TSC in the following reaction, because epoxy group on GMA has extraordinary ring-opening ability to react with −NH2 on TSC at high temperature;5 (ii) further improve mechanical strength and stability, since vinyl group on GMA is fairly prone to copolymerization in the presence of initiators; and (iii) increase adsorption sites, due to the ample supply of O on GMA. Finally, we grafted TSC onto PGMA-MACS microsphere surfaces to fabricate TSC-PGMA-MACS microspheres through ring-opening reaction. The resultant adsorbent should possess high antibacterial activity and adsorption selectivity for Hg(II), owing to the introduction of −NH2 and C=S. 5



Work presented here was to (1) fabricate TSC-PGMA-MACS microspheres as dual-purpose adsorbent; (2) characterize this adsorbent using Fourier transform infrared (FTIR) spectroscopy, X-ray diffraction (XRD) crystallography, elemental analysis (EA), energy dispersive X-ray (EDX) spectroscopy, differential scanning calorimetry (DSC), thermogravimetric and differential thermogravimetric (DG & DTG) analyses, scanning electron microscopy (SEM) and Brunauer-Emmett-Teller (BET) method; (3) investigate effects of pH, contact time, concentrations and temperatures on Hg(II) adsorption; (4) ascertain adsorption features via kinetic, isotherm and thermodynamic parameters; (5) verify adsorption selectivity for Hg(II) in binary-metal solutions; (6) determine the reusability of the adsorbent via five cycles; (7) gauge antibacterial activity of the adsorbent before and after adsorption; and (8) reveal the possible adsorption and antibacterial mechanisms.

2. MATERIALS AND METHODS 2.1. Preparation of MACS Microspheres. Information on materials and chemicals used in this work can be seen in Text S1. Specifically, CS powders (0.25 g) were dissolved in 12.5 mL acetic acid solution (2%, v/v) at 35 °C under ultrasonic vibrations (53 kHz) until transparent solution (solution A) was obtained. Solution B was prepared via dispersing MA (0.20 g), DMAP (0.18 g) and EDC (0.18 g) into DW (2 mL), magnetically stirring for 1 h, and adjusting pH to 5.0 with HCl or NaOH solution (0.1 M). Afterward, solution A was dropwise added into the dispersion medium composed of span-80 (2 drops) and liquid paraffin (40 mL) under 650 rpm of stirring for 1 h, and the water/oil emulsion was denoted by solution C. Solution B was slowly dropped into solution C by a sterile syringe under 650 rpm of stirring for 3 h at 60 °C. Finally, MACS microspheres were collected, rinsed three times with ethanol and DW, dehydrated by a graded ethanol series (70, 85 and 6


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99.5%, v/v) for 24 h, and dried in a vacuum desiccator. 2.2. Fabrication of TSC-PGMA-MACS Microspheres. Based on MACS microspheres, TSC-PGMA-MACS microspheres were fabricated, as shown in Scheme 1. The fabrication procedure included two steps: preparation of PGMA-MACS microspheres and fabrication of TSC-PGMA-MACS microspheres.

Scheme 1. Schematic Illustration of Major Chemical Reactions Involved in the Preparation Process of TSC-PGMA-MACS

Microspheres.

(TSC-PGMA-MACS,

TSC

grafted

PGMA-MACS;

TSC,

thiosemicarbazide; PGMA-MACS, PGMA grafted MACS; PGMA, poly(glycidyl methacrylate); MACS, MA grafted CS; MA, malic acid; CS, chitosan. EDC, 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide hydrochloride; DMAP, 4-dimethylaminopyridine; KSP, potassium persulfate.) 7



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GMA was grafted onto −NH2 on MACS microsphere surfaces by free radical polymerization. In brief, MACS microspheres (2.0 g), KPS (0.18 g), FeSO4·7H2O (0.056 g) and DW (100 mL) were in turn added into a 3-necked flask, and the mixture was magnetically stirred and heated to 60 °C under N2 protection. Then, GMA (5 mL) was dropwise added into the flask under magnetic stirring. After 2 h of stirring, the microspheres grafted were separated and rinsed five times with ethanol and DW. Finally, PGMA-MACS microspheres were dried to constant weight in an oven at 60 °C. TSC was grafted onto epoxy groups on PGMA-MACS microsphere surfaces by ring-opening reaction. Briefly, PGMA-MACS microspheres (1.5 g) were transferred into a 3-necked flask containing TSC (3.5 g) and DW (100 mL). Subsequently, the mixture was stirred at 80 °C for 16 h under N2 surroundings. Resultant TSC-PGMA-MACS microspheres were collected, washed five times with ethanol and DW, and dried in an oven at 60 °C. Information about the characterization of materials involved in this work can be seen in Text S2. 2.3. Batch Adsorption Experiments. All the adsorption tests were conducted in triplicate in a thermostatic shaker at 160 rpm. After adsorption, the adsorbent was separated from the suspension through a 0.45 μm syringe filter, and rinsed three times with DW. The residual Hg(II) concentration in filtrate was measured by an atomic absorption spectrophotometer (AA-6880F/AAC, Shimadzu Corp., Japan). Adsorption capacity and removal percentage for Hg(II) were calculated by using Eq. (1) and (2). 𝑞= 𝑟=

(𝐶0 - 𝐶𝑒)𝑉

(1)

𝑚 𝐶0 - 𝐶𝑒 𝐶0

(2)

× 100%

where q (mg g−1) is adsorption capacity, C0 and Ce (mg L−1) are initial and final concentrations of 8


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Hg(II) in solutions, m (g) is the mass of the adsorbent, and V (L) is the volume of Hg(II) solution. 2.3.1. Effect of pH. TSC-PGMA-MACS microspheres (25 mg) were added into a conical flask containing 25 mL Hg(II) solution (250 mg L−1) and then, the mixture was adjusted to a predefined pH with NaOH or HCl solution (0.1 M). Adsorption experiments were carried out in Hg(II) solutions with initial pH ranging from 2.0 to 7.0 at 298 K for 180 min. 2.3.2. Effect of Initial Concentration. Effects of concentrations (10, 20, 30, 40, 60, 80, 100, 150, 200, 300, 350, 400, and 500 mg L−1) were investigated using TSC-PGMA-MACS microspheres (25 mg) in Hg(II) solutions (25 mL, pH 6.0) at 298 K for 180 min. 2.3.3. Effect of Contact Time. Experiments on effects of contact time (5, 10, 20, 30, 60, 90, 120, 150, and 180 min) were performed using TSC-PGMA-MACS microspheres (25 mg) in Hg(II) solutions (25 mL, pH 6.0, 250 mg L−1) at 298 K. 2.3.4. Effect of Temperature. Experiments on effects of temperatures (278, 288, 298, 308, and 318 K) were conducted using TSC-PGMA-MACS microspheres (25 mg) in Hg(II) solutions (25 mL, pH 6.0, 250 mg L−1) for 180 min. 2.4. Adsorption in Binary-Metal Solution. Six binary-metal solutions (pH 6.0, 250 mg L−1 each) were prepared, which consisted of Hg(II) and Mg(II), Ca(II), Co(II), Cu(II), Pb(II) or Cd(II). Each experiment was carried out via adding TSC-PGMA-MACS microspheres (25 mg) into a conical flask containing binary-metal solution (25 mL) at 298 K for 180 min. Relative removal ratios were determined as per Eq. (3). 𝑞𝑒

(3)

𝑅 = 𝑞𝑠 × 100%

where qe (mg g−1) is the adsorption capacity at equilibrium in binary-metal solution, and qs (mg g−1) is the adsorption capacity at saturation in single-metal solution. 2.5. Desorption and Regeneration. The reusability of the absorbent was evaluated via five 9



adsorption-desorption cycles. EDTA solution (0.5 M) was chosen as desorbent. Briefly, TSC-PGMA-MACS microspheres (100 mg) were transferred into a conical flask containing 100 mL Hg(II) solution (pH 6.0, 250 mg L−1) and subsequently, the mixture was stirred at 298 K for 180 min. After adsorption, the adsorbent was separated from the suspension through a 0.45 μm syringe filter, and rinsed three times with DW. The residual Hg(II) concentration in filtrate was determined. The collected absorbent was desorbed in EDTA solution under magnetic stirring for 12 h. After desorption, the adsorbent was repeatedly rinsed with DW until no Hg(II) was detected in filtrate. The collected absorbent was further used in the next adsorption cycle. Each experiment was conducted in triplicate. 2.6. Antibacterial Experiments. Antibacterial experiments were performed in triplicate. The minimum inhibitory concentrations (MICs) of samples against E. coli and S. aureus were determined by a turbidimetric method. Briefly, a single colony was seeded in sterile nutrient broth (50 mL) and cultured overnight in an incubator shaker (110 rpm) at 37 °C, and the bacterial suspension was diluted with sterile nutrient broth to 1 × 105 CFU mL−1. Two tested samples were sterilized at 121 °C for 30 min (no physico-chemical alterations found) and then, a series of suspensions with various concentrations of TSC-PGMA-MACS microspheres (4, 2, 1, 0.5, 0.25, 0.125, 0.063, and 0 mg mL−1) and TSC-PGMA-MACS-Hg(II) microspheres (2, 1, 0.5, 0.25, 0.125, 0.063, 0.031, and 0 mg mL−1) were prepared via adding samples into conical flasks containing bacterial suspensions (5 mL each) at pH 6.0. After incubation at 37 °C for 24 h, the suspensions were ultrasonically detached (40 kHz, 160 W) for 2 min and filtered via 3 μm membrane filters (Millipore, Bedford, USA) for obtaining bacterial suspensions without samples (i.e., sample-free bacterial suspensions). Subsequently, each bacterial suspension (200 μL) was immediately transferred into a 96-well plate to record absorbance at 600 nm on a microplate reader (Bio-Red Model 550, Hercules, USA). Also, the MICs of the samples were determined by 10


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a colony forming unit assay, as described below. Similarly, TSC-PGMA-MACS microsphere, TSC-PGMA-MACS-Hg(II) microsphere, CS powder (1 mg mL−1 each), and Hg(II)-containing (56.3 and 250 mg L−1) bacterial suspensions were prepared. The inhibitory rates of samples against E. coli and S. aureus were determined using the same method as described above (but stirring speed of 160 rpm was used). The bacterial suspension (5 mL) without any sample was used as control, which was also ultrasonically treated and filtered through a 3 μm membrane filter. The inhibitory rate (IR) was calculated according to Eq. (4).

(

𝐴𝑒𝑥𝑝

)

(4)

𝐼𝑅 = 1 - 𝐴𝑐𝑡𝑟𝑙 × 100% where Aexp and Actrl represent the absorbance of experimental and control groups.

Additionally, we used colony forming unit assay to evaluate the antibacterial activity of samples against E. coli and S. aureus, as described previously,27 with slight changes. The suspensions of bacteria grown to the logarithmic phase were diluted with sterile nutrient broth to 10 CFU mL−1. Then the suspensions with the same concentration (1 mg mL−1) of CS powders, TSC-PGMA-MACS and TSC-PGMA-MACS-Hg(II) microspheres were prepared via adding samples into conical flasks containing diluted bacterial suspensions (3 μL each) and sterile nutrient broth (5 mL each) at pH 6. Simultaneously, the diluted bacterial suspensions (3 μL each) were added to conical flasks containing sterile nutrient broth (5 mL each) without or with 53.6 or 250 mg L−1 Hg(II). Afterward, the conical flasks were incubated in an incubator shaker (110 rpm) at 37 °C for 6 h, and each culture (2.5 μL) was spread on an LB agar plate and incubated for 24 h. Finally, the count of bacterial colonies on plates was obtained to compare antibacterial activity.

11



Figure 1. (A) FTIR spectra of CS powders, MACS, PGMA-MACS and TSC-PGMA-MACS microspheres. (B) XRD patterns of CS powders, MACS and TSC-PGMA-MACS microspheres, and the DSC curve of TSC-PGMA-MACS microspheres (inset). TG and DTG curves of (C) CS powders and (D) TSC-PGMA-MACS microspheres.

3. RESULTS AND DISCUSSION 3.1. Characterization of Materials. 3.1.1. FTIR Analysis. FTIR spectra of materials are illustrated in Figure 1A. The characteristic absorption bands of CS included: 3400–3460 (O−H stretching vibration), 2925 and 2862 (asymmetric and symmetric C−H stretching vibrations), 1655 (amide I), 1593 (−NH2 bending vibration), 1419 (−CH2 bending vibration), 1375 (C−H bending vibration), 1069 (C−O stretching vibration on C3−OH), and 1030 cm−1 (C−O stretching vibration on C6−OH).11,28 In MACS microsphere spectrum, compared with CS spectrum, the band at 1030 cm−1 disappeared almost 12


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completely, the intensity of bands at 1069 and 3400–3460 cm−1 decreased, and a new band appeared at 1720 cm−1 (O−C=O bending vibration), implying that C6−OH and partial C3−OH participated in esterification reaction. Moreover, the new band at 1576 cm−1 was attributed to the overlap of asymmetric stretching vibrations of COO− and −NH2, and another new band at 1387 cm−1 corresponded to the carbonyl symmetric stretching vibration, showing the presence of free −COOH in the product after esterification.29,30 The shifts of signals probably arose from the increase in structural disorder after cross-linking using MA as cross-linker, which was also proved by XRD analysis. In PGMA-MACS microsphere spectrum, bands at 1732 and 1265–757 cm−1 were assigned to an overlap of the stretching vibrations of C=O in both GMA and MACS moieties, and to asymmetric C−O−C and symmetric epoxide ring stretching vibrations.31,32 The band at 3034 cm−1 was due to C−H stretching vibration on epoxide rings.31 Besides, other bands in the range of 2900–3000 cm−1 (C−H stretching vibrations) significantly increased in intensity, and no −C=C− band (1550 cm−1) was present.33 These findings implied that GMA was grafted onto MACS microspheres in the form of polymerization. More importantly, the band at 1576 cm−1 disappeared almost completely, but a new band at 1637 cm−1 appeared, which might be attributed to the asymmetric stretching vibration of C=O on −COOH.30 Based on these findings, it could be concluded that −C=C− on GMA moieties was opened, and −NH2 on CS was involved in free-radical polymerization. In TSC-PGMA-MACS spectrum, several bands between 1265 and 757 cm−1 decreased in intensity even disappeared. Moreover, new bands and their assignments were v(C=S) band at 649 cm−1, v(N−H and −NH2) bands at 1575 and 3334 cm−1, and v(−OH on GMA) band at 3477 cm−1.32,34,35 These changes confirmed the occurrence of the ring-opening reaction of epoxide ring with TSC. Overall, it was concluded that TSC-PGMA-MACS microspheres were successfully fabricated. 13



Figure 2. (A) Elemental analysis results of CS powders, MACS and TSC-PGMA-MACS microspheres. EDX spectra of (B) MACS and (C) TSC-PGMA-MACS microspheres.

3.1.2. Elemental Analysis and EDX Spectra. EA and EDX techniques were employed to determine the presence and changes of elemental composition in materials. As shown in Figure 2A, the N content in MACS microspheres was lower than that in CS powders, mainly ascribed to an increase in C and O atoms derived from MA. In comparison with MACS microspheres, TSC-PGMA-MACS microspheres had a new element S and slightly higher N content (6.02%), which was attributed to the introduction of TSC onto PGMA-MACS microspheres. It could be noticed that, however, the C/N ratio in TSC-PGMA-MACS microspheres was higher than that in MACS microspheres, due to the graft of PGMA that contains plentiful C and O atoms. Besides, the S content (14.26%) indicated that the three-step modifications resulted in a product with TSC content of 40.73%. Taken together, the synthesis of TSC-PGMA-MACS microspheres was 14


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further validated by EA results. EDX analysis, a convenient and semi-quantitative method for surface-rough samples, was here used to further confirm the results of EA. In comparison to EDX spectra of MACS microspheres (Figure 2B), TSC-PGMA-MACS microsphere spectra (Figure 2C) displayed 14.53% of S, in good agreement with the results of EA. In general, EA and EDX results further manifested that TSC-PGMA-MACS microspheres were successfully fabricated. 3.1.3. XRD Spectra and DSC Analysis. XRD patterns in the range of 5–60° (2θ) are presented in Figure 1B. Typical fingerprints at 10 and 21° were attributed to stereoregularity of molecular chains and inter- and/or intra-molecular hydrogen bonds in semi-crystalline CS, and its crystallinity calculated was 19.7%. Notably, for MACS microspheres, two new diffraction peaks at 8.5 and 12° appeared, the peak at 10° was weakened, whereas the peak at 21° shifted to 17.4° and became tapered. These changes might be owing to the introduction of MA, causing the destruction and rearrangement of inherent hydrogen bonds, and also supporting the occurrence of esterification between −COOH on MA and −OH on CS.36 Moreover, the reduction in crystallinity (12.63%) after esterification could be interpreted as an outcome of the introduction of MA that substantially hindered the formation and ordering of crystalline phases and influenced the regularity of static packing of CS chains. Surprisingly, TSC-PGMA-MACS microspheres, with crystallinity of 2.44%, had only one broad diffraction peak. Such results indicated that TSC-PGMA-MACS microspheres had a loose crystalline structure with more amorphous phases, due to the successive graft of GMA and TSC that made the structural order significantly changed.37 The increase in amorphous phases is generally conducive to contact between internal adsorption sites and HMIs.36 A DSC test was performed to further probe the crystalline structure of TSC-PGMA-MACS microspheres. Previous studies show that a sharp exothermic peak at ~ 315 ºC is present in the DSC curve of CS, due to the decomposition of saccharine structures.38–40 As shown in Figure 1B 15



(inset), TSC-PGMA-MACS microspheres exhibited two exothermic peaks at 313 and 415 ºC, corresponding to thermal decomposition at the 2nd and 3rd stages in TG and DTG curves. Such findings confirmed that successive chemical modifications to CS influenced its degree of structural order, fully supporting XRD results about changes of crystalline structures. 3.1.4. TG & DTG Analyses. TG and DTG analyses were employed to evaluate the thermostability of materials in the temperature range of 50–800 ºC. Figure 1C showed CS having two decomposition stages: one had weight loss of 10.0% at the temperature ranging from 50 to 150 ºC, arising from the evaporation of moisture; another (52.5%) was from 200 to 500 ºC, which was ascribed to the thermal degradation of CS skeleton.9,11 Most strikingly, three decomposition stages were observed in TSC-PGMA-MACS microsphere profiles (Figure 1D). At the first stage, 3.0% of weight loss was due to moisture and volatile impurity removal. At the second stage, 37.4% of weight loss, corresponding to 40.7% of TSC as described in EA, was attributed to the decomposition of TSC moieties.41,42 At the last stage, 21.0% of weight loss was involved with the degradation of CS side chains and backbone.40 As shown in Table S1, TSC-PGMA-MACS microspheres had a lower onset temperature (185 ºC) at the second stage than CS powders (200 ºC), and its DTG curve revealed that the maximum decomposition took place at 293 ºC, lower than that of CS powders (313 ºC). Besides, TSC-PGMA-MACS microspheres had less residuals (26.5%) than CS powders (33.4%) at 600 ºC. These findings indicated that the thermostability of TSC-PGMA-MACS microspheres was slightly compromised, as compared with that of CS, due to the graft copolymerization and ring-opening reaction that damaged the orderly crystalline structure and morphology, agreeing with XRD and DSC analyses.

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Figure 3. Nitrogen adsorption-desorption isotherms of (A) MACS and (B) TSC-PGMA-MACS microspheres. BJH-adsorption pore size distribution curves of (C) MACS and (D) TSC-PGMA-MACS microspheres.

3.1.5. BET Measurement. Figure 3 illustrates N2 adsorption-desorption isotherms and pore size distribution curves. Two physisorption isotherms, in the judgment on the occurrence of hysteresis loops and convex upward trends at low P/P0, should be typical IV characteristics as per IUPAC classification, indicating that both microspheres belonged to mesoporous materials.28 Adsorption processes could be divided into monolayer adsorption that reached saturation at point B, multilayer adsorption and capillary agglomeration. Besides, both isotherms presented H1-typed hysteresis loops with two adsorption and desorption branches at a broad P/P0 range of 0.45–0.98. These findings manifested the relatively narrow pore size distribution of both microspheres, as well as the existence of cylinder-shaped pores with homogeneous size and regular shape. As shown in Table S2, TSC-PGMA-MACS microspheres possessed larger specific surface area than 17



MACS microspheres, capable of enhancing mass transfer performance and adsorption capacity for HMIs. The mean pore size (7.93 nm) was similar to that of MACS microspheres (7.94 nm), whereas the cumulative pore volume was larger, resulting in the increased specific surface area that was closely relevant to the grafting reactions on MACS microsphere surfaces. 3.1.6. Surface Morphology. SEM images of samples are shown in Figure 4, by which the surface morphology and microstructure of each sample were portrayed. An optical microscope was also used for statistically determining the diameters of microspheres (Figure S1). As expected, each detected sample was spherical or nearly spherical, facilitating the separation and reuse of the sample during applications. According to statistical results (Table S3), the mean, maximum and minimum diameters of TSC-PGMA-MACS microspheres were 33.59, 49.19 and 23.03 μm, respectively. Microscopically, SEM images at low magnification (Figure 4A, B and C) exhibited more smooth and homogeneous surfaces than those at high magnifications (Figure 4D, E and F). Compared with MACS microspheres, TSC-PGMA-MACS microspheres displayed coarse surfaces with protuberances and valleys (Figure 4E). These changes were substantially in connection with the graft of PGMA and the ring-opening reaction, resulting in exposure of hydrophilic moieties and/or collapse of pores on microsphere surfaces.43,44 Such outcomes also agreed well with BET results, as well as with the evolution of crystalline order from XRD determinations. More importantly, plicate and porous surfaces that increased the adsorption sites were beneficial to the coordination between functional groups and HMIs. After adsorption, TSC-PGMA-MACS-Hg(II) microsphere surfaces (Figure 4F) seemed to be more flattened than those of TSC-PGMA-MACS microspheres, due to the formation of polymer-Hg(II) complexes, covering the surfaces. However, tortoiseshell surfaces were still identified, implying that the new adsorbent had good mechanical strength and acid-insoluble stability, which was also supported by the mean diameter (33.67 μm), without apparent changes in size (Table S3). 18


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Figure 4. SEM images of MACS, TSC-PGMA-MACS and TSC-PGMA-MACS-Hg(II) microspheres. (A and D: MACS microspheres; B and E: TSC-PGMA-MACS microspheres; C and F: TSC-PGMA-MACS microspheres after five-time adsorption toward Hg(II). TSC-PGMA-MACS-Hg(II) microspheres are representative of the TSC-PGMA-MACS microspheres after Hg(II) adsorption.)

3.2. Batch Adsorption Experiments. 3.2.1. Effect of pH. Initial pH is one of the crucial factors to affect removal efficiency for Hg(II) by influencing the surface charge of adsorbents and Hg(II) speciation in solutions. Figure 5A showed that adsorption capacity for Hg(II) had an uptrend with pH increasing from 2.0 to 6.0. The reason why a low removal percentage appeared at low pH might be because Hg(II) was in competition with H+ and/or H3O+ for binding sites, whereas ion exchange between HgCl3− and −NH3+ occurred in the presence of abundant H+.12 With H+ decreasing, adsorption capacity gradually increased, indicating that the adsorption here had a preference for other complicated adsorption modes except ion exchange. A convincing explanation was that thione groups (C=S) on TSC were converted into thiol groups (C−SH) in acidic media, which had selective and 19



specific capability of binding Hg(II) to generate stable metal chelate-complex (S−Hg−S) via the deprotonation of thiol groups (Scheme S1).17 Moreover, the number of −NH3+ was lower, favorable for chelation with Hg(II), and the number of COO− became larger, resulting in the stronger electrostatic attraction between COO− and Hg(II). Besides, both adsorption capacity and removal percentage at pH 7.0 slightly decreased as compared with those at pH 6.0 (no significant differences, p > 0.05), likely due to the formation of hydroxides, such as soluble Hg(OH)+ and colloidal precipitate Hg(OH)2, to restrain complex formation. Altogether, Hg(II) adsorption on TSC-PGMA-MACS microspheres greatly depended on pH within the experimental pH values, and pH 6.0 was chosen as the optimal pH for Hg(II) adsorption in the following tests.

Figure 5. Effects of (A) pH, (B) contact time, (C) initial concentrations and (D) temperatures on Hg(II) adsorption on TSC-PGMA-MACS microspheres. (Dosage 1 g L−1, stirring speed 160 rpm. A: initial concentration 250 mg L−1, contact time 180 min, temperature 298 K; B: initial concentration 250 mg L−1, pH 20


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6.0, temperature 298 K; C: pH 6.0, contact time 180 min, temperature 298 K; D: initial concentration 250 mg L−1, contact time 180 min, pH 6.0.)

3.2.2. Effect of Contact Time and Adsorption Kinetics. Figure 5B displays the effects of contact time. Clearly, both adsorption capacity and removal percentage curves had a similar curvilinear trend over time. Within incipiently 10 min, adsorption amount quickly reached 141 mg g−1, more than half of the saturated adsorption capacity. Then, accumulative adsorption amount increased to 205 mg g−1 at 90 min, and the removal percentage was 88%. These results were mainly because numerous available adsorption sites and high ion-concentration gradient at liquid-solid interface, which drove TSC-PGMA-MACS microspheres to combine with Hg(II) easily. Subsequently, adsorption amount and removal percentage increased slowly and gradually tended to plateaus, which might be caused by the following reasons: with the increase in contact time, (1) the adsorption sites on microsphere surfaces were largely occupied, (2) the driving force for mass transfer in solutions was continuously weakened, and (3) the void resistance to adsorption constantly increased. In addition, adsorption behavior was also related to adsorption reactions of soft bases (e.g., −OH and −NH2) with Hg(II), as well as to the migration and diffusion of Hg(II) to pores or channels in TSC-PGMA-MACS microsphere matrixes. To explore potential rate-limiting steps during Hg(II) adsorption, including external film diffusion, intra-particle diffusion and chemisorption,17 we selected several adsorption kinetic models to fit the experimental data. Pseudo-first-order and pseudo-second-order kinetic models are expressed as Eq. (5) and (6). 𝑙𝑛 (𝑞𝑒1 - 𝑞𝑡) = 𝑙𝑛𝑞𝑒1 - 𝑘1𝑡 𝑡 𝑞𝑡

1

(5)

𝑡

(6)

= 𝑘 𝑞2 + 𝑞𝑒2 2 𝑒2

where qt (mg g−1) is adsorption capacity at contact time t (min), qe1 and qe2 (mg g−1) are 21



adsorption capacity at equilibrium, and k1 (min−1) and k2 (g mg−1 min−1) are equilibrium rate constants of pseudo-first-order and pseudo-second-order kinetic models. Kinetic parameters from linear fitting (Figure S2A and B) are listed in Table 1. Clearly, adsorption capacity (qe2cal) for Hg(II) calculated from pseudo-second-order model was closer to the experimental datum (qeexp), compared with that (qe1cal) from pseudo-first-order model. Moreover, the adsorption toward Hg(II) was better consistent with pseudo-second-order model, because of R22 > R12. Therefore, the rate-limiting step during Hg(II) adsorption on TSC-PGMA-MACS microspheres was chemisorption via chelation and/or electrostatic interaction(s). Table 1. Kinetic Model Parameters of TSC-PGMA-MACS Microspheres for Hg(II) Adsorption. Kinetic model

Pseudo-first-order

Pseudo-second-order

Intraparticle diffusion

Parameter qeexp (mg g−1)

225.1

qe1cal (mg g−1)

111.1

k1 (min−1)

0.029

R12

0.9562

qe2cal (mg g−1)

234.7

k2 (g mg−1 min−1)

5.4 × 10−4

R22

0.9995

Kid1 (mg g−1 min−1/2)

22.4


12.1


0.8

C1 (mg g−1)

28.7

C2 (mg g−1)

108.1

C3 (mg g−1)

212.8 22


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To further clarify the adsorption behavior, Weber and Morris intra-particle diffusion model was employed to deal with the experimental data, and this model is given as Eq. (7). 𝑞𝑡 = 𝐾𝑖𝑑𝑡1/2 + 𝐶

(7)

where Kid (mg g−1 min−1/2) is the rate constant of intra-particle diffusion, and C is the intercept of the linear fitting plot. Three linear segments were present in linear fitting plot (Figure S2C), suggesting that more than one stage influenced the adsorption process. However, Kid1 > Kid2 > Kid3 and C ≠ 0 (Table 1) demonstrated that intra-particle diffusion was not a rate-limiting step for this adsorption. In summary, all data drew a logical conclusion that the crucial rate-limiting step was chemisorption rather than intra-particle diffusion. Table 2. Isotherm Model Parameters of TSC-PGMA-MACS Microspheres for Hg(II) Adsorption at 25 °C. Isotherm model

Langmuir

Freundlich

Parameter qeexp (mg g−1)

225.1

Qm (mg g−1)

242.7

KL (L mg−1)

6.71 × 10−2

RL2

0.9970

KF (mg1−1/n L1/n g−1)

24.714

n

2.180

RF2

0.9404

3.2.3. Effect of Initial Concentration and Adsorption Isotherm. Figure 5C depicts the effects of initial Hg(II) concentrations on adsorption toward Hg(II) at 298 K. As initial Hg(II) concentrations increased, the adsorption capacity for Hg(II) gradually increased until the saturated adsorption appeared, mainly owing to the enhanced driving force for mass transfer at high initial Hg(II) concentrations. During the adsorption process, hydroxyl, amino, carboxyl and thione groups on TSC-PGMA-MACS microspheres might be responsible for Hg(II) adsorption, 23



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besides, the thiourea group on TSC with two tautomeric forms, which can form bidentate and/or quadridentate ligand(s) to coordinate with Hg(II),37,45 should be an active participant in the adsorption process. Likely, high Hg(II) concentrations cause a high affinity between adsorption sites and absorbates. In addition, the removal percentage decreased with the increase in Hg(II) concentrations, because of a lack of adsorption sites on microspheres. We here used Langmuir and Freundlich isotherm models, which are often applied to homogeneous monolayer, heterogeneous multilayer and reversible adsorption, to deal with the adsorption data. Two isotherm models are expressed as Eq. (8) and (9). 𝑄𝑚𝐾𝐿𝐶𝑒

𝑄𝑒 = 1 + 𝐾𝐿𝐶𝑒

(8)

𝑄𝑒 = 𝐾𝐹𝐶1/𝑛 𝑒

(9)

where Qe (mg g−1) and Ce (mg L−1) are adsorption capacity and the concentration of Hg(II) at adsorption equilibrium, Qm (mg g−1) is the maximum adsorption capacity, KL (L mg−1) is an equilibrium constant for Langmuir model associated with the affinity of adsorption sites and the binding energy of adsorption, and KF (mg1−1/n L1/n g−1) and n are Freundlich constants related to adsorption capacity and intensity, respectively. Relative isotherm parameters from linear fitting (Figure S3A and B) are summarized in Table 2. Obviously, RL2 was more near to 1 than RF2, and the maximum adsorption capacity (242.7 mg g−1) calculated from Langmuir isotherm model was much close to qeexp. Accordingly, Langmuir isotherm model well interpreted the adsorption toward Hg(II) on TSC-PGMA-MACS microspheres. However, Hg(II) adsorption was also considered an energetically heterogeneous and favorable process according with Freundlich isotherm model, since the heterogeneity factor 1/n associated with the favorability of adsorption was smaller than 1.0. Therefore, both monolayer and multilayer adsorption should coexist in the Hg(II) adsorption process, whereas monolayer adsorption was more dominant during this 24


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process. Figure 5C also depicts the nonlinear regression for Langmuir and Freundlich isotherms, further illustrating that Langmuir model was fitted better with the experimental data than Freundlich model, because the correlation coefficient for the former (0.9921) was larger than that for the latter (0.9864). To study the affinity between Hg(II) and microspheres, we calculated RLa closely related to Langmuir model. All RLa values (Table S4) were within 0–1, indicating that the adsorption process was favorable. Altogether, all results suggested that the adsorption toward Hg(II) on TSC-PGMA-MACS microspheres was monolayer adsorption, with finite identical adsorption sites. Table 3. Thermodynamic Parameters of Adsorption toward Hg(II) on TSC-PGMA-MACS Microspheres. Thermodynamic parameter a Temperature (K) ΔS (J mol−1 K−1)

ΔG (kJ mol−1)

278

−0.83

288

−1.48

298

a

ΔH (kJ mol−1)

64.82

17.19

−2.13

308

−2.77

318

−3.42

ΔS, the change in entropy; ΔH, the change in enthalpy; ΔG, the change in Gibbs free energy.

3.2.4. Effect of Temperature and Thermodynamic Analysis. Figure 5D shows the effects of temperatures on adsorption toward Hg(II). Both adsorption capacity and removal percentage increased with the increase of temperature, indicating that the increase in temperature promoted Hg(II) adsorption. Thermodynamic parameters, changes in Gibbs free energy (ΔG), enthalpy (ΔH) and entropy (ΔS), were calculated according to Eq. (10), (11) and (12). 𝑄𝑒

(10)

𝐾𝑣 = 𝐶𝑒

25



𝑙𝑛𝐾𝑣 =

∆𝑆 𝑅

∆𝐻

Page 26 of 43

(11)

- 𝑅𝑇

(12)

∆𝐺 = ∆𝐻 - 𝑇∆𝑆

where Kv (L g−1) is the equilibrium adsorption constant obtained from Langmuir isotherm, R (8.314 J mol−1 K−1) is an ideal gas constant, T (K) is absolute temperature, ΔH (kJ mol−1) and ΔS (J mol−1 K−1) denote the changes in enthalpy and entropy obtained from Figure S3C, and ΔG (kJ mol−1) is the change in Gibbs free energy. As presented in Table 3, positive ΔS implied the increase in randomness and disorder at the solid-solute interface during Hg(II) adsorption, further indicating that Hg(II) adsorption was an entropy-driven process. Positive ΔH showed that Hg(II) adsorption was endothermic in nature, consistent with the fact that the removal percentage of Hg(II) increased with the increase of temperature.9 Moreover, the negative values of ΔG at different temperatures implied the spontaneous nature and feasibility of Hg(II) adsorption. Overall, the adsorption toward Hg(II) on TSC-PGMA-MACS microspheres was an endothermic and spontaneous process. 3.3. Selective Adsorption in Binary-Metal Solution. It is meaningful to determine whether TSC-PGMA-MACS microspheres are of selective adsorption toward Hg(II) in binary-metal solutions, since more than one metal ion, in most cases, coexists in real polluted water. We here chose Mg(II), Ca(II), Co(II), Cu(II), Pb(II) or Cd(II) as a coexisting metal ion to prepare six binary-metal solutions. Effects of coexisting metal ions on the maximum adsorption capacity for Hg(II) are displayed in Figure 6A. Though all the relative removal ratios revealed that the divalent metal ions tested had no significant effects on adsorption toward Hg(II), there were slight changes as a result of competitive adsorption. Weak even negligible competition existed between Hg(II) and Mg(II) or Ca(II), and the relative removal ratio for Hg(II) was circa 100% in Hg(II)+Mg(II) or Hg(II)+Ca(II) solution. Such a result can be well explained by HSAB theory, 26


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namely, major functional groups like thiol (soft base) on TSC-PGMA-MACS microspheres in acidic surroundings are preferentially combined with Hg(II) (soft acid), rather than Mg(II) and Ca(II) (hard acids), in binary-metal solutions. As for other metal ions, the order of effects on Hg(II) removal was Pb(II) > Cu(II) > Cd(II) > Co(II). These outcomes mainly originated from three aspects: (1) theoretically, the influence of soft-acid Cd(II) on Hg(II) adsorption should be stronger than Pb(II), Cu(II) and Co(II) that belong to hard-medial-soft acids, but the metal ions like Pb(II) with larger size are more accessible to adsorption sites on the surfaces of TSC-PGMA-MACS microspheres;12,42 (2) Pb(II) and Cu(II) have stronger affinity for −NH2 on microspheres as compared with Cd(II);36 (3) it is well-illustrated that polymers with S and N atoms can readily bind Hg(II) via strong covalent bonds.16 Based on the analyses above, it was concluded that TSC-PGMA-MACS microspheres had a strong ability to selectively adsorb Hg(II) in binary-metal solutions.

27



Figure 6. (A) Effects of coexisting metal ions on Hg(II) adsorption in binary-metal solutions. (B) Adsorption and desorption toward Hg(II) on TSC-PGMA-MACS microspheres within five-time consecutive cycles. (C) FTIR spectra and (D) XRD patterns of TSC-PGMA-MACS microspheres before and after Hg(II) adsorption. (Initial concentration of each metal ion 250 mg L−1, contact time 180 min, pH 6.0, temperature 298 K, dosage 1 g L−1, stirring speed 160 rpm.)

3.4. Desorption and Reusability. Reusability is one of the crucial factors for evaluating whether an adsorbent has the actual application value. EDTA solution (0.5 M) was here chosen as desorbent used for eluting Hg(II) adsorbed onto TSC-PGMA-MACS microspheres. Figure 6B showed that there was a decreasing tendency for Hg(II) removal with the increase in reuse times, mainly related to the mass loss during adsorption and desorption, as well as to the loss of adsorption sites due to the strong affinity between Hg(II) and functional groups. However, the relative removal ratios within five-time consecutive cycles were 98.2, 94.5, 93.2, 88.3, and 28


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86.0%, indicating a good reusability. Additionally, Table S5 provides the comparison of the maximum adsorption capacity of TSC-PGMA-MACS microspheres for Hg(II) with adsorbents reported in journals. Obviously, TSC-PGMA-MACS microspheres presented 242.7 mg g−1 of maximum adsorption capacity, higher than most of the adsorbents reported previously. 3.5. Possible Adsorption Mechanism. To well understand the adsorption behavior toward Hg(II) on TSC-PGMA-MACS microspheres, and to find out as much information as possible about potential adsorption sites and bonding modes, FTIR spectra and XRD patterns before and after Hg(II) adsorption were recorded, as displayed in Figure 6C and D. As shown in Figure 6C, some characteristic absorption bands of TSC-PGMA-MACS-Hg(II) microspheres, compared with TSC-PGMA-MACS microsphere spectrum, were significantly changed in intensity and/or in position. Bands at 3477 (−OH) and 3334 cm−1 (−NH2) became weaker in intensity and were combined into a single broad band at 3446 cm−1, and the band at 1063 cm−1 (C−O on C3−OH ) shifted to 1055 cm−1, because O and N atoms donated their lone pair electrons to Hg(II), weakening or changing the vibration intensity of −OH and −NH2. Strong vibrations at 1732 (C=O) and 1387 cm−1 (COO−) were largely weakened and shifted to 1722 and 1384 cm−1, indicating the interaction of −COOH with Hg(II).11 Primary characteristic bands at 1575 (N−H) and 649 (C=S) cm−1 almost completely disappeared after Hg(II) adsorption, and a new band appeared at 1635 cm−1, demonstrating that N and S atoms on TSC moieties participated in the formation of Hg(II) complexes.16 FTIR analyses above were well supported by some literature, e.g., Li et al. report that the band at ~ 3437 cm−1 identified as −OH and −NH2 shifts to 3450 cm−1, after interactions between −OH or −NH2 and HMIs;36 and Chauhan et al. find that N−H vibrations at 1607 and 1557 cm−1 move to 1640 and 1547 cm−1 after the complex generation between sensing material and Hg(II).16 As shown in Figure 6D, the diffraction peak at 17.4° in TSC-PGMA-MACS-Hg(II) microsphere pattern became broader and weaker than that in 29



TSC-PGMA-MACS microsphere pattern, and the crystallinity after Hg(II) adsorption greatly decreased, indicating the possibility of reactions between adsorbent and Hg(II), which destroyed the symmetry and stereoregularity of polysaccharide molecules, leading to incomplete decrystallization. Similar findings are also reported by other researchers, e.g., Zhang and Kyzas find that crystallinity significantly compromises after HMI adsorption.28,46 More importantly, as documented in previous studies,2,12,15,16,17 high selectivity and affinity of TSC-PGMA-MACS microspheres with Hg(II) might be mainly owing to strong interactions between S- or N-containing ligands and Hg(II), which have been proved by phenylthiourea, thiocarbamoyl and thiourea modified adsorbents.2,12,17

Figure 7. Probable bonding modes and adsorption sites for Hg(II) on TSC-PGMA-MACS microspheres.

Based on FTIR and XRD analyses, it was reasonable to conclude that −OH, −COOH, −NH2 and C=S groups on TSC-PGMA-MACS microsphere surfaces were involved in chemical reactions during Hg(II) adsorption. Namely, S, N and O on TSC-PGMA-MACS microspheres in 30


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slightly acidic surroundings contributed lone pair electrons to empty orbits of Hg(II) to form complexes through coordinate covalent bonds. A series of potential adsorption sites and binding modes were here proposed, which were that Hg(II) was bonded to (1) two C=S (or S–H), (2) two –NH2 (or N–H), (3) one –NH2 and one –OH, (4) two −COOH, (5) two C3–OH, (6) two GMA–OH, (7) two O on GMA–OH and C3–OH, and (8) four S and/or N. The schematic adsorption sites and binding modes are illustrated in Figure 7. 3.6. Antibacterial Evaluation and Mechanism. Inhibitory effects of materials against Gram-negative (E. coli) and Gram-positive (S. aureus) bacteria, which are main representatives of the most common pathogenic strains associated with water contamination, were estimated by an MIC assay method. Figure 8A and B show antibacterial activity curves of TSC-PGMA-MACS and TSC-PGMA-MACS-Hg(II) microspheres in acidic media with various concentrations. Clearly, both TSC-PGMA-MACS and TSC-PGMA-MACS-Hg(II) microspheres showed a certain degree of antibacterial activity against E. coli and S. aureus, and the antibacterial activity of the former, as well as of the latter, against two tested bacteria did not show obvious differences. Most strikingly, the latter showed antimicrobial activity superior to the former, in view of much lower Abs 600 values at the same concentrations of 1.0 mg mL−1 of antiseptics. The MIC values of the former against both bacteria were all equal to 2.0 mg mL−1, whereas the counterparts of the latter were all equivalent to 0.25 mg mL−1. To confirm the reliability of the above findings, we also determined the MICs through the colony counting method, and the results (Figure S4) were consistent with the counterparts obtained via the turbidimetric method. Such a equivalent MIC of each tested sample against both E. coli and S. aureus, unlike our previous studies on water-soluble CS derivatives,22–25 might be because bacterial activity occurring on solid interfaces was dependent not only on antimicrobials’ concentration but also on contact probability and affinity between antimicrobials and bacteria in liquid media. As shown in 31



Figure 8C, the order of inhibitory rates of materials against two bacteria was TSC-PGMA-MACS-Hg(II) microspheres > TSC-PGMA-MACS microspheres > CS powders at the same concentration (1.0 mg mL−1), which was verified by Figure 8D. Moreover, Figure 8C and D revealed that both tested bacteria could not survive in nutrient broth medium containing 250 mg L−1 Hg(II) that was also the concentration used in batch adsorption experiments, indicating high toxic effects of Hg(II) on bacterial cells. Also, the inhibitory rate remained at a high level when Hg(II) concentration decreased to 56.3 mg L−1, which was equivalent to the Hg(II) concentration of 0.25 mg mL−1 of TSC-PGMA-MACS-Hg(II) microsphere suspension, implying that the higher antibacterial activity of TSC-PGMA-MACS-Hg(II) microspheres might be mainly derived from the participation of Hg(II). Undeniably, antibacterial activity was greatly compromised upon the change from free Hg(II) to Hg-complexes, which was illustrated by Figure 8B and Figure S5. More recently, researchers has proposed several possible antibacterial mechanisms for acidor water-soluble CS derivatives,22,23,25,47,48 but the most approved one is that CS derivatives bind to bacterial cytomembranes via electrostatic interactions, altering membrane permeability and further causing the death of bacteria. In the present work, newly-prepared TSC-PGMA-MACS microspheres were insoluble in neutral and acidic solutions, however, antibacterial experiments showed that TSC-PGMA-MACS microspheres were of high antibacterial activity against E. coli and S. aureus, and antibacterial activity of the microspheres after adsorption toward Hg(II) was much higher than before adsorption. As for such desirable findings, several possible explanations were summarized below: (1) coordination atoms S, N and O on TSC-PGMA-MACS microspheres readily chelated with Hg(II) to inhibit the growth of microorganisms; (2) functional groups (e.g., −NH2 and C=S) on TSC-PGMA-MACS microsphere surfaces could be protonated in acidic media, binding to negatively charged bacterial membranes via electrostatic interactions, 32


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changing cytomembrane permeability, and further resulting in the death of bacteria; (3) the introduction of TSC containing −NH2 and C=S onto PGMA-MACS microsphere surfaces not only increased the species of moieties that can be protonated in acidic solutions but also enhanced the positive charge density on microsphere surfaces, leading to stronger antibacterial activity superior to CS powders; (4) the positive charge density on microsphere surfaces after Hg(II) adsorption was higher than before, endowing TSC-PGMA-MACS-Hg(II) microspheres with higher

antibacterial

activity

superior

to

TSC-PGMA-MACS

microspheres;

(5)

TSC-PGMA-MACS-Hg(II) microspheres reacted easily with −NH2, −COOH and −SH on proteins and nucleic acids to hinder the growth of bacteria. Notably, −NH2 and C=S on TSC-PGMA-MACS microspheres might be protonated, to a lower degree, in slightly acidic media at pH 6.0, however, the acidic components produced during the growth of bacteria could promote the protonation of certain moieties, largely enhancing antibacterial activity.

33



Figure 8. MICs of (A) TSC-PGMA-MACS and (B) TSC-PGMA-MACS-Hg(II) microspheres against E. coli and S. aureus. (C) Inhibitory rates of CS powder, TSC-PGMA-MACS and TSC-PGMA-MACS-Hg(II) microsphere suspensions, and Hg(II) solutions against E. coli and S. aureus. (D) Growth of E. coli and S. aureus in LB agar plates after being treated with samples. (MICs, minimum inhibitory concentrations. Temperature 37 °C, sterile nutrient broth 5 mL, absorbent 5 mg, pH 6.0, stirring speed 160 rpm, Hg(II) solution 250 mg L−1.)

Altogether, the graft of TSC imparted high antibacterial activity to TSC-PGMA-MACS microspheres, and antibacterial activity after adsorption toward Hg(II) was greatly enhanced.

4. CONCLUSIONS Dual-purpose TSC-PGMA-MACS microspheres with adsorption selectivity for Hg(II) and antibacterial activity were first fabricated via elaborate three-step reactions for polluted water scavenging. Newly-prepared adsorbent, with 35.340 m2 g−1 of specific surface area, 7.933 nm of 34


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pore diameter, 0.158 cm3 g−1 of pore volume and abundant −NH2 and C=S groups, were characterized by FTIR, EA, XRD, EDX, DSC, TG, DTG, SEM, and BET methods, confirming successful fabrication, unambiguous crystallinity, good thermostability and well-defined mesoporous structures, beneficial for Hg(II) adsorption and anti-bacteria. Batch adsorption experiments demonstrated that the optimal pH was 6.0 and the maximum adsorption capacity for Hg(II) was 242.7 mg g−1 calculated on the basis of Langmuir isotherm model, higher than most of the available adsorbents. Kinetic studies showed that the adsorption process was well described by pseudo-second-order kinetic model, implying a monolayer and chemical adsorption process. Thermodynamic parameters revealed that Hg(II) adsorption was spontaneous and endothermic in nature. Competitive adsorption tests exhibited that TSC-PGMA-MACS microspheres had selective adsorption toward Hg(II) in binary-metal solutions. The adsorption capability after five-time cycles was maintained > 86.0% of the initial saturated adsorption capacity, showing outstanding reusability of the adsorbent. FTIR and XRD analyses confirmed that S, N and O atoms participated in coordination reactions. Besides, the order of inhibitory rates of materials against E. coli and S. aureus was TSC-PGMA-MACS-Hg(II) microspheres > TSC-PGMA-MACS microspheres > CS powders, and the MIC values of TSC-PGMA-MACS and TSC-PGMA-MACS-Hg(II) microspheres against both bacteria were 2.0 and 0.25 mg mL−1. Overall, TSC-PGMA-MACS microspheres, with high adsorption capacity, adsorption selectively, good reusability and antibacterial activity, might serve as new adsorbent for wastewater purification.

■ ASSOCIATED CONTENT Supporting Information Summary of materials and chemicals used; characterization of materials; characteristic 35



parameters during the thermal degradation; surface parameters; surface morphology; statistical microsphere diameters; adsorption modes on C=S; linear fitting plots of kinetic and isotherm models; calculated RLa values; comparison of maximum adsorption capacity; MICs of samples; inhibitory effects of Hg(II) solutions

■ AUTHOR INFORMATION Corresponding Author *Phone: +86 0532 82032586; fax: +86 0532 82032586; e-mail: [email protected]. ORCID Chengsheng Liu: 0000-0002-1454-0193 Notes The authors declare no competing financial interest.

■ ACKNOWLEDGMENTS Authors C. Liu and Q. Dang received funding from Applied Basic Research Program for Youngster of Qingdao Grant 15-9-1-42-jch, National Natural Science Foundation of China (NSFC) Grant 31400812, Natural Science Foundation of Shandong Province Grant ZR2014CQ052, and Science and Technology Development Funds of Qingdao Shinan Grant 2014-14-003-SW & 2015-5-015-ZH.

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ABSTRACT GRAPHIC

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Selective Adsorption toward Hg(II) and Inhibitory Effect on Bacterial

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