Preparation, characterization and properties of N-benzoyl-O- acetyl-chitosan

International Journal of Biological Macromolecules 77(2015)52–58

Contents lists available at ScienceDirect

International Journal of Biological

Macromolecules

j o u r n a l h o m e p a g e :w w w.e l s e v i e r.c o m /l o c a t e /i j b i o m a

c

Preparation and characterization of N -benzoyl-O -acetyl-chitosan

Jinping Cai a ,Qifeng Dang a ,?,Chengsheng Liu a ,?,Bing Fan a ,Jingquan Yan b ,Yanyan Xu a ,Jingjing Li c

a

College of Marine Life Science,Ocean University of China,5Yushan Road,266003Qingdao,PR China b

School of Medicine and Pharmacy,Ocean University of China,5Yushan Road,266003Qingdao,PR China c

College of Life Science and Bioengineering,Beijing University of Technology,Beijing 100022,PR China

a r t i c l e

i n f o

Article history:

Received 17September 2014

Received in revised form 14February 2015Accepted 1March 2015

Available online 14March 2015

Keywords:

N -benzoyl-O -acetyl-chitosan Characterization Foaming property Antimicrobial activity

a b s t r a c t

A novel amphipathic chitosan derivative,N -benzoyl-O -acetyl-chitosan (BACS),was prepared by using the selective partial acylation of chitosan (CS),benzoyl chloride,and acetic acid under high-intensity ultrasound.The chemical structure and physical properties of BACS were characterized by FTIR,1H NMR,TGA,and XRD techniques.The degrees of substitution of benzoyl and acetyl for the chitosan derivatives were 0.26and 1.15,respectively,which were calculated from the peak areas in NMR spectra by using the combined integral methods.The foaming properties of CS and BACS were determined and the results suggested BACS had better foam capacity and stability than those of chitosan.In addition,the antimi-crobial activities of CS and BACS were also investigated against two species of bacteria (Escherichia coli and Staphylococcus aureus )and a fungus (Aspergillus niger ),the results indicated that the antibacterial and antifungal activities of BACS were much stronger than those of the parent chitosan.These ?ndings suggested that BACS was preferable for use as a food additive with a dual role of both foaming agent and food preservative.

?2015Elsevier B.V.All rights reserved.

1.Introduction

According to the Food and Drug Administration (FDA),food additives are substances added to foods for speci?c physical or tech-nical effects.They may not be used to disguise poor quality yet may aid in preservation and processing,or improve the quality factors of appearance,?avor,nutritional value,and texture [1].Presently,there are more than 3000kinds of ingredients in the FDA’s list of safe food additives [2].The ideal food additive is bene?cial and harmless to the human body.In fact,many food additives have cer-tain toxicity,especially the chemically synthesized food additives,so the addition amount of food additives is strictly limited accord-ing to the regulations of the Codex Alimentarius Commission (CAC).Undeniably,it is bene?cial to get the same effect with less amount of food additives or a food additive playing a dual role of two food additives,such as acetic acid,which is used as both ?avoring agent and as preservative in food system.

Chitosan (CS)[poly ˇ-(1→4)-linked 2-amido-2-deoxy-D-glucopyranose and ˇ-(1→4)-linked 2-acetamido-2-deoxy-D-glucopyranose]is a unique cationic marine polysaccharide obtained by partial deacetylation of chitin,the second most

?Corresponding authors.Tel.:+86053282032586;fax:+86053282032586.E-mail addresses:qfdang@https://www.sodocs.net/doc/5515914985.html, (Q.Dang),liucsouc@https://www.sodocs.net/doc/5515914985.html, (C.Liu).

abundant nature polymer,under alkaline condition [3–5].Due to its non-toxicity,biodegradability [6],biocompatibility [7,8],antimi-crobial activity [9],and versatile chemical and physical properties,chitosan attracts considerable interest and has prospective applications in a variety of ?elds,such as medical applications,biotechnology,textiles,wastewater treatment,cosmetics,agricul-ture,and food science [10–12].There are a lot of researches about antimicrobial activity of chitosan,which is expected as a food additive to be used in the food system for preservation.However,chitosan’s antimicrobial activity is not ideal as compared with commercial preservative,especially in inhibiting mold growth,which greatly restrains its application as a food preservative in food industry [13,14].Recent studies have focused more on the preparation of chitosan derivatives that have strong antimicrobial activity and can be used as the good food preservatives,such as p-amino benzoyl chitosan ester [14],O-fumaryl-chitosan [15],chitosan glucose complex [16],and xylan chitosan conjugate [17].In addition,some amphiphilic chitosan derivatives have also been reported that have surface activity and can be used as the foaming agents,such as (2-hydroxyl-3-dodecanoxyl)propyl carboxymethyl chitosan,(2-hydroxypropyl-3-butoxy)succinyl chitosan,stearoyl chitosan,palmitoyl chitosan,and octanoyl chitosan [18].There-fore,if a chitosan derivative with strong antimicrobial activity and favorable foaming property was synthesized,it will greatly broaden the applications of chitosan in food industry.

https://www.sodocs.net/doc/5515914985.html,/10.1016/j.ijbiomac.2015.03.0070141-8130/?2015Elsevier B.V.All rights reserved.

J.Cai et al./International Journal of Biological Macromolecules77(2015)52–5853

Benzoic acid is generally recognized as safe(GRAS)for being used as a food preservative in high-acid foods and occurs natu-rally in some organisms.Furthermore,it is extensively used as a legal food preservative in most countries,due to its low cost and high antimicrobial activity,especially in inhibition on mold and yeast[19].But its usage has already sparked international contro-versy.For example,poisoning by accumulation of benzoic acid and its sodium salt has been reported,Hyperalive Children’s Support Group of EEC(HACSG)thinks that it should not be used in chil-dren’s food and Japan has also made a strict limit on the use of it. Therefore,we should be cautious about its use.By far,since there is no way to forbid its use,it is wise to reduce its addition amount in food.Chitosan modi?ed with benzoic acid maybe a proper way to reduce the amount of benzoic acid,broaden antimicrobial spec-trum,and endow amphipathicity of chitosan derivative.Acetic acid is a food-grade acidulant with low cost and strong antimicrobial activity,and is widely added to food system and daily diet.In order to reduce the amount of benzoic acid and endow amphipathic-ity of chitosan derivative,acetyl is introduced as a hydrophobic group to its reactive functional groups(the NH2or the OH group) and the hydrophilic backbones are substituted by hydrophobic groups.

In this paper,ultrasonic method was developed as a simple and novel method to synthesize N-benzoyl-O-acetyl-chitosan for the ?rst time.In the reaction system,allelocatalysis of benzoyl chloride and acetic acid make benzoyl and acetyl be introduced into chitosan to obtain the chitosan derivative BACS.The chemical structure and physical properties of BACS were characterized by FTIR,1H NMR, TGA,and XRD techniques.The foaming properties and the antimi-crobial activities of CS and BACS against a gram-negative bacterium Escherichia coli(E.coli),a Gram-positive bacterium Staphylococcus aureus(S.aureus),and a fungus Aspergillus niger(A.niger)were also investigated.

2.Experimental

2.1.Materials

Chitosan was purchased from Qingdao Honghai Biotechnol-ogy Co.,Ltd.(Shandong,China)and used as received.The degree of deacetylation(DD)was88.5%and the molecular weight was3×105Da.Acetic acid and all other reagents or solvents were purchased from Sinopharm Chemical Reagent Co.,Ltd. (Shanghai,China).Benzoyl chloride was puri?ed by vacuum dis-tillation.Other reagents were used without further puri?cation. S.aureus,E.coli,and A.niger supplied by Microbiology Laboratory of Ocean University of China were used for antibacterial activity test.

2.2.Synthesis of BACS

The N-benzoyl-O-acetyl-chitosan(BACS)was synthesized as follows(Scheme1):CTS(2g,11.0mmol calculated as glucosamine units)was dissolved in8ml pure acetic acid and sonicated at 50?C(53kHz,260W)for10min.Then benzoyl chloride(2.54ml, 2equiv/glucosamine unit of chitosan)was added and the mix-ture was sonicated continually for90min.The desired compound was precipitated in acetone overnight and collected with a?lter. Following that the collected substances were dissolved in30ml distilled water and the precipitate appeared once more when the pH was adjusted to7.0with1mol/L NH3·H2O.The precipitate was obtained by centrifugation and distilled water cleaning.Then the precipitate was freeze-dried as our target product and sealed stor-age for the standby application.2.3.Characterization of BACS

2.3.1.FTIR spectroscopy

Fourier transform infrared(FTIR)spectrum was recorded on a Nicolet AVATAR360instrument(Nicolet Instrument,Thermo Com-pany,Madison,USA)at25?C.About2mg of various samples was mixed with100mg of KBr,and prepared pellets were used for stud-ies.All spectra were scanned against a blank KBr pellet background at wave number range4000–400cm?1with resolution of4.0cm?1.

2.3.2.1H NMR spectroscopy

1H NMR spectra of samples were performed to determine the degrees of substitution of benzoyl and acetyl for the chitosan derivative.Samples were dissolved in a mixed solvent of DCl and D2O and the spectra were carried out on a BrukerAV400MHz (Bruker,Rneinstetten,Germany).

2.3.3.Thermogravimetric analysis(TGA,DTG)

Thermogravimetric analysis(TGA,DTG)was performed on a Rubotherm-DynTHERM thermogravimetric analyzer(Rubotherm Corp.,Bochum,Germany)equipped with the magnetic suspension balance.Samples were heated from50to500?C at a constant heat-ing rate of10?C/min under Ar at50ml/min during the analysis. 2.3.4.X-ray diffraction(XRD)

X-ray powder diffraction spectra of the samples were obtained at room temperature using a D-8advance diffractometer(Bruker AXS,Germany)with a Cu K?radiation( =0.154nm),operated at a voltage of40kV.The samples were analyzed in the2?angle range of5?–60?and the scanning rate was4?/min.

2.4.Foaming properties

The foaming properties of CS and BACS including foam capac-ity(FC)and foam stability(FS)were determined using a high-speed agitation method[20,21].Speci?cally,test samples(0.2%,w/v)were prepared in50mmol/L acetate buffer,pH4.0and containing with0 or0.6mol/L NaCl(which respectively represented pH,low and high salt concentrations corresponding to usual food systems).Then5ml sample was dropped into a25ml plastic measuring cylinder and blended with a touch mixer model for2min at25?C.The total vol-ume of foam in the measuring cylinder was measured immediately, and then the foam was allowed to stand undisturbed.The total vol-ume of the foam was measured after standing for0.5,1,and2h, respectively.Foam capacity(FC)and foam stability(FS)could be calculated,respectively,according to the following equations(eqs (1)and(2)):

FC(%)=

V i

V s

×100(1) FS(%)=

V f

V i

×100(2)

where V i was the initial foam volume,V s was the5ml sample solution,and V f was the tested(0.5,1,and2h)foam volume.

2.5.Antimicrobial assays

E.coli(Gram-negative bacteria)and S.aureus(Gram-positive bacteria)were used as the test bacteria.A representative microbe colony was picked off with a sterile wire loop,placed in steril-ized nutrient broth,and then incubated in incubator shaker at a speed of150r/min at37?C for24h.By diluting with sterile normal saline(0.9%)solution,the cultures of E.coli and S.aureus containing 103–104CFU/ml were prepared and used for the antibacterial test [14].

54

J.Cai et al./International Journal of Biological Macromolecules 77(2015)

52–58

Scheme 1.The synthesis of BACS.

A.niger was used as the test fungi.The culture of fungi was pre-pared by single spore isolation technique.Fungal strain was grown in 5ml sterilized sabouraud dextrose broth (glucose:peptone 40:10ratio)with some small sterile glass beads at 28?C for 3–4days to achieve 105CFU/mL and used for the antifungal test [14].

The inhibition rates of chitosan and BACS on growth of E.coli and S.aureus were determined using agar plates [14].The main solu-tions of chitosan and BACS were ?rst prepared by dissolving the test materials in 1%(w/v)acetic acid aqueous solution and then the different concentrations of chitosan and BACS solutions were pre-pared by duplicate twofold serial dilutions.In the same way,acetic acid aqueous solutions with various concentrations were prepared.All the solutions were sterilized by 0.22?m membrane ?ltration.The nutrient agar plates:a homogeneous mixture of beef extract paste–peptone–agar–sodium chloride (3:10:14:5)was sterilized by autoclaving at 121?C for 20min.The sterilized solution (25ml)was added into each sterilized Petri dish in laminar ?ow and left for 20min to form the solidi?ed nutrient agar plate.These plates were inverted and kept at 30?C for some time to remove the moisture and check for any contamination.Following 0.05ml of bacterial sus-pension was ?rst added into the nutrient agar plate and then 0.1ml of the samples with different concentrations was also added.Both of them were spread uniformly by sterilized triangular folded glass rod.In addition,the nutrient agar plates with only sterile water were also prepared for comparison.All the samples were plated in triplicate on agar plates and all the plates were incubated at 37?C for 24h.Then the plates were taken out to count the colonies.The inhibition rate (IR)was de?ned by Equation 3.

IR (%)=(N 1?N 2)

×100

(3)

Where N 1was the number of colony on the plates with sterile water and N 2was the number of colony after treatment with dif-ferent concentrations of the test materials and acetic acid aqueous solutions.

The antifungal activities of chitosan and BACS on growth of A.niger were investigated by agar well diffusion method [22].Sabouraud dextrose agar plates (glucose:peptone:agar 40:10:15ratio)were prepared according to the preparation of the nutri-ent agar plates.The fungal suspension (0.1ml)was spread out uniformly on the sabouraud dextrose agar plates by sterilized trian-gular folded glass rod.Plates were left for 5–10min so that culture was properly adsorbed on the surface of sabouraud dextrose agar plates.Wells were created in medium with the help of a thin ster-ile metallic bore (diameter 8mm)and the bottom of the wells were sealed with 0.8%soft agar to prevent the ?ow of test samples at the bottom of the well.Chitosan and BACS were prepared in 1%(w/v)acetic acid aqueous solution.In total,100?l of the test samples solution (10mg/ml)was loaded into the wells of the plates and the same amount of 1%acetic acid aqueous solution was also loaded as control.The experiment was repeated three times.The test sam-ples and acetic acid aqueous solutions were sterilized by 0.22?m membrane ?ltration before use.The plates were incubated at 28?C for 7days and examined for the formation of inhibition zone.Each inhibition zone was performed three times.

3.Results and Discussion

3.1.Characterization

3.1.1.FTIR analysis

Fig.1showed the FTIR spectra of CS and BACS.From the FTIR spectrum of CS,the broad band at around 3200–3600cm ?1was attributed to stretching vibration of OH,the extension vibration of the NH,and inter-and extra-molecular hydrogen bonding of chitosan molecules.The characteristic peaks at 1661,1597,and 1318cm ?1assigned to the amide I,the amine -NH2,and amide III absorption band of CS,respectively [23].In addition,the charac-teristic peaks at 1073and 1027cm ?1were,respectively,attributed to C O stretching vibration in C 3OH and C 6OH.For FTIR spec-trum of BACS,the new absorption peaks appeared at 1739and 1240cm ?1were attributed to the characteristic peaks of saturated fatty acid esters and the characteristic peaks became weak at 1073and 1027cm ?1,indicating that esteri?cation reaction occurred between acetic acid and -OH of chitosan.New peaks appeared at about 1601,1490,and 714cm ?1due to the characteristic absorbance of phenyl group.In comparison with the chitosan FTIR spectrum,the peak of amide I at 1661cm ?1moved to shorter wave-length and became stronger;meanwhile the peak at1597cm ?1disappeared,indicating that acylation reaction occurred between benzoyl chloride and -NH 2of chitosan.These results implied that the BACS was successfully synthesized.

3.1.2.1H NMR analysis

The 1H NMR spectra of CS and BACS in DCl/D 2O were shown in Fig.2.Fig.2a showed the 1H NMR spectrum of chitosan.The peak at 2.02ppm was assigned to three protons of N -acetyl glu-cosamine and the peak at 3.14ppm was attributed to the proton of glucosamine residues (H-2).The peaks from 3.5to 4.0ppm cor-responded to the non-anomeric protons (H-3,H-4,H-5,and

H-6)

Fig.1.The FTIR spectra of chitosan and BACS.

J.Cai et al./International Journal of Biological Macromolecules77(2015)52–58

55

Fig.2.The1H NMR spectra of chitosan(a)and BACS(b). while a small peak at4.85ppm represented anomeric protons(H-1)

of chitosan[24].In the1H NMR spectrum of BACS(Fig.2b),the signal

at2.02ppm became very strong due to more methane hydrogen.

The new broad signals at7.37–7.82ppm assigned to the hydrogen

of aromatic ring.The results certi?ed that the chitosan derivative

was comprised of benzoyl groups,acetyl groups,and the other

framework.The result was consistent with the conclusion obtained

from FTIR analysis.The degree of substitution of benzoyl(DB)was

de?ned as the number of benzoyl group per sugar residue of chi-

tosan and the degree of substitution of acetyl(DA)was de?ned as

the number of acetyl group linked to-OH of per sugar residue of

chitosan.They were calculated using the combined integral meth-

ods of peak areas in NMR spectrum of BACS(Fig.2b)according to

the following equations(Eqs(4)and(5)):

DB=

H

5H1

(4)

DA=[CH3]

3H1

?(1?DD)(5)

where H was the integral of the aromatic ring hydrogen (?=7.37–7.82ppm),H1was the integral of anomeric proton of chitosan(?=4.85ppm),[CH3]was the integral of methyl protons (?=2.02ppm)and the DD,degree of deacetylation of chitosan,was 88.5%.By the calculation,DB was0.26and DA was1.15.Hydropho-bic groups(benzoyl and acetyl groups)and hydrophilic groups (amino and hydroxyl)of BACS were almost equal.

3.1.3.Thermogravimetric analysis(TGA,DTG)

The TGA and DTG curves of CS and BACS were shown in Figs.3and4.Fig.3showed that chitosan had two stages of weight loss.The?rst stage at about100?C with weight loss about2.1% was observed corresponding to the water content in the chitosan sample.A further maximum weight loss of58.2%starting at about 180?C corresponded to pyrogenic decomposition and ablation of molecule chains[14].Chitosan had a high speed of decomposition between the temperature of200and230?C reaching its peak temperature at218?C(Fig.4).BACS also showed two degradations in Fig.3.The?rst stage at about100?C with weight loss about3.1% was ascribed to the volatile low molecular products and water.The second stage also started at about180?C with weight loss about 64.76%,which could be attributed to a complex process,including dehydration of the saccharide rings,depolymerization,and decom-position of the acetylated and benzoylated units of the polymer [15].BACS had a high speed of decomposition between the tem-perature of194and244?C,reaching its peak temperature at210?C from Fig.4.Fig.4showed that the second stage of degradation of CS and BACS both started at about180?C.At the beginning of the second stage,BACS had a higher speed of decomposition compared with CS,which could be due to the introduction of ester bond that had a lower decomposition temperature than amido bond.A high speed of decomposition of BACS recurred at about231?C,

which Fig.3.TGA thermograms of chitosan and BACS.

56J.Cai et al./International Journal of Biological Macromolecules77(2015)

52–58

Fig.4.DTG curves for chitosan and BACS.

could be attributed to decomposition of the benzoylated units of the polymer.The decomposition speed of BACS was less sharp than that of CS.BACS and CS had similar thermal stability that all might be due to the combined effect,which the new groups were introduced to result in the breakage of hydrogen bond of chitosan and the possible formation of strong hydrogen bond between CS backbones through the covalently synthetic benzoyl and acetyl side chains.3.1.4.X-ray diffraction(XRD)study

The crystalline properties of the materials could be identi?ed by XRD patterns.Fig.5a showed the XRD patterns of pure chitosan (CS)and its derivative N-benzoyl-O-acetyl-chitosan(BACS).It was observed that the diffractogram of CS consisted of two major crys-talline peaks locating at around10.7?and20.2?.Compared with CS, the diffractogram of BACS exhibited some changes in its diffraction angles,peak intensity,and peak width.The peak at10.7?disap-peared,while the peak at around20.2?,its intensity decreased and width increased.It was well known that peak intensity and width in X-ray diffraction pattern had close correlations with crystallite size[25].The weaker and broader peak implied that there was more amorphous phase in BACS matrix.For further investigation, the XRD patterns of CS and BACS were deconvoluted as depicted in Fig.5b by the software of MDI Jade6.The calculated results were that the crystallinities of CS and BACS were33.26and0%,respec-tively.Therefore,XRD studies demonstrated the pure amorphous phase in BACS matrix as compared to CS,comprising a partial-crystalline phase.These?nding illustrated that acylation reaction might induce the change of molecular interaction forces,symme-try,and stereoregularity of CS,leading to the breakdown of the crystalline structure[26].

3.2.The foaming properties

The foam capacity(FC)and foam stability(FS)of CS and BACS were shown in Figs.6and7,respectively.Foam formation

and Fig.5.(a)XRD of chitosan and BACS.(b)Deconvoluted XRD of(i)chitosan and(ii)BACS.

J.Cai et al./International Journal of Biological Macromolecules 77(2015)52–58

57

Fig.6.At pH 4.0,the foaming capacity (FC)of CS and ABCS at 2mg/ml with 0or 0.6M NaCl.

stability mainly depended on the interfacial properties of the com-ponents.Enhanced adsorption of the sample to the interface,which leaded to a reduction in surface tension,could improve foaming ability [21].At pH 4.0and 0mol/L NaCl,FC of CS and BACS were 4.3and 130.5%,respectively.And at pH 4.0and 0.6mol/L NaCl,FC of CS and BACS were 2.9and 86.2%,respectively.Chitosan exhibited weak foam capacity by itself.This might be due to the low surface activity of pure chitosan,which agreed with its chemical structure:a polysaccharide with cationic -NH3+and alcoholic -OH groups distributed along the hydrocarbon structure.The structure had no large hydrophobic group that might be adsorbed at the air/solution interface [18].BACS,as a chitosan-based amphiphilic compound that could concentrate on the surface with their hydrophobic chains pointing to the air while the hydrophilic backbones lay on the surface to reduce surface tension,showed excellent foam capacity.Besides,it had been reported that all the molecular interaction forces in chitosan solution,such as van der Waals interaction,hydrogen-bonding interaction,electrostatic interac-tion,and hydrophobic interaction had different effects on the surface tension [27].CS and BACS,which had different molecular interaction forces identi?ed by XRD studies,should have different surface tension.This could be used to explain why BACS and CS had different foam https://www.sodocs.net/doc/5515914985.html,pared with samples in 0mol/L NaCl,0.6mol/L NaCl decreased foam ability of CS and BACS.This was explained by the decreased solubility of CS and BACS due to the increased ionic strength [21].And higher solubility would increase adsorption ef?ciency,thus leading to higher FC [28].Fig.7showed the foam stability of BACS.FS of BACS in 0mol/L NaCl reached 82.2,70.3,and 65.9%after standing for 0.5,1,and 2h while in 0.6mol/L NaCl FS were 90.7,82.8,and 77.4%after standing for 0.5,1,and 2h.BACS had good foam stability in 0and 0.6mol/L NaCl.The

improved

Fig.7.At pH 4.0,the foaming stability (FS)of BACS at 2mg/ml with 0or 0.6M NaCl at 0.5,1,and 2h.

FS at high ionic strength indicated the importance of electrostatic interactions in the integrity of foams [21].CS had no foam after standing for 0.5h.In general,the foaming properties of BACS sug-gested that it was suitable for use as a foaming agent,especially in foaming food.

3.3.Antimicrobial assays

3.3.1.Antibacterial activity

Table 1and Table 2showed the effect of concentration on the antibacterial activities of acetic acid,CS,and BACS against E.coli (Gram-negative bacteria)and S.aureus (Gram-positive bacteria).Compared with CS,BACS had a higher antibacterial activity.Among the hypothetical antimicrobial mechanisms of CS,the direct inter-action of positively charged chitosan molecules and negatively charged microbial cell membrane and internal genetic material was most acceptable.The interaction was realized via the electro-static forces between the protonated NH 3+groups of chitosan and the electronegative charges on the surface and inside of microbial cells.This electrostatic interaction resulted in threefold interfer-ences:(i)by facilitating changes of permeation property of the membrane wall,thus provoking internal osmotic imbalances and consequently inhibiting the growth of the microorganisms,(ii)by the hydrolysis of the peptidoglycans in the microbial cell wall,lead-ing to the leakage of intracellular electrolytes,such as potassium ions and other low molecular weight proteinaceous constituents (e.g.,protein,nucleic acid,glucose,and lactate dehydrogenase),and (iii)by penetrating of CS into the nuclei of the microorgan-isms and binding with microbial DNA,leading to the inhibition of the mRNA and protein synthesis [29,30].Since such mecha-nism was mainly based on electrostatic interaction,it suggested that the greater the number of cationic groups was,the higher the antimicrobial activity would be.BACS prepared in this work had a small part of amino groups (DB =0.26)reacting with ben-zoyl chloride,but a large number of C O groups in BACS could be protonated and more amino groups were exposed because acetyl and benzyl were introduced into chitosan as branched chains,which effectively weaken inter-and extra-molecular hydrogen bonding of chitosan molecules.Furthermore,this was also the rea-son for the strong permeability of amphiphilic BACS,which was easier to enter into the cells of microorganisms and prevent the growth of the cells by inhibiting the DNA transcription.It had been reported in literatures that hydrophobic characteristic of chitosan was apt to lead to the interaction between chitosan and bacte-ria cells [31,32].BACS had higher hydrophobicity and was more prone to interact with bacteria cells than chitosan.In addition,benzyl group,as an antimicrobial group would inhibit the growth of microorganisms.This explained the observed higher antibacte-rial activity of BACS compared with the parent chitosan.Moreover,CS and BACS were more active against the Gram-positive bac-teria than the Gram-negative bacteria.When the concentration of CS and BACS was 0.25%,the growth of S.aureus was almost completely suppressed and the corresponding inhibition rates on E.coli were 60and 73%,respectively.This might be attributed to their different cell wall.The cell wall of Gram-positive bac-teria is mainly composed of peptidoglycan.The peptidoglycan layer is a netted structure with a mass of pores,which allow for-eign molecules to come into the cell without dif?culty and allow more rapid absorption of ions into the cell.However,besides a thin peptidoglycan layer,Gram-negative bacteria also possess an outer membrane constituted of lipopolysaccharide,lipoprotein,and phospholipids.Because of the complicated bilayer cell struc-ture,the outer membrane is a potential barrier against foreign molecules with high molecular weight [13].Therefore,the chitosan and chitosan derivative had different effects on the two kinds of bacteria.

58J.Cai et al./International Journal of Biological Macromolecules77(2015)52–58

Table1

The inhibition rate of chitosan and BACS on S.aureus(%).

Sample concentration(%)(w/v)0.031250.06250.1250.250.51 Inhibition rate(%)

Acetic acid31017192228 Chitosan6169929599100 BACS829098100100100

Table2

The inhibition rate of chitosan and BACS on E.coli(%).

Sample concentration(%)(w/v)0.031250.06250.1250.250.51

Inhibition rate(%)

Acetic acid2815172025 Chitosan204557607485 BACS455766738294

3.3.2.Antifungal activity

The wells of the plates that were loaded with chitosan and acetic acid solution did not form the inhibition zone,which indicated that they had no evident antifungal activity against A.niger.It might be because A.niger belongs to fungi category while the fungal cell wall contains chitosan and the A.niger has certain resistance to the antifungal performance of chitosan[30].While BACS revealed an excellent antifungal activity,the wells of which loaded with BACS solution formed the inhibition zone and its diameter was 15.1±0.25mm.It might be due to the introduction of benzyl group because benzoic acid has good inhibitory effect on mold and yeast. Evidently,BACS prepared in this work could not only enhance the antimicrobial activity of chitosan,but also expand the antimicrobial spectrum.

4.Conclusions

N-benzoyl-O-acetyl-chitosan(BACS),amphiphilic chitosan derivative,was prepared by using selective partial acylation of chitosan(CS),benzoyl chloride,and acetic acid under high-intensity ultrasound.FTIR and1H NMR spectra con?rmed that the benzyl and acetyl groups were selectively acylated onto the amino and hydroxyl group of chitosan,respectively.The degrees of substitution of benzoyl and acetyl for BACS were0.26and1.15, respectively,which were determined by the1H NMR technique. TGA and DTG studies revealed that BACS and CS had similar thermal stability,while the decomposition speed of BACS was less sharp than that of CS.XRD studies implied that acylation reaction might induce the destruction of crystalline structure of CS,since there was pure amorphous phase in BACS matrix as compared to CS,comprising a partial-crystalline phase.BACS had better foaming formation and foaming stability in usual food systems, which was mainly related to the amphipathicity of BACS.BACS not only exhibited higher antimicrobial activity than CS against E.coli and S.aureus,but also expanded the antimicrobial spectrum of CS in inhibiting the growth of A.niger.These results suggested that the BACS had the potential of becoming an alternative for food foaming and food preservation.

Acknowledgements

This work was supported by the National Natural Science Foun-dation of China(NSFC,31400812),the Shandong ProvinceNatural Science Foundation(ZR2014CQ052&ZR2011CZ003)and Science and Technology Development Funds of Qingdao Shinan(2014-14-003-SW&2014-13-005-SW).

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expand/enlarge one’s scope of knowledge knowledge reserve/base/storage theoretical knowledge practical skills social experience broaden one’s knowledge base promote one’s overall/ comprehensive competence accumulate experiences learn lessons from past experiences Work and experience the scarcity of employment o p p o r t u n i t i lay the foundations for career p r o s p e r i t y

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Describe a monument Describe an interesting building Describe a lake, river or sea. Describe a peaceful place Describe a leisure place Describe a park Describe a place of interest Describe a natural beauty Describe a city you want to live in Describe a place you have visited Describe a place you always go for shopping

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