Contents lists available at ScienceDirect

Microbial Pathogenesis

journal homepage: www.elsevier.com/locate/micpath

Comparative study between two red algae for biosynthesis silvernanoparticles capping by SDS: Insights of characterization and antibacterialactivity

Ragaa A. Hamoudaa,b,∗, Mahmoud Abd El-Mongyb, Kamel F. Eidb

a Department of Biology, Faculty of Sciences and Arts Khulais, University of Jeddah, Saudi ArabiabDepartment of Microbial Biotechnology, Genetic Engineering and Biotechnology Research Institute, University of Sadat City, Sadat City, Egypt

A R T I C L E I N F O

Keywords:Red algaeChlorella vulgarisCapping AgNPsAntibacterial

A B S T R A C T

Biosynthesis silver nanoparticles (AgNPs) have received a lot of attention as a cytotoxic and antimicrobial ac-tivity against pathogenic bacteria. This study was carried out to evaluate the potential ability of red marine algaeCorallina elongata and Gelidium amansii to biosynthesis AgNPs capping with Sodium Dodecyl Sulfate (SDS) and todetermine its antibacterial efficacy. Characterization of capping AgNPs were determined by Ultra violet-Visiblespectroscopy, Transmission electron microscope (TEM), Scanning electron microscopy (SEM), Fourier trans-forms infrared spectroscopy (FTIR), Energy dispersive X-ray spectroscopy (EDX), Zeta potential and sizer. Theresults indicated that there is no variation change between capping AgNPs synthesis by two red algae in plasmonresonance peak and also both stable along 3 weeks. The capping nanoparticles size were range from 8 to 25 nmin the case of G. amansii and 12–20 nmC. elongata. The results were obtained from Fourier transforms infraredspectroscopy (FTIR) indicated that same metals are present in both algae except Vanadium (V) was present withG. amansii. Capping AgNPs biosynthesis by C. elongata had more toxicity to Chlorella vulgaris than that of syn-thesized by G. amansii. Capping AgNPs by SDS have been shown to enhance antibacterial activity againstMicrococcus leutus, Kocuria varians and Escherichia coli ATCC 8739 compared to non-capping AgNPs. The anti-bacterial activity and toxicity of AgNPs is affected by concentrations of capping agent and the biomaterial (redalgae) that used for synthesis.

1. Introduction

In the last years of world, the infection diseases caused by multi-drug-resistant bacteria had dramatically increased and become seriouschallenge for healthcare [1]. Pathogenic bacteria obtain resistance toantibiotics during antibacterial therapy and become inheritable.Meanwhile using high-doses of antibiotics caused very toxicity [2]. Somany researchers endeavor to obtain a new antibacterial drug, toovercome antibiotic resistance bacteria [3]. Baker-Austin et al. [4] re-ported that nanoparticles can be used as a substitution to antibiotics.Nanoparticles have various applications in many fields includingbiology and medicine [5]. Mechanical, chemical and physicals methodsare used to synthesis nanoparticles; some of them are high cost, notecofriendly and used toxic chemicals [6]. Green synthesis is safe andeco-friendly that do not use toxic chemicals in the synthesis processes[7]. Biological products contain active compounds that can act as re-ducing agents and stabilizing agents to synthesize nanoparticles with

various sizes and shapes [8]. Marine algae are valuable sources ofbioactive compounds that can use in synthesis nanoparticles, as silvernanoparticles that had been synthesis by several marine algae [9]. Redalgae Laurencia aldingensis and Laurenciella sp. extracts were used tosynthesis AgNPs [10]. Compounds founds in algal seaweeds have theability to synthesize a huge variety of nanoparticles with very low or notoxicity risks [11]. Silver can be used as an antibacterial agent andexhibits cytotoxicity against many pathogenic microorganisms [12].Silver nanoparticles (AgNPs) have small size and large surface area so itcan be used as antibacterial agent [13]. The antibacterial activity ofsilver nanoparticles is affected by the shape, size and modification ofthe particles surface [13,14]. The surface modifiers or capping agents(surfactant) can use in the stabilization of smaller sized nanoparticles[15]. Capping agents such as sodium dodecyl sulphate (SDS) is used assilver nanoparticles stabilizer and has the ability to reduce the toxicityof the nanoparticles [16,17]. Hamouda et al. [18] reported that bio-synthesis silver nanoparticles using (SDS) as stabilizer had high

https://doi.org/10.1016/j.micpath.2019.02.016Received 13 May 2018; Received in revised form 10 February 2019; Accepted 11 February 2019

∗ Corresponding author. Department of Biology, Faculty of sciences and Arts Khulais, University of Jeddah, Saudi Arabia.E-mail addresses: ragaahom@yahoo.com, ragaa.hamuoda@gebri.usc.edu.eg (R.A. Hamouda).

Microbial Pathogenesis 129 (2019) 224–232

Available online 12 February 20190882-4010/ © 2019 Published by Elsevier Ltd.

T

Fig. 1. UV-visible visible spectrums (UV) of Ag nanoparticles suspension biosynthesis by G. amansii (a) and C. elongata (b) aqueous extract and capping by SDS (a)after 24 h and 3 weeks.

Fig. 2. Scanning Electron Microscope (SEM) of Ag nanoparticles biosynthesis by C. elongata (a) and G. amansii (b) aqueous extracts and capping by SDS.

Fig. 3. Transmission Electron Microscopic image of silver nanoparticles C. elongata (a) and G. amansii (b) aqueous extract and capping by SDS.

R.A. Hamouda, et al. Microbial Pathogenesis 129 (2019) 224–232

225

antibacterial activity compared with biosynthesis silver nanoparticleswithout capping by (SDS). Kvitek et al. [15] stated that the highestantibacterial activity was shown to be connected to the stabilizationsurface of nanoparticles. This study aimed to compare between thesilver nanoparticles biosynthesis by two red algae C. elongata and G.amansii, that capping by Sodium Dodecyl Sulfate (SDS), according tocharacterization, antibacterial potentiality and cytotoxic effects againstfresh alga C. vulgaris.

2. Material and methods

2.1. Algae

Corallina elongata and Gelidium amansii (red algae) were collectedfrom shallow water beside Abo-qur shore Alexandria Egypt and

identified according to Taylor [19].

2.1.1. Preparation of red algae aqueous extractOne gram of air dried red algae were added to 100ml Double dis-

tilled water (DD water) and boiled for 1 h and after that filtered and thefiltrate completed to 100ml by adding DD water.

2.2. Biosynthesis of silver nanoparticles using red algae aqueous extract

Mix 0.017 gm of AgNO3with 90ml DD water and then add drop bydrop 10ml of algal aqueous extracts with magnetic starrier at 60 °Cuntil the color become brownish [20].

Fig. 4. Energy dispersive X-ray spectrophotometry analysis of AgNPs biosynthesis by C. elongate (a) and G. amansii (b) aqueous extract and capping by SDS.

Fig. 5. Zeta potential analyses of Ag NPs biosynthesis by C. elongata (a) and G. amansii (b) aqueous extract and capping by SDS.

R.A. Hamouda, et al. Microbial Pathogenesis 129 (2019) 224–232

226

Fig. 6. Particles size distribution of Ag NPs biosynthesis by C. elongata (a) and G. amansii (b) aqueous extract and capping by SDS.

Fig. 7. FTIR spectra of green silver nanoparticles capping by SDS and biosynthesis by C. elongata (a) and G. amansii (b).

R.A. Hamouda, et al. Microbial Pathogenesis 129 (2019) 224–232

227

2.3. Capping of biosynthesis AgNPs

Sodium dodecyl sulphate (SDS) (1,3,6, and 9mM) was added tofreshly prepared silver nanoparticles with stirring and heating for30min at 40 °C [21].

2.4. Characterization of silver nanoparticles synthesis by red algae andcapping by SDS

The characterization of AgNPs is performed using various techni-ques such as Ultra violet-Visible spectroscopy (Shimadzu UV-1601PCSpectrophotometer, England) at wavelength 200–700 nm for threeweeks to determine the stability. Surface morphology and distributionof coating AgNPs by SDS were detected by Scanning ElectronMicroscopy (SEM) JEOL JSM-6510/v. Japan. Energy dispersive X-rayEDX detector system (JEOL, JEM-2100, Japan) was used to define theelements content of the nanoparticles sample. The shape and size ofcapping AgNPs were characterized by Transmission electron micro-scope (TEM) (JEOL, JEM-2100, Japan). Fourier-transform infrared(FTIR) was used to determine the active groups of red algae C. elongataand G. amansii aqueous extract that causes the reduction and capping ofsilver ions to form nanoparticles. Zeta potential value, Size distributionof the nanoparticles and Polydispersity Index (PdI) were determinedusing zeta potential analyser (Malven Zeta size Nano-Zs90).

2.5. Phytochemical Screening of C. elongata and G. amansii aqueousextract

Phytochemical analysis (Tannins, Saponins, Flavonoids, Phenol,Quinines, Terpenoids, Coumarins, Glycosides, Phlobatannins, Steroidsand Phytosteroids) was carried out for aqueous extract of C. elongataand G. amansii as per standard methods described by Sanjeet et al. [22].

2.6. Pathogenic bacteria

The antibacterial activity of AgNPs and capping AgNPs were testedagainst three human pathogenic bacteria one of them are Gram nega-tive bacteria, Escherichia coli ATCC 8739 the others are Gram positivebacteria Kocuria varians and Micrococcus leutus «pathogenic bacteriaobtained from microbiology lab of GEBRI University of Sadat cityEgypt»

2.7. Antibacterial activity of AgNPs and capping AgNPs by SDS

2.7.1. Paper disc diffusion assayThe agar diffusion techniques were used to determine the anti-

bacterial activity of capping AgNPs using Petri dishes. Briefly 25 μlAgNPs at different concentrations (25, 50, 75 and 100 μg/ml) wereladen on sterile and air dried filter paper (Whitman No. 1, 3 mm indiameter). The papers were put on the surface of nutrient agar mediaand 105 CFU/ml of bacteria cells were distributed on the surface of thenutrients agar plate. The plates were incubated with 30 °C, after 48 hthe clear zones were determined around the paper disc that specified, ofantibacterial activity of capping AgNPs against Escherichia coli ATCC8739, Micrococcus leutus, Kocuria varians. The same methods were ap-plied using 0.1mM AgNPs capping with different concentrations ofSDS1, 3, 6 and 9mM [21].

2.8. Algal toxicity

Chlorella vulgaris was obtained from «Microbial Biotechnology la-boratory, Genetic Engineering and Biotechnology Research Institute,University of Sadat City, Egypt».

C. vulgaris was cultivated in 250ml Erlenmeyer flasks each contain90ml of Kuhl's medium, after sterilization the concentrations of cap-ping AgNPs were adjusted (0.1, 0.05, 0.025, 0.012, 0.006 and0.003mM), and flasks were inoculated with 10ml of C. vulgaris with105 cell/ml. Optical density of growth was determined using Unico UV-2000 spectrophotometer with time [23].

2.9. Statistical analysis

Results were conducted in triplicates and expressed as means ±standard error of the mean. Significant differences between the meansof parameters (LSD) were determined using Duncan's multiple rangetests (P≤ 0.05). All analysis were carried by SPSS software version(16).

Table 1Screening of phytochemicals analysis of C. elongata and G. amansii.

Test G. amansii C. elongata

Tannins + +Saponins + –Flavonoids + +Phenol – –Quinines + –Terpenoids + +Coumarins + –Steroids and Phytosteroids + +Glycosides + +Phlobatannins – –Anthraquinones – –

Fig. 8. Effect of different concentrations of AgNPs biosynthesis by C. elongata (a) and G. amansii (b) capping by SDS on C. vulgaris growth.

R.A. Hamouda, et al. Microbial Pathogenesis 129 (2019) 224–232

228

3. Results and discussion

The aqueous extracts of algae are pale green and the silver nitratesolutions are colorless. In the beginning colorless solution was obtainedafter mixing the algal extracts (C. elongata and G. amansii) separatelywith the silver nitrate solution. After half an hour with heating at 60 °Cand stirring, the colorless solution was changed became a yellowishbrown color indicated that the formation of AgNPs The formation ofAgNPs was confirmed by color change followed by UV–Visible spec-trophotometer analysis. The UV–Visible spectrophotometer of bio-synthesized AgNPs by G. amansii showed the intense peaks with strong

surface plasma resonance between 413 and 410 nm where the intensitywas 0.236 and 0.259 when measuring after 1 h and three weeks re-spectively. Meanwhile the of UV–Visible spectrophotometer intensepeaks of biosynthesized AgNPs by C. elongata were 407 and 410 withintensity were 0.304 and 0.355 when measuring after 1 h and threeweeks Fig. 1 (a, b). The absorption peak of AgNPs biosynthesis by G.amansii measured by UV-Visible spectra is 420 and retains the stabilityfor about 6 months without any shift in the surface plasma absorbanceband [24,25].

The shape and distribution of capping AgNPs that synthesized by G.amansii and C. elongata aqueous extract estimated by Scanning Electron

Fig. 9. Effect of AgNPs biosynthesis by C. elongata (a) and G. amansii (b) capping by SDS on C. vulgaris.

Fig. 10. Effect of different concentrations of AgNPs biosynthesis by C. elongata (a) and G. amansii (b), Bars represent are standard error (means of triplicate). «Samelitters are not significantly different p≤ 0.05»

R.A. Hamouda, et al. Microbial Pathogenesis 129 (2019) 224–232

229

Microscope (SEM). The square shape was appeared with AgNPs syn-thesized by G. amansii and capping by SDS where spherical shape ap-peared with AgNPs synthesized by C. elongata and capping by SDS. Thisresult demonstrated that the nanoparticles differ in shape according totype of algae that were used in synthesis (Fig. 2).

The size and microstructures of the biosynthesized silver nano-particles that capping with SDS was determined by transmission elec-tron microscopy (TEM) analysis. Fig. 3 shows that the range of particlessize of AgNPs biosynthesized by G. amansii and capping by SDS was8–25 while with C. elongata the range was 12–20.

Results in Fig. 4 show peaks that represent of metals content of theaqueous AgNPs capping by SDS that examined by Energy dispersive X-ray spectrophotometry. Ten peaks Na, Al, Si, P, S, Cl, Ag, Ca and Fe andeleven peaks of same metals in addition to Vanadium (V) that is ap-proximately located between 0.5 and 6 keV of aqueous extract Ag NPsbiosynthesis by C. elongata and G. amansii respectively. Both samplesclear that higher percentage of silver content was 55.35 and 59.06

respectively.The results in Fig. 5 demonstrated Zeta potential that clear surface

charge of AgNPs capping by SDS and biosynthesized by C. elongata andG. amansii. The results show Zeta potential value was−8.61 and−13.1of Ag NPs capping by SDS and biosynthesized by C. elongate and G.amansii respectively that indicated that AgNPs capping by SDS werehighest physical stability. The negative value of the zeta potential in-dicate the efficiency of the capping compounds in stabilizing AgNPs bygiven intensive negative charges that preserve all the particles awayfrom each other [26]. The negative values clarify the repulsion betweenthe particles and thereby achievement of higher stability of AgNPsformation evading agglomeration in aqueous solutions [27]. Negativecharge of silver nanoparticles potent antibacterial activity [28].

Polydispersity Index PdI ranged from 0.08 to 0.7 represent mid-range value of PdI while higher than 0.7 indicates a very broad dis-tribution of particle sizes. The PdI of Ag NPs biosynthesis by C. elongatawas 0.533, meanwhile the PdI of Ag NPs biosynthesis by G. amansii was

Fig. 11. Effect of different concentrations of SDS capping AgNPs that biosynthesis by C. elongata (a) and G. amansii (b) on pathogenic bacteria, Bars represent arestandard error (means of triplicate) «Same litters are not significantly different p≤ 0.05»

R.A. Hamouda, et al. Microbial Pathogenesis 129 (2019) 224–232

230

0.716. It is noticed that some aggregations among Ag NPs biosynthesisby G. amansii more than biosynthesis by C. elongata. It was shown thatthe particle size measured by TEM is smaller than the particles sizemeasured by Malvern Master sizer particles size analyser. It may be dueto presonication step in TEM procedure (Fig. 6) [29].

Fig. 7 shows that various peaks of FT-IR spectra related to silvernanoparticles capping by SDS and biosynthesis by C. elongate and G.amansii. A very sharp peaks was observed at 1637.95 cm−1and1638.38 cm−1in both silver nanoparticles biosynthesized by C. elongataand G. amansii respectively, which was related to free-N–H stretch vi-brations in the amide linkages of the proteins. Abdel-Raouf et al. [30]reported that proteins probably form a coat covering the metal nano-particles and prevent agglomeration of the nanoparticles. Balaji et al.[14] investigated that extracellular protein compound can bind andsynthesized silver nanoparticles through free amine groups. The peaksdenoted by FT-IR spectra of biosynthesized silver nanoparticles of bothC. elongata and G. amansii were at 1384.92 cm−1 and 1384.58 cm−1

revealed to–OH bending vibrations, and also peaks at 1235.21 cm−1

and 1230.55 cm−1 that related to C(O)–O stretching vibrations. Thesefunctional groups may be responsible to flavonoids and tannins whichmore abundant in red algae [31]. Mishra and Sardar [32] concludedthat the free thiol groups present in the proteins were responsible forthe reduction of silver nitrate to silver nanoparticle formation.

Table 1 shows that the both aqueous extracts red algae C. elongataand G. amansii contain flavonoids, tannins and terpenoids which helpsin reducing silver and contains AgNPs as agreement with Vijayar-aghavan et al. [33] they reported that proteins, flavonoids and tanninsbands which may be responsible for biosynthesis of nanoparticles thatreduction of metal ion to metal nanoparticles.

The results obtained in Fig. 8 investigated that the effects of dif-ferent concentrations of AgNPs biosynthesized by C. elongata and G.amansii capping by SDS on microgreen alga C. vulgaris growth that wasmeasured by optical density. The results indicated that the AgNPs hadtoxic effects on microgreen alga C. vulgaris, meanwhile AgNPs bio-synthesis by G. amansii had more toxic effect than AgNPs biosynthe-sized by C. elongata as shown in Fig. 9. Razack et al. [34] reported thatAgNPs have the ability to breaking down the cell wall of the microalgaC. vulgaris. Dash et al. [35] investigated that silver nanoparticles havebeen identified for algicidal. Hund-Rinke and Simon [36] shown thatnanoparticles had toxicity to algae. Silver nanoparticles (AgNPs) hasantialgal agent against the liver inducing cancer Microcystis aeruginosa[37].

3.1. Antibacterial activity of AgNPs biosynthesized by C. elongata and G.amansii

Fig. 10 displays the effects of various concentrations of AgNPsbiosynthesis by C. elongata and G. amansii on Gram positive bacteriaMicrococcus leutus, Kocuria varians and Gram negative bacteria Escher-ichia coli ATCC 8739. The results indicated that 0.1 mM of AgNPs wasthe best concentrations that more effective against tested bacteria. Andalso results demonstrated that Kocuria varians has more resistance toAgNPs biosynthesis by C. elongata among Micrococcus leutus and Es-cherichia coli ATCC 8739. AgNPs biosynthesized by C. elongata possessesmore inhibition clear zone with Escherichia coli ATCC 8739. Micrococcusleutus has more resistant by AgNPs biosynthesis by G. amansii, mean-while Escherichia coli ATCC 8739 has more sensitive by AgNPs bio-synthesized by G. amansii. The Ag nanoparticles synthesized usingmarine alga G. amansii are potential antibacterial agents especiallyagainst prominent microfouling bacteria [30]. Silver nanoparticlesbiosynthesized by C. elongata and G. crinale had cytotoxic activityagainst Ehrlich ascites carcinoma (EAC) [38]. Silver nanoparticlessynthesized by aqueous extract of green alga Caulerpa racemosa ex-hibited antibacterial activity against E. coli, B. subtilis, K. pneumoniae, S.aureus, and P. aeruginosa [39]. Nanoparticles can either show inhibitoryor lethal effect towards bacteria, depending upon its concentrations

[40].Fig. 11 represents the effect of different concentrations of sodium

dodecyl sulfate 1, 3, 6, and 9mM (SDS) capping biosynthesized AgNPsby C. elongata and G. amansii against pathogenic bacteria. Results re-vealed that biosynthesized AgNPs capping by SDS was more anti-bacterial activity than the biosynthesized AgNPs without capping bySDS. Meanwhile results display 6mM of (SDS) with 0.1 mM of bio-synthesized AgNPs by C. elongata is more antibacterial agents againstKocuria varians however the concentration 1.0mM of (SDS) with0.1 mM of biosynthesized AgNPs by C. elongata is high antibacterialactivity against both Micrococcus leutus and Escherichia coli ATCC 8739than other tested concentrations. Sodium dodecyl sulfate (9 mM) is thebest concentrations with 0.1 mM of biosynthesis AgNPs by G. amansiifor possessing antibacterial activity against all tested pathogenic bac-teria. Kora et al., [41] suggested that the antibacterial activity of silvernanoparticles is enhanced by capping with SDS. Kora and Rastogi [42]investigated that the enhancement in antibacterial activity of anti-biotics with silver nanoparticles influenced by the capping agent onnanoparticles.

The present study indicated that the ability of aqueous extracts oftwo red algae C. elongata and G. amansii to biosynthesized of silvernanoparticle using silver nitrate. The AgNPs synthesized by two algaehas been differed in characterization and also in potential activityagainst Gram positive bacteria Micrococcus leutus, Kocuria varians andGram negative bacteria Escherichia coli ATCC 8739. The AgNPs coatedby SDS has more effective against tested pathogen bacteria and also hascytotoxic activity against microgreen alga C. vulgaris. Different con-centrations of SDS were used to coat green synthesis of silver nano-particles and tested against pathogenic bacteria; the best concentrationsagainst pathogenic bacteria were 6mM and 9mM SDS coating AgNPsbiosynthesis by C. elongata and G. amansii respectively. The greensynthesis AgNPs is potent antibacterial activity and enhancement bycoating materials. Characterizations, antibacterial activity and cyto-toxicity differ according to the green sources that used for biosynthesis.

Conflicts of interest

The authors declare that they have no conflict of interest.

References

[1] M. Exner, S. Bhattacharya, B. Christiansen, J. Gebel, P. Goroncy-Bermes, et al.,Antibiotic resistance: what is so special about multidrug-resistant Gram-negativebacteria? GMS Hyg. Infect. Control 12 (2017) 1–24.

[2] M. Hajipour, K. Fromm, A. Ashkarran, D. Jimenez de Aberasturi, I.R. deLarramendi, T. Rojo, Antibacterial properties of nanoparticles, Trends Biotechnol.30 (2012) 499–511.

[3] M.A. Ansari, H.M. Khan, A.A. Khan, A. Malik, A. Sultan, M. Shahid, Evaluation ofantibacterial activity of silver nanoparticles against MSSA and MRSA on isolatesfrom skin infections, Biol. Med. 3 (2011) 141–146.

[4] C. Baker-Austin, M. Wright, R. Stepanauskas, J.V. McArthur, Co-selection of anti-biotic and metal resistance, Trends Microbiol. 14 (2006) 176–182.

[5] U.K. Parashar, S.P. Saxena, A. Srivastava, Bioinspired synthesis of silver nano-particles, Digest J. Nanomater. Biostruct. 4 (1) (2009) 159–166.

[6] E.E. Connor, J. Mwamuka, A. Gole, C.J. Murphy, M.D. Wyatt, Gold nanoparticlesare taken up by human cells but do not cause acute cytotoxicity, Small 1 (2005)325–327.

[7] V. Sarsar, K. Sanjeet, M. Kabi, M. Kumari, Study on phytochemicals analysis fromleaves of Bixa orellana, Emerg. Sci. 2 (2010) 1–5.

[8] P. Mohanpuria, N.K. Rana, S.K. Yadav, Biosynthesis of nanoparticles: technologicalconcepts and future applications, J. Nanoparticle Res. 10 (3) (2008) 507–517.

[9] S. Rajeshkumar, C. Kannan, G. Amnadurai, Synthesis and characterization of anti-microbial silver nanoparticles using marine brown seaweed Padina tetrastromatica,Drug Invent. Today 4 (10) (2012) 511–513.

[10] A.P. Vieira, E.M. Stein, D.X. Andreguetti, C. Pio, M.F. Ana, Preparation of silvernanoparticles using aqueous extracts of the red algae Laurencia aldingensis andLaurenciella sp. and their cytotoxic activities, J. Appl. Phycol. 28 (4) (2016)2615–2622.

[11] S. Narendhran, K.N. Reshma, Nanoparticles and their toxicology studies: a greenchemistry approach, Res. Dev. Mater. Sci. 2 (3) (2017) 1–8.

[12] M. Valodkar, A. Bhadoria, J. Pohnerkar, M. Mohan, S. Thakore, Morphology andantibacterial activity of carbohydrate- stabilized silver nanoparticles, Carbohydr.Res. 345 (2010) 1767–1773.

R.A. Hamouda, et al. Microbial Pathogenesis 129 (2019) 224–232

231

[13] O. Choi, Z. Hu, Size dependent and reactive oxygen species related nanosilvertoxicity to nitrifying bacteria, Environ. Sci. Technol. 42 (2008) 4583–4588.

[14] D.S. Balaji, S. Basavaraja, R. Deshpande, D.B. Mahesh, B.K. Prabhakar,A. Venkataraman, Extracellular biosynthesis of functionalized silver nanoparticlesby strains of Cladosporium cladosporioides fungus, Colloids Surf., B 68 (2009) 88–92.

[15] L. Kvitek, A. Panáček, J. Soukupová, M. Kolár, R. Večeřová, R. Prucek, Effects ofsurfactants and polymers on stability and antibacterial activity of silver nano-particles (NPs), J. Phys. Chem. 112 (2008) 5825–5834.

[16] Y. Yu-Nam, J.R. Lead, Manufactured nanoparticles: an overview of their chemistry,interactions and potential environmental implications, Sci. Total Environ. 400(2008) 396–414.

[17] Z. Shi, J. Tang, L. Chen, C. Yan, S. Tanvir, W.A. Anderson, R.M. Berry, K.C. Tam,Enhanced colloidal stability and antibacterial performance of silver nanoparticles/cellulose nanocrystal hybrids, J. Mater. Chem. B 3 (2015) 603–611.

[18] R.A. Hamouda, M. Abd El-Mongy, K.F. Eid, Antibacterial activity of silver nano-particles using ulva fasciata extracts as reducing agent and sodium dodecyl sulfateas stabilizer, Int. J. Pharmacol. 14 (2018) 359–368.

[19] W.R. Taylor, Marine Algae of the Eastern Tropical and Subtrobical Coasts of theAmerica, The University of Michigan studies Scientific Series 21 (1985), p. 825.

[20] J.S. Devi, V. Bhimba, K. Ratnam, Anticancer activity of silver nanoparticles syn-thesized by the seaweed Ulva lactuca in vitro, Sci. Rep. 1 (2012) 242–248.

[21] A.J. Kora, R. Manjusha, J. Arunachalam, Superior bactericidal activity of SDScapped silver nanoparticles: synthesis and characterization, Mater. Sci. Eng. C 29(2009) 2104–2109.

[22] K. Sanjeet, M. Kabi, M. Kumari, Study on phytochemicals analysis from leaves ofBixaorellana, Emerg. Sci. 2 (2010) 5.

[23] D.F. Wetherell, Culture of fresh water algae in enriched natural seawater, PlantPhysiol. (Copenh) 14 (1961) 1–6.

[24] G. Thirumurugan, M.D. Dhanaraju, Novel biogenic metal nanoparticles for 10pharmaceutical applications, Adv. Sci. Lett. 4 (2011) 339–348.

[25] A. Pugazhendhia, D. Prabakarb, J.M. Jacobc, I. Karuppusamyd, R.G. Saratalee,Synthesis and characterization of silver nanoparticles using Gelidium amansii and itsantimicrobial property against various pathogenic bacteria, Microb. Pathog. 114(2018) 41–45.

[26] M.J. Haider, M.S. Mehdi, Study of morphology and zeta potential analyzer for thesilver nanoparticles, Int. J. Sci. Eng. Res. 5 (2014) 381–385.

[27] S. Farhadi, B. Ajerloo, A. Mohammadi, Green biosynthesis of spherical silver na-noparticles by using date palm (phoenix dactylifera) fruit extract and study of theirantibacterial and catalytic activities, Acta Chim. Slov. 64 (2017) 129–143.

[28] L. Salvioni, E. Galbiati, V. Collico, G. Alessio, S. Avvakumova, F. Corsi, P. Tortora,D. Prosperi, M. Colombo, Negatively charged silver nanoparticles with potent an-tibacterial activity and reduced toxicity for pharmaceutical preparations, Int. J.

Nanomed. 12 (2017) 2517–2530.[29] S. Satapathy, S.P. Shukla, Application of a marine cyanobacterium Phormidium

fragile for green synthesis of silver nanoparticles, Ind. J. Biotechnol. 16 (2017)110–113.

[30] N. Abdel-Raouf, N.M. Al-Enazi, B.M. Ibraheem, Green biosynthesis of gold nano-particles using Galaxaura elongata and characterization of their antibacterial ac-tivity, Arabian J. Chem. 10 (2) (2013) 23–29.

[31] B.G. Wang, W.W. Zhang, X.J. Duan, X.M. Li, In vitro antioxidative activities of ex-tract and semi-purified fractions of the marine red alga, Rhodomela confervoides(Rhodomelaceae), Food Chem. 113 (2009) 1101–1105.

[32] A. Mishra, M. Sardar, Alpha-amylase mediated synthesis of silver nanoparticles, Sci.Adv. Mater. 4 (2012) 143–146.

[33] K. Vijayaraghavan, A. Mahadevan, M. Sathishkumar, S. Pavagadhi,R. Balasubramanian, Biosynthesis of Au(0) from Au (III) via biosorption and bior-eduction using brown marine alga Turbinaria conoides, Chem. Eng. J. 167 (1) (2011)223–227.

[34] S.A. Razacka, S. Duraiarasanb, V. Mani, Biosynthesis of silver nanoparticle and itsapplication in cell wall disruption to release carbohydrate and lipid from C. vulgarisfor biofuel production, Biotechnol. Rep. 11 (2016) 70–76.

[35] A. Dash, A.P. Singh, B.R. Chaudhary, S.K. Singh, D. Dash, Effect of silver nano-particles on growth of eukaryotic green algae, Nano-Micro Lett. 4 (2012) 158–165.

[36] K. Hund-Rinke, M. Simon, Ecotoxic effect of photocatalytic active nanoparticles TiOon algae and daphnids, Environ. Sci. Pollut. Control Ser. 13 (4) (2006) 225–232.

[37] M.M. El-Sheekh, H.Y. El-Kassas, Application of biosynthesized silver nanoparticlesagainst a cancer promoter cyanobacterium, Microcystis aeruginosa, Asian Pac. J.Cancer Prev. APJCP 15 (2014) 6773–6779.

[38] K.S. Khalifa, R.A. Hamouda, H.A. Hamza, In vitro antitumor activity of silver na-noparticles biosynthesized by marine algae, Digest J. Nanomater. Biostruct. 11(2016) 213–221.

[39] T. Kathiraven, A. Sundaramanickam, N. Shanmugam, T. Balasubramanian, Greensynthesis of silver nanoparticles using marine algae Caulerpa racemosa and theirantibacterial activity against some human pathogens, Appl. Nanosci. 5 (4) (2015)499–504.

[40] N.V.A. Núñez, H. Villegas, L. Turrent, C. Padilla, Silver nanoparticles toxicity andbactericidal effect against methicillin-resistant Staphylococcus aureus: nanoscaledoes matter, Nanobiotech 5 (2009) 2–9.

[41] A.J. Kora, M. Ranjit, A. Jayaraman, Superior bactericidal activity of SDS cappedsilver nanoparticles: synthesis and characterization, Mater. Sci. Eng. C 29 (7) (2009)2104–2109.

[42] A.J. Kora, L. Rastogi, Enhancement of antibacterial activity of capped silver na-noparticles in combination with antibiotics, on model gram-negative and gram-positive bacteria, Bioinorgan. Chem. Appl. (2013) 8710977 pp.

R.A. Hamouda, et al. Microbial Pathogenesis 129 (2019) 224–232

232