Green Synthesis of Silver Nanoparticles using Marine Sea Weed Acetabularia acetabulum and their Activity as MMT-Ag Nanocomposites towards Antifouling Applications

 

Sahithya K.¹*, K. Karthika²

¹Department of Microbiology, Indian Academy Degree College - Autonomous,

Bengaluru - 560043, Karnataka, India.

²Department of Microbiology, Karpagam Academy of Higher Education, Coimbatore - 641021, Tamil Nadu, India.

 

ABSTRACT:

The present study proposed the green synthesis of silver (Ag) nanoparticles using aqueous extract of Acetabularia acetabulum followed by their fabrication onto montmorillonite (MMT). Fourier transform infrared (FTIR) spectra revealed the involvement of multiple functional groups in the reduction of silver ions to Ag nanoparticles and their stabilization on MMT. The obtained MMT-Ag nanocomposites were characterized by UV–visible spectroscopy, powder X-ray diffraction (XRD), particle size analysis (PSA), scanning electron microscopy (SEM) and Energy Dispersive X-Ray (EDX) analysis. The synthesised Ag nanostructures were found to be cubic shaped with average size ranges from 37nm to 60 nm. The seaweed mediated MMT-Ag nanocomposites were evaluated for their potential antimicrobial properties against the isolated biofouling bacteria. Maximum bactericidal activity was recorded against S. aureus followed by E. coli, M. flavus, Pseudomonas aeruginosa, B. cereus, M. leteus and B.  subtilis. In addition, the viability of incorporating MMT-Ag nanocomposites in paint was examined where a significant inhibition of marine fouling bacteria was exhibited by the panel coated by MMT-Ag nanocomposites-based paint as compared to water-based paint. The addition of MMT-Ag nanocomposites in water-based paint was also found to be effective against corrosion from marine water. The present study shows cytotoxicity of MMT-Ag nanocomposites as nanoclay/metallic nanocomposites against A. salina with LD50 values of 200±3.4 µg/ml. The results of the present study suggested the application of A. acetabulum extract as a good bio-resource for the synthesis of Ag nanoparticles and their implementation to combat marine biofouling on ship hulls.

 

 

INTRODUCTION:

Metallic nanoparticles have attracted global interest in recent years in the area of industrial, environmental and medicinal applications owing to their exceptional physiochemical properties. Extensive use of nanomaterials has attracted global interest in sustainable strategies for their synthesis which can alter their properties. Inherent properties of the nanoparticles can be easily altered with minor changes in their process of synthesis.

 

Traditionally, nanoparticles are synthesized using physical and chemical approaches, however, these methods involve the use of non-biodegradable chemicals and expensive solvents as reducing agents and stabilizing agents that lead to production of toxic by-products which are detrimental to biological and environment systems^1,2.

 

In this context, green synthesis of metal nanoparticles by utilizing marine bioresources is under immense investigation in the last few years and thus, has become an innovative area of research^3,4. Seaweeds are the natural repository of various bioactive compounds and one of the major renewable resources from the marine environment^5,6. They are widely known for their antimicrobial⁷, antioxidant⁸, antiviral⁹, anticoagulant¹⁰, antithrombotic¹¹, spermicidal¹², cytotoxic¹³ and immune-inflammatory¹⁴ properties owing to several bioactive compounds such as alkaloids, amino acids, flavonoids, phenols, quinines, sterols, tannins and terpenoids^15-17.

 

Numerous reports suggested the exploitation of various seaweeds for the biosynthesis of nanomaterials with extensive applications in various fields³. Among the green algae, Acetabularia acetabulum is one of the abundant seaweeds widely distributed in the shores of Andaman Islands. Several studies have been published, with special emphasis to study the molecular diversity, structural and chemical properties of seaweeds using A. acetabulum as a model^18-20. However, reports on the reducing and stabilization properties of A. acetabulum in the synthesis of nanoparticles are scanty.

 

Clay minerals are well known for their exceptional properties such as high surface area, swelling capacity, thermal stability, negative surface charge, high ionic exchange capacity, adsorptive and desorptive capacities²¹. The development and application of nano-scale clays as antimicrobial agents are much reviewed in. Among the nano clays, montmorillonite (MMT) is a layered aluminosilicate chemically composed of calcium, hydrogen, sodium, aluminum, iron, magnesium, zinc and silica ions. MMT has been widely applied as nanofillers in various industries. In addition to direct antimicrobial activity of MMT, they also exhibited indirect antimicrobial activities in combination of metallic nanomaterials and polymers^22-25.

 

Marine biofouling on ships hulls represents an important problem from both environmental and economic points of view where it causes increased GHG emissions, surface roughness and fuel consumption²⁶. Fouling is initiated though marine bacterial attachment on the surface followed by the secretion of extracellular polysaccharides (EPS) leading to biofilm formation. Several reports suggested the development of novel methods and formulations of marine coating to their resistance against biofouling²⁷.

 

To the best of our knowledge, no report is available on green synthesis of Ag nanoparticles using Acetabularia acetabulum.  Hence, the present study is focused on the green synthesis of Ag nanoparticles supported on MMT using an aqueous extract of Acetabularia acetabulum and their application as antifouling agents against biofouling bacterial isolates as well as in the preparation of a cost effective and eco-friendly anti-biofouling paint.

 

MATERIALS AND METHODS:

Materials:

All the chemicals used in the present work were of analytical grade and purchased from Sigma Aldrich, India and Sisco Research Laboratories Pvt. Ltd, India.

 

Collection of samples:

The bio-film sample and the marine water sample were collected from the Kakinada port (17.08°N and 82.36° E), Andhra Pradesh, India. The seaweed, Acetabularia acetabulum was collected from coastal region of Chidiya Tapu (11.50°N and 92.70°E), Andaman Islands, India. The collected samples were stored in air tight containers and transferred to a Microbiology laboratory. The seaweed sample was thoroughly washed with tap water to eliminate foreign materials and then washed with sterilized milli Q water. The seaweed sample was dried at 30ºC and ground to fine powder for further analysis.

 

Isolation of bio-fouling bacteria:

Cultivable bacterial strains were isolated on Zobel Marine agar containing 50% (v/v) of distilled water and 50% (v/v) of marine water and incubated overnight for 24 h at 37°C in BOD incubator. Cultural, morphological and biochemical characteristics of the microbial isolates were studied following standard methods²⁸.

 

Preparation of seaweed extract and biosynthesis of MMT-Ag nanocomposites:

A solution of seaweed extract was initially prepared by heating powdered form of Acetabularia acetabulum in double distilled water at 80°C for 1 h followed by vacuum filtration of the heated mixture for removal of solid residues. Thereafter, 1% (w/v) MMT was dispersed in aforementioned seaweed extract followed by the addition of 0.1 M silver nitrate solution. The reaction mixture was maintained for 3 h at 60°C under continuous agitation. The synthesis was carried out under dark conditions to minimise the photo-activation of silver nitrate. Phyto-reduction of AgNO₃ into Ag nanoparticles was identified by the colour change from green to brown. After the synthesis, the reaction mixture containing MMT-Ag nanocomposites were centrifuged at 6000rpm for 15 min and the pellet containing MMT-Ag nanocomposites were vacuum dried for 24 h and stored in air tight container for further analysis. Aliquot of the reaction solution was analysed using UV–vis spectrophotometer (Jasco-V-670 B072061154) operated at a resolution of 2nm, from 300 to 800nm. The size distribution and particle stability were analysed using Particle Size Analyzer (PSA). The crystalline nature of biogenic Ag nanoparticles in MMT-Ag nanocomposites was characterized by X-ray diffraction analysis using Cu Ka radiation in the scan range of 30 to 80 degree (Shimadzu 6000 Diffractometer).

 

Spectroscopic studies:

Fourier transform infrared analysis of seaweed extract and MMT-Ag nanocomposites were performed over the range of 400 cm^-1 to 4000 cm^-1 at a resolution of 5 cm^-1 in the diffuse reflectance mode (Shimadzu model IR Affinity-1) in order to understand the involvement of functional groups in phyto-reduction and stabilization of biogenic Ag nanoparticles. The surface morphology and elemental composition of MMT-Ag nanocomposites were studied through Scanning Electron Microscope (SEM, Jeol JSM 6390) and Energy Dispersive X-ray analysis (EDX, Thermo Electron Corporation).

 

Assessment of anti-biofouling competence of MMT-Ag nanocomposites:

Bactericidal activity of MMT-Ag nanocomposites:

The bactericidal activity of MMT-Ag nanocomposites against biofouling bacterial isolates was evaluated by the well diffusion method previously described by Vijayan et al.²⁹. A suspension of sterile saline solution (0.85%) containing 24 h old bacterial isolates was prepared and the turbidity of the suspension sample was adjusted to match with 0.5 McFarland standards. One ml of suspension was added to assay plates containing 25ml of Zobell Marine agar. Twenty µl of MMT-Ag nanocomposites with different concentrations (25µg, 50 µg, 75µg and 100µg per well) were loaded into experimental wells of 5mm in diameter and 20µl of 1 ppm sodium hypochlorite solution was observed as control. All plates were incubated at 37°C for 48 h. The assay was carried out in triplicates and the zone of inhibition was expressed in millimetres.

 

Anti-crustacean assay of MMT-Ag nanocomposites:

Anti-crustacean assay is a screening technique to understand the toxic effects of MMT-Ag nanocomposites against the crustaceous organisms using Artemia salina as the model organism^31,32. The acute toxicity of MMT-Ag nanocomposites with different concentrations were evaluated in the present study. In brief, 100mg of capsulated A. salina cysts were kept in 500ml conical flask containing 150ml of sterilized seawater with a saline (sodium chloride) concentration of 30±0.5 ppt and were aerated for 24 to 48 h using oxygen air pump under the light source. Subsequently, ten newly hatched larvae were collected using capillary glass tube and placed in 24-well plates containing 2.5ml of 30±0.5 ppt seawater with different concentrations (12.5 to 800µg/mL) of MMT-Ag nanocomposites maintained at 27°C for 48 h where sterile seawater was deposited as blank sample. The mortality rate of A. solina was observed after every six hours and the percentage of A. salina larval mortality was determined and lethal concentration (LC₅₀) was assessed. The experiments were carried out in triplicates

 

Preparation of antifouling paint and panels:

MMT-Ag nanocomposites-based paint (MMT-AgNP) was prepared by adding 100mg of MMT-Ag nanocomposites to minimum volumes of acetone and uniformly dispersed in 2.5ml of water-based paint using an ultrasonicator. Prior to application of MMT-AgNP, surfaces of all the steel plates with rectangular size of 7 cm x 3cm x 1mm in shape were polished using abrasive sandpaper, rinsed with distilled water and degreased with ethanol again. A panel coated with water-based paint without MMT-Ag nanocomposites was used as a blank sample. Other panels were painted with MMT-Ag nanocomposites on both the sides in successive three layers leaving 12 h between applications to form films with ~1mm thickness. The coated panels were dried at room temperature (35±2°C) and further fixed on a metal support.

 

Biofilm inhibition assay of MMT-Ag NP :

Antifouling experiments were carried out during the warm months, which coincide with elevated activities of diatom and bacterial biofilms. All panels were immersed 25cm deep in marine water and inspected every three days to validate the degree of biofouling attachment on the panel surface. The changes in surface morphology of assay plates were photographed with a digital camera.

 

RESULTS AND DISCUSSION:

Isolation and identification of bio-fouling bacteria:

Seven distinct marine biofouling bacterial strains were isolated from biofilm and marine water samples. The isolated bacteria MFB1 to MFB7 were identified as S. aureus, M. leteus, E. coli, B. cereus, B.  subtilis, M. flavus and Pseudomonas aeruginosa based on morphological, colony, cultural and biochemical characteristics.

 

Characterization of biogenic MMT-Ag: nanocomposites:

The phyto-reduction of silver nitrate ions to silver nanoparticles in the reaction mixture was confirmed by UV-Vis spectrum where a significant peak was observed at 424nm corresponding to the surface plasmon resonance of silver nanoparticles as shown in figure 1(ai). Similarly, MMT supported silver nanoparticles showed characteristic silver SPR absorbance band around 418nm (Figure 1aii). Green synthesized silver nanoparticles supported on MMT showed good stability for six months without shifting the SPR absorbance band..

 

The formation of silver intercalated structures of MMT was confirmed by the XRD pattern of MMT-Ag nanocomposite (Figure not shown). In the original d-spacing of montmorillonite, 1.24nm was found to be increased to 1.45nm at smaller 2θ angles by Ag⁺ intercalation. An increase in d-spacing of MMT suggested the formation of Ag⁺ nanoparticles not only on the edges and external surface of nano clay but also in the interlamellar space.

 

Figure 1. (a) UV-visible spectrum of green synthesized (i) Ag nanoparticles and (ii) MMT-Ag nanocomposites; (b) Size distribution of MMT-Ag nanocomposites; (c) XRD patterns of MMT-Ag nanocomposite.

 

 

Figure 2. IR spectra of (a) A. acetabulum aqueous extract and (b) MMT-Ag nanocomposites.

 

The size distribution of MMT-Ag nanocomposites is presented in figure 1(b). The mean particle size of MMT-Ag nanocomposites was about 37.7nm. The diffraction profile of MMT-Ag nanocomposites is presented in figure 1(c), showed peaks at 37.9°, 44.2°, 64.4° and 77.5° could be attributed to 111, 200, 220 and 311 crystallographic plans of face centered cubic silver crystals respectively. Moreover, the presence of characteristic peaks corresponding to MMT nano clay (XRD Ref. No. 00-003-0010) established at 2θ of 62.1° in confirmed their stability.

 

Elaborate spectral analysis representing various functional groups resulting in the reduction and stabilization of silver nanoparticles is shown in figure 2 (a & b). The absorption peaks at 3419 cm^-1 depicts the characteristic -OH stretching of alcohols. Both the samples displayed stretching peaks around 2924 cm^-1 and 1629 cm^-1 characteristic –CH₂ of aliphatic compounds and N=O asymmetric of nitrate groups respectively³³. The spectral band observed at 1402 cm⁻¹ is due to stretching vibration of C–OH of carboxylic acids whereas, band situated at 881 cm⁻¹ corresponds to the C–H out-of-plane vibration of aromatic compounds, which indicated the presence of aromatic ring pigmented compounds (figure 2a). In addition, the bands at 1396 cm^-1 and 1388 cm^-1 attributed to C-N stretching vibrations of aliphatic and aromatic amines respectively (figure 2b). Stretching vibrations between 1200 cm^-1 to 900 cm^-1 and 900 cm^-1 to 600 cm^-1 are significant regions for structural characterization of polysaccharides³⁴.

 

The change in the shape and surface morphology of Ag nanoparticles in presence and absence of MMT was visualized by SEM images in figure 3 (a & b). The green synthesized Ag nanoparticles were cubic in shape whereas Ag nanoparticles synthesized in presence of MMT exhibited predominantly cubic shape and some were truncated and ellipsoidal in the form of agglomerates. In addition, the interaction between the clay layers and the nanoparticles was revealed where the presence of shiny white spots indicated the synthesis of Ag nanoparticles in MMT layers to give nanocomposites²³. Further, to confirm the existence of Ag nanoparticles in MMT, energy dispersive X-ray spectroscopic analysis of MMT-Ag nanocomposites was performed. As shown in figure 3(c), multiple peaks corresponding to elements C, O, Mg, Al and Si in addition to silver elements identified in the EDS spectrum established the existence of Ag nanoparticles in MMT-Ag nanocomposites^35,36.

 

Figure 3. Surface morphology of (a) Ag nanoparticles and (b) MMT-Ag nanocomposites, (c) EDX spectra of biogenic MMT-Ag nanocomposites

 

 

Bactericidal activity of MMT-Ag nanocomposites:

Antibacterial activity of MMT-Ag nanocomposites against isolated marine bacteria (MFB1 to MFB7) was studied by the inhibition zone formed around the well containing different concentrations of MMT-Ag nanocomposites. Antimicrobial effect of MMT-Ag nanocomposites was found to be highest at concentration of 100µg against all the tested bacterial isolates (Figure 4). Maximum zone of inhibition was noted against S. aureus (19.6±0.40 mm) followed by E. coli (18.3±0.45mm), M. flavus (17.5±0.46mm), Pseudomonas aeruginosa (16.1±0.47mm), B. cereus (14.6±0.47mm), M. leteus (14.1±0.49mm) and B.  subtilis (12.1±0.44mm). The maximum efficiency of MMT-Ag nanocomposites is attributed to their ability to alter bacterial cell permeability and denaturation of respiratory enzymes. In addition, inhibition of proteins synthesis by denaturing ribosome could be one of the possible mechanisms of antibacterial activity of MMT-Ag nanocomposites^37-39.

 

Anti-crustacean assay of MMT-Ag nanocomposites:

A. salina is a commonly used bioassay organism for the detection of toxic effects of nanomaterials which provides further information on their cytotoxicity towards various marine organisms. The toxicity of synthesized MMT-Ag nanocomposites towards A. salina was expressed based on LD₅₀ values. A gradual increase in cytotoxicity of synthesized MMT-Ag nanocomposites towards crustacean was recorded with an increase in concentration of nanocomposites concentration. The LD₅₀ value of MMT-Ag nanocomposites against A. salina was observed at 200±3.4µg/ml whereas complete mortality was noted at 400±6.0µg/ml after 24h of incubation.

 

Figure 4. Antibacterial activity of MMT-Ag nanocomposites against isolated marine biofilm forming bacteria (FB1–FB9)

 

In agreement with our results, few researchers have reported the cytotoxicity of marine seaweed mediated synthesized silver nanoparticles on marine crustaceans^3,41,42. Johnson et al.,⁴³ studied the lethal effects of silver nanoparticles synthesized using aqueous extracts of Dictyota bartayresiana on brine shrimp hatchability and LD50 was recorded at 196.5µl/L. Kumar et al.,⁴⁴ investigated the cytotoxicity of silver nanoparticles synthesized from Sargassum ilicifolium against A. salina and inferred that the maximum mortality rate was observed at 100nM concentration. Interestingly, the present study is the first report to evaluate the toxicity of MMT-Ag nanocomposite synthesized A. acetabularia against A. salina.

 

Biofilm inhibition assay of MMT-Ag nanocomposite-based paint:

To evaluate the long-term efficiency of MMT-Ag nanocomposites as an antifouling agent, steel panels coated with MMT-Ag nanocomposites-based paint were immersed in the natural environment. As shown in figure 5, control panel exhibited minimum water resistance and significantly fouled by marine organisms, including barnacles, algae, and unidentified larvae. Panel coated with water-based paint showed minimum water resistance and maximum resistance against fouling marine organisms whereas panel coated with MMT-Ag nanocomposite-based paint significantly inhibited the microbial growth and attachment of marine organisms in sea water owing to the release of MMT and Ag⁺ ions from the panel^45,46. 

 

Figure 5. Images of steel panel before (a to c) and after (d to f) immersion in sea water. Control panel (a and d), panel coated with MMT-Ag nanocomposite-based paint (b, c, e and f).

 

CONCLUSION:

A simple and rapid method was adopted for the biosynthesis of MMT-Ag nanocomposites using aqueous extract of marine seaweed, A. acetabulum. The biosynthesized MMT-Ag nanocomposites exhibited an excellent antibacterial activity against Gram positive and Gram-negative isolates. Furthermore, the anti-biofouling activity of MMT-Ag nanocomposite-based paint fulfills their promise as effective agents in inhibition of bacterial growth and attachment of marine organisms in sea water. The results of the current study can be further explored to develop potential broad-spectrum antimicrobial nanocomposites and in formulations of MMT-Ag nanocomposite-based paint can be further optimized to form a potential non-corrosive and less toxic remedy for marine biofouling.

 

CONFLICT OF INTEREST:

The authors have no conflicts of interest regarding this investigation.

 

ACKNOWLEDGMENT:

The authors are thankful to Karpagam Academy of Higher Education for providing laboratory facilities. We take this opportunity to thank Karunya University who helped us for the instrumental analysis

 

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Accepted on 16.04.2022           © RJPT All right reserved

Research J. Pharm. and Tech 2022; 15(12):5397-5404.