Abstract
Seaweed extracts are most studied recently for their ability to rapidly reduce metal ions than biomass such as bacteria, fungi, and plants. The reducing capacity of seaweeds depends on the presence of phytoconsitutents such as polysacchardies, phenolic compounds, proteins/enzymes, and other chelating agents. Marine seaweeds that belong to Chlorophyta, Rhodophyta, and Phaeophyta groups are reported to biosynthesize metal nanoparticles. The morphology and the stability of the nanoparticles obtained from seaweeds for biomedical and environmental applications are equivalent in most aspects to other “green” methodologies. The biosynthesis of nanoparticles using seaweeds can be scaled up to meet industrial requirements. Therefore, this review elaborates seaweeds as a better tool for the fabrication of metal nanoparticles.
1 Introduction
In the recent past, various interdisciplinary branches help to develop and fabricate nanomaterials via two approaches: top-down (reducing the size of bulk materials) and bottom-up (fabricating nanostructures in a controlled manner) (Figure 1) [1], [2], [3], [4]. Quite important to consider is the bottom-up method, which imitates several natural processes that are similar to protein synthesis, DNA replication, etc. [5]. The most classic example of a bottom-up approach involves the reduction of citrate or sodium borohydrate salts for metal nanoparticle formation [6], [7], [8], [9], [10]. However, these reactions involve the use of toxic and harsh chemicals that may have adverse environmental effects, which point to a need for nonpolluting, biocompatible, and eco-friendly nanomaterials fabricated via a “green” approach [11], [12]. Natural plants have the ability to reduce and detoxify metals by the processes of phytomining and phytoremediation, which makes them attractive candidates for the synthesis of metal nanoparticles to be used in the various fields such as applied microbiology, molecular diagnostics, drug delivery, waste water treatment, etc. [13], [14], [15], [16].
Methods in nanoparticle formation.
2 Mechanism for biosynthesizing nanoparticles
In the present scenario, there has been a growing importance toward synthesizing new nanomaterials using various routes constantly with innovative contributions [17] (Figure 2). Most significantly, the biological synthesis (well known as green synthesis) is considered as an imperative addition to synthesis nanomaterials [18], [19], [20]. This technology implies the production of nanomaterials with greater scientific interest without harming the environment (Figure 3). In this quest, the biosynthesis is nothing but the use of living organism toward the synthesis of nanomaterials. To achieve this, researchers commonly use two systems, viz., prokaryotic and eukaryotic systems. Prokaryotic organisms involve the biosynthesis of nanomaterials using microorganisms such as bacteria, archaebacteria, etc. [21], [22], [23] (Figure 4). It is a well-known fact that microorganisms have been used to remediate toxic metals because of its resistance mechanisms. This has been deliberately an inspiration to the modern synthesis of nanomaterials (such as gold, silver, oxides, etc.), either intracellular or extracellular mode [24], [25], [26]. The ability of prokaryotic organisms to reduce metal ions is well be attributed to the presence of anionic sites (such as teichoic phosphodiester groups, free carboxylic groups of the peptidoglycan layer, sugar hydroxyl groups from wall polymers, and amide groups of the peptide chains) on the cell wall [27], [28], [29], [30]. Comparatively, the synthesized nanomaterials from prokaryotic system can equally compete to those of chemical synthesis [31]. In addition to this, eukaryotic systems (such as plants, algae, diatoms, fungi, etc.) are shown to reduce inorganic metal ions to metal nanoparticles rapidly (Figure 5). The formation of nanomaterials by eukaryotic systems is principally due to the extracts containing hydroxyl, ketones, aldehydes, and certain amino acid groups [32], [33], [34], [35]. For this reason, the biosynthesis of metal nanoparticles using eukaryotic systems is now attracting the attention of researchers.
Routes for nanoparticles synthesis.
Difference between chemical and biological synthesis of nanoparticles.
Mechanism of nanoparticle synthesis using prokaryotic system.
Mechanism of nanoparticle synthesis using Eukaryotic system.
3 Seaweeds the future “nanofactories”
The marine life in general is being studied more intensively than in the past, in the hope that our increased understanding will result in a greater appreciation of seaweeds for their importance in nature and to man. Seaweeds are macroscopic, multicellular, benthic marine plants that are one of the commercially important renewable marine life resources [36]. They are the sole source of phytochemicals such as agar, carrageenan, mannitol, iodine, laminarin, furcellarin, and sodium alginate [37]. They also exhibit antimicrobial, antifungal, antiviral, and anticancer properties [38]. Currently, approximately 32,000 tonnes of wet seaweed are harvested to meet a wide range of industrial and domestic requirements worldwide. Seaweeds are classified into three main groups based on their distribution and occurrence of pigments [39], [40], [41]. Botanists refer to them as Chlorophyta (green algae), Rhodophyta (red algae), and Phaeophyta (brown algae). Both green and red algae belong to the kingdom Plantae, whereas the brown algae belong to the kingdom Chromista. The terms “macroalgae” and “seaweed” are most commonly used to refer to these organisms in the marine environment. Several studies have been published, with special emphasis on the bioactive potential of seaweeds found in extracts containing crude and purified compounds that are pharmacologically important. However, only a few of these compounds have reached the market by undergoing clinical trials. Metal nanoparticles (especially silver and gold nanoparticles) derived from seaweeds can be an appropriate alternative for nanoparticles obtained from plants (Figure 6) [42]. Hence, this review explores the interesting phenomenon that extracts from seaweeds can be used for the biosynthesis of metal nanoparticles (Figure 7).
Applications of nanoparticles from seaweeds.
Conventional methods for reducing metals using seaweeds.
4 Biosynthesis of nanoparticles using Chlorophyta (Green seaweeds)
Chlorophyta, informally called chlorophytes, resemble terrestrial plants and are grouped under the kingdom Plantae. They occur mostly in freshwater (90%) than at sea (10%) and account for more than 7000 known species. However, in this section, the biosynthesis of nanoparticles using Chlorophyta (Green seaweeds) will be discussed (Table 1).
Biosynthesis of nanoparticles using Chlorophyta (Green seaweeds).
| Seaweed name | Type | Size | Shape | Key factors | Application | Ref | ||
|---|---|---|---|---|---|---|---|---|
| Temperature | Conc. of aqueous metal solution | Capping agents | ||||||
| Ulva lactuca | Silver | 48.59 nm | Spherical | RT | 1 mm AgNO3 | Phenolic compounds, amines and aromatic rings | Photocatalytic degradation | [16] |
| Ulva lactuca | Silver | 10–30 nm | Spherical | 100°C | 1 mm AgNO3 | Phytochemicals | Antibacterial activity | [43] |
| Ulva fasciata (Delile) | Silver | 40.05 nm | Spherical | RT | 10−3m AgNO3 | Crude ethyl acetate extract | Antibacterial activity | [44] |
| Urospora spp. | Silver | 20–30 nm | Spherical | 70°C | 1 mm AgNO3 | Phytochemicals | Antibacterial activity | [45] |
| Codium capitatum | Silver | 3–44 nm | Nanocluster | RT | 1 mm AgNO3 | Proteins | – | [46] |
| Enteromorpha flexuosa | Silver | 2–32 nm | Circular | RT | 1 mm AgNO3 | – | Antimicrobial activity | [47] |
| Caulerpa scalpelliformis | Silver | – | Spherical and cubic | RT | 1 mm AgNO3 | Amino acids and proteins | Mosquitocidal assays | [48] |
| Ulva lactuca | Silver | – | Cubical | RT | 1 mm AgNO3 | Polyphenols | Malaria control | [49] |
The room temperature-mediated biosynthesis of AgNPs by Ulva lactuca has been described for the photocatalytic degradation of methyl orange dye [16]. The finding supports the use of AgNPs for degrading organic compounds and dyes under ambient temperature and visible light illumination in an eco-friendly manner. Another report elucidates that the biosynthesis of AgNPs mediated by U. lactuca shows evidence of antibacterial activity against clinical pathogens such as Staphylococcus aureus, Escherichia coli, and Pseudomonas aeruginosa [43]. Rajesh et al. [44] used a crude ethyl acetate extract of Ulva fasciata (Delile) for the biosynthesis of metallic AgNPs at ambient temperature. These nanoparticles effectively inhibited the growth of Xanthomonas campestris pv. Malvacearum, a Gram-negative bacterium that occurs in cotton plants, with a maximum inhibitory concentration of 40.00±5.77 μg/ml. The bioreduction of silver nitrate using an extract from the green seaweed Urospora spp. for antibacterial activity against S. aureus, E. coli, and P. aeruginosa was investigated by Suriya et al. [45]. Fresh and dry extracts of Codium capitatum were used in the biosynthesis of AgNPs for promising biomedical and agricultural applications [46]. AgNPs synthesized using green alga, Enteromorpha flexuosa, were evaluated for their antimicrobial activity [47]. Eco-friendly AgNPs were prepared from Caulerpa scalpelliformis and U. lactuca and evaluated for mosquitocidal activity [48], [49].
5 Biosynthesis of nanoparticles using Rhodophyta (Red seaweeds)
Rhodophyta are distinct eukaryotic algae characterized by the presence of pigments such as phycoerythrin, phycocyanin, phycobiliproteins, carotene, lutein, and zeaxanthin. Approximately 6000 species have been identified so far in which only a few are of freshwater origin. The biosynthesis of metal nanoparticles using Rhodophyta is shown in Table 2.
Biosynthesis of nanoparticles using Rhodophyta (red seaweeds).
| Seaweed name | Type | Size | Shape | Key factors | Application | Ref | ||
|---|---|---|---|---|---|---|---|---|
| Temperature | Conc. of aqueous metal solution | Capping agents | ||||||
| Acanthophora spicifera | Silver | 48 nm | Spherical | 60°C | 1 mm AgNO3 | Phenolic compounds | Antibiofilm activity | [50] |
| Gracillaria corticata | Silver | 18–46 nm | Spherical | 60°C | 1 m AgNO3 | Polyphenols and tannins | Antifungal activity | [51] |
| Gelidiella acerosa | Silver | 22 nm | Spherical | RT | 1 mm AgNO3 | Aromatic compound/alkanes/amines | Antifungal activity | [52] |
| Hypnea musciformis | Silver | 2–55.8 nm | Cubic | 28°C | – | Cyclic peptides | Photocatalytic degradation | [53] |
| Hypnea musciformis | Silver | 40–65 nm | Spherical | 1 mm AgNO3 | In situ oxidation of hydroxyl groups and by the intrinsic carbonyl groups | Larvicidal activity | [54] | |
| Galaxaura elongata | Gold | 3.8–77.1 nm | Spherical | RT | 10−3m HAuCl4 | Amino residues and peptides of proteins | Antibacterial activity | [55] |
| Pterocladiella capillacea | Silver | 11.4 nm | Spherical | RT | 10−3m HAuCl4 | Proteins | Anticancer activity | [56] |
| Corallina officinalis | Gold | 14.6 nm | Spherical | RT | 1 mm HAuCl4 | Hydroxyl and amino functional groups | Anticancer activity | [57] |
| Kappaphycus alvarezii | Cu@Cu2O-NPs | 52.99 nm | Spherical | 60°C–120°C | 0.4 g of CuSO4·5H2O | Hydrazinium hydroxide | – | [58] |
Kumar et al. [50] reported the biosynthesis of spherical AgNPs using an aqueous seaweed extract of Acanthophora spicifera that inhibited the production of exopolysaccharides by biofilm forming pathogens such as E. coli, Salmonella typhii, Shigella flexneri, S. aureus, and Vibrio cholerea. Kumar et al. [51] reported the synthesis of AgNPs by Gracilaria corticata and tested it against two Candida spp.: Candida albicans and Candida glabrata. The synthesized nanoparticles were effective against the fungal strains in deterring the growth. Vivek et al. [52] investigated the biogenic synthesis of AgNPs using the extract of red seaweed Gelidiella acerosa. The synthesized nanoparticles showed notable antifungal activity against Mucor indicus followed by Trichoderma reesei, Fusarium dimerum, and Humicola insolens. An eco-friendly method was adopted for the biosynthesis of AgNPs using seaweed Hypnea musciformis to degrade methyl orange under visible light illumination [53]. The nanoparticles fabricated using H.musciformis showed efficient larvicidal and pupicidal activity against dengue vector Aedes aegypti and the cabbage pest Plutella xylostella [54]. Galaxaura elongata extract and powder derived gold nanoparticles were effective antibacterial agents against E. coli, Klebsiella pneumoniae, MRSA, and P. aeruginosa [55]. The bactericidal and cytotoxic effect on HepG2 cancer cell line of biosynthesized AgNPs synthesized using Pterocladiella capillacea was reported by El-Kassas and Attia [56]. There is a report on the cytotoxic effect of gold nanoparticles synthesized using Corallina officinalis [57]. Cu@Cu2O core shell nanoparticles were synthesized using Kappaphycus alvarezii [58].
6 Biosynthesis of nanoparticles using Phaeophyta (Brown seaweeds)
Brown algae belong to the phylum Phaeophyta (Heterokontophyta). There are approximately 2000 known species of brown algae that dominate the marine waters out of which some are reported for the biosynthesis of nanoparticles as shown in Table 3.
Biosynthesis of nanoparticles using Phaeophyta (brown seaweeds).
| Seaweed name | Type | Size | Shape | Key factors | Application | Ref | ||
|---|---|---|---|---|---|---|---|---|
| Temperature | Conc. of aqueous metal solution | Capping agents | ||||||
| Sargassum wightii | Gold | 8–12 nm | Spherical | RT | 10−3m HAuCl4 | – | – | [59] |
| Sargassum wightii | Silver | 8–27 nm | Spherical | RT | 10−3m AgNO3 | Oxidation of alcoholic and carboxylic acid group | Antibacterial activity | [60] |
| Sargassum wightii | Silver | 15–20 nm | Spherical | 28°C | – | Polyphenols or proteins/enzymes or polysaccharide | Antibacterial activity | [61] |
| Sargassum longifolium | Silver | 30 nm | Cubical | RT | 1 mm AgNO3 | Proteins | Anticancer activity | [62] |
| Padina tetrastromatica | Silver | 20 nm | Spherical | RT | 1 mm AgNO3 | Aromatic compound or alkanes or amines | – | [63] |
| Sargassum ilicifolium | Silver | 33–44 nm | Spherical | 60°C | 1 m AgNO3 | – | Antibacterial and in vitro cytotoxicity | [64] |
| Sargassum tenerrimum | Silver | 20 nm | Spherical | 60°C | 1 mm AgNO3 | Hydroxyl/methoxy groups, ketones, polysaccharides | Antibacterial activity | [65] |
| Sargassum myriocystum | Gold | 10–23 nm | Spherical | 76°C | 1 mm HAuCl4 | Extracellular polysaccharides | – | [66] |
| Sargassum polycystum | Silver | 50–100 nm | Spherical | RT | 1 m AgNO3 | Carboxylic, amine, phosphate, and hydroxyl groups | Anticancer activity | [67] |
| Sargassum myriocystum | Zinc oxide | 76–186 nm | Spherical, triangle, radial, hexagonal, rod and rectangle | 80°C | 1 mm zinc nitrate | Alginic acid, ascorbic acid, protein, carbohydrates, flavanoids, tannins, mannitol, and lipids | Antibacterial activity | [68] |
| Turbinaria conodies | Silver | 96 nm | Spherical | RT | 1 mm AgNO3 | Polyphenols, polysaccharides, primary amines | Antimicrobial activity | [69] |
| Turbinaria conodies | Silver and gold | 2–17 nm 2–19 nm | Spherical | RT | 1 mm AgNO3 and HAuCl4 | Free hydroxyl and carboxylic acid groups | Antimicrofouling activity | [70] |
| Stoemchospermum marginatum | Gold | 18.7–93.7 nm | Mostly spherical occasionally triangular and rarely hexagonal | RT | 1 mm HAuCl4 | Terpenoids, polyphenols and phenolic compounds | Antibacterial activity | [71] |
| Cystophora moniliformis | Silver | 75 nm | Spherical | 45–95°C | 1 mm AgNO3 | – | – | [72] |
| Padina gymnospora | Silver | 25–40 nm | Spherical | 30°C | 0.004 m of AgNO3 | – | Antibacterial activity | [73] |
| Padina gymnospora | Platinum | 35 nm | Spherical | 50°C | 0.001 m of H2PtCl6 | Sulfated polysaccharide | Hemolytic assay | [74] |
| Padina gymnospora | Gold | 53 nm | Spherical | 75°C | 10−3m HAuCl4 | Fucoxanthin or flavonoids | Anticancer activity | [75] |
| Sargassum muticum | Magnetic Iron-oxide | 18 nm | Cubic | 25°C | – | Sulfated polysaccharides, hydroxyl, and aldehyde groups | – | [76] |
| Sargassum muticum | Magnetic iron-oxide | – | – | – | – | – | Anticancer activity | [77] |
| Sargassum muticum | Zinc oxide | 30–57 nm | Hexagonal wurtzite | 450°C | ZnO | Sulfated polysaccharides | – | [78] |
| Sargassum muticum | Silver | 43–79 nm | Spherical | RT | 1 mm AgNO3 | Sulfate or hydroxyl groups | Antibacterial and insecticidal activity | [79] |
| Sargassum muticum | Gold | 5.42 nm | Spherical | 45°C | 0.1 m HAuCl4 | Fucoxanthin or polysaccharides, polyphenol, and other biomolecules | Anticancer activity | [80], [81] |
| Sargassum cinereum | Silver | 45–75 nm | – | RT | 1 mm AgNO3 | – | Antibacterial activity | [82] |
| Sargassum swartzii | Silver | 35 nm | Spherical and hexagonal | 60°C | 1 mm HAuCl4 | Alcohol, carboxylic and amide I group | Anticancer activity | [83] |
| Sargassum plagiophyllum | Silver chloride | – | Spherical | RT | 1 mm AgNO3 | Alcoholic/carboxylic groups | Antibacterial activity | [84] |
In 2007, Singaravelu et al. [59] described an extracellular synthesis of monodispersed gold nanoparticles using Sargassum wightii. Govindaraju et al. [60] reported the extracellular synthesis of silver nanoparticles (AgNPs) using S. wightii for their antibacterial activity against Gram-positive S. aureus and B. rhizoids and Gram-negative E. coli and P. aeruginosa. In yet another study, AgNPs were synthesized using S. wightii, and their antibacterial activity was tested against human pathogens such as S. aureus, K. pneumoniae, and S. typhii [61]. Sargassum longifolium was used for the synthesis of AgNPs, which were tested against Human laryngeal Hep-2 cancer cell lines at different concentrations that resulted in a dose-dependent response [62]. Crude extract of Padina tetrastromatica was used for room temperature assisted synthesis of AgNPs within 72 h of incubation [63]. Kumar et al. [64] demonstrated the biological synthesis of AgNPs using the aqueous extract of Sargassum ilicifolium, which inhibited the growth of five prominent pathogenic strains such as E. coli, K. pneumoniae, S. typhii, S. aureus, and Vibrio cholerae. Nine pathogenic bacteria were treated with AgNPs synthesized using aqueous extract of Sargassum tenerrimum, which proved that AgNPs were effective compared with methanolic and aqueous extract of the seaweed [65].
Biofunctionalized gold nanoparticles were synthesized using Sargassum myriocystum with 1-cyclopentyl-4 (3-cyclopentylpropyl) dodecane as possible capping agent [66]. The crude methanolic extract of Sargassum polycystum was also used for the preparation of AgNPs by Thangaraju et al. [67]. Zinc oxide nanoparticles with antibacterial activity were synthesized using S. myriocystum with fucoidan as possible reducing and stabilizing agent [68]. The synthesized nanoparticles showed antibacterial activity against human pathogens and exhibited cytotoxic effect against MCF-7 breast cancer cell lines. The synthesis of gold nanoparticles mediated by Turbinaria conoides was reported as a single-step process [69]. Silver and gold nanoparticles synthesized using the aqueous extract of Turbinaria conodies displayed antibiofilm activity against marine biofilm forming bacteria [70].
Gold nanoparticles synthesized using Stoechospermum marginatum biomass showed an effective antibacterial activity [71]. Prasad et al. [72] reported the biosynthesis of AgNPs using an Australian marine brown alga Cystophora moniliformis. The biosynthesis of AgNPs mediated by Padina gymnospora was investigated by Shiny et al. [73]. Platinum-based nanoparticles synthesized using P. gymnospora were capable of oxidizing NADH to NAD(+) and possessed hemolytic assay [74]. The synthesized nanoparticles were effective in antibacterial activity against Bacillus cereus and E. coli. A facile green method was used for the biosynthesis of gold nanoparticles using P. gymnospora [75]. In yet another study, gold nanoparticles was fabricated using P. gymnospora was reported to show cytotoxic effects with cellular stress in liver (HepG2) and lung (A549) cancerous cell line [85].
Magnetic iron-oxide nanoparticles were biosynthesized using Sargassum muticum [76]. In a similar study, magnetic iron-oxide nanoparticles fabricated using the same species exhibited cytotoxic effects and induced cell cycle arrest against leukemia (Jurkat cells), breast (MCF-7 cells), cervical (HeLa cells), and liver (HepG2 cells) cancer cell lines [77]. Zinc oxide nanoparticles were also synthesized using the same seaweed species [78]. AgNPs fabricated using S. muticum possessed mosquitocidal activity [79]. Gold nanoparticles synthesized using S. muticum exhibited cytotoxic activity and induced apoptosis in leukemia cancer cell lines [80]. These nanoparticles were stabilized and subsequently capped by the presence of sulfated polysaccharides and/or hydroxyl group present in S. muticum.
Sargassum cinereum derived AgNPs showed promising antimicrobial activity against pathogens such as Enterobacter aerogenes, S. typhi, and Proteus vulgaris [81]. Gold nanoparticles synthesized using Sargassum swartzii is reported to be cytotoxic to cervical carcinoma (HeLa) cells [82]. Antibacterial silver chloride nanoparticles were prepared using marine alga Sargassum plagiophyllum [83].
7 Conclusion
To conclude this review, seaweeds are nutritionally rich food materials that can be used for the biosynthesis of metal nanoparticles. The possible reducing agents such as polysaccharides, polyphenols, proteins/enzymes, and other chelating agents play a vital in the formation of nanoparticles. However, the methods for achieving desirable size, shape, stability, and controlled crystal growth structure also require further investigations. Moreover, the biological nanoparticles from seaweeds can be scaled up to satisfy the increasing demands of drugs in the future.
About the authors
Kumar Ponnuchamy completed his PhD at Bharathidasan University, India, in 2015. Later, he joined Alagappa University, India, in 2016 as an assistant professor at the Department of Animal Health Management. His area of research pertains in developing nontoxic anticancer drugs from small molecules/nanomaterials for targeted applications. He has more than 15 international peer-reviewed publications.
Joe Antony Jacob is a PhD holder in Environmental Biotechnology at the Bharathidasan University, India. He has a biotechnology background in his bachelor’s and master’s degree at Periyar and Bharathiar Universities, India. He has 11 international peer-reviewed publications.
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