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Algae-based green AgNPs, AuNPs, and FeNPs as potential nanoremediators

  • Fernanda Maria Policarpo Tonelli EMAIL logo , Christopher Santos Silva , Vinicius Marx Silva Delgado and Flávia Cristina Policarpo Tonelli
Published/Copyright: May 19, 2023
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Abstract

This review addresses green algae-based gold (Au), iron (Fe), and silver (Ag) nanoparticles (NPs) as eco-friendly nanomaterials to deal with biological, organic, and inorganic environmental contaminants. Among nanotechnological tools that can fully degrade, adsorb, and/or convert pollutants into less harmful structures, AgNPs, AuNPs, and FeNPs deserve highlight for their efficiency and low cost. However, green protocols are preferable to produce them in an eco-friendly manner. Although phycosynthesis is still in its infancy, algae present various advantages as green raw materials to NPs’ synthesis; fast growth rate, low-energy input requirement, low costs, easy and eco-friendly cultivation, and high tolerance to metals are examples. To allow their large-scale application, however, challenges regarding obtaining sufficient biomaterial with good reproducibility, designing protocols to achieve desirable features on NPs, and recovering the biocompatible nanomaterial after use still need attention. Perspectives for the field involve surpassing these limitations, broadening knowledge on synthesis mechanisms, protocols, and new species useful to offer, in the future, commercial eco-friendly, and low-cost phycosynthesized AuNPs, AgNPs, and FeNPs to nanoremediation. The potential of these NPs to deal with environmental contaminants, their advantageous characteristics and biocompatibility, the main limitations associated with their large-scale application, and future prospects for the field will receive attention.

1 Introduction

Environmental pollution is a worldwide threat mainly as a consequence of human beings’ actions seeking development through rapid industrialization [1,2] but not taking into consideration sustainability principles. Pollutants are diversified when it comes to their chemical nature: organic molecules (e.g., dyes and herbicides), inorganic substances (e.g., heavy metals), and pathogenic living beings (e.g., methicillin-resistant Staphylococcus aureus). All of them can contaminate soil, water, and air, causing damage to humans that can range from acute intoxication to death [3].

The most harmful pollutants are the persistent ones that can last for a long time in polluted areas, accumulating and causing extensive damage to the environment, resulting in premature deaths [4,5,6]. These persistent pollutants can be, for example, heavy metals. They can intoxicate victims even at low concentrations and without the necessity of direct contact as they can bioaccumulate through the food chain [7,8,9].

Among human activities that largely contribute to environmental pollution are the ones related to the textile industry. This type of industry uses a wide array of dyes that are present in the produced wastewater. If this wastewater is not treated before being released into rivers, for example, it can end up contaminating them with substances such as methylene blue and rhodamine B [10,11].

Some agencies that have the mission of protecting the environment have set values for substances that are considered pollutants to be below the set values when present in water, air, and/or soil. This strategy facilitates surveillance and contributes to the reduction of pollution released into the environment [12,13]. However, dealing with the pollution already present in polluted areas is also urgent. It is necessary to deal with environmental contamination efficiently by restoring polluted areas and remediating pollution. In this sense, the nanotechnology field offers interesting solutions.

Among these solutions are metallic algae-based nanoparticles (NPs) containing gold, iron, or silver atoms. These nanostructures can deal with pollutants of diverse chemical nature, promoting their elimination, adsorption, and/or conversion into less harmful forms [12]. Table 1 presents recent examples of these NPs acting over environmental contaminants aiming to attenuate their harmfulness. The biological contaminant S. aureus, for example, is associated with causing waterborne disease symptoms when present in polluted water [14]. However, silver nanoparticles (AgNPs) produced using the material from the marine macroalgae Padina sp. [15], iron nanoparticles (FeNPs) synthesized using the aqueous extract of U. lactuca [16], and AgNPs and gold nanoparticles (AuNPs) produced from the extract of Chlorella vulgaris presented antibacterial effect and could efficiently fight this pathogen; it is interesting to highlight that these AgNPs produced from the extract C. vulgaris presented minimum bactericidal concentration equal to the one from chloramphenicol (5%) against E. coli and higher efficiency than the antibiotic to eliminate Streptococcus species’ cells [17]. When it comes to organic substances that are considered environmental contaminants, malachite green is a carcinogenic, genotoxic, mutagenic dye largely present in industrial effluents, negatively affecting not only human beings but also the flora [18]. At a concentration of 5 × 10−5 mol‧L−1, the pollutant diminished the germination index (GI) of Triticum aestivum seedlings from 100% (in clean water) to only (16.39%). However, after treating the polluted water with AgNPs synthesized using microalgae Anabaena variabilis, the GI increased to 74.65%; after the treatment with the AgNPs from Spirulina platensis, the GI reached 89.26%. Therefore, the NPs, by promoting dye adsorption, caused the reduction of water samples’ toxicity to the vegetal species in an efficient manner [19]. Crystal violet is another example of a toxic dye that pollutes ecosystems and endangers living beings [20]. However, FeNPs produced using the extract from Spirulina sp. offered an efficient dye removal (through adsorption) of 93.13% at 35°C after 100 min of exposure [21]. AuNPs produced using the extract of Sargassum horneri exhibited catalytic activity to promote the reduction of three highly toxic dyes [22]: methylene blue, methyl orange, and rhodamine B. The nanomaterial optimized the transfer of electrons from the donor to the acceptor structures, offering colorless samples after 6, 17, and 4 min, respectively [23]. Regarding inorganic contaminants, heavy metal lead (Pb) can intoxicate living beings and is a carcinogenic pollutant [24]. After the exposure, for 48 h, of a pharmaceutical effluent containing the metal to AuNPs produced using Nannochloropsis sp., the amount of the pollutant free in the sample reduced to 66.53%; when AgNPs produced using the same raw material were used, 68.86% of reduction was observed. The NPs exhibited a good adsorbent affinity for promoting the nanoremediation of wastewater [25]. Considering the heavy metal chromium, its more stable forms are trivalent (Cr3+) and hexavalent (Cr6+) forms; however, the latter is 100 times more toxic than Cr3+ and integrates group I of human carcinogen agents from the International Agency for Research on Cancer due to the high risk it offers to humans’ health [26]. FeNPs produced using the extract from Chlorococcum sp. MM11 exhibited a potential superior to the one from bulk iron to convert Cr6+ to Cr3+, which contributed to a reduction in the harmfulness of inorganic pollutants [27]. AuNPs, AgNPs, and FeNPs dealing with different types of environmental contaminants will be explored in detail in Section 3.

Table 1

Recent examples of green AgNPs, AuNPs, and FeNPs synthesized from algae materials to deal with environmental pollutants

Nanoparticles Algae material used in the green synthesis protocol Pollutant(s) remediated Reference
Silver nanoparticles Padina sp. S. aureus and Pseudomonas aeruginosa [15]
C. vulgaris Escherichia coli, Streptococcus sp., S. aureus and its methicillin-resistant strain [17]
Spirulina platensis Malachite green [19]
Anabaena variabilis Malachite green [19]
Nannochloropsis sp. Pb, Zn [25]
C. vulgaris Pb, Zn [25]
Caulerpa serrulata E. coli, P. aeruginosa, Salmonella typhi, Shigella sp. and S. aureus [77]
Congo red
Chlorella ellipsoidea Methyl orange and methylene blue [115]
Caulerpa racemosa Methylene blue [116]
Proteus mirabilis and S. aureus [130]
Sargassum myriocystum E. coli, S. aureus, Staphylococcus epidermidis, Proteus vulgaris, Klebsiella pneumonia, and P. aeruginosa [117]
Methylene blue
Sargassum serratifolium Methyl orange, methylene blue, and rhodamine B [118]
Ulva flexuosa P. aeruginosa, E. coli, S. aureus, and Bacillus subtilis [141]
Gelidium amansii Aeromonas hydrophila, E. coli, Vibrio parahaemolyticus, P. aeruginosa, Bacillus pumilus, and S. aureus [142]
Gelidiella acerosa Fusarium dimerum, Humicola insolens, Trichoderma reesei, and Mucor indicus [143]
Coelastrella aeroterrestrica BA_Chlo4 S. aureus, Streptococcus pyogenes, B. subtilis, E. coli, and P. aeruginosa [144]
Enteromorpha intestinalis Candida albicans, Candida krusei, Candida tropicalis, E. coli, S. typhi, S. aureus, and Vibrio cholera [145]
Portieria hornemannii Fish pathogenic bacteria [146]
FeNPs Ulva lactuca E. coli, S. typhimurium, Bacillus cereus, P. vulgaris, and S. aureus [16]
Spirulina sp. Crystal violet [21]
Chlorococcum sp. MM11 Cr6+ [27]
Padina pavonica Compounds containing nitrogen and phosphorus [119]
Colpomenia sinuosa
Harmful algae species
Petalonia fascia
S. platensis Crystal violet and methyl orange [120]
Sargassum acinarium Pb [122]
P. pavonica
Algae from the lichen Ramalina sinensis Cd, Pb [123]
C. sinuosa B. subtilis, E. coli, P. aeruginosa, S. typhi, S. aureus, V. cholera, Fusarium oxysporum, and Aspergillus flavus [148]
Pterocladia capillacea
Sargassum vulgare Biofilm forming bacteria [149]
Jania rubens
Ulva fasciata
Algae from the lichen R. sinensis S. aureus and P. aeruginosa [150]
Chlorella K01 Fusarium moniliforme, Fusarium oxysporum, Fusarium tricinctum, Pythium sp., and Rhizoctonia solani [151]
Gold nanoparticles C. vulgaris E. coli, S. aureus including its methicillin-resistant strain and Streptococcus sp. [17]
Sargassum horneri Methylene blue, methyl orange, and rhodamine B [23]
Nannochloropsis sp. Pb, Zn [25]
C. vulgaris
Sargassum tenerrimum 4-Nitrophenol and p-nitroaniline [121]
Turbinaria conoides
Galaxaura elongata E. coli, Klebsiella pneumoniae, S. aureus and its methicillin-resistant strain, and P. aeruginosa [151]
Ecklonia cava Aspergillus brasiliensis, Aspergillus fumigates, Aspergillus niger, B. subtilis, C. albicans, E. coli, P. aeruginosa, and S. aureus [152]

2 Nanoremediation of environmental pollution

In order to manage environmental contaminants, it is necessary not only to diminish contaminants production [28] and release into the environment but also to remove pollutants from polluted areas, degrade them, adsorb them into a material that can be recovered, or convert them into forms that are less harmful or do no harm to living beings. Among the solutions developed to perform these roles are nanomaterials: nanoscale materials that present unique features that allow them to perform desirable tasks, such as the ones mentioned, in an efficient way [12].

Nanomaterials present at least one dimension in the size range of 1–100 nm, and the most interesting fact associated with them is the difference in properties presented when comparing the material in its bulk size with it in nanosize. Unique properties such as the ability to promote catalysis, act as a conductor, and serve as a delivery vehicle, for example, arise and allow the nanotechnology field to offer interesting and elegant alternatives to relevant problems that humanity faces nowadays [3].

When it comes to nanoremediation, metallic NPs deserve to be mentioned because they can be produced through rapid, low cost and simple protocols, they present high reactivity and also stability, and possess interesting properties such as physicochemical, plasmonic, and photothermal ones, acting as catalysts efficiently (due to the maximization of metal catalyst’s exposure on the surface area) [29].

It is possible to apply different chemical and physical methods to synthesize metallic NPs. However, these protocols commonly involve the use of harmful chemicals (that can contribute to causing even more pollution) and require a lot of energy during the process, offering a non-satisfactory conversion yield, which results in an expensive and non-eco-friendly process [30].

In an attempt to avoid further damage to the environment due to the synthesis of nanoremediators, green synthesis protocols have been receiving increasing attention.

2.1 Green NPs in nanoremediation

NPs can be produced using protocols of physical, chemical, or biological synthesis [31,32]. Among the applied physical methods are microwave irradiation [33], laser ablation [34], and evaporation–condensation [35]. Among chemical ones, it is possible to highlight chemical vapor deposition [36] and thermal decomposition [37].

However, chemical and physical protocols commonly require the use of expensive pieces of equipment or harmful reagents to perform the synthesis. The necessity of special and expensive pieces of equipment can make it non-viable or difficult to obtain the nanomaterial and the harmful reagents are undesirable due to the risk they pose to manipulators and also to the environment [30].

Therefore, in order to obtain the NPs in an eco-friendly way and at low costs, biological protocols are interesting alternatives. The biological raw materials to be used in green synthesis protocols may be obtained from different sources such as plants, algae, fungi, lichens, bacteria, and viruses [38]. By applying this type of protocol, it is possible to synthesize the NPs and other materials on the nanoscale in a sustainable manner.

Regarding classifying the type of synthesis strategy considering what is necessary to go from starting material size to the size of NPs, there are bottom-up and top-down approaches (Figure 1). The bottom-up synthesis starts from smaller structures to construct larger ones. It can use a salt containing metal ions as a starting material and promotes its reduction from cations to synthesize the NPs; chemical vapor deposition and condensation are examples of this kind of approach [39]. The top-down synthesis, on the other hand, uses a larger material and reduces it to achieve the desired nanoscale; electro-explosion and laser ablation are examples of this type of synthetic approach that can use nanowires as the starting material [40,41].

Figure 1 
                  Nanomaterials as nanoremediators of environmental pollution.
Figure 1

Nanomaterials as nanoremediators of environmental pollution.

The bottom-up approach, which applies salt containing the metal of interest, requires reducing agents to produce the NPs due to the conversion of ions (cations) into a neutral metal form. After the reduction, clusters of the metal can be formed, and stabilizing agents are commonly added at this stage to avoid undesirable agglomeration. Stabilizing agents can be substances such as starch, polyvinyl pyrrolidone, and sodium carboxyl methyl cellulose [42]. Ascorbic acid, hydrazine, and sodium borohydride are examples of reducing agents that are commonly applied in chemical protocols of synthesis [43]. However, some of these chemicals used as reducing agents are a threat to the health of living beings and the ecosystem as a whole. Hydrazine, for example, presents good water solubility but due to its explosibility and extreme toxicity, it is a harmful reagent that can damage the lungs, liver, and nervous system, and cause death in humans [44]. In green synthesis, most commonly, the bottom-up approach is used to obtain metallic NPs; however, reducing and stabilizing agents are not required as they are provided by the biological raw material.

Different types of green NPs have already been produced aiming to deal with pollutants to restore polluted samples through nanoremediation. For example, soil pollution caused by heavy metals such as Cr6+ could be remediated by bentonite-supported zero-valent iron (nZVI) synthesized using green tea [45]; the nanomaterial promoted the adsorption of chromium. Ni2+, contaminating the soil, could be adsorbed by Fe3O4 NPs, produced using olive oil [46]. Sandy soil polluted by ibuprofen was restored by nZVI (produced using extracts obtained from bleach tea, grape marc, and vine leaves) that promoted the drug’s reduction [47]. The adsorption of this drug from wastewater could be performed by FeNPs, produced using black tea. Regarding surface water, contamination caused by bacteria capable of producing biofilm could be remediated by green TiO2 NPs, produced using bio-based material derived from Bacillus subtilis [48]. In the case of groundwater, Fe/Pd NPs synthesized using green tea extract could promote the reduction of the pollutant trichloroethylene, remediating this contamination [49]; this extract could also be used to produce Fe/Cu NPs capable of performing catalytic reduction of Cr6+ [50]. Wastewater polluted by the inorganic contaminant Cr6+ could be remediated by FeNPs, which promoted the heavy metal’s adsorption, produced using three plant extracts [51]. The organic dye methylene blue could be degraded by AgNPs, produced using the extract from Terminalia chebula [52] and by carbon dots produced from the extract of Musk melon [53]; the dye could also be adsorbed by Fe3O4 synthesized using the extract obtained from potato [54]. PbNPs produced using Cocos nucifera could degrade the pollutant malachite green [55]. nZVI contained in porous carbon could be synthesized using pinewood sawdust to remediate polychlorinated biphenyl from aqueous samples [56]. The organic contaminant 4-nitrophenol could be degraded from contaminated wastewater by AgNPs (produced using Terminalia bellirica) [57]. Adsorption of dye orange II from contaminated samples could be performed by Fe/Pd NPs, produced using the aqueous extract of grape leaves [58].

2.1.1 Algae as a raw material to produce green NPs, presenting the potential to deal with environmental pollutants

The interest in studying algae has been increasing, mainly due to the usefulness of the material that can be obtained from them to produce biofuel. As the demand for energy increases at a fast pace and fossil fuels continue to damage the ecosystems due to the emission of pollutants, sustainable energy sources, consequently, receive more attention [59]. Among these, algae deserve attention, as it does not require arable lands to be planted to be obtained in large amounts. Therefore, food crops need not be eliminated for the production of the raw material for biofuel, which is desirable as the growing population increases the demand for food [60]. Algae biomass, in fact, besides allowing low-cost and eco-friendly production of biofuel without requiring occupying arable lands, presents other advantages when compared to plants. Algae produce a higher useful lipid content to produce fuels and a superior rate of desirable molecules [59,60,61].

However, algae also produce chemicals that can act as stabilizing and reducing agents in the synthesis of green NPs when they are used in an eco-friendly protocol (phycosynthesis). These NPs may present the potential of dealing with environmental contaminants, such as removing, degrading, or converting them into less toxic or non-toxic forms, thereby promoting nanoremediation. These organisms are advantageous raw materials as they can be easily obtained in large amounts and in a simple way at low costs to offer sustainable NPs production [62,63]. Not only live organisms but also dead ones and dry biomass can be used to synthesize these materials on the nanoscale [64].

In fact, when compared to other bio-based raw materials that are used in the synthesis of green NPs, algae show not only the previously mentioned advantages (being easy to obtain on a large scale in a simple and cost-effective way), but also show fast growth rate, require low-energy input to be proliferated once they can perform photosynthesis, and can be kept in an aquaculture system that, aiming to deal with pollution, can be easily coupled with another system that collects wastewater for treatment. These organisms are a renewable energy source, and, as photosynthesizers, their cultivation can also contribute to reducing greenhouse gas emissions and accumulation in the atmosphere [65]. Besides, various algae species present a natural tendency to tolerate exposure to metals (by producing, e.g., chelating agents that can collaborate with NPs’ stabilization), including heavy metals, tolerating well the synthesis conditions of metallic NPs. These organisms are already largely explored in industrial processes to efficiently produce cosmetics, fertilizers, food, and pharmaceuticals, for example. This is a consequence of how rich algae-based material is in biomolecules and secondary metabolites, which are useful substances to produce various products, including NPs [66,67,68,69,70,71].

The word algae refers to a large diversity of organisms; in fact, to a polyphyletic group. These organisms are photosynthesizers and eukaryotes that can be divided into macroalgae and microalgae. Macroalgae comprise organisms that are macroscopic and multicellular, grow rapidly, and produce photosynthetic pigment; the pigment’s color allows the division of these organisms into brown, green, or red algae groups [72,73,74]. Microalgae, on the other hand, involves unicellular microorganisms that are photoautotrophic and can form colonies or live individually in different habitats [75].

To produce metallic NPs using algae material, one can adopt approaches that involve intracellular or extracellular protocols (Figure 2). In the intracellular methods, components from cells’ interior such as NADPH and pigments take part in the metal’s reduction [76]. This type of synthesis may involve (1) the cellular extract (obtained after the lysis of cells from organisms in a logarithmic growth phase) being exposed to the solution containing metallic salts [77] or (2) the exposition of living organisms (incubated under optimum conditions) to this solution [78]. The latter approach takes advantage of a common characteristic of living algae to promote the internalization and hyperaccumulation of metals, especially heavy metals [79]. The extracellular protocol involves the use of the filtrate obtained from the algae culture after centrifugation and filtration to remove cells. In this case, the cell membrane is not disrupted and the reducing agents are exuded substances.

Figure 2 
                     Approaches of NPs’ synthesis using algae-based materials and phases involved in the process.
Figure 2

Approaches of NPs’ synthesis using algae-based materials and phases involved in the process.

The process of the formation of metallic NPs involves three phases: (1) the reduction of metal ion and nucleation; (2) the growing of NPs with deposition of the reduced metal; and (3) the termination phase in which the final shape of NPs is defined (capping and stabilizing agents participate in this stage). The final morphology, size, and tendency to agglomeration exhibited by NPs suffer influence from various parameters such as the initial metal ion concentration, metal/algae-based material ratio, stirring features, pH, temperature, and the time of reaction [80,81].

Although microalgae are excellent precursors for NPs’ biosynthesis, there are still challenging aspects that need to be addressed to allow efficient, cost-effective, and large-scale applicability. Obtaining the raw algae material, the synthesis protocol, and obtaining NPs and/or the use of the NPs themselves still require further research efforts, as discussed in Section 4.

Phyconanotechnology is still little explored when compared to the use of fungi, bacteria, and plants to produce bioactive green nanomaterials [80]. However, it is a field that is receiving increasing attention from scientists who aim to develop nanoscale materials in a sustainable, easy, low-cost, and large-scale manner [82]. The majority of examples present in the literature address the potential of algae-based NPs containing metal atoms to deal with biological contaminants (such as pathogenic algae, bacteria, and fungi). The extracts obtained from red macroalgae species Corallina mediterranea and Corallina officinalis using water, for example, were used in the synthesis of CuNPs that could fight the biological contaminant Lyngbya majuscula (a harmful alga) [83]. The brown macroalgae species Sargassum muticum allowed the synthesis of green ZnO and CuO NPs that could remove the ability to synthesize biofilm and adhere to the surface from biological contaminants S. aureus, Pseudomonas aeruginosa, and Proteus mirabilis [84]. E. coli present in contaminated water could be eliminated by CuO NPs produced using the microalgae extract of Anabaena cylindrica [85]. Nonetheless, there are also studies involving green algae-based NPs dealing with environmental contaminants such as heavy metals (inorganic), hydrocarbons (organic), and dyes (organic). The extract from the brown macroalgae species Sargassum vulgare could be used to synthesize ZnO NPs capable of promoting photocatalysis aiming to promote decolorization of the dye methylene blue [86]. Microalgae such as Dunaliella tertiolecta and C. vulgaris could be successfully used to synthesize ZnO NPs capable of dealing with pollution caused by hydrocarbons in water samples. Paraffin hydrocarbons could undergo photocatalysis to promote the removal of contaminants at a rate of 100% when the initial concentration of the pollutant was 0.05% [87]. Living Chlamydomonas reinhardtii eliminated the pollution caused by Cu2+ in aqueous media by using the pollutant to synthesize green copper NPs [88]. The extract from microalgae belonging to the Chlorella genus produced ZnO NPs capable of promoting photocatalytic degradation of the organosulfur pollutant dibenzothiophene, a polycyclic aromatic hydrocarbon; the contaminant’s photo-desulfurization was efficiently performed by the nanomaterial [89].

Different types of metallic green NPs can be produced using algae-based raw materials. The examples previously presented involved oxides containing atoms from the metals zinc and copper. However, other diverse metals, alone or as oxides, can be exposed to the algae material in green protocols, allowing the production of eco-friendly metallic NPs. In fact, in the last two decades, the most phycosynthesized NPs were the AgNPs followed by gold NPs [82]. AgNPs and AuNPs draw attention, especially due to their antimicrobial potential as discussed later in Section 2.1.2, but there are also studies evidencing their photocatalytic potential and ability to adsorb pollutants. In this way, this review will dedicate attention to these NPs as tools, presenting the potential to deal with contaminants aiming for environmental restoration. Other types of metallic NPs will also receive attention: the ones containing iron due to their catalytic potential and the fact that there are iron oxide NPs that present magnetic properties. As the main focus of this review is the potential of Au, Ag, and Fe algae-based metallic NPs to deal with environmental pollutants, magnetic properties would be interesting to favor the recovery after use in a possible water treatment tank, for example.

2.1.2 Advantageous characteristics of AuNPs, FeNPs, and AgNPs to perform nanoremediation

FeNPs present various important applications in sensors, in the medical field (e.g., as nanocarriers) and as catalysts [90]. In fact, FeNPs is a term that refers to a group of nanomaterials and includes metallic, bimetallic, and oxides, among other structures. The different compositions result in different interesting features of the nanomaterial but some of them are common to all FeNPs, such as high reactivity and large surface area [91]. These characteristics allow the efficient catalysis promoted by these NPs that can convert environmental contaminants into less toxic structures or structures that are no longer toxic. However, these nanostructures can also promote the adsorption of some contaminants, after functionalization or even in a way independent of chemical surface modification, better than some traditional adsorbents suitable for this function [92,93].

Among FeNPs relevant to nanoremediation, Fe3O4 and zero-valent FeNPs stand out [90]. Fe3O4 (also known as magnetite) NPs are biocompatible particles in nanoscale [94] that also display magnetism, as a useful characteristic. Biocompatibility allows the successful association of remediation strategies using this nanomaterial with bioremediation using living organisms [95]. In the case of magnetism, it allows the use of magnetic separators, for example, to efficiently recover the nanomaterial after pollutant degradation or with the contaminant adsorbed to it [92,96]. nZVI can be synthesized at a lower cost when compared to magnetite, can efficiently absorb pollutants such as heavy metals [97,98], and presents a strong redox potential that can contribute, for example, to degrade dyes [99].

In the case of AgNPs, interesting features related to exploring their potential in remediation are silver’s ability to eliminate microorganisms (antimicrobial activity), their chemical stability, conductivity, and also their catalytic properties [100,101,102]. Regarding biological contaminants, AgNPs can eliminate and inhibit adhesion, or inhibit the growth of pathogenic bacteria, yeast, and fungi species, proving to be useful to restore areas polluted by these organisms [103,104,105]. AgNP, as a nanocatalyst, synthesized through simple protocols and at low costs, can increase the velocity of chemical reactions converting toxic pollutants into less harmful molecules or molecules that pose no harm to living beings [106,107]. However, the nanomaterial is also useful in pollutant detection promoted by sensors containing the NPs [108,109].

Regarding AuNPs, they are largely applied in the medical field due to interesting features such as unique localized surface plasmon resonance properties that favor their application in phototherapy and biosensors, for example [110,111]. Adjustments in synthesis protocols allow the production of AuNPs with a desirable size and geometric shape, which can influence the color they exhibit and their biocompatibility and electrical properties. Gold NPs are especially useful not only in imaging/diagnosis but also in medical treatments [108]. Functionalization can be performed in a simple manner allowing the nanostructure to support large loading amounts to perform delivery efficiently. However, when it comes to dealing with environmental contaminants, AuNPs are also catalytic nanomaterials, with good stability and biocompatibility. These NPs also present antimicrobial properties, especially after irradiation, which favors induction on the production of reactive oxygen species to eliminate microorganisms [110,112]. Gold’s antimicrobial properties have been studied systematically since the late nineteenth century when Robert Koch demonstrated the ability of K[Au(CN)2] to fight Mycobacterium tuberculosis [113]. In fact, since ancient times, gold and silver have been used in the medical field due to interesting properties such as antimicrobial ones [114].

3 The potential of gold, iron, and silver algae-based NPs to deal with environmental pollution

Phycosynthesis (the synthesis based on the algae raw material) of NPs can offer eco-friendly nanomaterials of different chemical nature that can be used to deal with environmental pollutants. As presented in Table 1, a considerable diversity of recent green protocols are available to synthesize AuNPs, FeNPs, and AgNPs from the algae material aiming to remediate pollution. The following subsections will present examples of the use of these NPs to deal with organic molecules, inorganic structures, and living organisms that can be considered, respectively, organic, inorganic, and biological environmental contaminants.

3.1 Gold, iron, and silver algae-based NPs dealing with organic contaminants

Silver NPs have been already produced from blue-green microalgae (also known as cyanobacteria). S. platensis and A. variabilis were used in the production of AgNPs capable of remediating the pollution caused by the toxic dye malachite green. The green nanomaterial acted as a bio-sorbent removing more than 80% of the pollutant from aqueous samples [19]. Green AgNPs could also be produced using the dried biomass of the microalga Chlorella ellipsoidea. The nanomaterial could be reused even after three cycles of reduction and was proved to be able to remove the pollution caused by the dyes methyl orange and methylene blue [115]. Green algae from Caulerpa racemosa sp. were used in the synthesis of eco-friendly and stable AgNPs capable of promoting the degradation of the organic dye methylene blue [116]. The aqueous extract obtained from the green macroalgae Caulerpa serrulata was used in the green synthesis of AgNPs capable of dealing with the organic dye Congo red, promoting its reduction [77]. Sargassum myriocystum (brown macroalgae) was used in the synthesis of AgNPs exhibiting photocatalytic activity to deal with the organic pollutant methylene blue [117]. Another brown macroalgae species, Sargassum serratifolium, could also be used to synthesize AgNPs to deal with pollution caused by organic dyes methyl orange, methylene blue, and rhodamine B [118].

Regarding FeNPs, the species of brown macroalgae Padina pavonica, Colpomenia sinuosa, and Petalonia fascia could be used to synthesize green Fe3O4-NPs capable of remediating wastewater by reducing nitrogen and phosphorus-containing compounds [119]. Blue-green microalgae from the Spirulina genus were used in the synthesis of eco-friendly iron oxide NPs that proved to be able to promote the decolorization of crystal violet (a cationic dye) by acting as an adsorbent [21]. In fact, S. platensis also proved to be useful in generating iron oxide NPs that could handle not only the pollution caused by the crystal violet but also the pollution caused by the anionic dye methyl orange [120].

Gold NPs synthesized using the extract from the brown marine algae S. horneri promoted efficient reduction of organic dyes (methyl orange, methylene blue, and rhodamine B), degrading them in aqueous samples [23]. Eco-friendly AuNPs produced using two different brown algae, Sargassum tenerrimum and Turbinaria conoides, exhibited the ability to induce the reduction of 4-nitrophenol and p-nitroaniline (nitroarenes) into aminoarenes [121].

3.2 Gold, iron, and silver algae-based NPs dealing with inorganic contaminants

Microalgae species C. vulgaris and Nannochloropsis could be successfully used in green protocols to synthesize AgNPs capable of adsorbing heavy metals. The nanomaterials showed a 74.62% and 70.35% reduction in the zinc concentration in polluted water and a 66.10% and 68.86% reduction in the lead concentration in water samples containing the inorganic pollutant [25].

Green microalgae from the Chlorococcum genus (Chlorococcum sp. MM11) were successfully used to synthesize iron spherical-shaped structures to remediate chromium pollution (Cr6+). The nanomaterial proved to be more efficient than bulk iron in converting Cr6+ to Cr3+ [27]. Fe3O4-NPs could be successfully produced by brown algae Sargassum acinarium and P. pavonica. Calcium alginate beads functionalized with these green NPs exhibited the potential to adsorb the inorganic pollutant lead (a heavy metal). The removal rate reached a maximum of 78% for NPs produced from S. acinarium and 91% for the ones produced from P. pavonica [122]. The algae species present in the lichen structure can also contribute to green synthesis protocols capable of generating NPs to serve as nanoremediators. Heavy metals such as cadmium and lead could be removed using iron oxide NPs synthesized from the extract of the lichen Ramalina sinensis [123].

The microalgae species C. vulgaris and Nannochloropsis, previously mentioned as raw materials for AgNPs, could also be used to synthesize AuNPs capable of promoting the adsorption of heavy metals zinc and lead. With regard to zinc, the reductions in concentrations observed were 66.83% and 60.32%, respectively; for lead; they were 57.41% and 66.53%, respectively [25].

3.3 Gold, iron, and silver algae-based NPs dealing with biological contaminants

As a consequence of environmental pollution, pathogenic microorganisms from various species can be present in water, soil, and air, contaminating them. Water is commonly more affected as a consequence of rivers receiving the untreated discharge of domestic sewage containing, for example, feces. As a consequence, drinking-water quality needs to be monitored to avoid the undesirable presence of pathogens [124]. Among these pathogens, there are some organisms, however, that cause major concerns such as species of bacteria resistant to antibiotics (especially the multi-resistant ones); these are a serious concern to the medical field. In 2019, it was estimated that antimicrobial resistance caused 4.95 million deaths worldwide [125,126].

In this sense, the nanotechnology field can offer interesting materials, such as FeNPs, AuNPs, and especially AgNPs, exhibiting antimicrobial activity to fight these organisms [127,128]; they may offer low-cost and efficient tools to overcome drug resistance [129,130].

An interesting aspect related to antimicrobial NPs is how they manage to cause microbial cell death. When a microorganism is exposed to NPs, the first step is the nanomaterial’s interaction with the membrane of the microbial cell, a process guided mainly by electrostatic interactions [131]. However, some events occur during these interactions to eliminate the microorganisms, and there are different proposed mechanisms to explain the antimicrobial activity exhibited by NPs such as AuNPs and AgNPs. One of these mechanisms involves NPs inducing disruption of the cell membrane’s structure and impairing the functions of proteins attached to it, such as electron transport chain complexes [132,133]. Green AgNPs, for example, can cause pores on the membrane of bacterial cells [134]. If NPs manage to enter cells without collapsing their membrane, in contact with the cytoplasm material, it is also possible for the nanostructures to establish interactions with functional groups of biomolecules such as thiol groups from proteins. These interactions may cause impairment in biomolecules’ functions and lead to cell death. The interaction of silver and gold atoms with thiol groups is already well studied [135,136]. It is also possible that NPs induce reactive oxygen species (ROS) production and these species, in turn, cause membrane disruption and consequently cell elimination [137]. The mechanism or mechanisms of inducing microbial cell death can vary with NPs’ features and from one target microorganism to another [138]. In fact, more than one mechanism described or other possible mechanisms can be triggered simultaneously resulting in the NPs exhibiting an efficient antimicrobial activity [139], including the ones produced using algae-based raw materials.

The extract from the algae species C. racemosa was used in the synthesis of AgNPs, which exhibited antibacterial activity against the pathogens P. mirabilis and S. aureus [140]. AgNPs produced using the raw material from Padina sp. exhibited antibacterial activity against S. aureus and P. aeruginosa [15]. AgNPs produced from the extract of C. vulgaris presented antibacterial potential against E. coli, S. aureus, Streptococcus sp., and methicillin-resistant S. aureus. The efficiency exhibited by these NPs surpassed the one presented by AuNPs [17]. Green macroalgae Ulva flexuosa could be used to produce AgNPs capable of dealing with water contaminants: P. aeruginosa, and E. coli (Gram negative), S. aureus, and B. subtilis (Gram positive) by impairing their growth and survival [141]. The macroalgae C. serrulata could also be applied in the green synthesis protocol to produce AgNPs capable of dealing with biological pollution. These NPs presented antimicrobial activity against E. coli, P. aeruginosa, Salmonella typhi, Shigella sp., and S. aureus [77]. Red macroalgae Gelidium amansii produced a nanoscale material capable of dealing with pathogenic bacteria: Aeromonas hydrophila, E. coli, Vibrio parahaemolyticus, P. aeruginosa (Gram negative), Bacillus pumilus, and S. aureus (Gram positive) [142]. Gelidiella acerosa, on the other hand, was used in the production of AgNPs presenting antifungal activity against biological contaminants Fusarium dimerum, Humicola insolens, Trichoderma reesei, and Mucor indicus [143]. The brow macroalgae S. myriocystum were used in the synthesis of AgNPs presenting the ability to deal with pathogenic bacteria E. coli, S. aureus, Staphylococcus epidermidis, Proteus vulgaris, Klebsiella pneumonia, and P. aeruginosa [117]. The biomass powder obtained from the microalgae Coelastrella aeroterrestrica strain BA_Chlo4 was used in the production of AgNPs that exhibited biocidal effect over S. aureus, Streptococcus pyogenes, and B. subtilis (Gram-positive bacteria) and E. coli and P. aeruginosa (Gram-negative bacteria) [144]. The macroalgae Enteromorpha intestinalis could be used to produce AgNPs that exhibited microbicidal properties over the pathogens Candida albicans, Candida krusei, Candida tropicalis, E. coli, S. typhi, S. aureus, and Vibrio cholera [145].

It is interesting to mention that not only microorganisms that can impair human health can be eliminated by NPs; for example, AgNPs produced using the raw material from Portieria hornemannii (red algae) exhibited the potential to fight fish pathogenic bacteria [146].

Regarding FeNPs, the water extract from Ulva lactuca was used in the synthesis of FeNPs that exhibited bactericidal effect against E. coli, S. typhimurium, Bacillus cereus, P. vulgaris, and S. aureus [16]. P. pavonica, C. sinuosa, and P. fascia (brown macroalgae) were already used to produce green Fe3O4-NPs capable of fighting harmful algae species [122]. The aqueous extracts obtained from the brown macroalgae C. sinuosa and from the red macroalgae Pterocladia capillacea were used in the synthesis of Fe3O4 NPs. Both NPs exhibited antibacterial (against B. subtilis, E. coli, P. aeruginosa, S. typhi, S. aureus, and V. cholera) and antifungal activity. However, the NP synthesized from the brown macroalgae exerted a larger inhibition over Fusarium oxysporum and Aspergillus flavus [147]. A species from the Sargassum genus, S. vulgare, proved to be useful to synthesize green FeNPs (Fe3O4) to fight marine bacteria that can form biofilm. This property was also identified in Fe3O4 NPs synthesized using Jania rubens and Ulva fasciata’s material. The activity of the nanomaterial surpassed the one observed when algae material alone was assayed [148]. The extract from the lichen R. sinensis, which contains microalgae in its composition, was used in the production of Fe3O4 NPs capable of fighting S. aureus and P. aeruginosa due to the nanomaterial’s antibacterial activity [149]. Fe3O4 NPs produced using the green microalgae Chlorella K01’s material exhibited properties to fight fungi from Fusarium genus (F. moniliforme, F. oxysporum, and F. tricinctum) and also Pythium sp. and Rhizoctonia solani [150].

The ethanolic extract from Galaxaura elongata was used in the synthesis of AuNPs that exhibited antibacterial activity against E. coli, K. pneumoniae, S. aureus, and its methicillin-resistant strain, and also P. aeruginosa. The powder of this algal species, on the other hand, was used to produce AuNPs capable of fighting E. coli and K. pneumoniae, but with lower efficiency when compared to the ones produced using the extract [151]. Ecklonia cava (species from brown algae) was used in the synthesis of AuNPs exhibiting antimicrobial activity against Aspergillus brasiliensis, Aspergillus fumigates, Aspergillus niger, B. subtilis, C. albicans, E. coli, P. aeruginosa, and S. aureus [152]. AuNPs synthesized using the extract from C. vulgaris exhibited antibacterial effects against E. coli, S. aureus and its methicillin-resistant strain, and Streptococcus sp. [17].

4 Main limitations associated with large-scale field application of algae-based AgNPs, AuNPs, and FeNPs

Although green AuNPs, FeNPs, and AgNPs synthesized from the algae material possess the potential addressed in this review to deal with environmental pollution from diverse chemical nature, they are not yet being commercialized or applied on a large scale to perform this role in the field. The main reasons associated with this can be related to: obtaining the raw material, synthesis protocol, obtaining the NPs and/or the use of the NPs themselves.

Regarding the limitations related to obtaining algae materials, it is still necessary to optimize protocols to enhance their growth rate to produce the necessary amount of raw materials in the condition that will allow the production of the NPs presenting the desirable characteristics; aiming for large-scale application, the cost associated with cultivation media is also relevant to cost-effective applicability [153]. Reproducibility is also an important technical challenge [154]. The metabolites present in the biological raw material are responsible for reducing and capping NPs and it is known that seasonal conditions interfere with metabolites’ production in living organisms such as algae [155]. In this way, to synthesize identical NPs, it is necessary to obtain bio-based materials under identical conditions every time that the synthesis is performed, which is difficult. Therefore, protocols need to specify, providing the maximum information possible, details regarding location, cultivation protocol, season, etc., in which the biomaterial was obtained for green synthesis.

Synthesis protocol also presents challenging aspects such as adjusting parameters to regulate the size and shape of NPs and to optimize the efficiency of the process. There are already protocols developed focusing specifically on some of these aspects; for example, there are protocols specifying conditions to obtain monodispersed NPs, avoiding large variations in the size and shape of the final product. Monodispersed AuNPs could be obtained using the green algae Rhizoclonium fontinale after adjustment in pH, the amount of algae-material to be used, and also the initial concentration of gold ions. At a pH of 9, adding 10 mg of the green raw material to each 100 mL of a 15 mg‧L−1 solution of auric chloride, after 72 h, spherical AuNPs of 16 nm were obtained [156]. Monodispersed silver/silver chloride NPs were synthesized using algae from the Chara vulgaris species that required, under magnetic stirring, an aqueous extract/silver nitrate ratio of 3:1 at 60°C for 1 h of reaction [157]. The downstream processing aiming to obtain the NPs when the synthesis is performed intracellularly by algae is also a challenging aspect. The particles produced by this type of method remain bound to the cell membrane and it is necessary to disrupt the cells to obtain free NPs [158]. So, if the synthetic route is an intracellular one, downstream processing is more expensive and laborious to obtain NPs free from the algae debris. If the extracellular route is chosen, however, simple high-speed centrifugation allows easy recovery of NPs [159].

Regarding challenging issues related to the use of NPs, it is possible to highlight the complete removal of the nanomaterial from the environment after remediation if they are applied in field experiments [160]. It is necessary to develop efficient technologies to completely remove NPs from water, soil, or air after remediation to avoid exposure of living beings to them in an uncontrolled way. In this sense, NPs presenting magnetic properties are extremely useful. Iron oxide NPs, for example, are already applied in protocols aiming for the efficient harvesting of microalgae. Based on the adhesion of NPs to algae cells from C. vulgaris and Scenedesmus ovalternus, an efficiency of harvesting higher than 95% could be obtained [161]; this efficiency reached values higher than 99% when cells of Nannochloropsis maritima were the target [162]. Consequently, as bioactive magnetic NPs can be produced by applying algae in green protocols, these materials can facilitate recovery after use; the Fe3O4 NPs produced from the extract of Chlorella K01, for example, exhibited not only antifungal activity but also magnetic properties [150].

Biocompatibility issues arise during NPs' application, and will be discussed in the following section.

All these challenges mentioned in this review are receiving attention from the scientific community, as they need to be addressed in order to allow advancements in the use of algae-based NPs aiming at efficient environmental pollution nanoremediation on a large scale.

5 Biocompatibility of algae-based NPs

A nanomaterial is considered biocompatible if it is capable of inducing an appropriate response in the living cells in contact with it, and not triggering toxic and/or immunogenic reactions that can cause death [163]. Various aspects can influence the compatibility of NPs such as the ones associated with the material itself: hydrophobicity, purity, shape, size, surface charge, and functional groups present [164].

There are some studies in the literature that present NPs as cytotoxic nanomaterials when assayed using some cell types as target cells. However, when it comes to green NPs, they are commonly referred to as biocompatible materials to human normal cells. The idea of green synthesis aims to reduce toxicity not only to the environment by avoiding the use of toxic chemicals during synthesis but also to human cells. An important strategy to increase a nanomaterial’s biocompatibility is functionalization. In this way, there is a large array of protocols aiming to functionalize and chemically modify the surface of nanomaterials to make them more compatible and also more stable [165]. Nevertheless, in the green synthesis protocol of metallic NPs, the functionalization step is already performed in the last phase of the process as the bioactive metabolites from bio-based raw material not only reduce the metal ions but also promote the capping of the nanomaterial. Consequently, algae-based NPs are considered biocompatible materials [65].

It is interesting to highlight that toxicity is a desirable feature in algae-based NPs if the target cell is a cancerous one or cells of pathogenic microorganisms. There are protocols that allow the synthesis of algae-based AuNPs, AgNPs, and FeNPs that can eliminate cancer cells but are biocompatible when assayed using non-cancerous human cells. The hexagonal AgNPs produced using the extract of microalgae Coelastrella aeroterrestrica strain BA_Chlo4 decreased the proliferative activity of cancer cells HCT-116, HepG2, MCF-7, and MDA. However, they were proved to be biocompatible when assayed on the non-cancerous cells HFS and Vero. In fact, the compatibility presented by the biogenic material surpassed that of AgNPs synthesized using a chemical protocol instead of a green one, confirming that green protocols can offer a material presenting optimized biocompatibility [144].

AuNPs produced using the extract from E. cava exhibited antimicrobial activity but proved to be biocompatible when assayed over the human keratinocyte cell line HaCaT [152]. The green AuNPs synthesized using the extract from the brown macroalgae Cystoseira baccata exhibited anticancer properties when assayed over colon cancer cell lines (Caco-2 and HT-29); however, they proved to be biocompatible in tests using non-cancerous primary neonatal dermal fibroblasts (PCS-201-010) [166]. Monodispersed AuNPs produced using the extract from Rhizoclonium fontinale were also non-toxic to cell lines of normal (non-cancerous) human cells [156]. C. vulgaris could be used in a protocol to synthesize AuNPs capable of eliminating A549 cells (human alveolar basal epithelial lung cancer cells) but were biocompatible when assayed on HEL299 normal lung fibroblasts [167].

FeNPs produced using the raw material from the brown algae Spatoglossum asperum could also exhibit target toxicity against human glioblastoma cells (LN-18). Fe3O4 NPs showed a half inhibitory concentration of 19.24 µg‧mL−1 [168].

6 Conclusions and future prospects

Sustainability principles have been receiving increasing attention worldwide, as it is urgent to repair the damage caused by anthropic actions over the ecosystems and stop the harmful consequences of industrialization in order to offer a better life quality to the population. Environmental pollution can be caused by organic molecules such as dyes largely present in industrial wastewater, inorganic substances such as heavy metal products of mining and/or industrial activities, and biological contaminants such as pathogenic microorganisms. Among the latter category are drug-resistant pathogenic bacteria that concern the medical field. So, developing safe and efficient tools to allow the management of environmental pollution and avoiding its harmful effects, is desirable.

Nanotechnology offers protocols to perform the green synthesis of nanomaterials capable of remediating contamination caused by organic and/or inorganic molecules and also pathogens. Among these materials, metallic NPs deserve to be highlighted due to their stability, fast, and low-cost production, as well as chemical and physical properties useful in eliminating, transforming into less harmful forms, and/or absorbing pollutants.

Regarding the use of the bio-based raw material in the synthesis of these NPs, algae offer advantages such as the possibility of low-cost and eco-friendly synthesis; due to their fast growth rate, they need low-energy input requirements, can be grown in aquaculture systems, and have a high tolerance to metals.

The chemicals present in algae allow metal-reducing and capping, favoring the synthesis of metallic eco-friendly NPs. In the literature, a large number of examples of algae green-based protocols can be found to synthesize these particles presenting the potential to remediate the pollution caused by diverse types of environmental pollutants. These biogenic nanomaterials are elegant and interesting tools in the search for sustainability/sustainable development.

This review focused on the potential of phycosynthesized AuNPs, AgNPs, and FeNPs to deal with environmental pollution to promote remediation. However, although these algae-based green NPs possess this potential, they are not yet been commercialized or applied on a large scale to perform this role. There are products containing AgNPs, for example, being commercialized to offer wound healing in an antibacterial environment or an efficient delivery, but these NPs are not derived from the algae material [169].

This scenario is a consequence of challenges that still need to be surpassed for obtaining the algae material (optimizing cultivation protocols and reaching satisfactory reproducibility), synthesizing and obtaining the NPs (optimizing synthesis protocols to regulate NPs’ features and possible necessary downstream steps), and also the problems related to biocompatibility and recovering NPs after use.

Efforts are being dedicated and are expected to continue for developing research related to these challenging aspects aiming to surpass them. These efforts would allow the advancements to reach large-scale field applications of algae-based NPs as nanoremediators. New protocols are expected to be proposed addressing current limitations and deeper studies focused on mechanisms of NPs’ production by algae-based materials are also expected. In silico approaches can be useful to allow a better understanding regarding influences on the determination of NPs’ features and properties as a consequence of variables associated with the synthesis.

As algae are the largest group of photoautotrophic microorganisms, there is also a large number of species that can still be studied as a source of a bio-based raw material for the phycosynthesis of metallic NPs that may serve as nanoremediators.

Despite these limitations, undoubtedly the capacity of these nanomaterials to deal with pollutants is a reality and algae-based AuNPs, AgNPs, and FeNPs present an interesting potential to be explored aiming for sustainability and environmental restoration. This field of expertise can offer future NPs produced with desirable quality control, at low-costs in a fast and efficient way that will make their market entrance and success viable as tools to restore polluted environments in an eco-friendly way.

  1. Funding information: The authors state that there was no funding involved.

  2. Author contributions: Fernanda Tonelli: conceptualization, writing – original draft, writing – review and editing; Christopher Silva: writing – original draft. Vinicius Delgado: writing – original draft. Flávia Tonelli: writing – original draft, figure drawing, writing – review and editing. All authors read and approved the final manuscript.

  3. Conflict of interest: The corresponding author (Fernanda Maria Policarpo Tonelli) is a Guest Editor of the Green Processing and Synthesis’ Special Issue “Biomolecules-derived synthesis of nanomaterials for environmental and biological applications” in which this article is published.

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Received: 2023-01-20
Revised: 2023-03-26
Accepted: 2023-04-20
Published Online: 2023-05-19

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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