Removal of Toxic Heavy Metals from Contaminated Aqueous Solutions Using Seaweeds: A Review

Heavy metal contamination affects lives with concomitant environmental pollution, and seaweed has emerged as a remedy with the ability to save the ecosystem, due to its eco-friendliness, affordability, availability, and effective metal ion removal rate. Heavy metals are intrinsic toxicants that are known to induce damage to multiple organs, especially when subjected to excess exposure. With respect to these growing concerns, this review presents the preferred sorption material among the many natural sorption materials. The use of seaweeds to treat contaminated solutions has demonstrated outstanding results when compared to other materials. The sorption of metal ions using dead seaweed biomass offers a comparative advantage over other natural sorption materials. This article summarizes the impact of heavy metals on the environment, and why dead seaweed biomass is regarded as the leading remediation material among the available materials. This article also showcases the biosorption mechanism of dead seaweed biomass and its effectiveness as a useful, cheap, and affordable bioremediation material.


Introduction
The severity of heavy metal pollution cannot be over-emphasized, as it has become a universal issue in recent years. The effects of heavy metals in the environment are harmful due to their high toxicity. Their release into the environment occurs as a result of various natural and anthropogenic activities. Unfortunately, most of these heavy metals, whether generated from human activities or nature, constantly undermine the existence and health of environmental resources. The toxicity, persistence, and non-biodegradable nature of these metal ions make them a threat to the environment [1,2]. These heavy metals are known to cause multiple and complicated health problems such as brain and lung damage, cancer, nausea, and vomiting [3,4]. Seaweed, also known as marine algae, serves as one of the major leading biosorption materials for the treatment of heavy metals [5]. Seaweed produces a variety of compounds such as xanthophylls, chlorophyll, carotenoids, vitamins, fatty acids, amino acids as well as antioxidants (such as halogenated compounds, alkaloids, and polyphenols), and polysaccharides (such as agar, alginate, carrageenan, proteoglycans, galactosyl glycerol, laminarin, rhamnan sulfate, and fucoidan) [6]. The presence of alginate in the seaweed makes it an effective eluted material for metal ion removal. Alginate, as well as fucoidan, has a high sorption capacity, which can mainly be attributed to polysaccharides found in the cell walls. The carboxylic and sulfonic acid functional groups are more active in the ion exchange process, and polysaccharides are The contamination of water bodies normally happens through leaching, erosion, wind, and other environmental means, thereby leading to negative health implications and risk to the ecosystem. Heavy metal pollution leaves a negative blueprint on the environment and people's lives. As shown in Figures 1 and 2, natural and anthropogenic sources are the known sources for heavy metal contamination. The natural sources for these toxic metals include volcanic eruptions, forest fires, biogenic sources, and the weathering of rock [25], while industrial estates, automobile exhaust, the spraying of insecticide, agricultural activities, transportation, and mining are the main anthropogenic sources of heavy metals pollution [26]. The contamination of water bodies normally happens through leaching, erosion, wind, and other environmental means, thereby leading to negative health implications and risk to the ecosystem. Heavy metal pollution leaves a negative blueprint on the environment and people's lives. As shown in Figures 1 and 2, natural and anthropogenic sources are the known sources for heavy metal contamination. The natural sources for these toxic metals include volcanic eruptions, forest fires, biogenic sources, and the weathering of rock [25], while industrial estates, automobile exhaust, the spraying of insecticide, agricultural activities, transportation, and mining are the main anthropogenic sources of heavy metals pollution [26]. As seen in Figure 3 below, topsoil and underground water are normally polluted by industrial activities, agricultural activities, weathering, volcanic eruptions, and other biogenic activities. The water bodies become contaminated as the topsoil is washed into them by either erosion, leaching, or landfill leakage. In turn, flora and fauna are affected as the polluted water bodies are consumed and accumulated into their systems, tissues, and organs. Human beings, on the receiving end, are exposed to multiple risks of biochemical disorder or organ failures following the ingestion of contaminated plants and animals. As seen in Figure 3 below, topsoil and underground water are normally polluted by industrial activities, agricultural activities, weathering, volcanic eruptions, and other biogenic activities. The water bodies become contaminated as the topsoil is washed into them by either erosion, leaching, or landfill leakage. In turn, flora and fauna are affected as the polluted water bodies are consumed and accumulated into their systems, tissues, and organs. Human beings, on the receiving end, are exposed to multiple risks of biochemical disorder or organ failures following the ingestion of contaminated plants and animals.

Structure and Classification of Seaweed
Seaweed does not have roots, but rather has holdfasts that anchor the seaweed to the bottom of the sea or ocean. These root-like holdfasts are composed of many finger-like components known as Haptera and are supported by a stalk or stem called a Stipe. The structure of the stem or stipe can be hard, filled with gas, soft or flexible, short, or long, and in some cases, they may be completely absent depending on the type of seaweed [27]. These stipes or stem-like structures are either filled with gas or empty. These are referred to as pneumatocysts, while the entire body of the seaweed is referred to as the thallus. Seaweed has leaves called blades, which assist in photosynthesis, although some seaweed species have only a single leaf, while others have many leaves. Figure 4 below shows the physical structure of seaweed.

Structure and Classification of Seaweed
Seaweed does not have roots, but rather has holdfasts that anchor the seaweed to the bottom of the sea or ocean. These root-like holdfasts are composed of many finger-like components known as Haptera and are supported by a stalk or stem called a Stipe. The structure of the stem or stipe can be hard, filled with gas, soft or flexible, short, or long, and in some cases, they may be completely absent depending on the type of seaweed [27]. These stipes or stem-like structures are either filled with gas or empty. These are referred to as pneumatocysts, while the entire body of the seaweed is referred to as the thallus. Seaweed has leaves called blades, which assist in photosynthesis, although some seaweed   [30]. Green seaweeds (chlorophyte) have chlorophyll, but with no dominant pigment justifying their green coloration; therefore, green seaweed is generally green. It is smaller in size than both red and brown seaweeds [5,31]. We further characterized seaweeds based on both their physical and chemical compositions as shown in Table 2. The alginate and the intercellular substance of the brown algae have high divalent cation uptakes. The cell walls of brown seaweeds are composed of cellulose, alginic acid, and polysaccharides, with alginates and sulfate being the dominant active groups [7]. The cell wall of red algae contains cellulose, but their biosorption capabilities can largely be attributed to sulfated polysaccharides made up of galactans. Similarly, the cell wall of the green algae contains cellulose with hydroxyl-proline glucosides; xylans and mannans are the main functional groups during biosorption [32,33].

Seaweed: Metal Ion Biosorption Material
The treatment of contaminated solutions has been a burden to engineers and scientists over the years. Recently, seaweed has been proven to be more effective than other natural sorption materials. Some of the other natural sorption materials that have been used to elute metal ions are discussed in the next subsection. Remediation of aqueous solution from metal ions is of serious concern to environmentalists, considering the threat Seaweed is divided into three (3) main groups based on color characterization, namely: Brown (Phaeophyceae), Red (Rhodophyceae), and Green (Chlorophyceae) seaweeds [28]. Brown algae (Phaeophyta) have various physical appearances either in crust or filament form. Brown algae are multicellular and contain chlorophyll, which aids in photosynthesis, with fucoxanthin being the dominant pigment. Physically, brown algae can range from a large size (Kelp) of about 60 m long to as small as 60 cm [29]. Red algae (Rhodophyta) have chlorophyll in which phycocyanin and phycoerythrin are the dominant pigments responsible for red coloration. Red seaweeds are normally not actually red, but brownishred or purple. Physically, red algae are smaller than brown algae in length [30]. Green seaweeds (chlorophyte) have chlorophyll, but with no dominant pigment justifying their green coloration; therefore, green seaweed is generally green. It is smaller in size than both red and brown seaweeds [5,31].
We further characterized seaweeds based on both their physical and chemical compositions as shown in Table 2. The alginate and the intercellular substance of the brown algae have high divalent cation uptakes. The cell walls of brown seaweeds are composed of cellulose, alginic acid, and polysaccharides, with alginates and sulfate being the dominant active groups [7]. The cell wall of red algae contains cellulose, but their biosorption capabilities can largely be attributed to sulfated polysaccharides made up of galactans. Similarly, the cell wall of the green algae contains cellulose with hydroxyl-proline glucosides; xylans and mannans are the main functional groups during biosorption [32,33].

Seaweed: Metal Ion Biosorption Material
The treatment of contaminated solutions has been a burden to engineers and scientists over the years. Recently, seaweed has been proven to be more effective than other natural sorption materials. Some of the other natural sorption materials that have been used to elute metal ions are discussed in the next subsection. Remediation of aqueous solution from metal ions is of serious concern to environmentalists, considering the threat it poses to the purity of the natural environment [34]. The non-biodegradability, carcinogenicity, and toxicity of heavy metals make them harmful, and treatment of these heavy metals is essential [35]. Sorption has been proven to be a sustainable and effective method for treating heavy metals in aqueous solutions using natural biomass [36]. Based on these outstanding results, seaweed has emerged as the leading material, with a high rate of metal ion removal. The biosorption method is one of the simplest, cheapest, and most eco-friendly methods, and requires little or no nutrient addition. The effectiveness and efficiency of treatments for heavy metals are directly related to the type of sorbent used [37]. In short, the remediation of heavy metals using seaweed offers a more reliable, cheaper, and more effective means of heavy metal removal from aqueous solutions than the previous methods. Various mechanisms of seaweed biomass (electrostatic interaction, ion exchange, and complex formation) have been used in the biosorption process of heavy metals, and ion exchange has been widely used and is considered the most important among the list of mechanisms [38,39]. The cell walls of the algae possess polysaccharides and protein, which serve as binding sites for metal ion uptake [40]. There are several factors responsible for the sorption capability of a seaweed cell surface; among these factors are accessibility of binding groups for metal ions, the affinity constants of the metal with the functional group, the chemical state of these sites, the number of functional groups in the algae matrix, and the coordination number of the metal ion to be sorbed [41]. The metal biosorption ability of seaweed varies because of the heterogeneity of their respective cell wall composition. For example, as seen in Table 3, brown, green, and red algae have high affinities for lead (Pb), copper (Cu), and cobalt (Co), respectively [7]. Physical or chemical treatment can enhance heavy metal uptake by seaweed, and the cell wall surface is modified, thereby providing additional binding sites for biosorption [7,42]. The physical treatment includes freezing, crushing, heating, and drying, as these increase the surface area on which biosorption can be achieved [42]. The most common seaweed pretreatments are glutaraldehyde, calciumchloride (CaCl 2 ), formaldehyde, sodium hydroxide (NaOH), and hydrogen-chloride (HCl). Pretreatment with calcium-chloride (CaCl2) enhances calcium binding with alginate, which plays a pivotal role in ion exchange [43]. The crosslinking bond between hydroxyl and amino group is strengthened by formaldehyde and glutaraldehyde [44]. The electrostatic interactions of metal ion cations are increased by sodium hydroxide (NaOH), while at the same time providing optimal conditions for ion exchange, while hydrogen-chloride (HCl) dissolves the polysaccharides of the cell wall and also replaces light metal ions with a proton, thereby increasing the biosorption binding sites [7]. It is in this regard that we aim to showcase the comparative advantages of seaweed over other sorption materials in the removal of heavy metals.    Table 3 shows the different species of algae used in the removal of heavy metals. The numbers for metal ion uptake qmax (mmol/g) for the different species are in the range (0-4), especially the brown alga species (Sargassum muticum), while all uptake occurs between pH values of (2-6), and pH influences the dissociation of heavy metals from the solution using different alga species [48,73]. The pH impacts metal ion uptake, which is a result of the influence of the "functional group on the biomass' cell wall and the metal ions solution" [33]. The polysaccharides present in the cell wall of seaweeds are the most highly metal-binding sites [64].

Various Natural Materials Used for Sorption
In recent years, engineers and scientists have directed much effort towards identifying the most suitable biosorption materials. Among many materials, seaweed has been revealed to be the most suitable and effective natural material. Table 4 shows some of the various other materials that have been used for the removal of metal ions.

Materials Used Heavy Metals References
Polymers Fe and Cr [74] Sawdust and tree barks Hg, Pb, and Zn [75] Electronic waste along with galvanic wastes Cu, Ni, Mn, Pb, Sn [76] charcoal: Cr(III) [77] Clay Cr(III) [78] Fungi Cr, Fe [79] Dead biomass Cr [80] Peat moss Cr, Fe [81] Peanut shells, Rice husk, Straw, and walnut cover Cr, Cu, Ni [82] Cocoa shell Al, Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, and Zn [83] Coconut husk Cr, As [82] Caol and fly ashes Cr, Cu, Ni [84] Banana pith and peels Ni, Pb [85] Cassava fiber Pb, Co [86] Chicken feathers Al, As [87] Sheep manure wastes Ca, Cd [88] Sunflower Co, Cr [89] Rice byproducts Cu, Fe [90] Orange peels Cu, Fe, Hg [91] Palm kernel fiber Fe, Hg [82] Grape stalks Cr, Fe, Hg [92] As highlighted in Table 4, the use of different biomass (living or dead) for the removal of heavy metals has been studied over the years, and microalgae have stood out among the others. For non-living organisms, the cell surface involves different functional groups like amini, hydroxyl, sulfhydryl, phosphate, sulfate, and carboxyl groups [93]. Sawdust and tree barks are rich in tannin/lignin, and have been studied by Fiset and team [94], as they proved effective in metal adsorption. The tannin is an active species during the metal adsorption (ion exchange) process because of the polyhydroxy polyphenol groups [95]. Lignin, which is extracted from black liquor and is also a waste product of the paper industry, has been considered for the removal of metals (Hg, Pb, and Zn) [96]. Alcohols, acids, aldehydes, ketones, phenol, hydroxides, and ethers are all polar functional groups of lignin that have varying metal-binding capabilities [97]. Phytoremediation or phytofiltration of metal-contaminated effluents have been tested and proven successful. Some examples of aquatic plants with such ability are Ceratophyllum demersum, Lemna minor, and Myriophyllum spicatum [98]. Cellular components such as amide, imine, imidazol moieties, carboxyl, hydroxyl, sulfate, sulfhydryl, phosphate of these plants have high metalbinding properties, as reported by Gardea and team [99]. Chitin and chitosan have also been used to treat metal ions in wastewater. Chitin, which is the second-most abundant natural biopolymer after cellulose, is commonly found in the exoskeletons of crustaceans and shellfish, while Chitosan is produced by alkaline N-deacetylation of chitin [100]. Similarly, peat moss has been studied based on heavy metal decontamination of wastewater. It is a complex material with both lignin and cellulose as its main constituents, which contain polar functional groups [101]. Plenty of other agricultural waste, such as rice residues, fruit and vegetable peels, tea/coffee residues, and coconut husks, have also been used for metal ion retention. Most of the materials have polyhydroxy, polyphenol, carboxylic, and amino groups, which play key roles in the metal adsorption process [83]. Animal bones, clay, human hair, and teeth have all been used to treat metal ions, but have not been effective or efficient when compared with seaweed [102]. In conclusion, the above-discussed natural sorption materials have not been effective either in terms of metal ions removal rate or socio-economic benefit when compared to seaweed.

Sorption Mechanism of Seaweed
Seaweed is characterized by both physical, biological, and chemical attributes, such as alginate, carrageenan, and photosynthesis features. It can also grow in extreme conditions, in the presence of heavy metals, salinity, and harsh temperatures. Owing to the aforementioned qualities, in addition to its high binding affinity, seaweed is considered a good bioremediation material for treating toxic metal ions in aqueous solutions [103]. Seaweed also has a "hormesis phenomenon feature", which refers to the toxic contamination of algae stimulating further algae growth [104]. Similarly, some cyanobacteria tend to grow in wastewater that is highly polluted with toxic heavy metals; examples of cyanobacteria include; spirogyra, oscillatoria, anabaena, and phormidium [105]. Seaweeds have both antioxidant enzymes and non-enzymatic antioxidants. Antioxidant enzymes include catalase, superoxide dismutase (SOD), ascorbate peroxidase, and reductase, while non-enzymatic antioxidants include glutathione (GHS), cysteine, proline, carotenoids, and ascorbic acid (ASC) [106]. During the sorption process, heavy metals in the seaweed ignite the phytochelatins (PCs) through biosynthesis. These phytochelatins are proteins and thiolrich peptides that can minimize toxic metal ions through interaction [107]. Superoxide dismutase (SOD) performs a defensive role against the superoxide anion, which is exerted by breaking the superoxide anion into hydrogen peroxide and oxygen molecules. The catalase degrades hydrogen peroxide to oxygen and water molecules, while cysteine is the precursor for metallothioneins, phytochelatins (PCs), glutathione (GSH), and other sulfur-related compounds. [108]. The reduction of free radicals and reactive oxygen species (ROS) is performed by both glutathione (GSH) and ascorbic acid (ASC), which are endogenous antioxidants that are synthesized by seaweed [109]. Additionally, seaweed produces a high level of ascorbic acid (ASC) as "hydrophilic redox buffer", which protects cytosol against the threat of oxidation. Similarly, the seaweed is protected by glutathione (GSH) by enabling phytochelatins (PCs), scavenging free radicals, and ascorbic acid (ASC) synthesis alongside the restoration of substrate for other antioxidants [106,107]. The chemistry involved in the interaction between the biomass (seaweed) and the metal ions is shown in Figures 5 and 6, respectively.
As shown in Figure 5, the removal mechanism of heavy metals is performed in two folds. These two folds include biosorption, which is the "rapid extracellular passive adsorption", and the latter is bioaccumulation, which is the "slow intracellular positive diffusion and accumulation". Seaweeds' cell walls are made up of cellulose and alginate (polysaccharides) and lipids, while the organic protein offers amino, phosphate, hydroxyl, thiol-rich, and carboxyl (functional groups), which all possess good ability to bind metal ions [105]. Additionally, the cell wall is composed of laminarin, deprotonated sulphate, and monomeric alcohols capable of attracting both cationic and anionic species of metal ions [110]. Adsorption on the surface of seaweed occurs rapidly when compared to inside the seaweed. On the surface, adsorption takes place through ion exchange with the cell wall and covalent bonding with the ionized cell wall, resulting in "seaweed exopolysaccharides". Conversely, adsorption is slow inside, and phytochelatins, GSH, and metal transporter play a leading role in the binding of metal ions. This accumulation of metal ions inside is carried across the cell membrane to the cytoplasm before diffusion [110,111].
According to Figure 6, the biochemical constituent of seaweed is responsible for the sequestration of metal ions, which are composed of alginate and fucoidan in the cell wall. The cell wall of microalgae is made up of a fibrillary skeleton (cellulose) and an amorphous embedded matrix (alginate) [5]. The cell wall of brown algae contain sulfated polysaccharides, while in red algae, galactans are found, and green algae, hydroxylproline [46].
The catalase degrades hydrogen peroxide to oxygen and water molecules, while cysteine is the precursor for metallothioneins, phytochelatins (PCs), glutathione (GSH), and other sulfur-related compounds. [108]. The reduction of free radicals and reactive oxygen species (ROS) is performed by both glutathione (GSH) and ascorbic acid (ASC), which are endogenous antioxidants that are synthesized by seaweed [109]. Additionally, seaweed produces a high level of ascorbic acid (ASC) as "hydrophilic redox buffer", which protects cytosol against the threat of oxidation. Similarly, the seaweed is protected by glutathione (GSH) by enabling phytochelatins (PCs), scavenging free radicals, and ascorbic acid (ASC) synthesis alongside the restoration of substrate for other antioxidants [106,107]. The chemistry involved in the interaction between the biomass (seaweed) and the metal ions is shown in Figures 5 and 6, respectively.   As shown in Figure 5, the removal mechanism of heavy metals is performed in two folds. These two folds include biosorption, which is the "rapid extracellular passive adsorption", and the latter is bioaccumulation, which is the "slow intracellular positive diffusion and accumulation". Seaweeds' cell walls are made up of cellulose and alginate (polysaccharides) and lipids, while the organic protein offers amino, phosphate, hydroxyl, thiol-rich, and carboxyl (functional groups), which all possess good ability to bind metal ions [105]. Additionally, the cell wall is composed of laminarin, deprotonated sulphate, and monomeric alcohols capable of attracting both cationic and anionic species of metal ions [110]. Adsorption on the surface of seaweed occurs rapidly when compared to inside the seaweed. On the surface, adsorption takes place through ion exchange with the cell wall and covalent bonding with the ionized cell wall, resulting in "seaweed exopolysac-

Conclusions
The usage of seaweed as a sorption material has attracted the attention of many researchers in recent times. Seaweed's relevance is not only restricted to the treatment of heavy metals; it is a precious food that is prominent in basic balanced diets. Considering the current state of heavy metal pollution in our environment, seaweed has been proven to be an excellent, cheap, effective, abundantly available, eco-friendly, and efficient material for remediating the environment when compared to other natural sorption materials. This multi-faceted and multi-dimensional seaweed has the potential to heal the world from various environmental menaces. It is evidence that seaweed could be economically prudent both for industrial and environmental uses. As seaweeds are among the most fascinating and resourceful species, more exploration is needed to reap the benefits of these unique species. For sorption purposes, seaweed has been proven to be a good biosorption material with high metal ion uptake (qmax (mmol/g)) within the range (0-4). The brown alga (Sargassum muticum) stands out efficiently at a pH value of 2 when compared to other natural sorption materials. The main biochemical interaction between the algae and the metal ions depends on the cell wall, with polysaccharides, lipids, and other organic proteins being the components that play the main roles during the sorption process. In conclusion, the sorption of metal ions using seaweed, especially brown algae, presents a solution that is more reliable, cheaper, and possesses more effective sorption ability than other natural sorption materials previously studied.