Next Article in Journal
A Method of Optimizing a Set of Programs for Mitigating Threats Related to the Undertaking of a Contract for the Execution of Construction Works
Previous Article in Journal
Improving the Climate Resilience of Rice Farming in Flood-Prone Areas through Azolla Biofertilizer and Saline-Tolerant Varieties
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 13
Issue 21
10.3390/su132112311
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

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

by
Edward Hingha Foday Jr
1,2,3,
Bai Bo
1,2,4,5,* and
Xiaohui Xu
1,2
1
Key Laboratory of Subsurface Hydrology and Ecological Effects in Arid Region of the Ministry of Education, Chang’an University, Xi’an 710054, China
2
Department of Environmental Engineering, School of Water and Environment, Chang’an University, Xi’an 710054, China
3
Faculty of Education, Eastern Technical University of Sierra Leone, Combema Road, Kenema City 00232, Sierra Leone
4
Key Laboratory of Tibetan Medicine Research, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810008, China
5
Qinghai Provincial Key Laboratory of Tibetan Medicine Research, Xining 810001, China
*
Author to whom correspondence should be addressed.
Sustainability 2021, 13(21), 12311; https://doi.org/10.3390/su132112311
Submission received: 20 September 2021 / Revised: 3 November 2021 / Accepted: 5 November 2021 / Published: 8 November 2021
(This article belongs to the Topic New Research on Detection and Removal of Emerging Pollutants)
Browse Figures
Review Reports Versions Notes

Abstract

:
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.

1. 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 responsible for these functional groups [5,7]. On the whole, seaweed has proven to be one of the most outstanding and important biosorption materials for the remediation of metal ions. Its low cost, availability, and eco-friendliness, coupled with its high metal ion uptake capability, make it an ideal biosorption material compared to other sorption materials [6,8]. In this review, dead seaweed biomass is of particular interest, and because of the scant knowledge regarding its usefulness and biosorption mechanism, we seek to throw light on the importance of dead seaweed biomass as a sorption material and to summarize its biosorption mechanism. This review also pinpoints the toxic effects of heavy metals on environmental resources, as well as comparing dead seaweed biomass with other natural sorption materials in terms of heavy metal removal.

2. Heavy Metal Contamination in Water

Water is a universal solvent needed by all living organisms and is also good at dissolving both organic and inorganic compounds. Water resources are critically affected by heavy metal contamination, and this has seriously altered the aquatic ecosystem [9]. On a large scale, aquatic ecosystems are contaminated by heavy metals from industrial effluent, domestic sewage, and agricultural runoff [10]. Most rivers, streams, and lakes are polluted through erosion and leaching, while atmospheric deposition, metal corrosion, sediment resuspension, and metal evaporation are some of the ways the environment gets polluted [11,12]. The non-biodegradable character of heavy metals and their persistence in the environment have led to bioaccumulation through the food chain, leading to complicated health issues and environmental pollution [13]. The term heavy metals refer to metals and metalloids whose mass is over 5 g/cubic centimeters (g/cm3) and are naturally occurring elements commonly found on earth [14]. They can be regarded as trace elements due to their trace concentrations in the environment. The set of environmental matrices for metal ion concentrations range from zero (0) ppb to ten (10) ppb [15,16]. Anthropogenic and natural activities such as mining, fossil fuel combustion, agriculture, volcanic eruptions, earthquakes, weathering of rocks, and industrial activity are the main causes of environmental contamination [17]. Direct contact with these heavy metals either through inhalation or ingestion poses serious health threats such as teratogenesis, cancer, and internal disorders [18]. Cadmium (Cd), Chromium (Cr), Lead (Pb), Mercury (Hg), and Arsenic (As) were identified by Tchounwou and team [16] as the most toxic heavy metals, and have been placed under the category “priority metals”, which means they are metals of public concern, due to their toxic nature. These aforementioned metal ions are innately toxic and are capable of inducing damage to multiple organs even at minimal exposure levels. Reactive oxygen species (ROS) together with oxidative stress (OS) play key roles in the carcinogenic and toxic nature of these metal ions [16]. Zinc (Zn), Copper (Cu), Molybdenum (Mo), and several other metals have also been considered essential elements because they assist in biochemical reactions, although excess exposure above the required threshold can impair human health [19]. Against this background, international institutions like the United States Environmental Protection Agency (USEPA), the World Health Organization (WHO), the European Union (EU), etc. have set acceptable thresholds referred to as Maximum Contaminant Levels (MCLs). Table 1 shows the internationally accepted thresholds of metal ion concentrations in drinking water.
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 Figure 1 and Figure 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.

3. 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.
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 brownish-red 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].

3.1. 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, calcium-chloride (CaCl2), 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].

3.2. 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.
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 metal-binding 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.

4. 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 thiol-rich 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 Figure 5 and Figure 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, hydroxyl-proline [46].

5. 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.

Author Contributions

Conceptualization—E.H.F.J., B.B.; Funding acquisition—B.B.; Methodology—E.H.F.J., B.B., X.X.; Resources—B.B.; Software—E.H.F.J.; Supervision—B.B., X.X.; Validation—X.X.; Writing—original draft—E.H.F.J.; Writing—review & editing—E.H.F.J., B.B., X.X.; Project administration—B.B. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Natural Science Basic Research Program of Shaanxi (Program No. 2021SF-497), and the Fundamental Research Funds for Central Universities (CHD 300102291403).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

This work has no conflict of interest.

References

  1. Ajjabi, L.C.; Chouba, L. Biosorption of Cu2+ and Zn2+ from aqueous solutions by dried marine green macroalga Chaetomorpha linum. J. Environ. Manag. 2009, 90, 3485–3489. [Google Scholar] [CrossRef]
  2. Bulut, Y.; Baysal, Z. Removal of Pb(II) from wastewater using wheat bran. J. Environ. Manag. 2006, 78, 107–113. [Google Scholar] [CrossRef]
  3. Al-Rub, F.; El-Naas, M.; Benyahia, F.; Ashour, I. Biosorption of nickel on blank alginate beads, free and immobilized algal cells. Process. Biochem. 2004, 39, 1767–1773. [Google Scholar] [CrossRef]
  4. Argun, M.E.; Dursun, S.; Ozdemir, C.; Karatas, M. Heavy metal adsorption by modified oak sawdust: Thermodynamics and kinetics. J. Hazard. Mater. 2007, 141, 77–85. [Google Scholar] [CrossRef] [PubMed]
  5. Davis, T.A.; Volesky, B.; Mucci, A. A review of the biochemistry of heavy metal biosorption by brown algae. Water Res. 2003, 37, 4311–4330. [Google Scholar] [CrossRef]
  6. He, J.; Chen, J.P. A comprehensive review on biosorption of heavy metals by algal biomass: Materials, performances, chemistry, and modeling simulation tools. Bioresour. Technol. 2014, 160, 67–78. [Google Scholar] [CrossRef] [PubMed]
  7. Romera, D.E.; González, F.; Ballester, A.; Blázquez, M.L.; Muñoz, J.A. Biosorption with Algae: A Statistical Review. Crit. Rev. Biotechnol. 2006, 26, 223–235. [Google Scholar] [CrossRef]
  8. Gupta, V.K.; Nayak, A.; Agarwal, S. Bioadsorbents for remediation of heavy metals: Current status and their future prospects. Environ. Eng. Res. 2015, 20, 1–18. [Google Scholar] [CrossRef]
  9. Abrar, M.; Hussain, Z.; Akif, M.; Sok, K.; Muhammad, A.; Khan, A.; Khan, M. Textile effluents and their contribution towards aquatic pollution in the Kabul River (Pakistan). J. Chem. Soc. Pak. 2011, 24, 106. [Google Scholar]
  10. Afzal, M.S.; Ashraf, A.; Nabeel, M. Characterization of industrial effluents and groundwater of Hattar industrial estate, Haripur. Adv. Agric. Environ. Sci. Open Access (AAEOA) 2018, 1, 70–77. [Google Scholar]
  11. Yang, X.E.; Jin, X.F.; Feng, Y.; Islam, E. Molecular mechanisms and genetic basis of heavy metal toler-ance/hyperaccumulation in plants. J. Integr. Plant Biol. 2005, 47, 1025–1035. [Google Scholar] [CrossRef]
  12. Nriagu, J.O. A global assessment of natural sources of atmospheric trace metals. Nat. Cell Biol. 1989, 338, 47–49. [Google Scholar] [CrossRef]
  13. Yang, J.; Wei, W.; Pi, S.; Ma, F.; Li, A.; Wu, D.; Xing, J. Competitive adsorption of heavy metals by extracellular polymeric substances extracted from Klebsiella sp. J1. Bioresour. Technol. 2015, 196, 533–539. [Google Scholar] [CrossRef] [PubMed]
  14. Duruibe, J.O.; Ogwuegbu, M.; Egwurugwu, J. Heavy metal pollution and human biotoxic effects. Int. J. Phys. Sci. 2007, 2, 112–118. [Google Scholar]
  15. Bravo, S.; Amorós, J.; Pérez-de-los-Reyes, C.; García, F.; Moreno, M.; Sánchez-Ormeño, M.; Higueras, P. Influence of the soil pH in the uptake and bioaccumulation of heavy metals (Fe, Zn, Cu, Pb and Mn) and other elements (Ca, K, Al, Sr and Ba) in vine leaves, Castilla-La Mancha (Spain). J. Geochem. Explor. 2017, 174, 79–83. [Google Scholar] [CrossRef]
  16. Tchounwou, P.B.; Yedjou, C.G.; Patlolla, A.K.; Sutton, D.J. Heavy Metal Toxicity and the Environment. Mol. Clin. Environ. Toxicol. 2012, 101, 133–164. [Google Scholar] [CrossRef] [Green Version]
  17. Jaishankar, M.; Tseten, T.; Anbalagan, N.; Mathew, B.B.; Beeregowda, K.N. Toxicity, mechanism and health effects of some heavy metals. Interdiscip. Toxicol. 2014, 7, 60–72. [Google Scholar] [CrossRef] [Green Version]
  18. Prasher, P.; Mudila, H.; Sharma, M. Biosorption and Bioaccumulation of Pollutants for Environmental Remediation. In Microorganisms for Sustainability; Springer International Publishing: Singapore, 2021; pp. 379–405. [Google Scholar]
  19. World Health Organization. Trace Elements in Human Nutrition and Health; World Health Organization: Geneva, Swizerland, 1996. [Google Scholar]
  20. World Health Organization. Guidelines for Drinking-Water Quality, First Addendum to the Fourth Edition; World Health Organization: Geneva, Swizerland, 2017. [Google Scholar]
  21. United States Environmental Protection Agency (USEPA). Code of Federal Regulations-2003, Title 40-PART 141—NATIONAL PRIMARY DRINKING WATER REGULATIONS, Subpart B—Maximum Contaminant Levels. Available online: https://www.epa.gov/sites/default/files/2015-11/documents/howepargulates_cfr-2003-title40-vol20-part141_0.pdf (accessed on 30 October 2021).
  22. European Union. Directive (EU) 2020/2184 of the European Parliament and of the Council of 16 December 2020 on the Quality of Water Intended for Human Consumption. Off. J. Eur. Union 2020, 435, 1–62. [Google Scholar]
  23. The National Standards of the People’s Republic of China. Environmental Quality Standards for Surface Water. Available online: http://english.mee.gov.cn/SOE/soechina1997/water/standard.htm (accessed on 30 October 2021).
  24. Water, E.A.W. The Water Supply (Water Quality) Regulations 2016, PART 13 Amendments and Revocations. Available online: https://www.legislation.gov.uk/uksi/2016/614/pdfs/uksi_20160614_en.pdf (accessed on 30 October 2021).
  25. Hayashi, K.; Rivai, I.F.; Herawati, N.; Suzuki, S.; Koyama, H. Cadmium, Copper, and Zinc Levels in Rice and Soil of Japan, Indonesia, and China by Soil Type. Bull. Environ. Contam. Toxicol. 2000, 64, 33–39. [Google Scholar] [CrossRef]
  26. He, Z.L.; Yang, X.E.; Stoffella, P.J. Trace elements in agroecosystems and impacts on the environment. J. Trace Elem. Med. Biol. 2005, 19, 125–140. [Google Scholar] [CrossRef]
  27. Mahadevan, K. Seaweeds: A sustainable food source. In Seaweed Sustainability; Elsevier BV: Manchester, UK, 2015; pp. 347–364. [Google Scholar]
  28. Collins, K.G. An investigation of the prebiotic potential and gut health benefits of Irish seaweeds. Univ. Coll. Cork 2017, 371, 31–35. [Google Scholar]
  29. Gade, R.; Tulasi, M.S.; Bhai, V.A. Seaweeds: A novel biomaterial. Int. J. Pharm. Pharm. Sci. 2013, 5, 975–1491. [Google Scholar]
  30. Harbo, J.R.; Harris, J.W. Heritability in Honey Bees (Hymenoptera: Apidae) of Characteristics Associated with Resistance to Varroa jacobsoni(Mesostigmata: Varroidae). J. Econ. Entomol. 1999, 92, 261–265. [Google Scholar] [CrossRef] [Green Version]
  31. Bittner, L.; Payri, C.; Couloux, A.; Cruaud, C.; De Reviers, B.; Rousseau, F. Molecular phylogeny of the Dictyotales and their position within the Phaeophyceae, based on nuclear, plastid and mitochondrial DNA sequence data. Mol. Phylogenetics Evol. 2008, 49, 211–226. [Google Scholar] [CrossRef]
  32. Yalçın, S.; Sezer, S.; Apak, R. Characterization and lead (II), cadmium (II), nickel (II) biosorption of dried marine brown macro algae Cystoseira barbata. Environ. Sci. Pollut. Res. 2012, 19, 3118–3125. [Google Scholar] [CrossRef] [PubMed]
  33. Sheng, P.X.; Ting, Y.-P.; Chen, J.P.; Hong, L. Sorption of lead, copper, cadmium, zinc, and nickel by marine algal biomass: Characterization of biosorptive capacity and investigation of mechanisms. J. Colloid Interface Sci. 2004, 275, 131–141. [Google Scholar] [CrossRef]
  34. Adamu, C.; Nganje, T.; Edet, A. Heavy metal contamination and health risk assessment associated with abandoned barite mines in Cross River State, southeastern Nigeria. Environ. Nanotechnol. Monit. Manag. 2015, 3, 10–21. [Google Scholar] [CrossRef] [Green Version]
  35. Badruddoza, A.Z.M.; Shawon, Z.B.Z.; Tay, W.J.D.; Hidajat, K.; Uddin, M.S. Fe3O4/cyclodextrin polymer nanocom-posites for selective heavy metals removal from industrial wastewater. Carbohydr. Polymers 2013, 91, 322–332. [Google Scholar] [CrossRef]
  36. Turan, N.G.; Mesci, B. Use of Pistachio Shells as an Adsorbent for the Removal of Zinc(II) Ion. CLEAN—Soil Air Water 2011, 39, 475–481. [Google Scholar] [CrossRef]
  37. Pozdniakova, T.A.; Mazur, L.P.; Boaventura, R.A.; Vilar, V.J. Brown macro-algae as natural cation exchangers for the treatment of zinc containing wastewaters generated in the galvanizing process. J. Clean. Prod. 2016, 119, 38–49. [Google Scholar] [CrossRef]
  38. Mata, Y.; Blázquez, M.; Ballester, A.; González, F.; Muñoz, J.A. Characterization of the biosorption of cadmium, lead and copper with the brown alga Fucus vesiculosus. J. Hazard. Mater. 2008, 158, 316–323. [Google Scholar] [CrossRef] [PubMed]
  39. Michalak, I.; Chojnacka, K. Interactions of metal cations with anionic groups on the cell wall of the macroalga Vaucheria sp. Eng. Life Sci. 2010, 10, 209–217. [Google Scholar] [CrossRef]
  40. Gupta, V.; Rastogi, A. Biosorption of lead from aqueous solutions by green algae Spirogyra species: Kinetics and equilibrium studies. J. Hazard. Mater. 2008, 152, 407–414. [Google Scholar] [CrossRef]
  41. Mehta, S.K.; Gaur, J.P. Use of Algae for Removing Heavy Metal Ions From Wastewater: Progress and Prospects. Crit. Rev. Biotechnol. 2005, 25, 113–152. [Google Scholar] [CrossRef]
  42. Errasquín, E.L.; Vázquez, C. Tolerance and uptake of heavy metals by Trichoderma atroviride isolated from sludge. Chemosphere 2003, 50, 137–143. [Google Scholar] [CrossRef]
  43. Bishnoi, N.R.; Kumar, R.; Kumar, S.; Rani, S. Biosorption of Cr(III) from aqueous solution using algal biomass spirogyra spp. J. Hazard. Mater. 2007, 145, 142–147. [Google Scholar] [CrossRef]
  44. Ebrahimi, B.; Shojaosadati, S.; Ranaie, S.; Mousavi, S. Optimization and evaluation of acetylcholine esterase immobilization on ceramic packing using response surface methodology. Process. Biochem. 2010, 45, 81–87. [Google Scholar] [CrossRef]
  45. Jalali, R.; Ghafourian, H.; Asef, Y.; Davarpanah, S.; Sepehr, S. Removal and recovery of lead using nonliving biomass of marine algae. J. Hazard. Mater. 2002, 92, 253–262. [Google Scholar] [CrossRef]
  46. Romera, E.; González, F.; Ballester, A.; Blázquez, M.; Munoz, J. Comparative study of biosorption of heavy metals using different types of algae. Bioresour. Technol. 2007, 98, 3344–3353. [Google Scholar] [CrossRef] [PubMed]
  47. Singh, R.K.; Chavan, S.L.; Sapkale, P.H. Heavy Metal Concentrations in Water, Sediments and Body Tissues of Red Worm (Tubifex spp.) Collected from Natural Habitats in Mumbai, India. Environ. Monit. Assess. 2006, 129, 471–481. [Google Scholar] [CrossRef]
  48. Pavasant, P.; Apiratikul, R.; Sungkhum, V.; Suthiparinyanont, P.; Wattanachira, S.; Marhaba, T.F. Biosorption of Cu2+, Cd2+, Pb2+, and Zn2+ using dried marine green macroalga Caulerpa lentillifera. Bioresour. Technol. 2006, 97, 2321–2329. [Google Scholar] [CrossRef]
  49. Lee, Y.-C.; Chang, S.-P. The biosorption of heavy metals from aqueous solution by Spirogyra and Cladophora filamentous macroalgae. Bioresour. Technol. 2011, 102, 5297–5304. [Google Scholar] [CrossRef]
  50. Karthikeyan, S.; Balasubramanian, R.; Iyer, C. Evaluation of the marine algae Ulva fasciata and Sargassum sp. for the biosorption of Cu(II) from aqueous solutions. Bioresour. Technol. 2007, 98, 452–455. [Google Scholar] [CrossRef]
  51. Rajfur, M.; Kłos, A.; Wacławek, M. Sorption of copper(II) ions in the biomass of alga Spirogyra sp. Bioelectrochemistry 2012, 87, 65–70. [Google Scholar] [CrossRef]
  52. Hashim, M.; Chu, K. Biosorption of cadmium by brown, green, and red seaweeds. Chem. Eng. J. 2004, 97, 249–255. [Google Scholar] [CrossRef]
  53. Sari, A.; Tuzen, M. Biosorption of Pb(II) and Cd(II) from aqueous solution using green alga (Ulva lactuca) biomass. J. Hazard. Mater. 2008, 152, 302–308. [Google Scholar] [CrossRef] [PubMed]
  54. Gupta, V.; Rastogi, A. Equilibrium and kinetic modelling of cadmium (II) biosorption by nonliving algal biomass Oedogonium sp. from aqueous phase. J. Hazard. Mater. 2008, 153, 759–766. [Google Scholar] [CrossRef]
  55. Rajfur, M.; Kłos, A.; Wacławek, M. Sorption properties of algae Spirogyra sp. and their use for determination of heavy metal ions concentrations in surface water. Bioelectrochemistry 2010, 80, 81–86. [Google Scholar] [CrossRef]
  56. Zakhama, S.; Dhaouadi, H.; M’Henni, F. Nonlinear modelisation of heavy metal removal from aqueous solution using Ulva lactuca algae. Bioresour. Technol. 2011, 102, 786–796. [Google Scholar] [CrossRef] [PubMed]
  57. Ibrahim, W.M. Biosorption of heavy metal ions from aqueous solution by red macroalgae. J. Hazard. Mater. 2011, 192, 1827–1835. [Google Scholar] [CrossRef]
  58. Vilar, V.J.; Botelho, C.M.; Boaventura, R.A. Copper removal by algae Gelidium, agar extraction algal waste and granu-lated algal waste: Kinetics and equilibrium. Bioresour. Technol. 2008, 99, 750–762. [Google Scholar] [CrossRef] [PubMed]
  59. Sari, A.; Tuzen, M. Biosorption of cadmium(II) from aqueous solution by red algae (Ceramium virgatum): Equilibrium, kinetic and thermodynamic studies. J. Hazard. Mater. 2008, 157, 448–454. [Google Scholar] [CrossRef] [PubMed]
  60. Herrero, R.; Lodeiro, P.; García-Casal, L.J.; Vilariño, T.; Rey-Castro, C.; David, C.; Rodríguez, P. Full description of copper uptake by algal biomass combining an equilibrium NICA model with a kinetic intraparticle diffusion driving force approach. Bioresour. Technol. 2011, 102, 2990–2997. [Google Scholar] [CrossRef] [Green Version]
  61. Rathinam, A.; Maharshi, B.; Janardhanan, S.K.; Jonnalagadda, R.R.; Nair, B.U. Biosorption of cadmium metal ion from simulated wastewaters using Hypnea valentiae biomass: A kinetic and thermodynamic study. Bioresour. Technol. 2010, 101, 1466–1470. [Google Scholar] [CrossRef] [PubMed]
  62. Murphy, V.; Hughes, H.; McLoughlin, P. Comparative study of chromium biosorption by red, green and brown seaweed biomass. Chemosphere 2008, 70, 1128–1134. [Google Scholar] [CrossRef]
  63. Holan, Z.R.; Volesky, B. Biosorption of lead and nickel by biomass of marine algae. Biotechnol. Bioeng. 1994, 43, 1001–1009. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Davis, T.; Volesky, B.; Vieira, R. Sargassum seaweed as biosorbent for heavy metals. Water Res. 2000, 34, 4270–4278. [Google Scholar] [CrossRef] [Green Version]
  65. Kleinübing, S.; Silva, E.; da Silva, M.G.C.; Guibal, E. Equilibrium of Cu(II) and Ni(II) biosorption by marine alga Sargassum filipendula in a dynamic system: Competitiveness and selectivity. Bioresour. Technol. 2011, 102, 4610–4617. [Google Scholar] [CrossRef] [Green Version]
  66. Ahmady-Asbchin, S.; Andres, Y.; Gerente, C.; Le Cloirec, P. Biosorption of Cu(II) from aqueous solution by Fucus serratus: Surface characterization and sorption mechanisms. Bioresour. Technol. 2008, 99, 6150–6155. [Google Scholar] [CrossRef] [PubMed]
  67. Luna, A.; Costa, A.; Da Costa, A.C.A.; Henriques, C. Competitive biosorption of cadmium(II) and zinc(II) ions from binary systems by Sargassum filipendula. Bioresour. Technol. 2010, 101, 5104–5111. [Google Scholar] [CrossRef]
  68. Lodeiro, P.; Cordero, B.; Barriada, J.L.; Herrero, R.; de Vicente, M.S. Biosorption of cadmium by biomass of brown marine macroalgae. Bioresour. Technol. 2005, 96, 1796–1803. [Google Scholar] [CrossRef] [Green Version]
  69. Cazón, J.P.; Bernardelli, C.; Viera, M.; Donati, E.; Guibal, E. Zinc and cadmium biosorption by untreated and calci-um-treated Macrocystis pyrifera in a batch system. Bioresour. Technol. 2012, 116, 195–203. [Google Scholar] [CrossRef]
  70. Pahlavanzadeh, H.; Keshtkar, A.; Safdari, J.; Abadi, Z. Biosorption of nickel(II) from aqueous solution by brown algae: Equilibrium, dynamic and thermodynamic studies. J. Hazard. Mater. 2010, 175, 304–310. [Google Scholar] [CrossRef]
  71. Yang, L.; Chen, J.P. Biosorption of hexavalent chromium onto raw and chemically modified Sargassum sp. Bioresour. Technol. 2008, 99, 297–307. [Google Scholar] [CrossRef] [PubMed]
  72. Bermúdez, Y.G.; Rico, I.L.R.; Guibal, E.; de Hoces, M.C.; Martín-Lara, M.Á. Biosorption of hexavalent chromium from aqueous solution by Sargassum muticum brown alga. Application of statistical design for process optimization. Chem. Eng. J. 2012, 183, 68–76. [Google Scholar] [CrossRef]
  73. Guo, D.; Mitchell, R.J.; Withington, J.M.; Fan, P.-P.; Hendricks, J.J. Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: Root branch order predominates. J. Ecol. 2008, 96, 737–745. [Google Scholar] [CrossRef]
  74. Pathe, P.P.; Nandy, T.; Kaul, S.N.; Szpyrokwicz, L. Chromium recovery from chrome tan wastewater. Int. J. Environ. Stud. 1996, 51, 125–145. [Google Scholar] [CrossRef]
  75. Lichtfouse, E.; Elbisser, B. 2nd European Meeting on Environmental Chemistry. In Proceedings of the 2nd European Meeting on Environmental Chemistry, Dijon, France, 12–15 December 2001; p. 273. [Google Scholar]
  76. Vegliò, F.; Quaresima, R.; Fornari, P.; Ubaldini, S. Recovery of valuable metals from electronic and galvanic industrial wastes by leaching and electrowinning. Waste Manag. 2003, 23, 245–252. [Google Scholar] [CrossRef]
  77. Dahbi, S.; Azzi, M.; Saib, N.; De la Guardia, M.; Faure, R.; Durand, R. Removal of trivalent chromium from tannery waste waters using bone charcoal. Anal. Bioanal. Chem. 2002, 374, 540–546. [Google Scholar] [CrossRef]
  78. Park, S.-J.; Jung, W.-Y. Removal of chromium by activated carbon fibers plated with copper metal. Carbon Lett. 2001, 2, 15–21. [Google Scholar]
  79. Bai, R.; Abraham, T. Studies on enhancement of Cr(VI) biosorption by chemically modified biomass of Rhizopus nigricans. Water Res. 2002, 36, 1224–1236. [Google Scholar] [CrossRef]
  80. Chong, K.H.; Volesky, B. Metal biosorption equilibria in a ternary system. Biotechnol. Bioeng. 1996, 49, 629–638. [Google Scholar] [CrossRef] [Green Version]
  81. Lee, S.-J.; Park, J.H.; Ahn, Y.; Chung, J.W. Comparison of Heavy Metal Adsorption by Peat Moss and Peat Moss-Derived Biochar Produced Under Different Carbonization Conditions. Water Air Soil Pollut. 2015, 226, 9. [Google Scholar] [CrossRef]
  82. Ofomaja, A.; Ho, Y.-S. Effect of pH on cadmium biosorption by coconut copra meal. J. Hazard. Mater. 2007, 139, 356–362. [Google Scholar] [CrossRef]
  83. Meunier, N.; Laroulandie, J.; Blais, J.; Tyagi, R. Cocoa shells for heavy metal removal from acidic solutions. Bioresour. Technol. 2003, 90, 255–263. [Google Scholar] [CrossRef]
  84. Tan, L.C.; Choa, V.; Tay, J.H. The Influence of pH on Mobility of Heavy Metals from Municipal Solid Waste Incinerator Fly Ash. Environ. Monit. Assess. 1997, 44, 275–284. [Google Scholar] [CrossRef]
  85. Foday Jr, E.H.; Ramli, N.A.S.; Ismail, H.N.; Malik, N.A.; Basri, H.F.; Aziz, F.S.A.; Nor, N.S.M.; Jumhat, F. Municipal solid waste characteristics in Taman Universiti, Skudai, Johore, Malaysia. J. Adv. Res. Des. 2017, 38, 13–20. [Google Scholar]
  86. Abia, A.; Asuquo, E. Lead (II) and nickel (II) adsorption kinetics from aqueous metal solutions using chemically modified and unmodified agricultural adsorbents. Afr. J. Biotechnol. 2006, 5, 1475–1482. [Google Scholar]
  87. Al-Asheh, S.; Banat, F.; Al-Rousan, D. Adsorption of Copper, Zinc and Nickel Ions from Single and Binary Metal Ion Mixtures on to Chicken Feathers. Adsorpt. Sci. Technol. 2002, 20, 849–864. [Google Scholar] [CrossRef]
  88. Abu Al-Rub, F.A.; Kandah, M.; Al-Dabaybeh, N. Competitive Adsorption of Nickel and Cadmium on Sheep Manure Wastes: Experimental and Prediction Studies. Sep. Sci. Technol. 2003, 38, 483–497. [Google Scholar] [CrossRef]
  89. Özdemir, N.; Horn, R.; Friedt, W. Construction and characterization of a BAC library for sunflower (Helianthus annuus L.). Euphytica 2004, 138, 177–183. [Google Scholar] [CrossRef]
  90. Ajmal, M.; Rao, R.A.K.; Anwar, S.; Ahmad, J.; Ahmad, R. Adsorption studies on rice husk: Removal and recovery of Cd(II) from wastewater. Bioresour. Technol. 2003, 86, 147–149. [Google Scholar] [CrossRef]
  91. Ajmal, M.; Rao, R.A.K.; Ahmad, R.; Ahmad, J. Adsorption studies on Citrus reticulata (fruit peel of orange): Removal and recovery of Ni(II) from electroplating wastewater. J. Hazard. Mater. 2000, 79, 117–131. [Google Scholar] [CrossRef]
  92. Fiol, N.; Villaescusa, I.; Martínez, M.; Miralles, N.; Poch, J.; Serarols, J. Sorption of Pb (II), Ni (II), Cu (II) and Cd (II) from aqueous solution by olive stone waste. Sep. Purif. Technol. 2006, 50, 132–140. [Google Scholar] [CrossRef]
  93. Kapoor, A.; Viraraghavan, T. Heavy metal biosorption sites in Aspergillus niger. Bioresour. Technol. 1997, 61, 221–227. [Google Scholar] [CrossRef]
  94. Vaishya, R.; Prasad, S. Adsorption of copper (II) on sawdust. Indian J. Environ. Prot. 1991, 11, 284–289. [Google Scholar]
  95. Vázquez, G.; Antorrena, G.; González-Álvarez, J.; Doval, M. Adsorption of heavy metal ions by chemically modified Pinus pinaster bark. Bioresour. Technol. 1994, 48, 251–255. [Google Scholar] [CrossRef]
  96. Srivastava, S.K.; Gupta, V.K.; Mohan, D. Removal of Lead and Chromium by Activated Slag—A Blast-Furnace Waste. J. Environ. Eng. 1997, 123, 461–468. [Google Scholar] [CrossRef]
  97. Bailey, S.E.; Olin, T.J.; Bricka, R.; Adrian, D. A review of potentially low-cost sorbents for heavy metals. Water Res. 1999, 33, 2469–2479. [Google Scholar] [CrossRef]
  98. Keskinkan, O.; Goksu, M.; Basibuyuk, M.; Forster, C. Heavy metal adsorption properties of a submerged aquatic plant (Ceratophyllum demersum). Bioresour. Technol. 2004, 92, 197–200. [Google Scholar] [CrossRef]
  99. Gardea-Torresdey, J.; Peralta-Videa, J.; Montes, M.; de la Rosa, G.; Corral-Diaz, B. Bioaccumulation of cadmium, chromium and copper by Convolvulus arvensis L.: Impact on plant growth and uptake of nutritional elements. Bioresour. Technol. 2004, 92, 229–235. [Google Scholar] [CrossRef]
  100. Dumitriu, S. Polysaccharides as Biomaterials. In Polymeric Biomaterials, Revised and Expanded; CRC Press: New York, NY, USA, 2001; pp. 15–76. [Google Scholar]
  101. Brown, P.; Gill, S.; Allen, S.J. Determination of optimal peat type to potentially capture copper and cadmium from solu-tion. Water Environ. Res. 2001, 73, 351–362. [Google Scholar] [CrossRef]
  102. Celis, R.; Hermosín, M.C.; Cornejo, J. Heavy Metal Adsorption by Functionalized Clays. Environ. Sci. Technol. 2000, 34, 4593–4599. [Google Scholar] [CrossRef]
  103. Cameron, H.; Mata, M.T.; Riquelme, C. The effect of heavy metals on the viability of Tetraselmis marina AC16-MESO and an evaluation of the potential use of this microalga in bioremediation. PeerJ 2018, 6, e5295. [Google Scholar] [CrossRef] [Green Version]
  104. Sun, K.; Tang, J.; Gong, Y.; Zhang, H. Characterization of potassium hydroxide (KOH) modified hydrochars from different feedstocks for enhanced removal of heavy metals from water. Environ. Sci. Pollut. Res. 2015, 22, 16640–16651. [Google Scholar] [CrossRef] [PubMed]
  105. Priatni, S.; Kosasih, W.; A Budiwati, T.; Ratnaningrum, D. Production of peptone from boso fish (Oxyeleotris marmorata) for bacterial growth medium. In IOP Conference Series: Earth and Environmental Science; IOP Publishing: Tangerang, Indonesia, 2017; p. 012009. [Google Scholar]
  106. Upadhyay, A.; Singh, N.; Singh, R.; Rai, U. Amelioration of arsenic toxicity in rice: Comparative effect of inoculation of Chlorella vulgaris and Nannochloropsis sp. on growth, biochemical changes and arsenic uptake. Ecotoxicol. Environ. Saf. 2016, 124, 68–73. [Google Scholar] [CrossRef]
  107. Gómez-Jacinto, V.; García-Barrera, T.; Gómez-Ariza, J.L.; Garbayo-Nores, I.; Vílchez-Lobato, C. Elucidation of the defence mechanism in microalgae Chlorella sorokiniana under mercury exposure. Identification of Hg–phytochelatins. Chemi-Co-Biol. Interact. 2015, 238, 82–90. [Google Scholar] [CrossRef]
  108. Balaji, S.; Kalaivani, T.; Sushma, B.; Pillai, C.V.; Shalini, M.; Rajasekaran, C. Characterization of sorption sites and differ-ential stress response of microalgae isolates against tannery effluents from Ranipet industrial area—An application towards phycoremediation. Int. J. Phytoremediat. 2016, 18, 747–753. [Google Scholar] [CrossRef]
  109. Devars, S.; Avilés, C.; Cervantes, C.; Moreno-Sánchez, R. Mercury uptake and removal by Euglena gracilis. Arch. Microbiol. 2000, 174, 175–180. [Google Scholar] [CrossRef] [PubMed]
  110. Pradhan, P.; Costa, L.; Rybski, D.; Lucht, W.; Kropp, J.P. A systematic study of sustainable development goal (SDG) in-teractions. Earth’s Future 2017, 5, 1169–1179. [Google Scholar] [CrossRef] [Green Version]
  111. Ibuot, A.; Dean, A.P.; McIntosh, O.A.; Pittman, J.K. Metal bioremediation by CrMTP4 over-expressing Chlamydomonas reinhardtii in comparison to natural wastewater-tolerant microalgae strains. Algal Res. 2017, 24, 89–96. [Google Scholar] [CrossRef]
Sustainability 13 12311 g001 550
Figure 1. Categories of heavy metal sources.
Figure 1. Categories of heavy metal sources.
Sustainability 13 12311 g001
Sustainability 13 12311 g002 550
Figure 2. Sources of heavy metals.
Figure 2. Sources of heavy metals.
Sustainability 13 12311 g002
Sustainability 13 12311 g003 550
Figure 3. Heavy metal contamination in water.
Figure 3. Heavy metal contamination in water.
Sustainability 13 12311 g003
Sustainability 13 12311 g004 550
Figure 4. Structure of seaweed.
Figure 4. Structure of seaweed.
Sustainability 13 12311 g004
Sustainability 13 12311 g005 550
Figure 5. Mechanism of metal ion interaction with seaweed.
Figure 5. Mechanism of metal ion interaction with seaweed.
Sustainability 13 12311 g005
Sustainability 13 12311 g006 550
Figure 6. Interaction between metal ions and algal biomass.
Figure 6. Interaction between metal ions and algal biomass.
Sustainability 13 12311 g006
Table
Table 1. Accepted thresholds of toxic metal ions in drinking water.
Table 1. Accepted thresholds of toxic metal ions in drinking water.
Drinking Water Acceptable Standards in (mg L−1)
MetalsWHO [20]USEPA [21]EU Standard [22]MEE-China [23]DWI-UK [24]
Nickel (Ni)0.07-0.0200.0000.02
Lead (Pb)0.010.0150.0050.0100.01
Zinc (Zn)-5.0-0.05-
Copper (Cu)2.01.02.0001.0002.0
Cadmium (Cd)0.0030.0050.0050.0050.005
Mercury (Hg)0.0060.0020.0010.000050.001
Arsenic (As)0.010.0100.010.0500.01
Chromium (Cr)0.050.1000.0250.0500.05
Antimony0.02-0.01-0.005
Bromate0.01-0.01-0.01
Uranium0.030.030.03--
Table
Table 2. Characteristics of Seaweed.
Table 2. Characteristics of Seaweed.
Common Name (Phylum)Body FormSizePigmentsColour CompositionCell Walls
Brown algae (Phaeophyta)Multicellular60 cm–60 mChlorophyll, Fucoxanthin, and several other xanthophyllsGolden-brown, Greenish-brownCellulose, Alginate, Fucoidan
Red algae (Rhodophyta)Multicellular50 cm–2 mChlorophyll, Phycocyanin, Phycoerythrin, and several xanthophyllsBrownish red, PurpleCellulose, Xylans,
Galactans
Green algae (Chlorophyta)Unicellular, Colonial, Filamentous, Multicellular1–1000 μma and b Chlorophyll and several xanthophyllsGreenCellulose Hydroxyl –proline glucosides
β- xylans,
β-mannans
Table
Table 3. Different algae species for heavy metal removal.
Table 3. Different algae species for heavy metal removal.
Species of AlgaeMetal Ionsqmax (mmol/g)pHReferences
Green Algae
Ulva lactucaPb(II)0.614.5[45]
Cladophora glomerata0.354.5[45]
Ulva sp. 1.465.0[33]
Codium vermilara0.305.0[46]
Spirogyra insignis0.245.0[46]
Spirogyra neglecta0.565.0[47]
Caulerpa lentillifera0.135.0[48]
Spirogyra sp. 0.435.0[49]
Cladophora sp. 0.225.0[49]
Ulva sp. Cu(II)0.755.0[33]
Codium vermilara0.265.0[46]
Spirogyra insignis0.304.0[46]
Spirogyra neglecta1.804.5[47]
Ulva fasciata1.145.5[50]
Caulerpa lentillifera0.085.0[48]
Cladophora sp0.235.0[49]
Spirogyra sp0.535.0[51]
Ulva sp. Cd(II)0.585.5[33]
Chaetomorpha linum0.485.0[52]
Codium vermilara0.196.0[46]
Spirogyra insignis0.206.0[46]
Ulva lactuca0.255.0[53]
Oedogonium sp. 0.795.0[54]
Caulerpa lentillifera0.045.0[48]
Spirogyra sp. 0.006 a-[55]
Ulva sp. Zn(II)0.545.5[33]
Codium vermilara0.366[46]
Spirogyra insignis0.326[46]
Caulerpa lentillifera0.045[48]
Spirogyra s0.02 a-[55]
Ulva sp. Ni(II)0.295.5[33]
Codium vermilara0.226.0[46]
Spirogyra insignis0.296.0[46]
Ulva lactuca1.144.5[56]
Red Algae
Gracilaria corticataPb(II)0.264.5[45]
Gracilaria canaliculata0.204.5[45]
Polysiphonia violacea0.494.5[45]
Gracillaria sp. 0.455.0[33]
Asparagopsis armata0.304.0[46]
Jania rubens0.145.0[57]
Pterocladia capillacea0.165.0[57]
Corallina mediterranea0.315.0[57]
Galaxaura oblongata0.425.0[57]
Asparagopsis armata0.335.0[46]
Chondrus crispus0.634.0[46]
Gelidium0.515.3[58]
Gracilaria changii0.235.0[52]
Gracilaria edulis0.245.0[52]
Gracilaria Salicornia0.165.0[52]
Asparagopsis armata0.286.0[46]
Ceramium virgatum0.355.0[59]
Mastocarpus stellatus0.596.0[60]
Jania rubens0.275.0[57]
Corallina mediterranea0.575.0[57]
Hypnea valentiae0.156.0[61]
Palmaria palmateCr0.57 (Cr(III))4.5 (Cr(III[62]
0.65 (Cr(VI))2 (Cr(VI))
Polysiphonia lanosa0.65 (Cr(III))4.5(Cr(III))[62]
0.88 (Cr(VI))2 (Cr(VI))
Jania rubens0.54 (Cr(III))5.0 (Cr(III))[57]
Pterocladia capillacea0.66 (Cr(III))5.0 (Cr(III))[57]
Corallina mediterranea1.35 (Cr(III))5.0 (Cr(III))[57]
Galaxaura oblongata2.02 (Cr(III))5.0 (Cr(III))[57]
Jania rubensCo(II)0.555.0[57]
Pterocladia capillacea0.895.0[57]
Corallina mediterranea1.295.0[57]
Galaxaura oblongata1.255.0[57]
Brown Algae
Ascophyllum nodosumPb(II)1.313.5[63]
Fucus vesiculosus1.113.5[63]
Sargassum vulgare1.103.5[63]
Sargassum hystrix1.374.5[45]
Sargassum natans1.144.5[45]
Padina pavonia1.044.5[45]
Sargassum sp. 1.165.0[33]
Padina sp. 1.255.0[33]
Fucus vesiculosus1.025.0[38]
Fucus spiralis0.983.0[46]
Ascophyllum nodosu0.863.0[46]
Padina sp. Cu(II)1.145.0[33]
Sargassum vulgarie0.934.5[64]
Sargassum fluitans0.804.5[64]
Sargassum filipendula0.894.5[64]
Fucus vesiculosus1.665.0[38]
Fucus spiralis1.104.0[46]
Ascophyllum nodosum0.914.0[46]
Sargassum filipendula1.324.5[65]
Fucus serratus1.605.5[66]
Sargassum sp. 1.135.5[50]
Sargassum sp. Cd(II)0.765.5[33]
Padina sp0.755.5[33]
Sargassum siliquosum0.735.0[52]
Sargassum baccularia0.745.0[52]
Padina tetrastomatica0.535.0[52]
Sargassum vulgarie0.794.5[64]
Sargassum fluitans0.714.5[64]
Sargassum muticum0.684.5[64]
Fucus vesiculosus0.966.0[38]
Fucus spiralis1.026.0[46]
Ascophyllum nodosum0.786.0[46]
Sargassum filipendula1.175.0[67]
Bifurcaria bifurcate0.654.5[68]
Saccorhiza polyschides0.844.5[68]
Ascophyllum nodosum0.704.5[68]
Laminaria ochroleuca0.564.5[68]
Pelvetia caniculata0.664.5[68]
Macrocystis pyrifera0.893.0[69]
Sargassum sp. Zn(II)0.505.5[33]
Padina sp. 0.815.5[33]
Fucus spiralis0.816.0[46]
Ascophyllum nodosum0.646.0[46]
Sargassum filipendula0.715.0[67]
Macrocystis pyrifera0.914.0[69]
Sargassum fluitansNi(II)0.753.5[63]
Ascophyllum nodosum0.693.5[63]
Sargassum natans0.413.5[63]
Fucus vesiculosus0.393.5[63]
Sargassum vulgare0.093.5[63]
Sargassum sp0.615.5[33]
Padina sp. 0.635.5[33]
Cystoseria indica0.856.0[70]
Nizmuddinia zanardini0.946.0[70]
Sargassum glaucescensand0.946.0[70]
Padina australis0.466.0[70]
Fucus spiralis0.856.0[46]
Ascophyllum nodosum0.736.0[46]
Sargassum filipendula1.074.5[65]
Fucus vesiculosusCr1.21 (Cr(III))4.5 (Cr(III))[62]
0.82 (Cr(VI))2 (Cr(VI))
Fucus spiralis1.17 (Cr(III))4.5 (Cr(III))[62]
0.68 (Cr(VI))2 (Cr(VI))
Sargassum sp. 0.60 (Cr(VI))2 (Cr(VI))[71]
Sargassum muticum3.77 (Cr(VI))2 (Cr(VI))[72]
a = Not maximum biosorption value.
Table
Table 4. Various natural materials used for the removal of metal ions.
Table 4. Various natural materials used for the removal of metal ions.
Materials UsedHeavy MetalsReferences
PolymersFe and Cr[74]
Sawdust and tree barksHg, Pb, and Zn[75]
Electronic waste along with galvanic wastesCu, Ni, Mn, Pb, Sn[76]
charcoal:Cr(III)[77]
ClayCr(III)[78]
FungiCr, Fe[79]
Dead biomassCr[80]
Peat mossCr, Fe[81]
Peanut shells, Rice husk, Straw, and walnut coverCr, Cu, Ni[82]
Cocoa shellAl, Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, and Zn[83]
Coconut huskCr, As[82]
Caol and fly ashesCr, Cu, Ni[84]
Banana pith and peelsNi, Pb[85]
Cassava fiberPb, Co[86]
Chicken feathersAl, As[87]
Sheep manure wastesCa, Cd[88]
SunflowerCo, Cr[89]
Rice byproductsCu, Fe[90]
Orange peelsCu, Fe, Hg[91]
Palm kernel fiberFe, Hg[82]
Grape stalksCr, Fe, Hg[92]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Foday Jr, E.H.; Bo, B.; Xu, X. Removal of Toxic Heavy Metals from Contaminated Aqueous Solutions Using Seaweeds: A Review. Sustainability 2021, 13, 12311. https://doi.org/10.3390/su132112311

AMA Style

Foday Jr EH, Bo B, Xu X. Removal of Toxic Heavy Metals from Contaminated Aqueous Solutions Using Seaweeds: A Review. Sustainability. 2021; 13(21):12311. https://doi.org/10.3390/su132112311

Chicago/Turabian Style

Foday Jr, Edward Hingha, Bai Bo, and Xiaohui Xu. 2021. "Removal of Toxic Heavy Metals from Contaminated Aqueous Solutions Using Seaweeds: A Review" Sustainability 13, no. 21: 12311. https://doi.org/10.3390/su132112311

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop