What do we know about the utilization of the Sargassum species as biosorbents of trace metals in Brazil?

Highlights

• The Sargassum spp. has biosorbent potential for metal removal in Brazil.

• Metal synergism and physical-chemical parameters affect the biosorption.

• Copper presented the highest affinity with Sargassum among tested metals.

• Metal biosorption by Sargassum may be more cost-effective than traditional methods.

Abstract

In the last decades, metal pollution has become one of the most critical environmental and public health concerns. Human use and processing of trace metals have altered these metals’ natural biogeochemical cycles, which is causing adverse impacts on human beings, natural communities, and aquatic ecosystems. In Brazil, mining and smelting are relevant metal contamination sources that affect many aquatic systems, besides agricultural residues, industrial and urban effluent discharges. In this context, seaweed biosorption is a promising technology for the removal of metals from wastewater that could prevent environmental contamination. Seaweeds show high metal sequestering capacities, cost-effectiveness, and eco-friendliness. In this review, we aimed to assess previous studies on trace metals biosorption using the brown seaweed of the genus Sargassum conducted in Brazil during the last two decades (1999–2019). An overview of metal pollution in Brazil and its possible treatments are presented. A theoretical basis regarding Sargassum and its mechanism of sorption of trace metals is described. We also discuss previous Brazilian studies on this topic, including their aims, the trace metals analyzed, and the experimental conditions that increase biosorption effectiveness, which include pH, temperature, algae pretreatment, and immobilization of the biosorbent in a matrix. Given the abundance of this genus throughout the Brazilian coast and its high metal recovering capacity, the algae sorption process remains an underexplored resource. We conclude this work with a patent search and a discussion of the future perspectives of Sargassum use by society.

Introduction

The term “trace metal” refers to any chemical element found at low concentrations (less than 100 μg g⁻¹) in the environment or biological compartments [1]. Among them are the so-called heavy metals, a group that is generally considered highly toxic. Nevertheless, the scientific classification for the term “heavy metal” is very controversial and has recently been subjected to a broad discussion [2]. Therefore, the decision was made to use the more general term “trace metals” in this text.

Some of these elements, including lead (Pb) and cadmium (Cd), do not have any known biological roles and are toxic to living beings, even at small concentrations. On the other hand, many trace metals, e.g., nickel (Ni), chromium (Cr), copper (Cu), manganese (Mn), and zinc (Zn), are considered essential because they have vital metabolic and redox functions in humans and other organisms. However, even essential metals are potentially toxic at high bioavailable concentrations in the environment, leading to numerous adverse impacts on biota [3,2,4].

The primary natural sources of trace metals in the environment are rock weathering, soil erosion, volcanic activities, dust storms, and wildfire [5,6]. However, human use and processing of trace metals have severely altered their natural biogeochemical cycle, making metals contamination one of the most critical environmental and public health concerns [6,7]. Anthropic activities associated with metal pollution include mining, smelting, the combustion of fossil fuels, the release of industrial, pharmaceutical, and chemical wastes, the incorrect disposal of electronic wastes and manufactured products, ferrous and non-ferrous metal production, the use of pesticides and fertilizers, among others [[5], [6], [7], [8]].

Trace metals reach aquatic ecosystems mainly by continental runoff, the release of effluents, contaminated groundwater, and atmospheric deposition [6,9]. Once in the aquatic environment, metals can associate with organic and inorganic components dissolved in water or with particulate matter, or be absorbed by living organisms, although the dominant part is attached to the sediment [[10], [11], [12]]. In this compartment, metals can be adsorbed or desorbed to/from the sediment particle surface. Metals can precipitate as carbonates, sulfates, or oxides, co-precipitate with iron and manganese oxides, bind with organic matter, or be incorporated into the crystalline network of primary and secondary minerals. When incorporated into the minerals, these metals are firmly bound to the sediment constituents and are not bioavailable [[10], [11], [12], [13], [14]]. In the other cases, metals can be available to organisms, as variations in biogeochemical parameters such as salinity, temperature, pH, redox potential, organic matter content, the microbial community, and concentrations of iron and manganese oxides can make them re-accessible to the food chain [9,10,13,15]. Therefore, beyond its concentration and speciation, trace metal toxicity is related to the environmental physicochemical conditions [13,10,11].

As trace metals are non-degradable, they may persist in the environment for a long time [6,7,9]. Many marine organisms can bioaccumulate metals in their tissues and organs throughout their life cycle [6,10,[16], [17], [18]]. Marine biota transfer metals through the trophic chain, in a process known as biomagnification [6,9,10,16,18]. Metals damage the DNA and enzymatic processes of organisms, affecting cellular and tissue functions and leading to disturbances in growth, reproduction, the immune system, and metabolism, or even to death. These individual-level effects, in turn, are reflected at the population and community levels. Therefore, metals act as a disturbing factor in natural communities, decreasing diversity and favoring opportunistic species [[19], [20], [21]]. In humans, metals can cause many deleterious effects, including carcinogenic, mutagenic, and neurotoxic effects [22,2,4,6].

In Brazil, mining is a historically significant economic activity fundamental to the country’s industrialization [23]. Copper, manganese, and nickel are among the main metallic substances explored, representing 7.6 %, 1.3 %, and 3.5 % of Brazil’s metal production, respectively. The gross production of these metals is concentrated mainly in Pará and Goiás states; in 2016 alone, Brazil exported a total value of almost 3 billion dollars’ worth of copper, 300 million dollars’ worth of manganese, and 620 million dollars’ worth of nickel [23].

Mining activities can contribute to local and extensive metal contamination. Veado et al. [24] showed the carriage of contaminated water and sediment within a distance of approximately 400 km from the mining source, reaching the ichthyofauna and a farming location. Likewise, Jordão et al. [25] found high concentrations of several metals in the river water and sediment, plants, and fishes collected from a smelting region in Minas Gerais state.

In addition to mining and smelting, agricultural residues and industrial and urban effluent discharges are relevant sources of metal contamination in Brazil, affecting many aquatic systems in the country [16,26,27]. In this way, the search for and development of biotechnological solutions to this problem are crucial. Macroalgae have been used as monitors of trace metals in coastal environments [28]. Researches on Sargassum spp. metal sequestering capacity is widespread throughout the Brazilian coast [[29], [30], [31], [32]]. However, no studies focus on large scale wastewater treatment or Sargassum spp. as a commercial biosorbent. Considering the need to promote further studies and new approaches to this topic, this review focuses on the Genus Sargassum as a metal biosorbent in Brazil, gathering and comparing postulated data and pointing to future perspectives on the community’s use of the algae biosorption process.

To treat metal-contaminated wastewater, many techniques have been studied and applied, including chemical precipitation, coagulation-flocculation, ion exchange, membrane filtration, electrochemical processes, microbial electrochemical technology, and adsorption through the biosorption variant. In the next paragraphs, we will present a summary of those techniques.

Chemical precipitation is a process in which ions of metals are converted into solid particles using pH variation [33]; these ions include carbonates, hydroxides, and metal sulfides [34]. Although this is an efficient technique for treating high concentrations of metals, a significant number of chemical agents and operations are required to treat the resulting hazardous sludge [35].

Coagulation is a physicochemical process that destabilizes colloidal particles. The addition of coagulating agents such as iron and aluminum salts increase the ionic strength of the colloidal particle [36]. This process facilitates aggregation and decanting by gravity due to the reduction in particle surface charges [37]. Subsequently, the flocculation process takes place, in which non-sedimentary and slow sedimentation colloidal particles are agglomerated as large-volume flocs, improving their decanting [35].

The membrane filtration technique considers the permeability gradient of the compounds present in the effluent. Membranes retain impermeable substances present in the effluent feed inlet [38]. The technique has proven effective at removing toxic metals [39]. The advantage of this technique is that it generates a low amount of waste, under the use of chemicals and materials [40], although the initial cost and energy consumption of the operation are high [35]. The removal of toxic metals from wastewater has been carried out by nanofiltration, ultrafiltration, electrodialysis, and reverse osmosis [41].

With electrochemical processes, an electrical potential for the migration of charged ionic particles is applied from one medium to another. Some of the techniques used for the recovery of toxic metals in wastewater are electroflotation, electrocoagulation, and electroplating [42,43]. The advantages of this unitary process are high selectivity, purity in metal recovery, and the fact that chemical reagents are not needed [40], while its disadvantages are high investment and operating costs, such as those related to energy consumption [41].

The ion exchange technique is a physicochemical process in which dissolved metal ions are replaced with equivalent amounts of other ions of the same charge on a solid material called an ion exchanger or resin [44]. Ion exchange presents advantages such as ease in the concentrated recovery of metals, low energy consumption, optimal operating costs, and the fact that it does not generate hazardous sludge [45].

Application of microbial electrochemical technologies (MET) is an emerging strategy in the treatment of effluents, which combines the postulates of electrochemistry and microbiology [46]. MET is originated from the process called extracellular electron transfer (EET), in which the metabolism of microorganisms is attached to solid-state electrodes [47]. It occurs due to the ability of some microbes, called electroactive, to use a solid electrode to donate and receive electrons. In this way, within microbial metabolism, the electrode replaces the role of electron acceptor for oxygen and nitrogen, as well as it can replace the role of organic matter and hydrogen in electron donation. Based on the characteristics of the effluents, contaminating ions and energetic requirements of the treatment, a MET platform can be developed as a microbial fuel cell (MFC) or as a microbial electrolysis cell (MEC) [46]. MFC corresponds to an independent device, where the energy is extracted, while in the MEC, the energy is supplied to carry out a bioelectrochemical process [48].

For the specific case of removal and recovery of metals from industrial effluents through MFC processes, configurations such as the electrochemical reduction in the cathode chamber, elimination by the anode route and absorption of metal ions by microorganisms present in the cathode have been used [49]. According to Pous et al. [48], MET in the treatment of effluents can be a viable technology due to low cost, low consumption of chemical products, and using dose selective and non-invasive. Also, Das et al. [49] indicate that MET is an excellent option for the treatment of organic refractory compounds and industrial effluents because removing contaminants from the effluents, to allowed recovering metals and generating electricity simultaneously during the process.

In addition, MFC technology can also capture atmospheric carbon dioxide during wastewater treatment and bioelectricity production [50]. It can be achieved by adding plants in the MFC anode chamber, a concept called P-MFC. In this process, CO₂ and solar rays are used in photosynthesis. Moreover, products stored in rhizodeposits can be oxidized by electrogenic microorganisms, generating new microbial matter, electrons, protons, and other by-products [50]. Therefore, anaerobic oxidation in the anodic chamber of P-MFC allows the reduction of methane and the use of CO₂, to later recover a by-product of the process, such as electricity [50].

Adsorption, in general terms, is the transfer of particles from the solution or liquid phase to the surface of a solid phase, called adsorbent. The mass transference can be achieved through physical, chemical, and electrostatic interactions [51,38]. The adsorption depends on factors such as the presence of acidic or basic functional groups on the adsorbent surface, the nature of the adsorbent, and the injection of toxic metal ions to the specific functionality with the adsorbent [52]. Because adsorption is a surface process, an adsorbent material must have various characteristics, including a high surface-volume ratio, selectivity, mechanical stability, easy accessibility, simple regeneration, non-toxicity, cost-effectiveness, and ease in use during operation [53]. For decades, activated carbon was the adsorbent of choice for industrial wastewater treatment [[54], [55], [56]]. In recent decades, there has been great interest in the use of adsorbent materials of biological origin, which, in turn, has led to an increase in the number of publications on the biosorption process [[57], [58], [59], [60]].

Biosorption became an attractive and emerging biological technology for the removal and recovery of heavy metals from wastewater due to its efficient results in terms of capture, as well as due to its ease in operation and the high availability of biomass [61,62]. This term has different definitions, some of them simpler than others. Gadd [63] emphasizes, in general terms, that biosorption is a physical-chemical process in which substances of a solution are removed using biological material. Specifically, adsorption occurs through the physical adhesion or union of ions and molecules to the surface of another molecule [64]. Likewise, Segretin et al. [65] and Davis et al. [66] define biosorption as a specific process of adsorption, determined by the passive capture of pollutants by inactive or dead biological material (non-living biomass) or adsorbent material, through various physicochemical mechanisms. Biosorption activity is not related to the metabolic process itself. Indeed, it is related to inactive or passive processes in which toxic metal ions are adsorbed on the surface of the biomass. Thus, biosorption is a phenomenon contrary to bioaccumulation, an active process that interferes with the organism’s metabolic activities [67].

The biosorption process comprises a solid phase known as a biosorbent, a solvent or liquid-phase (which is the effluent to be treated), and a third element known as sorbate (which is the contaminating compounds dissolved in the liquid phase) [57]. For this reason, biosorbent studies embrace a great variety of raw organisms, including marine algae, and the organic residue of industries that utilize biomass as raw material. These algae have received considerable attention due to their high capacity to capture toxic metals [[68], [69], [70]]. The seaweed biosorption phenomenon focuses directly on the cell wall of the algae, the biochemical constituents, and the chemical composition of the water to be treated [71].

Sargassum C. Agardh (Phaeophyceae, Fucales) is a conspicuous macroalga that forms banks on tropical and subtropical coasts worldwide [72]. It comprises 358 taxonomically accepted species [73], of which 14 are currently recognized as occurring along the Brazilian coast [74]. Sargassum’s populations, biomass, and their phenological features are affected by the temperature, the hydrodynamic of the locality, and flora and fauna associated with its thallus [[75], [76], [77], [78], [79]]. Due to its ecological importance, Sargassum species have been studied in Brazil as bioindicators of anthropogenic changes, such as organic [80] and thermal [81] pollution, the bioaccumulation of radionuclides (e.g. [[82], [83], [84], [85]],), the biostimulant of growth on olericulture [86] and others. In short, there is no established structural pattern of Sargassum species on benthic marine communities of the Brazilian coast [87].

Brown algae are known for their low resistance to high levels of organic pollution. Organic pollutants, including hydrocarbons, may affect the brown algae reproduction cycle [88]. Ammonia in concentrations higher than 50 μM may reduce photosynthesis performance [89]. However, there is not a study that defines the proper tolerance of the living brown algae for the toxicity of organic pollutants. When compared to red and green algae, Sargassum spp. are highly resistant to and tolerant of, heavy metals, as they can be found on the rocky shores of beaches contaminated by large concentrations of these chemical elements [90,91]. Due to this characteristic, Sargassum has been broadly investigated in terms of the absorption of metals [92]. The sorption is possible because of the presence of binding sites created by different functional groups like hydroxyl, carboxyl, sulfhydryl, sulfate, and amino groups on the cell wall surface [93] (Fig. 1). These groups with negative charges allow for ionic binding sites, i.e., natural ion-exchange reactions with protonated groups from the surface [94]. The justification of the higher capacity of brown algae as opposed to red or green algae lies in the existence of alginate in the former, constituting almost 40 % of the dry mass [95,96]. This compound is a linear polysaccharide of covalently linked blocks of 1,4-linked β-d-mannuronic (M) and α-l-guluronic (G) acid residues. The reactivity of the polysaccharide is influenced by the sequence of these blocks [97], which is related to the species [98], the season [99], and the age and source of the algae [100,101]. Hence, the better performance of the sorption of metals by Sargassum through the properties of the alginate (i.e., solubility, interaction with metal ions, viscosity) will rely upon these polysaccharide structures [102].

In recognition of the high metal sequestering capacity of genus Sargassum and the biotechnological potential of its biosorption process, this review aims: (1) to provide information about what has been done on the use of Sargassum sp. as a metal biosorbent in Brazil; (2) to explore postulated data on the conditions that increase metal uptake process effectiveness; (3) to point future perspectives on the community’s use of the algae biosorption process for the treatment of wastewater contaminated by metals. Toward this, a literature review was carried out covering two decades (1999–2019) of published papers on Sargassum spp. collected on the Brazilian coast as biosorbents of trace metals. The search for published research made use of the Onefile®, PubMed®, Science Citation Index Expanded®, Science Direct®, Scielo®, Google Scholar®, and Scopus® databases using the following keywords: Sargassum, biosorption, adsorption, metals, and Brazil.