Abstract
Marine environment is a predominant player in the overall ecosystem functioning with almost half of oxygen evolution into the atmosphere through the photosynthetic activity of plankton communities. Anthropogenic activities cause pollution at an enhanced pace and pose a major threat to the biological cyclings in the marine ecosystem. Pollutants such as heavy metals and organic compounds in the marine environment are a serious concern as they are associated with complex challenges. Marine microalgae are promising candidates in remediating inorganic and organic pollutants due to their versatile metabolic mechanisms. The present chapter provides a comprehensive understanding of the response of marine microalgae in the removal of heavy metals and organic pollutants. Initially, we present the importance of microalgae and the sources of heavy metals and organic pollutants that reach the marine environment besides highlighting the merits and demerits of the conventional and biological treatment systems used for the removal of these pollutants. Finally, we provide a general perspective on the implication of marine microalgae and the associated mechanisms in the removal of heavy metals and organic pollutants.
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3.1 Introduction
The environment is the global ecological life-supporting system that has been affected in complex and accelerating ways because of pervasive and profound human activities. The past few decades witnessed rapid industrial development, population growth, economic wealth, and urbanization, which ultimately disturb the very processes and components of the nature. Marine ecosystems are at serious risk due to the elevated levels of pollutants discharged from industrial and domestic activities (Bergmann et al. 2015; Nelms et al. 2017). The impact of these pollutants on coastal zone has been significantly greater in estuaries due to their residence time than in inland rivers (Saldarriaga-Hernandez et al. 2020). In fact, the occurrence of both heavy metals and organic pollutants in the marine environment is of significant ecological concern. International scientific experts on marine protection define marine pollution as “chemicals introduced by human activities either directly or indirectly into the marine environment affecting the biota and impairment of water quality” (Kuppusamy et al. 2020). Fish inhabiting polluted waters was reported to accumulate metals in the tissues and the accumulation depends on various biotic and abiotic factors (Zeitoun and Mehana 2014). The heavy metals tend to be widely distributed in liver, kidney, and other tissues and potentially get transferred to humans as they are at the top of the food web (Gabriel et al. 2006). Oils are the major sources of organic contaminants released into the marine environment either during processing or accidentally from drilling, production, and storage (Kuppusamy et al. 2020). Consequently, the deteriorated health of the oceans around the world impacted the social and economic status and prompted to bring international options for safer and healthier marine systems (Gelcich et al. 2014).
Several environmental agencies recognized the severity of these pollutants and proposed various policies in reducing the risk toward marine biota. For instance, a list of priority pollutants that should be universally avoided has been prepared as they can cause shorter or longer effects in any ecosystem (Grip 2017; Beiras 2018). The United States Environmental Protection Agency recently updated the priority pollutant list in the Clean Water Act, which includes several heavy metals, organic contaminants such as dyes, phenols, organophosphates, etc. (USEPA 2014). The United Nations Convention on Law of Sea proposed major duties for member states to investigate potential threats in the marine environment (Stelzenmüller et al. 2018). European Commission endorsed the marine strategy framework directive with an aim to manage Europe-bound seas to gain a healthy state following an ecosystem-based approach (Borja et al. 2013; Danovaro et al. 2016). Marine environments contain several biotas together with marine microalgae that serve as the primary producers and can also be used as sensitive bioindicators (Torres et al. 2008). This chapter highlights the implication of marine microalgae in the removal of heavy metals and organic pollutants.
3.2 Marine Microalgae—An Overview
Marine environments are inhabited by assemblages of several organisms (Tragin and Vaulot 2018). The diversity of marine plankters based on their size is presented in Fig. 3.1. They are easily distinguished based on the nutrition mode: autotrophic organisms, referred to as phytoplankton (microalgae), and grazing organisms, called zooplankton. In addition, marine microalgae are the major primary producers in the marine environment that use solar energy for CO2 uptake, thus contributing to ocean carbon sink (Huang et al. 2017). These microalgae are generally divided into two lineages such as green and red, with the former being originated by primary and the latter from the secondary or tertiary endosymbiotic process (Nakayama et al. 1998). Chlorophyta is the major algal group in marine waters representing the green lineage, whereas the protists and dinoflagellates fall within the red lineage. Chlorophyta encompasses prasinophytes and chlorophytes, where the abundance is dominated later with Ulvophyceae, Trebouxiophyceae, and Chlorophyceae, all known as the UTC Clade (Leliaert et al. 2012; Fučíková et al. 2014). Chlorophyta consists of chloroplasts surrounded by two membranes with chlorophyll b as the major pigment. Parsinophytes comprise eight lineages of different taxonomic levels, and the numbers increase based on the environmental sequences and novel cultures (Tragin and Vaulot 2018). Chlorophyceae alone comprises two thousand species and are well known for several biotechnological applications (Barra et al. 2014). For example, microalgal biomass is reported to yield several primary metabolites such as carotenoids, proteins, lipids, and polyunsaturated fatty acids (Becker 2004; Guedes et al. 2011; Sharma et al. 2012; Christaki et al. 2013). Due to their biomass productivity and surface ratio, microalgae also play a crucial role in biogeochemical cycling of pollutants in marine waters (Van Gestel and Van Brummelen 1996). For example, the cell wall composition of microalgae is reported to have greater capacity for the metal-binding that can be transferred to food chain through grazing (Wang et al. 1998).
Due to the abundance of microalgae in waters, they have been overwhelmingly considered as sensitive bioindicators to monitor pollutants in the marine environment (Levine 1984; Whitton and Kelly 1995; Ali et al. 1999; Volterra and Conti 2000). While thoroughly reviewing the toxic profile of marine algae, Torres et al. (2008) proposed that the widespread abundance of microalgae in the marine environment can be used for seasonal evaluation or the effect of time change in the ecosystem in response to heavy metals and organic pollutants. Owing to the presence of these pollutants, microalgae tend to respond through physiological changes. Reports indicate that among other marine plankton, diatoms are severely affected by pollutants than green microalgae (Harrison et al. 1986; González et al. 2009). In addition, the green marine microalgae are reported to often dominate the bloom of natural population in the marine environment, particularly at increased pollution levels (Bonin et al. 1986; Folgar et al. 2009). Microalgae are known to respond to pollutants through two mechanisms: accumulation and sorption, and they also synthesize phytochelatins that are responsible for metal detoxification (Gekeler et al. 1988; Folgar et al. 2009). Furthermore, the antioxidants and innate enzymes have been shown to detoxify organic pollutants (Sunda et al. 2002; Stahl and Sies 2003; Sharma et al. 2012). Despite their versatile biochemical mechanisms, a detailed understanding of metal and organic pollutant removal by marine microalgae is very limited. The following sections present a comprehensive overview on the role of marine microalgae in the removal of heavy metals and organic pollutants.
3.3 Pollution in the Marine Environment—Sources of Heavy Metals and Organics
Anthropogenic sources of heavy metals and organic pollutants in the marine ecosystem generally result from the direct discharge of wastes, water runoff, and airborne pollutants (Leprovost 2001). These pollutants are carried from inland through sewage, dredged spoil, rainwater, and domestic and industrial waste discharged into coastal waterbodies through estuaries that enter the oceans (Wu et al. 2001; Adeniji et al. 2017). Hydrocarbon pollution is one of the great threats to the marine environment, with estimates of discharge accounting for 1–8 million tons per year (National Research Council Committee on Oil in the Sea, 2003). In addition, around 25,000 ship cargo with 18.5 million barrels of oil per day navigates through gulf waters which can potentially result in minor accidental spills causing a threat to the marine environment (Chitrakar et al. 2019). These crude oil spills affect marine organisms by limiting gas exchange and reducing light penetration (González et al. 2009). Moreover, crude oil spills release several organic pollutants such as benzene, toluene, xylene, and aromatic hydrocarbons that can accumulate in marine biota and sediments, thus acting as a sink affecting the ecosystems (Kachel 2008).
The marine environment is also reported to receive copious and stable inputs of pyrogenic hydrocarbons from coal and oil combustion as well as other organic products such as wood (Ravindra et al. 2008; Page et al. 1999). The predominant source of heavy metals in the marine environment is the industrial effluents discharged into the ocean either through runoff or improper disposal. Three types of heavy metals that cause major environmental problems include toxic metals such as cadmium (Cd), lead (Pb), copper (Cu), zinc (Zn), nickel (Ni), cobalt (Co), etc., precious metals like silver (Ag), gold (Au), palladium (Pd), platinum (Pt), etc., and radionuclides such as uranium (U), thorium (Th), radium (Ra), etc. (Wang and Chen 2009). Human exposure to heavy metals has dramatically risen because of an exponential increase in their use in several industrial, domestic, agricultural and technological applications. Other potential anthropogenic sources of heavy metal pollution are industrial effluents, acid mine drainage associated with mining operations, and coal-based and nuclear power plants. Various industries produce and discharge different heavy metals at varying concentrations into the environment; few of them include electroplating, metallurgy, surface finishing industries, energy and fuel production, iron and steel manufacturing, lead-acid battery manufacturing, fertilizer and pesticide industry, electrolysis, electro-osmosis, microelectronics, leather manufacturing, electrical appliance manufacturing, photography, etc. (Ahmaruzzaman 2011). Natural phenomena such as weathering of rocks and volcanic eruptions also significantly contribute to heavy metal pollution.
3.4 Removal of Heavy Metals and Organic Pollutants by Marine Microalgae
A comparison of conventional remediation techniques such as chemical precipitation, ion exchange, membrane filtration, electrochemical treatment, coagulation, and flocculation with those of bioremediation approaches, in terms of their merits and demerits (Table 3.1), clearly indicates that remediation of the polluted sites following the conventional engineering approaches is challenging both technically and economically. Also, bioremediation that involves the capabilities of microorganisms in the removal of pollutants is the most promising, relatively efficient, and cost-effective technology. The following sections particularly deal with the innate capabilities of microalgae in the removal of heavy metals and organic pollutants from marine environments.
3.4.1 Removal of Heavy Metals by Marine Microalgae
Abundant occurrence of metals in the environment leads to their increased concentration in the organisms over time. Bioavailability most often refers to the availability of contaminants, such as heavy metals or organic pollutants, in an ecosystem. Frequently, it is also used to determine the potential risk of pollutants toward nontarget organisms in any system. Bioavailability in the environment primarily involves physical, chemical, and biological processes. Contaminants or pollutants may be present in varying forms: (i) associated with soil and or sediment particles (bound form), (ii) released from liquid and or gaseous phases (release form), and (iii) associated with living organisms (attached form). A contaminant enters a liquid or gaseous phase once it is released from the bound phase. During this stage contaminant transport will take place through advection, diffusion, and dispersion, which result in the movement of contaminant molecules in the medium (liquid or gas) and thereby reassociation of contaminant or return to the bound state (soil). Meanwhile, the contaminants are carried to the surface of the living organisms (Fig. 3.1). Similar processes occur in the medium and eventually the contaminant reaches the living organisms and enters their tissues through cell membrane. Thus, contaminant transport is an important component of its bioavailability. The contaminants after their entry into the cells are metabolized and/or excreted, causing adverse or toxic effects to living organisms (Fig. 3.2).
3.4.1.1 Biosorption of Metals
Biosorption is the process of removing sorbet (metal ions) from the solvent (water) using biological material called a biosorbent. Marine microalgae have recently gained attention for the development of biosorbent materials due to their high sorption capacity and availability in seas and oceans. Due to the presence of alkaline metal ions in the composition of algal cell walls the heavy metal ions in the water can be easily treated through a simple ion-exchange process. These sorbents have the metal-sequestering property that can be used to reduce the concentration of heavy metal ions in the solvent from parts per million (ppm) to parts per billion (ppb) level. Biosorption capacity determines the number of metal ions that microalgae can bind on the surface, and it is denoted by qmax. Brinza et al. (2007) reviewed the biosorption capacity of some marine microalgal species involving the commonly detected heavy metals found in the wastewater, as shown in Table 3.2.
Biosorption is an extracellular process that is carried out in the cell membrane in which the algal biomass binds the heavy metals in the cell wall. The algal cell wall is composed of polysaccharides that contain sulfate. Imidazole, phosphate, hydroxyl, amine, and amino functional groups act as a binding site for the heavy metals to be adsorbed. The biosorption mechanism (Fig. 3.3) can be divided into metabolism-dependent biosorption in which transportation of the pollutant across the cell membrane takes place, followed by intercellular accumulation or detoxification. Metabolism-independent mechanisms involve ion exchange, complexation, chelation, and precipitation process. For example, the cell wall of microalgae is composed of polysaccharides, lipids, and proteins that provide many functional groups capable of attracting both anionic and cationic heavy metal ions exchanging them with the functional groups present in the cell wall. While investigating the mechanism for removing Cr3+, Cd2+, and Cu2+ by Spirulina, Chojnacka et al. (2005) found that hydroxyl, carboxyl, and phosphate functional groups were involved in the removal of the metal ions by the ionic-exchange process. Similarly, a microalgal strain, Tetraselmis marina AC16-MESO, could remove Cu (90%), Fe (100%), and Mn (50%) after 72-h incubation period, mostly by complexation of metal ions onto functional groups at the cell surface (Cameron et al. 2018). In fact, complexation mechanism is the result of electrostatic attraction between heavy metal ions and organic molecules present on the cell which act as ligands. The complex formation between the metal ion and ligand is due to the covalent bonds. The functional group (phosphonate, carboxyl, and amine) present in the cell wall of Chlorella miniate removed Cr3+ by the complexation process (Han et al. 2006). Organic acids such as citric, fumaric, lactic, oxalic and gluonic have been found to chelate metal ions resulting in the formation of metallo-organic complexes. Chelation is the advanced form of complexation mechanism in which the metal ion would bond with a ligand in many positions at the same time with higher stability. Chlamydomonas reinhardtii removed Hg2+ by direct chelation mechanism in which glutathione not only adsorbed the metal ion but also reduced the toxicity of the pollutant in water (Perales-Vela et al. 2006).
Two marine algae, Chlorella sp. and Phormidium sp., exposed to tannery wastewaters removed Cr concentration by 81 and 90%, respectively, at the end of 15 days incubation period as revealed by metabolic mechanism (Das et al. 2018). When the metal ion solubility decreases, the bioavailability is reduced, resulting in the mechanism of precipitation. Upon exposure to the heavy metal-polluted medium, the algal biomass favored precipitation that was based on pH of the medium. If pH of the medium increases, the active sites on the cell wall attract heavy metal ions. Cu, Ag, and Pb ions were removed by the alga, Tertaselmis suecica, by the mechanism of precipitation due to the presence of phosphates on the cellular surface (Ballan-Dufrançais et al. 1991). While growing Chlorella sp. in seawater-based medium, nearly 4% of Cd supplemented was found precipitated due to an increase in pH to 8 besides 67% accumulation and 25% adsorption of the metal (Matsunaga et al. 1999).
3.4.1.2 Factors Influencing Biosorption of Heavy Metals
3.4.1.2.1 Biotic Factors
Algal Species
Marine microalgae can be classified into three broad categories based on the composition of pigment color in green algae (Chlorophyta), red algae (Rhodophyta), brown algae (Phaeophyta) (Davis et al. 2003). Romera et al. (2007) summarized the biosorption capacity of algae related to some heavy metals as indicated in Table 3.3. Brown algae have a higher sorption capacity than red and green algae due to their high alginate content and the presence of functional groups in the structure. But the use of brown and red marine algae has a major drawback due to the presence of certain organic compounds such as alginate. Also, the pigments generate secondary pollutants and reduce the biosorption capacity. In green algae the secondary pollutant generation is insignificant but their biosorption capacity is lower as compared to brown and red algae. While studying the impact of biotic factors on Cu adsorption capacity in marine microalgae, Levy et al. (2007) observed that Dunaliella tertiolecta was least sensitive than Minutocellus polymorphus and was depended on uptake rates across cell membrane rather than the taxonomic status and cell size.
Concentration of Biomass
In the biosorption process, the removal efficiency depends upon the biomass concentration because of the greater availability of binding sites on the cell surface. Increased biomass concentration enhances the removal percentage of heavy metals. An increase in biomass concentration of Ulva fasciata from 0.5 to 4 g L−1 resulted in the improvement of Pb removal efficiency in the range of 42–75%, while the removal efficiency of Cd increased from 43 to 73% with the increase in biomass concentration from 0.5 to 6 g L−1 (Nessim et al. 2011). Increased biomass concentration often reduces the biosorbent capacity of microalgae because of the reduction in intercellular distance and cell agglomeration. Kaparapu and Prasad (2018) observed higher biosorption of Cd(II) in Nannochloropsis oculata with biomass concentration of 7 g L−1 and a decrease in biosorption capacity with increased biomass concentration probably due to the partial biomass aggregation that results in surface area reduction.
Tolerance
Algal species are known to grow, adapt, and tolerate hazardous environmental conditions. Heavy metal tolerance in algae depends upon the algal species. However, members of Chlorophyceae are generally known to tolerate Cu2+, Zn2+, and Cd2+. Strains of Chlorella sp. isolated from mercury-contaminated sites tolerated higher Hg2+ concentration than the isolates from uncontaminated habitats (Gaur and Rai 2001). Pérez-Rama et al. (2010) observed 87% of Cd accumulation in a marine microalga, T. sueccia, and was related to phytochelatin synthesis. Folgar et al. (2009) reported that Dunaliella salina was tolerant to higher concentrations of Cd due to the intracellular metal-binding ligands.
Surface Area to Volume Ratio
The ratio of surface area to volume in microalgae influences the sequestration of heavy metals in the solution. The take-up nutrients, in terms of per biomass, are faster in microalgae than macroalgae because of the size, growth, metabolism, and biochemical composition (Hein et al. 1995). Khoshmanesh et al. (1997) reported that the uptake of Cd was similar in an algal species having different sizes. The microalgal culture with a specific surface area of 2.20 m2 mg−1 cells showed higher uptake of Cd ions as compared to the culture with a specific surface area of 0.98 m2 mg−1 cells.
3.4.1.2.2 Abiotic Factors
pH
Biosorption of heavy metals in solution depends upon pH conditions due to the functional groups that dissociate at certain pH levels in the algal biomass. The maximum sorption of heavy metal ions by the marine microalgal biomass was obtained at a pH range between 4.0 and 6.0. The observed percentage removal efficiency for Cr, Cd, As, Pb, and Hg at pH 6.0 were 98.30, 92.50, 96, 92.20, and 80, respectively (Kumar et al. 2020; Leong and Chang 2020). When the pH value is lower than 6.0, the hydrogen ion concentration does not compete with the metal ions, and during adsorption of heavy metals no vacant active sites are created in the algal biomass (Gupta et al. 2011). If the pH value is greater than 6.0, the metal species are hydrolysed and are no longer available for the biosorption process (Romera et al. 2007). Kaparapu and Prasad (2018) reported that the biosorption of Cd(II) at pH >7 was reduced in a marine microalga, Nannochloropsis sp., and at pH 2–4 there was a competition between metal ions and metal-binding sites located on algal cell surface. The reduced Cd biosorption at higher pH was attributed to the maximum immobilization of positive charges. When the initial pH was maintained at 7.8, the cells of T. suecica were metabolically active and increased in cell number from 30 to 40 mg g−1 within 48 h, suggesting that the live cells are more suitable for biosorption than dead cells (Pérez-Rama et al. 2010).
Temperature
Temperature plays a vital role in the biosorption process as it influences the process in both positive and negative ways depending upon the range in temperature (Khambhaty et al. 2009). The solubility of metal ions was found to be higher at elevated temperatures, but an increase in temperature decreases the biosorption capacity of the biomass. The maximum biosorption of Cu2+ ions attained at 37 °C was 90% in Spirulina species but the biosorption capacity was reduced to 82% at 60 °C and then gradually decreased with further increase in temperature (Al-Homaidan et al. 2014). The biosorption efficiency of N. oculata biomass increased with contact time up to 90 min and remained constant (Kaparapu and Prasad 2018).
Contact Time
The efficiency of biosorption process depends upon the contact time between the algal biomass and the heavy metal ion. It was observed that the optimum contact time for the maximum adsorption of 80–90% of Cu, As, Cd, Cr, Pb, and Hg by various marine algal species was within 60–90 min (Al-Homaidan et al. 2014; Leong and Chang 2020). Initially, many active sites are available on the cell surface for the adsorption of heavy metals, and there will be a reduction in active sites with time, resulting in a gradual decline in the removal capacity of biomass that requires regeneration of algal biomass. The amount of biosorbed Cd in D. salina biomass was greater after 24-h contact time and was subsequently reduced due to the enhanced sorption onto the cellular surface (Folgar et al. 2009). It has been reported that biosorption yield of Cd(II) decreased with increased temperature at an optimal contact time due to the following reasons: relative increase in leaching tendency of ions from solid phase to bulk phase, and weakness of active sites for biosorption in the sorbed phase (Kaparapu and Prasad 2018).
3.4.1.3 Desorption of Heavy Metals and Biomass Regeneration
Desorption of heavy metals is the process of recovering valuable metal ions from the algal biomass by adding eluent. The eluent restores the biosorbent to its original state for the reuse of biomass in the process. Mineral acids, complexing agents, and organic acids are used as the eluents as they are non-damaging to the sorbent, and they ensure the metal-binding capacity of microalgae. Desorption of Cr3+, Cd2+, and Cu2+ from biomass of Spirulina sp. by nitric acid resulted in 98% removal of the metal ions (Chojnacka et al. 2005). In fact, Chlorella vulgaris remains unaffected even after five cycles of biomass regeneration using 0.1 M EDTA as eluent to recover Cd metal ions, and the adsorption capacity loss was less the 5.8% (Kumar et al. 2018). Both HCl and EDTA are the most used eluents for desorbing algal biosorbents. However, HCl decreases biosorption capacity of algal biomass after every wash, and the use of EDTA is not eco-friendly as it dissolves alginate upon every use which can lead to secondary pollution. Therefore, it is essential to screen the desorbing agents for efficient metal ion recovery.
3.4.1.4 Heavy Metal Detoxification by Marine Microalgae
The ability of microalgae to adapt and survive in habitats contaminated with heavy metals and organic pollutants depends on genetic adaptation which enables them to develop defence mechanisms to resist and adapt the harsh environmental conditions (Nayaka et al. 2017). This mechanism of defence allows microalgae to develop some tolerance and resistance toward the pollutant that can detoxify the pollutants inside the cell. The defence mechanism involves the production of short-chained polypeptides such as phytochelatins (PCs) and metallothioneins (MTs) that are abundant in sulfhydryl and carboxyl groups and can bind to the pollutants (Cobbett and Goldsbrough 2002). The bound pollutant further moves in for internal detoxification process which involves conjugation of the pollutant with the polypeptides and further compartmentalization of the pollutants by transporting them into the vacuoles (Qin et al. 2006). Folgar et al. (2009) reported that metal complexing ligands in D. salina were rich in cystine although most of the known are GSH and PCs. They observed that levels of cystine synthesis led to maximum Cd accumulation intracellularly. In another study, D. salina was shown to be resistant to As which exhibited higher levels of lipid peroxidation with a differential expression of 65 proteins involved in energy metabolism, protein synthesis and folding, ROS scavenging, and amino acid synthesis (Ge et al. 2016). Wang et al. (2017) reported variation in thiols such as cysteine, glutathione, and PCs in D. salina exposed to arsenite and demonstrated that transformation of arsenite-induced several PCs initially and later decreased under various phosphate regimes. The synthesis of PCs varied with As(V) and As(III) which affected GSH levels, suggesting that the conversion of GSH to PCs is essential for arsenite mitigation (Wang et al. 2017). The biochemical mechanisms involved in heavy metal detoxification by microalgae (National Research Council 2003) are presented in Fig. 3.4. Sathasivam and Ki (2019) observed higher levels of phytoene synthase (PSY), phytoene desaturase (PDS), and β-lycopene cyclase (LCY-B) in T. suecica exposed to copper.
3.4.2 Removal of Organic Pollutants by Marine Microalgae
Human attempts to produce various organic compounds to protect many lives and support economic advantages significantly resulted in acute and chronic toxicity of some of these chemical substances making the biota deteriorate rapidly (Adeola 2004). Although these organic compounds are susceptible to degradation at a very slow process, they tend to persist in the environment or accumulate inside the biota (Subashchandrabose et al. 2013). Organic pollutants that are widely distributed in marine environments and prone to biodegradation by marine microalgae include phenolics, pesticides, persistent organic pollutants (POPs), and hydrocarbons (Dsikowitzky et al. 2011).
3.4.2.1 Pesticides
Pesticides including insecticides, fungicides, and herbicides are often detected in marine waters due to the urban or agriculture runoff causing serious threats to the marine biota. Atrazine sensitivity, in terms of 96-h growth inhibition, for the estuarine phytoplankter, D. tertiolecta, in nutrient-replete media was 159.16 μg L−1 and was influenced by the duration and nutrient-limited conditions (Flood et al. 2018). Chen and Jiang (2011) reported enhanced catalase activity in D. salina when exposed to trichlorfon and dimehypo at lower concentrations of 0.025 g L−1 and 0.0005 g L−1, respectively. In a toxicity study involving treatment of D. salina with dimethylphenol and dinitroaniline, Zhu and Jiang (2009) observed that the EC50 values were significantly higher when exposed to a single pesticide compared to their combination. However, increased concentrations led to significant inhibition in the growth of the microalga that was attributed to the effect on osmosis of cell membrane allowing toxicants to react with internal parts and damage membrane lipids. Thakkar et al. (2013) exposed D. tertiolecta and a brown tide alga, Aureococcus anophagefferens, to various concentrations of metachlor and observed a significant increase in cell size with glutathione production as detoxification mechanism. Although 40–50% of sublethal concentration of tributylin (TBT) could be removed by N. oculata and Dunaliella parava during 2–6 days of incubation, the former microalga adsorbed most of the added anti-fouling agent while the latter degraded it to mono-butyltin and di-butyltin (Taha et al. 2009). DeLorenzo and Serrano (2003) determined the toxicity of atrazine, chlorpyrifos, and chlorothalonil individually and as mixtures on D. tertiolecta and observed that atrazine and chlorothalonil concentrations at 25 and 33 μg L−1 decreased growth rate, while chlorpyrifos was toxic only at >400 μg L−1. In another study, the effect of herbicides such as diuron, irgarol, atrazine, and ametryn was tested toward D. tertiolecta in four different scenarios of increased temperature and salinity and reported that increasing temperature reduced growth but enhanced the contents of chlorophyll and starch and lipids (DeLorenzo et al. 2013).
3.4.2.2 Hydrocarbons
Water soluble fraction of crude oil containing mono- and diaromatic hydrocarbons affected D. tertiolecta within 24 h though photosynthesis impairment and cell division inhibition occurred. Despite the well-known tolerance of Dunaliella species, the exponential phase measured in terms of photosynthesis was reduced while lag phase showed growth inhibition, suggesting that duration of exposure influenced the overall growth (Siron et al. 1991). Fabregas et al. (1984) reported stimulation in the growth of T. suecica upon exposure to low hydrocarbon concentrations in crude oil whereas the dispersant did not exhibit any selective toxicity. Dunstan et al. (1975) observed that low concentration (10 mg L−1) of oil had no effect on the growth of D. tertiolecta. Similarly, low concentration (0.05%) of light diesel and an oil dispersant (0.005%), either alone or in combination stimulated the growth of Chlorella salina and impaired respiration (Chan and Chiu 1985). Photosynthesis in D. tertiolecta exposed to oil samples from tanker spill was significantly affected within 60 min, while survival of the cells was slightly affected (Carrera-Martinez et al. 2011). Jiang et al. (2002) exposed microalgal strains to four PAHs, viz., toluene, naphthalene, 2-methylnapthalene, and phenanthrene, and reported that C. vulgaris and Platymonas subcordiformis were least sensitive compared to other tested species.
Exposure of Chlorella salina to phenanthrene significantly increased the toxicity with an EC50 value that ranged from 1.893 to 0.23 mg L−1, and a decrease in pH from 9 to 6 was also significantly toxic suggesting that the acidification of sweater greatly influenced the effect of organic compounds (Chen et al. 2018a). Bretherton et al. (2018) observed that marine alga, D. tertiolecta, was resistant to oil and dispersant and referred to it as “robust” because chlorophyll was not affected during lag phase and was followed by biomass accumulation. Moreover, short-term exposure of D. tertiolecta to petroleum and diesel oil impacted the growth and photosynthetic performance and reported to recover during long-term incubation (Romero-lopez et al. 2012). Recently, Salinas-Whittaker et al. (2020) observed that D. tertiolecta exposed to water-soluble fraction (WSF) from fuel oil/diesel mixture increased physiological and biochemical response in unsaturated acyl chain of fatty acid suggesting the uptake of hydrocarbons. Mohammady et al. (2005) exposed Nannochloropsis salina to various concentrations (0–100%) of diesel fuel oil aqueous extract and observed a decrease in cell bioavailability leading to cell division and enhanced membrane permeability. Both the limitation of carbon and hormesis phenomenon, as evaluated by stable isotope analysis, were prevalent in Platymonas helgolandica when it was treated with water accommodated fraction of fuel oil (Liu et al. 2020). Dissolved crude oil at lower concentration (20 mg L−1) stimulated the growth of Dicrateria sp. but growth was inhibited with increased exposure time. However, consortia of marine microalgae involving Dicrateria sp. on biotreated seawater showed enhanced cell density that ranged from 4.0 × 105 to 1.7 × 106 cells mL−1. Chao et al. (2012) reported that four fuel oils, viz., F120, F180, F380, and F20 were toxic to a marine alga, Chlorella sp., due to the concentration of several PAHs. Hing et al. (2011) demonstrated that C. salina was able to tolerate diesel concentrations at steady state and was only affected when the concentration exceeded 170 mg L−1. Very recently, Marques et al. (2021) reported that N. oculata was able to grow in petroleum-contaminated water exhibiting a PAH removal efficiency of 94%. In particular, the percentage removal of several organic compounds such as naphthalene, benzopyrene, and acenaphthylene was 89–99% due to their intracellular biodegradation by oxidoreductase enzymes.
3.4.2.3 Other Organic Compounds
Phenol is an organic compound that results from the transformation of aromatic compounds via degradation, oxidation, and synthesis. Besides being enriched in coal tar, phenol is also produced as a by-product from several industrial processes as well as during organic matter decomposition (Michalowicz and Duda 2007). Mofeed and Abdel-Aal (2015) found that exposure of D. salina to various concentrations (50–200 μmol L−1) of phenol significantly affected antioxidant enzyme activities. Phenol at a concentration of 72 mg L−1 led to programmed cell death in marine microalgae by inducing changes in ultrastructure with shrinkage of the nucleolus and vacuole enlargement (Duan et al. 2017). During treatment of real refinery wastewater containing phenol and its derivatives such as o-cresol and p-cresol, marine alga, Nannochloropsis sp., removed >80% of both the cresols as compared to freshwater Chlorella sp. (Surkatti and Al-Zuhair 2018). The biodegradation was reported to occur in two steps: split in methyl group resulting in its conversion to methanol and further breakdown of phenol produced as an intermediate (Papazi et al. 2012). Bisphenol A, with production estimates of approximately two million tons, is well distributed in the environment and known for its endocrine disruption potential (Burridge 2003). While reporting the first toxicity data of chlorophenols on D. tertiolecta, Ertürk and Saçan (2012) reported that toxicity of chlorophenols decreased between 48 and 96 h due to the increase in pH of the medium or acclimation response of the marine microalga to the toxicants. Regardless of the exposure time, the toxicity was greater with an increasing number of chlorine atoms, while ortho-substituted chlorophenol was lesser than meta and para congeners (Ertürk and Saçan 2012). POPs are widely distributed due to domestic and industrial activities that are reported to reach marine environments (ter Schure et al. 2004; Lema et al. 2007). Polybrominated diphenyl ethers (PBDEs), the flame retardants, enhanced oxidative stress in D. salina with increased activities of superoxide dismutase, catalase, and glutathione reductase and decreased glutathione peroxidase activity (Zhao et al. 2017). Similarly, exposure of D. salina to dibutyl phthalate at 100 mg L−1 decreased glutathione peroxidase and superoxide dismutase (Wei et al. 2021).
3.5 Conclusions
Besides highlighting the advantages of the use of marine microalgae for the removal of heavy metals and organic pollutants, we presented the inherent drawbacks of the conventional treatment processes. Marine microalgae respond to heavy metals in several ways such as biosorption and bioaccumulation; however, there is a very clear paucity of data on organic contaminant removal and the associated mechanisms. Furthermore, it is very clear that marine microalgae can offer sustainable approach in the treatment of heavy metals and organic pollutants for safer marine ecosystem and biomass production from microalgae after detoxification. Thus, this chapter presents the overall understanding of the potential of marine microalgae in the removal of heavy metals and organic pollutants.
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Umamaheswari, J. et al. (2023). Removal of Heavy Metals and Organic Pollutants by Marine Microalgae. In: Encarnação, T., Canelas Pais, A. (eds) Marine Organisms: A Solution to Environmental Pollution?. Environmental Challenges and Solutions. Springer, Cham. https://doi.org/10.1007/978-3-031-17226-7_3
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