Mechanism of Microalgal Phycoremediation: Comparison
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Microalgae are continually exposed to heavy metals and metalloids (HMMs), which stifles their development and reproduction due to the resulting physiological and metabolic abnormalities, leading to lower crop productivity. They must thus change their way of adapting to survive in such a hostile environment without sacrificing their healthy growth, development, reproductive capacity, or survival. The mode of adaptation involves a complex relationship of signalling cascades that govern gene expression at the transcriptional and post-transcriptional levels, which consequently produces altered but adapted biochemical and physiochemical parameters. Algae have been reported to have altered their physicochemical and molecular perspectives as a result of exposure to a variety of HMMs.

  • microalgae
  • bioabsorption
  • heavy metals

1. Introduction

Heavy metals and metalloids (HMMs) play a key role in regulating the growth of organisms, as they influence their stress-response mechanisms. They are responsible for triggering many stress responses, including several biochemical responses in terrestrial plants as well as algal biosystems [1]. However, HMM excesses are among the most significant contaminants exerting a negative impact on crop growth and yield. In recent years, HMMs have become major problems, with a huge impact on nutritional, environmental, and ecological conditions [2]. As a result of various natural processes, such as weathering and erosion, and human actions, such as mining and industrial activities, wastewater, agrochemicals, and automobile exhaust gases, the accumulation of HMMs, such as lead, mercury, arsenic, and cadmium, in water bodies has been increasing day by day [3]. HMMs are responsible for water pollution and hamper the ecosystem. HMMs are present in two forms: immobilized and soluble. Compared to the soluble form, immobilized HMMs are more hazardous to plants and microalgae [4].
Metals with density values greater than 5 g/cm3 are classified as HMMs [5]. HMMs actually make up 53 of the 90 naturally occurring elements [6]. Water-soluble HMMs include manganese, iron, cadmium, arsenic, lead, mercury, etc., of which cadmium, lead, copper, molybdenum, nickel, and zinc are the ones that cause the most damage to crops [7]. Although some HMMs act as micronutrients at low doses, at higher concentrations they lead to growth inhibition and metabolic disorders [8]. Among the 17 HMMs important for living organisms, molybdenum, iron, and manganese are essential micronutrients, while cobalt, zinc, copper, nickel, vanadium, tungsten, and chromium are the trace metals with varying degrees of relevance [9]. On the other hand, mercury, silver, cadmium, antimony, uranium, and lead are not nutrients, and are deemed to be more or less harmful [10]. Excessive concentrations of various metals in the soil, such as nickel, cadmium, chromium, zinc, and copper, can harm natural and terrestrial ecosystems [11].

2. HMM Intake and Interactions in Microalgae

HMMs are the main concern in the current scenario [40][12]. Metals such as zinc, iron, nickel, copper, cobalt, manganese, and molybdenum are crucial for cellular metabolism. These metals are also found in metalloproteins, which are involved in a variety of cellular processes, including electron transport and protection from reactive oxygen species [41,42][13][14]. Concentrations of HMMs in the cell range from nanomolar to femtomolar, and the metal stoichiometry also differs among species [43][15]. Metal adsorption and transportation across the cell membrane normally occur in two stages of the uptake process, and the rate of transport is thought to be limited [44][16]. In a metabolism-independent process, metal ions are adsorbed to the cell wall by contact with the functional groups of important structural molecules, such as polysaccharides and proteins [45][17]. Subsequently, the metal ions can enter the cell membrane via active transport by binding to ion carriers or low molecular weight thiols, such as cysteine [46][18].

3. Bio-Removal of Extracellular HMMs by Microalgae

3.1. Microalgae Cell Wall Structure and Composition Play a Critical Role in HMM Biosorption

The cell wall acts as a barricade between the intracellular compartment and the outer environment [49][19]. The cell wall is made up of multifunctional macromolecules, such as carbohydrates, lipids, and proteins, which have several negatively charged functional groups on their surfaces, such as carboxyl, amino, hydroxyl, sulphate, phenol, sulfhydryl, phosphate, and so on [50][20]. The outer layer of the cell wall is the first participant in the elimination of HMMs because these negatively charged groups allow ions in the surrounding environment to bind [51][21]. When examining mechanisms of biosorption, it is crucial to comprehend the characteristics, structure, and composition of the cell wall [52][22]. Furthermore, other physicochemical factors, such as temperature, pH, other ions, and adsorbent ratio, also regulate the modality and efficacy of HMM removal [53][23]. In recent years, the most commonly employed microalgae strains in phycoremediation come from the phylum Chlorophyta; in particular, from the genera Chlorella and Scenedesmus [54][24]. The sensitivity and effectiveness of microalgae biosorption vary by genus and species, even under identical operating conditions [23][25]. For example, C. sorokiniana and S. obliquus grew differently in media polluted by copper(II), cadmium(II), lead(II), and chromium(VI) because of the different compositions and structures of their cell walls [55][26]. Within a phylum, the cell membrane can vary in complexity, from a simple lipid bilayer with peripheral and integrated proteins to a cap of glycolipids and glycoproteins enveloping the outer cell surface, as in Dunaliella and Isochrysis species. Complicated multilayer structures with additional intracellular material in vesicles can be found in dinoflagellates, cryptophytes, and euglenophytes species. They have both extracellular and intracellular material coupled with the cell membrane. Differences in the composition of the cell wall are also possible among species of the same genus; for example, C. vulgaris has an innermost layer [56][27], while C. zofingiensis and C. homosphaera have both an internal and an external layer, as well as a trilaminar form of the outer layer [57][28]. However, in C. trilaminar, sporopollenin forms the outermost layer, the middle layer consists of chitin and mannose-like polysaccharides, and the inner layer is composed of a phospholipid bilayer [58][29].

3.2. Physicochemical HMM Interactions and Role of Microalgal Cell Surface

Understanding how heavy metal ions interact with the cell surfaces of microalgae is difficult due to the complexity of the cell surface. A number of chemical and physical interactions have been documented. Chelation and complexation of HMMs with active groups in the cell wall are the main mechanisms involved. Ions, such as calcium, sodium, magnesium, and potassium, can be reversibly replaced in solution by other harmful HMMs via an ion-exchange mechanism on the surface of microalgae cells [59][30]. Physical factors, such as Van der Waals and electrostatic interactions, can influence the physical adsorption mechanism of the metal-binding onto the cell surface. In addition, microprecipitation is a process related to both active and passive metal absorption pathways [60][31].

3.3. HMM Interactions with Extracellular Polymeric Compounds

EPS are high-molecular-weight extracellular biopolymers produced by a variety of microorganisms, including microalgae. Proteins, lipids, nucleic acids, sugar, humic compounds, and other inorganic extracellular compounds that bind to carbohydrates are classified as EPS [61][32]. EPS soluble in media (SL-EPS), EPS connected to the cell wall or loosely bound EPS (LB-EPS), and tightly bound EPS (TB-EPS) are the three basic types of microalgal EPS [47][33]. The presence of harmful pollutants, such as toxic metals, is usually a threat to microalgae in aquatic habitats. EPS production is an adaptive process utilized as a self-defence strategy [62][34]. In general, when a metal is intercepted, EPS production increases. For example, Yu and colleagues found that, following cadmium exposure, production of LB-EPS by C. reinhardtii increased considerably [63][35]. Similarly, Li et al. recently showed that under Cd(II) and lead(II) stressors, C. reinhardtii produced more EPS [64][36]. In addition, an increase in EPS yields in copper enriched Chlorella sp. cultures indicated that EPS, rather than intracellular chelation, is responsible for copper absorption [65][37]. However, by comparing EPS-free and EPS-coated C. pyrenoidosa cells, EPS has been shown to improve adsorption capacity, minimize intracellular accumulation, and increase As ion tolerance [66][38]. EPS appears to have the ability to build an extracellular defensive barrier on the cell wall surface, consequently preventing HMMs from causing harm to the intracellular environment. [47][33]. Furthermore, EPS has a large number of charged hydrophobic groups that are responsible for dynamically binding to HMMs [66][38]. Hence, metal biosorption into the EPS can be related to the characteristics of the cell surface and of the functional groups [67][39].

4. Bioaccumulation Mechanisms of HMMs in Microalgae

4.1. Metal Transporters in Microalgae Cell Membrane

Metal transporters play a crucial role as they represent the first line of defence in terms of regulating osmotic balance. In addition, they regulate the intracellular absorption of ions critical for micronutrient homeostasis and mitigate the subsequent negative effects of non-essential HMMs [70][40]. The participation of several membrane transporters has been reported in a variety of microalgae species [71][41]. For example, entrance and outflow of metal ions in C. reinhardtii can be mediated by natural resistance-associated microphage proteins (NRAMP), the Fe-transporter (FTR), Zrt-Irt-like proteins (ZIP), and the copper transporter (CTR), ensuring the movement of HMMs from the extracellular surface to the cytosol [72][42]. These transporters have also been discovered in the vacuole membrane, and they serve the same purpose as the assimilative transporters. Through the efflux of active metal ions into the extracellular environment, members of the cation diffusion facilitator (CDF), FerroPortiN (FPN), P1B-type ATPases, and the calcium (II)-sensitive cross-complementer 1/Vacuolar iron transporter 1 (Ccc1/VIT1) lower the metal content in the cytoplasm. Once the metal concentration exceeds the cellular requirement, or when the metal peptide complex begins to interfere with cell metabolism, the metal transporters regulate the metal concentration in the cell [73][43]. With limited reports available about metal transporters in algae, further studies are needed to understand the exact mechanisms behind this process.

4.2. Pathways of Intracellular HMM Detoxification in Microalgae

Microalgae employ various processes to maintain intracellular ion concentrations and shield the cell from non-essential metals [74][44]. These include modification of plasma membrane permeability and cell wall function, stimulation of phytochelatin synthase, creation of HM-metallothionein and HM-polyphosphate complexes, compartmentalization into organelles, and activation of metal efflux mechanisms, allowing the maintenance of intracellular ionic homeostasis [75][45].

Chelation by Metallothioneins and Phytochelatins

Metallothioneins and phytochelatins are metal-binding proteins mainly responsible for maintaining a stable intracellular metal concentration [76][46]. Phytochelatins are small peptides that can be categorized into two classes: gene-encoded proteins, such as class I and II metallothioneins, and enzymatically produced polypeptides, such as class III metallothioneins [77][47]. Class II metallothioneins are a cysteine-rich superfamily of proteins found in the cytosol and have a low molecular weight of 6–7 kDa. Aureococcus, Chlorella, Nannochloropsis, Ostreococcus, Symbiodinium, and Thalassiosira are microalgae with the most known metallothioneins so far [78][48]. Microalgae have the potential to produce novel types of metallothioneins, as they can survive in heavy metal-contaminated environments. Phytochelations (PCs) can be produced enzymatically, rather than genetically by microalgae. PCs are thiol-containing peptides consisting of three amino acids: cysteine (Cys), glycine (Gly), and glutamate (Glu), and typically have a (γGlu-Cys)n-Gly structure, with 2 < n < 10. Metal binding is accomplished by the sulfhydryl group of the cysteine molecule. Production of -Glu-Cys by glutamylcysteine synthetase (GCS) is the first biosynthetic step. Subsequently, glutathione synthetase (GS) catalyses the synthesis of glutathione (GSH). Finally, another GSH molecule transfers -Glu-Cys to obtain (-Glu-Cys)2-Gly [79][49]. When intracellular metal concentrations are low, GSH is the main ligand; however, when high amounts of metals are absorbed, the PCs are responsible for their elimination [76][46]. Several studies have documented that the formation of class III MTs is responsible for detoxification in microalgal strains. In Chlorella fusca, MTs are formed after exposure to cadmium(II) ions [80][50]. Other studies aimed to clarify the biosynthesis of PCs when microalgae are exposed to HMMs. For instance, Gomez-Jacinto et al. discovered the formation of mercury–PC complexes in C. sorokiniana exposed to mercury [81][51], in copper(II)-treated Stichococcus bijugatus, and in lead(II)-treated Stichococcus bacillaris [82][52]. In addition, cadmium(II) was found to be the most powerful stimulator of PC synthase in Chlamydomonas species [64][36]. On the other hand, zinc was found to be the most potent inducer of PC synthesis in Dunaliella species [83][53]. A recent study discovered that GSH is the most abundant non-protein sulfhydryl molecule in D. salina [84][54]. Exposure to arsenic(V) and arsenic(III) led to the synthesis of PCs, implying that they are involved in As detoxification.

Chelation by Polyphosphates

Orthophosphate polymers (polyP) are abundantly found in both prokaryotic and eukaryotic cells. Several studies in algae revealed that polyP bodies accumulate in acidocalcisomes, which are formed primarily in granules of particular vacuoles in the trans-Golgi [85,86][55][56]. PolyPs are also present in the cytoplasm, nucleus, endoplasmic reticulum, mitochondria, and cell wall [87][57]. In C. reinhardtii, the metabolism of polyP can be regulated by acidocalcisome membrane transporters through enzymatic exopolyphosphatase reactions [88][58]. PolyPs are involved in a variety of functions, including HMM sequestration and detoxification [87][57]. The production of polyP also helps in the collection and storage of HMMs [89][59]. Indeed, the critical role of acidocalcisomes and polyPs in supporting cellular homeostasis of essential ions can be further expanded in relation to the bioaccumulation of hazardous HMMs [75][45].

4.3. Compartmentalization of HMMs in the Vacuole, Chloroplast, and Mitochondria

Sequestration of the MT-HMM complex in specific cell organelles, such as mitochondria, chloroplasts, and vacuoles, leads to the formation of metal bioaccumulation pathways and tolerance mechanisms. Transmission electron microscopy (TEM) with additional techniques and accessories, such as energy-dispersive X-ray spectroscopy (EDS), electron spectroscopic imaging (ESI), electron energy loss spectroscopy (EELS), and atomic force microscopy (AFM), can be used to study HMMs and their complexes (polyP-HMMs, MTs-HMMs, PCs-HMMs) [73][43]. Vacuolar assortment has been recognized as an essential component of HMM detoxification in several plant species [90][60]. On the other hand, metal sequestration has been discovered in a variety of cell organelles. A study discovered electron-dense black spherical entities in the vacuoles of Pseudochlorococcum typicum subjected to lead ions by using TEM examination [91][61]. Moreover, by using TEM, EELS, and ESI, the accumulation of chromium(IV) in a chromium–iron–oxygen complex and enhanced vacuolation inside Micrasterias denticulata cells were discovered [92][62]. In contrast, the chloroplast was the primary storage location for PC–cadmium(II) complexes in C. reinhardtii [70][40]. Similarly, a study revealed that the chloroplast of Euglena gracilis contains more than 60% of the accumulated cadmium(II) [93][63]. Another study discovered that the intracellular copper (II) in the thylakoids and pyrenoids of O. nephrocytioides also accumulates HMMs [94][64]. Furthermore, Mendoza-co et al. found that cadmium(II) and class III MTs-cadmium(II) complexes accumulated in the mitochondria and chloroplast of E. gracilis [93][63]. All the above studies suggest that microalgae may be the most important organisms for eliminating HMMs.

5. Biotransformation and Mitigation of HMMs by Microalgae

The mechanism by which endobiotic or xenobiotic compounds are converted into molecules that differ in activity, excretability, and toxicity is referred to as biotransformation (detoxification vs toxication) [95][65]. Although biotransformation may refer to a series of detoxification mechanisms, microalgae mainly use enzymatic and biochemical reactions to transform poisonous HMMs into harmless species.

Role of Enzymes in the Biochemical Transformation of HMMs

The enzymatic biotransformation of HMMs is described as the chemical transformation of a highly hazardous form into a less dangerous form through oxidation and reduction processes. HMMs cannot be destroyed, but they can be converted into an inorganic complex with minor harmful effects by changing their oxidation state. A few investigations focused on the involvement of oxidoreductase enzymes in HMM detoxification by microalgae. Arsenate reductase, mercuric reductase, and chromate reductases are the most common redox enzymes found in microalgae [96][66]. C. vulgaris has the ability to convert chromium(VI) to chromium(III) through an series of enzymatic reactions catalyzed by chromate reductase [97,98][67][68]. In addition, Selenastrum minutum, Galdiera sulphuraria, and C. fusca can catalyze the bio-transformation of Hg2+ into elemental mercury and metacinnabar (Mercury(II) sulfide) via the mercuric reductase enzyme [99][69]. C. reinhardtii also has arsenate reductase to detoxify arsenic [100][70]. Microalgae use biochemical mechanisms to mitigate HMMs during the phytoremediation process. The reduction of chromium from the hexavalent oxidation state to the trivalent form is catalysed by the transfer of electrons from the reduced form of GSH [98][68]. In addition, various detoxifying pathways reduce the toxicity of inorganic arsenic [101][71]. Some microalgae species appear to be capable of converting arsenic(V) to arsenic (III). A study revealed that after 72 h of exposure to arsenic(V), 32% of the total intracellular arsenic(V) concentration was transformed into arsenic (III) [102][72]. C. aciculare also converted some arsenic(V) in the cell medium to arsenic (III) [103][73]. With the use of oxidase and S-adenosylmethionine, the arsenic(V) was reduced to arsenic (III) and then methylated to monomethylarsonate (MMA(V)). The MMA was transformed to dimethylarsinate (DMA(V)), with subsequent reduction to DMA(III). Arsenic can also be reduced to arsenolipids, arsenosugars, arsenobetaine, and arsenoribosides [104][74].

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