Abstract
British Phycological APPLIED PHYCOLOGY Society 2023, VOL. 4, NO. 1, 15–33 Understanding and using algae https://doi.org/10.1080/26388081.2022.2158132 a a b c Sarah K. Read , Andrea J.C. Semião , Margaret C. Graham and Michael Ross a b School of Engineering, The University of Edinburgh, Edinburgh, UK; School of Geosciences, The University of Edinburgh, Edinburgh, UK; Scottish Association for Marine Science (SAMS), Scottish Marine Institute, Oban, Argyll, UK ABSTRACT ARTICLE HISTORY Received 9 July 2022 To increase the sustainability of industrial wastewater treatment, biological sorbents have been Accepted 27 November 2022 explored for the removal of potentially toxic elements (PTEs). Algae are particularly attractive biosorbents due to their high concentration of negatively charged extracellular binding sites. KEYWORDS Although there has been significant focus on dried algal sorbents for this reason, live algal sorbents Algae; bioaccumulation; may expand potential binding sites through intracellular accumulation and replenishment of biosorption; glutathione; active binding sites through algal growth. A barrier to the application of live algal sorbents in heavy metals; WWT is managing a sorbent’s metabolic requirements while achieving maximum PTE removal. phytochelatins; potentially toxic elements; wastewater Many reviews investigating the performance of live algal sorbents have focused on species-specific treatment differences in PTE removal, without defining how intracellular detoxification mechanisms may be impacted by system conditions. The following review explores the physico-chemical conditions and sorbents qualities that affect the production of an integral intracellular ligand for PTE accumulation, phytochelatins (PCs). This review uniquely highlights how system conditions may support or inhibit the proper functioning of intracellular detoxification mechanisms governed by PCs. Opportunities for optimization and areas requiring further research are also suggested. Introduction Algal biosorbents are particularly strong candidates for PTE removal due to their resilience to environmen- Globally, there has been an increase in potentially toxic tal stressors and their high concentration of extracellular element (PTE) pollution in terrestrial (Chibuike & sorption sites (Lin, Li, Luan, & Dai, 2020). These quali- Obiora, 2014; Friedlova, 2010), freshwater (Islam, ties allow algae to accumulate PTEs multiple orders of Ahmed, Raknuzzaman, Habibullah -Al- Mamun, & magnitude higher than ambient concentrations, even Islam, 2015; Lin, Li, Luan, & Dai, 2020; Ribeiro et al., −1 when PTEs exist at mg l concentrations, with order 2018) and marine ecosystems (Boran & Altinok, 2010; of magnitude varying depending on algae species and Gaudry et al., 2007; Luo et al., 2020) due to the dis- PTE concentration (Foster, 1982; Stevens, Mccarthy, & charge of PTE-containing wastewaters (WWs). Vis, 2001; Zbikowski, Szefer, & Latała, 2007). In a WWT Though conventional wastewater treatment (WWT) context, the total PTE accumulation and removal methods, like chemical precipitation, ion exchange, achievable by an algal biosorbent depends upon the adsorption, coagulation and reverse osmosis, may species, biosorbent dose, present PTEs, initial PTE con- reduce the concentration of PTEs, these methods pre- centration, exposure time, pH, temperature, presence of sent several environmental and economic shortcom- additional compounds, and biomass state (i.e., active or ings (Ahluwalia & Goyal, 2007; Patterson, 1985; Sud, inactive), among other factors (Foster, 1982; Lin, Li, Mahajan, & Kaur, 2008). Namely, depending on the Luan, & Dai, 2020; Mehta & Gaur, 2005). process employed, these systems can be expensive, To date, many studies have utilized dried or inactive energy-intensive, inefficient at PTE concentrations in –1 algal biomass for PTE accumulation. The current focus the µg1 range, and may produce toxic by-products on inactive biomass is likely due to the perceived com- with no sustainable disposal options (Ahluwalia & plications associated with live systems. In live algal WWT Goyal, 2007; He & Chen, 2014). Biosorbents, produced systems, uptake or accumulation may be impacted by the from plants, bacteria, yeast, fungi, or, the subject of this interaction of PTEs with ambient solution constituents, review, algae, provide more sustainable and cost- disparity in optimal pH for metal accumulation and effective alternatives to conventional PTE WWT meth- biomass maintenance, and occurrence of biomass degra- ods (Lata, Singh, & Samadder, 2015; Sud, Mahajan, & dation due to chronic PTE exposure and desorbing agent Kaur, 2008). CONTACT Sarah K. Read s1340388@ed.ac.uk © 2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 16 S. K. READ ET AL. application (Mehta & Gaur, 2005; Rajfur, 2013). in inert and storable forms following PTE import into the However, a more recent review has identified live algal cell (Pistocchi, Mormile, Guerrini, Isani, & Boni, 2000). sorbents as able to achieve comparable levels of PTE There are several other classes of intracellular compounds removal (Zeraatkar, Ahmadzadeh, Talebi, Moheimani, that prevent oxidative damage during PTE exposure, & McHenry, 2016). This is because in dried systems, including heat-shock proteins and antioxidants, however, PTE removal is restricted to surface adsorption, whereas these will not be covered in this review as they do not live algal sorbents may exploit surface adsorption as well directly contribute to increases in PTE uptake, but instead as intracellular storage of PTEs through active detoxifica- function as tolerance mechanisms (Danouche, El tion mechanisms. These detoxification mechanisms are Ghachtouli, El Baouchi, & El Arroussi, 2020). a result of physiological responses following PTE The extent of extracellular or intracellular compound exposure. generation impacts the location and level of PTE sto- Physiological responses to PTE exposure include non- rage, and subsequently PTE recovery potential. The transcriptional alterations to the occurrence of extracel- production of these compounds forms the basis for lular (Croot, Moffett, & Brand, 2000; Pistocchi, Mormile, extracellular and intracellular PTE detoxification and Guerrini, Isani, & Boni, 2000) and intracellular com- internal compartmentalization mechanisms in live pounds (Cobbett & Goldsbrough, 2002; Sinaei, algal sorbents. The role and production of EPSs, GSH, Loghmani, & Bolouki, 2018). Though both classes of and PCs are summarized in Fig 1. compounds contribute to PTE tolerance through PTE PCs, also known as class-III metallothioneins, and entrapment, chelation, and detoxification, the fate of associated thiol peptides like GSH form the foundation PTEs differs between classes (Cobbett & Goldsbrough, for PTE detoxification and active uptake in live algal 2002; Gekeler, Grill, Winnacker, & Zenk, 1988; Perales- sorbents (Ahner & Morel, 1995a; Ahner, Wei, Oleson, Vela, Peña-Castro, & Cañizares-Villanueva, 2006). & Ogura, 2002; Gekeler, Grill, Winnacker, & Zenk, 1988; Extracellular compounds, namely extracellular polymeric Pawlik-Skowron, 2001; Perales-Vela, Peña-Castro, & substances (EPSs), increase the passive binding and exclu- Cañizares-Villanueva, 2006; Pérez-Rama, Torres sion of ambient PTEs in the extracellular matrix. The role Vaamonde, & Abalde Alonso, 2006; Soldo & Behra, of EPSs in PTE sorption has already been evaluated in 2000). PCs are present in bacteria, higher plants and several research papers and reviews (Naveed et al. 2019; most species of algae (Devez, Achterberg, & Gledhill, Ozturk, Aslim, Suludere, & Tan 2010, 2014). Whereas 2015; Perales-Vela, Peña-Castro, & Cañizares- intracellular compounds, including phytochelatins (PCs) Villanueva, 2006; Priyadarshanee & Das, 2021). Once and glutathione (GSH), actively compartmentalize PTEs PTEs are transported into the cell, GSH molecules chelate Figure 1. A simplified diagram of potentially toxic element (PTE) detoxification by extracellular and intracellular ligands. Both passive and active entrance of PTEs into the cell are illustrated, as well as the potential EPS-PTE interactions that may occur during passive sorption. Active transport of PTEs into the cell have been illustrated with a generic transporter, though these may bePTE-specific. + symbols indicate the addition of an actor and not the relative charge. GSH = reduced glutathione,γ-glutamate-cysteine-glycine; GSH- PTE = PTE-loaded GSH; GST = glutathione S-transferase; PCS = phytochelatin synthetase; PC-PTE = PTE-loaded phytochelatin; EPS = Extracellular Polymeric Substances; ROS = reactive oxygen species; GSSG = oxidized glutathione. APPLIED PHYCOLOGY 17 non-essential PTEs, or those occurring at toxic concen- underlying physiological responses in these differences trations, through sulphhydryl (SH) complexes. GSH-PTE in performance. Whereas the following review focuses complexes then activate the production of phytochelatin on how PC production is impacted by system condi- synthetase (PCS) enzymes, which in turn catalyse the tions, including present PTEs, PTE concentration, expo- production of PCs from the GSH-PTE compounds sure time, and physico-chemical conditions, and sorbent qualities, including sorbent group, species, and (Perales-Vela, Peña-Castro, & Cañizares-Villanueva, GSH production. 2006). PCs may exist in chains of 2 to 6 PC complexes This critical review provides a comprehensive sum- (Gekeler, Grill, Winnacker, & Zenk, 1988; Kneer & Zenk, mary of the factors affecting PC production in different 1997) (Fig 2). With increasing oligomer length, the PC- algae-PTE systems and highlights the opportunities for PTE complexes increase in stability, improving retention optimization through algal sorbent and physico-chemical of PTEs and cellular tolerance (Kneer & Zenk, 1997; condition selection for effective PTE removal. This Lavoie, Le Faucheur, Fortin, & Campbell, 2009). In review evaluates the latest research on PC production terms of PTE fate, PCs are stored in intracellular vacuoles by micro- and macroalgae, with no restrictions in scope or extruded, depending on ambient PTE concentrations based on taxonomy or tested PTEs. Based on this review, (Cobbett, 2002; Perales-Vela, Peña-Castro, & Cañizares- PC production varied based on sorbent taxonomic clas- Villanueva, 2006). sification, generation of GSH compounds, and experi- Whereas GSH mitigates oxidative damage under mental physico-chemical conditions. Issues with multiple cell stress events, PCs perform a specialized reporting or opportunities for further research are also role in cellular detoxification by facilitating PTE entrap- highlighted to support the advancement of this field. ment (Oukarroum, 2016; Skowroński, De Knecht, Simons, & Verkleij, 1998). In terms of WWT and PTE remediation, PC content has been correlated to higher Sorbent Differences PTE tolerance and intracellular storage in multiple algal groups (Lavoie, Le Faucheur, Fortin, & Campbell, 2009; During PTE exposure, sorbent species or group may Navarrete et al., 2019; Skowroński, De Knecht, Simons, influence the magnitude of PC production with subse- & Verkleij, 1998; Wang & Wang, 2011). Although PC quent effects on PTE removal. PC production has been content generally has a positive relationship to PTE observed in several algal groups, including chlorophytes exposure (Table 1), there are interspecific differences macroalgae, chlorophytes microalgae, diatoms, xantho- in PC synthesis and variable excitation based on phy- phytes, dinoflagellates, and coccolithophores (Table 1). sico-chemical conditions. Although most algal sorbents identified in this review Many reviews to date compare the performance of produce PCs, the magnitude of this production is not live algal sorbents by evaluating the effects of sorbent uniform between or within algal groups. Differences in species and physico-chemical conditions on PTE the favoured detoxification mechanism under certain removal; however, they often fail to define the role of conditions may vary within or between groups resulting Figure 2. The chemical structure of glutathione (GSH) and the dimeric form of phytochelatin (PC). Amino acid constituents are colour- coded in both molecules. 18 S. K. READ ET AL. Table 1. Summary of phytochelatin (PC) response by multiple algae species following potentially toxic element (PTE) exposure. System conditions including present PTEs, PTE concentration, and exposure time are reported with units standardized where possible. PC content as well as the direction of PC change and the significance of this change are reported. PC content below the detection limit is reported as BD. When PCs are not detected, ND is reported in the PC content column. The Direction of PC change is determined −1 from the difference between 0.0 mg PTE l control and the experimental treatment. Direction of change may illustrate an increase ( ), decrease ( ), or lack of change ( ) in PC content. Significant difference between control and experimental cultures is marked with *. Significant difference between the PC content of two experimental treatments exposed to the same PTE concentration, but with different physico-chemical conditions is marked with . The units for PC content are reported in the first entry for each −1 evaluation. PTE concentrations have been converted to mg l where necessary with original concentrations have been reported in red. Units that could not be converted are marked with ·. Additional notes on biomass qualities or physico-chemical conditions are included in the Notes column. (Continued) APPLIED PHYCOLOGY 19 Table 1. (Continued). (Continued) 20 S. K. READ ET AL. Table 1. (Continued). 16∞C 8∞C 16∞C (Continued) APPLIED PHYCOLOGY 21 Table 1. (Continued). 16∞C 18∞C 4∞C 18∞C 18∞C in differences in PC production. These inter- and intra- Cd, and these Cd-PC complexes were only observable group differences can help to distinguish suitable algal between days 15 and 20 (Pistocchi, Mormile, Guerrini, groups and genera. Comparing PC production between Isani, & Boni, 2000). In this case, differences in PC algal sorbents, however, is restricted to studies that use production among the tested species likely occurred the same system conditions and quantify PCs using due to differences in the primary detoxification equivalent units (Dong et al., 2020, 2020; Lavoie, Le mechanism utilized. More specifically, only Faucheur, Fortin, & Campbell, 2009). Working within C. fusiformis utilized intracellular detoxification these restrictions, the following sections cover inter- and mechanisms in response to Cd stress, whereas intra-group differences in PC production in algal sor- A. brevipes excluded most of the ambient Cd in its bents exposed to various PTEs. extracellular matrix and P. micans released extracellular polysaccharides into the media. These alternate detox- ification mechanisms used by A. brevipes and P. micans Inter-group Differences resulted in low PC production as well as a lack of Cd adsorption and accumulation (Pistocchi, Mormile, The production of PC may differ between algal groups Guerrini, Isani, & Boni, 2000). Based on these results, despite similar system conditions. Two studies were it may seem that bloom-forming groups, or those that identified which evaluate PC production across multiple rely on granulation via the over-production of EPS, may algal groups under the same system conditions, not rely on intracellular detoxification mechanisms, Pistocchi, Mormile, Guerrini, Isani, & Boni (2000) and producing no or very low levels of PCs (Naveed et al., Ahner, Wei, Oleson, & Ogura (2002). Pistocchi, 2019; Pistocchi, Mormile, Guerrini, Isani, & Boni, Mormile, Guerrini, Isani, & Boni (2000) evaluated the 2000). However, other bloom-forming dinoflagellate effects of sorbent group and genus on PC formation species, like Lingulodinium polyedrum have been during long-term Cd and Cu exposure. These research- observed to produce PCs at concentrations of Cd greater ers studied two diatoms, Cylindrotheca fusiformis and −1 than 1.0 mg l (Romano, Liria, Machini, Colepicolo, & Achnanthes brevipes, and one bloom-forming dinofla- Zambotti-Villela, 2017). It is therefore possible that the gellate, Prorocentrum micans. Only C. fusiformis pro- observed differences in PC production between algal duced measurable levels of PC complexes in response to 22 S. K. READ ET AL. groups in the Pistocchi, Mormile, Guerrini, Isani, & detoxification mechanism employed by an algal group Boni (2000) study relate to species-specific tolerance to should be considered during sorbent species selection. tested PTE concentrations rather than differences in However, as will be covered in the following sections, a sorbent group’s complete detoxification response. even among groups that utilize intracellular detoxifica- Differences in PC production related to PTE concentra- tion mechanisms, further variation in PC production tion are covered in more detail in the PTE and PTE and PTE accumulation may occur on a species-specific Concentration section of this review. basis. Ahner, Wei, Oleson, & Ogura (2002) also explored intergroup differences in the production of PCs in sev- Intra-group Differences eral microalgae groups including diatoms, Phaeodactylum tricornutum, Thalassiosira pseudonana, Although it may be assumed that algal sorbents within and Thalassiosira weissflogii, a coccolithophore, the same group would produce similar levels of PCs, Emiliania huxleyi, and a chlorophyte, Dunaliella sp. In several studies have identified intra-group differences their study, PC production increased across almost all in PC production despite similar experimental phy- algal groups in response to Cu and Cd exposure, except sico-chemical conditions. Ahner, Wei, Oleson, & for P. tricornutum cultures grown in the lowest tested Ogura (2002) also evaluated these between diatoms. −1 concentration of Cd (0.3 mg Cd l with EDTA; For example, at the same Cd concentration. Table 1). Their results indicated that the magnitude of T. pseudonana and T. weissflogii produced over 5 PC production varied between algal groups. Namely, the times the level of PCs as P. tricornutum (Table 1). diatoms T. pseudonana and T. weissflogii, and the coc- Lavoie, Le Faucheur, Fortin, & Campbell (2009) also colithophore produced very high levels of PCs following illustrated intra-group differences through comparison Cu and Cd exposure, while the tested chlorophyte pro- of PC production in two chlorophyte microalgae, duced relatively low levels of PCs (Ahner, Wei, Oleson, Chlamydomonas reinhardtii and Raphidocelis subcapi- −3 & Ogura, 2002). The coccolithophore also accumulated tata, under increasing Cd exposure (0.079 × 10 − −1 the highest levels of Cd and Cu when compared against 0.028 mg Cd l ). Following Cd exposure, both species’ the Thalassiosira diatoms; however, only these three PC content tripled at the highest Cd concentrations −1 cultures were analysed for PTE accumulation and not (0.025–0.028 mg Cd l ; C. reinhardtii ≈700 amol SH −1 −1 every concentration was analysed for PTE removal cell and R. subcapitata ≈ 900 amol SH cell ). This (Ahner, Wei, Oleson, & Ogura, 2002). There were, how- evaluation, however, also suffers from reporting and ever, further issues with the data provided in this study unit selection issues. Specifically, though C. reinhardtii due to sample size and unit selection. Firstly, only the appeared to have higher PC content under control Cd exposure trials for E. huxleyi were duplicated: the PC conditions when reported by cell count, PC levels content reported in all other species and PTEs were were not significantly different between species when based on one culture of each biosorbent; therefore, adjusted for cell biovolume (C. reinhardtii: ~350 µM more trials are required to ensure reproducibility of SH; R. subcapitata ~270 µM SH). Unfortunately, these the reported results. Similarly, though many of these researchers do not report PC production following Cd results are reported based on the average internal exposure adjusted for cell biovolume. If this content volume of each cell, or cell biovolume, this study also was adjusted for cell biovolume, which the authors quantified PC content in relation to chlorophyll state is a factor of 1.3–2.5, it may emerge that a content for a set of experiments aimed at evaluating R. subcapitata actually boasted a higher relative pro- how culture age and sorbent group may relate to PC and portion of PCs as it is the smaller cell. This distinction GSH production. This unit might, however, not provide in PC content is important because C. reinhardtii accu- a reliable comparison for PC content between species, mulated higher levels of Cd corrected for cell biovo- since pigment content may vary between species and/or lume. The higher intracellular storage of Cd by can be affected by a species reaction to physico-chemical C. reinhardtii in Lavoie, Le Faucheur, Fortin, and conditions, including presence and concentration of Campbell (2009) evaluation can likely be attributed to PTE (Zucchi & Necchi, 2001). For this reason, those Cd storage in other intracellular ligands. Other evalua- culture age results have not been reported in Table 1. tions have also observed the storage of PTEs intracel- Essentially, Pistocchi, Mormile, Guerrini, Isani, & lularly via other ligands. For example, using elution Boni (2000) and Ahner, Wei, Oleson, & Ogura (2002) through HPLC, Howe & Merchant (1992) found that illustrate that inter-group differences in PTE tolerance in C. reinhardtii 70% of intracellular Cd was stored by and detoxification mechanism can affect PC production PCs: this would leave 30% of intracellular Cd stored by and subsequent PTE accumulation. Evidence of other intracellular ligands. APPLIED PHYCOLOGY 23 Dong, Wang et al., (2020) and Dong, Zhu et al., Other evaluations have observed significantly differ- (2020) also compare the PC production in two diatom ent PC production in different strains, and even mor- species under different levels of Cd exposure. These photypes, within a single species (Ma, Zhou, Chen, & evaluations are focused on understanding Cd toxicity Pan, 2021; Torricelli, Gorbi, Pawlik-Skowronska, Di and tolerance and quantify PC content as a relative Toppi, & Corradi, 2004). Sorbent strains may be proportion of total proteins (Dong et al., 2020, 2020). altered through historic adaptation to high PTE con- In these evaluations, PC content increased with increas- ditions to improve PC production and PTE removal. ing Cd exposure in both diatom species, P. tricornutum For example, in a comparison of wild-type and Cr- and Skeletonema costatum (Table 1; 400 ppm CO ) tolerant strains of Scenedesmus acutus, Torricelli, (Dong Zhu, et al., 2020; Dong, Wang, et al., 2020); Gorbi, Pawlik-Skowronska, Di Toppi, & Corradi however, the magnitude of PC production varied (2004) found that the Cr-tolerant S. acutus strain between species. Namely, P. tricornutum produced was able to achieve higher PC content during the −1 higher levels of PCs at the 0.4 mg Cd l treatment as highest level of Cd exposure (Table 1). This evalua- compared with S. costatum, and S. costatum produced tion suggests sorbents can develop co-tolerances to −1 higher levels of PCs at the 1.2 mg Cd l treatment certain PTEs. In terms of WWT and sorbent selection, (Table 1). These differences in PC production could these differences in PC production suggest that more potentially be correlated to a higher level of intracellular robust species that are tolerant to a wide range of Cd storage achieved with higher PC content. conditions and PTE concentrations may make highly Intracellular Cd storage was associated with higher PC effective bioaccumulators in PTE-containing WWs. production in S. costatum; however, intracellular Cd Similarly, in an evaluation of morphotype effects on storage was not measured in P. tricornutum as this PTE tolerance in P. tricornutum, cell characteristics evaluation was principally concerned with defining Cd associated with the oval morphotype of the dinofla- tolerance rather than biosorption capacity. Without gellate led to a doubling of PC content as compared information on intracellular Cd storage, it is not possi- with the fusiform or sickle-shaped morphotypes (Ma, ble to define the relative contribution of PC production Zhou, Chen, & Pan, 2021). in the P. tricornutum cultures. These differences in data As evidenced by the evaluations reported in this reporting in Dong, Zhu et al., (2020); Dong, Wang et al., section, though a sorbent’s species or genus may pro- (2020)), and Lavoie, Le Faucheur, Fortin, & Campbell vide fundamental information on the PTE tolerance (2009) highlight the importance of evaluating other and accumulation potential of that sorbent, many stu- factors alongside PC production to distinguish the dif- dies have identified a high-level of inter- and intra- ferences in sorbent performance. Specifically, though group variation in PC production. This variation may the production of PCs is valuable in terms of under- lead to case-specific differences in PTE tolerance and standing the relative PTE tolerance and indicate storage removal. Evidence of these differences in PC produc- location, complementing this information with an esti- tion and PTE removal may support the exploitation of mate of intracellular PTE content and the role of other a locally available or low-cost sorbent species that intracellular or extracellular ligands provides a complete come from genera previously discounted for low PTE picture of the PTE removal location and recovery removal. potential. The results from these evaluations also highlight Finally, though it may be expected that species the importance of reporting PC content adjusted by within the same genus would boast similar detoxifica- cell biovolume and reporting intracellular PTE con- tion responses, variation in PC generation persists tent to understand the role of PCs in the overall even at the genus and species-level. Genus-level var- detoxification response. For unit selection, units iation emerged in the Ahner, Wei, Oleson, & Ogura weighted by cell biovolume or dry weight offer the (2002) study where T. pseudonana generated nearly most reliable illustration of PC production, and stan- double the total PCs of T. weissflogii.at the 3.0 mg Cd dardization of these units will help with comparisons −1 l treatment (Table 1) (Ahner, Wei, Oleson, & between evaluations. Furthermore, evaluating the Ogura, 2002). This has also been observed in presence of other intracellular compounds or typify- a comparison of xanthophytes from the Vaucheria ing the magnitude of EPS production, can help to genus (Skowroński, De Knecht, Simons, & Verkleij, define the role of PCs in the sorbents detoxification 1998). In this evaluation, Vaucheria compacta pro- response. Despite these inconsistencies, the outlined duced 3–6 times more PCs than Vaucheria debaryana studies highlight the variability among live algal sor- under comparable system conditions and Cd levels bents, and, subsequently, the wealth of further (Skowroński, De Knecht, Simons, & Verkleij, 1998). research opportunities. 24 S. K. READ ET AL. Glutathione production et al., 2019). This decline is likely due to PC content, which reaches its peak concentration in this treatment As it forms the building blocks for PC production, GSH by day 12. As these researchers supplemented Cu and is essential for algae’s ability to cope with PTE stress and nutrients every 48 h, it is likely that the drop in GSH store PTEs intracellularly through PC complexes content is related to sustained PC production rather (Kawakami, Gledhill, & Achterberg, 2006b) (Fig 2). than nutrient deficiency or reduction in the magnitude GSH is present in plants and algae, and mitigates oxida- of the GSH response after an alleviation of Cu stress. tive and radiative damage, acting as a non-specific Understanding the length of time resulting in exhaus- reductant during oxidative stress and PTE exposure tion of GSH stores can help to optimize exposure time (Kawakami, Gledhill, & Achterberg, 2006b; Rezayian, to peak PC production and PTE accumulation. From Niknam, & Ebrahimzadeh, 2019). The production a WWT perspective, reducing exposure time to the dynamics of this thiol peptide can be complex as GSH minimum required period will be essential in designing serves several antioxidative functions in the cell (Howe the most efficient WWT systems. & Merchant, 1992; Kawakami, Gledhill, & Achterberg, GSH production and exhaustion may also be affected 2006b; Lavoie, Le Faucheur, Fortin, & Campbell, 2009). by present PTEs. Specifically, present PTEs may interact GSH may also be extruded to support PTE detoxifica- with GSH-related enzymes to inhibit or promote GSH tion in an alga’s immediate environment (Kawakami, production. Nagalakshmi and Prasad’s (2001) evalua- Gledhill, & Achterberg, 2006b; Laglera & Van Den Berg, tion of S. bijugatus, for example, explores the inhibitory 2003). GSH dynamics during PTE exposure, and how dynamics in greater detail. In this evaluation, the activ- they affect PC synthesis, have been quantified in several ity of the GSSG-reductase (GSSG-R) is restricted by the laboratory studies. interaction of Cu with an SH group on the enzyme GSH typically increases with PTE exposure, however, (Devez, Achterberg, & Gledhill, 2015; Nagalakshmi & the length of PTE exposure may alter GSH production. Prasad, 2001). This enzyme normally reduces oxidized Initially, over the first few hours of PTE exposure, GSH GSH, GSSG, back to GSH (Fig 1). This reduction is an production may be excited by the presence of PTEs. essential recovery step following oxidative stress to This dynamic has been observed in several studies regenerate available GSH pools (Anjum et al., 2012). −1 (Ahner, Wei, Oleson, & Ogura, 2002; Dong et al., At Cu concentrations of ~6.5 and 13 mg l GSSG-R 2020; Kawakami, Gledhill, & Achterberg, 2006a, activity declined by 44 and 69%, respectively, as com- 2006b). As PTE exposure continues over days in batch pared with Cu-free rates of activity (Nagalakshmi & exposure experiments, GSH stores may drop, either in Prasad, 2001). With GSSG-R partially incapacitated, response to exhaustion of GSH stores, reduction of GSH replenishment is restricted. Under these condi- ambient PTEs, or transformation of GSH-PTE com- tions, PC-PTE complexes are synthesized from existing plexes to PC-PTE complexes. All of these factors may PTE-loaded GSH without replenishment of GSH from be the source of the overwhelmingly negative trends in GSSG, resulting in the exhaustion of GSH stores. GSH production observed in the Ahner, Wei, Oleson, & Though Volland, Schaumlöffel, Dobritzsch, Krauss, & Ogura (2002) study. In this evaluation, diatom, micro- Lütz-Meindl (2013) also tested the effect of Cu on GSH algae, and coccolithophore cultures were exposed to levels, their evaluation used a Cu concentration of 0.02 −1 various concentrations of Cd or Cu in “long-term” mg l . This comparatively low concentration may not exposure experiments (exposure period defined as achieve detectable inhibition of the GSSG-R enzyme; “two generations”). In the majority of cultures, GSH however, there is also evidence that beneficial enzyme- content dropped between Day 0 and the final day of PTE interactions in algae and higher plants may also sampling. It is difficult to distinguish the source of this impact GSH production. In the Nagalakshmi and GSH production without more detailed sampling time, Prasad’s (2001), the enzyme γ-glutamylcysteine (γ- −1 or analysis of other media constituents. Navarrete et al. GCS) increased in response to ~3.0 and 6.0 mg Cu l (2019) provide a more detailed assessment of GSH exposure by 6 to 18%, respectively. γ-GCS is generally dynamics, cataloguing changes to GSH production in the limiting enzyme in GSH production, as it is upre- Ulva compressa over 12 days. In U. compressa, GSH gulated by the absence of GSH; however, in the case of content increases over the first 5 days of exposure in S. bijugatus, GSSG-R is the limiting enzyme to GSH −1 solutions containing 0.3 and 0.6 mg Cu l , but the GSH production as it is inhibited to a far greater extent than content then declined slightly at the day 12 measure- γ-GCS is upregulated (Nagalakshmi & Prasad, 2001; −1 ment (Navarrete et al., 2019). In the 1.0 mg l treat- Noctor et al., 1995). Other PTEs have improved γ-GCS ment, GSH reached its peak levels on day 5 and then performance in plant systems. Cd, for example, has been declined below control content by day 12 (Navarrete observed to have a beneficial effect on the enzyme γ- APPLIED PHYCOLOGY 25 GCS in plant cells, promoting GSH production (Anjum mats in response to synthetic mine drainage containing et al., 2012; Nagalakshmi & Prasad, 2001; Rüegsegger & multiple PTEs. In this study, wild-harvested Brunold, 1992; Schäfer, Haag-Kerwer, & Rausch, 1998). Stigeoclonium mats were cleaned and exposed to syn- Despite a thorough literature review, upregulation of γ- thetic mine drainage containing µM concentrations of GCS by Cd was not identified in this review, and there Zn, Cu, Cd, Pb, Ca, Mg, and Fe (Pawlik-Skowrońska & was no evidence of this effect in any of the PTE-algae Bačkor, 2011). Depending on the solution pH and systems covered in this work. Lavoie, Le Faucheur, resulting bioavailability of the present PTEs, PC produc- Fortin, & Campbell (2009), for example, did not identify tion increased by up to ~2.5–2.8 fold (Pawlik-Skowron, an increase in intracellular GSH in studied microalgae 2001). The researchers suggest that a ~ 4× increase in species following Cd exposure (C. reinhardtii and the labile proportion of Zn in the pH 6.8 mine drainage R. subcapitata) (Lavoie, Le Faucheur, Fortin, & led to the steep increase in PC production as compared Campbell, 2009). This could be due to the concentration with Stigeoclonium grown in the pH 8.2 synthetic mine of Cd in this study, which was only introduced in the drainage. pH may also directly affect algal sorbents by −3 −1 range of 0.078 × 10 to 0.03 mg l or could be related impacting individual survival (Hansen, 2002), growth to differences between algal and plant cells. Therefore, rate (Chen & Durbin, 1994; Hansen, 2002), biochemical enzymes integral to GSH production may be affected by profile (Khalil, Asker, El-Sayed, & Kobbia, 2010; PTE exposure, having downstream consequences on Moheimani, 2013), photosynthetic rate (Qiu, Gao, GSH stores and PC production. Furthermore, the Lopez, & Ogden, 2017), protonation of negatively inconsistencies in enzyme behaviour between algae- charged surface structures (Holan & Volesky, 2014; PTE systems illustrate the high-level of variability Tüzün et al., 2005), and CO uptake (Chen & Durbin, between algal sorbents, and the myriad opportunities 1994). However, there were no evaluations identified in for further research in the field this review comparing metabolic changes. In terms of WWT, adequate GSH levels are vital to Similar to pH, temperature may indirectly affect PC the synthesis of PC-PTE complexes, intracellular PTE generation through changes to culture productivity, or tolerance, and, ultimately, a culture’s ability to survive directly impact it by effecting enzymatic activity neces- PTE exposure and accumulate PTEs (Piña-Olavide sary for its synthesis (Hedayatkhah et al., 2018; Lambert et al., 2020; Torricelli, Gorbi, Pawlik-Skowronska, Di et al., 2016; Wang & Wang, 2008). Impact of tempera- Toppi, & Corradi, 2004). Therefore, if GSH content or ture on subcellular PC pools has also been investigated production drops significantly, GSH may not be avail- in benthic macroalgae and diatom species (Skowroński, able for PC synthesis, halting proper PTE accumulation. De Knecht, Simons, & Verkleij, 1998). Skowroński, De Factors affecting GSH production, like exposure time Knecht, Simons, and Verkleij (1998) explored changes and the interaction of present PTEs, should be consid- to Cd accumulation in Vaucheria compacta and ered during live algal sorbent system design. V. debaryana. In this evaluation, Cd accumulation cor- related significantly with temperature, Cd concentra- tion, and exposure time in the studied species. For Physico-chemical conditions V. compacta, increasing the temperature from 8°C to Due to the metabolic requirements of live sorbents, PC 16°C led to a doubling of PC and PC , and measurable 2 3 production may be impacted by physico-chemical con- production of PC (33; Table 1). By changing the tem- ditions including pH, temperature, light intensity (LI), perature from 4°C to 18°C, V. debaryana exhibited and CO enrichment. Beginning with pH, pH is often a smaller increase of PC production in PC at 31%, but considered the key physio-chemical condition restrict- PC content increased by 56%. These temperature- ing the use of live algal sorbents for WWT. The reason dependent changes to PC production also resulted in for this restriction is the incongruence between the pH increases to the Cd content. For example, for at which PTE availability is generally optimized (pH 3– V. debaryana, when temperature increased from 4°C 5), and the pH at which aquatic and marine alga gen- to 18°C, Cd accumulation increased from 17.6 ± 2.2 to −1 erally thrive (pH 6.5–8). Although pH-related mobility 24.3 ± 3.4 µmol Cd g DW. A similar result was and availability vary between PTEs, the optimal pH for obtained for V. compacta, where increasing the tem- a PTE will be a range at which the PTE exists in solution perature from 8°C to 16°C, led to ~40% increase in Cd −1 rather than precipitating or volatilizing out of solution accumulation (12.9 ± 1.5 to 20.3 ± 3.4 µmol SH g (Wood, 1985). For this reason, pH may indirectly affect DW). At lower temperatures, reduced efficiency of PC PC production in multi-PTE solutions by affecting the production and Cd accumulation may be attributed to bioavailability of present PTEs. Pawlik-Skowron (2001), reduced Cd ion transport into the cell and diminishing for example, evaluated PC dynamics in Stigeoclonium functionality of the temperature-dependent PC synthase 26 S. K. READ ET AL. enzyme, which has an optimal temperature of 35°C photosynthetic capacity relating to high irradiance (Skowroński, De Knecht, Simons, & Verkleij, 1998). may also impact PC production and PTE accumula- Wang and Wang (2008) also found that increasing the tion. For example, in Sarcodia suiae, increasing LI temperature from 18° to 24°C increased subcellular PC negatively impacted the accumulation of As, due to pools, resulting in higher intracellular Cd accumulation damage to photosynthetic organs, resulting in depig- in the diatom Thalassiosira nordenskioeldii, increasing mentation (Libatique, Lee, & Yeh, 2019). Although −1 from 523 ± 14.5 to 718 ± 18.6 µmol Cd mol C , respec- this evaluation does not measure PC pools, it is pos- tively. These authors connect the temperature- sible that a reduction in photosynthetic activity dependent Cd accumulation to changes in PCs as well restricted available energy for PC generation. as other thiol-containing compounds; however, there Finally, energy availability may also modulate PC was a limit to the beneficial effects of temperature. pools in CO enriched environments, however, not in Though the Vaucheria sp. study suggests that PC the same manner that occurs based on temperature synthase enzyme is optimal at 35°C, Wang and Wang and LI. Dong, Wang, et al. (2020) and Dong, Zhu, et (2008) observed a drastic drop in intracellular Cd, 211 ± al. (2020) tested PC production in response to Cd −1 2.34 µmol Cd mol C , when T. nordenskioeldii was exposure marine diatoms, Skeletonema costatum and grown at 30.5°C, accompanied by a reduction in the P. tricornutum, respectively, at normal CO content magnitude of PC pools as compared with the cultures (400 ppm CO ) and CO content typical of ocean 2 2 grown in similar levels of Cu exposure at 18°C and 24°C. acidification (1500 ppm CO ). Both studies identified However, the magnitude of this decline in Cd accumu- a reduced generation of PCs as a result of CO enrich- lation and detoxification can only partially be explained ment, but despite this reduction, toxicity related to Cd by reduced PC production, as temperature changes may exposure was mitigated, allowing for higher growth also affect other aspects of the detoxification process, and chlorophyll a content over long-term exposure. including GSH, resulting in higher Cd sensitivity (Wang For example, under CO enrichment, P. tricornutum −1 & Wang, 2008). cultures grown in 0.4 and 1.2 mg l of Cd reached In industrial algae production, LI is most often densities 160.69% and 187.59%, respectively, greater −1 considered for its effect on biomass production than the control cultures at 0 mg Cd l and 400 ppm (Peckol et al., 1994) or fatty acid synthesis (Pinto CO (Dong, Wang, et al. (2020) and Dong, Zhu, et al. et al., 2011). Similar to other physio-chemical condi- (2020). The authors traced this mitigated toxicity to tions, algal sorbents may require different optimal LI, a shift in the principle ligand responsible for intracel- which depends on the culture density and algae spe- lular detoxification from PCs to GSH (Dong et al., cies. Culture density had a parabolic relationship to 2020a, 2020b). In order to conserve energy under the LI. In densely packed cultures, light can be attenuated combined stress of CO enrichment and Cd exposure, quickly, leading to uneven LI and reductions in it seems that both marine diatoms favoured production growth rate (Wahal & Viamajala, 2010). On the of the multifunctional GSH molecules to combat oxi- other hand, low density cultures can be overexposed dative damage, rather than investing in costly and to light, leading to the inhibition of photosynthesis PTE-specific PCs (Dong, Wang, et al. 2020; Dong, (Wahal & Viamajala, 2010). Only one evaluation Zhu, et al. 2020; Kawakami, Gledhill, & Achterberg, assessed the impact of LI on PC generation using 2006b). Despite the switch in ocean acidification con- two macroalgae species from the Vaucheria genus, ditions, S. costatum cultures’ intracellular Cd accumu- V. compacta and V. debaryana. In this study, though lation significantly increased from ~2.2 to ~3.2 mg −1 −1 PCs were produced in response to Cd in both light Cd kg DW and ~2.4 to ~4.1 mg Cd kg DW in the −1 and dark conditions, PC pools in the dark conditions 0.4 and 1.2 mg Cd l treatments, respectively (Dong, were 50–60% lower than those observed in the light Wang, et al., 2020). In terms of wastewater treatment, sufficient conditions (Skowroński, De Knecht, this increased intracellular PTE tolerance under CO Simons, & Verkleij, 1998). This reduced generation enrichment could support the inclusion of flue gas into resulted in Cd accumulation falling by ~47% and 43% certain PTE remediation systems, though not through in V. compacta and V. debaryana, respectively. These the increased generation of PC pools (Onyancha, trends in PC content and Cd accumulation were most Lubbe, & Brink, 2021). likely related to photosynthetic activity and available Essentially, physico-chemical conditions can alter the energy. With reduced photosynthetic activity, there PC pools either through contribution to cellular stress may be lower levels of energy available for cellular or alterations to energy available for the energy- “work”, and high-energy detoxification methods like intensive detoxification mechanism. In active sorbents, PC production may be restricted. Alterations to like live algae, metabolic requirements must be met in APPLIED PHYCOLOGY 27 order to maintain cell productivity, support a sufficient dynamics of multi-PTE solutions is therefore essential detoxification response, and ensure PTE accumulation. for proper WWT, as multiple PTEs may be present in Identifying the optimal system conditions for each sor- WW effluent. Mixed-PTE solutions have been evaluated bent to maximize PC production and PTE accumulation in PTE removal more generally, but this review did not is essential to ensure the viability of these WWT tools; find evidence of a comprehensive analysis of PC pro- however, observing shifts in the predominant detoxifi- duction in mixed-PTE solutions, except for Pawlik- cation response will also help to understand if shifting Skowron’s (2001) evaluation of Stigeoclonium mats. As conditions simply alter the favoured detoxification previously mentioned in the Physico-Chemical route without negatively impacting PTE removal. Conditions section, PC production was chiefly affected by changes in Zn concentration in the mixed PTE solu- tion. In this same evaluation, the researchers also PTE and PTE concentration exposed Stigeoclonium mats to 10 µM of single-PTE Since PC production plays a dominant role in detoxifi- solutions of Cd, Pb, and Zn. Although pH changes in cation and subsequent tolerance to PTE pollution, PCs the mixed-PTE solutions identified Zn as the major predominantly have a positive relationship to PTE determinant of PC production in the mixed-PTE solu- exposure and increasing PTE concentrations. In terms tion, in single-PTE solutions, Cd produced the highest of present PTEs, PC production has been linked to Cd, total PC response, followed by Pb and then Zn. These Cu, Cr, Zn, Pb, and Hg exposure (Table 1). However, differences in PC production in single- versus mixed- the occurrence and magnitude of PC production is not PTE solutions illustrate the value of testing both expo- uniform in response to these PTEs. For instance, Ahner sure mediums to determine changes to sorbent perfor- & Morel (1995b) found that PC production by mance. Although this was performed in the Pawlik- T. weissflogii was highly dependent on present PTE. In Skowron’s (2001) study, in the wider literature there is this study, T. weissflogii, was grown in the presence of a lack of information on the changes to PC synthesis and Cd, Pb, Ni, Cu, Zn, Co, Ag, and Hg. Cd, Zn, and Cu, to PTE storage in response to mixed-PTE solutions. a lesser extent, excited PC formation in short-term Understanding the relative contribution of PTEs to PC exposure experiments; however, these results were production, in single- and mixed-PTE solutions is reported in nmol PCs per chlorophyll a content essential for defining the sorbent’s suitability to WW (Ahner & Morel, 1995b). As outlined previously, this effluents where PTE content and concentration may be unit is not reliable due to the changeable nature of varied and episodic. chlorophyll a. Subsequently, though PCs were generated In terms of PTE concentration, several studies iden- in response to these PTEs, the relative magnitude of PC tified changes to PC production based on PTE concen- production between PTEs cannot be determined. tration (Ahner, Wei, Oleson, & Ogura, 2002; Dong Volland, Schaumlöffel, Dobritzsch, Krauss, and Lütz- Wang, et al., 2020; Dong, Zhu, et al., 2020; Navarrete Meindl (2013) also evaluated the varying effects of sin- et al., 2019; Skowroński, De Knecht, Simons, & Verkleij, gle-PTE solutions on PC production. In short-term 1998; Torricelli, Gorbi, Pawlik-Skowronska, Di Toppi, batch exposures to Cd, Cr, and Cu, Micrasterias denti- & Corradi, 2004). All of these evaluations observe an culata produced PCs in response to Cd and Cr, but not increase in PC production at higher PTE concentrations Cu (Volland, Schaumlöffel, Dobritzsch, Krauss, & Lütz- (Table 1). Ahner & Morel (1995a) also found that PC Meindl, 2013). The lack of PC production during PTE levels declined as PTE concentration decreased in the exposure may indicate an alternate detoxification media over the exposure period (Ahner & Morel, method for Cu, e.g., exclusion in the EPS or alternate 1995a). This study indicated that PC production was intracellular ligands in this particular sorbent (Pawlik- highly reactive to PTE stress as well as the alleviation of Skowrońska, 2003). These evaluations illustrate the that stress. Wang and Wang (2011) also explored this complex variation in live algal sorbent performance in principal further, evaluating how PC production reacted PTE remediation and highlight the high-level of opti- to periods of recovery following PTE stress. In this mization available through sorbent selection. study, T. nordenskioeldii PC production was dependent Most evaluations in this review, however, define PC on ambient Cd concentration, quickly responding to excitation following exposure to single-PTE solutions increased Cd concentration as well as to the reduction without evaluating the effects of mixed-PTE solutions. of it. In this evaluation, following 24 h of recovery from In mixed-PTE solutions, PTEs may interact at binding Cd exposure, T. nordenskioeldii produced higher levels sites, working in coordination or competition, altering of PC in response to another round of high Cd expo- −5 −1 the magnitude of PC production through changes to sure (0.944×10 mg l ) (Wang & Wang, 2011). intracellular PTE transport. Understanding the Changes to PTE removal following short-periods of 28 S. K. READ ET AL. recovery have also been observed in Microcystis aerugi- does provide information on the behaviour of PTEs in nosa exposed to Cd and Zn (Zeng, Yang, & Wang, related detoxification systems. The role of mixed-PTE 2009). In this evaluation, the accumulation increased solutions on PC production across multiple species were following a 24 hr recovery from PTE exposure; however, not identified in this exhaustive literature review. On the the researchers do not measure PC production and so other hand, nutrient concentrations may shift tempo- the nature and magnitude ligand’s role in this change is rally and spatially in WWs, and these shifts may affect unclear. From a WWT perspective, elevated accumula- PC production and, ultimately, PTE removal. There are tion following a period of recovery could improve sor- studies that have evaluated the effects of nutrient con- bent performance in WWs where PTE exposure is ditions on PTE import without defining changes to PC episodic. production (Hedayatkhah et al., 2018; Neumann, De Wang & Wang (2011), however, also found that Souza, Pickering, & Terry, 2003; Taboada-de la when ambient Cd concentration is reduced, PCs may Calzada, Villa-Lojo, Beceiro-González, Alonso- be quickly extruded resulting in a decline in intracel- Rodrı́guez, & Prada-Rodrı́guez, 1998). For example, lular Cd (Ahner & Morel, 1995a; Wang & Wang, 2011). Taboada-de la Calzada et al. (1998) found evidence 3– This response resulted in Cd returning to the ambient that toxic AsO may share a common uptake route 3– environment instead of being locked in sorbent cells. with NO – and PO in C. vulgaris. Under nutrient 3 4 Although this presents issues in WW streams with depleted conditions, C. vulgaris accumulated 12% more 3– intermittent PTE pollution, it also presents an oppor- AsO than under nutrient sufficient conditions tunity for non-destructive PTE recovery. For example, (Taboada-de la Calzada, Villa-Lojo, Beceiro-González, after WWT, PTE-loaded algal sorbents could be trans- Alonso-Rodrı́guez, & Prada-Rodrı́guez, 1998). The ferred to a much smaller volume of clean media, allow- researchers suggest that the toxic metalloid species has ing for the controlled release of accumulated PTEs. a similar chemistry to these nutrients suggesting that 3– This method of recovery is an area of emerging AsO may exploit the same uptake route as NO – and 3 3 3– research in macro- and microalgae with studies pre- PO . This dynamic has also been observed in Se sys- 2− dominately focusing on the release of PTE-loaded PCs tems, where selenate (SeO ) shares the sulphate 2− to indicate individual and culture resilience rather than (SO ) uptake route in freshwater Chlorella sp. as a PTE recovery method (Pesce, Ghiglione, & (Neumann, De Souza, Pickering, & Terry, 2003). Martin-Laurent, 2017). Alternatively, there is evidence Neumann, De Souza, Pickering, & Terry (2003) identi- that, in certain sorbents, PCs are stable over short-term fied that under nutrient deprivation 90% of the 20 mM recovery periods. Navarrete et al. (2019) evaluation of of provided selenate was accumulated by the Chlorella U. compressa found that although accumulated PTEs biomass; however, when supplemented with 1 mM of were extruded following a period of Cu-free recovery, sulphate, the remediation efficiency dropped to 1.8% they also identified that PCs were not released into the (Neumann, De Souza, Pickering, & Terry, 2003). PTE-free seawater. Instead, PTEs were extruded via Although there were no studies in this review that GSH during the recovery period (Navarrete et al., directly analysed the effects of nutrient deprivation on 2019). This lack of exudation of PC complexes shows PTE transport and PC production, it would be necessary a route for stable PTE retention, potentially cushioning to define these interactions before field-scale testing of PTE loss during episodic PTE exposure. The mismatch many of the algal sorbents identified in this review. in PC exudation in T. nordenskioeldii and U. compressa Overall, there were several examples of increased also illustrates the level of variability between live algal PC synthesis in response to Cd, Cu, Zn, Pb, and Hg, sorbents. and some algae-PTE systems showed evidence of In terms of the effects of PTE and PTE concentration highly responsive and dynamic PC production in on PC production, future research should consider response to changes in PTE exposure. Though more complex PTE solutions like those containing many systems showed that PC production changed a mixture of PTEs or other potentially competitive with PTE exposure, the magnitude of PC change ions. PTE interactions have been explored in higher was not standardized in all algae-PTE systems or plant systems and indicate that combined exposure between PTEs. This inconsistency shows the impor- can increase negative consequences to the exposed sor- tance of assessing multiple live sorbents and PTEs bent. For example, in Brassica napus exposed to Cr and under the same system conditions to understand the Cu, combined exposure enhanced oxidative damage, comparative effects. Similar to other sections, units reduced pigment content and impacted plant quality need to be standardized and consider cell bio- (Li et al., 2018). Although trends observed in higher volume and potential changes to water content fol- plants may not directly translate to algal systems, it lowing PTE exposure. APPLIED PHYCOLOGY 29 Exposure time selected instead. On the other hand, long-term exposure with a PC producing algal sorbent could improve the PC production had a positive relationship to exposure stability of PC-PTE complexes as longer chain oligo- time. This trend has been observed over long-term expo- mers are synthesized. Although it is not clear if these sure to PTEs in C. fusiformis and U. compressa (Navarrete trends would be mirrored in other systems, et al., 2019; Pistocchi, Mormile, Guerrini, Isani, & Boni, In conclusion, overall, sorbent species, present PTEs, 2000). In Pistocchi, Mormile, Guerrini, Isani, & Boni PTE quantity, exposure time, and changes to physico- (2000) study, C. fusiformis produced PCs in response to chemical conditions may affect PC synthesis and, sub- Cd exposure, and the level of production was positively sequently, PTE removal. Changes in PC production as correlated to exposure time. In this evaluation during a result of these factors highlight the range of opportu- −1 exposure to 0.5 mg Cd l , Cd accumulation by PCs nities for system optimization to maximize PTE removal increased from 79% to 90% between days 15 and 21. This through increased PC production by different algal rise suggests that PC pools would have increased species. between day 15 to 21 to accommodate the higher percen- With the ligand only being identified in higher plants in tage of PC-bound Cd (Table 1, 16). Navarrete et al. (2019) the 1980s, however, this area of research is still relatively also found increasing PC production in semi-batch expo- new and there is a range of opportunities for standardiza- sure experiments, providing a more detailed account PC tion of experimental methods and further research (Singh content. In this evaluation, researchers observed the com- & Schwan, 2019). In terms of standardizations, unit choice plementary detoxification response of GSH, PCs, and was one of the key restricting factors to comparing PC class-II metallothioneins in the marine seaweed. production in different sorbents. At the moment, units Navarrete et al. (2019) also identified that the production relating PC content to SH content per cell, pigmentation, of different PC oligomers was affected by time in or protein content leave room for confounding results. U. compressa’s Cu detoxification response. In terms of Even Navarrete et al. (2019) use of fresh weight in the PC production, over a 12-day exposure period, PC dimers PC content unit for U. compressa could be skewed by (PC ) and tetramers (PC ) were consistently produced at 2 4 osmotic responses to PTE toxicity (Sánchez-Thomas −1 a high level in the 0.843 mg Cu l treatment. There was et al., 2020). Adjusting PC content for cell biovolume, as also a slower increase in PC dimers in 0.3, 0.6, and 1.0 mg in Lavoie, Le Faucheur, Fortin, & Campbell (2009), or dry −1 Cu l . Peak PC content occurred on the final weight may help to reduce confounding factors affecting −1 sampling day in the 1.0 mg Cu l . Production of PC comparison of live algal sorbents. occurred to a much lower extent, peaking at ~80 nmol Ultimately, in the field of bioaccumulation, there are −1 −1 G FW on day 1 in the 0.843 mg Cu l treatment, and a wealth of opportunities for optimization and further after 12 days of exposure the highest PC content was in research, particularly as it pertains to understanding and −1 −1 the 1.124 mg Cu l treatment (~60 nmol g FW), again to optimizing the role PCs play in live algal biosorbents. a much lower extent than PC . This increase in longer PC Specifically, defining the impact of system conditions on polymers over long-term exposure at the highest Cd con- PC production, will help to vet the efficacy of algal biosor- centration may be specific to the U. compressa – Cu bents for certain WW streams and define routes for PTE system, but it suggests that exposure time may improve recovery. the stability of PC-PTE complexes as longer oligomers are synthesized over time in the higher PTE treatments (Kneer & Zenk, 1997; Lavoie, Le Faucheur, Fortin, & Campbell, Acknowledgements 2009; Navarrete et al., 2019). This response, however, was dependent on the concentration of PTEs. We would like to acknowledge the support of the British Phycological Society through their Covid-19 Recovery Award. These evaluations into the effects of continued PTE exposure on PC production provide interesting insights into PTE storage location and stability over long-term exposure. As there is evidence PC production may con- Disclosure statement tinually increase with PTE exposure time, exposure time No potential conflict of interest was reported by the authors. may be modulated to control PTE storage location. For example, if PTEs must be easily recovered through non- destructive processes, such as desorption, shorter expo- Funding sure times may prevent high levels of intracellular PTE accumulation, or a sorbent which predominately uses Funding for this literature review came from the British exclusion as the main detoxification response could be Phycological Society through their Covid-19 Recovery Award 30 S. K. READ ET AL. Cobbett, C., & Goldsbrough, P. (2002). Phytochelatins and Abbreviations metallothioniens: roles in heavy metal detoxification and EPS Extracellular Polymeric Substances homeostasis. Annual Review of Plant Biology, 53, 159–182. GSH Glutathione doi:10.1146/annurev.arplant.53.100301.135154 LI Light Intensity Croot, P. L., Moffett, J. W., & Brand, L. E. (2000). Production PC Phytochelatins of extracellular Cu complexing ligands by eucaryotic phy- PTE Potentially Toxic Element toplankton in response to Cu stress. Limnology and RE Removal Efficiency Oceanography, 45, 619–627. doi:10.4319/lo.2000.45.3.0619 SD Standard Deviation Danouche, M., El Ghachtouli, N., El Baouchi, A., & El SH sulphhydryl Arroussi, H. (2020). Heavy metals phycoremediation WW Wastewater using tolerant green microalgae: enzymatic and WWT Wastewater Treatment non-enzymatic antioxidant systems for the management of oxidative stress. Journal of Environmental Chemical Engineering, 8, 104460. doi:10.1016/j.jece.2020.104460 Devez, A., Achterberg, E., & Gledhill, M. (2015). 15 metal Author Contributions ion-binding properties of phytochelatins and related ligands. In Metallothioneins and Related Chelators. doi:10. S.K.R., M.E.R., A.J.C.S., and M.C.G. conceived and planned 1515/9783110436273-020 the project. S.K.R. reviewed the literature. S.K.R. wrote the Dong, F., Wang, P., Qian, W., Tang, X., Zhu, X., Wang, Z. . . . manuscript. S.K.R., M.E.R., A.J.C.S., and M.C.G. reviewed and Wang, J. (2020). Mitigation effects of CO2-driven ocean edited the manuscript. M.E.R., A.J.C.S., and M.C.G supervised acidification on Cd toxicity to the marine diatom skeleto- the project. S.K.R. acquired the funding. nema costatum. Environmental Pollution, 259, 113850. doi:10.1016/j.envpol.2019.113850 Dong, F., Zhu, X., Qian, W., Wang, P., & Wang, J. (2020). References Combined effects of CO2-driven ocean acidification and cd stress in the marine environment: enhanced tolerance of Ahluwalia, S. S., & Goyal, D. (2007). Microbial and plant phaeodactylum tricornutum to cd exposure. Marine derived biomass for removal of heavy metals from Pollution Bulletin, 150, 110594. doi:https://doi.org/10. wastewater. Bioresource Technology, 98, 2243–2257. 1016/j.marpolbul.2019.110594 doi:10.1016/j.biortech.2005.12.006 Foster, P. L. (1982). Species associations and metal contents of Ahner, B. A., & Morel, F. M. M. (1995a). Phytochelatin pro- algae from rivers polluted by heavy metals. Freshwater duction in marine algae. 1. An Interspecies comparision. Biology, 12, 17–39. doi:10.1111/j.1365-2427.1982.tb00601.x Limnology and Oceanography, 40, 658–665. doi:10.4319/lo. Friedlova, M. (2010). The influence of heavy metals on soil 1995.40.4.0658 biological and chemical properties. Soil and Water Ahner, B. A., & Morel, F. M. M. (1995b). Phytochelatin Research, 5, 21–27. doi:10.17221/11/2009-swr production in marine algae. 2. Induction by various Gaudry, A., Zeroual, S., Gaie-Levrel, F., Moskura, M., metals. Limnology and Oceanography, 40, 658–665. doi:10. Boujrhal, F. -Z., El Moursli, R. C. , andDelmas, R. (2007). 4319/lo.1995.40.4.0658 Heavy metals pollution of the Atlantic marine environment Ahner, B. A., Wei, L., Oleson, J. R., & Ogura, N. (2002). by the Moroccan phosphate industry, as observed through Glutathione and other low molecular weight thiols in mar- their bioaccumulation in Ulva lactuca. Water, Air, and Soil ine phytoplankton under metal stress. Marine Ecology Pollution, 178, 267–285. doi:10.1007/s11270-006-9196-9 Progress Series, 232, 93–103. doi:10.3354/meps232093 Gekeler, W., Grill, E., Winnacker, E. L., & Zenk, M. H. (1988). Anjum, N. A., Ahmad, I., Mohmood, I., Pacheco, M., Algae sequester heavy metals via synthesis of phytochelatin Duarte, A. C., Pereira, E. . . . Prasad, M. N. V. (2012). complexes. Archives of Microbiology, 150, 197–202. doi:10. Modulation of glutathione and its related enzymes in 1007/BF00425162 plants’ responses to toxic metals and metalloids-a review. Gómez-Jacinto, V., García-Barrera, T., Gómez-Ariza, J. L., Environmental and Experimental Botany, 75, 307–324. Garbayo-Nores, I., & Vílchez-Lobato, C. (2015). doi:10.1016/j.envexpbot.2011.07.002 Elucidation of the defence mechanism in microalgae Boran, M., & Altinok, I. (2010). A review of heavy metals in Chlorella sorokiniana under mercury exposure. identifica- water, sediment and living organisms in the black sea. tion of Hg–phytochelatins. Chemico-Biological Interactions, Turkish Journal of Fisheries and Aquatic Sciences, 10, 238, 82–90. doi:10.1016/j.cbi.2015.06.013 565–572. doi:10.4194/trjfas.2010.0418 Hansen, P. J. (2002). Effect of high pH on the growth and Chen, C. Y., & Durbin, E. G. (1994). Effects of pH on the survival of marine phytoplankton: Implications for species growth and carbon uptake of marine phytoplankton. succession. Aquatic Microbial Ecology, 28, 279–288. doi:10. Marine Ecology Progress Series, 109, 83–94. doi:10.3354/ meps109083 3354/ame028279 Chibuike, G. U., & Obiora, S. C. (2014). Heavy metal polluted He, J., & Chen, J. P. (2014). A comprehensive review on soils: effect on plants and bioremediation methods. Applied biosorption of heavy metals by algal biomass: Materials, and Environmental Soil Science, 1–12. doi:https://doi.org/ performances, chemistry, and modeling simulation tools. 10.1155/2014/752708 Bioresource Technology, 160, 67–78. doi:10.1016/j.biortech. Cobbett, C. (2002). Phytochelatins and their roles in heavy 2014.01.068 metal detoxification. Plant Physiology, 123, 825–832. Hedayatkhah, A., Cretoiu, M. S., Emtiazi, G., Stal, L. J., doi:10.1104/pp.123.3.825 Bolhuis, H., Hedayatkhah, A. . . . Bolhuis, H. (2018). APPLIED PHYCOLOGY 31 Bioremediation of chromium contaminated water by dia- Li, L., Zhang, K., Gill, R. A., Islam, F., Farooq, M. A., Wang, J., & Zhou, W. (2018). Ecotoxicological and Interactive Effects toms with concomitant lipid accumulation for biofuel of Copper and Chromium on Physiochemical, production. Journal of Environmental Management, 227, Ultrastructural, and Molecular Profiling in Brassica napus 313–320. doi:10.1016/j.jenvman.2018.09.011 Holan, Z. R., & Volesky, B. (2014). Biosorption of heavy L. BioMed research international. doi:10.1155/2018/ metals: Review. Journal of Chemical Science and 9248123 Technology, 3, 74–102. Luo, H., Wang, Q., Liu, Z., Wang, S., Long, A., & Yang, Y. Howe, G., & Merchant, S. (1992). Heavy metal-activated (2020). Potential bioremediation effects of seaweed Gracilaria lemaneiformis on heavy metals in coastal sedi- synthesis of peptides in Chlamydomonas reinhardtii. Plant ment from a typical mariculture zone. Chemosphere, 245, Physiology, 98, 127–136. doi:10.1104/pp.98.1.127 125636. doi:10.1016/j.chemosphere.2019.125636 Islam, M. S., Ahmed, M. K., Raknuzzaman, M., Habibullah - Ma, J., Zhou, B., Chen, F., & Pan, K. (2021). How marine Al- Mamun, M., & Islam, M. K. (2015). Heavy metal pollu- diatoms cope with metal challenge: Insights from the tion in surface water and sediment: A preliminary assess- morphotype-dependent metal tolerance in Phaeodactylum ment of an urban river in a developing country. Ecological tricornutum. Ecotoxicology and Environmental Safety, 208, Indicators, 48, 282–291. doi:10.1016/j.ecolind.2014.08.016 111715. doi:10.1016/j.ecoenv.2020.111715 Kawakami, S. K., Gledhill, M., & Achterberg, E. P. (2006a). Mehta, S. K., & Gaur, J. P. (2005). Use of algae for removing Effects of metal combinations on the production of phyto- heavy metal ions from wastewater: Progress and prospects. chelatins and glutathione by the marine diatom Critical Reviews in Biotechnology, 25, 113–152. doi:10.1080/ Phaeodactylum tricornutum. BioMetals, 19, 51–60. doi:10. 1007/s10534-005-5115-6 Moheimani, N. R. (2013). Inorganic carbon and pH effect on Kawakami, S. K., Gledhill, M., & Achterberg, E. P. (2006b). growth and lipid productivity of tetraselmis suecica and Production of phytochelatins and glutathione by marine Chlorella sp (chlorophyta) grown outdoors in bag phytoplankton in response to metal stress. Journal of photobioreactors. Journal of Applied Phycology, 25, Phycology, 42, 975–989. doi:10.1111/j.1529-8817.2006. 387–398. doi:10.1007/s10811-012-9873-6 00265.x Nagalakshmi, N., & Prasad, M. N. V. (2001). Responses of Khalil, Z. I., Asker, M. M. S., El-Sayed, S., & Kobbia, I. A. glutathione cycle enzymes and glutathione metabolism to (2010). Effect of pH on growth and biochemical responses copper stress in Scenedesmus bijugatus. Plant Science, 160, of Dunaliella bardawil and Chlorella ellipsoidea. World 291–299. doi:10.1016/S0168-9452(00)00392-7 Journal of Microbiology & Biotechnology, 26, 1225–1231. Navarrete, A., González, A., Gómez, M., Contreras, R. A., doi:10.1007/s11274-009-0292-z Díaz, P., Lobos, G. . . . Moenne, A. (2019). Copper excess Kneer, R., & Zenk, M. H. (1997). The formation of detoxification is mediated by a coordinated and comple- cd-phytochelatin complexes in plant cell cultures. mentary induction of glutathione, phytochelatins and Phytochemistry, 44, 69–74. doi:10.1016/S0031-9422(96) metallothioneins in the green seaweed Ulva compressa. 00514-6 Plant Physiology and Biochemistry, 135, 423–431. doi:10. Laglera, L. M., & Van Den Berg, C. M. G. (2003). Copper 1016/j.plaphy.2018.11.019 complexation by thiol compounds in estuarine waters. Naveed, S., Li, C., Lu, X., Chen, S., Yin, B., Zhang, C., & Ge, Y. Marine Chemistry, 82, 71–89. doi:10.1016/S0304-4203(03) (2019). Microalgal extracellular polymeric substances and 00053-7 their interactions with metal(loid)s: A review. Critical Lambert, A. S., Dabrin, A., Morin, S., Gahou, J., Foulquier, A., Reviews in Environmental Science and Technology, 49, Coquery, M., & Pesce, S. (2016). Temperature modulates 1769–1802. doi:10.1080/10643389.2019.1583052 phototrophic periphyton response to chronic copper Neumann, P. M., De Souza, M. P., Pickering, I. J., & Terry, N. exposure. Environmental Pollution, 208, 821–829. doi:10. (2003). Rapid microalgal metabolism of selenate to volatile 1016/j.envpol.2015.11.004 dimethylselenide. Plant, Cell & Environment, 26, 897–905. Lata, S., Singh, P. K., & Samadder, S. R. (2015). Regeneration doi:10.1046/j.1365-3040.2003.01022.x of adsorbents and recovery of heavy metals: A review. Noctor, G., Strohm, M., Jouanin, L., Kunert, K., Foyer, C. H., International Journal of Environmental Science and & Rennenberg, H. (1995). Synthesis of glutathione in leaves Technology, 12, 1461–1478. doi:10.1007/s13762-014-0714-9 of transgenic poplar overexpressing y-glutamylcysteine Lavoie, M., Le Faucheur, S., Fortin, C., & Campbell, P. G. C. synthetase. Plant Physiology, 112, 1071–1078. doi:10.1104/ (2009). Cadmium detoxification strategies in two phyto- pp.112.3.1071 plankton species: Metal binding by newly synthesized thio- Onyancha, F., Lubbe, D., & Brink, H. G. (2021). Enhancing lated peptides and metal sequestration in granules. Aquatic low-carbon wastewaters with flue gas for the optimal culti- Toxicology, 92, 65–75. doi:10.1016/j.aquatox.2008.12.007 vation of Desmodesmus multivariabilis. Chemical Libatique, M. J. H., Lee, M. –. C., & Yeh, H. –. Y. (2019). Effect Engineering Transactions, 86, 355–360. doi:10.3303/ of light intensity on the mechanism of inorganic arsenic CET2186060 accumulation and patterns in the red macroalga, Sarcodia Oukarroum, A. (2016). Alleviation of Metal-Induced Toxicity suiae. Biological Trace Element Research, 195, 291–300. in Aquatic Plants by Exogenous Compounds: A doi:10.1007/s12011-019-01833-0 Mini-Review. Water, Air, & Soil Pollution, 227. doi:10. Lin, Z., Li, J., Luan, Y., & Dai, W. (2020). Application of algae 1007/s11270-016-2907-y for heavy metal adsorption: A 20-year meta-analysis. Ozturk, S., Aslim, B., & Suludere, Z. (2010). Cadmium(ii) Ecotoxicology and Environmental Safety, 190, 110089. sequestration characteristics by two isolates of doi:10.1016/j.ecoenv.2019.110089 Synechocystis sp. in terms of exopolysaccharide (EPS) 32 S. K. READ ET AL. production and monomer composition. Bioresource Pistocchi, R., Mormile, M. A., Guerrini, F., Isani, G., & Technology, 101, 9742–9748. doi:10.1016/j.biortech.2010. Boni, L. (2000). Increased production of extra- and intra- 07.105 cellular metal-ligands in phytoplankton exposed to copper Ozturk, S., Aslim, B., Suludere, Z., & Tan, S. (2014). Metal and cadmium. Journal of Applied Phycology, 12, 469–477. removal of cyanobacterial exopolysaccharides by uronic doi:10.1023/A:1008162812651 acid content and monosaccharide composition. Priyadarshanee, M., & Das, S. (2021). Biosorption and removal Carbohydrate Polymers, 101, 265–271. doi:10.1016/j.carb of toxic heavy metals by metal tolerating bacteria for bior- pol.2013.09.040 emediation of metal contamination: A comprehensive Patterson, J. W. (1985). Industrial wastewater treatment tech- review. Journal of Environmental Chemical Engineering, 9, nology (Second edition (2nd ed.). Stoneham, USA: 104686. doi:10.1016/j.jece.2020.104686 Butterorth Publisher. Qiu, R., Gao, S., Lopez, P. A., & Ogden, K. L. (2017). Effects of Pawlik-Skowron, B. (2001). Phytochelatin production in pH on cell growth, lipid production and CO addition of freshwater algae Stigeoclonium in response to heavy metals microalgae Chlorella sorokiniana. Algal Research, 28, contained in mining water; effects of some environmental 192–199. doi:10.1016/j.algal.2017.11.004 factors. Aquatic Toxicology, 52, 241–249. doi:10.1016/ Rajfur, M. (2013). Algae - heavy metals biosorbent. Ecological S0166-445X(00)00144-2 Chemistry and Engineering, 20, 23–40. doi:10.2478/eces- Pawlik-Skowrońska, B. (2003). When adapted to high zinc 2013-0002 concentrations the periphytic green alga Stigeoclonium Rezayian, M., Niknam, V., & Ebrahimzadeh, H. (2019). tenue produces high amounts of novel Oxidative damage and antioxidative system in algae. phytochelatin-related peptides. Aquatic Toxicology, 62, Toxicology Reports, 6, 1309–1313. doi:10.1016/j.toxrep. 155–163. doi:10.1016/S0166-445X(02)00080-2 2019.10.001 Pawlik-Skowrońska, B., & Bačkor, M. (2011). Zn/pb-tolerant Ribeiro, C., Couto, C., Ribeiro, A. R., Maia, A. S., Santos, M., lichens with higher content of secondary metabolites pro- Tiritan, M. E. . . . Almeida, A. A. (2018). Distribution and duce less phytochelatins than specimens living in unpol- environmental assessment of trace elements contamination luted habitats. Environmental and Experimental Botany, 72, of water, sediments and flora from Douro River estuary, 64–70. doi:10.1016/j.envexpbot.2010.07.002 Portugal. The Science of the Total Environment, 639, Peckol, P., DeMeo-Anderson, D., River, J., Valiela, I., 1381–1393. doi:10.1016/j.scitotenv.2018.05.234 Maldonado, M., & Yates, J. (1994). Growth, nutrient uptake Romano, R. L., Liria, C. W., Machini, M. T., Colepicolo, P., & capacities and tissue constituents of the macroalgae Zambotti-Villela, L. (2017). Cadmium decreases the levels Cladophora vagabunda and Gracilaria tikvahiae related to of glutathione and enhances the phytochelatin concentra- site-specific nitrogen loading rates. Marine Biology, 121, tion in the marine dinoflagellate Lingulodinium polyedrum. 175–185. doi:10.1007/BF00349487 Journal of Applied Phycology, 29, 811–820. doi:10.1007/ Perales-Vela, H. V., Peña-Castro, J. M., & Cañizares- s10811-016-0927-z Villanueva, R. O. (2006). Heavy metal detoxification in Rüegsegger, A., & Brunold, C. (1992). Effect of cadmium on γ- eukaryotic microalgae. Chemosphere, 64, 1–10. doi:10. glutamylcysteine synthesis in maize seedlings. Plant 1016/j.chemosphere.2005.11.024 Physiology, 99, 428–433. doi:10.1104/pp.99.2.428 Pérez-Rama, M., Torres Vaamonde, E., & Abalde Alonso, J. Sánchez-Thomas, R., García-García, J. D., Marín-Hernández, Á., (2006). Composition and production of thiol constituents Pardo, J. P., Rodríguez-Enríquez, S., Vera-Estrella, R. . . . induced by cadmium in the marine microalga Tetraselmis Moreno-Sánchez, R. (2020). The intracellular water volume suecica. Environmental Toxicology and Chemistry, 25, modulates the accumulation of cadmium in Euglena gracilis. 128–136. doi:10.1897/05-252R.1 Algal Research, 46, 101774. doi:10.1016/j.algal.2019.101774 Pesce, S., Ghiglione, J. F., & Martin-Laurent, F. (2017). Schäfer, H. J., Haag-Kerwer, A., & Rausch, T. (1998). cDNA Microbial Communities as Ecological Indicators of cloning and expression analysis of genes encoding GSH Ecosystem Recovery Following Chemical Pollution. In C. synthesis in roots of the heavy-metal accumulator Cravo-Laureau, C. Cagnon, B. Lauga, & R. Duran (Eds.), Brassica juncea L.: Evidence for Cd-induction of Microbial Ecotoxicology Cham: Springer. doi:10.1007/978- a putative mitochondrial γ-glutamylcysteine synthetase iso- 3-319-61795-4_10 form. Plant Molecular Biology, 37, 87–97. doi:10.1023/ Piña-Olavide, R., Paz-Maldonado, L. M. T., Alfaro-De La A:1005929022061 Torre, M. C., García-Soto, M. J., Ramírez-Rodríguez, Sinaei, M., Loghmani, M., & Bolouki, M. (2018). Application A. E., Rosales-Mendoza, S. , and García De la-Cruz, R. F. of biomarkers in brown algae (Cystoseria indica) to assess (2020). Increased removal of cadmium by Chlamydomonas heavy metals (Cd, Cu, Zn, Pb, Hg, Ni, Cr) pollution in the reinhardtii modified with a synthetic gene for γ- northern coasts of the Gulf of Oman. Ecotoxicology and glutamylcysteine synthetase. International Journal of Environmental Safety, 164, 675–680. doi:10.1016/j.ecoenv. Phytoremediation, 22, 1269–1277. doi:10.1080/15226514. 2018.08.074 2020.1765138 Singh, S. P., & Schwan, A. L. (2019). Sulfur metabolism in Pinto, E., Carvalho, A. P., Cardozo, K. H. M., Malcata, F. X., plants and related biotechnologies. In Comprehensive dos Anjos, F. M., & Colepicolo, P. (2011). Effects of heavy Biotechnology (Vol. 4, Third Edit ed.). Elsevier. doi:10. metals and light levels on the biosynthesis of carotenoids 1016/B978-0-444-64046-8.00225-1 and fatty acids in the macroalgae Gracilaria tenuistipitata Skowroński, T., De Knecht, J. A., Simons, J., & Verkleij, J. A. C. (var. liui Zhang & Xia). Brazilian Journal of (1998). Phytochelatin synthesis in response to cadmium Pharmacognosy, 21, 349–354. doi:10.1590/S0102- uptake in Vaucheria (xanthophyceae). European Journal of 695X2011005000060 Phycology, 33, 87–91. doi:10.1080/09670269810001736573 APPLIED PHYCOLOGY 33 Soldo, D., & Behra, R. (2000). Long-term effects of copper on the Wahal, S., & Viamajala, S. (2010). Maximizing algal growth in structure of freshwater periphyton communities and their batch reactors using sequential change in light intensity. tolerance to copper, zinc, nickel and silver. Aquatic Applied Biochemistry and Biotechnology, 161, 511–522. Toxicology, 47, 181–189. doi:10.1016/S0166-445X(99)00020-X doi:10.1007/s12010-009-8891-6 Stevens, A. E., Mccarthy, B. C., & Vis, M. L. (2001). Metal Wang, M. J., & Wang, W. X. (2008). Temperature-dependent content of Klebsormidium-dominated (chlorophyta) algal sensitivity of a marine diatom to cadmium stress explained mats from acid mine drainage waters in Southeastern Ohio. by subcelluar distribution and thiol synthesis. Journal of the Torrey Botanical Society, 128, 226–233. Environmental Science & Technology, 42, 8603–8608. doi:10.2307/3088714 doi:10.1021/es801470w Sud, D., Mahajan, G., & Kaur, M. P. (2008). Agricultural waste Wang, M. J., & Wang, W. X. (2011). Cadmium sensitivity, material as potential adsorbent for sequestering heavy metal uptake, subcellular distribution and thiol induction in ions from aqueous solutions - a review. Bioresource a marine diatom: Recovery from cadmium exposure. Technology, 99, 6017–6027. doi:10.1016/j.biortech.2007.11.064 Aquatic Toxicology, 101, 387–395. doi:10.1016/j.aquatox. Taboada-de la Calzada, A., Villa-Lojo, M. C., Beceiro- 2010.11.012 González, E., Alonso-Rodrı́guez, E., & Prada-Rodrı́guez, Wood, J. M. (1985). Effects of Acidification on the Mobility of D. (1998). Determination of arsenic species in environmen- Metals and Metalloids : An Overview. Environmental tal samples : Use of the alga Chlorella vulgaris for Arsenic Health Perspective, 63, 115–119. (III) retention. Trends in Analytical Chemistry, 17, Zbikowski, R., Szefer, P., & Latała, A. (2007). Comparison of 167–175. doi:10.1016/S0165-9936(98)00002-8 green algae Cladophora sp. and Enteromorpha sp. as poten- Torricelli, E., Gorbi, G., Pawlik-Skowronska, B., Di tial biomonitors of chemical elements in the southern Toppi, L. S., & Corradi, M. G. (2004). Cadmium tolerance, Baltic. The Science of the Total Environment, 387, cysteine and thiol peptide levels in wild type and 320–332. doi:10.1016/j.scitotenv.2007.07.017 chromium-tolerant strains of Scenedesmus acutus Zeng, J., Yang, L., & Wang, W. X. (2009). Acclimation to and (chlorophyceae). Aquatic Toxicology, 68, 315–323. doi:10. recovery from cadmium and zinc exposure by a freshwater 1016/j.aquatox.2004.03.020 cyanobacterium, Microcystis aeruginosa. Aquatic Tüzün, I., Bayramoǧlu, G., Yalçin, E., Başaran, G., Çelik, G., & Toxicology, 93, 1–10. doi:10.1016/j.aquatox.2009.02.013 Zeraatkar, A. K., Ahmadzadeh, H., Talebi, A. F., Arica, M. Y. (2005). Equilibrium and kinetic studies on biosorption of Hg(II), Cd(II) and Pb(II) ions onto micro- Moheimani, N. R., & McHenry, M. P. (2016). Potential algae Chlamydomonas reinhardtii. Journal of Environmental use of algae for heavy metal bioremediation, a critical Management, 77, 85–92. doi:10.1016/j.jenvman.2005.01.028 review. Journal of Environmental Management, 181, Volland, S., Schaumlöffel, D., Dobritzsch, D., Krauss, G., & 817–831. doi:10.1016/j.jenvman.2016.06.059 Lütz-Meindl, U. (2013). Chemosphere identification of Zucchi, M. R., & Necchi, O. J. (2001). Effects of temperature, irradiance and photoperiod on growth and pigment content phytochelatins in the cadmium-stressed conjugating green alga Micrasterias denticulata. Chemosphere, 91, 448–454. in some freshwater red algae in culture. Phycological Research, doi:10.1016/j.chemosphere.2012.11.064 49, 103–114. doi:10.1111/j.1440-1835.2001.tb00240.x
Journal
Applied Phycology
– Taylor & Francis
Published: Dec 31, 2023
Keywords: Algae; bioaccumulation; biosorption; glutathione; heavy metals; phytochelatins; potentially toxic elements; wastewater treatment
