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Article history: Algae have several industrial applications that can lower the cost of biofuel co-production. Among these
Received 25 April 2016 co-production applications, environmental and wastewater bioremediation are increasingly important.
Received in revised form Heavy metal pollution and its implications for public health and the environment have led to increased
11 June 2016
interest in developing environmental biotechnology approaches. We review the potential for algal bio-
Accepted 26 June 2016
Available online xxx
sorption and/or neutralization of the toxic effects of heavy metal ions, primarily focusing on their cellular
structure, pretreatment, modification, as well as potential application of genetic engineering in bio-
sorption performance. We evaluate pretreatment, immobilization, and factors affecting biosorption ca-
Keywords:
Algae biomass
pacity, such as initial metal ion concentration, biomass concentration, initial pH, time, temperature, and
Biosorption capacity interference of multi metal ions and introduce molecular tools to develop engineered algal strains with
Heavy metals higher biosorption capacity and selectivity. We conclude that consideration of these parameters can lead
Bioremediation to the development of low-cost micro and macroalgae cultivation with high bioremediation potential.
Biofuel © 2016 Elsevier Ltd. All rights reserved.
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2. Industrial wastewater . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3. Bioremediation of heavy metal ions using algae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.1. The main factors influencing heavy metal ion biosorption . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.2. The influence of initial metal ion concentration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.3. The influence of pH on sorption selectivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.4. The influence of biomass concentration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.5. The influence of temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.6. The influence of contact time . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.7. The influence of multi metal ion systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.8. The influence of other factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4. Metal ion sorption by pretreated algae biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5. Macro vs micro algae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
6. Living vs non-living algae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
7. Immobilized algae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
8. Metal ion biosorption enhancement using molecular tools . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
9. Coupling wastewater treatment and biofuel production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
10. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
* Corresponding author.
E-mail address: h.ahmadzadeh@um.ac.ir (H. Ahmadzadeh).
http://dx.doi.org/10.1016/j.jenvman.2016.06.059
0301-4797/© 2016 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Zeraatkar, A.K., et al., Potential use of algae for heavy metal bioremediation, a critical review, Journal of
Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.06.059
2 A.K. Zeraatkar et al. / Journal of Environmental Management xxx (2016) 1e15
Please cite this article in press as: Zeraatkar, A.K., et al., Potential use of algae for heavy metal bioremediation, a critical review, Journal of
Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.06.059
A.K. Zeraatkar et al. / Journal of Environmental Management xxx (2016) 1e15 3
heavy metal ions often poison the living cells. Moreover, the negative, which is related to the deprotonation of carboxyl and
sorption process shows large variations based on the growth phase phosphate groups on the cell surface (Mehta and Gaur, 2005).
of algae. More specifically, living algae are affected by several Fig. 1 shows a schematic representation of the binding sites on
environmental factors which directly influence the metal ion bio- the algal cell wall. Metal ions adsorbed by the algal cell wall acts as
sorption capacity. Absorption mechanisms in living algae are more the first step in bioaccumulation. Different binding groups, such as
complex than non-living algae since absorption takes place during OH, SH, COO, PO3
4 , NO3 , RNH2 , RS and RO promote the
the growth phase and intracellular uptake of heavy metal ions metal ion adsorption. These binding groups are present at the cell
usually occur in this phase. In contrast, non-living algae cells absorb surface, in the cytoplasm, and especially vacuoles. If the mechanism
metal ions biosorption on the surface of the cell membrane and it is of metal ion bioremediation is the uptake of ions by algal cells,
_
considered an extracellular process (Godlewska-Zyłkiewicz, 2001). cytosolic proteins mediate the transfer of metal ions into the cells
Non-living algal biomass can be regarded as an assemblage of (Perales-Vela et al., 2006). Consequently, the vacuoles could be
polymers (such as sugars, cellulose, pectins, glycoproteins, etc.) that regarded as an organelle that accumulates metal ions. Table 2
are capable of binding to heavy metal cations as adsorbents with presents a summary of the affinity between different metal ions
the potential of cost-effective wastewater treatment (Volesky, and the cellular ligands, with R showing alkyl groups such as pro-
2007; Arief et al., 2008). pyl, CH3eCH2CH2, and metal ions classified into classes A, B, and
The toxic level of heavy metal ions in variant algal species can be borderline. Class A tends to establish links with ligands in Group I
highly strain specific, which consequently determines the potential through their oxygen atoms. Metal cations belong to class B tend to
remediation capacity using a specific algal strain. In other words, a bridge with ligands in Groups II and III, and the borderline metal
heavy metal ion may exhibit a selective interaction with one spe- ions can be linked with different atoms of Groups I, II, and III
cific algal strain, in addition to differences between similar species. (Volesky, 2007). Although metal-ligand complex formation is well
For example, Monteiro et al. (Monteiro et al., 2010). investigated classified into different Groups and Classes, but from the chemistry
cadmium ion removal using two strains of Desmodesmus plei- perspective it would have been more beneficial to include the
omorphus cells, and found a 25% difference between the capacity of complex formation constants between the metal ions and the
cadmium biosorption using ‘L’ and ‘ACOI 561’ strains. In terms of different ligands at the cell surface. This will enable the researchers
species differences, Romera et al. (Romera et al., 2007). found the decide on preferential metal ion biosorption and the effects of
following macroalgal species possess differing copper sorption interfering ions. According to the pKa of functional groups listed in
capacity: Fucus spiralis > Ascophyllum nodosum > Chondrus Table 3, carboxyl groups, sulfonate, phosphate, and phosphodiester
crispus > Asparagopsis armata > Spirogyra insignis > Codium ver- have the largest contribution in sorption capacity. Due to the
milara. The physicochemical conditions affecting the maximum relative abundance of each of these functional groups in different
capacity of metal ion removal for different micro and macro algae algal strains, each will exhibit a different capacity for metal ion
strains are summarized in Table 1. This table shows that most metal biosorption.
ion uptake occurs at a low pH (3e5), and that dried algal biomass Algae cell walls are the first barrier against the biosorption of
exhibits a greater metal ion biosorption capacity compared to live heavy metal ions. Polysaccharides and proteins present in algae cell
algae. The solution pH has a significant influence on dissociation of walls have the most metal binding sites (Schiewer and
the surface functional groups of non-living algal biomass and on VoleskyValdes, 2000). Due to the different distribution and abun-
the solution chemistry of heavy metal ions (Pavasant et al., 2006; dance of cell wall compositions in different algal strains, the ca-
Guo et al., 2008). The impact of pH on metal uptake can be influ- pacity of metal ions biosorption by the variant algal strains will
enced by the surface functional groups on the biomass’ cell walls, vary. Romera et al. (Romera et al., 2006). introduced brown algae as
and the solution metal chemistry (Sheng et al., 2004). Table 1 also a very good candidate for biosorbents of heavy metal ions based on
reports the optimal time for heavy metal ion sorption. Accordingly, the comparison of different algal strains and biomass-metal ion
biosorption capacity could usually reach to the acceptable level affinity. Brown algae, with alginate in their cell wall composition
during the first 120 min. has a high affinity for biosorption of lead ions (Romera et al., 2007).
Heavy metal ion accumulation by microorganisms generally Alginate polymers constitute the primary means of sorption of
occurs in two phases (Monteiro et al., 2011a, 2012). The first phase heavy metal ions in brown algae, and their biosorption capacity is
occurs on the cell surface and consists of fast inactive biosorption, directly related to the presence of binding sites on this polymer
which is completely independent of cellular metabolism. The sec- (Romera et al., 2006; Davis et al., 2003).
ond phase consists of active sorption of heavy metal ions into the
cytoplasm of algal cells. This phase is dependent on cell metabolism 3.1. The main factors influencing heavy metal ion biosorption
and is known as intracellular ion uptake (TalebiTabatabaei et al.,
2013). Intracellular ion uptake has a large contribution in heavy Biosorption of heavy metal ions by algae may be affected by
metal ions biosorption and detoxification (Wilde et al., 2006; several factors, including concentration of metal ions and algae
Perales-Vela et al., 2006). biomass, pH, temperature, and the presence of competing ions. This
Heavy metal ion biosorption capacity has been attributed to the section aims to review these factors and their possible effects on
presence of different types of binding groups on the algal cell sur- the metal ions biosorption.
face i.e. hydroxyl, phosphoryl, carboxyl, sulphuryl, amine, imid-
azole, sulfate, phosphate, carbohydrate, etc. (KaplanRichmond and 3.2. The influence of initial metal ion concentration
Hu, 2013). The availability of active sites for heavy metal ion uptake
in algal cells can be probed by FTIR spectroscopy (Gupta and Heavy metal ion removal by algal biomass depends largely on
Rastogi, 2008a). The sorption capacity of an algae cell surface to a the initial concentration of metal ions in the solution phase. Bio-
specific ion also depends on factors such as the number of func- sorption initially increases as the initial concentration of metal ion
tional groups in the algae cells, the coordination number of the increases. In following, no more considerable increase in metal
metal ion to be sorbed, the accessibility of binding groups for metal sorption is observed by a tandem increase of metal ions concen-
ions, the complex formation constants of metal ion with the func- tration (Singh et al., 2010). This phenomenon could be used to in-
tional group, and the chemical state of these sites. Usually the crease biosorption capacity. For example, Monteiro et al. (Monteiro
presence of binding groups make the net charge of the cell surface et al., 2011b). reported a 5-fold increase in initial concentrations of
Please cite this article in press as: Zeraatkar, A.K., et al., Potential use of algae for heavy metal bioremediation, a critical review, Journal of
Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.06.059
4 A.K. Zeraatkar et al. / Journal of Environmental Management xxx (2016) 1e15
Table 1
Biosorption capacity of 14 different heavy metal ions using variant micro and macroalgal strains under optimal conditions. (The potential of macroalgal vs. microalgal strains
and living vs. non-living cells are summarized).
Metal Algae species Treatment Max. sorption Optimal Initial metal conc. Biomass conc. Temp Time References
(mg g1) pH (mg L1) (g L1) (C ) (hour)
Please cite this article in press as: Zeraatkar, A.K., et al., Potential use of algae for heavy metal bioremediation, a critical review, Journal of
Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.06.059
A.K. Zeraatkar et al. / Journal of Environmental Management xxx (2016) 1e15 5
Table 1 (continued )
Metal Algae species Treatment Max. sorption Optimal Initial metal conc. Biomass conc. Temp Time References
(mg g1) pH (mg L1) (g L1) (C ) (hour)
Zn (II) (from 10 to 50 ppm) boosted the metal ion sorption from 19 yield of the metal ions. In other words, the higher the metal ion
to 209.6 mg Zn (II)/g dry biomass of Scenedesmus obliqus. This leads concentrations the lower the efficiency and removal yield would be
to an increased biosorption capacity and a reduction in the removal (Malkoc and Nuhoglu, 2003). At low metal ion concentrations
Please cite this article in press as: Zeraatkar, A.K., et al., Potential use of algae for heavy metal bioremediation, a critical review, Journal of
Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.06.059
6 A.K. Zeraatkar et al. / Journal of Environmental Management xxx (2016) 1e15
Table 2
Functional groups in biological systems and three types of metals.
Table 3
Important functional groups involved in metal ion biosorption.
Binding group Structural formula pKa Ligand atom Occurrence in selected biomolecules
PS ¼ polysaccharides; UA ¼ uronic acids; SPS ¼ sulfated PS; Cto ¼ chitosan; PG ¼ peptidoglycan; AA ¼ amino acids; TA ¼ teichoic acid; PL ¼ phospholipids; LPS ¼ lipoPS.
(Adapted from (Volesky, (2007), with permission).
removal takes place more efficiently than higher concentrations. to continue in the presence of toxic/lethal concentrations of heavy
For example, Mehta and Gaur (Mehta and Gaur, 2001a) reported metal ions (Monteiro et al., 2012). However, the presence of
that Chlorella vulgaris biomass is able to remove 69% and 80% of Ni excessive toxicity of heavy metal ions could lead to protein struc-
(II) and Cu (II) cations in concentrations of 2.5 ppm, respectively. ture denaturation, replacing essential elements or damage to the
While increase in the initial concentration of Ni (II) and Cu (II) to oxidative balance of the live algae. Intensity of the stress on algal
10 ppm, the metal removal rate was reduced only to 37 and 42%, cells depends on the content of oxidized proteins and lipids in the
respectively. This clearly shows that the increase in metal ion algae cells. The protection response of algae cells against heavy
concentration from 2.5 to 10 ppm reduced the bioremoval rates by metal ions is extremely dependent on their resistance to the
about half. Due to the toxicity of some heavy metal ions for live oxidative damages (TalebiTabatabaei et al., 2013; Arunakumara and
algal strains metal ions uptake will be reduced by destruction of Zhang, 2008).
algal cells, and an optimization of metal ion concentrations is
necessary for the efficient growth of algae. Shanab and Essa 3.3. The influence of pH on sorption selectivity
(Shanab and Essa, 2007) investigated the effects of concentrations
of mercury, cadmium, and lead ions on the growth of Scenedesmus pH is one of the most important determining parameters of the
quadricauda. They observed that low concentrations of lead and capacity of metal ion uptake by algal biomass (Mata et al., 2009a;
cadmium ions (5e20 ppm) enhanced algae growth through Mehta et al., 2002a; Han et al., 2006; Gupta et al., 2001; Zeroual
increased chlorophyll content, while mercury ions had a toxic effect et al., 2003; Rangsayatorn et al., 2002). Dependence of metal ion
on the algal cells in any concentration. Lamaia et al. (Lamaia et al., uptake on pH is related to the metal ion complexation chemistry in
2005). continually increased the exposure time and concentrations solution, and behavior of many different functional groups present
of lead and cadmium ions to explore the toxicity in a common in the surface of algal cells as well as to complex formation con-
filamentous live green algae, Cladophora fracta. The main toxicity stants (Gupta and Rastogi, 2008a; Han et al., 2006; Sheng et al.,
Please cite this article in press as: Zeraatkar, A.K., et al., Potential use of algae for heavy metal bioremediation, a critical review, Journal of
Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.06.059
A.K. Zeraatkar et al. / Journal of Environmental Management xxx (2016) 1e15 7
2007). Han et al. (Han et al., 2006). investigated the Cr (III) uptake buffer to adjust the pH may result in the formation of phosphate
by Chlorella miniata biomass and found that biosorption capacity in precipitate.
pH 3, 4 and 4.5, was 14.17, 28.72 and 41.12 mg Cr (III)/g dried algae,
respectively. Similar research by Gupta and Rastogi (Gupta and 3.4. The influence of biomass concentration
Rastogi, 2008b) on the uptake of Pb (II) by Spirogyra sp. biomass
showed that biosorption of Pb (II) at the pH < 3, is very low. When The amount of metal ions removed from a solution phase is
the pH increased in the range of 3e5, an increase in lead ions dependent on the algae biomass concentration, and increasing
sorption was observed, with the maximum amount of sorbed ions biomass concentrations reduces metal ion uptake per gram of
being 140 mg/g at pH 5. Considering lead (II) hydroxide solubility biomass (Mehta and Gaur, 2001a; Gokhale et al., 2008; Singleton
product (KSP) to be 1.4 1020, and assuming 1.4 mM lead ion and Simmons, 1996; Finocchio et al., 2010). In practical terms,
concentration, the hydroxide ions from Ksp calculations would be increased biomass concentrations positively increases final bio-
KSP ¼ 1.4 1020 ¼ (1 106) (OH)2, or hydroxyl ion concentra- removal, although it negatively affects biosorption capacity of
tion of 107 M and pH ¼ 7. This implies that even at a micromolar heavy metal ions (Mehta and Gaur, 2001b). Electrostatic in-
concentration of lead ions, at pH 7 or higher, the lead(II) ions will teractions between cells have a significant effect on metal ion up-
precipitate as lead(II) hydroxide before biosorption by algae cells. In take by algal biomass, with high biomass concentrations having a
the case of biosorption using living algal cells, it can be inferred that ‘shell effect’ on the outer structure of biomass and avoiding func-
during photosynthesis the inorganic carbon content of the culture tional group binding to metal ions (Romera et al., 2007; Fraile et al.,
medium was depleted, and consequently the pH increased. 2005). The shell effect enables the control of complex formation by
Concurrently, the biosorption of some metal ions such as Pb (II) adjusting pH to the isoelectric point. Mehta and Gaur (Mehta and
might increase. Thus, injection of CO2 can be used to control the Gaur, 2001b) found out that a 100-fold increase in biomass con-
acidity of the culture medium (Raeesossadati et al., 2014, 2015). centration of C. vulgaris is accompanied by a significant increase in
The absence of Hþ ions increases the ability of establishing links removal of Ni (II) and Cu (II). In a similar study on Scenedesmus
between metal cations and ligands, leading to improved metal ion abundans by Terry and Stone (Terry and Stone, 2002), competition
removal by algal biomass. Conversely, functional groups in acidic between Cu (II) and Cd (II) for binding sites was observed, and
solutions are protonated and prevented from binding cations to higher concentrations of biomass prevented such competition.
functional groups (Han et al., 2006; Gupta and Rastogi, 2008b), There is also a variable effect of biomass concentrations on the
resulting in a reduction of biosorption capacity. Therefore, finding metal ion biosorption capacity This was investigated by Romera
the optimal pH for maximum metal ion removal by specific algae is et al. (Romera et al., 2007). using different algal strains and metal
paramount, as it strongly correlates with the biomass surface ions, and was reported that maximum biosorption efficiency could
charge, degree of ionization, and absorbing sites. be obtained at the lowest biomass concentration.
The first step in the mechanism of biosorption and bio-
accumulation of heavy metal ions is the diffusion of ions to the 3.5. The influence of temperature
algae cell surface which is negatively charged from ionization of
functional groups. The negatively charge surface will adsorb the Biosorption efficiency of each metal ion is different for each
counterions, ie heavy metal ions in this case, to have a double layer algae species with different response to the temperature (Monteiro
originated from the cell surface. The sorption of the metal ions et al., 2010; Gupta et al., 2010). Although metal ligand complex
causes the depletion of ions in media (growth media for live algae) formation constants are primarily a function of temperature, some
and this depletion lowers the ionic strength of the media that previously published studies claimed that increased algal culture
causes the expansion of double layer thickness. Therefore, the temperatures could potentially increase metal ion biosorption ca-
biosorption of heavy metal ions is more efficient in dilute media pacity (Gupta and Rastogi, 2008b; Deng et al., 2006; Deng et al.,
(Ahmadzadeh et al., 2007). 2007; Khan et al., 2012; Sari and Tuzen, 2009; Saǧ and Kutsal,
The tendency for selective metal ion uptake at an optimized pH 2000), with no consideration of formation constants changes by
is useful in targeted biosorption in multi metal ion solutions. Aksu temperature. The possible reasons for increasing temperatures to
et al. (Aksu et al., 1999). in a study on C. vulgaris biomass, deter- result in increasing metal ion biosorption include: (1) An increased
mined the optimal Cu (II) and Cr (VI) biosorption at pH 4 and 2, number of active sites involved in metal ion uptake; (2) an
respectively. The optimal pH for these metal ions is related to their increased tendency of active sites to absorb metal ions (Mehta and
chemical interaction with the algal cells. In an investigation by Gaur, 2005); (3) a reduction in mass transfer resistance in the
Cimino et al (Cimino et al., 2000). the influence of pH on the dis- diffusion layer by a reduction of the thickness of the diffusion
tribution of Cr(VI) in solution showed that for pH values under 3.0 boundary layer around the adsorbent groups (Meena et al., 2005),
the HCrO 2
4 and Cr2O7 ions species were predominant and effi- and (4) change of complex formation constant with temperature
ciently absorbed on the protonated cell binding sites. At pH values (Bayes et al., 2012; Harris, 2010). However, other studies suggest
over 5.0 the total chromium bioremoval was negligible since that metal ion uptake by some algae is exothermic and uptake
increasing pH shifted HCrO 2
4 to CrO4 . Therefore, increasing pH capacity increases with decreasing temperature (Gupta et al., 2010;
negatively affected the final capacity of chromium bioremoval. Tuzen et al., 2009). There is also observation that indicate tem-
Due to the various chemical forms of metal ions found in IW, pH perature has no significant influence on the metal ion uptake by
adjustment could play an important role in biosorption capacity algal cells (Rangsayatorn et al., 2002; Lodeiro et al., 2006; Martins
(Wilde et al., 2006). Usually NaOH and HCl (Areco et al., 2012), et al., 2004), and similarly several studies have determined
H2SO4 (Uzunog lu et al., 2014), HNO3 (Yaqub et al., 2012), or the temperature-linked changes in metal ion uptake by living algal cells
buffer (Tamilselvan et al., 2012) are used for adjusting pH of IW (Mehta et al., 2000, 2002a). These seemingly incompatible results
solutions. Based on the properties of metal ions, suitable acids, may be resolved by noting that optimum temperatures is usually a
bases, or buffers should be chosen to adjust the pH. For example, in narrow range for active biological reactions in living cells, and
biosorption of lead due to the formation of the PbSO4 precipitates, temperature variations cause different biosorption behaviors in
H2SO4 should not be used. Buffering interferences with metal ions various algal strains with different metal ions. Most importantly is
in the solution is also important and should be considered. For the change of complex formation constant with temperature which
example, Ni (II) and Cd (II) concentrations when using a phosphate is apparently been neglected by most researchers. The biosorption
Please cite this article in press as: Zeraatkar, A.K., et al., Potential use of algae for heavy metal bioremediation, a critical review, Journal of
Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.06.059
8 A.K. Zeraatkar et al. / Journal of Environmental Management xxx (2016) 1e15
capacity of cadmium ions increase with decreasing temperature for point of view is the gradual depletion of nutrients and reduction of
specific algae because of the exothermic nature of cadmium ion the ionic strength of the growth media with time. This will affect
bioremoval (Aksu, 2001; Cruz et al., 2004; Sari and Tuzen, 2008a, the biosorption capacity of heavy metal ions onto the algae cell
2008b). Similarly, research by Aksu (Aksu, 2001, 2002) investi- surface.
gated the effect of temperature on the C. vulgaris biomass for bio-
sorption of Cd (II) and Ni (II). They observed the maximum 3.7. The influence of multi metal ion systems
biosorption for Cd (II) and Ni (II) occurred at 20 and 45 C,
respectively. The type, combinations, and concentrations of heavy metal ions
Temperature also influences biosorption of metals by non-living vary greatly among wastewaters. For example, electrolytic effluent
algal biomass as the adsorption equilibrium is determined by the contain a mixture of metal ions such as Hg, Mn, Ni, Pb, and Cu ions
exothermic or endothermic nature of the process. A number of (Veglio et al., 2003). Bioremoval of multiple metal ions in solution is
studies on the effect of temperature on adsorption isotherms, metal a common situation rather than relatively simple single metal ion
uptake, and also biosorption thermodynamics parameters have solutions. Despite investigation of single metal ion solutions being
been performed (Dundar et al., 2008; Malkoc and Nuhoglu, 2007; routinely surveyed in the research literature, the real situation for
Gupta and Rastogi, 2008c). Due to intracellular absorption and IW treatment is more complicated due to the presence of multiple
enzymes in the transfer of ions into the living algae cell, increasing metal ions that needs further investigations. The presence of
temperature might have a greater impact on the absorption ca- multiple heavy metal ions in the algal growth media imparts major
pacity as compared with non-living algae. Altogether, these factors physiological and biochemical consequences (Bajguz, 2011; El-
will lead to reduced absorption capacity of the living algae more Sheekh et al., 2005). In multi-metal ion systems metal ions
than non-living algae. compete for binding to algal ligands, and the presence of some
cations significantly influence the uptake of other metal ions by
3.6. The influence of contact time algal cells (Bayo, 2012; El-Naas et al., 2007). Aksu and Do €nmez
(Aksu and Do € nmez, 2006) studied the effect of cadmium ions on
Heavy metal ion biosorption is highly dependent on contact the removal of nickel ions and vice versa, and found simultaneous
time. Based on the previously published reports discussing the ki- biosorption of nickel and cadmium ions significantly repressed the
netics of heavy metal ion biosorption on algae cell surface, the total biosorption capacity in comparison to the single ion solutions.
mechanism of biosorption is algae strain specific (Yaqub et al., Table 4 presents heavy metal ion uptake in binary solutions. In
2012; Zhang et al., 2016; Lee et al., 2016). Biosorption takes place general all binary solutions show a decrease of metal ion bio-
in two stages, where; (1) for algae biomass, ions adsorb to cell sorption. There are several studies showing that the role of light
membrane passively and biosorption of metal ions occurs rapidly metal ions on the toxicity of heavier metal ions biosorption is very
within the first minutes, and; (2) for live algae, active sorption small (Deng et al., 2006, 2007). However, high concentrations of
occurs as heavy metal ions slowly uptake into the algal cell. Vogel monovalent cations of Naþ and Kþ, could increase the ionic
et al. (Vogel et al., 2010). investigated the uptake of uranium by strength of wastewater, leading to a reduction in biosorption ca-
non-living C. vulgaris and observed that more than 90% of the pacity of biomass (Schiewer and Wong, 2000; Vilar et al., 2008). In
dissolved uranium adsorb during the first 5 min. In another study, water contaminated with multiple heavy metal ions, competition
Tüzün et al. (Tüzün et al., 2005). showed that the biomass of among the metal ions to bind to the active sites of cell surface is
Chlamydomunas reinhardtii microalgae rapidly adsorbed free ions of directly influenced by the concentration of each ion and their
Hg (II), Cd (II) and Pb (II), with the biosorption equilibrium achieved properties, primarily electronegativity and ionic radius (Bayo, 2012;
in 60 min. Mata et al. (Mata et al., 2009a). reported the amount of Sulaymon et al., 2012). For example, aluminium ions can interfere
Au (III) adsorbed at a pH of 7 on the biomass of Fucus vesiculosus with biosorption of copper ions preventing access to the binding
macroalgae, after 1 and 8 h were 28.95 mg/g and 74.05 mg/g of dry sites at the cell surface (Lee et al., 2004), while the copper ions in
algae, respectively. This demonstrates that biosorption of heavy the solution had no significant effect on Alþ3 ion biosorption (Lee
metal ions is a passive process that occurs relatively rapidly, even and Volesky, 1999). Similar research by Kaewsarn et al. (Kaewsarn
when algal cells are non-living. In living algae contact time has a et al., 2001). showed the effect of interfering anions including
greater effect on the biosorption capacity. For example, Lamai et al. ethylenediaminetetraacetic acid (EDTA), SO2 3 2
4 , PO4 and CO3 ions
(Lamaia et al., 2005). measured the uptake of cadmium and lead on the biosorption of Cu (II). They reported that the biosorption of
ions by Cladophora fracta, separately harvested after 2, 4, 6, and 8 copper relatively decreased in the presence of EDTA, SO2 3
4 , PO4 ,
2
days, and found while the algal growth rate decreased over time, a and CO3 , respectively.
greater biosorption capacity was obtained in older cultures. These
results suggest that while passive heavy metal biosorption com- 3.8. The influence of other factors
mences swiftly in the first moments of contact, a greater level of IW
heavy metal bioremoval can be achieved with longer contact times Growth rates, level of dissolved nitrates, and light intensity can
using living algae. The issue with ‘older’ cultures from chemistry contribute to the removal of heavy metal ions by algae. Nitrate is a
Table 4
Comparison of biosorption capacity of metal ions using algal biomass in the binary solution vs. sole systems.
Type of algae Metal ion Binary solution Maximum sorption (mg g1) Reference
Sole Binary
Please cite this article in press as: Zeraatkar, A.K., et al., Potential use of algae for heavy metal bioremediation, a critical review, Journal of
Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.06.059
A.K. Zeraatkar et al. / Journal of Environmental Management xxx (2016) 1e15 9
primary nutrient for algae growth, and changing in initial nitrate Pb (II) biosorption capacity of CaCl2 treated biomass was higher
concentration can influence algae growth and biomass production than the control sample.
(Taziki et al., 2015a). Nitrate depression results in algae producing The effectiveness of implemented treatments in metal ion bio-
high amounts of lipids or low amounts of biomass, and therefore, sorption is directly dependent on the type of active sites present on
low metal ion biosorption (Taziki et al., 2015b). the cell surface. In a study, Zhao et al. (Zhao et al., 1994). investi-
The effect of light intensity on metal ion uptake is largely un- gated the effects of different treatments (HNO3, HCl, NaOH, acetone
known. The metal ion biosorption is proposed to be metabolism- and water, 60 C) on the biosorption of variant metal ions such as
independent for algal biomass and a two phase of metabolism- Pb, Cu, Zn, Cd, Cr, Mn, Ni, Co, Hg, Au, and Ag using six species of
independent and metabolism-dependent for living algae marine algae. They found that to varying extents all treatments
(Garnham et al., 1992), the former is slow and the latter is fast. The successfully increased the ability of biomass to bind metal ions and
initial metabolism-independent step, commonly valid for bio- improve biosorption capacity. Other chemical treatments (such as
sorption of metal ions on biomass is independent of light and phosphorylation) can enhance the biosorption of radioactive ions
temperature. However, research by Subramanian et al. from aquatic environments (Klimmek et al., 2001). For example,
(Subramanian et al., 1994). found biosorption of Zn (II) in the dark Pohl and Schimmack (Pohl and Schimmack, 2006) performed
regions is slightly higher than that in light regions. Culture medium phosphorylation of Laminaria japonica and two species of cyano-
dissolved gas concentration is also another factor that affects the bacteria biomass to increase the biosorption capacity of radioactive
growth rate of biomass and its contents. For example, Ota et al. (Ota nuclei (134Cs, 85Sr, 226Ra, 241Am). However, chemical pretreatments
et al., 2011). investigated the effect of dissolved oxygen on lipid do not always produce predictable results, and may even cause
synthesis in Chlorococcum littorale, and found that the lipid pro- opposite effects. For example, Zhang et al. (Zhang et al., 1997).
duction can be imitated by dissolved oxygen in photoautotrophic observed a decrease in uranium uptake by Scenedesmus obliqus
culture. The numerous variations in growth conditions affecting the after treatment with HCl, NaOH, NaCl, and diluted ethanol. Modi-
availability of binding groups also influence the characteristics of fication of the growth media (i.e. introducing supplements such as
the algal biomass, resulting in changes to relative heavy metal ion glucose, ammonium sulfate, phosphate, etc.) can potentially
biosorption capacity. improve the metal ion uptake by the biomass (Wang and Chen,
2006). The goal of all these growth media treatments are
4. Metal ion sorption by pretreated algae biomass improving the conditions to favor contact between functional
groups and metal ions through additional binding sites or improved
Increased heavy metal ion uptake by algal biomass can be linkage between the chains of biopolymers (Rinco n et al., 2005; Yan
enhanced by several physical/chemical treatments that change the and Viraraghavan, 2000).
algal cell surface properties to provide additional binding sites.
Algal biomass physical treatments such as heating/boiling, freezing, 5. Macro vs micro algae
crushing, and drying usually lead to an enhanced level of metal ion
biosorption. These treatments influence the important role of the Seaweed, green macroalgae and their alginate derivatives
cell wall in biosorption of metal ions, as non-living cell membrane exhibit high affinity for many metal ions (Mani and Kumar, 2014).
destruction provides more surface area to increase the biosorption The passive removal of toxic heavy metals by biological materials is
capacity (Lopez Errasquın and Vazquez, 2003) and release the cell an emerging potential known as biosorbents.
contents for possible increase in binding cell components to metal To investigate the biochemical properties of the brown algae a
ions. The most common algal pretreatments are CaCl2, formalde- comprehensive review was previously published (Davis et al.,
hyde, glutaraldehyde, NaOH, and HCl. Pretreatment by CaCl2 causes 2003); A detailed description of cellular structure, storage poly-
calcium binding to alginate that plays an important role in ion saccharides, cell wall and extracellular polysaccharides were dis-
exchange (Rinco n et al., 2005; Bishnoi et al., 2007). Formaldehyde cussed in terms of their potential role in metal biosorption in
and glutaraldehyde help strengthening the crosslinking between brown macroalgal strains. Alginate plays a critical role in metal
functional groups, especially hydroxyl groups and amino groups biosorption by brown algae. Alginate participate in ion-exchange
(Dabbagh et al., 2008; Ebrahimi et al., 2009). NaOH increases the and complexation result in binding of heavy metals by this poly-
electrostatic interactions of metal ion cations, and provides opti- mer. The adsorption capacity of the brown algae is directly related
mum conditions for ion-exchange, while HCl replaces light metal to the alginate content, availability and its specific macromolecular
ions with a proton and also dissolves polysaccharides of cell wall conformation. Alginate comprises a significant component up to
(Romera et al., 2006), or denatures proteins (Srinivasa Rao et al., 40e45% of the dry weight of Sargassum biomass (Fourest and
2005), and increase bonding sites to improve biosorption. Volesky, 1995). The affinity of alginates for divalent cations such
Arica et al. (Arıca et al., 2005). investigated the effect of heat and as Pb2þ,Cu2þ,Cd2þ and Zn2þ donate 227, 51, 79 and 78 mg g1 metal
acid treatment on the uptake of Cr (VI) by the biomass of Chlamy- uptake (Davis et al., 2003). Sargassum packed columns was inves-
domunas reinhardtii. The Cr (VI) biosorption capacity for the treated tigated to be used in flow-through column systems. Implementa-
biomass was 25.6 and 21.2 mg/g, respectively; significantly higher tion of such packed bed columns inactively adsorb and detoxify
than the untreated dried biomass (18.2 mg/g). Table 1 summarizes heavy metals bearing industrial wastewater (Bertagnolli et al.,
the effect of different physicochemical treatments on the bio- 2014). Algal biomass immobilization techniques will be further
sorption capacity of different algal strains, enabling a comparison of discussed in the next section.
implemented treatments on biosorption capacity. In order to in- To reply to the question about finding suitable freshwater fila-
crease biosorption of Cu(II) and Ni(II), Mehta and Gaur (Mehta and mentous algae that possess a high metal ion removal capability, Lee
Gaur, 2001a) treated chlorella vulgaris biomass by HCl, HNO3, and and Chang (Lee and Chang, 2011) evaluate the Pb(II) and Cu(II)
NaOH, and observed Cu(II) and Ni(II) bioremoval were higher than bioremoval capacity in two green macroalgae species, Spirogyra
the control sample. Several studies indicated that CaCl2 is a cost- and Cladophora, the results indicated that although the functional
effective treatment to increase the metal ion sorption by algal groups of these two genera of algae were similar, but the adsorption
biomass. For example, in order to increase biosorption of Pb (II), efficiency of Spirogyra spp. for Pb(II) and Cu(II) were superior to
Rincon et al. (Rinco n et al., 2005). treated Fucus vesiculosus mac- those of Cladophora spp. (87.2 and 38.2 mg g1 for Spirogyra and
roalgal biomass by CaCl2, HCl, and formaldehyde, and observed the 45.4 and 13.7 mg g1 for Cladophora, respectively). Further example
Please cite this article in press as: Zeraatkar, A.K., et al., Potential use of algae for heavy metal bioremediation, a critical review, Journal of
Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.06.059
10 A.K. Zeraatkar et al. / Journal of Environmental Management xxx (2016) 1e15
of biosorption capacity of different heavy metal ions using diverse and bioremediation interference.
macroalgal strains under varying physicochemical conditions are Regarding to the summarized data in Table 1, meaningful dif-
summarized in Table 1. ferences could not be tracked among removal efficiencies of living
Comparison of living and non-living algal species will be and non-living algae; in more details, different living and non-
comprehensively reviewed in the next section from other stand- living samples of C. vulgaris presented the same ion removal effi-
points. Microalgae usually step further in contamination bio- ciency for U4þ (Vogel et al., 2010) and Ni2þ (Al-Rub et al., 2004)
removal. In more details, denitrification, dephosphorylation and biosorption. In summary, the living cells having metabolic activities
COD reduction beside heavy metal biosorption are well established possibly present higher uptake of metal ions compared to dead
in microalgae wastewater treatment (Larsdotter et al., 2003). biomass. They could also adsorb more diverse range of ions (Doshi
et al., 2007), However, non-living cells present faster uptake ki-
netics. The dead biomass materials could be successfully reused in
6. Living vs non-living algae successive adsorptionedesorption cycles (Areco et al., 2012).
Finally, low cost and ease of use in non-living cells have developed
Although clear differences exist between accumulation of metal this technology as a serious candidate for bioremediation of for IW
ions onto living algae cells and biosorption of metal ions onto non- in large scale. Consequently, to achieve the highest removal effi-
living algae biomass, the process with the largest contribution in ciency, interaction between algal strains, dead or live cells and
biosorption of heavy metal ions in both living and non-living algae pollutants should be optimized.
is mostly the ion exchange process (Monteiro et al., 2012). Since the
influence of operating parameters such as pH, temperature and
contact time have been previously discussed, herein the efficiency 7. Immobilized algae
and also the applicability of living and non-living algae in the
removal processes of metal ions will be introduced. While meta- Techniques such as flocculation, adsorption on surfaces, cova-
bolic processes in living algae generally contribute to heavy metal lent binding to carriers, crosslinking of algal cells, and entrapment
bioremediation (Gadd, 1988), using non-living algae has recently of algae in polymeric matrix are used for cell/biomass immobili-
gained popularity for biosorption of heavy metal ions from solu- zation (Rangsayatorn et al., 2004; Lo pez et al., 1997). For immobi-
tions. Non-living biomass biosorption advantages include a heavy lization of biomass, natural biopolymers (such as agar and alginate)
metal biosorption several times greater in non-living algae as or synthetic compounds (such as silica gel and polyacrylamide) can
compared to living algae (Mehta and Gaur, 2005; Tsang et al., 1999; be used as supporting materials. Natural polymers are often
Tam et al., 2002). Moreover, the possibility to recycle non-living preferred to synthetic polymers due to non-toxicity to biomass, and
algal biomass is a unique characteristic dealing by dead biomass for this reason calcium alginate has been widely used for immo-
(Aksu and Do € nmez, 2001). For example, metal ions bound to the bilization of algal cells and many other biomass sources (Mehta and
algal cell wall may be removed by washing the biomass with Gaur, 2001b; Bayramog lu et al., 2006; Bayramoglu and Yakup Arica,
deionised water and desorption agents (HCl, NaOH, CaCl2) (Chen 2009). Among synthetic polymers, polyacrylamide has been most
et al., 2012), whereas living algae have a low mechanical and extensively used (Darnall et al., 1986; Nakajima et al., 1982), as it is
chemical resistance to physical and chemical treatments for recy- more resistant than calcium alginate, although its application for
cling. It is worth quoting that the non-living algae can be easily immobilization processes is limited by its high cost and toxicity to
treated using physical and chemical protocols to enhance adsorp- living cells. Table 5 presents research where immobilized algae has
tion capacity (Arıca et al., 2005). The use of non-living algal biomass resulted in an increase in biosorption capacity relative to free algal
also removes the risks of exposures to highly toxic environments, cells, and prevented loss of biomass during the biosorption cycle
and do not require intensive management or addition of further (Eroglu et al., 2015). Biomass immobilization enhances photosyn-
growth nutrients (Arunakumara and Zhang, 2008; Franklin et al., thetic capacity (Bailliez et al., 1986) and reduces toxicity of some
2002). Nonetheless, several environmental factors influence non- substances (Bozeman et al., 1989). It also facilitates repetitive use of
living algae heavy metal ion biosorption. For example, changes in algal cells during successive sorption/desorption cycles of metal
pH impact living algae to a greater extent than non-living algae as ions bioremoval from aqueous solutions. Enhanced surface sorption
most algae grow in neutral or slightly alkaline mediums (Kong in the immobilized powdered algal cells result in a 2-fold increase
et al., 2010), and acidic media can affect the algae growth rate, in nickel removal in comparison to the free non-living C. vulgaris
and basic media might cause precipitation of the metal ions (Skoog cells (Al-Rub et al., 2004). The same observation was reported by
et al., 2013; Fu and Wang, 2011). Heavy metal removal in solutions Murugesan et al. (Murugesan et al., 2008). on the potential of
with an extreme pH favors non-living algae over living algae, as immobilized algal cells of Spirulina platensis in cadmium ion bio-
using live algae adds complexity to culture medium chemistry sorption. While algae immobilization has a high potential for
management that might lead to unwanted metal ion precipitation removing toxic metal ions from IW, it requires an ideal cost
Table 5
Comparison of biosorption capacity of metal ions using immobilized algal biomass vs. living algae.
Algae species Immobilization system Initial metal ion conc. (mg L1) Metal ion Max. sorption (mg g1) References
Chlamydomonas reinhardtii Ca e alginate 500 Cd(II) 28.9 79.7 (Bayramoglu et al., 2006)
Chlorella sorokiniana Loofa sponge 300 Cr(III) 58.8 69.26 (Akhtar et al., 2008)
Scenedesmus quadricauda Ca e alginate 600 Cu(II) 35.9 75.6 (Bayramoglu and Yakup Arica, 2009)
C. reinhardtii Ca e alginate 500 Cu(II) 35.9 106.6 (Bayramoglu et al., 2006)
C. sorokiniana Loofa spong 200 Ni(II) 48.08 60.38 (Akhtar et al., 2004)
C. vulgaris Blank alginate 100 Ni(II) 15.6 28.6 (Al-Rub et al., 2004)
S. quadricauda Ca e alginate 600 Ni(II) 9.7 30.4 (Bayramoglu and Yakup Arica, 2009)
C. reinhardtii Ca e alginate 500 Pb(II) 230.5 308.7 (Bayramoglu et al., 2006)
S. quadricauda Ca e alginate - Zn(II) 20.2 55.2 (Bayramoglu and Yakup Arica, 2009)
Please cite this article in press as: Zeraatkar, A.K., et al., Potential use of algae for heavy metal bioremediation, a critical review, Journal of
Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.06.059
A.K. Zeraatkar et al. / Journal of Environmental Management xxx (2016) 1e15 11
Please cite this article in press as: Zeraatkar, A.K., et al., Potential use of algae for heavy metal bioremediation, a critical review, Journal of
Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.06.059
12 A.K. Zeraatkar et al. / Journal of Environmental Management xxx (2016) 1e15
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