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PII: S0960-8524(20)30155-3
DOI: https://doi.org/10.1016/j.biortech.2020.122886
Reference: BITE 122886
Please cite this article as: Kit Leong, Y., Chang, J-S., Bioremediation of heavy metals using microalgae: Recent
advances and mechanisms, Bioresource Technology (2020), doi: https://doi.org/10.1016/j.biortech.2020.122886
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ABSTRACT
Five heavy metals namely, arsenic (As), cadmium (Cd), chromium (Cr), lead (Pb) and
mercury (Hg) are carcinogenic and show toxicity even at trace amounts, posing threats to
availability, inexpensive, excellent metal removal efficiency and eco-friendly nature. This
review presents the recent advances and mechanisms involved in bioremediation and
biosorption of these toxic heavy metals utilizing microalgae. Tolerance and response of
different microalgae strains to heavy metals and their bioaccumulation capability with
of heavy metals by microalgae are also explored. This review aims to provide useful insights
to help future development of efficient and commercially viable technology for microalgae-
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1. INTRODUCTION
“Heavy metals” is a term generally referred to metals and metalloids with density more
than 5 g/cm3 which include arsenic (As), cadmium (Cd), chromium (Cr), copper (Cu), iron
(Fe), lead (Pb), mercury (Hg), silver (Ag), zinc (Zn) and others (Duruibe et al., 2007). They
are widely involved in human activities, such as fossil fuel combustion, mining,
electroplating, dye and pigments manufacturing, fertilizers, and other industrial activities,
which are then released in large amount into the environment daily via wastewater or other
metals tend to persist in nature, leading to bio-accumulation in food chain which causes
contamination limits (MCL) of As, Cd, Cr, Hg and Pb are 0.01, 0.005, 0.1, 0.002 and 0.015
mg/L respectively (USEPA, 2016). These heavy metals and their compounds, even at very
low concentrations, are highly toxic, carcinogenic, mutagenic and teratogenic. Direct
contact, inhalation and ingestion of these heavy metals poses serious threats to human
physical and mental health, causing mutations and genetic damage, damaging central
nervous system as well as escalating the risk of cancers (Balaji et al., 2016a; Jaafari &
Yaghmaeian, 2019). Hence, it is crucial to remediate these toxic heavy metals in wastewater
Conventional techniques employed for heavy metals removal from wastewater include
electrocoagulation) (Fu & Wang, 2011). However, these techniques have the disadvantages
of expensive operation and maintenance costs, as well as secondary pollution due to toxic
3
sludge formation. Furthermore, most of these techniques are further expensive and/or
ineffective at very low concentrations of heavy metals, specifically below 100 mg/L
bacteria, microalgae, yeasts and fungi have been widely applied as alternatives to
biological characteristics such as high photosynthetic efficiency and simple structure has
the ability to grow well under extreme environmental conditions such as presence of heavy
metals, high salinity, nutrient stress and extreme temperature. Therefore, there is an
its high binding affinity, abundance of binding sites and large surface area (Cameron et al.,
2018). Furthermore, both living cells and non-living biomass of microalgae can be
employed as biosorbents. Other than outstanding removal capacity and being eco-friendly,
bioremediation of heavy metals using microalgae has the benefits of robust and simple
process, lack of toxicity constraint, rapid growth rate compared to higher plants as well as
formation of value-added products such as biofuels and fertilizers (Abinandan et al., 2019;
Balaji et al., 2016b). In addition, oxidative stress induced by heavy metals enhances the lipid
employed for the recovery of precious metal ions, such as thallium, silver and gold (Birungi
In this review, we present the recent advances and in-depth summary of the development
of bioremediation of five non-threshold toxic heavy metals, which are arsenic (As),
cadmium (Cd), chromium (Cr), lead (Pb) and mercury (Hg) by microalgae. These heavy
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metals have gained much attention and became a significant research focus due to their
severe deteriorating effects to the environmental ecology and human health (Rahman &
Microalgae consume heavy metals such as boron (B), cobalt (Co), copper (Cu), iron (Fe),
molybdenum (Mo), manganese (Mn), and zinc (Zn) as trace elements for enzymatic process
and cell metabolism, though other heavy metals such as As, Cd, Cr, Pb and Hg are toxic to
microalgae. Due to hormesis phenomenon, low toxic heavy metal concentrations can
stimulate the growth and metabolism of microalgae (Sun et al., 2015). Some cyanobacterial
species, such as Anabaena, Oscillatoria, Phormidium and Spirogyra can naturally grow in
water contaminated by heavy metals due to their tolerance towards heavy metal stress
(Balaji et al., 2016a). Other than heavy metals, microalgae have reactive groups with active
binding sites which can form complexes with pollutants in wastewater. This leads to
flocculation and subsequently reduces the content of both total dissolved solids (TDS) and
toxicity of heavy metals, such as heavy metal immobilization, gene regulation, exclusion
and chelation as well as antioxidants or reducing enzymes which reduce heavy metals via
redox reactions (Gómez-Jacinto et al., 2015). Microalgae can form cellular protein-heavy
metals complexes without changing its own activity (Priatni et al., 2017). The
organometallic complexes are further separated insides vacuoles to help regulate the heavy
metal ions concentration in cytoplasm which subsequently mitigate their toxic effects
(Balaji et al., 2016b). In addition, heavy metals activate the biosynthesis of phytochelatins
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(PCs) which are thiol-rich peptides and proteins that minimize heavy metal stress by
To counteract with free radicals released by heavy metals during adsorption, microalgae
antioxidants such as carotenoids, cysteine, ascorbic acid (ASC), glutathione (GSH) and
proline (Upadhyay et al., 2016). SOD acts as the first line of defence against superoxide
anion by breaking it down into oxygen molecules and hydrogen peroxide. The hydrogen
peroxide is further degraded by catalase into water and oxygen molecules (Balaji et al.,
2016b). Cysteine indirectly or directly serves as the precursor for PCs, GSH,
metallothioneins and other sulphur containing compounds, hence serving as the indicator
GSH and ASC are important endogenous antioxidants synthesized by microalgae and
they play a key role in the reduction of reactive oxygen species (ROS) and free radicals
(Devars et al., 2000). Other than maintaining the equilibrium of ROS production and
surplus excitation energy and scavenging ROS. Furthermore, high level of ASC is secreted
by microalgae as a hydrophilic redox buffer that is responsible for the protection of cytosol
and other cellular components against oxidative threats. On the other hands, high level of
GSH protect the microalgae by providing tolerance, scavenging free radicals, facilitating
PCs and ASC synthesis as well as restoration of substrate for other antioxidants (Gómez-
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Removal of heavy metals by microalgae is attained via a two-stage mechanism. The first
stage is the rapid extracellular passive adsorption (biosorption), while the second stage is
cell polymeric substances such as peptides and exopolysaccharides with uronic groups, cell
wall of microalgae are mainly composed of polysaccharides (cellulose and alginate), lipids
and organic proteins, provides many functional groups (such as amino, carboxyl, hydroxyl,
imidazole, phosphate, sulfonate, thiol and others) capable of binding heavy metals (Priatni
et al., 2017). Furthermore, they consisted of huge amount of monomeric alcohols, laminaran,
deprotonated sulphate and carboxyl groups which attract both anionic and cationic species
of different heavy metals. Microalgae biomass also has different functional groups, such as
amide, carbonyl, carboxylic acid, ether and hydroxyls which contribute to the biosorption
(Pradhan et al., 2019). Fourier-transform infrared (FTIR) analysis and nuclear magnetic
microalgae that are responsible for formation of complexes with heavy metals as well as
examine the interaction between them. The knowledge of biosorbents chemical structure
provides important information for prediction of their affinities for heavy metal ions.
Adsorption of heavy metal on the surface of microalgae is a rapid process and can
happen via different paths, which are formation of covalent bond between ionized cell wall
with heavy metals, ionic exchange of heavy metal ions with cell wall cation and binding of
heavy metal cations with negatively charged uronic acids of microalgae exopolysaccharides.
On the other hand, the process of heavy metal accumulation inside the cell is much slower.
The heavy metals are actively transported across the cell membrane and into the cytoplasm
followed by diffusion and subsequent binding with internal binding sites of proteins and
peptides such as GSH, metal transporter, oxidative stress reducing agents and
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phytochelatins (Ibuot et al., 2017; Pradhan et al., 2019). Figure 1 illustrates the mechanisms
A and category 1 carcinogen, arsenic (As) is one of the major toxic heavy metals that cause
China, Finland, India, South East Asia and USA (Arora et al., 2018; Upadhyay et al., 2016;
such as combustion of fossil fuels, mining, medical use, fertilizers and pesticides, smelting,
electrolytic process, sewage sludge as well as pigments, semiconductor, glass and alloy
manufacturing processes (Arora et al., 2017; Singh et al., 2016). Physical exposure to As
even at low concentrations (0.1 µg/mL) cause lung, skin, kidney and bladder cancers, while
diabetes, infant morbidity, immune alteration, impairment to the central nervous system,
hepatic damage and hyperkerotosis (Li et al., 2019). Conversely, in plant and microalgae,
arsenic causes impairment to cell organelle and DNA, lipid peroxidation and protein
state and chemical form. Arsenic has four oxidation states, which are arsenic (As0), arsine
[As(-III)], arsenite [As(III)] and arsenate [As(V)]. The most commonly occurring oxidation
states of As are trivalent [As (III)] and pentavalent [As(V)] forms, of which the former is
8
more toxic (Zhu et al., 2018). In aqueous solution, As (III) exists predominantly as H3AsO3
with other forms such as H4AsO3+, H2AsO3-, HAsO32- and AsO33-, while As(V) exists as
H3AsO4, H2AsO4-, HAsO42- and AsO43- (Arora et al., 2017). The inorganic form of arsenic
is much more toxic than its organic form. Thus, it is beneficial to transform arsenic into its
arsenocholine (ArsC) and arsenobetaine (ArsB) (Wongrod et al., 2019). Microalgae reduces
the toxicity of inorganic arsenic by As (III) oxidation and complex formation with
excretion from the cell (Papry et al., 2019). Oxidation of As(III) mainly happens outside the
cells by interacting with functional groups such as -OH, -NH, -CH of aldehyde and aliphatic
as well as -CN of amino groups (Arora et al., 2018; Wang et al., 2014). On the other hand,
cellular metabolism of arsenic starts with rapid reduction of As(V) to As (III) followed by
a slower step-by-step methylation first to MMAs, and then to DMAs. Microalgae have been
shown to excrete both methylated arsenic species and/or reduced As(III) (Baker &
Wallschläger, 2016).
electron configuration as arsenate [As(V)] (Sun et al., 2015). Therefore, the high affinity
phosphate transporters of microalgae (such as PIT and PST) can participate in the uptake of
arsenic. PO43- limitation induces the synthesis of arsenic transporter and thus, accelerates
arsenic uptake (Wang et al., 2014). On the other hand, increased phosphate concentration
significantly reduced the arsenic uptake in microalgae such as Chlorella sp. (Bahar et al.,
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2016), C. vulgaris (Baker & Wallschläger, 2016; Li et al., 2019), C. salina (Karadjova et
al., 2008), Dunaliella salina (Wang et al., 2017; Wang et al., 2016), Chlamydomonas
reinhardtii and Scenedesmus obliquus (Wang et al., 2013). This is because both As(III) and
extracellular PO43-. However, it is reported that PO43- concentration has negligible impact
on the removal of arsenic by fungal-algal pellets and high removal capacity was achieved,
though arsenite methylation did not occur (Li et al., 2019). Wang and co-workers reported
that PO43- and As(V) has a synergistic interaction and significantly promoted the initial
growth of axenic cultures of Dunaliella salina, though the growth experienced inhibition
after 9 days of cultivation. The presence of symbiotic bacteria and PO43- limitation are
shown to promote the reduction of As(V) and induce the excretion of As (III) and DMA by
Different freshwater and marine microalgae have varying tolerance to arsenic, thus
experience different growth rate and bioaccumulation capacity in the presence of arsenic.
tricornutum, Morelli and colleagues observed a gradual decrease in growth rate when the
concentration of As(V) was above 0.1 µm and the microalgae experienced maximum
freshwater microalgae, Levy and co-workers found that Chlorella sp. has more tolerance to
arsenic compared to Monoraphidium arcuatum (Levy et al., 2005). Jiang and co-workers
reported high tolerance of Chlorella vulgaris to As(V) up to 200 mg/L with constant arsenic
removal of 70%. Extracellular heavy metal adsorption serves a critical role in As(V)
removal by microalgae at concentrations below 100 mg/L (Jiang et al., 2011). Huang and
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aeruginosa and Oscillatoria tenuis experienced up to 2.6-fold slower growth rate in As(V)-
containing medium compared to control. Among these microalgae, A. affinis and O. tenuis
removed As(V) by binding them to extracellular cell wall active sites, while intracellular
(Huang et al., 2014). Upadhyay and colleagues has reported that Nannochloropsis sp. can
grow well in As (III) concentration up to 100 µm and have a significant decrease in biomass
content at As (III) concentration further increases to 500 µm. Rapid decrease in biomass at
high concentration of arsenic might be caused by the blocking of -SH group, leading to
2016). Singh and colleagues also reported high accumulation of arsenic up to 760 µg/g in
Phormidium sp. and Oscillatoria sp. found in As-contaminated area, showing potential in
bioremediation of As (Singh et al., 2016). Arora and co-workers found that Chlorella
minutissima and Scenedesmus sp. IITRIND2 can tolerate up to 500 mg/L arsenic with
removal up to 161 µg/g (Arora et al., 2017). Comparing between four green microalgae
Responding to arsenic stress, decrease in protein and chlorophyll content was observed in
both C. minutissima and Scenedesmus sp. In addition, cell size reduction was recorded in C.
minutissima, while Scenedesmus sp. has increased lipid content at the cost of carbohydrate
reserve (Arora et al., 2017). Upon bioaccumulation of arsenic, the total chlorophyll content
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Nannochloropsis sp. treated with 100 µm As(III) has the highest lipid productivity of 20.27
mg/L/day and produce biofuel meeting EN 14214 standards (Upadhyay et al., 2016). Sun
and co-workers observed an increase in the external cell surface area of Nannochloropsis
sp. due to formation of measles-like granules and wrinkles caused by arsenic toxicity. The
acids which is desirable for high quality biofuel production (Sun et al., 2015). Scenedesmus
sp. IITRIND2 cultured in As-containing synthetic soft water produced microalgal lipid with
linoleic acid, oleic acid, palmitic acid and stearic acid as major constituents. The biodiesel
produced from this lipid not only met the requirement of biodiesel standards (EN14214 and
ASTM D6751-52), but also has higher oxidative stability, leading to a longer shelf life
(Arora et al., 2017). Table 1 summarizes the biosorption of arsenic (As) by different
microalgae strains.
Characterized as a highly toxic invasive heavy metal, cadmium is released into the
metals and alloys, ceramics, colour pigment, fertilizers and pesticides, nickel-cadmium
batteries, plastic, and also electroplating, mining, smelting and welding process (Abinandan
et al., 2019). Due to its carcinogenic and teratogenic nature, cadmium induces severe
damage to reproductive organs, kidney, liver and lungs even at trace amount, leading to
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Microalgae strains respond differently under cadmium stress. In addition to reducing
cell growth and chlorophyll content, Cd(II) induces the production of phytochelatins,
Chlamydomonas moewusii and Monoraphidium sp. (Mera et al., 2016; Zhao et al., 2019).
cadmium with maximum adsorption capacity of 35.65 mg/g. Uptake of 0.6 mM Cd(II) have
shown to enhance both microalgal lipid content and productivity up to 42.1% and 2.17 fold
compared to control. The maximum lipid productivity of 249.36 mg/L.day was also higher
than many reported in literature (Yang et al., 2015). Monoraphidium sp. QLY-1 treated with
80 µm Cd(II) showed enhanced lipid content (52.78 %) of 1.59 fold compared to control
(Zhao et al., 2019). A 0.02 µm of free Cd(II) improved growth rate and total lipids of
Chlorella vulgaris by 13.4% and 51.5% respectively (Chia et al., 2013). Similarly, acid-
tolerant microalgae, Heterochlorella sp. MAS3 and Desmodesmus sp. MAS1 can
simultaneously remove 2 mg/L Cd(II) with >58% efficiency and accumulated lipids rich in
With the advantage of cost-effective biomass harvesting from diluted culture, self-
flocculating microalgae, such as Chlorella vulgaris JSC-7 (Alam et al., 2015) and
Scenedesmus obliquus AS-6-1 (Zhang et al., 2016), have been utilized for the removal of
Cd(II). Due to the distinctive cell wall components, enhanced synthesis of phytohormones
and higher antioxidation activity, C. vulgaris JSC-7 was more tolerant to Cd2+ with an
improved heavy metal removal capacity of 21.5 mg/g compared to 6.5 mg/g of non-
flocculating control species, (i.e., C. vulgaris CNW11) (Alam et al., 2015). Other than the
main contribution from phosphate and carboxyl groups, functional groups such as amide,
C-N, hydroxyl and S-O groups also responsible for adsorption of Cd(II) in S. obliquus AS-
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6-1. Successive adsorption/desorption cycle studies showed that S. obliquus AS-6-1
maintained its flocculating properties as cadmium chloride did not impair the flocculating
properties and might even help induce chemical flocculation (Zhang et al., 2016).
immobilization and bio-pellets have been studied to improved cadmium biosorption. Gene
reinhardtii, which showed a 2.29 and 3.06 fold increased in Cd2+ tolerance and uptake,
respectively, when compared with wild type C. reinhardtii (Ibuot et al., 2017). However,
the natural strains adapted to wastewater growth such as Parachlorella hussii, Parachlorella
kessleri and Chlorella luteoviridis still demonstrated better heavy metal tolerance and
selenium for bio-fabrication of fluorescent CdSe NPs has been performed. The reducing
reductase were speculated to play a crucial role in the formation of CdSe NPs (Zhang et al.,
2019). Immobilized Chlorella sp. in alginate bead has demonstrated biosorption of Cd(II)
214.7 mg/g higher than both Chlorella sp. and biochar alone due to enhancement of the
surface potential. Functional groups such as -OH, -NH, P=O (phosphoryl group), P=S
cadmium biosorption (Shen et al., 2017). Similarly, Chlorella sp. immobilized with water-
hyacinth leaf biochar pellets achieved 92.5% Cd(II) removal efficiency and remained viable
at 10 mg/L Cd(II) (Shen et al., 2018). Bio-pellets composed of C. vulgaris microalgae and
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Apsergillus niger fungi showed better performance for the removal of Cd(II) at low level of
1 µg/L up to 56% compared to 40% of microalgae alone, with the advantages of lower final
On the other hand, utilization of non-living microalgae cells for the removal of
cadmium via passive surface binding have been studied as well. Dirbaz and Roosta have
sp., Scenedesmus sp. and Spirulina sp. due to the presence of a large amount of acidic
functional groups such as carboxylic acid. Functional groups such as -OH, -NH, C=O of
amide and C-O of alcoholic groups contributes to cadmium biosorption (Dirbaz & Roosta,
2018). The residual lipid extracted biomass of Chlorella sp. CHA-01, Chlamydomonas sp.
TAI-03 and Coelastrum sp. PTE-15 with broken cell wall have been investigated for the
biosorption of Cd2+ and suggested that the intracellular cell wall components also contribute
in heavy metal binding (Zheng et al., 2016). Freeze-dried biomass of Chlorella minutissima
UTEX2341 was a superior biosorbent compared to growing algae (Yang et al., 2015).
beads have been utilized for Cd2+ removal with at least 63.1% adsorption efficiency up to
50 ppm Cd2+ at pH 6 (Hwang et al., 2018). Most of the literature reported that the adsorption
of Cd2+ followed Langmuir isotherm, suggesting that the predominant sorption step is a
single surface reaction at constant adsorption energy (Dirbaz & Roosta, 2018; Jena et al.,
2015; Shen et al., 2017; Zhang et al., 2016; Zheng et al., 2016). Table 2 summarizes the
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Chromium compounds have industrial applications in dyes, paint, ink and pigment
manufacturing, leather tanning, metal electroplating, production of steel and alloys as well
as wood preservation (Gupta & Rastogi, 2008). Chromium has several oxidation states
ranging from +2 to +6, with the two most common and stable states are trivalent Cr(III) and
hexavalent Cr(VI) (Shokri Khoubestani et al., 2015). Cr(VI) is much more toxic than Cr(III)
as the former can penetrate cell membrane without difficulty and disturb its integrity, while
the cell membrane is almost impermeable to the latter. Cr(VI) shows toxicity even at very
low concentration in parts per billion (ppb) due to its carcinogenic and mutagenic properties
(Pradhan et al., 2019). Furthermore, Cr(VI) is highly water-soluble and have strong
oxidizing properties to damage genetic materials and modify the DNA transcription process
(Gokhale et al., 2008; Shen et al., 2019). Ingestion of Cr(VI) can cause lung, skin and
stomach cancer as well as chronic bronchitis, epigastric pain, liver damage, kidney problem,
and DNA impairment by interference with DNA polymerase (Daneshvar et al., 2019;
Kayalvizhi et al., 2015). Cr(III) and Cr(VI) occurs as cationic and anionic species in the
Several mechanisms have been proposed for the reduction and removal of Cr(VI)
by microalgae, depending on the binding properties of the functional groups and the nature
Organelles, granules and cytosolic heat-stable peptides and proteins accumulated the
majority of Cr(VI) inside microalgal cells (Aharchaou et al., 2017). Other than extracellular
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adsorption and intracellular accumulation of Cr(VI), enzymatic chromium reductase is also
responsible for removal of the heavy metal ions (Lee et al., 2017; Yen et al., 2017).
Furthermore, Cr(VI) also interacts with the electron donor of reducing agents (such as
hydroxyl group and secondary alcohol groups) on the biomass surface favourably at acidic
pH and is reduced to Cr(III), which subsequently binds to the negatively charged functional
groups (such as sulfonate group and carboxyl group). The reduction of Cr(VI) anionic
microalgae biomass, which might due to the release of glutathione (Yen et al., 2017). Some
Cr(III) complexes are released into the medium due to complex formation with adjacent
negatively charged functional groups, ion exchange with competitor ions (such as Ca2+,
Mg2+ and Na+) as well as electrostatic repulsion between Cr(III) complex and positively
charged functional groups (Pagnanelli et al., 2013; Shen et al., 2019). HPO42- and H2PO4
ions significantly inhibited the adsorption of Cr(VI), while common background anions
have a minor detrimental effect on Cr(VI) reduction in the order of SO42- < Cl- < NO3-
Cr(VI). Chlorella sorokiniana can tolerate up to 100 ppm Cr(VI) for three days and achieved
removal efficiency up to 99.7 % after 24 h contact time (Husien et al., 2019). Navicula
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respectively, in laboratory conditions and natural chromium-containing water. The
microalgae can almost completely remove the heavy metal up to 98% in culture containing
20 mg/L Cr(VI) (Cherifi et al., 2016). Phaeodactylum tricornutum and Navicula pelliculosa
(Hedayatkhah et al., 2018). Pseudanabeane mucicola and Pediastrum duplex can tolerate
Cr(VI) up to 1.936 and 0.224 g/L, respectively, and the former has a Cr removal efficiency
of 71% (Dao et al., 2018). Four microalgae presented different tolerance when cultivated
with Cr(VI) in the order of Lyngbya sp. > Chlorella sp. > Scenedesmus dimorphus >
Oscillatoria sp. (Nath et al., 2017). Also, Scenedesmus acutus and Chlorella vulgaris can
Spirogyra sp., the functional groups responsible for metal ion binding on microalgal cell
wall were carboxylate, ester and hydroxyl groups (Balaji et al., 2016b). The growth rate of
growth and reduction of cell division caused by heavy metal stress. Similarly, microalgae
also experience a reduction in total protein content with increase in heavy metal
the electron transport system. The microalgae Oscillatoria sp. is a better candidate for
well as higher antioxidant activity (Balaji et al., 2016a; Balaji et al., 2016b). Jacome-Pilco
and colleagues have studied the removal of Cr(VI) in continuous cultivation system using
The culture reached steady state after 14 days; uptake and removal efficiency of Cr(VI)
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achieved were 1.7 mg/g and 43.5%, respectively (Jácome-Pilco et al., 2009). Shen and co-
workers have studied Cr(VI) removal potential of three heterotrophic microalgae strains
namely, Botryococcus sp. NJD-1, Scenedesmus sp. NJD-6 and Chlorella sp. NJD-9 and the
strain NJD-1 showed higher tolerance to Cr(VI) compared to the other two strains.
Cultivating at 3 % v/v of sodium acetate and 5mg/L Cr(VI), the microalgae achieved
removal efficiency of 94.2 %, 66.9 %, 99.2 % and 98.2 % for Cr(VI), NO3, PO4 and TOC
respectively. The functional groups such as -OH, -NH, aliphatic C-H, amino, carboxyl and
secondary alcohol groups participated as electron donors in the reduction of Cr(VI) to Cr(III)
On the other hand, literature has reported the utilization of non-living biomass of
microalgae as biosorbent for the removal of Cr(III) and Cr(VI) which summarized in Table
3. Pre-treatment techniques such as methylation (Finocchio et al., 2010) and treatment with
NaOH and SDS (Nath et al., 2017) were performed to improve Cr(VI) removal by
efficiency of > 80% for Cr(VI) up to 25 mg/L with 2-4 g/L biomass (Finocchio et al., 2010).
Lyngbya sp. with 0.1 N NaOH and 0.01 % SDS both showed better Cr(VI) removal
performance compared to untreated non-living consortia and live consortia cells (Nath et
al., 2017). In addition, immobilization of microalgae biomass on PVA (Ardila et al., 2017)
and calcium alginate beads (Kwak et al., 2015; Singh et al., 2012) were performed for the
purpose of easier harvesting. However, the harsh process of immobilization damaged the
microalgae cell wall and resulted in reduced heavy metal removal efficiency (Ardila et al.,
2017). Among the different forms of dried S. quadricauda (powder, pellet and biochar),
19
Cr(VI) (Daneshvar et al., 2019). For cost-effective Cr(VI) bioremediation, lipid-extracted
spent biomass (Nithya et al., 2019) and β-carotene pigment-extracted biomass of Spirulina
plantesis (Gokhale et al., 2008) were utilized for Cr(VI) removal. The pigment extracted
compared to 73.6% of fresh biomass, which might due to increased surface area of biomass
caused by cell membrane rupture during pigment extraction process (Gokhale et al., 2008).
microalgae where heavy metal ions carrying positive or negative charge adsorbed on the
reduction mechanism where Cr(VI) is removed by direct reduction of the biomass electron
donor (Park et al., 2007). The functional groups such as aldehydes, alkyl chains, amide,
and aliphatic organic chains of cellulose were identified as functional groups for the
removal efficiency at pH 6, due to the increase of species such as CrOH2+ and CrOH2+ which
have stronger binding affinity to negative functional groups. On the contrary, the maximum
removal of Cr(VI) was achieved at pH 1-2, due to formation of anionic species of Cr(VI)
Furthermore, the biomass surface consisted of high levels of hydronium ions at acidic
conditions which promoted interaction between Cr(VI) and microalgae binding sites
increased with increasing temperature (Kayalvizhi et al., 2015; Nithya et al., 2019; Pradhan
20
et al., 2019). Sibi also reported that Cr(VI) removal of C. vulgaris increased with increasing
electrical conductivity up to 2.9 mS/cm, but decreased sharply at the electrical conductivity
of 3.8 mS/cm due to competition between anionic species of Cr(VI) with chloride ion for
binding sites and inhibition of cell membrane permeability by NaCl (Sibi, 2016).
Lead has various applications in paint, battery making, cosmetics, weaponries and
building materials. Being one of the most toxic heavy metal, lead seriously endangers the
safety of human health and aquatic organisms. Other than causing serious physical and
mental health problems in children, Pb2+ can cause anaemia, brain disease, damage to the
central nervous system, dementia, kidney malfunction, reproduction abnormality and even
Literature has reported the utilization of Spirulina platensis (Malakootian et al., 2016),
Chlamydomonas reinhardtii (Bayramoğlu et al., 2006), Phormidium sp. (Das et al., 2016),
Rhizoclonium hookeri (Suganya et al., 2016) as well as Chaetoceros and Chlorella sp.
(Molazedah et al., 2015) as the biosorbent for the removal of lead. Das and co-workers have
further studied semi-packed bed adsorption of Pb2+ and found that bed height and flow rate
were the significant parameters in the semi-batch biosorption process (Das et al., 2016). The
functional groups such as acyl-amino, amide, amine, carbonyl, carboxyl, hydroxyl, phenols
and phosphate were identified for the biosorption of Pb2+. The adsorption of lead ions
charge density on the binding sites and competition with H+ for occupancy of sorption sites.
The biosorbent generally has the maximum efficiency of Pb2+ removal at pH 5-6, due to the
increase of species such as Pb2+ and Pb(OH)+. The formation of Pb(OH)2 which precipitated
21
was observed at pH > 6 (Akhtar et al., 2004). Ion exchange mechanism can be employed to
explain the adsorption of cationic species of Pb2+ on Chlorella sp. surface. The
The adsorption enthalpy value and enthalpy change showed that the adsorption of Pb2+ by
agreed that the biosorption of Pb2+ by microalgae followed a pseudo-second order kinetic
model (Das et al., 2016; Malakootian et al., 2016; Molazedah et al., 2015; Suganya et al.,
2016). This suggested that the chemical sorption which involves ion exchange and electron
sharing between Pb2+ and the biomass might be the rate-limiting step.
cell type “incrassatulus” and increased morphology type “obliquus”. Therefore, peripheral
detection of lead pollution (Batsalova et al., 2017). Similarly, marine microalgae Nitzchia
closterium has become a potential candidate for rapid, simple and effective detection of lead
Mercury has been primarily released by industrial activities such as mining, smelting,
waste incineration and coal combustion in gaseous and aqueous form (Peng et al., 2017).
Mercury and its compounds are considered as one of the most toxic and hazardous heavy
22
metals in the environment as mercury can be converted into the potent neurotoxin methyl-
mercury (MeHg). Mercury toxicity is mainly associated with its capability to penetrate the
blood-brain barrier, interference with the uptake of essential metals, modification of cell
redox status, and the disruption of proteins and metal thiolate bonds (Huang et al., 2006;
Rezaee et al., 2006). They can cause adverse health issues such as antibiotic resistance,
“biomagnification” of mercury happens at every level of aquatic food chain (Mason et al.,
1996).
Microalgae have the ability to bio-transform acid reducible Hg2+ into elemental Hg0
and metacinnabar (β-HgS) to varying degrees (Kelly et al., 2007). After enzymatic reduction
of Hg2+ to Hg0 catalysed by mercuric reductase, the volatile Hg0 is removed by both
biological and non-biological volatilization and most of the remaining unreduced Hg2+ is
converted into β-HgS. Majority of Hg0 volatilization happens rapidly, within 20 min to few
hours, as shown in microalgae such as Selenastrum minutum, Chlorella fusca var. fusca,
volatilization was light-independent, but depended on metal concentration and cell density
(Devars et al., 2000). Accelerated volatilization was shown in microalgae pretreated with 5
express mercuric reductase (MerA) from Bacillus megaterium B1 in Chlorella sp. DT. The
transgenic strains have improved Hg(II) removal ability, up to two fold compared to control
and experienced a reduced level of oxidative stress (Huang et al., 2006). In addition, other
potential routes of Hg(II) removal are thiol chelation and bio-methylation to methylmercury
23
(MeHg). However, it was reported that unlike other heavy metals, accumulation of mercury
poorly induces phytochelatin synthesis (Devars et al., 2000). Growth photoperiods have
reported to influence the composition of binding ligands and its complexation with Hg. Hg-
binding ligands are more homologous and aromatic in nature at longer light exposure period,
while formation of smaller, more aliphatic Hg-ligand complexes rich in thiols and sulphur
mineralization was used to pretreat Chlorella vulgaris for Hg2+ removal. The mineralized
calcium phosphate mineral layer doped with sulphur atoms. The mineral layer serves as a
protection layer for microalgae from heavy metals poisoning and the microalgae can grow
well in high concentration of mercury up to 100 µg/L with no obvious reduction in lipid
yield. Raw C. vulgaris has the optimal pH of 5.5 for the removal of Hg2+ up to 62.85 %, as
Hg2+ compete with H+ for binding sites at lower pH, while complex formation of (Hg)OH2
at higher pH significantly deterred the binding of Hg2+ with organic functional groups. On
the other hand, the biomimetic mineralized C. vulgaris has enhanced adsorption efficiency
systems for wastewater treatment has gained a lot of attention due to its high efficiency.
Microalgae dynamic membrane formed using C. vulgaris powder was utilized in dynamic
membrane bioreactor for the bioremediation of Hg2+ from synthetic dental wastewater with
the advantages of promoted removal yield as well as reduction in fouling and expensive cost
24
removal efficiency compared to control membrane bioreactor at 300-800 ppb concentrations
The development of a rapid and sensitive biological monitoring technology for heavy
metal pollutants is of utmost importance for the protection of aquatic environment. Other
than significant increase in SOD gene expression levels and activity as well as chlorophyll
a content, the frustule of Halamphora veneta deformed and increased in size when exposed
to mercury. Therefore, SOD gene expression levels and activity, changes in frustule
morphology and chlorophyll a content of Halamphora veneta are promising candidates for
mercury toxicological assessment in aquatic habitats (Mu et al., 2017). Table 5 summarizes
4. CHALLENGES
contamination by other microorganisms, nutrient variability, high content of TSS and high
Table 6 summarizes the issues that could challenge the feasibility of using microalgae-
based biosorbents for heavy metal removal as well as the proposed strategies that could
solve the problems raise when applying this technology. From the information provided in
when it is integrated with other technologies. Still, more powerful microalgal strains should
be isolated and better treatment processes should be developed to further improve the
25
efficiency of heavy metal remediation and to reduce the operation costs. The future
5. FUTURE PROSPECTS
bioremediation, the future prospects of large scale application look promising by taking into
accounts few considerations. Firstly, screening and choosing the suitable microalgae strains
is an important step in bioremediation of heavy metals wastewater. Other than having high
tolerance to heavy metal pollutants with fast and stable growth, it is beneficial if the
microalgae has the following attributes: (i) able to accumulate high content of lipids and
other valuable co-products, (ii) high CO2 sequestration ability and low nutrient requirements,
microorganism species, and (iv) ability to self-flocculate for cost-effective cell harvesting.
for heavy metals biosorption and bioaccumulation by microalgae is also crucial. Recently,
heavy metals removal and recovery have gained much attention because of their potential
techniques as well as integration with other heavy metal removal techniques for microalgae
biomass can help to improve heavy metals removal efficiency. Microalgae biomass
harvesting has always been a challenging task as microalgae are minute in size and their
negatively charged surface keep them in stable dispersed state. Innovation of conventional
26
harvesting technologies and development of new techniques are essential to reduce the
On the other hands, heavy metals have both enhancement and inhibition effect on
Although usually having inhibition effect on microalgae growth, some heavy metals such
as Al, As, Cd Co, Pb, elements from the lanthanide group, metallic nanoparticles and others
microalgae strains as reported in a recent review (Miazek et al., 2015). Similarly, certain
heavy metals also played a positive role in the accumulation of lipids (such as As, Cd, Cu,
Ni), exopolymers (such as Ag, Cd, Co, Cu), pigments (such as As, Cd, Cu, Fe, Ni and Te),
phytochelatin (such as As, Cd, Cu, Pb) and phytohormones (such as Cd, Cu, Pb) due to the
inducing effect by metal stress. In particular, heavy metal stress can be exploited to modify
microalgal fatty acids composition in order to produce biodiesel with desirable properties
and quality (Miazek et al., 2015). However, the presence of heavy metals might interfere
with downstream processing of these valuable products. Therefore, more research work
6. CONCLUSIONS
proteins and peptides are responsible for metal-binding. Mechanisms such as extracellular
of heavy metals. More efforts in the areas of genetic engineering, immobilization techniques,
27
pretreatment strategies and integration with other technologies are required to fully explore
Acknowledgements:
Ministry of Science and Technology under grant number MOST 109-3116-F-006 -016 -
28
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Figure 1. Mechanism of heavy metals removal by microalgae
43
Table 1. Performance of biosorption of arsenic (As) by different microalgae strains
Scenedesmus
- 9.5 12 1 180 5.0 41.7
almeriensis
44
Table 2. Performance of biosorption of cadmium (Cd) by different microalgae strains
Microalgae Temp (°C) Optimal pH Initial metal Biomass conc. Time (min) Max. sorption Removal Reference
strains conc. (mg/L) (g/L) (mg/g) efficiency (%)
45
Table 3. Performance of biosorption of chromium (Cr(VI)) by different microalgae strains
46
Scenedesmus 25 6 for Cr(III) 100 2 120 - 98.3 for (Shokri
quadricauda Cr(III) Khoubestani et
1 for Cr(VI) al., 2015)
47.6 for
Cr(VI)
Scenedesmus 22 2 10 2 240 - 100 (Daneshvar et
quadricauda al., 2019)
biochar
Rhizoclonium - 2 1000 1 45 67.3 6.7 (Kayalvizhi et
hookeri al., 2015)
47
Table 4. Performance of biosorption of lead (Pb) by different microalgae strains
48
Table 5. Performance of biosorption of mercury (Hg) by different microalgae strains
49
Table 6: Challenges and proposed strategies of heavy metal removal by microalgae
50
Yoong Kit Leong: Investigation, Writing- Original draft preparation; Jo-Shu Chang: Supervision, Conceptualization, Writing- Reviewing and Editing
Highlights
Challenges and proposed strategies were summarized along with future prospects.
Declaration of interests
☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the
work reported in this paper.
☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:
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