Journal of Environmental Chemical Engineering 11 (2023) 109943

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Journal of Environmental Chemical Engineering

journal homepage: www.elsevier.com/locate/jece

Symbiosis of microalgae and bacteria consortium for heavy metal

remediation in wastewater
Dehua Zhao a, Wai Yan Cheah b, *, Sai Hin Lai a, *, Eng-Poh Ng c, Kuan Shiong Khoo d, e,
Pau Loke Show f, Tau Chuan Ling g
a
Department of Civil Engineering, Faculty of Engineering, Universiti Malaya, Kuala Lumpur 50603, Malaysia
b
Centre for Research in Development, Social and Environment (SEEDS) Faculty of Social Sciences and Humanities, Universiti Kebangsaan Malaysia, UKM, Bangi 43600,
Selangor Darul Ehsan, Malaysia
c
School of Chemical Sciences, Universiti Sains Malaysia, USM, Penang 11800, Malaysia
d
Department of Chemical Engineering and Materials Science, Yuan Ze University, Taoyuan, Taiwan, ROC
e
Department of Biotechnology, Saveetha School of Engineering, Saveetha Institute of Medical and Technical Sciences, Chennai 602105, India
f
Department of Chemical Engineering, Khalifa University, P.O. Box 127788, Abu Dhabi, United Arab Emirates
g
Institute of Biological Sciences, Faculty of Science, Universiti Malaya, Kuala Lumpur 50603, Malaysia

A R T I C L E I N F O A B S T R A C T

Editor: Yujie Men Heavy metals in industrial wastewater are hazardous, not easily biodegradable, and can be enriched in the food
chain. This will lead to serious global environmental problems. Traditional physicochemical heavy metal
Keywords: remediation treatments have limitations, including high costs and secondary contamination. However, bio­
Adsorption sorption is an effective and affordable way for treating wastewater containing heavy metals. A large specific
Bioremediation
surface area of microorganisms makes them attractive as biosorbents for the removal of heavy metals. In
Heavy Metal
particular, more benefits exist for heavy metal adsorbents when microalgae and bacteria are combined. The
Microalgae-bacteria consortium
Wastewater treatment combined system biological adsorption method of microalgae and bacteria is an ideal method for the remediation
of large volume and low concentration heavy metal wastewater. The reuse of biological biomass of algae and
bacteria resources can also be achieved. Therefore, it has very promising application prospects. This present
review aimed to discuss the removal of heavy metals from wastewater using presently applied conventional
treatments followed by the treatment using consortia of microalgae-bacteria, modes of microalgae-bacteria
consortia system, the advantages of microalgae-bacterial consortia as biosorbents, the mechanisms of bio­
sorption for heavy metals and the factors affecting the biosorption efficiency of heavy metals. Moreover, the
feasibility of industrial applications and the potential product applications of harvested microalgae-bacterial
consortia were also discussed. This review is foreseen to bring significance to industrial stakeholders
including engineers, environmental technologists and business entities in developing and investing in more
effective ways of bioremediating heavy metals from wastewater, for overall environmental sustainability.

1. Introduction environmental pollution in industrial and mining areas, particularly in

In recent years, industrial development and social progress have led
to increasing heavy metal pollution of water systems. The increasing
amount of heavy metals used in industrial production activities has led
to an increasing discharge of waste containing heavy metals. This has
caused environmental pollution problems, affecting the biotic life in the
receiving water bodies. Heavy metals released by numerous industrial
activities, including mining, chemical processing, leather
manufacturing, and electroplating, have led to significant
Asia. Heavy metals are among the most ecologically hazardous pollut­
ants due to their persistence and limited biodegradation. This results in
long-term contamination and potential adverse health impacts [1,2].
Heavy metal pollution events have occurred frequently, posing a threat
to human health and the ecological environment with excessive cad­
mium in rice, methylmercury in aquatic products, and even children’s
blood lead concentrations [3,4]. The Cd, Cr, and Pb atmospheric emis­
sions have found increased from 31.14 tonnes, 1019.07 tonnes, and
2671.73 tonnes in 1980–261.52 tonnes, 8593.35 tonnes, and 12,561.77

* Corresponding authors.
E-mail addresses: cheahwaiyan@ukm.edu.my (W.Y. Cheah), laish@um.edu.my (S.H. Lai).

https://doi.org/10.1016/j.jece.2023.109943
Received 17 January 2023; Received in revised form 31 March 2023; Accepted 15 April 2023
Available online 17 April 2023
2213-3437/© 2023 Elsevier Ltd. All rights reserved.
D. Zhao et al.
tonnes in 2008, respectively [5]. In addition, heavy metal pollution in
the aquatic environment is also of concern. Heavy metal is brought
together into the groundwater, lakes, and oceans by surface runoff
processes, and then it enters the plants and animals through the
enrichment effect of the food chain [3]. After entering the organisms,
heavy metals react with body components such as proteins, fatty acids or
amino acids to form organic acid salts and chelates. In addition, they can
react with inorganic carbonate and phosphate to form inorganic metal
salts, which will be causing human physiological health problems. As a
result, efficient metallic wastewater treatment has emerged as a critical
study issue in the realm of environmental protection [3].
Current methods mainly focus on chemical precipitation, ion ex­
change, electrochemical treatment, reverse osmosis, membrane tech­
nology, electro-dialysis, and activated carbon adsorption [6]. These
methods achieve a relatively desirable performance at heavy metal
treatment but the drawback is the by-product generation that is difficult
to reprocess after treatment might probably cause secondary pollution.
Moreover, when treating low-concentration heavy metal wastewater,
the removal rate is low and the operation expense is high. Chemical
methods incur high chemical costs and subsequently higher energy
consumption. Moreover, most of these treatment techniques are envi­
ronmentally destructive and less efficient and have operational limita­
tions and high costs, all of which limit their application [7]. For
example, the activated carbon adsorption method only has a good
adsorption effect on certain types of heavy metals [7]. The chemical
electrolysis method is only suitable for the remediation of wastewater
with low concentrations of heavy metal, and it is difficult to reduce the
heavy metal to an ideal concentration range. The ion exchange method
and membrane biotechnology method have ideal treatment effects on
heavy metal wastewater, but due to the influence of solution tempera­
ture and pH value, the control cost is high, which is difficult to be
applied in the practical industry [8,9]. Therefore, the large-scale ap­
plications of conventional heavy metal treatment methods are limited by
multifaceted aspects. This would cause difficulty for industries to meet
the increasingly stringent discharge criteria of industrial wastewater
according to the US Environmental Protection Agency’s (USEPA
1974–2021) standards, which for instance the effluent limitations for
heavy metals in wastewater of common electroplating are respectively,
0.7 mg L− 1 for Cd, 4.0 mg L− 1 for Cr, 2.7 mg L− 1 for Cu, 0.4 mg L− 1 for
Pb, 2.6 mg L− 1 for Ni, 0.7 mg L− 1 for Ag, 2.6 mg L− 1 for Zn.
The biosorption method is an emerging method for treating waste­
water containing heavy metals. Biosorption can be divided into (i)
extracellular enrichment precipitation (ii) cell surface adsorption pre­
cipitation (iii) intracellular enrichment depending on the manner of de-
shield metal ions in solution. Special chemical structures and biological
compositions of some organisms are applied to adsorb dissolved heavy
metals from wastewater [10]. Microalgae-bacteria consortium bio­
sorption has shown its potential in removing heavy metals and recov­
ering valuable metals. The recovered valuable metals offer broad
development potential, high commercial value, and great social benefits
[11]. A consortium of microalgae-bacteria has symbiotically beneficial
properties. Microalgae take up carbon dioxide by photosynthesis and
convert inorganic into organic while releasing oxygen.
Oxygen-consuming bacteria consume both oxygen and organics,
releasing carbon dioxide. Both of these depend on one another to ach­
ieve symbiosis to form a consortium. Microalgae and bacteria are
characterized by small size, large specific surface area, vigorous growth
and metabolism, high reproductive capacity, high biological activity,
high adsorption capacity, environmental adaptability, ubiquitous in the
water environment, inexpensiveness and easy availability. The source of
species is wide and can be obtained and screened almost from any car­
rier material, especially from areas contaminated with heavy metals.
Therefore, these characteristics make them more advantageous as bio­
sorbents. Their superior performance in treating wastewater with a low
concentration of heavy metals and a large amount of wastewater is
especially outstanding. Especially, using microalgae and bacteria
2
Journal of Environmental Chemical Engineering 11 (2023) 109943
treatments for heavy metals have the advantages of a high removal rate,
fast reaction rate, easy regeneration, no secondary pollution and simple
operation [12]. In addition, at low concentrations, selective removal of
specific metal ions of this method is possible and the treatment is highly
efficient with efficient recovery of some precious metals, and small in­
vestments with low operating expenses [13]. Consequently,
microalgae-bacteria consortia have higher metabolic efficiency and
higher adsorption capacity for substances in the environment [14,15].
However, despite its advantages, there are some drawbacks to consider.
Microalgae-bacteria consortia for heavy metal removal involve a com­
plex interaction between different microorganisms and the physical and
chemical environment. Therefore, understanding the mechanism of
heavy metal removal and optimizing the process can be challenging.
This requires significant research efforts and expertise, which limits the
applicability of the technology to specialized research and industrial
settings. Overall, the microalgae-bacteria consortium is among the most
promising technologies for removing heavy metals from wastewater
because of its high efficiency and sustainability.
Although several successful results were published [16,17], there are
still knowledge gaps present on heavy metal treatment by
microalga-bacteria consortia including the interrelationships, the
metabolic mechanisms, and the roles played by each are unclear. In
addition, the influencing factors for effective biosorption performance of
microalgae-bacteria consortia including temperature, pH, light in­
tensity, coexisting ions, and microbial pretreatment, are also not well
defined. Therefore, this article aims to discuss the present applied con­
ventional treatment followed by the treatment using consortia, modes of
microalgae-bacteria consortium system, and subsequently the advan­
tages of treating heavy metals by microalgae-bacteria consortia, as well
as the adsorption mechanism and optimal parameters, industrial appli­
cation feasibility and the potential utilization value of algal biomass.
Finally, the improvement of wastewater treatment by algal symbiotic
systems is suggested and future research directions are also put forward.
2. Treatment of heavy metals from industrial wastewater
2.1. Conventional treatment: Physical, chemical and biological methods
There are three main conventional wastewater treatment methods
for heavy metal removal. The first method enables the heavy metals in
wastewater to be adsorbed, concentrated, and separated under condi­
tions that do not change their chemical morphology, including adsorp­
tion, solvent extraction, ion exchange and other methods [18]. The
second approach involves removing heavy metals from wastewater by
causing chemical reactions, including neutralization precipitation
method, sulfide precipitation method, ferrite co-precipitation method,
chemical reduction method, electrochemical reduction method and high
molecular heavy metal trap method [19]. The third method is to remove
heavy metals from wastewater with the help of flocculation, absorption
accumulation, enrichment and other effects of microorganisms or
plants, such as bioflocculation, biosorption, phytoremediation and other
methods [20]. Given the complex composition of heavy metal waste­
water, the treatment compliance requirements are very strict, and con­
ventional wastewater treatment technologies each have advantages and
disadvantages, as shown in the following Table 1.
Hadi et al. [21] adopted the hydroxylation technology, which can
effectively functionalize the surface of aluminosilicates from waste
sources, and treat heavy metals by ion exchange technology. The func­
tionalized materials have exhibited high absorption capacity of
aluminum Silicate but the operation cost is high. Similarly, Krystynik
et al. [22] operated a continuous pilot-scale device in a polluted in­
dustrial site and found that the removal rate of Cr6+ by this process was
over 95%, confirming that the electro-flocculation process has certain
prospects in the actual industrial treatment of wastewater containing
heavy metals. However, during the operation of the device, the cathode
is passivated, the anode is consumed, and the electrode needs to be
D. Zhao et al. Journal of Environmental Chemical Engineering 11 (2023) 109943

Table 1
Comparison of conventional treatment methods of heavy metals in wastewater.
Method Raw material Principle Advantage Disadvantage Reference

Neutralization CaO Generate hydroxide or carbonate It is easy to operate, has a mature The consumption of [26]
precipitation Ca(OH)2 precipitation and solid-liquid separation process, a small investment, and has neutralizer is large, the
method NaOH a wide range of neutralizer sources operation is time-
consuming and easy to
secondary pollution
Sulfide Na2S Sulfide precipitation and solid-liquid The treatment is effective, and the The operation is [27]
precipitation NaHS separation sediment has low water content and troublesome and the
method H2S, FeS is not easy to dissolve, without curing agent is expensive
secondary contamination
Ferrite FeSO4 or iron filings Ferrite precipitation and solid-liquid Ferrite sedimentation properties are No separate recovery of [28,29]
precipitation with FeCl3 separation good and exploitable heavy metal resources,
method acid and alkali
consumption
Barium salt BaCl2 Solid-liquid separation of barium chromate The effect of treating Cr6+ is good If the treated effluent [30]
precipitation BaCO3 precipitation contains toxic barium ions,
method gypsum must be used to
remove barium
Reducing method Na2SO3 Reduction of Cr6+ to Cr3+ and re- The utility model has the advantages Large amount of reducing [31]
with low-valent Na2S2O3 neutralization or chemical precipitation of convenient use, easy operation and agent and a small amount
sulfide NaHSO3 less sludge of wastewater treatment
FeSO4 FeSO4 FeSO4 reduces Cr6+ to Easy to use and operate Large amount of reducing [32,33]
reduction Cr3+forreneutralization or chemical agent, a small amount of
method precipitation wastewater treatment and
a large amount of slag
Iron powder Iron powder Reduce Cr6+ to Cr3+, solidify Cu2+, Ni2+and Iron powder comes from a wide Small amount of [34]
method then neutralize or precipitate range of sources, which can treat wastewater treatment and
waste with waste. It is easy to use and a large amount of slag
operate
Hydrazine hydrate N2H4⋅H2O N2H4⋅H2O reduces Cr6+ to Cr3+for Mature process, simple operation and High processing cost [35]
reduction reneutralization or chemical precipitation less sludge
method
Electrolytic Iron panels, iron chips Electrolysis produces Fe2+, reduces Cr6+ to After treatment, the water quality is Generate a large amount of [36]
method and NaCI Cr3+, pH rises, and heavy metal form stable, the operation process is sludge and consume
hydroxides simple, and the equipment design has electricity
mature experience
Ion air float Ionic aerosols Ion floatation agent forms precipitation with The treatment of diluted The treated effluent [37]
method heavy metals and then adheres to bubbles for electroplating wastewater has the contains salt, high oil and
separation advantages of low residual difficult to reuse water
concentration of metal ions, fast resources
operation speed, less land occupation
and strong adaptability
Foam air float Foam air floaters The foam floatation agent forms the The treatment of dilute The treated effluent [38]
sediment air surface-active agent complexion with heavy metals, and then electroplating wastewater has the contains salt, high oil and
float Precipitant adheres to the bubbles to form chemical advantages of low residual difficult to reuse water
precipitation, and then separates through the concentration of metal ions, fast resources
surfactant bridge or directly adheres to the operation speed, less land occupation
bubble and strong adaptability
Ion exchange Ion exchange resins, Ion exchange and heavy metal exchange on Large treatment capacity, good Frequent regeneration, [39]
method acid or base ion exchange resin effluent quality, recyclable water and complex, second pollution
regenerant heavy metal resources and high operation cost
Reverse osmosis Semipermeable Water is permeated, heavy metals cannot be It can reuse water resources, compact The membrane has a short [40]
method membrane permeated, and then electroplating equipment and energy consumption service life, small
wastewater is concentrated wastewater treatment
capacity and limited
concentration ratio
Electrodialysis Cation anion The electroplating wastewater is The equipment is not compact and High pretreatment [41,42]
method permeable membrane concentrated and desalinated by cation easy to operate requirements, high
permeation of cationic membrane and anion membrane quality
permeation of anionic membrane requirements and a limited
concentration ratio
Adsorption Adsorbents (activated The active surface of the adsorbent directly Convenient operation and good The adsorbent has a short [43]
method carbon, zeolite, etc.) attracts heavy metals treatment effect service life, difficult
regeneration and difficult
reuse of heavy metal
resources
Liquid Organic solvent, The mobile carrier complex and deconjugate The process equipment is simple, the Poor stability of the liquid [44]
membrane surfactant, internal with heavy metals to enrich heavy metals in separation speed is fast and the film
method phase solution, mobile the inner phase solution selectivity is high
carrier
Solvent extraction Extractant The solubility of heavy metals in the aqueous It is easy to operate and can reuse Extractants are expensive [45]
method phase and extraction phase is different, but valuable heavy metals
they are concentrated in the extraction phase

3
D. Zhao et al.
replaced regularly, which makes the cost high and the processing pro­
cess cumbersome. Kumar and Pakshirajan [23] used sulfide precipita­
tion to remove Cd2+, Cu2+, Zn2+, and Pb2+ in synthetic wastewater, and
found that the removal rate of each ion was higher than 95%. The
precipitation method overcomes the lack of selectivity of the hydroxide
precipitation treatment for the removal of heavy metals in wastewater,
but the heavy metal sulfide precipitation particles are small (at the
nanometer level), easy to form colloids, and difficult to perform the
solid-liquid separation. Moosavirad et al. [24] used ion exchange for
heavy metal remediation of industrial wastewater. In the study, they
chose Dowex 50WX8(H+) resin was used as an adsorbent. The experi­
ment found that the adsorption effect of the resin was better when the
pH value was 4–6, the flow rate was 4 mL⋅min− 1 and the resin amount
was 200 mg. The advantage of the ion exchange method is to restore the
utilization value of metals. Moreover, the purity of the recovered metal
is high, and the amount of sludge produced is small and can be met
emission specifications. This method requires elution and regeneration,
and complex technology, easy to produce high concentration eluent,
resulting in secondary pollution. Chen et al. [25] added lime to a single
solution of Zn2+, Cu2+, and Pb2+ with a 100 mg L− 1 initial concentra­
tion. The experiment found that lime was quite effective in removing
Zn2+ and Cu2+, and the removal rate could be as high as 99.65% and
99.99%. Due to the continuous addition of alkaline precipitant, the pH
of the wastewater increased, resulting in the dissolution of Pb(OH)2 into
the solution, and the removal efficiency of Pb2+ was as low as 76.14%. It
showed that adding alkaline precipitant to wastewater has certain
selectivity to remove heavy metals, which is limited in practical appli­
cation. To sum up, the conventional heavy metal treatment has many
shortcomings, potentially causing secondary pollution, complicated
procedure, energy-intensive, and high cost. Therefore, a more
economical and effective way to treat heavy metals in wastewater is
required.
2.2. Symbiosis of microalgae-bacteria consortium
Microalgae and bacteria are widely occurring biological species in
natural water bodies and they are essential for boosting the water en­
vironment’s material cycle and preserving the ecological equilibrium in
the aquatic environment. However, a complex relationship exists be­
tween microalgae and bacteria. Microalgae and bacteria secrete extra­
cellular products like secondary metabolites into their surroundings
during growth and it is through these extracellular products that they
influence each other [46]. The action outcomes of extracellular products
can be split into two categories either performing a positive function in
promoting or a negative function in inhibiting growth. Extracellular
compounds released by bacteria that are advantageous to microalgae
include vitamin-like substances, enzymes that can break down organic
materials and glycopeptides that can enhance microalgae development.
Besides, bacteria also secrete proteins and enzymes which are toxical or
inhibitory to microalgae. The extracellular secretions of microalgae are
predominantly amino acids, which may boost the development of bac­
teria, whereas the extracellular products that inhibit bacteria are certain
antibiotic-like compounds [47]. According to one study, co-cultivation
of microalgae and bacteria can be used in the palm oil mill effluent
(POME) treatment facility. This enables enough biomass and lipid yields
for biofuel generation, and also efficient wastewater bioremediation.
C. sorokiniana CY-1 produced the most lipids when co-cultured with
Pseudomonas sp. at a ratio of 1:1 in non-pretreatment POME, and also
conclude that CY-1 has a reciprocal interaction with Pseudomonas sp.
rather than parasitism [48].
Ecosystems are in relative equilibrium, and the ecological niches of
each species do not overlap in principle. Competition between species
arises when the ecological niches of different species of organisms in an
ecosystem coincide under specific conditions [49]. For example,
microalgae are capable of photosynthesis under light conditions,
absorbing CO2 to produce oxygen but both perform respiration in the
4
Journal of Environmental Chemical Engineering 11 (2023) 109943
dark which will lead to microalgae and bacteria competing for oxygen.
In addition, they also compete for nutrients like nitrogen and phos­
phorus. Nutrient salts like nitrogen and phosphorus are important raw
materials for the production of organic matter. When certain nutrient
salts in water bodies are low, microalgae and bacteria compete for these
nutrients [50].
The interactions between microalgae and bacteria are considerably
symbiotic, and they may inhibit each other as a result of rivalry for
nutrition or may exploit each other with facilitation or even rely on one
another to create a sophisticated symbiotic system as shown in Fig. 1
Microalgae and bacteria capable of forming symbiotic systems are often
complimentary with regard to metabolic activity, particularly with re­
gard to the release and consumption of oxygen and nutrients. Micro­
algae can transform CO2 into O2 through photosynthesis when exposed
to light and bacteria can convert O2 into CO2 to complete respiration. In
terms of nutrient metabolism, microalgae produce organic compounds
by ingesting inorganic nutrients like nitrogen and phosphorus. Both
dead algal cell bodies and organic material generated by algae may be
broken down and used by bacteria, and conversely, bacterial metabo­
lites can be absorbed and used by microalgae [50]. Microalgae and
bacteria can also release enzymatic substances to the periphery during
their growth, such as glucoxigenase, lactoxygenase, phosphatase, hep­
aranase and lipase. These extracellular enzymes mainly break down
polysaccharides and proteins by hydrolysis, so that they can turn into
small molecules that can pass through the cytoplasmic membrane.
Co-culture of Pseudomonas diminuta and Pseudomonas vesicularis, with
algae, could promote the growth of Scenedesmus obliquus and Chlorella
sp., but the bacteria were not found to secrete any material that pro­
moted the growth of microalgae [51]. Some algae can form a tight
exo-symbiosis with bacteria that have some specific functions, such as
Aburai et al. [52] used electron microscopy to look at nitrogen-fixing
bacteria and found that nitrogen-fixing bacteria consistently stay near
the surface of microalgae. This finding showed that C and N fixation by
the microalga and bacterium happened under aerobic circumstances,
and that the microorganisms were able to proliferate despite nutritional
deficits by self-supplying nutrients. These show that the
microalgae-bacteria consortium can form a complex and stable symbi­
otic system.
The microalgae-bacteria symbiosis system can be applied to a more
sustainable wastewater treatment approach, as a low energy input is
required as oxygen is produced via microalgal photosynthesis. The
microalgal biomass produced in this system can be utilized for energy
recovery, including biofuel production, and subsequent wastewater
treatment [53]. Under the microalgae-bacteria symbiosis system, the
production of oxygen and organics by microalgal cells through
Fig. 1. The symbiotic relationship between microalgae and bacteria.
D. Zhao et al.
photosynthesis can accelerate bacterial metabolism. Meanwhile, the
CO2 produced by bacteria through respiration can act as a carbon source
for utilization by microalgal cells [54]. Through the interaction between
microalgal and bacteria cells, it is not only beneficial to the development
of microalgal cells and bacteria each, while improving the wastewater
treatment efficacy and strengthening the removal of heavy metals and
pollutants [55]. In addition, CO2 produced by bacteria could be
metabolized to organic matter and utilized by microalgae, so the global
greenhouse effect due to the emission of CO2 can be reduced. The
symbiotic system of algae-bacteria contains the symbiotically advanta­
geous symbiotic interaction of symbiotic use of metabolites and sym­
biotic competition and suppression of nutrients, so that the whole
system can achieve a dynamic balance. Therefore, combined treatment
of heavy metals from wastewater by microalgae-bacteria consortium is
considerably a greener, more environmentally friendly and
pollution-free treatment process.
2.3. Modes of microalgae-bacteria consortium in wastewater remediation
2.3.1. Suspended algae-bacteria system
The attachment of bacteria to the surface of algal cells during the
growing phase of the suspended algal consortium system supports the
flocculation of the algal cells and enhances the performance of the algal
consortium during sedimentation. Typical suspended microalgae-
bacteria consortium systems are available in high-rate algal ponds
(HRAP) and activated sludge/algae (ASA) [56,57]. HRAP is a complex
ecosystem formed by the addition of microorganisms such as microalgae
and bacteria to traditional bio-stable ponds. ASA system involves algae
and activated sludge, and combines the two to deal with wastewater
synergistically. The use of artificial intensive cultivation of high con­
centrations of algae is cultured with activated sludge for effective floc­
culation and precipitation. Treatment of wastewater by suspended algal
systems can achieve better results, however, aggregated microorganisms
may resuspend because of sediment attributes like shear pressure, bac­
terial attachments and flow rate. This can result in poor water quality,
and its removal efficiency still depends on algae natural development
and semi-artificial techniques of management. Light exposure, biomass,
and hydraulic retention time are still factors that hinder algal growth
[58]. Despite the fact that the suspended algae-bacteria system settled
satisfactorily, periodic mud drainage is required for ASA and the treat­
ment effect is unstable leading to many limitations in practical
applications.
2.3.2. Immobilized algae-bacteria system
Cell immobilization is a technique in which microalgae and bacteria
are immobilized on specific support at a certain ratio, which uses the
synergistic effect between the bacteria to improve the biomass per unit
area and facilitate the harvesting of microalgae at the same time. The
common support compounds are calcium alginate, carrageenan, agar
polyacrylamide [59]. The immobilized algae-bacteria system provides
effective biomass harvesting, as well as the immobilization technique
improves the wastewater treatment efficiency by the
microalgae-bacteria consortium system, but there are still many draw­
backs in the application process. For instance, the entrapment matrix of
immobilized support materials may hinder the delivery of metabolites,
oxygen and carbon dioxide between microalgae and bacteria. In addi­
tion, degradation may occur with the prolonged use of culture substrates
and toxic hazardous substances can be generated, which can affect the
normal metabolism of the consortium and it is difficult as well to find a
non-toxic, transparent, porous, resistant to bacterial decomposition,
robust and stable carrier that does not dissolve in the wastewater [58].
2.3.3. Microalgae-bacteria biofilm system
Bacterial and microalgal biofilm technology was developed based on
immobilized bacteria and microalgal technology [60]. Microalgae can
easily attach to the surface of the support while cultivating under
5
Journal of Environmental Chemical Engineering 11 (2023) 109943
specific conditions, the density of microalgae in the domesticated
forming bacterial and microalgal biofilm system. It was characterized by
the stable efficacy of denitrification and better treatment than the
common suspended alga system. The symbiotically attached bacterial
and microalgal communities grow on solid support easily forming
photosynthetic biofilms. They form a stable symbiotic relationship with
each other within the biofilm system. Photosynthetic biofilms vary in
composition and structure based on abiotic and biotic elements in the
environment. During the biofilm generation and development phase,
microalgae control the rate of extracellular polymer (EPS) synthesis by
raising or lowering the expression of particular initiators, which in turn
will respond to environmental changes. Shen et al. [61] showed that
increasing the nutrient concentration, especially the nitrogen concen­
tration, could increase EPS production in diatoms and green algae. In
addition, temperature fluctuation and mineral (Ca2+) buildup may also
alter EPS generation by algae. The maturation of bacterial and micro­
algal biofilms determines the succession of species present, e.g., regu­
lating the amount and ratio of EPS, algae, and bacteria [62,63].
There are several major processes involved in the biofilm formation
and creation of microalgae and bacteria. In the initial stage of formation
in bacterial and microalgal biofilms, also known as (i) the solid carrier
surface regulation stage, in which extracellular polymers secreted by
cells attach to solid carriers, bacteria start to grow. At that which stage
biofilms contain a higher proportion of EPS and bacteria while cyano­
bacteria and algae are relatively less. Subsequently, (ii) the early growth
stage of photosynthetic biofilms, in which various types of microalgae
start to attach to the EPS matrix on the surface of solid supports for
growth. During (iii) the development phase of photosynthetic biofilms,
algal cells grow rapidly, forming a symbiotic microenvironment with
bacteria in the EPS matrix. If nutrients are abundant in the culture
medium, photosynthetic biofilms will progress to (iv) the mature stage
with more abundant algal cells, bacteria, and nutrients in the EPS matrix
[64,65].
Hydraulic algal beds are typical of bacterial and microalgal biofilm
systems. Hydraulic algal bed systems, in which filamentous algae, sus­
pended microalgae and bacteria are attached in oblique water channels
for heavy metal remediation. Chavan and Mukherji [66] reported the
inoculation of microalgae and bacteria on a rotating biological contactor
(RBC) for the treatment of diesel wastewater using the formed bacterial
and microalgal biofilms. Wang and Higgins [67] applied the symbiosis
principle of microalgae and bacteria, developed tubular bacteria and
microalgal biofilm photobioreactor with Chlorella sorokiniana and acti­
vated sludge for water treatment. A high concentration of ammonia
nitrogen diffused from each side of the membrane, meanwhile achieving
high efficiency of nitrification by nitrifying bacteria and photosynthesis
of microalgae. There are certain advantages of bacterial and microalgal
biofilm systems in treating wastewater, including lower cost and over­
coming the shortcomings of water in suspended microalgae and bacteria
systems. Further, it is easy to form a biofilm and the dominant species
and algae are not easy to flow. EPS released by microalgae and bacteria
during biofilm development might offer a buffered microenvironment
for bacteria and microalgal symbionts which can sustain high activity in
challenging conditions and continually remove contaminants such as
heavy metals from sewage [54]. However, biofilms are easy to shed, and
external factors such as light exposure and hydraulic flow rate need to be
comprehensively considered when designing and operating reactors to
control the microbial attenuation coefficient of biofilms. Several types of
wastewater treatment by microalgae-bacteria consortium systems and
some applications are shown in microalage-bacteria consortium for
heavy metal removal summarised in Table 2.
2.4. Advantage of biosorption in Microalgae-bacteria consortium
Based on our recent literature research, there is a very serious lack of
available studies involving the treatment of heavy metals from waste­
water using the microalgae-bacteria consortium. Table 3 summarises
D. Zhao et al. Journal of Environmental Chemical Engineering 11 (2023) 109943

Table 2
Microalgae-bacteria symbiotic systems used for wastewater treatment.
Type Application Advantage Disadvantage References

Suspended Active algal system Compared with the traditional biological treatment The settled bacteria and algae are easy to be resuspended [68]
bacteria algae High-efficiency Algae method, the treatment effect is better. The settled by external interference, affecting the effluent quality. At
system Pond bacteria and algae are easy to be resuspended by the same time, it needs reflux and sludge discharge. The
external interference, which has good flocculation and dominant bacteria and algae are easy to lose and the
sedimentation characteristics and is easy to settle treatment effect is unstable
Immobilized Fluidized bed The solid-liquid separation effect is good, the problem of The embedded matrix may hinder the transmission of [69]
bacteria -algae photobioreactor difficult separation between suspended algae cells and bacterial and Algal Metabolites, oxygen and carbon
system system treated effluent is solved, the biomass per unit area is dioxide. In addition, the matrix will degrade and produce
improved, the dominant bacteria and algae are not easy toxic substances after long-term use, which will alter the
to lose, and the sewage treatment effect is good regular metabolism of bacteria and algae. The
immobilization cost is significant, and it is challenging to
develop a non-toxic, transparent, porous and stable
carrier that is not dissolved in the treatment medium or is
not easy to be biodegraded
Bacteria algae Hydraulic algal bed Taking advantage of the easy attachment characteristics There is a problem that biofilm falls off the carrier. When [70]
biofilm system Tubular bacteria of bacteria and microalgae, they are easy to form constructing and running the reactor, factors such as light
algae biofilm reactor photosynthetic biofilm on the carrier surface, the and water flow rate should be comprehensively studied to
Biological turntable dominant bacteria and algae are not easy to lose, and the control the proliferation, attenuation and balance of
cost is low biofilm

some examples of heavy metal treatment by microalgae-bacteria con­
sortia. The current study showed how innovative algal-bacterial AGS
can be used to remove Cr(VI) and decontaminate the environment. Cr
(VI) biosorption by algal-bacterial AGS was studied for Cr(VI) reduction
and total Cr removal, with a maximum Cr(VI) reduction rate of 99.3% at
pH 2 after 6 h of biosorption, and the highest total Cr removal rate of
89.1% at pH 6. The loaded Cr in algal-bacterial AGS was fully in the type
of Cr(III), with internal accumulation accounting for 66.8%, showing
that intracellular accumulation outpaced total Cr elimination[71]. The
microalgae-bacteria consortium showed high adsorption efficiency for
Cr.
For Cr(VI) removal, Yang et al. [72] compared the efficacy of
algal-bacterial aerobic granular sludge (AGS) as a biosorbent. Batch
testing demonstrated that Cr(VI) removal from algal-bacterial AGS was
pH sensitive, with a maximum Cr(VI) removal rate of 51.0 mg g− 1 at pH
2. Biosorption and bioreduction processes were discovered to be
involved in Cr(VI) remediation. Furthermore, desorption studies
revealed that NaHCO3 could recover 64–73% of the adsorbed Cr, with
the majority in the form of Cr (III). Algal-bacterial AGS showed greater
biosorption capability and granular stability than standard bacterial
AGS, meaning that algal-bacterial AGS would be more beneficial for the
remediation of Cr(VI) wastewater [72].
Munoz et al. [73] investigated the microalgae-bacteria consortium
for the remediation of Cd(II), Ni(II), Cu(II), and Zn(II)-containing
wastewater, demonstrating that heavy metals were first readily adsor­
bed by cell surfaces in the algae-bacteria combination, followed by a
delayed period of metabolically driven absorption. A study on the
removal of pollutants from industrial wastewater by a
microalgae-bacteria consortium shows that BOD was removed up to
97%, COD up to 51%, oil spills up to 96%, phenols up to 85%, anionic
surface active chemicals up to 73%, zinc up to 90%, manganese up to
70%, iron up to 64%, copper up to 62%, and nickel up to 62% [74].
2.5. Comparison of the effectiveness of microalgae and consortium
systems
Pure microalgae systems have been found to have limited efficiency
in heavy metal removal due to several factors such as low biomass
concentration, slow growth rates, and limited tolerance to heavy metal
toxicity. In contrast, microalgae-bacteria consortium systems exhibit a
higher heavy metal removal efficiency due to the synergistic relation­
ship between the two organisms [76,77].
Several studies have reported the higher efficiency of microalgae-
bacteria consortium systems in the removal of various heavy metals,
including Cr, Cd, Cu, and Zn. For instance, a study by Tangahu et al. [78]
showed that a consortium of Chlorella vulgaris and Azotobacter S8. was
more efficient in the removal of chromium than the control group. A
co-culture of Chlorella vulgaris and Enterobacter sp. for heavy metals
remediation from textile wastewater has demonstrated the importance
of microalgae associated bacteria in bioremediation processes. The
presence of the bacteria stimulated microalga growth which resulted in
a reduction of Cu, Cr, Cd, and Pb by over 70%. Another study has also
found that Enterobacter sp. inoculum increased the effectiveness of the
removal of Chlorella vulgaris microalgae biomass was stimulated by
bacterial inoculation owing to the growth promoting characteristics of
Enterobacter sp. [79].
Overall, the efficiency comparison between pure microalgae and
microalgae-bacteria consortium systems for heavy metal removal shows
that the latter is generally more effective. The synergistic relationship
between microalgae and bacteria enhances the heavy metal removal
efficiency by detoxifying heavy metals or transforming them into less
toxic forms. Additionally, the higher growth rate and biomass concen­
tration of the consortium increases the overall heavy metal removal
efficiency [77].
2.6. Mechanisms of microalgae-bacteria consortium in wastewater
remediation
The complexity of microbial structure and the difference in affinity
between the microorganism and different heavy metals determine that
the mechanism of microbial heavy metal adsorption is complicated.
According to current research on biosorption, some explanations for the
mechanism of biosorption are as follows: the biosorption mechanism can
be divided into metabolism dependent and metabolism independent,
which is an active mode of action and a passive mode of action, ac­
cording to the degree to which cells rely on metabolism [11]. Relying on
metabolism for adsorption is only applicable to living cells of living
organisms. The pathway by which heavy metals are biosorbed is
generally through metabolism to penetrate the cell membrane into
intracellular enrichment. Living cells have a flocculation mechanism so
the heavy metals can be eliminated from the solution by the way of
precipitation. This process is often accompanied by the consumption of
energy, characterized by slow adsorption speed, long duration of action,
irreversible processes and may be inhibited by inhibitors of energy
metabolism. The adsorption of heavy metals by dead cells is metabolism
independent but dead biological cells can remove heavy metals from
solution through ion exchange, complexation, iron chelation, phys­
isorption and precipitation. This type of adsorbent can be applied to
resting cells, cell metabolites or cell preparations [80]. This metabolism
independent, biosorbed physicochemical phenomenon of heavy metals,

6
D. Zhao et al. Journal of Environmental Chemical Engineering 11 (2023) 109943

Table 3
. Performance of metal removal from wastewater using microalgae and bacteria species.
Microalgae Bacteria Species Wastewater Metal Removal (%)/mg g− 1 Other Pollutants Modes and Mechanisms References
Maximum Metal Biosorption Removal (%)
Capacity

Algal-bacterial aerobic granular
sludge (AGS)
No microbial name provided
Algal-bacterial aerobic granular
sludge (AGS)
No microbial name provided
Chlorella sorokiniana 211/8k
Ralstonia basilensis
AY047217
Chlorella sp., Scenedesmus obliquus,
Stichococcus strains, Phormidium
sp.
and Rhodococus,
Kibdelosporangium aridum
Spirulina sp. and Sulphate
reducing bacteria
Spirulina sp. and Sulphate
reducing bacteria
Spirulina sp. and Sulphate
reducing bacteria
Artificial Synthetic Cr(VI) 99.3% (pH=2) N/A Electrostatic Interactions, [71]
preparation of Cr(VI) Total Cr 89.1% (pH=6) Ion exchange, Surface
ionic solution Complexation,
Bioreduction.
Aerobic granular sludge (AGS)
Artificial Synthetic Cr(VI) 51.0 mg g− 1（pH= 2） N/A -Aerobic granular sludge (AGS) [72]
preparation of Cr(VI)
ionic solution
Synthetic wastewater: Algal-bacterial suspension: N/A Ion exchange, Chemisorption, [73]
Cu(II), Cd(II), Ni(II) and Single metal solution: Exchange of heavy
Zn(II), Salicylate Cu(II) 6.7 ± 0.0 mg g− 1（pH= 5） metals for counterions,
Ni(II) 0.3 ± 0.2 mg g− 1（pH= 5） Covalent bonding, Surface
Zn(II) and Cd(II): No significant precipitation, Redox reactions,
adsorption Crystallization
Effect of the initial concentration: Algal-bacterial biomass
Cu(II): 6.1–6.4 ± 0.2 mg g− 1
Influence of pH:
Cu(II) 5.3 ± 0.0 mg g− 1（pH= 5）
Ni(II) 6.4 ± 0.1 mg g− 1（pH= 9）
Ni(II) and Zn(II): No significant
adsorption
Effect of Cu(II) and biomass
concentration:
Cu(II) 8.5 ± 0.4 mg g− 1（pH= 5）
(Initial concentration 20 mg L− 1)
Industrial Wastewater Zn 90% BOD 97% Biofilter [74]
pond Mn 70% COD 51% Immobilization onto a solid
Fe 64% Phenols 85% carrier
Cu 62% Anionic surface active
Ni 62%- Substances (anionic
SAS) 73%
Oil spills 96%
Acid mine drainage Fe optimum sulphate Chemical groups, [75]
wastewater 100 mg⋅l− 1 reduction 80% Extracellular metal
(Initial concentration 500 mg⋅l− 1) Complexing compounds
51.0( ± 17.0) mg⋅l− 1 (1000 mg⋅l− 1) Algal biomass
41.3 ( ± 58) mg⋅l− 1 (1500 mg⋅l− 1) and
61.0 ( ± 4.9) mg⋅l− 1 (2000 mg⋅l− 1) Algal Sulphate Reducing
57.1 ( ± 4) mg⋅l− 1 (2500 mg⋅l− 1) Ponding Process for the
60.3 ( ± 6.7) mg⋅l− 1 (3000 mg⋅l− 1) Treatment of Acidic and Metal
Wastewaters (ASPAM)
Acid mine drainage Zn optimum sulphate Chemical groups, [75]
wastewater 88.0( ± 13) mg⋅l− 1 reduction 80% Extracellular metal
(Initial concentration 500 mg⋅l− 1) Complexing compounds
67.9 ( ± 6.2) mg⋅l− 1 (1000 mg⋅l− 1) Algal biomass
38.9 ( ± 16) mg⋅l− 1 (1500 mg⋅l− 1) and ASPAM
32.6 ( ± 16) mg⋅l− 1 (2000 mg⋅l− 1)
38.0 ( ± 23) mg⋅l− 1 (2500 mg⋅l− 1)
36.7 ( ± 19) mg⋅l− 1 (3000 mg⋅l− 1)
Acid mine drainage Cu optimum sulphate Chemical groups, [75]
wastewater 79.2 ( ± 9.0) mg⋅l− 1 reduction 80% Extracellular metal
(Initial concentration 500 mg⋅l− 1) Complexing compounds
77.4 ( ± 19.0) mg⋅l− 1 (1000 mg⋅l− 1) Algal biomass
66.3 ( ± 14) mg⋅l− 1 (1500 mg⋅l− 1) and ASPAM
46.4 ( ± 4) mg⋅l− 1 (2000 mg⋅l− 1)
50.6 ( ± 15.8) mg⋅l− 1 (2500 mg⋅l− 1)
51.1 ( ± 8.6) mg⋅l− 1 (3000 mg⋅l− 1)

with relatively fast, short-time, reversible, cell-independent energy
metabolism and similar chemical characteristics to those of ion ex­
change resins or activated carbons, has great advantages in industrial
applications. Most recent studies have shown that ion exchange is
dominant in bioadsorption, especially for microalgae- bacteria con­
sortium adsorption, since biosorbents provide a large number of active
groups such as carboxyl, sulfate, phosphate, amine salts for performing
ion exchange [81–84]. There may be more than one mechanism mode of
action in the microalgae- bacteria consortium of biosorption of heavy
metals and several mechanistic modes of action may operate
simultaneously.
2.6.1. Electrostatic attraction
Electrostatic attraction is an adsorption reaction that occurs between
negatively charged cell surface groups and positively charged metal
ions. Most metal ions are cations, while the biological surface is nega­
tively charged, so the organism adsorbs metal ions that can be consid­
ered to undergo electrostatic adsorption with each other [85]. The
electrostatic attraction is crucial to the biosorption of heavy metals by
microalgae-bacteria consortium. This is because the surface of micro­
algae and bacteria is negatively charged due to the presence of carboxyl,
hydroxyl, and amine functional groups. In contrast, heavy metals in
solution are positively charged due to the loss of electrons. Therefore,
the electrostatic attraction between the positively charged metal ions

7
D. Zhao et al.
and the negatively charged functional groups on the microalgae and
bacteria cell surfaces drives the biosorption process [86,87].
2.6.2. Ion-exchange
The microalgae-bacteria consortium can effectively remove heavy
metals from wastewater through several mechanisms, one of which is
ion exchange. This mechanism involves the exchange of metal ions with
ions present in the biomass. The exchange process is driven by electro­
static attraction between the positively charged metal ions and the
negatively charged functional groups on biomass. Carbonyl, hydroxyl,
and amine groups constitute the functional groups responsible for ion
exchange in biomass. These groups can form bonds with metal ions,
exchanging their associated counter-ions, which results in the removal
of metal ions from solution [88,89]. Microalgae-bacteria consortium can
enhance the ion exchange mechanism in various ways. For example,
bacteria in the consortium can produce extracellular polymeric sub­
stances (EPS), which can increase the surface area and the charge den­
sity of the microalgae cell surface. This increases the number of available
ion-exchange sites, which enhances the removal efficiency of heavy
metals. The consortium can enhance the nutrient availability and
stimulate the growth of microalgae, which can increase the production
of EPS and enhance the metabolic processes of microalgae, facilitating
the ion-exchange mechanism and increasing the removal efficiency of
heavy metals [90–92].
2.6.3. Redox mechanism
Redox reactions can also play a role in the biosorption of heavy
metals by microalgae-bacteria consortia. This mechanism involves the
transfer of electrons from the biomass to the metal ions, resulting in the
reduction or oxidation of metal ions [93]. In the case of
microalgae-bacteria consortia, the reduction of metal ions can be facil­
itated by the production of certain molecules, such as flavins, which can
act as electron shuttles. These molecules can transfer electrons from the
biomass to the metal ions, reducing them and facilitating their uptake by
the biomass[94,95]. The oxidation of metal ions can also occur through
the action of enzymes produced by the bacteria in the consortium. These
enzymes, such as peroxidases and laccases, can oxidize metal ions,
making them more prone to adsorption by biomass[95].
2.6.4. Enzymatic mechanism
Enzymatic reactions are also involved in the biosorption of heavy
metals by microalgae-bacteria consortium. This mechanism involves the
action of enzymes produced by the consortium on the metal ions,
leading to their immobilization and removal from solution[96]. The
enzymes produced by the consortium can act in several ways, such as by
cleaving metal-chelating ligands, hydrolyzing metal complexes, or
altering the redox state of metal ions. These enzymatic reactions can
facilitate the adsorption of metal ions by the biomass by altering their
chemical properties or by breaking down metal-chelating molecules
present in the wastewater[97]. Microalgae-bacteria consortium can
enhance the enzymatic mechanism through various ways. For example,
bacteria in the consortium can produce extracellular enzymes that act on
metal ions, increasing the availability of heavy metals by the microor­
ganism cells[98].
2.6.5. Surface complexation
Surface complexation is another mechanism involved in the bio­
sorption of heavy metals by microalgae-bacteria consortia. This mech­
anism involves the formation of surface complexes between the metal
ions and biomass surface functional groups [85,99]. The functional
groups present on the biomass, including carboxyl, hydroxyl and amino
groups, can form complexes with metal ions through electrostatic in­
teractions, covalent bonding, or ion exchange. The formation of these
surface complexes can lead to the removal of heavy metals from the
wastewater and their immobilization on the biomass[100,101]. More­
over, the microalgae-bacteria consortium can enhance the surface
8
Journal of Environmental Chemical Engineering 11 (2023) 109943
complexation mechanism by creating a microenvironment that is
conducive to surface complexation. The production of EPS by the bac­
teria in the consortium can create a matrix that concentrates metal ions
and increases the accessibility of functional groups on the biomass to
metal ions[102].
2.6.6. Cell transformation
Cell transformation is a mechanism involved in the biosorption of
heavy metals by microalgae-bacteria consortium, whereby the uptake of
metal ions triggers physiological and biochemical changes in the cells of
the biomass, resulting in their immobilization and removal from solu­
tion[103]. The exposure of microalgae-bacteria consortium to heavy
metals can induce various physiological and biochemical changes in the
cells, such as the upregulation of metal-binding proteins, the synthesis of
chelating molecules, and the modification of cell wall components[104,
105]. For example, microalgae-bacteria consortium can produce met­
allothioneins, a group of proteins that bind to metal ions and protect the
cells from metal toxicity. The expression of metallothioneins can be
induced by exposure to heavy metals, leading to the immobilization of
metal ions on biomass[85]. Moreover, microalgae-bacteria consortia
can produce exopolysaccharides, which are chelating molecules that
bind to heavy metals and immobilize them on the biomass surface. The
production of exopolysaccharides can be induced by exposure to heavy
metals, enhancing the removal efficiency of biomass [104,106].
2.6.7. Cellular absorption
Cellular absorption is another mechanism involved in the bio­
sorption of heavy metals by microalgae-bacteria consortium. This
mechanism refers to the uptake of metal ions from the surrounding
medium into the cells of the biomass, where they are immobilized and
removed from the wastewater. The process of cellular absorption in­
volves the transport of metal ions across the cell membrane and their
accumulation in the intracellular compartments of the cells, such as the
cytoplasm, vacuoles, and cell wall. The transport of metal ions can occur
through various channels and transporters, such as ion pumps, ion ex­
changers, and ion channels [107,108]. Microalgae-bacteria consortia
can utilize cellular absorption to remove heavy metals from the waste­
water by exploiting the natural metal uptake mechanisms of the cells.
For example, microalgae have been shown to accumulate heavy metals
through the active transport of metal ions across the cell membrane, the
chelation of metal ions by cell surface molecules, and the precipitation
of metal ions in intracellular compartments [109,110]. Bacteria in the
consortium can also contribute to the cellular absorption mechanism by
producing siderophores, which are chelating molecules that bind to
metal ions and facilitate their transport across the cell membrane.
Moreover, bacteria can enhance the accumulation of metal ions in the
intracellular compartments by producing exopolysaccharides, which
create a matrix that traps metal ions and enhances their uptake by the
cells [111].
2.6.8. Inorganic micro-precipitation
Inorganic micro-precipitation is a mechanism involved in the bio­
sorption of heavy metals by microalgae-bacteria consortia. This mech­
anism refers to the precipitation of metal ions as inorganic precipitates
within the cells or on the surface of biomass[84]. The process of inor­
ganic micro-precipitation occurs when metal ions interact with the cells
or extracellular polymeric substances (EPS) of the microalgae-bacteria
consortium. The metal ions can be adsorbed onto the surface of the
cells or EPS through various mechanisms, such as electrostatic attrac­
tion, ion exchange, and surface complexation. Once adsorbed, the metal
ions can react with other ions or molecules within the cells or the sur­
rounding medium, leading to the formation of inorganic precipitates[90,
112]. Microalgae-bacteria consortia can utilize inorganic
micro-precipitation to remove heavy metals from the wastewater by
immobilizing the metal ions as insoluble precipitates. The formation of
inorganic precipitates can occur both inside and outside the cells,
D. Zhao et al.
depending on the metal species and the microorganism involved in the
biosorption process[113]. For example, microalgae can form inorganic
precipitates within the cells by accumulating metal ions in the cytoplasm
and organelles, such as chloroplasts and mitochondria. Bacteria in the
consortium can also contribute to the formation of inorganic precipitates
by producing EPS. This can trap metal ions and facilitate their precipi­
tation[90,114].
3. Factors affecting microalgae-bacteria consortium on
biosorption of heavy metals
3.1. Light intensity
Light exposure is a prerequisite for the photosynthetic activity of the
algal cell. It impacts the effectiveness of the photosynthetic activity of
the algal cell and thus its oxygen production capacity. The heavy metal
removal is enhanced with the increase of light intensity in a certain
range. However, it would decrease slightly when the light intensity
exceeded the light saturation point, indicating that the light intensity
control was optimal at the light saturation point [115]. The growth of
microalgae accelerated with the increase of light intensity when the
light intensity was lower than the light saturation point, when light
intensity exceeds the point of light saturation, microalgal growth is
inhibited [116]. At the point of light saturation, the microalgal biomass
was the largest and heavy metal absorption was also the strongest by the
algae. For example, Ankistrodesmus falcatus, Phormidium bohneri, and
Oscillatoria agardhii demonstrated optimum growth in conditions of light
intensities ranging from 3 to 650 mol m− 2 s− 1, and at temperatures of
20 ◦ C or less [117]. Tangahu et al. [78] used Azotobacter S8 and Chlorella
vulgaris consortia to remove Chromium from wastewater in their study.
A 12-hour light exposure was conducted in the HRAR reactor. The op­
timum light intensity for consortium growth was 6000–7000 lux using a
fluorescent lamp. There was a chromium removal at a maximum rate of
18.68%. Light intensity can affect the consortia removal rate of heavy
metals.
3.2. pH
pH affects the solubility of metal ions, concentration of protons,
adsorption sites on the cell surface and the physicochemical state of
metal ions in solution, which manifests as a significant change in bio­
sorption efficiency with pH [118]. Furuhashi et al. and Nateras-Ramírez
et al. [119,120]’s studies have shown that the biosorption of the
microorganism adsorption system, such as microalgae and bacteria,
increases as the pH increases, and when it is close to neutral, the
adsorption capacity starts to decrease again due to hydroxide precipi­
tation generated on the microbial surface, and eventually affecting the
cells’ adsorption. For example, pH of 8.1 was shown to be the optimal
pH for Desmodesmus sp. biomass production and 99% of inorganic car­
bons are accessible in forms suitable for microanalysis at this pH [121].
At EPS concentration of 0.2 g L− 1 and pH 6.0, the highest biosorption
capacity of extracellular polymeric substances (EPS) of Klebsiella sp. for
Pb (II) was 99.5 mg g− 1 [122].
The pH value influences not only the charge of the metal ions
adsorption groups on the cell surface but also the hydration of the metal
ions and thus the adsorption of metal ions. It is reported that at higher
acidity, complexation groups exhibit greater affinity with hydronium
ions and H+ occupies a large number of adsorption active sites, thus
preventing the contact of metal ions from the microalgae adsorption
active sites [118]. Meanwhile, when the pH value was very low, pro­
tonation of the cell walls of the bacteriophage increases the electrostatic
repulsion on the microbial surface, which may have an effect on the
adsorptive removal of metal ions to some extent. As the pH increases and
exceeds the isoelectric point of the microbial surface, the complexation
groups expose more negatively charged sites, exhibiting enhanced af­
finity for positively charged heavy metals. At the same time, most of the
9
Journal of Environmental Chemical Engineering 11 (2023) 109943
enzyme activities within microorganisms increase and the action
mechanisms such as carrier-assisted transport of heavy metals begin to
play an essential role, directly manifested by the elevation of the
adsorption efficiency of microalgae and bacteria for heavy metals [123,
124].
3.3. Temperature
Temperature also has a significant impact on the biosorption process.
The adsorption temperature mainly affects the adsorption effect by
influencing the physicochemical properties, adsorption thermody­
namics and heat capacity of adsorption on the surface of the biosorbent.
For different biosorbents, the temperature has different effects on the
adsorption of heavy metals. A process that involves the adsorption of
heavy metals by microalgae and bacteria that is related to heat changes
[118]. Higher than 32 ℃ will reduce the activity of microalgae, but will
increase the activity of nitrifying bacteria [50]. The effect of tempera­
ture change on the adsorption process is due to a certain thermal effect
on the adsorption process and the change of temperature can make the
position of the adsorption equilibrium change, thereby increasing or
decreasing the adsorption amount [125]. The Azotobacter S8 and
Chlorella vulgaris consortia removed Cr at a maximum rate of 18.68% at
25–27 ◦ C, indicating that temperature affects the rate of Cr removal.
Furthermore, this experiment also identified important factors such as
pH, total chromium concentration, microalgal cell count, and bacterial
colonization [78].
3.4. Coexisting Ions
Other metal cations present in the solution will have competitive
adsorption with the target heavy metal ions and thus interfering with the
microalgae and bacteria’s adsorption of the target heavy metal ions. This
is because these coexisting ions compete with the major ions for the
limited negatively charged groups on the cells, thereby leading to a
reduction in the adsorption quantity of the primary heavy metals [126,
127]. The radii and electronegativity of coexisting metal ions will vary,
thus making the kinds of coexisting metal ions have different effects on
the respective adsorption capacities [128]. The interference ability of
coexisting ions on target ions is strengthened by enhanced electroneg­
ativity. Coexisting ions’ impact on the adsorption of target ions is either
(i) promotion effect and the adsorption amount after mixing is larger
than that of single components before mixing (ii) Inhibition effect, the
adsorption amount after mixing is less than that of the single component
before mixing, or (iii) No effect, no change in the adsorption amount of
each component before and after mixing [129–131]. Competitive ions
can compete with heavy metal ions for binding sites on the surface of
microalgae and bacteria cells, reducing their HM uptake capacity. For
example, calcium (Ca2+) and magnesium (Mg2+) ions are commonly
found in wastewater and can compete with heavy metal ions for binding
sites. Therefore, the presence of competitive ions can reduce the overall
efficiency of the consortium [132,133]. Synergistic ions can enhance the
adsorption capacity of microalgae and bacteria for heavy metal ions by
forming complexes with them. For example, sulfide (S2-) ions can form a
complex with heavy metal ions, increasing their solubility and
enhancing their adsorption by microalgae and bacteria [134]. There­
fore, the presence of synergistic ions can improve the overall efficiency
of the consortium.
3.5. Adsorption time
The adsorption duration of microalgae and bacteria affects the
adsorption impact significantly. The process of heavy metals adsorption
by active organisms can be temporally divided into two phases, the first
being a fast adsorption phase, about most part of the total adsorbed
amount in a few minutes [135,136]. The second phase is slower. The
transfer rate of heavy metals to the intracellular can take several hours
D. Zhao et al.
to reach the final adsorption equilibrium. The process of heavy metal
adsorption by inactive cells belongs to the fast adsorption stage.
Although the time required for the adsorption equilibrium of inactive
cells is very short, the time is too short to achieve a good adsorption
effect. However, if the time is too long, the adsorbed heavy metals may
dissolve from the surface of the adsorbent and enter the solution, for
example, in the experiment of Cu(II) absorption by Arthobacter sp. Sphe3
and Bacillus sphaericus cells, the maximum adsorption amount can be
reached in 5 min and 10 min of contact time respectively [126,137]. The
Cu(II) in the aqueous solution was removed using fungi-algae pellets
(FAPs). Results from this study demonstrated that FAPs formed at
different capture times all adsorb Cu(II) well, with FAPs formed within
2 h having the highest Cu(II) adsorption capacity at 80.42 mg g− 1 [138].
3.6. Initial concentration of heavy metal
In the case of other influencing factors determined, heavy metal
adsorption amount increases as the initial concentration of heavy metal
increases. But after increasing to a certain value, the adsorption amount
will no longer continue to increase because of the saturation of
adsorption sites on the adsorbent surface. In the process of active cell
adsorption of heavy metals, the increasing concentration of heavy metal
may increase the toxicity to microalgae and bacteria cells and thus affect
the adsorption effect [126]. The initial concentration of heavy metal is a
crucial factor that affects the biosorption efficiency of
microalgae-bacteria consortium systems for heavy metal removal. The
choice of initial concentration depends on the biosorption capacity of
the cells, the specific heavy metal ions to be removed, and the toxicity of
the heavy metal ions to the cells [139]. For example, Cu(II) adsorption
rose between 0.5 and 1.2 ± 0.1 g l− 1 of algal-bacterial biomass, while it
reduced above 1.6 ± 0.1 g l− 1 of algal-bacterial biomass [73].
4. Product applications and future perspectives
4.1. Product application of microalgae-bacteria consortium (Biogas,
Biofuel, feed, fertilizer)
The synergistic effect between microalgae and bacteria can purify
wastewater, greatly improve the efficiency of wastewater treatment and
increase the utilization of organic matter, nitrogen, phosphorus and
other substances in wastewater. Moreover, the symbiosis between bac­
teria and microalgae does not affect the development of microalgae in
the processes of wastewater treatment. Besides, the biomass of the
microalgae-bacteria consortium has many valuable applications.
Microalgae and bacteria need to be co-harvest and separate first then
only can extract many beneficial and economic value components such
as protein amino acids of high-value classes or directly post-processing
into biofuels, animal feed, baits and soil amendments [140,141].
Some biomass value-added products are shown in Table 4. In conclu­
sion, this process is a low-cost and highly effective method for the pu­
rification and utilization of wastewater with great environmental and
economic benefits.
Microalgae contain abundant biodiesel that can be extracted, but the
cultivation of microalgae alone causes difficulty in the harvesting of
microalgae, which could be resolved by microalgae and bacteria co-
culture. Liu et al. [140] studied the effects of transesterification reac­
tion variables on biofuel manufacturing and also the disparities in fea­
tures between biodiesel derived from aerobic granular sludge (AGS,
Aerobic Granular Sludge) and microalgae-bacteria symbiotic aerobic
granular sludge (ABGs, Algal-bacterial Granular Sludge). The results
revealed that the impacts of different extraction operation factors on
biodiesel production decrease in the sequence of methanol amount
> catalyst concentration > reaction duration, although parameter
modifications do not substantially influence biodiesel performance. The
maximal biodiesel production of ABGs was 66.21 ± 1.08 mg g− 1 SS,
which was substantially greater than that of AGS (35.44 ± 0.92 mg g− 1
10
Journal of Environmental Chemical Engineering 11 (2023) 109943
Table 4
Microalgae-bacteria consortium in the valorization of biomass to value-added
products.
Application Example Reference
Biogas Bacterial symbionts can improve the photo- [142]
fermentative hydrogen evolution of
Chlamydomonas by removing oxygen from the
air and efficiently respiring bacteria, which
activates algal Fe-hydrogenase
Biofuels Large amounts of poly-unsaturated fatty acid [140]
methyl esters (FAMEs) are produced due to the
inclusion of algae in the biodiesel synthesis of
Algae-bacteria granular consortia (AAG), which
demonstrate a greater yield
Animal feed Probiotic bacteria linked with algae may [143]
dramatically increase the biomass of
N. oceanica, which can be utilised as animal
feed.
High value Yield improvement of Eicosapentaenoic acid [143]
Biomolecules like (EPA) production with a microalgae-bacteria
EPA consortium
Fertilizer For increasing soil fertility, microalgae cells and [144]
PGPB (plant growth-promoting bacteria) have
been found as potential substitutes for
fertilisers.
SS). Methyl palmitate was the predominant element of biofuel derived
from two particles, however the quantity of polyunsaturated fatty acids
was larger in ABGs (21.86%) than in AGS (1.2%) [140].
Saba et al. [145] summarized the research results of microbial algal
fuel cells (MFCs) applications such as electricity production, wastewater
treatment, algal bioculture, pigment manufacturing, carbon dioxide
absorption and oxygen generation. Majee et al. [146] summarized the
characteristics and applications of several polysaccharide substances
produced by marine microalgae and bacteria in toxicology, pharma­
ceuticals, and cosmetics, exemplifying their sustainable application as
renewables. However, the biomass generated in wastewater treatment is
rarely used in food and high-value chemicals due to the limitation of
high-quality pursuit and people acceptance. In addition, there is a
problem that biomass containing heavy metals and recalcitrant com­
pounds cannot be used to produce fertilizers. So, the best use is to
convert these biomass to biogas generated via anaerobic digestion.
4.2. Current challenges and future prospect
Current research shows that heavy metal remediation from waste­
water using an aerobic system is effective and could save aeration costs
[147,148]. Therefore, at present the treatment of heavy metals using the
microalgae-bacteria symbiosis system offers a greener and environ­
mentally friendly process with low running costs, chemical agents free
and efficient degradation of heavy metals while accumulating micro­
algal biomass for bioenergy and refineries [149,150].
The treatment of wastewater using the microalgae-bacteria con­
sortium system shows great potential but the high concentration of
pollutants could inhibit the growth of microalgal cells and bacteria, thus
affecting the treatment efficiency. At present, the main challenges faced
are:
(i) high heavy metal concentrations present in wastewater due to
different sources.
(ii) difficulty to separate bacteria and alga for biofuel and products
extraction, which will increase the operation cost of the downstream
process for refineries (iii) Higher chroma and turbidity of industrial
effluent may block light penetration and inhibit photosynthesis in
microalgae.
The future prospect of heavy metal wastewater treatment may be a
way to utilize the integrated treatment technology which is mixed with
multiple wastewater treatment processes including biosorption, as a
whole. The wastewater was treated by a comprehensive utilization of
D. Zhao et al.
various biological metabolic activities, including biosorption, bio­
reduction, and bioprecipitation. The combination of bioprocesses with a
commercialization process, such as air flotation, chemical precipitation,
electrochemistry and membrane technology, is also beneficial for the
large-scale treatment of heavy metal wastewater [151]. Combining
remediation of complex heavy metal wastewater with the comprehen­
sive utilization of mixed biosorption materials of multiple microorgan­
isms, combined with multiple biosorption, bioprecipitation processes
and physicochemical processes, could be a development trend in the
biosorption field. Using the multiple life metabolic activities of living
cells, such as biosorption, bioaccumulation transformation, bio­
precipitation and a series of biological metabolic activities, it is possible
to achieve the simultaneous removal of multiple pollutants from water
bodies in one reactor [152].
Therefore, future research directions for biosorption technologies for
heavy metals should include:
(i) Further exploration of the adsorption mechanism of the interac­
tion between heavy metals and microbial cells to provide a multilevel
technical analysis of the biosorption process using analytical techniques
at the molecular and atomic levels;.
(ii) Exploration on improving the efficiency of the adsorption process
and reducing the cost of the adsorption process, which is beneficial for
application in practical industrialization and in-depth exploration of the
parameters controlling biosorption;.
(iii) Heavy metal wastewater treatment by a consortium of bacteria
and microalgae to explore the network structure relationships between
microorganisms with common metabolic relationships at the systems
level;.
(iv) Mixed culture should be considered as the direction of remedi­
ation research for the actual environmental situation, and as far as
possible to be applied in practice;.
(v) Screening of high-efficiency heavy metal treatment microorgan­
isms and constructing genetically engineered microorganisms with
excellent biosorbent characteristics;.
5. Conclusion
Industrial development and social progress have caused the
increasing pollution of heavy metals in water bodies which not only
affect the aquatic ecological environment but also affect human health
in the food chain. As a consequence, it is critical to take strategic mea­
sures in treating heavy metals from wastewater at the source, to mitigate
severe heavy metal pollution for environmental sustainability and the
well-being of society. Microalgae-bacteria consortia exhibit effective
bioadsorption capacity for heavy metals which can be widely used in the
bioremediation of heavy metals from wastewater. Bacteria can bio-
transform algal adsorbed toxic heavy metals to achieve the purpose of
detoxification by bacterial self-decomposition, resulting in improved
remediation efficiency. In summary, the use of combined microalgae
and bacteria for the remediation of heavy metals in contaminated water
bodies offers many advantages, including high efficiency, economic
feasibility and simplicity. The accumulated biomass energy of the
microalgae-bacteria consortium can output a series of applied value-
added products, however, there is currently no established and devel­
oped technology of microalgae and bacteria system to remove heavy
metals with high biomass production. Therefore, research on developing
the mechanism of algal-bacteria symbiosis for heavy metal treatment, as
well as the reaction device ought to be advanced further for a broad
variety of potential applications, social values as well as economic
benefits.
CRediT authorship contribution statement
Dehua Zhao: Writing – original draft, Writing – review & editing,
Conceptualization. Wai Yan Cheah: Writing – original draft, Writing –
review & editing, Conceptualization. Sai Hin Lai: Conceptualization,
11
Journal of Environmental Chemical Engineering 11 (2023) 109943
Reviewing, Project administration. Eng-poh Ng: Conceptualization,
Reviewing, Project administration. Kuan Shiong Khoo: Writing –
original draft, Writing – review & editing, Conceptualization. Pau Loke
Show: Reviewing, Editing. Tau Chuan Ling: Project administration,
Reviewing, Funding acquisition.
Declaration of Competing Interest
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.
Data Availability
No data was used for the research described in the article.
Acknowledgement
This work was supported by the Fundamental Research Grant
Scheme (FRGS) (Grant Number FRGS/1/2020/SKK01/UM/01/1) and
Geran Galakan Penyelidik Muda Universiti Kebangsaan Malaysia
(GGPM) (Grant Number GGPM 2020-056).
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