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Retracted: Advances in Heavy Metal Bioremediation: An Overview

Applied Bionics and Biomechanics

Received 28 November 2023; Accepted 28 November 2023; Published 29 November 2023

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References
[1] A. Sayqal and O. B. Ahmed, “Advances in Heavy Metal
Bioremediation: An Overview,” Applied Bionics and Biomechan-
ics, vol. 2021, Article ID 1609149, 8 pages, 2021.
Hindawi
Applied Bionics and Biomechanics
Volume 2021, Article ID 1609149, 8 pages
https://doi.org/10.1155/2021/1609149

Review Article
Advances in Heavy Metal Bioremediation: An Overview

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T
1 2
Ali Sayqal and Omar B. Ahmed
1
Chemistry Department, Faculty of Applied Science, Umm Al-Qura University, Makkah, Saudi Arabia
2
Department of Environmental and Health Research, The Custodian of the Two Holy Mosques Institute of Hajj and
Umrah Research, Umm Al-Qura University, Makkah, Saudi Arabia

C
Correspondence should be addressed to Omar B. Ahmed; abuaglah1@hotmail.com

Received 20 September 2021; Revised 11 October 2021; Accepted 1 November 2021; Published 11 November 2021

Academic Editor: Fahd Abd Algalil

A
Copyright © 2021 Ali Sayqal and Omar B. Ahmed. This is an open access article distributed under the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work
is properly cited.

The pollution of toxic heavy metals is considered one of the most important environmental issues which has accelerated

R
dramatically due to changing industrial activities. This review focuses on the most common methods, strategies, and biological
approaches of heavy metal bioremediation. Also, it provides a general overview of the role of microorganisms in the
bioremediation of heavy metals in polluted environments. Advanced methods of heavy metal remediation include
physicochemical and biological methods; the latter can be further classified into in situ and ex situ bioremediation. The in situ

T
process includes bioventing, biosparging, biostimulation, bioaugmentation, and phytoremediation. Ex situ bioremediation
includes land farming, composting, biopiles, and bioreactors. Bioremediation uses naturally occurring microorganisms such as
Pseudomonas, Sphingomonas, Rhodococcus, Alcaligenes, and Mycobacterium. Generally, bioremediation is of very less effort, less
labor intensive, cheap, ecofriendly, sustainable, and relatively easy to implement. Most of the disadvantages of bioremediation
relate to the slowness and time-consumption; furthermore, the products of biodegradation sometimes become more toxic than

E
the original compound. The performance evaluation of bioremediation might be difficult as it has no acceptable endpoint.
There is a need for further studies to develop bioremediation technologies in order to find more biological solutions for
bioremediation of heavy metal contamination from different environmental systems.

R
1. Introduction
Heavy metals refer to metals with relatively high densities
(more than 5gm/cm3), atomic weights (greater than 50),
and atomic numbers. They are often present in the earth as
a normal component due to erosion process to rocks, natu-
rally occurring decay of plant and animal waste matter,
precipitation or atmospheric accumulation of airborne parti-
cles from volcanic eruption, and forest fire smoke. Moreover,
wind erosion and oceanic spray also contribute to the expo-
sure of heavy metals in the environment [1]. The pollution
of toxic heavy metals is considered one of the most important
environmental issues that has been accelerated dramatically
due to changing industrial activities. Pollutants can be intro-
duced and built up in the environment due to various human
activities such as domestic waste, vehicles emission, indus-
trial processes (e.g., electroplating, dyeing, and mining), the
random disposal of electronic waste, agricultural fields, sew-
age sludge, and waste treatment plants [2, 3]. In addition,
heavy metals may be present at high levels in aquatic and soil
ecosystems as compared with the atmosphere (e.g., vapors or
particulate) [4, 5]. The source of heavy metals may be either
natural or due to human activities, which eventually leads to
their presence in soil, water, and air [5–8] (Figure 1). Con-
taminated soils and ground waters put human health at risk
through the consumption of food grown on polluted areas,
dermal contact, and the inhalation of dust [9–11]. Pollution
by heavy metals is a serious threat to environmental living
organisms depending on the concentration of heavy metal
and the overdose absorbance rate. The negative impact of
heavy metals to human and animal health is related to their
long-term presence in the environment, and many heavy
metals have high level of toxicity even at low concentrations
(e.g., mercury, arsenic, lead, fluorine, and cadmium) [12–14].
Lead is considered one of the most persistent heavy metals
because it can persist in soil up to 5,000 years with a high
2 Applied Bionics and Biomechanics
Industrials, fuels,
fertilizers, pesticides
Air Soil
Plants
Animals
Humans
Figure 1: Sources and cycles of heavy metals in the environment [5].
average biological half-life [15]. The main problem with
A
heavy metals is the difficulty of biodegradation when bioac-
cumulation occurs in tissues. They are also capable of bio-
magnification along with the nutritional levels [16]. The
discharge of heavy metals in the environment occurs
through geological process (e.g., weathering and volcanic
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eruptions). Arsenic, lead, cadmium, nickel, chromium,
cobalt, zinc, and selenium are highly toxic even in minor
concentrations [17, 18]. Remediation can be defined as the
removal of pollution or contaminants from the environment
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(e.g., sediment, groundwater, and surface water and soil) to
protect human health and restore the environment. This
review discusses advances in heavy metal bioremediation
from the existing literature by collecting databases and
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information from more than 60 publications that address
the last issues related to bioremediation in the context of
polluted environments. It also focuses on the most common
methods, strategies, and biological approaches of heavy
metal bioremediation and provides a general overview of
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the role of microorganisms in the bioremediation of heavy
metals in polluted environments.
2. Methods of Heavy Metal Remediation
In recent years, variable technologies and methods have
been used in heavy metal remediation in contaminated envi-
ronments such as soil and water. Such methods include
physicochemical and biological methods; the latter is further
classified into in situ and ex situ bioremediation.
2.1. Physicochemical Methods. Physicochemical methods
include processes that work to remove heavy metals from
any contaminated environment. They can be applied on
the form of particulate of metals or metal-containing parti-
cles. This remediation can be conducted through physical
and chemical processes such as ion exchange, precipitation,
reverse osmosis, evaporative recovery, solvent extraction,
filtration, chemical oxidation, chemical leaching, electroki-
Rocks
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Water
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C T
netics, land filling, electrochemical treatment, electrodialysis,
ultrafiltration, solvent extraction, chemical precipitation,
chemical reduction, and isolation (mechanical) separation
of metals [1, 9, 19, 20]. However, these methods may show
incomplete metal removal; in addition, they require high sol-
vent and production of poisonous waste products. They also
have an inherent negative environmental impact and are
usually soil disturbing, besides that fact that they are labor
intensive and expensive [10]. So, these methods are limited
by their high costs, high energy requirements, low efficiency,
unpredictable metal ion removal, and generation of toxic
sludge [21–27].
2.2. Biological Methods. Biological remediation or biodegra-
dation constitutes many types of methods involved in the
removal or degradation of heavy metals through biological
activity. These biological treatments may either include aer-
obic (presence of oxygen) or anaerobic (absence of oxygen)
processes and can be used for heavy metal removal. Biodeg-
radation is a process wherein the polluted environment is
biologically degraded under certain conditions to levels
below the concentration limits established by regulatory
authorities [28–32]. Bioremediation can further be classified
into in situ or ex situ categories based on the strategies
involved in Table 1.
2.2.1. In Situ Bioremediation. In situ bioremediation
methods treat the contamination at the site without remov-
ing soil. The use of these specific methods depends on many
factors: the area contaminated, properties of the compounds
involved, concentration of the contaminants, and time
required to complete the bioremediation. This process is
usually recommended because it requires moving fewer
materials and is less expensive. In situ bioremediation is
sometimes classified into intrinsic bioremediation and engi-
neered in situ bioremediation. It includes so many types
mainly bioventing, biosparging, biostimulation, bioaugmen-
tation, and phytoremediation [33–36].
Applied Bionics and Biomechanics
Table 1: Types of bioremediation.
Strategy Degradation
In situ bioremediation
Bioventing
Biosparging
Biotransformation
Biostimulation
Bioaugmentation
Phytoremediation
Ex situ bioremediation
Land farming
Composting Biodegradation
Biopiles
Bioreactors
Others Mineralization
(1) Bioventing. Bioventing technique is the most commonly
used in situ mechanism in which air and nutrients are sup-
plied to polluted soil to stimulate the microorganisms (bac-
teria). Bioventing requires limited air flow and low oxygen
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rates to release pollutants to the atmosphere through biodeg-
radation. It can simulate in situ biodegradation of simple
hydrocarbons in the soil, and hence, the contamination
occurs deep under the surface [37]. Bioventing is limited
by the inability to deliver oxygen to the polluted soil and
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the insufficient aeration of shallow contamination [38].
(2) Biosparging. Biosparging is defined as the injection of law
pressure air below the water table to raise the level of ground-
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water oxygen and enhance the rate of bacterial bioremediation
of contaminants [33]. Both bioventing and biosparging tech-
niques have been utilized simultaneously to guarantee the
efficient removal of the soil contaminants despite any unfa-
vorable conditions. Biosparging can also combine soil and
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groundwater to reduce the concentration of dissolved oil
compounds in groundwater, mixed with soil under level
under water table and within the capillary fringe. It is an ease
and low-cost procedure with considerable flexibility.
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(3) Biostimulation. Biostimulation involves enhancing bacte-
rial growth to initiate the bioremediation process. First, the
polluted soil is mixed with enriched nutrients and vital sub-
stances to stimulate microbial activity for the fast degrading
of contaminants or toxic compounds into the carbon source
or nitrogen and phosphorous source [39]. Microorganisms
such as bacteria and fungi represent nature’s original recy-
clers. The capability of microorganism to transform chemi-
cal pollution into sources of energy and useful materials
suggests important biological processes which are lower in
cost and friend to environment.
(4) Bioaugmentation. In bioaugmentation, there are certain
sites where microorganisms are required to extract the con-
taminants. They are also able to outcompete indigenous
microorganisms, which means that they can clean up the site
rapidly. The removal of toxic chemicals through bioaugmen-
tation has been reported in environments such as soil and
3
Organism References
D
Bacterioremediation
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[32–36]
Mycoremediation
T
Phytoremediation
Compost bioremediation
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water. However, a number of limitations have also been doc-
umented. For instance, it has been observed that there is a
decrease in the number of exogenous microorganisms after
their addition to a polluted site due to abiotic and biotic
stresses. They occur due to insufficient growth nutrients
such as substrates, temperature changes, and pH, in addition
to the competition between introduced and indigenous
microorganisms [40, 41].
(5) Phytoremediation. Phytoremediation represents an
emerging technology that uses plants to remove pollution
from soil and water. It has a potential use in the biodegrada-
tion of organic contaminants and may be a promising choice
in the future. This technology is suitable for sites with shal-
low contaminants. Nevertheless, many studies have high-
lighted several limitations of this technology, such as
contamination concentration, toxicity, bioavailability, the
type of plant, and stress tolerance [42].
2.2.2. Ex Situ Bioremediation. Ex situ bioremediation means
excavating and treating soil prior to returning the soil to its
original state. If the contaminated material is excavated, it
can be treated on or off site, which is often a more rapid
method of decontaminating the area. Ex situ bioremediation
is categorized into solid phase and slurry phase systems. The
most important techniques include land farming, compost-
ing, biopiles, and bioreactors [33].
(1) Land Farming. Land farming is a simple process which
implies that excavation of contaminated soil over a prepared
site with periodic tilling until pollutants is degraded through
microorganisms where the practice is limited to the treat-
ment of small part of soil [43]. The technique is easy and
much effective specially when used for petroleum-
contaminated soil. However, the technique is limited to the
treatment of a small space of upper soil (10–35 cm).
(2) Composting. A composting method involves combining
polluted soil with nonhazardous organic agricultural wastes
to support the growth of high microbial number with
increased temperatures (40-65°C). The method is applied
4 Applied Bionics and Biomechanics
to a mixture of excavated soils and biosolids (wood chips,
animal, and vegetative wastes) contaminated with organic
materials (petroleum hydrocarbons and pesticides) [33, 43].
(3) Biopiles. Biopiles are a mix or hybrid between land farm-
ing and composting. Biopiles produce enriched environ-
ments for different microorganisms (both aerobic and
anaerobic). The aqueous reactors represent an ex situ treat-
ment of a contaminated environment, where reactors are
pumped up from a certain site. It involves bioremediating
a contaminated environment by using a special engineered
technology [33]. Engineered cells are made for the treatment
of surface pollutants to regulate physical losses of the
contaminants through leaching, which is then followed by
volatilization [43]. Biopiling is considered a feasible, cost-
effective technique for contaminated soils.
(4) Bioreactor. A bioreactor is a vessel used after a certain
optimization of an external environment in which a bio-
chemical reaction occurs. The system may include enzymes,
tissues, microorganisms, and animal and plant cells to
achieve a high yield of bioremediation. Overall, biodegrada-
A
tion is higher in bioreactor systems as compared with other
systems because the target environment is easy to manage,
control, and predict. Despite the advantages of reactor sys-
tems, it is found that the contaminated environment (e.g.,
soil) requires excavation of the contaminant from the soil
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through physical extraction before being processed by a bio-
reactor [33].
3. Role of Microorganisms
T
Various species of microorganisms can be used for bioreme-
diation, as they are nature’s original recyclers. They are also
capable of transforming chemicals into sources of energy
and raw materials for their own growth to produce a low-
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cost and environment-friendly biological process. Due to
their high industrial use, heavy metals have become a world-
wide real environmental problem. Toxic heavy metals are
accumulated through the food chain due the industrial activ-
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ities and fuel consumption leading to both environmental
and health problems. These heavy metals exert toxic effects
on living cells (mercury, silver, lead, cadmium, and arsenic).
Many types of bacteria carry resistant genes to many types of
cations and oxyanions of heavy metals in their DNA. To
survive, bacteria undergo many different mechanisms to
face the uptake of heavy metal ions. These mechanisms
include biosorption, entrapment, efflux, reduction, precipi-
tation, and complexation. Microorganisms therefore can be
a promising, unlimited resource for new environmental
biotechnologies. Bioremediation uses naturally occurring
microorganisms to degrade or detoxify hazardous sub-
stances to human health and/or the environment. The
microorganisms can either be used indigenously or be iso-
lated from other resources at the polluted site [44, 45].
Microorganisms which are involved in biodegradation are
shown in Table 2, including the following examples: Acine-
tobacter, Actinobactera, Alcaligenes, Arthrobacter, Bacillins,
Beijerinckia, Flavobacterium, Methylosinus, Mycobacterium,
Mycococcus, Nitrosomonas, Nocardia, Xanthobacter, Penicil-
lium, Phanerochaete, Pseudomonas, Rhizoctonia, Trametes,
and Serratia [46–66]. Most bioremediation processes are
D
completed under aerobic conditions, but running a system
under anaerobic conditions may permit microbial organ-
isms to degrade otherwise recalcitrant molecules [44]. Aero-
bic organisms depend on oxygen during their growth
activity. These are continuous processes which are known
E
as cellular respiration, which use oxygen to oxidize sub-
strates like fatty acid from oil in order to obtain energy.
Examples of degradative aerobic bacteria are Pseudomonas,
Sphingomonas, Rhodococcus, Alcaligenes, and Mycobacte-
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rium. Microorganisms can also be used to degrade toxic
chemicals such as pesticides besides hydrocarbons materials
[33]. Many bacteria use the contaminant as a metabolic
source (carbon and energy). An anaerobic bacterium is an
organism that does not need oxygen as a based metabolism,
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and it differs from aerobic bacteria. Anaerobic bacteria have
also been used for the bioremediation of biphenyls, dechlo-
rination, and chloroform [33]. Furthermore, fungi may be
able to degrade a high range of persistent or toxic environ-
mental pollutants [45]. There are many types of substrates
available, such as corn cobs, straw, and dust. The aerobic
bacteria that grow by utilizing methane for carbon and
energy. This aerobic degradation being initiated with
enzyme methane monooxygenase will be active against a
wide range of chemicals [33].
4. Factors Affecting Bioremediation
The removal of heavy metals through microorganisms may
have ecological and economic limits. Several factors should
be considered for the selection of a proper bioremediation.
There are certain variables that have a great impact on the
extent of biodegradation. First, nutrients in the polluted
environment such as nitrogen, phosphate, sulphur iron,
and potassium can stimulate and support strong microbial
growth, cellular metabolism, and microorganism growth
[34]. These nutrients represent basic life requirements and
help microorganisms produce necessary enzymes to break
down contaminants. Second, the remediation cost may also
play an important role in the continuity of bioremediation,
meaning that the cost should be low for financial feasibility.
Third, the nature of pollutants, meaning whether they are
solid, semisolid, liquid, or volatile in nature, may affect the
process, or the pollutants are toxic or nontoxic, organic,
and inorganic pollutants, heavy metals, polycyclic aromatic
hydrocarbons, pesticides, and chlorinated solvents. The
nature of the polluted area is also highly important, as it
can affect the quality of bioremediation. Fourth, pH, tem-
perature, and other physicochemical factors are important
for the bioremediation process. The selection of the opti-
mum range of these parameters can also greatly influence
the rate and extent of biodegradation, as it influences the
microbial growth and hence the removal of the contami-
nants [33]. Fifth, moisture content (water) is also a primary
factor for biological growth and efficient bioremediation.
Sixth, microbial diversity that can biodegrade any contami-
nant such as Pseudomonas, Aeromonas, Flavobacteria,
Applied Bionics and Biomechanics 5

Table 2: Heavy metal distribution in environment and microorganisms involved in biodegradation.

Heavy metal Distribution Microorganism Reference

D
As Soil, volcanic eruption Sporosarcina ginsengisoli [46, 47]
Bacillus sp.
Cd Soil, sedimentary rocks, water [48–50]
Klebsiella planticola
Bacillus cereus strain XMCr-6
Bacillus cereus

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Cr All environments Pseudomonas putida [51–54]
Enterobacter cloacae B2-DHA
Bacillus subtilis
Rhodobacter sphaeroides

T
Pb Soil Leclercia adecarboxylata [55]
Kocuria flava
Bacillus sp. strain CSB_B078
Klebsiella pneumoniae isolate
Hg Water, soil, and air [56]
Enterobacter sp. strain 08

C
Acinetobacterseohaensis strain
Cu Earth’s crust, oceans, lakes, and rivers Kocuria flava [57]
Zn Surface water, soil, and rock Pseudomonas putida [58, 59]
Desulfovibrio desulfuricans
Ni Air, soil, sediments, and water [60, 61]
Bacillus licheniformis

A
Bacillus sp.
Co Air, soil, and water [49, 62, 63]
Rhodopseudomonas palustris
As: arsenic; Cd: cadmium; Cr: chromium; Pb: lead; Hg: mercury; Cu: copper; Zn: zinc; Ni: nickel; Co: cobalt.

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Aeromonas, Chlorobacteria, Corynebacteria, Acinetobacter, removing pollutants from the site. Also, there is a difficulty
Mycobacteria, Streptomyces, Bacilli, Macrobenthos, and of bioremediation in treating inorganic contaminants and
other aquatic plants such as E. crassipes and L. hoffmeis- in confirming whether contaminants have been destroyed

T
teri can also degrade turbidity and chemical domestic
wastewater [35]. Seventh, oxygen is mainly used for the
initial breakdown of the hydrocarbon in the contaminated
sites and also can be used for both aerobic and anaerobic
bioremediation [36].
or not. Besides that, there is a slowness of highly chlorinated
materials biodegradation and generation of more toxic or
carcinogenic by-products [65, 66]. Furthermore, the prod-
ucts of biodegradation sometimes become more toxic than
the original compound. Its biological processes are also

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highly specific. Examples for effective site factors include
5. Advantages and Limitations the presence of microbial populations, growth conditions,
and quantity of nutrients and pollutants [33, 65].
Bioremediation is a simple process used by many scientists

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in the waste treatment process for contaminated environ-
ments such as soil. The microbes that degrade the contami-
nant increase in numbers and release harmless products.
The residues for the treatment are usually harmless products
such as carbon dioxide, water, and cell biomass. Bioremedi-
ation is of very less effort, less labor intensive, and cheap
compared to other methods that are used for the removal
of hazardous waste. Bioremediation is also ecofriendly, sus-
tainable, and relatively easy to implement. It is also useful
for the complete destruction of a wide variety of contami-
nants [64]. Many hazardous compounds can be transformed
into harmless products. Moreover, bioremediation can be
implemented on the site of contamination itself without
causing a major disruption of normal activities. There is no
need to transport large numbers of waste off-site, there is
no potential human health risk, and the environment will
remain uncontaminated. Most of the disadvantages of biore-
mediation relate to it needing a longer time to be completed
as compared with other options such as excavation and
6. Conclusion
Bioremediation technique is still a useful, natural, and envi-
ronmentally friendly process in which the polluted environ-
ment is biologically biodegraded. Microorganisms play a
significant role in the removal of heavy metals pollutants.
The heavy metals (e.g., mercury, silver, lead, cadmium, and
arsenic) exert toxic effects on living cells. Examples of degra-
dative aerobic bacteria are Pseudomonas, Alcaligenes, Sphin-
gomonas, Rhodococcus, and Mycobacterium. Anaerobic
bacteria have also been used for the bioremediation of
biphenyls, dechlorination, and chloroform. Furthermore,
fungus microorganisms can effectively degrade many toxic
environmental pollutants. Phytoremediation represents an
emerging technology through which plants can be used to
remove pollution from soil, water, and other environments.
Bioremediation is of very less effort, less labor intensive,
cheap, ecofriendly, sustainable, and relatively easy to imple-
ment. Most of the disadvantages of bioremediation relate to
6 Applied Bionics and Biomechanics
the slowness and time-consumption; furthermore, the prod-
ucts of biodegradation sometimes become more toxic than
the original compound. Bioremediation may be limited by
irregularity and uncertainty of completeness. Also, the per-
formance evaluation of bioremediation might be difficult as
there is no acceptable endpoint. There is a need for further
studies to develop bioremediation technologies in order to
find more biological solutions for bioremediation of heavy
metal contamination from different environmental systems.
Conflicts of Interest
The authors declare that they have no conflicts of interest.
Acknowledgments
The authors would like to thank the Deanship of Scientific
Research at Umm Al-Qura University for the continuous
support. This work was supported financially by the Dean-
ship of Scientific Research at Umm Al-Qura University
(Grant Code: 18-SCI-1-02-0002).
A
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