Geomicrobiology Journal

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Heavy Metals Clean Up: The Application of Fungi

for Biosorption

Imlitoshi Jamir, Lipenthung Y. Ezung, Liyani Merry, Leimapokpam Tikendra,

Rajkumari Sanayaima Devi & Potshangbam Nongdam

To cite this article: Imlitoshi Jamir, Lipenthung Y. Ezung, Liyani Merry, Leimapokpam Tikendra,
Rajkumari Sanayaima Devi & Potshangbam Nongdam (2024) Heavy Metals Clean Up:
The Application of Fungi for Biosorption, Geomicrobiology Journal, 41:3, 201-212, DOI:
10.1080/01490451.2024.2307899

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Published online: 30 Jan 2024.

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Geomicrobiology Journal
2024, VOL. 41, NO. 3, 201–212
https://doi.org/10.1080/01490451.2024.2307899

Heavy Metals Clean Up: The Application of Fungi for Biosorption

Imlitoshi Jamira, Lipenthung Y. Ezunga, Liyani Merrya, Leimapokpam Tikendrab, Rajkumari Sanayaima Devic,
and Potshangbam Nongdamb
Department of Biotechnology, Nagaland University, Dimapur, Nagaland, India; bDepartment of Biotechnology, Manipur University, Canchipur,
a

Manipur, India; cDepartment of Botany, Deen Dayal Upadhyaya College, University of Delhi, New Delhi, India

ABSTRACT ARTICLE HISTORY

Heavy metals are quickly becoming a primary environmental pollution concern. Though they can Received 27 October 2023
be considered rare and scarce compared to their other metal counterparts, they have a wide range Accepted 17 January 2024
of implications in the modern world. Heavy metals accumulate in our soil, water, and food chain KEYWORDS
with the rapid anthropogenic release in the ever-growing populace. These accumulations have Pollution; fungi; heavy metals;
adverse consequences on human health, with severe medical complications. Fungi belong to a biosorption; bioaccumulation
biological group considered the natural sink and the scavengers that degrade the living hydrocarbon.
They are known to thrive in adverse conditions, including tolerance to heavy metals. The organisms
offer unique advantages due to their morbid nature and the cellular construct they have grown
over years of evolution. Various structural and biological mechanisms are ascribed to their survival
in a heavy metal environment. As most of the known metal-sequestering fungi belong to yeast and
filamentous fungi, in this review, we attempted to analyze the metal-harnessing capacity of these
fungal groups.

Introduction and animal health. It is necessary to eliminate them from

Heavy metals, as the name indicates, are elements that have
a higher density than water. They have a relatively high
atomic mass with a density ranging from at least 3.5 g/cm3
to more than 6 g/cm (Tchounwou et al. 2012). Although
heavy as it sounds, the group comprises a broad range of
disparate elements and toxic compounds that living cells
cannot usually process (Duffus 2002). Heavy metals are
non-biodegradable, and their accumulation has become a
worldwide problem affecting human health and the environ-
ment (Qasem et al. 2021; Zou et al. 2016). They are released
due to anthropogenic activities such as mining, petrochemi-
cal plants, metallurgical, paper and tanning industries, and
industrial waste from oil refineries and coal-employed power
stations (Qasem et al. 2021). Livestock manure, contami-
nated food, volcanic eruptions, and other natural phenom-
ena like erosion and weathering also help produce heavy
metals (Verma and Sharma 2017). Over the years, anthropo-
genic and natural releases have led to the accumulation of
heavy metals in dangerous quantities, especially in water
bodies. Heavy metals can also be found naturally in the
environment as trace elements. Few heavy metals are essen-
tial nutrients required in trace amounts in the human body.
Having critical biological roles, they are present as crucial
co-factors for metalloenzymes and as constituents of hor-
mones and proteins (Mehri 2020). Still, most elements, even
in trace amounts, are dangerous to the body. The toxic
nature of heavy metals poses an inherent danger to human
the contaminated habitats to ensure a safer and pollution-free
environment. There are numerous approaches and efforts for
heavy metal removal from the environment. Some costly
efforts to remove heavy metals from wastewater include
using different approaches like chemical precipitation, floc-
culation, filtration, and electrochemical methods (Qasem
et al. 2021).
Biosorption appears to provide an appealing alternative
for heavy metal removal and processing. To this end, several
plants, animals, and microbial biomass have been studied for
potential biosorbents for heavy metals and various sorbate
substances (Volesky 1994). Though each biomass can have
advantages, microbial biomass provides a strong potential for
metal removal. Using fungi as biosorbents can have certain
benefits as they can consume diverse nutrients and acquire
unique metabolic processes that can utilize toxic waste prod-
ucts and organic compounds as their nutrients. Some fungi
degrade recalcitrant compounds outside by secreting special-
ized enzymes and later absorbing them inside the cells as
nutrients (Kapoor and Viraraghavan 1995). They can also
survive in diverse habitats unsuitable for other eukaryotes
(Selbmann et al. 2013). Moreover, high biomass yield can be
generated quickly as growing fungi is simple. The easy avail-
ability of biomass as raw material for heavy metal biosorp-
tion, primarily as a cheap byproduct of industrial
fermentation, makes fungi one of the most attractive candi-
dates for commercial biosorbent development (Kanamarlapudi

CONTACT Potshangbam Nongdam nongpuren@gmail.com Department of Biotechnology, Manipur University, Canchipur, Imphal - 795003, Manipur, India.
© 2024 Informa UK Limited, trading as Taylor & Francis Group
202 I. JAMIR ET AL.
et al. 2018). The present review delves into the potential uti-
lization of various fungi as biosorbents for removing toxic
heavy metals and identifies avenues for future research and
application.
It provides in-depth insights into the tolerance and
absorption capacities of different fungi and also attempts to
address the challenges in fungal bioremediation, including
lack of suitable fungal species, gaps in understanding bio-
sorption mechanisms, and difficulty in translating laboratory
findings to real-world applications. Overall, the paper will
serve as a valuable resource for many researchers interested
in harnessing the potential of fungi for sustainable heavy
metal remediation.
Potential hazards of heavy metals
There are numerous hazards of heavy metals in human
health and the environment. Metalloids, which have a
half-life longer than the average life span of humans, remain
present permanently within the body when there is exposure
to them (Ashrafizadeh et al. 2020). Heavy metals and their
ions interact with different cellular components, nucleic acid,
and proteins, resulting in cellular damage, cell death, and
carcinogenesis (Beyersmann and Hartwig 2008; Wang and
Shi 2001). Arsenic (As), lead (Pb), cadmium (Cd), nickel
(Ni), chromium (Cr), mercury (Hg), copper (Cu), and zinc
(Zn) are some heavy metals most abundantly exposed to
humans. These elements are most related to toxicity in
human health, affecting various organs and systems, even
with low exposure (Qasem et al. 2021; Verma and Sharma
2017). Arsenic, for years, has been commonly used as a pes-
ticide or herbicide and is prominently present in groundwa-
ter. It is classified as a potential human carcinogen affecting
many organs upon long-term exposure (Nurchi et al. 2020).
Prolonged exposure to As has also been shown to cause
neuropathy and cardiovascular disease (Bjørklund et al.
2020). Cadmium is classified as a Class B1 carcinogen by
the Environmental Protection Agency. Its continued expo-
sure generates reactive oxygen species (R.O.S.), leading to
tissue and renal injuries and osteoporosis. Epigenetic changes
in the DNA expression profile may also occur due to Cd
exposure (Bernhoft 2013). Though the molecular mechanism
of heavy metals like As, Cd, Cr, Pb, and Hg inducing cancer
is accurately not known, most of these elements are classi-
fied as human carcinogens based on various epidemiological
studies and further corroboration by experimental studies on
animals (Tchounwou et al. 2012).
There is a profound effect of heavy metals overexposure
in the environment as these elements persist and biomagnify
in the environment (Barwick and Maher 2003). Numerous
pieces of evidence of contamination in water affecting
aquatic life and plants have been reported over the years
(Rezania et al. 2016; Zhang et al. 2022). Fishes in freshwater
and marine environments are widely reported to bioaccumu-
late heavy metals in the food chain. With the amount of fish
being consumed globally, the accumulated heavy metal poses
a considerable health concern for consumers (Ali and Khan
2018). Cd, As, Pb, and Hg are all in concentrations above
the maximum allowed limits (M.A.L.) in different fishes,
acting as the primary source of exposure for Pb in some
coastal regions (Rubio et al. 2005). They are also the chief
exposure source and a health concern for Hg in humans
(Falcó et al. 2006). In the water, Hg is methylated into meth-
ylmercury (MeHg) either by photomethylation or microbes
in the sediments. MeHg can bioaccumulate and magnify
through the food chain, where the higher tropic level of fish
has a higher concentration of MeHg. It collects in the fish
muscle, and consuming mercury-laden fish has resulted in
brain damage, impaired hearing, blurred vision, and neuro-
logical disorders (Bosch et al. 2016). A consolidated source
of pollution and hazards to human health of the five most
commonly exposed heavy metals is given in Table 1.
Various plants, including agricultural and wild varieties,
have exhibited diverse responses to exposure to heavy metals,
ranging from deficits in stomatal conductance to photosyn-
thetic deficiencies (Bibi and Hussain 2005; Srivastava et al.
2012). Cd toxicity in plants damages the ion channels and
affects photosynthesis, leading to browning of roots and plant
death. Pb accumulation and its reaction can cause water
imbalance and disruption in plant nutrient uptake (Mishra
et al. 2019). Heavy metal accumulation, especially in aquatic
plants like rice, can disrupt the growth and yield of the plant
(Uddin et al. 2021). Besides affecting the plants, most of the
heavy metal contaminants that remain within the plant in the
food chain get tropically transferred to the human body,
resulting in serious health issues (Ali and Khan 2018).
Biosorption as a method of bioremediation
Bioremediation involves using biological materials, either liv-
ing or dead, to remove pollutants. There are many
physio-chemical methods by which heavy metals can be sep-
arated and removed within the polluted environment, like
precipitation, coagulation, ion exchange, complexation,
osmosis, and solvent extraction (Gadd 2009). Different strat-
egies involving various organisms and methods are being
utilized for bioremediation. Some common procedures cur-
rently being used are indicated in Figure 1. Many species of
microbes, plants, algae, and biosolids that can absorb, accu-
mulate, and degrade heavy metals within their surroundings
are applied for bioremediation strategies (Kanamarlapudi
et al. 2018).
Biosorption is described as a process of removing metal
ions, radionuclides, and other elements from a waste envi-
ronment using biomass. It is a physio-chemical process
involving different biological entities and their potential to
absorb or adsorb various contaminating substances for
removal (Mrvčić et al. 2012). Biomass, like biological sub-
strate, cell mass, and products, naturally behaves as an
absorbent, accumulating varieties of metals and organics. It
can be derived from plants, bacteria, fungi, and algae and
can be used in either active or dead form, fixed or free, but
all can naturally behave as absorbent (Fomina and
Gadd 2014).
The biosorption mechanism is based on the process of
“sorption,” which is uniformly used for two different
 Geomicrobiology Journal 203

Table 1. 5 Non-essential toxic heavy metals that are most habitually exposed to public health.
Sl.no. Toxic heavy metal Potential human diseases and injuries Main source of pollution References
1 Lead • gastrointestinal • Metal Plating Balali-Mood et al. 2021; Jaishankar
• disease • industries et al. 2014
• kidney damage • Smelting of ores
• CNS injury leading to • Fertilizer and
• headache, memory • pesticide industries
• loss and dullness • Battery industry
• liver damage • Automobiles
• hematologic disorder • exhaust
• -cancer(probable) • Paint and ceramics
• -Munition industry
2 Arsenic • cardiovascular • Mining and Jaishankar et al. 2014; Smith, Lingas,
• disease • processing industry and Rahman 2000; Yedjou, Moore,
• diabetes • Groundwater and Tchounwou 2006; Bjørklund et al.
• skin lesion (keratosis) • contamination 2020
• neuronal injury • by mineral deposit
• hematologic disorder • Pesticides and
• cancer of the bladder, • fertilizer
• kidneys and skin • Paint and ceramic
• industry
3 Chromium • renal damage • Metal processing Pavesi and Moreira 2020; Tchounwou
• dermatitis • Fertilizer industry et al. 2012; Deng et al. 2019
• cancer of the • Chemical and paper
• respiratory tract, • industry
• larynx and other • -Leather tanning
• organs
4 Cadmium • lung damage • Cigarette Li et al. 2019; Chen et al. 2019b; Paschal
• liver injuries • Battery and alloy et al. 2000
• renal disease • Mining and smelting
• cardiovascular • industries
• disease • -Fertilizers industry
• - osteoporosis
5 Mercury • neuronal toxicity • Metal smelting Tchounwou et al. 2003; Jaishankar et al.
• renal Injury and • industry 2014; Chen et al. 2019a; Li et al.
• disease • Electrical and 2015
• liver Injury • electronic industry
• cardiomyopathies • Gold mining
• respiratory problems • Soil erosion and
• gastrointestinal • volcanoes
• toxicity • Dental care and
• preventive medicine

phenomena of absorption and adsorption. Absorption is the
uptake of a substance (absorbate) by another substance
(absorbent) of a different state and is a bulk phenomenon.
Adsorption, by contrast, is a surface phenomenon where
molecules of a substance (adsorbate) get adhered or bonded
onto the surface of a solid (adsorbent) (Fomina and Gadd
2014). Many physio-chemical mechanisms are involved in
the process, namely surface affinity, ligand binding, precipi-
tation, accumulation, ion exchange, passive uptake, and
complexation, which can co-occur (Gadd 1994). In general,
there are two ways for a cell to capture sorbate metals:
metabolism-dependent (active metal transport), an
energy-driven process involving the transportation through
the cell membrane, and metabolism-independent (passive
metal transport), which includes reversible passive transport
like adsorption, ion exchange, affinity and precipitation (Saǧ
2001). Biosorption is more frequently referred to as those
metabolic-independent surface sorption processes mainly
involving dead biomass (Michalak et al. 2013).
Biosorbents and biosorbates
Many biosorbents are being uncovered, from the simplest
microbes to the more complex higher eukaryotes (Fomina
and Gadd 2014). Numerous biological materials can be
employed as biosorbents as biological materials naturally
tend to adhere with high affinity to organic and inorganic
compounds present as contaminants (Volesky 2007). Animals,
plants, and microbial biomass have been studied for poten-
tial biosorbents to various sorbate substances (Volesky 1994).
Some of the materials commonly employed as bioabsorbents
are represented in Figure 2. Most works have indicated a
general preference for non-living cells over living cells as
biosorbents. The preference for non-living cells is most likely
because living cells require optimal parameters, including
media, temperature, and pH. Moreover, waste material tends
to be toxic to living cells over long exposure (Modak and
Natarajan 1995; Vijayaraghavan and Yun 2008).
Nonetheless, heavy metal accumulation, adhesion, com-
plexation, and transformation under the influence of meta-
bolic processes in living cells that can ensure better removal
also cannot be ruled out (Malik 2004). There can be thou-
sands of biomass that can serve as potential biosorbents.
Much of such biomass has been evaluated in microbial cells
and its derivatives that have metal-sequestering properties.
Microbes belonging to families of bacteria, cyanobacteria,
fungi, and algae have all been employed as biosorbent mate-
rials. Agricultural waste like bran, straw and hulls, industrial
204 I. JAMIR ET AL.
Figure 1. Common strategies of bioremediation.
Figure 2. Commonly used materials as biosorbents.
Figure 3. Diverse metal binding groups present in the cell wall polymers of
fungi (ImH: Imidazole; S.H.: sulfhydryl; OH: Hydroxyl; C.O.O.H.: carboxyl group;
NH2: Amino group; R.C.O.O.R.: ester; PO4 3- : Phosphate; C = O: Carbonyl group).
waste sludges, and seaweeds have been assessed for prepar-
ing biosorbents (Michalak et al. 2013; Park et al. 2010).
Some criteria that generally determine the choice of biosor-
bents include having maximum biosorption capacity for any
targeted elements, low cost, rapid growth, and abundantly
availability like byproducts of industrial fermentation
(Fomina and Gadd 2014). Biosorbates include a wide range
of elements and compounds that can be eliminated from the
waste environment. It includes organic compounds like dyes,
phthalates, micro-plastics, and pharmaceutically generated
chemicals (Volesky 2007). Other sorbates that can be
removed from wastewater include metalloids, fluoride, and
xenobiotics (Crini and Badot 2008; Michalak et al. 2013).
Heavy metals and radioisotope removal have also been
extensively investigated as these elements are major contam-
inants in the modern world (Dhankhar and Hooda 2011;
Gadd 2009).
Fungi, the enigmatic cell
Many fungi are scavengers that can survive in diverse sur-
roundings and are found in those habitations that might be
considered adverse environments for other eukaryotes. They
are lower eukaryotes with varied cellular morphology, phys-
iology, and a diverse range of survivability (Walker and
White 2017). Fungi have the remarkable ability to utilize
waste products and toxic compounds for their nutrition,
effectively turning compounds considered toxic for other
eukaryotic cells into their dietary sources. Fungi range from
simple unicellular organisms like Saccharomyces cerevisiae,
the baker’s yeast, to large edible mushrooms. One unique
characteristic of a fungal cell is the carbohydrate component
of the cell wall. While their cell wall components and
arrangement distinguish them from prokaryotes and higher
eukaryotes, the composition of polysaccharides and proteins
in fungal cell walls varies among different fungal species.
The polysaccharides comprise approximately 80% of the
fungal cell wall dry weight, primarily containing chitin, chi-
tosan, α/β glucans, and mannose (Latgé 2007). In the model
yeast S. cerevisiae, the composition of chitin is lower, about
1-2%, while the majority of the carbohydrate component is
made up of β [1→3]‐glucan, β [1→6]‐glucan, and mannose
(Zlotnik et al. 1984). In filamentous fungi like Neurospora

crassa and Aspergillus fumigatus, a higher chitin composi-
tion of about 7-15% was reported (Brown et al. 2020;
Garcia-Rubio et al. 2019). The fungal cell wall composition
is of utmost importance in biosorption since it is a surface
phenomenon that depends on the cell surface, especially the
cell wall. Fungal cell wall polymers have functional groups
like hydroxyl, carboxyl, amino, sulfhydryl, ester, carbonyl,
phosphate, and imidazole, which bind to metal ions
(Dhankhar and Hooda 2011) (Figure 3). Such metal ions
binding to the cell wall tend to restrict the entry of toxic
metals into the cell (Naveena and Latha 2012). In addition
to cell surface sorption, various factors play a crucial role
in the overall adaptation of fungal cells to polluted environ-
ments. These processes may include mechanisms such as
complexation, ion exchange, and chelation, which can occur
independently of cellular metabolism, both inside and out-
side the cell. There are also metabolic-dependent processes,
such as intracellular accumulation, precipitation, sequestra-
tion, and biodegradation which involve a range of enzymes
like laccase, catalase, and peroxidases, which actively break
down the chemicals to detoxify them or are secreted out-
side the cell in response to toxicity (Negi and Das, 2023)
This potential for metal binding and adsorption by fungi is
being continuously studied, which is well enforced by the find-
ing that metal binding is equally efficient in both dead and
living cell walls in fungi (Lu et al. 2020). Moreover, from an
economic view, fungal biomass is abundant, cheap, and easy to
obtain, and lots of fermentation industry generates fungal bio-
mass without posing any environmental risk (Kapoor and
Viraraghavan 1995; Volesky and May-Phillips 1995).
Fungal heavy metal biosorption
Microbes such as bacteria, filamentous fungi, yeast, and
algae can tolerate the presence of concentrated heavy metals.
The cells can behave as an absorbent with the potent capac-
ity to accumulate heavy metals from the environment
(Coelho et al. 2020a). High metal recoveries are active in
environments where the biodiversity of microbial interac-
tions is diverse and rich. To this end, fungal cells rank high
in environmental metal accumulation. Fungal species are
known to absorb and accumulate heavy metals efficiently.
Over the years, studies have shown that notable fungal spe-
cies like S.cerevisiae, Aspergillus flavus, Aspergillus tamarii,
and Trichoderma atroviride have the natural capacity to
absorb copper, lead, nickel, iron, cobalt, arsenic, cadmium,
and chromium (Dusengemungu et al. 2020; López and
Vázquez 2003; Saad et al. 2019). Fungi such as Penicillium
simplicissimum possess a high copper absorption intake and
tolerate cobalt, chromium, and cadmium (Iskandar et al.
2011). Most studies on fungal biosorption of heavy metals
may be classified under two common fungal groups: yeast
and filamentous fungi.
Yeast
Yeast, the unicellular fungi, belongs to Ascomycota. It is a
suitable model organism for understanding the physiological
Geomicrobiology Journal 205
and molecular mechanism of eukaryotic cell interactions
with heavy metals (Bahafid et al. 2017). Ram et al. (2012)
reported that yeast, compared to bacteria, fungi, and microal-
gae, has superior biosorbent capability in removing heavy
metal ions because of their high growth rate and cell wall
structures. This might be because of the electrostatic inter-
actions between the metal ions and the cell surface of the
yeast, which is negatively charged due to phosphates and
carboxyl groups (Kordialik-Bogacka 2011). Several yeast spe-
cies are known for their capacity to sequester heavy metals
and have been successfully employed to remove metals such
as Zn, Pb, Cd, Co, Cr, Ag, and U (Podgorskiĭ et al. 2003).
Prominent genera, including Saccharomyces, Candida, and
Pichia, are recognized for their ability to adsorb and accu-
mulate heavy metals.
Saccharomyces cerevisiae
Saccharomyces cerevisiae has been extensively studied among
the yeast family and boasts a long and illustrious history of
being employed as a model eukaryotic organism. It has been
employed for different molecular studies, including the
molecular mechanism of metal accumulation and release
(Perego and Howell 1997). Some characteristics that make S.
cerevisiae an ideal organism are its simple unicellular eukary-
otic nature, nontoxic, easy to handle, fast harvesting growth,
and no sophisticated equipment or media requirement
(Perego and Howell 1997). This genetically easy-to-manipu-
late organism is the first eukaryote with a complete deletion
mutants collection available, which has been used in differ-
ent screens and assays, and also the first eukaryote with a
complete genome sequence (Giaever and Nislow 2014).
Many studies on metal uptake and accumulation, whether in
wild type or mutated S. cerevisiae, have provided knowledge
to understand better the molecular mechanism of biosorp-
tion in fungi (Eide 1998). Given the easy availability of S.
cerevisiae as a model organism, the organism has been
extensively utilized in various biosorption studies. The sorp-
tion capacity of S. cerevisiae has been investigated in its var-
ious forms: living or dead cells, immobilized or free cells,
raw or pretreated cells, engineered or non-engineered, wild
type, or mutant cells. This has provided a better understand-
ing of the heavy metal sequestration by this model cell and
overall insight into biosorption (Marques et al. 1999; Veglio
and Beolchini 1997; Wang and Chen 2006).
Studies on living S. cerevisiae have shown Cu sequestra-
tion in a range of about 0.163 mmol Cu/g cells, indicating a
possible copper-binding mechanism in the biomass (Volesky
and May-Phillips 1995). The more recent commercially avail-
able biomass of S. cerevisiae showed an efficient sorption
capacity to toxic Cu (II) metal ions in a range of about
4.73 mg g −1 (Nascimento et al. 2019). The biosorption capac-
ity for Pb (lead) in both immobilized and free cells ranged
around 40- 80 mg Pb/g (Al-Saraj et al. 1999); for Cd (cad-
mium), the range is between 10-60 mg Cd/g approximately
(Wang and Chen 2009). With Pb and Cd metal sequestra-
tion, the dead cell showed a higher biosorption capacity of
about 270 mg Pb/g for Pb (Özer and Özer 2003) and about
70 mg Cd/g for Cd (Volesky, May, and Holan 1993). Efficient
206 I. JAMIR ET AL.
biosorption of both Pb (II) and Cd (II) ions had also been
achieved by using functionalized S. cerevisiae cells with
CaCO3, showing a marked increase in uptake potential as
compared to the pristine cells, indicating that functionalized
cells could be a promising alternative for heavy metal removal
(Ma et al. 2015). The biosorption capacity of living cells for
As was reported at 62 µg/g (Wu et al. 2012), while that for
other heavy metals was recorded at 30 mg Zn/g, 64 mg Hg/g,
5.5 mg Cr/g and 8 mg Ni/g (Al-Saraj et al. 1999; Özer and
Özer 2003; Rapoport and Muter 1995; Rossi et al. 2018).
Radionuclides uranium (U) can be removed efficiently by S.
cerevisiae with biosorption capacity for U showing between
150 and 300 mg U/g dry weight biomass in free-living cells
(Chen et al. 2020; Volesky and May-Phillips 1995; Zhang
et al. 2020). Overall, S. cerevisiae cells showed high affinity
and efficient uptake of heavy metals like Pb, U, Hg, and Cd.
The metal sequestering ability of S. cerevisiae has been uti-
lized in the application of cleaning industrial effluents (Ruta
et al. 2010) and in the food industry (Massoud et al. 2019).
Candida spp
Candida is a genus of the yeast family, and many of the spe-
cies within the genus are pathogenic. It is the most common
cause of fungal infection in the human body. Candida species
have been widely studied and are popular microbes for heavy
metal removal (Luk et al. 2017). Luna et al. (2016) showed
that the presence of anionic biosurfactant in the cell wall of
Candida sphaerica could be precipitated and used for efficient
extraction of heavy metals like Fe, Zn, and Pb. In a study to
assess the heavy metal uptake of Ni and Cu by Candida bio-
mass in wastewater, Mersin & Açıkel (2021) showed that all
tested species Candida membranaefaciens, Candida utilis,
Candida tropicalis, and Candida lipolytica have the potential
for metal removal with C. lipolytica showing the highest effi-
ciency among the species. A study by Yin et al. (2008) has
shown that Cr and Ni ions were removed by combining two
yeast species of C. tropicalis and C. lipolytica. The efficiency
of removing heavy metals by the fused yeast was about 80%
for Cr and 64% for Ni after 30 minutes. Rehman et al. (2010)
have described the multiple metal tolerance capacity of C.
tropicalis. It could adsorb 70-90% of the Cd ions from the
medium, depending on the length of the incubation. The
common species of Candida albicans exhibited biosorption of
multiple heavy metals with varying efficiency, Cr with 76%
was the highest, followed by Pb (57%), Cd (46%), As (40%),
Co (37%), and Hg (36%) (Rodríguez et al. 2017). In a study
to analyze the performance of free and immobilized Candida
krusei, Luk et al. (2017) showed that both free and calcium
alginate immobilized C. krusei have good biosorption capacity
for Cu. They further demonstrated that encapsulating the cell
with calcium alginate provides an advantage as it can address
the clogging problem, which is a constant operational prob-
lem in waste treatment.
Filamentous fungi
Filamentous fungi are hyphae-producing macroscopic organ-
isms. The most defining feature of filamentous fungi is the
presence of tubular hyphae, which undergo myriad extensions
depending on the phylum (Harris 2019). Due to their versa-
tile nature, filamentous fungi have been used as cell factories
to produce enzymes, antibiotics, and various materials that
can be utilized as alternatives to plastic. They are known to
degrade organic compounds naturally and produce secondary
metabolites, which can be used in various applications, includ-
ing as anti-microbials (Wösten 2019). Like most fungal fami-
lies, filamentous fungi are cheap to grow, abundant, and
environmentally friendly and have a mesh mycelium network,
providing larger mass and surface retention areas
(Dusengemungu et al. 2020). In Neurospora crassa, a common
filamentous fungus, a study on its heavy metals biosorption
and removal potential showed that accumulation and removal
were achieved by a combined action of binding to the myce-
lial cell wall and proteins involved in accumulation and efflux
(Naveena and Latha 2012). Among the filamentous fungi,
Aspergillus spp., Trichoderma spp., Rhizopus spp., and
Penicillium spp., have been extensively studied.
Aspergillus spp
Aspergillus is a ubiquitous filamentous fungal genus with
several industrial applications and heavy metal-binding
capacity as biosorbent tools (Bapat et al. 2003; Wang and
Chen 2009). It is one of the most extensively investigated
organisms with various applications as a bioleaching agent in
the mining industry due to organic acid production.
Aspergillus spp. also have a good biosorption ability for Pb
(30-35 mg/g) and Cu (25 mg/g) (Dursun, 2006; Wang and
Chen 2009). Further, studies carried out by Kapoor et al.
(1999), Iskandar et al. (2011), Acosta-Rodríguez et al. (2018),
and Zhen et al. (2021) have shown the biosorption capacity
of Aspergillus niger for the removal of Cu, Pb, Cd, Zn, Co
and Hg ions. Aspergillus oryzae, another member of the gen-
era, has been employed to remove Cu, Zn, and Cd (Vianna
et al. 2000). Scleriotial A. oryzae cells displayed an increased
functional group in the sclerotia, which increased the bio-
sorption capacity of the species to Cu ions in solution (Long
et al. 2017). Significant potential for biosorption and removal
of uranium by Aspergillus fumigatus has also been reported
(Bhainsa and D’Souza 1999), though further works need to
be conducted for more validation. Aspergillus tamarii can
recover heavy metals with adsorption capacity in the follow-
ing order Cu, Pd, Co, Ni, and Cr (Saad et al. 2019).
Aspergillus transmontanensis isolated along with Cladosporium
cladosporioides, and Geotrichum candidum from high Cu and
Co contaminated mining soil was able to reduce significantly
the concentration of Cu, Co, Zn, Fe, Mn, and Pb from soil
(Dusengemungu et al. 2022). A practical application of tex-
tile wastewater treatment was executed at Kıvanç Textile,
Turkey, employing an ultrafiltration membrane derived from
Aspergillus carbonarius. The results were remarkable, with a
91% decolorization of the wastewater and achievement of a
substantial 72.3% reduction in COD (Chemical Oxygen
Demand). Significantly, the process demonstrated repeatabil-
ity with successful multiple reused of the ultrafiltration
membrane, underscoring the membrane’s viability for
real-world applications (Isik et al., 2019).

Trichoderma spp
Trichoderma spp. are filamentous ascomycetes. They are
commercially exploited as important biocontrol agents for
plant pathogenic fungi and growth-stimulating properties
(Howell 2003). Trichoderma atroviride, a model species,
shows high tolerance and uptake of heavy metals. The spe-
cies has been reported to be isolated from an industrial
sludge in a study showing tolerance to Cu, Zn, and Cd
(López and Vázquez 2003). A similar investigation on T.
atroviride obtained from Cu-polluted water also revealed
high Cu adsorption in the range of 0.8 to 11.2 mg Cu/g, sug-
gesting the biosorption potential of the cell (Yazdani et al.
2010). Singh et al. (2010) showed that Trichoderma viride
could serve as a potential cost-effective biosorbent for
removing metal ions of Cu, Cd, and Pb. Trichoderma virens,
another species, also displayed heavy metal tolerance to Pb,
Cd, Cu, As, and Zn (Babu et al. 2014). Uranium recovery
and removal by Trichoderma harzianum have been exam-
ined, showing good recovery. However, similar to Aspergillus
spp., more work needs to be done to validate its true poten-
tial as a useful biosorbent (Akhtar et al. 2007; 2009). A
recent study has demonstrated that Trichoderma brevicom-
pactum isolated from the gut of earthworms, is a promising
candidate for heavy metal remediation, with a very high tol-
erance to Pb (Zhang et al. 2020). Trichoderma ghanense iso-
lated from gold and gemstone mines exhibited tolerance to
Cu, Pb, Fe, and As, confirming the existence of fungal spe-
cies in mine tailings soils and the biosorption capacity of T.
ghanense for other heavy metals (Oladipo et al. 2018)
Penicillium spp
Penicillium spp. are diverse group of fungi found in different
environments, commonly in soils, air, and food. The group
contains many species that can remove a wide variety of
heavy metals. Penicillium chrysogenum has been the most
extensively studied species in the Penicillium genus. The
genome sequence of P. chrysogenum is available, which has
enabled lots of fundamental and application studies to be
carried out on the species (Berg 2011). It displayed a varied
level of biosorption capacity of most heavy metals, with the
highest capacity in Pb (116 mg/g), Cu (92 gm/g), Cd
(56 mg/g), and Zn (13 mg/g) (Deng and Ting 2005; Niu
et al. 1993; Wang and Chen 2009). The efficiency of remov-
ing heavy metals by P. chrysogenum has been tested in
wastewater filters. The fungal-based sand filters (FSF) gener-
ated using P. chrysogenum showed enhanced removal of Cu
and Fe (Bello et al. 2021). P. chrysogenum and Penicillium
janthinellum have been investigated as potential biosorbents
for eliminating uranium and thorium (Kapoor and
Viraraghavan 1995). P. chrysogenum isolated from refuse
dumpsite soil showed high lead removal of 1.07 ppm,
3.35 ppm, and 4.19 ppm at 5th, 10th, and 15th day respectively,
indicating the heavy metal removal capacity for both soil as
well as water pollutants (Bala et al. 2020). More recently, the
dead biomass of Penicillium piscarium has been shown to
remove uranium from contaminated water efficiently (Coelho
et al. 2020b). Penicillium simplicissimum also exhibited prom-
ising biosorption capacity to Cd, Cu, Co, Ni, and Cr,
Geomicrobiology Journal 207
showing higher metal binding capacity than other represen-
tative filamentous fungi (Iskandar et al. 2011; Mohammadian
et al. 2017).
Other fungi
Rhizopus arrhizus has demonstrated a significant affinity for
metal uptake, showing biosorption of heavy metals such as
Cu (Preetha and Viruthagiri 2007), Pb (Naja et al. 2005), as
well as Ni and Cr (Bhattachayya et al. 2002). Mushrooms are
fungi extensively studied for its potential for metal uptake.
Mushrooms are macrofungi considered a dietary delight
with vast consumption as a nutritious food source. The
mycelium, stalk, and other body parts display considerable
metal uptake potential. One of the most popular mush-
rooms, Pleurotus, commonly known as oyster mushrooms,
when grown in the vicinity of the smelting area, showed an
accumulation of heavy metals thousand times more than
those in any uncontaminated natural area (Kapahi and
Sachdeva 2017). High Cd, Co, Cu, and Hg uptake has been
reported in a few Pleurotus spp. (Brunnert and Zadražil
1983; Purkayastha et al. 1994). Dulay et al. (2015), while
studying the lead myco-accumulation in five different
Pleurotus spp. observed that the accumulation was maxi-
mum in the third flush of fructification, indicating that the
mycelia gather metals over time, with each fruitification dis-
playing more metal content than the previous. The metal
distribution within the fungal mycelium was mainly uneven,
though the pileus contained more metals than the remaining
body (Oyetayo et al. 2012). Pleurotus ostreatus has been
shown to have potential uses as a biosorbent for radionu-
clides uranium. Its biosorbent capacity was found to be
about 19.9 mg/g under experimental conditions (Zhao et al.
2016). The mechanism for the uptake of metals can be var-
ied, but chemisorption and ion exchange have been the two
most common mechanisms of metal biosorption in Pleurotus
spp. (Joo et al. 2011; Kapahi and Sachdeva 2017). Fibroporia
radiculosa, a brown rot fungus grown on treated wood is
known to increase the production of oxalate, which in turn
can accumulate toxic levels of Cu from the environment as
copper oxalate crystals (Akgul and Akgul 2018). A summary
of some commonly studied fungi for removing 5 systemic
toxicants (Pb, Cd, Cr, As, and Hg) is given in Table 2.
Factors for sustaining the efficiency of fungal
biosorption
Many factors influence the capacity of the cell undergoing
biosorption. Depending on the nature of the requirement, a
well-balanced investment of both chemical and physical
parameters might ensure sustained efficiency. The process
parameters include the chemical and physical properties of
absorbates, the nature of the sorbents, surface areas, reten-
tion time, concentration (metals and biomass), temperature,
and pH (Singleton and Simmons 1996). Studies have revealed
that the efficiency of silver removal by Saccharomyces cerevi-
siae biomass is the highest in the inert stage. The same
study reported decreased biosorption with increasing
208 I. JAMIR ET AL.

Table 2. Summary of potential fungi with their removal capacity for the 5 sys- limited availability of fungal species suitable for use as bio-
temic toxicants (Pb, Cd, Cr, As, and Hg). sorbents, in stark contrast to the broader spectrum offered
Reported by plants and algae. Furthermore, while the metal removal
heavy Biosorption
metal capacity (mg/g) capacity of various fungal-metal interactions is well recog-
Sl.no Fungi species removal or % removal References nized, limited comprehensive information on the underlying
1 Saccharomyces Pb, Cd, Pb: 40-80 mg/g Dong et al. 2023; mechanisms, equilibrium dynamics, and kinetics of sorption
cerevisiae Cr, As, Cd: 10-60 mg/g Wang and Chen, 2009; and desorption hampers the full realization of biosorption
Hg Cr: 5.5 mg/g Al-Saraj et al. 1999;
As: 0.062 mg/g Özer and Özer, 2003 potential (Ramya et al. 2021). Without a profound under-
Hg: 64 mg/g standing of these aspects, the enhancement of biosorption
2 Candida Pb, Cd, Pb: 57% Baysal et al. 2009; capabilities remains an elusive goal. Another obstacle arises
albicans Cr, As, Cd: 40 % Rodríguez et al. 2017
Hg Cr: 76% from the fact that, although numerous pilot-scale batch reac-
As: 46 % tor and ex-situ studies on heavy metal removal exist, the
Hg: 36 % translation of these findings to in-situ natural ecosystems is
3 Neurospora Pb, Cr Pb: up to 95 % Sharma et al. 2021;
crassa (mixed with Tunali, Kiran, and markedly limited. Bioremediation is most effectively applied
other fungi) Akar 2004 in situ, and the scarcity of applications within natural eco-
Cr: up to 95% systems presents a formidable challenge (Negi and Das
4 Aspergillus niger Pb, Cd, Pb: 59 % Dursun, 2006; Kapoor
Cr, As, Cd: 57 % et al. 1999 ; 2023). Bridging this gap between controlled laboratory stud-
Hg Cr: 100 % Acosta-Rodríguez ies and real-world environmental conditions is crucial for
Hg: 83.2 % et al. 2018; the successful implementation of fungal biosorption on a
As: 66 - 98 % Duborská et al.
2020; Littera et al. broader scale. In short, the constrained availability of suit-
2011 able fungal species, the lack of comprehensive knowledge
5 Trichoderma Pb, Cd, Cr Cr: 94 − 100 % Singh et al. 2010; Ali regarding biosorption mechanisms, and the scarcity of in-situ
viride Pb and Cd: Not and Hashem 2007;
defined Morales-Barrera and applications collectively contribute to the underutilization of
Cristiani-Urbina fungal biosorption’s vast potential. Addressing these chal-
2006 lenges needs concerted efforts in research, encompassing a
6 Penicillium Pb, Cd, Pb: 96-116 mg/g Niu et al. 1993; Deng
chrysogenum Cr, As Cd: 21- 56 mg/g and Ting, 2005; deeper investigation of fungal-metal interactions, the refine-
As: 33- 57 mg/g Skowroński, Pirszel, ment of biosorption mechanisms, and the successful transla-
Cr: 18 - 27 mg/g and Skowrońska tion of laboratory findings to real-world ecological contexts.
2001; Loukidou
et al. 2003; Tan and
Cheng 2003
7 Rhizopus Pb, Cd, Cr Pb: 200 mg/g Fourest, Canal and Conclusions
arrhizus Cr: 64 − 78 mg/g Roux 1994; Aksu
Cd: 57.5 - 84 % and Balibek 2007; Fungi, as a diverse group of organisms, encompass various
Uslu et al. 2002; genera that can be regarded as valuable natural resources.
Tobin, L’homme, They serve as proven natural repositories for various chem-
and Roux 1993
icals, offering an environmentally friendly platform for utili-
zation. While substantial research has been conducted on
the biosorption of heavy metals, this wealth of knowledge
biomass concentration, enhanced incubation temperature, provides an economically feasible and sustainable bioremedi-
and decreasing pH (Singleton and Simmons 1996). However, ation approach utilizing a low-cost substrate. Although
more recent works in filamentous fungi have indicated numerous laboratory-scale studies have indicated the poten-
increased metal recovery with increasing biomass concentra- tial of many fungi, their practical application on a commer-
tion, pH, and temperature (Dusengemungu et al. 2020), cial scale remains elusive. The way forward necessitates
though most of the required parameters can be very specific. scaling up operations while concurrently enhancing
Investigations by Tsekova and Todorova (2002) and Cárdenas large-scale industrial applications. Advancements in the bio-
González et al. (2019) showed that rising Cu concentration technology field present an opportunity to improve micro-
in living Apergillius cells stimulated enzymatic activity, which bial organisms, either by enhancing their absorption capacity
led to an increase in Cu uptake, indicating metal sequestra- or through genetic engineering to bolster the bioaccumula-
tion potential and removal of the living cells when ade- tion of pollutants released into the environment. Research
quately stimulated. The influence of these different has demonstrated that functionalized or chemically modified
parameters on the metal recovery process largely varies with cells can increase metal accumulation capacity in certain
the species. Therefore, a more precise influence by different species. Therefore, earnest efforts should be directed toward
parameters has to be investigated for any fungal species developing alternative customized cell designs through
when used for various applications. chemical treatment or genetic engineering to create novel
biosorbents.
Fungal bioremediation challenges An area for future exploration should involve a compre-
hensive understanding of the mechanisms underlying the
Fungal biosorption, despite its considerable bioremediation interaction between adsorbates and adsorbents. The com-
potential and minimal drawbacks, has yet to achieve wide- plexity of this interaction, involving numerous parameters,
spread application. One contributing factor may be the poses a challenge for efficient metal binding if the requisite

conditions are not clearly defined. While fungi are recog-
nized for their effectiveness as adsorbents, the intricacies of
the biosorption process have not been adequately explored.
Only with a thorough comprehension of this mechanism can
we endeavor to engineer or manipulate organisms to enhance
biosorption efficiency. Another prospect worth considering
is the economic viability of the process. Often, research
focuses on dealing with extensive industrial effluents, which
tend to falter in large-scale commercial applications due to
their high costs. Exploring alternatives in smaller-scale appli-
cations at localized sites within industries like cosmetics, fer-
tilizer, and pharmaceuticals, which are major sources of
heavy metal release, may mitigate the challenges associated
with fungal biosorption. Biosorption is an expanding tech-
nology with vast potential applications in environmental
waste cleanup. The application of fungal biosorption for
heavy metal removal can be implemented in terrestrial and
aquatic ecosystems. It holds the immense potential to allevi-
ate heavy metal toxicity within natural habitats and serves as
a potent catalyst for controlling the release of harmful envi-
ronmental pollutants. Given its significance and potential,
further research into fungal biosorption is undoubtedly
warranted.
Disclosure statement
No potential conflict of interest was reported by the author(s).
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