Review

Received: 19 November 2020 Revised: 28 February 2021 Accepted article published: 9 March 2021 Published online in Wiley Online Library:

(wileyonlinelibrary.com) DOI 10.1002/jctb.6721

Surfactant-aided mycoremediation of soil

contaminated with polycyclic aromatic
hydrocarbon (PAHs): progress, limitation,
and countermeasures
Abiram Karanam Rathankumar,a Kongkona Saikia,a
Ponnusamy Senthil Kumar,b Sunita Varjani,c* Shravani Kalita,a
Nikhil Bharadwaj,a Jenet Georgea and Vinoth Kumar Vaidyanathana*

Abstract
Soil contaminated with hydrophobic organic hydrocarbons, such as polycyclic aromatic hydrocarbons (PAHs), pose a serious
threat to the ecosystem and human health. Moreover, the sorption and desorption of the PAHs, due to the interaction with
the soil organic matter (SOM) and other contaminants, greatly affect the fate and mycoremediation efficiency of the contami-
nated soil. On the other hand, the application of surfactants with or without additives for the mobilization of PAHs from con-
taminated soil has garnered increasing attention for soil remediation. In this context, several commercial surfactants and
biosurfactants were reported either as soil flushing agents or soil additives, followed by either in situ or ex situ mycoremedia-
tion of the PAHs from contaminated soil. Hence, for a successful implementation of surfactants for mycoremediation of contam-
inated soil, a comprehensive introspection on its chemistry and mechanism is necessary. Thus, this review focuses primarily on
understanding the effect of surfactants and the mechanism of desorption of PAHs from the soil. This work also emphasizes the
effect of surfactants on the efficiency of mycoremediation of contaminated soil. Further, the review summarizes various
surfactant-assisted mycoremediation strategies of contaminated soil. Finally, the limitations of surfactant-assisted mycoreme-
diation, precipitative, and partitioning loss, along with toxicity of the surfactants, were reviewed. Thus, this review will aid in
understanding the underlying mechanism and efficiency of surfactant-assisted mycoremediation and it also proposes current
research trends to improve the efficiency and enhance the bioremediation of PAHs-contaminated soil.
© 2021 Society of Chemical Industry (SCI).

Keywords: surfactant; mycoremediation; polycyclic aromatic hydrocarbons; reactor; soil flushing agents; soil additives

INTRODUCTION
The burgeoning population of the world and its associated
increase in industrial, human, and anthropological activities have
contributed to an exponential increase in the concentration of
toxic contaminants in the environment. Per the International
Union for Nature Conservation, the impact of these contaminants
is considered high and this is reflected by the threat to more than
1141 species.1 On the other hand, due to the visible contaminant
impact on the air and water ecosystems, more emphasis has been
given to air and water pollution by both scientific and non-
scientific communities. Apart from major nuclear disasters, such
as Fukushima Daiichi (2011) and Chernobyl (1986), and heavy
metal contaminantion, such as Dzerzhinsk (Russia), Kabwa
(Zambia), and La Oroya (Peru), a prevalent emphasis on the other
Bangladesh (tannery waste), Tirupur, India (textile dyes), has chan-
ged the course of environmental research towards the soil
pollution.
Due to the vast classifications of contaminants present in the
soil, for the sake of simplicity, these compounds are grouped
either as organic or inorganic contaminants.2 Almost all of the
organic pollutant structures consist of carbon and hydrogen as a
backbone and can be classified as petroleum hydrocarbons,
* Correspondence to: S Varjani, Gujarat Pollution Control Board, Gandhinagar
382010, Gujarat, India. E-mail: drsvs18@gmail.com; or VV Kumar, Integrated
Bioprocessing Laboratory, Department of Biotechnology, SRM Institute of Sci-
ence and Technology, Chennai, Tamil Nadu 603203, India. E-mail:
vinothkv@srmist.edu.in

sources of soil pollution is still needed. Because soil acts as the ulti-
mate sink for contaminants, soil pollution leads to several hazard-
ous health effects, including premature birth, gastric problems,
cancer, mental retardation, and miscarriage. Moreover, the pres-
ence of major soil polluted lands areas, such as Niger river delta
(petroleum Hydrocarbon), Accra, Ghanaian (e-waste), Hazaribagh,
a Integrated Bioprocessing Laboratory, Department of Biotechnology, SRM Insti-
tute of Science and Technology, Chennai, India
b Department of Chemical Engineering, Sri Sivasubramaniya Nadar College of
Engineering, Chennai, India
c Gujarat Pollution Control Board, Gandhinagar, India
1

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 www.soci.org
pesticides, pharmaceutical and their derivatives, and chlorinated
compounds.3 On the other hand, the inorganic contaminants
consist of radioactive compounds, heavy metals, salts, and nutri-
ents. Irrespective of the structural and chemical diversity of these
contaminants, their hydrophobic nature and structural stability
makes them persistent to degradation. These contaminants have
the ability to bind to soil organic matter (SOM), which masks their
presence and, thus, resists the process of degradation. The Envi-
ronmental Protection Agency (EPA) grouped 126 contaminants
as priority pollutants under the Clean Water Act of 1977 depend-
ing on their levels of toxicity and persistency.4 Among these prior-
ity pollutants, polycyclic aromatic hydrocarbons are the most
widely investigated petroleum hydrocarbons compounds due to
their potential toxicity and persistence in nature for degradation.5
On the other hand, the hydrophobic nature of the Polycyclic Aro-
matic Hydrocarbons (PAHs) often makes conventional treatment
strategies less efficient due to its low bioavailability. One of the
strategies used to increase the bioavailability of the PAHs in the
soil matrix is by the application of surface-active compounds or
surfactants.6, 7 Having the ability to increase the bioavailability
of PAHs in soil by reducing the surface tension between two
phases, the surfactant-based remediation process has become a
focus of interest in soil remediation. Despite the several reviews
avaiable on surfactant-aided bioremediation, most of the studies
have reported on the role of surfactants in PAHs solubilization,6
remediation of soil with surfactants,7 comparison studies on vari-
ous surfactants in bioremediation of PAHs,8 and techniques
involved in surfactant-aided remediation.9 However, there is a
limited review on the surfactant-aided mycoremediation of
PAHs-contaminated soil and their interactive role in the degrada-
tion of PAHs. Hence, this review aims to address the research gap
on the surfactant-aided mycoremediation of PAHs-contaminated
soil by emphasizing the role of surfactants in bioremediation,
exploring the interactive effect of surfactants in enhancing the
bioremediation efficiency of fungi, and discussing various
surfactant-enhanced mycoremediation technologies.
OCCURRENCE, TOXICITY, AND NEED FOR
PAHS REMEDIATION
Polycyclic aromatic hydrocarbons (PAHs) are some of the most
severely detrimental organic contaminants to the soil ecosystem,
and they are classified under Hydrophobic Organic Compounds
(HOCs).10 Most of the PAHs occurr due to anthropogenic activities
associated with urbanization and industries, as well as those due
to natural activities, such as volcanic eruption. Depending on their
occurrence, PAHs can be grouped into four types: (i) Petrogenic
(derived from fuels), (ii) Pyrogenic (derived from incomplete com-
bustion), (iii) Biogenic (produced by organic metabolism), and
(iv) Diagenetic (produced by transformation process)11 (Fig. 1).
With a linear fused aromatic ring to cluster the arrangement of
rings, these PAHS are electrochemically stable, persistent, and
resist degradation, and they also exhibit an increase in toxicity
with an increase in the aromatic ring number, hydrophobicity,
and structural angularity.4
The toxicity from chronic exposure to PAHs includes cancers
and skin irritation, and it has been reported to also affect the
immune, endocrine, and neural systems.12 In general, low molec-
ular weight PAHs (LWM) with two or three aromatic rings are con-
sidered toxic, and high molecular weight PAHs (HWM) are
considered to be genotoxic.13 Besides, the ability of the PAHs to
adduct covalently to genetic material (DNA, RNA, and proteins)
2
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AK Rathankumar et al.
makes them carcinogenic. Based on their toxicity and abundance
in the environment, 16 PAHs have been listed as priority pollut-
ants (which are highly toxic) by the United States Environmental
Protection Agency (US-EPA).4 Out of these 16, naphthalene causes
methemoglobinemia and acute intravascular hemolysis,14 ace-
naphthylene is carcinogenic to humans, and acenaphthene
induces intraperitoneal toxicity and irritation to humans and ani-
mals' skin.12 Further, fluorene was found to cause oral neurotoxic-
ity, as well as intraperitoneal and behavioral toxicity in adult male
rats.15 Phenanthrene was found to induce hepatotoxicity in rats
and affect the translation and adenosine triphosphate synthesis-
coupled electron transport in Enchytraeus crypticus.16 Another
common PAH, pyrene, reduces the reproduction rates in nema-
tods.17 Benz[a]anthracene and benzo[b]fluoranthene inhibit anti-
oxidant capacity, which causes lipid peroxidation and cell
damage.18, 19 Chrysene is another toxic PAH that antagonizes
the estrogen receptor and causes cardiac malformations, as well
as ocular and circulatory defects in aquatic organisms.19 Benzo
[e]pyrene affects human health by inhibiting apoptosis in human
retinal pigment epithelial cells.20 Similarly, benzo[a]pyrene
induces tumor formation in humans, along wit, immunosuppres-
sion, teratogenicity, hormonal effects, and disruption of protein–
protein signaling pathways.21 The physical and chemical proper-
ties of the 16 PAHs are mentioned in Table 1.
Consequently, the remediation of PAHs is considered crucial to
restoring the environment. Due to the toxicity effects of PAHs, sig-
nificant interest has been focused on the development of various
physical,9 chemical,22 and biological treatment technologies.23
However, most of the conventional (physical and chemical) pro-
cesses involve the removal or transfer of PAHs from one environ-
ment to another, resulting in partial remediation of PAHs from the
soil. Moreover, the utilization of multiple chemicals or adsorbents
involving complex and less environmentally-friendly processes
makes most of the conventional processes not very feasible
industrially . On the other hand, utilization of microorganisms
for the bioremediation of PAHs by exploring their detoxification
ability has gained more attention recently. Bioremediation
addresses the demerits of the conventional remediation process
by bio transforming hazardous PAHs into less toxic compounds,
making them eco-friendly and economic. In a conventional biore-
mediation strategy, the application of microorganisms involves
applying (as single or in a consortium) bacteria, fungi, yeast, or
algae to the remediating site. This microorganism either reduces
the organic compounds into inorganic compounds, such as water
and carbon dioxide (biomineralization), or transformation them
into lesser toxic small chains of organic compounds (biotransfor-
mation). Being a natural process, the application of microorgan-
isms for the bioremediation strategy ensures the release of
harmless products into the environment. Moreover, in compari-
son with other strategies, in situ augmentation of microorganisms
causes less damage or disruption to the native environment and is
also considered to be a cost-effective process. However, due to
the ability of fungi to secrete an extensive range of degradative
enzymes, fungi are widely applied as bioremediating agents over
microorganisms. The ability of fungi to utilize complex organic
hydrocarbon as a carbon source made them preferable to bacte-
ria. Further, application of surfactants during bioremediation
strategy was reported to enhance the mass transfer of nutrients
and, thereby, increase the degradation efficiency of the microor-
ganisms. However, due to the complexity of the soil and its inter-
action with PAHs and other organic pollutants, complete
remediation involving biological systems is often limited.5
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Figure 1. Key characteristics, major sources, and toxicity of PAHs.

Table 1. List of 16 -PAHs along and their carcinogenicity group, as per US-EPA (where B2:possibly carcinogenic to humans; D: non carcinogenic; and
NA: not available)

Name Molecular weight (g mol−1) Partition coefficient (log Kow) Water solubility (mg L−1) Carcinogenicity group

Acenaphthene 154.21 3.98 1.93 NA

Acenaphthylene 152.2 4.07 3.93 D
Anthracene 178.2 4.45 0.0076 D
Benz(a)anthracene 228.29 5.61 0.010 B2
Benzo(a)pyrene 252.3 6.06 0.0023 B2
Benzo(b)fluoranthene 252.3 6.04 0.00125 × 10−7 B2
Benzo(ghi)perylene 276.34 6.50 0.00026 D
Benzo(k)fluoranthene 252.31 - — B2
Chrysene 228.3 5.16 0.0028 B2
Dibenz(a,h)anthracene 278.35 6.84 0.00051 × 10−10 B2
Fluoranthene 202.26 4.90 0.20–0.26 D
Fluorene 166.2 4.90 1.68–1.98 D
Indeno(1,2,3-cd) pyrene 276.3 6.58 0.062 B2
Naphthalene 128.17 3.37 — D
Phenanthrene 178.2 4.45 1.20 D
Pyrene 20.3 4.88 0.077 NA

Moreover, in a real soil matrix, the PAHs are often present in
anoxic conditions, which makes aerobic microorganisms less effi-
cient in the degradation of PAHs in the soil.24 In addition, the
masking ability of the soil organic matters (due to hydrophobic
interaction of the PAHs), and its role as the bioremediation decid-
ing factor, makes the study of soil properties pivotal.
To understand the fate of PAHs in the soil environment, it is cru-
cial to know about the soil properties and functionality. The
dynamic naturally-occurring soil on the soil surface is generally
formed from earth crust, either due to living organism action or
weather agents.25 Being the ultimate sink for pollutants, the phys-
ical and chemical properties of the soil are diverse and depend on
the solid fraction raised from the parental earth crust. A major
fraction of the soil includes minerals, soil organic matter, water,
and air, and their combination determines the texture, color,
porosity, permeability, soil microbiota, and chemical profile of
the soil.25 Among them, the negatively charged organic fraction
in the soil is reported to be responsible for sequestering positively
charged compounds (including minerals, nutrients, and other
hydrophobic compounds), thereby acting as a prime nutrient
source for the plants and other soil living organisms. On the other
hand, SOM also plays a major role in sequestering the PAHs in the
soil, either by hydrophobic interaction or pi-pi interactions.26
Moreover, the presence of surface functional groups (such as
-OH-,-COOH, -SH, and -C=O-) on the SOM, due to humic com-
pounds, attributes a strong affinity towards PAHs in the soil,
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thereby reducing their bioavailability.26 In addition, the presence
of other inorganic ions (Cl-, HPO4, NO3-, and SO42-) and chelating
agents (EDTA, organic acids), in turn, substantially influences the
bioavailability of the PAHs for bioremediation.27 One of the strat-
egies to enhance the bioavailability of PAHs in the soil is the appli-
cation of surface-active compounds or surfactants.
SURFACTANTS IN THE REMEDIATION OF
CONTAMINATED SOIL
Surfactants
Surfactants, or surface-active compounds, are amphiphilic com-
pounds with a hydrophobic ‘head’ and a hydrophilic ‘tail’, and
they exhibit a wide range of properties, such as surface tension,
emulsification index, etc.28 The commonly utilized surfactants
and biosurfactants for the bioremediation of PAHs are mentioned
in Table 2. The major property of surfactants is their ability to
reduce the interfacial tension between two immersible phases.
Both synthetic and biosurfactants have the ability to reduce the
surface tension of water below 30 mN/m.29 At lower concentra-
tions, the surfactant molecules tend to exist in the form of mono-
meric units in aqueous solutions. Upon reaching a specific
aqueous concentration, which is exclusive to each kind of surfac-
tant and termed as Critical Micelle Concentration (CMC), the mol-
ecules of surfactant start formulating into micelles.30 The number
of monomer surfactants required for micelle formation generally
differs between 50 and 100, it is identified as aggregation number
and, in general, the higher the hydrophobicity of the surfactant,
the higher will be the aggregation number.31 Factors such as
the composition and structure of the surfactant, ionic strength,
and temperature govern the CMC value.32 In terms of structural
property, with the increase in the hydrocarbon chain length,
CMC values were reported to decrease due to the increase in
hydrophobicity.33 Per Traube's rule, the addition of -CH2- to the
hydrophobic group leads to the 3-fold reduction in the CMC
value.34 Also, electrolytes in the solution may trend to reduce
the CMC value by reducing the electrical repulsion among surfac-
tant hydrophilic heads, and this effect was more prominent in cat-
ionic and anionic surfactants than in non-ionic surfactants.
Apart from CMC, the hydrophilic and hydrophobic moieties bal-
ance (HLB) is considered another governing factor of the effi-
ciency of a surfactant.35 The value of HLB provides information
on whether a surfactant produces oil in water or water in oil
emulsion. The surfactants with low HLB values (3–6) are lipophilic
and form water in oil emulsion, whereas those with high HLB
Table 2. Commonly utilized surfactant and its surface active properties utilized in bioremediation (*: MW = Molecular weight)
Surfactant MW* (g mol−1)
SDS 288
Triton X-100 628
Tween 80 1310
CTAB 364.45
Brij 35 1198
Rhamnolipid 577
Saponin 1800–2000 Da
Lecithin 773
Sorpholipids 706
Abbreviations: CTAB: Cetyl trimethylammonium bromide; MW: Molecular weight; SDS: Sodium Dodecyl Sulphate.
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AK Rathankumar et al.
(10–18) are hydrophilic in oil in water emulsion.36 Classification
of surfactants by HLB values aids in the selection of the best sur-
factant for various applications. In the case of PAHs remediation
from contaminated soil, the surfactant with more than 10 HLB
has been reported to be efficient.37 Surfactants possessing high
HLB tend to increase the water solubility of the contaminants pre-
sent in the soil.
Mechanism of surfactant on PAHs remediation
When surfactants are introduced into the soil water environment,
they tend to interact with soil particles and may adsorb on the sur-
face of the soil. The hydrophobic ‘tail’ is apt to interact with soil
particles and, at below the concentration of CMC values, the sur-
factant (as a monomer) accumulates at solid–liquid or liquid–
liquid interface.29 The increase in the surfactant concentration
results in the gradual replacement of interfacial water solvents
and it reduces surface tension, which results in the acceleration
of PAHs dissolution. In addition to this, adsorption of the surfac-
tants on the soil surface creates a repulsion force, which promotes
the partitioning and mobilization of contaminants.38, 39 Further,
these repulsion forces decrease the oil-soil and water–oil values
of interfacial tension, thereby leading to an overall reduction in
the the capillary force that holds soil together with crude oil.38
Further increase in the concentration of surfactants leads to the
formation of spheroidal or ellipsoidal micelles with a lipophilic
core and a hydrophilic surface, thereby aiding in trapping PAHs
and drastically improving their solubility in the aqueous phase.
In general, surfactant-enhanced PAHs remediation can result from
two discrete mechanisms: (i) soil roll-up mechanism (mobiliza-
tion), and (ii) solubilization.40 The surfactant monomer adsorbed
on the surface of the soil particles below the CMC is responsible
for the soil roll-up mechanism.40 The adsorbed surfactants cause
repulsion between the hydrophilic head group and the soil parti-
cles, resulting in the dissolution of PAHs from the soil particles.41
In addition, the surfactants change the wettability of the soil sys-
tem by accumulating on soil water and soil PAHs interface.42 Once
adsorption attains saturation, the surplus surfactant molecules
begin to form aggregations and, subsequently, formulate into
micellar particles in a heavy solution. At the concentration above
the CMC value, solubilization of PAHs occurs by trapping the
hydrophobic organic pollutants in the lipophilic micelle core of
surfactants.28 After attaining micelle level, the surfactant exhibits
its lowest possible surface tension. The shape and structural prop-
erties of the micelle formed determine the efficiency of surfac-
tants in solubilizing (or detaching) and mobilizing PAHs from
Charge type CMC (mM) HLB
Anionic 8.10 40.0
Non ionic 0.31 13.5
Non ionic 0.01 15.0
Cationic 0.9 10
Non ionic 0.05 16.9
Anionic 0.02 22–24
Non ionic 0.87 —
Zwitterionic 0.6 3–4
Zwitterionic 0.15 12–13
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Surfactant-aided mycoremediation of soil contaminated with PAHs
soil.43 Although solubilization starts at a point belonging to CMC
itself, the most suitable efficiencies of removal are found at con-
centrations that are way higher with respect to the CMC value.
On the other hand, the CMC required for micelle formation greatly
varies with respect to the interface. For instance, Triton X-100
(or TX-100) exhibits CMC at 0.3 mmol L−1 in an aqueous system;
however, in a soil matrix, its CMC value was found to increase
up to 0.9–1.7 mmol L−1.
Types of surfactants utilized in PAHs remediation
Surfactants utilized for soil remediation can be broadly classified
as ionic (anionic and cationic) and non-ionic surfactants based
on their surface charge of head moieties (Fig. 2). These distinct
classes of surfactants are characterized by having a diverse surfac-
tant property affecting the ability for solubilization of PAHs in a
significant manner.
Classification based on the polarity of surfactant head group
Ionic surfactants:. Cationic surfactants are those possessing a posi-
tive charge on their surface and they dissociate in water to yield
an amphiphilic cation and an anion. A considerable fraction of this
particular class contains nitrogenous compounds, like fatty salts of
amine and quaternary salts of ammonium. Each surfactant has a
head group carrying a positive charge and a tendency to rigidly
adsorb onto surfaces with negative charges (such as hair, fabric, sed-
iment, bacterial cell membranes, and soil) with the link established
by electrostatic synergies.44 Generally, these positively charged cat-
ionic surfactants constitute a smaller surfactant class that finds its
common uses in the form of antibacterial agents, hair conditioners,
and fabric softeners.45 Cationic surfactants have good compatibility
with the non-ionic case of surfactants to form mixed surfactants but
they are mostly incompatible with those of anionic surfactants.
However, utilization of cationic surfactants for the process of soil
washing is limited due to its high adsorption towards soil particles,
resulting in loss of the surfactant and, subsequently, requiring a high
volume of surfactants to achieve a desirable PAHs remediation
efficiency.44, 46
Anionic surfactants are characterized by the presence of a
negatively charged hydrophilic head group. This class of sur-
factant is the most abundantly used and it is commonly utilized
in shampoos and in liquids for dishwashing and laundering
agents because of its exceptional cleaning property. The most
commonly utilized anionic surfactants include linear alkylben-
zene sulfonates (LAS), sodium dodecyl sulfate (SDS), alcohol
Figure 2. Classification of surfactants based on chemical structure and the source of occurrence.
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sulfates (AS), secondary alkane sulfonates (SAS), and alcohol
ether sulfates (AES). Amongst LAS is considered to be a first-
generation surfactant that was popular for its efficient deter-
gent properties. In comparison with cationic surfactants,
anionic surfactants are less toxic.47 However, anionic surfac-
tants exhibit a binding tendency towards bioactive molecules
(such as DNA, proteins, and enzymes) that makes them poten-
tially toxic to the soil microbiota.48 In addition, most of the
anionic surfactants exhibit higher values of CMC, which results
in the need for a higher concentration of surfactants for the sol-
ubilization of PAHs from the soil.
Non-ionic surfactants:. Non-ionic surfactants are a group of
surfactants that are hardly ionized in aqueous solution and usually
consist of an oxygen-containing functional group in their hydro-
philic moiety. The solubility of this class of surfactants can be
attributed to the formation of intermolecular hydrogen bonds
between the hydrophilic groups and the water molecules. The
process of micelle formation takes place rapidly due to the sepa-
ration of the hydrophilic groups in the aqueous phase and the
subsequent agglomeration of the hydrophobic cores with each
other.38 The non-ionic surfactant overcomes the difficulty of ionic
surfactants in micellization due to the electrostatic repulsion
between head groups during aggregation. As a result, most of
the non-ionic surfactants exhibit lower CMC values than the ionic
surfactants.29, 49 On the other hand, with their enhanced solubili-
zation property and low toxicity, these surfactants are commonly
utilized in the remediation of PAHs-contaminated soil. It has been
reported that non-ionic surfactants can perform efficiently under
adverse contaminants (such as hardness, salinity, and acidity)
because these surfactants are unaffected by the presence of elec-
trolytes and divalent cations49, 50. However, the high adsorption
property of non-ionic surfactants on the soil particles, resulting
in lower availability of surfactants for remediation, makes the
use of this class of surfactants uneconomical.46
Classification based on source of surfactant
Depending on the source of the surfactant, surfactants can be
widely classified as synthetic (chemical) surfactants and biosurfac-
tants (Fig. 2). The surfactants that were synthetized by chemical
process using synthetic chemicals or fossil fuel as a raw material
are called synthetic surfactants. On the other hand, the surfac-
tants that were synthesized by biological means are categorized
as biosurfactants.
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Biosurfactants:. The wide availability and low production cost of SURFACTANT-ASSISTED

synthetic surfactants have made them the most commonly uti-
lized for remediation of the soil. However, their resistance to deg-
radation with adsorption ability to bioactive macromolecules
resulted in them being less eco-friendly.28 As an alternative, the
surfactant that is produced via a biological process and is grouped
as a biosurfactant is considered to be a substitute for synthetic
surfactants. Most of the biosurfactants are metabolic by-products
of microorganisms and have high surfactant properties with high
tolerance to extreme environmental conditions.51, 52 Similar to syn-
thetic surfactants, biosurfactants are amphiphilic with a hydropho-
bic tail and a hydrophilic head and they have the characteristic
feature of hydrophobic-hydrophilic balance (HLB).51 The majority
of the biosurfactants are either anionic or non-ionic in nature, with
an exceptional few being cationic. Unlike synthetic surfactants, bio-
surfactants are categorized by their molecular weight as low-molec-
ular-mass biosurfactants (glycolipids, phospholipids) and high
molecular mass biosurfactants (lipopolysaccharides, lipoproteins).53
In general, high molecular weight biosurfactants are efficient as
emulsifiers, whereas low molecular weight biosurfactants are effec-
tive in lowering the interfacial tension and surface tension. The bio-
surfactant has the ability to reduce the surface tension of water to as
low as 20 mN/m from 72 mN/m.53 The commonly utilized microbial-
biosurfactant for the bioremediation of PAHs in contaminated soil
includes glycolipids (rhamnolipids, sophorolipids), lipopeptides
(Iturin, surfactin), and humic substances (Table 3). Commercially,
these biosurfactants were produced using fermentation technol-
ogy, for example, rhamnolipids by Pseudomonas aeruginosa,76 sur-
factin by Bacillus subtilis,77 and mannosylerythritol lipids by
Candida antarctica.78 Similar to the synthetic surfactants, the biosur-
factants exhibit a similar mechanism in the remediation of PAHs
involving mobilization and solubilization steps.
MYCOREMEDIATION
Mycoremediation of PAHs-contaminated soil
Among several bioremediation approaches of PAHs, mycoreme-
diation is considered efficient and environmentally friendly for
the remediation of contaminated soil.79 Fungi are a diverse group
of organisms with a ubiquitous nature and they are considered a
prime decomposer of organic matter. Their ability to grow in a
wide range of habitats (ranging from water to terrestrial environ-
ments) and in extreme environments (such as in alkaline soil
and deserts) makes them ideal for the remediation of PAHs-
contaminated soil;38 the commonly utilized fungi (basidiomycota
and ascomycota) are mentioned in Table 4. In this context,
Rathankumar et al. showed that Trametes hirsuta, Phanerochate
chrysosporium, Pleurotus ostreatus, and Cadophora sp. displayed
a high capacity for mycoremediation of PAHs in hyperalkalophile
industrial effluents.5 Further, González-Abradelo et al. used Asper-
gillus sydowii and Aspergillus destruens for PAHs mycoremediation
in high salinity conditions.105 The massive fungal growth aids in
the enhancement of soil properties by entrapment mechanism
and adhesion of the soil particles with mycelia, and it also helps
in the improvement of nutrient bioavailability.79 Further, the
hyphae growth of the fungi enables it to penetrate into the soil
particles, making the PAHs available for degradation. On the other
hand, the PAHs have a structural similarity with lignin molecules,
and fungi degrade the PAHs in the soil by secreting a series of
intracellular and extracellular enzymes.5 Depending on the group
of fungi and the secreted enzymes, the fungi utilized for mycore-
mediation can be categorized as ligninolytic fungi and non-
ligninolytic fungi.79 Most of the macro-fungi include wood- and
soil-inhabiting ascomycota and basidiomycota, which have the

Table 3. Biosurfactants and their sources, bacteria, and fungi

Source organism

Biosurfactant Bacteria Fungi Reference

Trehalose lipids Tsukamurella spumae 54

Tsukamurella pseudospumae
Rhodococcus sp. 55
Gordoniae sp 56
Nocardia farcinica 57
Rhamnolipids Pseudomonas aeruginosa 58
Burkholderia Sp 59
Engineered Saccharomyces cerevisiae 60
Sophorolipids Candida bombicola 61
Candida keroseneae 62
Starmerella bombicola 63
Cellobiose lipids Sporisorium scitamineum 64
Trichosporon porosum 65
Pseudozyma hubeisensis 66
cryptococcus humicola 67
Xylolipids Lactococcus lactis 68
Surfactin Bacillus subtilis ,6970
Bacillus nealsonii 71
Iturin Bacillus amyloliquefaciens 72
Bacillus natto 73
Mannosylerythritol lipids Pseudozyma aphidis 74
Ustilago maydis 75
6

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Table 4. Commonly utilized ascomycota and basidomycota for bioremediation of polycyclic aromatic hydrocarbons (PAHs)

Technique and conditions utilized

S.No. Fungi for mycoremediation PAH(s) removed Removal percentage(s) Reference

Basidiomycota
1. Pleurotus ostreatus Sterilized wheat straw inoculated Fluoranthene, Phenanthrene, Fluoroanthene: 77%; Phenanthrene: 80
with agar plugs from 14-days-old Anthracene, Pyrene, 87%; Anthracene: 62%; Pyrene:
P. ostreatus cultures on malt Chrysene, Benzo[a]pyrene 70%; Chrysene: 57%; Benzo(a)
extract agar, incubated for pyrene: 69%
14 days at 28°C and colonized
matrix mixed with contaminated
soil (1:4, wheat straw: soil)
2. Oudemansiella Soil spiked with pyrene, placed in Pyrene 87.2% 81
radicata individual plastic pots, inoculated
with O. radicata along with
compost transplanted into each
pot and cultivated in a greenroom
3. Peniophora Fungal stock inoculated in petri dish Phenanthrene, Fluoranthene, Phenanthrene: 86.5%; Fluoranthene: 82
incarnata containing 50 g of soil with PAHs Pyrene 77.4%; Pyrene: 82.6%
KUC8836 and incubated in dark at 27°C for
4 weeks
4. Coriolopsis Incubated in minimal salt broth in a Phenanthrene, Anthracene, and phenanthrene (~78%), anthracene 83
caperata conical flask containing 50 mg L−1 Pyrene (~65%), and pyrene (~78%)
5. Fomes fomentarius of each PAHs under 120 rpm phenanthrene (~90%), anthracene
BM745 agitation (~78%), and pyrene (~72%)
6. Pluteus phenanthrene (95.6%), anthracene
chysophaeus BM (85.2%), and pyrene (89.5.9%)
792
7. Crucibulum laeve Attenuation of Crucibulum left in soil Phenanthrene and Pyrene Phenanthrene (64%) and pyrene 84
for 60 days (41.7%).
8. Pleurotus ostreatus Fungus grown at 24–26°C in a Pyrene 89.8% 85
basidiomycete rich medium
supplemented with yeast extract,
D-glucose, peptone and
0.05 mg L−1 PAHs
9. Pleurotus dryinus Incubation of 5% culture in Phenanthrene and Benzo(a) Phenanthrene 99% and Benzo(a) 5
IBB 903-A phenanthrene and benzo(a) pyrene pyrene 48.5%
pyrene spiked soil
10. Irpex lacteus Incubation of contaminated soil with Fluorene, Phenanthrene, Fluorene: 67%; Phenanthrene: 56%; 86
I. lacteus for 14 weeks Anthracene, Fluoranthene, Anthracene: 49%; Fluoranthene:
Pyrene, Chrysene and Benzo 57%;Pyrene: 42%; Chrysene: 32%;
[a]anthracene and Benzo[a]anthracene: 20%
11. Anthracophyllum Inoculation of autoclaved soil with A. Phenanthrene, Anthracene, Phenanthrene (62%); Anthracene 87
discolor discolor without the presence of Fluoranthene, Pyrene, Benzo (73%); Fluoranthene (54%);
indigenous microorganisms [a]pyrene Pyrene (60%); Benzo(a)pyrene:
(75%)
12. Fomes Fungal strains isolated upon Anthracene 91% 88
inoculation on malt agar extract
medium and incubated at 26°C
for 7 days.
13. Hypoxylon Incubation of white rot fungi in acenaphthene; acenaphthylene, acenaphthene 82.0%; 89
fragiforme liquid media containing 2% malt anthracene; acenaphthylene 90.3%;
extract and 0.05% glucose 1,2-benzanthracene; benzo(k) anthracene 17.8%;
fluoranthene; byphenil; 1,2-benzanthracene 5.8%;
fluorene; phenanthrene and byphenil 50.5%; fluorene 85.8%;
pyrene. phenanthrene 65.5%; pyrene
42.5%.
7

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 www.soci.org AK Rathankumar et al.

Table 4. Continued

Technique and conditions utilized

S.No. Fungi for mycoremediation PAH(s) removed Removal percentage(s) Reference

14. Coniophora acenaphthene 79%; acenaphthylene

puteana 80%; anthracene 41.3%;
1,2-benzanthracene 53.8%;
benzo(k)fluoranthene 20.3%;
byphenil 15.8%; fluorene 74.8%;
phenanthrene 47.5%; pyrene
50.5%.
15. Ganoderma Incubation in mineral salt broth Phenanthrene and Pyrene Phenanthrene 99.65% and pyrene 90
lucidum CCG1 containing 20 mg L−1 of 99.58%
phenanthrene and pyrene for
30 days at 27 °C
16. Trametes hirsute Incubation of wood assisted fungal Phenanthrene and Benzo(a) Phenanthrene 91.26% and Benzo(a) 28
system in liquid media spiked with pyrene pyrene 87.72%
phenanthrene and benzo (a)
pyrene
17. Marine-derived Incubation of 0.08 mg mL−1 of Pyrene 100% 91
Marasmiellus sp. pyrene with fungus for 48 h under
CBMAI 1062 saline condition
18. Spent mushroom of Incubation of spent mushroom in 16 PAHs cocktail 34.5% 92
Pleurotus age old soil for 60 days
ostreatus
19. Spent mushroom of 41.3%
Pleurotus eryngii,
20. Spent mushroom of 19.4%
Auricularia
auricular
Ascomycota
1. Scopulariopsis 30 days of incubation of soil with Phenanthrene, Fluoranthene, Phenanthrene: 60%; Fluoranthene: 93
brevicaulis fungal strain in liquid medium Pyrene, Benzo[a]pyrene 62%; Pyrene: 64%; Benzo[a]
pyrene: 82%
2. Trichoderma Incubation of oil refinery soil with Phenanthrene 90% 94
longibrachiatum fungus on minimal salt medium
FLQ-4 along with phenanthrene
3. Trichoderma reesei Incubation of 12 mg L−1 of benzo[a] Benzo[a]pyrene 54% 95
FS10-C pyrene and glucose (10 g L−1)
supplementation as a co-
metabolic substrate with T. reesei
4. Acremonium sp. Acremonium sp. P0997 inoculated to Naphthalene, fluorene, 64.9–96.9% 96
P0997 the matrix spiked with different phenanthrene, anthracene,
heavy metals, crude oil, and PAH, fluoranthene
and incubated at 28°C and 16 rpm
for 2–4 days
5. Trichoderma sp 14 days of incubation at 28°C in an Pyrene, Anthracene, 37.4% pyrene; 36.4% anthracene; 97
inorganic Czapek-Dox medium Fluoranthene 14.3% fluoranthene
6. Fusarium sp with PAHs 18.2% pyrene; 15.3%
anthracene;12.8% fluoranthene
7. Aspergillus oryzae Grown in the liquid media spiked Phenanthrene 235 mg L−1 degraded 98
MF13 with phenanthrene
8. Scopulariopsis Inoculation on malt agar extract Anthracene 80% 88
brevicaulis medium and incubated at 26°C
for 7 days
9. Talaromyces helicus 500 μg of Benzo[a] pyrene Benzo[a]pyrene 26% 99
10. Fusarium solani incubated with T. helicus for 18%
30 days
8

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Table 4. Continued

Technique and conditions utilized

S.No. Fungi for mycoremediation PAH(s) removed Removal percentage(s) Reference

11. Aspergillus ustus Incubation of culture in crude oil, Total petroleum hydrocarbons in crude oil 30.43%, diesel 21.27% and 100
HM3 diesel, and UE oil spiked soil crude oil, diesel and UE oil UE oil 16.00%
12. Purpureocillium crude oil 44.55%, diesel 27.22%and
lilacinum UE oil 14.39%
13. Aspergillus flavus Inoculated into a aqueous culture Total PAHs 95.87% 101
containing crude oil for 15 days
14. Trichoderma Inoculated into a aqueous culture Pyrene 78% 102
sp. F03 containing pyrene of 100 mg L−1
15. Aspergillus sydowii Inoculated into a 0.2% saline spiked Anthracene 98.7% 103
bpo with 100 mg L−1 of anthracene
and incubated for 72 h, pH 7.0 and
30 °C
16. Fusarium strain ZH- Inoculated in mineral salt in the HWM-PAHs 85.9% 104
H2 presence of heavy molecular
weight PAHs as sole carbon
sources

Figure 3. Mechanism of degradation of PAHs by ligninolytic and non-ligninolytic fungi.

ability to secrete ligninolytic enzymes and to degrade lignin in the
wood, and are considered to be ligninolytic fungi. The ligninolytic
fungi also oxidize the PAHs nonspecifically by the action of cyto-
chrome P450 monooxygenases along with ligninolytic enzymes.
The mechanism for the PAHs degradation was reported to be
similar to that of lignin metabolism by the fungi. The key lignino-
lytic enzymes (such as lignin peroxidase, manganese peroxidase,
and aryl alcohol oxidase), along with the oxidative enzyme, lac-
case, act either by direct or indirect oxidation of PAHs5 (Fig. 3).
Hammel suggested the mutualistic working mechanism of these
enzymes in the degradation of PAHs.106 Among these four
enzymes, the laccase and aryl alcohol oxidase work together by
the direct oxidation of PAHs compounds, whereas lignin peroxi-
dase and manganese peroxidase work through the secretion of
reactive peroxide species.5 Hofrichter suggested a radicle medi-
ated reaction by secreting the freely diffusible Mn(III) by the man-
ganese peroxidase, which indirectly oxidizes the terminal
polyphenol or phenol group of PAHs, followed by decarboxyl-
ation.107 Overall, ligninolytic fungi biomineralize the PAHs into
PAHs quinones and, further, into inorganic compounds of carbon
dioxide and water. On the other hand, non-ligninolytic fungi oxi-
dize PAHs via intracellular cytochrome P450 monooxygenase
9

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 www.soci.org AK Rathankumar et al.

Table 5. List of companies utilizing surfactants or biosurfactants for the remediation of contaminated soil (‘-’ details about the surfactants were not
reported)

S.No. Company Country Surfactants/Product name

1 EcoChem Lts. Canada Rhamnolipids

2. Peterobuster Inc USA Peterobuster
3. VeruTEK Technologies Inc USA VeruSOL
4. Gannett Fleming Inc USA Non-ionic surfactants
5. EthicalChem USA E-Mulse (formerly VeruSOL)
6. Injektaenviro Australia anionic linear surfactants
7 jrwbioremediation USA C2–C4 carboxylic acids and hydroxy acids
8. EOS remediation LLC USA EOS PRO
9. Tersus environmental LLC USA eZVI
10. Biogenie UK —
11. Savannah River Nuclear Solutions LLC USA Biosurfactants
12. LocusBioenergy USA AssurEOR STIM
13. SCG industries Canada —
14. Surbec USA TASK
15. BIOGENESIS ENTERPRISES, INC. USA BioGenesis cleaning chemical
16. Biotrol USA Neutravec
17. Surfactant associates incorporated USA —
18. Halliburton USA Ascend Surfactant
19. Recon USA SURFAC

enzymes (CYP450).108 The PAHs that are adsorbed by the fungal
mycelium system are oxidized by incorporation of single oxygen
and transform into unstable arene oxide, which is either nonenzyma-
tically transformed into phenol derivates or hydrated by epoxide
hydrolase into trans dihydrodiols.79, 108 The final phenol derivates
and tran dihydrodiols were further subjected to enzymatic transfor-
mation for the liberation of sulfates, xylosides, glucosides, etc. (Fig. 3).
Despite the efficiency of the ligninolytic fungi for the degrada-
tion of PAHs in the contaminated soil, the low bioavailability of
the PAHs in the soil gradually reduces their remediation efficiency.
As a result, researchers developed a hybrid technique by incorpo-
rating surfactants along with mycoremediation, which not only
resulted in the enhanced remediation of PAHs but also aided in
improving the growth of mycelia and the efficient release of ligni-
nolytic enzymes. Due to the efficiency of surfactants on increasing
the bioavailability of the PAHs, several industries have applied
surfactants as a major strategy for soil remediation (Table 5).
Surfactant-enhanced mycoremediation
Effect of surfactants on fungi performance
Although there are contradictory reports regarding the surfactant
functionality as a bio stimulant or inhibitor of PAHs bioremedia-
tion, the application of surfactants defiantly increases the bio-
availability of the PAHs, often aiding in efficient bioremediation.
On this account, several studies have reported both positive and
negative effects on mycoremediation efficiency on the applica-
tion of surfactants (Table 6).
The presence of a surfactant exhibits a modulating effect on the
growth of fungi and these effects are considered to be species-spe-
cific.38 Surfactants increase the bioavailability of less soluble sub-
strates for the fungi. Moreover, surfactants stimulate the growth
and transport of fungal spores,123 which directly have a positive
impact on the growth of fungi. Also, different classes of surfactants
have been reported to exhibit varying effects on the growth of the
10
tolerates the presence of non-ionic surfactants (such as Triton X-100
and tween 80) in the concentration of their CMC values due to their
ability to utilize non-ionic surfactant as a growth substrate. However,
the same Pleurotus ostreatus growth was found to be inhibited in the
presence of anionic surfactants, such as SDS.6 Similarly, Hamzah
et al. reported the ability of 1.0 CMC rhamnolipids to be adsorbed
20% more than the nonionic surfactant; 0.5 CMC triton X-100 on
the hyphae cell surface of the Aspergillus brasiliensis resulted in a
gradual reduction in the fungal hydrophobicity.124 Ruiz-Aguilar
et al. examined the effect of different non-ionic surfactants, triton
X-100 (75 mg/L), tween 80 (302 mg/L), and Tergitol NP-100
(74 mg/L), on the growth of Trametes versicolor and found that
tween 80 had no inhibitory effect on the growth of the fungi,
whereas the presence of triton X-100 and tergitol NP-100 exhibited
a 75–95% growth inhibition.125
During the bioremediation process, lignocellulosic material (specif-
ically cellulose) has been introduced in the mycoremediation site as a
selective nutrient for the growth of fungi. In this aspect, the addition
of a surfactant was reported to have a positive effect in making the
hydrophobic cellulose more easily available for the enzymatic hydro-
lysis.38 In another study, the presence of soybean oil was found to
enhance the growth of fungi – P. ostreatus,126 Grifola frondosa,127 T.
hirsuta,128 Polyporus sp129 – during soil remediation in the presence
of PAHs. On the other hand, in the real soil matrix, a variety of micro-
organisms were reported to have the ability to metabolize the surfac-
tant as a carbon source, which often leads to unnecessary nutrient
competition to the bioaugmented fungi.130 Further, the adsorption
ability of most of the surfactants to the soil particles makes the treated
soil more toxic.46 On the other hand, due to their surface-active prop-
erties, the surfactant affects the membrane permeability of the fungi
and hinders the excretion process.5 In addition, the presence of the
surfactant was found to solubilize the soil organic matter, which is
considered a soil nutrient sink leading to impact on the growth of
bioaugmented fungi. Further, the synthetic surfactants are toxic to

fungi during bioremediation. For instance, Pleurotus ostreatus better the indigenous bacteria of soil, causing a reduction in the

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Table 6. Toxicity profile of synthetic surfactants

Type of Adsorption
surfactant Synthetic surfactant to soil Toxicity of surfactants towards soil Reference

Cationic Alkyl benzyl dimethyl High Highly toxic and environmentally not feasible 109
ammonium chloride Toxic effects on microorganisms and poses significant health problems to 110
(ABDMA) humans
Cetyl trimethyl ammonium High — 111
bromide (CTAB) Cytotoxicity wherein interaction with the phospholipid bilayer destabilizes 112
the cell membrane, leading to soil microorganism death
Perfluoro octane sulfonate High Phytotoxicity in Brassica chinensis 113
(PFOS) Hepatotoxicity, Neurotoxicity, Reproductive toxicity, Immunotoxicity 114
Anionic Sodium Dodecyl Benzene Low — 115
Sulphonate (SDBS) Toxic effect on aquatic organisms 116
Linear Alkylbenzene Low — 117
Sulphonates (LAS) Inhibited growth and metabolic activity initially, after which metabolic activity 118
also ceased
Ammonium lauryl sulfate Low Low acute oral toxicity 118
Nonionic Tween 80 Low Phytotoxicity in Tall wheatgrass, 119
Intraperitoneal and oral toxicity to mice and rats 120
Triton X-100 Low — 121
Cytotoxic for human cells on prolonged exposures 122

bioremediation outcome, which often resulted due to the synergistic
interaction of fungi and the indigenous microorganism.
Apart from the growth of fungi, the presence of surfactants also
has a modulating effect on the activity of the secreted ligninolytic
and oxidative enzymes. Regarding the production of ligninoly-
tic enzymes, the presence of surfactants was reported to stim-
ulate the secretion of an enzyme cocktail (which includes
laccase, aryl alcohol oxidase, manganese peroxidase, and lignin
peroxidase) in effluent water by wood-assisted Trametes versi-
color in the presence of PAHs and rhamnolipids.5 The presence
of SDS was reported to exhibit high activity of Pleurotus ostreatus
on the lignin peroxidase. Similarly, Singh and Singh reported that
the presence of the non-ionic surfactants (tween 20 and triton
X-100) led to the enhanced production of laccase by Ganoderma.
Sp and Lentinus sp. in the solid-state fermentation, which indi-
cated the stimulatory effect of the surfactants on enzyme produc-
tion.131 The ability of surfactants to release the trapped secreted
enzyme from the fungal mycelium was predicted to be the main
reason for the enhanced enzyme activities.28, 132 Moreover, sur-
factants enhance the production of extracellular enzymes in fungi
by promoting both the uptake and exit of compounds from the
cells by modifying the cell structure and promoting the perme-
ability of the plasma membrane.123, 133 Thus, an increase in the
permeation of the enzymes through the plasma membrane
increases the concentration of enzymes in the medium, thereby
increasing the enzyme activities. Despite the positive effects of
the surfactant on the enzyme secretion, some reports have
described the negative effect of the surfactants on the stability
of the secreted enzymes. Zheng and Obbard reported that the
presence of a non-ionic surfactant (tween 80 or triton X-100) in
the liquid culture of P. chrysoporium resulted in the reduction of
lignin peroxidase and manganese peroxidase activities.134
Further, due to the adsorption of surfactants onto soil particles,
discrepant effects of surfactants have been frequently reported
for liquid cultures consisting of the same species with the same
surfactant concentrations.38
TECHNIQUES INVOLVED IN THE
SURFACTANT-ASSISTED PAHS
MYCOREMEDIATION
Mycoremediation of PAHs-contaminated soil can be classified
into two wide classes depending on the site of application: ex-situ
and in-situ (Fig. 4). Ex-situ techniques mainly involve the excava-
tion of PAHs-contaminated soil, followed by treatment of the col-
lected soil and, finally, rehabilitation of the soil to the original site.
On the other hand, in situ techniques focus on treating the pol-
luted soil at its place. In situ techniques are superior to ex-situ tech-
niques because they require less involvement of labor,
excavation, and transportation costs, and they also cause less
damage to the soil ecosystem. However, in situ soil remediation
techniques are often considered to be long term and the involve-
ment of multiple factors makes the remediation process
unpredictable.
Surfactant-aided mycoremediation (bioaugmentation)
Bioaugmentation is a technique used to treat the PAHs-
contaminated soil by introducing selective fungal strain(s) to
enhance the bioremediation process. Amongst the many pro-
cesses available, white-rot fungi are the commonly employed
basidiomycota for bioaugmentation due to their ability to secrete
key degradative ligninolytic enzymes.8, 135 In the ascomycota,
Aspergillus and Trichoderma were reported to be widely utilized
for bioaugmentation. Most of the in situ studies on the mycoreme-
diation of PAHs were performed in a contaminated soil simulated
environment using microcosm studies5 (Table 7). The bioaugmen-
tation of fungi in the contaminated site often requires a continu-
ous supply of key nutrients and air (in the case of anoxic soil) for
the growth of the fungi.24 The conventional application of
nutrients for the growth of fungi, including synthetic nutrients
(such as malt extract and glucose) and waste organic supple-
ments (sewage sludge), was reported.149 Potin et al. reported
11

the application of 2% malt extract as a stimulant for the growth

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 www.soci.org
Figure 4. Soil remediation techniques involving surfactants and fungal
treatments for the removal of PAHs from contaminated soil.
of Cladosporium sphaerospermum, a fungal isolate from PAHs-con-
taminated soil, and reported an average of 23% degradation of
benzo(a)pyrene in unsterile soil microcosm studies.150 However,
the application of carbon-rich nutrients into the soil also acts as
a growth enhancer for other soil microbiota; this results in the
exponential growth of unwanted microorganisms, thereby creat-
ing competition for the bioaugmented fungi. To overcome this
problem, fungal-specific nutrient media (such as cellulose and lig-
nocellulose) were utilized during mycoremediation studies. To
further enhance the bioaugmentation efficiency, a combination
of nutrients and surfactants is often employed. Márquez-Rocha
et al. studied the effect of surfactants on the degradation effi-
ciency of PAHs (pyrene, anthracene, and phenanthrene) in con-
taminated soil and an enhancement of the degradation
efficiency by 1.5 fold was reported in the presence of 0.15% tween
80 by Pleurotus ostreatus.136 Apart from conventional surfactants,
the application of soya oil, fatty oil, and fish oil with surface-active
properties has also been utilized to enhance the bioavailability of
the PAHs. With the application of fish oil, an average of 86%
mycoremediation of 16 PAHs in contaminated soil by the oyster
mushroom (Pleurotus ostreatus) was reported.137 Similarly, Leon-
ard et al. utilized soyabean oil for the degradation of 6 PAHs in soil
by the Pleurotus ostreatus and Irpex lacteus 617/93, and they
reported an enhanced degradation in comparison with the com-
mercial surfactants tween-20 and tween −80.126
On the other hand, it has been reported that the performance of
the fungal strain in liquid media varies greatly from the real soil
matrix; therefore, screening of the fungal strains for their capabil-
ities to degrade the PAHs in the soil is important for successful
bioremediation. In this context, Novotný et al. reported a compar-
ative study on the degradation and ligninolytic enzyme produc-
tion by Trametes versicolor and found that the enzyme secretion
and degradation efficiency of the ligninolytic fungi was better in
the liquid medium than in the soil matrix.23 This study also proved
the influence of external soil parameters on the remediation effi-
ciency. Further, from previous work, it was established that the
presence of surfactants in the media influences the performance
of the mycoremediation process.28 In most of the bioaugmenta-
tion studies, the application of non-ionic and anionic surfactants
(such as Triton X-100, tween 80, SDS, and rhamnolipids) is com-
monly reported (Table 2). Depending on the HLB index of the sur-
12
factants, Mohanty and co-workers recommended the application
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AK Rathankumar et al.
of mid-range HLB, rather than low and very high HLB, surfactants
for efficient bioremediation studies.151 Low concentration of sur-
factant [i.e., below effective CMC (CMCeff)] is often degraded or
lost due to soil adsorption without elucidating any prominent
impact on the soil remediation. On the other hand, a high concen-
tration of surfactant sometimes masks the availability of the PAHs
for the fungi degradation by forming a protective layer around
them or by trapping PAHs in their micelle hydrophobic core. In
addition, a higher concentration of surfactants is often reported
to affect the key PAHs’ degradative enzyme stability, thereby
reducing the remediation efficiency.134 Apart from the surfactant
and its concentration, several abiotic and biotic factors have been
reported to influence the efficiency of bioaugmentation.152 Some
of the abiotic factors that influence the efficiency of bioaugmen-
tation include moisture, pH, soil organic matter, and nutrient con-
tent.153 On the other hand, the biotic factors influencing
bioaugmentation are the presence of indigenous soil microorgan-
isms that compete with the bioaugmented fungi for nutrition and
the presence of bacteriophages and protozoa that may act as a
predator for the bioaugmented fungi.152
Surfactant flushing coupled mycoremediation
Surfactant flushing is another common in situ strategy utilizing
surfactants for soil remediation. Surfactant flushing is consid-
ered to be one of the oldest and most investigated commercial-
ized techniques for the remediation of contaminants in the soil.
This in situ soil flushing coupled with mycoremediation
involves two stages: in the first stage, the surfactant is utilized
as a flushing agent to wash away the PAHs present in the con-
taminated soil; in the second stage, the PAHs present in the
flushed solution are degraded by fungi.154 During the first
phase of soil flushing, the surfactant used as flushing fluid is
flushed either on the surface of PAHs-contaminated soil or
injected into the PAHs-contaminated soil zone. The common
technique to introduce the flushing solution includes surfac-
tant flooding, basin infiltration system, infiltration well, and
leach field. Depending on the presence of other pollutants, a
surfactant solution often combines with chelating agents, such
as organic acids or EDTA. Saeedi et al. reported the application
of nonionic surfactant triton X-100 coupled with EDTA for the
simultaneous removal of PAHs and heavy metals from the soil
and they achieved a maximum of 54% and 90% removal of
PAHs and heavy metals, respectively.121 Similarly, Hahladakis
et al. coupled citric acid with commercial surfactant poloxamer
407 for the effective removal of heavy metal and PAHs from the
soil.27 Some of the examples of surfactant flushing coupled
with mycoremediation are shown in Table 7. The continuous
injection of surfactants into the contaminated soil solubilizes
the PAHs by trapping them into their micellar and the resultant
PAHs-surfactant flushed solution is commonly extracted by
downgradient extraction wells. With recent advancements,
the strategic coupling of electrokinetics with surfactant flush-
ing was reported and it enhanced the PAHs remediation effi-
ciency by increasing the soil- surfactant-PAHs interaction.155
The separated surfactant can either be discharged or reinjected
into the contaminated site for flushing. The PAHs-surfactant
flushed solution is separated for the surfactants and bioreme-
diated with a fungal system. The presence of the surfactant in
the flushed solution was reported to affect the efficiency of
fungi in the degradation of PAHs in the solution. It was reported
that rhamnolipids beyond 0.5 mg/mL are toxic for the growth
of white-rot fungi (Trametes versicolor).28 The soil properties
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Table 7. Surfactant-assisted mycoremediation of PAHs

Surfactants Fungus Soil contaminated with PAHS Technique utilized Removal Reference

Tween 80 Anthracophyllum Phenanthrene, anthracene, Microcosm phenanthrene (95.4%), 87

discolor pyrene, fluoranthene (Bioaugmentation anthracene (61.5%),
benzo(a)pyrene. with surfactants) fluoranthene (43.1%) pyrene
(43.1%) benzo(a)pyrene
(15.3%)
Tween 80 Pleurotus Pyrene, anthracene and (Bioaugmentation Pyrene (75%), anthracene (80%) 136
ostreatus phenanthrene with surfactants) and phenanthrene (75%)
Fish oil Pleurotus 16 PAHs (Bioaugmentation 86% 137
ostreatus with surfactants)
Tween 80 Pleurotus Phenanthrene, anthracene, (Bioaugmentation - 126
Tween 20 ostreatus fluoranthene, pyrene, with surfactants)
Soyabean oil chrysene, benzo[k]
fluoranthene, and benzo[a]
pyrene
Tween 80 Irpex lacteus Phenanthrene, anthracene, (Bioaugmentation - 126
Tween 20 617/93 fluoranthene, pyrene, with surfactants)
Soyabean oil chrysene, benzo[k]
fluoranthene, and benzo[a]
pyrene
Tween 80 Irpex lacteus PAHs-contaminated age old soil Bioaugmentation Tween 80 (~82%) 138
Tween 20 617/93 with surfactants Tween 20 (~81%)
Olive mill Olive mill wastewater(~19%)
wastewater
Tween 80 Pleurotus PAHs-contaminated age old soil Bioaugmentation Tween 80 (~67%) 138
Tween 20 ostreatus with surfactants Tween 20 (~66%)
Olive mill Olive mill wastewater (~19%)
wastewater
Montanox 80™ Trametes PAHS 38% 139
versicolor
Tween 80 Phanerochaete PAHs-contaminated soil Surfactant flushing 56% after 11 days 140
chrysosporium and
mycoremediation
Tween 80 P. chrysosporium 9 PAHs in soil Surfactant flushing >90% 141
and
mycoremediation
Tween 80 White rot fungi PAHs Surfactant flushing 8
and
mycoremediation
Tween 80 Penicillium spp 14
C- pyrene Surfactant flushing 90% 142
and
mycoremediation
Tween 80 Trametes PAH Mixture Bioaugmentation 57–99% 143
versicolor with surfactants
Triton X-100 Glomus phenanthrene Bioaugmentation 144
etunicatum with surfactants
Pseudomonas C. versicolor Pyrene Bioaugmentation ~93.7% 145
sysnthesized with surfactants
rhamnolipids
B-cyclodextrin White rot fungi PAHs cocktail Bioaugmentation 146
with surfactants
Tween 80 Armillaria isolate fluoranthene Bioaugmentation 100% 83
with surfactants
SDS Armillaria isolate fluoranthene Bioaugmentation 80% 83
with surfactants
CTAB Armillaria isolate fluoranthene Bioaugmentation 40% 83
with surfactants
13

J Chem Technol Biotechnol 2021 © 2021 Society of Chemical Industry (SCI). wileyonlinelibrary.com/jctb
 www.soci.org
Table 7. Continued
Surfactants Fungus Soil contaminated with PAHS
Tween 80 Fungal cocktail PAHs-contaminated soil
Tween 80 Lasiodiplodia Benzo (a) pyrene
theobromae
(such as hydraulic permeability, soil organic matter, grain size
distribution, and moisture content) are considered to deter-
mine the efficiency of soil flushing. The hydraulic permeability
of at least 1X10−7 m/s was reported to be effective for soil flush-
ing.156 On the other hand, the application of surfactants may
also solubilize the soil organic matter, which can lead to a
reduction in the quality of residual soil.
CHALLENGES AND FUTURE PERSPECTIVES
Recently, various green technologies have been developed for
the remediation of PAHs- contaminated soil. Although most of
these bioremediation technologies resulted in enhanced PAHS
remediation, the application of these technologies at a field-scale
is still rare due to various limitations. The major factors that affect
the biosurfactant-aided mycoremediation process can be classi-
fied as being soil and weather related, contaminant and co-
contaminant related, and cost related. The dynamic interaction
of the soil environment, the oxygen availability, the concentration
of PAHs and their interaction with other pollutants, the water con-
tent of the soil, and the presence of indigenous soil microbiota all
greatly influence the efficiency of this mycoremediation system.
Moreover, even though biosurfactants are known to flush con-
taminants from the soil system, application of this technology at
a large-scale is not cost-effective. Further, the choice of fungi with
superior degradation potential is necessary because the presence
of PAHs at higher concertation may be detrimental for the growth
of fungi. The mycoremediation of contaminants is often limited
by the nutrient availability and by competition with the indige-
nous microbiota. Additionally, the growth suppression of the
introduced fungi by the soil microbiota will limit the application
of the process at a field-scale. Hence, the optimization of growth
parameters of the fungal system must to be done at a
laboratory-scale before its large-scale application. Another limita-
tion of the mycoremediation process is the inability to measure
and control the biochemical pathways (like toxicity induced by
the process, the fate of the remediated compounds etc.) in
complex soil environments.
For the application of the biosurfactant-aided mycoremediation
process at a large-scale, a rapid, low-cost, and risk-based PAHs
cleanup strategy should be developed. A better understanding
of the solubilization of PAHs by biosurfactants and of the physical,
chemical, and biological interactions of biosurfactants with other
factors will mediate in establishing a robust bioremediation system.
Moreover, there is a need to design an optimal biosurfactant/
fungi/target soil environment combination to enhance the PAHs
remediation and project its large-scale application. Further, under-
standing the interaction of the introduced fungi with the indigenous
microbiota will provide useful information on the process of remedi-
ation. Subsequently, the development of an additive mixture that is
14
suitable for extreme environment conditions (consisting of a
wileyonlinelibrary.com/jctb © 2021 Society of Chemical Industry (SCI).
AK Rathankumar et al.
Technique utilized Removal Reference
Bioaugmentation 93.8% 147
with surfactants
Bioaugmentation ~80% 148
with surfactants
combination of microbial strains with biosurfactants and nutrients,
along with other factors in appropriate proportions) may provide a
suitable arena for the bioremediation of contaminants. Considering
these perspectives, a detailed understanding of the microbial degra-
dation abilities and their interactions, along with metabolic engineer-
ing for cellular resistance and adaptation mechanism, will provide a
strong framework for the application of surfactant-aided bioremedi-
ation process for the remediation of contaminants in real soil matrix.
CONCLUSIONS
A large number of green technologies for the remediation of
PAHs-contaminated soil are still in the bench-scale level, so it is
important to investigate and analyze the feasibility of these tech-
nologies towards their application in the field-scale for the reme-
diation of real soil matrix. Biosurfactant-aided remediation and
mycoremediation are individually well-established studies; how-
ever, a detailed understanding of the interactions of biosurfac-
tants with the soil environment and soil microbiota, and the
study of the dynamics of subsequent remediation by a fungal sys-
tem will provide new avenues for the enhanced remediation of
PAHs-contaminated soil. Studies on the structural and functional
make-up of soil microbial communities on different temporal
and spatial scales, along with their responses and interactions
with a biosurfactant-fungal assisted system through community
fingerprinting and environmental genomics techniques, will aid
in improving the bioremediation process. Even though it is
impractical to restore all the natural environments of PAHs-
contaminated soil to their pristine state, the application of risk-
directed green remediation technologies will improve the man-
agement of PAHs-contaminated soil to a considerable extent.
ACKNOWLEDGEMENTS
Vinoth Kumar Vaidyanathan would like to thank All India Council
of Technical Education for sponsoring under Research Promotion
Scheme (File no. 8-60/FDC/RPS (POLICY-1)/2019-20) and Indo-
Mexican bilateral cooperation project (INT/Mexico/P-13/2016)
funded by the Department of Science and Technology, Govern-
ment of India. The authors express their sincere gratitude to
SRM Institute of Science and Technology, Tamil Nadu, India for
the help and for aiding in facilitating the research.
CONFLICT OF INTERESTS
None.
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