Gupta - Biodegradation of Polycyclic Aromatic Hydrocarbons by Microbial Consortium A Distinctive Approach For Decontamination of Soil - 2016 PDF

Soil and Sediment Contamination: An International
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Biodegradation of Polycyclic Aromatic

Hydrocarbons by Microbial Consortium: A
Distinctive Approach for Decontamination of Soil
Gauri Gupta, Vipin Kumar & Asim Kumar Pal
To cite this article: Gauri Gupta, Vipin Kumar & Asim Kumar Pal (2016) Biodegradation
of Polycyclic Aromatic Hydrocarbons by Microbial Consortium: A Distinctive Approach for
Decontamination of Soil, Soil and Sediment Contamination: An International Journal, 25:6,
597-623, DOI: 10.1080/15320383.2016.1190311
To link to this article: http://dx.doi.org/10.1080/15320383.2016.1190311
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Published online: 01 Jun 2016.
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Date: 18 October 2016, At: 22:38
SOIL AND SEDIMENT CONTAMINATION

2016, VOL. 25, NO. 6, 597623
http://dx.doi.org/10.1080/15320383.2016.1190311
Biodegradation of Polycyclic Aromatic Hydrocarbons

by Microbial Consortium: A Distinctive Approach for
Decontamination of Soil
Gauri Gupta, Vipin Kumar, and Asim Kumar Pal
Department of Environmental Science and Engineering, Indian School of Mines, Dhanbad, Jharkhand, India
ABSTRACT
KEYWORDS
The presence of polycyclic aromatic hydrocarbons (PAHs) in the soil is a

major cause of concern due to their toxic nature and ubiquitous
occurrence. As PAHs are hydrophobic substances, their solubility in
water is very low. This makes them unt for natural degradation.
However, it has been found that several microorganisms have the
capability to efciently degrade soil-sorbed PAHs using different
metabolic pathways. As the microbial degradation process is quite
economical and does not cause ecological damage, it has been a
subject of extensive research for the past several decades. In
numerous studies, it has been found that a consortium of microbes is
more effective than the individual microbial isolates. The process
remains affected by different environmental factors. Therefore, in this
article, the current status of the work done on various aspects of
biodegradation of ecologically toxic PAHs using different microbial
consortia has been reviewed along with the biological aspects of
biosurfactants produced during the process. The role of recent
technologies such as the next-generation sequencing using omics
techniques, metagenomics and metatranscriptomics, has also been
discussed. These technologies are critical in understanding the
application of microbial consortium, including its potential for future
bioremediation in microbial ecology.
Biodegradation;
biosurfactants; microbial
consortium; PAHcontaminated soil; polycyclic
aromatic hydrocarbons
Introduction
Polycyclic aromatic hydrocarbons (PAHs) belong to a class of organic compounds that consist of two or more fused benzene rings that are arranged in linear, angular, or cluster congurations. They bear toxic, carcinogenic, and mutagenic properties. Therefore, they are
considered as environmental pollutants that can have a deleterious effect on the ora and
fauna of contaminated sites and can cause serious health problems and genetic defects in
human beings.
PAHs are ubiquitous in the environment. They can be found in air (Mandalakis et al.,
2002), water (Soclo et al., 2000), soil (Makkar and Rockne, 2003), as well as sediments
CONTACT Vipin Kumar

vipinmicro1@gmail.com
Department of Environmental Science and Engineering, Indian
School of Mines, Dhanbad 826 004, Jharkhand India.
Color versions of one or more of the gures in this article can be found online at www.tandfonline.com/bssc.
2016 Taylor & Francis Group, LLC
598
G. GUPTA ET AL.
(Gan et al., 2009; Johnsen et al., 2005). Their generation in the environment occurs from
natural (biogenic and geochemical) and anthropogenic sources. Some examples of their
formation from natural sources are exudates from trees, volcanic eruptions, forests, and
rangeland res. Some of the most signicant anthropogenic sources include burning of fossil
fuels, coal tar, wood and garbage, petroleum oil rening, electric power generation, home
heating, internal combustion engines, municipal solid waste incineration, and petroleum
spills (Haritash and Kaushik, 2009).
In view of the abundance of PAHs in the environment and their adverse effects on human
beings, it becomes mandatory to clean PAH-contaminated sites. PAHs are included in the
US Environmental Protection Agency (EPA) and European Community (EC) priority pollution list (Anyakora et al., 2005). The EPA currently regulates 16 PAH compounds as priority
pollutants in water, soil, and sediments (Liu et al., 2001; Moustafa, 2004).
PAHs are hydrophobic in nature. Therefore, their solubility in water is very low. They
mainly interact with nonaqueous phases. This makes them unt for natural degradation.
Only a limited amount of degradation of PAHs takes place in the environment by processes
such as photolysis, chemical degradation, volatilization, and adsorption (Bacosa et al.,
2015a). Thus, PAHs are one of the most persistent pollutants in the environment (Jor
et al., 2013).
Various conventional methods are available for degradation of PAHs. These methods
include electrochemical remediation (Yeung and Gu, 2011), land lling (Mandal et al.,
2011), solvent extraction (Ahn et al., 2008), air sparging (Mandal et al., 2011), thermal
destruction/incineration (Gan et al., 2009; Vidali, 2011), photocatalytic remediation
(Gan et al., 2009), and use of synthetic surfactants (Mandal et al., 2011). However, due to
extravagant cost and pollutant phase transfer in certain cases, biological methods are becoming prevalent these days. Bioremediation, degradation of PAHs using microbes, is a much
more cost-effective method compared to these methods. Therefore, the bioremediation
method is now being increasingly used.
According to the Ofce of Technology Assessment (1991), bioremediation is dened as
the act of adding materials to contaminated environments to cause an acceleration of the
natural biodegradation processes. The process of bioremediation involves microbial degradation of soil PAHs into less complex metabolic compounds without using any other
medium (Gonzalez et al., 2011; Yu et al., 2011). Almost all types of hydrocarbons are responsive to microbial attack (Atlas, 1991; Head, 1998). In addition to being quite economical,
bioremediation does not cause any ecological damage. During the process, PAHs serve as a
food source for certain soil bacteria and therefore are degraded by them into harmless substances such as carbon dioxide, water, and fatty acids (Sarma et al., 2004). Carbon dioxide is
used by plants performing carbon sequestration (Mandal et al., 2011). Further, during the
process, microbes present at the site can multiply in numbers when in contact with the contaminants, and they naturally decline after the contaminants are degraded. Another advantage is that bioremediation decontaminates the pollutants on the site itself, thus reducing the
cost of transfer and also the human health hazards during transportation. It may be mentioned that as anthropogenic sources of PAHs are the major cause of environmental pollution, a large number of bioremediation programs are focused on anthropogenic sources.
Bioremediation can be of two basic types: (1) Biostimulation, which is a process in which
nutrients are provided to indigenous microorganisms for proper growth and metabolic
rate in order to increase their degradation efciency (Mandal et al., 2011), and
599
(2) Bioaugmentation, which involves introduction of group of microbes which are competent enough to survive in contaminated environment to perform the bioremediation process
(Vidali, 2011). The biodegradation of PAHs in soil is completed in two steps. The rst step
involves the uptake of PAHs by soil microbes, which is affected by several factors such as the
bioavailability of PAHs in soil (aqueous phase), properties of soil, and environmental conditions. The second step involves degradation of PAHs by microbes, which mostly depends on
the biological ability of microbes (MacLeod et al., 2001; Maeir et al., 2000; Margesin and
Schinner, 2001; Semple et al., 2003). There are several bioremediation techniques used for
decontamination of polluted soils, sediments, and groundwater. Bioremediation techniques
can be categorized as in situ or ex situ. The in situ methods involve cleaning of contaminants
on the site. Some of the in situ methods are biosparging, bioventing, bioaugmenting, and
groundwater circulation (Mohan et al., 2006). The ex situ methods involve transfer of contaminants to another site for the treatment purpose. Bioreactors, landfarming, composting,
and engineered soil cells are some of the examples of ex situ treatment methods (Mohan
et al., 2006). Biodegradation of PAHs is inuenced by a variety of environmental factors,
such as soil pH, nutrient availability, and bioavailability of the contaminant. These factors
are responsible for promoting or inhibiting the growth of PAHs degrading microorganisms.
Various factors that affect the viability of biodegradation are listed in Table 1. The applicability of bioremediation can vary, but this is generally due to unfavorable site conditions.
Therefore, a thorough understanding of the site conditions is required for optimization of
the bioremediation process (Bamforth and Singleton, 2005). During a bioremediation trial,
total PAH levels are generally reduced from approximately 3000 to 1000 mg/kg (Bamforth
and Singleton, 2005).
In the terrestrial as well as aquatic ecosystems, the environmental fate of PAHs is
determined by the degree of their degradation by microbes. Several PAH-contaminated
soils and sediments have active populations of PAHs degrading microorganism
Table 1. Factors affecting the rate of PAH biodegradation.
Factors
Environmental factors
Temperature
Effect on PAH degradation
References
Oxygen
Moisture
Degree of contamination
Sorption
Nutrients
Microbial metabolism rate; bioavailability

(physical nature and chemical
composition of oil); mass transfer
Bioavailability; microbial metabolism rate;
mass transfer
Essential for the enzymatic activity
Microbial growth and metabolism
Microbial metabolism rate; mass transfer
Bioavailability; mass transfer
Microbial metabolism rate
Biological factors
Microbial population
Microbial metabolism rate; bioavailability
Reid et al. (2000); Johnsen et al. (2005); Tang

et al. (2005); Semple et al. (2006)
Bioavailability; mass transfer; microbial

metabolism rate
Bioavailability; mass transfer
Microbial metabolism rate
Microbial metabolism rate; competition for
nutrients
Johnsen et al. (2005); Tang et al. (2005);

Semple et al. (2006)
Johnsen et al. (2005); Pan et al. (2006)
Bamforth and Singleton (2005)
Juhasz and Naidu (2000); Johnsen et al.
(2005); Tang et al. (2005)
pH
Physicochemical factors
Physicochemical properties of
PAHs
Structure/particle size of soil
Soil organic content
Presence of contaminants
Bamforth and Singleton (2005); Sartoros

et al. (2005); Tang et al. (2005)
Bamforth and Singleton (2005); Tang et al.
(2005); Betancur-Galvis et al. (2006)
Zhang et al. (2006)
Leahy and Colwell (1990)
Bamforth and Singleton (2005)
Johnsen et al. (2005)
Taylor and Jones (2001); Betancur-Galvis
et al. (2006); Semple et al. (2006)
600
G. GUPTA ET AL.
(mainly bacteria and fungi). The soil may act as a sink for high-molecular-weight PAHs
and also as a source for low-molecular-weight PAHs (Okere and Semple, 2012). Therefore, it has been found that soil stores more than 90% of total PAHs in the environment (Agarwal et al., 2009). The organic layer of soil accumulates most of the PAHs
present in the soil. Therefore, degradation of PAH depends on the rate of desorption
from soil organics (Rockne et al., 2002). The longer it persists, the more irreversible is
its adsorption, and the lower is the chemical and biological extractability (Hatzinger
and Alexander, 1995). Low bioavailability of PAHs can be attributed to its highly
hydrophobic nature and strong tendency to be absorbed (Santos et al., 2011; Yang
et al., 2009). This is particularly true for PAHs with high molecular weight. However,
organic solvents or biosurfactants can be used to increase the bioavailability and rate of
biodegradation of PAHs (Santos et al., 2011). Biosurfactants act as a bridge between
the hydrophobic PAH molecule and the hydrophilic microbial cell. Thus, they help in
enhancing desorption of PAHs from the soil matrix by lowering interfacial tension
(Makkar and Rockne, 2003) and increasing the bioavailability of water-insoluble substrates. The degradation rate of PAHs decreases with increase in its molecular weight.
Figure 1 shows the bioavailable PAH fractions in soil.
Several microbial species isolated from PAH-contaminated sites are found to be the most
suitable PAH degraders (Thavasi et al., 2011). The structure of PAHs in crude oil is very
complex, and pure cultures of bacteria do not have the ability to degrade different classes of
PAHs (Wu et al., 2013). Therefore, a consortium of bacteria has been used. Various bacterial
species have synergistic interactions among themselves. Thus, they perform the maximum
possible degradation (Wu et al., 2013). Biotechnology has been applied in decontamination
Figure 1. Bioavailable PAH fractions in soil.
601
of PAH-polluted sites, but it still requires a deeper knowledge of biochemical pathway

involved in the process of degradation of PAHs.
This article mainly focuses on the degradation of ecologically toxic PAHs using different
bacterial consortia. Enhanced degradation by the bacterial consortium compared to pure
bacterial isolates has been emphasized. The article also highlights the biological aspects of
biosurfactants produced during the process as biosurfactants enhance the bioavailability of
soil-sorbed (nonaqueous phase) PAHs.
Mechanism of PAH degradation

The general base of mechanism begins with aromatic ring oxidation, followed by PAH
breakdown into its metabolites or PAHs. Figure 2 illustrates the major pathways involved in
the mechanism of PAH degradation by bacteria and fungi.
PAH degradation by bacteria

In the case of PAH degradation by some bacteria, the initial oxidation step incorporates two
oxygen atoms into the benzene ring to form cis-dihydrodiols. This reaction remains
catalyzed by a dioxygenase enzyme. The complex fused ring structure of certain PAHs
causes bacteria to metabolize PAHs at multiple sites to form isomeric cis-dihydrodiols
(Mueller et al., 1996). The cis-dihydrodiols undergo dehydrogenation by the action of dehydrogenase enzymes to form dihydroxylated intermediates (Bamforth and Singleton, 2005).
Figure 2. Major pathways involved in the mechanism of PAH degradation by bacteria and fungi.
602
G. GUPTA ET AL.
Further catabolism involves ring cleavage by dioxygenase to form aliphatic intermediates.

Some bacteria such as Mycobacterium sp. are capable of oxidizing PAHs by the action of the
cytochrome P450 monooxygenase enzyme to form trans-dihydrodiols (Kelley et al., 1990).
Several bacterial species such as Pseudomonas alcaligenes, Rhodococcus sp., Mycobacterium
sp., and Sphingomonas sp. are found to be capable of degrading PAHs. Most of these bacteria
have the capability to grow on low-molecular-weight PAHs such as naphthalene, uorene,
and phenanthrene. However, in the past few years, several bacteria (especially Mycobacterium) able to grow on four-ring PAHs have been isolated. The hydrophobic surfaces of these
bacteria help them to adhere to hydrophobic PAHs, leading to their mass transfer inside the
cell (Seo et al., 2009). Isolation of two new strains, Mycobacterium austroafricanum GTI-23
and Mycobacterium vanbaalenii, has been reported by Bogan et al. (2003) and Moody et al.
(2004), respectively. These strains have been shown to mineralize PAHs such as uorene
and benzo[a]pyrene in soil as well as liquid media.
PAH degradation by fungi

Unlike bacteria, fungi do not utilize PAHs as the source of carbon and energy. They cometabolically convert them to detoxied metabolites (Bamforth and Singleton, 2005). The fungal
metabolism of PAHs is mediated by ligninolytic and non-ligninolytic fungi.
Ligninolytic fungi
The microbial degradation of PAHs by ligninolytic fungi (white-rot fungi) has been inclusively studied during the past two decades (Bamforth and Singleton, 2005; Brodkorb and
Legge, 1992; Cajthaml et al., 2001; Harayama, 1997; Mester and Tien, 2000; Pozdnyakova,
2012). The irregular structure of lignin causes ligninolytic fungi to produce H2O2-producing
enzymes and extracellular enzymes, such as lignin peroxidase, manganese-dependent peroxidase, phenol oxidase, and laccases (Mester and Tien, 2000). These extracellular enzymes
play an important role in the degradation process either by completely mineralizing or by
partially degrading the PAH compounds (Pozdnyakova, 2012). Manganese peroxidases are
heme glycoproteins whose synthesis is induced by Mn2C. Further, laccases are blue copper
oxidases. Fungal peroxidases and laccases produce water-soluble metabolites, such as
quinones, which can be further degraded to carbon dioxide by indigenous bacteria present
in soils and sediments (Brodkorb and Legge, 1992). Lignin peroxidases and manganese peroxidases oxidize PAHs by donating an electron to produce PAH quinones, which can be further metabolized via ring ssion (Pozdnyakova, 2012). Laccase catalyzes one-electron
oxidation of PAHs along with the four-electron reduction of molecular oxygen to water
(Harayama, 1997). Moreover, these extracellular enzymes are capable of diffusing into soil
and oxidizing less bioavailable PAHs. Pyrene, anthracene, benz[a]anthracene, and benzo[a]
pyrene have been found to be oxidized by enzyme lignin peroxidase and manganese peroxidase produced by Phanerochaete chrysosporium (Bogan et al., 1996a, b; Harayama, 1997).
Andersson et al. (2003) assessed the efcacy of white-rot and brown-rot fungi to degrade
PAH-contaminated soil. Pleurotus ostreatus and Antrodia vaillantii were inoculated in an
articially contaminated soil to degrade several PAHs. This increased PAH degradation but
resulted in accumulation of toxic PAH metabolites.
603
Non-ligninolytic fungi
In the case of degradation of PAHs using non-ligninolytic fungi, the rst step involves the
incorporation of one oxygen atom into the aromatic ring by a cytochrome P450 monooxygenase enzyme to form an arene oxide (Sutherland et al., 1995). The next step involves the
hydration reaction to form a trans-dihydrodiol via an epoxide hydrolase-catalyzed reaction
(Bamforth and Singleton, 2005). Moreover, arene oxide undergoes isomerization to form
either methylate or phenol (which can act as a substrate for subsequent sulfation). Arene
oxide may also conjugate with glucose or glucuronic acid. Such PAH conjugates produced
are mostly less toxic and more soluble than parent PAH compounds. Chrysosporium pannorum, Aspergillus niger, and Cunninghamella elegans are some examples of non-ligninolytic
fungi, which make use of P450 monooxygenase enzyme-mediated oxidative pathway for
PAH degradation (Bamforth and Singleton, 2005). Kanaly et al. (2000) have reported the
transformation of several PAHs, including benzo[a]pyrene, pyrene, and chrysene.
Efciency of microbial degradation of PAHs

The environmental fate of PAHs in both the terrestrial and aquatic ecosystems is affected by
microbial degradation. In general, a PAH-contaminated soil has been found to have
microbes belonging to several genera (Assih et al., 2002; Fernandez-Luque~
no et al., 2011;
Thavasi et al., 2011). Several bacterial strains of the genera Pseudomonas, Stenotrophomonas,
Corynebacterium, Staphylococcus, Micrococcus, and Bacillus isolated from hydrocarbon-contaminated environments are able to grow and degrade PAHs (Fernandez-Luque~
no et al.,
2011; Kalzadeh et al., 2011; Pawar et al., 2013; Thavasi et al., 2011). Fungal genera, namely,
Amorphotheca, Neosartorya, Talaromyces, and Graphium, were isolated from petroleumcontaminated soil and proved to be the potential organisms for hydrocarbon degradation
(Chaillan et al., 2004). Use of microbial consortium is effective in cases where there is a lack
of sufcient microorganisms for degradation or there is high pollutant toxicity (Wu et al.,
2013).
Several terrestrial fungi, namely, Aspergillus sp., Cephalosporium sp., and Penicillium sp.,
were found to be the potential degraders of crude oil hydrocarbons (Singh, 2006). Lowmolecular-weight PAHs (two to three rings) were found to be degraded mostly by Aspergillus sp., Trichocladium canadense, Fusarium oxysporum, and species such as T. canadense,
Aspergillus sp., Verticillium sp., and Acremonium sp. were found to have degraded highmolecular-weight PAHs extensively (Haritash and Kaushik, 2009). Eggen and Majcherczyk
(1998) noticed that in aged soil contaminated with creosote, P. ostreatus removed benzo[a]
pyrene most extensively in the rst month. The most abundant fungi in polluted environments are yeast (Berdicevsky et al., 1993), and they can oxidize PAH with alternative carbon
sources. The rate of degradation of phenanthrene by Rhodotorula glutinis, yeast isolated
from contaminated stream, was found to be almost equal to the rate of degradation observed
when bacteria Pseudomonas aeruginosa was used (Romero et al., 1998).
Table 2 presents the data gathered on degradation rates of PAHs from a number of different studies in which different microbial consortia were used. In most of these studies, a
consortium containing all the microbial species isolated from the same contaminated site
was used. It has been proved that naturally enriched bacterial consortium isolated from contaminated soils is more efcient than the articial consortium (Yu et al., 2005a). It is so
because naturally enriched consortium is highly adapted to the natural environment if used
Roseovarius pacicus
Marinobacter hydrocarbonoclasticus
Pseudidiomarina sediminum
Rhodococcus sp., Acinetobacter sp., Pseudomonas
sp.
Achromobacter sp. AYS3
Marinobacter sp. AYS4
Rhodanobacter sp. AYS5
Microbial consortia (bacteria, fungi, and bacteria

fungi complex)
Microbial consortia (bacteria, fungi, and bacteria

fungi complex)
Bacterium FJ037700.1
Bacterium JF733793.1
Bacterium JF&33804
Raoultella ornithinolytica HQ259705.1
A.Flavus H6, Aspergillus nominus H7, Rhizomucor
variabilis H9, Trichoderma asperellum H15,
Aspergillus fumigatus H19, Klebsiella
pneumoniae B1, Enterobacter sp. B3, Bacillus
cereus B4, Pseudomonas aeruginosa B6,
Streptomyces sp. B8, Klebsiella sp. B10,
Stenotrophomonas maltophilia B14
Bacillus, Micrococcus, Staphylococcus,
Pseudomonas, Alcaligenes, Psychrobacter sp.
Bacteria, fungi, and bacteriafungi complex
Gammaproteobacteria AY972873.1, Citrobacter sp.

S-77 AB668058.1, Citrobacter sp. AB668058.1
Rhodococcus sp., Acinetobacter sp., Pseudomonas

sp.
Microbial consortium
Fluorene and Phenanthrene

Pyrene
Benzo(e)pyrene
4 weeks
7 days
Marine environment
20 days
N/A
Mangrove sediment
Mangrove sediment
Slurry
30 days
Soil
Slurry
Soil
N/A
24 days
Oil-contaminated site
Anthracene, Phenanthrene,
Pyrene
PAHs
Anthracene
Fluoranthene
Benz(a)anthracene
Anthracene
Fluoranthene
Benz(a)anthracene
Fluorene
Phenanthrene
14 days
Crude oil-contaminated soil
Phenanthrene
Pyrene
Benzo[a]pyrene
10 days
4 weeks
Time period
for degradation
N/A
Soil
Mangrove sediments
Sources
Soil
Fluorene
Phenanthrene
Pyrene
Anthracene
Phenanthrene
Pyrene
Anthracene
Phenanthrene
Pyrene
Polycyclic aromatic
hydrocarbons
Table 2. Degradation rates of PAHs by microbial consortium.
99.0
90.0
80.0
50.1
55.4
45.95.5
62.03.7
64.54.5
46.05.8
50.26.1
54.35.7
92.2
89.8
46.255.3
87.8
48.2
56.6
75.0
85.0
100.0
100.0
Degradation
rate (%)
Arulazhagan
et al. (2014)
Yu (2007)
Moghadam
et al. (2014)
Li et al. (2008)
Li et al. (2008)
Malik and
Ahmed (2012)
Li et al. (2008)
Zafra et al. (2014)
Wu et al. (2013)
Wu et al. (2013)
Yu et al. (2005a)
References
604
G. GUPTA ET AL.
Achromobacter sp. AYS3

Marinobacter sp. AYS4
Rhodanobacter sp. AYS5
Pseudomonas sp. BPS1-8
Bacillus sp. IOS1-7
Pseudomonas sp. HPS2-5
Corynebacterium sp. BPS2-6
Mycobacterium fortuitum, Bacillus cereus,
Microbacterium sp., Gordonia
polyisoprenivorans, Microbacteriaceae
bacterium, naphthalene-utilizing bacterium
Enterobacter cloacae
Pseudomonas sp.
Consortium YL
B. cereus Py 5
Bacillus megaterium Py 6
Consortium
Mycobacterium sp. strain A1-PYR
Sphingomonas sp. strain PHe B4
Bacterial fungal consortium, Bacillus sp. PY1,
Sphingomonas sp. PY2, Fusarium sp. PY3
Microbial consortium
Table 2. (Continued )
Marine environment
Oil-contaminated soil
PAH-contaminated soil
Crude oil-contaminated soil

Mangrove sediment (same site)
N/A
Soil near coking plant (same site)
Crude oil
Anthracene
Phenanthrene
Pyrene
Crude oil
Pyrene
Pyrene
Pyrene
Sources
Phenanthrene
Polycyclic aromatic
hydrocarbons
9 days
7 days
21 days
N/A
70 days
25 days
5 days
Time period
for degradation
96.05
50
92.1
67.1
99.0
99.0
96.0
77.0
99.0
Degradation
rate (%)
Liu et al. (2013)
Zhong et al. (2011)
Lin and Cai (2008)
Darvishi et al. (2011)
Jacques et al. (2008)
Muthuswamy et al. (2008)
Arulazhagan et al. (2014)
References

605
606
G. GUPTA ET AL.
for bioremediation of a contaminated site. However, the synthetic consortium made by combining various isolates is usually not effective in the natural environment. They may perform
well in the laboratory, but cannot survive in competition with other bacteria in the soil.
In the past two decades, several studies have been carried out using naturally enriched
consortium for bioremediation of PAH-polluted sites (Lin and Cai, 2008; Trzesicka-Mlynarz
and Ward, 1995; Yu et al., 2005b). Trzesicka-Mlynarz and Ward (1995) have reported the
isolation of a naturally enriched mixed culture from soil contaminated with PAHs. This
culture grew on and degraded uoranthene in aqueous media supplemented with glucose,
yeast extract, and peptone. This naturally enriched mixed culture contained four predominant isolates, all of which were Gram-negative rods. Three of these were identied as Pseudomonas putida, Flavobacterium sp., and Pseudomonas aeruginosa. The culture was found to
be capable of degrading a range of other PAHs also. These included benzo[a]pyrene, anthracene, phenanthrene, acenaphthene, and uorene. Moreover, better degradation of a PAH
mixture was observed with the mixed culture than with individual isolates.
Yu et al. (2005b) observed an efcient degradation of uorene, phenanthrene, and
pyrene by a bacterial consortium made up of Rhodococcus, Acinetobacter sp., and Pseudomonas sp. isolated from mangrove sediments under sediment-free and sediment
slurry conditions. The naturally enriched consortium had a degradation ability of 100%
toward uorene and phenanthrene in the sediment-free liquid medium after 4 weeks of
growth. They reported a preferential utilization of low-molecular-weight PAHs (uorene, phenanthrene) compared to pyrene during the biodegradation process. It was
found that the percentage degradation values for uorene and phenanthrene were
higher in the sediment slurry than the corresponding values observed in the liquid
medium. Yu et al. (2005a) studied the degradation of uorene, phenanthrene, and
pyrene in mangrove sediments. They found that when the autochthonous microorganisms and a process of natural attenuation were used, at the end of the fourth week, the
degradation percentages for uorene and phenanthrene were more than 99% but only
around 30% for pyrene. The use of bioaugmentation (inoculation of the enriched consortium to sediments) also gave similar results, though some inhibitory effect was
observed during the rst week (only 50% and 70% degradation of uorene and phenanthrene). They concluded that autochthonous microbes might interact and compete with
the enriched consortium during PAH biodegradation. Lin and Cai (2008) reported the
degradation of PAHs using microbial consortium enriched from the sediment samples
of Huian mangroves. This naturally enriched consortium was shown to degrade 92.1%
of pyrene, 87.6% of uoranthene, 92.3% of phenanthrene, and 95.8% of uorene at a
concentration of 50 mg/L after 21 days of incubation. A mixed consortium composed of
15 bacteria was isolated by the enrichment technique from an oil-contaminated site. This natural bacterial consortium was incubated with 2% crude oil in mineral salt medium, at 37 C
for 24 days. Among the several crude oil components, the degradation of polyaromatic fractions (anthracene, phenanthrene, and pyrene) was reported to be ranging from 46.17% to
55.3% after 24 days by the bacterial consortium (Malik and Ahmed, 2012). Moghadam et al.
(2014) have reported that a naturally enriched consortium, isolated from the mangrove surface
sediments of Nayband Bay, grew on and degraded phenanthrene (Phe) and uorene (Flu).
This consortium was composed of six Gram-negative bacterial strains: Roseovarius pacicus,
Marinobacter hydrocarbonoclasticus, Pseudidiomarina sediminum, and three unidentied
strains. The enriched consortium was able to degrade 64.0% Flu and 58.4% Phe in 7 days.
607
They also concluded that the enriched consortium composed of indigenous bacteria from
mangrove surface sediments has high degradation efciency toward Flu and Phe.
In the studies carried out by Arulazhagan et al. (2014), Muthuswamy et al. (2008), and
Zafra et al. (2014), the consortium was made using microbial isolates collected from different
contaminated sites. Zafra et al. (2014) isolated the consortium species from three soils contaminated with heavy crude oil. Arulazhagan et al. (2014) have used a mixture of seven sampling sites from the marine environment for the isolation of microbial species used in the
consortium for biodegradation of benzo[e]pyrene and phenanthrene. Similarly, Muthuswamy et al. (2008) have used a microbial consortium composed of species from different gasoline and diesel-spilled gas stations.
Salleh et al. (2003) studied the diesel degradation using three microbial consortium
(of three, ve, and eight strains) isolated from the hydrocarbon-polluted soils. The study
concluded that the maximum degradation rate was found using bacterial consortium with
the maximum number of strains (eight strains). Dastgheib et al. (2012) reported that a halophilic bacterial consortium consisting of Halomonas and Marinobacter was capable of
degrading 90% of phenanthrene in 9 days.
Muthuswamy et al. (2008) studied the biodegradation of crude oil using bacterial consortium made up of four strains. They demonstrated that the consortium was more effective in
the degradation of crude oil than pure isolates. The degradation rate by the consortium was
77%, which was higher than the individual strains (Pseudomonas sp. BPS18: 69%; Bacillus
sp. IOS1-7: 64%; Pseudomonas sp. HPS2-5: 45%; and Corynebacterium sp. BPS2-6: 41%).
Similarly, Rahman et al. (2002) reported that in the case of the Bombay High crude oil, the
degradation rate obtained with the mixed bacterial consortium was signicantly higher than
the rates obtained when the constituent bacterial cultures were used individually (mixed
consortium: 78%; Pseudomonas sp. DS10-129: 66%; Bacillus sp. DS6-86: 59%; Micrococcus
sp.GS2-22: 49%; Corynebacterium sp. GS5-66: 43%; and Flavobacterium sp. DS5-73: 41%).
However, Cerqueira et al. (2011) found that the degradation rate obtained with the bacterial
consortium was signicantly lower than the rate obtained with one of the constituent
bacterial cultures (mixed consortium: 51.8%; Bacillus cibi: 64.3%; Bacillus cereus: 51.8%;
Pseudomonas aeruginosa: 40.3%; Bacillus megaterium: 39.6%; and Stenotrophomonas acidaminiphila: 33.2%). Therefore, it appears that interactions among different bacteria also play
an important role in determining the degradation rate.
Deppe et al. (2005) studied an arctic microbial consortium and reported that it was able to
degrade 77% of crude oil at 20 C in 7 days and 70% of crude oil in 4 weeks at 4 C. This
shows that the metabolic capability of the consortium was not restricted to one type of crude
oil. However, such a result cannot be expected from pure cultures, which have specicity
toward substrate compounds (Muthuswamy et al., 2008).
The data gathered in various comparative studies on the efciency of single bacterial cultures and mixed bacterial consortium (made up of same pure cultures) in the degradation of
aromatic hydrocarbons in crude oil are given in Table 3.
Bacosa and Inoue (2015) used PAH-degrading microbial communities obtained from
tsunami sediments in Miyagi, Japan. These bacteria were cultured by the enrichment
technique using PAH mixture or pyrene alone as carbon and energy sources. Ten consortium were tested for PAH mixture. It was found that seven consortia completely
degraded uorene and more than 95% of phenanthrene in 10 days, whereas four consortia partially degraded pyrene. The following degradation pattern was observed:
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G. GUPTA ET AL.
Table 3. Comparative study of degradation of aromatic hydrocarbons in crude oil using pure bacterial
species and mixed bacterial consortium.
Degradation rate (%)
Sources
Soil
Oily sludge
Soil
Soil
Bacterial
species
Single
bacterial
species
Pseudomonas sp. BPS1-8

Bacillus sp. IOS1-7
Pseudomonas sp. HPS2-5
Corynebacterium sp. BPS2-6
Stenotrophomonas
acidaminiphila
Bacillus cibi
B. megaterium
Pseudomonas aeruginosa
B. cereus
Pseudomonas sp. DS10-129
Bacillus sp. DS6-86
Micrococcus sp. GS2-22
Corynebacterium sp. GS5-66
Flavobacterium sp. DS5-73
Enterobacter cloacae
69.0
64.0
45.0
41.0
33.2
64.3
39.6
40.3
51.8
66.0
59.0
49.0
43.0
41.0
59.6
Pseudomonas sp.
40.4
Bacterial
consortium
77
Aromatic
hydrocarbon
degraded
Incubation
time
References
Crude oil
25 days
Muthuswamy
et al. (2008)
Aliphatic and
aromatic
hydrocarbons
40 days
Cerqueira
et al. (2011)
78
Crude oil
20 days
Rahman
et al. (2002)
67.1
Crude oil
48 hr
Darvishi
et al. (2011)
51.8
degradation of uorene was observed rst, which was followed by phenanthrene and
then pyrene. Therefore, it was concluded that low-molecular-weight PAHs are degraded
faster than high-molecular-weight PAHs due to more water solubility and increased
bioavailability. They also concluded that in the process of competitive inhibition, more
soluble PAHs repress enzymes used to degrade high-molecular-weight PAHs. When
pyrene was used as the sole source of carbon and energy, six consortia partially
degraded pyrene, and three consortia degraded more pyrene compared to the pyrene
degradation observed in the PAH mixture. These results suggested that pyrene-degrading enzymes were present but were repressed in cultures grown in the mixture of
PAHs. The remaining four consortia demonstrated negligible pyrene degradation, leading to the conclusion that pyrene degraders are not as common as uorene or phenanthrene degraders. The authors concluded that for the degradation of pyrene, bacteria
require unique metabolic capabilities so that their degradation cannot be interfered
with other high-molecular-weight PAHs. The consortia were found to consist of several
known PAH degraders, including Sphingomonas, Pseudomonas, and Sphingobium, and
also some of the previously unknown degraders such as Dokdonella and Luteimonas.
A potentially novel and PAH-degrading Dokdonella was detected for the rst time.
Rhodobacter and Paracoccus were found to be equally dominant in pyrene cultures. It
was reported that Novosphingobium might play an active role in the degradation of
pyrene in sole and mixed substrate cultures. Bacosa and Inoue (2015) are the rst
investigators to compare the primer sets for PAH ring-hydroxylating dioxygenase
(PAH-RHDa) and nidA genes in the detection of pyrene-degrading bacteria. PAHRHDa gene was shown to be more effective than nidA in estimating pyrene-degrading
bacteria in the enriched consortia. These investigators concluded that these consortia,
which may be ubiquitous in tsunami sediments, can be valuable sources of bacteria for
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remediation of PAH-contaminated sites. However, the degradation metabolites in these

cultures need further investigation.
Some of the studies have demonstrated that several noncontaminated sites also have
PAH-degrading microorganisms. Paracoccus strain has been isolated from contaminated
and noncontaminated soils and was reported to be a PAH degrader (Bacosa and Inoue,
2015; Guo et al., 2005; Zhang et al., 2004). Geiselbrecht et al. (1996) studied the enumeration
of PAH-degrading populations from marine sediments using most probable number (MPN)
technique with naphthalene and phenanthrene as the sole carbon and energy sources. Using
this technique, they demonstrated the differences between PAH-degrading populations
from contaminated (Eagle Harbor) and noncontaminated (Blakely Harbor) sediments. It
was observed that higher microbial concentrations were found in the contaminated sediments. It was further concluded that although the total bacterial count was relatively constant between contaminated and noncontaminated sediments, the PAH-degrading microbes
were more in number at contaminated sediments. It was also reported that Cycloclasticus
strains may not be numerically predominant in contaminated sediments but seem to be
widely distributed in noncontaminated sediments. The isolation of the genus Cycloclasticus
has been reported several times from a variety of uncontaminated and PAH-polluted sites.
The ability of strain to degrade PAHs has been well documented in cultures (Dyksterhouse
et al., 1995; Geiselbrecht et al., 1998). Marine Sphingomonas specie was also reported to be
isolated from both contaminated and noncontaminated sites. The specie was capable of
degrading PAHs (Chung and King, 2001; Guo et al., 2005).
Although some PAHs are pyrogenic in origin, most PAHs in the environment are of petrogenic sources that are present with other aliphatic hydrocarbons in a complex soil matrix.
The bacterial consortium generally degraded the aliphatic hydrocarbons more readily. Thus,
the bacterial consortium that degrades the PAHs faster than the aliphatics is highly desirable.
Bacosa et al. (2010) investigated the biodegradation of equivalent carbon number-based
hydrocarbon fractions in kerosene, which was used as a representative mineral oil. Based on
cloning and sequencing of the 16S rRNA gene, the microbial community was predominantly
identied as Betaproteobacteria of the genera Achromobacter, Alcaligenes, and Cupriavidus.
Degradation experiments revealed that aromatic fractions, which are more toxic than aliphatic fractions, were degraded faster than aliphatic fractions. A follow-up investigation
using a binary mixture of aliphatic and aromatic compounds suggested that these characteristics are unique to the consortium (Bacosa et al., 2011). Moreover, real-time polymerase
chain reaction (PCR) analysis targeting the major bacteria in the consortium revealed that
Burkholderia was potentially the key player for the degradation of PAHs (Bacosa et al.,
2012). In particular, fractions containing compounds of lower molecular weights were found
to degrade more quickly than fractions containing higher-molecular-weight compounds.
These ndings obtained through combined chemical and microbiological analyses should be
quite useful for the bioremediation of complex petroleum hydrocarbon products in petroleum-contaminated environments and reduction of associated health risks.
Mechanisms of degradation by a consortium
As discussed earlier, the biodegradation of environmentally toxic PAHs using a mixture of
bacterial species has been found to be a more promising approach. For a successful biodegradation process, often more than one species of microbes are required. Pure cultures of
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microbes are capable of metabolizing only a certain range of PAHs due to their complex
structure. Therefore, several microbial species are assembled to form a microbial consortium
with broad enzymatic capacities to increase the rate and degradation of PAHs. Such mixed
cultures display metabolic versatility and superiority to pure cultures (Ohgew et al., 2011).
Therefore, a microbial consortium that can synthesize the degradative enzymes for different
parts of the decomposition pathway should be found to be well suited to the degradation of
aromatic hydrocarbons.
Due to the synergistic interactions among the members of the consortium, it has been
found that possibly the rst species degrades the metabolites, which may impede further
degradation of compounds by the second species. Then the second species degrades the
compounds left undegraded or half-degraded (Ghazali et al., 2004). It should be pointed out
that the degradative capacity of any microbial consortium is not necessarily the result of
merely adding together the capacities of the individual strains forming the association. Various organisms have the capability of degrading various forms of hydrocarbons. Thus, when
a consortium of these microbes is applied to degrade various forms of hydrocarbons in a single source such as crude oil, the total degradation is more effective.
Komukai-Nakamura et al. (1996) studied the degradation of Arabian light crude oil using
two different genera, Acinetobacter sp. T4 and P. putida PB4, where Acinetobacter sp. T4
degraded the hydrocarbons, producing the accumulation metabolites. Subsequently, P.
putida PB4 grew on those metabolites and performed the nal degradation of aromatic compounds in crude oil. Use of the microbial consortium composed of bacteria and fungi has
gained attention for PAH degradation. Such consortia have proved to be more effective than
pure cultures as they have high degradation and mineralization rates (Boonchan et al., 2000;
Kohlmeier et al., 2005; Wick et al., 2007). Jacques et al. (2008) studied a microbial consortium made up of bacteria and fungi, both isolated from the same PAH-contaminated soil for
the degradation of anthracene, phenanthrene, and pyrene. The degradation rates were found
to be 99%, 99%, and 96% for anthracene, phenanthrene, and pyrene, respectively. However,
inoculation of soil with pure cultures of bacteria and fungi resulted in less effective degradation. It has been pointed out by Li et al. (2008) that fungus has hyphae, which may act as
vectors and provide voids and continuous surfaces for bacterial movement in soil and over
fungal growth. Thus, the ubiquitous coexistence of bacteria and fungi in soil, and their
known catabolic cooperation, suggests that physical interactions between them may be of
importance for PAH degradation.
Role of omics technology in PAH degradation

Compared to a pure microbial culture, the process involved in the degradation of PAHs by a
microbial consortium is poorly understood. There are several techniques that help to examine the microbial actions at the community level in response to PAH exposure. These techniques include stable isotope probing (SIP) molecular ngerprinting, clone libraries, and
quantitative PCR (qPCR) of particular genes responsible for degradation of PAHs (de
Menezes et al., 2012). These techniques involve information about gene sequences, which
are available for pure microbial culture but still lack behind at the community level. Using
next-generation sequencing technologies, we can now explore a broader coverage of genetic
material of microorganisms at the community level. Although a metagenome expresses the
genetic diversity of a community, a metatranscriptome also captures the active metabolic
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processes by providing information on gene expression (Gilbert et al., 2008). In practice,

metatranscriptomics involves more complex analysis because individual transcripts vary due
to species diversity and different gene expressions (Simon and Daniel, 2011). Microbial community analysis using pyrosequencing (Bacosa et al., 2015b; Singleton et al., 2011) and Illumina sequencing techniques (Jiang et al., 2013; Sun et al., 2015) revealed the diversity and
richness of hydrocarbon-degrading bacteria in oil-contaminated environments.
Mason et al. (2012) studied the members of the Oceanospirillales found in the Gulf of
Mexico due to the Deepwater Horizon (DWH) oil spill. Isolation and sequencing of two
Oceanospirillales single cells revealed that both cells possessed gene coding for n-alkane and
cycloalkane degradation. An analysis of the metagenomic and metatranscriptomic data
showed a near-complete pathway for cyclohexane oxidation in each cell. Further, it was
found that the draft genome included genes for chemotaxis, motility, and nutrient acquisition strategies, which were also identied in the metagenomes and metatranscriptomes.
Thus, the data provided in this study on the role of Oceanospirillales in oil disposition can
help in understanding how members of the deep-sea microbial community can rapidly
respond and become enriched in the presence of hydrocarbons.
In another study, Mason et al. (2014) investigated the impact of oil deposition due to the
DWH oil spill in the Gulf of Mexico on microbial communities in the surface sediments of
the Gulf of Mexico. The 16S rRNA gene data indicated that the most heavily oil-impacted
sediments were enriched in an uncultured Gammaproteobacteria and a Colwellia species,
both of which were highly similar to sequences in the DWH deep-sea hydrocarbon plume.
To validate the ability of the sediment community to degrade specic hydrocarbon compounds, Mason et al. (2014) conducted microcosm studies with 14C-labeled model compounds and followed their mineralization rates over 90 days of incubation. Based on the
analysis of the metagenomic data, it was concluded that although alkanes and simple aromatics could be degraded by native sediment microbes, it appeared that PAHs could not be
degraded signicantly.
de Menezes et al. (2012) investigated the response of soil microbial community toward
phenanthrene using the metatranscriptomics technique. A marked increase in transcripts
involved in aromatic compound metabolism, respiration, and stress responses, and concurrent decreases in virulence, carbohydrate, deoxyribonucleic acid (DNA) metabolism, and
phosphorus metabolism transcripts were discovered. They demonstrated that on phenanthrene addition, there was a drastic increase in the abundance of dioxygenase, stress
response, and detoxication transcripts. They, for the rst time, have reported the abundance of the proteins heavy metal P-type adenosine triphosphatases (ATPases) and thioredoxin in microorganisms in response to PAH stress in microorganisms. Annotation with
custom databases was constructed with the protein sequences of bacteria or fungi involved
in PAH metabolism and demonstrated an increase in the gene expression, responsible for
PAH degradation. The taxonomic determination of messenger RNA (mRNA) transcripts
illustrated extensive changes in the bacteria, archaea, and fungi. They also showed that Actinobacteria were responsible for the majority of de novo expression of transcripts associated
with dioxygenases, stress response, and detoxication genes. This is the rst study about
experimental metatranscriptomics elaborating microbial community responses toward the
priority pollutants. It also throws light on the novel in situ effects of PAHs on soil microbes.
As this information on the subject is novel, this area can be further explored.
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G. GUPTA ET AL.
As pointed out by Uhlik et al. (2013), it is important to carry out a thorough analysis of
the labeled metagenomes of bioremediative populations using the SIP technique. This analysis enables us to directly link microbial metabolic capability to phylogenetic and metagenomic information by tracking isotopically labeled substances into phylogenetically and
functionally informative biomarkers. Thus, valuable information can be generated for assessing bioremediation potential of autochthonous microorganisms as well as designing and
monitoring engineered bioremediation strategies. Moreover, a great advantage of SIP is its
ability to enable a focused detection and analysis of the organisms active in the utilization of
a specic substrate, either directly or indirectly through the food web. In the context of bioremediation in particular, SIP metagenomics can be quite valuable for revealing the identity
of contaminant degraders and their functional genes. Using this information, an assessment
can be made of their response to biostimulation methods, and the organisms and genes useful for bioaugmentation can also be identied.
The limitations of SIP and the alternatives to SIP have also been discussed by Uhlik et al.
(2013). A major limitation of SIP is very limited availability and high cost of labeled substrates.
Role of biosurfactants in PAH degradation

The environmental persistence of PAHs is due to their low water solubility and ability to be
sorbed to soil organics, which limits their availability to degrade microbes (Yi et al., 2009).
The microbial growth rate becomes limiting on hydrocarbons due to interfacial surface area
between water and oil, which results in less efcient degradation of hydrocarbons (Li and
Chen, 2009). Use of biosurfactants is a more promising approach for enhancing the bioavailability of PAHs (Santos et al., 2011; Yang et al., 2009; Zhao et al., 2011). Biosurfactants are
amphiphilic compounds produced on living surfaces consisting of hydrophilic and hydrophobic parts in their structure (Banat et al., 2010). Microbial degradation of PAHs results in
the production of a variety of biosurfactants.
The use of biosurfactants has proved to be more advantageous over synthetic surfactants due to
its cost-effective nature, biodegradability, and ability to be produced and function in extreme conditions. By contrast, chemically synthesized surfactants are extortionate, nonbiodegradable, and
toxic in nature. Therefore, they contaminate the environment (Makkar and Rockne, 2003). However, the literature reports contradicting results regarding the effects of synthetic surfactant addition on PAH biodegradation. Although some researchers have reported an enhancement in the
biodegradation process (Churchill et al., 1995; Volkering et al., 1995), others have found the inhibition effect in the process of biodegradation by using synthetic surfactants (Makkar and Rockne,
2003; Stelmack et al., 1999). Recent studies have proved that some PAH-degrading bacteria are
able to grow on synthetic nonionic surfactants (e.g., Tween-80) as carbon source, demonstrating
their biodegradability (Bautista et al., 2009; Franzetti et al., 2006; Zhang and Zhu, 2012). These
contrasting reports indicate a need to better understand the mechanisms of biodegradation of
PAHs in the presence of synthetic surfactants.
Biosurfactants increase the surface area of hydrophobic water-insoluble substrates, thus
increasing their bioavailability (Jor et al., 2013). They have a wide range of properties such
as reduction in surface tension, interfacial tension, and critical micelle formation (CMC)
(Mulligan, 2005). These properties result in dissolution of hydrocarbons in microemulsions
or micellar structures produced by biosurfactants. Biosurfactants can be of low molecular
weight as well as high molecular weight. Low-molecular-weight surfactants lower surface
613
tension and interfacial tension, whereas high-molecular-weight surfactants tightly bind to

surfaces (Smyth et al., 2010). Literature reports certain bacteria capable of producing biosurfactants include P. aeruginosa (Thu et al., 2008), Bacillus subtilis (Vaz et al., 2012), Rhodococcus spp. (Mutalik et al., 2008), Bacillus licheniformis, Arthrobacter spp. (Gudi~
na et al., 2010),
Flavobacterium, and Staphylococcus spp. (Ilori et al., 2005).
Abalos et al. (2004) studied the biodegradation of total petroleum hydrocarbons in Casablanca crude oil by a microbial consortium. They reported the increased biodegradation
from 31% to 61% on addition of a biosurfactant (rhamnolipid) produced by P. aeruginosa
AT10. The production of a glycolipid type of biosurfactant by a bacterial strain P. aeruginosa
SP4 was reported during bioremediation of pyrene-contaminated soil (Jor et al., 2013). In
the presence of the glycolipid type of biosurfactant, the degradation rate was found to be
84.6%, which otherwise was only 59.8%. Similarly, Das and Mukherjee (2007) reported the
production of biosurfactants by bacterial strains during the biodegradation of petroleum-oilcontaminated soil from northeast India. B. subtilis DM-04 produced lipopeptide-containing
surfactins and itarins; P. aeruginosa M and NM strains produced a mixture of lipopeptide
and glycoproteins. P. aeruginosa NM strain reported signicantly higher PAH solubilization
in comparison with P. aeruginosa M strain. This strengthens the hypothesis that minor variations in isoforms of biosurfactants produce noticeably large changes in solubilization
effects of biosurfactants (Das and Mukherjee, 2005). Lai et al. (2009) studied the removal of
total petroleum hydrocarbons (TPHs) from soil by two biosurfactants and compared their
efciency with synthetic surfactants. They found that the removal efciency of TPHs was
63%, 62%, 40%, and 35% on using rhamnolipids, surfactin, Tween 80, and Triton X-100,
respectively. It was concluded that biosurfactants exhibited much higher efciency to remove
TPHs than the synthetic ones. Reddy et al. (2010) studied the degradation of phenanthrene
by Brevibacillus sp. PDM-3. They reported that the strain was capable of degrading 93% of
phenanthrene and was also capable of producing biosurfactants.
Mechanism of PAH uptake by surfactants
The increase in surfactant concentration above the critical micelle concentration (CMC) results
in the aggregation of surfactant monomers present in the aqueous solution to form colloidal
micelles. This incorporates PAH molecules into the cores of micelles leading to their solubilization. Above the CMC, surfactants decrease the interfacial tension and incorporate hydrophobic compounds in the micelles, thus improving the mass transfer from the solid or
nonaqueous liquid phase into the aqueous phase (Li and Chen, 2009). The biodegradation of
PAH involves the microbial utilization of PAHs directly from the micellar phase. The process
consists of the following steps. The rst step involves the transport of PAH-solubilized micelles
to the cell boundary. The next step is the transfer of PAH molecules from the lled micelles to
the hemimicelles around the cell. Guha et al. (1998) and Li and Chen (2009) have described
the formation of the hemimicelle layer around the cell in dissolution/dispersion/diffusion of
PAHs. The next step leads to the transfer of PAH molecules from the hemimicelles to the cell.
Effect of micronutrients on biodegradation

Several mineral nutrients such as carbon, nitrogen, phosphate, and potassium are required
for proper growth and metabolism of microorganisms. Contaminated sites often lack
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G. GUPTA ET AL.
available nutrients required for microbial metabolism due to high organic carbon levels
(Breedveld and Sparrevik, 2000). Therefore, contaminated sites can be provided with augmentation of nutrients (generally nitrogen and phosphates) to stimulate the in situ microbial
community to enhance bioremediation (Atagana et al., 2003). The high carbon content of oil
and the low level of other nutrients (such as nitrogen and phosphorus) that are essential for
microbial growth limit the rate and extent of degradation. Therefore, the growth of hydrocarbon-degrading bacteria and hydrocarbon degradation can be strongly enhanced by fertilization of the soil with inorganic N and P (Bamforth and Singleton, 2005). Though little work
has been done on nutrient levels, it is necessary to know the site status before supplementation of additional nutrients. On the basis of quantity and need by the microorganism,
nutrients can be categorized as macro- and micronutrients. In a majority of the treatments,
the C:N:P ratio is maintained as 120:10:1 (Leys et al., 2005; Rodrguez-Martnez et al., 2006).
Simarro et al. (2011) have reported that the most effective molar ratio of C, N, and P was
found to be 100:21:16. Nitrogen is the nutrient most commonly added in bioremediation
projects. It is mainly used by microorganisms for their cellular growth. It is mostly added as
ammonium chloride, urea, ammonia salt, or ammonium nitrate. These nitrogen forms can
be easily assimilated in bacterial metabolism. Simarro et al. (2011) also suggested that
sodium nitrate is a better source of nitrogen than ammonium nitrate due to its solubility
and availability to microorganisms, whereas ammonium nitrate has adsorbent properties.
A recent study (Sihag et al., 2014) has shown that optimal microbial growth and creosote
biodegradation occurred in soil with a C:N ratio of 25:1. In a microbial biomass with a much
lower C:N ratio of 5:1, no enhancement in microbial growth was observed. The second most
commonly added nutrient in the bioremediation process is phosphorus. It is used by
microbes as a source for their cellular growth. Phosphorus can be added as phosphate or
orthophosphoric and polyphosphate salts. Bamforth and Singleton (2005) have pointed out
that even though microbial metabolism may be temporarily increased by the addition of
inorganic N and P, it may cause the long-term inhibition of functionally important organisms leading to the failure of bioremediation. Thomas and Dabkowski (2011) have shown
that enumeration of bacteria capable of degrading PAHs can be signicantly enhanced by
adding glucose (0.025%) (m/v) and (or) root exudates.
Liebeg and Cutright (1999) studied the effect of adding macro- and micronutrients for
enhancing the bioremediation of PAH- or petroleum-contaminated soil. They demonstrated
that the bioactivity of foreign consortium used in bioremediation was maximum when high
levels of micronutrients and low levels of macronutrients were used. The proportion of mineral nutrients that are best suited for bioremediation was 75% sulfur, 3% nitrogen, and 11%
phosphorus on a dry weight basis. It was also shown that microbes had a greater need for
phosphorus than for nitrogen in this particular study. Therefore, it can be stated that
the need of nutrients varies from one site to another due to differences in the soil type, type
of contaminant, degree of contamination, type of microorganisms, and environmental
conditions.
Bioremediation of heavy metal-contaminated sites

Heavy metal pollution has become a matter of serious concern in the world. Heavy metals
are naturally present in soil, but anthropogenic activities are the major source of heavy metal
contamination. Unlike organic substances, heavy metals are nonbiodegradable in nature.
615
This results in their accumulation in soil and water, posing a threat to the environment. The
toxicological effects of heavy metals in soil also result in the reduction of microorganisms
(Khan et al., 2010). Thus, there is a need for remediation of heavy metal-contaminated sites.
The conventional methods generally employed in metal remediation are expensive and
cause pollution. Bioremediation is an eco-friendly and cost-effective method for decontamination of heavy metal-polluted soil. During bioremediation, heavy metals cannot be
degraded but can only be transformed from one oxidation state to another. The transformed
state of heavy metals is generally less toxic. It may be mentioned that bioremediation of
heavy metal-polluted soil is more efcient when the site is simultaneously used for crop production, as it is a nondisruptive method of soil remediation.
Phytoremediation is a type of bioremediation that involves the use of plants and associated
soil microbes to reduce the concentrations or toxic effects of contaminants in the environments (Ali et al., 2013). It leads to an increase in the soil organic matter, thus enhancing its
fertility (Mench et al., 2009). There are several phytoremediation techniques: phytostabilization, phytoextraction (or phytoaccumulation), phytodegradation, phytovolatilization, and phytoltration (Ali et al., 2013; Alkorta et al., 2004). Several researchers have reported the
accumulation of heavy metals in soil through enhanced phytoextraction (Chibuike and Obiora,
2014; Marques et al., 2006), whereas others have shown metal immobilization through
enhanced phytostabilization (Chibuike and Obiora, 2014). Simultaneous application of plants
and microorganisms results in a faster and more efcient cleanup of the contaminated sites
(Weyens et al., 2009). Several microorganisms produce siderophores, iron-complexing molecules, which have high afnity for heavy metals (Garbisu and Alkorta, 2003). It has also been
reported by the same investigators that several bacteria can reduce toxic and mutagenic compounds such as hexavalent chromium to their less toxic trivalent form.
Various algae and bacteria produce secretions that bind with the metals and remove them
from the food chain. Several microorganisms such as Pseudomonas, Bacillus, Escherichia,
and Enterobacter help in contamination of heavy metal-polluted sites by performing bioabsorption and bioaccumulation (Kotas and Stasicka, 2000).
Mycorrhizal fungi and plant growth-promoting rhizobacteria both have been successfully
used in phytoremediation (Reed and Glick, 2005). However, sometimes mycorrhizal fungi
may not perform the remediation of heavy metal-polluted soils due to either high metal concentration or incapability of the some species toward heavy metal decontamination
(Chibuike and Obiora, 2014). Madhaiyan et al. (2007) inoculated tomato plant with
Methylobacterium oryzae and Burkholderia spp. and reported an increased plant growth due
to the reduction in the accumulation of cadmium and nickel in the shoot and root tissues of
the plant. There are several other aspects of phytoremediation that are being currently investigated. These include identication of native plants for phytoremediation, assessment of the
effects of different parameters on phytoremediation efciency, and genetic modication of
plants to enhance their efciency for decontamination of heavy metal-polluted sites. Results
of these investigations may help in enhancing the efciency of phytoremediation (Chen
et al., 2015).
Conclusions
The application of several microorganisms in combination is found to be a universally efcient system to achieve synergistic enhanced rates for PAH degradation. PAH-contaminated
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soils can be remediated using microorganisms (bacteria and fungi individually or in combination). The rate and extent of PAH biodegradation depend on several environmental, biological, and physicochemical factors.
A diverse range of microorganisms have been isolated and applied for PAH degradation,
yet the microbial interactions within the PAH-degrading microbial consortium need to be
further explored. Moreover, most of the experiments have been performed under aerobic
conditions. Therefore, potential anaerobic remediation methods are yet to be explored and
applied to decontaminate several subsurface sites contaminated with PAHs.
Although new pathways involved in PAH degradation have been identied, further
research is needed to explore the microbial interactions within the PAH-degrading consortium and the mechanisms involved during the biodegradation of low- and high-molecularweight PAHs.
Several new technologies in the eld of molecular biology have helped in the identication
of microorganisms and the genes responsible for degradation of PAHs. However, there is a
need to explore the omics technology (metagenomics and metatranscriptomics), which is an
essential tool for the studies on biodegradation of PAHs in contaminated sites. This technology has been recently employed in the environmental microbiology studies and has made a
high impact in the eld of bioremediation.
We conclude that the biodegradation of PAHs using a microbial consortium is a feasible
process, and modern biological methods will play a signicant role in the future developments in this eld.
References
Abalos, A., Vinas, M., Sabate, J., Manresa, M. A., and Solanas, A. M. 2004. Enhanced biodegradation of
Casablanca crude oil by a microbial consortium in presence of a rhamnolipid produced by Pseudomonas aeruginosa AT10. Biodegradation 15, 249260.
Agarwal, T., Khillare, P. S., Shridhar, V., and Ray, S. 2009. Pattern, sources and toxic potential of PAHs
in the agricultural soils of Delhi, India. J. Hazard. Mater. 163, 10331039.
Ahn, C. K., Kim, Y. M., Woo, S. H., and Park, J. M. 2008. Soil washing using various nonionic surfactants and their recovery by selective adsorption with activated carbon. J. Hazard. Mater. 154, 153
160.
Ali, H., Khan, E., and Sajad, M. A. 2013. Phytoremediation of heavy metalsConcepts and applications. Chemosphere 91, 869881.
Alkorta, I., Hernandez-Allica, J., Becerril, J., Amezaga, I., Albizu, I., and Garbisu, C. 2004. Recent ndings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and
metalloids such as zinc, cadmium, lead, and arsenic. Rev. Environ. Sci. Biotechnol. 3, 7190.
Andersson, R. T., Lundstedt, S., Tornberg, K., Schnurer, Y., Oberg, L. G., and Mattiasson, B. 2003.
Incomplete degradation of polycyclic aromatic hydrocarbons in soil inoculated with wood-rotting
fungi and their effects on the indigenous soil bacteria. Environ. Toxicol. Chem. 22, 12381243.
Anyakora, C., Ogbeche, A., Palmer, P., Coker, H., Ukpo, G., and Ogah, C. 2005. GC/MS analysis of
polynuclear aromatic hydrocarbons in sediment samples from the Niger Delta region. Chemosphere 60, 990997.
Arulazhagan, P., Sivaraman, C., Kumar, S. A., Aslam, M., and Banu, J. R. 2014. Co-metabolic degradation of benzo (e) pyrene by halophilic bacterial consortium at different saline conditions. J. Environ. Biol. 35, 445452.
Assih, E. A., Ouattara, A. S., Thierry, S., Cayol, J. L., Labat, M., and Macarie, H. 2002. Stenotrophomonas acidaminiphila sp. nov., a strictly aerobic bacterium isolated from an upow anaerobic sludge
blanket (UASB) reactor. Int. J. Syst. Evol. Microbiol. 52, 559568.
617
Atagana, H. I., Haynes, R. J., and Wallis, F. M. 2003. Optimization of soil physical and chemical conditions for the bioremediation of creosote-contaminated soil. Biodegradation 14, 297307.
Atlas, R. M. 1991. Microbial hydrocarbon degradationBioremediation of oil spills. J. Chem. Tech.
Biotechnol. 52, 149156.
Bacosa, H. P., and Inoue, C. 2015. Polycyclic aromatic hydrocarbons (PAHs) biodegradation potential
and diversity of microbial consortia enriched from tsunami sediments in Miyagi, Japan. J. Hazard.
Mater. 283, 689697.
Bacosa, H. P., Erdner, D. L., and Liu, Z. 2015a. Differentiating the roles of photooxidation and biodegradation in the weathering of Light Louisiana Sweet crude oil in surface water from the Deepwater
Horizon site. Marine Poll. Bull. 95, 265272.
Bacosa, H. P., Liu, Z., and Erdner, D. L. 2015b. Natural sunlight shapes crude oil-degrading bacterial
communities in northern Gulf of Mexico surface waters. Front. Microbiol. 6, 1325.
Bacosa, H., Suto, K., and Inoue, C. 2010. Preferential degradation of aromatic hydrocarbons in kerosene by a microbial consortium. Int. Biodeterior. Biodegrad. 64, 702710.
Bacosa, H. P., Suto, K., and Inoue, C. 2011. Preferential utilization of petroleum oil hydrocarbon components by microbial consortia reects degradation pattern in aliphaticaromatic hydrocarbon
binary mixtures. World J. Microbiol. Biotechnol. 27, 11091117.
Bacosa, H. P., Suto, K., and Inoue, C. 2012. Bacterial community dynamics during the preferential degradation of aromatic hydrocarbons by a microbial consortium. Int. Biodeterior. Biodegrad. 74, 109
115.
Bamforth, S. M., and Singleton, I. 2005. Bioremediation of Polycyclic aromatic hydrocarbons: Current
knowledge and future directions. J. Chem. Technol. Biotechnol. 80, 723736.
Banat, I. M., Franzetti, A., Gandol, I., Bestetti, G., Martinotti, M. G., Fracchia, L., and Marchant, R.
2010. Microbial biosurfactants production, applications and future potential. Appl. Microbiol. Biotechnol. 87, 427444.
Bautista, L. F., Sanz, R., Molina, M. C., Gonzalez, N., and Sanchez, D. 2009. Effect of different nonionic surfactants on the biodegradation of PAHs by diverse aerobic bacteria. Int. Biodeterior. Biodegrad. 63, 913922.
Berdicevsky, I., Duek, L., Merzbach, D., and Yannai, S. 1993. Susceptibility of different yeast species to
environmental toxic metals. Environ. Pollut. 80, 4144.
Betancur-Galvis, L. A., Alvarez-Bernal, D., Ramos-Valdivia, A. C., and Dendooven, L. 2006. Bioremediation of polycyclic aromatic hydrocarbon-contaminated salinealkaline soils of the former Lake
Texcoco. Chemosphere 62, 17491760.
Bogan, B. W., Lahner, L. M., Sullivan, W. R., and Paterek, J. R. 2003. Degradation of straight-chain aliphatic and high-molecular-weight polycyclic aromatic hydrocarbons by a strain of Mycobacterium
austroafricanum. J. Appl. Microbiol. 94, 230239.
Bogan, B. W., Lamar, R. T., and Hammel, K. E. 1996a. Fluorene oxidation in vivo by Phanerochaete
chrysosporium and in vitro during manganese peroxidase dependent lipid peroxidation. Appl. Environ. Microbiol. 62, 17881792.
Bogan, B. W., Schoenike, B., Lamar, R. T., and Cullen, D. 1996b. Expression of lip genes during growth
in soil and oxidation of anthracene by Phanerochaete chrysosporium. Appl. Environ. Microbiol. 62,
36973703.
Boonchan, S., Britz, M. L., and Stanley, G. A. 2000. Degradation and mineralization of high-molecularweight polycyclic aromatic hydrocarbons by dened fungal-bacterial cocultures. Appl. Environ.
Microbiol. 66, 10071019.
Breedveld, G. D., and Sparrevik, M. 2000. Nutrient limited biodegradation of PAHs in various soil
strata at a creosote contaminated site. Biodegradation 11, 391399.
Brodkorb, T. S., and Legge, R. L. 1992. Enhanced biodegradationof phenanthrene in oil tar-contaminated soils supplemented with Phanerochaete chrysosporium. Appl. Environ. Microbiol. 58, 3117
3121.
Cajthaml, T., Pacakova, V., and Sasek, V. 2001. Microbial degradation of polycyclic aromatic hydrocarbons, Chem. Listy. 95, 404.
618
G. GUPTA ET AL.
Cerqueira, V. S., Hollenbach, E. B., Maboni, F., Vainstein, M. H., Camargo, F. A. O., Peralba, M. C. R.,
and Bento, F. M. 2011. Biodegradation potential of oily sludge by pure and mixed bacterial cultures.
Bioresour. Technol. 102, 1100311010.
Chaillan, F., Le Fleche, A., Bury, E., Phantavong, Y. H., Grimont, P., Saliot, A., and Oudot, J. 2004.
Identication and biodegradation potential of tropical aerobic hydrocarbon-degrading microorganisms. Res. Microbiol. 155, 587595.
Chen, M., Xu, P., Zeng, G., Yang, C., Huang, D., and Zhang, J. 2015. Bioremediation of soils contaminated with polycyclic aromatic hydrocarbons, petroleum, pesticides, chlorophenols and heavy metals by composting: Applications, microbes and future research needs. Biotechnol. Adv. 33, 745755.
Chibuike, G. U., and Obiora, S. C. 2014. Heavy metal polluted soils: Effect on plants and bioremediation methods. Appl. Environ. Soil. Sci. 2014, 112.
Chung, W. K., and King, G. M. 2001. Isolation, characterization, and polyaromatic hydrocarbon degradation potential of aerobic bacteria from marine macrofaunal burrow sediments and description
of Lutibacterium anuloederans gen. nov., sp. nov., and Cycloclasticus spirillensus sp. nov. Appl.
Environ. Microbiol. 67, 55855592.
Churchill, P., Dudley, R., and Churchill, S. A. 1995. Surfactant-enhanced bioremediation. Waste Manage. 15, 371377.
Darvishi, P., Ayatollahi, S., Mowla, S. D., and Niazi, A. 2011. Biosurfactant production under extreme
environmental conditions by an efcient microbial consortium, ERCPPI-2. Colloids Surf., B. 84,
292300.
Das, K., and Mukherjee, A. K. 2005. Characterization of biochemical properties and biological activities of biosurfactants produced by Pseudomonas aeruginosa mucoid and non-mucoid strains isolated from hydrocarbon-contaminated soil samples. Appl. Microbiol. Biotechnol. 69, 192199.
Das, K., and Mukherjee, A. K. 2007. Crude petroleum-oil biodegradation efciency of Bacillus subtilis
and Pseudomonas aeruginosa strains isolated from a petroleum-oil contaminated soil from Northeast India. Bioresour. Technol. 98, 13391345.
Dastgheib, S. M. M., Amoozegar, M. A., Khajeh, K., Shavandi, M., and Ventosa, A. 2012. Biodegradation of polycyclic aromatic hydrocarbons by a halophilic microbial consortium. Appl. Microbiol.
Biotechnol. 95, 789798.
de Menezes, A., Clipson, N., and Doyle, E. 2012. Comparative metatranscriptomics reveals widespread
community responses during phenanthrene degradation in soil. Environ. Microbiol. 14, 25772588.
Deppe, U., Richnow, H. H., Michaelis, W., and Antranikian, G. 2005. Degradation of crude oil by an
arctic microbial consortium. Extremophiles 9, 461470.
Dyksterhouse, S. E., Gray, J. P., Herwig, R. P., Lara, J. C., and Staley, J. T. 1995. Cycloclasticus pugetii
gen. nov., sp. nov., an aromatic hydrocarbon degrading bacterium from marine sediments. Int. J.
Syst. Bacteriol. 45, 116123.
Eggen, T., and Majcherczyk, A. 1998. Removal of polycyclic aromatic hydrocarbons (PAH) in contaminated soil by white rot fungus Pleurotus ostreatus. Int. Biodet. Biodegrad. 41, 111117.
~ez, E.,
Fernandez-Luque~
no, F., Valenzuela-Encinas, C., Marsch, R., Martnez-Suarez, C., Vazquez-N
un
and Dendooven, L. 2011. Microbial communities to mitigate contamination of PAHs in soilPossibilities and challenges: A review. Environ. Sci. Pollut. Res. 18, 1230.
Franzetti, A., Di Gennaro, P., Bevilacqua, A., Papacchini, M., and Bestetti, G. 2006. Environmental features of two commercial surfactants widely used in soil remediation. Chemosphere 62, 14741480.
Gan, S., Lau, E. V., and Ng, H. K. 2009. Remediation of soil contaminated with PAHs. J. Hazard.
Mater. 172, 532549.
Garbisu, C., and Alkorta, I. 2003. Basic concepts on heavy metal soil bioremediation. Eur. J. Miner.
Process. Environ. Prot. 3, 5866.
Geiselbrecht, A. D., Hedlund, B. P., Tichi, M. A., and Staley. J. T. 1998. Isolation of marine polycyclic
aromatic hydrocarbon (PAH)-degrading Cycloclasticus strains from the Gulf of Mexico and comparison of their PAH degradation ability with that of Puget Sound Cycloclasticus strains. Appl.
Environ. Microbiol. 64, 47034710.
Geiselbrecht, A. D., Herwig, R. P., Deming, J. W., and Staley, J. T. 1996. Enumeration and phylogenetic
analysis of polycyclic aromatic hydrocarbon-degrading marine bacteria from Puget sound sediments. Appl. Environ. Microbiol. 62, 33443349.
619
Ghazali, F. M., Rahman, R. N. Z. A., Salleh, A. B., and Basri, M. 2004. Biodegradation of hydrocarbons
in soil by microbial consortium. Int. Biodeterior. Biodegrad. 54, 6167.
Gilbert, J. A., Field, D., Huang, Y., Edwards, R., Li, W., Gilna, P., and Joint, I. 2008. Detection of large
numbers of novel sequences in the metatranscriptomes of complex marine microbial communities.
PLoS ONE 3, e3042.
Gonzalez, N., Simarro, R., Molina, M. C., Bautista, L. F., Delgado, L., and Villa, J. A. 2011. Effect of
surfactants on PAH biodegradation by a bacterial consortium and on the dynamics of the bacterial
community during the process. Bioresour. Technol. 102, 94389446.
Gudi~
na, E. J., Teixeira, J. A., and Rodrigues, L. R. 2010. Isolation and functional characterization of a
biosurfactant produced by Lactobacillus paracasei. Colloids Surf. B. Biointerfaces. 76, 298304.
Guha, S., Jaffe, P. R., and Peters, C. A. 1998. Bioavailability of mixtures of PAHs partitioned into the
micellar phase of a nonionic surfactant. Environ. Sci. Technol. 32, 23172324.
Guo, C. L., Zhou, H. W., Wong, Y. S., and Tam, N. F. Y. 2005. Isolation of PAH-degrading bacteria
from mangrove sediments and their biodegradation potential. Mar. Pollut. Bull. 51, 10541061.
Harayama, S. 1997. Polycyclic aromatic hydrocarbon bioremediation design. Curr. Opin. Biotechnol. 8,
268273.
Haritash, A. K., and C. P. Kaushik. 2009. Biodegradation aspects of polycyclic aromatic hydrocarbons
(PAHs): A review. J. Hazard. Mater. 169, 115.
Hatzinger, P. B., and Alexander, M. 1995. Effect of aging on chemicals in soil on their biodegradability
and extractability. Environ. Sci. Technol. 29, 537545.
Head, I. M. 1998. Bioremediation: Towards a credible technology. Microbiology 144, 599608.
Ilori, M., Amobi, C., and Odocha, A. 2005. Factors affecting biosurfactant production by oil degrading
Aeromonas spp. isolated from a tropical environment. Chemosphere 61, 985992.
Jacques, R. J. S., Okeke, B. C., Bento, F. M., Teixeira, A. S., Peralba, M. C. R., and Camargo, F. A. O.
2008. Microbial consortium bioaugmentation of a polycyclic aromatic hydrocarbons contaminated
soil. Bioresour. Technol. 99, 26372643.
Jiang, X. T., Peng, X, Deng, G. H., Sheng, H. F., Wang, Y., Zhou, H. W., andTam, N. Y. 2013. Illumina
sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a Mangrove
wetland. Microb. Ecol. 66, 96104.
Johnsen, A. R., Wick, L. Y., and Harms, H. 2005. Principles of microbial PAHs-degradation in soil.
Environ. Pollut. 133, 7184.
Jor, S., Rezaee, A., Mobeh-Ali, G-A., and Jaafarzadeh, N. A. 2013. Application of Biosurfactants Produced by Pseudomonas aeruginosa SP4 for Bioremediation of Soils Contaminated by Pyrene. Soil
Sediment Contam. 22, 890911
Juhasz, A. L., and Naidu, R. 2000. Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: A review of the microbial degradation of Benzo[a]pyrene. Int. Biodeterior. Biodegrad. 45,
5788.
Kalzadeh, F., Raee, S., and Tahery, Y. 2011. Evaluation of bioremediation of naphthalene using
native bacteria isolated from oil contaminated soils in Iran. Ann. Biol. Res. 2, 610616.
Kanaly, R. A., Bartha, R., Watanabe, K., and Harayama, S. 2000. Rapid mineralization of benzo [a]
pyrene by a microbial consortium growing on diesel fuel. Appl. Environ. Microbiol. 66, 42054211.
Kelley, I., Freeman, J. P., Evans, F. E., and Cerniglia, C. E. 1990. Identication of metabolites from degradation of naphthalene by a Mycobacterium sp. Biodegradation 1, 283290.
Khan, S., Hesham, A. E.-L., Qiao, M., Rehman, S., and He, J.-Z. 2010. Effects of Cd and Pb on soil
microbial community structure and activities. Environ. Sci. Pollut. Res. 17, 288296
Kohlmeier, S., Smits, T. H. M., Ford, R. M., Keel, C., Harms, H., and Wick, L. Y. 2005. Taking the fungal highway: Mobilization of pollutant-degrading bacteria by fungi. Environ. Sci. Technol. 39,
46404646.
Komukai-Nakamura, S., Sugiura, K., Yamauchi-inomata, Y., Toki, H., Venkateshwaran, K., Yamamoto, S., Tanaka, H., and Harayama, S. 1996. Construction of bacterial consortia that degrade Arabian light crude oil. J. Ferment. Bioeng. 82, 570574.
Kotas, J., and Stasicka, Z. 2000. Chromium occurrence in the environment and methods of its speciation. Environ. Pollut. 107, 263283.
620
G. GUPTA ET AL.
Lai, C. C., Huang, Y. C., Wei, Y. H., and Chang, J. S. 2009. Biosurfactant-enhanced removal of total
petroleum hydrocarbons from contaminated soil. J. Hazard. Mater. 167, 609614.
Leahy, J. G., and Colwell, R. R. 1990. Microbial degradation of hydrocarbons in the environment.
Microbiol. Rev. 54, 305315.
Leys, N. M., Bastiaens, L., Verstraete, W., and Springael, D. 2005. Inuence of the carbon/nitrogen/
phosphorus ratio on polycyclic aromatic hydrocarbon degradation by Mycobacterium and Sphingomonas in soil. Appl. Microbiol. Biotechnol. 66, 726736
Li, J. L., and Chen, B. H. 2009. Surfactant-mediated biodegradation of polycyclic aromatic hydrocarbons. Materials 2, 7694.
Li, X., Li, P., Lin, X., Zhang, C., Li, Q., and Gong, Z. 2008. Biodegradation of aged polycyclic aromatic
hydrocarbons (PAHs) by microbial consortia in soil and slurry phases. J. Hazard. Mater. 150, 21
26.
Liebeg, E. W., and Cutright, T. J. 1999. The investigation of enhanced bioremediation through the
addition of macro and micro nutrients in a PAH contaminated soil. Int. Biodeter. Biodegrad. 44,
5564.
Lin, Y., and Cai, L. X. 2008. PAH-degrading microbial consortium and its pyrene-degrading plasmids
from mangrove sediment samples in Huian, China. Marine Pollut. Bull. 57, 703706.
Liu, K., Han, W., Pan, W., and Riley, J. T. 2001. Polycyclic aromatic hydrocarbon (PAH) emissions
from a coal-red pilot FBC system. J. Hazard. Mater. 84, 175188.
Liu, S., Hou, Y., and Sun, G. 2013. Synergistic degradation of pyrene and volatilization of arsenic by
co-cultures of bacteria and a fungus. Front. Environ. Sci. Eng. 7, 191199.
MacLeod, C. J., Morriss, A. W., and Semple, K. T. 2001. The role of microorganisms in ecological risk
assessment of hydrophobic organic contaminants in soils. Adv. Appl. Microbiol. 48, 171212.
Madhaiyan, M., Poonguzhali, S., and Sa, T. 2007. Metal tolerating methylotrophic bacteria reduces
nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.).
Chemosphere 69, 220228.
Maeir, R. M., Pepper, I. L., and Gerba, P. C. 2000. A Textbook of Environmental Microbiology. Academic Press, San Diego, CA.
Makkar, R. S., and Rockne, K. J. 2003. Comparison of synthetic surfactants and biosurfactants in
enhancing biodegradation of polycyclic aromatic hydrocarbons. Environ. Toxicol. Chem. 22, 2280
2292.
Malik, Z. A., and Ahmed, S. 2012. Degradation of petroleum hydrocarbons by oil eld isolated bacterial consortium. Afr. J. Biotechnol. 11, 650658.
Mandal, A. K., Sarma, P. M., Singh, B., Jeyaseelan, C. P., Channashettar, V. A., Lal, B., and Datta, J.
2011. Bioremediation: A sustainable eco-friendly biotechnological solution for environmental pollution in oil industries. J. Sustain. Dev. Environ. Prot. 1, 523.
Mandalakis, M., Tsapakis, M., Tsoga, A., and Stephanou, E. G. 2002. Gasparticle concentrations and
distribution of aliphatic hydrocarbons, PAHs, PCBs and PCDD/Fs in the atmosphere of Athens
(Greece). Atmos. Environ. 36, 40234035.
Margesin, R., and Schinner, F. 2001. Biodegradation and bioremediation of hydrocarbons in extreme
environments. Appl. Microbiol. Biotechnol. 56, 650663.
Marques, A. P. G. C., Oliveira, R. S., Rangel, A. O. S. S., and Castro, P. M. L. 2006. Zinc accumulation
in Solanum nigrum is enhanced by different arbuscular mycorrhizal fungi. Chemosphere 65, 1256
1263.
Mason, O. U., Hazen, T. C., Borglin, S., Chain, P. S., Dubinsky, E. A., Fortney, J. L., and Mackelprang,
R. 2012. Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to
Deepwater Horizon oil spill. ISME J. 6, 17151727.
Mason, O. U., Scott, N. M., Gonzalez, A., Robbins-Pianka, A., Blum, J., Kimbrel, J., and Fortney, J. L.
2014. Metagenomics reveals sediment microbial community response to Deepwater Horizon oil
spill. ISME J. 8, 14641475.
Mench, M., Schwitzguebel, J. P., Schroeder, P., Bert, V., Gawronski, S., and Gupta, S. 2009. Assessment
of successful experiments and limitations of phytotechnologies: Contaminant uptake, detoxication and sequestration, and consequences for food safety. Environ. Sci. Pollut. Res. 16, 876900
621
Mester, T., and Tien, M. 2000. Oxidation mechanism of ligninolyticenzymes involved in the degradation of environmental pollutants. Int. Biodeterior. Biodegrad. 46, 5159.
Moghadam, M. S., Ebrahimipour, G., Abtahi, B., Ghassempour, A., and Hashtroudi, M. S. 2014. Biodegradation of polycyclic aromatic hydrocarbons by a bacterial consortium enriched from mangrove sediments. J. Environ. Health Sci. Eng. 12, 114.
Mohan, S. V., Kisa, T., Ohkuma, T., Kanaly, R. A., and Shimizu, Y. 2006. Bioremediation technologies
for treatment of PAH-contaminated soil and strategies to enhance process efciency. Rev. Environ.
Sci. Biotechnol. 5, 347374.
Moody, J. D., Freeman, J. P., Fu, P. P., and Cerniglia, C. E. 2004. Degradation of benzo[a]pyrene by
Mycobacterium vanbaalenii PYR-1. Appl. Environ. Microbiol. 70, 340345.
Moustafa, Y. M. 2004. Contamination by polycyclic aromatic hydrocarbons in some Egyptian Mediterranean Coasts. Biosci. Biotechnol. Res. Asia 2, 1524.
Mueller, J. G., Cerniglia, C. E., and Pritchard, P. H. 1996. Bioremediation of environments contaminated by polycyclic aromatic hydrocarbons. In: Bioremediation: Principles and Applications, pp.
12151294 (Crawford, R. L., Crawford, D. L., Eds), Cambridge University Press, UK.
Mulligan, C. N. 2005. Environmental applications for biosurfactants. Environ. Pollut. 133, 183198.
Mutalik, S., Vaidya, B., Joshi, R., Desai, K., and Nene, S. 2008. Use of response surface optimization for
the production of biosurfactant from Rhodococcus spp. MTCC 2574. Bioresour. Technol. 99, 7875
7880.
Muthuswamy, S., Binupriya, A. R., Baik, S., and Yun, S. 2008. Biodegradation of crude oil by individual
bacterial strains and a mixed bacterial consortium isolated from hydrocarbon contaminated areas.
CLEANSoil Air Water 36, 9296.
Ofce of Technology Assessment. 1991. Bioremediation of Marine Oil Spills: An Analysis of Oil Spill
Response Technologies, OTA-BP-O-70, Washington, DC.
Ohgew, K., Seong, J. K., Ricky, D. H., Hongyan, C., Dae, W. K., Gao, Y., Yu, Li-Rong., Baek, S., Baek,
Dong-Heon., Ahn, H., and Cerniglia, C. E. 2011. Polycyclic Aromatic Hydrocarbon metabolic network in Mycobacterium vanbaalenii PYR-1. J. Bacteriol. 193, 43264337.
Okere, U. V., and Semple, K. T. 2012. Biodegradation of PAHs in Pristine soils from different climatic regions. J. Bioremed. Biodegrad. S1, 111.
Pan, B., Xing, B. S., Liu, W. X., Tao, S., Lin, X. M., Zhang, X. M., Zhang, Y. X., Xiao, Y., Dai, H. C., and
Yuan, H. S. 2006. Distribution of sorbed phenanthrene and pyrene in different humic fractions of
soils and importance of humin. Environ. Pollut. 143, 2433.
Pawar, A. N., Ugale, S. S., More, M. G., Kokani, N. F., and Khandelwal, S. R. 2013. Biological degradation of naphthalene: A new era. J. Bioremed. Biodegrad. 4, 203.
Pozdnyakova, N. N. 2012. Involvement of the ligninolytic system of white-rot and litter-decomposing
fungi in the degradation of polycyclic aromatic hydrocarbons. Biotechnol. Res. Int. 2012, Article ID
243217, 20.
Rahman, K. S. M., Thahira-Rahman, J., Lakshmanaperumalsamy, P., and Banat, I. M. 2002. Towards
efcient crude oil degradation by a mixed bacterial consortium. Bioresour. Technol. 85, 257261.
Reddy, M. S., Naresh, B., Leela, T., Prashanthi, M., Madhusudhan, N. C., Dhanasri, G., and Devi, P.
2010. Biodegradation of phenanthrene with biosurfactant production by a new strain of Brevibacillus sp. Bioresour. Technol. 101, 79807983.
Reed, M. L., and Glick, B. R. 2005. Growth of canola (Brassica napus) in the presence of plant growthpromoting bacteria and either copper or polycyclic aromatic hydrocarbons. Can. J. Microbiol. 51,
10611069.
Reid, B. J., Jones, K. C., and Semple, K. T. 2000. Bioavailability of persistant organic pollutants in soils
and sedimentsA perspective on mechanisms, consequences and assessment. Environ. Pollut.
108, 103112.
Rockne, K. J., Shor, L. M., Young, L. Y., Taghon, G. L., and Kosson, D. S. 2002. Distributed sequestration and release of PAHs in weathered sediment: The role of sediment structure and organic carbon properties. Environ. Sci. Technol. 36, 26362644.
Rodrguez-Martnez, E. M., Perez, E. X., Schadt, C. W., Zhou, J., and Massol-Deya, A. A. 2006. Microbial diversity and bioremediation of a hydrocarbon-contaminated aquifer (Vega Baja, Puerto
Rico). Int. J. Environ. Res. Public Health 3, 292300.
622
G. GUPTA ET AL.
Romero, M. C., Cazau, M. C., Giorgieri, S., and Arambarri, A. M. 1998. Phenanthrene degradation by
microorganisms isolated from a contaminated stream. Environ. Pollut. 101, 355359.
Salleh, A. B., Ghazali, F. M., Rahman, R. N. Z. A., and Basri, M. 2003. Bioremediation of petroleum
hydrocarbon pollution. Indian J. Biotechnol. 2, 411425.
Santos, H. F., Carmo, F. L., Paes, J. E., Rosado, A. S., and Peixoto, R. S. 2011. Bioremediation of mangroves impacted by petroleum. Water Air Soil Pollut. 216, 329350.
Sarma, P. M., Bhattacharya, D., Krishnan, S., and Lal, B. 2004. Assessment of intra-species diversity
among strains of Acinetobacter baumannii isolated from sites contaminated with petroleum hydrocarbons. Can. J. Microbiol. 50, 405414.
Sartoros, C., Yerushalmi, L., Beron, P., and Guiott, S. R. 2005. Effects of surfactant and temperature on
biotransformation kinetics of anthracene and pyrene. Chemosphere 61, 10421050.
Semple, K. T., Dew, N. M., Doick, K. J., and Rhodes, A. H. 2006. Can microbial mineralization be used
to estimate microbial availability of organic contaminants in soil? Environ. Pollut. 140, 164172.
Semple, K. T., Morriss, A. W. J., and Paton, G. I. 2003. Bioavailability of hydrophobic organic contaminants in soils: Fundamental concepts and techniques for analysis. Eur. J. Soil Sci. 54, 809818.
Seo, J. S., Keum, Y. S., and Li, Q. X. 2009. Bacterial degradation of aromatic compounds. Int. J. Environ. Res. Public Health 6, 278309.
Sihag, S., Pathak, H., and Jaroli, D. P. 2014. Factors affecting the rate of biodegradation of polyaromatic hydrocarbons. Int. J. Pure Appl. Biosci. 2, 185202.
Simarro, R., Gonzalez, N., Bautista, L. F., Sanz, R., and Molina, M. C. 2011. Optimisation of key abiotic
factors of PAH (naphthalene, phenanthrene and anthracene) biodegradation process by a bacterial
consortium. Water Air Soil Pollut. 217, 365374.
Simon, C., and Daniel, R. 2011. Metagenomic analyses: Past and future trends. Appl. Environ. Microbiol. 77, 11531161.
Singh, H. 2006. Mycoremediation: Fungal bioremediation, Wiley Interscience, New York, NY.
Singleton, D. R., Richardson, S. D., and Aitken, M. D. 2011. Pyrosequence analysis of bacterial communities in aerobic bioreactors treating polycyclic aromatic hydrocarbon-contaminated soil. Biodegradation 22, 10611073.
Smyth, T. J. P., Perfumo, A., Marchant, R., and Banat, I. M. 2010. Isolation and analysis of low molecular weight microbial glycolipids. In: Handbook of Hydrocarbon and Lipid Microbiology, pp. 3705
3723 (Timmis, K. N., Ed), Springer, Berlin.
Soclo, H. H., Garrigues, P., and Ewald, M. 2000. Origin of polycyclic aromatic hydrocarbons (PAHs)
in coastal marine sediments: Case studies in Cotonou (Benin) and Aquitaine (France) areas. Mar.
Pollut. Bull. 40, 387396.
Stelmack, P. L., Gray, M. R., and Pickard, M. A. 1999. Bacterial adhesion to soil contaminants in the
presence of surfactants. Appl. Environ. Microbiol. 65, 163168.
Sun, W. M., Li, J. W., Jiang, L., Sun, Z. L., Fu, M. Y., and Peng, X. T. 2015. Proling microbial community structures across six large oilelds in China and the potential role of dominant microorganisms in bioremediation. Appl. Microbiol. Biotechnol. 99, 87518764.
Sutherland, J. B., Rai, F., Khan, A. A., and Cerniglia, C. E. 1995. Mechanisms of polycyclic aromatic
hydrocarbon degradation. In: Microbial Transformation and Degradation of Toxic Organic Chemicals, pp. 269306 (Young, L. Y., and Cerniglia, C. E., Eds), Wiley-Liss, New York, NY.
Tang, Y., Qi, J. L., and Krieger-Brockett, B. 2005. Evaluating factors that inuence microbial henanthrene biodegradation rates by regression with categorical variables. Chemosphere 59, 729741.
Taylor, L. T., and Jones, D. M. 2001. Bioremediation of coal tar PAH in soils using biodiesel. Chemosphere 44, 11311136.
Thavasi, R., Jayalakshmi, S., and Banat, I. M. 2011. Effect of biosurfactant and fertilizer on biodegradation of crude oil by marine isolates of Bacillus megaterium, Corynebacterium kutscheri and Pseudomonas aeruginosa. Bioresour. Technol. 102, 772778.
Thomas, J. C., and Dabkowski, R. T. 2011. Glucose and plant exudate enhanced enumeration of bacteria capable of degrading polycyclic aromatic hydrocarbons. Can. J. Microbiol. 57, 10671072.
Thu, T., Noha, N., Michael, Y., and Sabatini, M. 2008. Rhamnolipid biosurfactant mixtures for environmental remediation. Water Res. 42, 17351743.
623
Trzesicka-Mlynarz, D., and Ward, O. P. 1995. Degradation of polycyclic aromatic hydrocarbons

(PAHs) by a mixed culture and its component pure cultures, obtained from PAH-contaminated
soil. Can. J. Microbiol. 41, 470476.
Uhlik, O., Leewis, M. C., Strejcek, M., Musilova, L., Mackova, M., Leigh, M. B., and Macek, T. 2013.
Stable isotope probing in the metagenomics era: A bridge towards improved bioremediation. Biotechnol. Adv. 31, 154165.
Vaz, D., Gudina, E., and Alameda, E. 2012. Performance of a biosurfactant produced by a Bacillus subtilis strain isolated from crude oil samples as compared to commercial chemical surfactants. Colloids Surf. B: Biointerfaces 89, 167174.
Vidali, M. 2011. Bioremediation: An overview. Pure Appl Chem 73, 11631172.
Volkering, F., Breure, A., Andel, J., and Rulkens, W. 1995. Inuence of non-ionic surfactants on bioavailability and biodegradation of polycyclic aromatic hydrocarbons. Appl. Environ. Microbiol. 61,
16991705.
Weyens, N., van der Lelie, D., Taghavi, S., Newman, L., and Vangronsveld, J. 2009. Exploiting plant
microbe partnerships to improve biomass production and remediation. Trends Biotechnol. 27,
591598.
Wick, L. Y., Remer, R., Wurz, B., Reichenbach, J., Braun, S., Schafer, F., and Harms, H. 2007. Effect of
fungal hyphae on the access of bacteria to phenanthrene in soil. Environ. Sci. Technol. 41, 500505.
Wu, M., Chen, L., Tian, Y., Ding, Y., and Dick, W. A. 2013. Degradation of polycyclic aromatic hydrocarbons by microbial consortia enriched from three soils using two different culture media. Environ. Pollut. 178, 152158.
Yang, S. Z., Jin, H. J., Wei, Z., He, R. X., Ji, Y. J., Li, X. M., and Yu, S. P. 2009. Bioremediation of Oil
Spills in Cold Environments: A review. Pedosphere. 19, 371381.
Yeung, A. T., and Gu, Y-Y. 2011. A review on techniques to enhance electrochemical remediation of
contaminated soils. J. Hazard. Mater. 195, 1129.
Yi, C., Yu-Hong, C., and Jo, W. 2009. Biosurfactant-enhanced removal of total petroleum hydrocarbons from contaiminated soil. J. Hazard. Mater. 167, 609614.
Yu, S. H. 2007. Bioremediation of polycyclic aromatic hydrocarbons (PAHs) by microorganisms in
mangrove sediments, Doctoral dissertation, City University of Hong Kong.
Yu, K. S. H., Wong, A. H. Y., Yau, K. W. Y., Wong, Y. S., and Tam, N. F. Y. 2005a. Natural attenuation,
biostimulation and bioaugmentation on biodegradation of polycyclic aromatic hydrocarbons
(PAHs) in mangrove sediments. Mar. Pollut. Bull. 51, 10711077.
Yu, S. H., Ke, L., Wong, Y. S., and Tam, N. F. Y. 2005b. Degradation of polycyclic aromatic hydrocarbons by a bacterial consortium enriched from mangrove sediments. Environ. Int. 31, 149154.
Yu, X. Z., Wu, S. C., Wu, F. Y., and Wong, M. H. 2011. Enhanced dissipation of PAHs from soil using
mycorrhizal ryegrass and PAH-degrading bacteria. J. Hazard. Mater. 186, 12061217.
E., Cuevas, M. D. C., and Cortes-Espinosa, D. V. 2014. Isolation and selection of
Zafra, G., Absal
on, A.
a highly tolerant microbial consortium with potential for PAH biodegradation from heavy crude
oil-contaminated soils. Water Air Soil Pollut. 225, 118.
Zhang, X. X., Cheng, S. P., Cheng-Jun, Z. H. U., and Shi-Lei, S. U. N. 2006. Microbial PAH-degradation in soil: Degradation pathways and contributing factors. Pedosphere 16, 555565.
Zhang, H. M., Kallimanis, A., Koukkou, A. I., and Drainas, C. 2004. Isolation and characterization of
novel bacteria degrading polycyclic aromatic hydrocarbons from polluted Greek soils. Appl. Microbiol. Biotechnol. 65, 124131.
Zhang, D., and Zhu, L. 2012. Effects of Tween 80 on the removal, sorption and biodegradation of pyrene by Klebsiella oxytoca PYR-1. Environ. Pollut. 164, 169174.
Zhao, Z., Selvam, A., and Woon-Chung Wong, J. 2011. Synergistic effect of thermophilic temperature
and biosurfactant produced by Acinetobacter calcoaceticus BU03 on the biodegradation of phenanthrene in bioslurry system. J. Hazard. Mater. 190, 345350.
Zhong, Y., Luan, T., Lin, L., Liu, H., and Tam, N. F. 2011. Production of metabolites in the biodegradation of phenanthrene, uoranthene and pyrene by the mixed culture of Mycobacterium sp. and
Sphingomonas sp. Bioresour. Technol. 102, 29652972.

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Soil and Sediment Contamination: An International

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Biodegradation of Polycyclic Aromatic

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Date: 18 October 2016, At: 22:38

SOIL AND SEDIMENT CONTAMINATION

Biodegradation of Polycyclic Aromatic Hydrocarbons

The presence of polycyclic aromatic hydrocarbons (PAHs) in the soil is a

CONTACT Vipin Kumar

SOIL AND SEDIMENT CONTAMINATION

Effect on PAH degradation

Microbial metabolism rate; bioavailability

Microbial metabolism rate; bioavailability

Reid et al. (2000); Johnsen et al. (2005); Tang

Bioavailability; mass transfer; microbial

Johnsen et al. (2005); Tang et al. (2005);

Bamforth and Singleton (2005); Sartoros

Figure 1. Bioavailable PAH fractions in soil.

SOIL AND SEDIMENT CONTAMINATION

of PAH-polluted sites, but it still requires a deeper knowledge of biochemical pathway

Mechanism of PAH degradation

PAH degradation by bacteria

Further catabolism involves ring cleavage by dioxygenase to form aliphatic intermediates.

PAH degradation by fungi

SOIL AND SEDIMENT CONTAMINATION

Efciency of microbial degradation of PAHs

Microbial consortia (bacteria, fungi, and bacteria

Microbial consortia (bacteria, fungi, and bacteria

Gammaproteobacteria AY972873.1, Citrobacter sp.

Rhodococcus sp., Acinetobacter sp., Pseudomonas

Fluorene and Phenanthrene

Crude oil-contaminated soil

Table 2. Degradation rates of PAHs by microbial consortium.

Zafra et al. (2014)

Achromobacter sp. AYS3

Crude oil-contaminated soil

Liu et al. (2013)

Zhong et al. (2011)

Lin and Cai (2008)

Darvishi et al. (2011)

Jacques et al. (2008)

Muthuswamy et al. (2008)

Arulazhagan et al. (2014)

SOIL AND SEDIMENT CONTAMINATION

SOIL AND SEDIMENT CONTAMINATION

Pseudomonas sp. BPS1-8

SOIL AND SEDIMENT CONTAMINATION

remediation of PAH-contaminated sites. However, the degradation metabolites in these

Role of omics technology in PAH degradation

SOIL AND SEDIMENT CONTAMINATION

processes by providing information on gene expression (Gilbert et al., 2008). In practice,

Role of biosurfactants in PAH degradation

SOIL AND SEDIMENT CONTAMINATION

tension and interfacial tension, whereas high-molecular-weight surfactants tightly bind to

Effect of micronutrients on biodegradation

Bioremediation of heavy metal-contaminated sites

SOIL AND SEDIMENT CONTAMINATION

SOIL AND SEDIMENT CONTAMINATION

SOIL AND SEDIMENT CONTAMINATION

SOIL AND SEDIMENT CONTAMINATION