Eevers Et Al (2017) - Bio e Fitorremediação

CHAPTER SEVEN
Bio- and Phytoremediation of

Pesticide-Contaminated
Environments: A Review
Nele Eevers*, Jason C. Whitex, Jaco Vangronsveld*, 1 and
Nele Weyens*
*Hasselt University, Diepenbeek, Belgium
x
Connecticut Agricultural Experiment Station, New Haven, CT, United States
1
Corresponding author: E-mail: jaco.vangronsveld@uhasselt.be
Contents
1. Introduction 278
2. Pesticides: Different Types and Characteristics 279
3. Behaviour of Pesticides in the Environment 281
3.1 Transport of Pesticides 282
3.2 Transfer of Pesticides 282
3.3 Transformation 283
4. Remediation of Pesticides 283
4.1 Bioremediation 284
4.2 Plant-Associated Remediation 293
4.2.1 Rhizoremediation 293
4.2.2 Phytoremediation 296
5. Advantages and Disadvantages of Natural Remediation Technologies 304
6. Conclusion, Future Perspectives and Challenges 306
References 306
Abstract
Pesticide-contaminated fields can be found worldwide due to excessive use of
insecticides, herbicides and fungicides. Many of the pesticides that were once used
intensively are now forbidden and have been shown to have deleterious health effects.
Plants, bacteria and fungi have been shown to possess pesticide-degrading capacities,
which can be applied in the successful remediation of contaminated fields and water.
This article will first provide an overview of the different types of pesticides,
their application and their key characteristics, followed by an analysis of their
behaviour in the environment. Pesticides that are introduced into the environment
seldom stay where they were applied. A complex system of transport, transfer and
transformation of pesticides throughout different environmental compartments
often takes place. These processes all influence the possible remediation of the
Advances in Botanical Research, Volume 83
© 2017 Elsevier Ltd.
j
ISSN 0065-2296
http://dx.doi.org/10.1016/bs.abr.2017.01.001 All rights reserved. 277
278 Nele Eevers et al.
pesticide-contaminated media. We will then review several possible remediation

strategies that are currently available. Bioremediation is the first technology that is
reviewed. With bioremediation, the focus is on the remediation of pesticides by micro-
organisms in bulk soil, without the aid or presence of plants. Second, plant-associated
remediation is discussed. When focussing on plant-associated remediation, a distinc-
tion has to be made between rhizoremediation in the rhizosphere and phytoreme-
diation within the plant tissues. While rhizoremediation and phytoremediation
processes are possible solely with the use of plants, many of these processes are
optimized by associations between plants and microorganisms. Plants and bacteria
or fungi often live in a symbiotic relationship that aids them in surviving contaminated
environments, as well as with the degradation of the contaminants they encounter.
In the last part of the review, we discuss the advantages and disadvantages of
“natural” remediation strategies as compared to more classical industrial approaches.
1. INTRODUCTION
Pesticides have been extensively used worldwide for crop protection
in agriculture and gardening as well as in the management of insect-borne
diseases such as malaria and typhus (McKone & Ryan, 1989). This wide-
spread use has led to the contamination of many agricultural soils, natural
water reservoirs and rural areas by persistent organic pesticides (Chaudry,
Blom-Zandstra, Gupta, & Joner, 2005; Pascal-Lorber & Laurent, 2011).
For a long period, the primary goal in farming was to protect crops against
pests and thus gain the highest crop yields possible. In the meantime, the
toxicity of the compounds used to both the farmers and consumers of the
crops, as well as the environment, were likely underestimated and not always
the primary concern when applying pesticides (Mackay & Fraser, 2000).
Many of the pollutants were applied globally for years before it was
discovered that they possessed unacceptable toxicity and hazard with regard
to human health (Berdowski, Baas, Bloos, Visschedijk, & Zandveld, 1997).
Often, these chemicals were also persistent in natural environments. Long
after their original use, the analytes remain in soils and sediments, from
which they can subsequently enter the food chain and surface and ground
water (Gavrilescu, 2004; Li, Scholdz, & Van Heyst, 2000). One primary
concern for these persistent organic pollutants (POPs) is that their hydro-
phobicity can lead to accumulation in adipose tissues of animals, which
can cause biomagnification in higher trophic levels. These increasing levels
of toxic compounds in the body may cause health problems over time
(Kaufman, 1983; Moerner, Bos, & Fredrix, 2002).
Nature-Based Remediation of Pesticides 279
Classical remediation technologies for areas contaminated with POPs

include physicochemical methods such as incineration, burning, land filling,
composting and chemical amendments (Kempa, 1997; Wehtje, Walker, &
Shaw, 2000). As these methods are mainly ex situ, there is a high cost
associated with excavation and transportation. Furthermore, since a signifi-
cant part of the soil is removed, these methods are invasive and destructive to
the overall ecosystem. Consequently, over the last decades there has been
increasing interest for in situ remediation technologies, since they are nonin-
vasive, low-cost, low-maintenance and often solar-driven (Chaudry et al.,
2005). Bioremediation and phytoremediation, either with or without the
assistance of plant-associated bacteria, are two “natural” remediation tech-
nologies that have been proven successful in many instances. Both strategies
rely on the natural capacities of soil microorganisms and plants to take up
contaminants as they do with nutrients and to metabolize, store, or even
co-metabolize them (McGuinness & Dowling, 2009). The efficient applica-
tion of these technologies is complicated by the wide variety of contami-
nants that are present in soils. Since every contaminated soil has its own
specific physicochemical properties and contaminant profile, each remedia-
tion process has to be optimized or even tailored accordingly (Glick, 2003).
Depending on the situation, a choice has to be made whether to utilize
bioremediation, which relies solely on soil microorganisms such as bacteria
and fungi, or for phytoremediation, which relies on plants for the remedia-
tion of contaminated soils. A third option is to exploit the symbiotic
relationships between plants and their associated microorganisms for an
enhanced phytoremediation efficiency of POPs and other contaminants
(Weyens, Van Der Lelie, Taghavi, Newman, & Vangronsveld, 2009).
In this review, an overview will be given on the common remedial
options for different pesticides. Bioremediation and phytoremediation,
with or without plant-associated microorganisms, are both discussed in
detail and a summary of plant and microbial species that have proven effec-
tive in remediation is provided. Lastly, the future challenges and perspectives
are described.
2. PESTICIDES: DIFFERENT TYPES AND

CHARACTERISTICS
“Pesticides” is the collective term for all chemicals that are used to
counteract a certain group of organisms. The primary classes of pesticides
are insecticides (against insects), herbicides (against plants) and fungicides
(against fungi). However, inside these different classes, there still is a wide
variety between the compounds and their chemical properties. They are
defined by their ionic or nonionic properties, hydrophobic properties,
mechanism of action and their molecular structure (Gavrilescu, 2005).
The four main groups of insecticides are: organochlorines, organophos-
phates, carbamate esters and pyrethroids. When considering insecticide
contamination, organochlorines are often the chemicals of greatest concern.
Commonly known members of this group are the DDTs (dichlorodiphe-
nyltrichloroethane), DDE (dichlorodiphenyldichloroethylene), DDD
(dichlorodiphenyldichloroethane), the HCHs (hexacyclochlorohexanes:
a, b, g, d, t) and chlordane (Pascal-Lorber & Laurent, 2011). No less than
eight compounds of the “Dirty Dozen” that were defined by the Stockholm
Convention on persistent organic pollutants are organochlorine insecticides
(Annex A, Stockholm Convention, 2001). The Stockholm Convention
states that these compounds are banned and that remediation for their pres-
ence in the environment is needed. Many soils are contaminated with low to
moderate levels of DDT and its breakdown products, although the use of
this compound has been forbidden for decades (Thomas, Ou, & Al-Agely,
2008). These molecules are highly hydrophobic, with log KOW values
between 5.5 and 6.9. When these compounds reside in soils for decades, a
significant weathering effect can be observed (Lunney, Zeeb, & Reimer,
2004). Weathered DDTs strongly adsorb to soil particles, further enhanced
by alternate drying and wetting. Due to their hydrophobic and lipophilic
nature, DDTs naturally accumulate in adipose tissue and often get magnified
in the food chain. Several higher trophic level animals have been shown to
experience deleterious effects of DDT exposure, e.g., egg shell thinning in
birds and endocrine disruptors in mammals (Sharpe, 1995).
The most widespread herbicide contamination occurs with atrazine
(Pascal-Lorber & Laurent, 2011). Atrazine (2-chloro-4-(aminoethyl)-6-
(aminoisopropyl)-s-1,3,5-triazine) is a photosynthesis-inhibiting herbicide
and is used in agriculture for the control of annual grasses and broad-leaved
weeds, as well as in industrial sites and along railroads (Garmouna, Teil,
Blanchard, & Chevreuil, 1998). This caused widespread contamination of
surface and groundwater reservoirs. Atrazine is known to be an endocrine
disruptor, and significant toxicity has been noted in amphibians (Forson &
Storfer, 2006; Hayes et al., 2002).
Less is known about fungicide contamination, but the most important
contaminants are hexachlorobenzene (HCB) and pentachlorophenol.
HCB is a hydrophobic organic compound that is known for its
bioaccumulation and the analyte has been detected in air, soil, fish,
birds and even human milk (Qiu et al., 2004). Although HCB has not
been produced since the 1970s, it is still being released into the environ-
ment as a by-product of simazine and thus, overall contamination has
been increasing (Bailey, 2001).
3. BEHAVIOUR OF PESTICIDES IN THE ENVIRONMENT

The behaviour of pesticides in the environment is influenced by a
combination of natural processes. When in the environment, pesticides
interact with soils, water and organisms and the interactions are controlled
by a complex collection of biological, physical and chemical reactions
(Gavrilescu, 2005). Generally speaking, the processes that influence pesticide
contamination can be classified into three types: (1) transport processes,
which move the pesticide from the original point of introduction, (2) trans-
fer processes that control the pesticides movement through environmental
compartments such as water, sediments, the atmosphere and biota and (3)
transformation processes that change the structure/nature of a pesticide or
even completely degrade it to its constituent elements. All these processes
are in turn influenced by different soil and climatic factors, as well as the
characteristics of the pesticides themselves. The most important soil factors
are the following:
• Soil texture and the distribution of soil particles. Soils that have a fine
texture have a larger surface to volume ratio and a lower permeability.
Therefore, the water and pesticides tend to diffuse more slowly, giving
the pesticide a longer time for sorption to soil particles. Soils containing
larger particles will retain considerably less pesticide residues.
• Soil depth influences the amount of time the pesticides spend in contact
with soil particles before being washed out to deeper layers.
• Soil pH has an effect on the adsorption potential of soils and the rate of
the biological processes that can remove pesticide residues.
• Soil organic matter content can change the sorption potential towards
pesticide molecules as well as the number of biologically active microor-
ganisms (Fukushima & Tatsumi, 2001). Organic matter provides an
energy source for the microorganisms during the possible degradation
of pesticide residues and is a highly complex medium that can interact
significantly with organic and inorganic analytes.
• Soil slope is an external geological factor that can change the time that
water and pesticides have to infiltrate the soil. Steep areas have consider-
ably more runoff, giving pesticides less time to seep through.
The climate can also have an effect on the remediation of pesticides in
the environment. A well-studied example is weathering of pesticides.
Weathering is the process where pesticides molecules become more firmly
attached to soil particles through the process of becoming wet by rain or
dew and drying again (White et al., 2005). Weathered pesticides are known
to be accumulated to a lesser extent easily than their recently applied
equivalent.
In addition to soil and climatic factors, the chemical characteristics of the
pesticide itself will greatly influence the fate of these compounds in the envi-
ronment. Important characteristics include water solubility, tendency to
adsorb to the soil particles and the half-life period or persistency in the
environment.
The contaminant’s availability is determined by combining the above
mentioned soil and pesticide characteristics. Contaminant availability refers
to the rate and the extent that the pesticide molecules will be released to
and remain in the environment and greatly influences the possible remedi-
ation potential of a certain technology.
3.1 Transport of Pesticides

Transport of pesticides is the movement of the compounds from their point
of introduction to the environment (Gavrilescu, 2005). Most pesticides are
applied by spraying, causing a partial evaporation of the analytes into the air.
Second, pesticides can evaporate from the soil and from plant surfaces.
When the pesticides interact with soil, the fraction of the analyte that
does not adsorb to soil particles can leach through the matrix into surface
waters and cause contamination there.
3.2 Transfer of Pesticides

In addition to transport through the environment, pesticides can also be
transferred between the different individual compartments: soil, water,
atmosphere and biota (Gavrilescu, 2005).
Originally, most pesticides are applied in solid or liquid state to soils and
plant surfaces, but volatilization can take place. Volatilization is a process
where solid and liquid pesticides are converted into the gas phase, with sub-
sequent transfer to the air (Frazar, 2000; Whitford et al., 1995). Once in the
air, the pesticides can be transported over long distances and contamination
can be spread throughout larger areas.
Precipitation events will partially convert the solid and liquid pesticides
into dissolved from. Part of this water will run off the soil, which can cause
pesticide contamination in the bodies of water where the runoff accumulates.
However, a significant part of the rain water will also enter the soil system at
distance from the site of application; in this case, leaching occurs. The amount
of leaching that takes place is highly dependent on both the pesticide prop-
erties and the geological conditions.
From soil, air or water, pesticides can also be transferred into plants,
microorganisms and animals. This capacity of plants and microorganisms
to accumulate pesticides is the foundation of the natural remediation
technologies that will be discussed in detail below.
3.3 Transformation
A third process to which pesticides are susceptible in the environment is
transformation (Gavrilescu, 2005). Pesticide transformation or degradation
is the oxidation of pesticide molecules. When a pesticide is introduced
into the environment, it is prone to different transformation pathways. First,
there is a chemical degradation, where the analytes react with organisms or en-
zymes in the environment and degradation occurs. Secondly, the molecules
can be degraded by exposure to light; photodegradation. Thirdly, microbial
degradation can occur in both bulk and rhizosphere soil. The microbial
degradation process is the basic process for bioremediation of pesticide-
contaminated soils and will be further explored below.
4. REMEDIATION OF PESTICIDES
Remediation strategies for soils and water contaminated with
pesticides can be physical, chemical, biological or a combination of some
or all of these approaches (Pascal-Lorber & Laurent, 2011). Traditionally,
pesticide contamination has been remediated using physico-chemical
technologies where soils are excavated and subsequently transported to
specialized landfills; the material may also be incinerated or stabilized on
site (McGuinness & Dowling, 2009). Although efficient, these technologies
have significant limitations. The excavation and transport of contaminated
soils is both labour-intensive and costly. Furthermore, when soils are treated
in this manner, ecosystem disruption is significant and recovery may take
years (Dijkgraaf & Vollebergh, 2004). Another limitation to these technol-

ogies is the area on which they can be applied. Since they are so costly and
intensive, they are only cost-effective for small areas of high contamination;
use on large-scale areas with moderate contamination is not feasible (Jin,
Wang, & Ran, 2006).
Viable alternatives to these traditional remediation technologies are bio-
and phytoremediation. These approaches are innovative technologies that
show promise for alleviating pesticide contamination in both soils and water
(Hussain, Siddique, Arshad, & Saleem, 2009). An overview of the main con-
cepts underlying bio- and phytoremediation follows below.
4.1 Bioremediation
Bioremediation is the partial or complete conversion of the contaminant of
interest to its elemental constituents by soil microorganisms (Megharaj,
Ramakrishnan, Venkateswarlu, Sethunathan, & Naidu, 2011). It is esti-
mated that 1 g of bulk soil contains more than 1 million bacterial cells of
5000e7000 different species and more than 10,000 fungal colonies (Dindal,
1990; Melling, 1993). These metabolic potential of the indigenous microbial
community can be used for the detoxification of pesticide residues in soil
(Karpouzas, Fotopoulou, Menkissoglu-Spiroudi, & Singh, 2005; Kumar &
Philip, 2006; Siddique, Okeke, Arshad, & Frankenberger, 2003).
The efficiency of bioremediation depends on the bioavailability of the
contaminant (related to analyte adsorption to solid materials and to surface
complexation) and on the degradation potential of the microorganisms
(Chaudry et al., 2005). Here, we review the relevant bioremediation and
in these articles, many microorganisms showing pesticide-degrading capac-
ities are described as shown in Table 1 (bacteria) and Table 2 (fungi).
When considering the bacteria, a dominant presence of the Proteobac-
teria is clearly evident. Of the 35 bacterial species that were recently noted to
have the ability to remediate pesticide contamination, 21 belong to the
Proteobacteria (6 Alphaproteobacteria, 4 Betaproteobacteria and 11
Gammaproteobacteria). When focussing on the species level, Pseudomonas
sp. is the most abundant group present in literature. This species was
mentioned in 16 publications and was shown to facilitate the remediation
of 25 different pesticide residues and metabolites. The Pseudomonas species
that were described were isolated from bulk soils, as well as the rhizosphere
and from plants themselves, proving that this species is both omnipresent and
adaptable.
Table 1 Overview of the Bacterial Genera Proven to Show Pesticide Degrading Capacities and Their Source of Isolation
Nature-Based Remediation of Pesticides

Bacterial Genus Pesticide Isolated From References
Aeromonas sp. Chlorpyrifos, fenpropathrin Phragmites communis Chen et al. (2012)

Carbaryl Bulk soil Hamada, Matar, and Bashir (2015)
Agrobacterium sp. Atrazine, metalachlor Rhizosphere Andropogon Zhao, Arthur, Moorman, and Coats
gerardii (2005)
Anabaena sp. Butachlor Bulk soil Agrawal, Sen, Yadav, Rai, and Rai
(2015)
Arthrobacter sp. Cyhalothrin, cypermethrin, DDT, Rhizosphere Nicotiana Wang, Wang, Li, and Gao (2015)
HCH tabacum
Azospirillum sp. Ethion Sludge Foster, Kwan, and Vancov (2004)
Chlorpyrifos, cyanophos Bulk soil Romeh (2014)
Bacillus sp. Acibenzolar-S-methyl, Bulk soil Myresiotis et al. (2012)
metribuzin, napropamide,
propamocarb hydrochloride,
thiamethoxam
Bifenthrin, chlorpyrifos Phragmites communis Chen et al. (2012)
Carbaryl Bulk soil Hamada et al. (2015)
Chlorpyrifos Bulk soil Pailan, Gupta, Apte, Krishnamurthi,
and Saha (2015)
Lolium multiflorum Ahmad et al. (2012)
Cypermethrin Bulk soil Pankaj et al. (2016)
Methyl parathion Bulk soil Sreenivasulu and Aparna (2001)
Monocrotophos Bulk soil Acharya, Shilpkar, Shah, and
Chellapandi (2015)
Trifluralin Bulk soil Bellinaso, Greer, Peralba, Henriques,
and Gaylarde (2003)
285
(Continued)
Table 1 Overview of the Bacterial Genera Proven to Show Pesticide Degrading Capacities and Their Source of Isolationdcont'd
286
Bordetella sp. HCHs Bulk soil Kengara et al. (2010)
Brevibacterium sp. Phorate Bulk soil Jariyal, Gupta, Mandal, and Jindal
(2015)
Chryseobacterium sp. DDT Bulk soil Qu, Xu, Ai, Liu, and Liu (2015)
Corynebacterium sp. Carbaryl Bulk soil Hamada et al. (2015)
Cupriavidus sp. Azoxystrobin Bulk soil Howell, Semple, and Bending (2014)
Enterobacter sp. Bifenthrin Phragmites communis Chen et al. (2012)
Chlorpyrifos Bulk soil Singh et al. (2006) and Awas, Sabit,
Abo-Aba, and Bayoumi (2011)
DDE Cucurbita pepo Eevers, Van Hamme, Bottos, Weyens,
and Vangronsveld (2015a, 2015b,
2015c)
Fenamiphos Bulk soil Singh et al. (2006)
Flavobacterium sp. Bifenthrin Phragmites communis Chen et al. (2012)
Herbaspirillum sp. Trifluralin Bulk soil Bellinaso et al. (2003)
Klebsiella sp. Bifenthrin, fenpropathrin, Nymphaea tetragona Chen et al. (2012)
Naphtalene
Chlorpyrifos Sludge Ghanem, Orfi, and Shamma (2007)
Fenpropathrin Spirodela polyrhiza Xu et al. (2015)
Trifluralin Bulk soil Bellinaso et al. (2003)
Lactobacillus sp. Chlorpyrifos Rice straw Wang et al. (2016)
Chlorpyrifos, coumaphos, Kimchi (food dish) Islam et al. (2010)
Nele Eevers et al.

diazonin, methyl parathion,
parathion
Lactococcus sp. Fenpropathrin Nymphaea tetragona Chen et al. (2012)
Mesorhizobium sp. Chlorpyrifos Lollium multiflorum Jabeen, Iqbal, Ahmad, Afzal, and
Firdous (2015)
Methylobacterium sp. DDE Cucurbita pepo Eevers et al. (2015a, 2015b, 2015c)
Microbacterium sp. Chlorpyrifos, fenpropathrin Phragmites communis Chen et al. (2012)
Morganella sp. Carbaryl Bulk soil Hamada et al. (2015)
Nocardia sp. Sulfentrazone Bulk soil Martinez et al. (2010)
Novosphingobium sp. 2,4-Dichlorophenoxyacetic acid Bulk soil Dai, Li, Zhao, and Xie (2015)
Paenibacillus sp. Chlorpyrifos Nymphaea tetragona Chen et al. (2012)
Chlorpyrifos, cyanophos Bulk soil Romeh (2014)
Fenpropathrin Najas marina Chen et al. (2012)
Paracoccus sp. Alachlor, Acetochlor, butachlor, Bulk soil Zhang et al. (2011)
metolachlor, propisochlor
Chlorpyrifos Sludge Xu, Li, Wang, Zhang, and Yan (2008)
Pseudomonas sp. Aldrin, dieldrin, heptachlor, Bulk soil Bandala, Andres-Octaviano, Pastrana,
heptachlor epoxide and Torres (2006)
Atrazine, metolachlor Rhizosphere Sorghastrum Zhao et al. (2005)
nutans
Bifenthrin Phragmites communis Chen et al. (2012)
Carbaryl Bulk soil Hamada et al. (2015)
Chlorpyrifos Bulk soil Gilani et al. (2016) and Awas et al.
(2011)
Chlorpyrifos, cypermethrin, Bulk soil Zuo et al. (2015)
fenitrothion, fenpropathrin,
methyl parathion, permethrin
Cyhalothrin, cypermethrin, Bulk soil Tang et al. (2015)
fenpropathrin, fenvalerate
2,4-Dichlorophenoxyacetic acid Populus trichocarpa x deltoides Germaine et al. (2006)
Dimethoate, malathion Bulk soil Al-Qurainy and Abdel-Megeed (2009)
Endosulfan Bulk soil Narkhede et al. (2015)
287
(Continued)
288
Table 1 Overview of the Bacterial Genera Proven to Show Pesticide Degrading Capacities and Their Source of Isolationdcont'd
Ethion Sludge Foster et al. (2004)
Fenpropathrin Spirodela polyrhiza Xu et al. (2015)
Glyphosate Bulk soil Al-Arfaj, Abdel-Megeed, Ali, and Al-
Shahrani (2013)
Phorate Bulk soil Jariyal, Gupta, Jindal, and Mandal
(2015)
Quinalphos Bulk soil Nair, Rebello, Rishad, Asok, and Jisha
(2015)
Pseudoxanthomonas Profenos Bulk soil Talwar and Ninnekar (2015)
sp.
Psychrobacter sp. Chlorpyrifos Bulk soil Khalid and Hashmi (2016)
Rhodanobacter sp. Azoxystrobin Bulk soil Howell et al. (2014)
Rhodococcus sp. HCHs Cytisus striatus Becerra-Castro et al. (2012)
Simazine Bulk soil Eker and Uyar (2016)
Serratia sp. Monocrotophos Bulk soil Abraham and Silambarasan (2015)
Quinalphos Bulk soil Nair et al. (2015)
Sphingomonas sp. Acetachlor, alachlor, butachlor Sludge Chen et al. (2015)
Nele Eevers et al.

DDE Cucurbita pepo Eevers et al. (2015a, 2015b, 2015c)
Diclofop-methyl Bulk soil Adkins (1999)
HCHs Bulk soil Becerra-Castro et al. (2012)
Stenotrophomonas sp. Chlorpyrifos, diazonin, methyl Sludge Deng et al. (2015)
parathion, parathion, phoxim,
profenofos, triazophos
DDT Bulk soil Zhu et al. (2012) and Pan et al. (2016)
Streptomyces sp. Atrazine Saccharum officinarum Mesquini, Sawaya, Lopez, Oliveira,
and Miyasaki (2015)
Chlordane, HCHs, methoxychlor Bulk soil Fuentes, Benimeli, Cuozzo, and
Amoroso (2010)
HCHs Bulk soil Alvarez, Benimeli, Saez, Giuliano, and
Amoroso (2015)
Variovorax sp. Linuron Bulk soil Horemans, Vandermaesen,
Vanhaecke, Smolders, and Springael
(2013)
289
290
Table 2 Overview of the Fungal Genera Known to Degrade Pesticides and Their Source of Isolation
Fungal Genus Pesticide Isolated From References
Aspergillus sp. Pentachlorophenol Didemnun ligulum Vacondio et al. (2015)

Bjerkandera sp. Azinphos methyl, phosmet, Wood Jauregui et al. (2003)
terbufos, tribufos
Cladosporium sp. Pentachlorophenol Didemnun ligulum Vacondio et al. (2015)
Cordyceps sp. Dieldrin Bulk soil Xiao and Kondo (2013)
Coriolus sp. Aldicarb, alachlor, atrazine Bulk soil Hai et al. (2012)
Fusarium sp. Pentachlorophenol Didemnun ligulum Vacondio et al. (2015)
Glomus sp. Phoxim Medicago sativa Wang et al. (2011)
Lentinula sp. Difenoconazole, pendimethalin, Bulk soil Pinto et al. (2012)
terbuthylazine
Penicillium sp. Sulfentrazone Bulk soil Martinez et al. (2010)
Phanerochaete sp. Azinphos methyl, DDT, phosmet, Wood Jauregui et al. (2003) and
terbufos, tribufos Thomas and Gohil (2011)
Pleurotus sp. Azinphos methyl, phosmet, terbufos, Wood Jauregui et al. (2003)
tribufos
Trichoderma sp. Pentachlorophenol Didemnun ligulum Vacondio et al. (2015)
Verticillium sp. Chlorpyrifos Brassica chinensis Fang et al. (2008)
Nele Eevers et al.

Significantly less has been published on the possible remediation of

pesticides using fungal species (Table 2). A total of 13 fungal species were
mentioned, of which seven belonged to the Ascomycota, five to the
Basidiomycota and one to the Glomeromycota. Many of these species
were isolated from decaying wood (white rot fungi) and bulk soils. The large
difference in the number of studies focussing on bacteria and fungi could be
the result of (1) fungi showing less pesticide-degrading potential or (2) fungi
that are simply less studied in the context of natural remediation
technologies.
The pesticides described in this literature are quite broad and we review
the most common analytes here. Chlorpyrifos is an organophosphorus
pesticide that has been used in agriculture and can be very persistent in soils.
However, many bacterial and fungal strains have shown potential for
degrading the compound (Gilani et al., 2016). Serratia sp. was shown to
completely degrade 100 mg/L of chlorpyrifos in as little as 18 h (Xu, Li,
Zheng, & Peng, 2007); Stenotrophomonas sp. displayed similar results in
28 h (Yang, Liu, Guo, & Qiao, 2006). Gilani et al. (2016) identified 14
different Pseudomonas strains isolated from soil that degraded chlorpyrifos.
Many soils, such as those from former pesticide production facilities, are
contaminated with mixtures of pollutants (Moklyachuk, Gorodiska,
Slobodenyuk, & Petryshyna, 2010; Nurzhanova et al., 2010). To remediate
these contaminations scenarios, researchers may have to use consortia of
different bacterial strains such as that employed by Fan and Song
(2014) for the degradation of atrazine and deisopropylatrazine. Alternatively,
one may apply bacterial strains that can degrade several pesticides, such as the
Bacillus strain used by Myresiotis, Vryzas, and Papadopoulou-Mourkidou
(2012) to remediate soil contaminated with acidobenzolar-S-methyl,
metribuzin, napropamide, propamocarb hydrochloride and thiamethoxam.
The efficiency of bioremediation processes depends largely on the local
environmental conditions, such as soil moisture, redox status, temperature,
pH and organic matter content (Singh, Walker, & Wright, 2006). The
soil moisture is determined by the soil water content and influences not
only the availability of water to soil microorganisms, but also the redox
conditions that can impact possible biochemical degradation reactions
(Schroll et al., 2006). Furthermore, high soil water content can create anoxic
conditions, which can alter the microbial activity (Phillips, Lee, Trevors, &
Seech, 2006). For example, anoxic conditions can enhance the degradation
of pesticides, as demonstrated by Phillips et al. (2006) showed for HCH and
Wu, Chen, Li, and Li (2014) for DDT .
Temperature and pH are also two major parameters that influence biodeg-
radation processes in soils (Arshad, Hussain, & Saleem, 2007). Like most
other enzymes, those molecules shown to be active in the degradation of
pesticides are known to be temperature dependent (Alberty, 2006, pp.
43e70). Temperatures ranging between 15 C and 40 C were shown to
be optimal conditions for the degradation of pesticides such as fenitrothion
(Hong, Zhang, Hong, & Li, 2007) and fenamiphos (Singh et al., 2006).
Enzymatic activity is also dependent on pH. Most bacteria function
optimally in a pH range between 6.5 and 7.5; conditions that approximate
intracellular pH (Hussain et al., 2009). In addition to affecting enzyme
activity, soil pH can also influence abiotic adsorption and desorption
processes of pesticides in soils. Lowering soil pH can increase pesticide
desorption from soil particles (Ferrell, Witt, & Vencill, 2003), which
enhances the bioavailability and bioremediation efficiency.
Another factor influencing the adsorption and desorption of pesticide
molecules to soil particles is the soil organic matter content. When soils contain
higher levels of organic matter, two competing effects are possible. On the
one hand, pesticides may bind more strongly to organic soil particles and
thus become less available for biodegradation. Alternatively, in high organic
matter soils more nutrients may be available for the soil microorganisms,
which can then stimulate microbial growth and an increase in pesticide
degradation (Briceno, Palma, & Duran, 2007). Zhang, Sheng, Feng, and
Miller (2005) made a comparison between the inhibition by adsorption
and the stimulation by nutrient presence in benzonitrile-contaminated soils
and concluded that the contaminant degradation increased with the addition
of wheat-derived char. However, the more hydrophobic compounds with a
higher log KOW were likely to become more strongly associated with the
solid phase of the organic matter (Aronstein, Calvillo, & Alexander,
1991). Many soil microorganisms produce organic acids, which may cause
the desorption of pesticide molecules from organic matter particles and
thus increase biodegradation potential (Chen & Zhu, 2005; Mata-Sandoval,
Karns, & Torrents, 2000).
Since microorganisms are capable of excreting a large number of
surfactants and enzymes, it is possible that the pesticides are also degraded
extracellularly by these released enzymes (Hussain et al., 2009). This strategy
could be exploited and serve as a rapid method for the remediation of pesti-
cide-contaminated soils since no energy-demanding processes to transport
the analytes into biota are needed. In fact, some have reported the successful
bioremediation experiments using free enzymes (Seffernick et al., 2002;
Sutherland et al., 2004; Wackett, 2004; Wackett, Sadowsky, Martinez, &

Shapir, 2002). However, their application under field circumstances and
optimization for site-specific environmental factors has yet to be deployed
on a large scale.
4.2 Plant-Associated Remediation

Phytoremediation is based on the same principles as bioremediation,
although in this case pesticide degradation takes place in the plant or its
rhizosphere. Similar to bioremediation, phytoremediation is also to be
considered to be an innovative, cost-effective and ecologically beneficial
technology (Hussain et al., 2009). Phytoremediation is a collection of
processes, including phytotransformation, phytodegradation, phytovolatili-
zation and rhizoremediation (Fig. 1). For the first three processes, uptake
of the contaminant into the plant tissues is necessary; rhizoremediation takes
place at the soil-root interface or rhizosphere.
All of the above-mentioned phytoremediation processes can be
influenced by plant-associated microorganisms. Both rhizospheric and
endophytic microorganisms can play a role in the remediation through
pesticide-degrading and plant growthepromoting capacities (Glick, 2003,
2010; Weyens, Monchy, Vangronsveld, Taghavi, & Van Der Lelie, 2010).
4.2.1 Rhizoremediation
The degradation of pesticides is often greater in rhizosphere soil than it is in
bulk soil. This can be explained by a phenomenon known as the rhizosphere
effect (Hussain et al., 2009). The rhizosphere is the soil volume directly
around the roots and is heavily influenced by the activities of the plant.
This activity makes the rhizosphere a more complex environment than
bulk soil, supporting large numbers of metabolically active microbial com-
munities. These numbers can be 10e100 times larger than the number of
microorganisms in unvegetated or bulk soil (Lynch, 1990; Pascal-Lorber
& Laurent, 2011; Weyens et al., 2009), reaching up to 1012 cells per gram
of soil (Whipps, 1990). Notably, the presence of plants with a large
rhizospheric community can even increase the number of microbial cells
in surrounding bulk soils (Leigh et al., 2006; Siciliano, Germida, Banks, &
Greer, 2003). The presence of microbial communities in the soil can be
beneficial to the plant by producing protective or beneficial compounds
such as 1-aminocyclopropane-1-carboxylate (ACC) deaminase (Glick,
2003). ACC is the precursor molecule for ethylene, which is a stress
hormone that plants often produce in contaminated soils. When
Figure 1 Overview of processes included in bio- and phytoremediation.

ACC-deaminase degrades ACC, ethylene levels are lowered and the plants
experience less stress from contaminant exposure. All of these mechanisms
can decrease plant phytotoxicity, increase plant growth and increase phytor-
emediation potential. Furthermore, microorganisms are capable facilitating
the uptake of essential nutrients by plants through the production of organic
acids (Lunney, Rutter, & Zeeb, 2010); the microbiota may also protect
plants against pathogens by competing for a position in the plant micro-
biome and degrade contaminants before they negatively affect the plant
(Gerhardt, Huang, Glick, & Greenberg, 2009).
Rhizodegradation is a process that occurs naturally, but that can be
enhanced by planting the most appropriate plant species, or by adding
pesticide-degrading bacteria through inoculation. Plant root systems can
excrete enzymes that degrade pesticides in the rhizosphere (Gerhardt
et al., 2009), but they also release photosynthetic products that can serve
as nutrients for rhizospheric bacteria. Several researchers have isolated rhizo-
spheric bacteria that show pesticide-degrading capacities (Table 1). If these
pesticide-degrading bacteria are enriched by means of inoculation, the
process is considered to be bacteria-enhanced rhizodegradation. Kidd,
Prieto-Fernandez, Monterroso, and Acea (2008) showed a higher dissipation
of HCHs in the rhizosphere when Cytisus striatus and Holcus lanatus were
inoculated with HCH-degrading bacteria. Ahmad et al. (2012) reported a
50% increase in chlorpyrifos degradation in the Lolium multiflorum rhizo-
sphere when the plant roots were inoculated with Bacillus pumilus C2A1.
Wang, Tong, Shi, Xu, and He (2011) described the successful
degradation of phoxim when carrot (Daucus carota) and green onion (Allium
fistulosum) were inoculated with the arbuscular mycorrhizal fungi Glomus
intraradices and Glomus mosseae; notably, contaminant degradation was
negligible in noninoculated plants. The fungus Trichoderma harzianum was
isolated from a marine plant Didemnum ligulum and had the capacity to
degrade 50 mg/L phoxim in liquid medium in 7 days (Vacondio et al.,
2015). Jauregui, Valderrama, Albores, and Vazquez-Duhalt (2003) conduct-
ed a large experiment on pesticide degradation by fungi. These researchers
tested 17 white rot fungi; 16 were able to degrade the pesticides parathion,
terbufos, azinphos-methyl, phosmet and tribufos after a four-day growth
period.
Similar to bioremediation, rhizoremediation processes are also heavily
influenced by plant, soil and pesticide characteristics. Factors such as temper-
ature, pH and soil organic matter content will influence pesticide bioavail-
ability, as well as the bacterial and enzymatic degradation potential in the
rhizosphere. However, the presence of the root system can moderate some
of these effects and in general, the degradation potential is higher in
comparison to bulk soil (Hussain et al., 2009).
The rhizosphere can also play another role in phytoremediation
processes: rhizostabilization. As explained earlier, pesticides can move
through the soil as runoff from agricultural fields and subsequently contam-
inate surface waters. However, root systems and their associated microbial
communities may intercept the pesticide molecules and thus stabilize
them in the soil (Pascal-Lorber & Laurent, 2011).
4.2.2 Phytoremediation
In contrast to rhizoremediation, the accumulation of the pesticide is a
prerequisite for phytotransformation, phytodegradation and phytovolitaliza-
tion. Many plants have been reported to efficiently accumulate pesticides; an
overview is given in Table 3. Cucurbita pepo and Zea mays are the plant
species most frequently used in research paper addressing the phytoremedia-
tion of pesticides (11 and 7, respectively). These plants are often considered
for phytoremediation because of their high number of cultivars as a result of
their important role in agriculture and gardening, as well as their good
accumulation potential of a wide range of organic contaminants (White,
2010; White et al., 2005). Ricinus communis is the plant shown to accumulate
the greatest number of different contaminants. Rissato et al. (2015) and
Huang et al. (2011) described the uptake of 11 different pesticides with a
wide variety of characteristics.
The plant’s uptake efficiency of these compounds is determined by many
soil and plant characteristics (Hussain et al., 2009). The soil factors that can
influence the pesticide availability to microorganisms and plants were dis-
cussed earlier in this review. In addition to soil moisture, temperature, pH
and organic matter content, the time that the pesticide resides in soils can
also influence the pesticide uptake; time-dependent decreases in availability
are often described during weathering or ageing of the residues (Lunney
et al., 2010, 2004).
The potential of plants to take up pesticide residues varies greatly
between plant species (Dosnon-Olette, Trotel-Aziz, Couderchet, &
Eullaffroy, 2010; Gent et al., 2007; Lunney et al., 2004; Mitton,
Miglioranza, Gonzalez, Shimabukuro, & Monserrat, 2014; Moklyachuk
et al., 2010; Moore & Locke, 2012; Mukherjee & Kumar, 2012;
Nurzhanova et al., 2010; Romeh, 2015; Sun, Xu, Yang, Liu, & Dai,
2004; Wang, Zhang, Li, & Xiao, 2012; White et al., 2005) and even
Table 3 Overview of the Plant Species That Have Shown Pesticide

Phytoremediation Potential
Plant Species Pesticide
Achillea millefolium DDT (Moklyachuk, Petryshyna, Slobodenyuk, &

Zatsarinna, 2012)
Acorus calamus Atrazine (Wang et al., 2012)
Allium fistulosum Phoxim (Wang et al., 2011)
Amaranthus caudate Dimethoate, malathion (Al-Qurainy & Abdel-Megeed,
2009)
Glyphosate (Al-Arfaj et al., 2013)
Andropogon gerardii Atrazine, metolachlor, pendimethalin (Zhao et al., 2005
and Henderson, Belden, Zhao, & Coats, 2006)
Arachis hypogaea DDE (White et al., 2005)
Avena sativa HCHs (Calvelo Pereira, Camps-Arbestain, Rodríguez-
Garrido, Macias, & Monterroso, 2006)
Brassica campestris Endosulfan (Mukherjee & Kumar, 2012)
Brassica juncea DDE (White et al., 2005)
Brassica napus DDE (White et al., 2005)
Cabomba aquatica Copper sulphate, dimethomorph, flazasulfuron (Olette,
Couderchet, Biagianti, & Eullaffroy, 2008)
Cajanus cajan DDE (White et al., 2005)
Canna x hybrida Simazine (Knuteson, Whitwell, & Klaine, 2002)
Chenopodium spp. HCHs (Calvelo Pereira et al., 2006)
Cirsium arvense Chlordane (Mattina et al., 2003)
Cucumis sativus Chlordane (Gent et al., 2007)
DDE (Gent et al., 2007)
Endosulfan sulphate (Somtrakoon, Kruatrachue, & Lee,
2014)
Cucurbita pepo Chlordane (Mattina et al., 2003)
DDD, DDE, DDT (Bogdevich & Cadocinicov, 2010;
Chhikara et al., 2010; Gent et al., 2007; Lunney et al.,
2010; Lunney et al., 2004; Matsuo, Yamazaki, Gion,
Eun, & Inui, 2011; Moklyachuk et al., 2010; Whitfield
Aslund & Zeeb, 2010)
Dieldrin, endrin (Matsumoto, Kawanaka, Yun, &
Oyaizu, 2009; Otani et al., 2007)
HCHs (Bogdevich & Cadocinicov, 2010; Moklyachuk
et al., 2010)
Cytisus striatus HCHs (Becerra-Castro et al., 2012; Calvelo Pereira et al.,
2006; Kidd et al., 2008)
Daucus carota DDD, DDE, DDT (Bogdevich & Cadocinicov, 2010;
Moklyachuk et al., 2012)
HCHs (Bogdevich & Cadocinicov, 2010)
Phoxim (Wang et al., 2011)
(Continued)

Phytoremediation Potentialdcont'd
Digitaria sp. Atrazine, metolachlor, trifluralin (Anderson, Kruger, &
Coats, 1994)
Eichhornia crassipes Aldrin, chlorpyrifos, DDT, dieldrin, endosulfan,
malathion, methyl parathion (Mercado-Borrayo,
Heydrich, Perez, Quiroz, & Hill, 2015)
Ethion (Xia & Ma, 2006)
Elodea canadensis DDT (Gao, Garrison, Hoehamer, Mazur, & Wolfe,
2000)
Copper sulphate, dimethomorph, flazasulfuron (Olette
et al., 2008)
Erigeron canadensis DDD, DDE, DDT (Moklyachuk et al., 2012)
Festuca arundinacea DDT (Lunney et al., 2004)
Glycine max Azoxystrobin (Romeh, 2015)
DDD, DDE, DDT (Moklyachuk et al., 2010; Mitton
et al., 2014)
HCHs (Moklyachuk et al., 2010)
Halimione portulacoides DDD, DDE, DDT (Carvalho, Rodrigues, Evangelista,
Basto, & Vasconcelos, 2011)
Helianthus annus Azoxystrobin (Romeh, 2015)
DDD, DDE, DDT (Mitton et al., 2014)
Holcus lanatus HCHs (Kidd et al., 2008)
Hordeum vulgare DDD, DDE, DDT, HCHs (Moklyachuk et al., 2010)
Dodemorph, tridemorph (Chamberlain, Patel, &
Bromilow, 1998)
Iris Pseudacorus Atrazine (Wang et al., 2012)
Chlorpyrifos (Wang, Yang, Cui, Xiao, & Xiaoe, 2013)
Jathropa curcas HCHs (Abhilash, Singh, Srivastava, Schaeffer, & Singh,
2013)
Juncus effusus Chlorpyrifos (Lytle & Lytle, 2002)
Gamma-cyhalothrin (Bouldin et al., 2006)
Atrazine (Bouldin et al., 2006; Lytle & Lytle, 2002)
Juncus maritimus DDD, DDE, DDT (Carvalho et al., 2011)
Kanthium strumarium DDD, DDE, DDT (Moklyachuk et al., 2012)
Kochia sp. Atrazine (Anderson et al., 1994; Kruger et al., 1997)
Metolachlor, trifluralin (Anderson et al., 1994)
Lactuca sativa Chlordane (Mattina et al., 2003)
Dimethoate, malathion (Al-Qurainy & Abdel-Megeed,
2009)
Leersia oryzoides Atrazine, diazonin, permethrin (Moore & Locke, 2012)
Lemna minor Copper sulphate, dimethomorph, flazasulfuron (Olette
et al., 2008)

Atrazine, clofibric acid, 2,4-dichlorophenoxyacetic acid,
picloram (Reinhold, Vishwanathan, Park, Oh, &
Saunders, 2010)
Glyphosate, isoproturon (Dosnon-Olette, Couderchet,
Oturan, Oturan, & Eullaffroy, 2011)
Lemna punctate Atrazine, clofibric acid, 2,4-dichlorophenoxyacetic acid,
picloram (Reinhold et al., 2010)
Lolium multiflorum Atrazine (Merini, Bobillo, Cuadrado, Corach, &
Giulietti, 2009)
Chlorpyrifos (Ahmad et al., 2012; Jabeen et al., 2015)
DDE (White et al., 2005)
DDT (Lunney et al., 2004)
Terbuthylazine (Mimmo, Bartucca, Del Buono, &
Cesco, 2015)
Lolium perenne 2,4-Dichlorophenoxyacetic acid (Shaw & Burns, 2004)
Pentachlorophenol (He, Xu, Tang, & Wu, 2005)
Ludwigia peploides Atrazine, gamma-cyhalothrin (Bouldin et al., 2006)
Lupinus albus Chlordane (Mattina et al., 2003)
DDE (White et al., 2005)
Lupinus angustifolius Atrazine, fenamiphos, isoproturon, simazine (Garcinu~ no,
Fernandez-Hernando, & Camara, 2003)
Carbaryl, linuron, permethrin (Garcinu~ no et al., 2003;
Garcinu~ no, Fernandez-Hernando, & Camara, 2006)
Lycopersicon esculentum Chlordane (Mattina et al., 2003)
Lythrum salicaria Atrazine (Wang et al., 2012)
Medicago sativa DDD, DDE, DDT (Lunney et al., 2004; Mitton et al.,
2014)
Napropamide (Cui & Yang, 2011)
Myriophyllum aquaticum Atrazine, cycloxidim, tertbutryn, trifularin (Turgut,
2005)
DDT (Gao et al., 2000)
Simazine (Knuteson et al., 2002)
Najas marina Bifenthrin, chlorpyrifos, fenpropathrin, naphtalene
(Chen et al., 2012)
Nasturtium officinale Dimethoate, malathion (Al-Qurainy & Abdel-Megeed,
2009)
Nicotiana tabacum HCHs (Singh, Sherkhane, Kale, & Eapen, 2011)
Sulfentrazone (Ferrell et al., 2003)
Nymphaea tetragona Bifenthrin, chlorpyrifos, fenpropathrin, naphtalene
(Chen et al., 2012)
Oenotheria biennis DDD, DDE, DDT (Moklyachuk et al., 2012)
(Continued)

Orychophragmus DDD, DDE, DDT, HCHs (Sun et al., 2015)
violaceus
Oryza sativa DDT (Chu, Wong, & Zhang, 2006)
Panicum virgatum Atrazine, metolachlor, pendimethalin (Zhao et al., 2005;
Henderson et al., 2006)
Phaseolus vulgaris DDD, DDE, DDT, HCHs (Moklyachuk et al., 2010)
Dimethoate, malathion (Al-Qurainy & Abdel-Megeed,
2009)
Phragmites australis DDT (Chu et al., 2006)
Hexachlorbenzene (Zhou et al., 2013)
Phragmites communis Bifenthrin, chlorpyrifos, fenpropathrin, naphtalene
(Chen et al., 2012)
Pisum sativum 2,4-Dichlorophenoxyacetic acid (Germaine et al., 2006)
Plantago lagopus DDD, DDE, DDT (Moklyachuk et al., 2012)
Plantago major Azoxystrobin (Romeh, 2015)
Chlorpyrifos (Romeh & Hendawi, 2013)
Cyanophos (Romeh, 2014)
Polygonum sp. Atrazine, metolachlor, trifluralin (Anderson et al., 1994)
Populus deltoides x nigra Atrazine (Burken & Schnoor, 1997)
Potamogeton crispus Bifenthrin, chlorpyrifos, fenpropathrin, naphtalene
(Chen et al., 2012)
Potentilla argentae DDD, DDE, DDT (Moklyachuk et al., 2012)
Raphanus sativus DDT, HCHs (Mikes, Cupr, Trapp, & Klanova, 2009)
Ricinus communis Aldrin, chlordane, chlorpyrifos, DDE, diclofop methyl,
dieldrin, endrin, HCHs, heptachlor, methoxychlor
(Rissato et al., 2015)
DDT (Huang et al., 2011; Rissato et al., 2015)
Salix alba Metalaxyl, trifluralin (Warsaw et al., 2012)
Salix humboldtiana DDD, DDE, DDT (Mitton et al., 2012)
Sambucus nigra Metalaxyl, trifluralin (Warsaw et al., 2012)
Scenedesmus obliquus Isoproturon, dimethomorph, pyrimethanil (Dosnon-
Olette et al., 2010)
Scenedesmus quadricauda Isoproturon, dimethomorph, pyrimethanil (Dosnon-
Olette et al., 2010)
Schoenoplectus Aldrin, chlordane, DDD, DDE, DDT, dieldrin,
californicus endosulfan, HCHs, heptachlor, heptachlor epoxide
(Miglioranza, de Moreno, & Moreno, 2004)
Scirpus maritimus DDD, DDE, DDT (Carvalho et al., 2011)
Sedum alfredii DDD, DDE, DDT (Zhu et al., 2012)
Sesamum indicum HCHs (Abhilash & Singh, 2010)
Solanum lycopersicum DDD, DDE, DDT (Mitton et al., 2014)

Solanum nigrum HCHs (Calvelo Pereira et al., 2006)
Sorghastrum nutans Atrazine, metolachlor, pendimethalin (Henderson et al.,
2006; Zhao et al., 2005)
Sorghum bicolor DDD, DDE, DDT, HCHs (Bogdevich & Cadocinicov,
2010)
Sparganium americanum Atrazine, diazonin, permethrin (Moore & Locke, 2012)
Spinacia oleracea Chlordane (Mattina et al., 2003)
HCHs (Dubey, Tripathi, Singh, & Abhilash, 2014)
Spirodela polyrhiza Fenpropathrin (Xu et al., 2015)
Taraxacum officinalis DDD, DDE, DDT (Moklyachuk et al., 2012)
Trifolium incarnatum DDE (White et al., 2005)
Trifolium pretense 2,4-Dichlorophenoxyacetic acid (Shaw & Burns, 2004)
Triticum vulgare Butachlor (Yu et al., 2003)
DDD, DDE, DDT, HCHs (Moklyachuk et al., 2010)
Typha latifolia Atrazine, diazonin, permethrin (Moore & Locke, 2012)
Hexachlorobenzene (Zhou et al., 2013)
Methyl parathion (Amaya-Chavez, Martinez-Tabche,
Lopez-Lopez, & Galar-Martinez, 2006)
Vicia villosa DDE (White et al., 2005)
Vigna radiate Aldicarb (Sun et al., 2004)
Vigna sinensis Endosulfan sulphate (Somtrakoon et al., 2014)
Vigna unguiculata Aldicarb (Sun et al., 2004)
Withania somnifera HCHs (Abhilash & Nandita, 2010)
Zea mays Aldicarb (Sun et al., 2004)
DDD, DDE, DDT (Bogdevich & Cadocinicov, 2010)
Endosulfan (Mukherjee & Kumar, 2012)
Endosulfan sulphate (Somtrakoon et al., 2014)
HCHs (Alvarez et al., 2015; Bogdevich & Cadocinicov,
2010)
Napthalene (Sun et al., 2004)
between different subspecies (Otani, Seike, & Sakata, 2007; White, 2010).
To maximize the phytoremediation potential in a contaminated field, the
optimum combination of soil, plant and possibly endophytes has to be
established. Bouldin, Farris, Moore, Smith, and Cooper (2006) tested two
different plants (Juncus effusus and Ludwigia peploides) for their uptake
potential of two different pesticides (atrazine and lambda-cyhalothrin) and
noticed a higher uptake of atrazine in J. effuses, while L. peploides accumu-
lated more lambda-cyhalothrin. Atrazine was efficiently translocated to
the shoots of J. effuses, but L. peploides showed a 98.2% retention of the

analyte in the roots. The differences in uptake and translocation efficiency
of certain plants towards pesticides depends on pesticide and plant character-
istics. The log KOW or octanolewater partitioning coefficient greatly influ-
ences the bioavailability and translocation of pesticides in plants (Bromilow
& Chamberlain, 1995). Turgut (2005) investigated the uptake of trifluralin,
atrazine, terbutryn and cycloxidim in Myriophyllum aquaticum and observed
an increasing root concentration factor and submerged shoot concentration
factor with an increasing log KOW. The more polar (hydrophilic) a com-
pound is, the more difficulties the analyte has in crossing biological
membranes, which causes a lower uptake in comparison to lipophilic com-
pounds that easily cross biomembranes (Burken & Schnoor, 1997; Trapp,
2000, 2004).
In environments that are contaminated with several pollutants, signifi-
cant interactions between the contaminants may occur. Su, Zhu, Lin, and
Zhang (2005) documented that the interaction between Cd2þ and atrazine
reduced the individual toxicities of the contaminants to Oryza sativa seed-
lings and increased the uptake and translocation of atrazine into the plant
tissues.
Plants mainly accumulate pesticides through a soil-to-plant pathway,
although deposition from the air is also possible in the form of straight depo-
sition from the gas phase or contaminants that are sorbed to particles that are
subsequently deposited. Lee, Iannuci-Berger, Eitzer, White, and Mattina
(2003) studied the uptake of chlordane and reported different profiles of
chlordane in Cucurbita pepo when taken up through air or soil in parallel
studies.
In case of the soil-to-plant uptake, several plant characteristics such as
water uptake potential and root depth/structure can influence the accumu-
lation potential. Once pesticides are retained by plant root tissues, they can
be immobilized in the roots or translocated to the aerial plant parts where
the analytes can be stored, metabolized or volatilized (Fig. 1). Generally,
pesticide accumulation in roots is inefficient for remediation purposes;
although the soil contaminant concentration decreases, the root tissues
are not cost-effectively harvested. Aquatic plant-based remediation systems
are an obvious exception to this, where contaminant removal by plant
roots can be significant. Eichhornia crassipes (water hyacinth) can accumulate
the insecticide ethion more efficiently in its root system than in its shoot
system. Given that the roots make up over 50% of the plant mass and
that the total plant, including roots, can easily be harvested, this system
can be efficiently used for the phytoremediation of ethion-contaminated

waters (Xia & Ma, 2006).
After being accumulated by plant roots, pesticide molecules can be trans-
ported to the xylem vessels and translocated with the transpiration stream of
the plants. Many studies have been devoted to the transport of pesticides
within crop species, largely because of the plants’ high growth rates and
easy cultivability (Vila, Lorber-Pascal, & Laurent, 2007). Several crops
have been reported to have significant accumulation potential for a range
of pesticides (Table 3). White et al. (White, 2010; White et al., 2005; Chhi-
kara, Paulose, White, & Dhankher, 2010; Mattina, Lannucci-Berger,
Musante, & White, 2003) studied the uptake of DDE by different Cucurbita
pepo cultivars and reported shoot bioconcentration factors up to 23.7 for the
Raven cultivar. A fraction of the pesticide molecules that are translocated to
shoots can be adsorbed within vessel macromolecules, such as lignin or cel-
lulose. The use of trees, mainly poplar and willow, takes this mechanism into
account for phytoremediation as well as for phytopumping (Burken &
Schnoor, 1997; Mitton, Gonzalez, Pe~ na, & Miglioranza, 2012; Warsaw
et al., 2012). Phytoremediation using solely phytoaccumulation requires
harvest of the shoots after the uptake period. The shoot tissues can subse-
quently be burned or composted or otherwise disposed of by other means
(Pascal-Lorber & Laurent, 2011).
Pesticides that are volatile such as triflutrin can be transported to the
shoot system and subsequently be volatilized to the atmosphere (Fig. 1).
This process is often an unwanted side effect of the transport processes in
the plant, since the end result is merely a relocation of the contamination
from soil to air; the exception would be if the plant evaporation is captured
(Pascal-Lorber & Laurent, 2011).
Generally, the aim of efficient phytoremediation is not solely phytoac-
cumulation, but also the metabolic breakdown of the contaminant within
the plant tissues; this can be done with or without the aid of endophytic
bacteria. Plants often metabolize pesticides into more polar molecular
structures that can be stored in vacuoles or bound as residues in the cell
walls (Sandermann, 1994). In rape (Brassica rapa), atrazine residues were
shown to be incorporated into plant cell walls as hydroxyatrazine
(HO-A) (Dupont, Khan, & Bound, 1993). In roots, this process can lead
to stabilization of the pesticides and therefore limit redispersion of the con-
taminants after plant death; in this scenario, the degrading capacity of
white-rot fungi for lignin becomes very important (Jauregui et al., 2003;
Thomas & Gohil, 2011).
Few compounds can be completely degraded by only plant metabolic

pathways since most pesticides contain one or more aromatic cycles that
are inherently difficult to break. In this case, bacteria- or fungi-enhanced
phytoremediation may become important. As discussed earlier, many bacte-
ria and fungi show pesticide-degrading capacities in soils; the same is true for
endophytic microorganisms (Tables 1 and 2). Xu, Sun, Nie, and Wu
(2015) showed that Spirodela polyrhiza stimulated the growth of their endo-
phytes, which in their turn led to the degradation of fenpropathrin inside the
plant tissues. Chen, Tang, Mori, and Wu (2012) also concluded that the
efficient remediation of waters polluted by a mixture of chlorpyrifos,
fenpropathrin, naphthalene and bifenthrin was mainly due to the endo-
phytic bacteria residing in the aquatic plants, Phragmites communis, Potamoge-
ton crispus, Nymphaea tetragona and Najas marina, as opposed to the plants
themselves. Endophytic bacteria that show pesticide-degrading capacities
have an advantage over their nondegrading competitors in contaminated
environments and tend to dominate the community in those scenarios
(Megharaj et al., 2011).
Using endophytes in the phytoremediation process not only has an
advantage when it comes to pesticide degradation, but they also often possess
plant growthepromoting properties. This plant growth promotion is shown
through enhanced cycling of nutrients such as nitrogen and phosphate
(Ryan, Germaine, Franks, Ryan, & Dowling, 2008). Endophytes have
also been shown to have phosphate solubilisation abilities (Verma, Ladha,
& Tripathi, 2001; Wakelin, Warren, Harvey, & Ryder, 2004), indole-3-
acetic acid production (Lee et al., 2004), iron-binding siderophores produc-
tion (Costa & Loper, 1994) and ACC-deaminase production (Glick, 2003);
all will enhance plant growth.
Furthermore, the bacteria can also indirectly protect the plants. Symbi-
otic plant endophytes can prevent or lessen the deleterious effects of certain
pathogens, often by outcompeting these organisms within the microbial
community (Compant, Clement, & Sessitsch, 2010).
5. ADVANTAGES AND DISADVANTAGES OF NATURAL

REMEDIATION TECHNOLOGIES
Bio- and phytoremediation show many advantages, which make them
preferred over the classical physico-chemical remediation strategies. These
alternative remediation technologies are based on the natural abilities of
plants and microorganisms to utilize a wide range of organic compounds
and to metabolize these analytes into harmless products such as carbon diox-
ide and water. These technologies exploit the natural ability of an environ-
ment to restore itself. The greatest advantage is that these technologies
remediate the soils in situ without major disruptions in the environment.
No excavation and transportation is needed, which makes the technologies
inherently less costly and labour intensive, as well as more readily acceptable
by the public.
Phytoremediation has some additional advantages over bioremediation.
In the case of microbe-enhanced phytoremediation, the plants and microor-
ganisms provide protection and nutrients for each other. Therefore, it is
easier to stabilize the remediation system when compared to bulk soil, where
microorganisms have to compete to a greater extent to become established
in the community. In addition, the plants that are grown during phytoreme-
diation provide stabilization of the soil and could potentially be used for
green energy purposes.
Although the advantages of these technologies are obvious, some
disadvantages do also exist. First, not all contaminants are susceptible to
biodegradation. The contaminants can also be toxic to plants and microor-
ganisms that may not possess the required degradation pathways. Secondly, if
the parent compound is only partially degraded, products might appear that
are more toxic and persistent than the original contaminant. And even
though bio- and phytoremediation require less resources in the field than
the classical remediation strategies, greater effort is needed to address the
site-specific requirements of each contamination, plant and/or microorgan-
isms scenario. Also, if degradation does not occur in the plants, the contam-
inant might be released into the environment again through
evapotranspiration or through decaying tissues associated with natural
senescence.
Lastly, the period that is needed for efficient decontamination of the soil
has to be taken in consideration. As is the case when considering the reme-
diation strategy, the treatment is also heavily dependent on the specific cir-
cumstances. The traditional thinking here is that bio and phytoremediation
approaches are slower (Gerhardt et al., 2009), although some studies have
shown otherwise. Compernolle et al. (2012) investigated a case study where
a BTEX plume was remediated using poplar trees. In this study, the cost-
effectiveness of phytoremediation is compared to that of classical remedia-
tion strategies such as pump-and-treat. These researchers concluded that
both phytoremediation and pump-and-treat reached the remediation goal
within 1 year of treatment, with phytoremediation being of lower cost.
Therefore, though depending on the situation, natural remediation technol-

ogies can be the cost-effective approach.
6. CONCLUSION, FUTURE PERSPECTIVES AND

CHALLENGES
The contamination of soil with pesticides is a major concern to the
environment and public health. Although bioremediation and phytoreme-
diation are efficient technologies that have significant potential, physico-
chemical remediation strategies are still being applied more frequently. Soils
and plants host a wide range of microbial communities with many metabolic
pathways that can be applied for the efficient degradation of pesticide
residues in soil and water. Recent progress in both plant biotechnology
and microbiology, such as next generation sequencing to identify and utilize
total microbial communities, have made these technologies more and more
efficient. The findings that are discussed in this review show that bio- and
phytoremediation have been successfully applied in several field trials and
that these technologies should see greater use in the remediation of pesti-
cide-contaminated field sites.
To expand the scale and efficiency of these technologies, greater focus is
needed on unravelling the elucidating mechanisms of bio-, rhizo- and
phytoremediation in the relevant biota. New technologies such as next
generation sequencing might be useful in this regard; by investigating the
composition of the total microbial community that is present in soils,
rhizospheres and plants, an efficient method to introduce new microorgan-
isms to the community, may be developed. However, for every specific
contaminated site, a specific plan has to be constructed to appropriately
address the location-specific characteristics. Additional research is needed
to expand the knowledge base on how to efficiently translate successful
lab trials into robust field applications.
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CHAPTER SEVEN

Bio- and Phytoremediation of

pesticide-contaminated media. We will then review several possible remediation

Classical remediation technologies for areas contaminated with POPs

2. PESTICIDES: DIFFERENT TYPES AND

3. BEHAVIOUR OF PESTICIDES IN THE ENVIRONMENT

3.1 Transport of Pesticides

3.2 Transfer of Pesticides

years (Dijkgraaf & Vollebergh, 2004). Another limitation to these technol-

Nature-Based Remediation of Pesticides

Aeromonas sp. Chlorpyrifos, fenpropathrin Phragmites communis Chen et al. (2012)

Nele Eevers et al.

Nele Eevers et al.

Aspergillus sp. Pentachlorophenol Didemnun ligulum Vacondio et al. (2015)

Nele Eevers et al.

Signiﬁcantly less has been published on the possible remediation of

Sutherland et al., 2004; Wackett, 2004; Wackett, Sadowsky, Martinez, &

4.2 Plant-Associated Remediation

Figure 1 Overview of processes included in bio- and phytoremediation.

Table 3 Overview of the Plant Species That Have Shown Pesticide

Achillea millefolium DDT (Moklyachuk, Petryshyna, Slobodenyuk, &

Table 3 Overview of the Plant Species That Have Shown Pesticide

Table 3 Overview of the Plant Species That Have Shown Pesticide

Table 3 Overview of the Plant Species That Have Shown Pesticide

Table 3 Overview of the Plant Species That Have Shown Pesticide

the shoots of J. effuses, but L. peploides showed a 98.2% retention of the

can be efﬁciently used for the phytoremediation of ethion-contaminated

Few compounds can be completely degraded by only plant metabolic

5. ADVANTAGES AND DISADVANTAGES OF NATURAL

Therefore, though depending on the situation, natural remediation technol-

6. CONCLUSION, FUTURE PERSPECTIVES AND

inoculants: Developing a phytoremediation strategy. Plant and Soil. http://dx.doi.org/

Moore, M. T., & Locke, M. A. (2012). Phytotoxicity of atrazine, S-metolachlor, and

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