1 s2.0 S2352186421006672 Main

Environmental Technology & Innovation 24 (2021) 102019
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Environmental Technology & Innovation

journal homepage: www.elsevier.com/locate/eti
Current methods and technologies for degradation of atrazine

in contaminated soil and water: A review
Saeid Rostami a , Shaghayegh Jafari a , Zohre Moeini a , Marta Jaskulak b,c ,
Leila Keshtgar a , Ahmad Badeenezhad d , Abooalfazl Azhdarpoor a ,
∗
Majid Rostami e , Katarzyna Zorena c , Mansooreh Dehghani f ,
a
Department of Environmental Health Engineering, School of Health, Shiraz University of Medical Sciences, Shiraz, Iran
b
Univ. Lille, IMT Lille Douai, Univ. Artois, Yncrea Hauts-de-France, ULR4515 - LGCgE, Laboratoire de Génie Civil et
géo-Environnement, F-59000 Lille, France
c
Department of Immunobiology and Environment Microbiology, Medical University of Gdańsk, Poland
d
Department of Environmental Health Engineering, School of Health, Behbahan Faculty of Medical Sciences, Behbahan, Iran
e
Department of Agronomy, Faculty of Agriculture, Malayer University, Iran
f
Research Center for Health Sciences, Department of Environmental Health, School of Health, Shiraz University of Medical
Sciences, Shiraz, Iran
article info a b s t r a c t
Article history: Atrazine is one of the most widely-used chlorine herbicides in agriculture. In recent
Received 5 June 2021 years, studies have shown a potential hazard of atrazine use in environmental health
Received in revised form 30 September 2021 and human health. Due to its toxicity, widespread use, relatively high stability in water
Accepted 7 October 2021
and soil, determining safe and efficient methods of its removal is crucial. The main aim
Available online 12 October 2021
of this review was to showcase the recent progress of atrazine degradation methods,
Keywords: along with their main advantages, disadvantages, potential efficiency, and degradation
Environmental pollution pathways. The overall goal was to create an information gateway for researchers, and
Herbicide stakeholders interested in choosing the best method for atrazine degradation. Thus, the
Metabolites of atrazine current technologies for atrazine degradation are systematically reviewed and can be
Atrazine degradation pathway
used for future improvements or the selection of the most appropriate strategy for a
Endocrine disruptors
specific place.
© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Contents
1. Introduction – Atrazine and environmental contamination ............................................................................................................... 2

2. Biological effects of atrazine ................................................................................................................................................................... 3
3. Biological methods of atrazine degradation.......................................................................................................................................... 3
3.1. Microbial remediation ................................................................................................................................................................. 3
3.2. Phytoremediation......................................................................................................................................................................... 4
3.3. Vermiremediation ........................................................................................................................................................................ 5
3.4. Microbial electro-remediating cells ........................................................................................................................................... 6
3.5. Novel bioorganic fertilizer for the degradation of atrazine.................................................................................................... 6
4. Chemical and physicochemical methods of atrazine degradation ..................................................................................................... 6
4.1. Photolysis ...................................................................................................................................................................................... 6
4.2. Fenton ........................................................................................................................................................................................... 7
4.3. Photocatalysis ............................................................................................................................................................................... 7
∗ Corresponding author.
E-mail address: mdehghany@sums.ac.ir (M. Dehghani).
https://doi.org/10.1016/j.eti.2021.102019
2352-1864/© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.
org/licenses/by-nc-nd/4.0/).
S. Rostami, S. Jafari, Z. Moeini et al. Environmental Technology & Innovation 24 (2021) 102019
4.4. Plasma oxidation.......................................................................................................................................................................... 7

4.5. Electrokinetic process.................................................................................................................................................................. 7
4.6. Reversible electrokinetic adsorption barrier (REKAB) ............................................................................................................. 8
4.7. Nano zero-valent iron ................................................................................................................................................................. 8
4.8. Activated carbon .......................................................................................................................................................................... 9
4.9. Biochar adsorption....................................................................................................................................................................... 9
5. Metabolites of atrazine ............................................................................................................................................................................ 9
6. Pathways of atrazine degradation .......................................................................................................................................................... 9
7. Metabolites during different methods of atrazine degradation.......................................................................................................... 12
7.1. Non-thermal plasma.................................................................................................................................................................... 12
7.2. Photocatalysis ............................................................................................................................................................................... 13
7.3. Zero-valent Iron (ZVI) ................................................................................................................................................................. 13
7.4. Bioremediation ............................................................................................................................................................................. 14
7.5. Phytoremediation......................................................................................................................................................................... 14
8. Implementation of eco-technologies to remediate atrazine contaminated environments along with future
prospects ................................................................................................................................................................................................... 15
9. Conclusions................................................................................................................................................................................................ 15
CRediT authorship contribution statement ........................................................................................................................................... 15
Declaration of competing interest.......................................................................................................................................................... 15
Acknowledgment ...................................................................................................................................................................................... 15
References ................................................................................................................................................................................................. 15
1. Introduction – Atrazine and environmental contamination
In recent decades, the use of herbicides and pesticides in agricultural activities has become a standard and necessary
to control agricultural pests, increase efficiency, and prevent notable economic damage. S-Atrazine is one of the most
widely-used chlorine herbicides in agriculture (Hayes et al., 2002; Lassere et al., 2008). It was firstly developed in 1958,
and while it can be found under various names, atrazine with 2-chloro-4-(ethylamino)-6-(isopropylamino)-s-triazine has
the widest usage. After entering the market, atrazine became one of the most popular herbicides due to its high efficiency,
lower toxicity compared to older herbicides, its inexpensiveness, and its wide range of use (Agbekodo et al., 1996; Byrne
et al., 2018). Atrazine is a selective herbicide for controlling different broadleaf weeds and grasses in major crops such as
maize and sugarcane. The higher application dose of atrazine in non-agricultural lands is recommended for non-selective
control of weeds (Dehghani et al., 2007, 2013). Due to the various methods of atrazine application (pre-emergence, and
post-emergence), this herbicide has received more attention from farmers. A multitude of characteristics such as high
leakage potential, and absorption by organic materials and clay, quickly transformed atrazine from a leading herbicide to
a dangerous surface and groundwater pollutant (Graymore et al., 2001; Yu et al., 2020). The environmental persistence
of atrazine had been shown to be a vastly significant problem. One study from 2014 monitored the contamination of
groundwater in western Germany and found atrazine present in groundwater after 20 years of its ban. It was hypostasized
that a continued release of atrazine from the soil into the groundwater combined with the low atrazine degradation in
groundwater contributed to its elevated levels and persistence. Such residues had also been found in deep layers of soil
including even at a depth of 300 cm from the surface in areas where atrazine was last applied in 1991. In deeper layers
of soil and groundwater, atrazine half-life is significantly longer, and the long-term environmental behavior of atrazine
needs to be reconsidered. This problem could be even more prominent in fields with a long history of atrazine application
(Vonberg et al., 2014). Such effect had been recently shown in a study by Liu et al. (2020a), where despite the presence of
atrazine-degrading bacteria, the concentration of atrazine and its residues reached 100 times the soil safety limit after a
prolonged and annual application of atrazine. It was also showed that soil fertilization with organic fertilizers, including
sewage sludge and animal manure, could also inhibit the atrazine degradation in the soil due to the presence of antibiotics
and antibiotic resistance, which transform soil microbiota (Jiang et al., 2021). In addition, lower temperatures, especially
in deep layers of soil and in groundwater, also inhibit atrazine degradation and prolong its half-life. As such, it was shown
that in the lower temperatures (20 ◦ C), atrazine could remain in clay loam soil for several years (Chowdhury et al., 2021).
Due it the growing concerns surrounding areas with prolonged atrazine use, the main objectives of this review were
to; (1) showcase the recent progress on the development of new methods for atrazine degradation; (2) present the main
advantages, disadvantages, potential efficiency, and degradation pathways of different methods for atrazine degradation;
(3) systematically review all available technologies for atrazine treatment which can be used for future improvements in
those methods or the selection of the most appropriate strategy for a specific contaminated site.
2
2. Biological effects of atrazine
The United States Environmental Protection Agency reported the Maximum Contaminant Level (MCL) of atrazine in
water to be 3 µg L−1 . Environmentally relevant concentrations of atrazine were shown to be toxic to almost all members of
the food chain. From phytoplankter, Dunaliella tertiolecta, and microalgae, where the exposure to atrazine contamination
was shown to cause the inhibition of photosystem (Flood et al., 2018; Sun et al., 2020). Similarly, to microalgae, atrazine
also modifies the growth, enzymatic processes, and photosynthesis in higher plants. It also exerts severe mutagenicity,
genotoxicity, as well as a defective cell division, and endocrine disruption in aquatic organisms, most notably amphibians.
Atrazine was also shown to induce oxidative stress, cause DNA damage, and abnormal gene expression of annetocin, heat
shock protein 70, translationally controlled tumor protein, and calreticulin genes in earthworms (Cheng et al., 2020; Song
et al., 2009). In Prochilodus lineatus, Carassius auratus fish, atrazine was proven to be an enzyme inhibitor that impaired
hepatic metabolism and produced genotoxic damage (Cavas, 2011; Santos and Martinez, 2012). Recently, it was also
shown to trigger neutrophil apoptosis in common carp (Wang et al., 2019c), and histological damage in the liver and
testis of Astyanax altiparanae (Destro et al., 2021). In addition, it is threatening the sustainability of agricultural soils due
to its detrimental effects on soil microbiota (Singh et al., 2018). In humans, exposure to atrazine was associated with
decreased testosterone production, reduction in sperm motility, and an increase in sperm abnormality (Zhu et al., 2021b).
Atrazine use had been banned from use as early as 1991 in several European countries, including Germany and Italy. In
2004, the entire European Union (EU) banned the use of all atrazine products. However, three years after the complete
ban, research showed that atrazine was still present in drinking water and even in pregnant women’s urine. Finally, a
study from 2013 showed great success in limiting the atrazine presence in water and sediments in the EU countries after
its ban. The results showed that atrazine was no longer present in hundreds of samples taken from the Northern Adriatic
and Baltic Seas. In the Northern Aegean Sea, atrazine was still present, but its concentrations had dropped substantially
since the complete ban (Nödler et al., 2013). Nevertheless, despite the growing number of countries with the atrazine
ban, it is still widely used in some countries. Possible influences of atrazine on human health include its effects on the
expression of several proteins in various cell components, DNA damage, sperm mutagenesis, and disruption of endocrine
hormones (Lassere et al., 2008). Numerous studies have been performed to evaluate the biological effects of atrazine on
various animal species. One of these studies showed that exposure to certain levels, reported in the study, disrupts the
sexual evolution of amphibian species in the wild and reduces the number of animal species overall (Hayes et al., 2002).
There are several emerging approaches for atrazine removal from the environment. These include chemical filtration,
incineration, adsorption, nanofiltration, microwaves, chemical reduction, biological adsorption, biological filtration, oxida-
tion, photocatalytic processes, and bioremediation (Agbekodo et al., 1996; Atar et al., 2008; Baghapour et al., 2013; Brown
et al., 2004; Faghihian and Bahranifard, 2011; Gao et al., 2018; Hu et al., 2015; Khandarkhaeva et al., 2017; Moeini et al.,
2019). The accumulation of atrazine and the increase of its concentration in soil may cause widespread toxicity in plants.
For example, at concentrations >2 mg kg−1 , toxic responses such as reduced biomass and chlorosis have been observed
in some plant species (Sánchez et al., 2017). Following the use of atrazine for agricultural purposes, large amounts of
the herbicide can be found in the runoff, causing the contaminant to leak into rivers, water reservoirs, and surface and
underground streams. In some contaminated aquatic ecosystems, atrazine may inhibit photosynthetic activity, a primary
link in the food chain, raising an ecological concern (Graymore et al., 2001; Stratton, 1984). Due to the toxicity of atrazine
and its metabolites, its widespread use, relatively high stability in water and soil, and the possibility of toxicity to plants,
determining safe and efficient methods to remove this contaminant from environments is crucial. Therefore, in this study,
a variety of methods of atrazine removal from soil and water have been investigated. Table 1 shows the studies related
to the degradation of atrazine in the last 5 years in different environments.
3. Biological methods of atrazine degradation
3.1. Microbial remediation
Microbial remediation has many advantages such as the possibility to be applicable on a broad scale, the relatively sim-
ple procedure, low cost, and the absence of secondary contamination. Simultaneously, various factors, including ambient
temperature, salinity, pH, nutrient content, toxic substances, and other factors, limit the efficiency of microorganisms.
Therefore, using microorganisms with better performance and higher adaptation to the environment will have a more
favorable result (Table 2). Certain fungi and bacteria break down the atrazine molecule through alkylation and chlorination
reactions. In the study of Pelcastre et al. (2013) Trichoderma species were identified and isolated from three samples of
cultivable soil. They found that the resistance of this species to the atrazine was up to 10 000 mg L−1 . Also, in vitro, it can
decompose 89% of atrazine in soil within 40 days at a concentration of 500 mg kg−1 . Overall, the search and isolation
of specific bacterial strains that can degrade atrazine quickly with high efficiency are of great interest. New microbial
capsulation methods within different biodegradable materials containing bacterial traits, nutrients, fertilizers, and even
plant hormones are being developed for soil contaminated with organic pollutants. Such techniques can also be used for
atrazine, among other organic pollutants (Rostami et al., 2021; Wang et al., 2019b).
3
Table 1
Overview of the major studies dealing with atrazine degradation during the last 5 years (2017–2021) along with the applied methods.
Method Media Atrazine dose Degradation efficiency Reference
Persulfate (PS) activation via nanoscale Water 10 mg L−1 92.1% within 21 min Wu et al. (2018a)
zero-valent iron (nZVI) and graphene (GR)
composite
Cobalt-mediated activation of Water 10 µM 0.225 min−1 Zhu et al. (2019)
peroxymonosulfate (PMS)
Magnetic Fe3 O4 -sepiolite composite Water 10 mmol L−1 71.6% in 60 min Xu et al. (2019)
Aerobic zero-valent aluminum (ZVAl/Air) and Water 20 mg L−1 Maximum 96.3% Shen et al. (2018)
zero-valent iron (ZVI/Air) system
Peroxymonosulfate activation via Water 10 µM Degradation efficiency from Liu et al. (2020b)
cobalt-impregnated biochar 0.76 to 0.36 min−1
Peroxymonosulfate activated via Water 5 ppm >93% within 30 min Dong et al. (2020)
CoNi3 O4 /diatomite hybrid
Persulfate coupled with dithionite Water 1 µM 100% within 90 min Song et al. (2019)
Persulfate (PS) activated by pyrite (FeS2 ) Water 20 mg L−1 70% within 10 min Wang et al. (2020)
−1 −1
Photolytic degradation mechanism of atrazine Water 3 mg L 3.35 mg L in 20 min Moreira et al. (2017)
using a UV reactor and UV/MW (electrodeless
discharge lamp (Hg-EDL))
Co/Sm co-modified Ti/PbO2 anode Water 20 mg L−1 92.6% within 3 h Chen et al. (2021)
Iron-catalyzed photo-activation of persulfate Water 4 mg L−1 90% within 15 min Popova et al. (2019)
(UV/PS/Fe2+ system) under mercury-free KrCl
excilamp irradiation (222 nm)
Fe3 O4 /PMS system in the presence of Water 23 µM 94% within 15 min Li et al. (2019)
hydroxylamine (HA)
Cu–ZnO integrated with g-C3 N4 to create Water 100 ppm 97% within 120 min Truc et al. (2019)
Cu–ZnO/g-C3 N4 Z -direct scheme photocatalyst
for advanced atrazine removal
Ferrate (Fe(VI))/peroxymonosulfate (PMS) Water 46.5 µM 81.5%, within 60 min Wu et al. (2018b)
process
Nanosized BaFe1−x Cux O3 powder Water 10–40 mg L−1 >90% in 120 min Jamil et al. (2018)
Co3 O4 /g-C3 N4 hybrid photocatalyst with Water 50 µM 78.5% after 35 min Yang et al. (2021)
peroxymonosulfate
Photo-Fenton-like process using persulfate (PS) Water 4 mg L−1 90% within 60 min Garkusheva et al. (2017)
and ferrous iron (Fe2+ ) under simulated solar
radiation
Manganese porphyrins as biomimetic Water 3.0 × 10−5 100% when iodobenzene Lage et al. (2019)
cytochrome P450 models. PhIO, PhI(OAc)2 , mol diacetate was the oxidant
H2 O2 , t-BuOOH, m-CPBA, and Oxone⃝
R
as 6.0 × 10−8 mol
oxidants
CoMgAl layered double oxides catalyzed Water 10 mg L−1 98.7% Hong et al. (2019)
peroxymonosulfate
Bioaugmentation with Water 5 mg L−1 100% in 43 days Zhao et al. (2019)
Pseudomonas and Arthrobacter
ZnIn2 S4 -based catalysts Water 20 mg L−1 90% in 1 h Bo et al. (2020)
Nanoscale LaFe1−x Cux O3−δ perovskite activated Water 23 µM 100% in 60 min Wang et al. (2019a)
peroxymonosulfate
Biodegradation of atrazine by the Water 50 mg L−1 50 mg L−1 atrazine in 66 h Yang et al. (2018)
novel Citricoccus sp. strain TT3
Bioremediation with Arthrobacter sp. ZXY-2 Water 100 mg L−1 100% after 15 h Zhao et al. (2017)
(continued on next page)
3.2. Phytoremediation
To date, many researchers have used phytoremediation technology to deal with atrazine-contaminated environments.
Phytoremediation is a well-known technology, using plants for the treatment of both organic and inorganic pollutants
from the environment. The plant removes contaminants from the environment through mechanisms including degra-
dation, uptake, evaporation, accumulation, or improvement of soil rhizosphere activity. The advantages of this method
include its simplicity, low cost, the absence of secondary pollution, and environmental compatibility. In addition to these
4
Table 1 (continued).
Method Media Atrazine dose Degradation efficiency Reference
CdS/BiOBr/Bi2 O2 CO3 ternary heterostructure Water 10 mg L−1 >95% in 30 min Majhi et al. (2020)
materials
Bentonite-supported nZVI (B-nZVI) as a Water 0.046 mM 98% in 60 min Diao and Chu (2021)
catalyst to activate H2 O2 in the presence of
FeS2
Zero-valent iron and biochar composite Water 25 mg L−1 73.47% within 30 min Jiang et al. (2020)
(ZVI/BC) activated persulfate (PS)
Znx Cu1−x Fe2 O4 nanomaterial-catalyzed sulfite Water 4.4 µM 95% in 30 min Huang et al. (2018)
under UV–vis light irradiation
Enhanced electro-Fenton performance by Water 30 mg L−1 93% within 15 min Zhao et al. (2018)
fluorine-doped porous carbon
Phytoremediation with Ryegrass (Lolium Water 2.5, and 10 mg 36% increase in 16 days Sánchez et al. (2017)
perenne), Tall festuce (Festuca arundinacea), kg−1 compared to control
Barley (Hordeum vulgaree), Maize (Zea mays)
Bacillus atrophaeus strain, YQJ-6 Soil 50 mg L−1 99.2% after 7 days Zhu et al. (2021a)
Vermicomposting with epigeic Eisenia Soil 10 mg kg−1 94.9%–95.7% in 28 days Lin et al. (2018)
foetida and endogeic Amynthas robustus
Electrokinetic-assisted phytoremediation Soil 2 mg kg−1 80% of the initial atrazine Sánchez et al. (2017)
(EKPR) was removed from soils in
the first 4 days of treatment
Reversible electrokinetic adsorption barrier Soil 30 mg kg−1 90% within 15 days Dos Santos et al. (2017)
(REKAB)
Dielectric Barrier Discharge (DBD) method Soil 100 mg kg−1 87% within 60 min Aggelopoulos et al. (2018)
Soil fertilization with a Mix of agricultural Soil 15 mg kg−1 >95% within 10 days Chen et al. (2019)
waste and organic cattle manure (76.20%),
with the addition of biochar (4.46%), poly-
(γ -glutamic (8.63%) acid), and atrazine
degrading strains as well as Arthrobacter
DNS10 strain (0.91 × 108 CFU g−1 )
benefits, phytoremediation also has a positive visual impact on the environment. Due to the advantages of this method,
and its effectiveness in removing organic pollutants, it is commonly used to remove atrazine from soil environments,
and it has demonstrated a high efficiency (Sánchez et al., 2017). Merini et al. (2009) selected Lolium multiflorum, an
atrazine-resistant plant species, for atrazine degradation as it can grow and germinate in atrazine-contaminated soil
at a concentration of 1 mg kg−1 . They found that this plant could increase the atrazine degradation capacity (by 20%)
during natural processes. In another study, Sánchez et al. (2017) examined the phytoremediation potential of four plants,
including ryegrass (Lolium perenne), tall fescue (Festuca arundinacea), barley (Hordeum vulgare), and maize (Zea mays) in
atrazine degradation. The results showed that all studied plants could accumulate atrazine in their tissues. Among these
plants, maize was the species that had the highest ability to accumulate atrazine derivatives and accumulated > 38.4%
of the initial atrazine concentration.
3.3. Vermiremediation
Earthworms are known as ecosystem engineers and have high environmental compatibility, reproductive capacity,
and high resistance to organic pollutants. Due to their biochemical and physical actions and behaviors, earthworms cause
significant changes in the physicochemical properties of soil, changes in the availability of organic pollutants, and the
benefit of bioremediation (Jaskulak et al., 2021).
Burrowing and movement of earthworms in the soil improves soil structure, increases soil porosity, and increases
microbial activity. Earth-shaped burrows also improve gas emissions and moisture drainage. Earthworms help disperse
soil masses, release organic matter, and disperse soil by swallowing, digesting, and disposing of soil grains. Besides,
earthworms increase soil pH and water holding capacity, improve nutrient content and availability, and promote
indigenous microorganisms. Therefore, vermiremediation by earthworms, in addition to improving soil aeration and
increasing fertility, is also efficient in the bioremediation of organic pollutants (Rorat et al., 2017). In the study of Lin et al.
(2019) the effect of two types of earthworms (epigeic Eisenia foetida and endogeic Amynthas robustus) on atrazine and its
degradation path in red soil was investigated. The reason for choosing these two species of earthworms is their distinct
maps and different mechanisms in the vermiremediation process. The researchers found that E. foetida accelerates the
degradation of organic matter and stimulates microbial growth by breaking down organic debris into smaller particles.
Simultaneously, A. robustus increases porosity and oxygen supply to other soil layers by creating tunnels. Earthworms
significantly accelerate the degradation of atrazine through the secretion of humus-fixed atrazine, increase the availability
5
of atrazine, and stimulate the metabolism of atrazine degraders. By examining the degradation pathway of atrazine, it
was found that earthworms, by swallowing and digestion, increase ionized atrazine and neutralize soil pH. On the other
hand, ionized atrazine is more soluble. Studies on vermiremediation have shown that earthworms alter the structure
of the bacterial population, enrich native destroyers, and thus enhance atrazine bioremediation. The rate of available
atrazine increased from 8.80% in bulk soil to 10.30% and 16.42% in the vermiremediation treatments. Also, atrazine residue
decreased from 4.23 mg kg−1 in bulk soils with E. foetida and A. robustus to 0.51 and 0.43 mg kg−1 , respectively.
3.4. Microbial electro-remediating cells
As mentioned before, in the bioremediation methods, organic pollutants can be degraded by microorganisms in
nature. However, often, the lack of a suitable electron receptor limits microbial respiration. In the absence of oxygen
as the terminal electron receptor (TEA) in aerobic processes, the electron transfer chain is interrupted. This problem
can be overcome using an electrically conductive material, similar to the electrodes used in Sediment Microbial Fuel
Cells (SMFCs). Bioelectrochemical devices consist of an electrode (anode) buried in sediment or soil that combines with
the microbial oxidation of organic matter to reduce the number of electrons and acts as an electron sink. This anode
is connected to a cathode through an external resistor, where the electrons are eventually consumed by the electron
receiver (as oxygen) to obtain electrical energy (Yang and Chen, 2020). If SMFC is used in contaminated environments, the
microbial biodegradation rate is improved. Graphite electrodes were first used as the final electron acceptor for toluene
and benzene degradation in contaminated slurries (Rodrigo et al., 2014). Since then, several studies have reported an
improvement in the biodegradation of various chemical contaminants such as polycyclic aromatic hydrocarbons (PAHs),
petroleum hydrocarbons, pesticides, and herbicides. Nutrients, oxygen as electron donors and receptors, are unusable in
the soil that requires a constant additional supply, and their availability requires appropriate environmental conditions
(pH, temperature, humidity, etc.). Therefore, bioelectroventing-based refinement overcomes this limitation due to the
presence of an electrode that acts as an endless electron receptor in anaerobic soils, allowing microorganisms to exert
oxidative metabolism beyond normal conditions. Besides, the competitive role of the electrode may reduce the formation
of hydrogen sulfide and even methane, which is a secondary contaminant. Degradation of atrazine in the soil is mainly the
result of microbial activity, and many types of microorganisms like Pseudomonas sp. strain ADP (De Souza et al., 1998),
Agrobacterium radiobacter J14a (Struthers et al., 1998), or Nocardioides (Topp et al., 2000) are involved. Herbicides are
broken down by metabolic processes that eventually lead to the formation and accumulation of atrazine metabolites. In
the study of Domínguez-Garay et al. (2016) the Microbial Electroremediating Cells (MERC) method was used to stimulate
the biodegradation of atrazine in soil. By removing the limitations in the electron transfer chain, they improved cellular
respiration and proposed this method under the term bioelectroventing. The study results showed that the presence of
electrodes as electron acceptors effectively increased the degradation rate of atrazine by five times that of the control.
3.5. Novel bioorganic fertilizer for the degradation of atrazine
While different techniques, such as biodegradation, and physical adsorption, can remove atrazine from contaminated
soils at different levels of efficiency, studies are still needed to find more efficient, cost-effective, and environmentally
friendly remediation techniques. An ideal approach would be to limit the use of atrazine and other chemical contaminants
and to substitute them with suitable alternatives. Alternative and usable materials are bioorganic fertilizers (BOF). BOF
is a type of fertilizer that is a combination of specific microorganisms and organic matter. It mainly consists of refined
animal and plant residues (i.e., livestock and poultry manure, agricultural residues, and crop straw, etc.). Studies have
shown that the use of biological fertilizers, in addition to improving soil quality, promotes plant growth, suppression of
soil-borne diseases, and sustainable agricultural development. Chen et al. (2019) studied the degradation of atrazine from
soil and demonstrated a reduction in stress effects on soybean growth when bioorganic fertilizer was used. This fertilizer
was prepared using agricultural waste and organic cattle manure (76.20%), biochar (4.46%), and poly-(γ -glutamic acid
(8.63%), as well as one of the atrazine degrading strains (DNS10) belonging to Arthrobacter sp. (0.91 × 108 CFU g−1 ).
This strain of bacteria was isolated from atrazine-containing soils. In this study, using Design-Expert software, an optimal
formulation was obtained to maximize atrazine degradation for the preparation of BOF, called DNBF10. Using DNBF10, the
degradation efficiency of atrazine with an initial concentration of 15.26 mg kg−1 was 95.05% after just ten days. In general,
the results of soybean planting in soil containing 75% chemical fertilizer and 25% DNBF10 fertilizer showed better growth
than soil with 100% chemical fertilizer. The application of DNBF10 also reduces atrazine-induced damage to soybeans.
Other studies have examined the use of microbial species in bioorganic fertilizers preparation and the effect of a specific
microbial consortium in these fertilizers on improving plant growth and eliminating soil contaminants (Patil and Solanki,
2016; Yao et al., 2017).
4. Chemical and physicochemical methods of atrazine degradation
4.1. Photolysis
Light radiation can break down many types of herbicides and pesticides. Atrazine, like other herbicides, is affected
by this radiation. Therefore, atrazine content in the contaminated soil gradually decreases. This gradual decrease can be
6
due to the process of photolysis caused by sunlight and ultraviolet rays (UV) in the soil. But under natural conditions,
due to the low penetration of UV, the reduction in atrazine concentration occurs slowly and only in the upper layers
of the soil. Various factors such as pH, radiation intensity, soil granularity, presence of organic matter, and surfactants
(dodecylbenzenesulfonate (DBS)) affect the photolysis rate of atrazine. In one study, Xiaozhen et al. (2005) reached a
constant degradation rate of 0.08 to 0.17 per day at a depth of 0.5 mm from the soil surface. In addition, it was found
that a smaller soil particle size and the presence of certain organic compounds as humic acid increase this constant rate
of degradation (Table 2).
4.2. Fenton
One of the most well-known and developed AOP methods used to treat herbicide and pesticide-contaminated soil is the
Fenton process. Fenton reactions are based on the oxidation of iron ions (Fe2+ ) in a hydrogen-containing bed (H2 O2 ) and
the production of a hydroxyl radical. Hydroxyl radicals oxidize atrazine to less dangerous substances. Various oxidant
compounds such as permanganate (MnO4 − ), persulfate (S2 O8 −2 ), and ozone (O3 ) can be used in the Fenton reaction,
each with its advantages and disadvantages (Baldissarelli et al., 2019). Catalysts can also be used in Fenton/Fenton-like
reactions. In one study, atrazine was removed from contaminated soil through a Fenton-like process using Steel Converter
Slag (SCS) as the catalyst, demonstrating a high efficiency (93.7%). This efficiency was obtained under optimal conditions
with a concentration of 10% H2 O2 and an SCS load of 80 g kg−1 . At the end of the process, the amount of dissolved organic
carbon (DOC) increased from 0.339 to 1.206 g kg−1 (Cheng et al., 2016).
4.3. Photocatalysis
In the photocatalytic method, strong hydroxyl radicals are produced in the presence of a catalyst and under UV or
visible light, which oxidize and decompose the pollutant. Zhang et al. (2018) studied the light degradation of atrazine
in the presence of natural montmorillonite clay and the plant hormone indole-3-acetic acid (IAA) under visible light
irradiation. They found that a reaction is caused in the hydrated electrons of the IAA when ionized by light. These
electrons then react with protons and dissolved oxygen to form hydroxyl radicals, which promote further degradation
of atrazine. Montmorillonite increases the lifespan and efficiency of hydrated electrons by stabilizing radical cations with
electrostatically absorbing negative charges in the clay. Besides, montmorillonite increases the likelihood of active radicals
colliding with atrazine molecules by creating a confined space. Due to the high presence of IAA and montmorillonite in
the environment, it is predicted that this reaction will play an essential role in the degradation of atrazine and other
resistant organic pollutants.
In photocatalytic processes, oxides of various semiconductor metals such as TiO2 , ZnO, CdS, GaP, and WO3 are
used as catalysts. Among the semiconductor metal oxides, TiO2 is distinguished in anatase form due to its unique
properties, including high photocatalytic activity, chemical and temperature stability, non-toxicity, easy access, and low
cost (Karthikeyan et al., 2020).
4.4. Plasma oxidation
Various factors such as light intensity (Bo et al., 2020), organic matter, and soil moisture (Marican and Durán-
Lara, 2018) can affect the pollutant’s degradation rate during photocatalytic processes. Plasma oxidation is considered
competitive with other existing technologies for the degradation of organic pollutants from the soil. Recently, this process
has been used to recover contaminated soils as an innovative and environmentally friendly alternative. Low-Temperature
Plasma (LTP) is more commonly used, especially the technique based on Pulsed Corona Discharge (PCD) (Wang et al.,
2014). The Dielectric Barrier Discharge (DBD) method was used by Aggelopoulos et al. (2018) to remove atrazine from the
soil. This process was performed in a plane-to-grid reactor at atmospheric pressure. The degradation efficiency of atrazine
is a function of the parameters of voltage and discharge frequency. The degradation efficiency of atrazine in soil reached as
high as 86.9% and 98.1% after 60 min of plasma treatment, starting from initial atrazine concentrations of 100 and 10 mg
kg−1 , respectively. The study results showed that relative humidity (5%–10%) improves atrazine degradation. By measuring
the total amount of organic carbon (TOC), it was found that after 60 min, 65.5% atrazine mineralization occurred. Various
parameters as treatment time, initial concentration of contaminants, soil moisture, airflow rate, discharge frequency, and
energy efficiency affect the efficiency of the DBD method.
4.5. Electrokinetic process
The electrokinetic remediation involves the application of low and continuous current intensities between electrodes
in the soil. The electrodes must be made of neutral materials such as graphite or platinum. When an electric current
is applied, water electrolysis occurs, and an acidic solution forms near the anode. Acid migrates from the anode to the
cathode, leading to the desorption of soil contaminants. This phenomenon causes the pollutants to move directly and
condense in a small area.
7
The primary disadvantage of this method is energy consumption, which comprises about 10 to 15% of the total costs
(Vocciante et al., 2021). Due to the success of phytoremediation in atrazine degradation, it is recommended that this
method be combined with an electrokinetic remediation technique to achieve better efficiency in the purification of
atrazine contaminated soils. Electrokinetic-assisted phytoremediation (EKPR) involves applying a low voltage electric
field to instigate electrochemical reactions. These reactions also cause water, pollutants, free ions, and nutrients to move
through the soil via various mechanisms such as electroosmosis, electromigration, and electrophoresis. There are some
limitations to the phytoremediation method, such as long-term purification and low availability of contaminants. In the
study by Sánchez et al. (2019), the use of EKPR increases the atrazine degradation efficiency by 27% and 7%, compared
to natural purification and phytoremediation, respectively. About 80% of the initial atrazine was removed from the soil
during the first four days of treatment.
4.6. Reversible electrokinetic adsorption barrier (REKAB)
Electrokinetic Remediation combined with Permeable Reactive Barriers (PRBs) is a promising process for herbicide
degradation. In soils with low permeability, the application of the PRB process is limited. Therefore, in the REKAB hybrid
process, EK also implements the PRB process in soils with low permeability. In PRB technology, the pollutant is driven
forward by a groundwater hydraulic gradient. If the EK is combined with PRB, the pollutant current is transmitted by the
electro-osmotic flow of soil pore fluid, electromigration, or electrophoresis (Dos Santos et al., 2017; Li et al., 2011; Wan
et al., 2010).
Reactive materials commonly considered in this barrier include reduction using elemental metals, adsorption with
high-level porous materials, ion exchange with resin materials, biological degradation, limestone, hydroxyapatite, acti-
vated carbon, and zeolite. However, by using inexpensive materials like granular activated carbon (GAC) as the reaction
material, this combined process can be more cost-effective. It prevents reversible changes in the polarity, acidity, and
alkalization of contaminated soils in the vicinity of cathodes and modifies the EK process by preventing ionic species
reduction. This feature is especially important in Electrokinetic Soil-flushing Technology (EKSF) or Electrokinetic Leaching
Technology with Biological Barriers as these irreversible processes lead to the loss of nutrients (exhaustion of nutrients)
in the soil. In the study by Dos Santos et al. (2017), they used Reversible Electrokinetic Adsorption Barrier (REKAB)
technology, a combination of GAC-PRB and EK, to remove atrazine and oxyfluorfen from low-permeability soils. In this
method, GAC was placed as a reactive permeable barrier (PRB) to enhance the degradation of atrazine between the anode
and the cathode. After 15 days, the experiment results were compared with studies using conventional EKSF technology,
and very significant differences were observed. The result obtained using REKAB technology was better than that of the
EKSF study. After 15 days of treatment, only about 10% of the herbicides remained in the soil. Adsorption on GAC substrate
was also a principal mechanism in herbicide removal.
4.7. Nano zero-valent iron
Some persistent herbicides decompose more easily in aerobic environments under reducing conditions. Therefore,
creating a reducing (electron-rich) environment in soil, sediments, and groundwater aquifers is a good option for
degradation of pollutants. One application of this technique is to use zero-valent iron (ZVI) as a chemical reducing agent. In
aerobic conditions, oxygen is a common electron acceptor, while in anaerobic environments, electron release from the ZVI
reaction with water can be accompanied by the reaction of chlorinated and nitro-aromatic compounds. ZVI remediation
can improve rapid non-biological degradation through reduction chlorination.
In many cases, nano zero-valent iron (nZVI) can be seen as a perfect adsorbent with several advantages that include its
high reactivity and core–shell structure. However, the most commonly used way of nZVI synthesis consists of a reduction
reaction by NaBH4 or KBH4 , which are expensive and toxic. Recently, as an alternative, new green methods of its extraction
had been shown also to be effective and reduce costs and environmental concerns. Such methods include extraction
from green tea extract, lemon balm, and leaves of fruit trees (Qu et al., 2021a). To date, ZVI has been used successfully
to deform various contaminants, including pesticides and herbicides, such as atrazine. Implementing the nanoscale ZVI
technique provides advantages over the application of granular ZVI, such as greater reactivity, higher velocity, and greater
concentration of contaminant degradation. Nano ZVI particles are also easier to inject into soil pores than granular ZVI
particles. Satapanajaru et al. (2008) determined the effectiveness of laboratory-synthesized nano ZVI with Pd catalyst
in removing atrazine from aqueous and soil solutions. The results showed that the rate of atrazine degradation kinetics
(Kobs ) in purification with synthesized nano ZVI (1.39 days−1 ) in this study was about seven times higher than this rate
in commercial nano ZVI (0.18 days−1 ) available in the market. Reductive dechlorination is the predominant process in
atrazine degradation with nano ZVI. The atrazine degradation efficiency was approximately 52% using nano-synthesized
ZVI and about 20% using commercial ZVI. The effect of other parameters on atrazine degradation such as iron source,
solution pH, presence of Pd catalyst, presence of ferrous sulfate salts, and ZVI nano aluminum was investigated. The
results also showed that lowering the pH from 9 to 4 increased the degradation of atrazine by nano ZVI. Besides, they
found that Pd plays an important role as a catalyst during atrazine degradation in the nano ZVI/Pd process.
8
4.8. Activated carbon
Activated carbon has a porous structure and a large specific surface area, and these properties allow for the effective
absorption of various pollutants. Activated carbon, which is available in granules, powders, and fibers, is the most common
adsorbent used for atrazine degradation. However, studies have shown that activated carbon in fiber absorbs seven times
more atrazine than commercial granular activated carbon (He et al., 2019; Martın-Gullón and Font, 2001). Due to the
remarkable capabilities of activated carbon in organic pollutant degradation, this adsorbent is used in combination with
other atrazine degradation technologies. For example, after examining the degradation of atrazine using a reversible
electrokinetic barrier process in combination with activated carbon, Dos Santos et al. (2017) found that the electrokinetic
process is not the predominant one for atrazine degradation. The absorption of pollutants on the activated carbon bed
located in the soil column also has a significant role in removing herbicides.
4.9. Biochar adsorption
Biochar is produced during a process that includes pyrolysis and the carbonization of biomass materials, which are
used in environmental remediation (Qu et al., 2021b; Xiang et al., 2020). Biochar is used as an eco-friendly and cost-
effective remediation method for environmental remediation. It can effectively absorb organic pollutants such as PCBs,
PAHs, herbicides and pesticides such as diuron, carbaryl, acetochlor, and atrazine (He et al., 2019; Zheng et al., 2010).
Recently, more attention had been drawn toward biochar as a contaminant adsorbent, for water and soil environments,
due to its many advantages, such as several source materials, low cost, and relatively high specific surface area (Zhang
et al., 2021). Cao et al. (2011) investigated the ability of commercial activated carbon and Dairy-Manure Biochar to trap
and immobilize atrazine and Pb in contaminated soil. After preparing biochar from dairy waste, the resulting biochar
was added to atrazine and Pb-contaminated soil at a weight ratio of 0, 2.5, and 5%. The concentration of Pb and atrazine
was measured in the soil. After 210 days, CaCl2 and TCLP (toxicity characteristic leaching procedure) extraction tests
were performed. The results showed that the bioavailability (CaCl2 extraction) of atrazine was reduced by 66%–81%. TCLP
results also showed a 53%–77% reduction in concentration. In general, the results of this study showed that biochar from
livestock waste has good potential in stabilizing and immobilizing organic pollutants and heavy metals in contaminated
soils (Table 2). In another study, Zheng et al. (2010) prepared biochar from a waste biomass using the pyrolysis process.
Then, the absorption ability of unmodified biochar was investigated, focusing on atrazine and simazine. They found that
in the presence of atrazine and simazine simultaneously, competitive adsorption occurs, with the adsorption capacity (Kf )
of atrazine decreasing from 435 to 286 and the adsorption capacity of Simazine from 514 to 212.
5. Metabolites of atrazine
It should be noted that atrazine metabolites, as products of atrazine degradation, can leach from the soil surface,
penetrate the substrates, and are considered a significant hazard to groundwater (Naseri et al., 2009). When a herbicide
is released into the environment, it may decompose through biotic or abiotic processes. Most studies have evaluated the
amount of residue and the effects of maternal herbicides, whereas the transformed products resulting from degradation
processes are less developed. Degradation products are usually less toxic to living organisms than parent compound
(Sinclair and Boxall, 2003). However, in some cases, these substances may be more harmful than the primary contaminant
and pose a greater risk to the environment (Kolpin et al., 2001). In Europe, guidelines have been adopted to collect
information on all metabolites, reactions, and degradation products, in cases where they make up over 10% of the active
ingredient added (Directive, 1994). Sinclair and Boxall (2003) studied the relationship between transformed product
toxicity and parent compounds to provide a realistic approach to application in product risk assessment. In general,
the results of the study showed that the final degradation products were less toxic than the parent compound for fish,
daphnids, and algae. In cases where the products have been more toxic, an increase in toxicity has been reported as a
result of the toxicophore, or the active part of propesticide that becomes an active ingredient when used and absorbed
by the organism or may remain a pesticide or its degradation product. Also, the bioconcentration factor for the converted
products may be larger than the initial substance, and the product may accumulate more than the parent compound.
6. Pathways of atrazine degradation
The degradation pathways of atrazine are not yet well known. The main proposed pathways are dealkylation, dechlo-
rination, and deamination. Dealkylation and dechlorination are seen as the dominant mediating pathways in biological
and chemical processes, respectively. Some bacteria break down atrazine into hydroxyatrazine through a hydrolytic
dechlorination process using the atrazine chlorohydrolase enzyme. In this process, the OH group is replaced by a chlorine
atom. Hydroxyatrazine is then converted to N-isopropylammelide or N-ethylammelide intermediates through hydrolytic
deamination reactions catalyzed by the enzyme amidohydrolases, which fall into the triazine group and can eventually be
converted to cyanuric acid. Another pathway that may occur in the degradation of atrazine is N-dealkylation on the ethyl
and isopropyl side chains and their conversion to deethylatrazine, deisopropylatrazine, and deethyldeisopropylatrazine.
In this way, producing these materials provides the necessary energy for the growth and reproduction of microorganisms.
9
Table 2
Successful application of biological, physicochemical and chemical methods for the degradation of atrazine and their efficiency.
Method/Species used Atrazine Time Efficiency Other details Reference
dose
Bioremediation with 500 mg 40 days 89% Trichoderma sp. showed Pelcastre et al. (2013)
Trichoderma sp. kg−1 resistance to atrazine up to
10 000 mg L−1 in in vitro
conditions
Ryegrass Lolium 1 mg kg−1 21 days L. multiflorum presented L. multiflorum is a promising Merini et al. (2009)
multiflorum 20% higher atrazine candidate for large scale
removal capacity than phytoremediation of
the natural attenuation atrazine due to the
following factors: high
capacity to germinate in the
presence of atrazine,
elevated capacity for
atrazine removal, high
initial degradation rate
Pseudomonas sp. A02 100 mg L−1 24 h 99% The consortium formed by Fernandes et al.
A01 and A02 is not more (2018)
efficient in atrazine
degradation
Achromobacter sp. A01 100 mg L−1 48 h 39% The consortium formed by Fernandes et al.
A01 and A02 is not more (2018)
efficient in atrazine
degradation
Agrobacterium radiobacter 50 µg of 72 h 94% Atrazine was broken down Struthers et al. (1998)
strain J14a [14 C-U-ring] by metabolic processes that
atrazine eventually lead to the
ml−1 formation and accumulation
of the following atrazine
metabolites:
hydroxyatrazine,
deethylatrazine, and
deethylhydroxyatrazine
Microorganism 1.5 mg Kg−1 24 h, 1 83% after 7 days Toxicological tests using Domínguez-Garay
consortium living in the week, 2 Pseudokirchneriella et al. (2016)
soil weeks subcapitata green algae,
Salmonella typhimorium
bacteria, and Sorghum
saccharatum plant,
confirmed that
atrazine-polluted soil can
be effectively cleaned up in
a short time by the use of
MERCs method
Alfalfa Medicago sativa 0, 0.02, 6 days – In vitro conditions, the Zhang et al. (2014)
0.04, 0.06, outcome of the work
0.08, and showed the detailed
0.10 mg L−1 mechanisms for the
atrazine accumulation and
degradation in the alfalfa
plant
Arthrobacter sp. TES6 30 mg L−1 3 h 100% This bacterial isolate El Sebaï et al. (2011)
harbors the trzN, atzBC
gene combination
responsible for converting
atrazine to cyanuric acid
Ensifer CX-T 100 mg L−1 30 h 100% Degrading genes: atz A, atz Ma et al. (2017)
B, atz C, atz D, atz E and atz
F were amplified
Pseudomonas EGD-AKN5 100 mg L−1 87 h 98.3% Atrazine degradation Bhardwaj et al.
occurred via the action of (2015)
atz ABCDEF genes
10
dose
Arthrobacter HB-5 100 mg L−1 12 h 100% Strain HB-5 metabolizes Wang et al. (2011)
atrazine to hydroxyatrazine.
Then, the bacterium
metabolizes hydroxyatrazine
to cyanuric acid but does
not mineralize atrazine
Solar light 1000 µg Half-life 4–8 The rate constant of Parameters like soil Xiaozhen et al. (2005)
ml−1 days photolysis ranged from granularity, pH, humidity,
0.08 to 0.17 day−1 organic content, and
surface-active agents
affected the
photodegradation of
atrazine in soil
Fenton-like process with 617.5 mg 10, 20, 30 h 93.7% A high initial concentration Cheng et al. (2016)
Steel Converter Slag kg−1 of H2 O2 causes a rapid
(SCS) increase in soil
temperature. Steel converter
slag catalyzed Fenton-like
oxidation and slightly
increased soil pH
Photodegradation of 0.74 to 24 h 38.7%, with a Atrazine is photooxidized in Zhang et al. (2018)
atrazine in the presence 74.18 µM degradation rate presence of IAA and MMT.
of IAA and constant of 0.022 h−1 Montmorillonite clay can
montmorillonite significantly enhance this
process
Sunlight 10 mg L−1 180 min 93.1% Increased photocatalytic Li et al. (2012)
photodegradation of activity in comparison to
aqueous atrazine and pure titania was obtained
rhodamine B catalyzed for the treatment with
by the ordered graphene–titania/silica
mesoporous
graphene–titania/silica
composite material
N,F-codoped TiO2 5 mg L−1 6 h 60% Catalyst calcined at 600 ◦ C Zhang et al. (2015)
nanowires showed the best
photocatalytic activity
Photocatalytic 10 mg L−1 2 h 99.47% Atrazine degradation Shamsedini et al.
degradation of atrazine efficiency was increased by (2017)
herbicide with increasing initial atrazine
Illuminated Fe+3 -TiO2 concentration, catalyst, and
Nanoparticles contact time
Decomposition of 30 µg L−1 45 min 85% Atrazine absorption on the Vanraes et al. (2015)
atrazine traces in water nanofiber membrane
by combination of increased the degradation
non-thermal electrical efficiency. The generated
discharge and adsorption ozone and hydrogen
on nanofiber membrane peroxide contributed only
to 20% of the degradation
2% (w/v) of nano ZVI 30 mg L−1 60 h destruction kinetic rates The rate of degradation Satapanajaru et al.
and 5% (w/v) of of atrazine (3.36 day−1 ) kinetics with synthesized (2008)
commercial ZVI nano ZVI (1.39 days−1 ) in
this study was about seven
times higher than this rate
in commercial nano ZVI
(0.18 days−1 ). Reductive
de-chlorination was the
crucial process in atrazine
degradation with the nano
ZVI
11
dose
Dairy-manure biochar 50 mg kg−1 210 days 53%–77% The experiment showed the Cao et al. (2011)
potential of dairy-manure
biochar for immobilization
of heavy metal (Pb) and
herbicide (atrazine) at the
same time in
co-contaminated soils
Whether deisopropylatrazine or deethylatrazine is first formed depends on the microbial strain. In this process, one or
both N-alkyl side chains are removed. By performing a hydroxylation reaction on the dealkylated atrazine metabolites,
cyanuric acid is produced as the final product. The produced cyanuric acid is broken down into carbon dioxide, and
ammonia by the cyanuric acid amidohydrolase enzymes, biuret amidohydrolase, allophanate hydrolase, and the released
nitrogen is provided to the atrazine-degrading bacteria as a source of nitrogen. The presence of all associated enzymes
is essential for the complete mineralization of atrazine in biological processes (Cherifi et al., 2001; Ghosh and Philip,
2006; Kumar and Singh, 2016). Another biological metabolic pathway that may degrade atrazine is its combination
with glutathione. This pathway is the result of a thiol group nucleophilic attack. The thiol group originates from the
reduced nucleophilic on the electrophilic centers of lipophilic compounds. This conjugation is mediated by the enzyme
glutathione S-transferase (GST), which reduces the toxicity of atrazine in two ways. Detoxification occurs either through
structural changes at the reactive site of the molecule or by a significant increase in its hydrophilicity that leads to vacuole
accumulation. Glutathione is the only reducing compound used by GST. GST activity has been identified in many eukaryotic
organisms such as plants, insects, and animals (Cherifi et al., 2001). Atrazine degradation takes place through different
processes. Depending on the type of process, the amount of mineralization, and the residues left from the degradation
process vary. In this section, the degradation pathways that atrazine undergoes in various soil remediation processes, and
the intermediates and final products of these processes are investigated.
7. Metabolites during different methods of atrazine degradation
7.1. Non-thermal plasma
In the non-thermal plasma (NTP) technique, the isopropyl group is substantially preserved while ethyl-containing
species and chlorinated species are hard to find, unlike in the Fenton reagent solution, where desisopropylatrazine,
and desethylatrazine are by-products. This empirical fact of highly selective de-ethylation/de-chlorination of atrazine
mediators under non-thermal plasma treatment does not support · OH reactions as being the predominant ones at least
at the onset of atrazine degradation. These facts combined suggest that in the non-thermal plasma process the main
degradation-booster species may not be the OH· but a various species capable of elective reactions that are subject to
attaining proper transition situation geometry hence sensitive to residence time. These active species are most likely
singlet oxygen (1 O2 ). The 1 O2 is produced in significant amounts in the plasma system (Aggelopoulos et al., 2018; Sousa
et al., 2011; Takamatsu et al., 2014). Interpretation of ultraperformance liquid chromatography tandem mass spectrometry
(UPLC/MS) output data shows that atrazine degradation follows a logical pattern. Oligomeric products where the isopropyl
side chain is retained are first formed. Then the N-isopropyl group is oxidized to aminals and acetamides, like the
degradation pathway of atrazine by · OH species. Disruption stages of isopropyl oxidation mediators are observed. Finally,
complete degradation of the N-substituent occurs, either by hydrolysis of the amide group or by the nucleophilic addition
of water and displacement of the acetamido group. Fig. 1 shows the general processes that take place during the NTP
procedure on atrazine.
Since the deisopropylation process is fully compatible with the previously defined · OH pathways, oligomer formation
requires a different basis. Two logical mechanisms can be cited for the formation of these species, which are based on the
condensation and related reactions of desethylatrazine. In the first pathway, a nucleophilic attack on the atrazine carbon
atom carrying the halogen atom produces a DEA-ATZ and HCl dimer simultaneously. Selective de-ethylation of the dimer
product will produce a DEA-like derivative that may be compacted with further atrazine to produce a trimer and excess
HCl. Repeatedly, oligomers with preserved N-isopropyl groups will be formed through the DEA-ATZ condensation cycles
and the selective de-ethylation cycles of each compound. In the second pathway, desethylatrazine self-condensation is
equivalent to the polymerization reaction and shows a simpler process compared to the first pathway. But compared to
condensation with atrazine, it requires a significantly higher concentration of desethylatrazine and self-condensation. In
the early stages of the process, given that the reaction of the produced desethylatrazine with a large amount of ATZ, it
is expected that the first pathway is dominant. Both paths are good examples of autocatalysis since HCl by-products
accelerate desethylatrazine condensation by producing more excess HCl catalyst. The formation of desethylatrazine
oligomers refers to a rapid de-ethylation process that provides a sufficient concentration of desethylatrazine to compete
with soil and water for chloride replacement (Aggelopoulos et al., 2018).
12
Fig. 1. The process of NTP procedure on atrazine.
7.2. Photocatalysis
In the photocatalyst atrazine degradation method, the mineralization efficiency is usually much lower than the
degradation efficiency. This is due to the decomposition process during which organic mediators as hydroxyatrazine,
deethyldeisopropylatrazine, deisopropylatrazine, deethylatrazine, ammeline, and ammelide are formed, which are difficult
to fully mineralize (Parra et al., 2004). In the photocatalytic analysis of atrazine in the presence of · OH, the most important
product with the highest concentration is deethylatrazine. One of the important factors that can affect the atrazine
mineralization rate in the photocatalytic degradation method is the size of the photocatalyst particles. Sudrajat and
Sujaridworakun (2017) by changing the temperature of the photocatalyst synthesis, prepared nanoparticles in 4 different
sizes (11–27 nm) that the optimal mineralization efficiency (31.3%) was related to nanoparticles = 20.1 nm. In catalytic
degradation, complete mineralization is performed with the help of some photocatalysts such as S–TiO2 @rGO under light
irradiation (Khavar et al., 2018).
Zhang et al. (2018) reported, in the photodegradation of atrazine, the hydrated electrons react with protons and
dissolved oxygen due to the photoionization of indole-3-acetic acid, which improves the degradation of atrazine by
forming hydroxyl radicals. The primary products of this degradation are desethylatrazine and deisopropylatrazine, which
are the result of the breakage of the aliphatic side chain in the triazine ring due to the attack of hydroxyl radicals. The
results of mass spectrometry analysis also show the presence of 2-hydroxy-4-ethylamino-6-isopropylamino-s-triazine
(OIET).
7.3. Zero-valent Iron (ZVI)
In the degradation of atrazine using Zero-valent Iron (ZVI) nanoparticles, the most important by-product of the
decolorization process and the primary by-product of the ZVI reduction process is 2-ethylamino-4-isopropylamino-1,3,5-
triazine. The mechanism of acidic hydrolysis and reductive dechlorination in soil produces 2-hydroxy-4ethylamino-6-iso-
propylamino-1,3,5-triazine and 2-ethyl-amino-4-isopropylamino-1,3,5-triazine, respectively. Under anaerobic conditions,
atrazine can be degraded by reductive dechlorination followed by reductive alkylation (Satapanajaru et al., 2008).
13
Table 3
Atrazine derivatives and their abbreviations.
Compound Abbreviation
Atrazine ATZ
Desalkyl atrazine (diaminochlorotriazine) DAA
Desisopropyl atrazine DIA
Desethyl atrazine DEA
Desalkyl atrazine mercapturate DAA-Mer
Desisopropyl atrazine mercapturate DIA-Mer
Desethyl atrazine mercapturate DEA-Mer
Atrazine mercapturate ATZ-Mer
Desalkyl atrazine hydroxide DAA-OH
Desisopropyl atrazine hydroxide DIA-OH
Desethyl atrazine hydroxide DEA-OH
Atrazine hydroxide ATZ-OH
7.4. Bioremediation
Some fungi and bacteria can convert the atrazine molecule through alkylation and chlorination reactions to various
breakdown products i.e., Hydroxyatrazine, Desethylatrazine, and Desisopropylatrazine (Govantes et al., 2009). Microorgan-
isms and plants are subject to considerable selective pressure to complete metabolic processes that break down pollutants
into less toxic compounds (Madariaga-Navarrete et al., 2017).
Biodegradation of atrazine is usually performed under aerobic conditions by bacteria as Nocardia. These bacteria use
atrazine as the sole source of carbon and nitrogen, and form dealkylated and deaminated metabolites. A new metabolite
without phytotoxicity found as a result of these processes is 4-amino-2-chloro-1,3,5-triazine. None of these by-products
deethylatrazine, deisopropylatrazine, or deethyldeisopropylated atrazine were detected in degradation using Nocardia,
and only a small amount of 4-amino-2-chloro-1,3,5-triazine was found (Giardina et al., 1982). With bacterial isolation, we
cannot obtain atrazine mineralization. Measurement of atrazine and its metabolites in the soil showed that in the deeper
layers, deethylatrazine was found in higher amounts than deisopropylatrazine. It can be concluded that soil bacteria
preferably use the ethyl atrazine sub-chain (Ghosh and Philip, 2006).
In the treatment of atrazine contaminated soil using microbial inoculation (Pseudomonas sp. Strain), with concentra-
tions of 0.1 and 0.01 g kg−1 of biomass, metabolites of the maternal compound were observed during the experiment, but
no metabolites were visible until the end of the purification procedure. The identified metabolites were deethylatrazine
and deisopropylatrazine, which are metabolized by the N-dealkylation pathway.
The potential of bioremediation of three species of Pseudomonas sp. is compared in the degradation of atrazine. The
results showed that the ability of different species to dehalogenate intermediate metabolites in atrazine degradation is
different. Microbial dechlorination may occur in the soil following the removal of one or two alkyl atrazine groups (Behki
and Khan, 1986; Wenk et al., 1998). The four major metabolites of hydroxyatrazine, deisopropylatrazine, deethylatrazine,
and diaminochlorotriazine have been identified in methanol soil extracts from atrazine contaminated soils. Different
soil types have different effects on the formation of metabolites, mineralization, and microbial activity. After 250 days
of atrazine use, in acidified methanol extracts, two hydroxylated metabolites, 6-hydroxy-N-isopropyl-1,3,5-triazin-2-
ylamine, and N-ethyl- 6-hydroxy-1,3,5-triazin-2-ylamine were found. These metabolites had a higher tendency to be
adsorbed onto soil grains, which reduced the extraction efficiency with methanol (Assaf and Turco, 1994; Skipper and
Volk, 1972).
7.5. Phytoremediation
In investigating the phytoremediation potential of atrazine degradation by Sánchez et al. (2017) after phytoremedi-
ation, the atrazine residues (atrazine, deethylatrazine, and deisopropylatrazine) were measured. The amount of atrazine
in the soil sample in which phytoremediation was performed was significantly lower than in the control sample. Among
the degradation products of atrazine by phytoremediation, deethylatrazine was the most important known metabolite in
measurable concentrations in plant tissues, along with deisopropylatrazine.
Atrazine in plants and soil bacteria can be metabolized to hydroxyl derivatives such as Atrazine hydroxy (ATZ-OH),
desethyl hydroxy atrazine (DEA-OH), desisopropyl hydroxy atrazine (DIA-OH), and diamino hydroxy atrazine (DAA-OH).
In general, atrazine can be converted into 11 different intermediates and final compounds identified through various
processes. The names of these materials and their common acronyms are given in Table 3 (Kuklenyik et al., 2012). After
comparing the by- and end products of the various techniques used in soil remediation, by-products from the Fenton
process are generally biodegradable and less harmful (Baldissarelli et al., 2019).
14
8. Implementation of eco-technologies to remediate atrazine contaminated environments along with future

prospects
Due to the continually rising agricultural needs, the use of herbicides, for weed control has increased widely in
developing countries. Many farmers in developing countries still consider the use of herbicides to be the best way to
protect their crops from pests.
Laws restricting the use of atrazine are on the rise in many developing countries. Due to its harmful effects on animals,
humans, and entire ecosystems, extensive studies have been performed to find efficient ways to remove this substance.
However, to have a herbicide-free environment, efforts should be made to reduce the overall use of herbicides. Given the
great advances in plant science and genetic engineering, the production of weed-resistant plants can be considered a good
option to reduce the use of herbicides. In the meantime, different methods can be used to remove atrazine released into the
environment. The results of studies on the degradation of atrazine show that new physicochemical and biological methods
have high degradation efficiencies and can potentially be used on a large scale in the future. Therefore, transferring these
studies from the laboratory to the field is an essential step in reducing atrazine in the environment.
Recent technologies, using plants and microbes to degrade herbicides, especially when integrated into a synergistic
strategy of plant-microbial remediation, have been shown to be one of the best methods of atrazine degradation. Apart
from its efficiency, such action also improves the quality of contaminated soil for its future use. The physicochemical
approaches have the definite advantage of short treatment time. However, it is much more expensive to use in comparison
to biological methods and, in most cases, requires the treatment to be done ex-situ, which creates significant disruption
to the entire ecosystem and increases the operational cost. It is shown to be an excellent strategy for the remediation
of drinking water and water bodies but not soil. The chemical methods have similar disadvantages. They are effective,
but their cost is high, and there is an additional threat of atrazine and the chemical seep into deeper layers of soil and
groundwater. Thus, it has a limited number of actual applications. The biological methods take significantly more time
to be effective but are relatively low-cost and put little to no additional threat to the environment and the ecosystem.
Thus, screening for more efficient bacterial strains and plants is crucial to improve the time and the efficiency of biological
degradation.
9. Conclusions
Atrazine’s unique properties make it quite challenging to achieve high efficiency of its degradation using any one
method. Therefore, recent studies have shown that the combination of a few strategies and the synergistic treatment
using two or three approaches, at the same time could potentially become the future of herbicide treatment in the soil,
and future studies need to be focused on the synergistic application of a few technologies simultaneously. Moreover,
since most studies on the subject were performed in artificial soil and lab conditions, moving the research into the actual
environment will narrow the gaps between the efficiency of lab-made scenarios and actual practical application, which
will also make the prediction models more precise.
CRediT authorship contribution statement
Saeid Rostami: Wrote the manuscript. Shaghayegh Jafari: Wrote the manuscript. Zohre Moeini: Wrote the manuscript.
Marta Jaskulak: Wrote the manuscript. Leila Keshtgar: Edited the manuscript. Ahmad Badeenezhad: Edited the
manuscript. Abooalfazl Azhdarpoor: Edited the manuscript, Developed the theoretical framework. Majid Rostami:
Edited the manuscript, Developed the theoretical framework. Katarzyna Zorena: Edited the manuscript, Developed the
theoretical framework. Mansooreh Dehghani: Involved in planning, Supervised the work.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have
appeared to influence the work reported in this paper.
Acknowledgment
The authors would like to thank the Shiraz University of Medical Sciences, Shiraz, Iran.
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Environmental Technology & Innovation 24 (2021) 102019

Contents lists available at ScienceDirect

Environmental Technology & Innovation

Current methods and technologies for degradation of atrazine

1. Introduction – Atrazine and environmental contamination ............................................................................................................... 2

4.4. Plasma oxidation.......................................................................................................................................................................... 7

1. Introduction – Atrazine and environmental contamination

2. Biological effects of atrazine

3. Biological methods of atrazine degradation

3.1. Microbial remediation

(continued on next page)

3.4. Microbial electro-remediating cells

3.5. Novel bioorganic fertilizer for the degradation of atrazine

4. Chemical and physicochemical methods of atrazine degradation

4.4. Plasma oxidation

4.5. Electrokinetic process

4.6. Reversible electrokinetic adsorption barrier (REKAB)

4.7. Nano zero-valent iron

4.8. Activated carbon

4.9. Biochar adsorption

6. Pathways of atrazine degradation

(continued on next page)

(continued on next page)

7. Metabolites during different methods of atrazine degradation

7.1. Non-thermal plasma

Fig. 1. The process of NTP procedure on atrazine.

7.3. Zero-valent Iron (ZVI)

8. Implementation of eco-technologies to remediate atrazine contaminated environments along with future

CRediT authorship contribution statement

Declaration of competing interest

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