Recent Advances in Glyphosate Biodegradation

Download as pdf or txt
Download as pdf or txt
You are on page 1of 11

Applied Microbiology and Biotechnology

https://doi.org/10.1007/s00253-018-9035-0

MINI-REVIEW

Recent advances in glyphosate biodegradation


Hui Zhan 1 & Yanmei Feng 1 & Xinghui Fan 1 & Shaohua Chen 1

Received: 13 February 2018 / Revised: 16 April 2018 / Accepted: 17 April 2018


# Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract
Glyphosate has emerged as the most widespread herbicide to control annual and perennial weeds. Massive use of glyphosate for
decades has resulted in its ubiquitous presence in the environment, and poses a threat to humans and ecosystem. Different
approaches such as adsorption, photocatalytic degradation, and microbial degradation have been studied to break down glyph-
osate in the environment. Among these, microbial degradation is the most effective and eco-friendly method. During its degra-
dation, various microorganisms can use glyphosate as a sole source of phosphorus, carbon, and nitrogen. Major glyphosate
degradation pathways and its metabolites have been frequently investigated, but the related enzymes and genes have been rarely
studied. There are many reviews about the toxicity and fate of glyphosate and its major metabolite, aminomethylphosphonic acid.
However, there is lack of reviews on biodegradation and bioremediation of glyphosate. The aims of this review are to summarize
the microbial degradation of glyphosate and discuss the potential of glyphosate-degrading microorganisms to bioremediate
glyphosate-contaminated environments. This review will provide an instructive direction to apply glyphosate-degrading micro-
organisms in the environment for bioremediation.

Keywords Glyphosate . Biodegradation mechanism . Carbon-phosphorus lyase . Aminomethylphosphonicacid . Bioremediation

Introduction et al. 2012; Zhang et al. 2015). Massive use of glyphosate


is due to its efficient weeds elimination and development
Glyphosate [N-(phosphonomethyl)glycine], a synthetic of genetically modified glyphosate-resistant varieties of
phosphonate compound with stable carbon-phosphorus soybean, cotton, canola, and maize (Annett et al. 2014).
(C-P) bond (Fig. 1), is the active ingredient of broad spec- In 1996, first glyphosate-resistant soybean variety
trum, post-emergent, and non-selective systemic herbicide (Roundup Ready) was commercialized in the USA that
formulations like Roundup (Gill et al. 2016; Li et al. resulted in tremendous increase in glyphosate sales (Dill
2016; Norgaard et al. 2014). Henri Martin of Swiss phar- 2005). Glyphosate mode of action is unique and is the
maceutical company (Cliag) synthesized glyphosate mol- only herbicide that targets 5-enolpyruvyl-shikimate-3-
ecule but John. E. Franz of Monsanto conducted its initial phosphate synthase (EPSPS) without analogs, resulting
herbicidal tests in 1970 and commercialized in 1974 in the inhibition of aromatic amino acid biosynthesis in
(Duke and Powles 2008). Globally, glyphosate is one of shikimate pathway (Fig. 2) (Boocock and Coggins 1983;
the most widely used herbicides against annual and peren- Haslam 2014). EPSPS inhibition by glyphosate suppresses
nial weeds in agriculture, silviculture, urban areas, and the synthesis of necessary proteins and secondary metabolites,
domestic gardens (Van Stempvoort et al. 2014; Waiman and hinders the vital energy pathways in plants and soil mi-
croorganisms (Bai and Ogbourne 2016; Sviridov et al. 2015).
Glyphosate though considered safer as compared to other
herbicides, its extensive use poses chronic and remote hazards
* Shaohua Chen to humans and ecological environment (Sihtmäe et al. 2013;
shchen@scau.edu.cn
Wang et al. 2016). Improper application practices and
1
State Key Laboratory for Conservation and Utilization of Subtropical overspray result in its widespread presence in aquatic and
Agro-bioresources, Guangdong Province Key Laboratory of terrestrial environments (Hanke et al. 2010). Glyphosate binds
Microbial Signals and Disease Control, Integrative Microbiology
Research Centre, South China Agricultural University,
to soil particles and accumulates in the upper soil layer.
Guangzhou 510642, People’s Republic of China Therefore, it is often detected in groundwater, surface water,
Appl Microbiol Biotechnol

phytopathogenic fungi in the soil (Ermakova et al. 2010;


Hadi et al. 2013). Aminomethylphosphonic acid (AMPA)
(Fig. 1), the main metabolite of glyphosate or detergents deg-
radation, has also been frequently detected in surface water,
sediment and groundwater (Botta et al. 2009; Grandcoin et al.
Glyphosate 2017; Van Stempvoort et al. 2016). Several studies revealed
that AMPA slightly effects human erythrocytes in vitro
(Kwiatkowska et al. 2014) but can cause DNA and chromo-
somal damage in fish (Guilherme et al. 2014).
To eliminate glyphosate related health and environmental
risks, development of effective and eco-friendly bioremedia-
tion strategy is inevitable. Glyphosate can be degraded either
through biotic pathway or abiotic approaches such as adsorp-
tion, thermolysis, and photodegradation (Lund-HØie and
Friestad 1986). Recently, a combination of photocatalyst and
Aminomethylphosphonic acid ultraviolet (UV) light has emerged as a promising degra-
dation pathway for the treatment of pesticide pollutants.
Photocatalytic degradation system is capable of complete-
ly decomposing glyphosate into non-toxic products such
as carbon dioxide, inorganic ions, and water. Principal
mechanism is based on photocatalytic oxidation reaction
initiated by a highly reactive oxidant, hydroxyl radical
(Echavia et al. 2009; Manassero et al. 2010; Xu et al. 2011).
Major advantage of photocatalytic degradation is its efficiency
Sarcosine and cost-effectiveness along with non-toxicity, stability, and
low-price of the photocatalysts, whereas failing to control
O photocatalysis conditions in situ is the major drawback of this
O O technique. Generally, photocatalytic technology is applied to
degrade glyphosate in sewage treatment plant. Hence, it is
necessary to study glyphosate-degrading microorganisms as
P N microbial degradation is considered the most significant path-
HO OH way for glyphosate breakdown (Mercurio et al. 2014; Wang
HO et al. 2016). Different studies have reported effective and po-
Acetylglyphosate tential microorganisms for efficient and rapid bioremediation
Fig. 1 Chemical structures of glyphosate, aminomethylphosphonic acid, of glyphosate polluted environments. However, the literature
and sarcosine lacks reviews about the mechanism and pathway of different
glyphosate degrading strains. In this review, we aim to sum-
marize the glyphosate-degrading microbes along with their
and water-sediment from surface runoff, drift and vertical biodegradation mechanism, and analyze their bioremediation
transport in soil (Lupi et al. 2015; Newton et al. 1994; potential in glyphosate-contaminated environments.
Shushkova et al. 2010). Detection of glyphosate residues in
human urine samples concludes the increased exposure of
glyphosate to humans (Niemann et al. 2015). Glyphosate res- Microbial degradation of glyphosate
idues in humans never exceeded the threshold limit but its
Glyphosate-degrading microorganisms (Achromobacter sp.
negative effects cannot be conclusively denied. There is a re-
strain MPK 7A, Comamonas odontotermitis strain P2,
ported evidence that glyphosate contains carcinogenic contam-
Ochrobactrum intermedium strain Sq20 and Pseudomonas
inants and causes organ damage in non-mammalian species sp. strain 4ASW) had been previously isolated from con-
through oxidative stress and inhibition of acetylcholinesterase taminated sites by enrichment cultivation technique (Dick
(Mesnage et al. 2015). Glyphosate can also cause structural and Quinn 1995b; Ermakova et al. 2017; Firdous et al.
changes in local soil microbial communities by inhibiting the 2017a; Firdous et al. 2017b). Microbe derivatives such as
growth of soil microorganisms and facilitating the increase of Arthrobacter atrocyaneus ATCC 13752, Alcaligenes sp.
Appl Microbiol Biotechnol

Fig. 2 Glyphosate mode of action O


OH OH
in plants OH OH
O O P
P OH + O
+
OH O
O
OH
Phosphoenolpyruvate Erythrose-4-phosphate

DAHP Synthase

OH OH O
OH
O O-
P
OH
O OH O
3-deoxy-D-arainoheptulosonate-7-phosphate (DAHP)

DHQ Synthase

O O O- O O- O O-
OH O-

HO
O OH O OH HO OH O OH
P
OH OH OH HO OH
O
3-Dehydroquinate (DHQ) 3-Dehydroshikimate Shikimate Shikimate-3-phosphate

O O-
EPSPS

O-
inhibit
HO
O O
P
HO
O
OH O Glyphosate
5-Enolpyruvyl-shikimate-3-phosphate

O O-
Tyrosine

O- Phenylalanine
O

OH O
Chorismate Tryptophan

strain GL, Arthrobacter sp. strain GLP-1, Geobacillus most pivotal role (Bujacz et al. 1995; Hadi et al. 2013;
caldoxylosilyticus strain T20 and Pseudomonas sp. PG2982 Obojska et al. 1999). To assess the potential of glyphosate-
can utilize glyphosate as growth nutrient (Lerbs et al. 1990; degrading microorganisms for bioremediation, it is neces-
Moore et al. 1983; Obojska et al. 2002; Pipke and Amrhein sary to optimize their degradation conditions including
1988a; Pipke et al. 1987a). Among various glyphosate- initial pH, incubation temperature, glyphosate concentra-
degrading microorganisms (bacteria (Table 1), fungi tion, inoculation biomass and incubation time. Response
(Table 2), micromyces, and actinomycetes), bacteria play the surface methodology reveals that bacteria exhibit efficient
Appl Microbiol Biotechnol

Table 1 Glyphosate-degrading bacteria

Strain Source Gram Type of Detected metabolites Comments References


status degradation
pathway

Achromobacter Activated sludge from – AMPA pathway 1) AMPA 1. Utilization of glyphosate McAuliffe et al.
sp. LW9 glyphosate process as a sole carbon source in (1990)
waste stream presence of phosphate
Achromobacter Glyphosate-contaminated – Sarcosine pathway 1) Sarcosine 1. Utilization of glyphosate Ermakova et al.
sp. MPK 7A soil as sole phosphorus source (2017)
Achromobacter Methylphosphonic acid – Sarcosine pathway 1) Sarcosine 1. Utilization of glyphosate Sviridov et al.
sp. MPS 12A contaminated soil 2) Glycine as sole phosphorus source (2012)
3) Formaldehyde
Agrobacterium Sludge from water – Sarcosine pathway No data 1. Utilization of glyphosate Wackett et al. (1987)
radiobacter reatment (putative) as sole phosphorus source
plant in America
Agrobacterium Activated sludge from a – AMPA pathway 1) AMPA 1. Utilization of glyphosate McAuliffe et al.
radiobacter waste stream as a sole carbon source in (1990)
SW9 presence of phosphate
2. Capability of degrading
small amount of AMPA
Alcaligenes sp. Non-axenic cultures of the – Sarcosine pathway 1) Sarcosine 1. Utilization of glyphosate Lerbs et al. (1990)
GL cyanobacterium 2) Glycine as sole phosphorus source
Anacystisnidulans
Arthrobacter German collection of + AMPA pathway 1) AMPA 1. Utilization of glyphosate Pipke and Amrhein
atrocyaneus microorganisms and 2) CO2 as sole phosphorus source (1988a)
ATCC 13752 cell cultures 2. Capable of degrading glyphosate
per se without previous selection
culture
Arthrobacter sp. Accidental contaminant of + Sarcosine pathway 1) Phosphate 1. Utilization of glyphosate Pipke et al. (1987a)
GLP-1 Klebsiella pneumoniae 2) Glycine as sole phosphorus source
2. Capable of degrading glyphosate
per se without previous selection
culture
Arthrobacter sp. Mutant of Arthrobacter + Sarcosine pathway 1) Phosphate 1. Utilization of glyphosate Pipke and Amrhein
GLP-1/Nit-1 sp. GLP-1 as sole phosphorus source (1988b)
as well as sole nitrogen
source
Bacillus cereus Glyphosate-polluted soil + Both AMPA and 1) AMPA 1. Utilization of glyphosate Fan et al. (2012)
CB4 in sarcosine 2) Glyoxylate as sole phosphorus source
the herbicide plant, pathways 3) Sarcosine 2. 94.47% degradation in
China 4) Glycine 5 days under the optimal
5) Formaldehyde capacity
Comamonas Glyphosate-contaminated – Both AMPA and No data 1. Utilization of glyphosate as sole Firdous et al.
odontotermitis soil in Australia sarcosine carbon and phosphorus source (2017a)
P2 pathways 2. Complete degradation of
(putative) glyphosate (1.5 g/L) within
104 h
Enterobacter Rhizoplane of various – Sarcosine pathway 1) Sarcosine 1. Utilization of glyphosate Kryuchkova et al.
cloacae K7 plants 2) Glycine as sole phosphorus source (2014)
in Russia 2. 40% degradation of glyphosate
with initial 5 mM content
Enterobacter sp. Sandy soil from Algeria – No data No data No data Benslama and
Bisph2 Boulahrouf
(2016)
Flavobacterium Monsanto activated – AMPA pathway 1) AMPA 1. Utilization of glyphosate Balthazor and Hallas
sp. GD1 sludges 2) Phosphate as sole phosphorus source (1986)
Geobacillus Central heating system + AMPA pathway 1) AMPA 1. Utilization of glyphosate Obojska et al. (2002)
caldoxylosilyti- water 2) Glyoxylate as sole phosphorus source
cus T20
Ochrobactrum Glyphosate-contaminated – Both AMPA and 1) AMPA 1. Utilization of glyphosate Sviridov et al.
anthropi GPK3 soil sarcosine 2) Glyoxylate as sole phosphorus source (2012)
pathways 3) Sarcosine
4) Glycine
5) Formaldehyde
Ochrobactrum Glyphosate-contaminated – Sarcosine pathway 1) Sarcosine 1. Utilization of glyphosate as Firdous et al.
intermedium indigenous soil 2) Glycine sole carbon source (2017b)
Sq20
Appl Microbiol Biotechnol

Table 1 (continued)

Strain Source Gram Type of Detected metabolites Comments References


status degradation
pathway

2. Complete degradation of
glyphosate (500 mg/L) within
4 days
Ochrobactrum sp. Soil – AMPA pathway 1) AMPA 1. Utilization of glyphosate as Hadi et al. (2013)
GDOS sole phosphate source
2. Complete degradation (3 mM)
within 60 h
Pseudomonas Soil – AMPA pathway No data 1. Utilization of glyphosate as Peñaloza-Vazquez
pseudomallei (putative) sole phosphorus source et al. (1995)
22 2. 50% degradation in 40 h
Pseudomonas sp. Glyphosate-contaminated – Sarcosine pathway 1) Sarcosine 1. Utilization of glyphosate as Dick and Quinn
4ASW soil sole phosphorus source (1995)
Pseudomonas sp. Mutant of Pseudomonas – Sarcosine pathway No data 1. Utilization of glyphosate as Selvapandiyan and
GLC11 sp. PAO1 on selective sole phosphorus source Bhatnagar (1994)
medium
Pseudomonas sp. Activated sludge from – Both AMPA 1) AMPA 1. Utilization of glyphosate as Jacob et al. (1988)
LBr glyphosate process (95%) and 2) Glycine sole phosphorus source
waste stream sarcosine (5%) 2. Capable of removing
pathway 20 mM glyphosate from
growth medium
Pseudomonas sp. Pseudomonas aeruginosa – Sarcosine pathway 1) Sarcosine 1. Utilization of glyphosate Moore et al. (1983);
PG2982 ATCC 9027 2) Phosphate as sole phosphorus source Shinabarger and
3) Glycine Braymer (1986);
4) Formaldehyde Kishore and Jacob
(1987)
Pseudomonas sp. Aerobic digester liquid – AMPA pathway 1) AMPA 1. Utilization of glyphosate Talbot et al. (1984)
SG-1 as sole phosphorus source
2. Within 18 h, 2 g
(wet weight) of cells
degraded 0.9 mg of
glyphosate from a 30-ml reac-
tion mixture
Rhizobiaceae Mutant of Rhizobiaceae – Sarcosine pathway 1) Sarcosine 1. Utilization of glyphosate as Liu et al. (1991)
meliloti 1021 meliloti induced by 2) Glycine sole phosphorus source
transposon Tn5
mutagenesis which is
resistant to
streptomycin
Streptomycete sp. Raw sludge from a + Sarcosine pathway 1) Sarcosine 1. Utilization of glyphosate as sole Obojska et al. (1999)
StC municipal sewage 2) Glycine phosphorus, nitrogen or nitrogen
treatment plant and phosphorus source

glyphosate degradation ability under the optimum condi- glyphosate as their sole phosphorus source (Bujacz et al.
tions (Fan et al. 2012; Firdous et al. 2017a). 1995; Fu et al. 2017; Klimek et al. 2001;
As illustrated in Tables 1 and 2, Alcaligenes sp. strain GL, Krzyśko-Łupicka and Orlik 1997; Krzyśko-Lupicka
Arthrobacter sp. strain GLP-1, Flavobacterium sp. strain GD1 et al. 1997). However, several strains can use glyphosate
and Pseudomonas pseudomallei strain 22 utilize glyphosate as a s o t h e r ty p e s o f e n e rg y s o u r c e . F o r e x a m p l e ,
sole phosphorus source (Balthazor and Hallas 1986; Lerbs et al. Arthrobacter sp. GLP-1/Nit-1 (mutant of Arthrobacter
1990; Peñaloza-Vazquez et al. 1995; Pipke et al. 1987a). sp. GLP-1) can utilize glyphosate both as sole phosphorus
Similarly, Achromobacter sp. strain LW9, Agrobacterium source and sole nitrogen source (Pipke and Amrhein
radiobacter strain SW9, and Ochrobactrum intermedium strain 1988b); Comamonas odontotermitis P2 uses glyphosate
Sq20 utilize glyphosate as sole carbon or nitrogen source as sole carbon and phosphorus source (Firdous et al.
(Firdous et al. 2017b; McAuliffe et al. 1990). Most of the bac- 2017a); Streptomycete sp. StC utilizes glyphosate as sole
teria and fungi (Aspergillus niger, Aspergillus oryzae A-F02, phosphorus source, sole nitrogen source or sole nitrogen
Mucor IIIR, Penicillium IIR, Penicillium notatum, and sole phosphorus source (Obojska et al. 1999).
Scopulariopsis sp., Trichoderma harzianum) decompose Arthrobacter atrocyaneus ATCC 13752 spontaneously
Appl Microbiol Biotechnol

Table 2 Glyphosate-degrading fungi

Strain Source Type of degradation Detected Comments References


Pathway metabolites

Aspergillus niger Soil AMPA pathway 1) AMPA 1. Utilization of Krzyśko-Lupicka


glyphosate as et al. (1997)
sole phosphorus source
Aspergillus oryzae Aeration tank in a AMPA pathway 1) AMPA 1. Utilization of Fu et al. (2017)
A-F02 pesticide factory 2) Methylamine glyphosate as
sole phosphorus source
Mucor IIIR Sandy-clay soil in arable AMPA pathway 1) AMPA 1. Utilization of Krzyśko-Łupicka
land farm, Poland glyphosate and Orlik
as sole phosphorus (1997)
source
Penicillium IIR Sandy-clay soil in arable AMPA pathway 1) AMPA 1. Utilization of Krzyśko-Łupicka
land farm, Poland glyphosate and
as sole phosphorus Orlik (1997)
source
Penicillium Soil AMPA pathway No data 1. Utilization of Klimek et al.
chrysogenum (putative) glyphosate (2001)
as sole nitrogen source
Penicillium notatum Spontaneous growth on AMPA pathway 1) AMPA 1. Utilization of Bujacz et al.
a solid sample of glyphosate (1995)
hydroxyfluorenyl- as sole phosphorus
9-phosphonate source
Scopulariopsis sp. Soil AMPA pathway 1) AMPA 1. Utilization of Krzyśko-Lupicka
glyphosate et al. (1997)
as sole phosphorus
source
Trichoderma Soil AMPA pathway 1) AMPA 1. Utilization of Krzyśko-Lupicka
harzianum glyphosate et al. (1997)
as sole phosphorus
source

degraded glyphosate and AMPA without enrichment cul- (Jacob et al. 1988; Quinn et al. 1989) are known to utilize
tivation (Pipke and Amrhein 1988a). Flavobacterium sp. AMPA as Pi source. Unlike the AMPA pathway, isolates
GD1 can utilize both glyphosate and AMPA as a sole which metabolize glyphosate to sarcosine, completely de-
phosphorus source. Inorganic phosphorus (Pi) concentra- toxify glyphosate by utilizing sarcosine as their growth nutri-
tion had no effect on glyphosate metabolism but sup- ent. Some reports indicate that isolates such as Bacillus cereus
presses AMPA degradation process (Balthazor and Hallas CB4, Ochrobactrum anthropi GPK 3 and Pseudomonas sp.
1986). Pi inhibits several isolates such as Pseudomonas sp. LBr simultaneously convert glyphosate to AMPA and
PG2982 and Pseudomonas sp. GLC11 from utilizing glypho- sarcosine (Fan et al. 2012; Jacob et al. 1988; Sviridov et al.
sate as a sole phosphorus source (Kishore and Jacob 1987; 2012). Bacterial strains exhibiting significant degradation
Moore et al. 1983; Selvapandiyan and Bhatnagar 1994; ability provide a potential tool to bioremediate glyphosate-
Shinabarger and Braymer 1986). contaminated environments. Sequencing of glyphosate oxido-
To date, three main intermediate metabolites of glyph- reductase and carbon-phosphorus lyase (C-P lyase) genes, re-
osate metabolism AMPA, sarcosine, and acetylglyphosate veal that both pathways are concurrent in Comamonas
(Fig. 1) have been found which are further metabolized odontotermitis P2 (Firdous et al. 2017a). Another glyphosate
through different metabolism pathways. The most fre- metabolic process converts it to acetylglyphosate but isolates
quently detected metabolite of glyphosate degradation is cannot further utilize acetylglyphosate as a phosphorus
AMPA. Intracellular metabolism of AMPA is impossible source. Achromobacter sp. Kg 16 utilizes glyphosate as a sole
and is released to the environment resulting in secondary phosphorus source and transforms it into acetylglyphosate,
contamination (Balthazor and Hallas 1986; Jacob et al. but is unable to further utilize acetylglyphosate, thus leading
1988; Lerbs et al. 1990). Several bacterial strains such to its poor growth. Surprisingly, Achromobacter sp. Kg 16 can
as Bacillus megaterium 2BLW, Pseudomonas sp. metabolize glyphosate to AMPA in the absence of carbon
4ASW, Pseudomonas sp. 7B and Pseudomonas sp. LBr source in culture medium (Ermakova et al. 2017).
Appl Microbiol Biotechnol

Mechanism of glyphosate bacterial ATCC 13752, Arthrobacter sp. GLP-1, and Pseudomonas sp.
degradation LBr (Jacob et al. 1988; Pipke and Amrhein 1988a; Pipke et al.
1987a). Recently, another totally different AMPA degradation
Degradation pathways of glyphosate in bacteria pathway has been found in Ochrobactrum anthropi GPK3,
where it was metabolized to phosphonoformaldehyde by trans-
As mentioned above, conversions of glyphosate to AMPA aminase and then catabolized to formaldehyde by
and sarcosine are two major degradation pathways in phosphonatase (Sviridov et al. 2014).
glyphosate-degrading microorganisms. Bacterial biodeg- Second glyphosate degradation pathway catalyzed by
radation mechanism of glyphosate includes (i) cleavage C-P lyase produces sarcosine and Pi. Pseudomonas sp.
of carboxymethylene-nitrogen (C-N) bond, catalyzed by PG2982 decomposes glyphosate via C-P lyase pathway
an oxidase yielding AMPA and glyoxylate; and (ii) direct with the formation of sarcosine which is further metabo-
cleavage of carbon-phosphorus (C-P) bond, catalyzed by lized by sarcosine oxidase to glycine and formaldehyde
C-P lyase yielding sarcosine. Both of the degradation (Kishore and Jacob 1987; Shinabarger and Braymer
pathways may involve C-P lyase to break C-P bond in 1986). Arthrobacter sp. GLP-1 utilizes glycine for protein
AMPA molecule. biosynthesis by inducing the formation of peptide back-
First major step in the degradation pathway of glypho- bone and amino acids (serine and threonine). According
sate, catalyzed by glyphosate oxidoreductase, is the for- to Pipke et al. (1987a), one-carbon compound combined
mation of AMPA and glyoxylate. Pseudomonas sp. LBr with tetrahydrofolic, biosynthesis nucleic acids (purine
metabolizes glyphosate via AMPA and glycine pathway and thymine), and proteins (serine, cysteine, methionine,
with 5% conversion of glyphosate to glycine and formal- and histidine). The fate of glyphosate biodegradation me-
dehyde. Solid-state 13C NMR revealed that isolate utilized tabolites has been clearly traced by isotope labeling.
glyoxylate and formaldehyde for its growth (Jacob et al. Degradation pathways of glyphosate in bacteria are sum-
1988). Arthrobacter atrocyaneus ATCC 13752 catabo- marized in Fig. 3.
lized glyphosate to AMPA and CO2, whereas CO2 was
not the product of AMPA (Pipke and Amrhein 1988a). Enzymes of glyphosate metabolism in bacteria
Intermediate metabolite AMPA can be either excreted to
the environment because of its bacterial toxicity or further Glyphosate oxidoreductase (GOX) is the key enzyme of
metabolized by different enzymes (Jacob et al. 1988; glyphosate degradation to AMPA via C-N bond cleavage.
Pipke and Amrhein 1988a; Sviridov et al. 2012). AMPA most- GOX-encoding genes have been identified in Ochrobactrum
ly serves as a substrate of C-P lyase, producing methylamine sp. G1 (GU214711.1), Ochrobactrum anthropi GPK 3 and
and Pi as a phosphorus source for Arthrobacter atrocyaneus Comamonas odontotermitis P2 (KX980206.1) with 99%

O
O O
O
P O
Environment HO
Phosphonatase P
P +
HO HO OH H H
HO OH
+ H2N CH3 HO
HO H
Phosphate Methylamine Phosphonoformaldehyde Phosphate Formaldehyde
Excretion
C-P lyase Transaminase

O
O
Tetrahydrofolate cycle
H Tricarboxylic acid cycle
P NH2 OH CO2
HO +
Glyphosate HO O
oxidoreductase AMPA Glyoxylate

O
O O Microbial biosynthesis
O O
and metabolism
P NH
HO OH P N
HO HO OH
Glyphosate HO
Acetylglyphosate
Tetrahydrofolate cycle

O
C-P lyase O O
O
P Sarcosine
HO OH + NH oxidase
OH H2N +
HO H H
OH
Phosphate Sarcosine Glycine Formaldehyde

Fig. 3 Degradation pathways of glyphosate in bacteria


Appl Microbiol Biotechnol

similarity, and partial GOX gene in Comamonas Generally, glyphosate biodegradation to AMPA is not sub-
odontotermitis P2 product enzyme (ATE50174.1). There is a jected to Pi concentration, except in Arthrobacter atrocyaneus
synthetic construct between GOX (ADV58259.1) and GOX ATCC 13752 where glyphosate degradation was repressed by
gene (HQ110097.1) that has been used as a transgene in Pi (Pipke and Amrhein 1988a). However, glyphosate metabolic
glyphosate-tolerant canola (Duke 2010; Hadi et al. 2012). conversion to sarcosine seems to be regulated by the Pi concen-
However, purified GOX enzymes, either from a microorgan- tration. For example, glyphosate degradation was suppressed in
ism or the product enzyme from cloned gox gene, exhibit low the presence of Pi in Arthtobacter sp. (Pipke et al. 1987b) and
affinity to glyphosate (Hove-Jensen et al. 2014; Sviridov et al. Pseudomonas sp. 4ASW (Dick and Quinn 1995a). The trans-
2014). GOX purified from Ochrobactrum anthropi GPK 3, port system in glyphosate-degrading microorganisms for
containing flavin adenine dinucleotide (FAD), belongs to bac- glyphosate uptake is likely to depend on Pi level (Hove-
terial flavin monooxygenase superfamily (Sviridov 2012). Jensen et al. 2014). In addition, C-P lyase activity is controlled
Two open reading frames glpA and glpB related to glyphosate by phn genes which are upregulated in Pi absence (Metcalf and
utilization have been found in Pseudomonas pseudomallei 22. Wanner 1993b). Therefore, it can be assumed that Pi level
Specifically, glpA is related to the glyphosate tolerance, and affects the sarcosine pathway of glyphosate degradation.
glpB is associated with the conversion of glyphosate to Besides, PhoR-PhoB-based two-component system responds
AMPA which is a substrate of Escherichia coli C-P lyase to the exogenous and endogenous Pi concentrations in E.coli
(Peñaloza-Vazquez et al. 1995). (Santos-beneit 2015).
Till now, four C-P bond catabolic enzymes including C-P
lyase, phosphonoacetaldehyde hydrolase, phosphonoacetate Bioremediation potential of glyphosate-degrading
hydrolase and phosphoenolpyruvate hydrolase have been microorganisms
characterized in bacteria (Villarreal-Chiu et al. 2012).
However, only C-P lyase can split C-P bond of glyphosate Bioremediation refers to the transformation of pollutants into
whereas the other three enzymes are highly specific to their less toxic compounds by using microorganisms and their deg-
own substrate (Bujacz et al. 1995). Glyphosate C-P bond is radation enzymes (Chen et al. 2012; Liu et al. 2015; Sharma
hydrolytically stable and resistant to chemolysis and photoly- et al. 2018; Zhan et al. 2018). Bioremediation is supposed to
sis. Consequently, C-P lyase complex with high specificity to be more promising for the removal of chemical pollutants in
glyphosate is essential for glyphosate degradation via cleav- water and soil environment. Microorganisms and their
age of inactivated C-P bond and formation of sarcosine. C-P enzymes-based bioremediation of contaminated environments
lyase complex, which can metabolize a wide variety of differ- are efficient, safe and cost-effective (Chen et al. 2011a, b;
ent phosphonates, has been adequately studied in E.coli Karigar and Rao 2011; Xiao et al. 2015). Under natural con-
(Kamat and Raushel 2013). E.coli C-P lyase complex is the ditions, degradation of glyphosate in the soil depends on mi-
product of 14 genes operon (phnCDEFGHIJKLMNOP), crobial degradation. Hence, it is necessary to identify
which is a part of Pho regulon (Chen et al. 1990; Metcalf glyphosate-degrading microorganisms and confirm their po-
and Wanner 1993a, 1993b). According to previous genetic tential for the bioremediation of glyphosate-contaminated en-
and biochemical studies, phnCDE encode an ATP-binding vironments. Though plentiful glyphosate-degrading microor-
cassette transporter and the gene product PhnF is a repressor ganisms have been isolated, their ability to remediate
protein (Hove-Jensen et al. 2010; Hovejensen et al. 2011; glyphosate-contaminated environments still remains a conun-
Metcalf and Wanner 1993b). Seven proteins (PhnG, PhnH, drum because of low efficiency in situ and in vitro. Potent
PhnI, PhnJ, PhnK, PhnL, and PhnM) are supposed to consti- glyphosate-degrading microorganisms should be available
tute the core components of the membrane-bound C-P lyase, both in liquid media and soil. Potential of glyphosate-
metabolizing phosphonates to phosphate by PhnJ catalyst degrading microorganisms for glyphosate-contaminated soils
(Hovejensen et al. 2011; Metcalf and Wanner 1993b). remediation has only been studied in only a few bacteria.
Furthermore, PhnNOP is considered to perform regulatory Strain Bacillus subtilis Bs-15 degraded 66.97% of 5000 mg/L
and accessory functions in C-P lyase catabolic metabolism glyphosate in sterile soil and 71.57% of glyphosate in the un-
reaction (Hovejensen et al. 2011; Metcalf and Wanner sterilized soil that shows its bioremediation potential for
1993b). However, purified and characterized C-P lyase could glyphosate-contaminated soils and microbial diversity in the
not split the glyphosate C-P bond. To date, the C-P lyase with soil (Yu et al. 2015). Introduction of Achromobacter sp. Kg16
high-specificity to glyphosate has not been clearly character- and Ochrobactrum anthropi GPK3 strains to the soil
ized at genetic and biochemistry level (Sviridov et al. 2014). remediated glyphosate-treated soil within 1 to 2 weeks, show-
There is another non-specific glyphosate C-P lyase which can ing 2–3 folds higher degradation rate as compared to endoge-
split C-P bond of AMPA for further degradation. Hence, prob- nous microorganisms (Ermakova et al. 2010).
ably two different C-P lyases with different substrate specific- Additionally, many glyphosate-degrading bacterial
ity co-exist in one bacterium. strains via sarcosine pathway effectively degraded
Appl Microbiol Biotechnol

glyphosate only under laboratory conditions, because of Funding This study was partially funded by grants from the National
Natural Science Foundation of China (31401763), the National Key
C-P lyase catalysis inhibition by Pi concentrations in the
Project for Basic Research (2015CB150600), Guangdong Natural
natural environment. Persistence of inter-metabolite Science Funds for Distinguished Young Scholar (2015A030306038),
AMPA in the soil also contaminates the environment, the Science and Technology Planning Project of Guangdong Province
and thus microbes that are either unable to utilize (2016A020210106, 2017A010105008) and Pearl River S&T Nova
Program of Guangzhou (201506010006).
AMPA or excrete it cannot be used for bioremediation
of glyphosate-contaminated environment.
Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict of


Conclusion and future perspectives interest.

Excessive use of glyphosate also plays a vital role to Ethical approval This article does not contain any studies with human
achieve maximum crop yield and rapid agricultural devel- participants or animals performed by any of the authors.
opment. However, due to its intensive use, glyphosate
contamination has emerged as an urgent issue. The invet-
erate negative effects of glyphosate on the environment References
should attract considerable attention to remove glyphosate
residues from the polluted environments. Recently, photo- Annett R, Habibi HR, Hontela A (2014) Impact of glyphosate and glyph-
osate-based herbicides on the freshwater environment. J Appl
catalytic technology has been developed to efficiently de-
Toxicol 34(5):458–479
grade glyphosate but because of uncontrollable reaction Bai SH, Ogbourne SM (2016) Glyphosate: environmental contamination,
conditions, it is not suitable against glyphosate residues toxicity and potential risks to human health via food contamination.
in situ. Hence, the glyphosate-degrading microorganisms Environ Sci Pollut Res 23(19):18988–19001
having efficient degradation and bioremediation potentials Balthazor TM, Hallas LE (1986) Glyphosate-degrading microorganisms
from industrial activated sludge. Appl Environ Microbiol 51(2):
in glyphosate-contaminated environments are considered 432–434
as the most promising strategy. Hitherto, varieties of mi- Benslama O, Boulahrouf A (2016) High-quality draft genome sequence
croorganisms have been characterized to degrade glypho- of Enterobacter sp. Bisph2, a glyphosate-degrading bacterium iso-
sate by utilizing glyphosate as sole phosphorus, carbon or lated from a sandy soil of Biskra, Algeria. Genomics Data 8:61–66
nitrogen source. However, genetic and biochemical as- Boocock MR, Coggins JR (1983) Kinetics of 5-enolpyruvylshikimate-3-
phosphate synthase inhibition by glyphosate. FEBS Lett 154(1):
pects of highly efficient degrading enzymes have yet not 127–133
been properly explored. Most of the glyphosate-degrading Botta F, Lavison G, Couturier G, Alliot F, Moreau-Guigon E, Fauchon N,
isolates are bacteria in which complete degradation path- Guery B, Chevreuil M, Blanchoud H (2009) Transfer of glyphosate
way has been clearly understood. The most prevalent and its degradate AMPA to surface waters through urban sewerage
systems. Chemosphere 77(1):133–139
glyphosate degradation pathway in bacterial strains is
Bujacz B, Wieczorek P, Krzysko-Lupicka T, Golab Z, Lejczak B,
the cleavage of C-N bond and conversion to AMPA which Kavfarski P (1995) Organophosphonate utilization by the wild-
is either further decomposed or excreted to the environ- type strain of Penicillium notatum. Appl Environ Microbiol 61(8):
ment. Cleavage of C-P bond catalyzed by C-P lyase is 2905–2910
negatively regulated by Pi supply. In order to deal with Chen CM, Ye QZ, Zhu ZM, Wanner BL, Walsh CT (1990) Molecular
biology of carbon-phosphorus bond cleavage. Cloning and sequenc-
glyphosate contamination in the environment, the poten- ing of the phn (psiD) genes involved in alkylphosphonate uptake
tial of degrading microbes and enzymes for bioremedia- and C-P lyase activity in Escherichia coli B. J Biol Chem 265(8):
tion is worth studying. Generally, microbial community 4461–4471
has great potential for glyphosate degradation as com- Chen S, Lai KP, Li Y, Hu M, Zhang Y, Zeng Y (2011a) Biodegradation of
deltamethrin and its hydrolysis product 3-phenoxybenzaldehyde by
pared to single isolate. Therefore, collective degradation a newly isolated Streptomyces aureus strain HP-S-01. Appl
by various degrading microbes can be more effective Microbiol Biotechnol 90:1471–1483
against glyphosate residues. Moreover, to understand the Chen S, Yang L, Hu M, Liu J (2011b) Biodegradation of fenvalerate and
degradation mechanism, studying the role of functional 3-phenoxybenzoic acid by a novel Stenotrophomonas sp. strain ZS-
S-01 and its use in bioremediation of contaminated soils. Appl
genes and enzymes in bioremediation of glyphosate-
Microbiol Biotechnol 90:755–767
contaminated environments is crucial. Although a large Chen S, Geng P, Xiao Y, Hu M (2012) Bioremediation of β-cypermethrin
number of glyphosate degrading microorganisms have and 3-phenoxybenzaldehyde contaminated soils using Streptomyces
been isolated and characterized yet only a few have been aureus HP-S-01. Appl Microbiol Biotechnol 94:505–515
explored for their functional genes and enzymes. Therefore, Dick RE, Quinn JP (1995) Control of glyphosate uptake and metab-
olism in Pseudomonas sp. 4ASW. FEMS Microbiol Lett
before the large-scale application of glyphosate-degrading mi- 134(2–3):177–182
croorganisms for bioremediation, detailed foundation work Dill GM (2005) Glyphosate-resistant crops: history, status and future.
should be accomplished. Pest Manag Sci 61(3):219–224
Appl Microbiol Biotechnol

Duke SO (2010) Glyphosate degradation in glyphosate-resistant and-sus- Kamat SS, Raushel FM (2013) The enzymatic conversion of
ceptible crops and weeds. J Agric Food Chem 59(11):5835–5841 phosphonates to phosphate by bacteria. Curr Opin Chem Biol
Duke SO, Powles SB (2008) Glyphosate: a once‐in‐a‐century herbicide. 17(4):589–596
Pest Manage Sci 64(4):319–325 Karigar CS, Rao SS (2011) Role of microbial enzymes in the bioremedi-
Echavia GR, Matzusawa F, Negishi N (2009) Photocatalytic degradation ation of pollutants: a review. Enzym Res 7:805187
of organophosphate and phosphonoglycine pesticides using TiO2 Kishore G, Jacob GS (1987) Degradation of glyphosate by Pseudomonas
immobilized on silica gel. Chemosphere 76(5):595–600 sp. PG2982 via a sarcosine intermediate. J Biol Chem 262(25):
Ermakova IT, Kiseleva NI, Shushkova T, Zharikov M, Zharikov GA, 12164–12168
Leontievsky AA (2010) Bioremediation of glyphosate- Klimek M, Lejczak B, Kafarski P, Forlani G (2001) Metabolism of the
contaminated soils. Appl Microbiol Biotechnol 88(2):585–594 phosphonate herbicide glyphosate by a non-nitrate-utilizing strain of
Ermakova IT, Shushkova TV, Sviridov AV, Zelenkova NF, Vinokurova Penicillium chrysogenum. Pest Manag Sci 57(9):815–821
NG, Baskunov BP, Leontievsky AA (2017) Organophosphonates Kryuchkova YV, Burygin GL, Gogoleva NE, Gogolev YV, Chernyshova
utilization by soil strains of Ochrobactrum anthropi and MP, Makarov OE, Fedorov EE, Turkovskaya OV (2014) Isolation
Achromobacter sp. Arch Microbiol 199(5):665–675 and characterization of a glyphosate-degrading rhizosphere strain,
Enterobacter cloacae K7. Microbiol Res 169(1):99–105
Fan J, Yang G, Zhao H, Shi G, Geng Y, Hou T, Tao K (2012) Isolation,
Krzyśko-Łupicka T, Orlik A (1997) The use of glyphosate as the sole source
identification and characterization of a glyphosate-degrading bacterium,
of phosphorus or carbon for the selection of soil-borne fungal strains
Bacillus cereus CB4, from soil. J Gen Appl Microbiol 58(4):263–271
capable to degrade this herbicide. Chemosphere 34(12):2601–2605
Firdous S, Iqbal S, Anwar S (2017a) Optimization and modeling of Krzyśko-Lupicka T, Strof W, Kubś K, Skorupa M, Wieczorek P, Lejczak
glyphosate biodegradation by a novel Comamonas odontotermitis B, Kafarski P (1997) The ability of soil-borne fungi to degrade
P2 through response surface methodology. Pedosphere. https://doi. organophosphonate carbon-to-phosphorus bonds. Appl Microbiol
org/10.1016/S1002-0160(17)60381-3 Biotechnol 48(4):549–552
Firdous S, Iqbal S, Anwar S, Jabeen H (2017b) Identification and analysis Kwiatkowska M, Huras B, Bukowska B (2014) The effect of metabolites
of 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene and impurities of glyphosate on human erythrocytes (in vitro). Pestic
from glyphosate resistant Ochrobactrum intermedium Sq20. Pest Biochem Phys 109:34–43
Manage Sci 74:1184–1196. https://doi.org/10.1002/ps.4624 Lerbs W, Stock M, Parthier B (1990) Physiological aspects of glyphosate
Fu GM, Chen Y, Li RY, Yuan XQ, Liu CM, Li B, Wan Y (2017) Pathway degradation in Alcaligenes sp. strain GL. Arch Microbiol 153(2):
and rate-limiting step of glyphosate degradation by Aspergillus 146–150
oryzae A-F02. Prep Biochem Biotechnol 47(8):782–788 Li H, Joshi SR, Jaisi DP (2016) Degradation and isotope source tracking
Gill JPK, Sethi N, Mohan A (2016) Analysis of the glyphosate herbicide of glyphosate and aminomethylphosphonic acid. J Agric Food
in water, soil and food using derivatising agents. Environ Chem Lett Chem 64(3):529–538
15(1):85–100 Liu CM, McLean P, Sookdeo C, Cannon F (1991) Degradation of the
Grandcoin A, Piel S, Baures E (2017) Amino methyl phosphonic acid herbicide glyphosate by members of the family rhizobiaceae. Appl
(AMPA) in natural waters: its sources, behavior and environmental Environ Microbiol 57(6):1799–1804
fate. Water Res 117:187–197 Liu J, Chen S, Ding J, Xiao Y, Han H, Zhong G (2015) Sugarcane
Guilherme S, Santos MA, Gaivao I, Pacheco M (2014) DNA and chro- bagasse as support for immobilization of Bacillus pumilus HZ-2
mosomal damage induced in fish (Anguilla anguilla L.) by and its use in bioremediation of mesotrione-contaminated soils.
aminomethylphosphonic acid (AMPA)—the major environmental Appl Microbiol Biotechnol 99(24):10839–10851
breakdown product of glyphosate. Environl Sci Pollut Res 21(14): Lund-HØie K, Friestad HO (1986) Photodegradation of the herbicide
8730–8739 glyphosate in water. Bull Environ Contam Toxicol 36(1):723–729
Hadi F, Mousavi A, Salmanian AH, Akbari Noghabi K (2012) Lupi L, Miglioranza KS, Aparicio VC, Marino D, Bedmar F, Wunderlin
Glyphosate tolerance in transgenic canola by a modified glyphosate DA (2015) Occurrence of glyphosate and AMPA in an agricultural
oxidoreductase (gox) gene. Prog Biol Sci 2(1):50–58 watershed from the southeastern region of Argentina. Sci Total
Hadi F, Mousavi A, Noghabi KA, Tabar HG, Salmanian AH (2013) New Environ 536:687–694
bacterial strain of the genus Ochrobactrum with glyphosate- Manassero A, Passalia C, Negro AC, Cassano AE, Zalazar CS (2010)
degrading activity. J Environ Sci Heal B 48(3):208–213 Glyphosate degradation in water employing the H2O2/UVC process.
Hanke I, Wittmer I, Bischofberger S, Stamm C, Singer H (2010) Water Res 44(13):3875–3882
Relevance of urban glyphosate use for surface water quality. McAuliffe KS, Hallas LE, Kulpa CF (1990) Glyphosate degradation by
Chemosphere 81(3):422–429 Agrobacterium radiobacter isolated from activated sludge. J Ind
Microbiol Biotechnol 6(3):219–221
Haslam E (2014) The shikimate pathway: biosynthesis of natural prod-
Mercurio P, Flores F, Mueller JF, Carter S, Negri AP (2014) Glyphosate
ucts series. Elsevier, New York
persistence in seawater. Mar Pollut Bull 85(2):385–390
Hovejensen B, Mcsorley FR, Zechel DL (2011) Physiological role of
Mesnage R, Defarge N, Spiroux de Vendomois J, Seralini GE (2015)
phnP-specified phosphoribosyl cyclic phosphodiesterase in catabo-
Potential toxic effects of glyphosate and its commercial formulations
lism of organophosphonic acids by the carbon-phosphorus lyase
below regulatory limits. Food Chem Toxicol 84:133–153
pathway. J Am Chem Soc 133(10):3617–3624
Metcalf WW, Wanner BL (1993) Evidence for a fourteen-gene, phnC to
Hove-Jensen B, Rosenkrantz TJ, Zechel DL, Willemoës M (2010) phnP locus for phosphonate metabolism in Escherichia coli. Gene
Accumulation of intermediates of the carbon-phosphorus lyase path- 129(1):27–32
way for phosphonate degradation in phn mutants of Escherichia Moore JK, Braymer HD, Larson AD (1983) Isolation of a Pseudomonas
coli. J Bacteriol 192(1):370–374 sp. which utilizes the phosphonate herbicide glyphosate. Appl
Hove-Jensen B, Zechel DL, Jochimsen B (2014) Utilization of glypho- Environ Microbiol 46(2):316–320
sate as phosphate source: biochemistry and genetics of bacterial Newton M, Horner LM, Cowell JE, White DE, Cole EC (1994)
carbon-phosphorus lyase. Microbiol Mol Biol Res 78(1):176–197 Dissipation of glyphosate and aminomethylphosphonic acid in north
Jacob G, Garbow J, Hallas L, Kimack N, Kishore G, Schaefer J (1988) American forests. J Agric Food Chem 42(8):1795–1802
Metabolism of glyphosate in Pseudomonas sp. strain LBr. Appl Niemann L, Sieke C, Pfeil R, Solecki R (2015) A critical review of
Environ Microbiol 54(12):2953–2958 glyphosate findings in human urine samples and comparison
Appl Microbiol Biotechnol

with the exposure of operators and consumers. J Verbr glyphosate and methylphosphonate catabolism systems in soil bac-
Lebensm 10(1):3–12 teria Ochrobactrum anthropi and Achromobacter sp. Appl
Norgaard T, Moldrup P, Ferré TPA, Olsen P, Rosenbom AE, de Jonge LW Microbiol Biotechnol 93(2):787–796
(2014) Leaching of glyphosate and aminomethylphosphonic acid Sviridov A, Shushkova T, Ermakova I, Ivanova E, Leontievsky A (2014)
from an agricultural field over a twelve-year period. Vadose Zone Glyphosate: safety risks, biodegradation, and bioremediation.
J 13(10):10–13 Current environmental issues and challenges. Springer, Dordrecht,
Obojska A, Lejczak B, Kubrak M (1999) Degradation of phosphonates by pp 183–195
Streptomycete isolates. Appl Microbiol Biotechnol 51(6):872–876 Sviridov AV, Shushkova TV, Ermakova IT, Ivanova EV, Epiktetov DO,
Obojska A, Ternan NG, Lejczak B, Kafarski P, McMullan G Leontievsky AA (2015) Microbial degradation of glyphosate herbi-
(2002) Organophosphonate utilization by the thermophile cides (review). Appl Biochem Microbiol 51(2):188–195
Geobacillus caldoxylosilyticus T20. Appl Environ Microbiol Talbot HW, Johnson LM, Munnecke DM (1984) Glyphosate utilization
68(4):2081–2084 by Pseudomonas sp. and Alcaligenes sp. isolated from environmen-
Peñaloza-Vazquez A, Mena GL, Herrera-Estrella L, Bailey AM (1995) tal sources. Curr Microbiol 10(5):255–259
Cloning and sequencing of the genes involved in glyphosate utili- Van Stempvoort DR, Roy JW, Brown SJ, Bickerton G (2014) Residues of
zation by Pseudomonas pseudomallei. Appl Environ Microbiol the herbicide glyphosate in riparian groundwater in urban catch-
61(2):538–543 ments. Chemosphere 95:455–463
Pipke R, Amrhein N (1988a) Degradation of the phosphonate herbicide Van Stempvoort DR, Spoelstra J, Senger ND, Brown SJ, Post R, Struger J
glyphosate by Arthrobacter atrocyaneus ATCC 13752. Appl (2016) Glyphosate residues in rural groundwater, Nottawasaga
Environ Microbiol 54(5):1293–1296 River watershed, Ontario, Canada. Pest Manag Sci 72(10):1862–
Pipke R, Amrhein N (1988b) Isolation and characterization of a mutant of 1872
Arthrobacter sp. strain GLP-1 which utilizes the herbicide glypho-
Villarreal-Chiu JF, Quinn JP, McGrath JW (2012) The genes and en-
sate as its sole source of phosphorus and nitrogen. Appl Environ
zymes of phosphonate metabolism by bacteria, and their distribution
Microbiol 54(11):2868–2870
in the marine environment. Front Microbiol 3:19
Pipke R, Amrhein N, Jacob GS, Schaefer J, Kishore GM (1987a)
Wackett LP, Shames SL, Venditti CP, Walsh CT (1987) Bacterial carbon-
Metabolism of glyphosate in an Arthrobacter sp. GLP-1. FEBS J
phosphorus lyase: products, rates, and regulation of phosphonic and
165(2):267–273
phosphinic acid metabolism. J Bacteriol 169(2):710–717
Pipke R, Schulz A, Amrhein N (1987b) Uptake of glyphosate by an
Waiman CV, Avena MJ, Garrido M, Fernández Band B, Zanini GP
Arthrobacter sp. Appl Environ Microbiol 53(5):974
(2012) A simple and rapid spectrophotometric method to quantify
Quinn JP, Peden JM, Dick RE (1989) Carbon-phosphorus bond cleavage
the herbicide glyphosate in aqueous media. Application to adsorp-
by Gram-positive and Gram-negative soil bacteria. Appl Microbiol
tion isotherms on soils and goethite. Geoderma 170:154–158
Biotechnol 31(3):283–287
Santos-beneit F (2015) The Pho regulon: a huge regulatory network in Wang S, Seiwert B, Kastner M, Miltner A, Schaffer A, Reemtsma T, Yang
bacteria. Front Micribiol 6:402 Q, Nowak KM (2016) (Bio)degradation of glyphosate in water-
Selvapandiyan A, Bhatnagar RK (1994) Isolation of a glyphosate- sediment microcosms—a stable isotope co-labeling approach.
metabolising Pseudomonas: detection, partial purification and Water Res 99:91–100
localisation of carbon-phosphorus lyase. Appl Microbiol Xiao Y, Chen S, Gao Y, Hu W, Hu M, Zhong G (2015) Isolation of a
Biotechnol 40(6):876–882 novel beta-cypermethrin degrading strain Bacillus subtilis BSF01
Sharma B, Dangi AK, Shukla P (2018) Contemporary enzyme based and its biodegradation pathway. Appl Microbiol Biotechnol 99:
technologies for bioremediation: a review. J Environ Manage 210: 2849–2859
10–22 Xu X, Ji F, Fan Z, He L (2011) Degradation of glyphosate in soil
Shinabarger DL, Braymer HD (1986) Glyphosate catabolism by photocatalyzed by Fe 3 O 4 /SiO 2 /TiO 2 under solar light. Int J
Pseudomonas sp. strain PG2982. J Bacteriol 168(2):702–707 Environ Res Public Health 8(4):1258–1270
Shushkova T, Ermakova I, Leontievsky A (2010) Glyphosate bioavail- Yu XM, Yu T, Yin GH, Dong QL, An M, Wang HR, Ai CX
ability in soil. Biodegradation 21(3):403–410 (2015) Glyphosate biodegradation and potential soil bioreme-
Sihtmäe M, Blinova I, Künnis-Beres K, Kanarbik L, Heinlaan M, Kahru diation by Bacillus subtilis strain Bs-15. Genet Mol Res
A (2013) Ecotoxicological effects of different glyphosate formula- 14(4):14717–14730
tions. Appl Soil Ecol 72:215–224 Zhan H, Wang H, Liao L, Feng Y, Fan X, Zhang L, Chen S (2018)
Sviridov A (2012) Enzyme systems of organophosphonate catabolism of Kinetics and novel degradation pathway of permethrin in
soil bacteria Achromobacter sp. and Ochrobactrum anthropi GPK3. Acinetobacter baumannii ZH-14. Front Microbiol 9:98
PhD thesis (in Russian). Pushchinoa 152:120–132 Zhang C, Hu X, Luo J, Wu Z, Wang L, Li B, Wang Y, Sun G (2015)
Sviridov AV, Shushkova TV, Zelenkova NF, Vinokurova NG, Morgunov Degradation dynamics of glyphosate in different types of citrus or-
IG, Ermakova IT, Leontievsky AA (2012) Distribution of chard soils in China. Molecules 20(1):1161–1175

You might also like