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 glyphosate in the environment. Among these, microbial degradation is the most effective and eco-friendly method. During its degradation, 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 microorganisms in the environment for bioremediation. Keywords Glyphosate . Biodegradation mechanism . Carbon-phosphorus lyase . Aminomethylphosphonicacid . Bioremediation
Introduction Glyphosate [N-(phosphonomethyl)glycine], a synthetic phosphonate compound with stable carbon-phosphorus (C-P) bond (Fig. 1), is the active ingredient of broad spectrum, post-emergent, and non-selective systemic herbicide formulations like Roundup (Gill et al. 2016; Li et al. 2016; Norgaard et al. 2014). Henri Martin of Swiss pharmaceutical company (Cliag) synthesized glyphosate molecule but John. E. Franz of Monsanto conducted its initial herbicidal tests in 1970 and commercialized in 1974 (Duke and Powles 2008). Globally, glyphosate is one of the most widely used herbicides against annual and perennial weeds in agriculture, silviculture, urban areas, and domestic gardens (Van Stempvoort et al. 2014; Waiman
* Shaohua Chen
[email protected] 1
State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou 510642, People’s Republic of China
et al. 2012; Zhang et al. 2015). Massive use of glyphosate is due to its efficient weeds elimination and development of genetically modified glyphosate-resistant varieties of soybean, cotton, canola, and maize (Annett et al. 2014). In 1996, first glyphosate-resistant soybean variety (Roundup Ready) was commercialized in the USA that resulted in tremendous increase in glyphosate sales (Dill 2005). Glyphosate mode of action is unique and is the only herbicide that targets 5-enolpyruvyl-shikimate-3phosphate synthase (EPSPS) without analogs, resulting in the inhibition of aromatic amino acid biosynthesis in shikimate pathway (Fig. 2) (Boocock and Coggins 1983; Haslam 2014). EPSPS inhibition by glyphosate suppresses the synthesis of necessary proteins and secondary metabolites, and hinders the vital energy pathways in plants and soil microorganisms (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 to humans and ecological environment (Sihtmäe et al. 2013; Wang et al. 2016). Improper application practices and overspray result in its widespread presence in aquatic and terrestrial environments (Hanke et al. 2010). Glyphosate binds to soil particles and accumulates in the upper soil layer. Therefore, it is often detected in groundwater, surface water,
Appl Microbiol Biotechnol
Glyphosate
Aminomethylphosphonic acid
Sarcosine O O P HO
O N OH
HO
Acetylglyphosate Fig. 1 Chemical structures of glyphosate, aminomethylphosphonic acid, and sarcosine
and water-sediment from surface runoff, drift and vertical transport in soil (Lupi et al. 2015; Newton et al. 1994; 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 residues in humans never exceeded the threshold limit but its negative effects cannot be conclusively denied. There is a reported evidence that glyphosate contains carcinogenic contaminants and causes organ damage in non-mammalian species through oxidative stress and inhibition of acetylcholinesterase (Mesnage et al. 2015). Glyphosate can also cause structural changes in local soil microbial communities by inhibiting the growth of soil microorganisms and facilitating the increase of
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 degradation, has also been frequently detected in surface water, sediment and groundwater (Botta et al. 2009; Grandcoin et al. 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 chromosomal damage in fish (Guilherme et al. 2014). To eliminate glyphosate related health and environmental risks, development of effective and eco-friendly bioremediation strategy is inevitable. Glyphosate can be degraded either through biotic pathway or abiotic approaches such as adsorption, thermolysis, and photodegradation (Lund-HØie and Friestad 1986). Recently, a combination of photocatalyst and ultraviolet (UV) light has emerged as a promising degradation pathway for the treatment of pesticide pollutants. Photocatalytic degradation system is capable of completely 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 and cost-effectiveness along with non-toxicity, stability, and low-price of the photocatalysts, whereas failing to control photocatalysis conditions in situ is the major drawback of this technique. Generally, photocatalytic technology is applied to degrade glyphosate in sewage treatment plant. Hence, it is necessary to study glyphosate-degrading microorganisms as microbial degradation is considered the most significant pathway for glyphosate breakdown (Mercurio et al. 2014; Wang et al. 2016). Different studies have reported effective and potential microorganisms for efficient and rapid bioremediation of glyphosate polluted environments. However, the literature lacks reviews about the mechanism and pathway of different glyphosate degrading strains. In this review, we aim to summarize the glyphosate-degrading microbes along with their biodegradation mechanism, and analyze their bioremediation potential in glyphosate-contaminated environments.
Microbial degradation of glyphosate Glyphosate-degrading microorganisms (Achromobacter sp. strain MPK 7A, Comamonas odontotermitis strain P2, Ochrobactrum intermedium strain Sq20 and Pseudomonas sp. strain 4ASW) had been previously isolated from contaminated sites by enrichment cultivation technique (Dick and Quinn 1995b; Ermakova et al. 2017; Firdous et al. 2017a; Firdous et al. 2017b). Microbe derivatives such as Arthrobacter atrocyaneus ATCC 13752, Alcaligenes sp.
Appl Microbiol Biotechnol O
Fig. 2 Glyphosate mode of action in plants
OH OH
OH
O
P
OH
O
OH
+
O
+
O
OH
P
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OH Erythrose-4-phosphate
Phosphoenolpyruvate DAHP Synthase
OH OH
O O-
O
P
OH
OH
O
OH
O
3-deoxy-D-arainoheptulosonate-7-phosphate (DAHP)
DHQ Synthase O OH
O
O-
O
O-
OH
O
OH
OH 3-Dehydroquinate (DHQ)
O-
O
HO
O
OH
OH
OH
3-Dehydroshikimate
Shikimate
HO HO
P
O
O-
OH
OH O Shikimate-3-phosphate
O-
O
EPSPS
HO HO
O
P
O-
O OH
O
inhibit Glyphosate
O
5-Enolpyruvyl-shikimate-3-phosphate
O-
O
Tyrosine
O-
O OH
O
Chorismate
strain GL, Arthrobacter sp. strain GLP-1, Geobacillus caldoxylosilyticus strain T20 and Pseudomonas sp. PG2982 can utilize glyphosate as growth nutrient (Lerbs et al. 1990; Moore et al. 1983; Obojska et al. 2002; Pipke and Amrhein 1988a; Pipke et al. 1987a). Among various glyphosatedegrading microorganisms (bacteria (Table 1), fungi (Table 2), micromyces, and actinomycetes), bacteria play the
Phenylalanine
Tryptophan
most pivotal role (Bujacz et al. 1995; Hadi et al. 2013; Obojska et al. 1999). To assess the potential of glyphosatedegrading microorganisms for bioremediation, it is necessary to optimize their degradation conditions including initial pH, incubation temperature, glyphosate concentration, inoculation biomass and incubation time. Response surface methodology reveals that bacteria exhibit efficient
Appl Microbiol Biotechnol Table 1
Glyphosate-degrading bacteria
Strain
Source
Gram Type of status degradation pathway
Detected metabolites Comments
References
Achromobacter sp. LW9
Activated sludge from glyphosate process waste stream Glyphosate-contaminated soil Methylphosphonic acid contaminated soil
–
AMPA pathway
1) AMPA
McAuliffe et al. (1990)
–
Sarcosine pathway 1) Sarcosine
–
Sludge from water reatment plant in America Activated sludge from a waste stream
–
Sarcosine pathway 1) Sarcosine 2) Glycine 3) Formaldehyde Sarcosine pathway No data (putative)
1. Utilization of glyphosate as a sole carbon source in presence of phosphate 1. Utilization of glyphosate as sole phosphorus source 1. Utilization of glyphosate as sole phosphorus source 1. Utilization of glyphosate as sole phosphorus source
Wackett et al. (1987)
1. Utilization of glyphosate as a sole carbon source in presence of phosphate 2. Capability of degrading small amount of AMPA 1. Utilization of glyphosate as sole phosphorus source
McAuliffe et al. (1990)
Achromobacter sp. MPK 7A Achromobacter sp. MPS 12A Agrobacterium radiobacter Agrobacterium radiobacter SW9
–
AMPA pathway
1) AMPA
Sarcosine pathway 1) Sarcosine 2) Glycine
Arthrobacter atrocyaneus ATCC 13752
Non-axenic cultures of the – cyanobacterium Anacystisnidulans + German collection of microorganisms and cell cultures
Arthrobacter sp. GLP-1
Accidental contaminant of + Klebsiella pneumoniae
Sarcosine pathway 1) Phosphate 2) Glycine
Arthrobacter sp. GLP-1/Nit-1
Mutant of Arthrobacter sp. GLP-1
+
Sarcosine pathway 1) Phosphate
Bacillus cereus CB4
Glyphosate-polluted soil in the herbicide plant, China
+
Both AMPA and sarcosine pathways
Comamonas odontotermitis P2
Glyphosate-contaminated soil in Australia
–
Both AMPA and sarcosine pathways (putative)
Enterobacter cloacae K7
Rhizoplane of various plants in Russia
–
Sarcosine pathway 1) Sarcosine 2) Glycine
Enterobacter sp. Bisph2
Sandy soil from Algeria
–
No data
No data
1. Utilization of glyphosate as sole phosphorus source 2. Capable of degrading glyphosate per se without previous selection culture 1. Utilization of glyphosate as sole phosphorus source 2. Capable of degrading glyphosate per se without previous selection culture 1. Utilization of glyphosate as sole phosphorus source as well as sole nitrogen source 1. Utilization of glyphosate as sole phosphorus source 2. 94.47% degradation in 5 days under the optimal capacity 1. Utilization of glyphosate as sole carbon and phosphorus source 2. Complete degradation of glyphosate (1.5 g/L) within 104 h 1. Utilization of glyphosate as sole phosphorus source 2. 40% degradation of glyphosate with initial 5 mM content No data
Flavobacterium Monsanto activated sp. GD1 sludges Central heating system Geobacillus water caldoxylosilyticus T20 Ochrobactrum Glyphosate-contaminated anthropi GPK3 soil
–
AMPA pathway
+
AMPA pathway
1) AMPA 2) Phosphate 1) AMPA 2) Glyoxylate
1. Utilization of glyphosate as sole phosphorus source 1. Utilization of glyphosate as sole phosphorus source
–
Both AMPA and sarcosine pathways
Glyphosate-contaminated indigenous soil
–
Alcaligenes sp. GL
Ochrobactrum intermedium Sq20
AMPA pathway
1) AMPA 2) CO2
1) AMPA 2) Glyoxylate 3) Sarcosine 4) Glycine 5) Formaldehyde No data
1) AMPA 2) Glyoxylate 3) Sarcosine 4) Glycine 5) Formaldehyde Sarcosine pathway 1) Sarcosine 2) Glycine
Ermakova et al. (2017) Sviridov et al. (2012)
Lerbs et al. (1990)
Pipke and Amrhein (1988a)
Pipke et al. (1987a)
Pipke and Amrhein (1988b)
Fan et al. (2012)
Firdous et al. (2017a)
Kryuchkova et al. (2014)
Benslama and Boulahrouf (2016) Balthazor and Hallas (1986) Obojska et al. (2002)
1. Utilization of glyphosate as sole phosphorus source
Sviridov et al. (2012)
1. Utilization of glyphosate as sole carbon source
Firdous et al. (2017b)
Appl Microbiol Biotechnol Table 1 (continued) Strain
Source
Gram Type of status degradation pathway
Detected metabolites Comments
Ochrobactrum sp. Soil GDOS
–
AMPA pathway
1) AMPA
Soil
–
AMPA pathway (putative)
No data
Glyphosate-contaminated soil Mutant of Pseudomonas sp. PAO1 on selective medium Activated sludge from glyphosate process waste stream
–
Sarcosine pathway 1) Sarcosine
–
Sarcosine pathway No data
–
Both AMPA (95%) and sarcosine (5%) pathway
Pseudomonas pseudomallei 22 Pseudomonas sp. 4ASW Pseudomonas sp. GLC11 Pseudomonas sp. LBr
1) AMPA 2) Glycine
Pseudomonas sp. PG2982
Pseudomonas aeruginosa – ATCC 9027
Pseudomonas sp. SG-1
Aerobic digester liquid
–
AMPA pathway
Rhizobiaceae meliloti 1021
Mutant of Rhizobiaceae meliloti induced by transposon Tn5 mutagenesis which is resistant to streptomycin Raw sludge from a municipal sewage treatment plant
–
Sarcosine pathway 1) Sarcosine 2) Glycine
+
Sarcosine pathway 1) Sarcosine 2) Glycine
Streptomycete sp. StC
Sarcosine pathway 1) Sarcosine 2) Phosphate 3) Glycine 4) Formaldehyde
glyphosate degradation ability under the optimum conditions (Fan et al. 2012; Firdous et al. 2017a). As illustrated in Tables 1 and 2, Alcaligenes sp. strain GL, Arthrobacter sp. strain GLP-1, Flavobacterium sp. strain GD1 and Pseudomonas pseudomallei strain 22 utilize glyphosate as sole phosphorus source (Balthazor and Hallas 1986; Lerbs et al. 1990; Peñaloza-Vazquez et al. 1995; Pipke et al. 1987a). Similarly, Achromobacter sp. strain LW9, Agrobacterium radiobacter strain SW9, and Ochrobactrum intermedium strain Sq20 utilize glyphosate as sole carbon or nitrogen source (Firdous et al. 2017b; McAuliffe et al. 1990). Most of the bacteria and fungi (Aspergillus niger, Aspergillus oryzae A-F02, Mucor IIIR, Penicillium IIR, Penicillium notatum, Scopulariopsis sp., Trichoderma harzianum) decompose
1) AMPA
2. Complete degradation of glyphosate (500 mg/L) within 4 days 1. Utilization of glyphosate as sole phosphate source 2. Complete degradation (3 mM) within 60 h 1. Utilization of glyphosate as sole phosphorus source 2. 50% degradation in 40 h 1. Utilization of glyphosate as sole phosphorus source 1. Utilization of glyphosate as sole phosphorus source 1. Utilization of glyphosate as sole phosphorus source 2. Capable of removing 20 mM glyphosate from growth medium 1. Utilization of glyphosate as sole phosphorus source
1. Utilization of glyphosate as sole phosphorus source 2. Within 18 h, 2 g (wet weight) of cells degraded 0.9 mg of glyphosate from a 30-ml reaction mixture 1. Utilization of glyphosate as sole phosphorus source
References
Hadi et al. (2013)
Peñaloza-Vazquez et al. (1995) Dick and Quinn (1995) Selvapandiyan and Bhatnagar (1994) Jacob et al. (1988)
Moore et al. (1983); Shinabarger and Braymer (1986); Kishore and Jacob (1987) Talbot et al. (1984)
Liu et al. (1991)
1. Utilization of glyphosate as sole Obojska et al. (1999) phosphorus, nitrogen or nitrogen and phosphorus source
glyphosate as their sole phosphorus source (Bujacz et al. 1995; Fu et al. 2017; Klimek et al. 2001; Krzyśko-Łupicka and Orlik 1997; Krzyśko-Lupicka et al. 1997). However, several strains can use glyphosate 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 , Arthrobacter sp. GLP-1/Nit-1 (mutant of Arthrobacter sp. GLP-1) can utilize glyphosate both as sole phosphorus source and sole nitrogen source (Pipke and Amrhein 1988b); Comamonas odontotermitis P2 uses glyphosate as sole carbon and phosphorus source (Firdous et al. 2017a); Streptomycete sp. StC utilizes glyphosate as sole phosphorus source, sole nitrogen source or sole nitrogen and sole phosphorus source (Obojska et al. 1999). Arthrobacter atrocyaneus ATCC 13752 spontaneously
Appl Microbiol Biotechnol Table 2
Glyphosate-degrading fungi
Strain
Source
Type of degradation Pathway
Detected metabolites
Aspergillus niger
Soil
AMPA pathway
1) AMPA
Aspergillus oryzae A-F02
Aeration tank in a pesticide factory
AMPA pathway
Mucor IIIR
Sandy-clay soil in arable land farm, Poland
AMPA pathway
Penicillium IIR
Sandy-clay soil in arable land farm, Poland
AMPA pathway
Penicillium chrysogenum
Soil
AMPA pathway (putative)
Penicillium notatum
Spontaneous growth on a solid sample of hydroxyfluorenyl9-phosphonate Soil
AMPA pathway
AMPA pathway
Soil
AMPA pathway
Scopulariopsis sp.
Trichoderma harzianum
degraded glyphosate and AMPA without enrichment cultivation (Pipke and Amrhein 1988a). Flavobacterium sp. GD1 can utilize both glyphosate and AMPA as a sole phosphorus source. Inorganic phosphorus (Pi) concentration had no effect on glyphosate metabolism but suppresses AMPA degradation process (Balthazor and Hallas 1986). Pi inhibits several isolates such as Pseudomonas sp. PG2982 and Pseudomonas sp. GLC11 from utilizing glyphosate as a sole phosphorus source (Kishore and Jacob 1987; Moore et al. 1983; Selvapandiyan and Bhatnagar 1994; Shinabarger and Braymer 1986). To date, three main intermediate metabolites of glyphosate metabolism AMPA, sarcosine, and acetylglyphosate (Fig. 1) have been found which are further metabolized through different metabolism pathways. The most frequently detected metabolite of glyphosate degradation is AMPA. Intracellular metabolism of AMPA is impossible and is released to the environment resulting in secondary contamination (Balthazor and Hallas 1986; Jacob et al. 1988; Lerbs et al. 1990). Several bacterial strains such as Bacillus megaterium 2BLW, Pseudomonas sp. 4ASW, Pseudomonas sp. 7B and Pseudomonas sp. LBr
Comments
1. Utilization of glyphosate as sole phosphorus source 1) AMPA 1. Utilization of 2) Methylamine glyphosate as sole phosphorus source 1) AMPA 1. Utilization of glyphosate as sole phosphorus source 1) AMPA 1. Utilization of glyphosate as sole phosphorus source No data 1. Utilization of glyphosate as sole nitrogen source 1) AMPA 1. Utilization of glyphosate as sole phosphorus source 1) AMPA 1. Utilization of glyphosate as sole phosphorus source 1) AMPA 1. Utilization of glyphosate as sole phosphorus source
References
Krzyśko-Lupicka et al. (1997) Fu et al. (2017)
Krzyśko-Łupicka and Orlik (1997) Krzyśko-Łupicka and Orlik (1997) Klimek et al. (2001) Bujacz et al. (1995)
Krzyśko-Lupicka et al. (1997)
Krzyśko-Lupicka et al. (1997)
(Jacob et al. 1988; Quinn et al. 1989) are known to utilize AMPA as Pi source. Unlike the AMPA pathway, isolates which metabolize glyphosate to sarcosine, completely detoxify glyphosate by utilizing sarcosine as their growth nutrient. Some reports indicate that isolates such as Bacillus cereus CB4, Ochrobactrum anthropi GPK 3 and Pseudomonas sp. LBr simultaneously convert glyphosate to AMPA and sarcosine (Fan et al. 2012; Jacob et al. 1988; Sviridov et al. 2012). Bacterial strains exhibiting significant degradation ability provide a potential tool to bioremediate glyphosatecontaminated environments. Sequencing of glyphosate oxidoreductase and carbon-phosphorus lyase (C-P lyase) genes, reveal that both pathways are concurrent in Comamonas odontotermitis P2 (Firdous et al. 2017a). Another glyphosate metabolic process converts it to acetylglyphosate but isolates cannot further utilize acetylglyphosate as a phosphorus source. Achromobacter sp. Kg 16 utilizes glyphosate as a sole phosphorus source and transforms it into acetylglyphosate, but is unable to further utilize acetylglyphosate, thus leading to its poor growth. Surprisingly, Achromobacter sp. Kg 16 can metabolize glyphosate to AMPA in the absence of carbon source in culture medium (Ermakova et al. 2017).
Appl Microbiol Biotechnol
Mechanism of glyphosate bacterial degradation
ATCC 13752, Arthrobacter sp. GLP-1, and Pseudomonas sp. LBr (Jacob et al. 1988; Pipke and Amrhein 1988a; Pipke et al. 1987a). Recently, another totally different AMPA degradation pathway has been found in Ochrobactrum anthropi GPK3, where it was metabolized to phosphonoformaldehyde by transaminase and then catabolized to formaldehyde by phosphonatase (Sviridov et al. 2014). Second glyphosate degradation pathway catalyzed by C-P lyase produces sarcosine and Pi. Pseudomonas sp. PG2982 decomposes glyphosate via C-P lyase pathway with the formation of sarcosine which is further metabolized by sarcosine oxidase to glycine and formaldehyde (Kishore and Jacob 1987; Shinabarger and Braymer 1986). Arthrobacter sp. GLP-1 utilizes glycine for protein biosynthesis by inducing the formation of peptide backbone and amino acids (serine and threonine). According to Pipke et al. (1987a), one-carbon compound combined with tetrahydrofolic, biosynthesis nucleic acids (purine and thymine), and proteins (serine, cysteine, methionine, and histidine). The fate of glyphosate biodegradation metabolites has been clearly traced by isotope labeling. Degradation pathways of glyphosate in bacteria are summarized in Fig. 3.
Degradation pathways of glyphosate in bacteria As mentioned above, conversions of glyphosate to AMPA and sarcosine are two major degradation pathways in glyphosate-degrading microorganisms. Bacterial biodegradation mechanism of glyphosate includes (i) cleavage of carboxymethylene-nitrogen (C-N) bond, catalyzed by an oxidase yielding AMPA and glyoxylate; and (ii) direct cleavage of carbon-phosphorus (C-P) bond, catalyzed by C-P lyase yielding sarcosine. Both of the degradation pathways may involve C-P lyase to break C-P bond in AMPA molecule. First major step in the degradation pathway of glyphosate, catalyzed by glyphosate oxidoreductase, is the formation of AMPA and glyoxylate. Pseudomonas sp. LBr metabolizes glyphosate via AMPA and glycine pathway with 5% conversion of glyphosate to glycine and formaldehyde. Solid-state 13C NMR revealed that isolate utilized glyoxylate and formaldehyde for its growth (Jacob et al. 1988). Arthrobacter atrocyaneus ATCC 13752 catabolized glyphosate to AMPA and CO2, whereas CO2 was not the product of AMPA (Pipke and Amrhein 1988a). Intermediate metabolite AMPA can be either excreted to the environment because of its bacterial toxicity or further metabolized by different enzymes (Jacob et al. 1988; Pipke and Amrhein 1988a; Sviridov et al. 2012). AMPA mostly serves as a substrate of C-P lyase, producing methylamine and Pi as a phosphorus source for Arthrobacter atrocyaneus
Enzymes of glyphosate metabolism in bacteria Glyphosate oxidoreductase (GOX) is the key enzyme of glyphosate degradation to AMPA via C-N bond cleavage. GOX-encoding genes have been identified in Ochrobactrum sp. G1 (GU214711.1), Ochrobactrum anthropi GPK 3 and Comamonas odontotermitis P2 (KX980206.1) with 99% O
O P HO
HO
OH
H2N
+
HO
CH3
Phosphonatase
O
P HO
HO H
OH
HO
+
H
H
Formaldehyde
Phosphate
Phosphonoformaldehyde
Methylamine
Phosphate
O O
P
Environment
Excretion Transaminase
C-P lyase
O
O NH2
P HO
Glyphosate oxidoreductase O P HO
HO
H
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Tetrahydrofolate cycle
Tricarboxylic acid cycle OH
CO2
O
AMPA
Glyoxylate
O
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N
P
OH
HO
Glyphosate
Microbial biosynthesis and metabolism
O
O
OH
HO
Acetylglyphosate Tetrahydrofolate cycle
O
O
C-P lyase P HO
HO
OH
Phosphate
Fig. 3 Degradation pathways of glyphosate in bacteria
+
Sarcosine oxidase
NH OH
Sarcosine
O
O H2N
+ OH
Glycine
H
H
Formaldehyde
Appl Microbiol Biotechnol
similarity, and partial GOX gene in Comamonas odontotermitis P2 product enzyme (ATE50174.1). There is a synthetic construct between GOX (ADV58259.1) and GOX gene (HQ110097.1) that has been used as a transgene in glyphosate-tolerant canola (Duke 2010; Hadi et al. 2012). However, purified GOX enzymes, either from a microorganism or the product enzyme from cloned gox gene, exhibit low affinity to glyphosate (Hove-Jensen et al. 2014; Sviridov et al. 2014). GOX purified from Ochrobactrum anthropi GPK 3, containing flavin adenine dinucleotide (FAD), belongs to bacterial flavin monooxygenase superfamily (Sviridov 2012). Two open reading frames glpA and glpB related to glyphosate utilization have been found in Pseudomonas pseudomallei 22. Specifically, glpA is related to the glyphosate tolerance, and glpB is associated with the conversion of glyphosate to AMPA which is a substrate of Escherichia coli C-P lyase (Peñaloza-Vazquez et al. 1995). Till now, four C-P bond catabolic enzymes including C-P lyase, phosphonoacetaldehyde hydrolase, phosphonoacetate hydrolase and phosphoenolpyruvate hydrolase have been characterized in bacteria (Villarreal-Chiu et al. 2012). However, only C-P lyase can split C-P bond of glyphosate whereas the other three enzymes are highly specific to their own substrate (Bujacz et al. 1995). Glyphosate C-P bond is hydrolytically stable and resistant to chemolysis and photolysis. Consequently, C-P lyase complex with high specificity to glyphosate is essential for glyphosate degradation via cleavage of inactivated C-P bond and formation of sarcosine. C-P lyase complex, which can metabolize a wide variety of different phosphonates, has been adequately studied in E.coli (Kamat and Raushel 2013). E.coli C-P lyase complex is the product of 14 genes operon (phnCDEFGHIJKLMNOP), which is a part of Pho regulon (Chen et al. 1990; Metcalf and Wanner 1993a, 1993b). According to previous genetic and biochemical studies, phnCDE encode an ATP-binding cassette transporter and the gene product PhnF is a repressor protein (Hove-Jensen et al. 2010; Hovejensen et al. 2011; Metcalf and Wanner 1993b). Seven proteins (PhnG, PhnH, PhnI, PhnJ, PhnK, PhnL, and PhnM) are supposed to constitute the core components of the membrane-bound C-P lyase, metabolizing phosphonates to phosphate by PhnJ catalyst (Hovejensen et al. 2011; Metcalf and Wanner 1993b). Furthermore, PhnNOP is considered to perform regulatory and accessory functions in C-P lyase catabolic metabolism reaction (Hovejensen et al. 2011; Metcalf and Wanner 1993b). However, purified and characterized C-P lyase could not split the glyphosate C-P bond. To date, the C-P lyase with high-specificity to glyphosate has not been clearly characterized at genetic and biochemistry level (Sviridov et al. 2014). There is another non-specific glyphosate C-P lyase which can split C-P bond of AMPA for further degradation. Hence, probably two different C-P lyases with different substrate specificity co-exist in one bacterium.
Generally, glyphosate biodegradation to AMPA is not subjected to Pi concentration, except in Arthrobacter atrocyaneus ATCC 13752 where glyphosate degradation was repressed by Pi (Pipke and Amrhein 1988a). However, glyphosate metabolic conversion to sarcosine seems to be regulated by the Pi concentration. For example, glyphosate degradation was suppressed in the presence of Pi in Arthtobacter sp. (Pipke et al. 1987b) and Pseudomonas sp. 4ASW (Dick and Quinn 1995a). The transport system in glyphosate-degrading microorganisms for glyphosate uptake is likely to depend on Pi level (HoveJensen et al. 2014). In addition, C-P lyase activity is controlled by phn genes which are upregulated in Pi absence (Metcalf and Wanner 1993b). Therefore, it can be assumed that Pi level affects the sarcosine pathway of glyphosate degradation. Besides, PhoR-PhoB-based two-component system responds to the exogenous and endogenous Pi concentrations in E.coli (Santos-beneit 2015).
Bioremediation potential of glyphosate-degrading microorganisms Bioremediation refers to the transformation of pollutants into less toxic compounds by using microorganisms and their degradation enzymes (Chen et al. 2012; Liu et al. 2015; Sharma et al. 2018; Zhan et al. 2018). Bioremediation is supposed to be more promising for the removal of chemical pollutants in water and soil environment. Microorganisms and their enzymes-based bioremediation of contaminated environments are efficient, safe and cost-effective (Chen et al. 2011a, b; Karigar and Rao 2011; Xiao et al. 2015). Under natural conditions, degradation of glyphosate in the soil depends on microbial degradation. Hence, it is necessary to identify glyphosate-degrading microorganisms and confirm their potential for the bioremediation of glyphosate-contaminated environments. Though plentiful glyphosate-degrading microorganisms have been isolated, their ability to remediate glyphosate-contaminated environments still remains a conundrum because of low efficiency in situ and in vitro. Potent glyphosate-degrading microorganisms should be available both in liquid media and soil. Potential of glyphosatedegrading microorganisms for glyphosate-contaminated soils remediation has only been studied in only a few bacteria. Strain Bacillus subtilis Bs-15 degraded 66.97% of 5000 mg/L glyphosate in sterile soil and 71.57% of glyphosate in the unsterilized soil that shows its bioremediation potential for glyphosate-contaminated soils and microbial diversity in the soil (Yu et al. 2015). Introduction of Achromobacter sp. Kg16 and Ochrobactrum anthropi GPK3 strains to the soil remediated glyphosate-treated soil within 1 to 2 weeks, showing 2–3 folds higher degradation rate as compared to endogenous microorganisms (Ermakova et al. 2010). Additionally, many glyphosate-degrading bacterial strains via sarcosine pathway effectively degraded
Appl Microbiol Biotechnol
glyphosate only under laboratory conditions, because of C-P lyase catalysis inhibition by Pi concentrations in the natural environment. Persistence of inter-metabolite AMPA in the soil also contaminates the environment, and thus microbes that are either unable to utilize AMPA or excrete it cannot be used for bioremediation of glyphosate-contaminated environment.
Conclusion and future perspectives Excessive use of glyphosate also plays a vital role to achieve maximum crop yield and rapid agricultural development. However, due to its intensive use, glyphosate contamination has emerged as an urgent issue. The inveterate negative effects of glyphosate on the environment should attract considerable attention to remove glyphosate residues from the polluted environments. Recently, photocatalytic technology has been developed to efficiently degrade glyphosate but because of uncontrollable reaction conditions, it is not suitable against glyphosate residues in situ. Hence, the glyphosate-degrading microorganisms having efficient degradation and bioremediation potentials in glyphosate-contaminated environments are considered as the most promising strategy. Hitherto, varieties of microorganisms have been characterized to degrade glyphosate by utilizing glyphosate as sole phosphorus, carbon or nitrogen source. However, genetic and biochemical aspects of highly efficient degrading enzymes have yet not been properly explored. Most of the glyphosate-degrading isolates are bacteria in which complete degradation pathway has been clearly understood. The most prevalent glyphosate degradation pathway in bacterial strains is the cleavage of C-N bond and conversion to AMPA which is either further decomposed or excreted to the environment. Cleavage of C-P bond catalyzed by C-P lyase is negatively regulated by Pi supply. In order to deal with glyphosate contamination in the environment, the potential of degrading microbes and enzymes for bioremediation is worth studying. Generally, microbial community has great potential for glyphosate degradation as compared to single isolate. Therefore, collective degradation by various degrading microbes can be more effective against glyphosate residues. Moreover, to understand the degradation mechanism, studying the role of functional genes and enzymes in bioremediation of glyphosatecontaminated environments is crucial. Although a large number of glyphosate degrading microorganisms have been isolated and characterized yet only a few have been explored for their functional genes and enzymes. Therefore, before the large-scale application of glyphosate-degrading microorganisms for bioremediation, detailed foundation work should be accomplished.
Funding This study was partially funded by grants from the National Natural Science Foundation of China (31401763), the National Key Project for Basic Research (2015CB150600), Guangdong Natural Science Funds for Distinguished Young Scholar (2015A030306038), the Science and Technology Planning Project of Guangdong Province (2016A020210106, 2017A010105008) and Pearl River S&T Nova Program of Guangzhou (201506010006).
Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest. Ethical approval This article does not contain any studies with human participants or animals performed by any of the authors.
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