Biodegradation of chlorpyrifos and its hydrolysis product 3,5,6-trichloro-2-pyridinol using a novel bacterium Ochrobactrum sp. JAS2: A proposal of its metabolic pathway
Graphical abstract
Introduction
The moderately hazardous organophosphate insecticide chlorpyrifos [O,O-diethyl-O-(3,5,6-trichloro-2-pyridinyl) phosphorothioate] is commonly used in India [1]. Chlorpyrifos is a non-systemic insecticide, acaricide, and termiticide against gall midge, cutworms, corn rootworms, leaf folder, leaf hopper, etc. which is effective against a wide range of insect pests of economically important crops [2]. It enters into the insect body by contact and ingestion, and is also absorbed through the gut, skin and pulmonary membranes [3]. Usually, it affects the nervous system of the target insects by inhibiting the activity of acetylcholinesterase by phosphorylation, both at the synapse of neurons and in the plasma [4]. As a result, acetylcholine is accumulated at the neuron synapse which causes the death of the target insect. The half-life of chlorpyrifos in soil is usually between 10 and 120 days, but can range from 2 weeks to over one year, depending on the soil type, climate, and other conditions [5].
The biodegradation of chlorpyrifos results in the formation of TCP, which is the primary and major degradation product. It has greater water solubility than chlorpyrifos and causes the widespread contamination in soils and in the aquatic environment. TCP is not only persistent towards degradation by microorganisms but also affects the biodegradation of chlorpyrifos owing to its antimicrobial activities [6]. Living organisms has been exposed to pesticide residues in soil and water, resulting in a risk to the ecological balance [7]. The remediation of chlorpyrifos contaminated sites to mitigate the hazardous effects of such toxic chemicals is required. Biotic degradation is one of the most viable options for the remediation of chlorpyrifos in soil and water. Several researchers have focused on the microbial degradation which has been reported as a primary mechanism of pesticide dissipation from the soil and water environment. To date, few microorganisms capable of degrading chlorpyrifos and its metabolite TCP have been isolated. Such microorganisms include, Alcaligenes faecalis strain DSP3 degraded 100% and 93.5% of 100 mg l− 1 chlorpyrifos and TCP within 12 days [8], and Sphingomonas sp. strain Dsp-2 degraded 100 mg l− 1 chlorpyrifos within 24 h, but only 30 mg l− 1 of TCP within 48 h [9]. Paracoccus sp. TRP degraded 50 mg l− 1 chlorpyrifos and TCP in 4 days [10] and Bacillus pumilus C2A1 degraded 89% of 1000 mg l− 1 chlorpyrifos within 15 days, and 90% of 300 mg l− 1 TCP within 8 days [11]. Cupriavidus sp. DT-1 degraded completely 100 mg l− 1 chlorpyrifos within 6 h and 100% of 50 mg l− 1 TCP within 14 h [12]. To the best of our understanding, very few reports are available on the microorganisms with concurrent plant growth promoting abilities besides their role in pesticide degradation [13], [14], [15]. Thus, the prime objective of the present investigation was to screen the chlorpyrifos and its metabolite TCP resistant bacteria isolate from paddy rhizospheric soil for selection of an efficient strain with inherent chlorpyrifos degrading ability, and multiple auxiliary plant beneficial traits.
Section snippets
Chemicals
Analytical grade chlorpyrifos methyl PESTANAL (99.9%) and TCP (99.3%) were procured from Sigma-Aldrich (St. Louis, MO, USA). The pesticide used in this study of technical grade chlorpyrifos 20% (EC) purchased from Isagro (Asia) Agrochemical Pvt. Ltd., Mumbai. All other reagents used in this study were of high purity and analytical grade.
Isolation and characterization of chlorpyrifos and its metabolite TCP degrading bacterial strain
Bacterial strains capable of degrading chlorpyrifos were isolated from paddy rhizosphere of chlorpyrifos treated soil by the enrichment culture technique. 20 g
Isolation and characterization of strain JAS2
The chlorpyrifos degrading bacterium JAS2 is a Gram-negative, rod shaped, motile bacterium, positive for citrate, catalase, oxidase, urease, nitrate reduction, glucose, sucrose, arabinose, mannitol and rhamnose, negative for indole, methyl red, Voges–Proskauer, H2S production, starch hydrolysis, gelatine liquefaction, lactose and sorbitol. Comparative analysis of the 16S rRNA gene sequence of strain JAS2 illustrated 98% similarity with the species Ochrobactrum oryzae of the genus Ochrobactrum
Conclusion
A novel chlorpyrifos degrading bacterium was isolated and characterized as Ochrobactrum sp. JAS2 with the unique capability of degrading chlorpyrifos and its major metabolite TCP with concurrent plant growth promoting and biocontrol potential. This is the first report involving biodegradation of both chlorpyrifos and TCP by a bacterial strain from the genus Ochrobactrum. The present study offers successful technology for the development of a powder based bioformulation. The ability to degrade
Acknowledgment
This research work was funded by the Department of Science and Technology (DST), Govt of India, New Delhi. Research grant sanction no. DST/TSG/NTS/2009/67.
References (40)
- et al.
Pesticide use and application: an Indian scenario
J. Hazard. Mater.
(2009) - et al.
Analytical chemistry of chlorpyrifos and diuron in aquatic ecosystems
Anal. Chim. Acta
(1998) - et al.
Isolation and characterization of a chlorpyrifos and 3,5,6-trichloro-2-pyridinol degrading bacterium
FEMS Microbiol. Lett.
(2005) - et al.
Isolation of chlorpyrifos degrading bacterium, Sphingomonas sp. strain Dsp-2, and cloning of the mpd gene
Res. Microbiol.
(2007) - et al.
Biodegradation of chlorpyrifos and 3,5,6-trichloro-pyridinol by a newly isolated Paracoccus sp. strain TRP
Int. Biodeterior. Biodegrad.
(2008) - et al.
Biodegradation of chlorpyrifos and its hydrolysis product 3,5,6-trichloro-2-pyridinol by Bacillus pumilus strain C2A1
J. Hazard. Mater.
(2009) - et al.
Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by Cupriavidus sp. DT-1
Bioresour. Technol.
(2013) - et al.
Characterization of a novel carbofuran degrading Pseudomonas sp. with collateral biocontrol and plant growth promoting potential
FEMS Microbiol. Lett.
(2004) - et al.
Biodegradation of isoproturon using a novel Pseudomonas aeruginosa strain JS-11 as a multi-functional bioinoculant of environmental significance
J. Hazard. Mater.
(2011) Effect of pesticides on phosphate solubilization by Bacillus sphaericus and Pseudomonas cepacia
Pestic. Biochem. Physiol.
(2011)
Changes in labile phosphorus forms during maturation of vermicompost enriched with phosphorus solubilizing and diazotrophic bacteria
Bioresour. Technol.
Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas sp. mediated plant growth stimulation
Soil Biol. Biochem.
Halophilic bacterium JAS4 in biomineralisation of endosulfan and its metabolites isolated from Gossypium herbaceum rhizosphere soil
J. Taiwan Inst. Chem. Eng.
Solubilization of zinc compounds by the diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus
Chemosphere
A new bioprocess to produce low cost powder formulations of biocontrol bacteria and fungi to control fusarial wilt and root-knot nematode of pulses
Biol. Control
Dissipation of chlorpyrifos in pakchoi-vegetated soil in a greenhouse
J. Environ. Sci.
Hydrolysis of chlorpyrifos in aqueous solutions at different temperatures and pH, Malays
J. Anal. Sci.
SCS/ARS/CES pesticide properties database for environmental decision making
Rev. Environ. Contam. Toxicol.
Toxicity of chlorpyrifos and TCP alone and in combination to Daphnia carinata: the influence of microbial degradation in natural water
Water Res.
Fungal degradation of chlorpyrifos by Acremonium sp. strain (GFRC-1) isolated from a laboratory-enriched red agricultural soil
Biol. Fertil. Soils
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