Rapid biodegradation of chlorpyrifos by plant growth-promoting psychrophilic Shewanella sp. BT05: An eco-friendly approach to clean up pesticide-contaminated environment
Introduction
The modern agriculture has been practiced continuous application of synthetic pesticides to gain better crop yield as well as food security (Aswathi et al., 2019). Even though the pesticides play an important role in modern agriculture, continuous practice of pesticides causes critical damages to the ecosystem (Köck-Schulmeyer et al., 2019, Barbieri et al., 2019). Gluckman and Hanson (2004) reported that the continuous pesticide exposure cause immunological troubles, immunodeficiency syndrome and malignancy associated diseases (Gluckman and Hanson, 2004). The extreme use of pesticides causes severe soil, and water pollution leads to the loss of soil and water microflora and fauna (Jaiswal et al., 2019). Among the synthetic pesticides chlorpyrifos (CPs) is one the most popular and widely used pesticide in India.
CPs (O, O-diethyl O-3, 5, 6-trichloro-2-pyridinyl phosphorothioate) is commonly practiced pesticide in farming with vast range of biological action and control variety of pests, beetles along with earth inhabitants (Yadava et al., 2015). It’s not soluble in aqueous solution owing to persistent recalcitrant (Ch et al., 2019). However, persistent CPs and their bi-products migrated in soil and water and entered into food chains (Oritz-Hernandez, 2013). It has been reported that the CPs residues in cereals, vegetables, and grains are increased gradually (Jaiswal et al., 2019). Thus, elimination of CPs from the ecosystem is important and needs immediate attention. Physical and chemical methods to eliminate or remove CPs pollution may cause secondary pollution to the environment. Thus, biodegradation is considered a more reliable, gainful and green approach towards the decontamination of CPs.
To date, several studies have reported the biodegradation of CPs through the catabolic and co-metabolic mechanisms of various microorganisms. Among these microorganisms, Streptomyces (Fuentes et al., 2017), Stenotrophomonas (Feng et al., 2017), Sphingomonas (Li et al., 2007), Bacillus (Pailan et al., 2015), Synechocystis (Singh et al., 2011), Pseudomonas (Aswathi et al., 2019), Actinobacteria (Briceno et al., 2012), and Klebsiella (Wang et al., 2013) have been recognized as potential CPs degraders. However, the degradation of CPs by Shewanella sp. has not been reported.
Shewanella sp. is typical environmental Gram-negative bacteria widespread in fresh water and marine eco-system in warm climates and is rarely pathogenic. It is well known genus for their potential removal of metals and dyes (Zhou et al., 2018, Liu et al., 2018). Therefore, current investigation was centered on the utilization of psychrophilic Shewanella sp. for the biodegradation of CPs. Furthermore, optimization of environmental variables is important for enhanced degradation process. It has been reported that the ecological and nutritional factors prominently affects the removal of CPs (Khalid et al., 2016). Thus, the software based statistical tool Box-Behnken (BB) design is employed to identify the favorable abiotic environment for the successful enhanced biodegradation of CPs. Hence, the aim of this work was (i) to isolate and identify CPs degrading bacterial strains from brackish water; (ii) to explore the plant growth promoting activity (PGP), (iii) to investigate CPs degrading ability of the isolate under in-vitro conditions, (iv) optimization of abiotic variables using BB design for enhanced biodegradation of CPs, and (v) identification of CPs products by high-performance liquid chromatography (HPLC).
Section snippets
Materials
Chlorpyrifos (20% EC) was obtained from Agro-service centre, Mallasamudram, Tamil Nadu, India. 10 g/L of CPs was prepared and used as a working concentration. Analytical grade chemicals and reagents employed in this study were procured from Sigma-Aldrich (USA) and Hi Media (India).
Isolation of CPs degrading bacteria from brackish water
Brackish water samples were collected from a mangrove forest located at Pichavaram (11°06′–33.91′ N, and 78°36′–05.60′ E), Tamil Nadu, India. The location of the sampling site is presented in Fig. 1. CPs-degrading
Identification and PGP traits of the isolate
Five morphologically diverse colonies were identified on the nutrient agar (NA) plates amended with CPs (0–50 mg/L) and the isolates were designated as BT01, B02, BT03, BT04 and BT05. Among the five isolates, BT05 was grown on NA agar plates with 50 mg/L of CPs as well as rapid growth and high degrading efficiency. Thus, the strain BT05 was selected for further studies. Based on biochemical characteristics (Table 1) and 16 S rDNA nucleotide sequence analysis, isolated strain was identified as
Conclusion
In conclusion, we report the bacterial isolate BT05 capable of CPs degradatioon isolated from brackish water. The isolate Shewanella sp. BT05 showed rapid degradation of CPs (94.3%) within 24 h. The isolate showed enhanced removal rate (80.5%) up to the concentration of 50 mg/L of CPs. However, the optimization studies showed that 13% increased CPs removal (93%) in the presence of 3.5% glucose, pH 7.0 and 32.5 °C. The CPs removal by the isolate is further validated by FT-IR and HPLC analysis.
CRediT authorship contribution statement
M. Govarthanan: Conceptualization, Methodology, Formal analysis, Data curation, Writing - original draft, Writing - review & editing. Fuad Ameen: Writing - review & editing, Funding acquisition. S. Kamala-Kannan: Conceptualization, Formal analysis, Data curation, Writing - original draft, Writing - review & editing. T. Selvankumar: Methodology, Writing - review & editing. A. Almansob: Writing - review & editing, Funding acquisition. S.S. Alwakeel: Writing - review & editing, Funding
Acknowledgements
This work was supported by a National Research Foundation of Korea (NRF) grant funded from the Korean government (MSIP, South Korea) (No. 2018R1D1A1B07050040), and also supported by the Korea Institute of Energy Technology Evaluation and Planning (KETEP) grant funded by the Korea government (MOTIE) (No. 20194110100100, Full-scale feasibility study of the stability and efficiency improvement of a biogas production facility based on biomass from urban/living environments). Alwakeel extended
References (29)
- et al.
Soil bacteria showing a potential of chlorpyrifos degradation and plant growth enhancement
Braz. J. Microbiol.
(2016) - et al.
Rapid degradation of the organophosphate pesticide – chlorpyrifos by a novel strain of Pseudomonas nitroreducens AR-3
Bioresour. Technol.
(2019) - et al.
Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp-mediated plant growth-stimulation
Soil Bio. Biochem.
(1987) - et al.
Analysis of 52 pesticides in fresh fish muscle by QuEChERS extraction followed by LC-MS/MS determination
Sci. Total Environ.
(2019) - et al.
Biodegradation of organochlorine pesticide, endosulfan, by a fungal soil isolate, Aspergillus niger
Int. Biodeterior. Biodegrad.
(2007) - et al.
Chlorpyrifos biodegradation and 3,5,6-trichloro-2-pyridinol production by actinobacteria isolated from soil
Int. Biodeterior. Biodegrad.
(2012) - et al.
Saliva and urine metabolic profiling reveals altered amino acid and energy metabolism in male farmers exposed to pesticides in Madhya Pradesh State, India
Chemosphere
(2019) - et al.
Microbial degradation of chlorpyrifos in liquid media and soil
J. Environ. Manag.
(2013) - et al.
Enhanced degradation of chlorpyrifos in rice (Oryza sativa L.) by five strains of endophytic bacteria and their plant growth promotional ability
Chemosphere
(2017) - et al.
Removal of a mixture of pesticides by a Streptomyces consortium: influence of different soil systems
Chemosphere
(2017)