Elsevier

Journal of Environmental Management

Volume 114, 15 January 2013, Pages 372-380
Journal of Environmental Management

Microbial degradation of chlorpyrifos in liquid media and soil

https://doi.org/10.1016/j.jenvman.2012.10.032Get rights and content

Abstract

Chlorpyrifos is a broad-spectrum insecticide which is used extensively in agriculture worldwide. Its massive application has led to the contamination of water and soil, and disruption of biogeochemical cycles. In addition, its residues have been detected in various ecological systems. A number of methods are currently available that can be used for the detoxification of such pesticides, however, this review focuses on microbial biodegradation which is considered to be one of the most viable options for the removal of organophosphate pesticides from the environment. Identification of genes and enzymes responsible for the cleavage of specific functional groups of the pesticide and understanding the kinetics of biodegradation are critical to accomplish successful bioremediation. Recently, the use of indigenous or genetically modified microorganisms and/or plants has increased the chances for in-situ bioremediation of contaminated sites. The literature provides evidence that the bioremediation process can be enhanced by maintaining an effective chlorpyrifos-degrading microbial community in the contaminated site and optimizing environmental conditions.

Highlights

► Several microbial species have been reported to degrade chlorpyrifos in liquid culture and soil. ► Specific enzyme-encoding degrading genes for chlorpyrifos can be used to mineralize chlorpyrifos. ► Knowledge of the kinetics of biodegradation is essential in understanding the persistence of a pesticide. ► Bioremediation could be an effective strategy for the detoxification of chlorpyrifos.

Introduction

Chlorpyrifos [O,O-diethyl O-(3,5,6-trichloro-2-pyridinyl)-phosphorothioate] is one of the most widely used organophosphate pesticides. It was first developed by the Germans in the 1930s and first introduced in 1965 in the USA as a home and garden insecticide by Dow Chemicals (Worthing, 1979). Chlorpyrifos is a non-systemic insecticide, which is effective against a wide range of insect pests of economically important crops (Fang et al., 2006). It enters into an insect body by contact and ingestion, and is also absorbed through the gut, skin and pulmonary membranes (Simon et al., 1998). 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 (Hui et al., 2010). As a result, acetylcholine is accumulated at the neuron synapse which causes the death of the target insect.

It has been documented that organophosphate pesticides account for about 38% of the total pesticides used worldwide (Singh and Walker, 2006). A considerable amount of the pesticide either accumulates in the soil or enters into water bodies after application. Unfortunately, less than 0.1% of the total applied pesticide reaches the target and the rest remains in the environment (Pimentel, 1995). Chlorpyrifos residues were detected up to eight years after application for termite treatment in 16 houses in North Carolina (Wright et al., 1994). Living organisms are exposed to pesticide residues in soil and water, resulting in a risk to the ecological balance (Kulshrestha and Kumari, 2011). There are also some reports on chlorpyrifos residues in the food chain (Aysal et al., 2004; Chandra et al., 2010). Several ecosystems across the world have been reported to be contaminated as a result of indiscriminate use of organophosphate pesticides, causing poisoning of millions of people and over 200,000 deaths annually (Cisar and Snyder, 2000; Singh et al., 2009). Moreover, serious damage to non-target species, such as endocrine disruption, birth defects, low birth weights, reduced head circumference, nervous system disorders and immune system abnormalities, has also been reported (Furlong et al., 2006; Rauh et al., 2011). Oxidative stress in animals is also induced by exposure to chlorpyrifos (Giordano et al., 2007). In addition, it is found to be associated with bladder cancer and chromosomal damage (Lee et al., 2004). Similarly, hyperglycaemia has been observed in a number of animals as a result of chlorpyrifos acute and sub-chronic exposures (Abdollahi et al., 2004).

The remediation of chlorpyrifos-contaminated sites to mitigate the hazardous effects of such toxic chemicals is required. A number of methods, including chemical treatment, volatilization, photodecomposition and incineration, can be applied for the detoxification of chlorpyrifos (Racke, 1993; Muhammad, 2010; Gao et al., 2012). However, most of them are not applicable for diffused contamination at low concentration because they are expensive, inefficient and not always environmental friendly. 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 (Awad et al., 2011; Massiha et al., 2011). In some early studies, chlorpyrifos was reported to be resistant to biodegradation due to accumulation of the antimicrobial degradation products in soil (Serdar et al., 1982; Racke et al., 1990). Later, several studies have revealed that many microorganisms are capable of degrading chlorpyrifos efficiently (Singh et al., 2004, 2006; Zhu et al., 2010; Kulshrestha and Kumari, 2011; Liu et al., 2012).

Section snippets

Fate of chlorpyrifos in the environment

The fate of chlorpyrifos is affected not only by its own physico-chemical properties (Table 1), but also by characteristics of the soil, management practices and environmental conditions (Halimah et al., 2010). Pesticides are distributed in the solid, liquid and gaseous phases in the vadose zone after their application depending upon the constant of adsorption, desorption and volatilization (Marino et al., 2002). The applied chlorpyrifos binds to plants, soil particles or sediments (Gebremariam

Biodegradation of chlorpyrifos in liquid media and soil

Biotic degradation is a common process for the removal of organic pollutants because of its low cost and less collateral destruction of indigenous organisms. Several species of bacteria and fungi have been reported to degrade organophosphate pesticides in liquid media and soil (Table 2).

Genes and enzymes responsible for biodegradation of chlorpyrifos

Chlorpyrifos is degraded by a variety of microorganisms. These microorganisms are capable of producing pesticide-degrading enzymes such as organophosphorus hydrolase (OPH) (Gao et al., 2012), phosphotriesterase (PTE) (Theriot and Grunden, 2011), acid organophosphorus anhydrolase (OPAA) (Cheng et al., 1993) and methyl parathion hydrolase (MPH) (Chino-Flores et al., 2012). The biochemistry of organophosphate pesticide degradation by most of the microorganisms appears to be identical, where OPH or

Kinetics and modeling of biodegradation

Knowledge of the kinetics of biodegradation is essential in understanding the persistence of an organic pollutant and to evaluate its exposure to humans, animals and plants (Alexander, 1999). The rate of biodegradation is dependent on the target compound, its concentration and the microorganism responsible for its biodegradation under given environmental conditions (Fulekar and Geetha, 2008; Hussain et al., 2009). In particular, the initial concentration of the pesticide is very critical to

Environmental factors affecting chlorpyrifos biodegradation

It is highly desirable to establish optimal biotic and abiotic factors for successful bioremediation in a particular environment; otherwise field application of microbes fails sometimes due to ambiguity on the part of pre-adjustment and the establishment of biotic and abiotic parameters that are necessary for microbial functioning (Arshad et al., 2008). The biodegradation process is influenced by many factors including temperature, solar radiation, type of soil, pH, the presence of oxygen or

Conclusions

Bioremediation is an effective strategy where microbial metabolic potential can be harnessed for in-situ and ex-situ detoxification of chlorpyrifos. Compared to bacterial mono-cultures, mixed cultures were shown to be more effective in the degradation of chlorpyrifos-contaminated soil. There are many studies that show complete degradation of chlorpyrifos in liquid culture and soil. The literature provides reasonable evidence that application of plasmid-encoding chlorpyrifos-degrading genes is

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