Elsevier

Chemosphere

Volume 83, Issue 10, May 2011, Pages 1297-1306
Chemosphere

Review
Chlorophenols and other related derivatives of environmental concern: Properties, distribution and microbial degradation processes

https://doi.org/10.1016/j.chemosphere.2011.04.009Get rights and content

Abstract

Chlorophenols are chlorinated aromatic compound structures and are commonly found in pesticide preparations as well as industrial wastes. They are recalcitrant to biodegradation and consequently persistent in the environment. A variety of chlorophenols derivatives compounds are highly toxic, mutagenic and carcinogenic for living organisms. Biological transformation by microorganisms is one of the key remediation options that can be exploited to solve environmental pollution problems caused by these notorious compounds. The key enzymes in the microbial degradation of chlorophenols are the oxygenases and dioxygenases. These enzymes can be engineered for enhanced degradation of highly chlorinated aromatic compounds through directed evolution methods. This review underscores the mechanisms of chlorophenols biodegradation with the view to understanding how bioremediation processes can be optimized for cleaning up chloroaromatic contaminated environments.

Highlights

► Properties, distribution and environmental fate of chlorophenols. ► Biodegradation and biotransformation of chlorophenols. ► Genetics of 2,4,6-trichlorophenol (2,4,6-TCP) degradation. ► The functional role of flavin reductase and quinone reductase in degradation. ► Evolution of genes involved in chlorophenol degradation in bacteria.

Introduction

In recent decades, the discharge of large quantities of synthetic chemicals, such as solvents, plasticizers, insecticides, herbicides, and fungicides, into the environment through industrial, agricultural, medical, and domestic activities has produced significant ecotoxicological problems with serious consequences for all living organisms (Furukawa, 2006). These substances include chlorophenols, which have been classified as priority pollutants by the US Environmental Protection Agency (ATSDR, 2007).

Chlorophenols are of serious environmental concern because of their widespread occurrence throughout the environment. They are found in wastewater, sludge products, surface waters, and groundwater (Samanta et al., 2002, Zhang and Bennett, 2005, Geng et al., 2006). Other sources of contamination are accidental spills, hazardous waste disposal sites, storage tanks, or municipal landfills. They are also used as bactericides, insecticides, herbicides, fungicides, wood preservatives and as intermediates in the production of dyes and pharmaceuticals (ATSDR, 2007, Murcia et al., 2007, Yang and Lee, 2008, El-Sayed et al., 2009). Other sources of chlorophenols in the environment are processes of biodegradation of pesticides and herbicides. Microbial degradation of herbicides especially of 2,4-dichlorophenoxyacetic acid (2,4-D), 2,4,5-trichlorophenoxyacetic acid (2,4,5-T) and pesticides, yields numerous chlorophenols as intermediate metabolites of their decomposition (Czaplicka, 2004). The herbicides 2,4-dichlorophenoxyacetic acids (2,4-D) and 2,4,5-trichlorophenoxyacetic acid (2,4,5-T) often used on food crop can be broken down to 2,4-dichlorophenols and 2,4,5-tricholorphenols (ATSDR, 2007). During the combustion of organic matters chlorophenolic compounds are formed (Al-Thani et al., 2007). Findings have shown that chlorophenols are formed during the incineration of municipal waste (El-Sayed et al., 2009). In the world today, because of their adverse environmental effects, of this group of compounds were significantly limited to plant protection, if not left out completely. Presently, limitations are imposed on use and production of chlorophenols in many countries.

Chlorophenols are major group of pollutants of environmental concern because of their toxicity and widespread uses (Häggblom and Bossert, 2003). Chlorophenols (CPs) include mono-, di-, tri-, tetra-, and penta-chlorinated phenols (CP, DCP, TCP, TTCP, and PCP, respectively). Among the 19 possible congeners of chlorophenols, 2-chlorophenol (2-CP), 2,4-dichlorophenol (2,4-DCP), 2,4,6-trichlorophenol (2,4,6-TCP) and pentachlorophenol (PCP) are listed in the Priority Pollutant List of the US Environmental Protection Agency (ATSDR, 2007). The 2-CP, 2,4-DCP and 2,4,6-TCP are widely chosen as precursors for the manufacturing of other chlorophenol products and 2,4-DCP, 2,4,6-TCP and PCP are used as pesticides, herbicides, fungicides, molluscides, acaricides, bactericides, and mould inhibitors (Yang and Lee, 2008, El-Sayed et al., 2009). Besides, 2-CP, 4-CP, 2,4-DCP and 2,4,6-TCP are the most significant chlorinated phenols formed as by-products of water chlorination (ATSDR, 1999, Czaplicka, 2004). A number of physical, chemical and biological methods have been used to eliminate chlorophenols from industrial effluents and neither of these methods and their combinations has been used to achieve complete mineralization of chlorophenols (La Rotta et al., 2007, Herrera et al., 2008). Although, chemical methods are efficient, they may generate undesirable by-products, besides being very expensive. By contrast, biological methods are generally more efficient and relatively cheaper than chemical methods.

In spite of the fact that microbial degradation of chlorophenols has been investigated for many years, there is still considerable interest in the metabolic capacity of bacteria able to degrade chlorophenols within indigenous microbial consortia in various ecosystems (Solyanikova and Golovleva, 2004). Chlorinated phenols such as the trichlorophenols, tetrachlorophenols, and pentachlorophenol (PCP) have been used extensively since the 1920s as preservatives to prevent fungal attack on wood (Al-Thani et al., 2007, El-Sayed et al., 2009). During this time, they have become serious environmental contaminants. PCP-degrading bacteria are present in soils worldwide (Mahmood et al., 2005, Yang et al., 2006). Several reports are available on biodegradation of chlorophenols by Pseudomonas sp., Sphingomonas sp., Alcaligenes sp., Rhodococcus sp. and fungal species like white-rot basidiomycetes sp. Among these microorganisms, Arthrobacter chlorophenolicus A6 has been demonstrated to degrade a wide variety of toxic substituted phenols (Nordin et al., 2005, Pedroza et al., 2007, El-Sayed et al., 2009, González et al., 2010). It is also reported that among the aerobic chlorophenol degrading microorganisms, A. chlorophenolicus A6 degrade the compound by a novel route via hydroxyquinol pathway with reductive dechlorination being one of the key intermediate steps in the process (Nordin et al., 2005).

Many chlorophenolic compounds and their metabolites pose a health hazard due to their toxicity to numerous organisms. It is both relevant and important to reduce the input of toxic chemicals into the environment and to study methods for their removal from contaminated sites. Understanding the microbial metabolism of these compounds will assist in developing management strategies to minimize their persistence in the environment. The fate of chlorophenols in ecosystems continued to be a focal point for studies of environmental contamination. In this review, we present an overview of the role of microorganism in the degradation of chlorophenols contaminant in the environment which is the subject of on-going intensive investigation in our laboratory.

Section snippets

Properties of chlorophenols

Chlorophenols are chlorinated aromatic ring structures consisting of the benzene ring, –OH group and atom(s) of chlorine. Jointly with the 19 possible isomers, chloroderivatives of methyl- and ethyl-phenols are also considered as chlorophenols (Ivanciuc et al., 2006). All chlorophenols are solids at room temperature except 2-chlorophenol (2-CP), which is a liquid. The aqueous solubility of chlorophenols is low, but the sodium or potassium salts of chlorophenols are up to four orders of

Distribution and environmental fate of chlorophenols

As earlier highlighted chlorophenols are introduced into the environment as effluents waste from several industrial processes, through its use as biocides or as by-products of other industrial operations, such as pulp bleaching with chlorine, water disinfection or even waste incineration (Murialdo et al., 2003). Chlorophenols have also been used as general purpose disinfectants, and it has been found that they can also appear as degradation products of other chlorinated xenobiotics. Because of

Biodegradation and biotransformation of chlorophenols

Microbial degradation of chlorophenols have been reported by several groups (Reddy and Gold, 2000, Cortés et al., 2002, Murialdo et al., 2003, Crawford et al., 2007). Chlorophenols are subject to abiotic and biotic degradation and transformations (Cortés et al., 2002). There are several studies regarding the microbial degradation of chlorophenols in water and sediments (Demnerova et al., 2005), as well as studies concerning the degradation of these compounds by sludge (Lallai and Mura, 2004).

Reductive dehalogenation of chlorophenols

Reductive dehalogenation is a process which may prove to be of paramount importance in dealing with a particularly persistent class of contaminants often in soil and ground water sites (Sims et al., 1991). Reductive dehalogenation of chlorinated aromatic compounds whereby chlorines are being replaced by hydrogen occurs extensively under anaerobic conditions (Genthner et al., 1989). Genthner et al. (1989) have shown the order of degradability of monochlorophenol was meta > ortho > para.

Mikesell and

Genetics of 2,4,6-trichlorophenol (2,4,6-TCP) degradation

The degradation pathway of 2,4,6-trichlorophenol (2,4,6-TCP), a hazardous pollutant, in the aerobic bacterium Cupriavidus necator JMP134(pJP4) (formerly Ralstonia eutropha JMP134) is encoded by the tcp genes (Sánchez and González, 2007). A catabolic pathway for (2,4,6-TCP) has been proposed (Padilla et al., 2000, Louie et al., 2002, Xun and Webster, 2004). The pathway is initiated by the conversion of 2,4,6-TCP to 2,6-dichloro-p-hydroquinone (2,6-DCHQ) and then to 6-chlorohydroxyquinol (6-CHQ);

The functional role of flavin reductase and quinone reductase in 2,4,6-TCP and PCP degradation

The tcpRXABCYD operon of C. necator JMP134 is involved in the degradation of 2,4,6-trichlorophenol (2,4,6-TCP), a toxic pollutant (Louie et al., 2002, Sánchez and González, 2007). TcpA is a reduced flavin adenine dinucleotide (FADH2)-dependent monooxygenase that converts 2,4,6-TCP to 6-chlorohydroxyquinone. It has been implied through genetic analysis that TcpX acts as an FAD reductase to supply TcpA with FADH2 (Belchik and Xun, 2008), whereas the function of TcpB in 2,4,6-TCP degradation has

Evolution of genes involved in chlorophenol degradation in bacteria

Biotransformation of chloroaromatic compounds usually involves enzymes catabolizing ortho or intradiol ring cleavage that is between the hydroxyl groups, to chlorosubstituted cis,cis-muconates. An ancestral pathway for degradation of naturally occurring chloroaromatics has been proposed to be the origin of a set of chlorocatechol catabolic genes which then presumably spread in the environment after the advent of industrial use of chloroaromatics in the 20th century (Schlömann, 1994). However,

Future outlook

Many organic pollutants have entered the ecosystem in the second half of the last century. The potential of biodegradative bacteria in the development of bioremediation processes for bio-mineralization of organic pollutants and bio-immobilization of inorganic compounds has not yet been fully realized, but examples of both types of strategies have been reported. As a consequence, microorganisms have only been exposed to such compounds for a short period on the evolutionary timescale. As gene

Conclusion

The production and usage of chlorophenolic compounds in industries has led to the entry of many xenobiotics into the environment. Chlorophenolic compounds are recalcitrant to biodegradation and therefore persistent in the environment. However, microorganisms exposed to these synthetic chemicals have evolved the ability to biodegrade some of them. Thus, such biological degradation can be exploited to alleviate environmental pollution problems. The pathways by which a given compound is degraded

Acknowledgements

This study was supported by the National Research Foundation (NRF) of South Africa and the University of KwaZulu-Natal (Postdoctoral Fellowship and Competitive Research Grant).

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