Chlorinated Pharmaceutical and Personal Care Products

An expanding array of substances called 'Endocrine-disrupting compounds' (EDC) include chemicals of natural and anthropogenic origin. EDCs are widely distributed in the environment. They constitute a potential health risk to humans and aquatic life. Only a couple of EDCs are covered here. Triclosan is one such synthetic antimicrobial compound that is present in a wide range of health care products, such as tooth-paste, deodorant sticks and soaps. It has been detected in various environmental matrices due to its low degradation by conventional wastewater treatment processes. The fact, that triclosan shows remarkable toxicity towards bacteria, makes white rot fungi interesting candidates to test for biodegradation of this compound. Triclosan was degraded by seven strains of white rot fungi including P. chrysosporium ME 446, P. magnoliae, T. versicolor, I. lacteus, P. ostreatus, P. cinnabarinus, and D. squalens, while B. adusta was the only organism included in the screening that did not degrade triclosan (Cajthaml et al. 2009). I. lacteus and P. ostreatus were found to be the most efficient triclosan degraders with a degradation efficiency exceeding 90 and 80%, respectively.

In another study, triclosan was shown to inhibit the growth of T. versicolor over the first 3 d of incubation, but the ability of the fungus to transform triclosan to glucoside and xyloside conjugated forms and small amounts of 2,4-dichlorophenol lowered the toxicity due to triclosan and allowed the subsequent normal growth of the fungus (Hundt et al. 2000). The white rot fungus P. cinnabarinus also converted triclosan to the glucoside conjugate and additionally produced 2,4,4'-trichloro-2'-methoxydiphenyl (Hundt et al. 2000).

Several studies have focused on the applicability of purified laccases to oxidize and detoxify triclosan. The enzymatic transformation of triclosan by laccase was found to be optimal at pH 5 and 50°C and was negatively affected by the presence of sulfite, sulfide, cyanide, chloride, Fe(III) and Cu (II) ions that may be present in a wastewater matrix (Kim and Nicell 2006; Cabana et al. 2007). The use of polyethylene glycol (PEG) to prevent the inactivation of laccase resulted in an enhancement of triclosan degradation, but influenced negatively the toxicity of the treated solution (Kim and Nicell 2006). Immobilized laccase showed higher ability to degrade triclosan and had greater stability than free laccases (Cabana et al. 2009a, b). Degradation rates of triclosan by laccase were substantially improved through the use of laccase mediators (Murugesan et al. 2010). For example, * 90% triclosan degradation was observed in the presence of mediators, such as 1-hydroxybenzotriazole (HBT) and syringaldehyde (SYD). Other investigators did not see enhanced degradation of triclosan in the presence of mediators (Kim and Nicell 2006; Cabana et al. 2007). Two different mechanisms of triclosan degradation catalyzed by laccase were proposed. In the absence of redox mediators, laccase transformed triclosan to dimers, trimers and tetramers formed by oxidative coupling of the phenoxy radicals of triclosan (Cabana et al. 2007; Murugesan et al. 2010). Although the basic structure of triclosan was unaffected, laccase-mediated detoxification of triclosan was demonstrated using bacterial growth inhibition tests (Murugesan et al. 2010). In the presence of redox mediators HBT and SYD, the ether bond linkage of triclosan was cleaved producing 2,4-dichlorophenol, which was further dechlorinated through oligomerization reaction (in the case of HBT) or oxidative dechlorination to 2-chlorohydroquinone (in the case of SYD) (Murug-esan et al. 2010). Recently, direct dechlorination of triclosan resulting in the formation of dechlorinated oligomers was shown in the presence of laccases conjugated with chitosan (Cabana et al. 2010). MnP seems to be a more promising choice than laccase for triclosan degradation, evidenced from the higher degradation rates obtained with MnP than laccase only or laccase + HOBT (Inoue et al. 2010). However, the transformation products were not described. Algal and bacterial growth inhibition tests showed that triclosan treated with MnP results in greatly reduced toxicity in the effluent.

Clofibric acid (CA) is the pharmacologically active derivative of clofibrate and several other fibrates that are used as blood lipid regulators in human medicine. Limited removal of CA, that was observed in municipal wastewater treatment plants, deserves more attention because of the risk of CA passing later barriers in partly closed water cycles. Of the four white rot fungi screened for their ability to degrade CA, only T. versicolor was able to degrade nearly 90% of CA (8 mg l-1)

in defined liquid medium after 7 d (Marco-Urrea et al. 2009c); but three other fungi, P. chrysosporium, G. lucidum and I. lacteus, were unable to degrade CA under similar conditions. CA was not oxidized by the purified MnP or laccase even in the presence of redox mediators. However, CA degradation by T. versicolor cultures was inhibited by more than half in the presence of cytochrome P450 inhibitors piperonyl butoxide or 1-aminobenzotriazole, suggesting that P450 plays a role in CA degradation by this organism (Marco-Urrea et al. 2009c). Degradation of CA in cultures of T. versicolor was also attempted by inducing hydroxyl radicals, through the quinone redox cycling mechanism (Marco-Urrea et al. 2010). Based on time-course experiments, using 10 mg l-1 of CA, these cultures showed >80% degradations after 6 h of incubation. An intermediate showing hydroxyl-ation of the benzene ring of CA was detected early in the incubation, but it was not detectable in the cultures after 24 h (Marco-Urrea et al. 2010).

2.4 Conclusions

White rot fungi have become increasingly attractive as candidates for designing effective bioremediation strategies, because of the broad substrate specificity of the ligninolytic enzymes which enable these fungi to degrade or mineralize quite a broad spectrum of chloro-organics (and other environmental pollutants). Even though a large majority of the bioremediation studies to date were done with P. chrysosporium as the model, a greater number of other genera of white rot fungi have also been studied in recent years and this may help determine the right organism with the right characteristics for carrying out a desired bioremediation application. Basic studies designed to obtain a better understanding of the mechanisms of actions as well as the basic protein and gene structures of the major extracellular ligninolytic enzymes (LiP, MnP, VP, and laccase), that catalyze degradation of chloro-organics through free radical mediated reactions, have been described. Recent studies indicate that intracellular enzymes as exemplified by cytochrome P450 monooxygenases are widespread in white rot fungi and appear to be key players involved in the degradation of a number of the chloro-organic pollutants.

Although most studies on lab or field scale bioremediation were done using bacteria, white rot fungi are beginning to gain prominence in this area, because they offer a number of advantages over bacteria for biodegradation of chloro-organic environmental pollutants. For example, reductive dechlorination of toxic PCE and TCE by bacteria usually leads to accumulation of toxic cis-dichloro-ethylene and vinyl chloride in the environment, whereas white rot fungi not only can degrade PCE and TCE to less toxic intermediates, but also have the ability to mineralize TCE. Also, compared to most degradative enzymes of bacteria, the ligninolytic enzymes of white rot fungi are non-specific and allow these organisms to degrade several classes of organo-pollutants individually or in mixtures.

Most published studies on biodegradation of chloro-organo-pollutants have been carried out in defined or complex laboratory media or in small samples of autoclaved soils and the effect of temperature, pH, moisture, nutrient (mainly C, N and S) and oxygen concentration, and small molecular weight growth/enzyme inducers on the quantitative and qualitative production of degradative enzymes, and biochemical pathways for the degradation of various pollutants have been studied. However, less number of pilot scale or field scale studies have been done to date. Because of the great versatility of white rot fungi in degrading a broad array of environmental pollutants, it is important to study bioremediation applications on a larger scale using large bioreactors and contaminated soils, sediments, and effluent streams, and other pollutant sites. Some of these studies have been reviewed by Baldrian (2008) and he described some of the limitations for the practical applicability of white rot fungi for field scale bioremediations. The specific physico-chemical properties of some chloro-organics can also restrict the application of white rot fungi. For instance, some chloro-organics, such as PCE and TCE are highly volatile, have low solubility, and are denser than water and therefore, they accumulate in the form of pools in groundwater when released into the environment. In these environments, anoxic conditions are predominant and the white rot fungi which are aerobic would require oxygen and this may add to the costs. Successful use of immobilized enzymes of white rot fungi, such as LiP, MnP, and laccases for bioremediation would obviate some of the difficulties associated with the use of whole mycelia cells. In turn, this points to the importance of detailed characterization of the ligninolytic enzymes/isoenzymes produced by different strains or species of white rot fungi that offer the most promise for different bioremediation applications, because fungal strains vary a great deal in their repertoire of enzymes/isoenzymes. Recently, application of laccases immobilized on solid supports has been explored for the treatment of contaminated effluents in adapted bioreactors. In general, immobilization of laccase on solid supports allows enhanced enzyme stability and continuous utilization of the bio-catalyst for bioremediation applications. For successful bioremediation, white rot fungi should be able to survive and successfully compete with autochthonous soil flora for carbon, nitrogen, and other nutrient sources. Even though, woody materials are their natural substrates, recent studies indicate that several species of white rot fungi can survive in soil and their soil colonizing ability is comparable to those of soil-inhabiting basidiomycetes utilizing the available lignocellulosic and other substrates in soil. Also, some of the white rot fungi appear to compete well with the complex soil microbial flora.

White rot fungi are extraordinary in their versatility to degrade a large variety of complex and recalcitrant environmental pollutants that contaminate soil and groundwater ecosystems, constituting a potential danger to human and animal health. It is fairly well proven now that white rot (as well as some non-white rot fungi) have the ecological and biochemical capability to degrade important categories of toxic chloro-organic pollutants. There has been much progress in screening and identifying strains/species of white rot fungi isolated from different ecosystems that are increasingly more efficient than previously described organisms in degrading selected chloro-organic pollutants generated by different industrial processes. There has been also much advancement in our understanding of the basic physiology, biochemistry, and molecular biology of enzymes and enzyme systems involved in the degradation of chloro-organic pollutants by white rot fungi. Current genomics and proteomics tools offer significant opportunities to determine the role and interactions of known genes and for identifying new genes involved in degradation of chloro-organics by white rot fungi. This information would also be of great interest to monitor and better understand the behaviour of white rot fungi in soils and to use them more efficiently as the agents of biore-mediation in contaminated sites. More research is needed to obtain better understanding of the ecology, enzymology, genomics, and proteomics of some of the more important species of white rot fungi that appear more desirable from a bioremediation perspective. Despite of great promise of white rot fungi as biore-mediation agents, a number of challenges remain to be surmounted in translating the basic knowledge on these organisms into cost-effective practical bioremedia-tion applications.

Acknowledgments The authors wish to acknowledge past students, postdoctoral fellows, and visiting scientists in their labs who contributed to the research results presented in this chapter. C. A. Reddy is also grateful for the funding received from Department of Energy over the years that contributed in part to the research presented here.


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