Appl Microbiol Biotechnol (2009) 84:205216 DOI 10.

1007/s00253-009-2094-5

MINI-REVIEW

Bioremediation of the organochlorine pesticides, dieldrin and endrin, and their occurrence in the environment
Emiko Matsumoto & Youhei Kawanaka & Sun-Ja Yun & Hiroshi Oyaizu

Received: 11 May 2009 / Revised: 15 June 2009 / Accepted: 15 June 2009 / Published online: 4 July 2009 # Springer-Verlag 2009

Abstract Dieldrin and endrin are persistent organic pollutants that cause serious environmental problems. Although these compounds have been prohibited over the past decades in most countries around the world, they are still routinely found in the environment, especially in the soil in agricultural fields. Bioremediation, including phytoremediation and rhizoremediation, is expected to be a useful cleanup method for this soil contamination. This review provides an overview of the environmental contamination by dieldrin and endrin, along with a summary of our current understanding and recent advances in bioremediation and phytoremediation of these pollutants. In particular, this review focuses on the types and abilities of plants and microorganisms available for accumulating and degrading dieldrin and endrin. Keywords Bioremediation . Phytoremediation . Dieldrin . Endrin . Persistent organic pollutants

Introduction The organochlorine pesticides, dieldrin and endrin, have a long history of use in the control of agricultural pests around the world. Although dieldrin and endrin are very efficient insecticides, their use has been prohibited in many countries since the 1970s due to their high toxicity and long persistence in the environment. However, these pesticides continue to be detected in a wide variety of environments, especially in the soils of agricultural fields in which these pesticides were used previously (Manirakiza et al. 2003; Hashimoto 2005; Wan et al. 2005; Gonalves and Alpendurada 2005; Hilber et al. 2008). Therefore, contamination with dieldrin and endrin is still a serious environmental problem, and an efficient method for remediation is required. Bioremediation, including phytoremediation and rhizoremediation, is expected to be a useful cleanup method for soil contaminated by persistent organic pollutants (POPs), including dieldrin and endrin (Lal and Saxena 1982; Mohn and Tiedje 1992; Hiraishi 2003; Otsubo et al. 2004; Philips et al. 2005; Pilon-Smits 2005). Bioremediation has a number of advantages over thermal and some physicochemical techniques in terms of cost and preservation of soil condition suitable for plant growth. The maintenance of soil function is of particular importance in agricultural fields. Biodegradation of dieldrin and endrin was reviewed in 1982 (Lal and Saxena 1982), but there have been no subsequent reviews of biodegradation research for these compounds. This review examines recent research regarding (1) dieldrin and endrin residues in the environment, (2) the potential of plants for phytoremediation of these pesticides, and (3) the potential of anaerobic and aerobic microorganisms for bioremediation of these pesticides.

E. Matsumoto (*) : Y. Kawanaka : S.-J. Yun The Institute of Basic Environmental Research, Environmental Control Center Co., Ltd., 323-1 Shimo-ongata, Hachioji-shi, Tokyo 192-0154, Japan e-mail: ematsumoto@kankyo-kanri.co.jp H. Oyaizu Biotechnology Research Center, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan

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Physical and chemical properties The chemical structures of dieldrin and endrin are shown in Fig. 1. Dieldrin (CAS number: 60-57-1) is a colorless crystalline compound (IPCS 1998), and technical dieldrin (95%) is a light-tan compound with mild odor (WHO/IPCS 1989). Dieldrin remains a solid at ambient temperature with a melting point of 175176C, and its vapor pressure is 0.4 mPa at 20C. It is practically insoluble in water (0.186 mg/L at 20C) but is moderately soluble in aromatic hydrocarbons, halogenated hydrocarbons, ethers, esters, ketones, and alcohols. It has a high octanolwater partition coefficient (log Kow =6.2; IPCS 1998). Endrin (CAS number: 72-20-8) is a white to light-tan crystalline compound with mild odor (WHO/IPCS 1992). It has a melting point of 226230C, with vapor pressure and water solubility of 0.036 mPa and 0.230 mg/L at 25C (practically insoluble), respectively. Endrin is quite soluble in acetone, benzene, carbon tetrachloride, and xylene and moderately soluble in aliphatic hydrocarbons. It has a high octanolwater partition coefficient (log Kow =5.34; IPCS 2000).

Residues of dieldrin and endrin in the environment Dieldrin and endrin are very persistent in the environment. Therefore, although these pesticides have been prohibited over the past several decades in most countries around the world, they are still found in many environments, such as soil, sediment, and groundwater. The recent data regarding environmental contamination by dieldrin and endrin are summarized in Table 1. High levels of these pesticide residues have been found in the soil in agricultural and horticultural fields (Singh 2001; Manirakiza et al. 2003; Wan et al. 2005; Gonalves and Alpendurada 2005; Hilber et al. 2008). Moreover, several studies have indicated serious contamination by these pesticides of the water environment around agricultural fields, including groundwater (Singh 2001; Singh et al. 2006), surface water (Matin
Cl Cl

et al. 1998), and ditch water (Wan et al. 2005). Although the half-lives of dieldrin and endrin in soil differ to some extent among reports, most studies have shown that these pesticides are highly persistent in soil. Meijer et al. (2001) evaluated the persistence of various organochlorine pesticides in soil using the data of their concentration changes in soil in the UK over a period of 22 years. The calculations showed that the half-life of dieldrin in soil was about 25 years. McDougall et al. (1995) followed the decline of dieldrin in soil in the subtropical environment over 140 weeks and calculated the half-life of dieldrin as 241 41 weeks (4.6 0.8 years). Donoso et al. (1979) reported that the half-life of endrin in soil ranged up to 12 years. Dieldrin and endrin residues in agricultural fields cause contamination of not only the water environment but also of crops grown in contaminated soil. High levels of these pesticides have been detected in a variety of crops around the world. In Togo, West Africa, dieldrin and endrin residue levels of 39.50 and 13.16 ng/g, respectively, were found in cowpea and a dieldrin residue level of 18.09 ng/g was found in maize (Mawussi et al. 2009). In Serbia, a dieldrin residue level of 573 ng/g was reported in wheat (krbi 2007). In Nigeria, dieldrin residues of 680 ng/g were found in tubers (Adeyeye and Osibanjo 1999). Other researchers have also reported residues of these pesticides in cucumbers in Japan (Hashimoto 2005), winter squash in the USA (Johgenson 2001), and vegetables such as spinach, garlic leaf, and pumpkin in China (Gao et al. 2005).

Bioremediation of dieldrin and endrin Phytoremediation Phytoremediation is defined as the use of plants to extract, degrade, or immobilize contaminants, including recalcitrant organic compounds or heavy metals in the environment. This remediation method has many advantages compared to other methods. The main advantages of phytoremediation are that: (1) it is far less disruptive for the environment, (2) it has better public acceptance, and (3) it avoids the need for excavation and heavy traffic (Macek et al. 2002). The most important aspect of phytoremediation is to find accumulator plants that show effective uptake of target contaminants. Although there have been few studies on phytoremediation of dieldrin and endrin, cucurbits have attracted attention because of their high-level accumulation ability. Otani et al. (2007) compared the uptake of dieldrin and endrin of 32 plant species of arable crops in 17 families grown in contaminated soil and demonstrated that the family Cucurbitaceae took up more dieldrin and endrin than the others. Among the cucurbits, zucchini showed the highest uptake level. Other than cucurbits, only jute in the

Cl Cl Cl Cl

Cl Cl Cl O Cl

Cl

Cl

O
Endrin

Dieldrin
Fig. 1 Chemical structures of dieldrin and endrin

Table 1 Concentrations of dieldrin and endrin in the environmental samples Type of sample n n Mean 41 10 9 1.64 60b 0.2 ND130 Range Hilber et al. 2008 Manirakiza et al. 2003 Wang et al. 2007a Gonalves and Alpendurada 2005 Harner et al. 1999 36 36 36 70b 70b 40b ND110 ND310 ND50 Wan et al. 2005 Mean Soil (horticultural fields) Soil (agricultural fields) 41 10 43b 12.0 ND140 ND88.2 Range Concentrationa Concentrationa Dieldrin Endrin Reference

Location

Switzerland BHG, Gambia

Appl Microbiol Biotechnol (2009) 84:205216

Taihu, China North Portugal

Alabama, USA

Soil Soil Soil Soil Soil 133435 255466 147408 ND23.8

(agricultural (agricultural (agricultural (agricultural (agricultural

fields, 0-20 cm) fields, surface) fields, 10 cm) fields, 20 cm) fields)

9 4 4 4 36

3.01 286 340 267 5.19

Lower Fraser Valley, Canada

Agra, India

Singh 2001 McDougall et al. 1995 Jiries et al. 2002 Shegunova et al. 2007 Ozkoc et al. 2007 Hong et al. 2006 Wang et al. 2007b Zhang et al. 2002 Malik et al. 2009 Hung and Thiemann 2002 Lalah et al. 2003 Matin et al. 1998 Singh et al. 2006

New South Wales, Australia Karak, Jordan Czech Republic Black Sea, Turkey South Korea Daliaohe River, China Wuchuan river, China

Gomti River, India

Red River, Vietnam

36 36 36 150 105 3 45 9 4 138 12 8 8 8 8 11 11 9 4 138 12 8 8 8 8 11 11 6 640 830b 200b 1020,000 203,000 1.05b 8.2b 0.02 0.29b 0.06 7.15 0.54 0.17 34.8b 26.0b 484 3 24 24

450b 240b 60b 780 230 80 12.6 1.78 4.3b 0.08 0.05b 0.06 6.98 0.19 5.72 4.92b 5.77b

ND2,310 ND1,180 ND320 2501,340 91471 40110 1.137.6 0.582.78 ND5.0 ND1.12 ND0.07 0.030.24 1.7821.1 ND1.65 ND22.5 ND14.2 ND18.6

ND1.20 ND11.7 ND0.41 ND0.52 0.020.13 1.9026.4 ND12.0 ND4.25 ND169 ND99.6

Tana River, Kenya Gaibanda, Bangladish Varanasi, India

Soil (agricultural fields) Sediment (ditch sediment) Water (ditch water) Soil (agricultural fields) Ground water (agricultural fields) Soil (paddock) Soil (wastewater disposal sites) Soil (mountain area) Sediment (coast) Sediment (coastal region) Sediment (river) Sediment (river) Water (river) Sediment (river) Water (river) Water (river, dry season) Water (river, rainy season) Water (river) Surface water (crop fields) Ground water (rural area) Ground water (urban area)

n Number of samples

Concentration in soil and sediment (ng/g) and in water (ng/L)

Shown is mean of positive findings 207

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Appl Microbiol Biotechnol (2009) 84:205216

family Tiliaceae took up both dieldrin and endrin, while the other 15 families showed negligible uptake. However, noncucurbits, such as komatsuna (Japanese mustard spinach), soybean, and tomato plants, which do not usually accumulate dieldrin and endrin in soil, could absorb free dieldrin and endrin in quartz sand culture that shows low capability for adsorbing these compounds to sand itself. Other studies also indicated that several cucurbits have the unique ability to remove and accumulate dieldrin in soil (Lichtenstein et al. 1965; Johgenson 2001). Johgenson (2001) reported that dieldrin in soil was readily absorbed into the pulp of vegetables, such as squash, melons, and cucumbers. In general, organic compounds that have high log Kow and Koc values, such as dieldrin and endrin, adsorb strongly to soil and their water solubilities are very low. Therefore, it was anticipated that plants were unlikely to take up such compounds from soil. However, cucurbits were found to be an exception and readily take up such compounds in soil and translocate them to the leaves and fruits. Interestingly, as shown in Table 2, cucurbits show uptake from contaminated soil of not only dieldrin and endrin but also other highly hydrophobic POPs, such as polychlorinated dibenzo-p-dioxins and dibenzofurans (Hlster et al. 1994; Inui et al. 2008), PCBs (White et al. 2006; Inui et al. 2008), DDT and its metabolites (White 2001; White et al. 2003a; Lunney et al. 2004), chlordane (Mattina et al. 2000, 2004), HCB (Ecker and Horak 1994), heptachlor (Lichtenstein et al. 1965), and heptachlor epoxide (Campbell et al. 2009). Although the reason why cucurbits, such as zucchini and cucumber, have the ability to take up and translocate highly persistent hydrophobic contaminants, such as dieldrin and endrin, from soil into plants is unclear, a number of hypotheses have been proposed. The uptake of organic compounds by plants occurs via a number of pathways (Collins et al. 2006). The accumulation of hydrophobic organic compounds in soil into plants takes place via a pathway consisting of four key steps: (1) desorption from soil, (2) root uptake from soil solution, (3) translocation into aerial parts within the xylem, and (4) metabolic stability in plants (Collins et al. 2006; Inui et al. 2008). It is suggested that cucurbits absorb POPs by these processes because these compounds were detected in the xylem sap and the tissues of aerial parts that were grown without contact with contaminated soil (Lichtenstein et al. 1965; Hlster et al. 1994; Lunney et al. 2004; Mattina et al. 2004). Previous studies suggested that cucurbit plants may produce molecules in their root exudates that help to desorb and solubilize hydrophobic compounds from soil particles, rendering them more available for uptake by the plant. Root exudates from Cucurbita showed marked differences in composition in comparison to those from other plant species (Richardson et al. 1982). They have high protein content, low total sugar content, and a high percentage of

monosaccharides in sugar. In most other plant exudates, the proportions of proteins and sugars are reversed and monosaccharide sugars are essentially absent. These unique root exudates of Cucurbita may be involved in its unique translocation system that differs from other plant species. In addition, some studies showed that incorporation of lowmolecular-weight organic acids (LMWOAs) such as citric acid, which are released in root exudates, to soil increased the POP uptake by cucurbits (White et al. 2003b, 2006). These data indicated that LMWOAs might also be important contaminant-solubilizing substances in the root exudates of cucurbits. It was reported that there were correlations between the concentrations of LMWOAs in the exudates from cucurbit roots and concentrations of desorbed chlordane in the soil solution (Mattina et al. 2007). Therefore, it seems that LMWOAs play a role in contaminant desorption from soil. Another hypothesis is the presence of the binding compounds capable of increasing solubility of hydrophobic pollutants in root extracts and leaf tissues of cucurbit (Campanella and Paul 2000). It is suggested that there are compounds in root exudates of zucchini and melon that can reversibly bind to hydrophobic sites of pollutants, resulting in changes in solubility properties, and one of these compounds would be of a proteinic nature. Recent grafting experiments provided interesting information on phytoaccumulation, indicating that rootstocks are likely to play an important role in regulation of phytoaccumulation. Otani and Seike showed that rootstock varieties substantially influenced dieldrin and endrin concentrations in grafted plants (Otani and Seike 2006) and that the dieldrin concentration in cucumber fruits grafted on lowuptake rootstock was considerably decreased compared with those grafted on high-uptake rootstock (Otani and Seike 2007). Moreover, other grafting experiments showed that the absorption of chlordane in xylem sap and aerial plant tissue depended on the genotype of rootstock plants (Mattina et al. 2007). There has been remarkable progress in research regarding the accumulation of organic compounds by cucurbits. The information provided by these studies will facilitate a better understanding of the potential for soilplant transfer of these compounds in the future. It is expected to establish an effective method for phytoremediation of POPscontaminated soil using cucurbits. Bioremediation under anaerobic conditions Studies on biodegradation of dieldrin and endrin began in the late 1960s. Many studies were reported regarding the aerobic biodegradation of dieldrin and endrin. Most organochlorine compounds, such as dieldrin and endrin, were shown to be persistent in aerobic environments. In

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209

contrast, it was reported that degradation of endrin proceeded under anaerobic conditions (Siddarame Gowda and Sethunathan 1977). Therefore, studies on anaerobic biodegradation of dieldrin and endrin began in the late 1980s. Biodegradation studies of dieldrin and endrin under anaerobic conditions are summarized in Table 3. Maule et al. (1987) reported that anaerobic microbial populations developed from soil, freshwater mud, sheep rumen, and chicken litter could transform dieldrin to monodechlorinated products. These populations monodechlorinated dieldrin at the methylene bridge carbon atom and produced endo products, syn- and anti-monodechlorodieldrin. The anaerobic population grown in the presence of formate showed the most rapid dechlorination of dieldrin and endrin. Three isolates from this culture, classified as the genus Clostridium, were capable of dieldrin dehalogenation, although the dehalogenation rate by each isolate was much less than that by the parent population. This study showed that biodegradation capacity of microbial populations was quantitatively and qualitatively greater than that of isolated strains. Baczynski et al. (2004) reported that methanogenic granular sludge could dechlorinate dieldrin and endrin. Degradation of these compounds by the sludge differed from that reported in previous studies in some aspects. There were not only two monodechlorinated metabolites of dieldrin that were found in the previous study but also three additional metabolites, i.e., aldrin and two monodechlorinated metabolites of aldrin. Transformation of dieldrin to aldrin through epoxide reduction was also observed in another study using anaerobic enrichment culture obtained from river sediment (Chiu et al. 2005). In addition, only two monodechlorinated metabolites of endrin were observed previously, whereas three monodechlorinated and three didechlorinated metabolites of endrin were found. These studies clearly indicated the potential of anaerobic microorganisms to catalyze reductive dehalogenation of dieldrin and endrin. Recently, Watanabe and Yoshikawa (2008) reported anaerobic microbial strains that have the remarkable ability to degrade various types of POPs, such as HCB, dieldrin, endrin, aldrin, and heptachlor. These strains had novel morphological and physiological characters. Although the metabolic pathways of dieldrin and endrin by these microorganisms are not yet clear, they reported that similar anaerobic microorganisms isolated from PCBcontaminated sediment using the same enrichment and isolation method were capable of dechlorinating HCB (Watanabe et al. 2007). Bioremediation under aerobic conditions Studies of the degradation of dieldrin and endrin by aerobic microorganisms performed up to 1980 were reviewed in

detail by Khan (1980) and Lal and Saxena (1982). Aerobic dieldrin- and endrin-degrading bacteria are summarized in Table 4. Pseudomonas sp., Bacillus sp., Trichoderma viride (Matsumura and Boush 1967), Aerobacter aerogenes (Wedemeyer 1968), Mucor alternans (Anderson et al. 1970), and Trichoderma koningi (Bixby et al. 1971) were isolated as dieldrin-degrading microorganisms. In contrast, there have been few studies of endrin degradation by aerobic microorganisms. Pseudomonas sp., Micrococcus sp., and several other unidentified bacteria and yeast (Matsumura et al. 1971) were found to be endrindegrading microorganisms. Another study indicated that dieldrin-degrading microorganisms, such as Pseudomonas sp., Micrococcus sp., Arthrobacter sp., Bacillus sp., and T. viride, were also able to degrade endrin (Patil et al. 1970). Although the metabolic pathways of dieldrin and endrin by these microorganisms are still unclear, there have been reports of the conversion of these pesticides to watersoluble and organic solvent-soluble compounds. The principal compound among the organic solvent-soluble metabolites produced by Pseudomonas sp., Bacillus sp. (Matsumura and Boush 1967), A. aerogenes (Wedemeyer 1968), and T. viride (Matsumura and Boush 1968) was reported to be 6,7-trans-dihydroxydihydroaldrin. This conversion would be catalyzed by epoxide hydrolase, although there have been no studies focusing on the enzyme responsible for this conversion. Moreover, photodieldrin, previously reported as a major product converted from dieldrin by the action of sunlight, was also reported as the metabolic product of dieldrin by aerobic microorganisms (Matsumura et al. 1970). Among the transformation products of endrin, only ketoendrin was identified, and aldehyde and ketone derivatives of endrin were also demonstrated (Matsumura et al. 1971). To achieve in situ bioremediation, bacteria should show degradation capability in the natural environment equivalent to that in the laboratory. However, there have been no reports that augmented degrading microorganisms can demonstrate their ability to degrade dieldrin and endrin in soil. In contrast, M. alternans was reported to lose its ability to degrade dieldrin when added to soil contaminated with dieldrin (Anderson et al. 1970). The efficiency of degrading microorganisms introduced into contaminated sites depends on many factors. In particular, the pollutant characteristics (e.g., concentration, bioavailability, and microbial toxicity), the physicochemical characteristics of the environment, microbial ecology (e.g., predatory and competition), the characteristics of the degrading microorganisms themselves, and methodology for site remediation are dominant factors (Goldstein et al. 1985; Vogel 1996; Fantroussi and Agathos 2005). Therefore, it is important to understand the characteristics of the microorganisms and appropriate environmental conditions to achieve optimal degradation

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Table 2 Uptake of POPs from soil by cucurbits Target compound Initial soil conc.a 594/58 594/58 594/58 594/58 594/58 594/58 1,365d 2,870d 940d 148 Shoots 590c/55c Experiments were conducted in soil treated with dieldrin or heptachlor. Fruits were harvested when they reached 5 to 6 in. long Shoots 1,100c/36c Shoots 1,000c/77c Shoots 1,000c/25c Shoots 1,200c/73c Shoots 1,704/140c Plant part Uptake amountb Experimental design

Reference

Plant name (scientific name and cultivar name) Dieldrin/Endrin Dieldrin/Endrin Dieldrin/Endrin Dieldrin/Endrin Dieldrin/Endrin Dieldrin/Endrin Dieldrin Heptachlor Heptachlor epoxide PCDD+PCDF

Otani et al. 2007

Seedlings n 1 20 were planted in each of three pots (400 mL) containing 270 g of soil contaminated with dieldrin and endrin. Plants were grown in a greenhouse at 25C under natural light for 21 days

Lichtenstein et al. 1965

Zucchini (Cucurbita pepo L. Black Tosca) Cucumber (Cucumis sativus L. Sharp-1) Pumpkin (Cucurbita moschata Duch. Hayato) Winter squash (Cucurbita maxima Duch. Miyako) Figleaf squash (Cucurbita ficifolia Bouch. Kurodane) Watermelon (Citrullus lanatus Matsum. et Nakai Kyougou) Cucumber (Cucumis sativus L. Straight Eight)

Hlster et al. 1994 PCDD+PCDF 148

Zucchini (Cucurbita pepo L. convar. giromontiina Diamant F1)

Pumpkin (Cucurbita pepo L. Gelber Zentner)

43 32 23 17 68 48 18.1 20.5 22.0 11.8 3.3

Experiments were carried out in highly PCDD/PCDFcontaminated areas. Zucchini plants were cultivated conventionally in the contaminated soil. On some of the plants, fruits were grown without soil contact. Pumpkin and cucumbers were grown in the same plot. Fruits were harvested when they were ripe for consumption (6 weeks) 3.0 2.4 0.2

Cucumber (Cucumis sativus L. Delikatess)

PCDD+PCDF

148

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White et al. 2006

Zucchini (Cucurbita pepo L. Black Beauty)

PCB (Arochlor 1268)

105,000

Whole fruite Whole fruitf Whole fruite Whole fruitf Whole fruite Whole fruitf Fruitse Fruitsf Leaves Fruits (outer parts) Fruits (inner parts) Leaves Fruits (outer parts) Fruits (inner parts) Leaves Roots Stems Leaves Fruit 2.7 430,000g 22,000g 9,800g 6,700g

One seedling was planted in a pot (5544 cm) containing 70 kg of soil contaminated with Arochlor 1268. Pots were maintained outside for 70 days

Table 2 (continued) Target compound Initial soil conc.a 225397 Field experiments were conducted at a farm in areas contaminated with p,p-DDE (50500 g/kg). Experimental plots were 22 m. Zucchini and pumpkin seeds were planted in three separate mounds per plot. This resulted in four to five separate zucchini or pumpkin plants per plot. Plants were cultivated for 83 days Plant part Uptake amountb Experimental design

Reference

Plant name (scientific name and cultivar name) p,p-DDE

White 2001

Zucchini (Cucurbita pepo L. Raven)

Appl Microbiol Biotechnol (2009) 84:205216

Pumpkin (Cucurbita pepo L. Baby Bear )

p,p-DDE

155397

Roots Stems Leaves Whole fruit Flesh Peel Roots Stems Leaves Whole fruit

8,300h 9,600h 300h 210h 22h 360h 7,100h 4,300h 200h 29h

Lunney et al. 2004 150 DDTi 3,700 150 Chlordane 3,350

Zucchini (Cucurbita pepo L. Senator hybrid)

DDTi

3,700

Flesh Peel Roots Shoots Roots Shoots

Trace levelh 350h 2,273 2,991 214 99

Pumpkin (Cucurbita pepo L. Howden)

Seedlings were planted separately in bottom-perforated 28 1 6 cm trays with a soil depth of 6 cm. All trays were covered with laboratory Parafilm to limit volatilization. Plants were grown in a greenhouse at 232C in soil contaminated with DDT and its metabolites, DDD and DDE, for 50 days

Mattina et al. 2004 Heptachlor epoxide 376 Vine

Zucchini (Cucurbita pepo L. Black Beauty)

Roots Shoots Roots Shoots Roots Aerial tissue 1,000j

2,393 4,262 323 375 37,60052,000 2,2203,900

Campbell et al. 2009

Summer squash (Lagenaria siceraria Hyotan)

Rhizotron was filled with 3.5 kg of soil contaminated with chlordane and placed in a greenhouse for 8 weeks Seedlings were planted in pots containing 13.6 kg of soil contaminated with heptachlor and heptachlor epoxide. Plants were cultivated for 13 weeks

Concentrations of compounds other than PCDD and PCDF (g/kg) and those of PCDD and PCDF (ng I-TEQ/kg)

Uptake amounts of compounds other than PCDD and PCDF (g/kg) and those of PCDD and PCDF (ng I-TEQ/kg)

Approximated from the graph in Fig. 1 of Otani et al. (2007)

Concentration in the soil at harvest

Fruits were grown with soil contact

Fruits were grown without soil contact

Approximated from the graph in Figure 3 of White et al. (2006)

Approximated from the graph in Figure 2 of White (2001)

DDT refers to all of DDT, DDD, and DDE

Approximated from the graph in Figure 3 of Campbell et al. (2009) 211

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Table 3 Degradation of dieldrin and endrin by microorganisms under anaerobic conditions Growth substrate Target compound Initial concentration (g/mL) 10 96 7 days syn- and antimonodechlorodieldrin % Removal Incubation time Metabolites produced Reference

Anaerobic communities or microorganisms

Origin

Enriched anaerobic microbial population Dieldrin Endrin Monodechlorinated product Dieldrin Dieldrin 9 88 3 months 10 80 5495 days 10 10 90 99.7 4 days 4 days

Soil, freshwater mud, sheep rumen, chicken litter

Sodium acetate, sodium formate, yeast extract, peptone Formate Formate Formate

Dieldrin

Maule et al. 1987

Clostridium spp.

Batch culture with methanogenic granular sludge Endrin 7 99 28 days

Above anaerobic microbial population Methanogenic granular sludge

Maule et al. 1987 Baczynski et al. 2004

Enriched anaerobic microbial population

River sediment contaminated with organochlorine pesticides (dieldrin included)

Yeast extract Yeast extract Yeast extract

Two monodechlorinated products, aldrin, two monodechlorinated derivatives of aldrin Three monodechlorinated products, three didechlorinated products Aldrin Aldrin Aldrin

Chiu et al. 2005

Batch culture with digesting sludge Unidentified HCBdegrading bacteria Dieldrin Endrin 100 100

Digesting sludge

Dieldrin Dieldrin Dieldrin Dieldrin 24.467.2 1.260.0

0.5 2.0 10 50

100 100 100 26

Paddy field soil uncontaminated and contaminated with PCB

70 days 84 days 140 days >75 days (Lag) 14 days 14 days

Battersby and Wilson 1989 Watanabe and Yoshikawa 2008

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Appl Microbiol Biotechnol (2009) 84:205216 Table 4 Degradation of dieldrin and endrin by microorganisms under aerobic conditions Aerobic community or microorganisms Pseudomonas sp. Bacillus sp. Trichoderma viride Aerobacter aerogenes Mucor alternans Trichoderma koningi Pseudomonas sp. Bacillus sp. Micrococcus sp. Unidentified yeast Phanerochaete chrysosporium Trichoderma harzianum ECH enrichment culture Burkholderia sp. Cupriavidus sp. Source of isolation Target compound Reference

213

Soil heavily contaminated with various insecticides from dieldrin factory yards and orchard area Soil heavily contaminated with various insecticides from peach orchard Soil heavily contaminated with various insecticides from the dieldrin factory yards and apple orchard

Dieldrin, endrin Dieldrin, endrin Dieldrin, endrin Dieldrin Dieldrin Dieldrin Endrin Endrin Endrin Endrin Dieldrin Dieldrin Dieldrin, endrin Dieldrin, endrin Dieldrin, endrin

Matsumura and Boush 1967; Patil et al. 1970

Cranberry mold Soil heavily contaminated with various insecticides from dieldrin factory yards, orchard area, and farm Soil heavily contaminated with various insecticides from apple orchard area Soil heavily contaminated with various insecticides from apple orchard area Soil heavily contaminated with various insecticides from farm Banana plantation field soil Uncontaminated forest soil Uncontaminated forest soil Uncontaminated forest soil

Wedemeyer 1968 Anderson et al. 1970 Bixby et al. 1971 Matsumura et al. 1971

Kennedy et al. 1990 Katayama and Matsumura 1993 Matsumoto et al. 2008

ability. Furthermore, it is necessary to isolate new competitive microorganisms that can degrade dieldrin and endrin efficiently in natural environments as well as in the laboratory. Matsumoto et al. (2008) attempted to isolate dieldrinand endrin-degrading microorganisms. The conventional enrichment method requires considerable time and labor, but is not so efficient. Thus, an efficient method for isolation of dieldrin- and endrin-degrading bacteria from soil was developed using 1,2-epoxycyclohexane (ECH), a structural analog of dieldrin and endrin (Matsumoto et al. 2008). ECH was shown to be a useful growth substrate for selective isolation of microorganisms capable of degrading dieldrin and endrin. With this method, novel aerobic bacteria, Burkholderia sp. and Cupriavidus sp., with high degradation activity toward dieldrin and endrin were obtained. Moreover, the degradation efficiencies of dieldrin and endrin of the isolates were higher in the presence of ECH than in its absence. Under these conditions, the degradation efficiencies of the two isolates, Burkholderia sp. and Cupriavidus sp., were 49% and 38% toward dieldrin, respectively, and 51% and 40% toward endrin, respectively, for 14 days. Another study also indicated enhancement of the degradation activity of dieldrin in soil by addition of pesticide analogs (Hugenholtz and MacRae 1990). Therefore, pesticide analogs, such as ECH, are expected to be useful not only as substrates for isolation of

microorganisms capable of degrading dieldrin and endrin but also as soil amendments for enhancement of the microbial degradation activity toward these pesticides. The development of new sources of microbial degraders is also important to isolate new effective and functionally diverse microbial degraders. In previous studies, heavily contaminated soils with dieldrin and endrin were used to search for aerobic dieldrin- and endrin-degrading microorganisms (Matsumura and Boush 1967; Matsumura et al. 1971). However, some reports indicated that the bacterial community was much less diverse in contaminated soils than in uncontaminated soils (Konzdroj and van Elsas 2001; Gans et al. 2005; Ahn et al. 2006). These observations suggest that uncontaminated soils can be sources for screening of new degrading microorganisms. In fact, recent studies indicated that diverse microbial communities with the potential for degradation of POPs exist in soil and sediment that have not been subjected to contamination with these chemicals, such as PCBs (Baba et al. 2007; Macedo et al. 2007) and dieldrin and endrin (Matsumoto et al. 2008).

Conclusions Cucurbits have the ability to take up considerable amounts of dieldrin and endrin from contaminated soil. However,

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Appl Microbiol Biotechnol (2009) 84:205216 Bedford CT, Huston DH, Natoff IL (1975) The acute toxicity of endrin and its metabolites of rates. Toxicol Appl Pharmacol 33:114121 Bixby MW, Boush GM, Matsumura F (1971) Degradation of dieldrin to carbon dioxide by a soil fungus Trichoderma koningi. Bull Environ Contam Toxicol 6:491494 Campanella B, Paul R (2000) Presence, in the rhizosphere and leaf extracts of zucchini (Cucurbita pepo L.) and melon (Cucumis melo L.), of molecules capable of increasing the apparent aqueous solubility of hydrophobic pollutants. Int J Phytoremediation 2:145158 Campbell S, Arakaki AS, Li QL (2009) Phytoremediation of heptachlor and heptachlor epoxide in soil by Cucurbitaceae. Int J Phytoremediation 11:2838 Chiu TC, Yen JH, Hsieh YN, Wang YS (2005) Reductive transformation of dieldrin under anaerobic sediment culture. Chemosphere 60:11821189 Collins C, Fryer M, Grosso A (2006) Plant uptake of non-ionic organic chemicals. Environ Sci Technol 40:4552 Donoso J, Dorigan J, Fuller B, Gordon J, Kornreich M, Saari S, Thomas L, Walker P (1979) Reviews of the environmental effects of pollutants XIII Endrin. Oak Ridge National Laboratory, Oak Ridge (EPA-600/1-79-005) Ecker S, Horak O (1994) Pathways of HCB-contamination to oil pumpkin seeds. Chemosphere 29:21352145 Fantroussi SE, Agathos SN (2005) Is bioaugmentation a feasible strategy for pollutant removal and site remediation? Curr Opin Microbiol 8:268275 Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:13871390 Gao HJ, Jiang X, Wang F, Wang DZ, Bian YR (2005) Residual levels and bioaccumulation of chlorinated persistent organic pollutants (POPs) in vegetables from suburb of Nanjing, Peoples Republic of China. Bull Environ Contam Toxixol 74:673680 Georgacakis E, Khan MAQ (1971) Toxicity of the photoisomers of cyclodiene insecticides to freshwater animals. Nature 233:120 121 Goldstein RM, Mallory LM, Alexander M (1985) Reasons for possible failure of inoculation to enhance biodegradation. Appl Environ Microbiol 50:977983 Gonalves C, Alpendurada MF (2005) Assessment of pesticide contamination in soil samples from an intensive horticulture area, using ultrasonic extraction and gas chromatography-mass spectrometry. Talanta 65:11791189 Harner T, Wideman JL, Jantunen LMM, Bidleman TF, Parkhurst WJ (1999) Residues of organochlorine pesticides in Alabama soils. Environ Pollut 106:323332 Hashimoto Y (2005) Dieldrin residue in the soil and cucumber from agricultural field in Tokyo. J Pestic Sci 30:397402 Hilber I, Mder P, Schulin R, Wyss GS (2008) Survey of organochlorine pesticides in horticultural soils and there grown Cucurbitaceae. Chemosphere 73:954961 Hiraishi A (2003) Biodiversity of dioxin-degrading microorganisms and potential utilization in bioremediation. Microbes Environ 18:105125 Hong SH, Yim UH, Shim WJ, Li DH, Oh JR (2006) Nationwide monitoring of polychlorinated biphenyls and organochlorine pesticides in sediments from coastal environment of Korea. Chemosphere 64:14791488 Hugenholtz P, MacRae IC (1990) Stimulation of aldrin and dieldrin loss from soils treated with carbon amendments and saturated-ring analogues. Bull Environ Contam Toxicol 45: 223227 Hlster A, Muller JF, Marschner H (1994) Soil-plant transfer of polychlorinated dibenzo-p-dioxins and dibenzofurans to vegetables of

their mechanism of uptake for these compounds is still not completely understood. To achieve practical phytoremediation by cucurbits for dieldrin and endrin, it is necessary to elucidate the uptake mechanisms of cucurbits and determine the factors that can increase their uptake and translocation. On the other hand, for bioremediation, efficient dieldrinand endrin-degrading bacteria and communities have been reported. However, there have been no reports that these degrading microorganisms can demonstrate their ability to degrade dieldrin and endrin in soil and sediment environment to date. Therefore, it is important to confirm their degradation activity in actual contaminated environments and determine the appropriate environmental conditions to achieve optimal degradation ability. Further advances in research on metabolites and pathways for microbial metabolism of dieldrin and endrin are expected. The study of dieldrin and endrin metabolism by microorganisms is at a less advanced stage compared with that of PCB and HCH, for which metabolic pathways and degrading enzymes produced by microorganisms have been discussed in detail. For actual application of bioremediation on polluted sites, it is necessary that the metabolic products of dieldrin and endrin should be nontoxic or at least have low toxicity. Previous studies indicated that photodieldrin (Georgacakis and Khan 1971) and ketoendrin (Bedford et al. 1975) produced by aerobic microorganisms were more toxic than their parent compounds. Thus, it is important for biodegradation and toxicological studies to focus not only on the disappearance of dieldrin and endrin but also on the toxicity of metabolites to define the real environmental impact of these compounds.

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