bioremediation of the organochlorine pesticides, dieldrin

MINI-REVIEW

Bioremediation of the organochlorine pesticides, dieldrinand 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 pol-lutants that cause serious environmental problems. Al-though these compounds have been prohibited over thepast decades in most countries around the world, theyare still routinely found in the environment, especiallyin the soil in agricultural fields. Bioremediation, includ-ing phytoremediation and rhizoremediation, is expectedto be a useful cleanup method for this soil contamina-tion. This review provides an overview of the environ-mental contamination by dieldrin and endrin, along witha summary of our current understanding and recent ad-vances in bioremediation and phytoremediation of thesepollutants. In particular, this review focuses on the typesand abilities of plants and microorganisms available foraccumulating and degrading dieldrin and endrin.

Keywords Bioremediation . Phytoremediation . Dieldrin .

Endrin . Persistent organic pollutants

Introduction

The organochlorine pesticides, dieldrin and endrin, have along history of use in the control of agricultural pests aroundthe world. Although dieldrin and endrin are very efficientinsecticides, their use has been prohibited in many countriessince the 1970s due to their high toxicity and long persistencein the environment. However, these pesticides continue to bedetected in a wide variety of environments, especially in thesoils of agricultural fields in which these pesticides were usedpreviously (Manirakiza et al. 2003; Hashimoto 2005; Wan etal. 2005; Gonçalves and Alpendurada 2005; Hilber et al.2008). Therefore, contamination with dieldrin and endrin isstill a serious environmental problem, and an efficientmethod for remediation is required.

Bioremediation, including phytoremediation and rhizore-mediation, is expected to be a useful cleanup method for soilcontaminated by persistent organic pollutants (POPs), includ-ing dieldrin and endrin (Lal and Saxena 1982; Mohn andTiedje 1992; Hiraishi 2003; Otsubo et al. 2004; Philips et al.2005; Pilon-Smits 2005). Bioremediation has a number ofadvantages over thermal and some physicochemical tech-niques in terms of cost and preservation of soil conditionsuitable for plant growth. The maintenance of soil function isof particular importance in agricultural fields.

Biodegradation of dieldrin and endrin was reviewed in1982 (Lal and Saxena 1982), but there have been nosubsequent reviews of biodegradation research for thesecompounds. This review examines recent research regard-ing (1) dieldrin and endrin residues in the environment, (2)the potential of plants for phytoremediation of thesepesticides, and (3) the potential of anaerobic and aerobicmicroorganisms for bioremediation of these pesticides.

E. Matsumoto (*) :Y. Kawanaka : S.-J. YunThe Institute of Basic Environmental Research,Environmental Control Center Co., Ltd.,323-1 Shimo-ongata, Hachioji-shi,Tokyo 192-0154, Japane-mail: [email protected]

H. OyaizuBiotechnology Research Center, The University of Tokyo,1-1-1 Yayoi, Bunkyo-ku,Tokyo 113-8657, Japan

Appl Microbiol Biotechnol (2009) 84:205–216DOI 10.1007/s00253-009-2094-5

Physical and chemical properties

The chemical structures of dieldrin and endrin are shown inFig. 1. Dieldrin (CAS number: 60-57-1) is a colorlesscrystalline compound (IPCS 1998), and technical dieldrin(95%) is a light-tan compound with mild odor (WHO/IPCS1989). Dieldrin remains a solid at ambient temperature witha melting point of 175–176°C, and its vapor pressure is0.4 mPa at 20°C. It is practically insoluble in water(0.186 mg/L at 20°C) but is moderately soluble in aromatichydrocarbons, halogenated hydrocarbons, ethers, esters,ketones, and alcohols. It has a high octanol–water partitioncoefficient (log Kow=6.2; IPCS 1998).

Endrin (CAS number: 72-20-8) is a white to light-tancrystalline compound with mild odor (WHO/IPCS 1992).It has a melting point of 226–230°C, with vapor pressureand water solubility of 0.036 mPa and 0.230 mg/L at 25°C(practically insoluble), respectively. Endrin is quite solu-ble in acetone, benzene, carbon tetrachloride, and xyleneand moderately soluble in aliphatic hydrocarbons. It has ahigh octanol–water 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 prohibitedover the past several decades in most countries around theworld, they are still found in many environments, such assoil, sediment, and groundwater. The recent data regardingenvironmental contamination by dieldrin and endrin aresummarized in Table 1. High levels of these pesticideresidues have been found in the soil in agricultural andhorticultural fields (Singh 2001; Manirakiza et al. 2003;Wan et al. 2005; Gonçalves and Alpendurada 2005; Hilberet al. 2008). Moreover, several studies have indicatedserious contamination by these pesticides of the waterenvironment around agricultural fields, including ground-water (Singh 2001; Singh et al. 2006), surface water (Matin

et al. 1998), and ditch water (Wan et al. 2005). Althoughthe half-lives of dieldrin and endrin in soil differ to someextent among reports, most studies have shown that thesepesticides are highly persistent in soil. Meijer et al. (2001)evaluated the persistence of various organochlorine pesti-cides in soil using the data of their concentration changes insoil in the UK over a period of 22 years. The calculationsshowed that the half-life of dieldrin in soil was about25 years. McDougall et al. (1995) followed the decline ofdieldrin in soil in the subtropical environment over140 weeks and calculated the half-life of dieldrin as 241 ±41 weeks (4.6 ± 0.8 years). Donoso et al. (1979) reportedthat the half-life of endrin in soil ranged up to 12 years.

Dieldrin and endrin residues in agricultural fields causecontamination of not only the water environment but alsoof crops grown in contaminated soil. High levels of thesepesticides have been detected in a variety of crops aroundthe world. In Togo, West Africa, dieldrin and endrin residuelevels of 39.50 and 13.16 ng/g, respectively, were found incowpea and a dieldrin residue level of 18.09 ng/g wasfound in maize (Mawussi et al. 2009). In Serbia, a dieldrinresidue level of 5–73 ng/g was reported in wheat (Škrbić2007). In Nigeria, dieldrin residues of 6–80 ng/g werefound in tubers (Adeyeye and Osibanjo 1999). Otherresearchers have also reported residues of these pesticidesin cucumbers in Japan (Hashimoto 2005), winter squash inthe 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 recalcitrantorganic compounds or heavy metals in the environment.This remediation method has many advantages compared toother methods. The main advantages of phytoremediationare that: (1) it is far less disruptive for the environment, (2)it has better public acceptance, and (3) it avoids the needfor excavation and heavy traffic (Macek et al. 2002). Themost important aspect of phytoremediation is to findaccumulator plants that show effective uptake of targetcontaminants. Although there have been few studies onphytoremediation of dieldrin and endrin, cucurbits haveattracted attention because of their high-level accumulationability. Otani et al. (2007) compared the uptake of dieldrinand endrin of 32 plant species of arable crops in 17 familiesgrown in contaminated soil and demonstrated that thefamily Cucurbitaceae took up more dieldrin and endrinthan the others. Among the cucurbits, zucchini showed thehighest uptake level. Other than cucurbits, only jute in the

Dieldrin

O

Cl

ClCl

Cl

ClCl

O

Cl

ClCl

Cl

ClCl

Endrin

Fig. 1 Chemical structures of dieldrin and endrin

206 Appl Microbiol Biotechnol (2009) 84:205–216

Tab

le1

Con

centratio

nsof

dieldrin

andendrin

intheenvironm

entalsamples

Location

Typ

eof

sample

Dieldrin

End

rin

Reference

nCon

centratio

nan

Con

centratio

na

Mean

Range

Mean

Range

Switzerland

Soil(horticulturalfields)

4143

bND–1

4041

60b

ND–1

30Hilb

eret

al.20

08

BHG,Gam

bia

Soil(agriculturalfields)

1012

.0ND–8

8.2

100.2

Manirakizaet

al.20

03

Taihu

,China

Soil(agriculturalfields,0-20

cm)

93.01

91.64

Wanget

al.20

07a

North

Portugal

Soil(agriculturalfields,surface)

428

613

3–43

5Gon

çalves

and

Alpendu

rada

2005

Soil(agriculturalfields,10

cm)

434

025

5–46

6

Soil(agriculturalfields,20

cm)

426

714

7–40

8

Alabama,

USA


365.19

ND–2

3.8

Harneret

al.19

99

Low

erFraserValley,

Canada


3645

0bND–2

,310

3670

bND–110

Wan

etal.20

05Sedim

ent(ditchsediment)

3624

0bND–1

,180

3670

bND–3

10

Water

(ditchwater)

3660

bND–3

2036

40b

ND–5

0

Agra,

India


150

780

250–

1,34

0Singh

2001

Groun

dwater

(agriculturalfields)

105

230

91–4

71

New

Sou

thWales,Australia

Soil(paddo

ck)

380

40–110

McD

ougallet

al.19

95

Karak,Jordan

Soil(w

astewater

disposal

sites)

4512

.61.1–37

.6Jiries

etal.20

02

Czech

Repub

licSoil(m

ountainarea)

91.78

0.58–2

.78

91.05

bND–1

.20

Shegu

nova

etal.20

07

Black

Sea,Turkey

Sedim

ent(coast)

44.3b

ND–5

.04

8.2b

ND–11.7

Ozkoc

etal.20

07

Sou

thKorea

Sedim

ent(coastal

region

)13

80.08

ND–1

.12

138

0.02

ND–0

.41

Hon

get

al.20

06

Daliaoh

eRiver,China

Sedim

ent(river)

120.05

bND–0

.07

120.29

bND–0

.52

Wanget

al.20

07b

Wuchu

anriver,China

Sedim

ent(river)

80.06

0.03–0

.24

80.06

0.02–0

.13

Zhang

etal.20

02Water

(river)

86.98

1.78–2

1.1

87.15

1.90–2

6.4

Gom

tiRiver,India

Sedim

ent(river)

80.19

ND–1

.65

80.54

ND–1

2.0

Malik

etal.20

09Water

(river)

85.72

ND–2

2.5

80.17

ND–4

.25

Red

River,Vietnam

Water

(river,dryseason

)11

4.92

bND–1

4.2

1134

.8b

ND–1

69Hun

gandThiem

ann20

02Water

(river,rainyseason

)11

5.77

bND–1

8.6

1126

.0b

ND–9

9.6

TanaRiver,Kenya

Water

(river)

648

4Lalah

etal.20

03

Gaiband

a,Bangladish

Surface

water

(cropfields)

364

0Matin

etal.19

98

Varanasi,India

Groun

dwater

(rural

area)

2483

0b10–2

0,00

0Singh

etal.20

06Groun

dwater

(urban

area)

2420

0b20–3

,000

nNum

berof

samples

aCon

centratio

nin

soilandsediment(ng/g)

andin

water

(ng/L)

bSho

wnismeanof

positiv

efind

ings

Appl Microbiol Biotechnol (2009) 84:205–216 207

family Tiliaceae took up both dieldrin and endrin, while theother 15 families showed negligible uptake. However, non-cucurbits, such as komatsuna (Japanese mustard spinach),soybean, and tomato plants, which do not usually accumu-late dieldrin and endrin in soil, could absorb free dieldrinand endrin in quartz sand culture that shows low capabilityfor adsorbing these compounds to sand itself. Other studiesalso indicated that several cucurbits have the unique abilityto remove and accumulate dieldrin in soil (Lichtenstein etal. 1965; Johgenson 2001). Johgenson (2001) reported thatdieldrin in soil was readily absorbed into the pulp ofvegetables, such as squash, melons, and cucumbers. Ingeneral, organic compounds that have high log Kow and Koc

values, such as dieldrin and endrin, adsorb strongly to soiland their water solubilities are very low. Therefore, it wasanticipated that plants were unlikely to take up suchcompounds from soil. However, cucurbits were found tobe an exception and readily take up such compounds in soiland translocate them to the leaves and fruits. Interestingly,as shown in Table 2, cucurbits show uptake fromcontaminated soil of not only dieldrin and endrin but alsoother highly hydrophobic POPs, such as polychlorinateddibenzo-p-dioxins and dibenzofurans (Hülster 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 etal. 1965), and heptachlor epoxide (Campbell et al. 2009).

Although the reason why cucurbits, such as zucchini andcucumber, have the ability to take up and translocate highlypersistent hydrophobic contaminants, such as dieldrin andendrin, from soil into plants is unclear, a number ofhypotheses have been proposed. The uptake of organiccompounds by plants occurs via a number of pathways(Collins et al. 2006). The accumulation of hydrophobicorganic compounds in soil into plants takes place via apathway consisting of four key steps: (1) desorption fromsoil, (2) root uptake from soil solution, (3) translocationinto aerial parts within the xylem, and (4) metabolicstability in plants (Collins et al. 2006; Inui et al. 2008). Itis suggested that cucurbits absorb POPs by these processesbecause these compounds were detected in the xylem sapand the tissues of aerial parts that were grown withoutcontact with contaminated soil (Lichtenstein et al. 1965;Hülster et al. 1994; Lunney et al. 2004; Mattina et al.2004). Previous studies suggested that cucurbit plants mayproduce molecules in their root exudates that help to desorband solubilize hydrophobic compounds from soil particles,rendering them more available for uptake by the plant. Rootexudates from Cucurbita showed marked differences incomposition in comparison to those from other plantspecies (Richardson et al. 1982). They have high proteincontent, low total sugar content, and a high percentage of

monosaccharides in sugar. In most other plant exudates, theproportions of proteins and sugars are reversed andmonosaccharide sugars are essentially absent. These uniqueroot exudates of Cucurbita may be involved in its uniquetranslocation system that differs from other plant species. Inaddition, some studies showed that incorporation of low-molecular-weight organic acids (LMWOAs) such as citricacid, which are released in root exudates, to soil increasedthe POP uptake by cucurbits (White et al. 2003b, 2006).These data indicated that LMWOAs might also beimportant contaminant-solubilizing substances in the rootexudates of cucurbits. It was reported that there werecorrelations between the concentrations of LMWOAs in theexudates from cucurbit roots and concentrations of des-orbed chlordane in the soil solution (Mattina et al. 2007).Therefore, it seems that LMWOAs play a role in contam-inant desorption from soil. Another hypothesis is thepresence of the binding compounds capable of increasingsolubility of hydrophobic pollutants in root extracts and leaftissues of cucurbit (Campanella and Paul 2000). It issuggested that there are compounds in root exudates ofzucchini and melon that can reversibly bind to hydrophobicsites of pollutants, resulting in changes in solubilityproperties, and one of these compounds would be of aproteinic nature.

Recent grafting experiments provided interesting infor-mation on phytoaccumulation, indicating that rootstocks arelikely to play an important role in regulation of phytoaccu-mulation. Otani and Seike showed that rootstock varietiessubstantially influenced dieldrin and endrin concentrationsin grafted plants (Otani and Seike 2006) and that thedieldrin concentration in cucumber fruits grafted on low-uptake rootstock was considerably decreased comparedwith those grafted on high-uptake rootstock (Otani andSeike 2007). Moreover, other grafting experiments showedthat the absorption of chlordane in xylem sap and aerialplant tissue depended on the genotype of rootstock plants(Mattina et al. 2007).

There has been remarkable progress in research regard-ing the accumulation of organic compounds by cucurbits.The information provided by these studies will facilitate abetter understanding of the potential for soil–plant transferof these compounds in the future. It is expected to establishan effective method for phytoremediation of POPs-contaminated soil using cucurbits.

Bioremediation under anaerobic conditions

Studies on biodegradation of dieldrin and endrin began inthe late 1960s. Many studies were reported regarding theaerobic biodegradation of dieldrin and endrin. Mostorganochlorine compounds, such as dieldrin and endrin,were shown to be persistent in aerobic environments. In


contrast, it was reported that degradation of endrin pro-ceeded under anaerobic conditions (Siddarame Gowda andSethunathan 1977). Therefore, studies on anaerobic bio-degradation of dieldrin and endrin began in the late 1980s.

Biodegradation studies of dieldrin and endrin underanaerobic conditions are summarized in Table 3. Maule etal. (1987) reported that anaerobic microbial populationsdeveloped from soil, freshwater mud, sheep rumen, andchicken litter could transform dieldrin to monodechlori-nated products. These populations monodechlorinateddieldrin at the methylene bridge carbon atom and producedendo products, syn- and anti-monodechlorodieldrin. Theanaerobic population grown in the presence of formateshowed the most rapid dechlorination of dieldrin andendrin. Three isolates from this culture, classified as thegenus Clostridium, were capable of dieldrin dehalogena-tion, although the dehalogenation rate by each isolate wasmuch less than that by the parent population. This studyshowed that biodegradation capacity of microbial popula-tions was quantitatively and qualitatively greater than thatof isolated strains. Baczynski et al. (2004) reported thatmethanogenic granular sludge could dechlorinate dieldrinand endrin. Degradation of these compounds by the sludgediffered from that reported in previous studies in someaspects. There were not only two monodechlorinatedmetabolites of dieldrin that were found in the previousstudy but also three additional metabolites, i.e., aldrin andtwo monodechlorinated metabolites of aldrin. Transforma-tion of dieldrin to aldrin through epoxide reduction wasalso observed in another study using anaerobic enrichmentculture obtained from river sediment (Chiu et al. 2005). Inaddition, only two monodechlorinated metabolites of endrinwere observed previously, whereas three monodechlori-nated and three didechlorinated metabolites of endrin werefound. These studies clearly indicated the potential ofanaerobic microorganisms to catalyze reductive dehaloge-nation of dieldrin and endrin.

Recently, Watanabe and Yoshikawa (2008) reportedanaerobic microbial strains that have the remarkableability to degrade various types of POPs, such as HCB,dieldrin, endrin, aldrin, and heptachlor. These strains hadnovel morphological and physiological characters. Al-though the metabolic pathways of dieldrin and endrin bythese microorganisms are not yet clear, they reported thatsimilar anaerobic microorganisms isolated from PCB-contaminated sediment using the same enrichment andisolation method were capable of dechlorinating HCB(Watanabe et al. 2007).

Bioremediation under aerobic conditions

Studies of the degradation of dieldrin and endrin by aerobicmicroorganisms performed up to 1980 were reviewed in

detail by Khan (1980) and Lal and Saxena (1982). Aerobicdieldrin- and endrin-degrading bacteria are summarized inTable 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) wereisolated as dieldrin-degrading microorganisms. In contrast,there have been few studies of endrin degradation byaerobic microorganisms. Pseudomonas sp., Micrococcussp., and several other unidentified bacteria and yeast(Matsumura et al. 1971) were found to be endrin-degrading microorganisms. Another study indicated thatdieldrin-degrading microorganisms, such as Pseudomonassp., 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 bythese microorganisms are still unclear, there have beenreports of the conversion of these pesticides to water-soluble and organic solvent-soluble compounds. Theprincipal compound among the organic solvent-solublemetabolites produced by Pseudomonas sp., Bacillus sp.(Matsumura and Boush 1967), A. aerogenes (Wedemeyer1968), and T. viride (Matsumura and Boush 1968) wasreported to be 6,7-trans-dihydroxydihydroaldrin. Thisconversion would be catalyzed by epoxide hydrolase,although there have been no studies focusing on theenzyme responsible for this conversion. Moreover, photo-dieldrin, previously reported as a major product convertedfrom dieldrin by the action of sunlight, was also reported asthe metabolic product of dieldrin by aerobic microorgan-isms (Matsumura et al. 1970). Among the transformationproducts of endrin, only ketoendrin was identified, andaldehyde and ketone derivatives of endrin were alsodemonstrated (Matsumura et al. 1971).

To achieve in situ bioremediation, bacteria should showdegradation capability in the natural environment equiva-lent to that in the laboratory. However, there have been noreports that augmented degrading microorganisms candemonstrate their ability to degrade dieldrin and endrin insoil. In contrast, M. alternans was reported to lose its abilityto degrade dieldrin when added to soil contaminated withdieldrin (Anderson et al. 1970). The efficiency of degradingmicroorganisms introduced into contaminated sites dependson 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), thecharacteristics of the degrading microorganisms them-selves, and methodology for site remediation are dominantfactors (Goldstein et al. 1985; Vogel 1996; Fantroussi andAgathos 2005). Therefore, it is important to understand thecharacteristics of the microorganisms and appropriateenvironmental conditions to achieve optimal degradation


Tab

le2

Uptakeof

POPsfrom

soilby

cucurbits

Reference

Plant

name(scientific

name

andcultivarname)

Targetcompo

und

Initial

soil

conc.a

Plant

part

Uptakeam

ount

bExp

erim

entaldesign

Otani

etal.20

07Zucchini(Cucurbita

pepo

L.‘Black

Tosca’)

Dieldrin/End

rin

594/58

Sho

ots

1,70

4/14

0cSeedlings

n¼

1�20

ðÞw

ereplantedin

each

ofthreepo

ts(400

mL)containing

270gof

soil

contam

inated

with

dieldrin

andendrin.Plants

weregrow

nin

agreenh

ouse

at25

°Cun

dernatural

light

for21

days

Cucum

ber(Cucum

issativus

L.‘Sharp-1’)

Dieldrin/End

rin

594/58

Sho

ots

1,20

0c/73c

Pum

pkin

(Cucurbita

moschata

Duch.

‘Hayato’)

Dieldrin/End

rin

594/58

Sho

ots

1,00

0c/25c

Wintersquash

(Cucurbita

maxima

Duch.

‘Miyako’)

Dieldrin/End

rin

594/58

Sho

ots

1,00

0c/77c

Figleaf

squash

(Cucurbita

ficifo

liaBou

ch.‘K

urod

ane’)

Dieldrin/End

rin

594/58

Sho

ots

1,10

0c/36c

Watermelon

(Citrulluslana

tus

Matsum.et

Nakai

‘Kyo

ugou

’)Dieldrin/End

rin

594/58

Sho

ots

590c/55c

Lichtenstein

etal.19

65Cucum

ber(Cucum

issativus

L.‘Straigh

tEight’)

Dieldrin

1,36

5dWho

lefruite

43Exp

erim

entswerecond

uctedin

soiltreatedwith

dieldrin

orheptachlor.Fruits

wereharvested

whenthey

reached5to

6in.long

Who

lefruitf

32

Heptachlor

2,87

0dWho

lefruite

23

Who

lefruitf

17

Heptachlorepox

ide

940d

Who

lefruite

68

Who

lefruitf

48

Hülster

etal.

1994

Zucchini(Cucurbita

pepo

L.conv

ar.

giromon

tiina

‘DiamantF1’)

PCDD+PCDF

148

Fruits

e18

.1Exp

erim

entswerecarriedou

tin

high

lyPCDD/PCDF-

contam

inated

areas.Zucchiniplantswerecultivated

“con

ventionally

”in

thecontam

inated

soil.

Onsome

oftheplants,fruitsweregrow

nwith

outsoilcontact.

Pum

pkin

andcucumbers

weregrow

nin

thesameplot.

Fruits

wereharvestedwhenthey

wereripe

for

consum

ption(6

weeks)

Fruits

f20

.5

Leaves

22.0

Pum

pkin

(Cucurbita

pepo

L.

‘GelberZentner’)

PCDD+PCDF

148

Fruits

(outer

parts)

11.8

Fruits

(inn

erparts)

3.3

Leaves

3.0

Cucum

ber(Cucum

issativus

L.‘D

elikatess’)

PCDD+PCDF

148

Fruits

(outer

parts)

2.4

Fruits

(inn

erparts)

0.2

Leaves

2.7

White

etal.20

06Zucchini(Cucurbita

pepo

L.‘Black

Beauty’)

PCB(A

rochlor12

68)

105,00

0Roo

ts43

0,00

0gOne

seedlin

gwas

plantedin

apo

t(55×44

cm)

containing

70kg

ofsoilcontam

inated

with

Arochlor12

68.Potsweremaintainedou

tside

for70

days

Stems

22,000

g

Leaves

9,80

0g

Fruit

6,70

0g


Tab

le2

(con

tinued)

Reference

Plant

name(scientific

name

andcultivarname)

Targetcompo

und

Initial

soil

conc.a

Plant

part

Uptakeam

ount

bExp

erim

entaldesign

White

2001

Zucchini(Cucurbita

pepo

L.‘Raven’)

p,p’-D

DE

225–

397

Roo

ts8,30

0hFieldexperimentswereconductedatafarm

inareas

contam

inated

with

p,p’-D

DE(50–500µg/kg).

Experim

entalplotswere2×2m.Zucchiniand

pumpkin

seedswereplantedin

threeseparate

moundsperplot.Thisresultedin

four

tofive

separate

zucchini

orpumpkin

plantsperplot.Plantswere

cultivatedfor83

days

Stems

9,60

0h

Leaves

300h

Who

lefruit

210h

Flesh

22h

Peel

360h

Pum

pkin

(Cucurbita

pepo

L.‘BabyBear’)

p,p’-D

DE

155–

397

Roo

ts7,10

0h

Stems

4,30

0h

Leaves

200h

Who

lefruit

29h

Flesh

Trace

levelh

Peel

350h

Lun

neyet

al.

2004

Zucchini(Cucurbita

pepo

L.‘Senator

hybrid’)

ΣDDTi

∼3,700

Roo

ts2,27

3Seedlings

wereplantedseparately

inbo

ttom-perforated

28�1�6cm

trayswith

asoildepthof

6cm

.All

trayswerecoveredwith

labo

ratory

Parafilm

tolim

itvo

latilization.

Plantsweregrow

nin

agreenh

ouse

at23

±2°Cin

soilcontam

inated

with

DDTandits

metabolites,DDD

andDDE,for50

days

Sho

ots

2,99

1

∼150

Roo

ts21

4

Sho

ots

99

Pum

pkin

(Cucurbita

pepo

L.‘H

owden’)

ΣDDTi

∼3,700

Roo

ts2,39

3

Sho

ots

4,26

2

∼150

Roo

ts32

3

Sho

ots

375

Mattin

aet

al.

2004

Zucchini(Cucurbita

pepo

L.

‘Black

Beauty’)

Chlordane

3,35

0Roo

ts37

,600

–52,00

0Rhizotron

was

filledwith

3.5kg

ofsoil

contam

inated

with

chlordaneandplaced

ina

greenh

ouse

for8weeks

Aerialtissue

2,22

0–3,90

0

Cam

pbellet

al.

2009

Sum

mer

squash

(Lag

enaria

siceraria‘H

yotan’)

Heptachlorepox

ide

376

Vine

1,00

0jSeedlings

wereplantedin

potscontaining

13.6

kgof

soilcontam

inated

with

heptachlor

andheptachlor

epox

ide.

Plantswerecultivated

for13

weeks

aCon

centratio

nsof

compo

unds

otherthan

PCDD

andPCDF(µg/kg

)andthoseof

PCDD

andPCDF(ngI-TEQ/kg)

bUptakeam

ountsof

compo

unds

otherthan

PCDD

andPCDF(µg/kg

)andthoseof

PCDD

andPCDF(ngI-TEQ/kg)

cApp

roximated

from

thegraphin

Fig.1of

Otani

etal.(200

7)dCon

centratio

nin

thesoilat

harvest

eFruits

weregrow

nwith

soilcontact

fFruits

weregrow

nwith

outsoilcontact

gApp

roximated

from

thegraphin

Figure3of

White

etal.(200

6)hApp

roximated

from

thegraphin

Figure2of

White

(200

1)iΣDDTrefers

toallof

DDT,

DDD,andDDE

jApp

roximated

from

thegraphin

Figure3of

Cam

pbellet

al.(200

9)


Tab

le3

Degradatio

nof

dieldrin

andendrin

bymicroorganism

sun

deranaerobiccond

ition

s

Anaerob

iccommun

ities

ormicroorganism

sOrigin

Growth

substrate

Target

compo

und

Initial

concentration

(µg/mL)

%Rem

oval

Incubatio

ntim

eMetabolitesprod

uced

Reference

Enrichedanaerobic

microbial

popu

latio

nSoil,freshw

ater

mud

,sheeprumen,chickenlitter

Sod

ium

acetate,

sodium

form

ate,

yeastextract,pepton

e

Dieldrin

1096

7days

syn-

andan

ti-mon

odechlorod

ieldrin

Maule

etal.19

87

Formate

Dieldrin

1090

4days

Formate

End

rin

1099

.74

days

Mon

odechlorinated

prod

uct

Clostridium

spp.

Abo

veanaerobic

microbial

popu

latio

nFormate

Dieldrin

1080

54–9

5days

Maule

etal.19

87

Batch

cultu

rewith

methano

genic

granular

slud

ge

Methano

genicgranular

slud

geDieldrin

988

3mon

ths

Twomon

odechlorinated

prod

ucts,aldrin,two

mon

odechlorinated

derivativ

esof

aldrin

Baczynski

etal.20

04

End

rin

799

28days

Three

mon

odechlorinated

prod

ucts,three

didechlorinatedprod

ucts

Enrichedanaerobic

microbial

popu

latio

nRiver

sedimentcontam

inated

with

organo

chlorine

pesticides

(dieldrininclud

ed)

Yeastextract

Dieldrin

0.5

100

70days

Aldrin

Chiuet

al.20

05Yeastextract

Dieldrin

2.0

100

84days

Aldrin

Yeastextract

Dieldrin

1010

014

0days

Aldrin

Batch

cultu

rewith

digestingslud

geDigestin

gslud

geDieldrin

5026

>75

days

(Lag)

Battersby

and

Wilson

1989

UnidentifiedHCB-

degradingbacteria

Paddy

fieldsoil

uncontam

inated

and

contam

inated

with

PCB

Dieldrin

100

24.4–6

7.2

14days

Watanabeand

Yoshikawa20

08End

rin

100

1.2–60

.014

days


ability. Furthermore, it is necessary to isolate new compet-itive microorganisms that can degrade dieldrin and endrinefficiently in natural environments as well as in thelaboratory.

Matsumoto et al. (2008) attempted to isolate dieldrin-and endrin-degrading microorganisms. The conventionalenrichment method requires considerable time and labor,but is not so efficient. Thus, an efficient method forisolation of dieldrin- and endrin-degrading bacteria fromsoil was developed using 1,2-epoxycyclohexane (ECH), astructural analog of dieldrin and endrin (Matsumoto et al.2008). ECH was shown to be a useful growth substrate forselective isolation of microorganisms capable of degradingdieldrin and endrin. With this method, novel aerobicbacteria, Burkholderia sp. and Cupriavidus sp., with highdegradation activity toward dieldrin and endrin wereobtained. Moreover, the degradation efficiencies of dieldrinand endrin of the isolates were higher in the presence ofECH than in its absence. Under these conditions, thedegradation efficiencies of the two isolates, Burkholderiasp. and Cupriavidus sp., were 49% and 38% towarddieldrin, respectively, and 51% and 40% toward endrin,respectively, for 14 days. Another study also indicatedenhancement of the degradation activity of dieldrin in soilby addition of pesticide analogs (Hugenholtz and MacRae1990). Therefore, pesticide analogs, such as ECH, areexpected to be useful not only as substrates for isolation of

microorganisms capable of degrading dieldrin and endrinbut also as soil amendments for enhancement of themicrobial degradation activity toward these pesticides.

The development of new sources of microbial degradersis also important to isolate new effective and functionallydiverse microbial degraders. In previous studies, heavilycontaminated soils with dieldrin and endrin were used tosearch for aerobic dieldrin- and endrin-degrading micro-organisms (Matsumura and Boush 1967; Matsumura et al.1971). However, some reports indicated that the bacterialcommunity was much less diverse in contaminated soilsthan in uncontaminated soils (Konzdroj and van Elsas2001; Gans et al. 2005; Ahn et al. 2006). Theseobservations suggest that uncontaminated soils can besources for screening of new degrading microorganisms.In fact, recent studies indicated that diverse microbialcommunities with the potential for degradation of POPsexist in soil and sediment that have not been subjected tocontamination with these chemicals, such as PCBs (Baba etal. 2007; Macedo et al. 2007) and dieldrin and endrin(Matsumoto et al. 2008).

Conclusions

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

Table 4 Degradation of dieldrin and endrin by microorganisms under aerobic conditions

Aerobic communityor microorganisms

Source of isolation Target compound Reference

Pseudomonas sp. Soil heavily contaminated with various insecticidesfrom dieldrin factory yards and orchard area

Dieldrin, endrin Matsumura and Boush 1967;Patil et al. 1970

Bacillus sp. Soil heavily contaminated with various insecticidesfrom peach orchard

Dieldrin, endrin

Trichoderma viride Soil heavily contaminated with various insecticidesfrom the dieldrin factory yards and apple orchard

Dieldrin, endrin

Aerobacter aerogenes Dieldrin Wedemeyer 1968

Mucor alternans Dieldrin Anderson et al. 1970

Trichoderma koningi Cranberry mold Dieldrin Bixby et al. 1971

Pseudomonas sp. Soil heavily contaminated with various insecticidesfrom dieldrin factory yards, orchard area, and farm

Endrin Matsumura et al. 1971

Bacillus sp. Soil heavily contaminated with various insecticidesfrom apple orchard area

Endrin

Micrococcus sp. Soil heavily contaminated with various insecticidesfrom apple orchard area

Endrin

Unidentified yeast Soil heavily contaminated with variousinsecticides from farm

Endrin

Phanerochaete chrysosporium Dieldrin Kennedy et al. 1990

Trichoderma harzianum Banana plantation field soil Dieldrin Katayama andMatsumura 1993

ECH enrichment culture Uncontaminated forest soil Dieldrin, endrin Matsumoto et al. 2008

Burkholderia sp. Uncontaminated forest soil Dieldrin, endrin

Cupriavidus sp. Uncontaminated forest soil Dieldrin, endrin


their mechanism of uptake for these compounds is still notcompletely understood. To achieve practical phytoremedia-tion by cucurbits for dieldrin and endrin, it is necessary toelucidate the uptake mechanisms of cucurbits and deter-mine the factors that can increase their uptake andtranslocation.

On the other hand, for bioremediation, efficient dieldrin-and endrin-degrading bacteria and communities have beenreported. However, there have been no reports that thesedegrading microorganisms can demonstrate their ability todegrade dieldrin and endrin in soil and sediment environ-ment to date. Therefore, it is important to confirm theirdegradation activity in actual contaminated environmentsand determine the appropriate environmental conditions toachieve optimal degradation ability.

Further advances in research on metabolites and path-ways for microbial metabolism of dieldrin and endrin areexpected. The study of dieldrin and endrin metabolism bymicroorganisms is at a less advanced stage compared withthat of PCB and HCH, for which metabolic pathways anddegrading enzymes produced by microorganisms have beendiscussed in detail. For actual application of bioremediationon polluted sites, it is necessary that the metabolic productsof dieldrin and endrin should be nontoxic or at least havelow toxicity. Previous studies indicated that photodieldrin(Georgacakis and Khan 1971) and ketoendrin (Bedford etal. 1975) produced by aerobic microorganisms were moretoxic than their parent compounds. Thus, it is important forbiodegradation and toxicological studies to focus not onlyon the disappearance of dieldrin and endrin but also on thetoxicity of metabolites to define the real environmentalimpact of these compounds.

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bioremediation of the organochlorine pesticides, dieldrin

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