bioremediation of the organochlorine pesticides, dieldrin
TRANSCRIPT
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
Soil(agriculturalfields)
365.19
ND–2
3.8
Harneret
al.19
99
Low
erFraserValley,
Canada
Soil(agriculturalfields)
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
Soil(agriculturalfields)
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
208 Appl Microbiol Biotechnol (2009) 84:205–216
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
Appl Microbiol Biotechnol (2009) 84:205–216 209
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
210 Appl Microbiol Biotechnol (2009) 84:205–216
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)
Appl Microbiol Biotechnol (2009) 84:205–216 211
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
212 Appl Microbiol Biotechnol (2009) 84:205–216
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
Appl Microbiol Biotechnol (2009) 84:205–216 213
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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