lable at ScienceDirect

Environmental Pollution 158 (2010) 1899–1906

Contents lists avai

Environmental Pollution

journal homepage: www.elsevier .com/locate/envpol

Fresh organic matter of municipal solid waste enhances phytoextraction of heavymetals from contaminated soil

S. Salati, G. Quadri, F. Tambone, F. Adani*

Dipartimento di Produzione Vegetale, Universita degli Studi di Milano, Via Celoria 2, 20133 Milano, Italy

Organic fraction of MSW affects the bioavailability of heavy metals in

soil.

a r t i c l e i n f o

Article history:Received 8 May 2009Received in revised form28 September 2009Accepted 26 October 2009

Keywords:PhytoremediationDissolved organic matterOrganic fraction of municipal solid wasteHeavy metalsZea mais L.

* Corresponding author.E-mail address: fabrizio.adani@unimi.it (F. Adani).

0269-7491/$ – see front matter � 2009 Elsevier Ltd.doi:10.1016/j.envpol.2009.10.039

a b s t r a c t

In this study, the ability of the organic fraction of municipal solid wastes (OFMSW) to enhance heavymetal uptake of maize shoots compared with ethylenediamine disuccinic acid (EDDS) was tested on soilcontaminated with heavy metals. Soils treated with OFMSW and EDDS significantly increased theconcentration of heavy metals in maize shoots (increments of 302%, 66%, 184%, 169%, and 23% for Cr, Cu,Ni, Zn, and Pb with respect to the control and increments of 933%, 482%, 928%, 428%, and 5551% for soilstreated with OFMSW and EDDS, respectively). In soil treated with OFMSW, metal uptake was favoredbecause of the high presence of dissolved organic matter (DOM) (41.6� than soil control) that exhibitedligand properties because of the high presence of carboxylic acids.

Because of the toxic effect of EDDS on maize plants, soil treated with OFMSW achieved the highestextraction of total heavy metals.

� 2009 Elsevier Ltd. All rights reserved.

1. Introduction

The contamination of soil by heavy metals is a global environ-mental issue. The remediation of contaminated soil is necessary notonly to preserve the soil resource but also to safeguard humanhealth (Li et al., 2005). Conventional remediation technologies suchas soil washing/flushing, excavation, and dumping are generallyexpensive and can damage some soil properties (Komarek et al.,2007). A Growing body of evidence shows that cost-effective andenvironmentally friendly phytoextraction is a promising approachapplicable to metal-contaminated soils (Tandy et al., 2006b).

However, the main drawback of this method is low mobility,thus the bioavailability of some heavy metals (especially Pb and Cu)in polluted soils (Adriano, 2001). The use of chelating agents hasbeen proposed to achieve higher removal rates. The use of syntheticchelators, such as ethylenediaminetetraacetic acid (EDTA) and itsderivatives, can pose environmental concerns because of their highsolubility and persistence in soils (Quartacci et al., 2007; Tandyet al., 2006b; Nowack et al., 2006). On the contrary, (S,S)-ethyl-enediamine disuccinic acid (EDDS), an EDTA isomer that is easilybiodegradable, has been investigated for chelant-enhanced phy-toextraction (Tandy et al., 2006a,b; Luo et al., 2006; Komarek et al.,2007).

All rights reserved.

Natural organic molecules can be used as an alternative to theuse of high-cost synthetic chelating agents. An important group ofnatural ligands (organic molecules that bind to complex metals)(Hamon et al., 1995; Guisquiani et al., 1998) are present in dissolvedorganic matter (DOM) of soils and in DOM of organic matrices suchas compost, sewage sludge, and manure (Antoniadis and Alloway,2002). DOM consists of both hydrophilic (organic acids, carbohy-drates, amino acids, and amino sugars) and hydrophobic (aromaticphenols, hydrocarbons, fats, and nucleic acids) components(Leenheer, 1981; Fox and Comerfield, 1990). These compounds,being rich in functional groups, give ligand properties to the DOMand thus influence metal binding in soil. DOM has also beenreported to play an important role in the chemistry of heavy metalsin soils (Antoniadis and Alloway, 2002) because it forms organo-metallic complexes or is preferentially adsorbed onto soils surfacein place of metals (Guisquiani et al., 1998; Kaizer and Zech, 1997;Davies et al., 2006). Thus, if DOM in soil affects the bioavailability ofheavy metals, the management of soil organic matter, such as theuse of organic amendment (Inaba and Takenaka, 2005), mayenhance heavy metal extraction by plants in metal-contaminatedsoils. Moreover, the capacity of organic substances to promote plantgrowth and improve macro- and micronutrient uptake has beenwidely recognized.

The literature reports many studies in which the use of exoge-nous organic matter increased the soil-DOM concentration, therebysignificantly reducing the sorption of metals by soils (Davis, 1984;Xu et al., 1989; Baham and Sposito, 1994; Temminghoff et al., 1997;

Table 2Total heavy metal contents in soil, OFMSW, and soil amended with OFMSW.

Heavy metalconcentration(mg kg�1)

Soil OFMSWa Soil þOFMSW

Soil þOFMSWb

Cd 0.61 � 0.08 0.10 � 0.08 0.55 � 0.16 0.615Cr 94.52 � 3.23 44.64 � 2.12 170.02 � 66.84 96.88Cu 144.15 � 84.73 34.50 � 0.62 106.70 � 10.26 145.9Ni 67.12 � 4.65 9.33 � 1.50 83.38 � 6.92 67.61Zn 249.20 � 1.59 35.55 � 3.48 315.92 � 31.89 251.08Pb 116.57 � 8.92 118.86 � 11.89 142.09 � 3.40 122.86

a Organic fraction of municipal solid waste.b Theoretical heavy metal contents for soils treated with OFMSW, calculated from

the heavy metal contents in the OFMSW and the total amount of OFMSW dosed.

S. Salati et al. / Environmental Pollution 158 (2010) 1899–19061900

Antoniadis and Alloway, 2002). Most of these studies used pre-digested organic matter, that is, animal manure, sewage sludge, andcompost (Baham and Sposito, 1994; Antoniadis and Alloway, 2002).

In organic amendments, DOM quantity and quality depend onthe kind of the organic matrix considered and, in particular, by itsdegree of maturity (Liang et al., 1996; Chefetz et al., 1998a). Freshorganic matter contains DOM characterized by a large number oflow molecular-weight hydrophilic fractions (Zi-gang et al., 2007)and hydrophobic molecules such as aromatic acids or aromaticphenols (Wu et al., 2004). In a study conducted by D’Imporzano andAdani (2007), the composting process resulted in a strong reduc-tion of the total DOM (g kg�1 compost dry matter) content and themodification of its characteristics. In particular, the degradation ofthe organic matter decreased the content of the hydrophilic frac-tion of DOM rich in acid functional group. Zi-gang et al. (2007)showed that DOM from fresh matrices enhanced the formation ofmetal–DOM complexes than a corresponding mature matrix.

The organic fraction of municipal solid wastes (OFMSW) isa widely distributed and available organic matrix that could beusefully employed as an amendment in phytoextraction. Compostmade from this fraction has been used for this purpose (Bhatta-charyya et al., 2005). Nevertheless, there is a lack of informationregarding the ability of the high DOM content in non-compostedOFMSW to mobilize soil heavy metals.

However, the use of non-composted OFMSW may be accom-panied by biological risks and before applying this solution, the lackof information should be adequately considered.

The aim of the present study was to evaluate the effect of thenon-composted OFMSW as soil amendment to improve metalextraction by plants in contaminated soil compared with thewell-studied and known synthetic chelating agent, EDDS (Kos andLestan, 2003a; Tandy et al., 2004, 2006a,b; Meers et al., 2005). Tothe authors’ knowledge, the use of non-composted OFMSW hasnever been proposed, making the technology a novelty in thisfield.

2. Materials and methods

2.1. Soil sampling

Soil samples (Table 1) were collected from a post-industrial area of 50 Ha. In thisarea, a sampling site of 0.5 Ha, particularly compromised because of high heavymetal contents (Table 2) was chosen for the study. Soil was drawn from a depth of1 m by randomized sampling of six spots. From each spot, about 200 kg of soil weresampled, completely homogenized, and successively quartered to obtain subsam-ples of about 20 kg. Subsamples from different spots were then combined and againquartered to obtain a final sample of 20 kg. Soil sample was riddled through a sieveof 20 mm, then homogenized and used for pot experiments.

Table 1Characteristics of soil, OFMSW, and soil amended with OFMSW.

Parameter Soil OFMSWa Soil þ OFMSW

C (g kg�1) 9.10 � 1.42 367.61 � 3.23 17.72 � 1.23Texture Sandy loamy Sandy loamySkeleton (%) 16 16Ntotal (g kg�1) 0.24 � 0.16 17.65 � 0.20 1.08 � 0.12Available P (mg kg�1) 24.36 � 1.56 61.33 � 9.32CEC (cmol(þ) kg�1) 6.47 � 0.91 8.34 � 0.56EC at 25 �C (mS cm�1) 0.305 0.69pHH2O 7.95 6.3 � 0.3 7.96Field water capacity % 26.57 39.65Nutrients (mg kg�1):Mg 103.15 � 6.72 184.10 � 12.62Ca 662.18 � 0.80 715.69 � 5.23K 219.10 � 40.17 444.01 � 56.15Na 148.73 � 8.57 364.87 � 12.46Mg/K 0.69 0.22

a Organic fraction of municipal solid waste.

2.2. Organic fraction of municipal solid waste preparation

The organic fraction (15 kg) of municipal solid waste (OFMSW) from separatecollections (foodwaste) was dried at 40 �C in an oven with forced aeration andground to 1 cm. Two-day-old OFMSW was collected directly from a compostingplant.

The OFMSW was then chemically evaluated for carbon (C), heavy metals, andnitrogen (N) contents (Tables 1 and 2).

2.3. Soil characterization

Soils were characterized for common chemical parameters and for heavy metalcontents (Table 1) according to standard soil science procedures (Faithfull, 2002)(Table 1). Soil samples were digested in concentrated HNO3 and H2O2 (EPA, 1996)and the heavy metals, Cd, Cr, Cu, Ni, Zn, and Pb were determined by inductivelycoupled plasma-optical emission spectrometry (ICP-OES) (AX liberty, Varian. FortCollins, USA). A certified standard reference material (GBW 07405, soil) from theNational Centre for Standard Materials (Beijing, China) was used in the digestion andanalysis. Average recovery was 92 � 4% for all the metals determined.

To ensure the accuracy and precision in the analyses, reagent blanks were runwith samples. Analyses were performed in duplicates.

2.4. Pot experiment and plant analyses

Three treatments were examined: untreated soil (control), soil amended withOFMSW, and soil with added EDDS. Phytoextraction trials were performed in 6 Lclosed-bottom pots each filled with 5 kg of air-dried and sieved soil. Three replicateswere performed by block randomized experimental design.

In the OFMSW treatment, soil was mixed with the organic matter at the rate of265 g dry matter (dm) of OFMSW per pot.

Maize (Zea Mays L.) was chosen for the plant test because of its high biomassyields and heavy metal tolerance (Komarek et al., 2007; Wu et al., 2004; Luo et al.,2005). Moreover, it represents a commonly cultivated crop in the study area (NorthItaly). Three seeds of maize were sown in each pot. Fifteen days from sowing, thenumber of maize plants was reduced to one. Maize pots were fertilized with 1.3 g ofN (NH4NO3), 0.42 g of P(KH2PO4), and 0.35 g K (K2PO4). Pots were kept ina controlled outdoor greenhouse with a day/night regime of 16/8 h and a lightintensity of 350–400 mmol photons m�2 s�1. During the day, the air temperature was26–28 �C and at night it was 16–18 �C. Pots were maintained at a 60% water holdingcapacity by adding deionized water every two days. Thirty-five days after sowing,EDDS treatment was carried out by 10 mmol EDDS per kg soil as a 0.5 mM solution(pH ¼ 10.1) (Luo et al., 2006).

Sixty days after sowing, the aboveground biomass was harvested, carefullywashed using deionized water, dried at 60 �C until constant weight, weighed, andthen finely ground. The heavy metal content of the harvested plants was thendetermined as reported for soil.

2.5. Spectroscopic analysis

DOM was extracted from soil before and after incubation using distilled water ina solid liquid ratio of 1:2 (w/w); samples were weighed in a plastic bottle and shakenfor 30 min in a mechanical shaker (Scaglia and Adani, 2009). The suspension thusobtained was centrifugated for 15 min at 6000 rpm and then filtered twice, first byusing a fast cellulose filter (Whatman paper filter n.4), and then by a 0.45 mm mil-lipore membrane (Advantec MFS, Pleasanton, CA). DOM fractions were analyzedquantitatively by dissolved organic carbon detection (DOC) (ISO InternationalStandard).

Diffuse Reflectance Infrared Fourier Transform (DRIFT) spectroscopy was used asthe qualitative approach to describe DOMs. DRIFT spectra were performed using anAvatar 370 Fourier transform infrared spectroscopy (FT-IR) from ThermoNicoletInstruments (Madison, WI, USA). Samples (7 mg), previously dried at 65 �C for 48 h,

S. Salati et al. / Environmental Pollution 158 (2010) 1899–1906 1901

and KBr (700 mg); FT grade, (Aldrich 105 Chemical Co, ST Louis, Missouri) werefinely ground for 10 min using an agate ball mill (Specamill-Greseby-Specac, Kent,UK). The instrument parameters used were: scanning 128, resolution 4 cm�1, andfrequency 400–4000 cm�1 gain 16.

2.6. Statistical analysis

All the statistical analyses were performed using analysis of variance(ANOVA) with the Tukey test used to compare means (SPSS statistical software,SPSS Chicago IL).

3. Results

3.1. Plant yield and plant heavy metal uptake

Plants in treated soils showed higher heavy metal contents thanthe control, except for the Cd content. The application of EDDScaused the highest heavy metal concentration in plants (Fig. 1).Results obtained were expected because synthetic chelants, such asEDDS, are commonly used to enhance the solubility of metals in

0

0,1

0,2

0,3

0,4

0,5

contro EDDS

mg

Cd

kgdr

y pl

ant-1

0

10

20

30

40

50

60

contro EDDS

mg

Cu

kgdr

y pl

ant-1

l OFMSW

l OFMSW

0

50

100

150

200

250

300

350

control OFMSW EDDS

mg

Znkg

dry

plan

t -1

Fig. 1. Metals content in dry maize shoots: control soil; OFMSW ¼ soil amended with

soils (Blaylock et al., 1997; Cooper et al., 1999; Shen et al., 2002; Kosand Lestan, 2003b). Interestingly, the use of OFMSW increased theuptake of heavy metal by plants. The increase in maize shoot heavymetal content of soil treated with OFMSW, with respect to thecontrol, was calculated to be 302%, 66%, 184%, 169%, and 23% for Cr,Cu, Ni, Zn, and Pb, respectively. However, the Cd content was lowerthan the control (Fig. 1).

The results above reported do not take into consideration thetotal amount of metals extracted by the plant, which depends onthe total plant yield. Total heavy metal uptake by the shoot of theplant was calculated by considering the production of plant drymatter (Control ¼ 58.9 � 1.9 g plant�1; Soil amended withOFMSW ¼ 62.8 � 2 g plant�1; Soil treated withEDDS ¼ 5.0 � 0.2 g plant�1) and the relative heavy metal concen-tration (mg kg�1 plant dry matter) (Fig. 2). In this case, the resultsobtained were quite different from those reported earlier. Thehighest performances were achieved by soil amended withOFMSW, with the exception of Cd and Pb (Fig. 2). Soil treated with

0

5

10

15

20

25

contro EDDS

mg

Nik

g dr

y pl

ant -1

0

10

20

30

40

50

60

70

80

90

100

control EDDS

mg

Pbkg

dry

plan

t -1

0

2

4

6

8

control

l OFMSW

OFMSW EDDS

mg

Crk

gdr

y pl

ant-1

OFMSW

the organic fraction of municipal solid waste; EDDS ¼ soil amended with EDDS.

0

0,002

0,004

0,006

0,008

0,01

0,012

mg

Cd

extra

cted

per

pla

nt

0

0,02

0,04

0,06

0,08

0,1

0,12

0,14

0,16

0,18

control OFMSW EDDS control OFMSW EDDS

control OFMSW EDDS control OFMSW EDDS

control OFMSW EDDS control OFMSW EDDS

mg

Cre

xtra

cted

per

pla

nt

0

0,2

0,4

0,6

0,8

1

1,2

mg

Cu

extra

cted

per

pla

nt

0

0,05

0,1

0,15

0,2

0,25

0,3

0,35

0,4

mg

Nie

xtra

cted

per

plan

t

0

2

4

6

8

10

12

mg

Znex

tract

ed p

er p

lant

0

0,1

0,2

0,3

0,4

0,5

0,6

mg

Pbex

tract

ed p

erpl

ant

Fig. 2. Metal extraction by maize shoots: control soil; OFMSW ¼ soil amended with the organic fraction of municipal solid waste; EDDS ¼ soil amended with EDDS.

S. Salati et al. / Environmental Pollution 158 (2010) 1899–19061902

EDDS showed lower or similar total heavy metal contents whencompared to the control (with the exception of Pb). In particular forsoil treated with OFMSW, with respect to the control, the shootuptake was calculated to be 366%, 115%, 222%, 237%, and 55.8% forCr, Cu, Ni, Zn, and Pb respectively (Fig. 2). Soil treated with EDDSshowed lower or similar total heavy metal contents whencompared to the control (with the exception of Pb).

3.2. Dissolved organic matter in soil studied

Quantitatively the dissolved organic carbon (DOC) content inthe OFMSW-amended soil was 41.6� with respect to the control atthe start of the trials (0.037 g C kg�1 soil dm and 1.54 g C kg�1 soildm for the control and OFMSW-amended soil, respectively), and2.5� at the end of the trials (0.048 g C kg�1 soil dm and0.12 g C kg�1 soil dm for the control and OFMSW-amended soil,respectively).

From a qualitative point of view at the beginning of the trials,soil-DOM in the control (Fig. 3a) was composed principally of

aromatic structures (wide peak at 1620–1650 cm�1 indicating C]Cin aromatic structure, COO�, H-bonded C]O) and sugar-likemolecules (peaks at 1129 and 1032 cm�1 indicating C–O stretch ofpolysaccharide and or organic acid) (Chefetz et al., 1998b). At theend of the trial, weak modification occurred (Fig. 3b). DOM spectraof soil amended with OFMSW, before and after the experiment(Fig. 3c,d), were very similar but different from those of the controlsoil. DOM were composed primarily of small or branched aliphaticmolecules [peak at 1420 cm�1 C–H deformation of CH2 or CH3

groups, (e.g., volatile fatty acid)] and carbohydrate structures (peakaround 1000 cm�1). In particular, the very intense peak around1590 cm�1 attributed to the carboxylate asymmetrical stretching(Said-Pullicino and Gligliotti, 2007) indicated the high presence ofcarboxylic acids (Said-Pullicino and Gligliotti, 2007).

4. Discussion

Three factors affect plant and soil metal concentrations: (1) thequantity factor, which represents the total amount of metals bio-

Fig. 3. DRIFT spectra for dissolved organic matter extracted from control soil (a ¼ t0; b ¼ tend) and soil amended with the OFSMW (c ¼ t0; d ¼ tend).

Table 3Heavy metal uptake by maize shoots obtained in this study in comparison withliterature data.

Heavymetal

Plant Plant uptakea

performanceTreatment Reference

Cu Zea Mays L. 2.153 OFMSW This workZea Mays L. 5.2� EDDS 5 mmol

kg�1 soilLuo et al., 2006

Zea Mays L. 21� EDDS 5 mmolkg�1

Luo et al., 2005

Zea Mays L. Below thecontrol

Citric acid 5mmol kg�1

Luo et al., 2005

Pb Zea Mays L. 1.63 OFMSW This workZea Mays L. 5.3� EDDS 5

mmol kg�1Luo et al., 2006

Zea Mays L. 4.3� EDDS 5mmol kg�1

Luo et al., 2005

Zea Mays L. Below thecontrol

Citric acid 5mmol kg�1

Luo et al., 2005

Zn Zea Mays L. 1.63 OFMSW This workZea Mays L. 1� EDDS 5

mmol kg�1Luo et al., 2005

Zea Mays L. Below thecontrol

Citric acid 5mmol kg�1

Luo et al., 2005

Cd Zea Mays L. Below thecontrol

OFMSW This work

Zea Mays L. Below thecontrol

Citric acid 5mmol kg�1

Luo et al., 2005

a Plant uptake performance was calculated as total plant uptake of treated soil/total plant uptake of control.

S. Salati et al. / Environmental Pollution 158 (2010) 1899–19061904

available; (2) the intensity factor, which represents the activity ofmetals in the soil solution; and (3) the reaction kinetics, whichrepresents the rate of metals transferred from the solid to the liquidphase and to the plant roots (Brummer et al., 1996; Schmidt, 2003).The effect of the organic matter on improved metal mobility in soilmay be attributed to its influence on factors 1 and 3, in the sensethat the high presence of DOM in soil treated with OFMSW acted asligands for metals, enhancing the metals’ availability for plants andtheir solubility in soil (Guisquiani et al., 1998; Kaizer and Zech,1997; Davies et al., 2006). This assumption was confirmed by thefact that the DOC content in the OFMSW-amended soil was muchhigher than control at the start of the trials.

Christensen and Christensen (1999) observed an increase inmetal content bound to DOM when a DOM concentration increasedin leachated-polluted groundwater. Antoniadis and Alloway (2002)reported that an increase in the concentration of DOM increasesmetal extractability from the soil through elevated metal uptake byplants.

The mechanism by which plants uptake heavy metals bound toDOM is not yet well understood. Nevertheless, some authors(Hamon et al., 1995; Krishnamurti et al., 1997) observed that DOMor low molecular-weight organic acids, which comprise DOM, canbe taken up by plant roots along with the metals that they havebound.

To explain the effect of DOM in the metal complex formation,the qualitative aspect of DOM must be also considered. The addi-tion of OFMSW to the soil strongly affected soil-DOM characteris-tics. In particular the abundance of carboxylic acid observed in theDOM of soil treated with OFMSW, seems to confirm the report onthe ability of DOM to mobilize heavy metal by forming metalcomplexes (Kalinichev et al., 2006; Inaba and Takenaka, 2005).Organic complexes have been recognized to have a strong impacton the migration of metals (Pb, Cu, Zn, and Cd) in soils (McBrideet al., 1997) and organic acids (e.g., formic, acetic, lactic, oxalic,malonic, succinic, malic, tartaric, gluconic, citric, and 2-ketoglu-conic) have been reported to be constituents of DOM and to formorganic complexes with heavy metals (Essington, 2004).

No metal speciation, in terms of the quantification of DOM-bound heavy metal, was considered in this study. Therefore, it wasnot easy to provide a complete explanation of the results obtained.Some qualitative considerations could be made, however.

Heavy metal solubility is conditioned by the hydrolysis constant(�log K), which affects metal solubility. Copper and lead, the lessOFMSW-affected heavy metals, have lower pKhydrolysis

(pKhydrolysis ¼ �log K) (CupKhydrolysis of 7.7; PbpKhydrolysis of 7.7) valuesthan the other metals, which were similar to the soil pH (pH of7.96). This means a lower availability of the metals becausehydrolyzed forms occurred (pKhydrolysis ¼ pH) (Essington, 2004).Hydrolyzed forms were not present in the other heavy metals, ashigher pKhydrolysis values than pH were observed (pKhydrolysis of 9.7,9.86, 8.96, 10.08, for Cr3þ, Ni2þ, Zn2þ and Cd2þ, respectively)(Essington, 2004).

Free soluble species can form metal–organic complexes with theDOM. The formation metal–organic complexes depend on theconcentration of the soluble metal and on the ion stability constant(log Kf) with the organic ligands. The high stability constant of themetal–organic complex ensures the protection of the metal fromspeciation into insoluble forms, such as hydrolysis reaction, solidparticle adsorption (inner sphere complexes), and salt formation(Essington, 2004).

Literature has reported the ion stability constant (log Kf) fordifferent organic acids in the range of 1.18–7.2 (Essington, 2004;Wang et al., 2004). Generally, the lowest values were reported forCd2þ, Zn2þ, and Ni2þ while Cr3þ, Cu2þ, and Pb2þ had the highestvalues.

Considering metal concentration, the hydrolysis constant, andthe ion stability constant, the influence of OFMSW–DOM on theheavy metal uptake by maize plant could explain the effect repor-ted earlier.

The same observation can be made for soil treated with EDDS. Inparticular, the ion stability constant was higher than those oforganic acid, and was reported to be in the range of 11.42 (Cd2þ)–19.42 (Cu2þ) (Quartacci et al., 2007). Therefore, as metal–EDSScomplexes were more stable than metal–DOM complexes, themetals were more protected from insolubility processes. Moreover,the EDDS content in soil (2.88 g C kg�1 dm) (calculated after EDDSapplication by considering the dose of 10 mmol kg�1 dry matterand an EDDS-MW of 289.97 g mol�1) was approximately twice thatof DOM (1.54 g C kg�1 dm) concentration in soil treated withOFMSW.

Therefore, both the EDDS concentration in soil and the ionstability constant explained the better performance obtained withthe synthetic chelating agent than with the OFMSW.

Heavy metal concentration and ion stability constant alsoexplained the lower Cd content observed in soil amended withOFMSW than that of control soil. Cd-log Kf of different organic acidshas been reported to be lower than those of other metals thatcompete with Cd to form organo-metallic complexes. In addition,Cd concentration in soil was lower than the other heavy metalscompeting with Cd. For example, Zn has been reported to depressCd plant uptake (Page et al., 1981; Christensen and Christensen,1999; Antoniadis et al., 2007; Perriguey et al., 2008).

Plant yields affect positively or negatively total heavy metaluptake. Low heavy metal uptake of plants treated with EDDS wasdue to plant dead at the end of the trials. Plant in this case showedboth chlorotic and necrotic symptoms, probably because of thetoxicity from both heavy metals and EDDS. Metal toxicity could beattributed to the excess of soluble heavy metals caused by theaddition of EDDS (Blaylock et al., 1997; Huang et al., 1997; Epsteinet al., 1999; Wu et al., 1999). Direct EDDS toxicity has been previ-ously reported for plant, including maize (Meers et al., 2005; Luo

S. Salati et al. / Environmental Pollution 158 (2010) 1899–1906 1905

et al., 2005). On the other hand soil treated with the OFMSW,showed the highest performance in the heavy metal uptake. Theseresults depended on both the ability of DOM to mobilize heavymetals, such as before explained, and the fertilizing effect ofOFMSW, which stimulated biomass production.

Nevertheless, the results of this study indicate lower perfor-mance in the uptake of heavy metals by maize shoots than otherstudies reported in the literature (Table 3) although a directcomparison with literature data, is difficult as many factors andvarious experimental conditions could influence metal uptake byplants.

5. Conclusion

The study showed the positive effect of the soil amendmentwith fresh OFMSW in the metal uptake of maize shoots incontaminated soil. This effect was attributed to the high presence ofDOM in soil treated with OFMSW (41.6�with respect to the controlsoil), which affected the availability of heavy metals in the plant. Incontrast to EDDS, OFMSW did not show any toxic effect, allowinghigh biomass production and as a consequence, attaining thehighest total heavy metal uptake.

References

Adriano, D.C., 2001. Trace Elements in Terrestrial Environments: Biogeochemistry,Bioavailability and Risks of Metals, second ed. Springer, New York, NY.

Antoniadis, V., Alloway, B.J., 2002. The role of dissolved organic carbon in themobility of Cd, Ni and Zn in sewage sludge-amended soils. EnvironmentalPollution 117, 515–521.

Antoniadis, V., Tsadilas, C.D., Ashworth, D.J., 2007. Monometal and competitiveadsorption of heavy metals by sewage sludge-amended soil. Chemosphere 68,489–494.

Baham, J., Sposito, G., 1994. Adsorption of dissolved organic carbon extracted fromsewage sludge on montmorillonite and kaolinite in the presence of metal ions.Journal of Environmental Quality 23, 147–153.

Bhattacharyya, P., Chakraborty, A., Chakrabarti, K., Tripath, y S., Powell, M.A., 2005.Chromium uptake by rice and accumulation in soil amended with municipalsolid waste compost. Chemosphere 60 (10), 1481–1486.

Blaylock, M.J., Salt, D.E., Dushenkov, S., Zakharova, O., Gussman, C., Kapulnik, Y.,Ensley, B.D., Raskin, I., 1997. Enhanced accumulation of Pb in Indian mustardby soil-applied chelating agents. Environmental Science and Technology 31,860–865.

Brummer, G., Gerth, j., Herms, U., 1996. Heavy metal species, mobility andavailability in soil. Zeitschrift fur pflanzenernaehrung und Bodenkunde 149,382–398.

Chefetz, B., Hadar, Y., Chen, Y., 1998a. Characterization of dissolved organic matterextracted from composted municipal solid waste. Soil Society of AmericanJournal 62, 326–332.

Chefetz, B., Hadar, Y., Chen, Y., 1998b. Dissolved organic carbon fractions formedduring composting of municipal solid waste: properties and significance. ActaHydrochimica et Hydrobiologica 26 (3), 172–179.

Christensen, J.B., Christensen, T.H., 1999. Complexation of Cd, Ni, and Zn by DOC inpolluted groundwater: a comparison of approaches using resin exchange,aquifer material sorption, and computer speciation models (WHAM and MIN-TEQA2). Environmental Science and Technology 33 (21), 3857–3863.

Cooper, E.M., Sims, J.T., Cunningham, S.D., Huang, J.W., Berti, W.R., 1999. Chelate-assisted phytoextraction of lead from contaminated soils. Journal of Environ-mental Quality 28, 1709–1719.

D’Imporzano, G., Adani, F., 2007. The contribution of water soluble and waterinsoluble organic fractions to oxygen uptake rate during high rate composting.Biodegradation 18, 103–113.

Davies, O.A., Allison, M.E., Uyi, H.S., 2006. Bioaccumulation of heavy metals in water,sediment and periwinkle (Tympanotonus fuscatus var radula) from the ElechiCreek Niger Delta. African Journal of Biotechnology 5 (10), 968–972.

Davis, J.A., 1984. Complexation of trace metals by adsorbed natural organic matter.Geochimica et Cosmochimica Acta 48, 679–691.

EPA, 1996. Method 3050B. Acid digestion of sediments, sludges, and soils. Revision 2(December 1996). In: Test Methods for Evaluating Solid Wastes: Physical/Chemical Methods, EPA SW-846, third ed., vol. I. U.S. Environmental ProtectionAgency, Office of Solid Waste and Emergency Response, Washington, D.CAvailable at: http://www.epa.gov/epaoswer/hazwaste/test/pdfs/3050b.pdf,Section A, Chapter 3 (Inorganic Analytes), pp. 3050B-1–3050B-12.

Epstein, A.L., Gussman, C.D., Blaylock, M.J., Yermiyahu, U., Huang, J.W., Kapulnik, Y.,Orser, C.S., 1999. EDTA and Pb–EDTA accumulation in Brassica juncea grown inPb-amended soil. Plant and Soil 208, 87–94.

Essington, M.E., 2004. Soil and Water Chemistry: an Integrative Approach. CRCPress, Boca Raton, USA, pp. 183–254.

Faithfull, N.T., 2002. In: CABI Publishing (Ed.), Methods in Agricultural ChemicalAnalysis: a Practical Handbook. CAB International, Wallingford, Oxon OX108DE, UK.

Fox, T.R., Comerfield, N.B., 1990. Low molecular weight organic acid in selectedforest soils of the south-eastern USA. Soil Science Society of America Journal 54,1763–1767.

Guisquiani, P.L., Concezzi, L., Businelli, M., Macchioni, A., 1998. Fate of pig sludgeliquid fraction in calcareous soil: agricultural and environmental implications.Journal of Environmental Quality 27, 364–371.

Hamon, R.E., Lorenz, S.E., Holm, P.E., Christensen, T.H., McGrath, S.P., 1995. Changesin trace metal species and other components of the rhizosphere during growthof radish. Plant and Environment 18, 749–756.

Huang, J.W.W., Chen, J., Berti, W.R., Cunningham, S.D., 1997. Phytoremediation oflead-contaminated soils: role of synthetic chelates in lead phytoextraction.Environmental Science and Technology 3, 800–805.

Inaba, S., Takenaka, C., 2005. Effects of dissolved organic matter on toxicity andbioavailability of copper for lettuce sprouts. Environment International 31,603–608.

ISO 14240–2:1997 (E), International Standards: Soil quality-determination of soilmicrobial biomass.

Kaizer, K., Zech, W., 1997. Competitive sorption of dissolved organic matter fractionsto soils and related mineral phases. Soil Science Society of America Journal 61,64–69.

Kalinichev, A.G., Xu, X., Kirkpatric, R., 2006. Cation complexation with dis-solved organic matter: insights from molecular dynamics computersimulations and NMR spectroscopy. American geophysical Union, Fallmeeting, #B32B-07.

Komarek, M., Tlustos, P., Szakova, J., Chrastnyb, V., Ettler, V., 2007. The use of maizeand poplar in chelant-enhanced phytoextraction of lead from contaminatedagricultural soils. Chemosphere 67, 640–651.

Kos, B., Lestan, D., 2003a. Induced phytoextraction/soil washing of lead usingbiodegradable chelate and permeable barriers. Environmental Science andTechnology 37, 624–629.

Kos, B., Lestan, D., 2003b. Influence of a biodegradable ([S, S]-EDDS) and non-degradable (EDTA) chelate and hydrogel modified soil water sorption capacityon Pb phytoextraction and leaching. Plant and Soil 253, 403–411.

Krishnamurti, G.S.R., Cieslinski, G., Huang, P.M., van Rees, K.C.J., 1997. Kinetics ofcadmium release from soils as influenced by organic acids: implication incadmium availability. Journal of Environmental Quality 26, 271–277.

Leenheer, J.A., 1981. Comprehensive approach to preparative isolation and frac-tionation of dissolved organic carbon from natural waters and wastewater.Environmental Science and Technology 15, 578–587.

Li, H., Wang, Q., Cu, i Y., Dong, I., Christie, P., 2005. Slow release chelateenhancement of lead phytoextraction by corn (Zea mais L.) fromcontaminated soil–a preliminary study. Science of the Total Environment339, 179–187.

Liang, B.G., Gregoric, E.G., Schnitze, r M., Schulten, H.R., 1996. Characterization ofwater extracts of two manures and their adsorption on soils. Soil Society ofAmerican Journal 60, 1758–1763.

Luo, C., Shen, Z., Li, X., 2005. Enhanced phytoextraction of Cu, Pb, Zn and Cd withEDTA and EDDS. Chemosphere 59, 1–11.

Luo, C., Shen, Z., Lou, L., Li, X., 2006. EDDS and EDTA-enhanced phytoextraction ofmetals from artificially contaminated soil and residual effects of chelantcompounds. Environmental Pollution 144, 862–871.

Meers, E., Ruttens, A., Hopgood, M.J., Samson, D., Tack, F.M.G., 2005. Comparison ofEDTA and EDDS as potential soil amendments for enhanced phytoextraction ofheavy metals. Chemosphere 58, 1011–1022.

McBride, M.B., Richard, B.K., Steenhuis, T., Russo, J.L., Sauve, S., 1997. Mobility andsolubility of toxic metals and nutrients in soil fifteen years after sludge appli-cation. Soil Science 162, 487–500.

Nowack, B., Schulin, R., Robinson, B.H., 2006. Critical assessment of chelant-enhanced metal phytoextraction. Environmental Science and Technology 40,5225–5232.

Page, A.L., Bingham, F.T., Chang, A.C., 1981. In: Lepp, N.W. (Ed.), Effect of Heavy MetalPollution on Plants. Effects of Trace Metals on Plant Function, vol. 1. AppliedScience Publishers, London, pp. 77–109.

Perriguey, J., Sterckeman, T., Morel, J., 2008. Effect of rhizosphere and plant-relatedfactors on the cadmium uptake by maize (Zea mays L.). Environmental andExperimental Botany 63, 333–341.

Quartacci, M.F., Irtelli, B., Baker, A.J.M., Navari-Izzo, F., 2007. The use of NTA andEDDS for enhanced phytoextraction of metals from a multiply contaminatedsoil by Brassica carinata. Chemosphere 68, 1920–1928.

Said-Pullicino, D., Gligliotti, G., 2007. Oxidative biodegradation of dissolved organicmatter during composting. Chemosphere 68, 1030–1040.

Scaglia, B., Adani, F., 2009. Biodegradability of soil water soluble organiccarbon extracted from seven different soils. Journal of EnvironmentalSciences 21, 1–6.

Shen, Z.G., Li, X.D., Wang, C.C., Chen, H.M., Chua, H., 2002. Lead phytoextractionfrom contaminated soil with high-biomass plant species. Journal of Environ-mental Quality 31, 1893–1900.

Schmidt, U., 2003. Enhancing phytoextraction: the effect of chemical soil manipu-lation on mobility, plant accumulation, and leaching of heavy metals. Journal ofEnvironmental Quality 32, 1939–1954.

S. Salati et al. / Environmental Pollution 158 (2010) 1899–19061906

Tandy, S., Bossart, K., Mueller, R., Ritschel, J., Hauser, L., Schulin, R., Nowack, B., 2004.Extraction of heavy metals from soils using biodegradable chelating agents.Environmental Science and Technology 38, 937–944.

Tandy, S., Schulin, R., Nowack, B., 2006a. The influence of EDDS on the uptake of heavymetals in hydroponically grown sunflowers. Chemosphere 62, 1454–1463.

Tandy, S., Schulin, R., Nowack, B., 2006b. Uptake of metals during chelant-assistedphytoextraction with EDDS related to the solubilized metal concentration.Environmental Science and Technology 40, 2753–2758.

Temminghoff, E.J., Vander Zeem, S.M., Anddehaan, F.A.M., 1997. Copper mobility ina copper-contaminated sandy soil as affected by pH and solid and dissolvedorganic matter. Environmental Science and Technology 31, 1109–1115.

Wang, J., Huang, C.P., Herbert, E.A., 2004. Modeling heavy metal uptake by sludge partic-ulates in the presence of dissolved organic matter. Water Research 37, 4835–4842.

Wu, J.G., Lu, Y., Wang, M.H., Jiang, Y.M., 2004. Study on decomposition of organicfertilizers by FTIR. Plant Nutrition and Fertilizer Science 10, 259–266 (in Chinesewith English abstract).

Wu, J., Hsu, F.C., Cunningham, S.D., 1999. Chelate-assisted Pb phytoextraction: Pbavailability, uptake, and translocation constraints. Environmental Science andTechnology 33, 1898–1904.

Xu, H., Ephraim, J., Ledin, A., Allard, B., 1989. Effects of fulvic acid on theadsorption of Cd(II) on alumina. The Science of the Total Environment 81/82,653–660.

Zi-gang, L., Chuan-zhou, B., Xiao-lei, J., 2007. Characteristic of Cd sorption in thecopper tailings wasteland soil by amended dissolved organic matter fromfresh manure and manure compost. African Journal of Biotechnology 6 (3),227–234.