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Published online 9 January 2007
Published in J Environ Qual 36:216-225 (2007)
DOI: 10.2134/jeq2006.0252RA
© 2007 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
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Application of Two Organic Wastes in a Soil Polluted by Lead

Effects on the Soil Enzymatic Activities

M. Tejadaa,*, M. T. Hernandezb and C. Garciab

a Departamento de Cristalografía, Mineralogía y Química Agrícola, E.U.I.T.A. Universidad de Sevilla, Crta de Utrera km. 1, 41013 Sevilla, Spain
b Departamento de Conservación de Suelos y Agua y Manejo de Residuos Orgánicos, Centro de Edafología y Biología Aplicada del Segura, CEBAS-CSIC, P.O. Box 4195, 30080 Murcia, Spain

* Corresponding author (mtmoral{at}us.es)

Received for publication June 30, 2006.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The effects of adding a crushed cotton gin compost (CCGC) and a poultry manure (PM) on the enzymatic activities of a Typic Xerofluvent soil polluted with Pb were studied in the laboratory. Three hundred grams of sieved soil (<2 mm) were mixed with PM at a rate of 10% or CCGC at a rate of 17.2%, applying to the soil the same amount of organic matter with each organic amendment. Urease, protease-BBA, ß-glucosidase, alkaline phosphatase, and arylsulfatase activities were measured at four different incubation times (1, 7, 15, and 45 d) in soils containing seven concentrations (100, 250, 500, 1000, 2500, 5000, and 8000 mg kg–1) of Pb, and in the same soils amended with CCGC and PM. In all treatments and incubation times, the inhibition percentage of soil enzyme activities by Pb was lower in soils amended with the PM and CCGC than in nonamended soils, and it differed with the organic amendment. In this respect, the in the 8000 mg Pb kg–1 treatment at the end of the incubation period, the protease-BBA activity inhibition percentage was lower (14.7 and 33.9% lower, respectively) in CCGC- than in PM-amended soils. Since the adsorption capacity of Pb was higher in CCGC- than the PM-amended soils, the addition of organic wastes with higher humic acid concentration is more beneficial for remediation of soils polluted with Pb.

Abbreviations: CCGC, crushed cotton gin compost • PM, poultry manure


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
HEAVY metal pollution has received increasing attention in recent years mainly because of the public awareness of environmental concerns that heavy metals are toxic at higher levels in both natural and man-made environment ecosystems (Guiller et al., 1998). Heavy metal contamination is a serious threat to soil quality due to heavy metal persistence after entering the soil (McGrath, 1987). It has been demonstrated repeatedly that heavy metals adversely affect biological functions in soil, including the size, activity and diversity of the soil microbial community (Kelly et al., 1999; Chander et al., 2001), and the activity of enzymes involved in transformations of C, N, P, and S (Moreno et al., 1999; Landi et al., 2000; Belyaeva et al., 2005). Lead toxicity has been widely reported in plants, animals, and human beings. In soil, Pb normally occurs in the range of 10 mg kg–1 but in polluted soils the Pb content may reach 1000 mg kg–1 (Pichtel et al., 2000).

In recent years, it has become common practice to add organic matter to soils contaminated by heavy metals for their bioremediation. Addition of sewage sludge (Moreno et al., 1999; Madejon et al., 2001; Moreno et al., 2003), beringite and compost (Vangronsveld et al., 1995; Vangronsveld et al., 1996), and Fe-rich limed compost (Li et al., 2000) to soils have been found to immobilize metals and reduce the negative effects on soil microbial populations and enzyme activities. However, the influence of organic matter on a soil's biological and biochemical properties depends on the amount, type, and size of the added organic materials. In turn, the effect of each organic material on soil biological properties depends on its dominant component.

Since many enzymes respond immediately to changes in soil fertility status, they can be used as potential indicators of soil quality for sustainable management (Garcia et al., 2000). Enzymes may react to changes in soil management more quickly than other variables and therefore may be useful as early indicators of biological changes (Bandick and Dick, 1999; Masciandaro et al., 2004). They may also indicate the soil's potential to sustain microbiological activity (Paul and Clark, 1989). Suter et al. (2000) emphasized the importance of using bioindicators in assessing ecological risks and not only to relay additional information on the soil physical-chemical properties in soil surveys.

Hydrolases act on the basic processes of organic matter decomposition. Hydrolytic enzymes such as ß-glucosidase, urease, phosphatase, and arylsulfatase involved in C, N, P, and S cycling, respectively, are sensitive indicators of management-induced changes in soil properties because of their strong relationship with soil organic matter content and quality (Pascual et al., 1998; Masciandaro and Ceccanti, 1999; Masciandaro et al., 2004). These parameters are the most sensitive to the changes which occur in a soil, and provide rapid and accurate information concerning soil quality, thereby helping decide on the best ways of maintaining sustainable productivity (Tejada et al., 2006).

The objective of this study was to investigate under laboratory conditions the effect of the adsorption capacity of two different organic wastes (a crushed cotton gin compost and a poultry manure) on a soil contaminated by Pb at various rates, studying this effect on the activities of ß-glucosidase, protease-BBA, urease, phosphatase, and arylsulphatase, which are important in the cycling of soil C, N, P, and S.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Soil and Organic Wastes
The soil used in this experiment is a Typic Xerofluvent, the general properties of which (0–25 cm) are shown in Table 1. The organic wastes applied were a crushed cotton gin compost (CCGC) and a poultry manure (PM) and their general properties are shown in Table 2.


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  		Table 1. Main soil characteristics and standard error in parenthesis (data are the means of 5 samples).

 

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  		Table 2. Characteristics of the organic wastes used and standard error in parenthesis (data are the means of 5 samples).

 
Organic matter content was determined by dry combustion method according to the official methods of the Spanish Ministry of Agriculture (MAPA, 1986). To determine humic and fulvic acid C, organic wastes were extracted with 0.1 M sodium pyrophosphate and 0.1 M sodium hydroxide. The supernatant was acidified to pH of 2 with HCl and allowed to stand for 24 h at room temperature. To separate humic acids from fulvic acids, the solution was centrifuged and the precipitate containing humic acids was dissolved with sodium hydroxide (Yeomans and Bremner, 1988). The carbon content of humic acid and fulvic acids was determined by the method of Sims and Haby (1971). Total N was determined by Kjeldahl method (MAPA, 1986). Inorganic soluble P (PO4H2– principally) was determined by Willians and Stewart method, described by Guitian and Carballas (1976) after nitric and perchloric acid digestion. Calcium, Mg, Fe, Cu, Mn, Zn, Cd, Pb, Ni, Cr, and Hg were determined by atomic absorption spectrometer after nitric and perchloric acid digestion. Potassium and Na were determined by atomic emission spectrometer after nitric and perchloric acid digestion.

Incubation Procedure and Analytical Determinations
Three hundred grams of sieved soil (<2 mm) were mixed with a solution of PbSO4 at seven concentrations (100, 250, 500, 1000, 2500, 5000, and 8000 mg kg–1 soil). Before the Pb solution was added, the soil samples were preincubated for 7 d at 30 to 40% of their water-holding capacity, according to Moreno et al. (2003). After this preincubation period, soil samples were mixed with PM at a rate of 10% or CCGC at a rate of 17.2%, applying to the soil the same amount of organic matter with each organic amendment. An unamended soil was used as the control. Distilled water was added to each soil to bring it to 60% of its water-holding capacity. Triplicate treatments were kept in semiclosed microcosms of the kind described by Naseby and Lynch (1998), and incubated in darkness at 25°C inside an incubation chamber for four lengths of time (1, 7, 15, and 45 d).

Five enzymatic activities were measured by the following procedures. Urease activity was determined by the buffered method described by Kandeler and Gerber (1988); the hydrolitic activity of protease on N-{alpha}-benzoyl-L-argininamide, (BBA) protease, was by the method proposed by Nannipieri et al. (1980); ß-glucosidase activity according to Masciandaro et al. (1994); alkaline phosphatase activity by the method of Tabatabai and Bremner (1969), except that incubation was at 30°C in maleate buffer, and arylsulfatase activity by the method described by Tabatabai and Bremner (1970).

The percentage inhibition of a biological activity was calculated from

Formula 1[1]
where T is the activity in the metal-polluted soil and C is the activity in the control soil.

Statistical Analysis
Analysis of variance (ANOVA) was performed for all variables and parameters, considering all the data collected (columns corresponding to incubation days and rows corresponding to soil Pb concentration) using the Statgraphics v. 5.0 software package (Statistical Graphics, 1991). The means were separated by the Tukey's test, considering a significance level of p < 0.05 throughout the study. For the ANOVA analysis, triplicate data were used of each treatment and every incubation day.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Tables 3GoGoGo through 7 show the values of the enzymatic activities of the soils polluted with Pb and for all the treatments during the incubation period. Figures 1GoGoGo through 5 show the inhibition percentage of the soil enzymatic activities of the soils polluted with Pb after four different incubation times (1, 7, 15, and 45 d).


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  		Table 3. Urease activity in soils polluted with Pb. Standard error in parenthesis.

 

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  		Table 4. BBA-protease activity in soils polluted with Pb. Standard error in parenthesis.

 

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  		Table 5. ß-glucosidase activity in soils polluted with Pb. Standard error in parenthesis.

 

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  		Table 6. Alkaline phosphatase activity in soils polluted with Pb. Standard error in parenthesis.

 

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  		Table 7. Arylsulfatase activity in soils polluted with Pb. Standard error in parenthesis.

 

Figure 1
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  		Fig. 1. Percentage inhibition of urease activity in soils polluted with different rates of Pb during (a) 1 d, (b) 7 d, (c) 15 d, and (d) 75 d. NS, *, **, ***: nonsignificant or significant at p < 0.05, 0.01, or 0.001, respectively.

 

Figure 2
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  		Fig. 2. Percentage inhibition of BBA-protease activity in soils polluted with different rates of Pb during (a) 1 d, (b) 7 d, (c) 15 d, and (d) 75 d. NS, *, **, ***: nonsignificant or significant at p < 0.05, 0.01, or 0.001, respectively.

 

Figure 3
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  		Fig. 3. Percentage inhibition of ß-glucosidase activity in soils polluted with different rates of Pb during (a) 1 d, (b) 7 d, (c) 15 d, and (d) 75 d. NS, *, **, ***: nonsignificant or significant at p < 0.05, 0.01, or 0.001, respectively.

 

Figure 4
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  		Fig. 4. Percentage inhibition of alkaline phosphatase activity in soils polluted with different rates of Pb during (a) 1 d, (b) 7 d, (c) 15 d, and (d) 75 d. NS, *, **, ***: nonsignificant or significant at p < 0.05, 0.01, or 0.001, respectively.

 

Figure 5
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  		Fig. 5. Percentage inhibition of arylsulfatase activity in soils polluted with different rates of Pb during (a) 1 d, (b) 7 d, (c) 15 d, and (d) 75 d. NS, *, **, ***: nonsignificant or significant at p < 0.05, 0.01, or 0.001, respectively.

 
In the nonamended soils, urease activity decreased during the incubation period both in polluted and unpolluted soils, the lowest values appearing at the highest rates of Pb at the end of the incubation period (Table 3). The statistical analysis indicated significant differences between the different rates of Pb applied in the soil during the incubation period. The urease activity inhibition percentage increased with increasing Pb concentrations and over incubation time (Fig. 1). In this respect, the urease activity inhibition percentage was the highest in the soil treated with 8000 mg Pb kg–1 at the end of the incubation period (90.4%) and lowest in the soil treated with 100 mg Pb kg–1 (26.9%).

The amended soils showed higher urease activity than the corresponding nonamended soils, and contrary to the latter, urease activity increased in these soils during the incubation period. Similarly to the nonamended soils, the values of activity decreased with the increasing Pb pollution. However, the inhibition effect of Pb contamination was lower than that observed in nonamended soils. In this respect at the end of the incubation period, the inhibition percentage of urease activity was 44.9 and 40.7% lower in soils amended with PM and CCGC, respectively, than in the nonamended soil.

For protease-BBA activity, the values were lower in the nonamended soils than in the amended soils (Table 4). For all treatments, the lowest values appeared in soils polluted with 8000 mg Pb kg–1 soil. With regards to the amended soils, the values were higher in the CCGC- than in the PM-amended soils. The protease-BBA activity inhibition percentage was greater in the nonamended soils than in the PM- and CCGC-amended soils (Fig. 2). In this respect, the protease-BBA activity inhibition percentage at the end of incubation period was 58.2 and 57.9% higher in the nonamended soils than in the PM- and CCGC-amended soils. Also, the protease-BBA activity inhibition percentage at the end of the incubation period was slightly higher (0.3%) in the PM- than in the CCGC-amended soil in soils with the highest rate of Pb. The inhibition of protease-BBA activity decreased significantly (p < 0.05) over incubation time in the CCGC-treated soils while this was not observed in the PM-treated soils.

The ß-glucosidase activity decreased with incubation in the nonamended soils, whereas it increased in the amended soils (Table 5). At each incubation period amended soils showed higher activity values than nonamended soils, values decreasing as the pollution level increased. In this respect, the inhibition percentage of this enzyme activity at the end of the incubation period in soils polluted with 8000 mg Pb kg–1 were 56.9 and 63.3% lower in soils amended with PM and CCGC, respectively, than in nonamended soil (Fig. 3). Again, the inhibition percentage of the enzymatic activity at the end of the incubation period was 14.7% lower in CCGC than in PM-amended soils polluted with 8000 mg Pb kg–1. The statistical analysis pointed to significant differences between the different rates of Pb applied to the soil.

Alkaline phosphatase activity in the nonamended soils decreased during the incubation period, the lowest values occurring at highest rate of Pb at the end of the incubation period (Table 6). The statistical analysis indicated significant differences between the different rates of Pb applied in the soil during the incubation period. The inhibition percentage of the enzyme activity increased when the Pb concentration increased in the soil (Fig. 4). In this respect, the inhibition percentage of the enzymatic activity was greatest at the end of the incubation period in the soil treated with 8000 mg Pb kg–1 (96.6%) and lowest in the soil treated with 100 mg Pb kg–1 (55.6%). For amended soils, this enzyme activity was higher than in the nonamended soils, the activity being highest in soils polluted with the lowest dose of Pb and lowest at the highest dose of Pb. Alkaline phosphatase activity inhibition was also higher in nonamended soil than in amended soils. In this respect and at the end of the incubation period, the alkaline phosphatase inhibition percentage was 42.7 and 62.1% lower in soils amended with PM and CCGC, respectively, than in nonamended soil. Again, the inhibition percentage of the enzymatic activity at the end of the incubation period was lower (33.9%) in CCGC- than in PM-amended soils polluted with 8000 mg Pb kg–1.

Arylsulfatase activity was lower in nonamended soils than the amended soils (Table 7). In all treatments, the lowest values were obtained in soils polluted with 8000 mg Pb kg–1. The statistical analysis indicated significant differences in activity between the different rates of Pb applied in the soil during the incubation period. Except for 8000 mg Pb kg–1, CCGC-amended soils showed higher arylsulphatase activity than PM-amended soils. The arylsulphatase activity inhibition percentage was higher in the nonamended soils than in the PM- and CCGC-amended soils (Fig. 5). In this respect, the inhibition percentage of the enzymatic activity at the end of the incubation period in soils polluted with 8000 mg Pb kg–1 soil was higher (24.5 and 16.9%) in nonamended soil than in the PM- and CCGC-amended soils.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Heavy metal pollution of soil has been recognized as a major factor impeding soil microbial processes (Stuczynskiel et al., 2003). Our results indicate that soil enzymatic activities decreased with increasing Pb concentrations, which indicates that Pb has a toxic effect on the biochemical reactions measured. Many of the enzyme activities were decreased already by 50% the first day of incubation with the lowest Pb pollution level. These results are in agreement with those of Chlopecka et al. (1996), Marzadori et al. (1996), and Stuczynskiel et al. (2003). According to Guiller et al. (1998) heavy metal pollution will not only result in adverse effects on various parameters relating to plant quality and yield, but also cause changes in the size and activity of soil microbial communities.

The interactions between Pb and enzymatic activities over time may not directly depend on the Pb activity in soil solution, which is the often-suggested mechanism of microbial process exposure to metal pollution (Stuczynskiel et al., 2003). Moreno et al. (1999) suggested that the decrease in soil enzymatic activities with incubation time is presumably due to the diminution with time of the substrates easily available to microorganisms. The dynamic of some enzyme activities during the incubation period after heavy metal addition may be related to the dynamics of the soil microbial populations. They decreased on depletion of readily available substrate resulting from heavy metal toxicity and starved as the reserves were exhausted, and decreased significantly in size up to 45 d. The reduction in soil microbial biomass under the heavy metal stress conditions was also due to the additional energy cost to soil microorganisms (Cervantes, 1994), which may result in a decrease in the amount of substrate that is available for growth (Akmal et al., 2005).

In our study negative relationships between total heavy metal content and soil enzymes were observed. The microbiological characteristics of a soil may show considerable differences that are associated with their sensitivity to heavy metals. Many authors have reported the negative effects of heavy metal contamination on the microbiological characteristics of soils; for example, Hattori (2000) found that CO2 production was significantly depressed in soils contaminated with heavy metals. Conversely, other authors have found that microbial biomass carbon and some enzyme activities increase in contaminated soils (Fließbach et al., 1994). According to Kizilkaya et al. (2004) differences in microbial community structure between soils, which vary in sensitivity to heavy metal toxicity, may be an important factor in explaining these discrepancies.

The results obtained in this study indicate that the addition of organic matter to the soil decreased the extent to which soil enzymatic activities were inhibited by Pb. These results are in agreement with those of Moreno et al. (1999) and Moreno et al. (2003), who observed a decrease in the inhibitory effects on biological parameters after the addition of sewage sludge to soils polluted with Cd and Ni. Also, Kiikkila et al. (2001) recorded an increase in soil microbial activities in soils polluted with Cu and Ni after the addition of a mixture of compost and wood chips.

The highest activities of urease and BBA protease (both involved in the N cycle) were observed in the soils receiving organic amendment. The stimulation of these two enzymatic activities with respect to the nonamended soil suggests that the amendment used did not contain compounds toxic for these activities, it increased soil microbial growth due to the substrates added, and added microbial cells and/or enzymes, which counteract any inhibitory effect of the toxic compounds. Garcia et al. (1994) studied the influence of some toxic compounds (including heavy metals) contained in organic amendments, such as municipal solid wastes, on soil microbial activity in semiarid zones, finding that the positive effect of the organic matter on biological soil quality counteracted the negative effect produced by these toxic compounds. In addition, the organic amendment binds the Pb, decreasing its availability.

The existence of phosphomonoesterase activity in amended soils is interesting since this hydrolase manages to hydrolize phosphorus organic compounds to render them inorganic and therefore more useable by microorganisms and plants (Speir and Ross, 2000). The high activity detected in amended soils suggests either the existence in organic wastes of phosphorus compounds that can act as substrate for the enzyme, or the existence of microbial populations which need inorganic phosphorus for their own development, stimulating the enzyme synthesis.

Humic substances influence the biological properties of toxic ions, acting as an accumulation phase for heavy metals following the formation of metal-humate complexes (chelates) with different degrees of stability, probably as a result of the humic substances containing several major functional groups, such as carboxyl, phenolic, alcohol, and carbonyl (Datta et al., 2001). Much of the Pb may have become unavailable due to reactions with minerals, soil organic matter, or inorganic anions (Undabeytia et al., 1996).

Our results pointed to differences in the percentage of inhibition of soil enzymatic activities in PM- and CCGC-amended soils. The principal difference between both organic wastes was the humic and fulvic acid concentration, CCGC having a higher humic acid concentration than PM. It is clear that materials that are formed through accelerated fermentation processes, such as composting, are able to immobilize enzymes in their humic fraction in a higher proportion than fresh materials (Pascual et al., 1998). It is possible that the organic material itself influences such complex formation. The PM has little humified material available (extractable carbon with sodium pyrophosphate), and this carbon type may be the one that collaborates in the formation of enzymatic complexes in our study.

In addition, humic and fulvic acids differ in their structures. Fulvic acids are macromolecules with a lower polymerization index, are more highly charged, more polar, and have a lower molecular weight than humic acids. Hayes (1991) suggested that humic substances with higher molecular fractions contain more strong acid groups than the lower molecular weight materials. Humic acids have greater aromaticity than fulvic acids, and this is also in keeping with the concept of greater numbers of aromatic carboxylic acids in the humic acids. For this reason, the formation of chelates with Pb may be more common in humic than in fulvic acids. These results also suggest that soil enzymatic activities are higher in humic acid- than in fulvic acid-amended soil.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
The application of CCGC and PM in the doses studied to a soil polluted with Pb under laboratory conditions improved the soil enzymatic activities compared with no organic amended soils. The enzyme activities studied were inhibited by Pb and both organic amendments decreased Pb toxic effects significantly. The inhibition of protease-BBA was similar in the PM- and CCGC-treated soils. However, urease, ß-glucosidase, alkaline phosphatase, and arylsulphatase activities were inhibited more significantly in PM- than the CCGC-treated soils. The following order of inhibition was found in the enzyme activities by the greatest Pb concentration (8000 mg kg–1 soil) in the nonamended soils compared to nonpolluted counterparts: protease-BBA (16 times lower) > ß-glucosidase (five times lower) > alkaline phosphatase = arylsulphatase (four times lower) > urease (three times lower). Our study provides trends of the extent that different levels of Pb pollution can negatively impact different soil enzyme activities important for soil functioning. Our results suggest that: (1) the addition of these organic materials may be considered a good strategy for remediating heavy metal-contaminated soils, and (2) the addition of organic materials with a high humic acid content is beneficial for such remediation.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 




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