Composite Biochar with Municipal Sewage Sludge Compost—A New Approach to Phytostabilization of PTE Industrially Contaminated Soils

Abstract

The presence of potentially toxic elements (PTEs) in soils can upset the natural balance and increase the risk of PTE incorporation into the food chain. The use of composite biochar with municipal sewage sludge compost (MSSC/C) can be an effective way of both managing waste, such as sewage sludge, and providing an effective additive-supporting phytostabilization processes. The effectiveness of D. glomerata and MSSC/C in the technique of assisted phytostabilization of industrially contaminated soils was determined under the pot experiment conditions. The PTE contents in D. glomerata and the soil were determined using the spectrophotometric method. The addition of MSSC/C to PTE-contaminated soil contributed to an 18% increase in plant biomass and increased the soil pH by 1.67 units, with the PTE concentration being higher in the roots than in the above-ground parts of D. glomerata. The MSSC/C addition had the strongest effect on the reduction in Cd, Cr, and Ni contents in the soil following the completion of the experiment. The current study confirmed the effectiveness of MSSC/C in aiding the phytostabilization processes in PTE-contaminated soils.

1. Introduction

The rapid development of industry, agriculture, and transport and the increase in urbanization over the last century have brought about environmental changes involving increased concentrations of potentially toxic elements (PTE) in the soil, water, and air [1]. PTE contamination can affect the entire environment, with the most severe and long-lasting effects, however, being noted in soils [2], which is due to the adsorption of large amounts of PTEs in clay and humus soil colloids. Currently, in heavily urbanized and industrially active areas, the PTE content exceeds acceptable standards, which necessitates their remediation. Therefore, new methods are being sought for cleaning up the soil environment that are more effective and economical, and, importantly, do not involve interfering with the soil structures and functions. In recent years, methods involving much less environmental interference than the previously known physico-chemical remediation methods have been increasingly employed [3]. An alternative solution involves increasingly popular biological methods [4]. One of the most rapidly developing and promising technologies is phytoremediation, which uses plants to clean up soils, waters, or sediments [5]. Increasing hopes are being raised for plant-using methods, including L. perenne, F. rubra, or B. juncea as tools for immobilizing PTEs in the soil environment [6,7]. Moreover, the above-ground part of plants can provide a space for PTE sorption or precipitation, thus performing a key task in groundwater protection and a reduction in the spread of PTEs [8]. By producing and secreting organic compounds to the rhizosphere, plants can affect changes in the soil pH and the oxidation/reduction potential and reduce PTE ions to unavailable forms [9].

Phytostabilization is a process that involves the immobilization of PTEs in the soil with the participation of compounds produced by plants, which prevents further movement of contaminants deep into the soil profile and, further, to waters and down the food chain [10]. This technique can also contribute to a reduction in PTE bioavailability by precipitating them into less soluble compounds [11]. Therefore, phytostabilization contributes to an improvement in the biological and chemical properties of the soil. This technique can be applied to both the PTE and organic contamination of the soil. A new approach to the phytostabilization technique is the incorporation of soil amendments to reduce the PTE bioavailability in the soil and convert them into hardly soluble or insoluble forms (aided phytostabilization) [12]. A variety of organic and inorganic materials can be used as soil additives, either alone or in combination.

Degraded areas are those with unfavorable conditions for vegetation growth. In this case, the effect of reducing the PTE mobility and improving the vegetation growth and development can be achieved by means of incorporating organic or mineral additives with a very high sorption capacity into the soil. To this end, various mineral additives, such as montmorillonite, halloysite, chalcedony, lime, and zeolite, are used [13,14]. The use of additives rich in organic matter, such as sawdust, biochar, or composts, can be an equally effective way of immobilizing PTEs in soils [15]. The use of stabilized organic matter rich in humic acids using the aided phytostabilization technique results in the permanent binding of PTEs and their immobilization. The beneficial effects of biochar include an increase in micro- and macro-element soil storage and retention capacity [16]. The highly exchangeable sorption capacity increases the macro- and micronutrient content in the soil profile, which increases the efficiency of their uptake by plants while reducing the risk of leaching and transport to the surface and underground water bodies [17]. Municipal sewage sludge (MMS) contains many valuable nutrients (N, P, Ca, Mg, and micronutrients) [18], has a high calorific value (it can be used to generate electricity and heat in processes such as thermal disposal) [19], and contains organic compounds that enable its fermentation to produce biogas for electricity and heat generation [20]. Currently, the predominant method of sewage sludge management is storage and natural utilization [21]. Therefore, it is necessary to develop environmentally friendly methods for the efficient management of MSS, particularly composting [22]. Considering the abundance of sewage sludge in nutrients and the relatively low costs of operating composting facilities, as well as the principles of circular economy, it appears that the MSS composting potential is not being fully exploited. Satisfying the quality criterion and ensuring proper process conditions allows compost of the right quality to be obtained [23]. After composting, MSS can be used as a substrate for the production of organic fertilizers or plant growth promoters or for the reclamation of degraded areas [24]. The agricultural use of MSS is popular due to the lower costs associated with sludge management as compared to other, more advanced methods [25]. Organic fertilizer produced from MSS serves many important functions: it regulates soil pH; enables the preservation of a proper soil structure; provides plants with nutrients, as well as macro- and microelements; and is a humus substrate [26]. The use of MSS compost as an additive to aid immobilization processes can maintain the nutrient cycle and close the element cycle in the ecosystem [9].

The study presented in this paper was aimed at assessing the effect of adding composite biochar with municipal sewage sludge compost and D. glomerata on the phytostabilization of soils industrially contaminated with PTE. The study evaluated the yield volume and the PTE content in the above-ground parts and the roots of the test plants after the completed aided phytostabilization experiment. Selected physical and chemical parameters of the soil before and after the experiment, such as the pH value and the Cu, Ni, Cd, Pb, Zn, and Cr contents in the soil, were determined as well.

2. Materials and Methods

2.1. MSSC/B Properties and Characterization

The MSSC/B composite was obtained by mixing compost produced from municipal sewage sludge (60% w/w) mixed with wood chips (15% w/w), rape straw (22% w/w), and mature compost as inoculation (3% w/w) with biochar produced from willow chips (pyrolyzed at 650 °C for 15 min at a heating rate of approximately 3 °C/s). The two additives were mixed together in a ratio of 70% compost to 30% biochar. The physical and chemical characteristics of the compost and biochar used in the experiment are presented in

Table 1. Selected physical and chemical characteristics of MSSC and biochar (n = 3 ± standard deviation).

Characteristic	Unit	MSSC	Biochar
Surface area BET	m2/g	12.5	313.73
Total area in pores	m2/g	1.13	92.9
Total volume in pores	cm3/g	0.011	0.113
pH	-	7.1 ± 0.2	10.4 ± 0.3
Electrical conductivity	mS/cm	12.2 ± 0.4	2.9 ± 0.1
Volatile matter	%	34.7 ± 0.7	16.5 ± 0.5
Cation exchange capacity	Cmol/kg	49.5 ± 1.4	48.59 ± 2.3
Cd	mg/kg	0.8 ± 0.2	0.2 ± 0.05
Cr	mg/kg	55.2 ± 2.8	9.6 ± 0.7
Cu	mg/kg	57.6 ± 7.6	13.9 ± 6.3
Ni	mg/kg	23.4 ± 3.6	10.2 ± 0.1
Pb	mg/kg	8.2 ± 0.8	1.1 ± 1.6
Zn	mg/kg	253.7 ± 18.2	200.2 ± 10.7
P2O5	wt%	2.57	6.01
CaO	wt%	1.04	29.8
SiO2	wt%	4.62	19.7
Na2O	wt%	0.93	1.1
MgO	wt%	1.44	3.7
K2O	wt%	0.64	14.4
Al2O3	wt%	2.2	2.5
Fe2O3	wt%	3.16	3.7

.

2.2. Soil Collection and Preparation

The soil used in the experiment was collected according to the methodology provided by Radziemska et al. (2021) [9]. The area selected for the study into the use of MSSC/B for aided phytostabilization of Cu, Ni, Cd, Pb, Zn, and Cr was a site in central Poland (52°09′30.7″ N 20°59′30.2″ E), on which metal scrap waste had been stored directly on the ground for more than 70 years. Approximately 10 kg of representative soil was collected by taking five sub-samples from a 1 × 1 m square. The soil was then transferred into appropriately labelled bags and transported to the laboratory. The soil samples were air-dried at room temperature and sifted through a 2 mm sieve. The soil was kept in a refrigerator at 4 °C until the experiment was set up. The soil was characterized by the following parameters: pH of 8.7 ± 0.16; CEC, 54.2 ± 0.7 Cmol/kg; Cu, 828 ± 5.59 mg/kg; Ni, 785 ± 76.20; Cd, 25.9 ± 12.98; Pb, 1532 ± 13.44 mg/kg; Zn, 7496 ± 51.54 mg/kg; and Cr 637 ± 7.15 mg/kg. The soil was classified as loamy sand (71.6% sand, 27.2% silt, 1.2% clay).

2.3. Experiment Design

The experiment was conducted in five replicates in a greenhouse under natural day/night conditions; during the day (14 h), the air temperature was 26 °C ± 3 °C, and ~10° lower (16 °C ± 2 °C) at night (10 h), with a relative humidity of 75% ± 5% for 65 days. The soil mixed with MSSC/B in an amount of 3.0% (w/w) was placed into 5 kg pots, while the soil alone (without MSSC/C, 0.0%, w/w) was designated as the control. Before sowing the plants, the pots were located in a dark room for more than two weeks in order to equilibrate the soil mixture. After this time, 5 g of D. glomerata cv. Berta seeds per pot were sown. The plants were watered every second day with distilled water to 60% of the maximum water-holding capacity of the soil. Soil moisture content for each pot was maintained at the field capacity every three days. After the completion of the experiment, soil samples, as well as the above-ground part and the roots of the plants, were collected from each pot.

2.4. Determination of Physico-Chemical Parameters in Plants, Soil, and MSSC/B

Before the analyses, the plants were powdered in an analytical mill (Retsch type ZM300, Hann, Germany) after pre-washing them in tap water, followed by deionized water, and then dried at room temperature. The above-ground parts and the roots of D. glomerata were mineralized in nitric acid (HNO₃, analytical grade) and 30% H₂O₂ in a MARSXpress microwave digestion vessel (CEM Corporation, Matthews, NC, USA). The total concentration of Cu, Ni, Cd, Pb, Zn, and Cr was determined by the atomic absorption spectroscopy (AAS) method using a Varian spectrophotometer AA28OFS. The pH values in distilled water extracts (1:2.5 w/v) were determined in the soil samples before and after phytostabilization using a pH meter (Model HI 221, Orion, NC, USA). The particle size of the soil was determined using a Mastersizer 2000 apparatus (Malvern, UK). The cation exchange capacity of the soil and MSSC/C was calculated as the sum of hydrolytic acidity (in 1 M Ca(CH₃COO)₂) and exchangeable bases (in 0.1 M HCl). Total PTE contents in the soil and MSSC/C were determined following mineralization in a mixture of concentrated HCl, HNO₃, and H₂O₂ in a microwave digestion vessel (MARSXpress, CEM Corporation, Matthews, NC, USA) using a spectrophotometer (Varian, AA28OFS, Mulgrave, Australia). The correctness of the analyses was assessed using the reference material (CRM 142 R), and the obtained recoveries ranged from 95% to 101%. All analyses were conducted in triplicate.

2.5. Statistical Analyses

Statistica 13.3 software was used to conduct the statistical analysis. To analyze the data, a one-way analysis of variance (ANOVA) or the Kruskal–Wallis test was used as the statistical method. Following the application of Tukey’s test (HSD), further analyses were conducted regarding the data, with significant differences identified between variables.

3. Results

3.1. Effect of MSSC/B on D. Glomerata Growth

In order to assess the potential effects of the incorporation of MSSC/B into the soil on plant growth, the D. glomerata yield volume was determined after the completion of the experiment involving aided phytostabilization of industrially contaminated soils. The average test plant biomass yield is shown in Figure 1. The effect of the addition of MSSC/B, tested in the experiment, on the D. glomerata yield volume was significantly (p < 0.05) noticeable in the control series (without MSSC/B)—the test plant yield was lower and the plants developed slower, which may be associated with the presence of elevated PTE levels in the soil from industrial areas. The application of MSSC/B in the study resulted in a significant increase in the D. glomerata yield (by 18%) compared to the control series.

3.2. PTEs Contents in D. Glomerata following MSSC/B Application

To evaluate the effects of MSSC/Bs on PTE uptake, the concentrations of Cu, Ni, Cd, Pb, Zn, and Cr in the roots and the above-ground parts of D. glomerata were determined. As shown in Figure 2, in all the analyzed cases, the PTE concentrations were significantly higher in the roots than in the above-ground parts of the plant. This trend was particularly evident in the application of MSSC/B into the soil. As regards the individual PTEs in the above-ground parts of D. glomerata, a positive effect was exerted by the addition of MSSC/B, which reduced the Cd content by 22%, respectively, in this part of the plant. Regarding the effect of the application of MSSC/B into the soil on the increase in the PTE content in the roots of D. glomerata, an increase was observed in the Cu, Ni, Cd, Pb, Zn, and Cr contents by 33%, 29%, 19%, 54%, 11%, and 24%, respectively, as compared to the control series.

3.3. Soil pH after MSSC/B Application

The soil pH parameter value was significantly dependent on the MSSC/B incorporated into the soil and is presented in Figure 3. The application of MSSC/B into the soil in order to aid phytostabilization processes contributed significantly to an increase in the soil pH value by 1.67 units, as compared to the soil with none of this additive applied.

3.4. PTEs Content in the Soil after MSSC/B Application

Total Cu, Ni, Cd, Pb, Zn, and Cr contents in the soil following the completion of the aided phytostabilization experiment are presented in Figure 4. It should be noted that the PTE contents in the soil used in the experiment were higher than those predicted in permissible concentrations as provided in the Regulation of the Polish Minister of the Environment [27], which was particularly evident for Cu, Ni, Cd, and Pb. The application of MSSC/B led to a significant decrease in total Cu, Ni, Cd, Pb, Zn, and Cr concentrations in the soil as compared to the control (no MSSC/B) by 31%, 46%, more than twofold, 27%, 19%, and 46%, respectively.

4. Discussion

In the biogeochemical cycle of PTEs, a crucial role is played by the soil and rhizosphere, in which numerous interrelated reactions are observed. What is most ecologically hazardous is the elevated PTE concentration in the topsoil, as there is a danger of PTE entering through the root system and reaching the other plant parts [28]. The lines of activities aimed at sustainable management of soil resources require a reduction in the pressure resulting mainly from human activity, as well as a search for new and effective methods of protection against the contamination. The increasing amount of waste materials can serve as new, potentially useful soil amendments and, in many cases, can offer an alternative to the use of other traditional additives [29]. An important aspect of the so-called circular economy is the safe, natural use of organic materials, including municipal waste, which includes sewage sludge [30]. In the aided phytostabilization technique, an extremely important aspect is the proper development of vegetation on a PTE-contaminated site. This is associated with a number of benefits offered by plants, including a favorable effect on the initiation of soil-forming processes, improved biological life, and protection against water and wind erosion [31]. In the paper, the authors demonstrated a significant (p < 0.05) positive effect of the addition of MSSC/B into the soil on the development of D. glomerata cultivated on soil with high Cu, Ni, Cd, Pb, Zn, and Cr levels. The application of this soil amendment resulted in an 18% increase in the test plant yielding compared to the control series. The positive effect of compost application on the increase in the grass yield in the technique of aided phytostabilization of PTE-contaminated soils was also confirmed by studies conducted by other authors [9,32]. Composts contain considerable amounts of macro- and microelements, which largely occur in bioavailable forms so that the nutrients are more tightly bound in the sorption complex and, thus, have a positive effect on plant yielding and development [33]. However, biochar alkalizes the soil and enhances the effect of binding the mobile PTE fraction by absorbing, complexing, or precipitating PTEs, thus reducing their bioavailability and toxicity to plants [34]. Biochar increases the organic matter content, which also has a positive effect on plant growth and yielding [35,36,37,38]. Gonzaga et al. [36] used orange shell and coconut husk biochar to obtain an increase in the yield of B. juncea by 145–197% and 105–232%, respectively. The increase in the plant biomass, triggered by the application of biochar into the soil, was likely related to a temporary improvement in the carboxylation efficiency, which may be due to the fact that the plants were able to assimilate more CO₂ even where the intracellular CO₂ level was initially low [28]. Calcareous soils are also used to stabilize heavy metals. In addition, highly alkaline amendments are used for both acidic and calcareous soils. Wang et al. [39] used red mud, a strongly alkaline additive (pH 11.2), to stabilize heavy metals (Cd, Cu, Pb, and Zn) in calcareous agricultural soils with an initial pH of 8.3 at the field scale. Changes in soil pH can adversely affect crop growth and yield. However, in the current study, no negative effects on D. glomerata growth were observed despite the high soil pH. Similar observations were made by Wang et al. [39] in wheat grown on calcareous soil amended with red mud. Wheat yield was 406 kg/ha in the control soil and reached 506 kg/ha in soil amended with 5% red mud. The increase in wheat yield despite the high soil pH indicates that the addition of red mud increased the fertility of the soil, especially the content of available potassium. D. glomerata grows best in soils with a pH between 6 and 7, but can also be found in the range of 5.5 to 8.0. The increase in yield of D. glomerata in soils with highly alkaline pH values suggests that soil amendment with MSSC/C had a positive effect on soil fertility. Based on the characterization of the amendments used in the present study, biochar was rich in potassium (14.4% K₂O), which may be available to some extent even in highly alkaline environments. As reported by Licht and Smith [40], biochar also causes greater water consumption, thus making plants process the absorbed CO₂ more efficiently. Plants serve an important role in cleaning up the environment, including the PTE-contaminated soils. The amount of PTEs taken up depends on their concentration in the soil, the plant species, and the soil conditions, e.g., the pH, salinity, and organic substance content [39,40,41,42,43]. Grass species are used in the phytostabilization process due to their perennial growth cycle and the branched root system that stabilizes the soil structure [44,45]. Moreover, the rapid effect of vegetation cover greening, obtained in the cultivation of grasses, prevents the penetration of nitrogen and phosphorus compounds, which promotes soil renewal [46]. The application of MSSC/B in the experiment may have promoted the formation of insoluble PTE complexes with limited bioavailability to plants, as evidenced by the fact that for all the analyzed PTEs, their amount in the above-ground parts was significantly lower following the application of this additive into the soil, as compared to the control series. The greatest increase in the PTE content in the roots of D. glomerata was noted for Pb, Cu, Ni, and Cr. It is noteworthy that other authors also noted the ability of the plant root system to accumulate PTEs, with only negligible amounts of PTEs being transported to the above-ground parts of plants, especially when organic additives, such as sewage sludge compost or fish byproduct compost, were added to the soil [9,14,32]. PTEs can be bound by organic substances by means of exchange sorption, complexation, or chelation [47]. The soil pH affects the plant growth and development, and also determines the solubility of PTEs and the nutrient availability to plants, affects the rate and direction of the biological and physico-chemical processes occurring in the soil, and determines the equilibrium state of the sorption and desorption processes taking place in the soil [48]. The pH of soils affects PTE mobility in the soil environment. Moreover, the acidic and very acidic reactions of contaminated soils pose an environmental hazard associated with increased PTE mobility and, thus, their increased involvement in the biogeochemical cycle [49]. In the current study, the application of MSSC/B into the soil contributed to a significant increase in the soil pH value. Alkalization of the soil environment is one of the crucial mechanisms leading to a minimized risk of PTE leaching from the ground [9]. This effect can be obtained, for example, by incorporating composts or biochar into the soil. Similar observations were made by Radziemska et al. [9], who used composts and biochar in order to aid the phytostabilization of soils severely contaminated with PTEs in post-industrial areas. The additional incorporation of soil amendments in the aided phytostabilization technique, e.g., in the form of composts, results in organic matter forming simple or complex chelate compounds [50], which prevents the movement of PTEs by immobilizing them in the soil. The results clearly show that the application of MSSC/B significantly contributed to a reduction in the soil accumulation of PTEs, particularly Cu, Ni, Cd, Pb, Zn, and Cr. In view of the conducted study, it can be concluded that the use of this type of soil amendment can be regarded as an effective induction of PTE immobilization in the soil.

5. Conclusions

Environmental contamination with PTEs is a common environmental problem of ever-increasing importance. The main idea behind the concept of using waste soil amendments in the aided phytostabilization technique is to increase both the level of PTE immobilization and the ecological potential of degraded areas. The experiment described in this paper demonstrated the effectiveness of MSCC application in soil contaminated with Cu, Ni, Cd, Pb, Zn, and Cr in supporting the growth and development of D. glomerata. The greatest increase in the PTE content in the roots, as compared to the D. glomerata control series, was noted for Pb, Cu, Ni, and Cr, while the greatest reduction in the PTE content in the soil following the application of MSSC/B was noted for Cd, Ni, and Cr. MSSC also had a positive effect on the increase in the soil pH value. In summary, it can be concluded that composite biochar with municipal sewage sludge compost may provide an excellent alternative to other soil amendments in the technique of aided phytostabilization of PTE-contaminated soils.