Effects of adding biochar on the preservation of nitrogen and passivation of heavy metal during hyperthermophilic composting of sewage sludge

ABSTRACT

Hyperthermophilic composting (HTC) is regarded as an effective method for processing sewage sludge. The aim of the study was to investigate effects of using biochar as an amendment on the preservation of nitrogen and passivation of heavy metal during the HTC process of sewage sludge. Results showed that HTC improved the fermentation efficiency and the compost maturity by increases in the temperature and germination index (GI) value, and decreases in the moisture and C/N ratio compared to conventional thermophilic composting. HTC process and the biochar addition resulted in a decrease of the nitrogen loss compared with the control pile during composting by promoting transforming ammonium into nitrite nitrogen. Adding biochar to composting inhibited the transformation of Cu, Zn and Pb into more mobile speciation compared to the control pile although their contents increased during composting, which lead to reduction in availability of heavy metals. Thus, HTC process with the addition of biochar is viable for the reduction of the nitrogen losses and mobility of heavy metal in compost.

Implications: The treatment of sewage sludge is imminent due to its threat to general health and ecosystems. This work represents the effects of adding biochar on the preservation of nitrogen and passivation of heavy metal during hyperthermophilic composting of sewage sludge. Our results indicate that the additions of biochar and hyperthermophilic composting engendered the several of positive effects on the preservation of nitrogen and passivation of heavy metal. Thus, HTC process with the addition of biochar is viable for the reduction of the nitrogen losses and mobility of heavy metal in compost.

Introduction

With the increase in numbers of wastewater treatment plants (WWTPs), sewage sludge (SS) is generated as a by-product of WWTPs in China (Yu et al. 2018). The total amount of sewage sludge generated by the three major economies of the USA, China, and the European Union, was 137 million tons in 2018 according to GEP Research. Now it is imminent to find methods for efficiently treating sewage sludge (SS). Large quantities of organic matter (OM) in SS have a considerable potential for recovering to use for land applications and providing nutrients for plant growth (Li et al. 2018). However, the recovery of SS lies a potential threat to general health and ecosystems, that is, a higher content of heavy metal in SS will be introduced into the soil when used for land applications. Therefore, there is an urgent need to reduce the potential risks of spreading heavy metal pollution across farming environment and to introduce efficient techniques for passivation.

Composting technology has been globally employed for managing and reusing sewage sludge by the mineralization and partial humification of the OM to obtain stabilized and detoxicated final products (Guo et al. 2020a; Meng et al. 2018; Nguyen and Shima 2019; Yu et al. 2019). The land-application after the composting is widely employed to treat 4 × 10⁷ tons per year of dewatered sludge in China. However, conventional thermophilic composting (TC) with a maximum temperature range of 55–60°C is limited by these technical shortcomings of low processing efficiency, long fermentation cycle and insufficient nutrient quality of compost. Nitrogen emissions (mainly N₂O and 40–80% of NH₃) are mainly derived from an incomplete humification process of OM (especially proteins) during composting, which are the main causes of lower nutrient quality of final compost (Cáceres, Magrí, and Marfà 2015; Courtens et al. 2016). The bio-oxidative process of OM is mainly affected by multiple interacting factors in the composting system, and increasing temperature is regarded as the most effective method for accelerating the humification process and achieving the quick recycling of SS (Cui et al. 2019a; Robledo-Mahón et al. 2019; Yu et al. 2018).

Recently, hyperthermophilic composting (HTC) that involves a hyperthermophilic stage of ≥80°C, is considered as an innovative technology for managing SS due to the application of hyperthermophilic microbe (Liao et al. 2017; Cheng et al., 2018; Cui et al. 2019a; Liu et al. 2020). HTC technology is reported to overcome the disadvantages of conventional TC technology and is provided with more advantages, including improving the OM decomposition to achieve higher efficiency, promoting the deactivation of pathogenic microbes to achieve higher harmlessness and accelerating the evaporation of moisture to reduce the mass of SS (Yu et al. 2018). Meanwhile, it is effective for controlling the nitrogen loss by rising temperatures of composting, which can accelerate the humification of OM to form recalcitrant humic substances (HSs) that are major carrier of recalcitrant nitrogen in compost (Cui et al. 2019b; Gao et al. 2019). Also, growing evidence illustrates that raising temperature can reduce the substrate for ammonification reactions by decreasing ammonification enzyme activities, affecting the expression of NOx-related genes and the ammonifier relative abundance (Cui et al. 2019b; Liu et al. 2020). And, the activity of fungi related to the nitrogen conversion is not affected by higher temperature.

The pollution of heavy metals in sewage sludge has been concerned as potential environmental issues in the land application of compost (Mulchandani and Westerhoff 2016). An increase in the mobility of heavy metal in SS during composting indicates the risk of pollution. HTC technology has obvious advantages in the passivation of heavy metals due to the quickly formation of lots of HSs under the higher temperature. HSs has higher solubility in water and more acidic functional groups for reaction with heavy metal ions to decrease its mobility. Meanwhile, adding additives into compost is an effective way to reduce their mobility and reduce the risk of pollution when using compost in agriculture. Biochar can immobilize heavy metals and organic pollutants during the composting process due to the characteristics of porosity, large specific surface area, and in direct physical adsorption, binding of surface functional groups, ion exchange reaction, and static adsorption (Guo, Liu, and Zhang 2020b). In this respect, biochar that can effectively reduce the mobility of heavy metals in compost, also is added during composting. However, to date, little is known about the complexation effect of biochar on the preservation of nitrogen and passivation of heavy metals during the HTC process.

Based on this background, the research hypothesis is that adding biochar has positive effects on the preservation of nitrogen and passivation of heavy metal during the hyperthermophilic composting of SS. The aim of this study was to: 1) confirm the humification and maturity level during HTC process of SS; 2) determine effects and mechanism of the nitrogen preservation during composting; 3) investigate variation in the mobility of heavy metals and their passivation mechanism during HTC process.

Materials and methods

Experimental materials

The dewatered SS was collected from a municipal wastewater treatment plant (Shijiazhuang, China) and applied as the raw material during composting. Corn straw (CS) used as a bulking agent, was taken from a suburban farm and pulverized to particles (<5 cm in length). Hyperthermophiles of Ureibacillus terrenus (preservation no. 22,991, referred to as UT) that can maintain higher activity during hyperthermophilic condition, and resist to external harmful factors, was supplemented into composting as an agent. The biochar used for the composting experiments was from the pyrolysis of wheat straw at ~550°C in a pyrolysis reactor at the Sanli New Energy Company, China. The basic physicochemical characteristics of raw materials for composting are listed in Table 1.

Table 1. The basic physicochemical characteristics of raw materials.

Materials	TOC/g·kg^−1	TN/g·kg^−1	pH	EC/mS·cm^−1	Moisture content/%	C/N ratio
sewage sludge	410.1	30.6	7.02	2.75	82.8	13.4
corn straw	347.3	8.23	7.11	3.87	8.2	42.2

TOC: total organic carbon. TN: total nitrogen. EC: electrical conductivity

Composting design and operation

Hyperthermophilic composting (HTC) of sludge were conducted using lab-scale composting devices (80 L in volume) for 21 days. Three devices were operated for each pile and 0.4 L·kg·min⁻¹ of air was supplied to the bottom of the reactor to maintain aerobic conditions. The sludge was thoroughly mixed at a dry weight ratio of 3:2 with corn stalk while adding the agent and biochar according to their corresponding amounts. The C/N ratio of the composting mixture was adjusted to 25:1 and the moisture content was adjusted to 60–65%. The ammonia gas from the composting device was introduced into plastic gas bags of 10 L. Composting sampling and turning from each device were performed on days 0, 1, 3, 6, 10, 15, and 21. The experiment design of composting was as follows: SC pile: sewage sludge + corn straw; SCA pile: sewage sludge + corn straw + 5‰ UT agent; SCAB pile: sewage sludge + corn straw + 5‰ UT agent +5% biochar. Each pile was performed in triplicate.

Index measurements

The temperature of the piles and ambient temperature was monitored in real time through inserting thermometer into the pile center connected to a recorder. The moisture content was determined by measuring weight lost after 12 h at 105°C in an oven. The pH and EC values were measured using a multiparameter quality tester (Mettler-Toledo, Switzerland). The germination index (GI) was measured based on the specific measurement method in previous study (Wang, Chen, and Zheng 2020a). Total nitrogen was measured using an element analyzer (Vario EL cube CHNOS, Elementar, USA). Nitrate and ammonium nitrogen, and ammonia gas were measured with a continuous flow analyzer (SEAL,Germany). Cu, Zn and Pb are major heavy metals found in sewage sludge, and can cause serious pollution for the soil (Wang et al. 2020b). Therefore, four speciation of Cu, Zn and Pb, i.e., exchangeable, reducible, oxidizable and residual speciation was extracted by a modified BCR (community bureau of reference) sequential extraction method, and determined using inductively coupled plasma mass spectrometry (ICP-MS, PerkinElmer, USA).

Statistical analysis

All analyses were performed in triplicate. Data are represented as the error bars in the figures. All statistical analyses were carried out using Microsoft Excel 2016, IBM SPSS Statistic v.22 software package and Origin 2018 64bit.

Results and discussion

Variation of physicochemical parameters during composting

Temperature is a critical factor that affects the microbial activity and ammonia emissions during composting and characterizes the efficiency of composting (Ma et al. 2019; Wang et al. 2021a, 2019). The variation in temperature of all piles had a similar trend of heating, thermophilic (temperature > 50°C) and even hyperthermophilic (temperature >70°C), and cooling phases (Figure 1(a)). The temperature in SC pile on day 1 achieved thermophilic phase for 8 days, and the SCA and SCAB piles on day 1 especially entered the hyperthermophilic phase, and maintained for 7 and 9 days. Compared to the SC pile, the piles of SCA and SCAB had a better performance in temperature, mainly manifesting in the realization of the hyperthermophilic phase and the extension of thermophilic phase. These results show positive effects on the evaporation of moisture, deactivation of pathogens, and decomposition of OM in SS (Wang et al. 2021a). Therefore, the addition of UT agent might achieve HTC process as well as increase the microbe activity in compost, thus promote the efficiency of composting.

Figure 1. Changes of (a) temperature, (b) moisture level and (c) pH in each pile during the composting process.

The removal of moisture reflects the dewatering performance during composting, and the better the dewatering performance, the more significant the sludge mass reduction (Wang et al. 2021a). The variation of moisture level during composting is shown in Figure 1(b). During the composting processing, the moisture level in all piles indicated a trend of decrease due to the water evaporation in higher temperature environment. The moisture removal is mainly dependent on rising temperature during composting. Hyperthermophilic conditions in SCA and SCAB piles promote the evaporation of more water by destroying the links between extracellular polymeric substances (EPSs) and water to remove the intracellularly bound water between sludge particles for either liquid separation or evaporation (Wang, Liu, and Wang 2015). Xu et al. (2018) reported that the bound water that cannot be effectively removed only by mechanical force, exceeded 30%. After composting for 21d, the moisture level of the SCA and SCAB piles had a more obvious decrease to 34.2–35.8%, which was consistent with the result of the dewatering performance in Yu et al. (2018).

The pH value can affect the mobility of heavy metals and the nitrogen loss in compost, and its variation during composting is shown in Figure 1(c). During the composting, the pH in each pile showed a trend of increase first and then decrease, and fluctuated over an alkaline range, which was consistent with previous results (Chang et al. 2019; Li and Song 2020). An increase in pH might be caused by the production of ammonium by the degradation of protein (Jiang et al. 2015). The rise in pH values in SCA and SCAB piles is more obvious than the SC pile, indicating that the addition of UT agent can sharply induce organic substances metabolism to increase the ammonia oxidation. After composting to 21d, a decrease in pH of each pile was contributed to the enhanced nitrification, and formation of fatty acids and phenolic compounds under the action of microbes (Li et al. 2016).

Analyses of maturity in compost

Seed germination index (GI) is used for an indicator determining the quality, maturity and phytotoxicity of compost (Li and Song 2020; Wang et al. 2020b). From Figure 2(a), the GI value of the SCA and SCAB piles exceeded that of the SC pile during the composting. In the initial stage of composting, the GI indexes in all piles had a decrease to 14.2%, 20.8%, and 20.9%, respectively, for SC, SCA, and SCAB piles, which was in parallel with the results observe d by Li and Song (2020). This result may be attributed to large amounts of ammonia, organic acid and phenol produced during this phase, thus resulted in phytotoxicity to the plants. As those toxic substances gradually decomposed into harmless substances during the composting, the GI value of compost was increasing to 80.6%, 102.5% and 110.2% in SC, SCA, and SCAB piles on day 21. The final GI values in three piles all exceeded 80%, which satisfied the requirements for GI in the maturity assessment system, and the GI of SCA and SCAB was higher than that of the SC pile. The result was explained the fact that higher temperature, and the degradation or adsorption of harmful substances by the addition of UT agent and biochar, could improve the harmlessness of compost, and the synthesis of humus could provide some nutrients for plant growth.

Figure 2. Changes of germination index and C/N ratio in each pile during the composting process.

The C/N ratio also reflects the stability and maturity of compost, its variations in all piles were showed in Figure 2(b). The C/N ratios in each pile exhibited an increasing trend during the early phase of composting because the decomposition of total nitrogen exceeded total carbon. As the composting progressed, lots of easily degradable organic substances in each pile were converted and mineralized by microbe action as the main energy and carbon source while the content of total nitrogen remained in compost owing to the synthesis of the microbial cells (Jain, Paul, and Kalamdhad 2019). Therefore, the C/N ratio gradually decreased after the composting for 21d, and the decreasing order of the C/N ratio was as follows: SCAB>SCA>SC. These results indicated that the appropriate addition of biochar might have a positive effect on composting performance through improving pore structure as well as contributing to microbial load.

Preservation of nitrogen

Nitrogen loss in hyperthermophilic composting mainly was caused by the mineralization of organic nitrogen, the volatilization of ammonia and the denitrification of nitrate nitrogen. Figure 3(a) showed the variation in total nitrogen during the composting. On the composting for 1d, the content of total nitrogen in each pile had a lightly reduction, and the content of total nitrogen gradually increased with the composting progressing. This was attributed to organic nitrogen was decomposed into ammonium nitrogen by the microbe action, then volatilized as a form of ammonia gas. After composting for 21d, the reduction in weight of compost was due to the reduction in the ammonia volatilization, the release of CO₂ and the decline of moisture, thereby induced the concentration effect of the total nitrogen even if the absolute content of total nitrogen decreased. From the composting process, the content of total nitrogen in SCAB pile was higher than the SC and SCA piles, indicating that biochar can adsorb ammonia gas in the composting and has a certain nitrogen-fixing effect.

Figure 3. Changes of TN, NH₄⁺-N, and NO₃^–N in each pile during the composting process.

The difference in effects of increasing the temperature and adding biochar on the ammonium content was extremely significant. Before composting for 6d, the content of ammonium in each pile obviously increased by the decomposition of OM (i.e., protein), and the peak value of ammonium in SC, SCA, and SCAB piles increased respectively by to 58.1%, 45.4% and 34.6% (Figure 3(b)). The results suggested that compared with the SC and SCA piles, the addition of biochar could reduce the ammonium content in compost due to large specific surface area and strong sorption of biochar as carbon-based adsorbent. That may be explained by the fact that acidic functional groups (i.e., carboxyl and phenolic hydroxyl groups) on the biochar surface could bond the ammonium, then promote the transformation of ammonium to other speciation. Therefore, the addition of biochar could enhance the adsorption of ammonium nitrogen in pile and promote the conversion of ammonium into oxidized nitrogen in later phase of composting (Chan, Selvam, and Wong 2016; Li and Song 2020). As the composting processed, the ammonium content in each pile decreased because ammonium was used by the nitrification of microbes and volatilized in the later stage of composting.

It could be seen from Figure 3(c) that the nitrate content of all piles followed a continuously increasing trend during the composting process. Because the activity of nitrifying microbes was inhibited under high temperature conditions in the thermophilic or hyperthermophilic phases, the significant increase in nitrate content occurred in the cooling phase of composting, not the heating phase. The increase of nitrate content in the SCA and SCAB piles exceeded that in the SC pile. The finding suggested that hyperthermophilic conditions and adding the biochar could enhance the nitrification of microbes, and promote conversion to the nitrate nitrogen. On the composting for 21d, the contents of nitrate nitrogen in SC, SCA and SCAB piles increased to 2.69, 3.08, and 3.11 g/kg, respectively. Among these piles, the most increase of nitrate content was the SCAB during the composting, while the increase in SC piles was the least, which suggested that the biochar addition could induce a positive effect on the activity of anammox microbe for the nitrogen removal. Also, the biochar has a high sorption capacity for ammonia gas that could enhance the accumulation of nitrogen, and could provide a better condition for nitrifying microbe to promote conversion to nitrate nitrogen in pile.

Ammonia emission is a primary factor that cause the nitrogen loss during composting (Zhao et al. 2020), which not only reduces the nutritional value of compost, but also induces environmental pollution. The accumulation of ammonia gas during composting in each pile was shown in Figure 4. The accumulation of ammonia gas in piles gradually increased from the degradation of degradable nitrogenous OM, and was highest in SC pile, followed by SCA pile, and SCAB pile. This indicated that an optimal addition of UT agent could induce HTC fermentation and reduce the ammonia emission. However, previous study published an opposite result that is, ammonia gas evolution was enhanced at thermophilic conditions during the composting, which were preferable for enhancing ammonia recovery (Koyama et al. 2020). Further, HTC process can reduce the emission of ammonia by deactivating urease and protease, and of NOx by affecting the expression of NOx-related genes during higher temperature (Cui et al. 2019b; Liu et al. 2020). And, the activity of fungi related to the nitrogen conversion is not affected by hyperthermophilic condition (Cui et al. 2019b). The addition of biochar also decreased the ammonia emission by 20.6% in the SCAB pile than that of the SC pile after the composting for 21d. A reduction in ammonia was due to the higher adsorption capability of biochar on urea, uric acid, and ammonia gas (Wang et al. 2021b). Alkaline biochar was used into composting to cause an increase in the pH value of compost, thus promoted the transformation of NH₄⁺-N to NH₃, preserved more nitrogen during the composting. However, an obvious reduction of ammonia emission in composting by biochar suggests that the adsorption on biochar had a significantly higher impact on ammonia emission than its alkalinity.

Figure 4. Ammonia emission in each pile during the composting process.

Passivation of heavy metal

The major heavy metals in sewage sludge mainly include highly toxic Cu, Zn and Pb, and causes pollution for the soil. The concentration and different speciation of Cu, Zn, and Pb in compost are shown in Figure 5. The concentration of Zn, Cu and Pb in each pile had a trend of increase during the composting (Figure 4(a–c)), which was closely related to the degradation of organic matter in large quantities, which can produce a relative enrichment of heavy metal. The increase of Zn, Cu and Pb content was obvious in SCA and SCAB piles compared to that of the SC pile, which suggested that the OM degradation was more sufficient to cause an obvious enrichment. The mobile heavy metal includes exchangeable, reducible and oxidizable speciation, which is used for evaluating the mobility of heavy metals in compost. Figure 5(a)’ showed that there was lower residual Zn in the SC pile compared with that the SCA and SCAB piles as well as an increase in these coefficients of mobile speciation of Zn during the composting. However, the residual Zn of the SCA and SCAB piles increased to 44.6–45.5 mg/kg, and the coefficients of mobile speciation reduced in composting. These results showed that HTC process with the addition of biochar had an obvious passivation effect on Zn in compost due to the electrostatic interactions, replacement of exchangeable cations, and formation of oxygen-containing functional groups (i.e., – OH, – COOH) or delocalized π electron from biochar (Liu et al. 2017; Yang et al. 2019). Singh et al. (2018) also report that high surface area and pore space revealed it utilization potential as adsorbent.

Figure 5. Changes in the (a) Zn concentration, (a’) Zn fraction, (b) Cu concentration, (b’) Cu fraction, (c) Pb concentration, and (c’) Pb fraction during the composting process.

The reducible fraction of Cu in all piles decreased during the composting, and the coefficient of exchangeable and oxidizable speciation of Cu increased (Figure 5(b)’). This indicates that exchangeable and oxidizable Cu were generated from the transformation of reducible Cu in composting. The coefficient of residual Cu in SC, SCA and SCAB piles respectively improved to 31.8, 45.5 and 47.4 mg/kg. The proportion of mobile Cu decreased by 4.1% and 6.5% in SCA and SCAB piles, respectively while it increased by 2.2% in SC pile. These results showed that compared with traditional TC process, HTC process could promote the Cu to convert into higher stable speciation, thus to reduce the bioavailability of Cu in compost as well as with the addition of biochar, which was consistent with previous results of Zn. These results are consistent with the passivation results in another study that added wheat stalk biochar and rice husk biochar for poultry manure composting (Zhang, Wei, and Wang 2021). The exchangeable Pb was not detected in compost in the work. The relative content of residual Pb decreased by 8.9% for SC pile, but it increased 6.4% and 10.1% for SCA and SCAB piles, respectively. In addition, the residual Pb in SCAB pile increased at a larger rate than that in SCA pile during composting, which indicated that biochar could strengthen the passivation of Pb during composting. Also, biochar is mostly alkaline due to rich in extractable inorganic nutrients (i.e., phosphate, calcium and magnesium), which can inhibit the activation of heavy metal (Liu et al. 2017). Therefore, one reason for the Pb passivation was provided by phosphate to form insoluble precipitates during composting.

Conclusion

The work verified the positive effects of biochar and hyperthermophiles agent on the nitrogen preservation and heavy metal passivation in pile during composting of sewage sludge, thereby improving the maturity and quality of the compost. Hyperthermophilic composting (HTC) improved the fermentation efficiency and the maturity of compost by increases in the temperature and GI value, and decreases in the moisture and C/N ratio compared to conventional thermophilic composting. HTC process as well as the biochar addition resulted in a reduction of the nitrogen loss compared with the control (CK) pile during composting by promoting transforming ammonium into nitrite nitrogen. Adding biochar to composting inhibited the transformation of Cu, Zn and Pb into more mobile speciation compared to the CK pile although these contents increased during composting, which lead to reduction in availability of heavy metals. Thus, HTC process with the addition of biochar is viable for the reduction of the nitrogen losses and mobility of heavy metal in compost.

Abbreviations

Table

WWTPs	Wastewater Treatment Plants
SS	Sewage Sludge
OM	Organic Matter
TC	Thermophilic Composting
HTC	Hyperthermophilic Composting
HSs	Humic Substances
CS	Corn Straw
UT	Ureibacillus Terrenus
SC pile	Sewage sludge + Corn straw
SCA pile	Sewage sludge + Corn straw + 5‰ UT Agent
SCAB pile	Sewage sludge + Corn straw + 5‰ UT Agent +5% Biochar; GI: germination index
ICP-MS	Inductively Coupled Plasma Mass Spectrometry
Bcr	Community Bureau Of Reference
EPSs	Extracellular Polymeric Substances

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data availability statement

Due to the nature of this research, participants of this study did not agree for their data to be shared publicly, so supporting data is not available.

Additional information

Funding

This work was supported by the grants from the Science and Technology Plan Project of Tianjin, China [Grant Number 18ZXSZSF00170] and the Science and Technology Research and Development Plan Project of Shijiazhuang, China [Grant Number 201240343A].

Notes on contributors

Xue Qin

Xue Qin is the technician at School of Environmental Science and Engineering, Hebei University of Science and Technology.

Xiaosha Wu

Xiaosha Wu is the assistant engineer at Hebei Haoyuan Environmental Engineering Co., Ltd.

Zhinan Teng

Zhinan Teng is the master postgraduate at School of Environmental Science and Engineering, Hebei University of Science and Technology.

Xiaoyue Lou

Xiaoyue Lou is the senior engineer at Tianjin Redsun Water Industry Co., Ltd.

Xuebin Han

Xuebin Han is the senior engineer at Hebei Haoyuan Environmental Engineering Co., Ltd.

Zaixing Li

Zaixing Li is the professor at School of Environmental Science and Engineering, Hebei University of Science and Technology.

Yonghui Han

Yonghui Han is the senior engineer at School of Environmental Science and Engineering, Hebei University of Science and Technology.

Fan Zhang

Fan Zhang is the senior engineer at Hebei Haoyuan Environmental Engineering Co., Ltd.

Gong Li

Gong Li is the senior engineer at Tianjin Redsun Water Industry Co., Ltd.