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/lp/springer-journals/effects-of-biochar-carried-microbial-agent-on-compost-quality-m9SqWkoFVq
- Publisher
- Springer Journals
- Copyright
- Copyright © The Author(s) 2023
- ISSN
- 2524-7972
- eISSN
- 2524-7867
- DOI
- 10.1007/s42773-022-00202-w
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- See Article on Publisher Site
Abstract
1 Introduction the total nitrogen loss, respectively (Yuan et al. 2019). The development of specialization, large-scale and During composting, 14–51% of the organic carbon in intensification of livestock industry has generated the compost material can be released into the atmos- a large volume of animal manure. Currently, the phere as C H and CO (Barrington et al. 2002). Gener- 4 2 amount of livestock manure produced is approximately ally, the emission of gases will lead to the reduction of 3.8 × 10 t every year, but the comprehensive utilization compost quality (Wang et al. 2022). Therefore, it is cru - rate is less than 60% in China (Yao et al. 2021). A large cial to develop a method to reduce gas emissions and number of livestock manure is stacked, which causes improve the quality of compost at the same time. a series of harms to the soil, water and atmospheric A number of studies have indicated that the addition environment, and constantly threatens the sustain- of additives is a very available way for reducing car- able development of the ecological environment (Wang bon and nitrogen losses and gas emissions during the et al. 2018). So, we must find a feasible method to solve composting process (Ren et al. 2020; Pan et al. 2019; the problem of livestock manure. Aerobic composting Soudejani et al. 2019). Because of its particular porous can convert livestock manure into a safe and mature structure and abundant surface functional groups, fertilizer due to its high content of organic matter, biochar can reduce gas emissions (Yin et al. 2021a). nitrogen, phosphorus, potassium and trace elements, Besides, biochar can also improve the environmental achieving the reduction, detoxification and recycling of conditions of the heap, which is beneficial to the com - livestock and poultry manure (Ravindran et al. 2018). posting quality improvement (Zainudin et al. 2020). However, aerobic composting of livestock manure is Awasthi et al. (2017) found that biochar significantly usually accompanied by the production of greenhouse reduced CH, N O and NH emissions by 92.85– 4 2 3 gases and other gases, including methane (CH ), carbon 95.34%, 95.14–97.30% and 58.03–65.17%. Hagemann dioxide (CO ), nitrous oxide (N O), ammonia (N H ), et al. (2018) reported that addition of three different 2 2 3 etc. (Chan et al. 2016). A large amount of gas emissions biochars increased nutrient retention, moisture content can lead to the loss of carbon and nitrogen during com- and total organic carbon content in the mature com- post (Tong et al. 2019). Among them, NH and N O post. Wang et al. (2021) showed that 10% biochar addi- 3 2 emissions account for 73.68–92.91% and 1.23–4.16% of tion reduced nitrogen losses to 25.69% and increased W ang et al. Biochar (2023) 5:3 Page 3 of 17 organic matter degradation, thereby shortening com- 2 Materials and methods posting period and promoting microbial succession in 2.1 Collection and preparation of raw materials the composting process. Fresh sheep manure and corn straw came from Guanji- As we know, composting is a series of complex bio- ang village (Baotou, Inner Mongolia, China). Corn straw logical, physical and chemical processes (Guo et al. was cut into 2 cm lengths as a conditioning agent, which 2020), and microorganisms play a crucial role in com- can regulate the C/N ratio and moisture content of com- posting systems. Many researchers have pointed out post. The biochar was prepared from corn straw by slow that the inoculation of native or exogenous microor- pyrolysis at 550 ℃ in a muffle furnace (SK16BYL, Nanjing ganisms improves the composting process, especially Boyun Tong Instrument Technology Company, Nanjing, the introduction of exogenous compound microbial China). The basic physical and chemical properties of agents (Wang et al. 2022; Xu et al. 2022a, 2022b; Zhao composting materials are shown in Table 1. et al. 2022). In addition, biochar is a biocompatible The sheep manure extract medium and correspond - material, which is conducive to the reproduction and ing selective solid medium for inorganic phosphorus habitat of microorganisms, and can increase the num- dissolving bacteria, organic phosphorus dissolving bac- ber and activity of microorganisms (Wang et al. 2022). teria, potassium dissolving bacteria and nitrogen fixing Therefore, it is supposed that in the perspective of bacteria were prepared. The single bacteria isolation and engineering practice and microbial inoculation stor- purification experiments were carried out. Six strains of age, biochar carried microbial agent (microbial agent bacteria were obtained by dilution and culture of solid was sprayed on the biochar) is beneficial for the stor- separation medium. Then, the six strains were crossed in age, transportation and utilization of microbial inocu- pairs for antagonistic experiment. The strains could grow lation in practice, and thus benefits its utilization in well, and there was no antagonistic reaction between high value compost production (Tu et al. 2019). Tu them. They could coexist for mixed culture so as to pre - et al. (2019) used the bamboo biochar loaded com- pare compound microbial agents. The detailed prepara - mercial bacteria agent for enhancing the pig manure tion methods are provided in the Additional file 1. After composting. However, the composing process was mixed fermentation, the numbers of nitrogen-fixing, strongly related to the feedstock, composing system inorganic phosphorus dissolving, organic phosphorus and amendment (including biochar) types (Wang et al. dissolving and potassium dissolving bacteria were 10 , 5 8 7 −1 2022). So far, the application of corn straw biochar car- 10, 10 and 10 mL , respectively. ried compound microbial agent in sheep manure com- The biochar carried microbial agent was prepared by posting is still limited, and its effects on composting spraying and mixing the compound microbial agents quality, greenhouse gas emissions and bacterial com- and biochar according to the mass ratio of 1:10, inoculat- munity changes are not clear. ing and multiplying for 2 weeks. The scanning electron Therefore, the regulatory effect of biochar carried microscope images of biochar and biochar carried micro- microbial agent on the biological stabilization process bial agent are shown in Fig. 1. The pore structure of corn of sheep manure compost was investigated. The aims straw biochar was clear and rich because it contained of this study were (1) to evaluate the effect of biochar cellulose and hemicellulose (Fig. 1a). It can be obviously carried microbial agent on physicochemical param- observed that microorganisms were well loaded on the eters, nitrogen transformation, gas emissions and bac- surface of biochar (Fig. 1b). terial community succession during composting; (2) to reveal the relationship between bacterial community, environmental factors and gas emission. The results of 2.2 Composting experiment this study are expected to provide valuable informa-2.2.1 Composting device tion for the promotion of livestock manure composting The aerobic composting was conducted in 25 L self- technology. designed cylindrical devices made of stainless steel (with Table 1 The physico-chemical properties of the raw materials −1 −1 −1 TN (g kg ) TC (g kg ) pH EC (mS cm ) OM (%) Moisture (%) C/N Sheep manure 18.01 ± 0.55 392.82 ± 4.12 8.52 ± 0.03 3.23 ± 0.03 69.84 ± 0.11 71.69 ± 0.55 21.82 ± 0.12 Corn straw 7.61 ± 0.05 508.03 ± 5.34 6.41 ± 0.02 0.28 ± 0.01 68.52 ± 0.25 6.21 ± 0.02 66.84 ± 1.06 Biochar 5.27 ± 0.02 693.22 ± 5.56 7.62 ± 0.03 0.21 ± 0.01 90.62 ± 1.15 3.52 ± 0.01 131.54 ± 2.13 Values indicate mean ± standard deviation based on determination with three replications. TN (total nitrogen), TC (total carbon), EC (electricity conductivity), OM (organic matter) Wang et al. Biochar (2023) 5:3 Page 4 of 17 2.2.2 Experimental design The sheep manure and corn straw were mixed evenly in a ratio of 8:1 (w/w, dry weight basis). The mixture was further adjusted to a moisture content of 60% and a C/N ratio of 25 prior to the addition of biochar, com- pound microbial agent and biochar carried microbial agent. Four aerobic composting treatments were (i) sheep manure + corn straw (CK), (ii) CK + 0.1% biochar (B), (iii) CK + 0.01% compound microbial agent (M), and (iv) CK + biochar carried microbial agent (BM, adding 0.01% compound microbial agent to 0.1% biochar before natural air drying). All of the treatments were replicated three times. About 4.5 kg of compost material for each treatment was loaded into reactor and composted for 28 days. Temperature was monitored every day between 14:00 and 15:00. Samples weighing about 200 g were col- lected from each treatment on 0, 4, 8, 12, 16, 20, 24 and 28 days after mixing them well, and then homogenized to obtain a representative sample. The samples were stored in a refrigerator at 4 ℃ for the determination of phys- icochemical and maturity indexes. 0.5 g of sample from each treatment group on 6, 14, and 28 days was frozen at − 20 ℃ for microbial analyses. Gas samples were col- lected every 5 days using a 1 L gas sampling bag. 2.2.3 Samples analysis Fresh compost samples and deionized water were mixed Fig. 1 SEM images of biochar (a) and biochar carried microbial agent (b) at a ratio of 1:10 (w/v), and the mixture was shaken for 30 min to analyze pH, electric conductivity (EC), E /E , 4 6 and seed germination (GI). The pH and EC were meas - ured using a pH meter (pHS-3C, China) and conduc- tivity meter (DDS-307A, China). The absorbance of E / E was determined at 465 and 665 nm using an ultravio- let–visible spectrophotometer (UH4150, Japan). GI test was performed with Glycine max (Linn.) Merr. seeds as described by Li et al. (2020). The GI was calculated according to Eq. (1). Organic matter (OM), moisture content, total Kjeldahl nitrogen (TKN), NH -N, and NO -N were determined according to a standard test, the Test Method for the Examination of Composting and Compost (TMECC 2002). The contents of total carbon (TC) and total nitrogen (TN) were determined using a Vario MACRO elemental analyzer (Elementar Analysen- Fig. 2 The diagram of the composting reactor systeme GmbH, Hanau, Germany). To assess the forma- tion of clumps within the pile, composts smaller than 70 mm were screened and weighed to quantify the dif- the height of 46 cm and the inner diameter of 30 cm). ferent compositions (70–25, 25–4 and < 4 mm). The gas There were 4 cm thick insulation layers on the outer wall produced in the composting process was collected by the of the reactors. The devices had sealing covers at the top. gas bag. The concentrations of CH, CO and N O were 4 2 2 −1 −1 Fresh air was supplied at a gas flow rate of 0.5 L h kg measured by gas chromatography (Agilent 6890N, USA). (dry weight basis) at the bottom of the composting reac- The NH in compost was adsorbed in boric acid solution −1 tors (Fig. 2). and detected by titration with 1 mol L HCl according W ang et al. Biochar (2023) 5:3 Page 5 of 17 to Mao et al. (2019). The compositions and succession was reached on day 6, 5, 4 and 2, which lasted 5, 8, 6 and of the bacterial communities were assessed on samples 9 days, and the peak temperatures were 60.1, 60.3, 60.9 taken at three major stages, including thermophilic (day and 63.9 ℃, respectively. All four treatments met the 6), cooling (day 14) and mature composts (day 28) by criteria for harmless composting (Jain et al. 2018). After 16S rRNA gene high-throughput sequencing using the that, the temperature decreased gradually and finally Illumina MiSeq platform at Majorbio (Shanghai, China). reached ambient temperature. It was discovered that the According to the manufacturer’s instructions, DNA of BM treatments reached faster peak temperature, higher compost samples was extracted using the E.Z.N.A. Soil peak temperature and longer thermophilic period. Add- DNA Kit (Omega Bio-tek, Norcross, GA, USA). The ing biochar carried microbial agent to the compost could hypervariable regions V3-V4 of the bacterial 16S rDNA rapidly heat up and prolong the duration of high tem- gene were amplified with primer pairs 338F (5′-ACT perature, indicating that it was beneficial to composting. CCT ACG GGA GGC AGC AG-3′) and 806R (5′-GGA CTA This was probably because the biochar carried micro - CHVGGG TWT CTAAT-3′) by an ABI GeneAmp 9700 bial agent promoted the decomposition of organic mat- PCR thermocycler (ABI, CA, USA). ter, thus generating more heat (Zhao et al. 2020). Also, Seed germination rate of treatment (%) × Root length of treatment (mm) (1) GI = ×100% Seed germination rate of control (%) × Root length of control (mm) 2.3 Statistical analysis biochar carried microbial agent filled the pores between All analyses were conducted in triplicate to obtain the composting materials and reduced heat loss (Awasthi average value. Figures were drawn by Origin 2022. All et al. 2017). statistical data were tested for normality and homogene- ity of variance. Significant differences between the treat -3.1.2 Changes in pH ments were determined by a one-way analysis of variance Figure 3b shows the change trend of pH value during (ANOVA) using the SPSS 26.0 software package (SPSS the composting. The initial pH values of B, M, BM and for Windows, Version 26.0, USA), and multiple compari- CK were 8.67, 6.88, 8.61 and 8.48, respectively. The pH sons using the least significance difference (LSD) post increased slightly, reaching a maximum value for all hoc test were done whenever the ANOVA indicated sig- treatments on day 4. This might be related to the rapid nificant differences (p ≤ 0.05). The relationships between decomposition of organic matter during this period, with gaseous emissions and microbial community were ana- organic nitrogen being ammoniated and mineralized lyzed by Pearson’s correlation analysis. Redundancy (Gao et al. 2010). The maximum pH values of the four analyses (RDA) were performed by the CANOCO 5.0 to treatment groups were B > BM > CK > M. The pH value of recognize environmental factors and microbial commu- M was significantly lower than that of B and BM treat - nities during thermophilic stage, cooling stage and matu- ments (p < 0.05). Adding biochar increased the pH in the rity stage. composting while adding microbial agents showed the opposite trend, which was closely related to the pH of raw 3 Results and discussions materials. The pH values of microbial agent, biochar and 3.1 E ec ff t of additive on the basic parameters biochar carried microbial agent were 6.89, 10.01 and 8.16, during composting respectively. The pH values of treatment groups were 3.1.1 Changes in temperature affected by alkaline biochar and acidic microbial agents. Temperature is an important index reflecting the matu - From day 4 to day 12, the ammoniation was weakened, rity of composting process, as it may affect microbial the nitrification was gradually enhanced, and the pH of metabolism and activity (Yang et al. 2020). The ambient compost gradually decreased with low-molecular-weight temperature was maintained between 26.8 ℃ and 38.5 ℃. organic acids and C O accumulation (Chen et al. 2019). Figure 3a shows the changes of temperature during the On days 12–24, the continuous degradation of organic composting process. All treatment groups showed the acids further increased pH values (Wang et al. 2022; Xue same trends of change, which were heating, thermo- et al. 2021). As the compost slowly reached maturity, the philia, cooling and maturity stages. The temperature of pH decreased in 24–28 days. The final pH values of BM, all treatments rose sharply within the first 5 days. It could B, M and CK treatment groups were 7.58, 7.8, 7.38 and be because of the rapid degradation of available organic 7.58, respectively, which satisfied the pH value range of matter in sheep manure (Awasthi et al. 2016). The ther - the Chinese industry standard (5.5–8.5). mophilic stage (> 50 ℃) of CK, M, B and BM treatments Wang et al. Biochar (2023) 5:3 Page 6 of 17 (b) (a) 9.0 65 BM Ambient BM 8.5 CK CK 8.0 7.5 7.0 05 10 15 20 25 30 05 10 15 20 25 30 Time (days) Time (days) (c) (d) 6 40 BM BM 35 M CK CK 05 10 15 20 25 30 05 10 15 20 25 30 Time (days) Time (days) (e) (f) BM BM B M CK CK 20 2 05 10 15 20 25 30 05 10 15 20 25 30 Time (days) Time (days) (g) (h) 1.4 BM B M CK 3.5 BM B M CK 1.2 3.0 1.0 2.5 2.0 0.8 1.5 0.6 1.0 0.4 0.5 0.2 0.0 0.0 05 10 15 20 25 30 05 10 15 20 25 30 Time (days) Time (days) + − Fig. 3 Changes in temperature (a), pH (b), EC (c), C/N (d), OM (e), TKN (f), NH -N (g) and NO -N (h) in different treatments during composting. CK: 4 3 sheep manure + corn straw; M: CK + 0.01% compound microbial agents; B: CK + 0.1% biochar; and BM: CK + biochar carried microbial agent (0.01% compound microbial agent to 0.1% biochar before being naturally dried). Results are the mean of three replicates and error bars indicate standard deviation + -1 NH -N (g kg ) OM (%) Temperature ( ) 4 -1 EC (mScm ) - -1 -1 pH NO -N (g kg ) C/N 3 TKN (g kg ) W ang et al. Biochar (2023) 5:3 Page 7 of 17 3.1.3 Changes in EC of OM into small molecules such as CO and water, The EC value represents the soluble salt content in com - increasing the reactor temperature and the synthesis of post, which is one of the criteria for whether the compost humic acid through microbial action (Ren et al. 2019). would cause phytotoxicity on plant growth (Gao et al. Therefore, the OM content of each treatment decreased 2010). Figure 3c shows the water-soluble products in gradually in the composting process. The final OM values the piles mostly came from free water in the early stage for the BM, B, M and CK groups were 46.23%, 47.01%, of composting, and the EC contents remained at a low 47.99% and 46.47%, respectively. Moreover, the OM level. Owing to the fast decomposition of organic matter values for the BM, B, M and CK groups decreased by and the loss of water, the EC values began to rise (Singh 33.83%, 26.63%, 30.24% and 27.56%, respectively. OM and Kalamdhad 2013). Then, the four composting groups degradation rate was faster in the BM group than in the displayed a downward trend owing to the precipitation CK group, which may be due to the promotion of micro- of mineral salts and the volatilization of large amounts bial activity by biochar carried microbial agent addition of NH (Waqas et al. 2017). Although there were mod- (Yin et al. 2021b). In addition, materials with a high ini- erate fluctuations, the final EC values of BM, B, M and tial C/N ratio have been reported to result in higher OM −1 CK groups reached 3.09, 3.98, 2.49 and 1.07 mS·cm , degradation rates (Zhang et al. 2020). −1 respectively, which were under 4 mS c m , indicating that the compost could be applied to the soil safely (Wang 3.1.6 Cha nges in the formation of clumps et al. 2020). It is obvious that compared with the CK In this study, it was observed that the four treatments treatments, addition of biochar carried microbial agent formed clumps of variable sizes from the initial stage. In significantly increased the EC values (p < 0.05). Qu et al. order to evaluate the formation of clumps in the piles, (2020) found that the dilution effects and/or salt adsorp - particle size distributions of the four treatments were tion potential of biochar could reduce EC values. How- measured after composting and the results are shown in ever, the addition of the biochar carried microbial agent Additional file 1: Table S1. Most of the particle size distri- might be conducive to microbial reproduction, accelerate bution was less than 4 mm. In the BM treatment group, the degradation rate of organic matter, and accumulate a the proportion of particles smaller than 4 mm in size was large amount of inorganic substances, thus resulting in a 81.93%. was 81.93%, which was much larger than in the higher EC values in this study. other groups. This showed that the addition of biochar carried microbial agent increased the proportion of small 3.1.4 Changes in C/N clump fraction, avoided the generation of anaerobic envi- The variation of C/N ratio in the four composting treat - ronment, and promoted the diffusion of O (Sánchez- ment groups is shown in Fig. 3d. In the early stage, C/N García et al. 2015). values increased slightly due to nitrogen losses from NH emissions (Qiu et al. 2020). After that, the C/N ratios of 3.2 Eec ff t of additives on nitrogen transformation BM, B and M treatment groups decreased until the end during composting of composting with the degradation of carbon-containing TKN content is a significant parameter in assessing materials and accumulation of organic nitrogen (Chang the quality of compost products. The change of TKN et al. 2019). The C/N ratios in the CK treatment group of compost in each treatment is shown in Fig. 3f. In all increased within 10 to 16 days. The final C/N values four treatments, TKN values decreased initially and then for the BM, B, M and CK treatment groups were 15.13, increased gradually. During the thermophilic phase, 19.98, 19.78, and 18.56, respectively. The C/N values in all TKN levels were reduced due to the decomposition of four treatments were less than 20, indicating the compost organic nitrogen and the release of N H (Santos et al. reached maturity (Chung et al. 2021). Generally, the BM 2018). In the later stages of composting, the increase of treatment group was the most effective, probably because TKN content was related to the enrichment of nitrogen- of the higher nitrogen conservation and OM degrada- containing organic substances and rapid decomposition tion in the pile, resulting in lower C/N values (Jiang et al. of OM (Tong et al. 2019). The final TKN contents of the 2015). BM, B, M and CK treatment groups were 17.2, 12.3, 4.7 −1 and 3.2 g kg , respectively. Compared with the initial 3.1.5 Changes in OM stage of composting, the the content of TKN in BM, B As shown in Fig. 3e, the initial OM contents of the BM, and M groups increased by 109.76%, 19.77% and 20.51%, B, M and CK were 69.87%, 64.08%, 68.79% and 64.15%, while that in CK group decreased by 21.95%. Compared respectively. The OM contents showed a downward with the CK group, the addition of biochar carried trend, although there were fluctuations during the com - microbial agent significantly increased the TKN content posting process. This might be due to the decomposition (p < 0.05). Wang et al. Biochar (2023) 5:3 Page 8 of 17 Nitrogen transformation in compost mainly includes obtain stable humus (Cáceres et al. 2018). However, the ammonification, nitrification and denitrification reac - composting process produces many adverse by-products, tion (Liu et al. 2020). The NH -N content showed an including greenhouse gases from microbial metabolic increase trend during the first five days in all treatments activities (Fig. 4), which have received much attention in and then decreased until composting was completed recent years (Yin et al. 2021a). (Fig. 3g). In the initial stage, the increase of N H -N con- tent was mainly owing to the change of organic nitrogen to NH -N by ammonification reactions at higher tem -3.3.1 CH emission 4 4 peratures and pH (Guo et al. 2012). The highest values CH is an important greenhouse gas and produced by + −1 of NH -N were 2.34, 1.84, 3.18 and 2.83 g kg for the deoxidizing CO /H or acetic acid of methanogenic bac- 2 2 BM, B, M and CK groups, respectively. The M treatment teria under hypoxic/anaerobic conditions (Yang et al. group had the highest N H -N content compared to CK. 2013). As can be seen in Fig. 5a, CH emissions rapidly This suggested that compound microbial agent promoted increased during the first five days and then gradually rapid degradation of organic nitrogen (Li et al. 2019a). decreased until the end of composting. At the initial stage After that, with the volatilization of ammonia and the of composting, the degradation of OM consumed a lot of nitrification and denitrification of bacteria in the com - oxygen and formed a certain anaerobic area, increasing posting process, the NH -N contents began to decrease the activity of methanogenic bacteria (Yun et al. 2018). until the end (Wang et al. 2016a). Finally, the NH -N The peak values of CH emission on day 5 were 0.46, −1 contents in BM, B, M and CK groups were 0.38, 0.24, 0.18 4.02, 1.56 and 2.11 g day for BM, B, M and CK groups, −1 and 0.36 g kg , respectively, and the final compost prod - respectively. As composting proceeded, CH emissions ucts of each treatment satisfied the maturity standard of decreased gradually until the end of composting because −1 organic fertilizer (less than 0.4 g kg ). of the decrease of temperature and degradable carbon The NO -N content of all treatments showed an substances. increase trend from day 0 to the end of composting Cumulative CH emissions in BM, B, M and CK groups (Fig. 3h), which was consistent with the results of Jiang were 1.08, 6.68, 2.80 and 3.16 g, respectively. The findings et al. (2015). In the beginning of composting, the val- showed that the addition of biochar increased CH emis- ues of temperature, pH and NH -N were higher, which sions which was inconsistent with most research conclu- inhibited the activity and growth of nitrifying bacteria, sions. In general, the addition of biochar might suppress and NO -N content was lower (Ren et al. 2019). As methanogenic activity and C H emissions by improving composting temperature and pH decreased, NH -N was compost structure and changing the redox potential (Liu − + gradually transformed into N O -N, and the content et al. 2017). Besides, the adsorption of N H by biochar of NO -N increased (Chung et al. 2021; Wang et al. can also reduce the availability of methanogenic bacteria 2017a). After composting, the N O -N contents in the and reduce CH emissions (Karhu et al. 2011). However, BM, B, M and CK treatment groups were 1.22, 1.08, 1.19 in previous studies, the biochar addition was relatively −1 − and 0.73 g kg , respectively. The NO -N content in high, and in this study, the biochar addition was only BM group was significantly higher than that in CK group 0.1%, which may not be sufficient to improve the venti - (p < 0.05). lation conditions of the piles. This was consistent with After composting, the difference in NH -N and the distributions of compost particle size. The propor - NO -N content was little, while TKN showed great dif- tion of particles less than 4 mm in size in BM treatment ference among treatments, indicating that the difference group was the largest, while the proportion of B group came from organic nitrogen. The TKN in the BM treat - was close to that of the CK group. This showed that BM ment was higher, which meant that the organic nitrogen group could better promote the diffusion of O , avoid of this treatment was higher than that of other treatments. anaerobic environment and reduce the release of CH . The reason for the decrease of nitrogen loss may be related to the decrease of organic nitrogen loss in BM group. In 3.3.2 CO emission short, biochar carried microbial agent had the synergistic CO emissions reflect the activity of microbial and the effect of biochar and microbial agent in nitrogen retention efficiency of the composting process (Wang et al. 2017b; and quality enhancement of compost (Kolton et al. 2016). Li et al. 2020). Figure 5b shows the changes in C O emis- sion rates. The CO emissions of all four treatments sharply increased in the first 10 days, which was same 3.3 E ec ff t of additives on greenhouse gas emissions with the change trend of composting temperature. At Composting is a complex biochemical process in which the beginning of composting, an increase in tempera- microorganisms degrade organic matter and eventually ture promoted microbial activity, and then metabolically W ang et al. Biochar (2023) 5:3 Page 9 of 17 Fig. 4 Flow chart of greenhouse gas emissions during composting (a) (b) 8 500 BM B BM B BM B BM B M CK M CK M CK 4 M CK 200 3 150 2 100 1 50 0 0 0 0 05 10 15 20 25 05 10 15 20 25 Time (days) Time (days) (c) (d) 50 1.5 3 120 BM BM BM BM B B B B M M 40 100 CK CK CK CK 1.0 2 0.5 1 0 0 0.0 0 05 10 15 20 25 05 10 15 20 25 30 Time (days) Time (days) Fig. 5 Emissions of CH (a), CO (b), N O (c), and NH (d) in different treatments during composting. CK: sheep manure + corn straw; M: CK + 0.01% 4 2 2 3 compound microbial agents; B: CK + 0.1% biochar; and BM: CK + biochar carried microbial agent (0.01% compound microbial agent to 0.1% biochar before being naturally dried) active microorganisms converted OM to CO (Ren et al. of the composting process. This was attributed to the 2019). Thereafter, the CO emissions of the BM, M and rapid consumption of soluble organic matter, leading to CK treatment groups gradually decreased until the end a reduction in carbon sources (Ma et al. 2020). However, -1 N O emission (mg day ) -1 CH emission (g day ) N O cumulative emission (mg) CH cumulative emission (g) 2 4 -1 -1 CO emission (g day ) NH emission (g day ) NH cumulative emission (g) CO cumulative emission (g) 2 Wang et al. Biochar (2023) 5:3 Page 10 of 17 3.3.4 NH emission a smaller emission peak occurred on day 20 in the B and NH is an indirect greenhouse gas that can cause nitro- BM groups. This might be due to the fact that OM was gen loss (Chen et al. 2019). The trends of NH emis- not fully degraded at an early stage. As OM continued to sions in the four treatment groups are shown in Fig. 5d. degrade, CO emissions increased again. In the first 5 days, NH emissions increased sharply with The final cumulative emissions from the BM, B, M the rapid increase of temperature and pH, which can be and CK treatment groups were 151.32, 333.21, 436.73 explained by the conversion of large amounts of NH -N and 148.91 g, respectively. The CO emissions of the 2 4 to NH (Yang et al. 2015). On the fifth day, NH emission other three treatment groups increased compared with 3 3 rates reached peak, attaining maximum values of 0.75, CK treatment group, and the emission of BM treat- −1 1.03, 1.04 and 1.18 g day for BM, B, M and CK, respec- ment group increased the least, indicating the syner- tively. After five days, the NH release rates from the four gistic effect of biochar and compound microbial agent treatments gradually slowed down with the OM stabi- on CO emissions. On the hand, the combination of lized. NH release pattern was similar with the results of biochar and compound bacterial agent can improve the Maulini-Duran et al. (2014). adsorption capacity, resulting in limited C O emissions. The final cumulative emissions for the BM, B, M and On the other hand, the compound microbial inoculum CK treatment groups were 1.49, 2.06, 2.04 and 2.57 g, could adjust pH and water content around the biochar respectively. Compared with CK, the cumulative N H (Mishra et al. 2013), and accelerate the release of unsta- emissions of BM, B and M groups decreased by 42.05%, ble aliphatic compounds (which can be used as carbon 20.09%, and 20.59%, respectively. BM treatment group source of microorganisms) in the biochar (Steiner et al had the greatest inhibition effect on NH emission. Add- 2016), thus improving the effectiveness of biochar carried ing biochar carried microbial agent can effectively reduce microbial agent in the loss of CO . NH volatilization of compost. First, the porous struc- ture and large specific surface area of biochar were highly 3.3.3 N O emission favorable for N H adsorption (Yin et al. 2021b). Secondly, N O is an important greenhouse gas in composting and 2 3 the abundant reactive functional groups on the surface can be produced during incomplete nitrification and den - of biochar could availably adsorb N H and reduce the itrification under aerobic and anaerobic conditions (Yang emission of NH (He et al. 2019). In addition, adding et al. 2019). Figure 5c shows the peak of N O emission 2 3 exogenous compound microbial agent could inhibit the in the CK group occurred in the early composting stage, release of NH by altering the metabolism of carbon and while the peaks in the other treatment groups occurred nitrogen (Chen et al. 2019). during the cooling stage. This was different from the It is estimated that the loss of nitrogen during com- results of Xue et al. (2021), who found that the peak of posting accounts for 21–77% of the initial total nitrogen N O emission occurred at the early stage of composting (Chan et al. 2016). The loss of nitrogen is mainly medi - in all treatment groups. In this study, it might be because ated by microorganisms, so it is inevitably accompanied the CK group was more likely to form local anaero- by the loss of carbon due to microbial growth and main- bic environment at the beginning, resulting in a large tenance respiration (Tong et al. 2019). The carbon loss amount of N O emissions through denitrification (Yang during composting is 34–77% of the initial total carbon et al. 2015). There was a large release of N O from day 15 (Guo et al. 2012). In this composting process, the cumula- to day 20 in the BM, B and M treatment groups, which tive emissions of gases were CO > CH > NH > NO. CO may be related to nitrification of nitrogenous compounds 2 4 3 2 2 and NH emissions were the main causes of total car- with the increase of N O -N concentration (Wang et al. 3 3 bon and nitrogen losses, which was consistent with most 2016b). research conclusions (Li et al. 2018; Yuan et al. 2019; Ba The cumulative emissions of N O in the BM, B, M et al. 2020; Sun et al. 2020). The cumulative emissions of and CK treatment groups were 35.85, 94.86, 11.09 and gases compared with the CK group are listed in Table 2. 114.30 mg, respectively. Compared with CK, the cumu- The three treatment groups had different emission reduc - lative N O emissions of BM, B and M were reduced by tion effects on different gases. Compared with CK group, 68.64%, 17.01% and 90.29%, respectively. Microbial addi- CH and NH emissions in BM group were reduced by tives greatly reduced the emissions of N O in the com- 2 4 3 65.23% and 42.05%, respectively, which was the best posting process. This might be attributed to the addition among the three treatment groups. In terms of CO of exogenous compound microbial agent prevented the emissions, all three treatment groups increased, while growth of nitrifying microorganisms and the activity of BM treatment group only increased by 1.61%, which was related enzymes, thus inhibiting the nitrification of N O the lowest increase. Generally speaking, biochar carried production (Cui et al. 2019). W ang et al. Biochar (2023) 5:3 Page 11 of 17 Table 2 The cumulative emissions of gases compared with the CK group CH CO NH N O 4 2 3 2 BM − 65.23% ± 5.83 c 1.61% ± 1.43 b − 42.05% ± 5.57 b − 68.64% ± 9.68 b B 111.81% ± 5.52 a 123.77% ± 29.02 a − 20.09% ± 1.52 a − 17.01% ± 2.58 a M − 11.18% ± 2.15 b 193.28% ± 32.41 a − 20.60% ± 2.59 a − 90.30% ± 14.14 b Results are the mean of three replicates ± standard deviation. M: CK + 0.01% compound microbial agents; B: CK + 0.1% biochar; and BM: CK + biochar carried microbial agent (0.01% compound microbial agent to 0.1% biochar before being naturally dried) microbial agent could effectively reduce gas emissions kinds of organic acids, alcohols and lipids. Wang et al. and had good environmental benefits (Jindo et al. 2012; (2016b) showed that thermophilic Actinobactenia were Tu et al. 2019). important in the biodegradation of lignocellulose in cow manure composting. The relative abundance of Fir - 3.4 E ec ff t of additives on bacterial communities micutes and Actinobactenia in the BM treatments was The samples of four treatments on days 6 (thermophilic the highest at the thermophilic stages, reaching 39.24% stage), 14 (cooling stage) and 28 (maturity stage) were and 24.79%, respectively, which also explained that BM collected to analyze the changes of bacterial diversity and treatment group had higher peak temperature, longer richness by 16S rDNA gene sequences. All sequences thermophilic period and faster degradation rate of OM of each sample are clustered as Operational Taxonomic compared with the CK. With the decrease of pile tem- Units (OTU), and the recognition rate exceeds 97% (Xue perature, the relative abundance of Firmicutes in the et al. 2021). Chao 1 index can reflect the bacterial com - maturity stage dropped to 14.78%, 14.42%, 9.82% and munity richness (Mao et al. 2019). Shannon and Simpson 12.32% for BM, B, M and CK, respectively. In the cool- indexes are used to assess the species diversity and even- ing and maturity stages , the abundance of Proteobacte- ness. The better diversitycorresponds to higher Shannon ria in BM and B treatment groups was much higher than and lower Simpson index (Liu et al. 2018). As shown in that in CK. Some Proteobacteria had the functions of Additional file 1: Table S2, the coverage index was above nitrogen fixation and reducing nitrogen loss, which are 0.99, ensuring the accuracy of the results in the real state. related to the conservation of nitrogen in the compost According to the OTU number, Shannon, Simpson, and (Xi et al. 2016). This was consistent with the findings that Chao 1 index, biochar carried microbial agent could the addition of biochar carried microbial agent and bio- increase the abundance and diversity of bacterial com- char reduced N O and NH emissions and increased the 2 3 munities in compost. It also showed that the addition of TKN contents in the compost. Chloroflexi played a major biochar carried microbial agent in compost had a positive role in the metabolism of amino acids and carbohydrates impact on the activity of microbial community, which (Li et al. 2019b). In this study, the relative abundance of might be because the porous structure of biochar was Chloroflexi in all treatments increased as composting suitable for the growth and reproduction of microorgan- progressed, probably because of the ability of Chloroflexi isms (Sun et al. 2016). At the same time, biochar could to utilize metabolites and cellular compounds extracted also provide inorganic nutrients for the microorganisms, from the dead biomass (Xu et al. 2019). which was more conducive to the survival and reproduc- The dominant bacterial abundances in genus level tion of endogenous and exogenous microorganisms in are shown in Fig. 6b. In this study, legends with rela- the compost heap (Steiner et al. 2016). tive abundance less than 1% were not shown and were Relative abundance of the dominant bacterial taxo- classified into other groups. During the thermophilic nomic groups in phyla level is shown in Fig. 6a. The period, Rhizobiaceae, norank_f_JG30_KF_CM45, Pseu- microbial communities in each stage of composting domonas, Cellvibrionaceae, Bacillus and Cellulomonas showed similar change patters, but there were also some were the dominant bacteria, accounting for more than differences. The main bacterial phyla in the thermophilic 20%. In the thermophilic stage, Bacillus can produce phase were Proteobacteria, Actinobacteria and Firmi- spores to resist high temperature and high osmotic cutes, and their relative abundance exceeded 70%. Zhang pressure. However, the survival of Bacillus in the four et al. (2014) reported that Firmicutes could grow in the treatments was reduced due to a decrease in OM at heat by producing thick spores and mainly exist in the the end of composting (Grata et al. 2008). Both Pseu- thermophilic stage in the composting process. Pandey domonas and Rhizobiaceae have nitrogen fixation. The et al. (2013) showed that Firmicutes were able to degrade relative amounts of these two bacteria were higher cellulose, hemicellulose and lignin, and hydrolyze sug- in the BM and B treatments than in the CK group ars and proteins. As the same time, it could produce all throughout the composting process, which further Wang et al. Biochar (2023) 5:3 Page 12 of 17 Fig. 6 Bacterial abundance at phyla level (a), and bacterial abundance at genus level (b) in different treatments during composting. CK: sheep manure + corn straw; M: CK + 0.01% compound microbial agents; B: CK + 0.1% biochar; and BM: CK + biochar carried microbial agent (0.01% compound microbial agent to 0.1% biochar before being naturally dried) explained that the addition of biochar carried microbial of phenolic compounds (Vieyra et al. 2009). After that, agent and biochar had a promoting effect on nitrogen E /E showed a trend of first rising and then declining. In 4 6 conservation. the end, the E /E ratios of the BM, B, M and CK treat- 4 6 ment groups were 2.84, 3.47, 3.68 and 3.32, respectively. 3.5 E ec ff t of additives on maturity parameters Compared to CK, the BM treatment group showed a The ratio of E /E usually reflects the condensation and lower ratio, indicating that biochar carried microbial 4 6 aromatization of humus in compost (Ren et al. 2020). E / agent promoted the condensation and aromatization of E value is negatively correlated with the degree of matu- humus very well. ration in the compost. As shown in Additional file 1: Fig. Seed germination index (GI) is a significant indica - S4(a), E /E ratios decreased rapidly in the initial stage tor to assess phytotoxicity and maturity of compost 4 6 due to the mineralization of carbohydrates and oxidation (Qiu et al. 2020). Additional file 1: Fig. S4(b) shows that W ang et al. Biochar (2023) 5:3 Page 13 of 17 0.8 the GI curves for the four treatments increased stead- Halanaerobiaeota -0.455 -0.353 -0.475 -0.266 ily in the compost. All treatment groups had low initial Deinococcota -0.072 -0.139 -0.194 0.016 GI values. This is likely because of the rapid decomposi - 0.5 Acidobacteriota -0.02 0.109 0.646 0.525 tion of OM in the initial stages of composting, producing -0.087 0.589 0.1920.025 Gemmatimonadota large amounts of volatile fatty acids (VFAs) and ammo- 0.2 -0.372 0.09 -0.040.017 Patescibacteria nium, which were toxic to seed germination (Jiang et al. -0.037 0.266 0.764 0.506 Myxococcota 2018). Finally, the GI values in BM, B, M and CK were -0.1 Chloroflexi 0.105 0.208 0.8140.695 97.92%, 88.25%, 94.32%, and 84.66%, respectively. All -0.143 -0.511 -0.68-0.447 the GI values were above 80%, indicating that the com- Firmicutes -0.4 posts reached maturity and elimination of phytotoxicity -0.589 0.199 -0.039 -0.365 Actinobacteriota (Yang et al. 2015). The final GI values of the other three 0.523 -0.083 -0.28-0.152 Proteobacteria -0.7 treatments were all increased compared with CK, espe- N O NH CH CO 2 2 3 cially BM treatment. This indicated that the addition of Fig. 7 Correlation analysis between gaseous emissions and microbial biochar carried microbial agent accelerated the stabiliza- relative abundance in phyla level based on the spearman correlation. tion and reduced the phytotoxicity of the compost. The The right side of the legend is the color range of different r values. Red is positive and blue is negative correlation. The value of p < 0.05 is result could be attributed to the higher peak temperature marked with *, p < 0.01 is marked with ** and longer thermophilic period of BM treatment, which was beneficial for the killing of pathogenic bacteria and improvement of compost quality. on the abundant phyla. The total contribution rates of the two axes on the distribution of bacterial community struc- 3.6 The relationship between microbial community ture in thermophilic, cooling and maturity stages were and selected factors 96.20%, 96.46% and 97.56%, respectively, and the analysis The Pearson correlation coefficient of gas emissions results were relatively reliable. A certain distance between and microbial relative abundance in phyla level was cal- the points of different treatments was observed at different culated to explore the relationship between them. The stages of composting, indicating that additives can change results are shown in Fig. 7. Correlation analysis revealed the microbial structure in compost. The correlation order that N O emissions were positive related with Chloro- 2 of environmental factors affecting bacterial community flexi. Yang et al. (2019) and Xue et al. (2021) believed that structure in thermophilic, cooling and maturitystages were the anaerobic environment in composting was positively − + EC > E /E > NO -N > NH -N > OM > TKN > C/N > Tem- 4 6 3 4 correlated with the relative abundance of Chloroflexi, p era t ur e > p H > G I, which would increase the emission of N O, which was − + 2 EC > TKN > NO -N > pH > OM > NH -N > C/N > Tem- 3 4 consistent with the results of this study. NH emissions 3 perature > E /E > GI, TKN > T empera- 4 6 were positively related with the relative abundance of + − ture > OM > NH -N > EC > NO -N > E /E > C/N > pH > GI, 4 3 4 6 Myxococcota, Chloroflexi and Acidobacteriota, but nega - respectively. During thermophilic and cooling stages, EC tively with that of Firmicutes. The results indicated that was the critical factor influencing bacterial community these microorganisms likely played important roles in structure. The relative abundance of most bacteria has a the NH release processes. Lei et al. (2021) also showed 3 negative correlation with the EC value, indicating that the a strong and significant relationship between the main excessive salt content in compost has a significant inhibi - phyla (Firmicutes, Acidobacteriota, Proteobacteria, and tory effect on the growth and reproduction of microorgan - Chloroflexi) and variations in the nitrogen loss (NH and 3 isms, thus affecting the microbial community structure. The N O) in the composting process. CO emissions were 2 2 main reason is that salt affects the effectiveness of water or positively correlated with Gemmatimonadota. Actino- the physiological and metabolic processes of microbial cells. bacteria was negatively related with the CH emissions, 4 The amount of TKN mainly controlled the change of bacte - which suggested that Actinobacteria could inhibit the rial community structure in the maturity stage. Duan et al. proliferation of methanogens to reduce C H emissions 4 (2019) reported that temperature was the main factor influ - from compost (Xue et al. 2021). encing microbial community structure in thermophilic and Environmental factors will affect bacterial communi - maturity stages of composting. In this study, although tem- ties and their functions, and redundancy analysis (RDA) perature was not the most relevant environmental factor, it can express the correlation among environmental factors also played an important part in changing microbial com- and microbial communities during composting. Figure 8 munity structure throughout affecting the biological activity shows the effects of composting factors ( temperature , of microorganisms. + − pH, OM, C/N, EC, TKN, NH-N, NO-N, E /E and GI) 4 3 4 6 Wang et al. Biochar (2023) 5:3 Page 14 of 17 Fig. 8 Redundancy analysis (RDA) between environmental factors and microbial communities during thermophilic stage (a), cooling stage (b), maturity stage (c) Significant relationships were determined between the main host bacteria for nifH gene of nitrogen-fixing the main phyla (Proteobacteria, Firmicutes, Chloroflexi, microorganisms. In the cooling and maturation peri- Deinococcota, and Acidobacteriota) and variations in ods, Chloroflexi and Acidobacteriota revealed highly + − − the nitrogen contents (N H -N and N O -N) in the negative correlation with NO -N, but positive relation- 4 3 3 composting process. In thermophilic stage, Proteo- ship with NH -N, which might have played important bacteria had significant and positive correlations with roles in the transformation of nitrogen. In subsequent NH -N (p < 0.05), Firmicutes and Deinococcota were studies, functional microorganisms related to nitro- positively correlated with N O -N, indicating that these gen transformation in composting process can be fur- three phyla played an important role in nitrogen trans- ther explored through the level of microbial genera and formation and release in this stage. Xu et al. (2022a) related functional genes. also showed that Firmicutes and Proteobacteria were W ang et al. Biochar (2023) 5:3 Page 15 of 17 Author details 4 Conclusions School of Energy and Environment, Inner Mongolia University of Science This study showed that all four treatments satisfied the and Technology, Baotou 014010, China. Inner Mongolia Engineering Research sanitation standards and requirements of compost matu- Center of Evaluation and Restoration in the Mining Ecological Environment, Inner Mongolia University of Science and Technology, 014010 Baotou, China. rity during the 28-day aerobic composting. BM treat- ment significantly extended the high temperature stage Received: 14 July 2022 Revised: 15 December 2022 Accepted: 26 Decem- of compost, improved the degradation capacity of OM ber 2022 and minimized the formation of large clumps. It also reduced nitrogen losses and increased nutrient reten- tion during composting. Compared with CK, BM group References reduced CH by 65.23%, N H by 42.05% and N O by 4 3 2 Awasthi MK, Wang Q, Huang H, Ren X, Lahori AH, Mahar A, Ali A, Shen F, Li R, 68.64%, respectively. 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J Environ Manage 230:119–127. https:// doi. org/ and comments to further improve the quality of the manuscript.10. 1016/j. jenvm an. 2018. 09. 076 Chen HY, Awasthi SK, Liu T, Duan YM, Ren XN, Zhang ZQ, Pandey A, Awasthi Author contributions M (2019) Eec ff ts of microbial culture and chicken manure biochar on ZW: Conceptualization, supervision, writing—review and editing, Funding compost maturity and greenhouse gas emissions during chicken manure acquisition, project administration. YX: Formal analysis, data curation, writ- composting. J Hazard Mater 389:121908. https:// doi. org/ 10. 1016/j. jhazm ing—original draft. CZ: Supervision, conceptualization, funding acquisition. at. 2019. 121908 QJ: Supervision, conceptualization. TY: Formal analysis, data curation. YL: Chung WJ, Chang SW, Chaudhary DK, Shin JD, Kim H, Karmegam N, Govart- Formal analysis. TZ: Formal analysis. All authors read and approved the final hanan M, Chandrasekaran M, Ravindran B (2021) Eec ff t of biochar manuscript. amendment on compost quality, gaseous emissions and pathogen reduction during in-vessel composting of chicken manure. Chemosphere Funding 283:131129. https:// doi. org/ 10. 1016/j. chemo sphere. 2021. 131129 This work was supported by the National Key Research and Development Cui P, Chen Z, Zhao Q, Yu Z, Yi Z, Liao H, Zhou S (2019) Hyperthermophilic Program of China (2018YFC1802904), the National Science Foundation of composting significantly decreases N O emissions by regulating China (52264013 and 41867061), Inner Mongolia Science & Technology Plan N O-related functional genes. Bioresour Technol 272:433–441. https:// doi. 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Journal
Biochar – Springer Journals
Published: Jan 16, 2023
Keywords: Biochar carried microbial agent; Sheep manure; Composting; Nitrogen transformation; Bacterial community; Greenhouse gases