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Article

Large-Scale Biochar Incorporation Does Not Necessarily Promote the Carbon Sink of Estuarine Wetland Soil

by
Mengdi Xie
1,
Xiaojuan Lu
2,3,
Han Wang
2,
Xiaohua Fu
2,3 and
Lei Wang
2,3,*
1
State Key Laboratory of Geohazard Prevention and Geoenvironment Protection, Chengdu University of Technology, Chengdu 610059, China
2
Key Laboratory of Yangtze River Water Environment, Ministry of Education, College of Environmental Science and Engineering, Tongji University, Shanghai 200092, China
3
Shanghai Institute of Pollution Control and Ecological Security, Shanghai 200092, China
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(24), 16709; https://doi.org/10.3390/su152416709
Submission received: 25 August 2023 / Revised: 21 November 2023 / Accepted: 5 December 2023 / Published: 10 December 2023
Browse Figures
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Abstract

:
Biochar incorporation is a widespread approach for soil improvement and soil carbon sequestration. However, there have only been a few studies on the effects of large-scale biochar incorporation on the estuarine wetland soil. To assess the different rates and incorporation times of biochar effects on the soil carbon cycle, the effects and mechanisms of biochar actions on soil respiration and plant growth were clarified via an outdoor control experiment that analyzed the soil microbial activity and community structure of estuarine wetland soil. The results unconventionally showed that a higher rate (238.82 g·kg−1) of biochar incorporation achieved stimulated soil respiration compared to lower incorporation rates (9.14 g·kg−1, 23.89 g·kg−1, 47.79 g·kg−1 and 143.36 g·kg−1) and was 38.9%, −21.8%, and 6.23% higher than the soil respiration of the control on three incorporation months. The soil microbial biomass (45.54% in the higher rate of biochar incorporation soil than the control) and the activities of β-glucosidase enzymes (25.4% higher in the higher rate of biochar incorporation soil than the control) explained these differences in soil respiration. This phenomenon was confirmed to be a result of provoking the bacteria of a heterotroph or from a lower humification ability, which enhanced organic carbon degradation in a large amount of biochar incorporation soil. In conclusion, even large-scale biochar incorporation may introduce more stable carbon to the soil, and the carbon sink of estuarine wetland soil may weaken due to the greater carbon output generated in its specific soil microbial species.

1. Introduction

Biochar incorporation is a highly efficient straw-reusing method because it allows for the rapid consumption of considerable levels from arable agriculture [1]. Carbonizing straws endow straw biochar with high stability and biochemical resistance to decomposition and produce biochar that can remain stable in the soil for hundreds of years [2]. Numerous studies on the effects of straw biochar incorporation into soils have revealed soil quality improvement, a reduction in greenhouse gas emissions and plant growth promotion [3,4,5,6]. For CO2 sequestration, it is generally accepted that biochar application is beneficial to the C sink in most categories of soil [7,8]. Owing to its chemical and biological inertness, as well as the physical protection of its surrounding environment, straw biochar trapped 47% of soil organic carbon (SOC) in rice cultivation soil and 57% in maize cultivation soil [9]. As a result, researchers concluded that these effects after biochar incorporation into the soil were due to several factors such as soil type, biochar composition, and incorporation rate [10,11,12].
Many studies have confirmed the positive effects of an appropriate biochar incorporation rate on a soil C sink in a general type of soil. However, the estuarine wetland soil environment is significantly different from agricultural soils and forest soils due to the submerging condition and lack of O2 [13]. Therefore, the biochar incorporation into the estuarine wetland may arouse a varied mechanism of the soil C cycle processes. The disturbance to soil anaerobic conditions via biochar incorporation may weaken the C sink of estuarine wetlands by increasing SOC degradation [14]. Our preliminary study found that the CO2 emission in Yangtze River Estuary soil increased after biochar incorporation, the phenomenon of which lacks direct experimental evidence and substantial data support, and the reason for higher soil CO2 output after biochar incorporation to the estuarine soil is still unknown. As a result, estuarine wetland is a natural C pool because of its exceedingly high primary productivity and low decomposition of SOC associated with permanently submerged conditions. Biochar incorporation to reclaimed estuarine wetlands, with the goal of reclaimed estuarine wetland soil improvement and C sink value augment, needs more scientific data to further determine the method and effects of biochar incorporation.
Consequently, in this study, field experiments were conducted under different biochar incorporation rates on estuarine wetland with an analysis of the soil properties, soil respiration (SR), plant performance, and soil microorganisms to investigate whether the addition of biochar affects CO2 sequestration and plant growth, which will help us to identify an appropriate rate of biochar incorporation for straw return in an estuarine wetland soil. Moreover, the response of soil microbes and their correlation with plant growth and SOC stability were examined to elucidate the mechanisms behind the different effects of the biochar. The results offer many meaningful insights for future research about estuarine wetland soil development and provide a reference for biochar incorporation rates in practical applications.

2. Materials and Methods

2.1. Soil Collection and Biochar Preparation

The experimental soil was acquired from newly reclaimed spots (marked) in Chongming Dongtan wetland (121°45′ E, 31°30′ N), Yangtze Estuary, Shanghai, China, using the ‘W-shaped’ sampling method from the 0~20 cm layer of the soil [15]. The annual climate and precipitation (on average) were 15.5 °C and 1024 mm. The original soil exhibited the following properties: bulk density, 1.38 g·cm−3; water content, 21.67%; pH, 7.32; total nitrogen (TN), 2.29 g·kg−1; available phosphorus, 2.21 g·kg−1; and SOC, 11.4 g·kg−1. The soil sample was prepared by abandoning impurities and using a 0.22 mm sieve.
The biochar was produced via pyrolysis at 450 °C ± 20 °C in a reflux carbonization furnace designed by the Biochar Engineering Technology Research Center, Liaoning Province, China, with reference to Yin et al. [16]. In brief, the dried straw (soybean, Glycine max (Linn.) Merr) was stabilized in the furnace and heated with a slow increase in temperature from 25 °C to 450 °C. Afterward, the material was kept at 450 °C for at least 30 min to guarantee no release of volatile chemicals, and was then cooled down in a N2 atmosphere. The prepared biochar was then smashed to 2 mm for subsequent disposal. The following properties of the biochar were identified: bulk density, 0.57 g·cm−3; moisture content, 38.80%; pH, 7.51; total nitrogen (TN), 3.07 g·kg−1; and organic carbon (OC), 524.7 g·kg−1. The carbonization yield rate of the straw was 36.57%.

2.2. Experimental Procedures

Six treatments were set in three replicates as follows: the control soil without any biochar (CK); biochar incorporation rate of 9.14 g·kg−1 (B1); biochar incorporation rate of 23.89 g·kg−1 (B2); biochar incorporation rate of 47.79 g·kg−1 (B3); biochar incorporation rate of 143.36 g·kg−1 (B4); and biochar incorporation rate of 238.82 g·kg−1 (B5). Each treatment had a total weight of 35 kg after adequate mixing with the prepared soil incorporated with biochar, and the soil with different treatments was separated with boards to avoid soil interactions. The field study was conducted using the prepared soil treatments after their backfilling to the marked spot in Chongming Dongtan wetland and the backfilling was conducted three times in May, June, and July to compare the effects of biochar incorporation into the soil carbon cycle across different seasons.
In May, June, and July 2018, after balancing the backfilled soil with the surrounding environment, the experiment was conducted under natural conditions with a cultivation temperature of 28 °C ± 2 °C in the daytime and 25 °C ± 2 °C at night in the abovementioned spot. We selected soybean (Glycine max (Linn.) Merr) as the test plant because it is a common crop species with no strict habitat requirement. The seedling materials were provided by Shanghai Dongtan International Wetland Co., Ltd. (Shanghai, China). The soil was added with 60 g kg−1 of NPK fertilizer and 440 g kg−1 of OM. After 20 days of stabilization, eight soybean seedlings with identical growth performance were transplanted to each soil with different treatments. During cultivation, plants were irrigated every three days without any fertilization. Subsequently, the soybeans were harvested after 2 months of cultivation and the growth performance was recorded.
Three soil samples of each treatment over the three months were collected at depths of −5 to −20 cm and mixed to determine the soil index. One part of the mixed soil sample was stored at 4 °C to determine the soil microbial biomass (SMB) and soil enzyme activity within a week, while the other was air-dried and passed through a 60-aperture sieve for the tests of dehydrogenase activity and soil total organic carbon (TOC). The soil sample for microbial community analysis was stored in a −80 °C fridge for DNA extraction within a month.

2.3. Soil and Plant Analyses

2.3.1. Plant TC and TN Content

The seedlings aboveground were harvested and dried at 120 °C for 8 h and weighed to measure their biomass. Then, 5–10 mg dried plant samples were placed in a platinum vessel after passing through a 0.25 mm sieve to test the plant total carbon (TC) and TN. A Vario EL III elemental analyzer (Elementar Analysensysteme Co., Hanau, Germany) was then used to determine the plant nutrient elements.

2.3.2. Soil pH and SR

Soil pH was measured in a suspension of 25 mL of organic sample in CaCl2 solution (0.01 M, 25 mL) [10]. For the SR test, based on Han et al. [17], three PVC soil collars (10 cm-diameter) were installed with a soil chamber for gas collection. The chambers were connected to an SR-determination system (LI-8100A Automated Soil Flux System, LI-COR Biotechnology, Lincoln, NE, USA). The SR was tested both during the day and at night.

2.3.3. Soil Enzyme Activity

Soil β-glucosidase and dehydrogenase activities were analyzed using the standard method described in Tabatabai [18]. To determine the β-glucosidase activity, moist soil (3.00 g) was treated with 4 mL of modified universal buffer (pH 6.0) and 1 mL of 0.05 M p-nitrophenyl-β-glucosidase (pNPG) and then incubated at 37 °C. After 1 h, the reaction was terminated by adding 1 mL of 0.5 M CaCl2 and 4 mL of 0.1 M Tris–hydroxymethyl (NaOH treated). The pH was adjusted to the value of 12 with NaOH. The mixture was centrifuged for 10 min (1000 rpm) and the absorbance was measured at 492 nm. To determine the dehydrogenase activity, moist soil (2 g) was treated with 5 mL of 0.1% 2,3,5-triphenyltetrazolium chloride (TTC), 2 mL 1% glucose solution and 2 mL Tris buffer (pH 7.6) and then incubated at 37 °C in darkness for 24 h to reduce TTC to triphenyl formazan (TPF). The mixture was centrifuged (10 min), and the absorbance was measured on a spectrophotometer at 410 nm. The relative enzyme activity (REA) was determined using the enzyme activity of SOC.
The SMB was estimated based on the ATP levels, which were measured using an ATP bioluminescent somatic cell assay (Sigma, St. Louis, MO, USA) and a determination apparatus (US61M/SCC11-Profile-1 3560 10X, Beijing, China) [19].
We determined the easily oxidizable carbon (EOC) using the method of Blair et al. and Yang et al. [20,21]. A sample containing 15–30 mg of air-dried biochar was mixed with 333 mmol L−1 KMnO4 for 1 h. EOC was calculated using the amount of KMnO4 reduced via spectrophotometric analysis.

2.3.4. Soil DNA Extraction and Soil Microbial Structure Analysis

Based on the results regarding plant performance, soil enzyme activity, and SR, B4 and B5 showed the greatest difference among different treatments. Thus, in this study, the soil microbial structure analysis was performed in the CK, B4, and B5 treatments to achieve the most representative results for the soil microorganism system. A PowerSoil soil DNA isolation kit (MoBio Industries, Carlsbad, CA, USA) was used for DNA extraction from soils according to the manufacturer’s instructions. Subsequently, the quantity and purity of the extracted DNA were analyzed for qualification using the absorbance at 260 and 280 nm (OD260/OD280 > 1.8). The extracted DNA was then stored at –70 °C for further molecular analysis.
High-throughput sequencing was used to analyze the soil microbial community structure [22]. In brief, the V4-V5 regions of the bacterial 16S-rRNA genes were amplified using the following bacterial primers: 515F: (5′-GTGCCAGCMGCCGCGG-3′) and 907R (5′-CCGTCAATTCMTTTRAGTTT-3′). PCR amplifications were conducted in a 25 μL reaction system that contained 5 μL of 5×PCR buffer, 5 μL of 5×GC buffer, 5 μL of 10 mmol L−1 dNTP, 1μL of 10 μmol L−1 forward primer, 1μL of 10 μmol l-1 reverse primer, and 2 μL of DNA template and ddH2O. The following thermal cycling scheme was used: initial denaturation at 98 °C for 2 min, 28 cycles of repeated denaturation at 98 °C for 15 s, annealing at 55 °C for 30 s, and extension at 72 °C for 30 s, followed by the final extension process at 72 °C for 5 min.
Subsequently, the PCR amplification products were analyzed via 0.8% agarose gel electrophoresis. The PCR products of the 16S rRNA gene were then used as a template to establish a sequencing library using the Illumina MiSeq Platform (Majorbio, China) by Shanghai Personal Biotechnology. Subsequently, the QIIME software (V. 3.0) was then used to cluster the effective sequences into operational taxonomic units (OTUs) with a 3% level of evolutionary distance, and the results were presented in the form of a Venn diagram. The effective sequences obtained from pyrosequencing were compared with the Greengenes 16S rRNA gene database using NCBI’s BLASTN tool to obtain the microbial taxonomic information. The community composition statistics at the phylum and genus level were also analyzed. The diversity estimators of Chao, ACE, and Shannon indexes were obtained for each treatment.

2.4. Data Processing and Statistical Analysis

The results of each treatment were reported as an average of three parallel samples. Statistical analysis was conducted using SPSS 16.0 and Microsoft Excel 2018 including one-way analysis of variance (ANOVA) and principal component analysis (PCA). In addition, ANOVA analysis, Tukey’s multiple-comparison tests (p < 0.05), and Pearson’s correlation analysis were performed. The figures were created using Prism 8.0 and Microsoft PowerPoint.

3. Results

3.1. Plant Growth

As shown in Figure 1 and Table A1 (Appendix A), there was significant difference in plant TC among different treatments, and plant TC and TN exhibited an increasing trend from the small to the big scale of biochar incorporation rate (however acquired a decrease in plant TC and TN with 238.82 g·kg−1 of biochar incorporation (Table A1)). Furthermore, plant TC and TN incorporated with biochar in May were higher than those in June and July. In addition, a difference in plant biomass was observed in that it increased first with 23.89 g·kg−1 to 143.36 g·kg−1 of biochar incorporation, but decreased at a big scale of biochar incorporation. Here, the treatments with a 143.36 g·kg−1 rate of biochar incorporation (B4) on different months always achieved a higher biomass than the CK, with a differences of 201.8 g m−2 (May), 348.6 g m−2 (June), and 32 g m−2 (July). This indicated that the promotion of plant growth via biochar incorporation can be only generated when with an appropriated incorporation rate, while excessive biochar incorporation (i.e., 238.82 g·kg−1) may inhibit plant growth.

3.2. Response of Soil Respiration

As shown in Figure 2c, SR showed different changes, such as an increase in biochar incorporation rate with different incorporation times. First, the SR of the soil incorporated with biochar in June was much higher than that in May and July (eight times higher). In addition, the SR of the control was generally higher than that of lower biochar incorporation treatments in June and July; however, the SR of B1 to B5 incorporated with biochar in May was higher than that of the control. To elaborate, the SR of soil incorporated with biochar in May increased as the biochar incorporation rate increased (with the highest SR at B4 of 15.81 umoL·m−2·s−1). Although the SR with 238.82 g·kg−1 biochar incorporation showed a shrinking trend, it was still higher than the control (8.4 umoL·m−2·s−1 over 3.4 umoL·m−2·s−1). In addition, as the biochar incorporation rate increased in July, the difference in the SR in CK and biochar-incorporated treatments gradually increased. This indicated that the more biochar was added to the soil in estuarine wetlands, the greater its inhibition of SR. However, the SR of 238.82 g·kg−1 biochar-incorporated soil was inversely higher than that of other treatments, especially with an increase of 6.23% compared with the control (Figure 2c), which revealed that an excessive incorporation of biochar to estuarine wetland soil may stimulate SR.

3.3. Response of Soil β-Glucosidase and Dehydrogenase Activities

In general, the soil enzyme activity across different treatments showed similar changes over three incorporation times. The dehydrogenase activities of all biochar-incorporated treatments were higher than that of CK, with striking increases in 238.82 g·kg−1 biochar-incorporated soil of 50.01% (May), 45.45% (June), and 49.6% (July) (Figure 2a). In contrast, the β-glucosidase activity of the lower rates of biochar incorporation treatments exhibited lower values than CK, and the inhibition of β-glucosidase activity increased with the greatest decreases of 4.2% (May), 33.6% (June), and 78.9% (July). However, the β-glucosidase activity of 238.82 g·kg−1 biochar-incorporated soil showed a unique increase compared with that of the CK of 43.5% (May), 18.9% (June), and 25.4% (July), which demonstrated that an excessive addition of biochar to estuarine wetland soil would arouse the activity of β-glucosidase, which may be the reason for higher SR in the 238.82 g·kg−1 biochar-incorporated treatment, no matter on which incorporation months.

3.4. Response of Soil Microbial Biomass and Community Structure

As shown in Figure 2b, the SMB of soil incorporated with biochar in July was much higher than that in May and June, and the last two groups had similar changes in SMB. In addition, no matter on which incorporation months, despite the shrinking of SMB in biochar-incorporated treatments compared with the control, soil incorporated with 238.82 g·kg−1 of biochar seemed to mildly increase compared to other treatments. This indicated that the inhibition of biochar incorporation into SMB would weaken if excessive biochar was added to the soil.
Based on these results, the 143.36 g·kg−1 and 238.82 g·kg−1 rates of biochar-incorporated soil showed the greatest differences in plant performance, soil enzyme activity, and SR. Although there were differences in plant performance and soil index among soil incorporated with biochar on different months, a high biochar incorporation rate tended to stimulate more obvious changes in the plant and soil. Thus, a soil microbial structure analysis was performed in the CK, and 143.36 g·kg−1 and 238.82 g·kg−1 rates of biochar-incorporated soil were used to acquire the most representative microbe mechanism behind these results. First, OTUs were divided into 97% similarity levels, and the effective sequences of 32,247, 39,184, and 40,833 were obtained after the removal of chimeric or singleton sequences, respectively. As shown in Table 1, regardless of the applied microbial biodiversity model, the 238.82 g·kg−1 rate of biochar-incorporated soil presented the highest microbial biodiversity, followed by the lowest incorporation rate of biochar and CK, which revealed that biochar incorporation changed the soil microbe structure of the estuarine wetland soil.
Subsequently, the Venn diagram presented in Figure 3a shows the microbial variability among the different soil treatments based on the OTUs analysis. There were more unique OTUs in B5 than in B4 and CK, which suggests that the microbial community of the soil incorporated with a high level of biochar acquired significant alterations. In addition, PCA analysis (Figure A1) suggests a separation of bacterial communities in the three treatments, indicating a significant difference in bacterial communities among the three treatments. In summary, the high incorporation of biochar (238.82 g·kg−1) made a considerable difference in community composition.
Furthermore, the difference in the taxonomic composition of the microbial community was revealed at both the phylum level (Figure 3b) and genus level (Figure 4). In general, the three treatments initially shared similar dominant microbial structures at the phylum level (Figure 3b): Proteobacteria, Acidobacteria, and Actinobacteria. The change in microbe abundance of various species in different treatments was observed. For example, compared with the CK and B4 treatment, 238.82 g·kg−1 of biochar incorporation soil decreased Actinobacteria (by 1.9% and 18.2%, respectively) but increased Proteobacteria (by 4.4% and 6.6%, respectively). In addition, Chloroflexi in the B5 treatment also decreased by 18.57% and 0.68%, respectively, compared with that of CK and B4 treatment (Figure 3b). Bacteroides increased by 17.8% and 10% compared with the other two treatments (Figure 3b).
At the genus level, the difference in microbial community diversity was clear. High biochar incorporation in soil (238.82 g·kg−1 rate of biochar) showed mostly significantly enriched Nannocystis and Plesiocystis and Phenylobacterium, Agromyces, Arenimonas, Nitrospira, Planctomyces, and Steroidobacter were also slightly enriched in this treatment (Figure 4). In contrast, the abundance of Candidatus. Nitrososphaera, Rubricoccus, Pirellula, Gemmata, Rhodoplanes, Skermanella, Afifella, Streptomyces, and Opitutus of B5 treatment shrank compared with those of the control. In addition, Candidatus. Nitrososphaera, Rubricoccus, Gemmata, Candidatus. Koribacter, Cupriavidus, Arthrobacter, Opitutus, Flavisolibacter, Hyphomicrobium, Amaricoccus, Jiangella, Pilimelia, Nonomuraea, Rubrivivax, and Actinomadura were deactivated in the B5 treatment compared with those in the B4 treatment (Figure 4). The distinction in microbe abundance demonstrated the different response of the soil microbial structure to different rates of biochar incorporation, which may determine the activity of the soil enzyme responsible for SOC accumulation and degradation.

4. Discussion

4.1. Large-Scale of Biochar Incorporation May Weaken Its Promotion of Plant Growth and CO2 Sequestration in Estuarine Wetland Soil

Biochar incorporation applied to reclaimed estuarine wetland soil remains in a few studies [23]. Straw biochar is frequently used as a soil amendment to increase crop yield. Laird et al. showed that biochar-amended soil (0%, 0.5%, 1% and 2%) had lower soil bulk density, greater water retention, larger specific surface areas, higher cation exchange capacities, and pH values, and increased total N organic C and Mehlich III-extractable P, K, Mg and Ca, which finally promoted plant growth [24]. Moreover, as a sustained release fertilizer carrier, biochar improves plant biomass by increasing the utilization efficiency of fertilizers [25]. However, for reclaimed estuarine wetland soil, uncertainty remains regarding the positive effect of biochar incorporation on plant performance and crop yield because of the difference in soil structure and physicochemical properties of inland soil and estuarine wetland soil. In this sense, biochar from soybean was applied to a representative reclaimed soil in the Yangtze Estuary wetland, Shanghai, China, at various incorporation rates to clarify the exact effects of biochar incorporation to estuarine wetland soil.
First, the results have confirmed the benefit of biochar incorporation into plant biomass with a higher incorporation rate than most previous studies [26]. Such plant biomass improvement after a high scale of biochar incorporation can be explained by specific estuarine wetland soil structure and surrounding conditions. For estuarine wetland soil in a state of decay and semi-decay, the incorporated biochar can much more easily infiltrate into the soil, thus altering the availability of nutrients to plants and microorganisms by decreasing the competitiveness of microorganisms for scarce nutrition utilization because of aggregation [27,28]. This may explain why, in the current study, even the higher level of biochar-incorporated treatments also received larger amounts of plant TC and TN than the control soil, and, finally, resulted in a higher nutrient availability and plant biomass in this study. In addition, the treatments of different incorporation times generated diverse plant performance and soil nutrient content, which may be due to the different plant growth rate in different seasons. Furthermore, the higher soil pH (Table A2) observed in this current study helped to decrease the loss of nitrate nitrogen and further ‘fixed’ nutrient in the soil and contributed to increased plant biomass [29]. However, a large rate of biochar incorporation (238.82 g·kg−1) has not exhibited persistent benefits for plant performance, which maybe because the soil needs more time to absorb mineral N and dissolved OC from a large scale of biochar to fix nutrients, thus leading to decreased nutrient utilization efficiency [30,31].
Next, due to the anaerobic condition of estuarine wetlands and their vulnerability to constant tidal OM input disturbance, the OC stability and C cycle of estuarine wetlands differ from that in inland soil, which influences the effect of biochar incorporation on soil amendment. As a result, in this study, it was revealed that biochar addition had different effects on SR and CO2 sequestration with different incorporation rates. As shown in our results, the SR of soil with a 2~30% rate of biochar incorporation was smaller than that of the control, which was parallel with most results [7]. As an organic substrate, biochar is not easily decomposed by microorganisms because of its stable structure. This supports the EOC/TC results shown in Table A3, indicating that the degradability of biochar was much lower than that of the plain soil. In addition, biochar may inhibit the relative availability of native OM in soil via the direct adsorption of the native OM or enzymes related to soil OM decomposition [32,33,34]. It may also lower the decomposition rate of native OC [35]. Consequently, an appropriate incorporation of biochar definitely improves SOC stability, thus decreasing CO2 output (less CO2 emissions) and enhancing the C sink. However, the excessive incorporation of biochar, however, would weaken the C sink of soil by increasing the CO2 output (revealed in this study) in estuarine wetland. This may be derived from the damage to the anaerobic condition of estuarine wetlands after introducing large-scale biochar to the soil. In another respect, soil mineralization may be stimulated or inhibited via biochar incorporation depending on the soil OC level [36]. This means that after a great deal of biochar addition to the wetland soil, the change in the total OC may promote soil mineralization and increase CO2 emissions.

4.2. The Different Effect of Various Rate of Biochar Incorporation to Estuarine Wetland Soil Was Generated via Soil Microbes with Different Functions

In this study, microbial biomass and microbial organism structure help to verify the inhibition effect of the high rate of biochar incorporation on CO2 sequestration in estuarine wetlands [37,38].
First, soil enzymes (such as dehydrogenase, β-glucosidase, and phenol oxidase) catalyze several major biological processes involved in promoting the rate of soil metabolism and mediating OM decomposition [39,40]. In addition, soil microbial biomass affects soil OM turnover [41]. In this study, despite a clear decrease in SMB found in all biochar-incorporated groups, the SMB of the 238.82 g·kg−1 rate of biochar-incorporated soil was higher than the lower rate of biochar-incorporated treatments. Combined with the increase in the enzyme activity of β-glucosidase in large-scale biochar-incorporated soil, it is implied that the large rate of biochar incorporation affects soil microbial metabolism to adjust SR, which was also shown by Sagrilo et al., in that a large incorporation of biochar in soil increased CO2 emissions [42]. Thus, the stimulation of a large incorporation of biochar with regard to SR suggested that estuarine wetland soil needs limited biochar incorporation to stabilize SR strength and maintain C sink function.
Furthermore, the microbial structure and composition helped us to clarify the mechanism resulting in the different rate of the biochar effect on soil enzymes and the C and N cycle [43,44]. For example, at the phylum level, an increase in Proteobacteria in the 238.82 g·kg−1 rate of biochar-incorporated soil and its lower abundance in the 143.36 g·kg−1 rate of biochar-incorporated soil indicated that large biochar incorporation may enhance soil nitrogen fixation. In addition, Actinobacteri are ubiquitous and diverse in soils [45,46], and are well known for their ability to utilize refractory biomaterials to form humus [47]. Increase in the abundance of Actinobacteri in the 143.36 g·kg−1 rate of biochar-incorporated soil but a decrease in the 238.82 g·kg−1 rate one indicated that only the lower biochar incorporation can promote CO2 sequestration via more SOC accumulation in the humification process [48,49]. Furthermore, the relative abundance of Crenarchaeota was significantly enriched in B4. Crenarchaeota is common in soil and utilizes bicarbonate as a C source to perform C fixation [50,51], thus leading to the observation of lower SR in the 143.36 g·kg−1 rate of biochar-incorporated soil. In contrast, Crenarchaeota was found to decrease in 238.82 g·kg−1 rate one, and this meant that high biochar incorporation does not activate the mechanisms responsible for OC accumulation.
At the genus level, the most enriched genus species in the 143.36 g·kg−1 rate of biochar-incorporated soil is Candidatus. Nitrososphaera is one of the autotrophic microbes that utilizes inorganic C to acquire nutrients. The proliferation of this species helps OC to accumulate with a 143.36 g·kg−1 rate in biochar-incorporated soil. In contrast, Nannocystis was significantly enriched in the 238.82 g·kg−1 rate of biochar treatment. Nannocystis belongs to the Myxobacteria and is a heterotroph that can decompose soil OM by producing extracellular active substances such as antibiotics, polysaccharides, and proteases [52]. Combined with the low expression of Nannocystis in the control and a 143.36 g·kg−1 rate of biochar-incorporated soil, this suggests that the higher SR of the 238.82 g·kg−1 rate of biochar treatment was partially derived from the activation of Nannocystis. Furthermore, most other greatly enriched or depressed microbes with the 238.82 g·kg−1 rate of biochar treatment demonstrate soil stress resistance, including Phenylobacterium, Pseudonocardia, and Planctomyces [53,54,55].
In summary, the clear differences in the microorganism abundance provoked by different rates of biochar incorporation verified the mild stimulation of SR via the high rate of biochar incorporation in this study. In brief, small additions of biochar to soil can increase microorganisms that have an autotrophic function or the ability to utilize refractory biomaterials to form humus in estuarine wetland soil. Therefore, the OC degradation ability in these treatments was relatively low, thus inhibiting SR. In contrast, dominant microorganisms induced via high biochar incorporation were mainly heterotrophic microorganisms, which need to degrade OC to meet their nutritional requirements, resulting in increased SR and harm to CO2 sequestration in estuarine wetland.

5. Conclusions

Incorporating biochar into estuarine wetlands promoted plant growth as a result of enhancing plant-available nutrients. However, compared with the low rate (143.36 g·kg−1) of biochar incorporation into the soil which acquired depressed soil respiration, the high incorporation rate (238.82 g·kg−1) of biochar to soil induced heterotrophic microorganisms (such as Nannocystis) and inhibited several autotrophic microorganisms. This contributed to enzyme activity promotion and OC degradation, resulting in enhanced soil respiration and weakened CO2 sequestration in the estuarine wetland. The results aroused our concerns about the effect of the biochar incorporation rate on the C sink of estuarine wetland, which is different from that of general soil. This study also provides data to support estuarine wetland soil management, including straw resource utilization and C sink function development via the utilization of biochar.

Author Contributions

M.X. wrote the original draft. X.L. reviewed and edited the manuscript. H.W. used software and performed data processing. X.F. collected experimental statistics. L.W. offered the idea for the study. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Youth Fund of the National Natural Science Foundation of China (No.42307028), Natural Science Foundation of China (No. 21876127), and the China National Key Research and Development Project (No. 2017YFC0506004).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Informed consent was obtained from all individual participants included in the study.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors have no relevant financial or non-financial interests to disclose.

Appendix A

Table A1. The TN content of soybean cultivated on the soil incorporated with different rates of biochar in different seasons.
Table A1. The TN content of soybean cultivated on the soil incorporated with different rates of biochar in different seasons.
Treatments CKB1B2B3B4B5
TN, mg·kg−1May2.85 ± 0.03a2.56 ± 0.11b2.99 ± 0.13b3.14 ± 0.09b3.57 ± 0.15c2.90 ± 0.05b
June3.01 ± 0.22a3.06 ± 0.14a3.24 ± 0.22a3.17 ± 0.08b3.78 ± 0.21c3.44 ± 0.13a
July3.09 ± 0.12a a3.15 ± 0.22a 3.46 ± 0.23a 3.47 ± 0.19a 4.78 ± 0.31a 3.55 ± 0.17a
a mean ± standard deviations (n = 3), Data with the same letter were considered insignificant and data without the same letter were considered significant (significant level α = 0.05).
Table A2. The pH of the soil incorporated with different rates of biochar in different seasons.
Table A2. The pH of the soil incorporated with different rates of biochar in different seasons.
Treatments CKB1B2B3B4B5
pHMay7.21 ± 0.02b7.18 ± 0.02b7.16 ± 0.01b7.05 ± 0.01c7.08 ± 002c7.25 ± 0.03c
June7.32 ± 0.04a7.19 ± 0.02b7.19 ± 0.02b7.15 ± 0.01b7.28 ± 0.03b7.72 ± 0.04a
July7.23 ± 0.02 b a7.31 ± 0.05 a7.35 ± 0.04a 7.34 ± 0.04 a7.42 ± 0.05a7.29 ± 0.09c
a mean ± standard deviations (n = 3), Data with the same letter were considered insignificant and data without the same letter were considered significant (significant level α = 0.05).
Table A3. The EOC and TC contents of the control soil and biochar-incorporated soil.
Table A3. The EOC and TC contents of the control soil and biochar-incorporated soil.
ItemsSoilB4B5
TC (%)2.07 ± 0.098 a65.07 ± 9.8941.03 ± 2.71
EOC (%)0.74 ± 0.0197.23 ± 1.8036.60 ± 2.15
EOC/TC (%)35.5611.1289.21
a mean ± standard deviations (n = 3).
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Figure A1. PCA of the bacterial community of soils incorporated with biochar. CK represents the control treatment without any biochar addition; B4 represents 143.36 g·kg−1 rate of the biochar incorporation; B5 represents 238.82 g·kg−1 rate of the biochar incorporation. The first axis explains 72.4% cumulative percentage variance of species and the second axis explains 14.
Figure A1. PCA of the bacterial community of soils incorporated with biochar. CK represents the control treatment without any biochar addition; B4 represents 143.36 g·kg−1 rate of the biochar incorporation; B5 represents 238.82 g·kg−1 rate of the biochar incorporation. The first axis explains 72.4% cumulative percentage variance of species and the second axis explains 14.
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Figure 1. Response of soybean biomass and C content to different biochar incorporation treatments. CK represents the control treatment without any biochar addition; B1, B2, B3, B4, and B5 represent biochar incorporation rates of 9.14 g·kg−1, 23.89 g·kg−1, 47.79 g·kg−1, 143.36 g·kg−1, and 238.82 g·kg−1, respectively. S1, S2 and S3 represent the three incorporation months of May, June, and July. Vertical bars indicate standard deviations of the mean (n = 3). Data with the same letter were considered insignificant and data without the same letter were considered significant (significant level α = 0.05).
Figure 1. Response of soybean biomass and C content to different biochar incorporation treatments. CK represents the control treatment without any biochar addition; B1, B2, B3, B4, and B5 represent biochar incorporation rates of 9.14 g·kg−1, 23.89 g·kg−1, 47.79 g·kg−1, 143.36 g·kg−1, and 238.82 g·kg−1, respectively. S1, S2 and S3 represent the three incorporation months of May, June, and July. Vertical bars indicate standard deviations of the mean (n = 3). Data with the same letter were considered insignificant and data without the same letter were considered significant (significant level α = 0.05).
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Figure 2. Responses of soil enzyme activity (a), soil microbial biomass (b), and soil respiration (c) to different biochar incorporation treatments and months. CK represents the control treatment without any biochar addition; B1, B2, B3, B4, and B5 represent biochar incorporation rates of 9.14 g·kg−1, 23.89 g·kg−1, 47.79 g·kg−1, 143.36 g·kg−1, and 238.82 g·kg−1, respectively. Vertical bars indicate standard deviations of the mean (n = 3). Data with the same letter were considered insignificant and data without the same letter were considered significant (significant level α = 0.05).
Figure 2. Responses of soil enzyme activity (a), soil microbial biomass (b), and soil respiration (c) to different biochar incorporation treatments and months. CK represents the control treatment without any biochar addition; B1, B2, B3, B4, and B5 represent biochar incorporation rates of 9.14 g·kg−1, 23.89 g·kg−1, 47.79 g·kg−1, 143.36 g·kg−1, and 238.82 g·kg−1, respectively. Vertical bars indicate standard deviations of the mean (n = 3). Data with the same letter were considered insignificant and data without the same letter were considered significant (significant level α = 0.05).
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Figure 3. Venn diagram of unique and shared operational taxonomic units (a) and the microbial community relative abundance at the phylum level (b) of the soil incorporated with biochar. CK represents the control treatment without any biochar; B4 represents 143.36 g·kg−1 of biochar incorporation; B5 represents 238.82 g·kg−1 of biochar incorporation.
Figure 3. Venn diagram of unique and shared operational taxonomic units (a) and the microbial community relative abundance at the phylum level (b) of the soil incorporated with biochar. CK represents the control treatment without any biochar; B4 represents 143.36 g·kg−1 of biochar incorporation; B5 represents 238.82 g·kg−1 of biochar incorporation.
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Figure 4. Heatmap of cluster analysis at genus level of the soil incorporated with biochar. CK represents the control treatment without any biochar addition; B4 and B5 represent biochar incorporation rates of 143.36 g·kg−1 and 238.82 g·kg−1. The similarities and differences in the composition of the multiple samples at the classification level are reflected by the color gradient and similarity. Significant effects are noted at the genus level.
Figure 4. Heatmap of cluster analysis at genus level of the soil incorporated with biochar. CK represents the control treatment without any biochar addition; B4 and B5 represent biochar incorporation rates of 143.36 g·kg−1 and 238.82 g·kg−1. The similarities and differences in the composition of the multiple samples at the classification level are reflected by the color gradient and similarity. Significant effects are noted at the genus level.
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Table 1. Microbial biodiversity indices of soils under different rates of biochar incorporation.
Table 1. Microbial biodiversity indices of soils under different rates of biochar incorporation.
TreatmentsSequencesOTUs dChaoACEShannon
CK a50,92329893808.923901.239.85
B4 b67,76534993972.073933.159.94
B5 c70,64531094067.594099.5810.08
a the control treatment without biochar; b soil incorporated with 143.36 g·kg−1 biochar; c soil incorporated with 238.82 g·kg−1 biochar; d operational taxonomic units.
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Xie, M.; Lu, X.; Wang, H.; Fu, X.; Wang, L. Large-Scale Biochar Incorporation Does Not Necessarily Promote the Carbon Sink of Estuarine Wetland Soil. Sustainability 2023, 15, 16709. https://doi.org/10.3390/su152416709

AMA Style

Xie M, Lu X, Wang H, Fu X, Wang L. Large-Scale Biochar Incorporation Does Not Necessarily Promote the Carbon Sink of Estuarine Wetland Soil. Sustainability. 2023; 15(24):16709. https://doi.org/10.3390/su152416709

Chicago/Turabian Style

Xie, Mengdi, Xiaojuan Lu, Han Wang, Xiaohua Fu, and Lei Wang. 2023. "Large-Scale Biochar Incorporation Does Not Necessarily Promote the Carbon Sink of Estuarine Wetland Soil" Sustainability 15, no. 24: 16709. https://doi.org/10.3390/su152416709

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