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Article

Poplar Sawdust Biochar Altered Community Composition of Dominant Soil Fungi but Not Bacteria Depending on Pyrolysis Temperature

by
Yuanyuan Jin
1,
Ye Tian
1,2,*,
Rui Yang
1,
Wenhao Li
1,
Chengyu Liu
1 and
Tong Li
1
1
College of Forestry, Nanjing Forestry University, Nanjing 210037, China
2
Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, China
*
Author to whom correspondence should be addressed.
Forests 2023, 14(6), 1114; https://doi.org/10.3390/f14061114
Submission received: 7 May 2023 / Revised: 24 May 2023 / Accepted: 25 May 2023 / Published: 27 May 2023
(This article belongs to the Section Forest Ecology and Management)
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Abstract

:
There is a growing focus on the production of biochar from organic wastes and its forestry use. However, it is unclear how applying biochar pyrolyzed at different temperatures influences both soil bacterial and fungal communities. In this study, two kinds of biochar were pyrolyzed at 350 °C and 600 °C, from poplar sawdust, and then applied as an auxiliary substrate material (15% addition by volume) for the container seedling cultivation of Cyclocarya paliurus, a native timber and medically used tree species, to compare the response of the soil’s microbial traits. The results showed that after 5 months of cultivation, the addition of the biochar application improved the soil’s physical and chemical properties to a certain extent by decreasing its bulk density and increasing its field water-holding capacity, pH and organic carbon content. The soil’s pH and content of organic C, available N and available P were significantly higher in the substrate with the addition of the biochar pyrolyzed at 600 °C (Bioc600) than in that of the substrate with added pyrolyzed biochar at 350 °C (Bioc350). The biochar application also enhanced the soil’s microbial N (MBN) but showed no changes in the MBC/MBN ratio. The biochar application had no effect on the diversity and composition of the soil’s bacterial community, but showed a certain effect on its fungal community composition and had different influences between low and high pyrolysis temperatures. The relative abundance of several of the dominant fungal phyla and genera increased with the addition of biochar due to the increase in the soil’s pH when compared to the CK (no biochar or sawdust addition). When compared with Bioc350, the dominant phylum Basidiomycota and genus Vanrija further increased in abundance with Bioc600. These findings reveal the consistent effects of biochar pyrolysis temperature and demonstrate the different regulatory roles of biochar application in soil bacterial and fungal communities, providing valuable information on how biochar can effectively be used as a substrate for seedling cultivation.

1. Introduction

Biochar is a solid material obtained from the thermochemical conversion of biomass at temperatures between 300 and 900 °C and under an oxygen-limited environment [1,2]. It is often used as a soil amendment due to its ability to supply nutrients [3,4,5,6] and its stability with regard to being rich in aromatic components [7,8]. Many studies have proven that biochar application can improve the physical properties [9] and moisture conditions [10,11] of soil, maintain soil aggregate structures [12], mediate soil pH [13], increase the nutrient supply and reduce N leaching by increasing the cation exchange capacity [14,15]. Recent studies have paid more attention to the effects of biochar application on soil microflora because soil microorganisms generally participate and control almost all kinds of soil processes. It has been suggested that biochar application could increase soil microbial biomass and diversity [16,17,18] and modulate soil microbial communities [19,20,21,22,23].
However, previous studies have not achieved relatively consistent results, especially in terms of a biochar application’s impact on a soil’s microbial structure. Some research has shown that biochar application could alter the structure of a soil’s core microbial population by affecting the soil’s physicochemical properties and nutrient supply [24,25,26,27,28], but such effects were also inconsistent at different time scales [29,30], and most of the studies generally focused on a soil’s bacterial community while ignoring the soil’s fungal community [30,31]. The inconsistencies of the effects mentioned above were generally considered to be related to the feedstock materials, pyrolysis process and pyrolysis temperatures [31,32,33]. When the feedstock materials and pyrolysis process are kept the same, the pyrolysis temperature is the most important factor affecting the application effect of biochar [34]. Several studies have proven that when the pyrolysis temperature was lower or higher than 500 °C, the structure, physicochemical properties and stability of a prepared biochar varied greatly due to the functions of the biochar as a soil amendment [35,36,37,38]. However, in terms of the effects of biochar pyrolyzed at different temperatures on a soil’s microbial properties, especially with regard to the structure and composition of its microbial community, relevant studies are relatively lacking and thus, its effect is largely unknown [19,39,40].
Poplar (Populus spp.) is the most important fast-growing and high-yielding timber species in the mid-latitude plains of China. The rapid development of poplar plantations and subsequent wood processing have generated large amounts of harvesting and processing residues [41]. Using these residues to produce biochar and in turn applying the biochar for soil amendment can be conducive to the sustainable development of poplar plantations while reducing waste and environmental pollution and can also help achieve carbon neutrality. When using the residues to produce biochar, it is necessary to consider how the pyrolysis temperature affects soil improvement; relevant research is relatively lacking, especially in terms of the pyrolysis temperature’s impact on soil bacterial and fungal community structures after biochar application to the soil.
Therefore, we produced two kinds of biochar using poplar sawdust under low and high pyrolysis temperatures and conducted pot experiments to compare the effects of biochar application on a soil’s properties, as well as on both the soil’s bacterial and fungal community traits. Due to the differences in properties between biochar pyrolyzed under a low or high temperature, we hypothesized that its application would have varied roles in regulating the soil’s bacterial and fungal communities when the soil’s properties were changed. The results of this study will help lead to the effective use of harvesting and processing residues as biochar lead to soil amendment as well as the sustainable development of poplar plantations.

2. Materials and Methods

2.1. Biochar Pyrolysis and Properties

The biochar used in this study was pyrolyzed from poplar sawdust, and the wood processing waste was produced in Weifang City, Shandong Province, at 350 °C (<500 °C) and 600 °C (>500 °C). The main properties of the sawdust and two kinds of biochar are listed in Table 1.
Both of the biochar samples had an obviously larger specific surface area (SSA), total porosity (TPO), pH value and organic carbon (OC) and total nitrogen (TN) content than the poplar sawdust, especially for the biochar pyrolyzed at 600 °C. The C/N ratio of the biochar pyrolyzed at 350 °C was larger, while that of the biochar pyrolyzed at 600 °C was smaller than that of the poplar sawdust.

2.2. Experimental Design for Soil Sampling and Processing

This study was conducted in the greenhouse at the research nursery of Nanjing Forestry University in Baima Township (119°09′ E, 31°35′ N), Nanjing, China. The local climate is affected by subtropical monsoons. The basic substrate was a combination of yellow-brown soil, organic fertilizer and perlite at a volume ratio of 6:1:1. A square plastic container with a top and bottom diameter of 100 mm and 70 mm, respectively, and a height of 100 mm, was used for the seedling cultivation of Cyclocarya paliurus, an important native tree species for both timber and medical use.
In this study, four substrate treatments were designed by adding 15% (v/v) of poplar sawdust biochar pyrolyzed at 350 °C or 600 °C (Bioc350 and Bioc600) and 15% of poplar sawdust raw material (RawMa) to the basic cultivation substrate and using the basic substrate as the control (CK). The substrate weights per container for each treatment were 265 g, 270 g, 255 g and 285 g. The various substrates used for the experiment were prepared and potted in early May 2020 according to the treatments, and the selected seedlings of C. paliurus were uniformly transplanted with one plant in each pot. A completely randomized block design was set up with a total of 3 blocks of 30 containers per treatment in each block. During cultivation, yellow sticky traps were used to prevent pests and disease was prevented by ensuring ventilation. Regular water and weed management was performed, and the position of each treatment in the same block was periodically alternated.
Substrates were sampled in October 2020 from each treatment. Three containers were randomly selected from each treatment in each block for undisturbed soil core sampling and for the subsequent determination of soil bulk density and field water-holding capacity. Another three containers were randomly selected, and a hole punch (100 mm long with an internal diameter of 16 mm) was used to collect soil samples vertically from each container. The soil samples collected from the 3 containers were mixed to make a single composite sample and then were transported to the laboratory. After thoroughly being homogenized and sieved through a 2 mm mesh, the samples were divided into three portions. One portion of the fresh sample was air-dried at room temperature and further passed through a 0.25 mm sieve for the analysis of its pH and soil organic carbon (OC) content, the second portion was stored at −80 °C for the analysis of its microbial community structure and composition, and the third portion was stored at 4 °C for the analysis of its available nitrogen (AN), available phosphorous (AP), available potassium (AK) and soil microbial biomass content.

2.3. Analysis of Soil Physical and Chemical Properties

The analysis of the soil’s physical and chemical properties was carried out with reference to [42], which is briefly described as follows:
Soil bulk density (BD) and field water-holding capacity (FC) were determined using the core method. Soil bulk density was calculated as the ratio of the dry mass of the soil to the total volume of the soil core. For the measurement of the soil field water-holding capacity, the soil core was soaked in water for 24 h until saturated, and then the saturated soil core was placed on a sand plate for 2 days and the moisture content of the soil was determined as the soil field water-holding capacity.
Soil pH was measured using a glass combination electrode (EUTECH Instruments pH700) at a 1:2.5 (w/v) soil-to-solution ratio with CO2-free distilled water.
Soil organic C content (SOC) was detected using an automatic elemental analyzer (Vario Max CN; Elementar, Langenselbold, Germany) via the dry combustion method.
Alkali-hydrolyzed nitrogen (N) was analyzed as the soil’s available N (AN) using a NaOH-hydrolyzing, NH3-diffusing and H3BO3-absorbing method.
Soil available phosphorus (AP) was determined using the Olsen method. Two grams of fresh soil was extracted with 40 mL of a 0.5 mol/L NaHCO3 solution (pH 8.5) and the filtrate was determined with a molybdate-ascorbic acid method using a spectrophotometer (SPECORD 200 PLUS; Analytik Jena, Jena, Germany).
Soil available potassium (AK) was extracted with an ammonium acetate solution and determined using atomic absorption spectrophotometry (AA-7000).

2.4. Analysis of Soil Microbial Biomass

Soil microbial biomass carbon (MBC) and nitrogen (MBN) content was determined using the chloroform fumigation–extraction method [43]. The fresh soil was extracted with a 0.5 M K2SO4 solution at a 1:4 (w/v) soil-to-solution ratio. The content of MBC and MBN was calculated based on the differences in the C or N concentrations from the extracts of fumigated and non-fumigated soils using conversion factors of 2.22 and 5.0, respectively [44,45]. K2SO4-extracted C was analyzed using a total organic C analyzer (TOC-L CPH; Shimadzu, Kyoto, Japan), and N was analyzed with the ninhydrin reaction method [45] using a UV–visible spectrophotometer (SPECORD 200 PLUS; Analytik Jena, Germany).

2.5. Analysis of Soil Microbial Communities

The total genomic DNA of the soil samples was extracted using the CTAB method. After being checked for quality using 1% agarose gel electrophoresis, the diluted genomic DNA was used as the template. The bacterial and fungal community compositions in the soils of each treatment were determined by Illumina MiSeq sequencing. The V3–V4 region of bacterial 16S ribosomal RNA was amplified using the primer 515F-806R. The ITS1 region of the fungal ITS ribosomal RNA was amplified using the primer 1737F-2043R.
PCR products were analyzed by electrophoresis on 2% agarose gel. The qualified PCR products were purified using magnetic beads, quantified with enzyme labeling and then detected via 2% agarose gel electrophoresis. A TruSeq® DNA PCR-Free Sample Preparation Kit was used for library construction. The constructed library was quantified using Qubit and Q-PCR, and the library was sequenced by NovaSeq6000.

2.6. Data Processing and Statistical Analysis

All values are reported as the arithmetic mean ± the standard deviation of three replicates measured on an oven-dried soil basis.
According to the barcode sequence and PCR primer sequence, the sample data were split from the offline data. After the barcode and primer sequences were cut off, the reads of each sample were spliced using FLASH (version 1.2.7) [46] to obtain raw tags. After filtering [47], clean tags were obtained. The tags’ quality control process [48] was carried out in Qiime (version 1.9.1), and the chimeric sequences were removed by comparing them with a species annotation database [49] to obtain effective tags.
Effective tags were clustered into operational taxonomic units (OTUs) with 97% identified using the Uparse algorithm (v7.0.1001) [50]. OTU sequences were annotated and analyzed using the Mothur method with the SILVA138 [51] and SSUrRNA databases [52]. A rapid multiple sequence alignment was performed using MUSCLE (version 3.8.31) [53] to obtain the phylogenetic relationships of the sequences represented by all OTUs. Finally, the subsequent alpha diversity analysis and beta diversity analysis were based on the data after homogenization.
Qiime software (version 1.9.1) was used to calculate the observed OTUs, as well as the Chao 1, Shannon and ACE indices. R software (version 2.15.3) was used to create rarefaction curves and analyze the differences in the alpha and beta diversity indices between groups. The principal component analysis (PCA) plots were made by Origin Pro 2022b and the Pearson correlation coefficient was tested for significance. Analysis of similarity (ANOSIM) was conducted to test the microbial community structure significance between treatments using the data calculated by the Bray–Curtis algorithm. The redundancy analysis (RDA) was performed using CANOCO (version 5.0). One-way analysis of variance (ANOVA) of the soil’s BD, FC, pH, SOC, AN, AP, AK, MBC and MBN was performed with SPSS 26.

3. Results

3.1. Soil Basic Properties

Compared to the CK, the soil’s bulk density was significantly decreased by the poplar sawdust and biochar amendment treatments, while its field water-holding capacity was significantly increased by Bioc600 (Figure 1).
The addition of poplar sawdust and two kinds of biochar significantly increased the soil’s pH and organic C content after 5 months of seedling cultivation (Figure 2). The substrate with the addition of biochar pyrolyzed at 600 °C (Bioc600) showed the highest pH value, while no significant difference in soil pH was found between the Bioc350 and RawMa groups (Figure 2a). The soil’s organic C content between the four substrate treatments was significantly different, with Bioc600, Bioc350 and RawMa being 4.14 times, 3.17 times and 1.65 times higher than the CK, respectively (Figure 2b).
The available N, P and K content of RawMa were the highest, being significantly higher than those of the other three treatments (Figure 3). No significant differences existed in the available N and P content between Bioc350 and Bioc600 compared with the control, but the available N and P content in Bioc600 was significantly higher than in Bioc350 (Figure 3a,b). The available K content was significantly higher in Bioc350 and Bioc600 than in CK, while no significant difference existed between Bioc350 and Bioc600.

3.2. Soil Microbial Biomass

No significant difference existed in the MBC content among the four substrate treatments with Bioc600 having only a slightly higher value (Figure 4a). Meanwhile, for MBN content, the largest value was for RawMa, being significantly higher than that of the other three substrate treatments (Figure 4b). Biochar addition, especially for Bioc600, generally induced a higher MBN content than CK, while there was no significant difference between the pyrolysis temperatures (Figure 4b). Correspondingly, a significant difference existed in the MBC/MBN ratio with the lowest being present in RawMa and the highest in the control while there was no significant difference between the two biochar groups (Figure 4c).

3.3. Sequence Data and Alpha Diversity of Soil Microorganisms

In total, 1,097,080 and 1,176,227 raw sequences were obtained for the bacterial 16S gene and fungal ITS gene, respectively, from all 12 samples. After filtering out the low-quality ones and removing the chimera, there were 56,433 and 61,633 sequences for the bacterial 16S gene and fungal ITS gene per sample, respectively. Through operational taxonomic unit (OTU) clustering at a 97% identity, 8973 and 1725 OTUs of the bacterial and fungal communities were obtained, respectively. Rarefaction curves of the bacterial and fungal communities (Figure 5) showed that each sample tended to be flat when the number of sequences reached 40,000, indicating that the sampling was reasonable and the confidence in the microbial community structure was high.
The indices of alpha diversity (Table 2) were calculated by using the OTUs of each sample. The results showed that no significant difference existed for all the indices of alpha diversity for both the bacterial and fungal communities among the different substrate treatments. However, we still found a slight increase in OTUs and the indices of Shannon, Chao 1 and ACE for the bacterial communities in RawMa, Bioc350 and Bioc600 compared to that in the CK. Generally, there was no difference between Bioc350 and Bioc600, but when compared with RawMa, the addition of biochar showed a slight increase in OTUs and Chao1 and a slight decrease in the Shannon index. Contrarily, for the fungal communities, most of the alpha diversity indices were generally lower in RawMa, Bioc350 and Bioc600 than in the CK, with the lowest OTUs, Chao1 index and ACE index in RawMa and the lowest Shannon index in Bioc600.

3.4. Bacterial and Fungal Community Structures

Variations in the microbial communities of the control and the different substrates with either of the two biochar additions or the poplar sawdust addition were evaluated using principal component analysis (PCA) (Figure 6). OTU-based PCA yielded 40.9% and 54% of the total variability of the first two components for bacterial and fungal communities, respectively. The three replicates of each treatment were generally assembled together. Both the bacterial and fungal communities in RawMa could be distinguished from the other three treatments in the PC2, but at an insignificant level, and the addition of biochar did not lead to a significant difference for the soil microbial community structures. ANOSIM analysis confirmed that there was no significance between the two biochar treatments in both the bacterial (R = 0.04, p = 0.50) and fungal (R = −0.26, p = 0.90) community structures.

3.5. Bacterial and Fungal Community Composition

The OTUs of the bacterial communities were annotated into 82 phyla and 802 genera. The dominant phyla, including Proteobacteria, unidentified_bacteria, Firmicutes, Acidobacteriota, Bacteroidota, Cyanobacteria, Chloroflexota, Verrucomicrobiota, Actinobacteria, Planctomycetota, Myxococcota and Gemmatimonadetes, accounted for 84.5% to 86.6% of the bacterial reads, and the remaining annotated 70 phyla were at relatively low abundance of less than 1% each, accounting for less than 15% of the abundance in total (Figure 7a). For the dominant phyla, the abundance of Bacteroidota was lower in Bioc350 than in the other substrate treatments, and the abundance of Cyanobacteria was significantly lower in Bioc350 and Bioc600 than in the CK and RawMa.
Further taxonomical classification at the genus level revealed that the dominant bacterial genera included Ellin6067, Scytonema_VB-61278, Candidatus_Udaeobacter, RB41, Lachnospiraceae_NK4A136_group, Lactobacillus, Sphingomonas, Ramlibacter, Gemmatimonas, Candidatus_Solibacter, Pseudomonas, Subgroup_10 and Dongia with their relative abundances being higher than 1% in at least one of the soil samples in the four substrate treatments (Figure 7c). The results showed an obvious trend where the proportion of Ellin6067 was the lowest in RawMa, while that of Candidatus_Udaeobacter was highest in Bioc350 among the four substrate treatments. The abundance of Scytonema_VB-61278 was relatively high in the CK (2.7%) and RawMa (1.5%), but less than 1% in Bioc350 (0.3%) and Bioc600 (0.9%). The genus Candidatus_Udaeobacter accounted for more than 1% in the CK (1.8%), Bioc350 (2.1%) and Bioc600 (1.3%), but was only 0.6% in RawMa.
For the fungal community, the OTUs were annotated into 14 phyla and 452 genera. The dominant phyla, including Ascomycota, Basidiomycota, Rozellomycota and Mortierellomycota, accounted for 68.2% to 88.6% of the relative abundances in total, and among them, Ascomycota showed absolute dominance with an occupation of more than 50% of the relative abundances. The remaining 10 annotated phyla were at a relatively low abundance of less than 1% for each sample (Figure 7b). For the dominant phyla, the relative abundances of Ascomycota and Rozellomycota were relatively higher in Bioc350 and Bioc600 than that in the control and RawMa, and the abundance of Basidiomycota was the highest in the CK, while it was relatively low in Bioc350 and Bioc600 and was the lowest in RawMa.
The taxonomical classification at the genus level for the fungal communities showed that the dominant genera generally included Humicola, Pseudallescheria, Chaetomium, unidentified_Schacinales_sp, unidentified_Chaetothyriales_sp, Vanrija, Zopfiella, Fusarium, unidentified_Rozellomycota_sp, Saitozyma, Mortierella and Archaeorhizomyces, with relative abundances higher than 1% in at least one of the soil samples of the four substrate treatments (Figure 7d). The results showed that the proportion of Humicola, Pseudallescheria and unidentified_ Rozellomycota_sp was higher in the substrates with the biochar addition (Bioc350 and Bioc600) than in the RawMa and CK, and the proportion of unidentified_Schacinales_sp was much lower in RawMa (0.92%), Bioc350 (1.51%) and Bioc600 (2.01%) than in the CK (16.24%). It is worth noting that the proportion of Vanrija was the highest in Bioc600, while the relative abundance of Zopfiella was the highest in RawMa, showing great alteration of the compositional structure of the fungal community with the addition of biochar or poplar sawdust.

3.6. Linking Microbial Community Composition to Soil Properties

A redundancy analysis (RDA) was performed to study the relationship between the changed soil properties and soil microbial community compositions of the dominant bacteria and fungi under different substrate treatments. OTU-based RDA yielded 37.94% and 66.97% contributions at the phylum level (Figure 8a,b) and 35.91% and 47.74% contributions at the genus level (Figure 8c,d) for the total variance in the dominant bacterial and fungal communities, respectively, as explained by the first two axes.
The relative abundances of the dominant bacterial phyla of Proteobacteria, Actinobacteria and Myxococcota were positively correlated with the soil bulk density and the content of available K and P; the abundances of Planctomycetota and Chloroflexota were positively correlated with the field water-holding capacity and the abundances of unidentified_bacteria, Acidobacteriota, Verrucomicrobiota and Planctomycetota were negatively correlated with the soil available N content, soil pH and organic C content (Figure 8a). However, none of these correlations reached a significant level (p > 0.1), which indicates that the soil properties that were changed with the addition of poplar sawdust or biochar did not significantly alter the community composition of the dominant bacteria. Meanwhile, for the fungal community composition of the dominant phyla, the permutation test revealed that the soil pH (F = 4.40, p = 0.00), the content of available P (F = 3.2, p = 0.04) and the content of available N (F = 2.8, p = 0.05) accounted for 62.3% of the variance in the soil fungal community composition (Figure 8b) in total. The abundances of Ascomycota and Rozellomycota were significantly positively correlated with the increase in soil pH, while those of Basidiomycota and Mortierellomycota were significantly negatively correlated with it, which can be associated with the application of biochar (Bioc350 and Bioc600). All four dominant fungal phyla were significantly negatively correlated with the content of soil available N and P, which was, in turn, strongly affected by the addition of poplar sawdust. Therefore, at the phylum level, the application of biochar or poplar sawdust showed a greater significant influence on the soil’s fungal community than on its bacterial community.
From the genus aspect, the selected soil properties accounted for 56.9% and 71.6% of the variance in the soil bacterial and fungal composition (Figure 8c,d), respectively, of the dominant genus. Similar to the results obtained on a phylum basis, the permutation test revealed that no significant correlations existed for the bacterial community composition of the dominant genus (p > 0.1). Meanwhile, the soil available N content (F = 2.6, p = 0.02) and soil pH (F = 3.0, p = 0.01) explained 40.3% of the variance in soil microbial community composition of the dominant fungal genus (Figure 8d). The relative abundances of Zopfiella and Chaetomium were positively correlated with soil available N content, and those of Humicola, unidentified_Rozellomycota_sp, Vanrija and Pseudallescheria were significantly positively correlated with soil pH.

4. Discussion

Most previous studies have focused on the effects of biochar application on the physical and chemical properties of soil [54,55,56], and several have taken into account the specific effects of the addition of biochar with different application rates or amounts on the core community of a soil’s microorganisms and its relationship with the soil’s property changes [22,23,57], but few studies have examined the effects of biochar application on the structure and composition of both bacterial and fungal communities at different pyrolysis temperatures. In this research, the addition of biochar reduced the bulk density and increased the field water-holding capacity of the substrate, due to the high porosity and specific surface area of biochar, and increased the pH after 5 months of cultivation, which was consistent with the results of Liang et al. [9]. Generally, according to Zhang et al. [58] and Sheng and Zhu [25], the higher the pyrolysis temperature, the more alkaline the biochar generated in response, which is in line with the results of our study. The soil pH also increased after biochar application in our study, which might have been accompanied by the changes in nutrient cycling [59]. Soil organic carbon significantly increased with the addition of biochar in our study, which was consistent with the results of Zheng et al. [60] and Agegnehu et al. [61]. It has been suggested that the labile carbon in biochar could serve as an effective substrate for microbes [62,63] and thus could improve a soil’s microbial biomass and stabilize its microbial community structure [64,65]. Consistent with the findings from several studies [9,66,67], the results of our research showed that biochar pyrolyzed at 600 °C (Bioc600) led to an increase in soil available N and P content when compared with Bioc350, which suggests that pyrolysis temperature might have potential effects on microbial community structure by affecting soil nutrient availability. Soil microbial biomass, which provides an active nutrient pool in soil, is closely related with soil N mineralization, and the MBC/MBN ratio is generally considered as an indicator of the shift in soil microbial composition [68] and can reflect a soil’s microbial functions [64]. The results in our study showed no significant difference in the MBC and MBC/MBN ratio after biochar addition, which is inconsistent with the results of several studies [29,69]. According to Li et al. [70], this might be due to the low nutrient supply of biochar or the relatively short period of cultivation in our study. Of course, this might also be because of our different application patterns and the properties of the basic substrates we used [71]. Compared to biochar, the poplar sawdust we used in the RawMa treatment generally consisted of abundant, easily decomposed organic matter, which can support more demanding high-substrate microorganisms, such as bacteria, and thus may have led to the relatively high MBN content and low MBC/MBN ratio in the RawMa treatment due to the smaller C/N ratio of bacteria [72].
Different soil microorganisms perform their respective functions, and therefore, the diversity and compositional structure of a soil’s microbial community play important roles in the function of the whole soil environment [68], making them important indicators of soil quality [73]. Our study showed that, compared to the CK, the biochar application had no significant influence on the alpha diversity and structure of the bacterial community, and the dominant soil bacterial phyla in our study were similar to those in the studies of Wang et al. [23], Li et al. [70] and Lei et al. [74]. However, from the RDA analysis (Figure 8a), we found a positive but not significant correlation between the dominant bacterial phylum Bacteroidota and soil available N content. The AN content and the relative abundance of Bacteroidota were the lowest in Bioc350 (Figure 3a and Figure 7a) and were relatively high in RawMa, which indicates that biochar application may possibly still have effects on a soil’s bacterial composition by changing the soil environment to a certain extent. Meanwhile, in contrast to the results from our soil bacterial community analyses, our study revealed that biochar application had a relatively great impact on soil fungal communities, and the effect was somewhat relevant to the pyrolysis temperature of the biochar. The relative abundances of the fungal phyla Ascomycota and Rozellomycota and the fungal genus Humicola, which belongs to the phylum Ascomycota, were higher, while the relative abundance of the fungal phylum Basidiomycota was lower in Bioc350 and Bioc600 than in the CK and RawMa.
Many studies have demonstrated that changes in pH significantly influence a soil’s microbial community [58,75,76,77,78]. In our study, pH showed a positive correlation with the fungal phyla Ascomycota and Rozellomycota and a negative correlation with the fungal phylum Basidiomycota and genus unidentified_Sebacinales_sp (Figure 8), indicating that a shift in the dominant fungal community was caused by the biochar application, which is partly consistent with our hypothesis. However, no changes in bacterial communities due to biochar application were observed.
A soil’s bacterial community plays important roles in organic matter catabolic metabolism and the transformation of C and N [79,80]. The soil bacteria were generally not sensitive to a near neutral soil condition, and the changes in soil pH caused by the biochar application might have affected the bacterial communities by affecting the available nutrient supply [81,82] and the morphological and ionic valence transformation of iron and aluminum in the soil [83,84,85,86]. In our study, the soil available nutrients under the biochar additions only fluctuated slightly compared to the control, and none of them reached a significant level. This might be the reason both Bioc350 and Bioc600 did not show any changes in the diversity and community structure of their bacteria in this study. Unlike bacteria, fungi are more sensitive to a higher pH environment. Rousk et al. [87] found that the population and survival of fungi were inhibited due to bacterial competition under high pH conditions. In this study, the addition of biochar significantly increased the pH of the substrate, resulting in changes in the abundance of some dominant phyla or genera of the fungal community. In addition, the results of this study showed that the addition of poplar sawdust increased the soil N availability, thereby reducing the proportion of some dominant fungal phyla and genera, indicating that the supply of soil available N in addition to pH also affected the community structure of fungi.
Therefore, in order to evaluate the impact of biochar application on soil bacterial and fungal community structure, in addition to the effects caused by the changes in the soil pH and nutrient supply found in this study, more attention needs to be paid to the changes in other environmental factors caused by biochar addition, such as the morphological changes in other ions in the soil, the formation of soil aggregate structure and the possible production of microbial inhibition or promoting factors. From the perspective of seedling cultivation and soil sustainability, we need to pay attention not only to the community structure changes in soil microorganisms, but more importantly, to the changes in microbial functions after biochar addition. In addition, due to the short period after biochar application in this study, monitoring on a longer time scale is needed in the future to effectively evaluate the actual effects of biochar application at different pyrolysis temperatures on the structure and function of soil microbial communities.

5. Conclusions

The application of biochar pyrolyzed at both 350 °C and 600 °C improved soil physiochemical traits to a certain extent, showing a certain ameliorating effect on substrate properties, and the biochar with the higher pyrolysis temperature showed a more prominent nutrient improvement effect. However, the application of biochar did not significantly affect the overall composition of soil microorganisms. From the perspective of the composition of soil bacterial and fungal communities, pyrolyzing biochar at different temperatures basically had no effect on the bacterial communities, but had a certain impact on the composition of dominant fungal phyla and genera which was mainly due to the change in soil pH. On the contrary, the direct application of poplar sawdust significantly increased the soil MBN and decreased the MBC/MBN ratio, which was accompanied by a decrease in soil fungal species and diversity and a shift in microbial composition.

Author Contributions

Y.T. and Y.J. were mainly responsible for the conceptualization, methodology used, data evaluation, data validation and formal analysis. Pot experiment and data collection were conducted by all authors. The original draft of this article was prepared by Y.T. and Y.J. who were also responsible for the review and editing process of this article. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Key Research and Development Program of China (Grant No. 2021YFD2201202).

Data Availability Statement

Data is available upon request to the corresponding author.

Acknowledgments

We acknowledge Jiayu Zhang, Shichao Zhou, Zheng Zhai and Jiaqiu Yuan from Nanjing Forestry University for their laboratory assistance and suggestions to the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. (a) Soil bulk density (BD) and (b) field water-holding capacity (FC) of the substrate with poplar sawdust or biochar addition after 5 months of seedling cultivation. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C. The horizontal bars indicate the standard deviation. Different lowercase letters indicate the significant differences between the substrate treatments at p < 0.05 according to Duncan’s multiple range test.
Figure 1. (a) Soil bulk density (BD) and (b) field water-holding capacity (FC) of the substrate with poplar sawdust or biochar addition after 5 months of seedling cultivation. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C. The horizontal bars indicate the standard deviation. Different lowercase letters indicate the significant differences between the substrate treatments at p < 0.05 according to Duncan’s multiple range test.
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Figure 2. (a) Soil pH and (b) organic C content of the substrate with poplar sawdust or biochar addition after 5 months of seedling cultivation. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C. The horizontal bars indicate the standard deviation. Different lowercase letters indicate the significant differences between the substrate treatments at p < 0.05 according to Duncan’s multiple range test.
Figure 2. (a) Soil pH and (b) organic C content of the substrate with poplar sawdust or biochar addition after 5 months of seedling cultivation. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C. The horizontal bars indicate the standard deviation. Different lowercase letters indicate the significant differences between the substrate treatments at p < 0.05 according to Duncan’s multiple range test.
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Figure 3. The content of the soil’s (a) available N, (b) P and (c) K of the substrates with poplar sawdust or biochar addition after 5 months of seedling cultivation. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C. The horizontal bars indicate the standard deviation. Different lowercase letters indicate the significant differences between the substrate treatments at p < 0.05 according to Duncan’s multiple range test.
Figure 3. The content of the soil’s (a) available N, (b) P and (c) K of the substrates with poplar sawdust or biochar addition after 5 months of seedling cultivation. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C. The horizontal bars indicate the standard deviation. Different lowercase letters indicate the significant differences between the substrate treatments at p < 0.05 according to Duncan’s multiple range test.
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Figure 4. The (a) MBC and (b) MBN content and (c) the MBC/MBN ratio of the substrate with poplar sawdust or biochar addition after 5 months of seedling cultivation. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C. The horizontal bars indicate the standard deviation. Different lowercase letters indicate the significant differences between the substrate treatments at p < 0.05 according to Duncan’s multiple range test.
Figure 4. The (a) MBC and (b) MBN content and (c) the MBC/MBN ratio of the substrate with poplar sawdust or biochar addition after 5 months of seedling cultivation. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C. The horizontal bars indicate the standard deviation. Different lowercase letters indicate the significant differences between the substrate treatments at p < 0.05 according to Duncan’s multiple range test.
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Figure 5. Rarefaction curves of (a) bacterial communities and (b) fungal communities based on observed OTUs of 12 soil samples. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C.
Figure 5. Rarefaction curves of (a) bacterial communities and (b) fungal communities based on observed OTUs of 12 soil samples. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C.
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Figure 6. The compositional structure of (a) bacterial and (b) fungal communities in the substrates with poplar sawdust or biochar addition after 5 months of seeding cultivation as indicated by principal component analysis (PCA). CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C.
Figure 6. The compositional structure of (a) bacterial and (b) fungal communities in the substrates with poplar sawdust or biochar addition after 5 months of seeding cultivation as indicated by principal component analysis (PCA). CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C.
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Figure 7. Relative abundances of dominant (a) bacterial phyla and (b) genera, and (c) fungal phyla and (d) genera in the substrates with poplar sawdust or biochar addition after 5 months of seedling cultivation. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C.
Figure 7. Relative abundances of dominant (a) bacterial phyla and (b) genera, and (c) fungal phyla and (d) genera in the substrates with poplar sawdust or biochar addition after 5 months of seedling cultivation. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C.
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Figure 8. The redundancy analysis of dominant soil (a) bacterial phyla and (b) fungal phyla, and (c) dominant bacterial genera and (d) fungal genera showing the relationship between the changed soil properties and soil microbial community compositions under different substrate treatments. The dominant bacterial phyla included Proteobacteria, unidentified_bacteria, Firmicutes, Acidobacteriota, Bacteroidota, Cyanobacteria, Chloroflexota, Verrucomicrobiota, Actinobacteria, Planctomycetota, Gemmatimonadetes and Myxococcota, and the fungal dominant phyla included Ascomycota, Basidiomycota, Rozellomycota and Mortierellomycota. The dominant bacterial genera included Scytonema_VB-61278, Ellin6067, Candidatus_Udaeobacter, RB41, Lachnospiraceae_NK4A136_group, Lactobacillus, Sphingomonas, Ramlibacter, Gemmatimonas, Candidatus_Solibacter, Pseudomonas, Subgroup_10 and Dongia, and the dominant fungal genera included Humicola, Pseudallescheria, Chaetomium, unidentified_Sebacinales_sp, unidentified_Chaetothyriales_sp, Vanrija, Zopfiella, Fusarium, unidentified_Rozellomycota_sp, Saitozyma, Mortierella and Archaeorhizomyces. The soil properties included soil bulk density (BD), field water-holding capacity (FC), pH, soil organic carbon (SOC), available N (AN), available P (AP) and available K (AK). Red and dashed arrows indicate soil properties, blue and solid arrows indicate microbial phyla, and colored circles indicate sample groups. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C.
Figure 8. The redundancy analysis of dominant soil (a) bacterial phyla and (b) fungal phyla, and (c) dominant bacterial genera and (d) fungal genera showing the relationship between the changed soil properties and soil microbial community compositions under different substrate treatments. The dominant bacterial phyla included Proteobacteria, unidentified_bacteria, Firmicutes, Acidobacteriota, Bacteroidota, Cyanobacteria, Chloroflexota, Verrucomicrobiota, Actinobacteria, Planctomycetota, Gemmatimonadetes and Myxococcota, and the fungal dominant phyla included Ascomycota, Basidiomycota, Rozellomycota and Mortierellomycota. The dominant bacterial genera included Scytonema_VB-61278, Ellin6067, Candidatus_Udaeobacter, RB41, Lachnospiraceae_NK4A136_group, Lactobacillus, Sphingomonas, Ramlibacter, Gemmatimonas, Candidatus_Solibacter, Pseudomonas, Subgroup_10 and Dongia, and the dominant fungal genera included Humicola, Pseudallescheria, Chaetomium, unidentified_Sebacinales_sp, unidentified_Chaetothyriales_sp, Vanrija, Zopfiella, Fusarium, unidentified_Rozellomycota_sp, Saitozyma, Mortierella and Archaeorhizomyces. The soil properties included soil bulk density (BD), field water-holding capacity (FC), pH, soil organic carbon (SOC), available N (AN), available P (AP) and available K (AK). Red and dashed arrows indicate soil properties, blue and solid arrows indicate microbial phyla, and colored circles indicate sample groups. CK, no biochar or poplar sawdust addition; RawMa, 15% addition (volume ratio) of poplar sawdust; Bioc350, 15% addition (volume ratio) of biochar pyrolyzed under 350 °C; Bioc600, 15% addition (volume ratio) of biochar pyrolyzed under 600 °C.
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Table
Table 1. The basic traits of the poplar sawdust and biochar pyrolyzed at 350 and 600 °C. SSA, TPO, OC and TN refer to the specific surface area, total porosity, organic C content and total N content, respectively. Different lowercase letters in each column indicate significant differences between the treatments at p < 0.05 according to Duncan’s multiple range test. The data are presented as the mean ± standard deviation (SD).
Table 1. The basic traits of the poplar sawdust and biochar pyrolyzed at 350 and 600 °C. SSA, TPO, OC and TN refer to the specific surface area, total porosity, organic C content and total N content, respectively. Different lowercase letters in each column indicate significant differences between the treatments at p < 0.05 according to Duncan’s multiple range test. The data are presented as the mean ± standard deviation (SD).
MaterialPyrolysis Temperature
(°C)		SSA
(m2/g)		TPO
(cm3/g)		pHOC
(g/kg)		TN
(g/kg)		C/N Ratio
Poplar sawdust–1.810.0036.84 ± 0.18 c45.5 ± 0.06 c0.17 ± 0.00 b267.8 ± 10.8 b
Biochar3502.180.0037.43 ± 0.01 b74.1 ± 0.32 b0.19 ± 0.01 b385.4 ± 21.0 a
600147.150.089.82 ± 0.31 a87.0 ± 0.43 a0.41 ± 0.04 a211.2 ± 12.5 c
Table
Table 2. Alpha diversity at a depth of 56,433 and 61,633 sequences per sample for bacterial and fungal communities. Values are expressed as the mean ± standard deviation. Different lowercase letters in each column indicate significant differences between the treatments at p < 0.05 according to Duncan’s multiple range test.
Table 2. Alpha diversity at a depth of 56,433 and 61,633 sequences per sample for bacterial and fungal communities. Values are expressed as the mean ± standard deviation. Different lowercase letters in each column indicate significant differences between the treatments at p < 0.05 according to Duncan’s multiple range test.
TreatmentBacterial 16SFungal ITS
OTUsShannonChao 1ACEOTUsShannonChao 1ACE
CK3426 ± 266 a9.74 ± 0.20 a3899 ± 441 a3951 ± 414 a512 ± 52 a4.20 ± 0.35 a607 ± 53 a619 ± 55 a
RawMa3569 ± 343 a10.12 ± 0.16 a3966 ± 194 a4227 ± 227 a413 ± 45 a4.32 ± 0.24 a444 ± 57 a454 ± 56 a
Bioc3503661 ± 196 a9.94 ± 0.08 a4152 ± 110 a4228 ± 154 a511 ± 61 a4.07 ± 0.42 a613 ± 67 a613 ± 67 a
Bioc6003645 ± 152 a9.91 ± 0.05 a4187 ± 658 a4174 ± 386 a465 ± 40 a3.71 ± 0.16 a560 ± 37 a559 ± 43 a
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MDPI and ACS Style

Jin, Y.; Tian, Y.; Yang, R.; Li, W.; Liu, C.; Li, T. Poplar Sawdust Biochar Altered Community Composition of Dominant Soil Fungi but Not Bacteria Depending on Pyrolysis Temperature. Forests 2023, 14, 1114. https://doi.org/10.3390/f14061114

AMA Style

Jin Y, Tian Y, Yang R, Li W, Liu C, Li T. Poplar Sawdust Biochar Altered Community Composition of Dominant Soil Fungi but Not Bacteria Depending on Pyrolysis Temperature. Forests. 2023; 14(6):1114. https://doi.org/10.3390/f14061114

Chicago/Turabian Style

Jin, Yuanyuan, Ye Tian, Rui Yang, Wenhao Li, Chengyu Liu, and Tong Li. 2023. "Poplar Sawdust Biochar Altered Community Composition of Dominant Soil Fungi but Not Bacteria Depending on Pyrolysis Temperature" Forests 14, no. 6: 1114. https://doi.org/10.3390/f14061114

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