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Article

Trichoderma Bio-Fertilizer Decreased C Mineralization in Aggregates on the Southern North China Plain

by
Lixia Zhu
,
Mengmeng Cao
,
Chengchen Sang
,
Tingxuan Li
,
Yanjun Zhang
,
Yunxia Chang
and
Lili Li
*
College of Life Science and Agronomy, Zhoukou Normal University, Zhoukou 466001, China
*
Author to whom correspondence should be addressed.
Agriculture 2022, 12(7), 1001; https://doi.org/10.3390/agriculture12071001
Submission received: 9 June 2022 / Revised: 4 July 2022 / Accepted: 8 July 2022 / Published: 11 July 2022
(This article belongs to the Special Issue Soil Carbon and Microbial Processes in Agriculture Ecosystem)
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Abstract

:
Trichoderma bio-fertilizer is widely used to improve soil fertility and carbon (C) sequestration, but the mechanism for increasing C accumulation remains unclear. In this study, effects of Trichoderma bio-fertilizer on the mineralization of aggregate-associated organic C were investigated in a field experiment with five treatments (bio-fertilizer substitute 0 (CF), 10% (BF10), 20% (BF20), 30% (BF30) and 50% (BF50) chemical fertilizer nitrogen (N)). Aggregate fractions collected by the dry sieving method were used to determine mineralization dynamics of aggregate-associated organic C. The microbial community across aggregate fractions was detected by the phospholipid fatty acid (PLFA) method. The results indicated that Trichoderma bio-fertilizer increased organic C stock across aggregate fractions and bulk soil compared with CF. Cumulative mineralization of aggregate-associated organic C increased with the increasing bio-fertilizer application rate. However, the proportion of organic mineralized C was lower in the BF20 treatment except for <0.053 mm aggregate. Moreover, the PLFAs and fungal PLFA/bacterial PLFA first increased and then decreased with increasing bio-fertilizer application rates. Compared with CF, the increases of bacteria PLFA in >2 mm aggregate were 79.7%, 130.0%, 141.0% and 148.5% in BF10, BF20, BF30 and BF50, respectively. Similarly, the PLFAs in 0.25–2, 0.053–0.25 and <0.053 mm aggregates showed a similar trend to that in >2 mm aggregate. Bio-fertilizer increased the value of fungi PLFA/bacteria PLFA but decreased G+ PLFA/G− PLFA, and BF20 shared the greatest changes. Therefore, appropriate Trichoderma bio-fertilizer application was beneficial to improving soil micro-environment and minimizing risks of soil degradation.

1. Introduction

Increasing carbon (C) sequestration in cropland has been recognized as an effective way to reduce CO2 emissions, improve soil structure and promote soil microbial diversity [1,2]. Though protected from microbial decomposition [3], organic C in each aggregate fraction could be affected by agronomic practices (i.e., bio-fertilizer application). Furthermore, the inherent heterogeneity of microbes existing in different aggregate fractions was also influenced by organic material application [2]. Generally, soil aggregate fractions would affect the soil microbial diversity, while soil C contributed to the microbial community structure [4,5]. However, sequestration of soil organic carbon (SOC) was closely related to the C input and output, which were affected by the microbial mineralization of organic materials. Clay soil with high SOC content was more vulnerable to decomposition, showing that dynamics of SOC might also be affected by soil texture which was influenced by aggregate fraction [6]. Therefore, evaluating the sequestration and mineralization of organic C in aggregate fractions and its related microbial community is vital for a deeper understanding of soil C stability.
Studies have demonstrated that long-term fertilization significantly affected SOC stability in different aggregate fractions [7,8,9], and mineralization of organic C would vary with soil aggregates [6,10]. The mineralization of C in small aggregates was vulnerable to soil conditions in an experiment in which soil types concluded Alfisols, Inceptisols, Mollisols and Ultisols [11]. Reeves et al. [12] showed that the mineralization of C in micro-aggregates was higher in Vertisol, while Wang et al. [13] found an opposite trend in the soil of Udic Ferralsols. No difference in organic C mineralization between different aggregate fractions was also observed in Dermosols [14]. Such diverse results clearly indicated that mineralization of aggregate-associated organic C varied with soil profiles. Soil microbes, the driving force of organic C decomposition, were affected by soil textures and aggregate class [13,15]. Therefore, it is important to investigate changes in soil microbial community across aggregate fractions to deeply understand soil C stability. Generally, organic materials clearly increased fungi decomposing biosolids and decreased the abundance of CO2-emission-related fungi [16]. However, little is known about variations of soil microbial community in aggregate fractions and how different classes of aggregates protect and sequester C in soil cultivated with Trichoderma bio-fertilizer.
The winter wheat-summer maize cropping system is the major planting pattern in the North China Plain (NCP), which occupies around 16 M ha [17]. The Shajiang Calci-Aquic Vertosol, an important soil resource, is widely distributed in the southern NCP. However, research information is lacking about the mineralization of aggregate-associated organic C in this area. Thus, this study was conducted to investigate (1) the aggregate distribution and aggregate-associated organic C under the dry sieving method, (2) the mineralization dynamics of C in aggregates in soil treated with bio-fertilizer and (3) the soil microbial community within aggregate fractions in Shajiang Calci-Aquic Vertosol. We hope this research will provide fundamental evidence to strengthen the understanding of microbial regulation of C dynamics across aggregate fractions and guide appropriate bio-fertilizer application in the southern NCP.

2. Materials and Methods

2.1. Study Area and Experimental Design

The study was conducted in Xiping county in 2018 in the southern NCP, China (N 113°12′, E 33°27′, with an altitude of 64 m above sea level), with a mean annual precipitation of 786 mm. The field had been cultivated for more than 50 years before this study started. The mean annual temperature is 14.7 °C, and the sunshine duration has been 2181 h over the past 50 years. Based on the Chinese Soil Taxonomy, the soil in this area is classified as a Shajiang Calci-Aquic Vertosol with a pH value of 6.9. The soil bulk density, SOC, total nitrogen (TN), mineral nitrogen, available phosphorus and available potassium of the 0–20 cm depth are 1.31 g cm−3, 9.4 g kg−1, 0.88 g kg−1, 14.38 mg kg−1, 6.06 mg kg−1 and 179.23 mg kg−1, respectively.
Five treatments were included in this experiment: CF (100% chemical fertilizer N), BF10 (chemical fertilizer N supplemented with 10% Trichoderma bio-fertilizer N), BF20 (chemical fertilizer N supplemented with 20% Trichoderma bio-fertilizer N), BF30 (chemical fertilizer N supplemented with 30% Trichoderma bio-fertilizer N) and BF50 (chemical fertilizer N supplemented with 50% Trichoderma bio-fertilizer N). Each treatment received the same amounts of N, P2O5 and K2O (220, 90 and 90 kg ha−1, respectively) during the maize growing season. The chemical fertilizers were urea (N 46%), calcium super phosphate (P2O5 12%) and potassium sulphate (K2O 51%). The nitrogen, phosphorus and potassium contents of Trichoderma bio-fertilizer were deducted and supplemented with corresponding chemical fertilizer in each treatment. The details of the Trichoderma bio-fertilizer were listed in Zhu et al. [9]. Fermented with wheat straw, the bio-fertilizer had approximately 2 × 108 colony forming units per gram of Trichoderma asperellum ACCC30536, with 297.2 g kg−1 organic matter and 120.1 g kg−1 total nitrogen. Both the Trichoderma bio-fertilizer and chemical fertilizer were spread evenly on the surface of each plot and thoroughly mixed with the top 0–20 cm layer by a rotary cultivator a week before sowing the maize. Summer maize in each plot was planted at a density of 65,000 plants ha−1 in early June and harvested in early October each year.

2.2. Soil Sampling and Analysis

Soil cores were sampled after the maize harvest in October 2020. Five random soil cores from the top 20 cm layer of each plot were taken and mixed thoroughly as one composite sample. Visible materials were removed and stored at 4 °C before analysis. Subsamples of 300 g were shaken on a motorized vibratory sieve-shaker (8411; Zhejiang Chenxin Machine Equipment Co., Ltd., Shaoxing, China) for 3 min with a mesh size of 2, 0.25 and 0.053 mm to obtain four size fractions: >2, 0.25–2, 0.053–0.25 and <0.053 mm.
The incubation experiment was prepared as follows: 30 g samples of the four aggregate fractions were incubated in 500 mL buckets at 25 °C and at 60% water holding capacity for 60 days. The released CO2 was trapped in NaOH solution and determined after 5, 10, 15, 20, 30 and 60 days. The trapped CO2 was precipitated with 1.0 mol L−1 BaCl2 and then titrated with standard 0.1 mol L−1 HCl to quantify the released CO2. Cumulative mineralized CO2-C was used for comparison between aggregate size classes and fertilization treatments.
The PLFAs were extracted and identified according to Bligh and Dyer [18]. Fatty acid methylesters were analyzed using an Agilent 6850 system (Agilent Technologies, Palo Alto, CA, USA), equipped with a DP-5MS capillary column (25 m × 200 μm, i.d. 0.33 μm). Assignment of microbial categories to the various PLFA biomarkers was based on Luo et al. [19].

2.3. Data Analyses

The aggregate stability was determined by mean weight diameter (MWD), and MWD was calculated with the following equation:
MWD = ∑(XiWi)
Of which Xi was the mean diameter of the class (mm), and Wi was the proportion of each aggregate class in relation to the weight of the soil samples.
Total respiration was calculated with the CO2-C produced from each aggregate class (CO2Agg) and the mass of each aggregate class (MAgg) in the total soil mass (SM), according to Xie et al. [15]:
Total respiration (mg C kg−1) = CO2 Agg × MAgg/SM × 100
The contribution of organic C mineralization of each aggregate fraction to bulk soil was calculated with the ratio of cumulative CO2-C production of each aggregate multiplied by the mass of each aggregate fraction/total mineralization of organic C in bulk soil.

2.4. Statistical Analysis

For each of these variables, a mean value was obtained from the results for the three composite samples, significant differences between the means were identified by performing a one-way analysis of variance (ANOVA), and the least significant difference (LSD) was computed to compare the means of the above variables (p < 0.05) using the statistical package SPSS 19.0. Statistical correlations between mineralization of organic C and microbial community were assessed with correlation analysis, and Pearson correlation coefficients were presented. Prior to analysis, data were tested to ensure that they met homogeneity of variance and normality requirements. All the figures were accomplished with SigmaPlot 12.0 (Systat Software Inc., London, UK).

3. Results

3.1. Distribution of Soil Aggregates

Soil aggregate distribution was significantly affected by the bio-fertilizer application. As the dominant fraction, >2 mm aggregate accounted for 34.90% in CF treatment and for 48.94% in BF20 treatment. The proportion of 0.25–2 mm aggregate ranged from 26.08% (CF) to 36.60% (BF20) (Table 1). For the >2 mm aggregate, the highest value was recorded in BF20, followed by BF30, BF50, BF10 and CF. Compared with CF, the increases of >2 mm aggregate were 18.70%, 40.22%, 35.97% and 32.75% in BF10, BF20, BF30 and BF50, respectively (p < 0.05). No significance was observed among BF20, BF30 and BF50 in >2 mm aggregate. Additionally, bio-fertilizer significantly increased the content of 0.25–2 mm aggregate, while BF20, BF30 and BF50 showed no difference between each other. Differently, the distribution of 0.053–0.25 mm aggregate showed a trend of CF > BF10 > BF20 = BF30 = BF50. Bio-fertilizer significantly decreased the content of <0.053 mm aggregate, and no difference was observed among the four bio-fertilizer treatments. Moreover, bio-fertilizer significantly increased MWD and the increase of MWD in BF20 was the highest (35.6%). Trichoderma bio-fertilizer promoted the formation of macro-aggregate (>0.25 mm) in soil but decreased proportions of micro-aggregate (0.053–0.25 mm) and clay (<0.053 mm), and then increased soil aggregate stability.

3.2. Organic C in Bulk Soil and Aggregate Fractions

As shown in Figure 1, the aggregate-associated organic C was significantly affected by the bio-fertilizer application and aggregate size. Compared with CF, organic C in aggregates of >2, 0.25–2, 0.053–0.25 and <0.053 mm were significantly increased by 11.82%, 11.98%, 10.86% and 11.81% in BF10, respectively. The organic C in aggregates of >2, 0.25–2, 0.053–0.25 and <0.053 mm in BF20 was 18.15%, 18.60%, 17.75%, and 18.46% higher than that in CF, respectively. The increases of organic C in >2, 0.25–2, 0.053–0.25 and <0.053 mm aggregate fractions were 17.85%, 18.08%, 17.15% and 18.04% in BF30, and the increases were 17.99%, 18.31%, 17.15% and 17.74% in BF50, respectively, relative to CF. No difference in aggregate-associated organic C was observed in >2, 0.25–2 and 0.053–0.25 mm aggregate fractions among BF20, BF30 and BF50. Obviously, the organic C in <0.053 mm aggregate in BF50 was significantly lower than that in BF20.

3.3. Mineralization of Organic C in Aggregate

The mineralization dynamics of aggregate-associated organic C were noticeably affected by Trichoderma bio-fertilizer application, especially in the first 15 days (Figure 2), and then the mineralization rates were relatively low and remained stable. The BF50 treatment yielded the highest mineralization rate, and the lowest value was recorded in CF treatment across aggregate fractions and bulk soil. The >2 mm aggregate produced the highest amount of CO2-C, and the aggregate of <0.053 mm yielded the lowest value.
After 60 days of incubation, the cumulative mineralization of aggregate-associated organic C in the five treatments differed from each other (Figure 3a). The >2 mm aggregate shared the highest CO2-C among the five treatments, while 0.25–2 and 0.053–0.25 mm aggregate fractions produced similar amounts of CO2-C. The CO2-C yielded from the <0.053 mm aggregate was the lowest among the four aggregate fractions. Compared with CF, the highest values of CO2-C were recorded in the BF50 treatment across aggregate fractions. Increases of CO2-C in BF50 were 121.00% (>2 mm), 21.97% (0.25–2 mm), 35.18% (0.053–0.25 mm) and 77.66% (<0.053 mm) relative to CF, respectively. The bulk soil respired 130.28, 188.35, 244.37, 288.16 and 314.59 mg C kg−1 soil in CF, BF10, BF20, BF30 and BF50, respectively (Figure 3b). Further analysis showed that the mineralization rate of organic C was generally similar for CF and BF10, while a significantly lower value was observed in BF20 relative to CF (Table 2). There was no difference between BF20, BF30 and BF50 in aggregate fractions of 0.25–2, 0.053–0.25 and <0.053 mm. However, the highest mineralization rate was observed in BF50 treatment in bulk soil.

3.4. Microbial Community Composition in Aggregate

Trichoderma bio-fertilizer significantly increased the PLFAs of total microbes, bacteria, fungi, actinomycetes, G+ bacteria and G− bacteria across aggregate fractions and bulk soil (Figure 4). Total PLFA and bacteria PLFA in each aggregate fraction and bulk soil increased with increasing bio-fertilizer application rate, and BF50 yielded the highest PLFAs. Compared with CF, increases of bacteria PLFA in >2 mm fraction were 79.7%, 130.0%, 141.0% and 148.5% in BF10, BF20, BF30 and BF50; increases of fungi PLFA were 108.4%, 163.3%, 172.9% and 195.2%. Actinomycetes PLFAs were increased by 20.9%, 20.4%, 29.6% and 54.4% in BF10, BF20, BF30 and BF50, respectively, relative to CF. Increases of G+ PLFA reached 34.0%, 44.1%, 54.1% and 61.1% in BF10, BF20, BF30 and BF50, respectively, relative to CF. Additionally, G− PLFAs were enhanced by 22.5%, 34.3%, 38.8% and 45.5% in BF10, BF20, BF30 and BF50, respectively, in comparison with CF. The PLFAs in 0.25–2, 0.053–0.25 and <0.053 mm aggregate fractions showed a similar trend to that in >2 mm aggregate fraction.
The soil microbial community diversity was significantly affected by Trichoderma bio-fertilizer application and aggregate fractions (Table 3). No significance of Shannon index H was observed among treatments in >2 and 0.25–2 mm aggregate fractions. Compared with CF, BF30 and BF50 significantly decreased H by 11.72% and 10.94% in 0.053–0.25 mm aggregate and decreases of H were 8.00% and 4.80% in <0.053 mm in BF30 and BF50 treatments, respectively. Bio-fertilizer significantly decreased values of H in bulk soil, and the lowest H value was observed in BF30. Bio-fertilizer significantly increased the value of fungi PLFA/bacteria PLFA, and the highest value was recorded in BF30 in >2 mm aggregate fraction. Differently, BF20 yielded the highest value of fungi PLFA/bacteria PLFA in 0.25–2, 0.053–0.25 and <0.053 mm aggregates and bulk soil. BF10, BF20 and BF50 significantly increased values of G+ PLFA/G− PLFA, and the increases were 9.71%, 6.80% and 8.74%, respectively, relative to CF. No difference in G+ PLFA/G− PLFA was observed between CF and BF30 in >2 mm aggregate. Notably, decreases of G+ PLFA/G− PLFA in BF20 were the most in 0.25–2, 0.053–0.25 and <0.053 mm aggregate fractions and bulk soil relative to CF.
As shown in Table 4, aggregate-associated organic C was significantly positively correlated with bacteria PLFA (R = 0.865, p < 0.01) and fungi PLFA (R = 0.881, p < 0.01), but was significantly negatively correlated with G+ PLFA/G− PLFA (R = −0.450, p < 0.05) and H (R = −0.665, p < 0.05). A significant positive correlation was observed between aggregate distribution and fungi PLFA (R = 0.141, p < 0.05). However, there was no correlation between mineralization of aggregate-associated organic C and microbial community.

4. Discussions

4.1. Trichoderma Bio-Fertilizer Changed Aggregate Distribution and Its Associated Organic C Content

Generally, both wet and dry sieving methods are used to assess soil aggregate conditions. However, dissolved organic matter in soil would lose, and the habitat of microbes would be damaged when aggregates are sieved by the wet sieving method [13]. Therefore, it would be more convictive to assess the change of aggregate-associated organic C in soil using the dry sieving method.
Our results showed that Trichoderma bio-fertilizer improved the aggregation capacity of macro-aggregates (>0.25 mm), consistent with the results of Zhu et al. [9]. Wang et al. [20] also found that the proportion of 0.20–2.00 mm aggregate fraction increased, but the <0.002 mm aggregate fraction decreased after bio-fertilizer application, bio-fertilizer significantly promoted the formation of large aggregates. This might be due to the fact that amounts of fungi introduced by bio-fertilizer promoted the decomposition of soil organic matter and the formation of organo-mineral materials [2,21]. Higher soil microbial biomass after bio-fertilizer application might also promote soil aggregation [9]. Negatively charged polysaccharides and polyuronic acid, along with the growth of bacteria, were beneficial for clay bounding in soil [22], and cementation of organic matter in soil contributed to the formation of macro-aggregates. Increases of macro-aggregates protected labile C from microbial mineralization, which in turn promoted stabilization of soil aggregate [23]. Therefore, a decrease in physical protection caused by the destruction of macro-aggregates had negative effects on labile C, causing organic C mineralization [24].
Application of bio-fertilizer markedly increased soil organic C stock in bulk soil and almost each aggregate fraction, and macro-aggregate contained higher organic C than micro-aggregate. However, an opposite trend was observed by Xie et al. [15], who conducted a field experiment on Anthrosols. Diverse results among studies might be attributed to variations in binding agents during soil aggregation. Generally, increases in aggregate-associated organic C are in line with classes of aggregate fractions since organic matter is the major binding agent [25]. The organic C content was significantly higher in bio-fertilizer treatments than in CF treatment across aggregate fractions, and the BF20 treatment shared higher values. When organic material was applied, plant growth and soil microbes were both promoted [9,26], which in turn increased aggregate-associated organic C. The photosynthetic activities of algae species after bio-fertilizer application would also contribute to increasing aggregate-associated organic C [27]. Consistent with Yilmaz and Snmez [28], our results also showed that bio-fertilizer application increased organic C across aggregate fractions relative to the chemical fertilizer alone treated soil. In addition, aggregate-associated organic C was at a similar level among bio-fertilizer treatments. However, Wang et al. [20] observed that increases of organic C in macro-aggregate were higher than that in micro-aggregate after bio-fertilizer application. The diverse results suggested that soil type would be an inevitable factor in the sequestration of organic C in aggregates.
Most studies reported a linear relationship between organic C and organic materials addition rates [6,29,30]. However, in our study, organic C in aggregate fractions and bulk soil significantly increased when the bio-fertilizer application rate was below 20 t ha−1, while the increase was not significant when the bio-fertilizer application rate was above it. Thus, there was a threshold effect of the bio-fertilizer application on aggregate-associated organic C in the given soil.

4.2. Mineralization of Organic C in Aggregates

It is known that the rate of organic C respiration is an effective index to assess the capability of soil C sequestration. In the present study, significantly higher CO2-C in >2 mm aggregate was recorded. The mineralization rate of organic C in >2 mm aggregate was also significantly higher across aggregate fractions in bio-fertilizer-treated soil. These results were in line with that of Mustafa et al. [8], who recorded higher C mineralization per unit of organic C in macro-aggregate. Similarly, Kan et al. [6] found that organic C in macro-aggregate was the main source of mineralized C, of which >2 mm aggregate contributed 38.2–43.6% to the cumulative mineralization. This might be due to the fact that macro-aggregates dominated the bulk soil (>2 mm aggregate occupies 34.90–48.94% and 0.25–2 mm aggregate occupies 26.08–36.60% in the present study). Organic C in macro-aggregate, mainly originated from plant materials, was more labile. Additionally, larger pores in macro-aggregate increased the transposition of oxygen and microbial activities, which promoted the process of organic C mineralization in macro-aggregate. In the case of Anthrosols, Xie et al. [15] found greater CO2-C produced from micro-aggregate than macro-aggregate, suggesting that mineralizable C in micro-aggregate was much higher than that in macro-aggregate. However, Rabbi et al. [31] showed that there was no difference in organic C mineralization between macro-aggregate and micro-aggregate in Oxisols. Thus, mineralization of aggregate-associated organic C might be a better reflection of C sequestrated in aggregates. Generally, organic C in micro-aggregate was relatively stable for soil in which organic C dominated soil aggregation [32].
When compared with CF, the cumulative mineralization of organic C in aggregates and bulk soil significantly increased with increasing bio-fertilizer application rates. This might be due to the fact that bio-fertilizer application enhanced amounts of available nutrients and promoted microbial activities, which both contributed to the mineralization of organic C [33,34]. Similarly, Xie et al. [15] showed that manure application significantly increased the mineralization of aggregate-associated organic C, and that proportions of organic C mineralized were also similar in the surface layer. Notably, BF20 treatment shared a significantly lower rate of organic C respiration across aggregate fractions (except for <0.053 mm aggregate). The result might indicate that the bio-fertilizer application rate was an important factor in regulating the mineralization of aggregate-associated organic C. The decreased C mineralization in bio-fertilizer application treatments, especially in BF20, might be explained by the dilution effect. Namely, the significant increase of organic C mineralization was diluted by the large increase of aggregate-associated organic C. Generally, organic C in aggregate fractions and bulk soil in the BF20 treatment was more resistant to mineralization, which would be beneficial for soil C sequestration.

4.3. Bio-Fertilizer Alter Microbial Community in Aggregates

PLFA can well reflect changes in soil microbial communities influenced by fertilization. Our study showed that bio-fertilizer significantly increased total PLFA and each microbial group PLFA across aggregates and in bulk soil. Amounts of organic material introduced into the soil would provide extra nutrients and energy to soil microbes, which might directly increase the PLFAs of soil microorganisms within aggregates [35]. This was confirmed by the significant positive correlations between PLFAs and aggregate-associated organic C. In line with the results of Jiang et al. [36], our results also showed that total PLFA, bacteria PLFA and fungi PLFA in macro-aggregate were greater than that in micro-aggregate. It might be that levels of organic C and soil microbes were relatively low in micro-aggregates compared to those in macro-aggregates and that the turnover rate of C was slow. Differently, Wang et al. [37] showed that PLFAs of bacteria and fungi in macro-aggregate were significantly increased by manure application while no significant difference was observed in micro-aggregate. Due to the heterogeneity of soil properties, differences in microbial community composition across aggregate fractions would appear. Aggregates with larger particle sizes supported higher nutrient levels, which were conducive to microbial colonization [2,38].
Generally, bio-fertilizer high in C/N ratio would be more beneficial to fungal growth [39], which led to increased fungi PLFA/bacteria PLFA. In addition, significant changes in bacterial PLFA and fungal PLFA represented variations in soil microbial community, though bacteria were the dominant group among different treatments. It was believed that the higher ratio of fungi PLFA to bacteria PLFA indicated a more stable soil ecosystem and better soil quality [40]. The higher fungi PLFA/bacteria PLFA in BF20 treatment suggested that appropriate bio-fertilizer application helped maintain the stability of the soil ecosystem. Our results showed that bio-fertilizer significantly increased contents of >0.25 mm aggregates and its fungi PLFA, suggesting that fungi contributed to the formation of macro-aggregate and soil aggregate stability via filamentous growth and excretion production [41]. Thus, bio-fertilizer could increase the content of macro-aggregate by promoting fungal growth, and fungi were important factors for bio-fertilizer to promote the formation of macro-aggregates. Additionally, fungi could decompose foreign nutrients through hyphal movement and had high assimilation efficiency of C source, while bacteria did not have this advantage. However, extra organic material usually promoted the growth of G− bacteria, which preferred plant-derived carbon sources, while the G+ community usually participated in organic matter and litter decomposition [42]. A lower G+ PLFA/G− PLFA meant a better soil nutritional condition [43]. Thus, decreased G+ PLFA/G− PLFA after bio-fertilizer application indicated that the soil environment shifted to more eutrophic conditions. In addition, the fact that the ratio of G+ PLFA/G− PLFA was negatively correlated with aggregate-associated organic C also indicated the improved soil quality after bio-fertilizer application. Therefore, the bio-fertilizer application was beneficial to improving soil nutrient status and ecological buffer capacity of large aggregates in the farmland ecosystem. Though the mineralization of aggregate-associated organic C was positively correlated with fungi, Trichoderma was not distinguished from fungi in the present study. The abundance of specific microorganisms was also not assessed, which played vital roles in organic carbon turnover. Thus, further studies focusing on the effects of bio-fertilizer on soil microbial community composition are needed, which may help to develop an environmental bio-fertilizer application pattern in agricultural production.

5. Conclusions

Bio-fertilizer considerably increased proportions of macro-aggregate, organic C sequestration and microbial PLFAs across aggregate fractions and bulk soil. The increase of MWD in BF20 reached 35.6%, significantly higher than other treatments. Bio-fertilizer increased the fungi PLFA/bacteria PLFA but decreased G+ PLFA/G− PLFA, and the BF20 shared the greatest changes. Increases of aggregate-associated organic C of >2, 0.25–2, 0.053–0.25 and <0.053 mm in BF20 were 18.15%, 18.60%, 17.75% and 18.46%, respectively, relative to CF. However, the cumulative mineralization of organic C was relatively low in BF20. Thus, the promotion of organic C stock was generally higher in BF20, while the proportion of organic C mineralization was relatively low across aggregate fractions. Correlation analysis showed that microbial community in aggregate was correlated with increases of soil C, of which bacteria and fungi contributed more than actinomycetes. This study highlighted the vital role of Trichoderma bio-fertilizer in regulating C mineralization at the aggregate level and provided scientific bases for bio-fertilizer application in Shajiang Calci-Aquic Vertosol. However, we did not determine the distinct keystone taxa and their co-occurrence patterns. Further study concerning keystone taxa at the aggregate level after bio-fertilizer application is needed.

Author Contributions

Writing—original draft preparation, L.Z. and Y.C.; writing—review and editing, M.C., C.S. and T.L.; visualization, Y.Z.; funding acquisition, L.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the Scientific and Technological Project of Henan Provincial Science and Technology Department of China (222102320276), the National Key Research and Development Program of China (2018YFD0300704).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available upon request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Agriculture 12 01001 g001 550
Figure 1. Organic C in different aggregate classes in the five treatments. Different lowercase letters indicate significant differences between treatments, and different uppercase letters indicate differences between aggregate size classes at p < 0.05. Error bars represent standard deviation of means (n = 3). CF: 100% chemical fertilizer N; BF10: chemical fertilizer N supplemented with 10% bio-fertilizer N; BF20: chemical fertilizer N supplemented with 20% bio-fertilizer N; BF30: chemical fertilizer N supplemented with 30% bio-fertilizer N; BF50: chemical fertilizer N supplemented with 50% bio-fertilizer N.
Figure 1. Organic C in different aggregate classes in the five treatments. Different lowercase letters indicate significant differences between treatments, and different uppercase letters indicate differences between aggregate size classes at p < 0.05. Error bars represent standard deviation of means (n = 3). CF: 100% chemical fertilizer N; BF10: chemical fertilizer N supplemented with 10% bio-fertilizer N; BF20: chemical fertilizer N supplemented with 20% bio-fertilizer N; BF30: chemical fertilizer N supplemented with 30% bio-fertilizer N; BF50: chemical fertilizer N supplemented with 50% bio-fertilizer N.
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Figure 2. The dynamics of organic C of mineralization in >2 mm (a), 0.25–2 mm (b), 0.053–0.25 mm (c), <0.053 mm aggregate fractions (d) and bulk soil (e) for the five treatments. Values are means of three replicates. CF, BF10, BF20, BF30 and BF50 are defined as in Figure 1.
Figure 2. The dynamics of organic C of mineralization in >2 mm (a), 0.25–2 mm (b), 0.053–0.25 mm (c), <0.053 mm aggregate fractions (d) and bulk soil (e) for the five treatments. Values are means of three replicates. CF, BF10, BF20, BF30 and BF50 are defined as in Figure 1.
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Agriculture 12 01001 g003 550
Figure 3. Cumulative mineralization of organic C in different aggregate fractions (a) and bulk soil (b) under the five treatments. Different lowercase letters indicate significant differences among treatments at p < 0.05. CF, BF10, BF20, BF30 and BF50 are defined as in Figure 1.
Figure 3. Cumulative mineralization of organic C in different aggregate fractions (a) and bulk soil (b) under the five treatments. Different lowercase letters indicate significant differences among treatments at p < 0.05. CF, BF10, BF20, BF30 and BF50 are defined as in Figure 1.
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Agriculture 12 01001 g004 550
Figure 4. The soil microbial community in >2 mm (a), 0.25–2 mm (b), 0.053–0.25 mm (c), <0.053 mm aggregate fractions (d) and bulk soil (e) for the five treatments. Error bars represent the standard deviation of the mean (n = 3). Different lowercase letters above bars for each PLFA indicate significant differences at p < 0.05. CF, BF10, BF20, BF30 and BF50 are defined as in Figure 1.
Figure 4. The soil microbial community in >2 mm (a), 0.25–2 mm (b), 0.053–0.25 mm (c), <0.053 mm aggregate fractions (d) and bulk soil (e) for the five treatments. Error bars represent the standard deviation of the mean (n = 3). Different lowercase letters above bars for each PLFA indicate significant differences at p < 0.05. CF, BF10, BF20, BF30 and BF50 are defined as in Figure 1.
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Table
Table 1. Distribution of soil aggregate and soil aggregate stability assessed by dry sieving method.
Table 1. Distribution of soil aggregate and soil aggregate stability assessed by dry sieving method.
TreatmentDistribution of Soil Aggregate (%)MWD (mm)
>2 mm0.25–2 mm0.053–0.25 mm<0.053 mm
CF34.90 ± 1.34 c26.08 ± 2.40 c26.54 ± 1.46 a12.48 ± 3.92 a1.04 ± 0.04 d
BF1041.43 ± 0.90 b31.71 ± 1.00 b21.93 ± 1.59 b4.93 ± 1.95 b1.22 ± 0.01 c
BF2048.94 ± 0.96 a36.60 ± 0.96 a13.28 ± 0.40 c1.18 ± 0.33 b1.41 ± 0.00 a
BF3047.46 ± 1.00 a34.29 ± 1.28 a14.89 ± 1.27 c3.37 ± 1.01 b1.36 ± 0.03 b
BF5046.33 ± 1.04 a35.43 ± 0.63 a15.23 ± 0.89 c3.01 ± 1.15 b1.35 ± 0.02 b
Notes: Values are means ± standard deviation of three replicate plots. Different lower case letters in the same column indicate significant differences between treatments for the same aggregate fraction (p < 0.05). CF: 100% chemical fertilizer N; BF10: chemical fertilizer N supplemented with 10% bio-fertilizer N; BF20: chemical fertilizer N supplemented with 20% bio-fertilizer N; BF30: chemical fertilizer N supplemented with 30% bio-fertilizer N; BF50: chemical fertilizer N supplemented with 50% bio-fertilizer N.
Table
Table 2. The rate of organic C respiration in the four aggregate fractions and bulk soil.
Table 2. The rate of organic C respiration in the four aggregate fractions and bulk soil.
TreatmentRate of Organic C Respiration (%)
>2 mm0.25–2 mm0.053–0.25 mm<0.053 mmBulk Soil
CF1.78 ± 0.12 aA1.74 ± 0.14 aA1.61 ± 0.05 aA0.49 ± 0.12 aC1.56 ± 0.12 abB
BF101.71 ± 0.14 aA1.44 ± 0.22 aC1.44 ± 0.24 aC0.38 ± 0.05 aD1.54 ± 0.22 abB
BF201.41 ± 0.20 bA0.97 ± 0.13 bB0.92 ± 0.14 bB0.26 ± 0.13 aC1.35 ± 0.11 bA
BF301.61 ± 0.11 abA0.98 ± 0.21 bB1.00 ± 0.35 bB0.32 ± 0.05 aC1.58 ± 0.12 abA
BF501.79 ± 0.11 aA1.05 ± 0.15 bB1.08 ± 0.12 bB0.40 ± 0.08 aC1.72 ± 0.12 aA
Notes: Different lowercase letters within a column indicate significant differences between treatments, and different uppercase letters in the same row indicate differences between aggregate fractions at p < 0.05. CF, BF10, BF20, BF30 and BF50 are defined as in Table 1.
Table
Table 3. The diversity of soil microbial community in aggregate fractions and bulk soil in different treatments.
Table 3. The diversity of soil microbial community in aggregate fractions and bulk soil in different treatments.
Diversity IndexTreatmentAggregate Fractions (mm)Bulk Soil
>20.25–20.053–0.25<0.053
HCF1.33 ± 0.12 a1.26 ± 0.01 a1.28 ± 0.11 a1.25 ± 0.02 a1.32 ± 0.01 a
BF101.23 ± 0.11 a1.25 ± 0.08 a1.29 ± 0.12 a1.27 ± 0.03 a1.24 ± 0.01 b
BF201.17 ± 0.08 a1.25 ± 0.02 a1.22 ± 0.01 a1.30 ± 0.02 a1.24 ± 0.01 b
BF301.21 ± 0.08 a1.20 ± 0.13 a1.13 ± 0.01 b1.15 ± 0.02 b1.16 ± 0.03 c
BF501.14 ± 0.11 a1.20 ± 0.06 a1.14 ± 0.01 b1.19 ± 0.02 b1.19 ± 0.02 c
Fungi PLFA/Bacteria PLFACF0.078 ± 0.004 c0.08 ± 0.008 b0.09 ± 0.006 b0.08 ± 0.002 c0.09 ± 0.003 d
BF100.091 ± 0.004 b0.08 ± 0.005 b0.10 ± 0.008 b0.09 ± 0.000 c0.11 ± 0.002 b
BF200.091 ± 0.002 b0.09 ± 0.006 a0.11 ± 0.007 a0.10 ± 0.002 a0.12 ± 0.005 a
BF300.102 ± 0.005 a0.08 ± 0.002 b0.10 ± 0.003 b0.09 ± 0.003 b0.10 ± 0.001 c
BF500.089 ± 0.005 b0.08 ± 0.003 b0.09 ± 0.002 b0.09 ± 0.003 b0.10 ± 0.006 c
G+ PLFA/G− PLFACF1.03 ± 0.006 b1.27 ± 0.015 a1.20 ± 0.008 a1.23 ± 0.016 a1.18 ± 0.023 a
BF101.13 ± 0.016 a1.18 ± 0.032 b1.16 ± 0.020 b1.24 ± 0.008 a1.10 ± 0.006 b
BF201.10 ± 0.021 a1.14 ± 0.012 c1.13 ± 0.010 c1.05 ± 0.020 c1.08 ± 0.010 b
BF301.06 ± 0.062 b1.14 ± 0.017 c1.17 ± 0.016 b1.15 ± 0.016 b1.11 ± 0.015 b
BF501.12 ± 0.022 a1.15 ± 0.011 bc1.17 ± 0.010 b1.06 ± 0.003 c1.11 ± 0.030 b
Notes: Values are means ± standard deviation of three replicate plots. Different lowercase letters within a column for the same index indicated significant differences among treatments at p < 0.05. CF, BF10, BF20, BF30 and BF50 are defined as in Table 1.
Table
Table 4. Relationships between mineralization of organic C and microbial community.
Table 4. Relationships between mineralization of organic C and microbial community.
IndexBacteria PLFAFungi PLFAFungi PLFA/Bacteria PLFAG+ PLFA/G− PLFAH
Organic C in aggregate0.865 **0.881 **0.328−0.450 *−0.665 **
Mineralization of C in aggregate0.2150.2680.247−0.209−0.395
Aggregate distribution0.1140.141 *0.0900.1800.077
Notes: * indicated significance at p < 0.05; ** indicated significance at p < 0.01.
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Zhu, L.; Cao, M.; Sang, C.; Li, T.; Zhang, Y.; Chang, Y.; Li, L. Trichoderma Bio-Fertilizer Decreased C Mineralization in Aggregates on the Southern North China Plain. Agriculture 2022, 12, 1001. https://doi.org/10.3390/agriculture12071001

AMA Style

Zhu L, Cao M, Sang C, Li T, Zhang Y, Chang Y, Li L. Trichoderma Bio-Fertilizer Decreased C Mineralization in Aggregates on the Southern North China Plain. Agriculture. 2022; 12(7):1001. https://doi.org/10.3390/agriculture12071001

Chicago/Turabian Style

Zhu, Lixia, Mengmeng Cao, Chengchen Sang, Tingxuan Li, Yanjun Zhang, Yunxia Chang, and Lili Li. 2022. "Trichoderma Bio-Fertilizer Decreased C Mineralization in Aggregates on the Southern North China Plain" Agriculture 12, no. 7: 1001. https://doi.org/10.3390/agriculture12071001

APA Style

Zhu, L., Cao, M., Sang, C., Li, T., Zhang, Y., Chang, Y., & Li, L. (2022). Trichoderma Bio-Fertilizer Decreased C Mineralization in Aggregates on the Southern North China Plain. Agriculture, 12(7), 1001. https://doi.org/10.3390/agriculture12071001

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