Next Article in Journal
Fungal Biota and Mycotoxins Contamination in Soybean Expeller
Previous Article in Journal
Collision Dynamics of Cassava Seed Stems: Analyzing Recovery Coefficients and Influential Factors for Precision Agriculture
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agronomy
Volume 15
Issue 4
10.3390/agronomy15040806
agronomy-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Soil Fertility and Maize Residue Quality All Effect the Exogenous Carbon Sequestration Only in the Short Term in Macroaggregates, but Not in Microaggregates

by
Nan Ma
1,2,3,
Liangjie Sun
1,2,*,
Yingde Xu
1,2,
Shuangyi Li
1,2,
Jiayan Li
1,2,
Pingluo Xue
1,2,4,
Hongbo Yang
1,2,
Ramona Mörchen
3 and
Jingkuan Wang
1,2
1
National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, Key Laboratory of Arable Land Conservation in Northeast China, Ministry of Agriculture and Rural Affairs, Dongling Road 120, Shenyang 110866, China
2
College of Land and Environment, Shenyang Agricultural University, Dongling Road 120, Shenyang 110866, China
3
Institute of Crop Science and Resource Conservation—Soil Science and Soil Ecology, University of Bonn, Nussallee 13, 53115 Bonn, Germany
4
College of Land Science and Technology, China Agricultural University, Beijing 100193, China
*
Author to whom correspondence should be addressed.
Agronomy 2025, 15(4), 806; https://doi.org/10.3390/agronomy15040806
Submission received: 12 February 2025 / Revised: 23 March 2025 / Accepted: 23 March 2025 / Published: 24 March 2025
(This article belongs to the Section Farming Sustainability)
Browse Figures
Versions Notes

Abstract

:
Understanding the mechanisms of converting plant residue carbon (C) into soil C is important for managing the soil C pool and improving soil fertility. However, little is known yet about how the heterogeneous C from the plant residues, e.g., from the various plant parts, is bound in the aggregates of soil with different initial fertility. To address this, an incubating experiment was carried out through the addition of the 13C-labelled aboveground (stems and leaves) and belowground (roots) residue of maize into Mollisols with high and low fertility. Soil aggregates (> 250 μm and < 250 μm) were sieved, and their δ13C of soil organic carbon (SOC) was quantified. The amino sugar content (calculating for microbial residue C, MRC) and the contribution of MRC to the SOC pool (MRC/SOC) were calculated. The results showed that the SOC and maize residue-derived carbon (MDC) concentrations decreased quickly at the beginning, and then, the decrease slowed down until reaching a relatively constant level, and the two stages corresponded to two main microbial anabolism processes, which were entailing synthesizing living microbial biomass and producing microbial residues, respectively. During the beginning period, limited priming effects were observed, but this priming effect is stronger in the macroaggregates of high-fertility soil. The study further proved the existing conclusion that soil fertility and maize residue quality both influenced the C sequestration in the short term but not in the long term in macroaggregates. In the microaggregates, however, only maize residue quality influenced the C sequestration in the long term. In addition, the microaggregates exhibited higher MDC and SOC concentration, and reached a steady state for the MRC/SOC dynamics later than the macroaggregates. These indicated that the microaggregates had a larger C sequestrating capacity than the macroaggregates. The results suggest that soil aggregates are a major factor influencing exogenous C sequestration, even regulating the effective duration of soil fertility and plant quality.

1. Introduction

Long-term intensive cultivation, characterized by “more output but less input”, has led to a dramatic decrease in soil organic carbon (SOC) and consequently the degradation of farmland soil fertility, raising significant concerns [1,2]. The adoption of soil-management practices to enhance “more input”, such as crop residue return, could enhance the C sequestration and the amount of nutrients available for crops in soils, and improve soil fertility [3,4]. Additionally, the practices can mitigate the release of greenhouse gases from farmland, which could alleviate global warming [5]. It is therefore important to understand the underlying mechanisms of how returned crop residues transform C and enhance SOC storage in farmland under various artificial management measures.
Plant residue C sequestration in farmland soil has been studied extensively for many years. Some studies considered it highly influenced by the chemical composition of the added plant residues [6,7,8]. Residues with a lower C:N ratio typically contained higher amounts of readily decomposable compounds and had faster mineralization rates, and consequently, lower C immobilization [9,10]. However, recent studies highlighted that the SOC content was unaffected by plant residue quality in the long term [11,12]. Instead, it was the physical protection by soil clay particles that played a key role in regulating long-term SOC stabilization [13,14]. Researchers also further discussed the C decomposition and fixation of heterogenous substrates in soil aggregates to elaborate the exogenous residue C dynamics in soil microenvironments. Semenov et al. [15] found that the decomposition of the plant residues with a high C:N ratio (i.e., tree roots, tree branches, and barley roots) was enhanced with the decrease in soil aggregate size, while the decomposition of residues with a low C:N ratio was independent of aggregate size. The finding indicated that the decomposition and sequestration of plant residue C with diverse chemical composition responded differently to soil microenvironments. Wang et al. [7] also claimed that low-quality plant residue (roots) promoted the organic C sequestration of soil aggregates significantly more than high-quality plant residues (stems and leaves) over a relatively long-term scale (540 days). However, Gentile et al. [16] emphasized in their field and incubation experiments that although plant residue quality impacted the short-term soil C dynamics in soil aggregate fractions, it did not affect the amount of SOC stabilized in aggregates after three annual additions. The results were coincident with those effects in bulk soils mentioned above. However, there was a trade-off between high microbial activity and C saturation in bulk soil, and the C transfer among soil aggregate fractions was involved. These influences resulted in uncertain C sequestration in bulk soil and soil aggregates, thus challenging the consistent overall effect of crop residue addition and plant residue quality on the SOC distribution in soil aggregates.
Initial SOC stocks, which to some extent represented soil fertility, significantly influenced the sequestration of soil C in farmlands [17,18]. Studies have identified a significant negative correlation between the soil C sequestration potential and initial SOC stock in both paddy and upland soils [7,19]. A meta-analysis in northeast China [19] found that the response ratio of organic C stock in fluvo-aquic and loessial soils was higher than that of black soils (Mollisols). The result could be attributed to the greater potential to sequestrate C in soil with a lower initial SOC concentration, having higher SOC saturation [20]. The accumulation of straw-derived C and the net increase in the contribution of microbial residues C to SOC due to increasing microbial activity could be responsible for the greater C sequestration potential in low-fertility soil [21]. Wang et al. [22] explained that soil microorganisms were constrained by starvation in low-fertility soil and maintained in a high-metabolic-readiness status to assimilate available exogenous substrates. Bao et al. [23] considered that the low-fertility soil environment might favour slow-growing but efficiently metabolizing bacteria to degrade plant residues, influencing the dynamics of soil C sequestration. However, it is not known whether this is also true when these C and microbe reactions or their mechanisms are shifted to the soil aggregate microenvironment, which is more complex but important for understanding C sequestration in soil. Considering the internal physiochemical environment variation in aggregate fractions and the variation in aggregate composition at different soil fertility levels, the dynamics of exogenous C sequestration by aggregates should be largely divergent. Consequently, further efforts are still necessary to determine the C sequestration in soil aggregates, especially in soils with different fertility levels.
Mollisol is considered one of the most productive soils in the world owing to the richness of its soil organic matter (SOM) [24]. However, it has been affected by serious soil degradation due to “more output but less input” field management practices. Crop residue return is considered one of the best choices to improve SOM and recover the soil quality of degrading Mollisol farmland. Understanding the C sequestration mechanisms after straw return in Mollisol is therefore key to managing and stabilizing SOC. This study aimed to understand the accumulating dynamics of the heterogenous organic C and soil-native C in the aggregates of soils with different fertility levels. A 540-day indoor incubation experiment was carried out, and aboveground and belowground residues of 13C-labelled maize was added into Mollisols with high and low fertility, respectively. The amino sugar, SOC, and 13C abundances (δ13C of SOC) of soil aggregates were analyzed. The contribution of microbial residue C to SOC was calculated through the results of soil amino sugar contents. This study was designed to test the following hypotheses: (1) soil aggregates fix the aboveground and belowground maize residue-derived C in different ways since the microenvironment of aggregates varied, but with a similar amount in the long term; (2) soil fertility influences the C fixation of aggregates, and low-fertility soil fixes more maize residue-derived C in aggregates than does high-fertility soil.

2. Materials and Methods

2.1. Soil and Plant Materials Preparation

This study was conducted based on a long-term field experiment (45°40′ N, 126°35′ E), initiated in 1979 at the Heilongjiang Academy of Agricultural Sciences, Harbin, Heilongjiang Province, China. The main research aims of the field experiment was to observe the long-term impact of different fertilization methods on the topsoil fertility of a Mollisol. This region is characterized by a temperate continental monsoon climate, with a mean annual temperature of 3.5 °C and a mean annual precipitation of 533 mm. The soil was classified as Hapli–Udic Mollisol (The USDA Soil Taxonomy). The topsoil texture of the soils was sandy clay loam (Table 1). The experiment station has a total of 24 treatments with three replications, and each plot area is 36 m2. Since 1979, this field has been cultivated with one crop per year under a wheat–soybean–maize rotation, and the growing season for each crop is from May to October.
In this study, we collected soil materials under two experimental treatments with significant differences in soil fertility. They were added to high amounts of organic fertilizer combined with N and P fertilizer (regarded as a high-fertility soil source, referred to as HF) (organic manure at a rate of 1.86 × 104 kg ha−1 plus chemical fertilizer with 150 kg N ha−1 and 75 kg P2O5 ha−1 every year), and no fertilizer treatment (regarded as a low-fertility soil source, referred to as LF), respectively. The year of sampling was 2019, the crop grown was wheat, and the data on wheat grain yield is shown in Table 1. After crop harvesting, soil samples were obtained from randomly scattered points distributed in each treatment plot using a soil extractor at depths of 0–20 cm and were mixed well according to the treatment. All soil samples were then passed through a 5 mm sieve, and stones, soil animals, and plant residues were removed simultaneously. After air-drying, soils were passed through a 2 mm sieve for use in the incubation experiments. The basic properties of the soil samples are presented in Table 1.
The 13C-labelled maize residue materials used in the experiment were obtained through a pulse-labelling method (in 2016) [25]. The aboveground (stems and leaves) and belowground (roots) maize residue materials were separately collected at the maize harvest date. The aboveground part was cut with a sickle at the connection of the root and stem, and the aboveground part was then dug up with the adhesive soil using a shovel within a 0.05 m2 area and 40 cm depth around each plant. The obtained maize materials were washed carefully with water, oven-dried at 60 °C to a constant weight, and ground with a shredder until they could be passed through a 40-mesh sieve (0.425 mm). The belowground residue had an organic C content of 444.46 g kg−1, total nitrogen (TN) content of 6.14 g kg−1, C/N ratio of 72.39, and δ13C of 298.47‰, while the aboveground part had an organic C content of 407.54 g kg−1, TN content of 8.49 g kg−1, C/N ratio of 48, and δ13C of 386.06‰.

2.2. Incubation Experiment

The study was conducted via an incubation experiment using the soil and maize materials prepared as mentioned above. The incubation experiment treatments involved combining two soil fertility levels with two types of amended maize residue plus the non-maize residue-amended controls, resulting in six treatments: (1) and (2) were non-amended controls in the HF and LF treatments; (3) and (4) were HF soil added with belowground (HF + B) or aboveground (HF + A) maize residue; (5) and (6) were LF soil added with belowground (LF + B) or aboveground (LF + A) maize residue.
The incubating method was generally as following: amounts of 250 g prepared soil were placed in specimen bottles, and their moisture levels were adjusted to 40% of soil water-holding capacity. The soils were then pre-incubated at 25 °C for 7 days. Subsequently, 5 g (equal to 2% of dried soil weight) belowground or aboveground maize residue was mixed with each pre-incubated soil, and the soil moisture level was raised to 60% of soil water-holding capacity. The soil samples were still incubated at 25 °C. Water supplementation was performed weekly via a weighing method to maintain a constant moisture level in the incubated soils. The incubated soils were destructively sampled in triplicate on day 30 (February 2020), 60, 180, 360, and 540 (July 2021) for analysis.

2.3. Soil Aggregate Fractionation

Soil aggregates were separated via the dry-sieving method [26] once the soil was sampled. Briefly, 100 g fresh soil subsample was air-dried to a soil moisture of 8% at 4 °C, and the soil samples were then automatically sieved up and down with an amplitude of 1.5 mm for 2 min on a sieve with 250 μm meshes, installed on a Vibratory Sieve Shaker AS 200 (Retsch, Haan, Germany). The aggregate fractions that remained on (macroaggregates) and passed through the 250 μm sieve (microaggregates) were collected separately, air-dried, and ground until they were passed through 0.149 mm meshes for SOC and amino sugar analyses.

2.4. Soil Samples Analysis

The SOC, TN, and δ13C values of soil were determined using an EA-IRMS (Elementar vario PYRO cube coupled-IsoPrime 100 Isotope Ratio Mass Spectrometer, Hanau, Germany). The soil pH (soil/distilled water ratio, 1:2.5) was determined using a Thunder Magnetic pH Meter (PHS-3B, Cany, Shanghai, China). Soil available N was extracted with 2 M KCl and measured via the alkaline hydrolysis diffusion method [27]. Soil available P was extracted with 0.5 M NaHCO3 solution (pH = 8.5), and the concentration was determined via the molybdenum blue method [28]. The available K was extracted with 1 M CH3COONH4 solution (pH = 7) and determined via spectrophotometry and flame photometry [29].
The analytical procedures of soil amino sugars (Glucosamine, Muramic acid, and Galactosamine) were processed according to Zhang and Amelung [30]. First, soil samples weighed through 0.149 mm meshes were added to HCl (10 mL 6 M), and then hydrolyzed for 8 h at 105 °C. Next, the internal standard (Myo-inositol) was added before hydrolysate filtration, and the residues were obtained via rotary evaporation and dissolved. The solution was then adjusted to pH 6.6–6.8 using KOH solution. After centrifugation, the supernatant was dried again via rotary evaporation, and residues were dissolved in methanol after centrifugation. Finally, the residues were dried using N2 and then freeze-dried. The obtained amino sugars needed to be derivatized to aldononitrile derivatives. The amino sugars were quantified using a gas chromatograph (Agilent 7890B, Santa Clara, CA, USA) using a DB-5 column (30 m × 0.25 mm × 0.25 μm), equipped with a flame ionization detector. The contents of individual amino sugars, i.e., glucosamine (GluN), muramic acid (MurN), and galactosamine (GalN), were calculated via the internal standard method according to Zhang and Amelung [30]. The total amino sugar content was calculated as the sum of the three detectable individual amino sugars.

2.5. Data Analyses

The proportion of maize residue-derived C (MDC%) in SOC of aggregate fractions was calculated as following [31]:
M D C = δ 13 C s a m p l e − δ 13 C c o n t r o l × 100 / δ 13 C c − δ 13 C c o n t r o l
where δ13Csample is the δ13C values of organic C in soils added with labelled maize residue; δ13Ccontrol is the δ13C values of organic C of soils without maize residue addition; and δ13CC is the δ13C value of added maize residue.
Fungi-derived GluN was estimated by subtracting bacterial GluN, which is present in a 1 to 2 M ratio with MurN in bacterial cells, from total GluN [32]. In addition, a factor of 9 was estimated to convert GluN to fungal residue C [33,34], and a factor of 45 was estimated to convert MurN to bacterial residue C [35]. The calculations were as follows:
F u n g a l R e s i d u e   C m g   k g − 1 = G l u N m g   k g − 1 − 2 × M u r N m g   k g − 1 × 179.2 × 9
B a c t e r i a l R e s i d u e   C m g   k g − 1 = M u r N m g   k g − 1 × 45
where 179.2 is the molecular weight of GluN, and total microbial residue C (mg kg−1) was calculated as the sum of fungal residue C and bacteria residue C.
The data were compared using a two-way ANOVA and Duncan’s test for different soils and maize residues. Differences in soil samples at different times were compared using a one-way ANOVA. Significance was reported at the p < 0.05 level. All data were analyzed using the SPSS 22.0 statistical software (IBM Corporation, Chicago, IL, USA), and the graphs were drawn using Origin 2019b (Origin Lab Corporation, Northampton, MA, USA). All results are reported as means of three replicates ± standard errors.

3. Results

3.1. Organic Carbon in Soil Aggregates

The content of soil organic carbon (SOC) in soil aggregates all gradually decreased during incubation for the treatments with residue addition (p < 0.05) (Table S1), and the SOC of the microaggregates was higher than that of the macroaggregates almost all the time during the residue-addition treatments (Figure 1). Residue addition increased SOC for both the macro- and microaggregates. However, the increase in the range of SOC for the microaggregates was larger than that of the macroaggregates during the incubation period. Ultimately, the microaggregate SOC increased 46.4% on average compared to the control treatment (Figure 1b), while the macroaggregates exhibited only an 8.5% increase in the HF soils, with no increase in the LF soils (Figure 1a). The SOC content of treatments with aboveground residue addition in the macroaggregates was significantly lower than that of belowground residue-addition treatments in the first 180 days of incubation, but the influence of soil fertility was marginal during the period (Figure 1a). However, following that, the SOC concentration in HF soils was significantly larger than that in LF soils (p < 0.05), while there was no significant difference between the treatments of residue types (p > 0.05). The results showed that there was an obvious transformation effect of treatment from the residue type to soil fertility on SOC with time in the macroaggregates.

3.2. Maize Residue-Derived C and Native C in Soil Aggregates

Overall, the content of maize residue-derived C (MDC) in the macro- and microaggregates changed following a similar temporal trend to that of the SOC content (p < 0.05) (Figure 2, Table S1). The MDC decreased rapidly before day 180 of incubation, especially for the first 60 days. At this time, compared to the added maize C content, the MDC decreased by 47.5% and 13.5% in HF and LF soils, respectively, compared to the added straw carbon content. After day 180, the decrease in the MDC slowed down and eventually showed no change with time (p > 0.05) (Table S1). The remaining MDC was 19.6–22.9% of the input amount in the macroaggregates at the end of the incubation period.
In the microaggregates, the MDC continued to slowly decrease for belowground residue-addition treatments, while it fluctuated for the aboveground residue-addition treatments. There were significant differences for the different soil-fertility and different types of maize residue treatments only at day 180, showing that the MDC of the aboveground residue-addition treatments was significantly higher than that of the belowground residue-addition treatments, and the LF MDC was higher than that of the HF (p < 0.05). Finally, the MDC content of all treatments decreased to the lowest point and coincided with one another at day 540, except for the MDC content of the higher aboveground residue-addition treatments, which exceeded those of the belowground residue-addition treatments (p < 0.05. Figure 2b). The remaining MDC was 55.6–87% of the input amount in the microaggregates at the end of the incubation period.
Native C was significantly higher than the newly added MDC and also decreased significantly but less so than the MDC (p < 0.05). The native C in the macroaggregates exhibited no significant change during the initial 180 days for all treatments. However, the native C in the microaggregates significantly decreased in the HF and LF treatments, respectively, during the first 180 days (Figure 2, Table S1), and the decline was faster in treatments with aboveground residue addition. At the end of the incubation period, the native C of LF and HF soil in the macroaggregates decreased by 12.8% and 15.2%, while decreases of 2.8% and 5.1% were observed in the microaggregates. Accordingly, there was ultimately a larger decrease in the native C in the microaggregates than in the macroaggregates. The native C was higher in HF treatments than LF treatments in the macroaggregates from day 60 to the end of the incubation period, while no significant difference between soil fertility treatments was observed in the microaggregates.

3.3. Amino Sugars in Soil Aggregates

During the incubation period, the amino sugar content fluctuated with time generally in an upside-down “V” shape and was significantly affected by the soil fertility level and type of maize residue addition (Figure 3). The amino sugar content gradually increased before day 180 for almost all treatments with residue addition. In the macroaggregates, the HF and LF treatments increased by an average of 12.6% and 11.6%, respectively, and by an average of 15.3% and 12.3% in the microaggregates, respectively. This content subsequently declined to match the HF treatment at the end of the incubation period (on average, 1148 mg kg−1), but were generally maintained at day 180 for the LF treatments. Overall, the amino sugar content was significantly higher in the HF soil than in the LF soil (p < 0.05). It was also significantly greater under the treatments with aboveground residue addition than those with belowground residue addition, except for day 540 (Figure 3). At the end of the incubation period, the amino sugar content of residue-addition treatments was significantly greater than that of the treatments without residue addition in the microaggregates (p < 0.05), while there was no significant difference between them in the macroaggregates (p > 0.05).

3.4. Contribution of Microbial Residue C to SOC in Soil Aggregates

The contribution of microbial residue C to SOC (MRC/SOC) of all treatments with maize residue addition increased with time (Table S1), while the treatments without residue addition fluctuated with time (Figure 4). Specifically, the MRC/SOC in the macroaggregates reached its maximum at day 180 (on average, 50%) in residue-addition treatments and remained at a generally constant level thereafter (p > 0.05), except for the continuous increase in LF + B. However, for the microaggregates, the MRC/SOC in the HF soil increased until day 360 (on average, 43.2%), while the MRC/SOC of the LF soil continued increasing until the end of the experiment (on average, 44.3%). The MRC/SOC in the belowground residue-addition treatments was significantly lower than that in the aboveground residue-addition treatments under all soil fertility and aggregate fractions except for the microaggregates of HF. The MRC/SOC in the LF soils was always significantly lower than that of the HF soils regardless of the type of added residue and aggregate fraction (p < 0.05). Finally, following the increase in the MRC/SOC under residue-addition treatments with time, the contribution of MRC/SOC finally ranged between 43.3% and 51.6% in the macroaggregates and between 41.56% and 47.06% in the microaggregates, and there was no significant difference in the treatments with no residue addition (p > 0.05). The final MRC/SOC in the microaggregates (on average, 44%) was lower than that in the macroaggregates (on average, 48%).

4. Discussion

4.1. Microaggregates Exhibited Larger C Sequestrating Capacity than Macroaggregates

Although the general dynamics of SOC, its composition (MDC, native C), and MRC/SOC were similar between the macro- and microaggregates, there were still some significant differences (Figure 2 and Figure 4). Specifically, the microaggregate SOC content was lower than that of the macroaggregates without residue addition, but after the maize residue addition, the SOC content of the microaggregates remained higher than that of the macroaggregates during the whole experiment (Figure 1). The results demonstrated that the exogenous organic C in the microaggregates was more prone to be protected relative to the macroaggregates. In addition, the inference was also supported by the changes in the MDC, which showed a similar trend to SOC between the microaggregates and the macroaggregates after the maize residue addition. In addition, our results also revealed less mineralization of native C in the microaggregates after maize residue addition. Previous studies explained that the limitation of oxygen diffusion inside the microaggregates might lead to lower microbial activity [36,37], and that the SOC was physically enclosed by the microaggregates and chemically bound with fine mineral particles [38]. These processes all provided SOC or MDC protection against mineralization and facilitate more C sequestration inside the microaggregates than inside the macroaggregates [20,39].
Moreover, the MRC/SOC (the contribution of microbial residue C to SOC) was lower in the microaggregates than in the macroaggregates in our experiment, and the MRC/SOC reached a steady state in the microaggregates later than in the macroaggregates (Figure 4). These results demonstrated that it was harder for soil microbes to acquire organic C in the microaggregates than in the macroaggregates to transform into microbial residue C [40]. In addition, there might be a transfer of microbial residue from the macroaggregates to the microaggregates [41], resulting in the “delayed” steady state of the MRC/SOC in the microaggregates. The “delayed” period in the microaggregates has even been reported to be up to half a year [42] compared to our 180 days, leading to greater C sequestration from exogenous C in the microaggregates [43]. These results further proved the larger C sequestrating capacity for the microaggregates. However, the constituent of the aggregate fractions was rather unbalanced for the soils used in this experiment, which showed the weight percentage of the microaggregates was significantly lower than that of the macroaggregates. Consequently, the exogenous organic C should be mostly sequestrated in the macroaggregates rather than in the microaggregates, despite the larger C sequestration capacity for the microaggregates demonstrated in this experiment.

4.2. Soil Fertility Affected the C Sequestration in the Short Term but Not in the Long Term, and High Fertility Facilitated the Priming Effect

The SOC content decreased differently in the macroaggregates of HF and LF soils after the maize residue addition. Compared to the isotope labelling results, the MDC dynamics was synchronized with that of the SOC, but not with the native SOC (Figure 2), indicating that the changes in SOC were mostly caused by the MDC. In the early part of the incubation period (first 60 days), the MDC decomposed faster in the HF soil, with the results showing that maize residue decomposition could be regulated by soil fertility, a finding consistent with other studies [7,23]. Blesh and Ying [44] also observed a faster residue decomposition in high-fertility soil for the first 30 days and attributed it to the much higher inorganic N content in high-fertility soils providing more sufficient N for soil microorganisms to decompose. In addition, the characteristics of the microbial community in soils with different fertility levels could directly result in dissimilar decomposition. It had been shown that microorganisms cultivated in high-fertility soils lived with a fast-but-inefficient strategy in decomposing plant residues, while microorganisms in low-fertility soil exhibited the opposite, living a slow-but-efficient strategy [23]. Accordingly, the former microorganisms acclimated in HF soil could decompose organic C faster than the latter, resulting in a faster declining rate of SOC in HF soil.
However, the faster decomposition of maize residues in the macroaggregates of the HF soil became slower than that in LF soil (after day 60), and the diverse MDC content of soils with different fertility levels all ultimately decreased to the same level (Figure 2). These results contradicted our second hypothesis. As the easily decomposable part of maize residue for the microbial community of the HF soil was exhausted, the remaining relatively resistant part was not to the taste of microorganisms in the HF soil, leading to a relatively slow decomposition [45,46]. However, in the LF soil, the microbial community might have reacted slowly to the exogenous C relative to that of the HF soil, but the microbial community composition in the LF soil exhibited stronger adaptation to the remaining resistant substrates. Therefore, they maintained a relatively faster decomposition of the substrates compared to the decomposition in high-fertility soil [44,47]. The dynamics of MDC in the microaggregates was like that of the macroaggregates for similar reasons, except for the changes in the aboveground MDC at day 180, which might have been induced by the C exchange with the macroaggregates.
Finally, there was 19.63–22.9% MDC remaining for the macroaggregates and 55.6–86.96% MDC for the microaggregates (Figure 2), both with a tiny discrepancy between the HF and LF soils. In addition, the residual MDC remained unchanged in the soil from day 360 to the end of the experiment, which could be considered a final increment of the SOC pool. Accordingly, soil fertility levels did not affect the C fixation of aggregates, which is inconsistent with our second hypothesis. Finally, the MDC could be fixed by soil due to the following reasons: Firstly, the remaining MDC was chemically resistant to soil microorganisms [48], or it was transformed by soil microorganisms into a chemically resistant form, i.e., the microbial residues [36,49]. Secondly, this part of the MDC was protected by the strong combination with mineral particles [37,50]. In this experiment, the results showed that there was no significant difference in MRC/SOC between residue-addition treatments and their control in either the macro- or microaggregates of either the HF or LF soils at the end of incubation (Figure 4). This indicates that there must have been a similar rate of microbial residue in the fixed MDC to maintain the equivalence of MRC/SOC between residue-addition treatments and their control (41.56–51.63%, Figure 4). Accordingly, there was almost half of the fixed MDC sequestrated in soil through microbial residue. In addition, the rest of the fixed MDC should probably be minerally protected as plant residue rather than the chemically resistant MDC, considering that there was no difference in the fixed MDC between the residue-addition treatments with different chemical compositions. In a word, the fertility of soil could manipulate the sequestrating course of exogenous organic C in the short term but had no influence on the long term. The result was in accordance with Xu et al. [51], who found that, after 500 days of experimentation, the mineralization of exogenous C was essentially the same in both low- and high-fertility soils.
Notably, the native C in the macroaggregates of the HF soil decreased slightly but significantly after day 180, while no significant change was observed for the LF soil and for the microaggregates of both LF and HF (Figure 2). Moreover, there should probably be limited C transfer between the micro- and macroaggregates that led to the decrease in native C in the macroaggregates of the HF soil, based on the results showing that no large increase in native C was found in the microaggregates (Figure 2b). The results suggested that there might be a mild priming effect occurring in and constrained to the macroaggregates in HF soil during the later stages of residue decomposition. Mo et al. [52] also believed that differentiation of priming effects happened among soil aggregates based on their 13C-labelling laboratory study. Other studies also reported that the addition of exogenous substances to the macroaggregates resulted in a higher priming effect than that of the microaggregates [53]. Researchers mainly attributed the results to the greater level of protection on organic C provided by the microaggregates, thus slowing down the mineralization of native C [54]. These results are in accordance with our conclusion of a larger C fixation capacity in the microaggregates discussed above. In addition, the high fertility of soil provided the driving force for the priming effect with a larger microbial biomass and higher enzyme activities [55,56]. However, soil microorganisms should initially prefer to utilize newly added unstable organic C substrates compared to the native C of soil [57] (also see Figure 2a). As unstable exogenous substrates were gradually consumed, decomposing native C was encouraged because the increased biomass of soil microorganisms needed replenishment to maintain their biomass [58,59]. Above all, the study indicated that the priming effect induced by the exogenous organic C might more easily happen in the macroaggregates of soil with sufficient native organic C.

4.3. Maize Residue Quality Influenced the C Sequestration in the Short Term but Not in the Long Term Only in Macroaggregates

The varying and contrasting patterns of aboveground versus belowground residue-addition treatments were similar to high- versus low-fertility soil treatments. The SOC content of aboveground residue-addition treatments was significantly lower than that of belowground residue-addition treatments from day 30 to 60 in the macroaggregates (Figure 1), mainly induced by the lower MDC in aboveground versus belowground residue-addition treatments (Figure 2). The result agreed with that of previous studies, being frequently attributed to the different chemical composition of added C substrates at the beginning [60,61]. To be specific, the labile substrate, such as the plant leaf and stem compared to the root, could be more easily decomposed by soil microorganisms resulting in less SOC remaining in the soil [51,62].
A further observation in our experiment was there was a higher MRC/SOC in the aboveground residue-addition treatments than belowground during the period from day 30 to 60 (Figure 4). The result should be mainly attributed to the lower SOC content (denominator of “MRC/SOC”) (Figure 1), but not the higher microbial residue (numerator of “MRC/SOC”) in aboveground residue-addition treatments (Figure 3). It was found that soil respiration increased quickly in a short time because of the dramatic increase in living microbial biomass indicated by microbial biomass C (MBC) and phospholipid fatty acid (PLFA) [49,63,64,65,66]. Accordingly, the microbial decomposition at the beginning was performed by microbial catabolism and anabolism to build a soil microbial community sufficient to digest the newly added residue [67]. However, there was a marginal increase in amino sugar content at the same time, indicating that the rapid increase in anabolism was unrelated to soil C fixation through microbial necromass. Subsequently, the increased microbial residue in HF soil should have contributed to the higher MRC/SOC in the aboveground residue-addition treatment (Figure 4), because of its significant increase in amino sugar content compared to no change in the control treatment (Figure 3). The results indicated that soil microorganisms in the macroaggregates of the HF soil decomposed newly added maize aboveground residue mostly through a buildup of living microbial biomass via a “high catabolism and high anabolism” pathway at the beginning. They then quickly transformed the metabolism pathway to contribute to the exogenous C fixation into low catabolism but relatively high anabolism to accumulate microbial residue. In contrast, the transformation of microbial metabolism for the belowground-addition residue treatment in the HF soil (Figure 3a) happened at day 360, later than that in the aboveground residue-addition treatment (180 days). The result showed that belowground residue with low quality delayed the levelling-off of microbial residue contribution to SOC. This indicated the influence of plant residue quality on the microbial residue C fixation. The result partly proved the first hypothesis and was supported again by “the easy first” theory discussed above.
From day 180, the SOC content difference between aboveground and belowground residue-addition treatments in the macroaggregates of the same soil fertility level became smaller and ultimately disappeared after day 360 (Figure 1), and the changes were in accordance with those of MDC (Figure 2). The results were not surprising according to previous studies [51,68], which developed a popular theory that residue quality influenced the C sequestration in the short term but not in the long term, and our results proved the theory was also true in soil macroaggregates [6,51]. However, unlike in the macroaggregates, the MDC of the belowground residue-addition treatments was significantly lower than that of the aboveground residue-addition treatments in the microaggregates at the end of the incubation period (Figure 2b). We also found that the MRC/SOC did not differ significantly between aboveground and belowground residue-addition treatments at the end of the incubation period (Figure 4). Microbial communities with different decomposers living in soil, which represent quite complex systems, could develop a strong adaptation ability to consume different types of residue materials [69,70]. The soil C sequestration at this stage (from day 180) should therefore be mainly caused by microbial residue transformation and mineral protection, as discussed above, but influenced marginally by residue quality.

5. Conclusions

This incubation experiment was conducted to observe the sequestration of heterogenous maize residue-derived C in aggregates of soil with different fertility levels. The decomposition of maize residue-derived C (MDC) mostly led to the decrease in SOC after the addition of maize residues, indicating that a limited priming effect occurred in the experiment. However, the microenvironment of macroaggregates in soil with high fertility could facilitate the occurrence of a priming effect. In the macroaggregates, and in agreement with the theory concluded from a bulk soil study, both soil fertility and maize residue quality influenced the C sequestration in the short term but not in the long term. However, the theory did not hold true for microaggregates, likely due to the occasional transformation of residue C from macroaggregates. Mineral protection and microbial residue fixation were probably the main pathways of soil C sequestration in the studied Mollisols. Additionally, the microaggregates probably had a larger C sequestrating capacity than did the macroaggregates through aggregate protection, which could influence the C acquisition of soil microorganisms and the C allocation in soil.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy15040806/s1, Table S1: Results of ANOVA between the different treatments and at incubation times. HF+B and HF+A denoted high fertility soil added with belowground and aboveground maize residues, respectively; LF+B and LF+A denoted low fertility soil added with belowground and aboveground maize residues, respectively, HF and LF denoted high and low fertility soil without any straw input, respectively. HF and LF denoted without maize residues in the high and low fertility soils. MDC represent the maize derived carbon. Capital maize residue indicates changes in the same treatment at different times, lowercase letters indicate changes in the same time between treatments.

Author Contributions

Conceptualization, N.M., L.S., Y.X. and J.W.; Methodology, N.M., S.L., J.L., P.X. and H.Y.; Formal analysis, N.M. and L.S.; Investigation, J.L., P.X. and H.Y.; Data curation, N.M. and J.W.; Writing—original draft, N.M. and L.S.; Writing—review and editing, L.S., Y.X., S.L., R.M. and J.W.; Funding acquisition, L.S., Y.X. and J.W. All authors have read and agreed to the published version of the manuscript.

Funding

China Scholarship Council is appreciated for providing financial support to the visit of Nan Ma to the University of Bonn. This research was financially supported by the National Natural Science Foundation of China (42207383, 42277321), the Fundamental Scientific Research Project of the Educational Department of Liaoning Province (LJKMZ20220994), the Liaoning Provincial Science and Technology Major Project (2023JH1/10400001), and the Natural Science Foundation Project of Liaoning Province (2023-MS-203).

Data Availability Statement

The data sets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Lal, R. Soil Carbon Sequestration Impacts on Global Climate Change and Food Security. Science 2004, 304, 1623–1627. [Google Scholar] [CrossRef] [PubMed]
  2. Stockmann, U.; Adams, M.A.; Crawford, J.W.; Field, D.J.; Henakaarchchi, N.; Jenkins, M.; Minasny, B.; McBratney, A.B.; Courcelles, V.D.R.; Singh, K.; et al. The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agr. Ecosyst. Environ. 2013, 164, 80–99. [Google Scholar] [CrossRef]
  3. Ding, X.; Ling, N.; Zhang, W.; Lu, M.; Wen, J.; He, H.; Zhang, X. Distinct carbon incorporation from 13C-labelled rice straw into microbial amino sugars in soils applied with manure versus mineral fertilizer. Geoderma 2023, 436, 116537. [Google Scholar]
  4. Christianson, R.; Fox, J.; Law, N.; Wong, C. Effectiveness of Cover Crops for Water Pollutant Reduction from Agricultural Areas. Trans. ASABE 2021, 64, 1007–1017. [Google Scholar]
  5. Chenu, C.; Angers, D.A.; Barré, P.; Derrien, D.; Arrouays, D.; Balesdent, J. Increasing organic stocks in agricultural soils: Knowledge gaps and potential innovations. Soil Till. Res. 2019, 188, 41–52. [Google Scholar]
  6. Cadisch, G.; Giller, K. Soil organic matter management: The roles of residue quality in C sequestration and N supply. In Sustainable Management of Soil Organic Matter; CABI: Wallingford, UK, 2001; pp. 97–219. [Google Scholar]
  7. Whalen, J.K.; Gul, S.; Poirier, V.; Yanni, S.F.; Simpson, M.J.; Clemente, J.S.; Feng, X.; Grayston, S.J.; Barker, J.; Gregorich, E.G.; et al. Transforming plant carbon into soil carbon: Process-level controls on carbon sequestration. Can. J. Plant Sci. 2014, 94, 1065–1073. [Google Scholar]
  8. Schmatz, R.; Recous, S.; Aita, C.; Tahir, M.M.; Schú, A.L.; Chaves, B.; Giacomini, S.J. Crop residue quality and soil type influence the priming effect but not the fate of crop residue C. Plant Soil. 2017, 414, 229–245. [Google Scholar]
  9. Abiven, S.; Recous, S.; Reyes, V.; Oliver, R. Mineralisation of C and N from root, stem and leaf residues in soil and role of their biochemical quality. Biol. Fertil. Soils 2005, 42, 119–128. [Google Scholar]
  10. Thippayarugs, S.; Toomsan, B.; Vityakon, P.; Limpinuntana, V.; Patanothai, A.; Cadisch, G. Interactions in decomposition and N mineralization between tropical legume residue components. Agrofor. Syst. 2007, 72, 137–148. [Google Scholar]
  11. Wang, X.; Butterly, C.R.; Baldock, J.A.; Tang, C. Long-term stabilization of crop residues and soil organic carbon affected by residue quality and initial soil pH. Sci. Total Environ. 2017, 587–588, 502–509. [Google Scholar]
  12. Xu, Y.; Ding, F.; Gao, X.; Wang, Y.; Li, M.; Wang, J. Mineralization of plant residues and native soil carbon as affected by soil fertility and residue type. J. Soils Sediments 2018, 19, 1407–1415. [Google Scholar]
  13. Schmidt, M.W.I.; Torn, M.S.; Abiven, S.; Dittmar, T.; Guggenberger, G.; Janssens, I.A.; Kleber, M.; Kögel-Knabner, I.; Lehmann, J.; Manning, D.A.C.; et al. Persistence of soil organic matter as an ecosystem property. Nature 2011, 478, 49–56. [Google Scholar] [PubMed]
  14. Rabbi, S.M.F.; Wilson, B.R.; Lockwood, P.V.; Daniel, H.; Young, I.M. Soil organic carbon mineralization rates in aggregates under contrasting land uses. Geoderma 2014, 216, 10–18. [Google Scholar]
  15. Semenov, V.M.; Lebedeva, T.N.; Pautova, N.B.; Khromychkina, D.P.; Kovalev, I.V.; Kovaleva, N.O. Relationships between the Size of Aggregates, Particulate Organic Matter Content, and Decomposition of Plant Residues in Soil. Eurasian Soil. Sci. 2020, 53, 454–466. [Google Scholar]
  16. Gentile, R.; Vanlauwe, B.; Six, J. Litter quality impacts short-but not long-term soil carbon dynamics in soil aggregate fractions. Ecol. Appl. 2011, 21, 695–703. [Google Scholar] [CrossRef]
  17. Sun, W.; Huang, Y.; Zhang, W.; Yu, Y. Carbon sequestration and its potential in agricultural soils of China. Glob. Biogeochem. Cycles 2010, 24. [Google Scholar] [CrossRef]
  18. Dang, P.; Li, C.; Huang, T.; Lu, C.; Li, Y.; Qin, X.; Siddique, K.H.M. Effects of different continuous fertilizer managements on soil total nitrogen stocks in China: A meta-analysis. Pedosphere 2022, 32, 39–48. [Google Scholar] [CrossRef]
  19. Berhane, M.; Xu, M.; Liang, Z.; Shi, J.; Wei, G.; Tian, X. Effects of long-term straw return on soil organic carbon storage and sequestration rate in North China upland crops: A meta-analysis. Glob. Chang. Biol. 2020, 26, 2686–2701. [Google Scholar]
  20. Castellano, M.J.; Mueller, K.E.; Olk, D.C.; Sawyer, J.E.; Six, J. Integrating plant litter quality, soil organic matter stabilization, and the carbon saturation concept. Glob. Chang. Biol. 2015, 21, 3200–3209. [Google Scholar]
  21. Xu, Y.; Gao, X.; Liu, Y.; Li, S.; Liang, C.; Lal, R.; Wang, J. Differential accumulation patterns of microbial necromass induced by maize root vs. shoot residue addition in agricultural Alfisols. Soil Biol. Biochem. 2022, 164, 108474. [Google Scholar] [CrossRef]
  22. Wang, X.; Zhang, W.; Zhou, F.; Liu, Y.; He, H.; Zhang, X. Distinct regulation of microbial processes in the immobilization of labile carbon in different soils. Soil Biol. Biochem. 2020, 142, 107723. [Google Scholar] [CrossRef]
  23. Bao, Y.; Dolfing, J.; Chen, R.; Li, Z.; Lin, X.; Feng, Y. Trade-off between microbial ecophysiological features regulated by soil fertility governs plant residue decomposition. Soil Till. Res. 2023, 229, 105679. [Google Scholar] [CrossRef]
  24. Tong, Y.; Liu, J.; Li, X.; Sun, J.; Herzberger, A.; Wei, D.; Zhang, W.; Dou, Z.; Zhang, F. Cropping System Conversion led to Organic Carbon Change in China’s Mollisols Regions. Sci. Rep. 2017, 7, 18064. [Google Scholar]
  25. An, T.; Schaeffer, S.; Li, S.; Fu, S.; Pei, J.; Li, H.; Zhuang, J.; Radosevich, M.; Wang, J. Carbon fluxes from plants to soil and dynamics of microbial immobilization under plastic film mulching and fertilizer application using 13C pulse-labeling. Soil Biol. Biochem. 2015, 80, 53–61. [Google Scholar]
  26. Mary, E.; Schutter, R.P.D. Microbial Community Profiles and Activities among Aggregates of Winter Fallow and Cover-Cropped Soil. Soil Sci. Soc. Am. J. 2002, 66, 142–153. [Google Scholar]
  27. Spargo, J.T.; Alley, M.M. Modification of the Illinois Soil Nitrogen Test to Improve Measurement Precision and Increase Sample Throughput. Soil Sci. Soc. Am. J. 2008, 72, 823–829. [Google Scholar] [CrossRef]
  28. Olsen, S.R.; Cole, C.U.; Watanabe, F.S.; Deen, L.A. Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate; Miscellaneous Paper Institute for Agricultural Research Samaru; US Department of Agriculture: Washington, DC, USA, 1954. [Google Scholar]
  29. Helmke, P.A.; Sparks, D.L. Lithium, sodium, potassium, rubidium, and cesium. In Methods of Soil Analysis Part 3: Chemical Methods; Sparks, D.L., Ed.; SSSA Book Series No 5; SSSA: Madison, WI, USA, 1996. [Google Scholar]
  30. Zhang, X.; Wulf, A. Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biol. Biochem. 1996, 28, 1201–1206. [Google Scholar]
  31. De Troyer, I.; Amery, F.; Van Moorleghem, C.; Smolders, E.; Merckx, R. Tracing the source and fate of dissolved organic matter in soil after incorporation of a 13C labelled residue: A batch incubation study. Soil Biol. Biochem. 2011, 43, 513–519. [Google Scholar]
  32. Engelking, B.; Flessa, H.; Joergensen, R.G. Shifts in amino sugar and ergosterol contents after addition of sucrose and cellulose to soil. Soil Biol. Biochem. 2007, 39, 2111–2118. [Google Scholar]
  33. Joergensen, R.G.; Mäder, P.; Fließbach, A. Long-term effects of organic farming on fungal and bacterial residues in relation to microbial energy metabolism. Biol. Fertil. Soils 2010, 46, 303–307. [Google Scholar] [CrossRef]
  34. Liang, C.; Amelung, W.; Lehmann, J.; Kästner, M. Quantitative assessment of microbial necromass contribution to soil organic matter. Glob. Chang. Biol. 2019, 25, 3578–3590. [Google Scholar] [PubMed]
  35. Appuhn, A.; Joergensen, R. Microbial colonisation of roots as a function of plant species. Soil Biol. Biochem. 2006, 38, 1040–1051. [Google Scholar]
  36. Xu, F.; Li, C.; Chen, Y.; Wu, J.; Bai, H.; Fan, S.; Yang, Y.; Zhang, Y.; Li, S.; Su, J. Soil microbial community structure and soil fertility jointly regulate soil microbial residue carbon during the conversion from subtropical primary forest to plantations. Geoderma 2024, 441, 116767. [Google Scholar]
  37. Lehmann, J.; Solomon, D.; Kinyangi, J.; Dathe, L.; Wirick, S.; Jacobsen, C. Spatial complexity of soil organic matter forms at nanometre scales. Nat. Geosci. 2008, 1, 238–242. [Google Scholar]
  38. Huber, M.E.; Yavitt, J.B.; Wright, S.J.; Kirkham, M.B. Mineralogical control on physically protected soil organic matter in a neotropical moist forest. Soil Res. 2023, 61, 569–581. [Google Scholar]
  39. Six, J.; Elliott, E.T.; Paustian, K. Soil macroaggregate turnover and microaggregate formation: A mechanism for C sequestration under no-tillage agricul-ture. Soil Biol. Biochem. 2000, 32, 2099–2103. [Google Scholar]
  40. Ding, X.; Liang, C.; Zhang, B.; Yuan, Y.; Han, X. Higher rates of manure application lead to greater accumulation of both fungal and bacterial residues in macroaggregates of a clay soil. Soil Biol. Biochem. 2015, 84, 137–146. [Google Scholar]
  41. Liu, S.; Six, J.; Zhang, H.X.; Zhang, Z.B.; Peng, X.H. Integrated aggregate turnover and soil organic carbon sequestration using rare earth oxides and 13C isotope as dual tracers. Geoderma 2023, 430, 116313. [Google Scholar]
  42. Guan, S.; Dou, S.; Chen, G.; Wang, G.; Zhuang, J. Isotopic characterization of sequestration and transformation of plant residue carbon in relation to soil aggregation dynamics. Appl. Soil. Ecol. 2015, 96, 18–24. [Google Scholar]
  43. White, P.M.; Rice, C.W. Tillage Effects on Microbial and Carbon Dynamics during Plant Residue Decomposition. Soil Sci. Soc. Am. J. 2009, 73, 138–145. [Google Scholar]
  44. Blesh, J.; Ying, T. Soil fertility status controls the decomposition of litter mixture residues. Ecosphere 2020, 11, e03237. [Google Scholar]
  45. Abiven, S.; Menasseri, S.; Chenu, C. The effects of organic inputs over time on soil aggregate stability—A literature analysis. Soil Biol. Biochem. 2009, 41, 1–12. [Google Scholar]
  46. Shahbaz, M.; Kuzyakov, Y.; Sanaullah, M.; Heitkamp, F.; Zelenev, V.; Kumar, A.; Blagodatskaya, E. Microbial decomposition of soil organic matter is mediated by quality and quantity of crop residues: Mechanisms and thresholds. Biol. Fertil. Soils 2017, 53, 287–301. [Google Scholar]
  47. Lindedam, J.; Magid, J.; Poulsen, P.; Luxhøi, J. Tissue architecture and soil fertility controls on decomposer communities and decomposition of roots. Soil Biol. Biochem. 2009, 41, 1040–1049. [Google Scholar]
  48. Adhikari, A.D.; Shrestha, P.; Ghimire, R.; Liu, Z.; Pollock, D.A.; Acharya, P.; Aryal, D.R. Cover crop residue quality regulates litter decomposition dynamics and soil carbon mineralization kinetics in semi-arid cropping systems. Appl. Soil. Ecol. 2024, 193, 105160. [Google Scholar]
  49. Liang, C.; Schimel, J.P.; Jastrow, J.D. The importance of anabolism in microbial control over soil carbon storage. Nat. Microbiol. 2017, 2, 17105. [Google Scholar]
  50. Zhu, S.; Sainju, U.M.; Zhang, S.; Tan, G.; Wen, M.; Dou, Y.; Yang, R.; Chen, J.; Zhao, F.; Wang, J. Cover cropping promotes soil carbon sequestration by enhancing microaggregate-protected and mineral-associated carbon. Sci. Total Environ. 2024, 908, 168330. [Google Scholar]
  51. Xu, Y.; Sun, L.; Lal, R.; Bol, R.; Wang, Y.; Gao, X.; Ding, F.; Liang, S.; Li, S.; Wang, J. Microbial assimilation dynamics differs but total mineralization from added root and shoot residues is similar in agricultural Alfisols. Soil Biol. Biochem. 2020, 148, 107901. [Google Scholar]
  52. Mo, F.; Zhang, Y.Y.; Liu, Y.; Liao, Y.C. Microbial carbon-use efficiency and straw-induced priming effect within soil aggregates are regulated by tillage history and balanced nutrient supply. Biol. Fertil. Soils 2021, 57, 409–420. [Google Scholar] [CrossRef]
  53. Sarker, J.R.; Singh, B.P.; Cowie, A.L.; Fang, Y.; Collins, D.; Dougherty, W.J.; Singh, B.K. Carbon and nutrient mineralisation dynamics in aggregate-size classes from different tillage systems after input of canola and wheat residues. Soil Biol. Biochem. 2018, 116, 22–38. [Google Scholar]
  54. Tisdall, J.M.; Oades, J.M. Organic matter and water-stable aggregates in soils. J. Soil Sci. 1982, 33, 141–163. [Google Scholar]
  55. Lang, J.; Hu, J.; Ran, W.; Xu, Y.; Shen, Q. Control of cotton Verticillium wilt and fungal diversity of rhizosphere soils by bio-organic fertilizer. Biol. Fertil. Soils 2011, 48, 191–203. [Google Scholar] [CrossRef]
  56. Xu, H.; Vandecasteele, B.; Zavattaro, L.; Sacco, D.; Wendland, M.; Boeckx, P.; Haesaert, G.; Sleutel, S. Maize root-derived C in soil and the role of physical protection on its relative stability over shoot-derived C. Eur. J. Soil Sci. 2019, 70, 935–946. [Google Scholar]
  57. Blagodatskaya, E.; Kuzyakov, Y. Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: Critical review. Biol. Fertil. Soils 2008, 45, 115–131. [Google Scholar] [CrossRef]
  58. Wang, H.; Boutton, T.W.; Xu, W.; Hu, G.; Jiang, P.; Bai, E. Quality of fresh organic matter affects priming of soil organic matter and substrate utilization patterns of microbes. Sci. Rep. 2015, 5, 10102. [Google Scholar]
  59. Fanin, N.; Alavoine, G.; Bertrand, I. Temporal dynamics of litter quality, soil properties and microbial strategies as main drivers of the priming effect. Geoderma 2020, 377, 114576. [Google Scholar]
  60. Craig, M.E.; Geyer, K.M.; Beidler, K.V.; Brzostek, E.R.; Frey, S.D.; Stuart Grandy, A.; Liang, C.; Phillips, R.P. Fast-decaying plant litter enhances soil carbon in temperate forests but not through microbial physiological traits. Nat. Commun. 2022, 13, 1229. [Google Scholar]
  61. Kaštovská, E.; Choma, M.; Angst, G.; Remus, R.; Augustin, J.; Kolb, S.; Wirth, S. Root but not shoot litter fostered the formation of mineral-associated organic matter in eroded arable soils. Soil Till. Res. 2024, 235, 105871. [Google Scholar]
  62. Córdova, S.C.; Olk, D.C.; Dietzel, R.N.; Mueller, K.E.; Archontouilis, S.V.; Castellano, M.J. Plant litter quality affects the accumulation rate, composition, and stability of mineral-associated soil organic matter. Soil Biol. Biochem. 2018, 125, 115–124. [Google Scholar] [CrossRef]
  63. Ge, Z.; Li, S.; Bol, R.; Zhu, P.; Peng, C.; An, T.; Cheng, N.; Liu, X.; Li, T.; Xu, Z.; et al. Differential long-term fertilization alters residue-derived labile organic carbon fractions and microbial community during straw residue decomposition. Soil Till. Res. 2021, 213, 105120. [Google Scholar]
  64. Brown, R.W.; Chadwick, D.R.; Bending, G.D.; Collins, C.D.; Whelton, H.L.; Daulton, E.; Covington, J.A.; Bull, I.D.; Jones, D.L. Nutrient (C, N and P) enrichment induces significant changes in the soil metabolite profile and microbial carbon partitioning. Soil Biol. Biochem. 2022, 172, 108779. [Google Scholar]
  65. Bourget, M.Y.; Fanin, N.; Fromin, N.; Hättenschwiler, S.; Roumet, C.; Shihan, A.; Huys, R.; Sauvadet, M.; Freschet, G.T. Plant litter chemistry drives long-lasting changes in the catabolic capacities of soil microbial communities. Funct. Ecol. 2023, 37, 2014–2028. [Google Scholar]
  66. Duan, X.; Gunina, A.; Rui, Y.; Xia, Y.; Hu, Y.; Ma, C.; Qiao, H.; Zhang, Y.; Wu, J.; Su, Y.; et al. Contrasting processes of microbial anabolism and necromass formation between upland and paddy soils across regional scales. Catena 2024, 239, 107902. [Google Scholar]
  67. Chen, X.; Xia, Y.; Rui, Y.; Ning, Z.; Hu, Y.; Tang, H.; He, H.; Li, H.; Kuzyakov, Y.; Ge, T.; et al. Microbial carbon use efficiency, biomass turnover, and necromass accumulation in paddy soil depending on fertilization. Agric. Ecosyst. Environ. 2020, 292, 106816. [Google Scholar]
  68. Van De Vreken, P.; Gobin, A.; Baken, S.; Van Holm, L.; Verhasselt, A.; Smolders, E.; Merckx, R. Crop residue management and oxalate-extractable iron and aluminium explain long-term soil organic carbon sequestration and dynamics. Eur. J. Soil Sci. 2016, 67, 332–340. [Google Scholar]
  69. Helfrich, M.; Ludwig, B.; Thoms, C.; Gleixner, G.; Flessa, H. The role of soil fungi and bacteria in plant litter decomposition and macroaggregate formation determined using phospholipid fatty acids. Appl. Soil Ecol. 2015, 96, 261–264. [Google Scholar]
  70. Pan, F.; Li, Y.; Chapman, S.J.; Khan, S.; Yao, H. Microbial utilization of rice straw and its derived biochar in a paddy soil. Sci. Total Environ. 2016, 559, 15–23. [Google Scholar]
Agronomy 15 00806 g001
Figure 1. Changes in SOC in macroaggregates with high and low fertility after aboveground and belowground maize residue addition (a); Changes in SOC in microaggregates with high and low fertility after aboveground and belowground maize residue addition (b). Note: Ff denotes influences by soil fertility level; Fl denotes influences by exogenous maize residues quality; Ff×l means interaction effects by quality of exogenous maize residues and soil fertility level. *, **, and *** indicate significant differences at p < 0.05, p < 0.01, and p < 0.001, respectively. The same labels/definitions apply in the figure below.
Figure 1. Changes in SOC in macroaggregates with high and low fertility after aboveground and belowground maize residue addition (a); Changes in SOC in microaggregates with high and low fertility after aboveground and belowground maize residue addition (b). Note: Ff denotes influences by soil fertility level; Fl denotes influences by exogenous maize residues quality; Ff×l means interaction effects by quality of exogenous maize residues and soil fertility level. *, **, and *** indicate significant differences at p < 0.05, p < 0.01, and p < 0.001, respectively. The same labels/definitions apply in the figure below.
Agronomy 15 00806 g001
Agronomy 15 00806 g002
Figure 2. Maize residue-derived C and native C content in macroaggregates across fertility levels of soils added with different qualities of residues during incubation (a); Maize residue-derived C and native C content in microaggregates across fertility levels of soils added with different qualities of residues during incubation (b). Note: Ff denotes influences by soil fertility level; Fl denotes influences by exogenous maize residues quality; Ff×l means interaction effects by quality of exogenous maize residues and soil fertility level. * and ** indicate significant differences at p < 0.05 and p < 0.01, respectively.
Figure 2. Maize residue-derived C and native C content in macroaggregates across fertility levels of soils added with different qualities of residues during incubation (a); Maize residue-derived C and native C content in microaggregates across fertility levels of soils added with different qualities of residues during incubation (b). Note: Ff denotes influences by soil fertility level; Fl denotes influences by exogenous maize residues quality; Ff×l means interaction effects by quality of exogenous maize residues and soil fertility level. * and ** indicate significant differences at p < 0.05 and p < 0.01, respectively.
Agronomy 15 00806 g002
Agronomy 15 00806 g003
Figure 3. Content of total amino sugar in macroaggregates across fertility levels of soils added with different qualities of residues during incubation (a); Content of total amino sugar in microaggregates across fertility levels of soils added with different qualities of residues during incubation (b). Note: Ff denotes influences by soil fertility level; Fl denotes influences by exogenous maize residues quality. * and ** indicate significant differences at p < 0.05 and p < 0.01, respectively.
Figure 3. Content of total amino sugar in macroaggregates across fertility levels of soils added with different qualities of residues during incubation (a); Content of total amino sugar in microaggregates across fertility levels of soils added with different qualities of residues during incubation (b). Note: Ff denotes influences by soil fertility level; Fl denotes influences by exogenous maize residues quality. * and ** indicate significant differences at p < 0.05 and p < 0.01, respectively.
Agronomy 15 00806 g003
Agronomy 15 00806 g004
Figure 4. Percentage contribution of microbial residue C to SOC in macroaggregate across fertility levels of soils added with different qualities of residues during incubation (a); Percentage contribution of microbial residue C to SOC in microaggregate across fertility levels of soils added with different qualities of residues during incubation (b). Note: Ff denotes influences by soil fertility level; Fl denotes influences by exogenous maize residues quality; Ff×l means interaction effects by quality of exogenous maize residues and soil fertility level. * and ** indicate significant differences at p < 0.05 and p < 0.01, respectively.
Figure 4. Percentage contribution of microbial residue C to SOC in macroaggregate across fertility levels of soils added with different qualities of residues during incubation (a); Percentage contribution of microbial residue C to SOC in microaggregate across fertility levels of soils added with different qualities of residues during incubation (b). Note: Ff denotes influences by soil fertility level; Fl denotes influences by exogenous maize residues quality; Ff×l means interaction effects by quality of exogenous maize residues and soil fertility level. * and ** indicate significant differences at p < 0.05 and p < 0.01, respectively.
Agronomy 15 00806 g004
Table 1. Basic properties of bulk soil samples (2019). HF and LF represent the high- and low-fertility soils, respectively. SOC means soil organic carbon, and TN means total nitrogen. F indicates significant differences between high- and low-fertility soil.
Table 1. Basic properties of bulk soil samples (2019). HF and LF represent the high- and low-fertility soils, respectively. SOC means soil organic carbon, and TN means total nitrogen. F indicates significant differences between high- and low-fertility soil.
SoilHFLFF
SOC (g kg−1)18.0 ± 0.0416.7 ± 0.030.07
TN (g kg−1)1.75 ± 0.451.53 ± 0.000.012
C/N ratio10.3 ± 0.0211.0 ± 0.220.039
δ13C value (‰)21.7 ± 0.0321.5 ± 0.020.006
pH (H2O)6.15 ± 0.166.75 ± 0.010.021
Available N (mg kg−1)153.23 ± 9.44135.70 ± 0.460.137
Available P (mg kg−1)98.77 ± 7.7412.53 ± 0.59<0.001
Available K (mg kg−1)159.67 ± 2.19177.33 ± 9.170.134
Wheat grain yield (kg ha−1)3427.55 ± 483.95966.32 ± 142.830.008
Total amino sugars (mg kg−1)1171.82 ± 20.54990.02 ± 6.090.001
Sand (%)40.6 ± 1.1742.78 ± 0.930.221
Silt (%)27.1 ± 0.6425.92 ± 0.590.249
Clay (%)32.29 ± 0.5331.3 ± 0.390.207
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Ma, N.; Sun, L.; Xu, Y.; Li, S.; Li, J.; Xue, P.; Yang, H.; Mörchen, R.; Wang, J. Soil Fertility and Maize Residue Quality All Effect the Exogenous Carbon Sequestration Only in the Short Term in Macroaggregates, but Not in Microaggregates. Agronomy 2025, 15, 806. https://doi.org/10.3390/agronomy15040806

AMA Style

Ma N, Sun L, Xu Y, Li S, Li J, Xue P, Yang H, Mörchen R, Wang J. Soil Fertility and Maize Residue Quality All Effect the Exogenous Carbon Sequestration Only in the Short Term in Macroaggregates, but Not in Microaggregates. Agronomy. 2025; 15(4):806. https://doi.org/10.3390/agronomy15040806

Chicago/Turabian Style

Ma, Nan, Liangjie Sun, Yingde Xu, Shuangyi Li, Jiayan Li, Pingluo Xue, Hongbo Yang, Ramona Mörchen, and Jingkuan Wang. 2025. "Soil Fertility and Maize Residue Quality All Effect the Exogenous Carbon Sequestration Only in the Short Term in Macroaggregates, but Not in Microaggregates" Agronomy 15, no. 4: 806. https://doi.org/10.3390/agronomy15040806

APA Style

Ma, N., Sun, L., Xu, Y., Li, S., Li, J., Xue, P., Yang, H., Mörchen, R., & Wang, J. (2025). Soil Fertility and Maize Residue Quality All Effect the Exogenous Carbon Sequestration Only in the Short Term in Macroaggregates, but Not in Microaggregates. Agronomy, 15(4), 806. https://doi.org/10.3390/agronomy15040806

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop