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Article

Insights for Soil Improvements: Unraveling Distinct Mechanisms of Microbial Residue Carbon Accumulation under Chemical and Anaerobic Soil Disinfestation

by
Kejian Yang
1,
Jiangtao Yan
1,
Xianwei Wang
1,
Pengtao She
1,
Zhonghui Li
1,
Risheng Xu
2,* and
Yanlong Chen
2,*
1
Shaanxi Hydrogeology Engineering Geology and Environment Geology Survey Center, Xi’an 710068, China
2
School of Ecology and Environment, Northwestern Polytechnical University, Xi’an 710072, China
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(7), 1430; https://doi.org/10.3390/agronomy14071430
Submission received: 30 April 2024 / Revised: 25 June 2024 / Accepted: 28 June 2024 / Published: 30 June 2024
(This article belongs to the Section Soil and Plant Nutrition)
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Abstract

:
Soil disinfestation has been widely used as an effective strategy to improve soil health and crop yield by suppression of soil-borne plant pathogens, but its effect on soil organic carbon (SOC), a crucial factor linked to climate change, remains unknown. A microcosm trial was conducted to evaluate microbial residue carbon (MRC) and its contribution to SOC under chemical soil disinfestation (CSD) with quicklime (QL) and chloropicrin (CP), as well as anaerobic soil disinfestation (ASD) with maize straw (MASD) and soybean straw (SASD). The SOC concentrations were increased by both CSD and ASD. Also, total SOC-normalized MRC concentration was enhanced, with a considerable increase in soil bacterial and fungal MRC, particularly evident under CP and SASD treatment. Due to broad-spectrum biocidal activities, decreased SOC-normalized microbial biomass carbon (MBC) was consistent with the reductions in bacterial and fungal phospholipid fatty acids (PLFAs), consequently increasing MRC accumulation under CSD. Similarly, ASD decreased fungal PLFAs while shifting bacterial PLFAs from aerobic to anaerobic taxa or from gram-negative to -positive taxa, both of which contributed to both MBC and MRC buildup. Collectively, the findings demonstrate that ASD can efficiently increase SOC concentration, with distinct mechanisms underlying MRC generation when compared to traditional CSD.

1. Introduction

Continuous monoculture and outbreaks of soil-borne diseases threaten soil health and sustainable agriculture output in intensive agricultural practices [1]. Chemical soil disinfestation (CSD) employing dazomet or chloropicrin is a reliable strategy to decrease microbial abundance and suppress soil-borne pathogens, due to their broad-spectrum biocidal properties [2,3]. The use of quicklime as a popular chemical additive to control soil acidification and suppress harmful microbes such as plant pathogens is highly prevalent [4]. Nevertheless, the concerns regarding the use of chemicals during CSD have grown considerably in relation to environmental pollution and food safety [5]. Anaerobic soil disinfestation (ASD) represents an environmentally friendly biological alternative to CSD for controlling soil-borne pathogens such as Fusarium oxysporum [6,7]. During ASD, soil is dosed with easily decomposable organic wastes (e.g., green manure, crop straw, or molasses), and then it is saturated with water and covered with plastic film for approximately 3 weeks, creating reductive conditions that stimulate anaerobic degradation of the added organics [8,9,10]. Drastic bacterial community succession supports plant pathogen control during ASD, as it can induce the production of secondary metabolites with anti-pathogenic attributes from anaerobes [11,12,13]. These findings suggest that both CSD and ASD can inhibit or even kill substantial fungi and bacterial populations, thus increasing the microbial residues in soil. However, scarce information is available on microbial residue carbon (MRC) under CSD and ASD. Essentially, MRC is recognized as a primary stable C constituent for long-term soil carbon sequestration, which is crucial for soil health, carbon cycling, and reducing global warming [14,15]. However, the different contributions of MRC to soil organic carbon (SOC) remain unknown under CSD and ASD.
Therefore, a microcosm study was conducted in the present work to quantify MRC, living microbes, and the contribution of MRC to SOC under CSD and ASD. It was hypothesized that compared with CSD, which depletes living microbes without distinction, ASD would increase soil MRC by promoting bacterial community succession and suppressing pathogenic fungi. The objective of the present study was to clarify the different mechanisms underlying the soil MRC accumulation and its contribution to SOC under ASD when compared to traditional CSD.

2. Materials and Methods

2.1. Soil Preparation

The soil used was taken from a vegetable field (108°47″ E, 34°33″ N) in Yangling, Shaanxi, China. The soil suffered from salinization and soil-borne disease caused by overuse of chemical fertilizers and continuous monoculture [9]. The soil was classified as an Anthrosol (FAO, 2006) with a loamy clay texture, having 33.3% clay content (<2 µm) [16]. Other soil properties were as follows: pH 8.29, SOC 8.77 g kg−1, nitrate-N 505 mg kg−1, and ammonium-N 128 mg kg−1. After being transported to the laboratory, the soil was air-dried, homogenized, and passed through an 8 mm sieve, and then the fully air-dried soil was stored at room temperature in dry conditions until the start of the experiment.

2.2. Microcosm Design

The five soil treatments included the following: (1) CK, untreated soil; (2–3) CSD treatments using 1 g kg−1 quicklime (93% purity, 200 mesh, Shantian Chemical Co., Jinan, China) (named QL) or 25 mg kg−1 chloropicrin (99% purity, Dyestuffs and Chemicals Co., Dalian, China) (named CP); (4–5) ASD treatments using 10 g kg−1 maize straw (named MASD) or soybean straw (named SASD) [3,5]. The maize and soybean straw used were collected from the local maize and soybean field at the mature stage, and were ground to a size smaller than 2 mm. The maize straw contained 430 g C kg−1 and 8.08 g N kg−1, while the soybean straw contained 465 g C kg−1 and 26.3 g N kg−1. Each square foam box (212 mm length × 115 mm width × 140 mm height × 15 mm thickness) was filled with a 500 g sample of either soil or soil with prepared additives. All treatments were replicated three times in a randomized complete block design. These boxes were incubated in a greenhouse with a temperature of 25 to 35 °C. The CK and QL retained 70% of the soil field holding capacity for 30 days via periodic irrigation. The CP, MASD, and SASD lasted for 30 days under strict anaerobic conditions via irrigation with 3 cm water over the soil surface and being covered with a transparent plastic film (Polyolefin, thickness: 0.08 mm, Luchen Plastics Co., Weifang, China).

2.3. Sample Collection and Analysis

After incubation, the plastic film was removed and three random soil cores were taken from each replicate, homogenized, and divided into two subsamples. The first subsample was freeze-dried and stored at −80 °C for measurements of phospholipid fatty acids (PLFAs) and amino sugar. The remaining part was air-dried and ground through 0.15 mm sieves to measure SOC.
For amino sugar analysis, soil sample preparation involves hydrolysis with 6 M HCl for 8 h at 105 °C. After the solution was filtered, neutralized (pH: 6.6–6.8), and centrifuged (1006× g, 10 min), the supernatant was lyophilized, and the residue was washed with methanol for recovery of amino sugars. After internal standard myoinositol was added, the amino sugars were transformed into aldononitrile derivatives according to the procedure of [6]. The amino sugars were cetylated with acetic anhydride (v/v = 1:1) under a dichloromethane atmosphere; subsequently, the amino sugars were quantified with a fused silica column (HP-5, size: 25 m × 0.32 mm × 0.25 μm) on an Agilent 7890B gas chromatography platform (Agilent Technologies, Santa Clara, CA, USA) equipped with a flame ionization detector. The sum of the four amino sugars (glucosamine, galactosamine, mannosamine, and muramic acid) was calculated as the total amino sugar content [17]. Bacterial MRC was computed by multiplying the muramic acid concentration by 45, while fungal MRC was computed by subtracting bacterial muramic acid from total glucosamine, assuming that muramic acid and glucosamine occur at a 1 to 2 M ratio in bacterial cells [18,19]. Total MRC was estimated as the sum of fungal and bacterial MRC.
The microbial biomass carbon (MBC) was determined using the chloroform fumigation extraction method [20]. For living microorganisms, the community composition was assessed with PLFA analysis. Briefly, the phospholipid fatty acids were extracted from 8 g (dry weight) frozen soil using a phosphorus buffer/CHCl3/CH3OH at a 0.8:1:2 ratio. After being subjected to methyl esterification and purified, PLFAs were quantified by using an Agilent 7890B gas chromatograph (Agilent Technologies, Santa Clara, CA, USA). Individual PLFA peaks were identified with a Microbial Identification System (MIDI Inc., Newark, DE, USA). The PLFA markers for fungi, saprotrophic fungi (SF), and arbuscular mycorrhiza fungi (AM), bacteria, aerobic and anaerobic bacteria, and gram-positive and -negative bacteria are listed in Table 1.
The SOC concentration was measured with the Walkley–Black method [9]. Briefly, the concentrated H2SO4 and potassium dichromate were used to oxidize the SOC in the soil samples at 135 °C for 30 min, and then ferrous sulfate eliminated the excess dichromate. Thus, the consumed potassium dichromate was used to calculate SOC content. For the microbial biomass carbon (MBC), the organic C content in extracts was determined by comparing the difference between fumigated and non-fumigated samples, and then MBC was calculated based on the normalized coefficient 0.45.

2.4. Statistical Analysis

The aim of this study was to assess the differences in all detected SOC and microbial parameters under CSD and ASD with one-way ANOVA. Significant differences in means between treatments was assessed by the LSD method and indicated by using different lowercase letters at the 5% level. Linear regressions were conducted to identify the correlations among MRC, MBC, and microbial PLFAs. Statistical analysis was implemented by using SPSS version 20 for Win-10 (IBM Co., New York, NY, USA).

3. Results and Discussion

3.1. Soil Organic C Fractions and Concentration after ASD and CSD

The SOC concentration was not affected by CP, but increased by 6.8% with QL, 12% with MASD, and 21% with SASD as compared to CK (Figure 1A). This indicates that ASD resulted in a higher SOC concentration than CSD due to exogenous C input. As a straw management method, ASD may improve SOC protection by particle- and mineral-associated organic carbon [8,9]. On the other hand, microbial growth was promoted by input straw in ASD treatments; thus, the demand for microbial N was increased. That is to say, the high C/N ratio of the straw meant that enough N to meet the demand of microorganisms was needed, or it could restrict the litter decomposition. However, in general, the N in farmland is lacking [17]. As a consequence, the higher SOC levels under SASD were related to the lower C/N ratio of soybean straw, which accelerated its degradation for SOC preservation [24]. Calcium ions from QL served as the bonding bridges in the formation of organo-mineral complexes, chemically shielding SOC from microbial attack, and thus relatively increased the retention of SOC [25]. Moreover, the microbial necromass also contributed to the SOC accumulation under CSD and ASD.

3.2. The Effects of ASD and CSD on Soil Components and Concentrations of Amino Sugars

Both CSD and ASD increased soil concentrations of amino sugars and their components (Table 2), indicating the buildup of microbial residues. The concentration of SOC-normalized MRC displayed the order of CP > SASD > MASD > QL > CK (Figure 1B). This implied increased SOC stabilization under CSD and ASD because MRC is recognized as a soil-stable C pool [14]. Soil fumigation with CP results in high toxicity to living organisms due to a biothiol reaction, which disrupts multiple targets within biological cells [26]. Interestingly, greater spikes were observed in SOC-normalized fungal MRC after CP treatment (Figure 1C), most likely due to the higher sensitivity of fungi to CP than bacteria. Furthermore, fungal MRC has a slower turnover than bacterial MRC due to the higher biostability of chitin and melanin from fungal residues [7], which favors fungal MRC retention. However, CP did not enhance the SOC concentration, possibly because increased MRC was offset by native SOC mineralization. Once exposed to chemical stress, soil microorganisms tend to obtain more energy for resisting stress by respiration using SOC [27]. The QL could produce an acutely exothermic reaction with water and raise the soil pH to kill temperature- and pH-sensitive microbes [28]. This led to identical induction of SOC-normalized bacterial and fungal MRC. The QL treatment accumulated far less MRC than the CP, owing to its mild sterilization effect.
During ASD, as the soil is saturated and plastic-mulched, the addition of substances promotes the microbial shift from aerobic to anaerobic taxa [8], thus increasing necromass accumulation of aerobic microbes. When comparing SASD and MASD, the higher fungal MRC concentration occurred under the former, while the latter exhibited higher bacterial MRC, due to varying C/N ratios of added straw (Figure 2C). The bacterial biomass had a lower C/N ratio than the fungal biomass [20], indicating that bacterial growth requires a lower C/N ratio than fungal growth. Maize straw with a C/N of 53.2 displayed the N limitation for bacterial growth, which expedited the bacterial apoptosis and thus induced more bacterial MRC accumulation during MASD. However, during SASD utilizing soybean straw (C/N, 17.6), bacterial growth was enhanced while fungal growth was competitively inhibited, promoting fungal collapse and MRC buildup. The SOC-normalized MBC dropped under CSD (i.e., 26% under QL and 64% under CP treatment), but increased under ASD (i.e., 31% under MASD and 68% under SASD) (Figure 2B). This demonstrated that the sterilizing effect of biocides drove CSD-induced MRC accumulation, whereas accelerated microbial succession caused by straw addition and anoxia stress contributed to ASD-induced MRC accumulation (Figure 3A). In comparison to CK, the ratio of MBC/MRC was unaffected by ASD but lowered by CSD (i.e., 42% for QL and 80% for CP) (Figure 1D). This suggested a higher MRC buildup coefficient under CSD, which was most likely related to the low activity and biomass of viable microbes after CSD (see MBC in Figure 1D), minimizing soil MRC turnover. However, the increased activity of viable microorganisms after ASD means they most likely used microbial residues as an energy source, adversely affecting soil MRC accumulation.

3.3. Changes in Phospholipid Fatty Acids (PLFAs) and Their Relationship with Soil Organic C after ASD and CSD

Total PLFAs were decreased by CSD, while they were increased by ASD, which was in agreement with the pattern of soil MBC (Figure 1B and Figure 2A). The PLFAs of soil fungi and arbuscular mycorrhiza were reduced by CSD and ASD, resulting in depleted fungal PLFAs (Figure 2B). Essentially, most fungi are strictly aerobic and thus enriched in forest soil, wherein plant residues serve as a source of abundant energy and nutrients [29]. Despite crop straw addition into the soil, ASD created a strictly oxygen-free environment, which induced massive death of living soil fungi and arbuscular mycorrhiza for fungal necromass accumulation. The negative correlation between fungal MRC and PLFAs under ASD supports this view (Figure 3B). Regarding bacterial groups, total and specific PLFAs were decreased by CSD, while the PLFAs of aerobic and gram-negative bacteria were decreased and the PLFAs of anaerobic and gram-positive bacteria were increased by ASD (Figure 2C,D). Broad-spectrum antibacterials from CSD synchronously suppressed anaerobic and aerobic gram-negative or gram-positive bacteria, leading to MRC accumulation (Figure 3C). Nevertheless, the addition of crop straw during ASD promoted bacterial community succession from aerobic taxa to obligate/facultative anaerobic taxa [8]. Generally, gram-positive bacteria display higher resistance to environmental stress (e.g., temperature, nutrients, moisture, and hypoxia) than gram-negative bacteria due to the thicker murein layer of their cell walls [30]. Thus, straw addition during ASD consistently enhanced the proliferation of gram-positive bacteria under anaerobic stress (Figure 2D). Therefore, bacterial MRC accumulation under ASD could be attributed to a reduction in living aerobic or gram-negative bacteria (Figure 3D).
However, the significant depletion of living microbes under CSD has adverse consequences in terms of soil vitality and overall ecosystem service functions, which generates cautionary concern regarding their use in agricultural practices. Therefore, ASD serves as a promising strategy to improve soil health by increasing SOC, controlling soil-borne diseases, and addressing other soil barriers such as acidification, salinization, and heavy metal pollution [8,11]. Given the short duration of ASD practice, long-term evaluation should be conducted to better understand the subsequent fate of MRC in soil.

4. Conclusions

These critical findings have important implications in that both CSD and ASD increase SOC stability through MRC buildup despite their distinct mechanistic processes for MRC generation (Figure 4). Briefly, the toxicity of biocides (i.e., CP and QL) depleted the living microorganisms, including bacteria and fungi, indicating soil microbial death contributed to MRC buildup. However, living fungi were depleted and living bacteria were shifted from aerobic to anaerobic taxa or from gram-negative to -positive taxa during ASD, both contributing to MRC accumulation. In addition, soils under ASD tended to have higher microbial biomass and necromass accumulation compared to soils under CSD. To the best of the authors’ knowledge, this is the first report on increased soil MRC accumulation and its contribution to SOC under CSD and ASD. These findings indicate that apart from remediation of degraded soil, ASD can also efficiently increase SOC concentration.

Author Contributions

Conceptualization, K.Y. and Y.C.; methodology, Y.C.; software, R.X.; validation, K.Y., X.W. and Z.L.; investigation, K.Y., J.Y., P.S., X.W. and Z.L.; resources, K.Y.; data curation, K.Y., J.Y., P.S., X.W. and Z.L.; writing—original draft preparation, Y.C. and R.X.; writing—review and editing, K.Y., R.X. and Y.C.; project administration, Y.C. and R.X.; funding acquisition, K.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Research and Development of Microorganism Fertilizer (Special project for ecology in Shaanxi Province: Grant No. 202202).

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agronomy 14 01430 g001
Figure 1. Concentrations of soil organic carbon (SOC) (A), SOC-normalized microbial biomass carbon (MBC), and microbial residue carbon (MRC) (B,C), and the ratio of MBC to MRC (D) under chemical soil disinfestation with quicklime (QL) and chloropicrin (CP), as well as anaerobic soil disinfestation with maize straw (MASD) and soybean straw (SASD). Different lowercase letters denote significant differences (p ≤ 0.05) between soil treatments for each parameter. The values of the histogram are means, while error bars represent standard errors (n = 3).
Figure 1. Concentrations of soil organic carbon (SOC) (A), SOC-normalized microbial biomass carbon (MBC), and microbial residue carbon (MRC) (B,C), and the ratio of MBC to MRC (D) under chemical soil disinfestation with quicklime (QL) and chloropicrin (CP), as well as anaerobic soil disinfestation with maize straw (MASD) and soybean straw (SASD). Different lowercase letters denote significant differences (p ≤ 0.05) between soil treatments for each parameter. The values of the histogram are means, while error bars represent standard errors (n = 3).
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Figure 2. Concentrations of total PLFAs (A), fungal PLFAs (B), and bacterial PLFAs (C,D) under chemical soil disinfestation with quicklime (QL) and chloropicrin (CP), as well as anaerobic soil disinfestation with maize straw (MASD) and soybean straw (SASD). Different lowercase letters denote significant differences between soil treatments for each parameter. The values of the histogram are means, while error bars represent standard errors (n = 3).
Figure 2. Concentrations of total PLFAs (A), fungal PLFAs (B), and bacterial PLFAs (C,D) under chemical soil disinfestation with quicklime (QL) and chloropicrin (CP), as well as anaerobic soil disinfestation with maize straw (MASD) and soybean straw (SASD). Different lowercase letters denote significant differences between soil treatments for each parameter. The values of the histogram are means, while error bars represent standard errors (n = 3).
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Figure 3. The relationships between soil microbial residue carbon (MRC) and microbial biomass carbon (MBC) (A), fungal MRC and PLFAs (B) under chemical soil disinfestation (CSD) and anaerobic soil disinfestation (ASD); bacterial MRC and PLFAs under CSD (C) and ASD (D).
Figure 3. The relationships between soil microbial residue carbon (MRC) and microbial biomass carbon (MBC) (A), fungal MRC and PLFAs (B) under chemical soil disinfestation (CSD) and anaerobic soil disinfestation (ASD); bacterial MRC and PLFAs under CSD (C) and ASD (D).
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Figure 4. A conceptual diagram illustrating the responses of soil microbes and the mechanisms of microbial residue carbon (MRC) generation under chemical soil disinfestation with quicklime (QL) and chloropicrin (CP), as well as anaerobic soil disinfestation with maize straw (MASD) and soybean straw (SASD).
Figure 4. A conceptual diagram illustrating the responses of soil microbes and the mechanisms of microbial residue carbon (MRC) generation under chemical soil disinfestation with quicklime (QL) and chloropicrin (CP), as well as anaerobic soil disinfestation with maize straw (MASD) and soybean straw (SASD).
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Table 1. The markers of PLFAs for bacteria and fungi in the soil.
Table 1. The markers of PLFAs for bacteria and fungi in the soil.
MicroorganismsMarkers of PLFAsReferences
Fungi18:1w9c[20]
Arbuscular mycorrhiza16:1ω5c[21]
Saprophytic fungi18:2ω6, 18:1ω9[21]
Bacteria11:0; 12:0; 13:0; 14:0; 15:0; 16:1; 17:0; 18:1; 19:0; i15:0; a15:0; i16:0; a17:0; i17:0; 16:1ω7c; 18:1ω7c[20]
Anaerobic bacteriai-15:0; a-15:0; a-17:0; i-17:0; a-17:0[22]
Aerobic bacteria14:1; 18:1ω7c; 15:1ω6c; 16:1ω7c; 16:1ω7t; 18:1ω9c; 18:1ω9t[22]
Gram- positive bacteriai15:0; a15:0; i16:0; 16:1w9c; 16:1w7; i17:0; a17:0; 18:0; 18:1w9c[23]
Gram- negative bacteriai16:1w7c; i17:1w8c; cy17:0; 18:1w7c; 18:1w5c; cy19:0[23]
Table 2. Concentrations of soil amino sugar and its components under chemical soil disinfestation (CSD) and anaerobic soil disinfestation (ASD).
Table 2. Concentrations of soil amino sugar and its components under chemical soil disinfestation (CSD) and anaerobic soil disinfestation (ASD).
Soil Parameters (μg g−1 Soil)CKQLCPMASDSASD
Amino sugars 435 # d473 cd635 a519 c576 b
Glucosamine264 b281 b395 a297 b377 a
Mannosamine9.78 c11.3 bc12.4 ab14.4 a9.19 c
Galactosamine135 c147 c198 a185 ab162 bc
Muramic acid23.0 d26.6 c30.3 b33.9 a28.1 bc
# Values are means (n = 3). Different lowercase letters indicate a significant difference between soil treatments.
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Yang, K.; Yan, J.; Wang, X.; She, P.; Li, Z.; Xu, R.; Chen, Y. Insights for Soil Improvements: Unraveling Distinct Mechanisms of Microbial Residue Carbon Accumulation under Chemical and Anaerobic Soil Disinfestation. Agronomy 2024, 14, 1430. https://doi.org/10.3390/agronomy14071430

AMA Style

Yang K, Yan J, Wang X, She P, Li Z, Xu R, Chen Y. Insights for Soil Improvements: Unraveling Distinct Mechanisms of Microbial Residue Carbon Accumulation under Chemical and Anaerobic Soil Disinfestation. Agronomy. 2024; 14(7):1430. https://doi.org/10.3390/agronomy14071430

Chicago/Turabian Style

Yang, Kejian, Jiangtao Yan, Xianwei Wang, Pengtao She, Zhonghui Li, Risheng Xu, and Yanlong Chen. 2024. "Insights for Soil Improvements: Unraveling Distinct Mechanisms of Microbial Residue Carbon Accumulation under Chemical and Anaerobic Soil Disinfestation" Agronomy 14, no. 7: 1430. https://doi.org/10.3390/agronomy14071430

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