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Building microbial consortia to enhance straw degradation, phosphorus solubilization, and soil fertility for rice growth

Microbial Cell Factories volume 23, Article number: 232 (2024) Cite this article

Abstract

Straw pollution and the increasing scarcity of phosphorus resources in many regions of China have had severe impacts on the growing conditions for crop plants. Using microbial methods to enhance straw decomposition rate and phosphorus utilization offers effective solutions to address these problems. In this study, a microbial consortium 6 + 1 (consisting of a straw-degrading bacterium and a phosphate-solubilizing bacterium) was formulated based on their performance in straw degradation and phosphorus solubilization. The degradation rate of straw by 6 + 1 microbial consortium reached 48.3% within 7 days (The degradation ability was 7% higher than that of single bacteria), and the phosphorus dissolution rate of insoluble phosphorus reached 117.54 mg·L− 1 (The phosphorus solubilization ability was 29.81% higher than that of single bacteria). In addition, the activity of lignocellulosic degrading enzyme system was significantly increased, the activities of endoglucanase, β-glucosidase and xylanase in the microbial consortium were significantly higher than those in the single strain (23.16%, 28.02% and 28.86%, respectively). Then the microbial consortium was processed into microbial agents and tested in rice pots. The results showed that the microbial agent significantly increased the content of organic matter, available phosphorus and available nitrogen in the soil. Ongoing research focuses on the determination of the effects and mechanisms of a functional hybrid system of straw degradation and phosphorus removal. The characteristics of the two strains are as follows: Straw-degrading bacteria can efficiently degrade straw to produce glucose-based carbon sources when only straw is used as a carbon source. Phosphate-solubilizing bacteria can efficiently use glucose as a carbon source, produce organic acids to dissolve insoluble phosphorus and consume glucose at an extremely fast rate. The analysis suggests that the microbial consortium 6 + 1 outperformed individual strains in terms of both performance and application effects. The two strains within the microbial consortium promote each other during their growth processes, resulting in a significantly higher rate of carbon source consumption compared to the individual strains in isolation. This increased demand for carbon sources within the growth system facilitates the degradation of straw by the strains. At the same time, the substantial carbon consumption during the metabolic process generated a large number of organic acids, leading to the solubilization of insoluble phosphorus. It also provides a basis for the construction of this type of microbial consortium.

Introduction

With the ongoing development of global agriculture and the increasing food production demands, the use of chemical fertilizers and the generation of agricultural waste have increased gradually [1, 2]. This has resulted in an imbalance in soil nutrient ratios and initiated a detrimental cycle in crop growth [3]. Agricultural waste pollution, particularly stemming from the improper disposal of straw resources, such as through burning, is progressively becoming a more serious issue [4]. Notably, straw is rich in carbon, nitrogen, and phosphorus, making it an environmentally friendly resource with great potential in agricultural production if used reasonably [5]. Upon returning straw to the field, microorganisms decompose and release all kinds of nutrients present in straw and infiltrate into the soil, effectively renewing the soil’s nutrient status [6, 7]. This process, termed straw degradation, serves to fertilize the soil and enhance its overall quality. Microbial degradation of straw proves to be one of the most effective ways to effectively promote straw decomposition and maximize the utilization rate of straw bio-resources [8,9,10]. The construction of a functional degrading bacterial flora of crop straw in-situ return to the field is one of the most effective approaches to promote the full utilization of straw resources, improve soil quality, foster sustainable agricultural production, and enhance agricultural production in China [11]. The establishment of functional degradation bacteria for crop straw in-situ return to the field is of great significance in China. It not only promotes the comprehensive utilization of straw resources but also enhances soil fertility, contributing to the sustainable development of agriculture [12, 13].

The increasing depletion of phosphorus resources has become a worldwide problem, hindering the sustainable development of agriculture on a global scale [14]. Phosphorus plays a significant role in limiting crop yields. However, its utilization in the soil is inefficient since more than 90% of phosphorus is present in the ground in the form of orthophosphate and insoluble phosphate [15, 16]. Substantial amounts of soluble phosphorus fertilizers are commonly applied to the soil in production practices in order to increase crop yields. However, most of these phosphorus resources become immobilized by the soil, rendering them inaccessible for plant absorption. This leads to an efficiency rate of only 10–30% for phosphorus uptake by crops, as nutrient transformation and utilization become a challenge due to reduced microbial activity in the soil [17,18,19]. In addition, long-term phosphate fertilizer application can result in soil acidification, water pollution, and eutrophication [20]. Phosphorus-solubilizing bacteria offer a solution to this challenge by dissolving insoluble phosphates into an activated phosphorus state, thereby “mobilizing” farmland soil phosphorus resources [21]. This process enhances soil fertility, reduces the use of chemical phosphate fertilizers and high-grade phosphorus resources, and addresses the issue of inefficient soil phosphorus activation and resource depletion. In addition, it can be effectively used to develop and utilize a large number of low-grade phosphate fertilizers in China [22]. It can also effectively develop and utilize a large number of low-grade phosphorus ores in China, thus solving the environmental pollution problems caused during the mining and processing of phosphorus ores. Phosphorus-solubilizing bacteria have attracted much attention due to their environmental safety, cost-effectiveness, high efficiency, and so on [23].

Studies on microorganisms involved in straw degradation and phosphorus solubilization have made great progress, ranging from experimental material pre-treatment and mechanistic studies to practical applications [24, 25]. Straw degradation and phosphorus solubilization are mostly centered on pH, organic acids, related enzyme activities, and sugars in mechanistic studies [26]. However, little research has been reported on the combined treatment of straw-degrading bacteria with phosphorus-solubilizing bacteria. In this study, an artificial microbial consortium was created by combining straw-degrading bacteria with phosphorus-solubilizing bacteria and co-cultivating them. This consortium demonstrated the ability to both degrade straw and solubilize inorganic, insoluble phosphorus sources. The two functional bacteria in the microbial consortium have synergistic effects. The sugars produced by straw-degrading bacteria during the straw degradation process can be consumed by the growth of the two strains and the phosphorus-solubilizing bacteria. The consumption of a substantial amount of sugar led to a shortage of the carbon source content in the reaction system, creating a carbon source of stress that promotes sugar formation produced by straw degradation. On the other hand, various sugar absorption methods produced organic acids through the transformation of the sugar metabolism pathway, promoting phosphorus solubilization. It is worth noting that this study is the first time to combine straw-degrading bacteria with phosphate-solubilizing bacteria to treat soil straw accumulation and phosphorus deficiency. The establishment of this microbial consortium holds great significance for the efficient utilization of straw and phosphorus resources, the development of microbial fertilizers, and the sustainable development of modern agriculture [27, 28].

Materials and methods

Test strains

Three straw-degrading bacteria (ZJW-6、ZLZ-3 and DA-24) were isolated from different locations during the pre-laboratory period, including Zhiluo Town, Shaanxi Province (E 109.00, N 36.00), Zhangjiawan, Shaanxi Province (E 109.90, N 36.61), Da’an County, Baicheng City, Jilin Province (E 124.29, N 45.51), and Nong’an County, Changchun City, Jilin Province, China (E 125.75, N 44.91). In addition, three phosphorus-solubilizing bacteria (wj1、wj5 and wj6) were isolated from the inter-root soil of soybeans at Jilin Agriculture University’s soybean experimental site (E 125º19, N 43º43). Soil samples obtained at various locations were sent to the first author’s laboratory (School of Life Sciences, Jilin Agricultural University) for screening of bacteria, in which the strain with the strongest straw degradation ability is ZJW-6 (Cellulomonas iranensis), and the strain with the strongest phosphorus solubilization ability is wj1 (Pseudomonas sp.).

Strain culture substrate and conditions

The test strains were cultured using Luria-Bertani (LB) medium containing 10 g/L tryptone, 5 g/L yeast extract, 10 g/L NaCl. In addition, 5 g/L beef extract, 5 g/L peptone, 0.25 g/L MgSO4-7H2O, and 1 g/L(NH4)2SO4, 5 g/L Ca3(PO4)2, 0.2 g/L KCl, 0.5 g/L MgCl-6H2O, 0.3 g/L NaCl, 0.03 g/L MnSO4-H2O, and 2.5 g/L straw as co-culture medium (CCM).

The straw, obtained from JINONG 667, a japonica conventional rice variety from Changchun, Jilin Agricultural University (Jilin, China), was washed, dried at 60 °C until the quality was stable and uniformly dried, cut into 1-cm segments, and stored in sealed plastic bags at room temperature until use.

The strains were maintained at the same concentration (OD = 0.8) when inoculated into CCM using co-inoculation at a ratio of (1:1, 1%). The incubation was carried out in a constant temperature shaker (30 °C, 180 rpm).

Construction, screening microbial consortium, and capacity determination

Pairs of straw-degrading bacteria (ZLZ-3, ZJW-6, DA-24) and phosphorus-dissolving bacteria (wj1, wj5, wj6) were combined to form a microbial consortium. The straw degradation and phosphorus solubilization abilities of each combination were determined within seven days, and the combination with the best results was selected for further experiments.

Determination of straw degradation capacity

Straw degradation capacity was determined by measuring the weight of straw in the CCM before and after treatment with the microbial consortium. The weight was determined by filtering and washing the straw in the CCM and drying it at 60 °C until the mass was constant. The degradation rate was calculated using the following formula:

Straw degradation rate = (initial straw weight – straw weight after degradation)/initial straw weight x 100%.

Determination of phosphorus solubilizing capacity

The soluble phosphorus content in the CCM was determined using the molybdenum blue colorimetric method [29]. Capacity determination was performed over seven days, with one sample collected per day, resulting in nine sets of treatments, each with three replicates.

Microbial consortium growth characteristics

The seed solution of the best microbial consortium, with OD600 = 0.8, and the single strains constituting the consortium were diluted to 1 × 10− 7 using sterile water. The number of colonies from the three treatments was recorded within 72 h using the dilution-coated plate method, with one sample collected every 12 h. The total number of colonies was the total number of single colonies in the field of view of the coated plate. In addition, the growth of the best consortium and the single strain constituting the consortium were evaluated in this way at each time point. Growth of the best consortium and the single strain constituting the consortium at each time point. Plate photographs were taken at a dilution of 1 × 106, and the experiment was repeated three times.

Total reducing sugars and pH changes

The effect on total reducing sugars and pH was assessed before and after the recombination of single strains. Total reducing sugar content was measured using the 3,5-dinitrosalicylic acid method for the redox reaction with reducing sugars at 540 nm. pH was determined using an ultra-precision pH meter (FiveEasy Plus, Mettler Toledo, Switzerland).

Qualitative and quantitative analysis of reducing sugars and organic acids

Reducing sugars and organic acids in microbial consortia were determined using an AB Triple TOF 6600 mass spectrometer (AB SCIEX), an Agilent 1290 Infinity LC ultrahigh-pressure liquid chromatograph (Agilent), a Vanquish UHPLC ultrahigh-pressure liquid chromatograph (Thermo), and a low-temperature high-speed centrifuge (Eppendorf 5430R). Specific methods for the determination of organic acids refer to Wei et al. [30], determination of reducing sugar reference Tao et al. [31]. A Waters ACQUITY UPLC BEH Amide 1.7 μm, 2.1 mm×100 mm column, acetonitrile (Merck, 1499230-935), and ammonium acetate (Sigma, 70221) were used for qualitative and quantitative analyses.

Enzymatic analysis

The culture substrate in CCM was centrifuged at 12,000 rpm for 10 min to remove the bacterial bodies and suspended impurities. The supernatant was also used as the enzyme source to determine the activity of each enzyme over a period of seven days. Lignin peroxidase, laccase, and manganese peroxidase were determined based on the Mei technique [32]. β-glucosidase was determined based on Saha BC’s method [33], endoglucanase based on Haggag’s method [34], and xylanase based on Liang’s method [35].

The key enzymes of the predicted pathway were assayed as follows: phosphofructokinase was determined using the phosphofructokinase activity assay kit MAK093, pyruvate kinase was assayed with the pyruvate kinase activity assay kit MAK072, hexokinase was assayed with the hexokinase activity assay kit MAK091, and β-glucosidase was assayed using the β-glucosidase activity assay kit MAK129, all of which were sourced from Sigma-Aldrich (Merck, USA). In addition, endoglucosidase was detected using the endo-β-1,4-glucanase assay kit GMS047 (Isejiu Biotechnology Co., Ltd., Lianyungang, Jiangsu, China).

Analysis of straw degradation components

The content of cellulose, hemicellulose, and lignin was mainly analyzed after straw degradation by different treatments. The method used followed Zhan’s technique (Zhan, Lin et al., 2023).

Bacterial agent

The seed solution of the CCM-activated ZJW-6, wj1, and the microbial consortium was centrifuged at 12,000 rpm for 5 min. The supernatant was removed and centrifuged again three times. The bacteria were then mixed with humic acid fertilizer at a 1:2 ratio, dried at room temperature, processed into a powder, sealed, and stored at 4 °C. The humic acid fertilizer specifications were as follows: humic acid ≥ 30%, organic matter ≥ 70%. n, p, k ≥ 5%, water solubility ≥ 60%, pH = 8 (Heilongjiang Harvest Co., Ltd., China).

Rice promotion practical test

Rice varieties were obtained from Jilin Agricultural University, specifically Japonica conventional rice JINONG 667 from Changchun (Jilin, China). Cylindrical, opaque plastic buckets, each with a 15 cm diameter and 30 cm height, were used. Each bucket was filled with 5 kg of subsoil. Five different treatments were established, including viz.ZJW-6, wj1, 6 + 1, treatment with humic acid only (CK*), and a control with no special treatment (CK). The dried straws from Sect. 2.1 were cut into 10 cm-long segments and filled with 5 g each in nylon mesh bags, with 3 bags per pot. 8 g of mycorrhizal fungus (> 1 billion live bacteria/pot) was applied in the 10–15 cm soil layer. Three application points were designated in each pot, with 8 rice seeds planted in each point, and fine soil was evenly spread over the top of the potted plants. The plants were thoroughly watered, with subsequent irrigation every two days and daily manual weeding (5 treatments × 2 periods × 10 replications) (Table 1).

Table 1 Basic information of each treatment (day 0)
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Analysis of the soil nutrient environment

Rice soil-related indicators were recorded and analyzed 30 and 60 days after microbial agent application. Soil indexes were determined using the NaHCO3 leaching method to determine quick-acting phosphorus in the soil and the NaOH alkali diffusion method to determine quick-acting nitrogen. They were also determined using the NH4OAc leaching-flame spectrophotometer method to determine quick-acting potassium and the potassium dichromate volumetric method with an external heating approach to resolve underground organic matter.

Evaluation of the rice root promotion effect

Root vigor was determined using triphenyltetrazolium chloride (TTC). For the above-ground portion, intact above-ground tissues and rice roots were intercepted, washed with distilled water, and then dried. The surface water from roots and above-ground parts was blotted with filter paper, dried, and weighed at 65 °C, and the root-to-crown ratio (R/S) was calculated. The net photosynthetic rate of the above-ground parts was determined using a portable photosynthesis measurement system (LI-6400XT, LI-COR, USA). The chlorophyll levels were also measured with a chlorophyll analyzer (SPAD-502PLUS, Konica Minolta, Japan) to record chlorophyll content in the upper, middle, and lower portions of the leaves. Straw structure was further analyzed under different treatments using a scanning transmission electron microscope (SU8010, Hitachi, Japan), and root growth was scanned using a root scanner (i800plus, MICROTEK, Shanghai), and pictures of rice growth were taken.

Results

Analysis of straw degradation and phosphorus solubilization ability of test strains

The ability of the tested strains is shown in Fig. 1. In the determination of straw degradation ability, wj1, wj5 and wj6 had no straw degradation ability, and ZJW-6 had the strongest straw ability, reaching 41.3% on the seventh day. ZJW-6, ZLZ-3 and DA-24 had no phosphate-solubilizing ability, and wj1 had the strongest phosphate-solubilizing ability, reaching 82.5 mg·L− 1.

Fig. 1
figure 1

The straw degradation ability and phosphorus solubilization ability of the tested strains. A: Determination of straw degradation ability, B: Determination of phosphate solubilization ability. (The results were shown in a circular grouping histogram, and the number after the name of the strain was the repeated number of the same experimental group, p < 0.05)

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Evaluation of microbial consortia straw degradation and phosphorus solubilization capacity

The straw-degrading bacteria (ZLZ-3, ZJW-6, DA-24) and phosphorus-solubilizing bacteria (wj1, wj5, wj6) were paired to form a microbial consortium. The dynamic changes in straw degradation rates and soluble phosphorus content of each microbial consortium were quantitatively analyzed in the CCM within seven days (Fig. 2).

In the determination of straw degradation capacity, the degradation rate of all microbial consortia slowly increased from the third day. The microbial consortium composed of ZJW-6 and wj1 (6 + 1) achieved the highest straw degradation rate of 48.33% on the seventh day. Regarding phosphorus solubilization capacity, the efficiency decreased by the third day, with the 6 + 1 consortium reaching its peak on the sixth day, resulting in an increase of soluble phosphorus content by 117.54 mg·L− 1. The straw degradation and phosphorus solubilizing capacity of the 6 + 1 microbial consortium were significantly higher than those of the other combinations, making it the choice for subsequent studies.

Fig. 2
figure 2

Capability analysis of microbial consortiums. A: Straw degradation rate in 7 days. B: Phosphorus solubilization in 7 days

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Growth characteristics of the microbial consortium 6 + 1

Changes in the colony number of ZJW-6, wj1, and the microbial consortium 6 + 1 were recorded in diluted coated plates over seven days to initially investigate the growth characteristics of the microbial consortium 6 + 1 (Fig. 3).

Pure cultures of ZJW-6 and wj1 had up to 11 and 9 colonies, respectively, over seven days. In contrast, the mixed culture of the microbial consortium 6 + 1 resulted in up to 23 colonies. The co-culture treatment growth effect exhibited non-antagonistic quantitative growth compared to the pure cultures of the individual strains.

Fig. 3
figure 3

Growth of ZJW-6, wj1 and microbial consortium 6 + 1. A: Number of colonies in each treatment in 72 h. B: Growth of the wj1. C: Growth of the ZJW-6. D: Growth of the microbial consortium 6 + 1

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Comparison of straw degradation and phosphorus dissolving capacity of ZJW-6 and wj1 with microbial consortia

Straw degradation capacity and dissolved phosphorus dynamics of microbial consortium 6 + 1, culture-only treatment ZJW-6, and culture-only treatment wj1 were quantitatively assessed within seven days (Fig. 4).

In the determination of straw degradation capacity within seven days, the microbial consortium 6 + 1 achieved a straw degradation rate of 48.30%, while the straw-degrading bacteria ZJW-6 reached 41.3%. Neither the phosphorus-solubilizing bacteria wj1 nor the CK treatments demonstrated straw degradation capability. Any change in straw weight in the CCM containing these treatments was attributed to the slight decomposition of straw in the CCM medium during autoclaving [36]. The soluble phosphorus content of microbial consortium 6 + 1 reached up to 117.54 mg·L− 1 in the comparison of phosphorus solubilizing capacity, while the soluble phosphorus content of wj1 reached a maximum of 82.5 mg·L− 1. Both the straw-degrading bacteria and CK treatments showed no phosphorus solubilization capacity.

These findings indicate that the microbial consortium 6 + 1 had both straw degrading and phosphorus solubilizing abilities, and both abilities were significantly higher than those of the individual-bacteria treatments that constitute the consortium. The reasons for the enhanced abilities of microbial consortium 6 + 1 compared to those of single bacteria were analyzed later.

Fig. 4
figure 4

Comparison of each treatment capacity before and after 6 + 1 combination of microbial consortia. A: Straw degradation capacity in 7 days. B: Phosphorus solubilizing capacity in 7 days

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Enzymatic analysis

The experimental culture medium is inorganic insoluble phosphorus source, the activity of straw degradation enzyme system will be determined only. The activities of the microbial consortium 6 + 1 and the ZJW-6 pure culture straw-degrading enzyme system in the CCM were examined for seven days in this section (Fig. 5).

All the enzymes (endoglucanase, β-glucosidase, xylanase, lignin peroxidase, manganese peroxide, and laccase) measured by the microbial consortium, peaked on the third day, reaching values of 37.27 U·ml− 1, 19.60 U·ml− 1, 21.66 U·ml− 1, 15.27 U·ml− 1, 7.53 U·ml− 1, and 0.16 U·ml− 1, respectively. During the determination of ZJW-6 enzyme activities, endoglucanase, β-glucosidase, xylanase, lignin peroxidase, and laccase reached their highest levels on the fourth day, with values of 28.64 U·ml− 1, 14.11 U·ml− 1, 15.41 U·ml− 1, 17.11 U·ml− 1, and 0.11 U·ml− 1, respectively, while manganese peroxidase reached its highest on the fifth day at 6.13 U·ml− 1. The activity was highest at 6.13 U·ml− 1. For all enzymes, microbial consortium 6 + 1 had higher activity than ZJW-6 pure culture, except for lignin peroxidase.

Fig. 5
figure 5

Straw-degrading enzyme system activity of ZJW-6 and microbial consortium 6 + 1 in seven days. A: Endoglucanase. B: β-glucosidase. C: Xylanase. D: Lignin peroxidase. E: Manganese peroxidase. F: Laccase

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Determination of total reducing sugars, pH

The dynamics of total reducing sugars and pH of microbial consortia 6 + 1, ZJW-6, and wj1 were detected over a seven-day period (Fig. 6).

In the total reducing sugar content detection process, there was no significant difference between the total reducing sugar content of the wj1 pure culture and the CK treatment within seven days. This was attributed to the fact that wj1 lacks straw degradation ability to produce reducing sugars. Also, the small amount of reducing sugar present in the pure culture of wj1 and the CK treatment was caused by the minimal exudation from the straw after autoclaving. Microbial consortiums 6 + 1 and ZJW-6 showed the highest reducing sugar content on the third day, with values of 36.26 mg·L− 1 and 26.67 mg·L− 1, respectively. The observed peak in reducing sugar content for microbial consortium 6 + 1 on the third day coincided with the highest activity of its straw-degrading enzyme system on the same day.

Both microbial consortiums 6 + 1 and wj1 exhibited the most significant decrease in pH on the second and third days, with the lowest values recorded at 4.78 and 5.05, respectively. This decrease in pH may be attributed to the fact that microbial consortium 6 + 1 secreted more organic acids, both in terms of type and quantity, than the wj1 pure culture treatment.

The results indicated that microbial consortium 6 + 1 exhibited the highest activity of the straw-degrading enzyme system and total reducing sugar content on the third day. Moreover, the pH value demonstrated a gradual decrease at this time point. The phosphorus solubilization efficiency of microbial consortium 6 + 1 also peaked at this time point. By the fifth day, the pH reached its lowest point, and the phosphorus solubilization efficiency stabilized, while the activity of the straw-degrading enzyme system decreased to its lowest level.

Fig. 6
figure 6

Changes in total reducing sugar content and pH across treatments over seven days. A: Total reducing sugar content. B: Changes in pH across treatments

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Analysis of metabolites

There were notable reductions in sugar and pH values within the culture system on the third and fifth days. In addition, the changes in organic acids and sugars of microbial consortium 6 + 1 on the third day, the fifth day, and the third day of ZJW-6 and wj1 were qualitatively and quantitatively detected in order to gain a better understanding of the specific changes in pH and reducing sugar in consortium 6 + 1.

In terms of sugar metabolites, the primary compounds produced included glucose, lactose, and xylose. Among these, glucose was the most abundant, reaching 27.27 mg·L− 1 on the third day and 6.97 mg·L− 1 on the fifth day. Glucose was also the most consumed sugar molecule during this process, with a consumption rate of 74.44%. Glucose, as one of the end products of straw degradation, is a significant contributor to the reduction of sugar content in the reaction system. The substantial decrease in glucose content from the third to the fifth day can be attributed to its utilization in the vital activities of microbial consortium 6 + 1, the phosphorus solubilization process, and glycolytic conversion into more organic acids. The higher production of glucose by the microbial consortium 6 + 1 compared to ZJW-6 suggests its superior capacity for straw degradation.

In terms of organic acids, the predominant compounds were pyruvic acid, acetic acid, citric acid, and propionic acid. Microbial consortium 6 + 1 produced more of these organic acids compared to the wj1 pure culture, with pyruvic acid, in particular, reaching 22.40 mg·L− 1 on the third day. This high production of pyruvic acid can be attributed to the substantial glucose produced by ZJW-6’s straw degradation and its utilization by consortium 6 + 1 through glycolysis, resulting in the production of a large amount of organic acids. wj1, on the other hand, produced the most citric acid, with a content of 12.63 mg·L− 1 on the third day. The production of acetic acid and propionic acid by consortium 6 + 1 was attributed to further degradation and uptake of cellulose and xylan, resulting in the further production of pyruvic acid. The increased production of organic acids, such as pyruvic acid and acetic acid, by consortium 6 + 1 is favorable for the solubilization of tricalcium phosphate (Fig. 7).

Fig. 7
figure 7

Analysis of reducing sugars and organic acids produced by microbial consortium 6 + 1. A: Analysis of reducing sugar output on the third and fifth day of each treatment. B: Analysis of organic acid output on the third and fifth day of each treatment. Different lowercase letters, a, ab, b and c, indicate the statistical differences based on p < 0.05

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Consumption rate of carbon sources

The consumption rate of the carbon source by ZJW-6, wj1, and microbial consortium 6 + 1 in CCM with a carbon source of 1.5 mg·L− 1 was examined (Fig. 8).

Consortium 6 + 1 exhibited the fastest consumption rate of glucose, with only 0.03 mg·L− 1 of the remaining glucose on the fourth day. In comparison, wj1 had 0.04 mg·L− 1 of the remaining glucose on the fifth day, while ZJW-6 had the slowest consumption rate, with 0.11 mg·L− 1 of the remaining glucose on the seventh day. The ZJW-6 straw-degrading bacterium, in the absence of carbon source stress, consumed glucose slowly, while wj1, despite having no carbon source stress, exhibited increased glucose consumption due to its phosphorus solubilization effect. The faster carbon source consumption rate in consortium 6 + 1 can be attributed to the synergistic growth of the two bacteria and the phosphorus solubilization effect.

Fig. 8
figure 8

Rate of consumption of carbon sources by treatment

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Analysis of straw degradation components

Changes in the content of straw components degraded by the initially treated CK and the microbial consortium 6 + 1 following continuous fermentation treatment were determined over a period of 12 days (Fig. 9).

The cellulose, hemicellulose, and lignin contents of the straw did not change significantly over the seven days in the blank control treatment. Microbial consortium 6 + 1 exhibited degradation of 53.25% of cellulose, 59.34% of hemicellulose, and 17.91% of lignin. Microbial consortium 6 + 1 degradation of straw is mainly the degradation of cellulose and hemicellulose, lignin degradation ability of the second.

Fig. 9
figure 9

Straw composition analysis during degradation process. A: CK-treated. B: 6 + 1-treated

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Microbial consortium 6 + 1 bacterial application

ZJW-6, wj1, and microbial consortium 6 + 1 were prepared as mycorrhizal agents. In addition, straw was embedded in the soil to assess the effects of mycorrhizal agents on the soil environment, straw, and rice growth (Fig. 10).

Effect of microbial consortium 6 + 1 on soil nutrient environment

The soil organic matter content of each treatment at 30 and 60 days is shown in the figure, in which the control (CK), humic acid treatment (CK*), and wj1 reached 11.67 mg·kg− 1, 12.33 mg·kg− 1, 13.33 mg·kg− 1, and 13.33 mg·kg− 1, 13.67 mg·kg− 1, and 14.67 mg·kg− 1, respectively, at 30 and 60 days. The addition of humic acid and wj1 microbial agent had no significant effect on the changes in soil organic matter content. The combined treatments of ZJW-6 and consortium 6 + 1 showed greater changes in organic matter content at the seedling and tillering stages, with 14.33 mg·kg− 1, 15.33 mg·kg− 1, 16.33 mg·kg− 1, and 22.67 mg·kg− 1, respectively. ZJW-6 and 6 + 1 combinations produced glucosidase, xylanase, lignin peroxidase, and manganese peroxidase. Xylanase, lignin peroxidase, and manganese peroxidase are key enzymes for the conversion of soil organic matter [37]. Based on the changes in organic matter content in both periods, ZJW-6 in microbial consortium 6 + 1 played a significant role in transforming organic matter.

The quick nitrogen content of the soil in each treatment was determined at 30 and 60 days. The alkaline nitrogen content of ZJW-6 and wj1 was 190.33 mg·kg-1, 192.67 mg·kg− 1, and 197.76 mg·kg− 1, 203.98 mg·kg− 1, which was effectively increased compared to the blank control and humic acid treatments, respectively. The quick-acting nitrogen content of the microbial consortium 6 + 1 was 201.07 mg·kg− 1 and 214.36 mg·kg− 1 in both periods, significantly higher than the other treatments at 60 days.

During the determination of quick-acting phosphorus content, there was no significant difference between CK, CK*, and ZJW-6 treatments at 30 and 60 days, which were 6.79 mg·kg− 1, 7.21 mg·kg− 1, 7.3 mg·kg− 1, and 7.03 mg·kg− 1, 7.76 mg·kg− 1, and 7.9 mg·kg− 1, respectively. The effective phosphorus contents of CK* and ZJW-6 were all higher than CK, likely related to the addition of humic acid and microbial agents to promote soil microbial activity. The results showed that the effective phosphorus content of wj1 and the 6 + 1 microbial consortium was significantly higher at seedling and tillering stages, which were 8.78 mg·kg− 1, 12.01 mg·kg− 1, and 11.84 mg·kg− 1, 14.14 mg·kg− 1, respectively. pH changes in the soil did not show any significant changes in CK, CK* and ZJW-6 treatments within 60 days, while wj1 and the microbial consortium 6 + 1 pH decreased by 1.51 and 1.97, respectively. wj1 and consortium 6 + 1 produced organic acids that promoted phosphorus solubilization while appropriately decreasing soil pH.

The four microbial agent s had the most significant effect on quicklime potassium, with values of 119.04 mg·kg− 1, 126.06 mg·kg− 1, 132.37 mg·kg− 1, 145.61 mg·kg− 1, and 125.63 mg·kg− 1 at 30 and 60 days in the soils treated with CK*, ZJW-6, wj1, and consortium 6 + 1, respectively. These values were much higher than CK (73.18 mg·kg− 1, 76.60 mg·kg− 1) in both periods.

Fig. 10
figure 10

Effect of microbial consortium 6 + 1 microbial agent on soil nutrient environment. A: Organic matter. B: Available N. C: Available P. D: Available K. E: Soil pH. Different lowercase letters, a, ab, b and c, indicate the statistical differences based on p < 0.05

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Straw decomposition and SEM analysis

The rate of straw decay in soil buried deep in the soil at 30 and 60 days was determined and analyzed by SEM (Fig. 11).

The decay rates of five different treatments were measured. The results showed that ZJW-6 and the 6 + 1 microbial combinations showed very high decay rates of 55.67%, 62.23%, 60.08%, and 68.33% during the seedling and tillering stages, respectively (Fig. 11A). Among them, 6 + 1 had the highest decay rate at 60 days, which was 36% higher than CK.

In the electron microscopy analysis, the straw of the blank control exhibited a finely structured and neatly aligned appearance, with a fiber bundle structure and fewer holes. In contrast, the straw treated with ZJW-6 had a loose system with several cracks appearing on the surface of the straw fiber bundles, indicating a damaged structure. Inside the surface layer, the fiber bundles were loosened and the surface area increased, facilitating subsequent attachment and degradation by microorganisms and enzymes [38]. The 6 + 1 microbial combination was more effective, with significant disintegration of the straw structure visible. The intertwining of reticulated layers and the significant increase in surface area and porosity were mainly attributed to the fact that the lignocellulosic system could act more directly on the cellulosic fractions, degrading the amorphous structure, separating lignin and hemicellulose from cellulose, and exposing the crystalline fibrous tissues [1]. In addition, the presence of more depressions at the pores of the straw and the presence of irregular, tiny fragments destroyed by lignocellulose degradation made the degradation effect more pronounced.

Fig. 11
figure 11

Straw decay rate and straw scanning electron microscopy analysis. A: Straw decomposition rate of each treatment in 60 days. B: CK-treated SEM. C: CK*-treated SEM. D: ZJW-6-treated SEM. E: 6 + 1-treated SEM. Different lowercase letters, a, ab and b, indicate the statistical differences based on p < 0.05

Full size image

Evaluation of rice growth promotion

The microbial agent was applied to rice in pots and rice root (root vigor, root dry weight, average root diameter, root number). In addition, the aboveground (net photosynthetic rate, chlorophyll) indices were determined for 2 periods (seedling and tillering) in order to explore the potential of the 6 + 1 combination for future applications (Fig. 12).

Rice root system

Root vigor, a more intuitive indicator for assessing root growth [39], was 565.88 µg/(g·h), 582.96 µg/(g·h), and 585.54 µg/(g·h) for the wj1 and 6 + 1 treatments at the seedling stage and 630.97 µg/(g·h) at the tillering stage, as shown in Fig. 12A. Consortium 6 + 1 converted a large amount of fast-acting phosphorus, fast-acting nitrogen, and organic matter, which promoted root growth and root vigor.

The root dry weight of a single pore of 6 + 1, CK, and CK* microbial combinations at the seedling stage was 8.06 g, 9 g, and 16.54 g, which was 52.3% and 46.4% higher than that of CK and CK* at the end of the seedling stage, respectively. At the end of tillering, the root dry weight of the 6 + 1 combination was 61% and 39% higher than that of CK and CK*, respectively. The root dry weight of the 6 + 1 combination at the end of tillering increased by up to 45.93% over the seedling stage.

The mean root diameter of each treatment is shown in (Fig. 12C). The 6 + 1 combination had the highest mean root diameter of 0.92 mm at seedling stage, which was 55% and 34% higher than CK (0.42 mm) and CK* (0.58 mm), respectively. At the end of tillering, the 6 + 1 combination (1.94 mm) was 55% and 50% higher than CK (0.87 mm) and CK* (0.98 mm), respectively. In the root tip count Fig. 12D, the 6 + 1 combination had the best level of root tip count among the five treatments at seedling and tillering stages, with 847 and 1837 tips, respectively. Moreover, the difference with other treatments at the end of the tillering stage was more significant.

Aboveground part of rice

The root-crown ratios of the five treatments (Fig. 12E) showed that the wj1 and 6 + 1 combinations were the most significant at the seedling and tillering stages, with values of 0.48, 0.49, 0.55, and 0.58, respectively. The root-crown ratio of the 6 + 1 combination was 18% higher at the end of the tillering stage than that of the blank control, and higher root-crown percentages reflected the growth of the root system and aboveground parts to some extent. The higher root-crown ratio recalled the root system of rice at seedling and tillering stages. The higher root-crown ratio reflected the better development of the rice root system at seedling and tillering stages with adequate nutrient supply [40].

The 6 + 1 combination gave the best results in terms of net photosynthetic rate (Fig. 12F) and chlorophyll content (Fig. 12G), which were 15.33 µmolCO2·m− 2·s− 1, 26.67 µmolCO2·m− 2·s− 1, and 37.57 mg·g− 1 and 40.3 mg·g− 1, respectively. These values were 40% and 15% higher than those of the blank control at the end of tillering. The higher chlorophyll content and net photosynthetic rate reflect the fact that plants can produce and accumulate more organic matter [41].

Microbial consortium 6 + 1 showed better straw degradation ability and phosphorus solubilization performance in the pot experiment. As a result, it enriched the soil part of the nutrient environment and promoted plant growth (Fig. S1). ZJW-6 and wj1 strains interacted with each other in microbial consortium 6 + 1 to improve the degree of decomposition of agricultural wastes (straw) and increase the content of plant-absorbable phosphorus through the ability of their respective strains to enhance the microbial the application value of the microbial consortium was enhanced by the ability of each strain. It provides a feasible idea for the study of the application value of microorganisms.

Fig. 12
figure 12

Evaluation of Rice Growth Promotion. A: Root activity. B: Root dry weight. C: Average root diameter. D: Root tips. E: Root/shoot ratio. F: Net photosynthetic rate. G: Chlorophyll content. Different lowercase letters, a, ab, b and c, indicate the statistical differences based on p < 0.05

Full size image

Discussion

In this study, two microorganisms with different functions were mixed and cultured. The microbial consortium 6 + 1 showed slightly higher colony counts than the monofunctional strain before mixing, a phenomenon that was attributed to the absence of antagonism in the growth of the two strains in addition to the possibility that it could be related to the intermediate metabolites of the microbial consortium [38]. In addition to this, the microbial consortium 6 + 1 promoted both phosphorus solubilization and straw degradation in the absence of antagonistic growth effects. This artificial mixed culture of microorganisms for both straw degradation and phosphorus solubilization functions has not yet been studied. In terms of straw degradation, the microbial consortium expressed highly efficient straw degradation, with 48.30% straw degradation in seven days. The microbial consortium TC-5, which specialized in straw degradation, showed a straw degradation rate of 45.7% in nine days and also expressed multiple lignocellulose degrading enzyme activities. The microbial consortium showed a high level of straw degradation in a short period of time [42]. However, higher rates of straw degradation can also be achieved by pretreatment of straw. Guan et al. examined various combinations of biochemical pretreatments of straw and discovered that the pretreatment of straw with CaO-LFD (calcium oxide-swine manure inductor-source filtrate co-treatment) pretreatments was the most effective, with a degradation rate under anaerobic conditions of 48.83%. Moreover, CaO-LFD broke the ether and ester bonds between lignin and hemicellulose Conger more likely to lead to straw degradation [43]. Similarly, Sajid et al. pretreated compost with an isolated fungal microbial consortium, increasing the straw degradation rate to 84% (compared to 61% for the blank control and 79% for the chemically-treated control). This approach also led to higher carboxymethyl cellulase activity, xylanase activity, and laccase activity [44]. The straw degradation potential of microbial consortium 6 + 1 offers further opportunities for exploration in future experiments. The soluble phosphorus content reached a maximum of 117.54 mg·L− 1 in seven days without any additional treatments. Further enhancement of microbial phosphorus solubilizing capacity can be achieved by adding exogenous substances. Pantigoso et al. indicated that bacterial phosphorus solubilization was stimulated by the addition of root secretion compounds (galactitol, threonine, and 4-hydroxybutyric acid) induced by low phosphorus conditions. In response to these additions, the dissolved phosphorus content reached about 68 mg·L− 1, which was approximately 4.25 times higher than the amount of dissolved phosphorus in the initial no-addition treatment [45].

The straw degradation and phosphorus solubilization abilities of the artificially constructed microbial consortium 6 + 1 were significantly improved compared to the single-strain members, owing to the synergistic promotion between these member strains. The mechanism of this synergistic effect can be attributed to several factors. Firstly, microbial consortium 6 + 1 exhibited enhanced straw degradation ability as indicated by the higher lignocellulose degrading enzyme activities, with the exception of lignin peroxidase, which was slightly lower than that of ZJW-6. This increase in enzyme activity may be due to the synergy between the cellulase system (endoglucanase and β-glucosidase) and the xylanase system (xylanase), which reduces the blocking effect of xylan, allowing for easier access to cellulose for decomposition. This, in turn, results in more efficient overall degradation [46]. However, the slight decrease in lignin peroxidase may be due to the lower pH environment. Furthermore, the rate of carbon source consumption by microbial consortium 6 + 1 far exceeded that of the two individual member bacteria. This led to consortium 6 + 1 experiencing more intense carbon source stress, compelling it to decompose the sole carbon source, straw, at a faster rate within the same timeframe. This phenomenon of heightened stress conditions driving microbial activity is also observed in other fields. For instance, Allsup et al. demonstrated that inoculating stress-resistant microbial consortia into plants under specific stress conditions increased the plants’ tolerance to those conditions. This suggests that specific stress conditions can trigger microbial activities that contribute to resistance and can potentially be harnessed in various organisms or systems [47].

Over the first three days of mixed culture, consortium 6 + 1 produced greater quantities of sugars, predominantly glucose, lactose, and xylose, in comparison to the ZJW-6 pure culture treatment. Additionally, the microbial consortium 6 + 1 generated higher levels of organic acids, including pyruvic, acetic, citric, and propionic acids, compared to wj1. As glucose, the primary saccharide, became depleted, the increased production of pyruvate among the organic acids was likely due to the conversion of glucose into pyruvate through gluconeogenesis as it was utilized by the microbial consortium. The utilization of other sugars also resulted in the production of organic acids such as acetic acid, propionic acid, and citric acid. This suggests that these sugars, aside from being consumed in the microbial consortium’s metabolic activities, might also undergo conversion into cellulose to glucose through key metabolic pathways. This enhances the utilization of glucose, resulting in an increased production of pyruvic acid and acetic acid (KEGG: map00760), (KEGG: map00010). Consequently, consortium 6 + 1 created a lower pH environment that favors the solubilization of insoluble phosphorus. These adaptations contribute to improved straw degradation and phosphorus solubilization functions in comparison to ZJW-6 and wj1 pure cultures. In addition, to confirm the influence of carbon source stress on the reaction system, the rates of carbon source consumption under varying initial glucose concentrations over seven days were assessed (Fig. S2). The results revealed that consortium 6 + 1 exhibited significantly faster carbon source consumption than the wj1 and ZJW-6 treatments, completely depleting glucose by the fourth day, while wj1 and ZJW-6 consumed all glucose by the sixth and seventh days, respectively. In reaction systems with different initial glucose concentrations, the straw degradation rate within the 6 + 1 system significantly decreased as the initial glucose content increased. The lowest straw degradation rate, at 5%, was observed at an initial medium glucose concentration of 5 mg·L− 1. These experiments provided evidence that the rapid carbon source consumption by consortium 6 + 1 induced higher carbon source stress, thereby promoting straw degradation. To validate the proposed pathway, the activities of key enzymes within the predicted pathway were measured over seven days (Fig. S3). These key enzymes included phosphofructokinase, pyruvate kinase, hexokinase, β-glucosidase, and endoglucanase. The results indicated that phosphofructokinase, pyruvate kinase, and hexokinase activities were expressed in the ZJW-6, wj1, and 6 + 1 treatments, while β-glucosidase and endoglucanase remained inactive in the wj1 treatment. Intriguingly, in the 6 + 1 treatment, these enzyme activities peaked from the third to the fourth day, significantly surpassing the levels observed in the ZJW-6 and wj1 treatments. This further supported the notion that consortium 6 + 1 effectively promoted the reaction system along the predicted pathway.

In summary, the mechanism of action of the microbial consortium was hypothesized to be as follows: microbial consortium 6 + 1 was subjected to stronger carbon source stress by the reaction system due to its faster consumption of carbon source. Over the first three days, it produces greater quantities of sugars, particularly glucose, lactose, and xylose, compared to the ZJW-6 pure culture treatment. Microbial consortium 6 + 1 also generates more organic acids, such as pyruvate, acetate, citrate, and propionate. These sugars are not only utilized in the consortium’s metabolic processes but also undergo conversion via metabolic pathways, such as (KEGG: map00010) and KEGG: map00760). This allows consortium 6 + 1 to utilize glucose, cellulose, xylose, and other substances to produce more organic acids, creating a lower pH environment conducive to the solubilization of insoluble phosphorus. The substantial carbon source consumption by the microbial consortium continually imposes greater carbon source stress, promoting more effective straw degradation by consortium 6 + 1. Consequently, consortium 6 + 1 achieves enhanced straw degradation and phosphorus solubilization functions compared to the pure cultures of ZJW-6 and wj1. A visual representation of this mechanism is provided in Fig. S4.

In order to harness its potential, microbial consortium 6 + 1 demonstrated improved straw degradation and phosphorus solubilization in a pot experiment, enriching the soil’s nutrient environment and fostering plant growth (Fig. S1). The study indicated that fast-acting phosphorus and organic matter significantly enhanced plant root and aboveground development [48]. Through interaction, the wj1 and ZJW-6 strains within microbial consortium 6 + 1 produced more fast-acting phosphorus. Additionally, the degradation of straw led to increased organic matter production. This resulted in a substantial improvement in root sturdiness, length, and root number, ultimately promoting root development. Stem length, leaf length, and leaf number also experienced considerable enhancement. This underscores the practical applications of the microbial consortium by enhancing agricultural waste decomposition (straw) and increasing the plant-absorbable phosphorus content through the respective strains’ unique abilities. In addition, the experimental material of this experiment is rice straw. Replacing the type of straw and pretreating the straw may also improve the experiment. Studying the synergistic effect of the two strains can also use some means of molecular biology for further research. These findings offer valuable insights into the practical applications of microorganisms in research and industry.

Data availability

No datasets were generated or analysed during the current study.

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Acknowledgements

This research was supported by the Jilin Agricultural University.

Funding

We gratefully acknowledge financial support given by the Education Department of Jilin Province (JJKH20230379CY).

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Authors and Affiliations

  1. College of Life Science, Jilin Agricultural University, Changchun, 130118, Jilin, China

    Songhao Che, Yufeng Xu, Xueting Qin, Shiqi Tian, Jianing Wang, Xueying Zhou, Zhenning Cao, Meiying Yang, Lei Wu & Xue Yang

  2. Faculty of Agronomy, Jilin Agricultural University, Changchun, 130118, Jilin, China

    Dongchao Wang, Meikang Wu & Zhihai Wu

Authors
  1. Songhao Che
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  2. Yufeng Xu
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  3. Xueting Qin
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  4. Shiqi Tian
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  5. Jianing Wang
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  6. Xueying Zhou
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  7. Zhenning Cao
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  8. Dongchao Wang
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  9. Meikang Wu
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  10. Zhihai Wu
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  11. Meiying Yang
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  12. Lei Wu
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  13. Xue Yang
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Contributions

C.S. wrote the main manuscript text. X.Y. and Q.X. prepared Figs. 1 and 2. T.S. and W.J. prepared Figs. 3, 4 and 5. Z.X. and C.Z. prepared Figs. 6 and 7. W.D. and W.M. prepared Figs. 8, 9, 10, 11 and 12. W.Z. and Y.M. took charge of methods supervision. W.L. Y.X. took charge of methodology, supervision, funding acquisition.

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Correspondence to Lei Wu or Xue Yang.

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Che, S., Xu, Y., Qin, X. et al. Building microbial consortia to enhance straw degradation, phosphorus solubilization, and soil fertility for rice growth. Microb Cell Fact 23, 232 (2024). https://doi.org/10.1186/s12934-024-02503-0

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Microbial Cell Factories

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