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Article

Microbial Organic Fertilizer Improved the Physicochemical Properties and Bacterial Communities of Degraded Soil in the North China Plain

by
Dongze Niu
1,2,
Min Yu
1,2,
Chuanyang Xu
1,2,
Yongjiang Wang
3,
Chunyu Li
1,2,
Dongmin Yin
1,2,
Sasa Zuo
4 and
Jianjun Ren
1,2,*
1
Changzhou Key Laboratory of Biomass Green, Institute of Urban and Rural Mining, Changzhou University, Changzhou 213164, China
2
National-Local Joint Engineering Research Center for Biomass Refining and High-Quality Utilization, School of Petrochemical Engineering, Changzhou University, Changzhou 213164, China
3
Yongqing Agricultural Bureau, Langfang 065600, China
4
College of Engineering, China Agricultural University, Beijing 100083, China
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(1), 67; https://doi.org/10.3390/su16010067
Submission received: 22 September 2023 / Revised: 9 November 2023 / Accepted: 19 December 2023 / Published: 20 December 2023
(This article belongs to the Section Sustainable Materials)
Browse Figures
Versions Notes

Abstract

:
Applying microbial organic fertilizer (MOF) effectively improves soil tilth and microbial diversity. However, there were few studies about the changes incurred in the physicochemical properties and bacterial diversity in the farmland of North China at a large-scale following MOF application. This study aimed to investigate the soil physicochemical properties and bacterial community following MOF application. A total of 910 t MOF was used on 173 hectares of degraded soil, and the results indicated increased nutrients in the top plough layer. Compared to controls, the treated samples had significant higher organic matter, total nitrogen, available phosphorus, potassium, and hydrolyzed nitrogen (p < 0.05). Furthermore, MOF application also induced a slight increase in the soil bacterial richness, but a significant decrease in the evenness was observed, where Firmicutes, Actinobacteria, and Bacteroidetes were enriched in the treated group, with Bacillus and Arthrobacter being the dominant genera, accounting for 0.291 and 0.136, respectively. Similarly, an increase in the proportion of Pseudomonas and Psychrobacillus was also observed at up to 0.038 and 0.034, respectively. The MOF treatment improved complex carbon metabolism and nitrogen reduction functions, inhibiting nitrogen oxidation as represented by nitrification. Redundancy and correlation analyses showed that total nitrogen, available phosphorus, and pH were the main factors driving the soil microbial community. This study concluded that MOF application could improve the soil’s physicochemical properties and enhance the abundance and function of soil microbes, which is an effective method for improving the soil tilth and ecology of farmland in north China.

1. Introduction

As the second largest plain in China, the North China Plain is a pivotal grain-producing region and plays a crucial role in ensuring China’s food supply [1]. Nevertheless, due to its semi-arid climate, improper agricultural practices, and global warming, some farmlands in this region confront the challenge of soil degradation, including issues like compaction, desertification, and salinization [1,2]. Among these issues, the reduction of organic matter and soil salinity are especially severe in the North China Plain, and they have strong negative correlations with each other [2,3]. Generally, the reduction of organic matter and soil salinity are mainly caused by improper irrigation and/or land management and cause inevitable to damage soil tilth, alter soil element recycling, and decline soil biodiversity and agricultural production [4,5]. Therefore, it is imperative to develop suitable and efficient methods to increase the organic matter content and reduce salinity of the North China Plain.
Various approaches, including engineering, agricultural methods, and biological methods, can be used to ameliorate soil conditions, where the choice of approach depends on the soil conditions and the available resources [4,6]. Engineering measures, such as leaching with non-saline water, require a lot of water resources and relatively high investment, and most of the food crops are salt-sensitive [4,7]. In contrast, organic matter can reduce soil salinity, improve soil structural stability, and enhance soil nutrient contents without affecting soil quality [5,8]. Moreover, the use of organic fertilizers can promote the growth of beneficial microbes in the soil, in addition to their increased quantity and diversity [9,10], thereby increasing the soil ecosystem stability, which in turn further improves the soil fertility and reduces salinity. However, the effects of biological measures depend on the material characteristics and the application method [4,6]. Thus, exploring efficient materials is vital for developing hastened and cost-effective methods to ameliorate farmland.
Microbial organic fertilizer (MOF) belongs to the class of organic fertilizers enriched with specific and beneficial microbial strains, which can improve soil tilth and promote plant growth [4,8,11]. Bacillus subtilis is commonly found in soil and has been found to exert several beneficial effects in agriculture, including improving soil structure, reducing salt stress, enhancing nutrient availability, and plant pathogens suppression [12,13]. Recently, MOF enriched with B. subtilis has been reported to reduce nitrogen loss in agricultural soil, improving beneficial bacterial abundance and promoting strawberry plant growth [11,13,14]. Although there was no report about the use of B. subtilis-enriched MOF for improving the biological and physicochemical properties of degraded soils in the North China Plain, the application of MOF could improve soil nutrients and structure, water availability, and crop tolerance to high osmotic pressure [4,7]. Therefore, it is imperative to evaluate the effects of adding B. subtilis-enriched MOF to degraded soils on their physicochemical properties and bacterial communities.
In this study, MOF containing B. subtilis spores was applied to restore degraded soil on a large scale. Changes in physicochemical properties and bacterial diversity before and after the application were analyzed to determine the effects on improving the texture and fertilizer efficiency of degraded soil in North China.

2. Materials and Methods

2.1. Site Description

The experimental area is located at Nanbalizhuang Village, Langfang City, Hebei Province (39°15′18″ N, 116°28′25″ E). The area had a temperate continental monsoon climate with four distinct seasons and an average annual temperature ranging from −0.5 °C to 14.2 °C, while the highest extreme temperature usually happens in June and July. The experimental area was low-lying with some undulations in the east–west direction. The soil texture was sandy loam, alkaline, and occasionally had white chloride-sulfate spots on the surface.

2.2. Experimental Design and Sampling

The MOF enriched with B. subtilis (1.07 × 108 cfu/g FM) and B. megatherium (6.31 × 107 cfu/g FM) was provided by Hebei Cixin Environmental Protection Technology Co., Ltd. (Langfang, China) (Table 1). A total of 910 t MOF was applied to 173 hectares (5.25 t/hectare) of degraded soil on 16 June 2021. A total of 52 soil samples were randomly collected from 0 to 10 cm surface layers of each sampling spot with an auger before (14 June 2021) and after applying MOF over a period of 120 days (14 October 2021), as reported earlier [9,15]. Samples collected from the same site were evenly mixed and divided into equal fractions, where one part was introduced into sterile falcon tubes on ice and stored at −80 °C until further estimating of bacterial diversity later. In contrast, the other part was sieved through 2 mm mesh and dried for physicochemical characterization.

2.3. Analysis of Physicochemical Properties

The soil samples collected were subjected to various physicochemical characterization tests like pH, soil organic carbon (SOM), available phosphorus (AP), available potassium (AK), total nitrogen (TN), water-soluble nitrogen (HN), and total dissolved salt (TDS). Briefly, samples were mixed in water in a 1:5 (v/v) ratio, and their pH was determined using a calibrated pH meter [13]. Similarly, SOM was estimated using the potassium dichromate method, AP via the molybdenum antimony colorimetric method, and AK via the flame photometric method, respectively [7,16]. Moreover, TN and HN were quantified using the Kjeldahl method by dissolving the samples in concentrated sulfuric acid and sodium hydroxide, respectively, while TDS was estimated using the gravimetric method [7,8].

2.4. Bacterial Community and Functional Analysis

The DNA extraction and sequencing method is reported elsewhere [17,18]. Briefly, genomic DNA was extracted using a soil DNA extraction kit as per the kit’s instruction manual (TIANamp, Beijing, China) and amplified using the primers of 16 S rDNA V3–4 region (338 F: 5′-ACTCCTACGGGAGGCAGCA-3′; 806 R: 5′-GGACTACHVGGGTWTCT AAT-3′), respectively. The qualified samples were then sequenced by Biomarker Technology Co., Ltd. (Beijing, China) using the Illumina HiSeq2500 platform. Amplicon sequence variants (ASVs) were created using mothur and annotated using a pipeline with the RDP database. Further analysis and visualization were performed using MicrobiomeAnalyst (https://www.microbiomeanalyst.ca/ accessed on 1 September 2023) and ImageGP (https://www.bic.ac.cn/BIC/#/ accessed on 1 September 2023). Briefly, the average abundance of each ASV was calculated across the 52 samples, and ASVs with an average abundance of 0.1% or higher were selected to construct a Venn diagram. Principal component analysis (PCA) was calculated using Bray–Curtis distance matrices, with significance levels determined by one-way permutational multivariate analysis of variance (PERMANOVA). Linear Discriminant Analysis Effect Size (LEfSe) was conducted at class level with FDR-adjusted p-value < 0.1. Heat tree was constructed the Wilcoxon p-value at 0.05. Redundancy analysis (RDA) and correlation analysis of the relationship between bacterial community and environmental factors were the same as our previous reports [17]. The bacterial functions were also predicted using the Functional Annotation of Prokaryotic Taxa (FAPROTAX) [19].

2.5. Statistical Analysis

All the data were analyzed statistically using SPSS (version 21, SPSS Inc., Chicago, IL, USA). The inter-group difference analysis was conducted using a t-test, and data with p < 0.05 was regarded as significant. Similarly, the relation between environmental factors and bacterial communities was evaluated using Pearson correlation analysis using R3.1.0.

3. Results and Discussion

3.1. Physicochemical Properties of the Soils

Physicochemical attributes of the soil play a pivotal role in plant growth and soil health and serve as a fundamental basis for chemical and biological processes [20]. The physicochemical analysis results demonstrated a significant effect that MOF exerted on all selected samples’ physicochemical attributes. As shown in Table 2, the pH of the control and treated soil samples were 7.79 and 7.87, respectively, equivalent to greenhouse saline soil treated with MOF and soil conditioners [8]. Similarly, MOF application decreased the TDS from 2.97 to 2.80 g/kg, which was lower compared to other reports [8,21]; however, the final concentration was found to be equal to that reported by Zhu et al. (2021) [8], which could be attributed to an initial lower concentration in this study. Moreover, the SOM, TN, HN, AP, and AK contents of treated samples were increased significantly (p < 0.05, compared to that of controls. Although the increase in SOM of this study was lower than in the soil with added MOF and pig manure of other researchers, improved nutrients were observed higher than in earlier published reports [10,13]. The increase in the nutrient levels, such as SOM and nitrogen, is assumed to be a result of the organic matter present in the MOF, and the differences among studies could be due to differences in physicochemical properties and MOF quantity added to the soil.
The Person correlation analysis revealed a weak negative correlation between TDS contents and SOM (Figure 1), cementing the idea that organic matter is deemed favorable in reducing soil salts, which could be due to MOF, which promotes the formation and stability of large soil aggregates, thereby assisting in salt leaching, reducing surface evaporation, and inhibiting salt accumulation on the soil surface [8,10]. Additionally, organic matter can improve the soil microbial community and facilitate the absorption and/or fixation of inorganic nutrients by releasing extracellular polysaccharides forming organic-mineral complexes and/or converting them into organic nutrients, which further helps in reducing soil salinity [8,22]. Apart from soil structure, the existing forms and transformation pathways of nutrients can also be affected by microbial community changes, reducing losses and improving utilization efficiency [13]. Some researchers reported that organic fertilizers significantly affect the microbial community compared to aggregate soil size [10], which made us analyze the bacterial community and function in a subsequent experiment.

3.2. Bacterial Diversity and Community in the Soil Samples

A total of 22,119 ASVs were detected in the samples, and 18,138 low-abundance and 394 low-variance features were removed based on prevalence and inter-quantile range, respectively. After the data filtering step, 3587 ASVs remained. The higher ASV revealed that soil samples presented an incredibly diverse ecosystem for bacterial communities [23]. Concerning α-diversity, the treated soil had slightly higher ACE and Chao1 indices and significantly lower Shannon and Simpson indices (p < 0.05), respectively (Table 3). The ACE and Chao1 indices are commonly employed indicators of a sample’s microbial richness, whereas Shannon and Simpson indices are often used to describe microbial diversity, combining richness and evenness [17,24]. In this study, the higher richness and lower evenness of treated samples indicated a significant increase in the abundance of some species, which were also reported by other researchers, mainly attributed to organic fertilizers providing a more diverse range of nutrients and energy sources for soil microbes [25,26]; thus, a shift in the bacterial community from oligotrophic organisms to microbes decomposing complex organic compounds was observed [10]. Furthermore, the nutrients in organic fertilization can accelerate the resilience of soil functions and enhance the stability of the soil microbiome [27,28]. However, in some cases, the microbial community can revert to its original composition, particularly when no exogenous organic fertilizer is introduced for an extended period [10,27,29]. Therefore, longer-term application and scientific management are essential to maintain the stability of soil microbial composition and functions.
Axis 1 and 2 contributed 70.6% and 16.7% to the total variance in PCA, respectively (Figure 2). The PERMANOVA analysis confirmed significant differences in bacterial communities between the control and treated samples (R2 = 0.1902, p = 0.001). The distances among treated samples were higher than before treatment, indicating that the MOF addition increased the bacterial communities’ differences, which can be caused by the randomness of the fertilization process. The five most abundant phyla observed in the control group were Proteobacteria (36.5%), Acidobacteria (29.1%), Firmicutes (16.8%), Actinobacteria (8.1%), and Nitrospirae (5.0%). Proteobacteria was also reported by other researchers to be the most abundant phylum in soil libraries [23,30], which prefers to colonize in nutrient-rich environments [8]. Similarly, Firmicutes (38.8%) became the most abundant phylum, followed by Proteobacteria (24.8%), Actinobacteria (16.1%), Acidobacteria (13.6%), and Bacteroidetes (3.1%) in treated soil samples. However, opposite change trends in Proteobacteria and lower Firmicutes were observed in other soils with added MOF [8,13], possibly due to differences in the soils and the MOFs’ physicochemical properties. The Acidobacteria was also reported to decrease in other studies belonging to the oligotrophic community [8]. Furthermore, Bacillus became the most abundant genus at the genus level, followed by Arthrobacter, Luteitalea, Pseudomonas, and Psychrobacillus in treated samples. It is known that B. subtilis belongs to Firmicutes, indicating the bacteria in MOF effectively colonized the soil, indicating the importance of microbial community in MOF affecting the bacterial community in soil.

3.3. Comparison of Bacterial Community

The inter-treatment differences were analyzed using LEfSe and heat trees. The results indicated that Firmicutes, Actinobacteria, and Bacteroidetes, including seven bacterial classes, were enriched in the treated samples. In contrast, the other phyla and classes decreased significantly (Figure 3). The enrichment of Bacilli, Actinobacteria, Sphingobacteriia, and Flavobacteriia was also observed in heat tree analysis. The bacterial species with increased abundance were lesser than those with decreased abundance, also revealed by a lower evenness of α-diversity. Generally, Firmicutes, Actinobacteria, and Bacteroidetes are eutrophic bacteria and primary degraders of biomass [31,32,33,34]; hence, their higher levels in treated soil could be attributed to higher soil nutrients after fertilizer addition. At the genus level, Bacilli mainly comprised Bacillus, Psychrobacillus, Neobacillus, and Paludibaculum, while the other three enriched classes included Arthrobacter, Streptacidiphilus, Pedobacter, and Flavobacterium. Similarly, other factors like pathogen control, solubilizing potassium, and promoting plant growth for bacterial genera have already been reported earlier [12,35,36,37,38], indicating MOF addition contributes to the soil improvement in terms of production efficiency and ecological environment.
The decreased bacterial species observed in this study were Proteobacteria and Acidobacteria, where a decrease in the latter could have been due to how MOF enriched the nutritional composition of soil and bacterial communities for oligotrophic species [8]. However, previous studies reported that organic fertilizer increases the abundance of Proteobacteria [8,13,29], the largest phyla of soil bacteria with a higher potential to utilize manure-derived carbohydrates and fix nitrogen [23,39]. Hence, their decreased levels in this study could result from highly mature MOF. In addition, Nitrospira, belonging to Nitrospirae, recognized as versatile nitrifiers, were also reduced in the treated soil samples [40], depicting weak nitrification of the treated soil.

3.4. RDA and Correlation Analysis with Environmental Factors

The environmental factors showed a significant impact (p < 0.05) on the microbial community in the MOF-treated soil, as depicted by RDA analysis results, where TN, Ap, and pH had 28% of the total variance, as shown in Figure 4. Additionally, TN demonstrated to be the most significant factor (p < 0.01), having the highest impact on the microbial community in the samples, comprising 17.9% of the total variance, followed by AP with 3.7% (p < 0.05) and pH with 1.2% (p = 0.178) of the total variance, respectively. These results suggested that, despite lower explanatory power, the TN and AP in the soil were vital environmental factors affecting microbial communities in soils with added MOF. The driving function of TN, pH, and/or AP for the bacterial community in the soil was also observed previously, with TN being an undominant environmental factor [22,30]. The correlation analysis results revealed AP, TN, and HN had a strong correlation with the bacterial community, whereas other indicators showed a weak correlation, which was consistent with RDA analysis results where other indicators could not explain the total variance of the bacterial community, which could be attributed to their smaller range variation than TN and AP [41]. Among the 22 bacterial genera analyzed, Bacillus, Neobacillus, Arthrobacter, Pseudomonas, Massilia, and Psychrobacillus in region A showed a strong and positive correlation with AP, TN, and HN. In comparison, 12 bacterial genera in region B showed a strong but negative correlation with these indicators. Furthermore, the heat tree results demonstrated that Bacillus, Neobacillus, and Psychrobacillus were from Firmicutes, while Arthrobacter belonged to Actinobacteria. Similarly, Massilia and Pseudomonas were the only two enriched genera in Proteobacteria. The positive correlation between these bacteria and the contents of TN and AP has been reported previously, suggesting that soil nutrients were the critical environmental factors for constructing bacterial flora [42]. Moreover, Pseudomonas, Arthrobacter, and Bacillus have been reported to promote plant growth [26,38]; thus, further studies are required to pay more attention to their effects on the tolerance, survival, and production of crops in the degraded soil of the North China Plain.

3.5. Bacterial Functions Predicted Using FAPROTAX

The addition of organic fertilizers resulted in a significant alteration in the functional potential of soil bacteria, with 12 functions downregulated and 21 upregulated, most of which were related to the cycling of carbon, nitrogen, and sulfur (Figure 5). Among them, chemoheterotrophy and aerobic chemoheterotrophy were the most abundant, where the addition of MOF significantly increased their abundance. The high abundance of bacterial functions was also observed in other soil samples [43]. Generally, these functions refer to mechanisms of obtaining energy and carbon from organic compounds [43,44]; therefore, a higher abundance is thought to be due to organic matter in the fertilizer. Similarly, besides an increased chemoheterotrophy function, cellulolysis and aromatic compound degradation functions were also found to be upregulated, which are beneficial for improving lignocellulose degradation [18,45]. These results suggested that adding organic fertilizers can increase the cellulose and lignin content, thereby promoting the growth and activity of related degradation microbial communities.
The nitrogen cycling in treated samples includes nitrate reduction, nitrogen respiration, and nitrate respiration. A similar increase as a result of MOF addition into the soil was also reported previously [13], and nitrate reduction had a positive correlation with SOC and nitrogen contents [43]. Previous studies proved that denitrification is a clear signal of possible N2O emissions, which can be stimulated by organic matter [46], so a more comprehensive evaluation of N-oxides’ fluxes should be conducted in future studies to provide a more accurate assessment of the nitrogen cycle. Conversely, MOF treatment inhibited nitrification, aerobic nitrite oxidation, and aerobic ammonia oxidation in the soil samples, which was evident by the reduction in the Nitrospirae community. The reduction of nitrogen involves nitrate, nitrite, or other nitrogen compounds’ reduction under an anaerobic environment rich in organic carbon, since oxidation requires aerobic conditions to proceed [13,47,48]. Adding MOF provided organic carbon but could create a micro-anaerobic environment due to microbial growth, translating into an enriched nitrogen reduction process in the treated soil. Furthermore, MOF addition increased the ureolysis function, which could be attributed to affluent nutrients promoting the growth of ureolytic microbes, as reported previously [49,50]. These results suggested that adding fertilizer is a prime motivator for regulating soil nitrogen cycling.
Furthermore, five functions associated with the respiration of sulfur compounds were also inhibited in the treated samples, which facilitates converting various forms of sulfur compounds to produce energy for microbial growth [51]. It could be possible that alterations in the redox conditions of the soil samples following MOF addition provided alternative carbon sources for microbial communities [8,48,52], which affected the abundance and activity of microbial communities involved in the sulfur cycle, thereby decreasing their reliance on sulfur respiration processes. Additionally, adding MOF also increased the abundance of human pathogens, animal parasites, and symbionts, as reported previously [53,54], mainly due to the fertilizer derived from agricultural and animal waste products, posing an unprecedented threat to human and animal health, mainly if the soil was used for agriculture and the crops were consumed by humans or animals. Therefore, it is pertinent to properly handle and treat organic fertilizers to minimize the risk of contamination with these microorganisms.

4. Conclusions

The results showed that following the addition of MOF into the degraded soil of the North China Plain, the AP and HN contents in soil samples significantly increased, with a significant decrease in TDS. The abundance of soil bacteria increased after applying MOF, but their evenness decreased. The abundance of bacteria from the phyla Firmicutes, Actinobacteria, and Bacteroidetes significantly increased. In contrast, the abundance of the other five phyla was significantly reduced, mainly shaped by nitrogen and phosphorus contents. The nitrogen oxidation processes, mainly caused by Nitrospirae, were inhibited, but reduction processes were enriched. Above all, MOF improves soil fertility and regulates the microbial community.

Author Contributions

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

Funding

This research was funded by Natural Science Foundation of the Jiangsu Higher Education Institutions of China, grant number 23KJA610001 and 20KJB230004.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Sequence data was deposited in the NCBI Sequence Read Archive (SRA) (accession number PRJNA1019515).

Acknowledgments

Special thanks are given to the Analysis and Testing Center of Changzhou University for their support in the chemical analysis.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Han, D.; Wiesmeier, M.; Conant, R.T.; Kühnel, A.; Sun, Z.; Kögel-Knabner, I.; Hou, R.; Cong, P.; Liang, R.; Ouyang, Z. Large soil organic carbon increase due to improved agronomic management in the North China Plain from 1980s to 2010s. Glob. Chang. Biol. 2018, 24, 987–1000. [Google Scholar] [CrossRef] [PubMed]
  2. Yu, Z.; Deng, X. Assessment of land degradation in the North China Plain driven by food security goals. Ecol. Eng. 2022, 183, 106766. [Google Scholar] [CrossRef]
  3. Morrissey, E.M.; Gillespie, J.L.; Morina, J.C.; Franklin, R.B. Salinity affects microbial activity and soil organic matter content in tidal wetlands. Glob. Chang. Biol. 2014, 20, 1351–1362. [Google Scholar] [CrossRef] [PubMed]
  4. Bello, S.K.; Alayafi, A.H.; Al-Solaimani, S.G.; Abo-Elyousr, K.A.M. Mitigating soil salinity stress with gypsum and bio-organic amendments: A review. Agronomy 2021, 11, 1735. [Google Scholar] [CrossRef]
  5. Wichern, F.; Islam, M.R.; Hemkemeyer, M.; Watson, C.; Joergensen, R.G. Organic amendments alleviate salinity effects on soil microorganisms and mineralisation processes in aerobic and anaerobic paddy rice soils. Front. Sustain. Food Syst. 2020, 4, 30. [Google Scholar] [CrossRef]
  6. Yang, M.; Yang, R.; Li, Y.; Pan, Y.; Sun, J.; Zhang, Z. Effects of different biomass materials as a salt-isolation layer on water and salt migration in coastal saline soil. PeerJ 2021, 9, e11766. [Google Scholar] [CrossRef] [PubMed]
  7. Cui, Q.; Xia, J.; Yang, H.; Liu, J.; Shao, P. Biochar and effective microorganisms promote Sesbania cannabina growth and soil quality in the coastal saline-alkali soil of the Yellow River Delta, China. Sci. Total Environ. 2021, 756, 143801. [Google Scholar] [CrossRef]
  8. Zhu, L.; Jia, X.; Li, M.; Wang, Y.; Zhang, J.; Hou, J.; Wang, X. Associative effectiveness of bio-organic fertilizer and soil conditioners derived from the fermentation of food waste applied to greenhouse saline soil in Shan Dong Province, China. Appl. Soil Ecol. 2021, 167, 104006. [Google Scholar] [CrossRef]
  9. Kamaa, M.; Mburu, H.; Blanchart, E.; Chibole, L.; Chotte, J.-L.; Kibunja, C.; Lesueur, D. Effects of organic and inorganic fertilization on soil bacterial and fungal microbial diversity in the Kabete long-term trial, Kenya. Biol. Fertil. Soils 2011, 47, 315–321. [Google Scholar] [CrossRef]
  10. Lin, Y.; Ye, G.; Kuzyakov, Y.; Liu, D.; Fan, J.; Ding, W. Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa. Soil Biol. Biochem. 2019, 134, 187–196. [Google Scholar] [CrossRef]
  11. Liu, L.; Li, X.; Li, T.; Xie, Y.; Cao, Z.; Fang, P. Bio-organic Fertilizer with Bacillus subtilis F2 Promotes Strawberry Plant Growth and Changes Rhizosphere Microbial Community. J. Soil Sci. Plant Nutr. 2022, 22, 3045–3055. [Google Scholar] [CrossRef]
  12. Ren, J.; He, W.; Li, C.; He, S.; Niu, D. Purification and identification of a novel antifungal protein from Bacillus subtilis XB-1. World J. Microbiol. Biotechnol. 2019, 35, 150. [Google Scholar] [CrossRef] [PubMed]
  13. Sun, B.; Gu, L.; Bao, L.; Zhang, S.; Wei, Y.; Bai, Z.; Zhuang, G.; Zhuang, X. Application of biofertilizer containing Bacillus subtilis reduced the nitrogen loss in agricultural soil. Soil Biol. Biochem. 2020, 148, 107911. [Google Scholar] [CrossRef]
  14. Cheng, H.; Zhang, D.; Huang, B.; Song, Z.; Ren, L.; Hao, B.; Liu, J.; Zhu, J.; Fang, W.; Yan, D.; et al. Organic fertilizer improves soil fertility and restores the bacterial community after 1,3-dichloropropene fumigation. Sci. Total Environ. 2020, 738, 140345. [Google Scholar] [CrossRef]
  15. Zhang, H.; Shi, Y.; Dong, Y.; Lapen, D.R.; Liu, J.; Chen, W. Subsoiling and conversion to conservation tillage enriched nitrogen cycling bacterial communities in sandy soils under long-term maize monoculture. Soil Tillage Res. 2022, 215, 105197. [Google Scholar] [CrossRef]
  16. Chen, X.; Xiao, P.; Niu, J.; Chen, X. Evaluating soil and nutrients (C, N, and P) loss in Chinese Torreya plantations. Environ. Pollut. 2020, 263, 114403. [Google Scholar] [CrossRef] [PubMed]
  17. Niu, D.; Yu, C.; Zheng, M.; Ren, J.; Li, C.; Xu, C. Effects of ensiling on Irpex lacteus fermentation in wheat straw: Chemical composition, in vitro rumen digestibility, and fungal community. Anim. Feed Sci. Technol. 2022, 292, 115433. [Google Scholar] [CrossRef]
  18. Niu, D.; An, W.; Yu, C.; Zhu, P.; Li, C.; Yin, D.; Zhi, J.; Jiang, X.; Ren, J. Pre-pasteurization enhances the fermentation of wheat straw by Irpex lacteus: Chemical composition, enzymatic hydrolysis, and microbial community. Ind. Crops Prod. 2023, 202, 116962. [Google Scholar] [CrossRef]
  19. Louca, S.; Parfrey, L.W.; Doebeli, M. Decoupling function and taxonomy in the global ocean microbiome. Science 2016, 353, 1272–1277. [Google Scholar] [CrossRef]
  20. Raghavendra, M.; Sharma, M.; Ramesh, A.; Richa, A.; Billore, S.; Verma, R. Soil Health Indicators: Methods and Applications. In Soil Analysis: Recent Trends and Applications; Springer: Berlin/Heidelberg, Germany, 2020; pp. 221–253. [Google Scholar]
  21. Li, Q.; Zhang, D.; Song, Z.; Ren, L.; Jin, X.; Fang, W.; Yan, D.; Li, Y.; Wang, Q.; Cao, A. Organic fertilizer activates soil beneficial microorganisms to promote strawberry growth and soil health after fumigation. Environ. Pollut. 2022, 295, 118653. [Google Scholar] [CrossRef]
  22. Chang, T.; Shao, X.; Zhang, J.; Mao, J.; Wei, Y.; Yin, C.; Wang, W. Effects of bio-organic fertilizer application combined with subsurface drainage in secondary salinized greenhouse soil. J. Food Agric. Environ. 2013, 11, 457–460. [Google Scholar]
  23. Spain, A.M.; Krumholz, L.R.; Elshahed, M.S. Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J. 2009, 3, 992–1000. [Google Scholar] [CrossRef] [PubMed]
  24. Wang, Q.; Wang, C.; Xiang, X.; Xu, H.; Han, G. Analysis of microbial diversity and succession during Xiaoqu Baijiu fermentation using high-throughput sequencing technology. Eng. Life Sci. 2022, 22, 495–504. [Google Scholar] [CrossRef] [PubMed]
  25. Hartmann, M.; Frey, B.; Mayer, J.; Mader, P.; Widmer, F. Distinct soil microbial diversity under long-term organic and conventional farming. ISME J. 2015, 9, 1177–1194. [Google Scholar] [CrossRef] [PubMed]
  26. Liu, X.; Lu, X.; Zhao, W.; Yang, S.; Wang, J.; Xia, H.; Wei, X.; Zhang, J.; Chen, L.; Chen, Q. The rhizosphere effect of native legume Albizzia julibrissin on coastal saline soil nutrient availability, microbial modulation, and aggregate formation. Sci. Total Environ. 2022, 806, 150705. [Google Scholar] [CrossRef] [PubMed]
  27. Luo, J.; Liao, G.; Banerjee, S.; Gu, S.; Liang, J.; Guo, X.; Zhao, H.; Liang, Y.; Li, T. Long-term organic fertilization promotes the resilience of soil multifunctionality driven by bacterial communities. Soil Biol. Biochem. 2023, 177, 108922. [Google Scholar] [CrossRef]
  28. Sun, Y.; Tao, C.; Deng, X.; Liu, H.; Shen, Z.; Liu, Y.; Li, R.; Shen, Q.; Geisen, S. Organic fertilization enhances the resistance and resilience of soil microbial communities under extreme drought. J. Adv. Res. 2023, 47, 1–12. [Google Scholar] [CrossRef]
  29. Liu, Y.; Lv, Z.; Hou, H.; Lan, X.; Ji, J.; Liu, X. Long-term effects of combination of organic and inorganic fertilizer on soil properties and microorganisms in a Quaternary Red Clay. PLoS ONE 2021, 16, e0261387. [Google Scholar] [CrossRef]
  30. Wu, L.; Jiang, Y.; Zhao, F.; He, X.; Liu, H.; Yu, K. Increased organic fertilizer application and reduced chemical fertilizer application affect the soil properties and bacterial communities of grape rhizosphere soil. Sci. Rep. 2020, 10, 9568. [Google Scholar] [CrossRef]
  31. Francioli, D.; Schulz, E.; Lentendu, G.; Wubet, T.; Buscot, F.; Reitz, T. Mineral vs. Organic Amendments: Microbial Community Structure, Activity and Abundance of Agriculturally Relevant Microbes Are Driven by Long-Term Fertilization Strategies. Front. Microbiol. 2016, 7, 1446. [Google Scholar] [CrossRef]
  32. Kulichevskaya, I.S.; Belova, S.E.; Kevbrin, V.V.; Dedysh, S.N.; Zavarzin, G.A. Analysis of the bacterial community developing in the course of Sphagnum moss decomposition. Microbiology 2007, 76, 621–629. [Google Scholar] [CrossRef]
  33. Yang, L.; Sun, R.; Li, J.; Zhai, L.; Cui, H.; Fan, B.; Wang, H.; Liu, H. Combined organic-inorganic fertilization builds higher stability of soil and root microbial networks than exclusive mineral or organic fertilization. Soil Ecol. Lett. 2023, 5, 220142. [Google Scholar] [CrossRef]
  34. Zhang, Q.; Liang, G.; Guo, T.; He, P.; Wang, X.; Zhou, W. Evident variations of fungal and actinobacterial cellulolytic communities associated with different humified particle-size fractions in a long-term fertilizer experiment. Soil Biol. Biochem. 2017, 113, 1–13. [Google Scholar] [CrossRef]
  35. Boubekri, K.; Soumare, A.; Mardad, I.; Lyamlouli, K.; Ouhdouch, Y.; Hafidi, M.; Kouisni, L. Multifunctional role of Actinobacteria in agricultural production sustainability: A review. Microbiol. Res. 2022, 261, 127059. [Google Scholar] [CrossRef] [PubMed]
  36. Hollister, E.B.; Hu, P.; Wang, A.S.; Hons, F.M.; Gentry, T.J. Differential impacts of brassicaceous and nonbrassicaceous oilseed meals on soil bacterial and fungal communities. FEMS Microbiol. Ecol. 2013, 83, 632–641. [Google Scholar] [CrossRef] [PubMed]
  37. Kwak, M.J.; Kong, H.G.; Choi, K.; Kwon, S.K.; Song, J.Y.; Lee, J.; Lee, P.A.; Choi, S.Y.; Seo, M.; Lee, H.J.; et al. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat. Biotechnol. 2018, 36, 1100–1109. [Google Scholar] [CrossRef] [PubMed]
  38. Hu, J.; Wei, Z.; Weidner, S.; Friman, V.-P.; Xu, Y.; Shen, Q.; Jousset, A. Probiotic Pseudomonas communities enhance plant growth and nutrient assimilation via diversity-mediated ecosystem functioning. Soil Biol. Biochem. 2017, 113, 122–129. [Google Scholar] [CrossRef]
  39. Li, W.; Zhang, Y.; Mao, W.; Wang, C.; Yin, S. Functional potential differences between Firmicutes and Proteobacteria in response to manure amendment in a reclaimed soil. Can. J. Microbiol. 2020, 66, 689–697. [Google Scholar] [CrossRef]
  40. Vijayan, A.; Vattiringal Jayadradhan, R.K.; Pillai, D.; Prasannan Geetha, P.; Joseph, V.; Isaac Sarojini, B.S. Nitrospira as versatile nitrifiers: Taxonomy, ecophysiology, genome characteristics, growth, and metabolic diversity. J. Basic Microbiol. 2021, 61, 88–109. [Google Scholar] [CrossRef]
  41. Fan, Y.; Li, B.; Yang, Z.; Cheng, Y.; Liu, D.; Yu, H. Mediation of functional gene and bacterial community profiles in the sediments of eutrophic Chaohu Lake by total nitrogen and season. Environ. Pollut. 2019, 250, 233–240. [Google Scholar] [CrossRef]
  42. Jiang, S.Q.; Yu, Y.N.; Gao, R.W.; Wang, H.; Zhang, J.; Li, R.; Long, X.H.; Shen, Q.R.; Chen, W.; Cai, F. High-throughput absolute quantification sequencing reveals the effect of different fertilizer applications on bacterial community in a tomato cultivated coastal saline soil. Sci. Total Environ. 2019, 687, 601–609. [Google Scholar] [CrossRef] [PubMed]
  43. Qin, L.; Wang, Y.; Ming, A.; Xi, S.; Xiao, Z.; Teng, J.; Tan, L. Molecular Ecological Network Structure and Potential Function of the Bacterial Community in the Soil Profile under Indigenous Tree Plantations in Subtropical China. Forests 2023, 14, 803. [Google Scholar] [CrossRef]
  44. Tian, C.; Xi, J.; Ju, M.; Li, Y.; Guo, Q.; Yao, L.; Wang, C.; Lin, Y.; Li, Q.; Williams, W.J. Biocrust microbiomes influence ecosystem structure and function in the Mu Us Sandland, northwest China. Ecol. Inform. 2021, 66, 101441. [Google Scholar] [CrossRef]
  45. Qi, C.; Yin, R.; Cheng, J.; Xu, Z.; Chen, J.; Gao, X.; Li, G.; Nghiem, L.; Luo, W. Bacterial dynamics for gaseous emission and humification during bio-augmented composting of kitchen waste with lime addition for acidity regulation. Sci. Total Environ. 2022, 848, 157653. [Google Scholar] [CrossRef] [PubMed]
  46. Thilakarathna, S.K.; Hernandez-Ramirez, G. Primings of soil organic matter and denitrification mediate the effects of moisture on nitrous oxide production. Soil Biol. Biochem. 2021, 155, 108166. [Google Scholar] [CrossRef]
  47. Lu, X.; Wang, Z.; Duan, H.; Wu, Z.; Hu, S.; Ye, L.; Yuan, Z.; Zheng, M. Significant production of nitric oxide by aerobic nitrite reduction at acidic pH. Water Res. 2023, 230, 119542. [Google Scholar] [CrossRef] [PubMed]
  48. Surey, R.; Lippold, E.; Heilek, S.; Sauheitl, L.; Henjes, S.; Horn, M.A.; Mueller, C.W.; Merbach, I.; Kaiser, K.; Böttcher, J. Differences in labile soil organic matter explain potential denitrification and denitrifying communities in a long-term fertilization experiment. Appl. Soil Ecol. 2020, 153, 103630. [Google Scholar] [CrossRef]
  49. Wang, L.; Xiong, X. Long-term organic manure application alters urease activity and ureolytic microflora structure in agricultural soils. Agronomy 2022, 12, 3018. [Google Scholar] [CrossRef]
  50. Wang, L.; Xiong, X.; Luo, X.; Chen, W.; Wen, S.; Wang, B.; Chen, C.; Huang, Q. Aggregational differentiation of ureolytic microbes in an Ultisol under long-term organic and chemical fertilizations. Sci. Total Environ. 2020, 716, 137103. [Google Scholar] [CrossRef]
  51. Simon, J.; Kroneck, P.M. Microbial sulfite respiration. Adv. Microb. Physiol. 2013, 62, 45–117. [Google Scholar]
  52. Hamnér, K.; Kirchmann, H. Trace element concentrations in cereal grain of long-term field trials with organic fertilizer in Sweden. Nutr. Cycl. Agroecosyst. 2015, 103, 347–358. [Google Scholar] [CrossRef]
  53. Faissal, A.; Ouazzani, N.; Parrado, J.; Dary, M.; Manyani, H.; Morgado, B.; Barragán, M.; Mandi, L. Impact of fertilization by natural manure on the microbial quality of soil: Molecular approach. Saudi J. Biol. Sci. 2017, 24, 1437–1443. [Google Scholar] [CrossRef] [PubMed]
  54. Xu, Y.; Li, H.; Tan, L.; Li, Q.; Liu, W.; Zhang, C.; Gao, Y.; Wei, X.; Gong, Q.; Zheng, X. What role does organic fertilizer actually play in the fate of antibiotic resistome and pathogenic bacteria in planting soil? J. Environ. Manag. 2022, 317, 115382. [Google Scholar] [CrossRef] [PubMed]
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Figure 1. Correlation among the physicochemical properties of the soils. **, p < 0.01; ***, p < 0.01; TDS, total dissolved salt; SOM, soil organic matter; TN, total nitrogen; HN, hydrolyzed nitrogen; AP, available phosphorus; AK, available potassium.
Figure 1. Correlation among the physicochemical properties of the soils. **, p < 0.01; ***, p < 0.01; TDS, total dissolved salt; SOM, soil organic matter; TN, total nitrogen; HN, hydrolyzed nitrogen; AP, available phosphorus; AK, available potassium.
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Figure 2. β-diversity (a), Venn diagram ((b), ASV > 0.01%), and relative abundance of bacterial communities at phylum (c) and genus (d) levels.
Figure 2. β-diversity (a), Venn diagram ((b), ASV > 0.01%), and relative abundance of bacterial communities at phylum (c) and genus (d) levels.
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Figure 3. Differences in bacterial communities between the control and treated treatments. (a), LEfSe at class level; (b), heat tree analysis. The bacteria of heat tree labeled in blue were enriched in the treated group compared to the control.
Figure 3. Differences in bacterial communities between the control and treated treatments. (a), LEfSe at class level; (b), heat tree analysis. The bacteria of heat tree labeled in blue were enriched in the treated group compared to the control.
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Figure 4. RDA (a) and correlation (b) analysis of the relationship between bacterial community and environmental factors. TDS, total dissolved salt; SOM, soil organic matter; TN, total nitrogen; HN, hydrolyzed nitrogen; AP, available phosphorus; AK, available potassium.
Figure 4. RDA (a) and correlation (b) analysis of the relationship between bacterial community and environmental factors. TDS, total dissolved salt; SOM, soil organic matter; TN, total nitrogen; HN, hydrolyzed nitrogen; AP, available phosphorus; AK, available potassium.
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Figure 5. Functions of the bacterial community in the soils predicted using FAPROTAX.
Figure 5. Functions of the bacterial community in the soils predicted using FAPROTAX.
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Table 1. Chemical and biological properties of the microbial organic fertilizer.
Table 1. Chemical and biological properties of the microbial organic fertilizer.
ItemsValues
pH6.4
Moisture content (g/kg)156
Organic matter (g/kg DM)435
Nitrogen (g/kg DM)54.4
P2O5 (g/kg DM)30.4
K2O (g/kg DM)21.3
B. subtilis (log10 cfu/g FM)8.03
B. megatherium (log10 cfu/g FM)7.80
Enterobacteria (log10 cfu/g FM)ND
Roundworm (egg/g FM)ND
Pb (mg/kg DM)ND
Cd (mg/kg DM)ND
Hg (mg/kg DM)ND
As (mg/kg DM)2.9
Cr (mg/kg DM)22.6
FM, fresh matter; DM, dry matter; ND, not detected.
Table 2. Changes in the physicochemical properties of the soil before and after treatment.
Table 2. Changes in the physicochemical properties of the soil before and after treatment.
Items aControl bTreatment
pH7.79 ± 0.152 B7.87 ± 0.134 A
TDS (g/kg)2.97 ± 1.3002.70 ± 1.854
SOM (g/kg)20.8 ± 5.33 B23.6 ± 5.18 A
TN (g/kg)1.03 ± 0.167 B2.18 ± 0.636 A
HN (mg/kg)71.3 ± 13.47 B719.6 ± 371.37 A
AP (mg/kg)17.7 ± 8.33 B40.3 ± 19.73 A
AK (mg/kg)216 ± 33.6 B245 ± 27.8 A
a TDS, total dissolved salt; SOM, soil organic matter; TN, total nitrogen; HN, hydrolyzed nitrogen; AP, available phosphorus; AK, available potassium. b Different uppercase letters (A, B) in the same row indicate significant differences (p < 0.05).
Table 3. α-diversity of bacterial communities in the soils.
Table 3. α-diversity of bacterial communities in the soils.
ItemsControlTreatment
Observed7868 ± 7407774 ± 807
ACE11,371 ± 107111,684 ± 1034
Chao111,139 ± 98511,388 ± 1041
Goods10.92 ± 0.51010.13 ± 0.889
Shannon0.997 ± 0.005 A0.988 ± 0.012 B
Simpson0.952 ± 0.005 A0.949 ± 0.005 B
Different uppercase letters (A, B) in the same line indicate significant differences between samples (p < 0.05).
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Niu, D.; Yu, M.; Xu, C.; Wang, Y.; Li, C.; Yin, D.; Zuo, S.; Ren, J. Microbial Organic Fertilizer Improved the Physicochemical Properties and Bacterial Communities of Degraded Soil in the North China Plain. Sustainability 2024, 16, 67. https://doi.org/10.3390/su16010067

AMA Style

Niu D, Yu M, Xu C, Wang Y, Li C, Yin D, Zuo S, Ren J. Microbial Organic Fertilizer Improved the Physicochemical Properties and Bacterial Communities of Degraded Soil in the North China Plain. Sustainability. 2024; 16(1):67. https://doi.org/10.3390/su16010067

Chicago/Turabian Style

Niu, Dongze, Min Yu, Chuanyang Xu, Yongjiang Wang, Chunyu Li, Dongmin Yin, Sasa Zuo, and Jianjun Ren. 2024. "Microbial Organic Fertilizer Improved the Physicochemical Properties and Bacterial Communities of Degraded Soil in the North China Plain" Sustainability 16, no. 1: 67. https://doi.org/10.3390/su16010067

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