1 Introduction
Phosphorus (P) is an essential macronutrient for plant growth
[1] and its adequate supply is critical for crop health and yield
[2]. However, about one third of agricultural soils globally lack sufficient bioavailable P
[3], posing a significant challenge for long-term agricultural productivity. Large quantities of mineral fertilizers are typically applied to meet crop P needs
[4,
5]. Under a business-as-usual scenario, it is estimated that the global P requirement exceed P-fertilizer supply by around 2040
[6]. Also, due to the strong sorption of P by soil minerals, the P-acquisition efficiency of many crops is low, leading to the accumulation of P in soil known as legacy P
[7]. Although legacy P is not readily accessible to crops
[8], it can be transformed into dissolved forms and transported to rivers and lakes via runoff. This process contributes to environmental issues such as algal blooms
[9–
11]. Therefore, improving the effective use of legacy P not only reduces agricultural fertilizer costs but also mitigates non-point source pollution from croplands, thereby supporting the sustainable development of agriculture
[12–
14].
The introduction of earthworms to soil improves its structure, enhances P bioavailability and promotes soil biological activity
[15–
17]. However, directly adding earthworms to cropland soils is often impractical due to the widespread use of pesticides in modern agriculture. Vermicompost is a nutrient- and microorganism-rich organic fertilizer and soil conditioner produced through the natural decomposition of organic waste by earthworms. It provides superior efficacy in enhancing soil-P bioavailability compared to conventional organic fertilizers, characterized by: (1) elevated bioavailable-P content
[18–
20], and (2) enhanced phosphatase activity and carboxylic acid utilization capacity in soil
[21]. Critically, vermicompost provides superior sustained P supply capacity compared to mineral fertilizers. In the tomato-wheat rotation system, single superphosphate-amended soils exhibited a significantly greater reduction in bioavailable-P content than vermicompost-treated soils
[22]. Consequently, vermicompost is often applied to mobilize legacy P and enhance both P bioavailability and crop P-use efficiency
[23].
There are several mechanisms through which vermicompost enhances soil-P bioavailability. First, earthworms have selective feeding behavior
[24] and the microorganisms within their gut mobilize P, resulting in greater concentrations of total and bioavailable P in vermicompost than in the surrounding soil
[25–
31]. For example, a meta-analysis revealed that the concentration of bioavailable P in vermicompost is 84% higher than that in surrounding soil
[32], indicating significant implications for promoting plant growth and enhancing crop yield
[16,
33]. Second, vermicompost can increase the release of dissolved inorganic P by altering soil pH and reducing the active surface area available for P sorption, thus improving P bioavailability
[28,
34]. Third, vermicompost contains phosphatases
[35–
38] that mineralize organic P, releasing inorganic P that can be taken up by plants. These mechanisms are widely recognized and have been summarized in several reviews
[23,
28,
32].
With the advancement of molecular biological techniques, recent research has increasingly focused on the role of microorganisms in vermicompost in enhancing soil-P bioavailability. Alterations in the microbial community composition within earthworm intestines
[39] and the presence of efficient P-solubilizing microorganisms in vermicompost
[21,
40] are critical factors contributing to enhanced P bioavailability in soil
[41]. Although previous reviews have addressed the effects of earthworm activity on soil microbial communities and the P cycle
[42,
43], systematic summaries of the mobilization of sparingly-soluble P in soil following vermicompost application and the microbial mechanisms involved remain lacking. In addition, a research framework specifically aimed at enhancing legacy-P utilization through microorganisms in vermicompost is yet to be developed.
This review examines the effects of vermicompost on soil-P bioavailability and explores the underlying microbial mechanisms. The specific objectives are: (1) to review the key microbial mechanisms through which vermicompost application enhances soil-P bioavailability and (2) to identify knowledge gaps and to propose future research directions.
2 Potential microbial mechanisms of soil-P mobilization after vermicompost application
The application of vermicompost to soil enhances P bioavailability via three primary mechanisms: (1) the secretion of P-solubilizing compounds by microorganisms that dissolve inorganic P, (2) the release of phosphatases that mineralize organic P, and (3) microbial cell lysis that releases bioavailable P. These processes are further affected by the altered biotic and abiotic conditions resulting from vermicompost application (Fig. 1).
2.1 Microbial dissolution of inorganic P following vermicompost application
The microbial dissolution of inorganic P in soil occurs through several mechanisms. These includes the direct release of protons (H+) that dissolve sparingly-soluble P minerals, the secretion of carboxylates and siderophores that exchange with metal-bound inorganic P. These processes are impacted by a series of interconnected mechanisms (Fig. 1).
Following the application of vermicompost, P-solubilizing compounds in the soil originate primarily from two sources (Fig. 1). First, earthworm gut harbors a variety of P-solubilizing microorganisms
[44,
45]. When these microorganisms are introduced into soil, they can release protons
[46] and carboxylates, further enhancing the bioavailability of soil inorganic P. The examples provided
[22,
47,
48] are excellent for illustrating the diversity of P-solubilizing microorganisms. Pathma and Sakthivel
[47] isolated 52 strains of P-solubilizing bacteria from vermicompost made from rice straw and sheep manure, and Parastesh et al.
[22] isolated 18 bacterial strains capable of dissolving calcium phosphate from vermicompost produced from cow manure and sycamore leaf litter. Mejía-Guerra et al.
[48] identified 28 P-solubilizing bacterial strains in vermicompost derived from tea leaves, predominantly in genera such as
Acinetobacter, Bacillus, Kocuria, Leptothrix, Microbacterium, Micrococcus, Pantoea, Pseudomonas, Rahnella, Serratia and
Streptomyces. Bhattacharya et al.
[49] isolated 30 P-solubilizing fungal strains from
Eisenia fetida vermicompost, with
Aspergillus nidulans V1 being the most efficient, capable of dissolving 13% to 36% of four P-containing minerals after just three days of incubation.
Lichteimia corymbifera is another fungal species with strong P-solubilizing abilities
[48].
Second, vermicompost has a substantial concentration of carboxylates, which, upon incorporation into soil, facilitate the dissolution of inorganic P. Fourier-transform infrared spectroscopy and
13C-CP MAS NMR analyses have confirmed the presence of abundant carboxylates in vermicompost
[50,
51]. The degradation of macromolecular organic matter by earthworms and their gut microorganisms during the composting process increases the carboxylate concentration in vermicompost
[50]. However, few studies have reported the chemical nature of these carboxylates and it remains unclear how earthworm species and composting substrates influence the quantity and composition of these compounds.
Although the precise contributions of vermicompost-derived versus microorganism-derived carboxylates are not fully understood, the rapid increase in bioavailable soil P after vermicompost application can be attributed to the carboxylates in vermicompost. In the long-term, however, microbial-released carboxylates are expected to be more significant in the dissolution of inorganic P. This is because carboxylates are rapidly degraded
[52]; vermicompost-derived carboxylates in soil likely exist for a relatively short time, however, microorganisms can continue to release carboxylates.
Microorganisms in vermicompost can release siderophores
[22,
47,
48,
53], which can mobilize iron-bound P into bioavailable P through ligand exchange
[54]. The release of siderophores by microorganisms in vermicompost thus represents another potential pathway for enhancing soil P-bioavailability.
The microbial dissolution of inorganic P can be influenced by changes in soil properties induced by vermicompost application (Fig. 1). Following the addition of vermicompost, bioavailable soil P, organic carbon (C) and nitrogen (N) concentrations typically increase
[32]. The increase in bioavailable P can reduce the need for microbial release of carboxylates to dissolve P, and the increased organic C and N concentrations provide an energy and N source for microorganisms
[55,
56], potentially enhancing microbial activity yet immobilizing P in microbial biomass. Whether these changes exert a positive or negative impact on microbial P solubilization requires further investigation.
Given that bacterial communities and their functions are highly sensitive to pH
[26,
57] and vermicompost often differs in pH from the resident soil, its addition can significantly modify soil pH
[29], thereby reshaping the microenvironment for both earthworm-associated and indigenous microorganisms. Several studies have shown that soil pH strongly influences P-mobilizing bacterial communities having
pqqC genes
[58–
60], which serves as a widely recognized molecular marker for identifying microorganisms capable of solubilizing inorganic P. Deng et al.
[61] further reported that elevated soil pH promotes the activity of a small group of
pqqC-possessing bacteria, particularly
Burkholderia,
Variovorax,
Bradyrhizobium and
Leptothrix, which are key in reducing mineral-occluded and chelated inorganic-P fractions. Despite these insights, the specific effects of pH alterations induced by vermicompost application on the composition, diversity, and P-solubilizing activity of soil microbial communities remain poorly understood. Further studies are required to elucidate how vermicompost-mediated pH shifts regulate P-mobilizing microorganisms and, consequently, influence soil-P dynamics.
In alkaline soils, inorganic legacy P is typically bound to calcium (Ca
2+), whereas in acidic soils legacy P is predominantly bound to iron (Fe
3+) and aluminum (Al
3+) (hydr)oxides
[62,
63]. Therefore, in alkaline soils, proton-mediated dissolution of inorganic P can be the dominant process by which microbes increase the solubilization of legacy P whereas carboxylate-mediated ligand exchange and other dissolution processes are likely to be more prevalent in acidic soils. The relative contribution of protons and carboxylates to the dissolution of legacy inorganic P depends on the strength of soil-P sorption
[64]. Under conditions of medium to high adsorption strength of minerals, carboxylate dissolution is more significant, whereas proton-mediated acidification becomes more so under low to medium sorption strength.
2.2 Organic-P mineralization following vermicompost application
The secretion of phosphatases by vermicompost-associated microorganisms is a crucial mechanism influencing soil-P bioavailability (Fig. 1). Many studies have demonstrated that the activity of acid and alkaline phosphatases is greater in vermicompost than in bulk soil
[35,
36,
57,
65–
67]. Both pot and field experiments have shown that vermicompost application significantly increases soil phosphatase activity
[68–
73]. In addition, vermicompost application was found to sustain elevated alkaline phosphatase activity over extended periods. In tomato-cultivated soils amended with vermicompost, alkaline phosphatase activity increased from 326 ± 2.3 to 609 ± 23.7 μg·h
–1·g
–1 PNP after 100 d, and further rose to 804 ± 198 μg·h
–1·g
–1 PNP following an additional 90-d wheat rotation
[22]. Although the individual contribution of vermicompost, vermicompost-derived microorganisms and resident soil microorganisms to phosphatase activity remains unclear, it is plausible that vermicompost-derived phosphatases introduced into the soil are rapidly deactivated by protease degradation
[74,
75]. Phosphatases adsorbed onto soil minerals can retain their activity over extended periods. However, their ability to hydrolyze organic P is highly dependent on specific mineral surfaces that effectively concentrate both the enzymes and organic-P substrates
[76]. Consequently, over longer periods, the contributions of vermicompost-derived microorganisms and resident soil microorganisms to phosphatase activity can become more pronounced, leading to a greater impact on soil-P bioavailability.
The concentrations of C and N in vermicompost can also influence microbial secretion of phosphatases (Fig. 1). Several studies have reported a significant positive correlation between the C:N ratio in composting substrates or vermicompost and phosphatase activity
[65,
74,
77,
78]. For example, adding glucose to aged vermicompost significantly increased both microbial biomass and enzyme activity
[75]. In contrast, a field trial revealed that 5 years of continuous vermicompost application (2.4 t·ha
–1·yr
–1) did not significantly increase soil phosphatase activity whereas treatments with 10-fold the amount of organic fertilizer resulted in a significant increase in phosphatase activity
[79]. This highlights the role of vermicompost C and N concentrations, as well as their ratio, in influencing microbial mineralization of organic P.
The bioavailable P in vermicompost can influence the secretion of phosphatases by microorganisms (Fig. 1). Controlled experiments have shown that the addition of bioavailable P inhibits the secretion of phosphatases
[80,
81]. In the early stages after the addition of vermicompost, the high bioavailable-P concentration can inhibit microbial phosphatase synthesis and activity. However, as bioavailable-P concentrations decrease
[82], microbial phosphatase secretion and organic-P mineralization can increase. The increase in soil mineral N concentration from vermicompost can also promote microbial mineralization of organic P. According to microbial stoichiometric theory
[83], an increase in bioavailable N concentration can lead to a higher microbial demand for bioavailable P, which would induce phosphatase secretion
[84], enhancing the mineralization of organic P.
Another important factor influencing microbial mineralization of soil organic P is carboxylates. Although some studies have indicated that phosphatases can directly hydrolyze organic P on soil particle surfaces
[76,
85], while others proposed a two-step mechanism for soil organic-P mineralization. The first step involves carboxylates forming organic-metal complexes with polyvalent metals such as Ca, Al and Fe, releasing organic P into the soil solution. The second step involves extracellular phosphatases catalyzing the hydrolysis of organic P in the soil solution, releasing soluble inorganic P
[86,
87]. Therefore, the extent of organic-P mineralization by microorganisms might also depend on the dissolution capabilities of carboxylates and siderophores, as discussed above. Vermicompost-derived microorganisms, which can secrete both carboxylates and phosphatases, are likely key participants in this process.
2.3 Microbial cell lysis following vermicompost application contributes to soil-P bioavailability
After application of vermicompost, microbial death and cell lysis can release dissolved P into the soil solution, thereby enhancing soil-P bioavailability (Fig. 1). The released dissolved P includes both inorganic and organic forms of P
[88]. Although inorganic P is immediately available for uptake by plants and microorganisms, dissolved organic P requires prior hydrolysis by phosphatases to release dissolved inorganic P for plant uptake. Numerous studies have demonstrated that the application of vermicompost to soil significantly increases both the number of soil microorganisms
[21,
22,
40,
67,
89] and microbial biomass
[68,
71,
74,
90–
92]. This increase is partly due to the direct introduction of microorganisms from vermicompost into the soil
[93,
94] and partly due to the added mineral N, organic C and P, which promote the growth and activity of resident soil microbial populations
[95,
96]. In addition, substances such as carboxylates and phosphatases in vermicompost serve as high-quality C and N sources for soil microorganisms, potentially inducing priming effects
[97,
98] and leading to further increases in microbial abundance and activity.
Although there is some variation, soil bacteria typically have a higher P concentration (18 ± 4 to 23 ± 6 g·kg
–1 P freeze-dried material) than fungi (7.6 ± 1.9 to 9.5 ± 3.2 g·kg
–1 P freeze-dried material)
[99,
100]. The proportion of soluble inorganic P in fungi (31% ± 28% to 39% ± 15%) is higher than that in bacteria (13% ± 12% to 27% ± 18%) whereas the P in bacterial biomass is primarily organic P (72% ± 18% to 84% ± 12%). Microbial biomass P, although constituting a small fraction (< 5%) of total soil P in agricultural systems
[83,
101], has a high turnover rate
[102]. In some natural ecosystems, microbial biomass P is even a major biological P pool
[103,
104]. Turner et al.
[88] demonstrated that P released from lysed bacterial cells accounted for about 88% of the increase in water-extractable P following soil drying and Achat et al.
[105] similarly observed that microbial death under desiccation elevated inorganic-P concentrations in organic matter-rich soils. Although no studies have provided a quantification of the contribution of vermicompost-derived microbial cell lysis to soil-P bioavailability, those findings collectively suggest that an increase in soil microbial biomass following vermicompost application could substantively contribute to enhancing P availability. Nevertheless, this potential mechanism remains poorly understood, and further empirical studies are needed to evaluate its quantitative significance in soil-P cycling.
3 Overview, research gaps and perspectives
3.1 Overview
This paper has reviewed the primary microbial mechanisms by which vermicompost application mobilizes legacy P in agricultural soil and thus affects bioavailable soil P. First, vermicompost-derived microorganisms can secrete P-solubilizing substances, including protons, siderophores and carboxylates, that dissolve inorganic soil P. Second, these microorganisms secrete phosphatases that mineralize organic P. Notably, the mineralization of organic P by phosphatases can be influenced by the solubilization of stable organic P through substances like siderophores and carboxylates. Additionally, resident soil microorganisms can also be stimulated to contribute to the above P-mobilizing processes following the input of vermicompost-derived organic matter. Finally, this review has highlighted a previously insufficiently-examined mechanism: microbial cell lysis, which releases dissolved P and significantly contributing to the formation of the bioavailable-P pool. The occurrence of these mechanisms is influenced by changes in soil physical and chemical properties following vermicompost application, including pH, bioavailable-P concentration, and the concentrations of mineral N, organic C, N and P (Fig. 1). Amid the global P fertilizer crisis and the growing accumulation of legacy P in soils resulting from years of repeated fertilizer application
[106], elucidating these processes is crucial for improving crop utilization of soil legacy P. Such understanding will contribute to reducing P fertilizer dependency in agricultural production and mitigating P loading in downstream aquatic ecosystems.
3.2 Research gaps and perspectives
3.2.1 Identifying and harnessing highly efficient P-solubilizing microorganisms derived from vermicompost
To enhance soil-P bioavailability in croplands through the use of vermicompost, future research should focus on identifying and harnessing highly efficient P-solubilizing microorganisms derived from vermicompost for sustainable agricultural applications. Although numerous individual P-solubilizing strains have been isolated, microbial communities as functional consortia often outperform single strains due to their greater adaptability, metabolic flexibility and resilience under variable environmental conditions
[107]. However, the diversity and abundance of P-solubilizing microorganisms in vermicompost remain insufficiently characterized
[49]. Also, most previous studies have concentrated on vermicompost effects on genes encoding N-cycling enzymes, but research on functional genes involved in P cycling is still limited
[44]. Notably, even when vermicompost from the same earthworm species is applied to different soils, a core microbial community tends to persist
[108], yet it remains unclear whether a distinct core community specializing in P solubilization exists.
Emerging approaches such as metagenomics and microbiome-wide association studies (MWAS)
[109,
110] offer promising ways to uncover efficient P-solubilizing microorganisms within vermicompost-derived communities and to link them with functional genes encoding P-cycling enzymes (Fig. 2). Shotgun metagenomics allows high-resolution profiling of microbial taxa and their functional genes involved in P solubilization and cycling. Annotation of metagenomic reads against curated databases (e.g., KEGG
[111], eggNOG
[112] and MetaCyc
[113]) enables identification of genes encoding key P-cycling enzymes, such as
phoD,
phoA,
ppx,
gcd and
pqqC, as well as genes associated with the biosynthesis of P-solubilizing compounds, including organic acids, siderophores and exopolysaccharides. Quantitative analysis of these genes across microbial populations can reveal taxa that significantly contribute to P mobilization. MWAS further complements this approach by statistically linking microbial taxa, gene abundances, or metabolic pathways with experimentally measured P-solubilization traits, such as soluble phosphate release, phosphatase activity or shifts in soil-P fractions. Integrating metagenomics and MWAS with ecological network analyses can reveal co-occurrence patterns and synergistic interactions among taxa involved in P transformation. Collectively, these approaches enable the identification of keystone microorganisms and genetic determinants of P-solubilizing capacity, facilitating the development of targeted microbial inoculants or synthetic consortia for enhancing soil-P bioavailability in vermicompost-amended systems.
3.2.2 Explore the mechanisms of microbial interactions following vermicompost application
Understanding the mechanisms of microbial interactions following vermicompost application is essential for constructing complementary and efficient P-solubilizing microbial communities (Fig. 2). Vermicompost-derived microorganisms can interact dynamically with resident soil microbiota, jointly influencing community structure and ecosystem functioning
[24,
114,
115]. For example, Liu et al.
[116] reported that vermicompost amendments significantly altered bacterial and fungal communities by increasing the relative abundance of
Acidobacteria while reducing
Proteobacteria and
Chloroflexi, and by enriching
Basidiomycota and
Glomeromycota while suppressing
Ascomycota. Similarly, Zuo et al.
[92] found that vermicompost-derived microbes increased the abundance of beneficial soil bacteria, particularly P-solubilizing groups, and de Celis et al.
[117] indicated that these effects can persist for months. In addition, vermicompost-derived beneficial microorganisms can competitively exclude pathogenic fungi such as
Fusarium spp. and
Penicillium spp
[26,
89]. Zhao et al.
[19] also found that vermicompost addition reduced the abundance of
Fusarium solani and
Acrocalymma vagum while maintaining a relatively high abundance of beneficial
Trichoderma spp. Conversely, Sasse et al.
[118] proposed that vermicompost-derived and resident microorganisms can have complementary rather than competitive resource utilization patterns, and Lipiec et al.
[119] demonstrated that vermicompost microbial communities show higher metabolic activity toward C sources compared with resident soil microbiota. Despite this evidence, whether the relationship between vermicompost-derived and resident P-solubilizing microorganisms is primarily cooperative or competitive remains unresolved, as does the overall effect of these altered interactions on soil-P transformation.
Recent advances in multi-omics technologies, including metagenomics, transcriptomics, proteomics and metabolomics, combined with mathematical modeling
[120] and artificial intelligence techniques
[121,
122], offer powerful means to elucidate these complex microbial interactions. Metagenomics can reveal community composition and functional potential, whereas transcriptomics identifies actively expressed genes and pathways mediating microbial communication and nutrient cycling. Proteomics links gene expression to enzymatic function, and metabolomics characterizes signaling and metabolic exchanges (e.g., organic acids, phytohormones and secondary metabolites) that shape microbial interactions and soil nutrient dynamics. Integration of these omics layers provides a systems-level perspective of microbial ecology that transcends single-level analyses. Meanwhile, mathematical modeling and artificial intelligence, through network inference, machine learning and predictive modeling, can synthesize multi-omics data to identify key interaction hubs, infer causal relationships and predict community responses to environmental change. Together, these approaches promise to unravel the mechanistic basis of microbial cooperation and competition in vermicompost-amended soils, thereby advancing the design of data-driven management strategies for soil health and sustainable nutrient cycling.
3.2.3 Developing synthetic microbial communities with high P-solubilizing efficiency from vermicompost-derived microorganisms
Developing synthetic microbial communities with high P-solubilizing efficiency from vermicompost-derived microorganisms represents a crucial step toward translating fundamental research into practical agricultural applications (Fig. 2). Given that rhizosphere processes can vary widely between crops and strongly influence soil microbial community structure and function
[107,
117,
118,
120], the effectiveness of vermicompost-derived P-solubilizing communities most likely depends on crop species and soil conditions
[121]. Synthetic microbial communities, by contrast, offer advantages of simplicity, controllability, reproducibility and functional specificity, enabling targeted enhancement of plant nutrient acquisition
[122,
123].
Building upon insights given above, the development of such communities should begin with the systematic screening of vermicompost-derived microorganisms across soils differing in legacy P forms. Promising isolates should then be tested for their interactions with target crops using advanced tools such as microbiome-genome-wide association studies
[107]. Once key functional strains are identified, synthetic microbial communities can be rationally assembled following established frameworks (e.g., Jing et al.
[124]) and optimized for synergistic performance. Field trials under real-world agricultural conditions should then by used to evaluate their effectiveness in improving P bioavailability, crop productivity and soil health, with iterative refinement based on observed outcomes. Ultimately, vermicompost-based synthetic microbial communities could form the foundation for scalable and sustainable biofertilization strategies that promote efficient P utilization and long-term soil fertility.
The Author(s) 2026. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)