Open access peer-reviewed chapter
Major phosphate solubilizing microorganisms.
Abstract
Phosphorus (P) is one of the macronutrients required for the optimum growth and development of plants. The deficiency of P can be compensated by adding chemical fertilisers, which are expensive and have a negative impact on the ecosystem. Solubilisation of phosphate by microorganisms is an emerging application for eco-friendly and sustainable agriculture practices. This chapter discuss the importance of P for plants, the main problems related to the over-exploitation of natural reserves of P and chemical fertilisers, the diversity of phosphate-solubilising microorganisms (PSM), the ability of microorganisms to solubilise phosphates and key mechanisms of microbial P solubilisation, the capability of microorganisms to formulate phosphate-related nanoparticles, the potential of PSM to develop as commercial level biofertiliser and contribution of PSM for achieving Sustainable Development Goals (SDGs). This chapter will highlight the input of PSM in sustainable agriculture.
Keywords
- phosphate
- Solubilisation
- microorganisms
- plant
- soil
1. Introduction
Phosphorous (P) is an essential macronutrient in plants [1, 2] which represents 0.12% of earth’s crust [3, 4]. The sources of P are available in both organic and inorganic forms [2, 5], which are non-renewable and cannot be substituted [4, 6]. Rock phosphate (apatite) is the best P source compared to the other P resources such as soil, clay, plant and animal matter [4], which is commonly used for phosphate fertiliser production also [7]. Phosphorous is reaching to be a plant nutrient that will limit crop production in the next millennium. P is a major growth-limiting mineral, and unlike nitrogen, there is no large atmospheric source that can provide biologically available P. Furthermore, the low bioavailability of phosphate limits the efficacy of P fertiliser. As the option to manage the bioavailability of phosphate for plants, phosphate-solubilising microorganisms (PSM) can be an effective, eco-friendly and sustainable tool. PSM contributes to improving plant growth and yield while reducing the need for chemical fertilisers that can have negative impacts on the environment. Additionally, PSM phosphate solubilisation can help to improve the overall health and fertility of the soil, promoting sustainable agriculture practices [8].
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2. Importance of P for plants
P is engaged in biological processes that are shared by all living species [1, 2, 9]. P, in particular, is the second most limiting macronutrient for plant growth, accounting for 0.2% of plant dry weight [10, 11] and serving as a critical element in animal bodies [12, 13, 14]. As a result, P has become a fundamental and necessary component for human well-being [15].
Functions of P in all living organisms included energy metabolism and transmission [1, 9], cell division [2], protein and nucleic acids (DNA and RNA) synthesis [9, 16, 17], being a key component of enzymes, coenzymes, and phospholipids [18] and cell division [2]. In addition, P is essential for plants for photosynthesis [2], nitrogen fixation [14], improving crop quality [14, 16], development of disease resistance [18], root development [3], development of the stems and stalks [15], flower and seed formation [10], conversion of sugar to starch [10], laying down the primordia of propagative parts during the early stages of plant development [16], and proper stress reduction and maturation of plant [10]. A lack of phosphorus can lead to stunted growth, delayed maturity, and lower yield. Therefore, it is essential to ensure that plants receive adequate phosphorus to maintain their health and productivity.
The world population is expected to exceed 9000 million in 2050 [19] and food production requires to be increased globally by 50% as compared to the demand in 2012 [20]. Usability of phosphate has been severely limited due to its low bioavailability. Furthermore, the wastage of phosphate that is unable to be utilised by plants and animals causes additional issues such as eutrophication [10, 21]. The low bioavailability of phosphate is driving its increasing usage, with peak extraction occurring in 2030 [22]. Therefore, the sustainable utilisation of phosphate is needed to increase its bioavailability to avoid the wastage of phosphate [4]. Using microorganisms to increase the bioavailability of phosphate is the emerging eco-friendly technique for sustainable utilisation of phosphate [10, 23].
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3. Main problems related to the over-exploitation of natural reserves of P and chemical fertilisers
Global food production needs to be increased due to the rapidly increasing world population [20]. The low bioavailability of phosphate directly affects to not being able to fulfil the required amount of crop production. Due to the low bioavailability, an extra amount of phosphate has to be utilised as fertilisers to provide the optimum requirement of P of plants. Therefore, it is directed to high utilisation, and the peak extraction of phosphate will take place in 2030 [22]. Besides the depletion of natural P resources, over-exploitation of natural reserves of P and excessive use of chemical P fertilisers lead to several environmental and agricultural problems such as soil degradation, groundwater contamination, eutrophication and climate change [10, 21]. Hence, it is highly required for sustainable utilisation of phosphate to minimise wastage [4]. State-of-the-art technique to use microorganisms to solubilise the insoluble forms of phosphates and increase their bioavailability is an effective option [10, 23].
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4. Diversity of phosphate-solubilising microorganisms (PSM)
PSM are diverse and can be found in various environments such as water, and plant tissues while the soil is the key habitat [10, 12]. The population of PSMs in soil ranges between 104 and 106 g−1 of soil, and they are accumulated at the rhizosphere of plants, and those organisms are highly metabolically active [10, 24]. In the microbial profile of soil, phosphate-solubilising bacteria (PSB) were responsible for 1–50%, whereas phosphate-solubilising fungi (PSF) represent 0.1–0.5%. The population density of PSB ranged between 8 × 105 and 5.33 × 109 in the different rhizospheres of vegetable fields, with PSB accounting for 3.98% of the total population of bacteria [25]. Most of PSBs are coccus, bacillus or spirillum in shape while the bacillus is the most abundant and spirillum are rare. However, there is a high diversity of PSM in the soil. Among these microbial species,
The number of PSM is not sufficiently high to compete with other microbial species in the rhizosphere. The profile and population of these PSM vary between ecosystems due to the influence of complex biological factors [25]. Physical-chemical factors of soil such as the soil nutrient status, moisture content, organic matter, soil pH, and soil enzyme activities affect these variations [4, 12, 24]. The diversity of PSM (Table 1) is important for maintaining healthy ecosystems, as they play a critical role in the phosphorus cycle by making this important nutrient more available to plants [25].
| Microorganisms | Country | References |
|---|---|---|
| China | [26] | |
| Iran | [27] | |
| Spain | [28] | |
| Iran | [27] | |
| Indonesia | [29] | |
| India, China | [30, 31] | |
| Indonesia | [29] | |
| Italy | [32] | |
| Pakistan | [33] | |
| Spain, Iran | [27, 28] | |
| India | [34] | |
| Pakistan | [35] | |
| Pakistan | [35] | |
| China, Brazil, Spain, Thailand | [28, 36, 37, 38, 39] | |
| Thailand | [36] | |
| Mexico | [37] | |
| Pakistan | [35] | |
| USA | [38] | |
| Mexico | [37] | |
| India, Indonesia, Brazil | [29, 34, 39] | |
| Pakistan | [33] | |
| USA | [38] | |
| India | [34] | |
| Indonesia | [29] | |
| Indonesia | [29] | |
| China | [40] | |
| Spain | [28] | |
| India | [34] | |
| Indonesia | [29] | |
| Iran | [27] | |
| China | [26] | |
| Morocco | [41] | |
| China | [42] | |
| China | [43] | |
| China | [44] | |
| Italy | [32] | |
| India | [34] | |
| Brazil | [45] | |
| Morocco | [46, 47] | |
| China | [43] | |
| China | [42] | |
| China | [26] | |
| Brazil | [45] | |
| China | [43] | |
| Pakistan | [33] | |
| Tunisia, Morocco | [41, 48] | |
| USA | [38] | |
| Iran | [49] | |
| Brazil | [45] | |
| Pantoea roadsii(LMG26273) | China | [43] |
| Morocco | [41] | |
| USA | [38] | |
| China | [43] | |
| Pakistan | [35] | |
| Tunisia | [50] | |
| India | [51] | |
| Morocco | [41] | |
| Egypt | [52] | |
| China | [43] | |
| Tunisia | [50] | |
| China | [43] | |
| Morocco | [41] | |
| Mexico | [37] | |
| Egypt | [52] | |
| India | [51] | |
| China | [42] | |
| India | [51] | |
| USA | [38] | |
| Iran | [49] | |
| China | [42] | |
| Italy | [32] | |
| China | [40] | |
| Morocco | [41] | |
| India | [34] | |
| Tunisia, China | [26, 50] | |
| Morocco | [47] | |
| Morocco | [46] | |
| Morocco | [46, 47] | |
| Morocco | [46] | |
| Morocco | [46] | |
| Morocco | [46] | |
| Iran | [27] | |
| Iran, Indonesia | [27, 29] | |
| Iran | [27] | |
| China | [53] |
Table 1.
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5. Ability of microorganisms to solubilise phosphates and key mechanisms of microbial P Solubilisation
Phosphorous is available in the soil as a number of organic and inorganic compounds due to its high reactivity, and those are unavailable for plants [54]. PSMs solubilise these insoluble forms of phosphates into soluble by secreting complex compounds such as organic acid anions, protons, exopolysaccharides, siderophores, hydroxyl ions and extracellular enzymes [55]. The phosphate-solubilising mechanism of PSM has two major aspects as inorganic phosphate solubilisation and organic phosphate solubilisation based on the substrate of P [3].
5.1 Inorganic phosphate solubilisation by PSM
Microbial mobilisation of inorganic phosphates is involved with the production and secretion of organic acids, inorganic acids, siderophore and exopolysaccharide and proton extrusion by the PSM [3].
5.1.1 Organic acid production
The key mechanism of phosphate solubilisation is the secretion of the organic acids that result from the carbon metabolism of PSM, which is closely related to the concentration of soluble phosphate [3, 4, 24]. Low-molecular-weight organic acids are synthetised during glucose oxidation through direct periplasmic oxidation and intracellular phosphorylation. The synthesis of organic acids from glucose by the cells of PSMs in phosphate deficient conditions is higher than in phosphate sufficient conditions, which correlates with the effect of soluble phosphate on organic acid production [56].
The release of these organic acids into the environment is accompanied by a decrease in pH and chelate of the cations (such as Al3+, Fe3+, and Ca2+) bound to phosphate ions to release the phosphate [3, 8]. These organic acids compete with the phosphate binding sites of the medium and allow phosphates to be available in free [15] as HPO4−2 and HPO4−3 [10]. However, there is no correlation between pH and the amount of solubilised phosphates [56]. Gluconic acid is the frequent secretion among all organic acids released by PSM (Table 2) [3, 10, 54]. PSF may be even more important than PSB since they typically produce and excrete more acids [56].
| Organic acid | PSM | References | |
|---|---|---|---|
| Acetic acid | [57] | ||
| Caproic acid | [57] | ||
| Citric acid | [12] | ||
| [57] | |||
| [10, 58, 59, 60] | |||
| Formic Acid | [12] | ||
| [57] | |||
| Fumaric acid | [10, 59, 60] | ||
| Gluconic acid | [12] | ||
| [57] | |||
| [10, 58, 59, 60] | |||
| Glycolic acid | [12] | ||
| [10, 58] | |||
| Heptonic acid | [57] | ||
| Indole acetic acid | [12] | ||
| Isobutyric acid | [57] | ||
| Isocaproic acid | [57] | ||
| Isovaleric acid | [57] | ||
| Itaconic acid | [57] | ||
| Lactic acid | [12] | ||
| [57] | |||
| Malic acid | [12] | ||
| [57] | |||
| [10, 58, 59] | |||
| Malonic acid | [57] | ||
| Oxalacetic acid | [57] | ||
| Oxalic acid | [12] | ||
| [57] | |||
| [10, 58] | |||
| Propionic acid | [57] | ||
| Succinic acid | [12] | ||
| [57] | |||
| [10, 58, 59, 60] | |||
| Tartaric acid | [12] | ||
| [57] | |||
| [10, 59] | |||
| Valeric acid | [57] | ||
| 2-Keto gluconic acid | [12] | ||
| [57] | |||
| [10, 59, 60] | |||
Table 2.
Major examples of the production of organic acids by PSM.
5.1.2 Inorganic acid production
Inorganic acid-producing bacteria also involve with phosphate solubilisation through acidification. Bacteria, engaged in nitrification and sulphur-oxidation, which have the ability to produce inorganic acids, are involved with phosphate solubilisation by secreting nitric, carbonic, sulphuric [3] and hydrochloric acids [4, 24]. Nitrifying bacteria such as
5.1.3 Proton extrusion
Another alternative mechanism to solubilise phosphate is extrusion of proton, which minimise the requirement to synthesis acids [3]. Excretion of H+ through H2CO3 production, NH4+ assimilation and liberation of organic acid anions facilitate the solubilisation of phosphates by acidifying the media [3, 8, 10]. The release of H+ to the extracellular surface of PSM through the exchange of cation or the ATPase activity with H+ translocation, lead to the solubilisation of P [56].
5.1.4 Exopolysaccharide production
Exopolysaccharides are high molecular weight compounds that indirectly affect the solubilisation of P in soil [65]. Microorganisms secrete exopolysaccharides under stress conditions; exhibit the potential to promote phosphate solubilisation [3, 66]. Exopolysaccharides have a strong affinity with the metal ions in the soil, which have formed complexes with phosphates and release those phosphates. There is a positive correlation between the rate of phosphate solubilisation and the concentration of exopolysaccharides [3]. Different exopolysaccharides have different binding affinities with various metals, and there are also different binding strengths between the metals themselves.
5.1.5 Siderophore production
Siderophore production is a usual ability of microorganisms, while it is used by PSM as another alternative method to solubilise the phosphate [3, 10, 15]. Siderophores are low-molecular-weight secondary metabolites synthesised by PSM that have a strong affinity for inorganic iron and act as metal chelators. Siderophores contain three functional groups hydroxamates, catecholates, and carboxylates, which catalyse the reduction of Fe3+ to Fe2+. PSM use siderophores to obtain the Fe as the requirement of cellular functions, and during the dissociation of its bond, P is released and available for plants.
5.2 Organic phosphate solubilisation mechanisms
5.2.1 Enzyme production
The content of organic phosphorus in the soil can reach 30–50% of the total amount, which is represented by compounds such as phosphonates, phytic acid, polyphosphonates, sugar phosphates [3, 56], phosphomonoesters, phosphodiesters, phosphotriesters [8], phospholipids and nucleic acids [3, 8]. Generally, these high molecular weight organic compounds are resistant to chemical hydrolysis and need to be converted into soluble ionic phosphate or low-molecular-weight organic phosphates for plant uptake [56].
PSM produce and secrete the enzymes to solubilise the organic phosphates [8]. There are several groups of enzymes are secreted by PSM as [3, 8, 54, 55, 56],
Non-Specific Acid Phosphatases (NSAPs)
Phytases
Phosphonatases
Carbon–Phosphorus Lyases
NSAPs are a class of enzymes secreted extracellularly or bound to the lipoprotein membranes of PSM. NSAP are generally known as phosphomonoesterases, which dephosphorylate a wide variety of phosphoesters, solubilising around 90% of organic phosphate in soils. The proportion of phosphatases and abundance of P in the soil has a direct relationship, which influences the availability of phosphates to plants. According to the authors, the activity of NSAPs is more concentrated in the rhizosphere than in other parts of soil and phosphatase activity, P uptake by plants and nodule weight has a positive correlation [56].
Phytase enzymes are phosphatases produced by PSM, which have the capability to hydrolyse phytic acid by acting on the phosphomonoester bonds present in the compound, originating two subgroups, myo-inositol hexaphosphate or phytate. In addition to P, this process makes biologically available other nutrients such as zinc and iron [65].
Phosphatases (phosphonate hydrolases) are enzymes, which promote the breaking of C-P bonds of phosphonates by catalysing this reaction from a group carbonyl electron scavenger that allows heterologous cleavage between nutrients. Phosphonatases act on several substrates, including phosphoenolpyruvate, phosphonoacetate, and phosphoenol-acetaldehyde and make biologically available P for plants [56, 65].
Carbon–phosphorus lyases are a complex of membrane enzymes released by PSM that also allow the making available of P, cleaving the C–P bonds of phosphonates, producing hydrocarbons and inorganic Phosphate. This complex is the leading mechanism for the utilisation of phosphonates by PSM. The enzymes and proteins of C–P lyases are complex and specific to their substrates.
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6. Capability of microorganisms to formulate phosphate-related nanoparticles
Nanotechnology is a state-of-the-art technique of using particles between 1 to 100 nm, which originated as both organic and inorganic forms [67, 68, 69]. Nano minerals are currently used as plant fertilisers due to their Nano size, high surface area, and higher solubility in different solvents and penetrative capacity than conventional mineral fertilisers. Reduction of the particle size is directed to an increment of the surface area of particle and the number of particles per unit in fertiliser, which facilitate higher nutrient utilising efficacy. Nanoparticles enter into plants through nano and microscale openings, which are most commonly available in roots and leaves [70, 71]. Generally, root tips, rhizodermis, lateral root junctions and wounding of roots are the entering pathways to nanoparticles. Enhanced bioavailability of nano fertilisers than conventional fertilisers cause to prevent loss of nutrients from leaching, denitrification, volatilisation, and fixation in the soil to confirm the sustainable utilisation of minerals [70].
Microorganisms including bacteria, fungi, actinobacteria and viruses have the ability to synthesise phosphorus-related nanoparticles with well-defined chemical composition, morphology and size either intra-or extracellularly [71, 72, 73]. But no in-depth study or work has been done so far [74]. Enzymes [75, 76] such as phytase, phosphatases [75], extracellular polymeric substances (EPS) [76] and proteins [75] are the key potential materials to synthesise phosphorus-related nanoparticles which are produced by microorganisms. In addition, proteins act as capping agents to stabilise the produced nanoparticles [75]. This is a new arising area in nano formulations [74]. Therefore, limited research has been conducted on synthesising phosphorus-related nanoparticles by using microorganisms, as mentioned in Table 3.
| Microbe | Type of Nano P | Size/Shape | Application | References |
|---|---|---|---|---|
| Phosphorous | 17–64 nm | Plant fertiliser | [77] | |
| Phosphorous | 37-81 nm | Plant fertiliser | [77] | |
| Phosphorous | 23–88 nm | Plant fertiliser | [77] | |
| Phosphorous | 11–74 nm | Plant fertiliser | [77] | |
| Phosphorous | 5–49 nm | Plant fertiliser | [77] | |
| Phosphorous | 20–91 nm | To maintenance of soil fertility | [73, 75] | |
| Phosphorous | 55–92 nm | Plant fertiliser | [77] | |
| Phosphorous | 12–36 nm | Plant fertiliser | [77] | |
| Yeast | Zinc Phosphate | 10–80 nm in width and 80–200 nm in length, Butterfly like shape | Antirust pigment and electronic luminophore | [78] |
Table 3.
Microbial synthesis of phosphorus-related nanoparticles.
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7. Potential of PSM to develop as a commercial level biofertiliser
The distinctive and unique ability of PSMs to solubilise organic and inorganic phosphates, leads to their developed as commercial level bio fertilisers [10, 12]. Biofertilisers are microbiologically active, eco-friendly, low-cost products applied to soil expecting soil health and growth promotion of plants [10, 15]. Biofertilisers can be replaced by 50% instead of chemical fertilisers without any reduction of the yield [15]. These phosphate bio fertilisers are not crop-specific and able to be used for any type of plant, expecting growth promotion, high yield and crop quality through optimum phosphate absorption [10].
Biofilm inoculants and nano-bio inoculants are ultra-modern techniques in biofertiliser formulation technology. Biofilm inoculants are the combination of two microorganisms, while one microorganism colonises over the other microorganism. The second microorganism act as a biotic surface for the first microorganism to develop a metabolically enhanced biofilm rather than a single culture [3]. Even though these relationships affect the high phosphate solubilisation and growth promotion of plants, the abundance in the soil is very low [3, 79]. Therefore, applying these biofilms as biofertilisers through artificial formulation is advantageous in agriculture [3].
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8. Contribution of PSM to achieving sustainable development goals (SDGs)
Collection of 17 interlinked objectives focusing on prosperity for people and the planet called United Nations Sustainable Development Goals (SDGs) able to be enforced with PSMs. Microbial phosphate solubilisation makes way for sustainable development by promoting plant growth, food security, industrial growth, environmental sustainability and water security [81, 82].
Continuous fertilisation to supply the optimum requirement of phosphate for crops due to the low bioavailability is not the appropriate way, and it is a waste of the resource [83]. Responsible consumption of the resource (SDG 12) able to be confirmed by the involvement of PSMs in increasing the bioavailability of phosphate. It reduces the accumulation of excess phosphate with associated other chemicals as fertilisers to soil and contributes to building up sustainable terrestrial ecosystems with reverse land degradation to halt biodiversity loss (SDG 15) [84]. Moreover, the sequestration of phosphate in the soil leads to eutrophication, which causes disruptions of valuable aquatic resources and pollution the water [85]. Therefore, reducing the excess utilisation of phosphate fertilisers by developing PSM as biofertilisers will ensure the sustainable conservation of aquatic resources (SDG 14) and sustainable management of available clean water (SDG 06) [82, 86].
The contribution of PSM to sustainable agriculture through plant growth promotion ensures sufficient food production empowering food security, which promotes public nutrition and ends hunger (SDG 02) [87, 88]. Development of the sustainable agricultural industry (SDG 09) confirm sustainable economic growth (SDG 08) with moving forward to the reduction of poverty (SDG 01) [89]. Society, which reaches economic development by overcoming poverty and hunger, ensures a better living environment promoting a sustainable peaceful society by accessing justice (SDG 16) [90]. The direct and indirect contributions of PSMs to achieve the SDGs affect significantly strengthen the framework of the 2030 agenda of the United Nations [82].
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9. Conclusion
The application of PSMs as a tool in managing soil and plant nutrients through Solubilising phosphate is an efficient and eco-friendly method. Bacterial and fungal species are majorly involved in the phosphate solubilisation in soil, remarking
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Acknowledgments
The paper was supported by the research grant of “Accelerating Higher Education and Development” (AHEAD) under development-oriented research (DOR) of STEM grant number AHEAD/RA3/DOR/WUSL/LAS No.57 funded by the World Bank.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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