Home The potential of phosphorus-solubilizing purple nonsulfur bacteria in agriculture: Present and future perspectives
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The potential of phosphorus-solubilizing purple nonsulfur bacteria in agriculture: Present and future perspectives

  • Nguyen Quoc Khuong , Le Tien Dat , Ly Ngoc Thanh Xuan , Le Thanh Quang and Nguyen Khoi Nghia EMAIL logo
Published/Copyright: August 12, 2024

Abstract

Phosphorus (P) is one of the essential macronutrients for crops. It is present in soil in two forms: soluble and insoluble. However, plants cannot absorb the insoluble forms, including Al-P, Fe-P, and Ca-P; thus, the phosphorus use efficiency is reduced. Therefore, the biological approaches should focus more on sustainable agriculture to overcome this constraint. This article cites publications relating to the biological P solubilizer group of bacteria, which have a highly potential adaptation to many conditions in soils. Among the biological approaches, purple nonsulfur bacteria (PNSB) are a potent group of bacteria according to their adaptability in acidic, saline, and toxic conditions based on their mechanisms in producing exopolymeric substances and siderophores under such adverse environments like acid-sulfate and saline soils. PNSB can solubilize P in soil to have more P availability for soil microbes and plants. This particular group of bacteria has been widely applied in liquid and solid forms from agricultural waste to promote plant growth under submerged conditions. Moreover, this article summarized the P-solubilizing mechanisms of P-solubilizing bacteria and introduced future research perspectives on patterns of PNSB in aspects of nutrient-providing potency, plant growth-promoting capability, and biological control capacity. However, the specific mechanisms of P solubilization by PNSB have not been well documented since the P-solubilizing mechanisms have been investigated on general P-solubilizing bacteria. Thus, specific pathways and metabolites relating to the P-solubilizing PNSB should be investigated, and attention should be addressed to them soon.

1 Introduction

More and more crops are suffering from nutrient limitation to their productivity in soils, and phosphorus (P) is one of the most critical limiting nutrients [1]. Consequently, farmers tend to use more P chemical fertilizer to maintain crop yield as expected. However, its use may become excessive [2,3]. Also, despite their excessive intake, plants take up only 10–20% of the P fertilizer applied to soil [4] because P is precipitated and absorbed by minerals, for example, Al, Fe, and Ca [5]. Overusing P chemical fertilizer can lead to soil acidification, destruction of food web systems, water contamination, and decreased soil fertility [6,7,8,9]. Moreover, the P chemical fertilizer types are considered one of the highest crop input costs [10,11]. That is why biological approaches have been conducted to find a long-term efficient way to increase P use efficiency in agriculture. Manure has been applied to reduce the amount of P chemical fertilizer in crop cultivation, and the results are positive; for example, replacing more than 50% of chemical fertilizer with manure improves soil fertility and P use efficiency [12]. However, microbial applications are more potent because the microbes can make use of insoluble P compounds existing in the soil [13] rather than supplying more P from organic sources. For instance, in the study by Emami et al. [14], rhizospheric and endophytic bacteria enhanced P use efficiency in wheat. The most well-known bacterial genera are Pseudomonas, Bacillus, Rhizobium, and Enterobacter [15]. Among them, using purple nonsulfur bacteria (PNSB) is a promising and suitable approach for soils in the Mekong Delta of Vietnam. This is because apart from solubilizing P, the PNSB can adapt to a broad range of conditions; that is, they can grow well under anaerobic light aerobic dark cycles [16], acidic and saline conditions [17,18], and contaminated environments [19]. The PNSB can also fix nitrogen and produce plant growth-promoting compounds, e.g., indole 3-acetic acid [20], 5-aminolevulinic acid (ALA) [21], and exopolymeric substances (EPS) [22]. Recently, there has been an increase in studies investigating the roles of P-solubilizing PNSB in soil health and crop yield [23,24,25,26]. Still, the ways in which insoluble P compounds are solubilized and how PNSB are used to function in agriculture have not been well summarized. Ultimately, in this article, the mechanisms of solubilizing P from insoluble fractions in soil by phosphorus-solubilizing bacteria (PSB) have been clarified and reviewed along with the recent achievements in studying P-solubilizing PNSB. Moreover, the current P status is also mentioned, and possible ways to apply PNSB to crops are also discussed.

2 Applications of PSB to achieve sustainable agriculture

2.1 Importance of phosphorus nutrients to the crops

There is no doubt that P is one of the most essential nutrients for crops because it is a part of many biological molecules, such as enzymes and nucleic acids. It has been investigated for nearly 200 years to determine its relationship between the yield of crops [27]. P is involved in many processes within a plant, such as the development of roots and stalks, formation of flowers and seeds, strength of stem, maturity, N-fixation processes, and fruit quality [28]. However, the cycle of P is different from other essential nutrients, such as nitrogen (N) and carbon (C), since it does not go through gaseous forms under the temperature and pressure of the Earth [29]. Additionally, inorganic P in soil is typically immobilized by many forms of soil series, for example, Fe, Ca, and Al, resulting in insoluble P compounds [30]. That is why P is the most immobilized element compared to other macronutrients [28]. Therefore, P use efficiency is poor. In the study by Johnston and Poulton [27], crop yield and P availability are positively correlated, from which a threshold of P fertilizer required can be found by the analytical method of Olsen. If soils possess available P near a certain critical level, P use by plants is effective; that is, P chemical fertilizer applied is equal to the amount of P taken up by crops, thereby keeping soil P near the critical level. This will not only make crop yield and P applied efficiency optimal but also inhibit P amount leaking to the environment [27].

2.2 Disadvantages of chemical fertilizers

Although inorganic P is extremely important to plants, it comes from nonrenewable resources [31]. The increase in food demands led to higher production of P chemical fertilizers [32]. There are many sources of P chemical fertilizer with different P2O5 contents. It can be divided into three main types of P chemical fertilizer: (1) water-soluble, including superphosphate (16–20% P2O5), monoammonium phosphate (61% P2O5), and diammonium phosphate (46% P2O5); (2) insoluble, including apatite (rock phosphate, 20–30% P2O5) and bone meal (18–20% P2O5); and (3) citrate soluble, including dicalcium phosphate (35–40% P2O5), and basic slag (3–5% P2O5) [33]. In most acidic soils like acid-sulfate soils (high amount of H+), P is precipitated with Al and Fe oxides and, thereby, becomes insoluble for plants to uptake. The P chemical fertilizer is considered to be an easy solution to improve the availability of soil P for plants to overcome the limitation of P in soils not being available to plants [34]. However, P fertilizer applications may cause severe damage to surrounding environments, such as acidification and hardening of the soil and soil fertility reduction [35]. Moreover, manure is another additional source of organic P, which helps improve soil fertility, especially available P content, and crop yield [36,37,38,39].

2.3 Status of phosphorus nutrients in the soil

Most soils have higher total P content than other macronutrients, such as N and potassium (K) [31]. However, 80% of P is precipitated and unavailable for plants to uptake [40]. The unavailable P portion in the soil is usually organic and inorganic forms (organic P and inorganic P), whose ratio is different throughout the soil types [41]. Organic P interacts with soil particles weakly, but the inorganic one remains in more stable forms [42]. The P applied to the soil in the form of chemical fertilizer is usually deficient in plants and stored in the soil as unavailable forms of P because of the adsorption, precipitation, and immobilization processes [43]. For the adsorption, available P from chemical fertilizers applied to the soil surface alters other anions, whose affinity is worse in soil particles and gets adsorbed [44,45]. Although some P desorption processes happen in soil, the desorption rates are much slower than others [46]. Precipitation occurs due to metallic cations within the soil, i.e., P is bound to Fe, Ca, and Al [47]. Common P minerals are determined to be the following: strengite (FePO4·2H2O) and variscite (AlPO4·2H2O) in acidic soils; and tricalcium phosphate [Ca3(PO4)2], dicalcium phosphate (CaHPO4), dicalcium phosphate dihydrate (CaHPO4·H2O), fluorapatite [Ca5(PO4)3F], hydroxyapatite [Ca5(PO4)3OH], and octacalcium phosphate [Ca4H(PO4)3·2–5H2O] in neutral and calcareous soils [48]. Therefore, after P is fertilized chemically into the soil, P adsorption and precipitation happen until reaching the equilibrium [44]. Moreover, in some soils, these processes can account for 80% of the total P amount in soil [49]. Although the primary mechanism of P solubilization in soil is low soil pH [28], mechanisms to solubilize organic P and inorganic P fractions in soil are found differently.

2.3.1 Organic P

Organic P accounts for 20% of total P in soil [50]. It remains in three types of bonds in soil, including phosphate esters, phosphatases, and phosphoric acid anhydrides [2]. Insoluble organic P compounds have to go through mineralization processes to make available P for plants [30]. These processes are facilitated by phosphatases and phytases secreted by soil microorganisms [51,52]. Phytase is known to be the primary enzyme responsible for releasing the organic P in soil [53]. The half-life of the extracellular phosphatases secreted by soil microbes is usually short in soil because they can be inactivated by metal inhibitors, adsorption, proteolysis, pH, and ionic strength shifts [54]. Significantly, PSB have been reported to be able to enhance the activity of soil phosphatase. A similar reveal has also been found in the study by Khuong et al. [55], where the soil phosphatase activity was found to increase when PNSB strains of Rhodopseudomonas palustris were applied into the soil, in comparison to the control treatment without inoculation. In other words, the density of PNSB applied was positively correlated with the phosphatase enzyme activity; that is, these PNSB can produce phosphatase. Because plants can use only inorganic P to mobilize P from organic P compounds, a two-step process is required, consisting of P being released from precipitating and adsorbing positions and then mineralized by enzymes [56,57]. On the contrary, pH is also found to drive the P-solubilizing genes and microbial community composition [58]. When the culture pH dropped to 4.55, soluble P and the activity of acid phosphatase produced by Ochrobactrum sp. J023 were valued at 161.29 mg L−1 and 61.98 U mL−1, respectively [59].

2.3.2 Inorganic P

Popular forms of insoluble inorganic P are calcium phosphate [Ca3(PO4)2], aluminum phosphate (AlPO4), ferrous phosphate (FePO4), zinc phosphate [(Zn3(PO4)2], and manganese phosphate [(Mn3(PO4)2], which can be dissolved into soluble P under the contribution of microorganisms in the soil [30,60,61,62,63,64]. Although there have been many theories involved in microorganisms, the secretion of low molecular mass organic acids (OAs) has been considered a well-studied and accepted one as a principal mechanism of P-solubilization and those OAs have been studied for their identification and roles in solubilizing processes [65,66,67]. OAs are low molecular weight compounds and can solubilize P by chelating the phosphorus-bound cation with OAs’ hydroxyl and carboxyl groups to release the linkage between the P and the cations and simultaneously lower the rhizospheric pH [68]. Those acids usually are oxalic, lactic, citric, succinic, acetic, and formic acids [69,70]. The OAs can chelate metal ions to release P from the insoluble sources [71] or reduce soil pH to result in proton substitution for Ca2+ [72]. In the study by Maliha et al. [66], the production of OAs by the bacteria and fungi to solubilize P was roughly 2.4747 and 1.835 g L−1, respectively, along with the drop from pH 7.0 to below pH 3.0. A species of fungi, Penicillium oxalicum, was found to be able to solubilize P and lower medium pH at the same time, and the production of OAs by this fungus was lactic acid (0.054 mmol L−1), acetic acid (0.054 mmol L−1), oxalic acid (0.064 mmol L−1) with pH from 7.0 to 2.0 [70].

2.4 Biological P solubilization as an effective alternative

P-solubilizing microorganisms take part in remedying P deficiency for crops in soil. They can solubilize P for themselves and a vast amount of soluble phosphate to the environment in a quantity that exceeds the microbes’ P demand [73]. Some bacteria are found to be produced by OAs and phosphatases [13], which are key mechanisms of P solubilization and mineralization, respectively, and were isolated from peat soil [74]. Thus, this excess production of soluble P can be a source of the P nutrient for plants. Either individual or mixed application of P-solubilizing microbes (optionally with other beneficial microbes, e.g., bacteria) enhanced yield and P uptake of crops [28]. They appear in all kinds of soil, but their diversity and quantity differ from soil types and climates [73]. Moreover, higher concentrations of P solubilized by microbes were found in solid environments rather than liquid ones. For instance, in the study by Anu and Kundu [75], in chickpeas, 76 strains of PSB were isolated with P-solubilizing efficiencies ranging from 6 to 118% for the solid medium, while in the broth, the number was from 22 to 248 μg/mL. Moreover, the PSB strains obtained from the rhizosphere of tomatoes in the study by Kouam et al. [76] solubilized P from 277.44 to 1929.29 μg/mL in a liquid medium. Additionally, Acinetobacter pittii gp-1 solubilized P roughly from 7.91 to 250.77 μg/mL in liquid medium and from 3.80 to 7.11 μg/mL in solid medium [77]. Furthermore, in the study by Amri et al. [78], a PSB, Pseudomonas fluorescens, isolated from sandy soils showed a great P solubilization, roughly from 535.70 to 618.57 μg/mL. Additionally, from phosphate solid sludge, PSB strains of Pseudomonas, Serratia, Pantoea, and Enterobacter showed a high P-solubilizing capacity from 101.91 and 174.33 μg/mL [79]. Therefore, applying PSB into the soil helps reduce the chemical P fertilizer application but still supports crop growth and yield performance [73]. By improving crop productivity, soil health also benefits from P [80] in an environmentally friendly, inexpensive, and effective way [81].

3 Phosphate-solubilizing bacteria

3.1 Diversity of phosphate-solubilizing bacteria and their mechanisms

Bacteria and fungi account for the majority of P-solubilizing microorganisms. Of these microorganisms, bacteria, including Escherichia freundii, Bacillus subtilis, Pseudomonas spp., Arthrobacter spp., Bacillus spp., B. firmus B-7650, P. radicum, Enterobacter agglomerans, Bacillus amyloliquefaciens, Bacillus licheniformis, Penibacillus macerans, Xanthobacter agilis, Enterobacter aerogenes, Enterobacter intermedium, and P. fluorescens, make a more significant contribution than fungi [28]. Their habitat is mainly in the rhizosphere. PSB, for example, Bacillus, Burkholderia, Azospirillum, Erwinia, Pseudomonas, Rhizobium, and Serratia, are known to be able to transform insoluble P forms into soluble forms that plants may assimilate [82,83]. They play an essential role in the cycle of P, while they mineralize organic P, solubilize inorganic P, and store P in their biomass [84,85]. Some bacteria are salt-tolerant and capable of solubilizing P. Thereby, they can maintain P-solubilization in saline soils [73]. In the study conducted by Baliah et al. [86], some novel PSB were identified as Bacillus megaterium, Pseudomonas putida, and P. fluorescens. As mentioned above, there are two ways to solubilize P compounds in soil, regardless of whether they are organic or inorganic forms. For inorganic sources, the fundamental principle is to lower the pH of the soil by causing soil bacteria to produce low molecular weight OAs [73]. These acids can either release P as the mechanism of anion exchange or chelate with metal ions, such as Fe, Al, and Ca, which bind to P [73]. In the study by Behera et al. [87], a PSB strain PSB-37, whose identity was Serratia sp., was isolated from mangrove soil. This strain possessed the highest P-solubilizing activity at 44.84 μg/mL. Concurrently, the pH of the culture medium dropped from 7.00 to 3.15. Moreover, many OAs are found within the culture during the inoculation time, for example, malic acid 237.0 mg/L), lactic acid (599.5 mg/L), and acetic acid (5.0 mg/L). Moreover, the use of efficient OAs and the production of inorganic acids (H2CO3), exopolysaccharides, and siderophores contribute to P solubilization. Conversely, for organic P compounds, the term “mineralization” is used, i.e., activities of enzymes of phosphatases and phytase carry out the hydrolysis of ester or anhydride bonds of phosphate compounds and finally release soluble P into the soil [73]. Genes responsible for P cycles in soil have been analyzed in the study by Liang et al. [85]. In this research, 36 genes accountable for P cycles are found and divided into three functions: solubilization (mineralizing organic P and solubilizing inorganic P), transporter, and regulatory genes. Among these, gcd, phoD, and phoA account for 70% of abundance, and gcd can be considered the most important in the P solubilization process. However, the P solubilization of the PSB sometimes causes a decrease in pH due to the secretion of OAs by the bacteria [88]. Moreover, this is not suitable for farming on acidic soils, whose pH is already low. In particular, Vietnamese soils are suffering from both acidification and salinization. Nevertheless, under the P solubilization by the PNSB, the soil pH did not decrease in the studies by Huu et al. [23] and Khuong et al. [89]. Moreover, the PNSB can be active in aerobic and anaerobic conditions [90]. This makes the PNSB suitable for the Mekong River Delta’s wet–dry cycles [91].

3.2 PNSB

3.2.1 P-solubilizing PNSB

Among the PSB, PNSB are capable of interacting with plants [92], thus enhancing plant growth by solubilizing P [89,93] and secreting phytohormones [94]. As in the PSB group, PNSB may have similar P-solubilizing mechanisms. However, studies on the P-solubilizing mechanisms of PNSB are still rare. For example, in the study by Khuong et al. [95], siderophores are found to be a P-solubilizing metabolite produced by PNSB. Furthermore, Lo et al. [96] found some genes coding for phosphatase, lyase CP, phosphatase inositol-phosphate, and OAs, which are related to the P solubilization processes in the genomes of PNSB species. Therefore, further studies should take place to gain the molecular level of knowledge about the P-solubilization of this group of bacteria. Moreover, the PNSB can also adapt to a variety of field conditions, such as acidic [95], saline [17], acidic saline [89], and contaminated conditions [19]. This makes the PNSB group different from the PSB and promising in applying to different types of soils, especially soils being transformed by climate change and overfertilization [97,98]. The major groups of PNSB in agriculture are Rhodopseudomonas spp. and Rhodobacter spp. [99]. Their natural habitats are humid soils, wastewater ponds, lagoons, lakes, sediments, high-salt systems, wetland ecosystems, and marine ecosystems [100,101,102]. Most PNSB can live under aerobic dark or anaerobic light conditions [103]. The PNSB can live both as an autotroph and as a chemotroph based on the energy source. Moreover, the PNSB can also produce substances to reduce the adverse effects of the environment, such as ALA against salinity [104], EPS against acidity and salinity [105], and siderophores against heavy metals [106]. This makes them promising for being applied in soil in the Mekong River Delta, Vietnam, where soil and crops are usually submerged. Moreover, ALA and siderophores are believed to involve mechanisms to solubilize P [107]. Some applications of PNSB have been made in agriculture, and the outcomes are very interesting. Specifically, in rice and sugar leaf, yield rises by 29 and 69.2%, respectively [92,108]. In addition, PNSB are also able to synthesize bioactive compounds, such as bioherbicides, antiviral substances, and antimicrobial compounds for plant protection from pathogenic microbes [94]. They can also synthesize riboflavin, iron carriers, ALA, EPS, and bacterial acyl-high serine lactone for stimulating plant resistance to diseases [109]. In addition, the P solubilization usually relates to the pH reduction [73]. This is not appropriate for use in acidic soils, while some applications of PNSB to solubilize P increase soil pH [23,24,93]. Thus, the PNSB are suitable candidates to solubilize P in acidic soils. Some PNSB species determined to be able to solubilize P have been identified as R. palustris [110,111], Luteovulum sphaeroides [93], and Rhodospirillum rubrum [112]. Figure 1 shows how these bacteria improve plant growth. In particular, the P-solubilizing PNSB increases P availability by P solubilization and produces plant growth-promoting substances, leading to better root development and greater leaf area, that is, better photosynthesis capacity and a better crop yield [20].

Figure 1 
                     A summary of crop yield improvement by P-solubilizing PNSB. Source: Prepared by Authors.
Figure 1

A summary of crop yield improvement by P-solubilizing PNSB. Source: Prepared by Authors.

3.2.2 Recent applications of PNSB: Mixed and single-use

Forming spores is an essential property of PNSB as biofertilizers. Other P-solubilizing microbes that do not produce spores in their life cycle are more vulnerable when applied on the field [113,114]. Moreover, their inoculants need to be in an appropriate formula; if not, the bacteria may be damaged, short in half-life, and unable to survive under adverse conditions [115]. Some PNSB strains have been used as biofertilizers for different types of crops, as shown in Table 1.

Table 1

Types, origins, targets, and functions of recent PNSB biofertilizers

PNSB biofertilizer Form Origin Target Function Chemical fertilizer replacement Reference
Rhodopseudomonas palustris spp. N/A Peat swamp forest Rice in acidic soil Biocontrol, production of PGPS, N2-fixation, and P-solubilization N/A [111]
Rhodopseudomonas palustris TK103, PP803, and P1 (6.7–6.8 log CFU mL−1) Solid Rubber sheet wastewater and saline paddy soils Rice in saline soils Production of PGPS reduces methane emissions N/A [93]
Rhodopseudomonas palustris VNW64, VNS89, TLS06 and VNS02 (108 cells g−1) Solid Acidic paddy soils Sesame in salt-affected soil N2-fixation and P-solubilization 50% N and 50% P [116]
Rhodopseudomonas palustris TLS06, VNW02, VNW64, and VNS89 (108 CFU mL−1) Liquid Acidic paddy soils Rice in acid sulfate soil Al3+ and Fe2+ reduction, N2-fixation, and P-solubilization 25% N and 50% P [117]
Rhodobacter sphaeroides W48 and W42 (108 cells mL−1) Liquid Acid sulfate soil Pineapple in acid sulfate soil P-solubilization 25% P [23]
Rhodopseudomonas palustris ISP-1 (108 CFU mL−1) Liquid Peanut fields Peanut P-solubilization and organic P-mineralization N/A [25]
Rhodopseudomonas palustris VNW64, VNS89, TLS06, and VNW02 (108 cells mL−1) Liquid Acidic soils Canary melon in alluvial soil P-solubilization 25% P [24]
Rhodopseudomonas palustris YSC3, YSC4, and PS3 (4.0 × 106 CFU g−1 soil) Liquid Rice paddy fields Chinese cabbage N2-fixation P-solubilization 50% N [118]
Rhodopseudomonas palustris spp. (2.45 × 108 CFU mL−1) Liquid (Foliar) Paddy soils Rice N/A N/A [119]

N/A: not available; PGPS: plant growth-promoting substances.

3.2.2.1 In liquid form

One of the most common applications of PNSB is in liquid biofertilizers [120]. In this form, the bacteria are stored and supplied to plants as broth. The benefits of this procedure are that the inoculants are easy to make and store at a low cost in its additives, e.g., coconut juice, polyvinyl alcohol, xanthan gum, gelatin, mineral oil, horticultural oil, and Arabic gum, which can elongate the half-life of the cells within the products [121,122,123,124,125,126]. Horticultural oil is mainly added to liquid-based PNSB inoculants to maintain the cell for a long time (up to a month) at any temperature [123]. However, liquid inoculants may have some obstacles in transportation. In a study by Khuong et al. [55], a liquid application of PNSB, including R. palustris and R. harwoodiae, was used to supply rice in acid-sulfate soil and efficiently increased available P, thereby enhancing rice growth and grain yield.

3.2.2.2 In solid form

Unlike the liquid form, the solid form application of PNSB can simultaneously contain one or even more strains in a carrier material [94]. The PNSB’s survival was supported by an appropriate carrier material in this form. It gives the bacteria a safe environment to avoid adverse conditions and promotes a storage time of up to 6 months [127]. Carrier materials are usually made from formulations of dry, solid, or granular materials [127], such as peat, clay, compost, wheat bran, rice husk, wood ash, and sodium alginate, which are considered to have the highest efficiency [94,128,129,130]. Moreover, apart from the efficiency, the carrier materials should have low cost, enough availability in amounts, no toxicity to plants and inoculated bacteria, good moisture absorption, and good binding to the bacterial community [131]. In the meantime, wood ash can enhance the growth and activity of bacteria, i.e., higher expression of genes that contribute to metabolism and cell growth is induced [132]. In addition, palm oil may also be a fine carrier material since it can ameliorate soil fertility and plant development [133]. Furthermore, rice husk ash and spent coffee grounds, byproducts from rice production and the coffee industry, have features that promote plant growth. In detail, a rice husk ash carrier material has characteristics of good porosity and high water-holding capacity, which help maintain the bacteria and stimulate their growth inside the carrier material [134]. Concurrently, the spent coffee ground contains a high amount of K, Mg, and P [135], and it also assists the bacteria with good adhesion to soils [136]. In the study by Sakpirom et al. [131], a mixture of rubber wood ash, decanter cake rice husk ash, and spent coffee ground was used to carry PNSB strains of R. palustris and Rubrivivax gelatinosus, resulting in higher seedling growth than that of the liquid form of supplementation. Moreover, not only did a solid combination of six PNSB strains of R. palustris (TLS12, VNS19, VNS32, VNS62, and VNW95) and R. harwoodiae (TLW42) lead to a decrease of 20% in the chemical fertilizer used in this study via increasing available P content from P solubilization process, but also it reduced up to 36% of Mn content in rice grains [55].

3.2.3 Foliar application: A new and promising way to apply PNSB

A disadvantage of applying PNSB in either liquid or solid form is that the bacteria are easily affected by biological and nonbiological factors within the soil. Moreover, the addition of xenobiotic bacteria to the soil or the change in the density of indigenous bacteria in the soil may have tremendous effects on the microbial community and their structures. For these reasons, the advent of foliar fertilization has occurred. In the study by Yen et al. [119], rice was applied with PNSB by foliar fertilization. The result was robust, that is, root length, root dry biomass, productive tillers per plant, grains per plant, grain yield, 1,000-grain weight, and harvest index increased over the control treatment by 25, 57, 26, 38, 33, 1.6, and 41%, respectively. Unlike the nutrients providing function as the two above forms, this type of application is primarily aimed at preventing pathogens via biological control carried out by strains of PNSB. For instance, strains of PNSB could produce bioactive compounds such as EPS and lipopeptides to prevent diseases in crops. For EPS, R. palustris GJ-22 has been applied to tobacco plants to promote resistance against the tobacco mosaic virus [137]. This is due to the activity of an EPS called G-EPS, which can perform antiviral activity and stimulate the systematic resistance of tobacco plants [109]. Furthermore, the R. palustris GJ-22 strain has been used to prevent late blight in potatoes resulting from the oomycete Phytophthora infestans [138]. Not only does EPS secretion by PNSB benefit crops, but it can also boost their life under difficult conditions, as demonstrated by Nunkaew et al. [17], who found that R. palustris PP903 and TN114 produced EPS under high-salt conditions, extending their longevity. In the study by Nookongbut et al. [111], the PNSB strains, R. palustris KTSSR54, KTSWR26, KKSSG39, and KTSWR2, were applied on rice and showed activities against pathogens caused by fungi. Among them, the R. palustris KTSSR54 performed excellently on inhibitions against three types of diseases on rice, including brown spot (caused by Bipolaris oryzae NPT0508), leaf spot (caused by Curvularia lunata SPB0627), and rice blast (caused by Magnaporthe oryzae PTRC63), by releasing EPS [18]. For lipopeptides, Pseudomonas sp. can antagonize fungal pathogens on sugar beet and rice via lipopeptide production mechanisms [139,140]. Additionally, the GroEL protein, produced by the R. palustris PSB-06, can inhibit crop disease and boost plant resistance in rice against the M. oryzae [141]. Apart from solely protecting crops from pathogens, PNSB strains can work with other microorganisms to carry out antagonism against pathogens as well. For example, the combination of the yeast and the R. palustris can inhibit the grey mold disease due to the growth of Botrytis cinerea fungi [142]. Moreover, when the PNSB, R. faecalis, was paired with the Bacillus aerophilus, a high antifungal activity was found [143]. Ultimately, the above PNSB strains have great potential in being applied to the foliar application due to their high performance in either antagonizing pathogens or inducing plant resistance to them, particularly R. palustris KTSSR54 and GJ-22.

4 Future perspectives

Although PNSB have been widely studied in laboratories and greenhouses [120], their on-field performances have not been fully discovered [144]. In the field, the environment’s complexity and diversity caused by various biological or nonbiological factors may heavily affect the functions of the bacteria before they can deliver their benefits [127]. For all these reasons, biofertilizers made of PNSB have difficulties in commercialization. Therefore, ensuring PNSB’s survival and functions is a must. As a result, encapsulation is the next step in researching PNSB. In the study by Rohman et al. [130], mixing alginate with 4% (w/v) starch results in microcapsules whose entrapment efficiency is 70.83% (higher than 50.56% of the control beads) and spherical shape is maintained after drying. However, this encapsulation production has not been performed in the field. Additionally, appropriate frequencies and concentrations of PNSB biofertilizers applied to crops have not been standardized due to the diversity of data obtained from previous studies [145]. Thus, research on PNSB should concentrate on indigenous strains and factors that contribute to their survival in various conditions, such as saline, alluvial, and acidic soils.

5 Conclusions

This article revealed that there has been a great demand for the improvement of P in agriculture due to low P availability in the soils. However, applying P fertilizer is not an effective way to enhance the availability of P within the soil due to P being fixed by different compounds in soil types, and it may cause several severe impacts on the environment as well. Additionally, mechanisms of P mineralization and P solubilization processes have been reviewed. However, the P-solubilizing microbes encounter a problem in that they are vulnerable to the soil environment, while the PNSB appears to be a remarkably potent approach. This study was one of the first to summarize the current status of research on P-solubilizing PNSB and their applications and introduce a future outlook of applying P-solubilizing PNSB more effectively. The PNSB can form spores that make them more adaptable to the surrounding environment. In particular, they can survive and grow under various conditions (acidity, salinity, toxicity, etc.), common conditions in the Mekong River Delta, Vietnam, and they can also solubilize P without increasing soil acidity. Therefore, the P-solubilizing PNSB can reduce the dependence on chemical P fertilizers as biofertilizers to improve soil health and be in alignment with the goals of sustainable agriculture. However, although the PNSB can provide available P for crops from insoluble sources of soil P fractions, such as Fe-P, Al-P, and Ca-P, based on the improvement in soil P availability and decreases in insoluble P content, the accurate mechanisms of the P-solubilizing PNSB have not been thoroughly investigated up to now. Therefore, future studies should focus on the pathways and the metabolisms of P solubilization by PNSB. Moreover, the PNSB biofertilizers have been used in liquid and solid forms and newly sprayed to leaves instead of soil amendments. However, different studies used different concentrations of PNSB inoculants under different soil characteristics, regions, climates, crops, and so forth, leading to data from different research groups differing, though the results are all promising. Thus, PNSB should be investigated in relation to indigenous strains, how to keep them alive, and what their functions are.

  1. Funding information: This research was funded by Vietnam National University HoChiMinh City (VNU-HCM) under grant number B2024-16-02.

  2. Author contributions: All authors have accepted responsibility for the entire content of this manuscript and consented to its submission to the journal, reviewed all the results and approved the final version of the manuscript. NQK: conceptualization, writing – original draft; LTD: writing – original draft; LNTX: conceptualization, writing – original draft; LTQ: conceptualization, writing – review and editing; NKN: conceptualization, writing – review and editing.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.

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Received: 2024-01-14
Revised: 2024-06-20
Accepted: 2024-06-28
Published Online: 2024-08-12

© 2024 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  106. Harnessing synthetic microbial communities with nitrogen-fixing activity to promote rice growth
  107. Agronomic and economic benefits of rice–sweetpotato rotation in lowland rice cropping systems in Uganda
  108. Response of potato tuber as an effect of the N-fertilizer and paclobutrazol application in medium altitude
  109. Bridging the gap: The role of geographic proximity in enhancing seed sustainability in Bandung District
  110. Evaluation of Abrams curve in agricultural sector using the NARDL approach
  111. Challenges and opportunities for young farmers in the implementation of the Rural Development Program 2014–2020 of the Republic of Croatia
  112. Yield stability of ten common bean (Phaseolus vulgaris L.) genotypes at different sowing dates in Lubumbashi, South-East of DR Congo
  113. Effects of encapsulation and combining probiotics with different nitrate forms on methane emission and in vitro rumen fermentation characteristics
  114. Phytochemical analysis of Bienertia sinuspersici extract and its antioxidant and antimicrobial activities
  115. Evaluation of relative drought tolerance of grapevines by leaf fluorescence parameters
  116. Yield assessment of new streak-resistant topcross maize hybrids in Benin
  117. Improvement of cocoa powder properties through ultrasonic- and microwave-assisted alkalization
  118. Potential of ecoenzymes made from nutmeg (Myristica fragrans) leaf and pulp waste as bioinsecticides for Periplaneta americana
  119. Analysis of farm performance to realize the sustainability of organic cabbage vegetable farming in Getasan Semarang, Indonesia
  120. Revealing the influences of organic amendment-derived dissolved organic matter on growth and nutrient accumulation in lettuce seedlings (Lactuca sativa L.)
  121. Identification of viruses infecting sweetpotato (Ipomoea batatas Lam.) in Benin
  122. Assessing the soil physical and chemical properties of long-term pomelo orchard based on tree growth
  123. Investigating access and use of digital tools for agriculture among rural farmers: A case study of Nkomazi Municipality, South Africa
  124. Does sex influence the impact of dietary vitD3 and UVB light on performance parameters and welfare indicators of broilers?
  125. Design of intelligent sprayer control for an autonomous farming drone using a multiclass support vector machine
  126. Deciphering salt-responsive NB-ARC genes in rice transcriptomic data: A bioinformatics approach with gene expression validation
  127. Review Articles
  128. Impact of nematode infestation in livestock production and the role of natural feed additives – A review
  129. Role of dietary fats in reproductive, health, and nutritional benefits in farm animals: A review
  130. Climate change and adaptive strategies on viticulture (Vitis spp.)
  131. The false tiger of almond, Monosteira unicostata (Hemiptera: Tingidae): Biology, ecology, and control methods
  132. A systematic review on potential analogy of phytobiomass and soil carbon evaluation methods: Ethiopia insights
  133. A review of storage temperature and relative humidity effects on shelf life and quality of mango (Mangifera indica L.) fruit and implications for nutrition insecurity in Ethiopia
  134. Green extraction of nutmeg (Myristica fragrans) phytochemicals: Prospective strategies and roadblocks
  135. Potential influence of nitrogen fertilizer rates on yield and yield components of carrot (Dacus carota L.) in Ethiopia: Systematic review
  136. Corn silk: A promising source of antimicrobial compounds for health and wellness
  137. State and contours of research on roselle (Hibiscus sabdariffa L.) in Africa
  138. The potential of phosphorus-solubilizing purple nonsulfur bacteria in agriculture: Present and future perspectives
  139. Minor millets: Processing techniques and their nutritional and health benefits
  140. Meta-analysis of reproductive performance of improved dairy cattle under Ethiopian environmental conditions
  141. Review on enhancing the efficiency of fertilizer utilization: Strategies for optimal nutrient management
  142. The nutritional, phytochemical composition, and utilisation of different parts of maize: A comparative analysis
  143. Motivations for farmers’ participation in agri-environmental scheme in the EU, literature review
  144. Evolution of climate-smart agriculture research: A science mapping exploration and network analysis
  145. Short Communications
  146. Music enrichment improves the behavior and leukocyte profile of dairy cattle
  147. Effect of pruning height and organic fertilization on the morphological and productive characteristics of Moringa oleifera Lam. in the Peruvian dry tropics
  148. Corrigendum
  149. Corrigendum to “Bioinformatics investigation of the effect of volatile and non-volatile compounds of rhizobacteria in inhibiting late embryogenesis abundant protein that induces drought tolerance”
  150. Corrigendum to “Composition and quality of winter annual agrestal and ruderal herbages of two different land-use types”
  151. Special issue: Smart Agriculture System for Sustainable Development: Methods and Practices
  152. Construction of a sustainable model to predict the moisture content of porang powder (Amorphophallus oncophyllus) based on pointed-scan visible near-infrared spectroscopy
  153. FruitVision: A deep learning based automatic fruit grading system
  154. Energy harvesting and ANFIS modeling of a PVDF/GO-ZNO piezoelectric nanogenerator on a UAV
  155. Effects of stress hormones on digestibility and performance in cattle: A review
  156. Special Issue of The 4th International Conference on Food Science and Engineering (ICFSE) 2022 - Part II
  157. Assessment of omega-3 and omega-6 fatty acid profiles and ratio of omega-6/omega-3 of white eggs produced by laying hens fed diets enriched with omega-3 rich vegetable oil
  158. Special Issue on FCEM - International Web Conference on Food Choice & Eating Motivation - Part II
  159. Special Issue on FCEM – International Web Conference on Food Choice & Eating Motivation: Message from the editor
  160. Fruit and vegetable consumption: Study involving Portuguese and French consumers
  161. Knowledge about consumption of milk: Study involving consumers from two European Countries – France and Portugal
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