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Silva, L.I.D.; Pereira, M.C.; Carvalho, A.M.X.D.; Buttrós, V.H.; Pasqual, M.; Dória, J. Phosphorus-Solubilizing Microorganisms. Encyclopedia. Available online: https://encyclopedia.pub/entry/41866 (accessed on 21 December 2024).
Silva LID, Pereira MC, Carvalho AMXD, Buttrós VH, Pasqual M, Dória J. Phosphorus-Solubilizing Microorganisms. Encyclopedia. Available at: https://encyclopedia.pub/entry/41866. Accessed December 21, 2024.
Silva, Leandro Israel Da, Marlon Correa Pereira, André Mundstock Xavier De Carvalho, Victor Hugo Buttrós, Moacir Pasqual, Joyce Dória. "Phosphorus-Solubilizing Microorganisms" Encyclopedia, https://encyclopedia.pub/entry/41866 (accessed December 21, 2024).
Silva, L.I.D., Pereira, M.C., Carvalho, A.M.X.D., Buttrós, V.H., Pasqual, M., & Dória, J. (2023, March 03). Phosphorus-Solubilizing Microorganisms. In Encyclopedia. https://encyclopedia.pub/entry/41866
Silva, Leandro Israel Da, et al. "Phosphorus-Solubilizing Microorganisms." Encyclopedia. Web. 03 March, 2023.
Phosphorus-Solubilizing Microorganisms
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This entry is adapted from the peer-reviewed paper 10.3390/agriculture13020462

Phosphorus (P) is one of the essential macronutrients for plant growth, being a highly required resource to improve the productive performance of several crops, especially in highly weathered soils. However, a large part of the nutrients applied in the form of fertilizers becomes “inert” in the medium term and cannot be assimilated by plants. Rationalizing the use of phosphorus is a matter of extreme importance for environmental sustainability and socioeconomic development. Therefore, alternatives to the management of this nutrient are needed, and the use of P-solubilizing microorganisms is an option to optimize its use by crops, allowing the exploration of less available fractions of the nutrient in soils and reducing the demand for phosphate fertilizers.

phosphorus mobilization mineralization microbial mechanisms

1. Phosphate-Solubilizing Microorganisms

Phosphate solubilizing microorganisms (PSM) are a group of organisms composed of actinobacteria, bacteria, fungi, arbuscular mycorrhizae, and cyanobacteria capable of hydrolyzing organic and inorganic phosphorus into soluble forms, thus making it bioavailable to plants [1][2]. They are quite abundant in the soil, and commonly associated with the rhizosphere of plants [3]. Djuuna et al. [4] performed a sampling of these microorganisms in Indonesia. Agricultural soils with a relevant history of growing vegetables, cereals, and legumes from different regions were collected. The results showed a population of solubilizing bacteria ranging between 25 × 103 and 550 × 103 CFU g–1 of soil and solubilizing fungi between 2.0 × 103 and 5.0 × 103 CFU g–1 of soil in all areas examined.
There is also great diversity in PSM. Bacteria have several representatives of the genera Azospirillum, Bacillus, Pseudomonas, Nitrosomonas, Erwinia, Serratia, Rhizobium, Xanthomonas, Enterobacter, and Pantoea [1][3]. Among the non-mycorrhizal fungi are the genera Penicillium, Fusarium, Aspergillus, Alternaria, Helminthosporium, Arthrobotrys, and Trichoderma, [2][5]. Examples of mycorrhizal fungi are Rhizophagus irregularis, Glomus mossea, G. fasciculatum, and Entrophospora colombiana [6][7].
Among actinobacteria, the genera Streptomyces, Thermobifida and Micrococcus are examples of PSM [8][9][10][11], and cyanobacteria, Calothrix braunii, Westiellopsis prolifica, Anabaena variabilis, and Scytonema sp. [1][3].

2. Phosphate Solubilization Mechanisms

Phosphate-solubilizing microorganisms have several mechanisms to increase the availability of this element in the soil. Figure 1 brings together the mechanisms and processes involved in the nutrient dynamics in the soil and the various interactions with the microbiota. The main roles of microorganisms in P solubilization include (1) the release of extracellular enzymes (biochemical mineralization), (2) the release of P during substrate degradation (biological mineralization), and (3) the secretion of mineral-dissolving complexes or compounds (siderophores, protons, hydroxyl ions, organic acids) [6][12].
Agriculture 13 00462 g001 550
Figure 1. Phosphorus cycle and nutrient mobilization. The numbers and symbols at the base of the arrows are related to the P mobilization process described in the heading of the figure. The numbers related to the mechanisms correspond to the topics in which they are explained. NSAPs (4.1.1), phytases (4.1.2), phosphonatases (4.1.3), C–P lyases (4.1.4), organic acids (4.2.1), inorganic acids (4.2.2), enzymes or enzymolysis (4.2.3), siderophores (4.2.4), exopolysaccharides (4.2.5), proton release (4.2.6), H2S production (4.2.7), and direct oxidation (4.2.8).
Microorganisms interact in diverse ways in terms of the bioavailability of nutrients in plants. Mycorrhizal fungi, for example, can provide an increase in the root surface from the proliferation of their mycelium, helping in the exploitation of nutrients in the soil, thus accessing soil portions, such as microaggregates, previously not accessible to the plant only by root exploration [13][14].
In addition, PSM presents several mechanisms to make phosphate available in its soluble form. When the substrate is organic, the processes are described as mineralization, which is a step in the decomposition process of organic matter, while inorganic substrates undergo solubilization processes [1][6][15].

2.1. Organic Phosphate

Organic phosphate corresponds to 20–30% of the total amount found in the soil [6]. Its main source of entry into the environment is biomass, being present in animal and plant debris, and in microbial cell membranes, that is, they constitute biomolecules such as phosphides, nucleotides, phosphoproteins, co-enzymes, sugar phosphates, phosphonates and can be immobilized in the form of humus [16][17][18].

2.1.1. Non-Specific Acid Phosphatases (NSAPs)

NSAPs are a class of enzymes bound to the lipoprotein membranes of microorganisms or secreted extracellularly [19][20]. Also known as phosphomonoesterases, they act according to the optimal pH of the environment, and can therefore be acidic or alkaline [21][22]. These enzymes can dephosphorylate a wide variety of phosphoesters (RO–PO3), solubilizing around 90% of organic phosphate in soils [23][24]. 
The proportion of phosphatases is relative to the abundance of P in the soil and consequently influences the availability of this nutrient to plants. Fraser et al. [25] indicated that in soybean (Glycine max) fields labile P in bulk soil was negatively correlated with phoC and phoD genes abundance (acid and alkaline phosphatase encoders, respectively) and phosphatase activity. According to the authors, the activity of NSAPs is greater in the rhizosphere than in other soil portions. A positive correlation was also observed between phosphatase activity, P uptake by plants, and nodule weight.

2.1.2. Phytases

Phytic acid is the major form of organic P present in the soil and is a component of seeds and pollen [1][26][27]. However, because they form complexes with cations or are adsorbed on various soil organic components, they are not readily available for plant assimilation [1]. Phytase enzymes are phosphatases produced by soil microorganisms. They are capable of hydrolyzing phytic acid by acting on the phosphomonoester bonds present in the compound, originating two subgroups, myo-inositol hexaphosphate or phytate (salt form). This process means that, in addition to P, other nutrients associated with it also become available, such as zinc and iron [28][29]. 
Wang et al. [30] investigated the effect of mycorrhizal hyphae-mediated phytase activity. Maize (Zea mays) cultivars inoculated and non-inoculated with the arbuscular mycorrhizal fungi Glomus mosseae or Claroideoglomus etunicatum were evaluated, and the plants were separated into two compartments, one with only roots and the other with hyphae of the tested fungi supplemented with different concentrations of calcium phytate. The effect of phytase and acid phosphatase on phytate mineralization was analyzed. The authors observed that at higher phytate addition, the rate decreased, and lower phytate addition caused an increased hyphal length density; phytate addition increased phytase and acid phosphatase activity resulting in greater P uptake and plant biomass. It was concluded that the observed increases in P uptake were primarily due to phytase activity rather than phosphatase activity.

2.1.3. Phosphonatases

Phosphonates are organic phosphoric compounds rich in hydrolytically stable C–P bonds that are chemically inert and resistant to thermal and photolytic decomposition [31][32]. The enzymes that promote the breaking of this bond are known as phosphatases (phosphonate hydrolases) and act by catalyzing this reaction from a group β-carbonyl electron scavenger that allows heterologous cleavage between nutrients [32]. Phosphonatases act on several substrates, including phosphoenolpyruvate, phosphonoacetate, and phosphoenol-acetaldehyde. 
Furthermore, organophosphoric compounds are the active components of many pesticides, as they interfere with the catalytic activity of key enzymes in the target organism (such as acetylcholinesterase and phosphate synthases) [33][34]. However, studies indicate that these compounds are very persistent in the environment and may harm the quality of soil, water, and even the germination of non-target plants [35][36][37]. Soil microorganisms act on the bioremediation of these xenobiotics, using them as a source of P [38], thus contributing to the reduction of toxicity in the soil while converting the inert P of the phosphonate into a nutrient assimilable to plants.
Chávez-Ortiz et al. [39] studied the effects of glyphosate and commercial formulation (CH) on soil nutrient dynamics and microbial enzymatic activity. Two plots were used: one with a 5-year history of glyphosate application (NP) and the other with a history of agricultural management without glyphosate application (AP). The authors found that the application of CH in the AP soil favored the specific activity of the phosphonatase. The study shows how the application of the herbicide shapes the microbial community, and how it adapts to metabolize the xenobiotic.

2.1.4. Carbon–Phosphorus Lyases

Carbon–phosphorus lyases are a complex of membrane enzymes that also allow the release of P, cleaving the C–P bonds of several classes of phosphonates (i.e., alkyl, amino-alkyl, and aryl phosphonates), producing hydrocarbons and inorganic phosphate [40][41]. This complex is the main mechanism for the use of phosphonates by microorganisms [42].
The enzymes and proteins of C–P lyases are complex and specific to their substrates. In Escherichia coli, they are all encoded by the 14-cistron operon (Phn CDEFGHIJKLMNOP), which is activated under conditions of phosphate deficit allowing the use of phosphonates [43]. 
Kryuchkova et al. [38] analyzed the effect of several growth-promoting bacteria on glyphosate degradation. Among the bacteria analyzed, Enterobacter cloacae K7 proved to be both resistant to a 10 mM concentration of the herbicide and enabled its degradation in vitro (40% of the initial 5 mM content). The authors also analyzed the intermediate metabolites involved in the degradation and verified, using thin-layer chromatography, the activity of C–P lyase in the conversion of glyphosate to sarcosine, and later oxidation to glycine.

2.2. Inorganic Phosphate

In turn, inorganic P is the most abundant conformation of phosphorus found in soil, 70–80% of its total [1]. In soil, it can be a constituent of primary or secondary minerals or adsorbed on metallic oxides and clay [44][45].

2.2.1. Organic Acids

Organic acids are low-molecular-weight compounds secreted by PSM and produced in oxidative metabolic pathways [46]. They are described as the main mechanism for inorganic phosphate solubilization [47]. The main organic acids produced are gluconic and 2-keto gluconic [2][48]. In addition, the release of oxalic, acetic, fumaric, malic, succinic, and tartaric acid, among others, may also occur [49][50].
In general, when released, organic acids acidify the rhizosphere, which causes a drop in pH, and the cations linked to phosphorus are chelated from their hydroxyl and carbonyl groups [51][52]. In addition, these acids can compete with P-adsorption sites and form complexes with P-bound metal ions [1][53][54].
Mendes et al. [55] analyzed the effectiveness of organic acids commonly associated with P solubilization by microorganisms for the solubilization of phosphate rocks with different degrees of reactivity. Increasing concentrations of oxalic, gluconic, citric, malic, and itaconic acids were used in vitro, and their effectiveness in solubilization was compared with that of sulfuric acid. The authors saw that oxalic acid was the most effective for the solubilization of rocks composed of apatite and was superior to sulfuric acid. On average, each mmol of oxalic acid released 21 mg of P, while sulfuric acid solubilized 14 mg of P mmol−1.
Patel et al. [56] analyzed the ability of Citrobacter sp. DHRSS for solubilization of phosphate rocks. The researchers used different carbon sources to produce the organic acids responsible for solubilization. It was seen that on sucrose and fructose, the bacteria released 170 and 100 μM of phosphate and secreted 49 mM (2.94 g/L) and 35 mM (2.1 g/L) of acetic acid, respectively. With glucose and maltose, Citrobacter sp. DHRSS produced approximately 20 mM (4.36 g/L) of gluconic acid, and the released phosphate was 520 and 570 μM, respectively.

2.2.2. Inorganic Acids

In general, inorganic acids act in an equivalent way as organic acids, lowering the pH of the environment and acting as chelators; however, they are less effective in the same pH range [1][57]. Examples of these acids include sulfuric, nitric, carbonic, and hydrochloric [58][59].
Cantin et al. [60] conducted a series of experiments to figure out the effectiveness of the combination of a mixture containing commercial elemental sulfur + sewage sludge inoculated with different combinations of bacteria of the genus Thiobacillus in the solubilization of apatite P. The combinations used were (1) T. thioparus ATCC 23645, (2) T. thioparus C5 + T. thioparus ATCC 8085, and (3) T. thioparus ATCC 23645 + T. thiooxidans ATCC 55128. The phosphate solubilization capacity was verified in apatite–sulfur culture medium (ASM) with 1, 10, or 20% (P/V) of apatite. The results showed that T. thioparus ATCC 23645 alone lead to a decrease in pH in vitro (from 6.8 apatite 1; or 7.8 apatite 2 to 3.9), confirming that the bacterium is capable of oxidizing sulfur into sulfuric acid. Furthermore, the researchers saw that the consortia of combinations 2 and 3 were more effective for phosphate solubilization than the inoculum with isolated bacteria. In addition, researchers evaluated the release of P from the inoculum when applied to municipal wastewater sludge and incubated with concentrations of 1, 10, or 20% (P/V) of apatite for 33 days. It was seen that 28% of the initial P concentration was solubilized when the apatite–sulfur-sewage-sludge contained 20% apatite, this proportion increased to 86% when the mixture consisted of 1% apatite. The authors suggest that combinations such as pellet form of sulfur, apatite, and stabilized sewage sludge as a source of thiobacilli for agricultural use, would provide an effective P fertilizer source.

2.2.3. Enzymes or Enzymolysis

The ability of microorganisms to solubilize phosphate via this mechanism is briefly described in the literature [46].
Zhu et al. [61] evaluated the ability of the bacterium Kushneria sp. YCWA18 in the solubilization of P in two culture media, where the first contained calcium phosphate Ca3(PO4)2 as the only source of P and the second lecithin as the exclusive source of P. The results showed that for the medium containing Ca3(PO4)2 in 11 days of cultivation, there was the release of 283.16 μg/mL of P, and the pH varied from 7.21 to 4.24 in about 4 days. As for the medium containing lecithin, there was solubilization of 47.52 μg/mL of P in 8 days; however, the pH remained stable at approximately 7.0, a value similar to that of the control. Thus, the authors suggest that enzymolysis is the mechanism responsible for the solubilization of P from lecithin because compared to the culture medium containing Ca3(PO4)2 (where the solubilization possibly occurred through the release of organic acids), the acidity of the medium does not change. Thus, P is released through catalysis performed by enzymes that convert the substrate to choline.

2.2.4. Siderophores

Siderophores are low-molecular-weight secondary metabolites produced by PSM that have a high affinity for inorganic iron and function as metal chelators [62][63]. They have three functional groups, hydroxamates, catecholates, and carboxylates, and catalyze the reduction of Fe3+ to Fe2+ [64]. They act at neutral to alkaline pH; however, the mechanisms of this reaction are still not fully understood [65]. Microorganisms use siderophores to obtain the iron used in their cell, and so, during the breakage of its bond, they can release the P bound of the metal, making it assimilable to plants [1][64].
As discussed earlier, in acidic soils, much of the P is fixed in metals such as iron. Cui et al. [66] evaluated the ability of Streptomyces sp. CoT10 endophytic activity of Camellia oleifera on P mobilization in acidic and deficient soils. The authors saw a release of 72.49 mg/L for FePO4, which was prominent in the production of different siderophores. Moreover, the application of Streptomyces sp. aided in Fe-P mobilization improving P availability by 15% in the soil. The authors conclude that the production of siderophores leads to the observed results, including the promotion of plant growth.

2.2.5. Exopolysaccharides

Exopolysaccharides are compounds with high molecular weights that act indirectly on the solubilization of P in soil [67]. They are secreted by microorganisms under stress conditions. In bacteria, they form biofilms, which have a great affinity for binding with metallic ions in the soil, thus competing with free P, providing its availability [68][69]. It is seen that different exopolysaccharides have varying binding affinities with different metals, and there are also different binding strengths between the metals themselves [70][71].
Yi et al. [67] evaluated that Enterobacter sp. EnHy-401, Arthrobacter sp. ArHy-505, Azotobacter sp. AzHy-510 producing exopolysaccharides (EPS) have a higher tricalcium-phosphate solubilization capacity than Enterobacter sp. EnHy-402 which does not produce EPS. The authors analyzed that under the same conditions, Enterobacter sp. EnHy-402 solubilized 112 mg/L of P, the medium pH ranged from 7.0 to 4.5, had an organic acid production of 258 mg/L, and did not produce EPS. Meanwhile Enterobacter sp. EnHy-401 solubilized 623 mg/L of P, the medium pH varied from 7.0 to 4.3, had an organic acid production of 2092 mg/L, and produced 4 g/L of EPS. The authors suggest that EPS potentiates phosphate solubilization mainly by benefiting the production and activity of organic acids.

2.2.6. Proton Release

The release of protons is another mechanism that promotes rhizosphere acidification. Soil microorganisms use various sources of nitrogen to form amino acids, one of which is ammonium (NH4+) which, when metabolized, generates ammonia (NH3) [72][73]. At the end of the reaction, the excess H+ protons generated are released into the soil, allowing the desorption of P immobilized in metals [74].
Studies have shown different ways in which proton extrusion favors phosphate solubilization. Öğüt et al. [75] reported an increase in proton extrusion in maize roots after being inoculated with Bacillus sp. 189 causing acidification of nutrient solution supplemented with ammonium. The bacteria contributed to the increase in evaluable P by 8.0 mg/Kg, while in the control the concentration of evaluable P was 6.3 mg/Kg. The authors suggest that the increase in proton release was due to (1) stimulation of plasmalemma ATPase of plant roots, (2) proton release by the PSM associated with the release of organic acid anions, and (3) proton release by the PSM in response to NH4 uptake.
Habte and Osorio [76] verified the influence of various sources of nitrogen on the solubilization of phosphate rocks by Mortierella sp. The results showed that in the presence of NH4Cl and NH4N3, the pH of the solution decreased from first value of 7.6 to 3.4 and 3.7, respectively. When the N source was KNO3, the pH decreased to 6.7. As for P solubilization, it was seen that supplementation with NH4Cl was responsible for the release of 130 mg/L of P, with NH4N3 it was 110 mg/L of P, and with KNO3 only 0.08 mg/L of P. The authors also indicated that excess NH4+ negatively affected fungal growth. However, this may have promoted a greater pumping of H+ that significantly decreased the pH of the solution and consequently favored the solubilization of P.

2.2.7. H2S Production

Hydrogen sulfide is a compound produced by sulfur-oxidizing and acidophilic bacteria. It is released from metabolic pathways such as sulfate reduction and organic matter decomposition [1][77]. This compound interacts with minerals that have phosphate, releasing it into the soil solution [68]. An example is ferric phosphate, which forms ferrous sulfate with the release of immobilized phosphorus in the soil [78][79].
Phosphate solubilization mediated exclusively by the production of H2S does not have many practical examples in the literature. However, some studies have analyzed the synthesis of compounds by bacteria [80][81][82].

2.2.8. Direct Oxidation of Glucose

The direct oxidation of glucose is another strategy used by PSM to make P bioavailable. In bacteria, this mechanism begins with the oxidation of glucose in the periplasmic space by the enzyme glucose dehydrogenase, generating gluconic acid, which is eventually converted to 2-keto gluconic by the enzyme gluconate dehydrogenase [6][83]. Subsequently, the release of these acids to the outside of the cell occurs, acidifying the medium. As seen previously, these acids function as ferric ion chelators, releasing the P from its bond [84].
Phosphate solubilization by the direct oxidation pathway is a mechanism that is extremely restricted by the effectiveness of glucose dehydrogenase. Therefore, studies seek to identify the enzyme in microorganisms using molecular methods, as was the case with the work by Mei et al. [85] who identified the enzyme in the bacteria Pantoea vagans IALR611, Pseudomonas psychrotolerans IALR632, Bacillus subtilis IALR1033, Bacillus safensis IALR1035 and Pantoea agglomerans IALR1325.
In addition, studies have also highlighted the importance of gluconic acid in plant growth. Rasul et al. [86], showed that Acinetobacter sp. (MR5) and Pseudomonas sp. (MR7) producing gluconic acid were responsible for promoting rice growth, increasing grain yield (up to 55%), plant-associated P (up to 67%), and soil available P (up to 67%), with 20% reduced fertilization. The authors confirmed the activity of the enzyme based on the construction of new primers designed to amplify the gcd, pqqE, and pqqC genes responsible for glucose dehydrogenase-mediated phosphate solubilization.
Other studies have pointed out the reasons for the failure or reduction of phosphate solubilization from the inhibition of glucose dehydrogenase catalysis. The work by Bharwad and Rajkumar [87] and Iyer and Rajkumar [88] describe how succinate inhibits enzyme activity in Acinetobacter sp. and Rhizobium sp. respectively.

3. Applications of Phosphate-Solubilizing Microorganisms as Plant Growth Promoters

In addition to making P available, microorganisms can also promote plant growth in complementary ways. They have direct and indirect mechanisms of action for plant growth promotion, including biological nitrogen fixation [89] and phytohormone production [90][91].
They can stimulate tolerance to environmental stresses such as drought [92] and low soil fertility [93]. They can also induce host plant defense from the production of antibiotics and secondary metabolites [94][95], and biosurfactant compounds [96][97].
In addition, the application of isolated microorganisms or consortia can modulate the physiological response of plants and aid their growth and development. Thus, the inoculation of microorganisms plays a notable role in reducing the time required for the acclimatization of seedlings [98], improving foliar gas exchange [99], and the accumulation of fresh and dry matter, as well as increasing plant root growth [100].
Thus, the use of microorganisms and their versatility in growth promotion mechanisms constitute a notable resource to produce bioinoculants, and consequently, for sustainable agricultural production.
Furthermore, studies have strongly shown the use of PSMs as bioinoculants, either in isolated formulations or in consortia. The activity of microorganisms makes it possible to reduce the use of chemical fertilizers, both when applied together and when applied together with phosphate rocks. Microorganisms also benefit from improving soil quality, benefiting the dynamics of the rhizosphere of plants, enabling the solubilization of phosphate in acidic and alkaline soils, and degrading xenobiotic compounds.

4. Market and Agricultural Practices with Phosphate-Solubilizing Microorganisms

Production of biological inoculants is the main way to explore the potential of PSM in agriculture. Forecasts say that the biofertilizer market will register a compound annual growth rate of almost 14% until 2023. In 2016, the global market size of biofertilizers reached USD 1106.4 million and is projected to grow at the rate of 14% to reach USD 3124.5 million by the end of 2024 [101].
In general, for a microorganism to be selected as a bioinoculant, it must be multifunctional, present several mechanisms of growth promotion, and be a generalist, interacting with several cultures [102]. The work by Owen et al. [103] and Mącik et al. [104] lists several commercial bioinoculants, the microorganisms that compose them, and their modes of action.
Bioinoculants can be used in several ways. As seen throughout the text, the main method of using it is directly in the soil, favoring the release of the P part that is inaccessible to plants. Moreover, the inoculants can be applied together with phosphate rocks [105][106], in the treatment of wastewater [107], and in fermenting animal detritus [108], these being external sources of P.
The potential for some microorganisms to release P from the soil and promote plant growth is unequivocal. However, unlike what occurs with some N-fixing symbionts, such as those from the genera Rhizobium and Bradyrhizobium, the amount of P made available by PSM does not seem to be well regulated by plants. As a consequence, and allied to the fact that P is not in the air as N, PSM does not supply P in amounts corresponding to high levels of productivity of crops. For this reason, often capitalized farmers choose to apply high doses of phosphate fertilizers instead of applying or managing PSM in the soil. After all, using only PSM these farmers will not be able to reach yields comparable to the use of synthetic fertilizers, and by applying high doses of phosphate fertilizers the action of PSM tends to be minimized, as is the case with arbuscular mycorrhizal fungi. Thus, if the prices of synthetic phosphate fertilizers are not counterproductive at the current level of use, or there is a wide rupture in the productivity paradigm, with a greater appreciation of sustainability over productivity, inoculation with PSM will remain a market niche.

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Leandro Israel da Silva
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Marlon Correa Pereira
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André Mundstock Xavier de Carvalho
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Victor Hugo Buttrós
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Moacir Pasqual
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Joyce Dória
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