Betty Natalie Fitriatin1*
Oviyanti Mulyani1Diyan Herdiyantoro1Tahani Awad Alahmadi2Marika Pellegrini3- 1Department of Soil Sciences and Land Resources Management, Agriculture Faculty, Universitas Padjadjaran, Bandung, Jatinangor, Indonesia
- 2Department of Pediatrics, College of Medicine and King Khalid University Hospital, King Saud University, Riyadh, Saudi Arabia
- 3Environmental Microbiology, Environmental Sciences, Department of MeSVA, University of L'Aquila, L'Aquila, Italy
Phosphate solubilizing microbes (PSM) can improve soil P availability by P dissolution. These microbes can make substances that regulate plant growth, which promotes plant growth. The present study aimed to characterize PSM and determine how PSM application affected P solubilization, soil phosphatase activity, and upland rice yield. The greenhouse experiment used a factorial randomized block design (RBD) with two factors and three replications. The first factor was PSM isolates, which came in four different forms: without microbes, with microbes (Burkholderia sp.), with fungus (Penicillium sp.), and with a combination of microbes (Burkholderia sp. and Penicillium sp.). The PSM isolates were characterized to analyze the production of organic acids, phosphatase enzymes, and phytohormones. The second factor was the superphosphate fertilizer dose, which has four levels: 0, 50, 75, and 100 kg P ha−1. According to the PSM characterization, it produced organic acids such as lactate acid, oxalate acid, citric acid, and acetate acid, as well as phytohormones (IAA) and the enzyme phosphatase. The pot experiment results show that the PSM inoculation raised the available P and soil phosphatase, P content of the plant, decreased soil organic P, and increased upland rice production. For improving available P, phosphatase activity, P content of the plant, and upland rice yields, mixed inoculants of phosphate-solubilizing bacteria and fungi performed better. The availability of soil P, the activity of the enzyme phosphatase, and the upland rice yields were all improved by applying P fertilizer at 75 kg P ha−1. This study showed that PSM as a biofertilizer reduced the dosage of inorganic fertilizers by up to 25%.
Introduction
One of the macronutrients crucial for plant growth is phosphorus (P). However, several barriers prevent plants from accessing P in the soil, particularly in marginal soil. The primary issue with phosphorus is that it is present in high soil concentrations yet inaccessible to plants. In this instance, it heavily depends on the soil's qualities, properties, and management (Balemi and Negisho, 2012; Xu et al., 2020). In agricultural soils, high P fixation by Al and Fe hydroxides is frequently a problem (Penn and Camberato, 2019). The key factors that contributed to the lack of P in most soil are the low soil P availability, low soil P total, low fixation of soluble P, and the fact that most of the P in soil is still in organic form and not available to plants (Shen et al., 2011).
It is required to develop the usage of microbes that contribute to the transformation of P nutrients in the soil and can be utilized as biofertilizers, such as phosphate solubilizing microbes, to increase plant development and fertilization effectiveness (Kalayu, 2019). Recently, the genus Burkholderia has become necessary as phosphate solubilizing microbes (Moreno-Conn et al., 2021) and the genus Penicillium (Reyes et al., 2001; Countinho and Felix, 2012). The phosphate solubilizing microbes (PSM) can remove phosphorus (P) from bonds with aluminum, iron, calcium, and magnesium (Al, Fe, Ca, and Mg), allowing it to dissolve P that is unavailable to plants and make it available to them (Alori et al., 2017). Sharma et al. (2013) stated that PSM could solubilize and mineralize P from inorganic and organic pools of total soil P. This is because, in the soil, organic acids produced by bacteria can create stable complexes with P-binding cations (Menezes-Blackburn et al., 2016).
In addition to being able to release fixed P, the phosphate-solubilizing microbes have various benefits for promoting plant growth, including the ability to create phosphatase enzymes (Behera et al., 2017; Fitriatin et al., 2020). According to Stevenson (1986), between 15 and 80% of soil's phosphorus (P) is contained in its organic form. P availability may come from soils with a high organic P concentration (Khosa et al., 2021). Since plants cannot directly utilize the inorganic form of P, it must first be converted into a soluble (organic) P through a mineralization process helped by soil enzymes (Quiquampoix and Mousain, 2003; Tian et al., 2021).
The phosphate solubilizing microbes as plant growth-promoting rhizobacteria PGPR play an essential role in increasing plant growth and yield (Kalam et al., 2020; Basu et al., 2021; Hamid et al., 2021; Nasab et al., 2021) and can withstand the adverse effects arising from various biotic and abiotic stresses (Kour et al., 2019; Bhat et al., 2022; Gowtham et al., 2022; Shah et al., 2022; Verma et al., 2022). Kusale et al. (2021a,b) isolated Klebsiella variicola from the wheat rhizosphere, producing phytohormone, organic acid, phytase, salt ameliorating, and antioxidant metabolites. They found this bacterium as a potential bioinoculant for salinity stress management. Another potential for PGPR can inhibit plant diseases. Suriani et al. (2020) reported that the significant reduction of blast disease due to applying a mixture of piper leaves extracts and PGPR improved the growth and yield of rice.
The importance of phosphate-solubilizing microbes in increasing nutrient availability and food yield has been demonstrated in numerous studies. Common bean productivity and nutritional availability increased due to phosphate-solubilizing bacteria, promoting biological activity (Bamagoos et al., 2021). Pereira et al. (2020) applied phosphate-solubilizing bacteria as plant growth-promoting bacteria (PGPB) Azospirillum brasilense, Bacillus subtilis, and Pseudomonas fluorescens increased maize production by up to 34% and increased plant P uptake. To improve the soil P nutrient content and maximize the P fertilization, it is necessary to investigate the characteristics of PSM and their ability to increase P solubility in the soil through P organic mineralization into P inorganic and fixed P dissolving.
Materials and methods
Soil sample collection
Burkholderia sp. and Penicillium sp. were isolated from the rice rhizosphere. Ten grams of rhizospheric soil samples (10 cm depth) were collected from Jatinangor District, Sumedang Regency, West Java Province, Indonesia (6054′56, 4″S) and (107046′16, 9″E). Soil samples as a source of isolates of phosphate solubilizing microbes were stored in zip lock bags and transferred to the laboratory.
Isolation of P solubilizing microbes
Isolation of PSM was carried out by a serial dilution plate method using Pikovskaya media (10 g glucose, 5 g Ca3(PO4)2, 0.2 NaCl, 0.5 g (NH4)SO4, 0.1 g MgSO4·7H2O, 0.5 g yeast extract, 0.2 g KCl, 0.002 g FeSO4·7H2O, 0.002 g MnSO4·H2O, 15 g agar, in 1 L distilled water, pH 7) (Nautiyal, 1999). One gram soil sample was dissolved into 9 ml of sterilized distilled water in test tubes and mixed. The serial soil dilutions were made for 10−4, 10−5, 10−6, and 10−7. Furthermore, 0.5 ml of each dilution was drawn using a micropipette and placed on to plate with Pikovskaya media, and spread using a sterile L-shaped spreader. The plates were then inoculated for 2–5 days at room temperature. The clear zone indicated the ability of the isolate to dissolve phosphate in Pikovskaya media, which contains insoluble phosphate (Tricalcium phosphate). The characteristic morphology of Burkholderia sp. were small in diameter (about 1 mm) and white or pale yellow with well-defined margins. Burkholderia sp. are rod-shaped, motile, free-living, and Gram-negative bacteria. While Penicillium sp. are filamentous fungi that have branched conidiospores.
Estimation of organic acid production and phosphatase activity
Organic acid was measured using HPLC (Photodiode Array Detector, Singapore Product Waters 2998) (Sarker and Al-Rashid, 2013). The mobile phase used was 5.0 mM L−1 H2SO4 in ultrapure water (HPLC grade) at a flow rate of 0.6 ml per minute. 10 μl sample was injected with a run time of 40 min for each sample. Standard solutions were injected to obtain the retention time for each compound.
Phosphatase enzyme activity was determined according to Eivazi and Tabatabai method (Margesin, 1996). The substrate was added with p-nitrophenyl to form the p-nitrophenol compound through enzyme activity. Consecutively, it was stained by sodium hydroxide solution, which can be detected by a 400 nm spectrophotometer (Shimadzu Corp, Tokyo, Japan), indicating phosphate enzyme activity.
Screening and estimation of IAA
The synthesis of phytohormones (IAA) was determined by the colorimetric method of Gordon and Weber (Sarker and Al-Rashid, 2013) using Salkowski's reagent. Salkowski reagent is a mixture of 35% perchloric acid (HClO4) and 0.5 M ferric chloride (FeCl3), which pink color developed by positive reaction indicates IAA production. This method is mainly used for detecting IAA from microbes.
Greenhouse studies
The pot experiment was conducted at an elevation of ~782 meters above sea level in the greenhouse of the Agriculture Faculty at Universitas Padjadjaran in West Java, Indonesia. Ultisol from Jatinangor was employed and taken at a depth of 0 to 20 cm. The soil pH was 5.11, soil P availability was moderate (16.9 mg kg−1), its C-org level was moderate (2.86%), and its CEC level was high (38.5 cmol kg−1). C-org. Using the Walkley and Black method, the Bray method was used to determine P availability, and CEC was determined using the 1N ammonium acetate at pH 7 (van Reeuwijk, 2012).
A factorial randomized block design (RBD) with two factors and three replications was used for the experimental setup. The first factor was PSM isolates, which were divided into four levels: those without microbes, those with Burkholderia sp., those with Penicillium sp., and those with a combination of Burkholderia sp. and Penicillium sp. The second factor was the superphosphate fertilizer dose, which has four levels: 0, 50, 75, and 100 kg P ha−1. This dose was used to determine the efficient dose range caused by the application of PSM.
A mixture of soil (10 kg per pot with the size of 40 cm x 50 cm) and cow dung (50 g) was incubated for 2 weeks. When two plants were planted per pot, and P fertilizer was applied. In accordance with the specified dosage, P fertilizer was provided, and PSM isolate was conducted with a density of 106 CFU ml−1 and was inoculated to 10 ml pot−1.
According to the Eivazi and Tabatabai approach, soil phosphatase, P availability, soil organic P utilizing extraction method, and P content of plant were the observed responses (Kjeldahl method). Total P in the plant can be extracted by wet ashing method using a mixture of concentrated acids HNO3 and HClO4. The level of the P element in the extract was measured using a spectrophotometer (Soil Research Institute, 2005).
Statistical analysis
Data was collected for an analysis of variance (ANOVA), F-Test was done to show the significant effects of tested treatments on observed variables. Duncan Multiple Range Test (DMRT) at P < 0.05 was used to compare treatment means.
Results and discussion
Biochemical characteristics of PSM
The synthesis of organic acids, phosphatase activity, and concentration of P-dissolved in Pikovskaya media indicated the phosphate solubilizing capacity of the isolates (Supplementary Table 1). Analysis of the organic acids production revealed that both isolates, Burkholderia sp. and Penicillium sp. produced organic acids, including lactate acid, oxalate acid, citric acid, and acetate acid. Lactic acid was produced in more amounts compared to other organic acids. In comparison, glutamic acid was produced in the least amount. The capacity of these bacteria to dissolve phosphate will differ depending on their ability to produce organic acids (Sharma et al., 2016; Serna-Posso et al., 2017). Osmolovskaya et al. (2018) claimed that each organic acid has a different capacity to chelate metal ions. Two factors, including the stability constant of complex organic acids with metal ions and the structure of the hydroxyl and carboxyl molecules in the primary carbon chain, affect this variance. Yang et al. (2022) reported that the capacity of phosphate-solubilizing fungi to produce organic acids and a decrease in the pH of the medium is closely related to the ability of phosphate solubilizing to produce organic acids.
Burkholderia sp. produced more organic acids than Penicillium sp. As a result, it had a better capacity to dissolve P than Penicillium sp. It also showed higher phosphatase enzymes and more production of IAA. Bacteria generally exhibit higher Psolubilization than fungi. The synergism action of Burkholderia sp. and Penicillium sp. can increase the production of organic acids and, thus, more P solubilization. Previous studies have shown that the production of organic acids by the co-culture (bacteria and fungi) was more significant than the sum of organic acid production by the individual cultures (Rodrigues and Nahas, 2012).
Phosphatase activity and soil P
Analysis of soil phosphatase showed a rise carried on by PSM inoculation. Compared to the other treatments, mixed inoculations of Burkholderia sp. and Penicillium sp. usually had a stronger tendency to increase soil phosphatase. This investigation demonstrated that giving a mixed bacteria and fungi inoculant significantly impacted soil phosphatase more than the microbe alone.
Based on the phosphatase data from Supplementary Table 2, it could be seen that Burkholderia sp. isolate increased phosphatase activity by 142.7% compared to the control. Additionally, the phosphatase activity was increased by 147.9% when Burkholderia sp. isolate and Penicillium sp. were combined, which was significantly more significant than the control. The synergy between Burkholderia species and Penicillium species, which produced more phosphatase enzymes, was thought to be the origin of this phenomenon.
Under low pH or high acidity conditions, acid phosphatase activity will work more actively (Tagad and Sabharwa, 2018). Phosphatase activity will increase along with an increase in organic P. This is due to the PSM activity, which hydrolyzes the organic P in the soil. High phosphatase activity most likely occurred due to PSM hydrolyzing P organic from organic P in the soil. Phosphatase activity will also work with the amount of P organic (Ma et al., 2021).
Burkholderia sp. and Penicillium sp. were inoculated combined, increasing the amount of accessible P in the soil by 8.5% (Supplementary Table 2). PSM can produce organic acids that combine to form complex chemicals, which causes this behavior. This complex compound production will reduce P fixation, increasing the amount of accessible P (Rashid et al., 2016).
The results of this experiment revealed that applying 75 kg P2O5 ha−1 enhanced P availability in soil by 26.7% during the vegetative phase and by 20.7% when using 100 kg P2O5 ha−1. Additionally, when the amount of P fertilizer in the soil solution rises, P is absorbed into free elements like Al and Fe (Penn and Camberato, 2019). P availability increased more by applying 75 kg P2O5 ha−1 than by using 100 kg P2O5 ha−1. Fe minerals fixation is thought to be the reason for the low P transfer to soil. As a result, residual fertilization cannot be optimally absorbed by plants if fertilization dosage is increased.
According to the experiment, mixed inoculation of Burkholderia sp. and Penicillium sp. could improve P availability in the soil more than inoculation of Burkholderia sp. This ensures that fungi, rather than bacteria, may survive in soil with low pH levels as Ultisol.
Following inoculation with a phosphate-solubilizing bacteria, the organic soil P concentration was dropped (Supplementary Table 2). The fact that phosphatase-producing bacteria are present and have caused a decrease in the amount of organic soil P showed that organic P was being mineralized. According to de Oliveira Rita et al. (2013), the reduction in the organic soil P content indicates that P organic is mineralized.
The experiment's outcome demonstrated that a mixture of Burkholderia sp. and Penicillium sp. solubilized the least amount of organic soil P alone. But mixing these phosphate-solubilizing bacteria and fungi results in a faster mineralization rate than using a single isolate of either bacteria or fungi. Based on the results of this experiment, it can be inferred that a combination of Burkholderia sp. and Penicillium sp. increased the mineralization of P in organic soil. The finding supported it that treatment of combined inoculation of Burkholderia sp. and Penicillium sp. caused the maximum activity of soil phosphatase. According to the experiment results, the combined inoculation of Burkholderia sp. and Penicillium sp. decreased the soil organic P content and increased the soil P availability.
The P content of plant and yield of upland rice
The application of Burkholderia sp., Penicillium sp., and combined inoculant (Burkholderia sp. and Penicillium sp.) each considerably raised the P content of the plant, according to the observation at the end of the vegetative period (Supplementary Table 3). This is probably due to the usage of PSM, which can reduce the dose of phosphorus fertilizers. The inoculant of Burkholderia sp. and Penicillium sp. was applied, increasing the P content of the plant by 27.3%. The P content of the plant increased after an increase in P level. This is due to the fact that fungi can survive in highly harsh soil conditions and that they also maximize plant P uptake. Burkholderia sp. inoculant application, however, raised the P content in the plant by 18.2% at the end of the vegetative period.
Supplementary Table 3 shows that applying P fertilizer at doses of 75 and 100 kg P2O5 ha−1 significantly increased the P content of plants. This effect happens because plants respond to fertilization at the end of the vegetative period. The P fertilization at a dosage of 75% of the recommended dosage increased the concentration of plant P by 12.5%, while fertilization at 100% increased P fertilization by 16.7%. The presence of organic acids created by the upland rice root system is thought to be the reason for the P plant's high content, which is at 100% of the recommended dosage.
The results showed that PSM isolate and P fertilizer did not interact to alter upland rice output (milled dry grain). The combined inoculant of Burkholderia sp. and Penicillium sp. increased milled dry grain by 41.1%, even if the result did not show any interaction (Supplementary Table 3). It varies directly to how much PSM mixed inoculant is applied to the soil P availability parameter. Burkholderia sp. and Penicillium sp. inoculant each boost upland rice output by 33% and 21%, respectively (Supplementary Table 3). Even though Burkholderia sp. and Penicillium sp. separately improved yield, it was still lower than applying a combination inoculant of both types.
IAA produced by PSM can cause increased rice yields. Supplementary Table 1 shows that Burkholderia sp. produced higher IAA than Penicillium sp. In line with that, upland rice yield was higher in treatment Burkholderia sp. compared to rice yields in treatment Penicillium sp. Penicillium sp. and Burkholderia sp. will interact to fulfill each other requirements for food, especially P. Because Penicillium sp. and Burkholderia sp. work synergistically, phosphatase enzyme is released throughout the mineralization and immobilization processes, converting P organic to P inorganic. Therefore, until the end of the generative phase, the growth of any of them is ideal for plant growth.
Additionally, the ability of Burkholderia and Penicillium species to emit organic acids acts as a factor that can raise the P element produced as a result of Fe fixation. The synergy helps provide P for upland rice until harvest time, particularly in filling its grains, which eventually results in a rise in the yield of milled dry grains. According to Hutagaol et al. (2021), the application of phosphate-solubilizing fungi (PSF) improved the growth and production of rice compared to the control (no application of PSF). With its high phosphate-solubilizing capacity, Penicillium guanacastense could be used as a biofertilizer in forestry and agriculture (Qiao et al., 2019). The application of Burkholderia sp. in a particular soil type may help in plant nutrient uptake by solubilizing added and support their survival in extreme conditions by other qualities that promote plant growth (Baghel et al., 2020). Vafa et al. (2021) reported applying a combination of phosphate-solubilizing bacteria and N-fixing bacteria (Azotobacter sp. and Azospirillum sp.) mycorrhizal fungus, and seaweed extract improves growth parameters and grain yield in wheat.
Upland rice production was raised by 17.9% after P fertilizer application with a dose of 75 kg P2O5 ha−1. Upland rice yield was not increased by increasing the P dose over 75 kg P2O5 ha−1 but decreased by 11% with a 100 kg P2O5 ha−1. The response of the plants to fertilizer decreases with increasing soil nutrient levels (Li et al., 2019). P fertilizer in excessive quantities will impact soil micronutrient deficiencies (Zn, Fe, Bo, and Mn), making minerals unstable and competing with root activity to absorb nutrients.
Although there was no interaction between PSM and P fertilizer in terms of upland rice yield, excessive P content inhibits the role of PSM in phosphorus transformation. According to Liu et al. (2021), bacterial activity in P transformation increases in conditions of P deprivation. Behera et al. (2017) reached a similar conclusion. Their study revealed that a high P concentration in the medium decreased bacterial activity.
Conclusions
According to this study, phosphate-solubilizing microbes increased soil phosphatase activity, phosphorus availability, phosphorus concentration, and upland rice yield. This PSM inoculation can enhance P organic mineralization by lowering the soil P organic content. The effects of raising P available content, soil phosphatase activity, organic P mineralization, P content of the plant, and upland rice production are better when Burkholderia sp. and Penicillium sp. mixed inoculant are used. Applying phosphate fertilizer at 75% of the recommended rate positively affects soil phosphatase activity, phosphate availability, soil P organic soil, and upland rice production. Additionally, PSM can be developed as a biofertilizer to increase phosphorus fertilization efficiency.
Data availability statement
The original contributions presented in the study are included in the article/Supplementary material, further inquiries can be directed to the corresponding author.
Author contributions
BNF conducted experimental verification and wrote the original draft of the manuscript. OM contributed to the research idea, designing the study, and editing the manuscript. DH provision of laboratory facilities for the study, analyzed the data, and editing of the manuscript. TAA and MP writing-review and editing, formal analysis, and revision. TAA fund acquisition.
Funding
This project was supported by Universitas Padjadjaran grant RDPD (1959/UN6.3.1/PT.00/2021) and Researchers Supporting Project (RSP-2021/230), King Saud University, Riyadh, Saudi Arabia.
Acknowledgments
We thank the staff Laboratory of Soil Biology and Laboratory of Soil Fertility and Plant Nutrition Faculty of Agriculture, Universitas Padjadjaran, Jatinangor, Indonesia for their cooperation.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fsufs.2022.1032708/full#supplementary-material
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Keywords: available P, organic acid, phosphatase, organic P, P fertilizer
Citation: Fitriatin BN, Mulyani O, Herdiyantoro D, Alahmadi TA and Pellegrini M (2022) Metabolic characterization of phosphate solubilizing microorganisms and their role in improving soil phosphate solubility, yield of upland rice (Oryza sativa L.), and phosphorus fertilizers efficiency. Front. Sustain. Food Syst. 6:1032708. doi: 10.3389/fsufs.2022.1032708
Received: 31 August 2022; Accepted: 24 October 2022;
Published: 10 November 2022.
Edited by:
Javid A. Parray, Department of Environmental Science GDC Eidgah Srinagar, IndiaReviewed by:
Alka Sagar, Sam Higginbottom University of Agriculture, Technology and Sciences, IndiaSadia Zafar, University of Education Lahore, Pakistan
Hanuman Singh Jatav, Sri Karan Narendra Agriculture University, India
Copyright © 2022 Fitriatin, Mulyani, Herdiyantoro, Alahmadi and Pellegrini. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Betty Natalie Fitriatin, betty.natalie@unpad.ac.id