Chengdong Wang
Guojun Pan
Xin Lu
Weicong Qi- 1Key Laboratory of Tobacco Biology and Processing, Ministry of Agriculture, Tobacco Research Institute of Chinese Academy of Agricultural Sciences, Qingdao, China
- 2Institute of Agricultural Resources and Environment, Jiangsu Academy of Agricultural Sciences, Nanjing, China
- 3School of the Environment and Safety Engineering, Jiangsu University, Zhenjiang, China
- 4Excellence and Innovation Center, Jiangsu Academy of Agricultural Sciences, Nanjing, China
- 5Key Laboratory of Saline-Alkali Soil Improvement and Utilization (Coastal Saline-Alkali Lands), Ministry of Agriculture and Rural Affairs, Nanjing, China
Phosphate solubilizing microorganisms (PSMs) are known as bacteria or fungi that make insoluble phosphorus in soil available to plants. To date, as beneficial microbes, studies on PSMs indicated they have potential applications in agriculture, environmental engineering, bioremediation, and biotechnology. Currently high cost and competition from local microbe are the most important factors hindering PSMs commercialization and application as for instance biofertilizer, soil conditioner or remediation agent, etc. There are several technical strategies can be engaged to approach the solutions of these issues, for instance mass production, advance soil preparation, genetic engineering, etc. On the other hand, further studies are needed to improve the efficiency and effectiveness of PSMs in solubilizing phosphates, promoting plant growth, soil remediation preferably. Hopefully, PSMs are going to be developed into ecofriendly tools for sustainable agriculture, environment protection and management in the future.
1 Introduction
Phosphate solubilizing microorganisms (PSMs) are bacteria or fungi that are capable of breaking down insoluble forms of phosphorus, such as phosphates, in the soil and making it available to plants as a soluble form that can be easily absorbed (Figure 1) (Rawat et al., 2020). They are huge category of beneficial microbe including many genera for in stance Bacillus spp., Pseudomonas spp., Streptomyces spp., Aspergillus spp., Rhizobium spp. Fusarium spp., Trichoderma spp., Penicillium spp., Serratia spp., Micrococcus spp., Stenotrophomonas spp., Acinetobacter spp., and Agrobacterium spp. (Rodrı́guez and Fraga, 1999). This process increases the overall availability of phosphorus to plants, leading to improved plant growth and crop yields. PSMs are commonly found in soil and rhizosphere, and play an important role in nutrient cycling and soil fertility (Beheshti et al., 2022). PSMs have had several applications in biotechnology. For instance, in the pharmaceutical and food industries, PSMs are used to produce antibiotics, vitamins, and other bioactive compounds (Sekurova et al., 2019); furthermore, PSMs have the potential to play a role in the development of new and efficient bioprocesses for the sustainable production of biofuels and other bio-based products (Osanai et al., 2015). The most well-known uses of PMSs are in agricultural and environmental engineering. For their outstanding nature described above, PMS are used for improving soil fertility in agriculture, enhancing plant growth and tolerance against stress of instance salinity (Luo et al., 2022), nutrient deficiency (He et al., 2022; 2021; Chen et al., 2022a) etc.,; and hence increasing crop yields (Chen et al., 2022b); they can also be used for bioremediation along or combining with plants, to remove for instance heavy metals from contaminated soil and water (Pinilla et al., 2008; Chen et al., 2019a).
FIGURE 1. The mechanisms of phosphorus solubilizing microorganisms assisting plants nutrition absorption and soil remediation.
2 Potential uses of PSMs in agriculture and environmental engineering
There is great potential and expectation for the future of PSMs in agriculture and environmental engineering. As the world’s population continues to grow, the demand for food and other resources will increase, putting pressure on the world’s finite resources, including phosphates. PSMs have the potential to help address this challenge by improving soil fertility and reducing the need for chemical fertilizers (Sarmah and Sarma, 2022; Tian et al., 2022).
PSMs are an emerging biotechnology tools in agriculture and environmental engineering, but the application is still in its early stages of development and not yet for commercialization. While there have been several studies demonstrating the potential of PSMs for enhancing plant growth, improving soil fertility, and detoxifying contaminated environments, much of the research is still in the laboratory or experimental stage (Chen et al., 2020; 2019b; Lai et al., 2022a).
2.1 For agriculture
PSMs can regulate plant metabolism by providing an increased availability of soluble phosphorus. This increased availability of phosphorus can lead to changes in plant growth and metabolism (Rodrı́guez and Fraga, 1999), such as an increased rate of photosynthesis, improved root development, and an enhanced ability to defend against stressors such as drought or disease (Billah et al., 2019; Kour et al., 2020). PSMs can enhance plant endogenous gene expression and help plants cope with abiotic stress by providing an increased availability of soluble phosphorus. This increased availability of phosphorus can activate signaling pathways and trigger the expression of stress-responsive genes in plants, which can enhance their ability to tolerate and resist environmental stressors such as drought, salinity, heavy metal toxicity, and temperature extremes. For example, research has shown that PSMs can increase the expression of genes involved in the regulation of water uptake, antioxidant defense, and heat shock response, which can help plants better cope with abiotic stress (Paul et al., 2017). In addition, PSMs can also stimulate the production of phytohormones such as auxins, cytokinin, gibberellins et al., which can enhance plant growth and stress tolerance (Figure 1).
2.2 For environmental engineering
PSMs can play a role in remediation of heavy metal pollution in soil by indirectly reducing the bioavailability of heavy metals in the soil, as showed in Figure 1. When PSMs solubilize phosphates, they create a competition for metal ions, which can reduce the uptake of heavy metals by plants and lower their concentration in the soil alone or combining with other species or materials (Lai et al., 2022b; Feng et al., 2022; Chen et al., 2023). In addition, some PSMs have been shown to produce organic acids, such as citric acid, that can chelate heavy metals and make them less available for uptake by plants (Direct assistance, Figure 1).
Another way PSMs can help remediate heavy metal pollution in soil is by promoting the growth of plants that can tolerate high levels of heavy metals. This is known as phytoremediation, and it involves using plants to remove heavy metals from the soil by absorbing and accumulating them in their tissues (Indirect facilitation, Figure 1). PSMs can help improve the growth and health of these phytoremediation plants by providing them with an available source of phosphates, which are essential for plant growth and development.
As all the function and potential use of PMS, it worth to note that here is still a need for further research to fully understand the mechanisms by which PSMs interact with plants and the environment; and to develop cost-effective and scalable methods for their application in agriculture and environmental engineering. Additionally, there are challenges associated with the large-scale production, formulation, and storage of PSMs, which must be overcome in order to make their application more practical and widespread.
The potential uses of PSMs in agriculture and environmental engineering were summarized in Table 1.
TABLE 1. Potential uses and benefits of applying PSMs in agriculture and environment engineering.
3 The restraining factor in PSMs application and commercialization in agricultural and environmental engineering, and the promising solutions
There are several key challenges associated with the application of PSMs in crop fertilization and environmental engineering: 1) there is currently a lack of standardization in the production and application of PSMs as biofertilizers or soil remediation promoter, which can affect their efficacy and consistency; 2) PSMs are sensitive to soil conditions such as pH, salinity, and heavy metal toxicity, and may not be able to survive or function effectively in all soils; PSMs are often introduced into soil as suspensions or inoculants, but they may not persist in the soil for long periods of time, limiting their effectiveness over the long term; 3) PSMs may face competition from other microorganisms in the soil for nutrients and space, which can limit their ability to establish and grow in soil; 4) the production and application of PSMs as biofertilizers can be expensive, and the cost of this technology may be a barrier for widespread implementation in agriculture. These challenges highlight the need for further research to optimize the production and application of PSMs as biofertilizers, and to develop new and more cost-effective methods for enhancing soil fertility and crop productivity. Currently, high cost and competition from local microbe are the most important factors hindering PSMs commercialization and application.
There are several ways to reduce the cost of Phosphate Solubilizing Microorganisms (PSMs). Some of these were listed and interpreted below.
1) Mass production of PSMs: Mass production of PSMs using low-cost and efficient methods, such as fermentation, can help to reduce the cost of producing these microorganisms on a large scale.
2) Optimizing application methods: Developing more efficient and cost-effective methods for applying PSMs to soil, such as using granules (Jokkaew et al., 2022), liquid formulations (Goljanian-Tabrizi et al., 2016), or seed treatments, can help to reduce the cost of PSMs application.
3) Selecting low-cost PSMs (Lobo et al., 2019): Selecting PSMs that are naturally occurring and widely distributed, or that can be easily isolated and mass-produced, can help to reduce the cost of PSMs application.
4) Using natural sources of phosphates: Encouraging the use of natural sources of phosphates, such as rock minerals and guano, can help to reduce the need for costly commercial fertilizers.
5) Promoting the use of integrated nutrient management: Encouraging the use of integrated nutrient management practices, such as the use of cover crops, composting, and intercropping, can help to reduce the dependence on commercial fertilizers and increase the efficiency of PSMs application.
To avoid competition with local soil microorganisms for instance plant pathogens, decomposer, predatory microorganisms et al, the following factors should be optimized in the application of PSMs.
1) Soil preparation: To enhance the survival and persistence of PSMs, the soil should be prepared prior to their introduction. This may involve amending the soil with organic matter, adjusting the pH, or reducing soil salinity levels.
2) Inoculum preparation: The PSM inoculum should be prepared in a way that optimizes their survival and growth. This may involve selecting PSMs with high tolerance to environmental stress, such as heavy metal toxicity or salinity, or formulating the inoculum to enhance their survival and persistence in the soil (Johri et al., 1999).
3) Timing of application: PSMs should be applied at a time that minimizes competition with other soil microorganisms. For example, application during periods of low microbial activity, such as early in the growing season, may reduce competition and enhance the survival and growth of PSMs.
4) Selection of PSMs: PSMs should be selected for their ability to compete with local soil microorganisms. This may involve selecting PSMs with high competitiveness and/or selecting PSMs that are able to produce antibiotics or other metabolites that inhibit the growth of other soil microorganisms.
5) Microbial community management: The soil microbial community should be managed in a way that enhances the competitiveness of PSMs. This may involve applying compost, mulch, or other organic matter to the soil, or using other microorganisms or biostimulants to enhance the growth and competitiveness of PSMs. These factors should be optimized to ensure that PSMs are able to establish and persist in the soil, and to minimize competition with local soil microorganisms.
4 The current Frontier research areas in the field of PSMs
Microbial ecology: Researchers are working to understand the interactions between PSMs and other soil microorganisms, and the role that PSMs play in soil health and fertility. This research includes the study of microbial competition and cooperation, as well as the development of methods for enhancing the survival and persistence of PSMs in the soil (Nacoon et al., 2020).
Metagenomics: Metagenomic were used to approaches the diversity and function of PSMs in soil, and to identify new PSMs with enhanced abilities for solubilizing phosphates and improving soil fertility.
Biostimulants: Researches were carried out to Investigate the use of PSMs and other microorganisms as biostimulants to enhance plant growth and productivity, as well as the ability of plants to cope with environmental stress (Yahya et al., 2022).
Synthetic biology: Researchers are developing new approaches for engineering PSMs to enhance their abilities for solubilizing phosphates and improving soil fertility. This includes the use of synthetic biology to produce new strains of PSMs with improved abilities, as well as the use of CRISPR-Cas9 technology to engineer existing PSMs (Liu et al., 2020).
Soil remediation: Researchers are investigating the use of PSMs for soil remediation, with a focus on removing heavy metals and other contaminants from contaminated soils (Song et al., 2022). This research includes the development of new methods for applying PSMs to contaminated soils, as well as the study of the mechanisms by which PSMs remove contaminants from soil.
5 Prospect
In the future, it is expected that research into PSMs will continue to advance, with a focus on improving the efficiency and effectiveness of PSMs in solubilizing phosphates and promoting plant growth. This may involve the development of new strains of PSMs through synthetic biology and other techniques, as well as the optimization of existing PSMs for different environmental conditions and applications. In addition, it is expected that the use of PSMs will become increasingly widespread in agriculture and environmental engineering, as farmers and environmental engineers seek more sustainable and environmentally friendly solutions to the challenges posed by declining soil fertility and limited resources.
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 authors.
Author contributions
WQ and XL- Conceptualization; WQ and CW– Writing—original draft; CW, WQ, GP, and XL– Writing–review and editing; CW and XL– Funding acquisition.
Funding
We acknowledge financial support by Agricultural Science and Technology Innovation Program (ASTIP-TRIC03); The National Natural Science Foundation of China (No.32273137); The science and technology projects of Hunan Tobacco Industry Corporation (2020510000340394).
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.
References
Beheshti, M., Alikhani, H. A., Pourbabaee, A. A., Etesami, H., Asadi Rahmani, H., and Noroozi, M. (2022). Enriching periphyton with phosphate-solubilizing microorganisms improves the growth and concentration of phosphorus and micronutrients of rice plant in calcareous paddy soil. Rhizosphere 24, 100590. doi:10.1016/j.rhisph.2022.100590
Billah, M., Khan, M., Bano, A., Hassan, T. U., Munir, A., and Gurmani, A. R. (2019). Phosphorus and phosphate solubilizing bacteria: Keys for sustainable agriculture. Geomicrobiol. J. 36, 904–916. doi:10.1080/01490451.2019.1654043
Chen, H., Min, F., Hu, X., Ma, D., and Huo, Z. (2023). Biochar assists phosphate solubilizing bacteria to resist combined Pb and Cd stress by promoting acid secretion and extracellular electron transfer. J. Hazard Mater 452, 131176. doi:10.1016/j.jhazmat.2023.131176
Chen, H., Tang, L., Wang, Z., Su, M., Tian, D., Zhang, L., et al. (2020). Evaluating the protection of bacteria from extreme Cd (II) stress by P-enriched biochar. Environ. Pollut. 263, 114483. doi:10.1016/j.envpol.2020.114483
Chen, H., Zhang, J., Tang, L., Su, M., Tian, D., Zhang, L., et al. (2019a). Enhanced Pb immobilization via the combination of biochar and phosphate solubilizing bacteria. Environ. Int. 127, 395–401. doi:10.1016/j.envint.2019.03.068
Chen, H., Zhang, J., Tang, L., Su, M., Tian, D., Zhang, L., et al. (2019b). Enhanced Pb immobilization via the combination of biochar and phosphate solubilizing bacteria. Environ. Int. 127, 395–401. doi:10.1016/j.envint.2019.03.068
Chen, X., Meng, L., He, B., Qi, W., Jia, L., Xu, N., et al. (2022a). Comprehensive transcriptome analysis uncovers hub long non-coding RNAs regulating potassium use efficiency in nicotiana tabacum. Front. Plant Sci. 13, 777308. doi:10.3389/fpls.2022.777308
Chen, X., Wang, C., He, B., Wan, Z., Zhao, Y., Hu, F., et al. (2022b). Transcriptome profiling of transposon-derived long non-coding RNAs response to hormone in strawberry fruit development. Front. Plant Sci. 13, 915569. doi:10.3389/fpls.2022.915569
Feng, Y., Zhang, L., Li, X., Wang, L., Yusef, K. K., Gao, H., et al. (2022). Remediation of lead contamination by Aspergillus Niger and phosphate rocks under different nitrogen sources. Agronomy 12, 1639. doi:10.3390/agronomy12071639
Goljanian-Tabrizi, S., Amiri, S., Nikaein, D., and Motesharrei, Z. (2016). The comparison of five low cost liquid formulations to preserve two phosphate solubilizing bacteria from the genera Pseudomonas and Pantoea. Iran. J. Microbiol. 8, 377–382.
He, B., Hu, F., Du, H., Cheng, J., Pang, B., Chen, X., et al. (2022). Omics-driven crop potassium use efficiency breeding. Front. Plant Sci. 13, 1076193. doi:10.3389/fpls.2022.1076193
He, B., Meng, L., Tang, L., Qi, W., Hu, F., Lv, Y., et al. (2021). The landscape of alternative splicing regulating potassium use efficiency in nicotiana tabacum. Front. Plant Sci. 12, 774829. doi:10.3389/fpls.2021.774829
Johri, J. K., Surange, S., and Nautiyal, C. S. (1999). Occurrence of salt, pH, and temperature-tolerant, phosphate-solubilizing bacteria in alkaline soils. Curr. Microbiol. 39, 89–93. doi:10.1007/s002849900424
Jokkaew, S., Jantharadej, K., Pokhum, C., Chawengkijwanich, C., and Suwannasilp, B. B. (2022). Free and encapsulated phosphate-solubilizing bacteria for the enhanced dissolution of swine wastewater-derived struvite—an attractive approach for green phosphorus fertilizer. Sustainability 14, 12627. doi:10.3390/su141912627
Kour, D., Rana, K. L., Sheikh, I., Kumar, V., Yadav, A. N., Dhaliwal, H. S., et al. (2020). Alleviation of drought stress and plant growth promotion by Pseudomonas libanensis EU-LWNA-33, a drought-adaptive phosphorus-solubilizing bacterium. Proc. Natl. Acad. Sci. India Sect. B Biol. Sci. 90, 785–795. doi:10.1007/s40011-019-01151-4
Lai, W., Wu, Y., Zhang, C., Dilinuer, Y., Pasang, L., Lu, Y., et al. (2022a). Combination of biochar and phosphorus solubilizing bacteria to improve the stable form of toxic metal minerals and microbial abundance in lead/cadmium-contaminated soil. Agronomy 12, 1003. doi:10.3390/agronomy12051003
Lai, W., Wu, Y., Zhang, C., Dilinuer, Y., Pasang, L., Lu, Y., et al. (2022b). Combination of biochar and phosphorus solubilizing bacteria to improve the stable form of toxic metal minerals and microbial abundance in lead/cadmium-contaminated soil. Agronomy 12, 1003. doi:10.3390/agronomy12051003
Liu, Y.-Q., Wang, Y.-H., Kong, W.-L., Liu, W.-H., Xie, X.-L., and Wu, X.-Q. (2020). Identification, cloning and expression patterns of the genes related to phosphate solubilization in Burkholderia multivorans WS-FJ9 under different soluble phosphate levels. Amb. Express 10, 108. doi:10.1186/s13568-020-01032-4
Lobo, C. B., Juárez Tomás, M. S., Viruel, E., Ferrero, M. A., and Lucca, M. E. (2019). Development of low-cost formulations of plant growth-promoting bacteria to be used as inoculants in beneficial agricultural technologies. Microbiol. Res. 219, 12–25. doi:10.1016/j.micres.2018.10.012
Luo, C., He, B., Shi, P., Xi, J., Gui, H., Pang, B., et al. (2022). Transcriptome dynamics uncovers long non-coding RNAs response to salinity stress in Chenopodium quinoa. Front. Plant Sci. 13, 988845. doi:10.3389/fpls.2022.988845
Nacoon, S., Jogloy, S., Riddech, N., Mongkolthanaruk, W., Kuyper, T. W., and Boonlue, S. (2020). Interaction between phosphate solubilizing bacteria and arbuscular mycorrhizal fungi on growth promotion and tuber inulin content of helianthus tuberosus L. Sci. Rep. 10, 4916. doi:10.1038/s41598-020-61846-x
Osanai, T., Shirai, T., Iijima, H., Nakaya, Y., Okamoto, M., Kondo, A., et al. (2015). Genetic manipulation of a metabolic enzyme and a transcriptional regulator increasing succinate excretion from unicellular cyanobacterium. Front. Microbiol. 6, 1064. doi:10.3389/fmicb.2015.01064
Paul, S., Dukare, A. S., BandeppaManjunatha, B. S., and Annapurna, K. (2017). Plant growth-promoting rhizobacteria for abiotic stress alleviation in crops, 57–79. doi:10.1007/978-981-10-7380-9_4
Pinilla, P., Ruiz, J., Lobo, M. C., and Martínez-Iñigo, M. J. (2008). Degradation of oxadiazon in a bioreactor integrated in the water closed circuit of a plant nursery. Bioresour. Technol. 99, 2177–2181. doi:10.1016/j.biortech.2007.05.039
Rawat, P., Shankhdhar, D., and Shankhdhar, S. C. (2020). Plant growth-promoting rhizobacteria: A booster for ameliorating soil health and agriculture production, 47–68. doi:10.1007/978-3-030-44364-1_3
Rodrı́guez, H., and Fraga, R. (1999). Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17, 319–339. doi:10.1016/S0734-9750(99)00014-2
Sarmah, R., and Sarma, A. K. (2022). Phosphate solubilizing microorganisms: A review. Commun. Soil Sci. Plant Anal. 54, 1306–1315. doi:10.1080/00103624.2022.2142238
Sekurova, O. N., Schneider, O., and Zotchev, S. B. (2019). Novel bioactive natural products from bacteria via bioprospecting, genome mining and metabolic engineering. Microb. Biotechnol. 12, 828–844. doi:10.1111/1751-7915.13398
Song, P., Xu, D., Yue, J., Ma, Y., Dong, S., and Feng, J. (2022). Recent advances in soil remediation technology for heavy metal contaminated sites: A critical review. Sci. Total Environ. 838, 156417. doi:10.1016/j.scitotenv.2022.156417
Tian, D., Xia, J., Zhou, N., Xu, M., Li, X., Zhang, L., et al. (2022). The utilization of phosphogypsum as a sustainable phosphate-based fertilizer by Aspergillus Niger. Agronomy 12, 646. doi:10.3390/agronomy12030646
Keywords: phosphorus solubilizing microorganisms, biofertilizer, environment remediation, commercialization, cost-efectiveness, frontier research
Citation: Wang C, Pan G, Lu X and Qi W (2023) Phosphorus solubilizing microorganisms: potential promoters of agricultural and environmental engineering. Front. Bioeng. Biotechnol. 11:1181078. doi: 10.3389/fbioe.2023.1181078
Received: 07 March 2023; Accepted: 19 April 2023;
Published: 12 May 2023.
Edited by:
Da Tian, Anhui Agricultural University, ChinaReviewed by:
Kailou Liu, Jiangxi Institute of Red Soil, ChinaTianyi Yu, Shandong Peanut Research Institute, China
Copyright © 2023 Wang, Pan, Lu and Qi. 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: Xin Lu, bHhkZW5nQDEyNi5jb20=; Weicong Qi, d2VpY29uZ19xaUAxNjMuY29t