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Review on Mechanism of Mineral Phosphate Solubilization in Fast-Growing Rhizobia Based on Sugar Utilization
Plant Breed. Biotech. 2022;10:203-211
Published online December 1, 2022
© 2022 Korean Society of Breeding Science.

Bhumi R. Rajguru, Vaibhav D. Bhatt*

School of Applied Sciences and Technology (SAST-GTU), Gujarat Technological University, Ahmedabad 382424, India
Corresponding author: D. Bhatt, bhatt_vbhv@yahoo.co.in, Tel: +91-79-23267642, Fax: +91-79-23267564
Received May 18, 2022; Revised August 1, 2022; Accepted September 5, 2022.
This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Plant Growth Promoting Rhizobacteria (PGPR) were used in many previous studies for increasing plant growth and productivity. Some mechanisms were used to enhance the soil productivity such as mineral phosphate solubilization, siderophore production, biological nitrogen fixation, induced systemic resistance and indole acetic acid (IAA) production. Some of the related researches adopted the phosphate solubilization in organisms which was repressed in the presence of succinate resembling the phenomenon of catabolite repression. In addition, the sugar utilization pattern (monosaccharide, disaccharide, and trisaccharide), organisms showed the characteristics like slow and fast-growing rhizobia respectively. Whole-genome sequencing has been used for identifying unique genes in Fast-growing Rhizobia. Existing literature in PGPR studies has been considered and mechanisms for increasing plant growth and productivity have been identified. The review tries to analyse the mechanism of phosphate solubilization and sugar utilization in fast growing Rhizobia. On the contrary, repression due to various carbon sources such as succinate has been reported, leading to succinate mediated catabolite repression.
Keywords : Plant growth promoting rhizobacteria, Mineral phosphate solubilization, nitrogen fixation, Carbon catabolite repression, Fast-growing rhizobia, Whole-genome sequencing
INTRODUCTION

Plants produce amino acids, minerals, vitamins, organic acids, and other nutrients which are utilized by soil organ-isms that produce metabolite influencing plant growth (Lucas García et al. 2001). Plant Growth Promoting Rhizobacteria (PGPR) are a diverse group of micro-organisms found in the rhizosphere (root surfaces) or in association with roots that can legitimately and indirectly improve plant growth efficiency (Bhattacharyya and Jha, 2012). PGPR were used to create bio-inoculant that promote plant development and yield. Numerous bacterial genus such as Pseudomonas, Azospirillum, Azotobacter, Klebsiella, Enterobacter, Alcaligens, Arthobacter, Bur-kholderia, Bacillus and Serratia have been isolated from Rhizosphere of different plants in recent years (Ahmad et al. 2008).

PGPR are root nodulating bacteria that live in symbiotic relationships with leguminous plants that contribute the most to global nitrogen fixation. PGPR were classified into several genera such as Rhizobium, Bradyrhizobium, Esorhi-zobium and Ensifer. Phosphate solubilization, indole acetic acid (IAA) production, 1-aminocyclopropane-1-carboxylate (ACC) deaminase (ACCd) production, siderophore pro-duction, lytic enzymes, and antibiotic resistance were all reported to affect plant growth. Plant Growth Promoting Rhizobacteria (PGPR) has been found to have both direct and indirect mechanisms that affect plant growth (V. Bajpai et al. 2013). Direct mechanisms include those that affect the balance of plant growth regulators, either by releasing microbial growth regulators that are integrated into the plant or by acting as a sink for plant released hormones that induce the plant’s metabolism thereby increasing its adaptive capacity. In contrast, indirect mecha-nisms necessitate the involvement of the plant’s defensive metabolic processes, which respond to the signal sent by the bacteria influencing the plant growth (Goswami et al. 2016). It has been reported that phosphorus (P) is a critical nutrient for plants. In contrast to popular assumption, soil contains a significant amount of total phosphorus compared to the amount present in plants. Because the vast majority of soil P is contained in insoluble forms, plants can only take it in two soluble forms, monobasic (H2PO4) and dibasic (HPO42‒) ions. Several phosphate solubilizing microorganisms (PSMs) have been identified that can convert insoluble phosphorus to soluble phosphorus via acidification, organic acid secretion, or proton exchange (Rawat et al. 2021).

Nitrogen-fixing microorganisms are globally significant because they are the biosphere’s only natural biological source of fixed nitrogen. These organisms enzymatically convert dinitrogen gas from the environment into ammo-nium equivalents required for the biosynthesis of essential cellular macromolecules. The nitrogenase enzyme, whose multiple subunits are encoded by the genes nifH, nifD, and nifK, is responsible for nitrogen fixation (Gaby and Buckley, 2012). The growth of fast-growing Rhizobium and slow- growing Bradyrhizobium on laboratory media were re-ported (Temesgen and Assefa, 2020). Rhizobia strains isolated from pea, bean, and clover were known as fast growers, whereas those isolated from soybean and cowpea were known as slow growers. Mesorhizobium species that modulate a diverse range of hosts, including acacia, astragalus, chickpea, lotus, Lupinus, Leucaena, Prosopis, etc. exhibit intermediate growth rates. Rhizobia have been classified into six genera based on the 16S rRNA gene sequence, namely Azorhizobium, Allorhizobium, Brady-rhizobium, Mesorhizobium, Rhizobium and Sinorhizobium (Swarnalakshmi et al. 2020).

Bacteria that form nitrogen-fixing nodules on the roots of leguminous plants are currently classified as Rhizobium and Bradyrhizobium. The physiology of these two genera alongside nodulated plant host can be distinguished by growing them separately in yeast extract and mannitol medium. Rhizobium spp. are thought to be fast-growing, with generation times of less than 6 hour, whereas Brady-rhizobium strains have generation longer than 6 h (Scholla and Elkan, 1984). In order to identify genomic variants, Whole Genome Sequencing is the most comprehensive method. DNA from a single entire genome was broken up, put together in a single sequencing library, and then it was sequenced in a single run. Fast-growing rhizobial strain Sinorhizobium fredii HH103 was capable of nodulating legumes. The HH103 genome has a total size of 7.22 Mb and was made up of one chromosome and five plasmids (Weidner et al. 2012). WGS is the most global approach for identifying genetic variations.

The main contributions of this work are summarised below:

•Review important studies associated with PGPR

•Highlight previous work related to Mineral Phosphate Solubilization (MPS)

•Mention important studies linked with Fast-Growing Rhizobia

PHOSPHATE SOLUBILIZATION

Phosphorus (P) is one of the most fundamental plant macronutrients that is mixed with soil as inorganic phosphate. Soil P deficiency can severely limit plant growth efficiency. MPS is the most likely method for increasing plant-accessible P apart from treatment and enzymatic deterioration of natural mixes (Illmer and Schinner, 1992). MPS is the arrival of free P from insoluble mineral phosphates such as calcium phosphate (CaPO4), aluminium phosphate (AlPO4), or ferric phosphate (FePO4) via organic acid temperance (Aliyat et al. 2022). PSM organic acid secretion is dependent on carbon (C) source accessibility, ecological conditions, metabolic state and physiology of the life form, and carbon catabolite repres-sion (CCR) (Görke and Stülke, 2008). Glucose is by far the best carbon source in charge of organic acid production and the emergence of the MPS phenotype, but it is not the most preferred carbon source, and its limited accessibility in the soil creates a significant barrier to Phosphate solubilization (Chen et al. 2015). The total soil phosphate (P) can also be divided into natural and inorganic P. The wonder of P solubilization and precipitation in the soil is typically extremely sensitive to pH and soil type. Nitrogen (N), potassium (K), and sulfur (S) are important plant macro- nutrients that appear to be less affected legitimately by soil pH. However, phosphorus (P) is legitimately influenced by pH and soil type. At basic pH values, such as pH 7.5, phosphate particles will generally react quickly with calcium (Ca) and magnesium (Mg) to form less dissolvable compounds. Because, at high pH Phosphate tends to precipitate with Ca and Mg. Phosphate particles react with aluminium (Al) and iron (Fe) at acidic pH values to form less soluble compounds (Gyaneshwar et al. 1999). Whole genome sequence analysis of bacterial strains consisting of Pseudomonas, Bacillus and Rhizobium have been reported (Rodrı́guez and Fraga, 1999) and the genes involved in Phosphate solubilization are pqqB, pqqC, pqqD, pqqE, pstB, phnC, pstC.

Organic phosphate solubilization

Organic Phosphate solubilization or mineralization of organic Phosphate is done by organic matter by the presence of various microorganisms. With this phosphorus can be released by three groups of enzymes. Enzymes involved in organic phosphate solubilization are non-specific phosphatases, phytases, phosphonatases and C–P lyases and their functions are dephosphorylation of organic materials phospho-ester or phosphoanhydride linkages, phytases P release from phytic acid, and C–P cleavage in organic-phosphonates are all examples of dephospho-rylation.

Inorganic phosphate solubilization (mineralization)

Inorganic phosphate exists in a variety of structures, including tricalcium phosphate, dicalcium phosphate, hydroxyapatite, and rock phosphate. Mineral phosphate is found in soil as calcium phosphate. According to a few sources, these P are artificially solubilized by Gram- negative microorganisms by a specific organic acid, which is diffused by microbes in their region (Goldstein et al. 2003). Bacterial genus such as Azospirillum, Azotobacter, Bacillus, Beijerinckia, Burkholderia and schematic depic-tion of the role of phosphate-solubilizing microorganisms (PSM) in soil P accessibility and plant uptake. Table 1 presented the related works that consider the inorganic phosphate solubilization.

Table 1 . Various microorganism shows PGPR traits.

ReferencePGPRPlant growth- promoting traitsObjectiveFinding
Ahemad and Khan, 2011; Ahmad et al. 2008-Klebsiella sp-Pseudomonas putida; Bradyrhizobi-um sp.IAA, siderophores, HCN, ammonia, exo-polysaccharides, phosphate solubilizationEvaluation of bacterial isolates for their quantitative IAA production and antifungal activityEleven bacterial isolates (seven Azotobacter, three Pseudomonas and one Bacillus) were evaluated for PGP
Farokh et al. 2011Acinetobacter spp.

IAA, phosphate solubilization, siderophoresCharacterization of PGP traits of isolates from rhizosphere of Pennisetum glaucum31 Acinetobacter isolates (Acinetobacter sp. PUCM1022 significantly enhanced theparameters of Pennisetum glaucum)
Zahir et al. 2010Rhizobium phaseoliIAAIn a pot experiment, the most salt resistant and high auxin generating rhizobial isolate N20 was assessed in the presence and absence of L-tryptophan (L-TRP)Supplementing rhizobium inoculation with L-TRP produced more effects and showed an increase in physical and chemical parameters
Ahemad et al. 2009Mesorhizobium sp.IAA, siderophores, hydrogen cyanide (HCN), ammonia, exo-polysaccha-ridesTo remediate herbicide- contaminated soil through microbial applicationHerbicides (atrazine) can be metabolised by Rhizosphere bacteria through enzyme-catalyzed hydrolysis reactions yielding cyanuric acid
Ahemad and Khan, 2010Rhizobium sp. (pea)IAA, siderophores, HCN, ammonia, exo-polysaccha-rideTo determine Mesorhizobium sp. PGP activities in the presence of herbicides and their influence on herbicide toxicity in chickpea plantMesorhizobium isolate MRC4 could be used as a bio-inoculant to help chickpeas grow under herbicide stress
Ahemad and Khan, 2011Rhizobium sp.(lentil)IAA, siderophores, HCN, ammonia, exo-polysaccharidesTo explain the involvement of rhizosphere bacteria in pesticide breakdown and transformationThe most efficient and cost- effective way to clear pesticide- contaminated locations is to use microbes with degradative abilities
Ma et al. 2011Pseudomonas sp. A3R3IAA, siderophoresTo describe the role of PGPR and/or endophytic bacteria in accelerating phytoremediationPhytoremediation can be accelerated through modulation of PGP parameters, nutrients and production of antifungal metabolites
Kumar Jha, 2015Klebsiella oxytocaIAA, phosphate solubilization, nitrogenase activityTo characterize soil microbial communities for PGPMixed inoculants and plant growth promoting consortium (PGPC) could increase the PGP
Tank and Saraf, 2010Bacillus, Pseudomonas, Azotobacter, AzospirillumP-solubilization and IAATo conduct test of efficient rhizobial isolates in pot condition under 2% NaCl stressC4 and T15 were the best growth promoters for pot studies under salinity stress

MECHANISM OF MINERAL PHOSPHATE SOLUBILIZATION

Rhizobacteria like Rhizobium sp. and Pseudomonas sp. utilize carbon sources and produce organic acid which will lead to MPS. The true mechanism of MPS is an organic acid generation, which results in acidification of microbial cells and, as a result, P will be released from mineral phosphate via proton substitution. Organic acids that are commonly found include gluconic acid, oxalic acid, suc-cinic acid, citrus acid, lactic acid, and others (Singal et al. 1994). In presence of succinate (C4 acid), there is re-pression of preferred carbon source utilization which is termed succinate mediated catabolite repression (SMCR). According to the Acid production theory, the microorga-nisms convert insoluble form of phosphate to soluble form which are taken up by the plants. In addition, it was expressed that the Phosphate solubilization procedure occurs as a result of the production of organic acid, which is joined by acidification (Puentel et al. 2004). The examination of culture filtrates of PSMs have demon-strated the nearness of a number of organic acids such as malate, succinate, fumarate, tartrate, oxalate, citrate, 2-ketogluconic, and gluconic acid (Fasim et al. 2002). The amount of dissolvable phosphate released is determined by the type, quality, and strength of the acid. Moreover, fumaric acid has been shown to have the greatest phosphate solubilizing capacity. The most proficient MPS phenotype in Gram-negative microorganisms results from the extra-cellular oxidation of glucose to gluconic acid by the quinoprotein glucose dehydrogenase and the cofactor pyrroloquinoline quinone (PQQ) (Rodríguez et al. 2000). Additionally, diverse microbial species produced organic acids amongst which gluconic, succinic and oxalic acids were the most common acids observed (Table 2).

Table 2 . Organic acid produced by various microbial species.

ReferencesOrganismPredominant acid produced
Puente et al. 2009Bacillus spGluconic, Propionic, Isovaleric, Formic, Succinic, Lactic.
P. D. Bajpai and Sundara Rao, 1971Arthrobacter sp., Bacillus spLactic, citric
Puente et al. 2004Citrobacter spFormic, Succinic, Oxalic, Oxalacetic
Vazquez et al. 2000Xanthobacter agilis, Pseudomonas aerogenesLactic, itaconic, isovaleric, isobutyric, acetic
Hwangbo et al. 2003Enterobacter intermedium2-ketogluconic
Whitelaw, 1999P. radicumGluconic
Lopez et al. 2011Pseudomonas putida, Enterobacter sakazakiiGluconic, Formic, Succinic, Lactic.
Singal et al. 1994A. japonicus, A. foetidusOxalic, citric, gluconic succinic, tartaric
Prijambada et al. 2009Pseudomonas sp., Bacillus subtilisLactic, malic
Sperber, 1958Escherichia freundiiLactic acid

CARBON CATABOLITE REPRESSION

CCR is a dual regulatory mechanism that controls the special and consecutive use of sugars and plays an important role in gene expression for the use of optional C sources in all microorganisms (Görke and Stülke, 2008). The mechanism of CCR has been studied extensively in Enterobacteriaceae (Escherichia sp. and Salmonella sp.) and Firmicutes (Bacillus sp., Staphylococcus sp., and Lactobacillus sp.) where glucose is the preferred C source and is known to suppress the uptake and utilization of a few other sugars and organic acids (Deutscher, 2008). Phos-phoenolpyruvate (PEP): carbohydrate phosphotransferase framework (PTS) is the primary route of sugar uptake in these organisms, and glucose utilization in enteric micro-organisms occurs via the Embden-Meyerhof-Parnas path-way (EMP or glycolysis) (Postma et al. 1993). In these life forms, the suppression of secondary C sources is mostly controlled at the transcriptional level by inducer exclusion. The microorganisms can either co-metabolize or use the C sources that are most readily available and can undergo fastest growth. In some microorganisms, glucose is only an optional C source, and the gene for glucose utilization is suppressed as long as the preferred C sources are available. This mechanism is known as reverse carbon catabolite repression (CCR) (Van Den Bogaard et al. 2000). The phenomenon is found primarily in Pseudomonas and Rhizobium where organic acids such as succinate, malate, and so on are preferred C sources that inhibit glucose uptake and utilization. The C4 acid succinate is known to inhibit the utilization of sugars, sugar alcohols, hydro-carbons, etc. by a process known as succinate-mediated catabolite repression (SMCR). The hierarchy of carbon source consumption in bacteria is determined by the catabolite repression mechanism (Iyer et al. 2016).

Carbon catabolite repression and mineral phosphate solubilization phenotype

Glucose is preferred over other carbon sources for CCR, as a significant phenomenon of secondary carbon source utilization and preferred carbon source activities. There have been reports that CCR-related genes can suppress the MPS phenotype. For example, the gene IclR has been discovered in Klebsiella pneumonia (Mahendrapal et al. 2015). Both free-living and symbiotic rhizobia can use a wide range of carbon compounds, which raises the issue of catabolite repression control. A significant portion of the Sinorhizobium meliloti genome encodes genes involved in carbon catabolism and transport. Preliminary research on CCR in Rhizobium meliloti has revealed that a diverse range of sugars and tricarboxylic acid cycle (TCA) intermediates can promote growth in a variety of rhizobia. Sugar alcohols in Rhizobium leguminosarum and galac-tosides in Sinorhizobium meliloti have been shown to undergo glucose-mediated catabolite repression. Succinate inhibits glucosidase and galactosidase activity in R. meliloti (Iyer et al. 2016). In Rhizobium sp. and Brady-rhizobium sp., glucose catabolic enzymes are induced, and succinate inhibits them in a cyclic adenosine monophosphate- independent manner while glucose inhibits the absorption of b-D glucosides in Agrobacterium tumefaciens in a Cyclic adenosine monophosphate-dependent manner.

SUGAR UTILIZATION IN FAST-GROWING RHIZOBIA

Sugar utilization differentiates fast and slow-growing rhizobia. Sugar usage tests showed that the fast growers used a more noteworthy combination of sugar than the slow growers. The majority of the microorganisms observed used L-arabinose, D-fructose, D-galactose, D-glucose, D-mannitol, D-mannose, L-rhamnose, and D-xylose. Even though the fast-growing rhizobia were fit for using arabinose, individuals developed more gradually on ara-binose than the slow growers. Just the fast-growing rhizobia used cello-biose, I-inositol, lactose, maltose, raffinose, D-glucitol, sucrose, and trehalose while slow- growing rhizobia cannot (Iyer et al. 2016). Arabinose is also known as pectinose or pectin sugar when it is the only carbon source. It may be found in plants as a naturally occurring monosaccharide, and arabinose serves as a substrate for pentose sugar isomerase. It is a solid that dissolves in water in terms of its characteristics. From literature reviews, it has been reported L-arabinose takes after the Entner-Doudoroff pathway. Slow-growing rhizboia are mostly arabinose-containing. The foundation of the growth rate and influence of pH when growing on YEA medium under standard research facility conditions, glycolaldehyde and pyruvate will be produced by rhizobia. Here, oxalate cycle entry is made by glycolaldehyde, whereas TCA cycle entry is made through a-ketoglutaric semialdehyde (Joshi et al. 2019). Citrate was discovered to be advantageous as a carbon source in Rhizobium phaseoli and Rhizobium trifolii (both fast-growing Rhizobia) (Singh, 2015). Slow-growing Bradyrhizobium japonicum and Rhizobium leguminosarum on the other hand showed no color change and tested negative for citrate. Hence, sugar utilization in fast-growing Rhizobia is more effective for the production of fertilizer (Iyer et al. 2016).

CONCLUSION

Plant growth-promoting rhizobacteria was able to solubilize phosphorus by the production of organic acids. Although a mechanism similar to phosphate solubilization by several carbon sources such as glucose, arabinose, and xylose has been reported, the detailed characterization of carbon catabolite repression and utilization of other secondary carbon sources remains unknown. Major plant growth-promoting rhizobacteria and their traits involved in mineral phosphate solubilization have been thoroughly studied in Rhizobium sp., Pseudomonas sp., and Bradyrhi-zobium sp. The experiments reviewed in this manuscript conclude that fast-growing Rhizobia has the highest phosphate solubilization and sugar utilization, whereas catabolite repression by various carbon sources such as succinate has been reported, resulting in succinate mediated catabolite repression. In order to maintain agricultural output, it will be difficult to use fertilisers without having a negative impact on the environment. Growing plants should give way to the growth of plant-microbial communities in sustainable agriculture, which can achieve great production with little use of energy or chemicals and with little impact on the environment (Santos et al. 2011). Hence, studying whole-genome sequencing of Rhizobium sp. was important as it is strong phosphate solubilizer with gluconic acid production ability through periplasmic glucose oxidation pathway even under conditions of catabolite repression.

CONFLICT OF INTEREST

No potential conflict of interest relevant to this article was reported.

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