Genome analysis of Pantoea dispersa PGPR-24 reveals key genetic pathways for plant growth promotion, root colonization and nutrient mobilization
Cite as: Hossain, Tanim Jabid (2024) Genome analysis of Pantoea dispersa PGPR-24 reveals key genetic pathways for plant growth promotion, root colonization and nutrient mobilization. Preprint.
Article Type: Research Article
Published version: Will be available when published after peer-review
Subject: PGPR Genome | Plant-Microbe Interaction | Sustainable Agriculture
Author: Tanim Jabid Hossain1,2*
1 Department of Biochemistry and Molecular Biology, University of Chittagong, Chattogram, Bangladesh
2 Laboratory for Health, Omics and Pathway Exploration (HOPE Lab), Chattogram, Bangladesh
* Corresponding author: Tanim Jabid Hossain; email: tanim.bmb@gmail.com
Plant growth-promoting rhizobacteria (PGPR) are integral to sustainable agriculture, enhancing plant growth, nutrient availability, and soil health. The genome analysis of Pantoea dispersa PGPR-24, a rhizobacterium isolated from the chrysanthemum rhizosphere, reveals its extensive potential as a PGPR supported by diverse genetic pathways linked to nutrient mobilization, plant growth promotion, and stress adaptation. The 4.746 Mb genome, with 99.37% completeness and 4,411 coding sequences, encodes key genes for phosphate solubilization, siderophore-mediated iron acquisition, sulfate assimilation, and ammonia assimilation, highlighting its role in nutrient cycling and bioavailability. Genes associated with auxin and cytokinin biosynthesis suggest its potential to produce phytohormones that regulate root architecture, enhance nutrient uptake, and support plant development. Additionally, the genome encodes biosynthetic pathways for volatile organic compounds (VOCs), including acetoin and 2,3-butanediol, which are known stimulate root elongation, improve stress tolerance, and activate plant defense responses. Furthermore, the genome features compounds with antimicrobial and protective properties, such as siderophores, carotenoids and exopolysaccharides, which contribute to pathogen suppression, biofilm formation and enhanced rhizosphere colonization. Genes supporting motility, chemotaxis, and adhesion further strengthen potential for efficient colonization and plant-microbe interactions. Stress-response mechanisms, including pathways for osmoregulation, oxidative and periplasmic stress tolerance, and starvation resistance, equip the strain to thrive in diverse environmental conditions. These genomic insights, complemented by its reported in vitro plant growth-promoting traits, not only position P. dispersa PGPR-24 as a highly versatile rhizobacterium for sustainable agriculture but also offer a valuable genetic framework for advancing our understanding of PGPR-mediated plant growth promotion and stress resilience.
Keywords: Pantoea dispersa genome sequence, PGPR genome analysis, plant-microbe interaction, sustainable agriculture, rhizosphere colonization, nutrient cycling, nutrient bioavailability, stress tolerance mechanisms.
Cite: Hossain, Tanim Jabid (2024) Genome analysis of Pantoea dispersa PGPR-24 reveals key genetic pathways for plant growth promotion, root colonization and nutrient mobilization. Preprint.
Info: This is a preprint version; A preprint is a version of a scholarly paper that precedes formal peer review.
Full Text
Soil-microbe-plant interactions are fundamental to ecosystem health, where beneficial microbes act as natural allies, supporting plant growth, soil fertility, and environmental sustainability [1]. These microbes, increasingly recognized as plant probiotics, play crucial roles in supporting plant and soil health. Among them, plant growth-promoting rhizobacteria (PGPR) are key players known for improving nutrient availability, producing phytohormones, mitigating stress, and suppressing plant pathogens [2]. PGPR also contribute substantially to soil health through microbial interactions, nutrient cycling, and organic matter stabilization, thereby bridging plant and soil ecosystems [3,4]. Processes such as biofilm formation, exopolysaccharide (EPS) production [5], and microbial interactions further stabilize soil aggregates, retain moisture, and support nutrient exchange [6]. Given the rising demand for sustainable agricultural practices, PGPR are vital in developing biological alternatives to chemical fertilizers, emphasizing the need to explore these microbial allies to address modern agricultural challenges.
Within the PGPR community, species of Pantoea have emerged as important players due to their versatile roles in promoting plant health. Among these, P. agglomerans has been relatively well-studied for its PGPR activities [7]. Recently, a strain from another Pantoea species, P. dispersa PGPR-24, isolated from the rhizosphere of chrysanthemum, has demonstrated promising in vitro plant growth-promoting activities, such as auxin production, phosphate solubilization, nitrogen fixation, and ammonia production [8]. These abilities make it a promising microorganism for agricultural applications. Although P. dispersa remains relatively understudied, some research has documented its positive effects on plant growth, nutrient cycling, and soil health, positioning it as an emerging candidate for sustainable agriculture [9–13]. However, deeper investigation is required to fully understand its functional capabilities and establish its value as a biofertilizer.
The sequencing and analysis of microbial genomes are invaluable for elucidating the metabolic and functional capabilities of PGPR [14,15]. For Pantoea dispersa, where limited genomic analysis has been conducted, functional annotation can offer insights into its genetic potential, enabling the identification of genes associated with plant growth promotion and stress tolerance. This approach uncovers specific genetic pathways responsible for nutrient acquisition, phytohormone synthesis, siderophore production, and other beneficial PGPR activities. Genome analysis provides a clearer understanding of the genetic foundation underlying these beneficial traits, paving the way for further studies aimed at harnessing these capabilities for agricultural purposes [14,15]. Linking genome data to the functional traits of PGPR is essential for developing targeted strategies to enhance plant growth and soil health in a sustainable farming systems.
The primary objective of this study is to perform a comprehensive genomic analysis of P. dispersa PGPR-24, focusing on its potential as a plant growth-promoting rhizobacterium. While its pot and field trials are ongoing, this research aims to identify key genes and mechanisms that contribute to its beneficial effects on plants and soil. By examining its genetic components, we seek to uncover pathways that can enhance crop productivity and plant health in sustainable agricultural systems. These findings will contribute to the broader field of microbial ecology and plant-microbe interactions, offering new insights into how beneficial soil microbes like Pantoea dispersa can be integrated into bio-based agricultural technologies to foster resilient ecosystems.
The isolation, identification, and initial in vitro characterization of Pantoea dispersa PGPR-24’s plant growth-promoting traits were previously documented [8]. Briefly, the bacterium was isolated from root-associated soil using the spread plate method on agar media, purified through subculturing [16]. Out of a total of 39 isolates, Out of 39 isolates, six strains demonstrated prominent in vitro plant growth-promoting activity, including Staphylococcus hominis, Bacillus cereus, Acinetobacter oleivorans, Staphylococcus epidermidis, Pantoea dispersa, Serratia nematodiphila, and Pantoea anthophila. Species identification was confirmed by sequence similarity analysis of the 16S rRNA gene against the respective type strain. The isolates were preserved as glycerol stocks at -80°C. For further studies, including genome sequencing, P. dispersa PGPR-24 was cultured aerobically on nutrient agar or trypticase soy agar at 30°C.
For sequencing of the P. dispersa PGPR-24 genome, the extraction of genomic DNA, library preparation and sequencing were performed by BD Genomes, Bangladesh, essentially as previously described [17], with some modifications. For genomic DNA extraction, a 1.5 ml culture aliquot was centrifuged at 13,000 rpm for 10 minutes. The pellet was resuspended in 350 µl lysis buffer with 20 µl proteinase-K (20 mg/ml) and incubated at 65°C for 30 minutes. After cooling, 3 µl RNAse A was added, followed by incubation at 37°C for 10 minutes. An equal volume (373 µl) of phenol:chloroform:isoamyl alcohol (25:24:1) was added, vortexed, and centrifuged at 14,000 rpm for 10 minutes. The aqueous layer (~200 µl) was transferred to a new tube, mixed with chloroform:isoamyl alcohol (24:1), and centrifuged again. The upper phase (~150 µl) was collected, mixed with 800 µl ice-cold absolute ethanol, gently inverted, and incubated at -40°C for 1 hour. The DNA pellet was collected by centrifugation, washed with chilled 70% ethanol containing 20 µl 7.5 M ammonium acetate, incubated at -20°C for 30 minutes, air-dried, and dissolved in 50 µl TE buffer (pH 7.6) at 37°C for 10 minutes. The whole-genome sequencing of P. dispersa PGPR-24 was performed at Novogene, China on the Illumina NovaSeq 6000 platform (150 bp paired-end).
The quality check of the sequence reads, trimming of the unnecessary or low-quality sequences, and sequence assembly were carried out mostly following previously described protocols [17]. Quality control was performed using FastQC (v0.11.9). Sequencing adapters and low-quality bases were removed using Trimmomatic (v0.39). Trimming parameters included removing bases with quality scores below 20 (LEADING:20 TRAILING:20), using a sliding window of 4 bases with an average quality threshold of 15 (SLIDINGWINDOW:4:15), and discarding reads shorter than 36bp after trimming. The trimmed, high-quality reads were assembled de novo into contigs using Unicycler (v0.4.8).
The genome sequence of P. dispersa PGPR-24 has been deposited in Mendeley Data at https://doi.org/10.17632/n7fjw6hvz2.1.
Gene prediction and genome functional annotation were carried out essentially according to the method described in a previous study [17] using a number of annotation pipelines such as Prokka, DDBJ Fast Annotation and Submission Tool, and Rapid Annotations using Subsystems Technology (RAST). Functional categorization was performed using the RASTtk scheme [18,19] and with BlastKOALA [20,21]. The genes identified using RAST were categorized into functional subsystems within the SEED database. Moreover, protein sequences obtained from the genome annotations were provided to BlastKOALA to perform KEGG (Kyoto Encyclopedia of Genes and Genomes) orthology assignments (KO-assignment) for characterization of individual gene functions and the KEGG Mapper tool was used for KO-based metabolic pathway mapping. Additionally, functional annotation was also conducted using BLAST sequence similarity analysis, where sequences of specific target proteins were obtained from the NCBI or UniProt databases. These target sequences were then compared against a custom database containing only P. dispersa PGPR-24 protein sequences to identify matches based on sequence similarity. To predict carbohydrate-active enzymes (CAZymes), the genome sequence was analyzed using previously described method [17,22]. Annotation was performed using three tools using HMMER, DIAMOND, and dbCAN-sub. Only CAZymes predicted by all the three tools were considered.
The sequencing and assembly of the Pantoea dispersa PGPR-24 genome yielded a 4.746 Mb sequence, closely aligning with the size of the P. dispersa reference genome (GenBank accession: GCA_019890955.1) in the NCBI database, which is 4.885 Mb. This size is also consistent with the average genome size of 4.798 Mb observed across the 67 currently listed P. dispersa genomes. The assembly achieved 99.37% completeness (Table 1), resulting in a near-complete genome organized into 24 contigs, 22 of which were at least 200 bp long, with the longest sequence spanning 1,817,013 bp. The Genome had an N50 value of 736,526 and a GC content of 57.7%.
Table 1. Genomic features of Pantoea dispersa PGPR-24, including genome assembly and annotation results. An overview of the key genomic characteristics are presented based on a high-coverage genome assembly, including assembly statistics and functional annotation results. The assembly yielded a nearly complete genome with high average nucleotide identity to the type strain.
A total of 4,411 coding sequences (CDs) were predicted in the P. dispersa PGPR-24 genome, representing an 88.2% coding ratio. Additionally, the genome includes 3 rRNA genes and 74 tRNA genes (Table 1). The genome showed high similarity to the P. dispersa type strains CCUG 25232T (accession: GCA_008692915.1) and DSM 30073 (GCA_014155765.1) with average nucleotide identity (ANI) values of 98.15% and 98.07% respectively. Functional annotation using RAST tool identified 349 subsystems, with 1509 features grouped into 26 specific subsystem categories, predominantly associated with amino acids and derivatives, carbohydrates, and protein metabolism (Figure 1). Within carbohydrate metabolism, the majority of features were linked to central carbohydrate metabolic pathways, fermentation processes, and the metabolism of mono-, di-, and oligosaccharides, as well as sugar alcohols. In protein metabolism, most features were involved in protein synthesis, degradation, and folding.
Figure 1. Functional annotation of Pantoea dispersa PGPR-24 genome sequence highlighting key metabolic and cellular features. Prominent features include pathways for amino acid and carbohydrate metabolism, DNA and RNA processing, stress response, respiration, and protein synthesis, degradation, and folding, reflecting the bacterium’s versatile metabolic capabilities.
The genome of P. dispersa PGPR-24 encodes a versatile metabolic capacity, encompassing pathways involved in carbohydrate metabolism, energy production, and biosynthesis (Supplementary data; Table S1). Metabolic pathway reconstruction identified complete modules for glycolysis (Embden-Meyerhof pathway), gluconeogenesis, and the citrate cycle (TCA cycle), all of which are essential for efficient energy generation. The presence of oxidative and non-oxidative phases of the pentose phosphate pathway highlights the bacterium's ability to generate reducing power in the form of NADPH, as well as precursors for nucleotide synthesis. Moreover, the genome encodes pathways for the degradation of D-galacturonate and D-glucuronate, indicating its ability to utilize plant-derived sugars such as those from pectin and hemicellulose, which are abundant in the rhizosphere. The capacity for trehalose and glycogen synthesis and degradation further emphasizes its metabolic flexibility in using diverse carbohydrate sources, enabling the efficient conversion of carbohydrates into energy and biomass. This adaptability likely supports the bacterium's survival and competitive advantage in the plant-associated environment.
Additionally, the genome analysis revealed pathways for nucleotide sugar biosynthesis, including the production of UDP-N-acetyl-D-glucosamine, which is required for synthesizing key cell wall components and extracellular polysaccharides. The genome also features assimilatory and dissimilatory nitrate reduction pathways, facilitating the conversion of nitrate into ammonia - an important nitrogen source that supports plant growth. Similarly, the presence of assimilatory sulfate reduction pathways, which transform sulfate into hydrogen sulfide, ensures the incorporation of sulfur into amino acids and cofactors that are vital for both microbial and plant metabolic processes. Additionally, the detection of the phosphate acetyltransferase-acetate kinase pathway enables efficient acetate utilization, an important intermediary metabolite in carbon metabolism. The complete NADH oxidoreductase and cytochrome oxidase complexes within the electron transport chain highlight the bacterium’s capacity for efficient ATP synthesis and energy homeostasis, ensuring the maintenance of essential cellular functions. With this versatile metabolic capacity and energy generation, PGPR-24 appears to play a critical role in nutrient cycling, nutrient provisioning, and environmental adaptation. These capabilities likely facilitate its adaptation to the rhizosphere, making a valuable contribution to both plant and soil health.
Carbohydrate-active enzymes (CAZymes) are essential for the synthesis, modification and utilization of complex carbohydrates, playing a central role in microbial survival, nutrient cycling, and interactions with plants and the environment [23]. In plant-associated microbes, CAZymes can contribute to processes such as plant cell wall degradation, extracellular polysaccharide production, and nutrient mobilization [23], which are vital for their function as PGPR. The genome analysis of P. dispersa PGPR-24 revealed the presence of at least 88 CAZymes across diverse families, reflecting its ability to metabolize a wide range of carbohydrates (Supplementary data; Table S2). These CAZymes belong to various functional classes, including glycoside hydrolases (GHs), glycosyltransferases (GTs), carbohydrate-binding modules (CBMs), carbohydrate esterases (CEs), and auxiliary activities (AAs), underscoring the bacterium’s versatile carbohydrate-processing capabilities.
Among the CAZymes, GTs were the most abundant with GT2 being predominant, appearing 17 times. The GT2 family is associated with the biosynthesis of cellulose, hemicellulose, and other polysaccharides [24], which are essential for bacterial cell wall integrity, exopolysaccharide production, and biofilm formation. These attributes are likely critical for P. dispersa PGPR-24’s colonization and persistence in the rhizosphere, as well as its role in modulating plant-microbe interactions. Other glycosyltransferases, such as GT4 and GT8, were also identified and are associated with the biosynthesis of polysaccharides and glycoconjugates that may contribute to its plant-associated activities [25,26].
GHs, another major class of CAZymes [27], were well-represented including families such as GH1, GH3, GH23, and GH73. The GH enzymes are known for their ability to degrade plant-derived carbohydrates, oligosaccharides, and other polysaccharides [28,29], emphasizing the bacterium’s potential to metabolize plant exudates and contribute to nutrient cycling in the rhizosphere. This carbohydrate-degradation capability aligns with the requirements of a rhizosphere environment, where microbial access to diverse carbohydrate sources supports survival and ecological function.
Additionally, carbohydrate-binding modules (CBMs) (e.g., CBM48+GH13), carbohydrate esterases (CEs) (e.g., CE9, CE11), and auxiliary activity (AA) enzymes (e.g., AA3_2) were identified, indicating a capacity for interactions with complex carbohydrates, processing of plant-derived materials, and facilitation of nutrient release. These enzymes likely enhance the bacterium’s metabolic flexibility and ecological adaptability.
The diverse repertoire of CAZymes in P. dispersa PGPR-24 highlights its potential as a PGPR by contributing to nutrient acquisition and cycling in the rhizosphere. Its ability to utilize a braod range of carbohydrate substrates not only supports its survival in the rhizosphere but also facilitates mutualistic interactions with plants [23,28]. Glycosyltransferases, particularly the abundant GT2 family, may contribute to biofilm formation, exopolysaccharide production, and root adherence, potentially enhancing the bacterium’s ability to colonize and persist in plant-associated environments. Glycoside hydrolases likely enable the degradation of plant-derived carbohydrates into simpler sugars, promoting nutrient availability and cycling. Overall, the metabolic flexibility provided by CAZymes underscores the ecological and agricultural relevance of P. dispersa PGPR-24 as a promising candidate for sustainable agricultural applications, enhancing plant growth and health through efficient colonization and carbohydrate metabolism.
Phosphate solubilization is a critical plant growth-promoting trait of PGPR that enhances phosphorus availability in the soil by converting insoluble phosphate compounds into bioavailable forms that plants can readily absorb. The genome of P. dispersa PGPR-24 harbors several genes that contribute to this process (Table 3), emphasizing its role in the phosphorus cycle and its potential as a beneficial soil bacterium. Key gene systems identified include the pqq gene cluster (pqqABCDEF) responsible for the synthesis of pyrroloquinoline quinone (PQQ), a cofactor required for the activity of gluconate dehydrogenase (Gcd). The Gcd enzyme catalyzes the oxidation of glucose to gluconic acid, which acidifies the surrounding environment, solubilizing otherwise insoluble phosphate compounds [30]. PQQ-dependent glucose dehydrogenase activity is a well-established mechanism among phosphate-solubilizing PGPR. Similar systems in Pseudomonas and Acinetobacter strains have demonstrated enhanced phosphorus solubilization, subsequently improving plant growth [31,32], suggesting that P. dispersa PGPR-24 may also provide similar benefits. Additionally, the phosphate-specific transport (Pst) system, encoded by genes pstS, pstC, pstA, and pstB, contributes to phosphate uptake and homeostasis. The Pst system facilitates the transport of phosphate ions across the bacterial membrane, particularly under phosphate-limiting conditions [33]. Regulatory proteins PhoB and PhoU are also encoded in the genome, which function within the Pho regulon to modulate the expression of phosphate-responsive genes based on Pi availability. Specifically, PhoB acts as a transcriptional regulator, activating a suite of genes under phosphate-limiting conditions. PhoU is thought to inhibit excessive phosphate uptake through the Pst system, contributing to phosphate homeostasis by controlling intracellular phosphate accumulation [34]. The presence of genes encoding alkaline phosphatase and phytase further supports phosphate solubilization in P. dispersa PGPR-24. Alkaline phosphatase releases phosphate from organic phosphorus compounds [35], while phytase degrades phytate [36], a significant organic phosphorus source in soils, liberating phosphate ions (Pi) for plant uptake. Together, these enzymes underscore PGPR-24’s capability to mobilize both inorganic and organic phosphate sources. The activity of such hydrolytic enzymes plays a vital role in breaking down complex macromolecules [37,38], thereby enhancing nutrient availability for both microbial and plant utilization. Additionally, genes supporting bacterial phosphate utilization, such as ppk1 (polyphosphate kinase) and ppx-gppA (exopolyphosphatase), facilitate polyphosphate storage and mobilization, allowing the bacterium to manage internal phosphate reserves. Genes like phnG, phnH, phnI, and phnJ are involved in phosphonate degradation, enabling the use of phosphonates as alternative phosphorus sources.
These phosphate solubilization and utilization genes highlight the potential of P. dispersa PGPR-24 to enhance phosphorus bioavailability in the soil, thereby benefiting plant growth. Recent studies have shown that inoculation with phosphate-solubilizing microbes (PSMs) can significantly enhance plant phosphorus uptake and improve crop yields while reducing dependency on chemical phosphorus fertilizers. For instance, inoculating crops with PSM has been reported to reduce the need for phosphate fertilizer by up to 50% without compromising yield [39]. This potential makes P. dispersa PGPR-24 a promising candidate for promoting sustainable phosphorus management in agricultural systems.
Iron is an essential micronutrient for both plants and microbes, functioning as a cofactor in numerous enzymatic and metabolic processes, including photosynthesis, respiration, and nitrogen fixation. However, iron is often present in insoluble forms in soil, making it scarcely bioavailable to plants. PGPR contribute to plant iron acquisition by producing siderophores - small, high-affinity molecules that chelate ferric iron (Fe³⁺), enhancing its solubility and bioavailability in the rhizosphere [40]. In P. dispersa PGPR-24, genome analysis revealed genes associated with siderophore transport, including fhuA, encoding a ferric hydroxamate outer membrane receptor, and the fhuBCD cluster, encoding the ferric hydroxamate ABC transport system. This system facilitates the import of ferric hydroxamate complexes, essential for microbial iron acquisition in competitive soil environments. Studies have demonstrated similar siderophore transport systems in various PGPR strains, including Pantoea species [41]. The presence of this system in PGPR-24 highlights its potential to enhance iron mobilization in the rhizosphere, thereby improving iron availability for plant nutrition.
Additionally, P. dispersa PGPR-24 possesses the genetic framework for enterobactin production and transport, a siderophore with one of the highest known affinities for iron. Key genes include the entABCDEF cluster, which directs enterobactin biosynthesis, entS for export, and the fepABCDG cluster for the recognition, binding, and import of ferric-enterobactin complex. Enterobactin esterase (encoded by fes) releases iron from the ferric-enterobactin complex within the cell, enabling its utilization. Enterobactin-mediated iron acquisition is a highly effective system [42], and siderophore-producing PGPR have been associated with increased soil iron availability, which can help plants overcome iron deficiency symptoms and support plant health.
Table 2. Genomic features of Pantoea dispersa PGPR-24 involved in nutrient acquisition and cycling. Major genes and pathways responsible for nutrient solubilization, transport, and metabolic cycling have been listed, focusing on phosphorus, iron, nitrogen, sulfur assimilation pathways. These genes enhance nutrient bioavailability in the soil, promoting plant growth, stress tolerance, and soil health. The systems described contribute to the bacterium's ability to improve crop yield and soil sustainability, making PGPR-24 a promising tool for sustainable agriculture.
Beyond siderophore-mediated iron uptake, the PGPR-24 genome includes genes for direct ferrous iron transport, notably the EfeUOB system, which is induced under low-pH conditions. This system includes EfeU (permease), EfeO (periplasmic binding protein), and EfeB (peroxidase), which enable ferrous iron (Fe²⁺) transport across the bacterial membrane, offering an advantage when ferric iron is scarce or soil pH is acidic. Additionally, the hmuU (permease), hmuT (periplasmic binding protein), hmuV (ATPase), and hmuS (heme transport protein) components collectively facilitate heme import and iron release, providing an alternative iron source in depleted environments.
The presence of multiple siderophore systems, ferrous iron transport, and heme transport in P. dispersa PGPR-24 emphasizes the strain's robust iron acquisition mechanisms, which could contribute to improving plant iron nutrition - a crucial factor in growth, particularly in calcareous soils where iron availability is limited [43]. Previous studies have shown that inoculating plants with siderophore-producing bacteria, such as Pseudomonas and Bacillus species, can enhance plant iron uptake, sometimes increasing iron content by up to 26%, with associated improvements in crop yield [44]. By supporting plant iron acquisition, P. dispersa PGPR-24 has the potential to promote sustainable agricultural practices, particularly in soils with limited bioavailable iron.
Sulfate assimilation is an essential process that supports plant growth by ensuring the availability of sulfur, a critical nutrient involved in the synthesis of amino acids, coenzymes, and plant defense compounds. In the genome of P. dispersa PGPR-24, a comprehensive suite of genes was identified that encodes components responsible for sulfate uptake, activation, reduction, and assimilation, highlighting the bacterium's potential role in sulfur cycling and bioavailability in the rhizosphere. Key genes involved in sulfate transport include cysW and cysT, which encode permease proteins, cysA, an ATP-binding protein, cysP, a periplasmic sulfate-binding protein, and cysZ, a sulfate transporter. Together, these genes form a complete sulfate and thiosulfate transport system, providing P. dispersa PGPR-24 with an efficient mechanism for sulfur acquisition. Inside the cell, sulfate is converted to adenosine 5'-phosphosulfate (APS) by the sulfate adenylyltransferase complex encoded by cysN and cysD. APS is then phosphorylated by adenylylsulfate kinase (cysC) to produce 3'-phosphoadenosine-5'-phosphosulfate (PAPS), which is subsequently reduced to sulfite by phosphoadenylyl-sulfate reductase (cysH). The final reduction of sulfite to hydrogen sulfide is mediated by the sulfite reductase enzyme complex encoded by cysI and cysJ. This pathway, from sulfate uptake to sulfide production, supplies sulfur to downstream biosynthetic pathways, which are essential for synthesizing sulfur-containing amino acids and other metabolites that support plant nutrition. Additionally, P. dispersa PGPR-24 possesses genes such as ssuA and ssuD (involved in sulfonate uptake and metabolism) and tauD (encoding taurine dioxygenase), which broaden the range of sulfur sources it can metabolize. These genes allow PGPR-24 to utilize sulfonates and taurine—organic sulfur sources commonly found in soils. Furthermore, the presence of glpE, encoding thiosulfate sulfurtransferase, enables the conversion of thiosulfate to sulfite, further adding to the pool of sulfur available for reduction and assimilation.
The suite of sulfate assimilation and sulfonate utilization genes in P. dispersa PGPR-24 underscores its multifaceted role in sulfur cycling, potentially supporting plant growth and resilience. Study has shown that P. putida mutants lacking the ability to metabolize sulfonate-sulfur show diminished ability to promote tomato plant growth [45], highlighting the importance of sulfur mobilization as a critical function for supporting plant nutrition. These findings underscore the potential of P. dispersa PGPR-24, with its suite of sulfur metabolism genes, could play a valuable role in enhancing plant sulfur nutrition, thereby contributing to improved plant health and growth.
Ammonia assimilation is a critical process in nitrogen metabolism, enabling rhizobacteria to convert inorganic ammonia into organic nitrogen forms that are essential for cellular functions and beneficial for plant growth. In the rhizosphere, ammonia-assimilating bacteria enhance nitrogen availability, thereby supporting plant nutrition and soil fertility. The genome of P. dispersa PGPR-24 contains several genes central to ammonia assimilation, indicating the bacterium’s potential role in nitrogen cycling in the rhizosphere. Key genes include those encoding for an ammonium transporter (amtB), which facilitates the uptake of ammonium from the environment, and glutamine synthetase type I (glnA), which catalyzes the conversion of glutamate and ammonia into glutamine, an essential nitrogen reservoir. Further processing of glutamine takes place through the GS-GOGAT cycle, in which glutamate synthase (gltB) catalyzes the conversion of glutamine and 2-oxoglutarate to two molecules of glutamate, replenishing the cellular glutamate pool and facilitating nitrogen transfer to other biosynthetic pathways. Additionally, genes encoding regulatory proteins, such as nitrogen regulatory protein P-II (glnB), nitrogen regulation protein NR(I) (ntrC), and [Protein-PII] uridylyltransferase (glnD), were present, modulating the GS-GOGAT pathway in response to varying nitrogen levels. The ammonia assimilation pathways in P. dispersa PGPR-24 are particularly significant as they contribute to bioavailable nitrogen, enhancing plant growth by supplying organic nitrogen that plants can readily absorb. This capability to improve nitrogen bioavailability underscores the bacterium’s potential to enhance soil health and support sustainable plant productivity [46].
Auxin production is a well-recognized plant growth-promoting trait in rhizobacteria, with auxins like indole-3-acetic acid (IAA) playing a critical role in regulating plant growth and development. The genome of P. dispersa PGPR-24 contains several genes associated with IAA biosynthesis, notably the full trpEGDCFBA gene cluster (Table 4), which encodes enzymes critical to the tryptophan biosynthetic pathway [47]. This pathway, conserved across various organisms, includes anthranilate synthase subunits TrpE and TrpG, which catalyze the conversion of chorismate to anthranilate. Subsequently, anthranilate phosphoribosyltransferase TrpD incorporates phosphoribosyl pyrophosphate (PPi) to yield N-(5'-phosphoribosyl)-anthranilate, while phosphoribosylanthranilate isomerase and indoleglycerol phosphate synthase (TrpCF) catalyze the conversion to indole-3-glycerol phosphate. Finally, tryptophan synthase subunits TrpB and TrpA complete the conversion to L-tryptophan, a common precursor for IAA in many plant-associated bacteria. The presence of these genes in P. dispersa PGPR-24 supports its ability to synthesize tryptophan, providing a precursor substrate for auxin production. Moreover, the genome also harbors the ipdC gene encoding indolepyruvate decarboxylase, a key enzyme in the conversion of tryptophan to IAA via the indole-3-pyruvate (IPA) pathway. This enzyme catalyzes the decarboxylation of indole-3-pyruvate to indole-3-acetaldehyde, a vital step in the pathway leading to IAA synthesis. Although some accessory genes for IAA biosynthesis may be absent, the trpEGDCFBA cluster and ipdC gene collectively suggest a genetic basis for auxin production that could positively influence plant growth. For instance, the ipdC gene has been linked to enhanced IAA production and improved root architecture in PGPR such as Azospirillum brasilense [48]. In P. dispersa PGPR-24, the presence of these auxin-related genes supports it’s observed in vitro plant growth-promoting activities, indicating its potential as a beneficial rhizobacterium.
Table 3. Genetic components identified in the genome of Pantoea dispersa PGPR-24 that are involved in the biosynthesis of phytohormones auxin and cytokinin. These systems contribute to plant growth and development through auxin production (indole-3-acetic acid, IAA) and cytokinin production (enhancing root/shoot development and stress tolerance).
Cytokinin production is a valuable plant growth-promoting trait that enhances root and shoot development, delays senescence, and improves stress tolerance. In the genome of P. dispersa PGPR-24, key genes involved in cytokinin biosynthesis were identified, including the isp gene cluster (ispD, ispE, ispF, ispG, ispH) and the gene dxs, which encode enzymes involved in the methylerythritol phosphate (MEP) pathway. This pathway is responsible for the biosynthesis of isopentenyl pyrophosphate (IPP) and dimethylallyl pyrophosphate (DMAPP), which are precursors for isopentenyl cytokinins. In addition, the genome encodes miaA, miaB, and miaE genes associated with tRNA isopentenylation. miaA encodes tRNA adenosine(37)-N6-dimethylallyltransferase, a key enzyme in the tRNA-dependent cytokinin biosynthesis pathway, which catalyzes the isopentenylation of adenosine-37 in tRNA, forming precursors that can be converted into active cytokinins. The identification of these genes suggests the bacterium’s strong potential to plant growth-promoting activities through cytokinin-mediated mechanisms.
Volatile organic compounds (VOCs) produced by PGPR play a pivotal role in mediating plant-microbe interactions, enhancing plant growth, and providing protection against various stresses [49,50]. The genome of P. dispersa PGPR-24 includes genes encoding key enzymes involved in the synthesis of Volatile Organic Compounds (VOCs) known for their plant growth-promoting properties. These enzymes include acetolactate synthase (als), alpha-acetolactate decarboxylase (budA), diacetyl reductase (budC), and alcohol dehydrogenase, which are involved in the biosynthesis of acetoin and 2,3-butanediol, compounds that have been documented to stimulate plant growth by promoting root elongation and enhancing nutrient uptake. Additionally, the presence of pyruvate decarboxylase (pdc) and alcohol dehydrogenase (adh) genes suggests the potential for ethanol production by P. dispersa PGPR-24. Ethanol, another VOC, has been associated with improved root growth and enhanced stress tolerance in plants, potentially acting as a signaling molecule in plant-microbe interactions. The production of VOCs by P. dispersa PGPR-24 represents a promising mechanism for promoting plant growth and resilience. VOCs like acetoin and 2,3-butanediol have been shown in previous studies to improve root architecture, increase nutrient acquisition, and activate defense pathways [50], underscoring the potential of PGPR-24 as a beneficial rhizobacterium.
The production of antimicrobial compounds is a critical trait of beneficial microbes, allowing them to suppress pathogenic organisms [51,52]. In PGPR strains, antimicrobial activity supports plant health, promote beneficial interactions in the rhizosphere and foster resilience against biotic stress. Pantoea dispersa PGPR-24 possesses several gene clusters associated with the synthesis of antimicrobial compounds. The presence of genes involved in the synthesis of VOCs such as acetoin and 2,3-butanediol, as discussed previously, suggests that P. dispersa PGPR-24 may enhance systemic resistance in plants against pathogens. Studies have shown that VOCs stimulate plant defense mechanisms, providing indirect protection against pathogens through induced systemic resistance (ISR) pathways [53]. Additionally, P. dispersa PGPR-24 encodes genes for the siderophore enterobactin, which plays a significant role in inhibiting the growth of competing microorganisms by sequestering iron, an essential nutrient for microbial survival [41]. By depriving pathogens, siderophores confer a competitive advantage to PGPR in the rhizosphere.
A significant antimicrobial trait of PGPR-24 is linked to carotenoid biosynthesis. The genome contains genes encoding enzymes in this pathway, including dxs, dxr, ispDEFGH, idi, and crtEBIY, supporting the synthesis of compounds like lycopene, which is known for its antioxidant and antimicrobial properties. Lycopene exhibits antimicrobial action primarily by disrupting the cell membranes of pathogenic bacteria and fungi, which results in membrane damage and inhibition of cell division, providing bactericidal and antifungal effects [54].
A phenazine biosynthesis protein, PhzF-like, was also detected alongside a LysR-family transcription regulator and an MFS transporter in PGPR-24 genome. Although a complete phenazine biosynthetic pathway was not confirmed, LysR-family regulator has been shown to positively influence phenazine biosynthesis in PGPR such as Pseudomonas chlororaphis G05 [55], while the MFS transporter is likely involved in phenazine transport [56].
Furthermore, PGPR-24 harbors a gene cluster linked to the biosynthesis of a stewartan-like exopolysaccharide. This cluster includes genes encoding enzymes such as undecaprenyl-phosphate galactose phosphotransferase, polysaccharide export proteins, and several glycosyltransferase family proteins. Exopolysaccharides contribute to biofilm formation, which can improve bacterial colonization of plant roots, provide a protective barrier against desiccation, and facilitate competition against pathogens. Exopolysaccharides are also well-recognized for their broad-range antimicrobial activity [5,57].
Collectively, these antimicrobial traits make P. dispersa PGPR-24 a promising candidate for biocontrol applications. Its ability to produce VOCs, siderophores, carotenoids, and potential phenazine compound, along with its exopolysaccharide biosynthesis capabilities, positions it as an effective biocontrol agent capable of suppressing pathogen growth, supporting plant resilience, and fostering a favorable environment for plant growth.
Table 4. Genetic systems supporting motility, chemotaxis, and root colonization in Pantoea dispersa PGPR-24. These traits enable effective rhizosphere navigation, interaction with root exudates, and stable plant root association, essential for plant growth-promotion.
Motility, chemotaxis, and root colonization are fundamental traits of PGPR that enable them to explore the soil environment, respond to root exudates, and establish beneficial plant-microbe interactions. The genome of P. dispersa PGPR-24 harbors a wide array of genes supporting these traits, including those involved in flagellar assembly, chemotaxis, and adhesion.
The flagellar system in PGPR-24, which provides bacterial motility, includes an extensive set of genes encoding structural and functional components. These include the fli and flg gene clusters, which encode proteins for the flagellar filament, hook, basal body, and motor apparatus, along with regulatory proteins (Table 5) [59,60]. Genes encoding motor proteins MotA and MotB, essential for torque generation [60], were also identified. Together, these genes enable bacterial motility, an essential trait for exploring soil microenvironments and localization to root surfaces.
The chemotaxis system, vital for sensing and responding to chemical gradients such as root exudates, is represented by genes encoding methyl-accepting chemotaxis proteins (MCPs) including tsr, tar, trg, and aer [61,62]. These are complemented by key chemotaxis signaling proteins encoded by cheA, cheB, cheR, cheW, cheY, cheV, and cheZ, enabling bacterial movement toward nutrient-rich zones or plant-derived signals [61,62]. Substrate-binding proteins (RbsB, MglB, DppA, MalE) further enhance chemotaxis by facilitating nutrient sensing and uptake [63].
Adhesion and biofilm formation are supported by genes for type IV pili (pilD, pilF, pilQ, pilT), which mediate twitching motility and root adhesion [64]. Regulatory proteins such as FlhD, FlhC, and FliA are involved in quorum sensing and biofilm development [65], ensuring effective plant-bacterium interactions. The coordinated action of these genes facilitate P. dispersa PGPR-24's ability to navigate soil, colonize plant roots, and interact effectively with host plants, making it a promising candidate for plant growth promotion.
The ability of PGPR to endure environmental stress is vital for their survival and effectiveness in the rhizosphere. P. dispersa PGPR-24 possesses a diverse repertoire of stress-response genes (Table 5), enabling it to adapt to conditions such as osmotic stress, nutrient starvation, oxidative stress, and periplasmic stress. These genes play a pivotal role in supporting the bacterium’s resilience and facilitating plant growth under challenging conditions. One critical mechanism by which P. dispersa PGPR-24 withstands stress is through detoxification processes. These processes are essential for neutralizing harmful compounds such as reactive oxygen species (ROS) and toxic metabolites, which often accumulate under stress [67]. The genome encodes glutathione biosynthesis enzymes, including glutamate-cysteine ligase (GshA) and glutathione synthetase (GshB), which are essential for glutathione production, a critical antioxidant that protects against oxidative damage. Additionally, genes encoding enzymes involved in the glutathione-dependent formaldehyde detoxification pathway were identified, including S-(hydroxymethyl)glutathione dehydrogenase and S-formylglutathione hydrolase. These enzymes neutralize formaldehyde, a toxic compound generated through metabolic processes or environmental exposure. This pathway is a conserved mechanism in bacteria [68], providing protection against formaldehyde and other reactive compounds, and contributing to cellular stability under stress.
To counter osmotic stress, PGPR-24 contains a set of genes dedicated to osmoregulation and osmoprotection. These include genes encoding betaine aldehyde dehydrogenase and choline dehydrogenase which enable the conversion of choline into betaine, a critical osmoprotectant that stabilizes proteins and cellular structures under hyperosmotic conditions [69]. The high-affinity choline uptake protein BetT further supports this pathway by importing choline, the precursor of betaine [70]. Studies in Escherichia coli have shown that the choline-to-betaine conversion pathway significantly contributes to osmoprotection [71]. The genome also features OsmY, an osmotically inducible protein, which has been characterized in E. coli as a key player in facilitating cell volume recovery and adaptation to severe osmotic stress [72]. Furthermore, the presence of the glucan biosynthesis protein C suggests a role in producing osmoregulated periplasmic glucans. These glucans are involved in stabilizing the bacterial cell envelope under osmotic stress, likely contributing to the bacterium's stability in high-salt or drought-prone soils.
Genome analysis also revealed periplasmic stress-response mechanisms in PGPR-24, mediated by several proteases and chaperones. Genes encoding the outer membrane stress sensor proteases DegS and DegQ, along with the HtrA protease/chaperone protein, are likely involved in maintaining protein quality control within the periplasm by facilitating the degradation of misfolded proteins under stress conditions [73]. Moreover, PGPR-24 genome contains phage shock protein (Psp) operon, including pspA, pspB, pspC, pspD, and the Psp operon transcriptional activator. The Psp system is a stress response mechanism that stabilizes the bacterial cytoplasmic membrane, particularly under conditions that cause envelope stress or changes in the extracellular environment, ensuring membrane integrity [74]. Additionally, the genome includes regulatory proteins RseA and RseB, which modulate the activity of the alternative sigma factor RpoE, a key player in managing extracytoplasmic stress [75].
Table 5. Stress adaptation mechanisms in Pantoea dispersa PGPR-24. Genes involved in enabling environmental stress tolerance under challenging conditions are summarized.
For carbon starvation, P. dispersa PGPR-24 contains genes associated with stringent starvation response, including stringent starvation protein A (SspA) and carbon starvation protein A (CstA). SspA, an RNA polymerase-associated protein, inhibits H-NS accumulation, a global repressor of stress defense systems. By derepressing these systems, SspA activates the expression of the sigma factor RpoS, enhancing defenses against acid stress and nutrient starvation [76,77]. CstA is likely involved in nutrient scavenging and plays a role in bacterial survival during carbon starvation. [78]. Other genes include rspB, which encodes a starvation-sensing protein that modulates gene expression associated with stress resistance and metabolic adaptation, and csrA, which encodes carbon storage regulator that coordinates gene expression in response to cellular stress and nutrient availability [79].
Additionally, the Hfl operon encodes HflC, HflK, and the RNA-binding protein Hfq, which support bacterial stress adaptation by modulating proteolytic activity and stabilizing small regulatory RNAs to influence gene expression during stress [80]. Universal stress proteins (USPs), including UspA, UspB, and UspE, were also found in PGPR-24 genome. USPs are multifunctional proteins that contribute to bacterial survival under diverse stress conditions, including heat, oxidative, and osmotic stresses [81,82].
The collective stress response capabilities of P. dispersa PGPR-24 underscore its adaptability in diverse soil environments, which is a critical aspect of its role as a PGPR. The coordinated expression of stress response systems, including detoxification pathways, envelope stress mechanisms, compatible solute synthesis, and general stress response proteins, not only enhances the bacterium’s survival in the rhizosphere but also contributes to plant growth promotion under challenging conditions.
This study provided comprehensive genomic insights into P. dispersa PGPR-24, uncovering its genetic framework for nutrient mobilization, phytohormone synthesis, stress adaptation, and biocontrol activities. These findings highlight its potential as a versatile plant growth-promoting rhizobacterium and a promising biofertilizer candidate for reducing the environmental impacts of chemical inputs in agriculture. By bridging the gap between genomic understanding and practical application, this study lays the groundwork for integrating P. dispersa PGPR-24 into sustainable farming systems. Future research should explore field-level validation of its efficacy, explore its interactions with diverse crops and soil types, and evaluate its effectiveness in biocontrol strategies against phytopathogens. Ultimately, this work establishes a genetic framework that can guide the development of innovative microbial solutions, contributing to global efforts in sustainable agriculture and environmental conservation.
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Funding
This study was supported by a grant from University of Chittagong via Research and Publication Cell to TJH.
Conflict of interest
The author has no conflicts of interest to declare.
Ethical approval
This article does not contain any experiments done with human participants or animals performed by any of the authors.
Acknowledgment
The author sincerely thanks his lab members and family for their support and encouragement.
Author contributions
TJH planned and designed the study, secured funding, handled administrative tasks, performed data analysis and interpretation, and wrote the manuscript.
This study explores the genome of Pantoea dispersa PGPR-24, a plant growth-promoting rhizobacterium (PGPR) isolated from the chrysanthemum rhizosphere. The research identifies key genetic pathways responsible for phosphate solubilization, iron acquisition via siderophores, sulfate and ammonia assimilation, and phytohormone production, highlighting its potential to enhance plant growth, soil health, and nutrient bioavailability. The genome also reveals genes supporting root colonization, stress adaptation, and the production of volatile organic compounds (VOCs) and antimicrobial compounds, demonstrating its adaptability and multifunctional benefits for sustainable agriculture. This work contributes to understanding the molecular mechanisms underlying plant-soil-microbe interactions, making it a valuable resource for developing biofertilizers, improving crop productivity, and promoting environmentally resilient farming practices.
