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Article

Insights from a Genome-Wide Study of Pantoea agglomerans UADEC20: A Promising Strain for Phosphate Solubilization and Exopolysaccharides Production

by
Edith Elizondo-Reyna
1,†,
Humberto Martínez-Montoya
2,†,
Yahaira Tamayo-Ordoñez
3,
María Antonia Cruz-Hernández
3,
Mauricio Carrillo-Tripp
4,
María Concepción Tamayo-Ordoñez
1,
Gerardo de Jesús Sosa-Santillán
1,
José Antonio Rodríguez-de la Garza
1,
Mario Hernández-Guzmán
5,
Virgilio Bocanegra-García
3,* and
Erika Acosta-Cruz
1,*
1
Departamento de Biotecnología, Facultad de Ciencias Químicas, Universidad Autónoma de Coahuila, Saltillo C.P. 25280, Mexico
2
Departamento de Microbiología, U.A.M. Reynosa Aztlán, Universidad Autónoma de Tamaulipas, Reynosa C.P. 88740, Mexico
3
Laboratorio Interacción Ambiente-Microorganismo, Centro de Biotecnología Genómica, Instituto Politécnico Nacional, Reynosa C.P. 88710, Mexico
4
Biomolecular Diversity Laboratory, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Monterrey, Vía del Conocimiento 201, PIIT, Apodaca C.P. 66600, Mexico
5
Departamento de Innovación Biomédica, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Ensenada C.P. 22860, Mexico
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Curr. Issues Mol. Biol. 2025, 47(1), 56; https://doi.org/10.3390/cimb47010056
Submission received: 13 December 2024 / Revised: 10 January 2025 / Accepted: 11 January 2025 / Published: 16 January 2025
(This article belongs to the Special Issue Bioinformatics Research in Bacterial Genomics, Metagenomics and Metatranscriptomics)
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Abstract

:
The genome sequence of Pantoea agglomerans UADEC20 is presented, which is a strain isolated from agricultural fields in northeast Mexico. The genome was assembled into 13 scaffolds, constituting a total chromosome size of 4.2 Mbp, with two of the scaffolds representing closed plasmids. The strain exhibits activity in phosphate solubilization and exopolysaccharide (EPS) production and secretion; therefore, we explored its biotechnological potential via its genome sequencing and annotation. Genomic analyses showed that a total of 57 and 58 coding sequences (CDSs) related to phosphate solubilization and EPS production were identified within its genome, in addition to a reduced number of CDSs related to drug resistance and phages. The comprehensive set of genes supporting phosphate solubilization, EPS synthesis, and secretion, along with its low virulence and antibiotic resistance levels, justify further research for its potential biotechnological application and possible use as a plant growth-promoting agent in the field. These findings suggest a unique genetic background in the P. agglomerans UADEC20 strain.

1. Introduction

Pantoea agglomerans is a Gram-negative, non-encapsulated, non-sporulated bacillus, belonging to the Enterobacteriaceae family, which is included in the class of Gammaproteobacteria that includes facultative anaerobic and fermentative Gram-negative bacteria. P. agglomerans is the most studied species and model of the genus Pantoea, which includes approximately 20 species [1,2]. The wide biotechnological applications of this species have led the scientific community to focus on studying microbial cultures associated with important agricultural crops in Mexico. Pantoea spp. are known to enhance plant growth by increasing the nitrogen supply, solubilizing ammonia and inorganic phosphate, and producing phytohormones [1,3,4]. P. agglomerans exhibits great adaptability to a wide range of hosts, diverse environmental conditions, and geographic and ecological distributions. This adaptability positions this bacterium as an opportunity for use as a biological control agent and a biofertilizer, with plant growth-promoting activity (PGPR) and potential use for soil bioremediation. The known mechanisms of PGPRs are diverse, e.g., nitrogen fixation, phytohormone production, and phosphate solubilization [5,6,7,8,9].
For all the above properties, the production of acid phosphatases and organic acids, particularly gluconic acid (GA), is vital for solubilizing insoluble or poorly soluble mineral phosphates [10]. Moreover, exopolysaccharide (EPS) production has an important role in plant growth and drought tolerance [11]. Previous studies have focused on the sequencing of the strains of Pantoea species to investigate the genes and enzymes involved in direct and indirect genetic mechanisms of plant growth-promoting bacteria [12,13,14]. When using PGPRs for growth enhancement, it is preferable to use locally isolated strains since they have evolved to adapt to the chemical, physical, and biological soil conditions, which enhances their biotechnological potential. The genomic data on local strains such as UADEC20 and its properties help to acquire a better understanding of the physiology, adaptability, and potential use of these strains.
The aim of this study was the genomic characterization of a strain that was isolated from the alfalfa (Medicago sativa) rhizosphere with technified irrigation in northeast Mexico. The analysis included the sequencing, assembly, annotation, and genomic, structural, and functional characterization of P. agglomerans UADEC20. This genome presents important properties such as phosphate solubilization and EPS production, which renders it a promising candidate for its usage in agriculture and, therefore, for enhancing its further biotechnological applications.

2. Materials and Methods

2.1. Whole-Genome Sequencing, Assembly, and Annotation

The strain P. agglomerans UADEC20 was isolated from the rhizosphere of alfalfa plants (Medicago sativa) cultivated in soil with a pH of 8.1 in the northeastern region of Mexico (25°1′40″ N, 100°38′28″ W). After several serial dilutions and plating on PVK medium at 28 ℃, it was identified as P. agglomerans through 16S rDNA sequencing and analysis with BLAST [15]. Total DNA extraction and purification were performed using the Wizard Genomic DNA Purification Kit (Promega Corporation, Madison, WI, USA) following the manufacturer’s recommendations. DNA integrity analysis to determine its feasibility for next-generation sequencing was performed on an Agilent 2200 TapeStation System from Agilent Technologies. Whole-genome sequencing was carried out by the company Omega Bioservices (Norcross, GA, USA) using the Illumina HiSeq™ sequencing platform (2 × 150 paired-end, PE).
The quality of the raw reads was verified with FastQC v0.11.9 [16]. Trim Galore v0.6.6 (https://www.bioinformatics.babraham.ac.uk/projects/trim_galore/ [accessed on 15 April 2024]) was used to trim reads with Q-scores < 30, remove adapters, and discard reads < 50 bp. Genome assembly was carried out using the QIAGEN CLC Genomics Workbench bioinformatics software v10.0 (QIAGEN, Aarhus, Denmark). Assembly quality was assessed further with QUAST v5.0.2 [17], and genome integrity assessment was performed using BUSCO v4.0.5 [18]. The BUSCO tool employs quantitative metrics to assess genome assembly, using evolutionary information [18].

2.2. Phylogenetic Analysis

A phylogenetic analysis of P. agglomerans was conducted by aligning the 16S rRNA sequence from our strain with selected Pantoea species and strains retrieved from the data mining of previously sequenced strains (NCBI). The alignment was finalized using MUSCLE v3.7 via the CIPRES platform [19]. The final alignment was cured to eliminate ambiguous sequences and gaps using Gblocks 0.91b [20]. Phylogenetic reconstruction was performed using a maximum likelihood approach via the IQ-TREE server [21] (http://www.iqtree.org/ [accessed on 10 September 2024]), calculating the evolution model with ModelFinder [22]. The taxa used in the phylogenetic reconstruction were the P. agglomerans strains FDAARGOS 1447 (GenBank acc. no. NZ_CP077368), UADEC20 (CP125809), NCTC9381 (OQ619142), DSM 3493 (KY013009), NBRC 102470 (NR_114111), 33.1 (CP0830.1), L15 (CP034148.1), UAE018 (CP048033.1), DAPP-PG734 (OW970315.1), J22C (CP162620.1), PSV1-7 (CP091189.1), AR1a (CP059089.1), Y03 (CP144368.1), and AB378 (CP113085.1). In addition to the P. agglomerans strains, the following were included: P. ananatis strains 1846 (GenBank acc. no. NR_02604) and LMG 2665 (NR_119362), P. allii strain LMG 24248 (NZ_NTMH00000000), P. stewartii subsp. indologenes strain CIP 104006 (NR_104928), P. pleuroti strain JZB 2120015 (NR_178694), P. vagans strain LMG 24199 (NZ_CP038855), and P. rwandensis strain ND04 (CP009454.1).

2.3. Comparative Genome Annotation

Genome annotation was performed with the Prokaryotic Rapid Genome Annotation algorithm (Prokka v1.13; https://github.com/tseemann/prokka, accessed on 10 September 2024) [23]. The resulting P. agglomerans UADEC20 scaffolds were rearranged and aligned using the Mauve Contig Mover algorithm in Mauve (v2.4.0) [24] and aligned against the complete genome of P. agglomerans FDAARGOS1447 as a reference (GenBank accession number: CP077366.1). The two plasmids detected in P. agglomerans UADEC20 were aligned with the respective plasmids from P. agglomerans FDAARGOS1447 using Mauve [24]. In addition to Mauve, an alignment of the P. agglomerans UADEC20 genome against other strains of P. agglomerans was conducted. A Venn diagram of the pan-genome and core-genome of P. agglomerans UADEC20 with other strains was made, using the MicroScope (MaGe) platform of Genoscope´s bioinformatics resources [25]. A pairwise genomic alignment of UADEC20 with 6 closely related P. agglomerans strain genomes was plotted using NCBI databases with BRIG 0.95 [26]. The same strains were compared for genomic features including genome size, gene number, number of tRNAs and rRNAs, and GC content.

2.4. Predictions of Functional Metabolic Pathways

The complete genome of P. agglomerans UADEC20 was subjected to metabolic pathway predictions using Gapseq v1.2 [27]. The reconstruction of metabolic networks consists of the systematic annotation of genomic metabolic genes that are then linked to the corresponding enzymatic reactions. This program was used to predict the routes and transporters with the Gapseq find script (-b 150), and the network project was created using the Gapseq draft (-u 200 -l 100 -a 1). For the transporter search, sequence data from the Transporter Classification Database (TCDB) [28] were used. The set of sequences was reduced to a subset of transporters involving metabolites known to be produced or consumed by microorganisms (dat/sub2pwy.csv, accessed on 10 September 2024). It was compared with relevant pathways available in the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway database (https://www.genome.jp/kegg/pathway.html, accessed on 10 September 2024).
The visualization of metabolic pathways’ prediction was achieved as follows [29,30]: the generic feature annotation file (GFF Prokka’s annotation output) was filtered to retain all genes with a KO identifier assigned. Then, the “Minimal set of Pathways” tool (MinPath v1.4) [31] was used to obtain a conservative estimation of pathways to visually represent them on the microbial metabolic map through the interactive pathway explorer web-based tool (iPath v3, https://pathways.embl.de/ (accessed 5 October 2024)).

2.5. Virulence Factors

The BLASTn method was applied to the Virulence Factor Database (VFDB) [32] using an identity limit of 80% and an e-value of <10−6 (BLAST) to find virulence factor genes present in the P. agglomerans UADEC20 genome.

2.6. Prophages and Drug Resistance Genes

In silico identification of antibiotic resistance genes using the CARD (Comprehensive Antibiotic Resistance Database) and the Resistance Gene Identifier (RGI) was performed [33]. To support rapid identification, annotation, and visualization of prophage sequences within the bacterial genomes and plasmids, the PHASTEST (PHAge Search Tool with Enhanced Sequence Translation) web server was used [34].

3. Results

3.1. Whole-Genome Sequencing, Assembly, and Annotation

A total of 20,949,701 paired-end raw reads were obtained in this study. After trimming and QC filtering, a total of 20,873,634 bp reads were retained and used for downstream analysis. The de novo assembly of the clean reads resulted in 15 scaffolds with an N50 value of 209,743 bp. The longest scaffold was 1,523,742 bp in length. Thirteen assembled scaffolds corresponded to the chromosome, while the other two were identified as plasmids, i.e., plasmid 1 (CP125810), with a length of 543,479 bp and G+C content of 53.6%, and plasmid 2 (CP125811), with a length of 174,380 bp and G+C content of 52.0%. P. agglomerans UADEC20 has a single circular chromosome of 4,203,428 bp in length, with a G+C content of 54.94% (Table 1). The evaluation of genome completeness using BUSCO revealed that P. agglomerans UADEC20 was 99.1% complete, suggesting that most of the recovered genes could be classified as complete and single copies (Figure S1).

3.2. Phylogenetic Analysis

A total of 21 sequences were used to assess the phylogenetic reconstruction of the 16S rRNA gene. After curating the sequences in Gblocks, 620 bases were retained, representing 29% of the original alignment with 2082 nucleotide positions. The cured alignment underwent a maximum likelihood analysis to estimate the phylogenetic relationships. It contained 184 constant sites (29.6%) and 286 parsimony informative sites. The best evolution model according to the Bayesian information criterion (BIC) (5640.8911) was K2P+G4. The consensus tree shows two main clades when rooted to P. agglomerans FDARGOS 1447 (FIG) and suggests a close relationship with P. agglomerans strains UAEU18, AR1a, Y03, AB378, and ND04 in a cluster composed only of P. agglomerans strains (Figure 1).

3.3. Comparative Genome Annotation

Annotation of the P. agglomerans UADEC20 chromosome with Prokka [23] revealed that a total of 4511 genes were predicted: 3836 coding sequences (CDSs), 1 tmRNA, 22 rRNA operons, 99 tRNA genes, and 716 hypothetical proteins. Functional annotation allowed the identification of 1617 enzymes (EC number of annotated genes) that were visualized through the KEGG’s microbial metabolism map (Figure S2). The P. agglomerans UADEC20 genome was compared with different species and strains, with the P. agglomerans FDAARGOS 1447 strain (GenBank accession no. CP077366.1) being the tree root. The similarity can be observed in the results of the analysis conducted with the progressive software Mauve, which builds multiple genomic alignments in the presence of evolutionary events such as rearrangements and inversions. The chromosomal alignment between the two strains revealed the presence of 12 highly homologous blocks. However, a region in the chromosomal scaffold between scaffolds 3, 8, and 10 exhibits an inverse orientation, indicating differences in their synteny ratios (Figure 2). Furthermore, strain UADEC20 possesses a total of 49 unique coding sequences (CDSs) that are absent in strain FDAARGOS 1447, as outlined in (Table S1).
In the annotation of the plasmids, through an analysis with Prokka [23], a plasmid 1 (GenBank accession no. CP125810), with a size of 543,479 bp, containing 517 putative coding sequences, and a plasmid 2 (GenBank accession no. CP125811), with a size of 174,380 bp, containing 162 putative coding sequences, were predicted. The two plasmids contained in P. agglomerans UADEC20 were compared with the two plasmids of the P. agglomerans FDAARGOS 144 strain using progressiveMauve (v2.4.0), presenting two collinear blocks for each plasmid (Figure 3 and Figure 4).
In an overall analysis, the pan-genome is made up of 22,672 genes belonging to 6533 families, the core-genome is made up of 17,306 genes belonging to 3426 families, and the variable-genome is made up of 5366 genes belonging to 3107 families. Genes overlapping by at least 80% in length and having 80% similarity were considered orthologs (Figure 5).
Additionally, the genomic features of P. agglomerans strain UADEC20 and six closely related genomes were compared, such as sequence similarity, GC content distribution, and gene number, including tRNA and rRNA (Figure 6, Table 2). The genome size and total gene number of UADEC20 are similar to 299R but slightly smaller than those of FDAARGOS1447 and IG1, while 190, Tx10, and P5 appear to have a larger genome size of ~4.85 Mb.

3.4. Predictions of Functional Metabolic Pathways

3.4.1. Predictions of Metabolic Pathways Related to Phosphate Solubilization

After annotation of the chromosome of P. agglomerans UADEC20, 57 CDSs related to phosphate solubilization were identified using tools such as Prokka [23] and the UniProt database (https://www.uniprot.org/, accessed on 10 September 2024). These identified CDS were completely found within the chromosome (Table 3).
In the analysis of the predictions of the metabolic pathways obtained from the P. agglomerans UADEC20 genome related to the phosphate solubilization mechanism (Figure S2), using the Gapseq program (KEGG database), the following were found: D-gluconate degradation (GLUCONSUPER-PWY), glucose and glucose-1-phosphate degradation (GLUCOSE1PMETAB-PWY), sedoheptulose bisphosphate bypass (PWY0-1517), glycerol-3-phosphate to cytochrome bo oxidase electron transfer (PWY0-1561), succinate to cytochrome bd oxidase electron transfer (PWY0-1353), glycerol-3-phosphate shuttle (PWY-6118), phosphate acquisition (PWY-6348), and phosphate ABC transporter (PI-ABC-TRANS). In relation to the inference of transporters in P. agglomerans UADEC20, glycerol-3-phosphate, phosphate, and gluconate were obtained, which are related to the phosphate solubilization pathway.

3.4.2. Enzymes Involved in the Biosynthesis, Transport, and Secretion of Exopolysaccharides (EPSs) from the P. agglomerans Genome

We explored the identification of enzymes involved in EPS biosynthesis, transport, and secretion in the P. agglomerans UADEC20 genome (Table 4). Twenty-three CDSs of enzymes involved in exopolysaccharide biosynthesis were identified, particularly in the subcategory of central carbohydrate metabolism/pentose phosphate pathway and extracellular polysaccharide synthesis. The synthesis of polysaccharides requires the biosynthesis of precursor molecules from the central metabolism of carbohydrates: in this first group, we found transketolase (EC 2.2.1.1), ribose-phosphate pyrophosphokinase (EC 2.7.6.1), ribulose-phosphate 3-epimerase (EC 5.1.3.1), glucose-6-phosphate 1-dehydrogenase (EC 1.1.1.49), 6-phosphogluconate dehydrogenase, decarboxylating enzyme (EC 1.1.1.44), 6-phosphogluconolactonase (EC 3.1.1.31), xylulose-5-phosphate phosphoketolase (EC 4.1.2.9), fructose-6-phosphate phosphoketolase (EC 4.1.2.22), and transaldolase (EC 2.2.1.2). In the extracellular polysaccharide synthesis group, we found dTDP-4-dehydrorhamnose reductase (EC 1.1.1.133), dTDP-glucose 4,6-dehydratase (EC 4.2.1.46), dTDP-4-dehydrorhamnose 3,5-epimerase (EC 5.1.3.13), glucose-1-phosphate thymidylyltransferase (EC 2.7.7.24), UDP-glucose 4-epimerase (EC 5.1.3.2), dTDP-4-dehydrorhamnose reductase (EC 1.1.1.133), dTDP-glucose 4,6-dehydratase (EC 4.2.1.46), dTDP-4-dehydrorhamnose 3,5-epimerase (EC 5.1.3.13), and glucose-1-phosphate thymidylyltransferase (EC 2.7.7.24). For the next phase of EPS biosynthesis, glycosyltransfers (GTs) play an important role in transferring the sugar nucleotides UDP-Glc/UDP-Gal/UDP-GlA to a repeating unit linked to a lipid transporter associated with the inner membrane. Within the category, D-inositol 3-phosphate glycosyltransferase, putative glycosyltransferase EpsJ, putative glycosyltransferase EpsJ, peptidoglycan glycosyltransferase MrdB, and putative peptidoglycan glycosyltransferase FtsW were identified.
In the P. agglomerans genome, we found 30 enzymes that participate in the Wzx-/Wzy-dependent pathway and the ABC transporter-dependent pathway. Within the Wzy-/Wzx-dependent pathway, in the genome, we found the presence of the wzxC_1 and 2 gene that encodes the Wzx flippase, Wzy polymerase (wzyE gene), pyrrolidone-carboxylate peptidase (pcp gene), and tyrosine-protein kinase wzc (wzc gene) genes; all of these are important elements for the production and transport of complex polysaccharides. Likewise, enzymes involved in the set of liposaccharides (LPSs) were identified: lipopolysaccharide assembly protein A and B, lipopolysaccharide heptosyltransferase 1, core lipopolysaccharide biosynthesis protein RfaG, ACE polysaccharide chain length modulation protein, core lipopolysaccharide heptosyltransferase RfaQ, lipopolysaccharide export system ATP-binding protein LptB, lipopolysaccharide export system protein LptA and LptC, and permease protein LptF and LptG.
The P. agglomerans UADEC20 strain possesses 12 genes encoding ATP-binding cassette ABC transporters, which are a family of integral membrane proteins for the ATP-dependent transport of various substrates, including putative phospholipid ABC transporter-binding MlaD, MlaB, YadG, and YheS proteins; inner membrane amino acid permease ABC transporter protein YhdY; inner membrane permease ABC transporter proteins YejE, YejB, YjfF, YtfT, and YdcV; periplasmic junctional ABC transporter protein YtfQ; and putative phospholipid ABC transporter protein MlaE. Within the EPS secretion system that this strain may contain, we find genes related to the membrane fusion protein of the type I secretion system PrsE (prsE_1,2) and the protein of the type II F and E secretion system (epsF and gspE).

3.5. Virulence Genes

Using BLAST searches against the VFDB database [32] and genome annotation, a total of 37 putative virulence factors were predicted in P. agglomerans UADEC20 (Table S2). The virulence factors identified are classified mainly in motility; however, tagH is identified as a gene associated with the type VI secretion system (T6SS) and ompA is identified in adhesion. Overall, the strain seems to have low virulence capability.

3.6. Prophages and Drug Resistance Genes

In the analysis of antimicrobial resistance-related elements, only sequences associated with efflux pumps and genes with point mutations linked to resistance were detected. This indicates the presence of limited intrinsic resistance mechanisms, and the absence of mechanisms acquired through horizontal gene transfer (Table S3).
The phage analysis identified sequences associated with prophages containing stress response proteins, replication mechanism proteins such as helicases, and phage lysis modules. However, no intact phages were found in the genome (Table S4).

4. Discussion

4.1. Phylogenetic Analysis and Comparative Genomics

The phylogenetic tree based on the 16S rRNA gene positioned FDAARGOS 1447 at the root (Figure 1). The comparative analysis with the FDAARGOS 1447 strain using Mauve (Figure 2) revealed substantial genetic overlap. The Venn diagram of the core genome showed that these strains share a total of 3875 genes (Figure 5). Notably, UADEC20 has 49 CDSs with critical functions, such as parA, virB, intA_3, hybG, and hemS; the hycADEG CDS of the hyc operon; and the hypABDEF CDS of the hyp operon (Table S1); these CDSs are important in anaerobic metabolism, providing the strain with the biochemical capabilities to thrive in the environment. CDS virB has been characterized as a key regulator of genes located on the high-virulence plasmid (pINV) in the bacterial pathogen Shigella flexneri; it is unrelated to other transcriptional regulators and belongs to a family of proteins that function primarily in plasmid and chromosomes [35]. CDS parA, known to be essential for plasmid cleavage, ensures the proper distribution of newly replicated plasmids to daughter cells during cell division [36]. The intA_3 CDS is also present in several rhizobia species, possibly with different specificities; it is known that the intA_3 system can be combined with other site-specific systems with different specificities to facilitate bacterial genome engineering [37]. It is known that the hemS CDS is also found in the Bartonella genome and contains a gene-encoding hemS that may be involved in the release of iron from heme [38]. The hycADEG operon encodes the products necessary for the formation of phosphate hydrogenase (FHL) present in UADEC20. This operon has also been reported in Escherichia coli, and hypABCDEF is found in many bacteria and archaea [39] (particularly hypA and hypB), which are involved in the insertion of the nickel atom into the large subunit precursor [40,41,42]. Coding sequences (CDSs) such as hycADGE have also been reported in Enterobacter species in the production of hydrogen, due to the enzyme hydrogenase 3 (encoded by hycABCDEFGHI); it presents important activities of hydrogen uptake and synthesis [43]. In E. coli, there is substantial evidence indicating that hydrogenase 3 activity is essential to produce hydrogen [44]; it has also been found to increase hydrogen yield in E. aerogenes hycE or hycG, which must be overexpressed in this species [45].

4.2. Metabolic Pathways Related to Phosphate Solubilization

We identified 57 coding sequences (CDSs) involved in phosphate solubilization (hereafter PS) metabolism within the chromosome of the UADEC20 strain (Table 3). This number surpasses the 10–40 CDSs reported in some bacteria of the same species [23,46,47]. The presence of intracellular enzymes involved in other metabolic processes, such as the pentose phosphate pathway, was detected. Additionally, CDSs corresponding to glucosyltransferases, which catalyze glucose residue transfer, crucial for polysaccharide synthesis, were annotated. For instance, UDP-glucose/alpha-D-galactose-1-phosphate uridylyltransferase catalyzes a key step in galactose metabolism. These enzymes are located in the periplasmic membrane, facilitating glucose residue accumulation for polysaccharide synthesis [48,49,50].
PS-associated genes include the pqq and gdh genes [51,52], which were also identified; they are critical for glucuronic acid production and gluconic acid secretion, respectively [53]. It is known that even if a strain has enzymes such as glucose dehydrogenase without the pqq genes, bacteria are not able to use it [54] (Table 3). These processes solubilize insoluble phosphates, with the pqqBCDE genes encoding enzymes essential for pyrroloquinoline quinone (PQQ) biosynthesis [51,52]. The strain also contains 17 phn genes related to phosphonate transport and degradation, compared to 13 in the P5 strain [55]. Additionally, the high-affinity phosphate transport system in UADEC20 includes eight pst operon genes, surpassing the four found in P5 [55] (Shariati et al. 2017). The gcd genes, involved in gluconic acid biosynthesis, further support UADEC20’s enhanced phosphate solubilization capabilities [56,57].
In the analysis of the predictions of the metabolic pathways obtained from the P. agglomerans UADEC20 genome, related to the phosphate solubilization mechanism, the following were found: D-gluconate degradation (GLUCONSUPER-PWY), glucose and glucose-1-phosphate degradation (GLUCOSE1PMETAB-PWY), sedoheptulose bisphosphate bypass (PWY0-1517), glycerol-3-phosphate to cytochrome bo oxidase electron transfer (PWY0-1561), succinate to cytochrome bd oxidase electron transfer (PWY0-1353), glycerol-3-phosphate shuttle (PWY-6118), phosphate acquisition (PWY-6348), and phosphate ABC transporter (PI-ABC-TRANS). In relation to the succinate-to-cytochrome bd oxidase electron transfer (PWY0-1353) predicted in the UADEC20 strain, Korshunov et al. [58] found that the E. coli bacterium can completely block primary cytochrome bd oxidase in the presence of low micromolar concentrations of hydrogen sulfide; it is known that this bacterium requires respiration for growth, and in such circumstances, respiration is maintained by shunting electrons to cytochrome bd oxidase; the authors conclude that the sulfur resistance of this enzyme may be critical to its role in bacteria.

4.3. Biosynthesis, Transport, and Secretion of Exopolysaccharides (EPSs)

The ability to synthesize and secrete polysaccharides is a notable property of PGPRs such as Pantoea [59]. These EPSs contribute to soil stability, water retention, and plant stress tolerance. The production of EPSs aids in protecting roots against phytopathogens and improving soil aeration and structure [59,60]. As mentioned earlier, the strain UADEC20 contains enzymes involved in the pentose phosphate pathway, which leads to polysaccharide synthesis (Table 4) [48,49,50]. These EPSs also contribute to maintaining the water film required for photosynthetic activity and plant growth, improving the process of soil aeration and infiltration, and covering and protecting roots against attack by phytopathogens. Under salt stress conditions, EPSs chelate cations available in the root zone, thus contributing to reducing the salinity of the rhizosphere. Bacterial EPSs under water stress conditions in the soil are responsible for limiting the desiccation of the medium. In the case of floods or heavy rain, EPSs help avoid the dispersion of clayey soils [60].
The Wzy-/Wzx-dependent pathway and ABC transporter systems for EPS transport are present in UADEC20. In the Wzy-/Wzx-dependent pathway, C55-anchored repeat units on the inner membrane are polymerized in the periplasm and exported to the cell surface [61,62,63]. Similarly, the ABC transporter system facilitates EPS export through a coordinated mechanism involving glycosyltransferases and transport proteins [64,65]. Enzymes for dTDP-rhamnose synthesis, a precursor for rhamnose found in lipopolysaccharides, capsular polysaccharides, and EPSs, were also identified [66].
In Gram-negative bacteria, six protein secretion systems have been identified to date, designated types I to VI, which differ greatly in composition and mechanism of action [67]. Analysis of the P. agglomerans genome indicates that it possesses type I and II EPS secretion systems [68]. The type I secretion system (T1SS) is responsible for transporting different molecules, mainly ions, carbohydrates, unfolded proteins, and RTX-type toxins [69,70,71]. The system is composed of an ABC transporter located on the inner membrane, a periplasmic tunneling protein, and a porin-like protein located on the outer membrane [71,72].
The type II secretion system (T2SS) depends on the Sec and Tat systems. These systems initiate secretion into the periplasmic space, which lies between the inner and outer membranes. Once in the periplasmic space, the transported molecule is secreted by the external part of the system that forms an exit channel. This external component is accompanied by another internal protein (chaperone) that ensures its stability by preventing it from degrading while it performs its job. The secreted molecules are mainly enzymes involved in degrading other membranes, so this system enhances bacterial competitiveness and pathogenesis capabilities [73,74,75,76].
In this study, we located enzymes involved in the synthesis of the capsule and extracellular polysaccharides, such as dTDP-4-dehydrorhamnose reductase. Further studies are needed to determine whether these LPSs can exhibit a bioactive effect. Polysaccharide synthesis and excretion properties are important for agricultural applications since these compounds are related to important phenomena such as biofilm formation in the rhizosphere, water and nutrient retention, osmotic stress protection, and better soil structure, and they also act as pathogen biocontrol effectors since their presence can activate defense mechanisms in the plants and protect the rhizome surface from pathogen colonization.

4.4. Virulence Genes and Antibiotic Resistance

The genomic analysis of UADEC20 showed the presence of 37 virulence genes. However, only a limited number of gene families associated with virulence factors were detected, e.g., those related to the type VI secretion system (T6SS), adhesion, and motility (Table S2). Among the identified virulence genes, the tagH gene encodes proteins that contain the lprI lysozyme inhibitor domain [77], and the ompA gene codes for a membrane protein that contributes to the adhesion and evasion of host defenses [78]. Motility-associated genes play roles in biofilm formation, adhesion, and virulence factor secretion [79]. This indicates that UADEC20 exhibits very low virulence potential towards other organisms.
Similarly, only a few genes associated with intrinsic antibiotic resistance were identified, suggesting that the strain has limited resistance and virtually no capacity for transferring resistance genes to other strains. Despite these virulence-related genes, UADEC20 has low overall virulence potential and limited antibiotic resistance, justifying the further study of the strain to enhance its suitability for agricultural applications.

5. Conclusions

The strain of Pantoea agglomerans UADEC20 was identified and isolated from the rhizosphere of alfalfa (Medicago sativa) cultivated in northeastern Mexico. Key genes were identified in this study, which code for the biosynthesis, transport, and secretion of exopolysaccharides, as well as for phosphate solubilization, resistance to abiotic stresses (such as water scarcity and drought), and effective rhizosphere establishment. These features suggest significant potential for agricultural applications in Mexico. Notably, phylogenetic analyses and pangenome comparisons revealed that this strain exhibits a distinct evolutionary lineage compared to other species within the genus Pantoea.
Genomic analysis of UADEC20 indicated a comprehensive set of genes supporting phosphate solubilization, EPS synthesis, and secretion. Its low virulence and antibiotic resistance levels further justify its potential as a plant growth-promoting agent. Nonetheless, functional assays are necessary to validate its agricultural utility and determine its efficacy under field conditions. This finding highlights the potential biotechnological benefits associated with the unique genetic background of this strain.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/cimb47010056/s1.

Author Contributions

E.E.-R. contributed to the methodology, software, validation, formal analysis, investigation, data curation, writing—original draft, and writing—review and editing; H.M.-M. contributed to the methodology, software, validation, formal analysis, investigation, data curation, and writing—review and editing; Y.T.-O. contributed to the methodology, validation, formal analysis, data curation, and writing—original draft; M.A.C.-H. contributed to the methodology, validation, and writing—original draft; M.C.-T. contributed to the software, resources, writing—original draft, writing—review and editing, and supervision; M.C.T.-O. contributed to the methodology, validation, and writing—original draft; G.d.J.S.-S. contributed in methodology, validation, and resources; J.A.R.-d.l.G. contributed to the methodology and validation; M.H.-G. contributed to the methodology, software, validation, writing—original draft, and writing—review and editing; V.B.-G. contributed to the formal analysis, investigation, resources, writing—original draft, review and editing, visualization, and supervision; and E.A.-C. designed this study and contributed to its conceptualization, methodology, validation, formal analysis, investigation, resources, writing—review and editing, visualization, supervision, project administration, and funding acquisition. All these authors made substantial contributions to the final manuscript and approved this submission. All authors are aware of the order of authorship and that no further change in authorship will be made after submission. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by FONCYT COECYT—Gobierno del Estado de Coahuila. Grant number COAH-2017-C12-C99.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Nucleotide sequence accession numbers. This genome sequence was deposited in GenBank under the accession numbers CP125809, CP125810, and CP125811 with BioProject number PRJNA955887.

Acknowledgments

We would like to thank Antonio Verástegui-Hernández, Arturo Reyes-Solís, Alexia Banda-Gutiérrez, Luis Ignacio Hernández-González, and Kimberly González-Valenzuela for technical support for this project. H.H.M., Y.T.O., M.A.C.H., M.C.T., M.C.T.O., G.J.S.S., J.A.R.G., M.H.G., V.B.G. and E.A.C. acknowledge to “Sistema Nacional de Investigadores” from the “Consejo Nacional de Humanidades, Ciencia y Tecnología” (SNII-CONAHCYT, México).

Conflicts of Interest

The authors declare no conflicts of interest.

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Cimb 47 00056 g001
Figure 1. Consensus tree showing the phylogenetic relationship of 21 strains from Pantoea. The final tree was constructed from 2000 bootstrap trees. Pantoea agglomerans UADEC20 is located in Cluster II.
Figure 1. Consensus tree showing the phylogenetic relationship of 21 strains from Pantoea. The final tree was constructed from 2000 bootstrap trees. Pantoea agglomerans UADEC20 is located in Cluster II.
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Cimb 47 00056 g002
Figure 2. Genome alignments showing synteny blocks of P. agglomerans UADEC20 (top) and P. agglomerans FDAARGOS 1447 (bottom) in Mauve 2.4.0 software. Each genome is presented horizontally with the homologous segment outlined as colored rectangles. Blocks of the same color represent a locally collinear block (LCB) or homologous region shared between the two genomes. The rearrangement of the genomic regions between the two genomes was observed in terms of collinearity; the regions inverted relative to FDAARGOS 1447 are located on the negative strand indicated by the genomic position below the black horizontal center line in the Mauve alignment. Colors indicates similar nucleotide regions between the two chromosomes.
Figure 2. Genome alignments showing synteny blocks of P. agglomerans UADEC20 (top) and P. agglomerans FDAARGOS 1447 (bottom) in Mauve 2.4.0 software. Each genome is presented horizontally with the homologous segment outlined as colored rectangles. Blocks of the same color represent a locally collinear block (LCB) or homologous region shared between the two genomes. The rearrangement of the genomic regions between the two genomes was observed in terms of collinearity; the regions inverted relative to FDAARGOS 1447 are located on the negative strand indicated by the genomic position below the black horizontal center line in the Mauve alignment. Colors indicates similar nucleotide regions between the two chromosomes.
Cimb 47 00056 g002
Cimb 47 00056 g003
Figure 3. Plasmid 1 of P. agglomerans UADEC20 (top) and plasmid 1 of P. agglomerans FDAARGOS 1447 (bottom) compared using Mauve 2.4.0 software. Colors indicates similar nucleotide regions between the two chromosomes.
Figure 3. Plasmid 1 of P. agglomerans UADEC20 (top) and plasmid 1 of P. agglomerans FDAARGOS 1447 (bottom) compared using Mauve 2.4.0 software. Colors indicates similar nucleotide regions between the two chromosomes.
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Figure 4. Plasmid 2 of P. agglomerans UADEC20 (top) and plasmid 2 of P. agglomerans FDAARGOS 1447 (bottom) compared using Mauve 2.4.0 software. Colors indicates similar nucleotide regions between the two chromosomes.
Figure 4. Plasmid 2 of P. agglomerans UADEC20 (top) and plasmid 2 of P. agglomerans FDAARGOS 1447 (bottom) compared using Mauve 2.4.0 software. Colors indicates similar nucleotide regions between the two chromosomes.
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Figure 5. Plot of the core-/pan-genome and Venn diagram for the core-genome and strain-specific CDSs of the P. agglomerans strains. The outer circles represent the pan-genomes of the different strains and show the conserved (core) and non-conserved (flexible) CDSs for each group. Genes overlapping by at least 80% in length and having 80% similarity were considered orthologs.
Figure 5. Plot of the core-/pan-genome and Venn diagram for the core-genome and strain-specific CDSs of the P. agglomerans strains. The outer circles represent the pan-genomes of the different strains and show the conserved (core) and non-conserved (flexible) CDSs for each group. Genes overlapping by at least 80% in length and having 80% similarity were considered orthologs.
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Figure 6. Genome comparisons of other P. agglomerans strains against the P. agglomerans UADEC20 draft genome. The black inner circle represents the complete genome of the reference strain UADEC20, and the shade of each color shows the similarities between each one of the strains and that of UADEC20.
Figure 6. Genome comparisons of other P. agglomerans strains against the P. agglomerans UADEC20 draft genome. The black inner circle represents the complete genome of the reference strain UADEC20, and the shade of each color shows the similarities between each one of the strains and that of UADEC20.
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Table 1. Summary of P. agglomerans UADEC20 genome.
Table 1. Summary of P. agglomerans UADEC20 genome.
RepliconNo. of Illumina ReadsReads After Clipping
QC > 30%		Length Size (bp)No. of ScaffoldsScaffolds N50 (bp)Maximum Length of ScaffoldsG+C Content (%)
Chromosome20,949,70120,873,6344,203,42813209,7431,523,74254.94
Plasmid 1--543,4791--53.6
Plasmid 2--174,3801--52.0
%Q30 = The percentage of bases with a quality score of 30 or higher; %GC = percent content of Guanines and Cytosines.
Table 2. The genomes of Pantoea agglomerans strains in comparative genome analysis.
Table 2. The genomes of Pantoea agglomerans strains in comparative genome analysis.
OrganismGenome Size (Mb)GC%No. of rRNANo. of tRNAScaffoldsNo. of GenesNo. of ProteinsGenBank
Accession No.
P. agglomerans UADEC204.2034354.922991345113843GCA_046352745.1
P. agglomerans 299R4.5814854.3276310942674157GCA_000330765.1
P. agglomerans FDAARGOS 14473.9996955.5569343614204GCF_019048385.1
P. agglomerans Tx104.8569955.1481422246274500GCA_000475055.1
P. agglomerans IG14.8295855.02631844434341GCA_000241285.2
P. agglomerans 1905.0025755.12477548784778GCA_000731125.1
P. agglomerans P55.1672655.476315047454674GCA_002157425.2
Table 3. CDSs related to phosphate solubilization found in the annotated genome of P. agglomerans UADEC20. Functions were validated on Uniprot (https://www.uniprot.org/ [4 April 2024]).
Table 3. CDSs related to phosphate solubilization found in the annotated genome of P. agglomerans UADEC20. Functions were validated on Uniprot (https://www.uniprot.org/ [4 April 2024]).
No.GeneProteinLocus Tag
1appAOligopeptide-binding protein AppANDPIJCJM_00337
2gcd_1Quinoprotein glucose dehydrogenaseNDPIJCJM_01104
3gcd_2Quinoprotein glucose dehydrogenaseNDPIJCJM_02657
4gdhlGlucose dehydrogenase, PQQ-dependent (EC 1.1.5.2)NDPIJCJM_02770
5glkGlucokinaseNDPIJCJM_00198
6gntKThermoresistant gluconokinaseNDPIJCJM_02222
7gntRHTH-type transcriptional regulator GntRNDPIJCJM_02223
8phnCPhosphate-import ATP-binding protein PhnCNDPIJCJM_00558
9phnDPhosphate-import protein PhnDNDPIJCJM_00559
10phnE_1Phosphate-import permease protein PhnENDPIJCJM_00560
11phnE_2Phosphate-import permease protein PhnENDPIJCJM_00561
12phnFPutative transcriptional regulator PhnFNDPIJCJM_00548
13phnGAlpha-D-ribose 1-methylphosphonate 5-triphosphate synthase subunit PhnG (EC 2.7.8.37)NDPIJCJM_00549
14phnHAlpha-D-ribose 1-methylphosphonate 5-triphosphate synthase subunit PhnH (EC 2.7.8.37)NDPIJCJM_00550
15phnIAlpha-D-ribose 1-methylphosphonate 5-triphosphate synthase subunit PhnI (EC 2.7.8.37)NDPIJCJM_00551
16phnJAlpha-D-ribose 1-methylphosphonate 5-phosphate C-P lyaseNDPIJCJM_00552
17phnKPutative phosphonates utilization ATP-binding protein PhnKNDPIJCJM_00553
18phnLAlpha-D-ribose 1-methylphosphonate 5-triphosphate synthase subunit PhnLNDPIJCJM_00554
19phnMAlpha-D-ribose 1-methylphosphonate 5-triphosphate diphosphataseNDPIJCJM_00555
20phnNRibose 1,5-bisphosphate phosphokinase PhnNNDPIJCJM_00556
21phnOAminoalkylphosphonate N-acetyltransferaseNDPIJCJM_01860
22phnPPhosphoribosyl 1,2-cyclic phosphate phosphodiesteraseNDPIJCJM_00557
23phnVPutative 2-aminoethylphosphonate transport system permease protein PhnVNDPIJCJM_02365
24phoBPhosphate regulon transcriptional regulatory protein PhoB (SphR)NDPIJCJM_02028
25phoHPhosphate starvation-inducible protein PhoH, predicted ATPaseNDPIJCJM_00650
26phoPTranscriptional regulatory protein PhoPNDPIJCJM_03210
27phoRPhosphate regulon sensor protein PhoR (SphS) (EC 2.7.13.3)NDPIJCJM_02027
28phoUPhosphate-specific transport system accessory protein PhoUNDPIJCJM_02471
29phyPhytaseNDPIJCJM_00083
30pitA_1Low-affinity inorganic phosphate transporter 1NDPIJCJM_01727
31pitA_2Low-affinity inorganic phosphate transporter 1NDPIJCJM_02277
32ppaInorganic pyrophosphataseNDPIJCJM_03544
33ppkT6SS Serine/threonine protein kinase (EC 2.7.11.1) PpkANDPIJCJM_00117
34ppxExopolyphosphataseNDPIJCJM_00116
35pqqBCoenzyme PQQ synthesis protein BNDPIJCJM_01165
36pqqCPyrroloquinoline-quinone synthaseNDPIJCJM_01164
37pqqDCoenzyme PQQ synthesis protein DNDPIJCJM_01163
38pqqECoenzyme PQQ synthesis protein ENDPIJCJM_01166
39psiFPhosphate starvation-inducible protein PsiFNDPIJCJM_02051
40pstA_1Phosphate transport system permease protein PstANDPIJCJM_00119
41pstA_2Phosphate transport system permease protein PstANDPIJCJM_00119
42pstBPhosphate import ATP-binding protein PstBNDPIJCJM_02470
43pstCPhosphate transport system permease protein PstCNDPIJCJM_02468
44pstS_1Phosphate-binding protein PstSNDPIJCJM_02026
45pstS_2Phosphate-binding protein PstSNDPIJCJM_02026
46ugpAsn-glycerol-3-phosphate transport system permease protein UgpANDPIJCJM_02231
47ugpBsn-glycerol-3-phosphate-binding periplasmic protein UgpBNDPIJCJM_02232
48ugpCsn-glycerol-3-phosphate import ATP-binding protein UgpCNDPIJCJM_02229
49ugpQGlycerophosphodiester phosphodiesterase, cytoplasmicNDPIJCJM_02228
50ushAProtein UshANDPIJCJM_01942
51zwfGlucose-6-phosphate 1-dehydrogenaseNDPIJCJM_00714
52ptxS2-ketogluconate utilization repressor ptxSNDPIJCJM_02300
53glpTGlycerol-3-phosphate transporterNDPIJCJM_02625
54uhpTHexose-6- phosphate:phosphate antiporterNDPIJCJM_02853
55phnRPutative transcriptional regulator of 2-aminoethylphosphonate degradation operonsNDPIJCJM_02369
56pstC1Phosphate transport system
permease protein PstC 1		NDPIJCJM_00118
57pstB3Phosphate import ATP-binding protein PstB 3NDPIJCJM_00120
Table 4. Genes and proteins related to the biosynthesis, transport, and secretion of exopolysaccharides identified in the genome of P. agglomerans UADEC20.
Table 4. Genes and proteins related to the biosynthesis, transport, and secretion of exopolysaccharides identified in the genome of P. agglomerans UADEC20.
No.GeneProteinLocus Tag
Biosynthesis of exopolysaccharides
1tktBTransketolase 2NDPIJCJM_00157
2cbbTTransketolase 2NDPIJCJM_03242
3tktATransketolase 1NDPIJCJM_03750
4prsRibose-phosphate pyrophosphokinaseNDPIJCJM_01374
5rpeRibulose-phosphate 3-epimeraseNDPIJCJM_02168
6zwfGlucose-6-phosphate 1-dehydrogenaseNDPIJCJM_00714
7gnd6-phosphogluconate dehydrogenase, decarboxylatingNDPIJCJM_00429
8pgl_16-phosphogluconolactonaseNDPIJCJM_00577
9talTransaldolaseNDPIJCJM_00158
10rfbDdTDP-4-dehydrorhamnose reductaseNDPIJCJM_00418
11rffGdTDP-glucose 4,6-dehydratase 2NDPIJCJM_02591
12rfbBdTDP-glucose 4,6-dehydrataseNDPIJCJM_00417
13rfbCdTDP-4-dehydrorhamnose 3,5-epimeraseNDPIJCJM_00420
14rffHGlucose-1-phosphate thymidylyltransferase NDPIJCJM_02592
15galEUDP-glucose 4-epimeraseNDPIJCJM_00416
16rfbDdTDP-4-dehydrorhamnose reductaseNDPIJCJM_00418
17rffGdTDP-glucose 4,6-dehydratase 2NDPIJCJM_02591
18rfbCdTDP-4-dehydrorhamnose 3,5-epimeraseNDPIJCJM_00420
19mshAD-inositol 3-phosphate glycosyltransferaseNDPIJCJM_00425
20epsJ_1Putative glycosyltransferase EpsJNDPIJCJM_01496
21epsJ_2Putative glycosyltransferase EpsJNDPIJCJM_01584
22mrdBPeptidoglycan glycosyltransferase MrdBNDPIJCJM_01847
23ftsWPutative peptidoglycan glycosyltransferase FtsWNDPIJCJM_02969
Polysaccharide transport and export system
24wzxC_1Lipopolysaccharide biosynthesis protein WzxCNDPIJCJM_00414
25wzxC_2Lipopolysaccharide biosynthesis protein WzxCNDPIJCJM_01530
26wzyEPutative ECA polymeraseNDPIJCJM_02597
27pcpPyrrolidone-carboxylate peptidaseNDPIJCJM_01797
28wzcTyrosine-protein kinase WzcNDPIJCJM_00404
29lapALipopolysaccharide assembly protein ANDPIJCJM_00864
30lapBLipopolysaccharide assembly protein BNDPIJCJM_00865
31rfaCLipopolysaccharide heptosyltransferase 1NDPIJCJM_01493
32rfaGLipopolysaccharide core biosynthesis protein RfaGNDPIJCJM_01498
33wzzEECA polysaccharide chain length modulation proteinNDPIJCJM_02588
34rfaQ_2Lipopolysaccharide core heptosyltransferase RfaQNDPIJCJM_03222
35rfaQ_3Lipopolysaccharide core heptosyltransferase RfaQNDPIJCJM_03224
36lptB_1Lipopolysaccharide export system ATP-binding protein LptBNDPIJCJM_02234
37lptB_2Lipopolysaccharide export system ATP-binding protein LptBNDPIJCJM_02719
38lptALipopolysaccharide export system protein LptANDPIJCJM_02720
39lptCLipopolysaccharide export system protein LptCNDPIJCJM_02721
40lptFLipopolysaccharide export system permease protein LptFNDPIJCJM_02803
41lptGLipopolysaccharide export system permease protein LptGNDPIJCJM_02804
42lptB_3Lipopolysaccharide export system ATP-binding protein LptBNDPIJCJM_02899
43mlaDPutative phospholipid ABC transporter-binding protein MlaDNDPIJCJM_02727
44mlaBPutative phospholipid ABC transporter-binding protein MlaBNDPIJCJM_02729
45yadGPutative ABC transporter ATP-binding protein YadGNDPIJCJM_03019
46yhdYInner membrane amino-acid ABC transporter permease protein YhdYNDPIJCJM_03327
47yejEInner membrane ABC transporter permease protein YejENDPIJCJM_00335
48yejBInner membrane ABC transporter permease protein YejBNDPIJCJM_00336
49yjfFInner membrane ABC transporter permease protein YjfFNDPIJCJM_01202
50ytfTInner membrane ABC transporter permease protein YtfTNDPIJCJM_01203
51ytfQABC transporter periplasmic-binding protein YtfQNDPIJCJM_01205
52ydcVInner membrane ABC transporter permease protein YdcVNDPIJCJM_01647
53yheSPutative ABC transporter ATP-binding protein YheSNDPIJCJM_02143
54mlaEPutative phospholipid ABC transporter permease protein MlaENDPIJCJM_02726
System secretion
55prsE_1Type I secretion system membrane fusion protein PrsENDPIJCJM_00316
56prsE_2Type I secretion system membrane fusion protein PrsENDPIJCJM_02849
57epsFType II secretion system protein FNDPIJCJM_02984
58gspEPutative type II secretion system protein ENDPIJCJM_02985
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Elizondo-Reyna, E.; Martínez-Montoya, H.; Tamayo-Ordoñez, Y.; Cruz-Hernández, M.A.; Carrillo-Tripp, M.; Tamayo-Ordoñez, M.C.; Sosa-Santillán, G.d.J.; Rodríguez-de la Garza, J.A.; Hernández-Guzmán, M.; Bocanegra-García, V.; et al. Insights from a Genome-Wide Study of Pantoea agglomerans UADEC20: A Promising Strain for Phosphate Solubilization and Exopolysaccharides Production. Curr. Issues Mol. Biol. 2025, 47, 56. https://doi.org/10.3390/cimb47010056

AMA Style

Elizondo-Reyna E, Martínez-Montoya H, Tamayo-Ordoñez Y, Cruz-Hernández MA, Carrillo-Tripp M, Tamayo-Ordoñez MC, Sosa-Santillán GdJ, Rodríguez-de la Garza JA, Hernández-Guzmán M, Bocanegra-García V, et al. Insights from a Genome-Wide Study of Pantoea agglomerans UADEC20: A Promising Strain for Phosphate Solubilization and Exopolysaccharides Production. Current Issues in Molecular Biology. 2025; 47(1):56. https://doi.org/10.3390/cimb47010056

Chicago/Turabian Style

Elizondo-Reyna, Edith, Humberto Martínez-Montoya, Yahaira Tamayo-Ordoñez, María Antonia Cruz-Hernández, Mauricio Carrillo-Tripp, María Concepción Tamayo-Ordoñez, Gerardo de Jesús Sosa-Santillán, José Antonio Rodríguez-de la Garza, Mario Hernández-Guzmán, Virgilio Bocanegra-García, and et al. 2025. "Insights from a Genome-Wide Study of Pantoea agglomerans UADEC20: A Promising Strain for Phosphate Solubilization and Exopolysaccharides Production" Current Issues in Molecular Biology 47, no. 1: 56. https://doi.org/10.3390/cimb47010056

APA Style

Elizondo-Reyna, E., Martínez-Montoya, H., Tamayo-Ordoñez, Y., Cruz-Hernández, M. A., Carrillo-Tripp, M., Tamayo-Ordoñez, M. C., Sosa-Santillán, G. d. J., Rodríguez-de la Garza, J. A., Hernández-Guzmán, M., Bocanegra-García, V., & Acosta-Cruz, E. (2025). Insights from a Genome-Wide Study of Pantoea agglomerans UADEC20: A Promising Strain for Phosphate Solubilization and Exopolysaccharides Production. Current Issues in Molecular Biology, 47(1), 56. https://doi.org/10.3390/cimb47010056

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