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Article

Genomic Analysis of Cadmium-Resistant and Plant Growth-Promoting Burkholderia alba Isolated from Plant Rhizosphere

by
Luyao Feng
1,2,3,†,
Xin Liu
1,2,†,
Nan Wang
2,
Zhuli Shi
1,2,
Yu Wang
1,2,
Jianpeng Jia
1,2,
Zhufeng Shi
2,
Te Pu
2 and
Peiwen Yang
2,*
1
School of Agriculture, Yunnan University, Kunming 650500, China
2
Institute of Agricultural Environment and Resources, Yunnan Academy of Agricultural Sciences, Kunming 650204, China
3
Chongqing Three Gorges Academy of Agricultural Sciences, Chongqing 404155, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2025, 15(8), 1780; https://doi.org/10.3390/agronomy15081780
Submission received: 30 May 2025 / Revised: 9 July 2025 / Accepted: 23 July 2025 / Published: 24 July 2025
(This article belongs to the Special Issue Innovations and Obstacles: Microbial Communities in the Journey of Soil Remediation)
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Abstract

Reducing the application of chemical fertilizers and remediating heavy metal pollution in soil are important directions in current agricultural research. Utilizing the plant-growth-promoting and remediation capabilities of bacteria can provide more environmentally friendly assistance to agricultural production. In this study, the Burkholderia alba YIM B08401 strain was isolated and identified from rhizospheric soil, subjected to whole-genome sequencing and analysis, and its Cd2+ adsorption efficiency and characteristics were confirmed using multiple experimental methods, including atomic absorption spectrometry (AAS), Fourier transform infrared spectroscopy (FTIR), and scanning electron microscopy with energy-dispersive X-ray spectroscopy (SEM-EDS). The results showed that the genome of strain YIM B08401 has a total length of 7,322,157 bp, a GC content of 66.39%, and predicts 6504 protein-coding sequences. It contains abundant functional genes related to nutrient conversion (phosphate solubilization, sulfur metabolism, zinc solubilization, siderophore production), plant hormone regulation (indole-3-acetic acid secretion, ACC deaminase production), phenolic acid degradation, root colonization, heavy metal tolerance, pathogen antagonism, and the production of antagonistic secondary metabolites. Additionally, strain YIM B08401 can specifically bind to Cd2+ through various functional groups on the cell surface, such as C-O-C, P=O, and O-H, enabling biosorption. In conclusion, strain YIM B08401 is an excellent strain with plant-growth-promoting, disease-resistant, and bioremediation capabilities, warranting further development as a biofertilizer for agricultural applications to promote green and sustainable agricultural development.

1. Introduction

With the rapid advancement of intensive modern agricultural production models, soil ecosystems are facing unprecedented multiple stresses. Excessive application of chemical fertilizers has increasingly exacerbated soil acidification and nutrient imbalance [1], while continuous cropping has led to phenolic acid accumulation and cropping obstacles, significantly reducing arable land productivity [2,3]. Industrial activities have also caused heavy metal pollution, such as cadmium (Cd) with high bioavailability, posing severe threats to agricultural product safety, agricultural productivity, and human health [4,5,6]. Traditional chemical remediation methods (e.g., lime amendment, chemical passivators), although capable of short-term pollution mitigation, often suffer from high costs and risks of secondary contamination [7,8]. Against this backdrop, rhizospheric microorganisms have emerged as a research hotspot in soil remediation due to their environmental friendliness and multifunctionality. As core mediators of “plant-soil” interactions, rhizospheric microorganisms enhance soil fertility and reduce heavy metal bioavailability through diverse mechanisms, including nitrogen fixation, phosphate solubilization, plant hormone synthesis, and heavy metal passivation [9,10,11]. These characteristics enable rhizospheric microorganisms to not only boost crop yields but also act as “biological filters” in contaminated soil remediation, achieving the dual goals of agricultural production and ecological security.
The Burkholderia represents a group of prominent plant-growth-promoting rhizobacteria (PGPR) with remarkable genetic and metabolic diversity. Certain strains within this genus exhibit multifunctional capabilities, including phosphate solubilization, nitrogen fixation, indole-3-acetic acid (IAA) production, pathogen antagonism, and heavy metal adsorption, achieved through mechanisms such as quorum sensing, nutrient conversion, and secondary metabolite synthesis [12,13,14]. These attributes enable Burkholderia strains to facilitate plant growth and enhance tolerance to abiotic stresses. For instance, Burkholderia sp. J62 has been shown to both absorb lead (Pb) and Cd from contaminated soils and significantly promote plant growth [15]. Burkholderia sp. LD-11 demonstrates dual functionality in copper- or lead-contaminated soils, combining heavy metal adsorption with the secretion of IAA, 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase, and siderophores. This strain not only increases plant dry weight in polluted soils, but also enhances soil urease activity and rhizobacterial community diversity [16]. Additionally, Burkholderia sp. Y4 can colonize rice root surfaces, enriching Cd ions through direct biosorption mediated by -C=O and -NH/-C=O groups in amino acids and proteins. Concurrently, it promotes the accumulation of essential elements (e.g., Fe, Mn) in rice while reducing Cd content [14].
However, the precise mining of rhizomicrobial functional potential still faces challenges. On one hand, the interaction mechanisms between microorganisms and plants are complex, involving multi-dimensional networks such as signal recognition, metabolic pathway regulation, and environmental adaptability. On the other hand, traditional phenotypic screening methods are insufficient to comprehensively decode functional genes and metabolic pathways, limiting the directional optimization and application of strains [17,18,19]. In recent years, the rapid development of genomics, metabolomics, and synthetic biology has provided new insights for addressing this challenge. Through whole-genome sequencing and functional annotation, it is possible to systematically uncover gene clusters related to plant growth promotion, stress resistance, and biocontrol, screen key functional modules, and evaluate their application potential, thereby laying a foundation for the development of efficient multifunctional microbial inoculants [20,21,22,23].
This study focuses on Burkholderia alba YIM B08401, a strain previously isolated from the rhizospheric soil of Pinus yunnanensis in Wuliang Mountain. Preliminary experiments have confirmed its multifunctional capabilities, including phosphate solubilization, nitrogen fixation, siderophore secretion, ACC deaminase production, and pathogen antagonism [24]. To deeply dissect its molecular mechanisms, whole-genome sequencing was performed, followed by comprehensive functional annotation using multi-database integration (COG (Clusters of Orthologous Groups of proteins), KEGG (Kyoto Encyclopedia of Genes and Genomes), antiSMASH (Antibiotics and Secondary Metabolites Analysis Shell)) to systematically identify gene clusters associated with plant growth-promoting functions. Meanwhile, phenotypic assays were conducted to validate the expression and reliability of selected functional genes, ensuring their practical applicability. The findings enrich the rhizomicrobial resource library with a high-value strain and provide a theoretical foundation for designing “microbe-plant” synergistic remediation systems and developing stress-resistant bioinoculants for yield improvement. Additionally, this research contributes to driving the sustainable transition of agriculture from “chemical dependency” to “biological-driven” models.

2. Materials and Methods

2.1. DNA Extraction, Identification, and Sequencing of Strain YIM B08401

The strain YIM B08401 was inoculated into NB medium and cultured at 30 °C with shaking at 180 r/min for 24 h. The bacterial cells were harvested by centrifugation of the culture at 10,000 rpm for 15 min. Genomic DNA was extracted using a bacterial genome DNA extraction kit following the manufacturer’s protocol (Thermo Fisher Scientific, Waltham, MA, USA). The DNA samples were then fragmented into approximately 400 bp segments using a Covaris M220 Focused-ultrasonicator (Thermo, Waltham, MA, USA) to construct the library. Paired-end (PE150) sequencing of the prepared library was performed on an Illumina sequencing platform (MajorBio, Shanghai, China).

2.2. Genome Assembly and Annotation of Strain YIM B08401

Genome assembly and annotation were performed following procedures described previously [25]. The optimized sequencing reads were assembled using SOAPdenovo v2.04. Plasmid identification in the bacterial genome assembly was conducted using PLASMe v1.1. Plasmid sequences were further annotated via BLAST+ v2.3.0 and the PLSDB Database v202106. For coding sequence (CDS) prediction, Glimmer v3.02, GeneMarkS v4.3, and Prodigal v2.6.3 were employed. tRNA and rRNA were predicted using tRNAscan-SE v2.0 and Barrnap v0.9, respectively. The predicted CDS were functionally annotated against databases including NR (Non-Redundant Protein Database), Swiss-Prot (Swiss-Prot Protein Knowledgebase), Pfam (Protein Families Database), COG, GO (Gene Ontology), and KEGG. Additionally, carbohydrate-active enzymes (CAZymes) were predicted using the Carbohydrate-Active Enzymes database (CAZy Database v8), and biosynthetic gene clusters (BGCs) responsible for secondary metabolite production were identified via AntiSMASH v7.1.0.

2.3. Experiment on Root Colonization Ability of Strain YIM B08401

Tomato seeds with no adhesion, plump particles, and uniform size were selected. The seeds were soaked in room-temperature water for 12 h, then disinfected in a sterile workbench with 75% ethanol for 5 min, followed by immersion in 15% sodium hypochlorite for 15 min. After disinfection, the seeds were transferred to a sterilized 50 mL centrifuge tube, rinsed with sterile water, shaken for 5 s, and the supernatant was discarded. This rinsing procedure was repeated three times before replacing it with a new centrifuge tube, and the rinsing steps were continued. After a total of five centrifuge tube replacements, the seeds were spread on sterile filter paper, transferred to Murashige and Skoog (MS) Medium using sterile tweezers, and 50 seeds were evenly distributed per bottle of medium. The cultures were placed in a light incubator with a 16 h light/8 h dark cycle at 26 °C, and aseptic seedlings were obtained after 5–6 days [26]. The strain YIM B08401 was inoculated into Luria-Bertani (LB) liquid medium and cultured with constant shaking at a constant temperature for 24 h. After centrifugation, the bacterial cells were resuspended in sterile ddH2O to prepare a bacterial suspension of strain YIM B08401 with an OD600 of 0.5. For inoculation, 100 mL of this bacterial suspension was used to immerse the roots of aseptic tomato seedlings for 2 h, with 10 replicates performed. Subsequently, the inoculated tomato seedlings were transferred to fresh MS medium for static culture for 2 days. Prior to observation, the roots were rinsed with sterile ddH2O, and at least 20 root tips were examined under a scanning electron microscope (SEM) to assess the colonization of strain YIM B08401 [27].

2.4. Qualitative Assays for Enzyme Production by Strain YIM B08401

Chitinase screening medium formulation: 20 mL of 1% colloidal chitin solution, 3 g yeast extract, 3 g peptone, 0.5 g MgSO4·7H2O, 0.7 g KH2PO4, 0.3 g K2HPO4, 0.01 g FeSO4·7H2O, 1000 mL distilled water, 20 g agar powder, pH 7. Preparation of colloidal chitin: 2 g of chitin powder was dissolved in 45 mL pre-cooled concentrated hydrochloric acid, followed by standing at 4 °C for 24 h. Then 300 mL of 50% ethanol was added to obtain a flocculent mixture. The mixture was centrifuged at 4000 rpm for 20 min to collect the precipitate, which was washed with distilled water until neutral and resuspended in 200 mL of water to prepare 1% colloidal chitin. Strain YIM B08401 was activated and inoculated onto the chitin medium; the formation of clear zones around colonies indicated its ability to produce chitinase [28]. Xylanase screening medium formulation: 2 g xylan, 1 g KH2PO4, 2 g (NH4)2SO4, 0.5 g MgSO4·7H2O, 0.5 g NaCl, 18 g agar, 1000 mL distilled water, natural pH. Preparation of Congo red solution (1 mg/mL): 1 g of Congo red was weighed and dissolved in 1000 mL of distilled water, and the solution was stored at 4 °C for later use. Activated strain YIM B08401 was inoculated onto the xylan screening medium and cultured at 30 °C for 3 days. The plate was covered with Congo red solution and left to stand for 15 min, then rinsed with 1 mol/L sodium chloride solution for 15 min. The presence of clear zones around colonies was used to determine the strain’s ability to secrete xylanase [29].

2.5. Cd Adsorption Assays of Strain YIM B08401

2.5.1. Cd2+ Adsorption by Strain YIM B08401

Strain YIM B08401 was inoculated into sterile NB medium and cultured at 30 °C with shaking at 180 rpm until the optical density at 600 nm (OD600) reached 0.6, serving as the seed solution. The seed solution was inoculated at a 1% inoculum ratio into NB liquid media containing 0 mg/L, 100 mg/L, and 200 mg/L Cd2+, with uninoculated medium as the blank control. Cultures were incubated at 30 °C and 180 rpm for 2 days, with three replicates per treatment. After cultivation, the culture broth was centrifuged at 4500 rpm for 15 min. The supernatant was collected, filtered through a 0.22 μm membrane, and the Cd2+ concentration was measured using atomic absorption spectroscopy (AAS) to calculate the strain’s adsorption efficiency. Meanwhile, the centrifuged bacterial cells were washed three times with distilled water via centrifugation at 4500 rpm for 15 min, followed by discarding the supernatant. The cell pellets were frozen at −80 °C for at least 5 h and then lyophilized using a freeze-dryer to obtain lyophilized biomass. The experiment was conducted from November 2023 to July 2024.

2.5.2. Fourier Transform Infrared Spectroscopy (FTIR) Analysis

Lyophilized bacterial cells from different Cd2+ concentrations were mixed with dry powdered potassium bromide (KBr) at a 1:100 ratio. The mixture was uniformly spread into a suitable disc, pressed at 800 MPa using a Fourier transform infrared (FTIR) spectrometer, and spectral data were recorded. The FTIR peaks were scanned over a wavenumber range of 4000 to 400 cm−1. The sample treated with 0 mg/L Cd2+ (lyophilized cells + KBr) served as the reference, and the treated samples were compared based on peaks indicating various bond stretching and bending vibrations [30].

2.5.3. SEM-EDS Analysis

Bacterial cells and sediments were collected from the cultures described in Section 2.5.1. (after incubation with different Cd2+ concentrations), washed three times with phosphate buffer solution, and then fixed with 2.5% (v/v) glutaraldehyde solution for 12 h. The samples were then dehydrated using an ethanol gradient series for purification, freeze-dried into powder, and subjected to scanning electron microscopy with energy-dispersive X-ray spectroscopy (SEM-EDS) to analyze morphological and elemental composition changes before and after bacterial adsorption [31].

3. Results and Discussion

3.1. General Genome Characteristics and Strain Identification of YIM B08401

Strain YIM B08401 was isolated from the rhizosphere soil of Pinus armandii Franch (100°49′25″ N, 24°27′00″ E) in Wuliangshan Mountain International Nature Reserve, Yunnan Province, China. Strain YIM B08401 showed the highest 16S rRNA gene sequence similarity of 100.00% with the closest type strain Burkholderia alba AD18T. Furthermore, it also showed high 16S rRNA similarities with B. oklahomensis C6786T (98.76%), B. rinojensis A396T (98.69%) and B. plantarii ATCC 43733T (98.63%) by Ez-biocloud. The NJ evolutionary tree based on 16S rRNA was constructed using MEGA 7.0, and the ML and MP evolutionary tree was used for auxiliary identification. Combined with physiological and biochemical results, strain YIM B08401 was identified as B. alba (Figure 1). However, B. alba AD18T had been effectively published, and the taxonomic name has not been verified.
The genome of YIM B08401 contained 204 scaffolds with the total length of 7,322,157 bp and GC content of 66.39%. A total of 6504 protein-coding sequences (CDSs) were annotated, and 3 rRNAs and 63 tRNA were also predicted. In addition, 15 gene islands and 2 prophage regions were predicted by the IslandViewer and Phage Finder predictions of the strains. The general genomic characteristics of strain YIM B08401 are shown in Table 1. The round genome representing the entire genome assembly is shown in Figure 2.

3.2. Genome Functional Annotation

The genome of strain YIM B08401 was functionally annotated using the NR, Swiss-Prot, Pfam, COG, GO and KEGG databases. A total of 6504 genes were annotated, with 6284 genes annotated in the NR database, 4592 in Swiss-Prot, 5358 in Pfam, 5353 in COG, 3990 in GO, and 3196 in KEGG.
Annotation with the COG database identified 5353 genes in strain YIM B08401, representing 82.30% of all annotated genes (Figure 3A). These genes were hierarchically classified into 4 major categories and 22 subcategories [32]. Given that some genes were assigned to multiple categories, genes related to “Information Storage and Processing”, “Cellular Processes and Signaling”, “Metabolism”, and “Poorly Characterized” accounted for 17.60%, 17.78%, 36.69%, and 27.93% of the total COG annotations, respectively. These results highlight the metabolic activity of strain YIM B08401, indicating its capacity to support bacterial growth by facilitating material synthesis, energy conversion, and metabolite production. Among the 22 subcategories, excluding genes with unknown functions (27.93%), genes involved in transcription (8.91%), amino acid transport and metabolism (8.83%), inorganic ion transport and metabolism (5.83%), cell wall/membrane/envelope biogenesis (5.81%), and carbohydrate transport and metabolism (5.54%) were highly abundant. Notably, the high proportions of genes involved in amino acid transport and metabolism, as well as inorganic ion transport and metabolism, suggest that strain YIM B08401 may possess inherent capabilities to compete with other microorganisms [33,34]. Furthermore, previous studies have demonstrated that in plant growth-promoting bacteria such as Bacillus velezensis SH-1471 and Pseudomonas qingdaonensis ZCR6, genes related to transcription and amino acid transport/metabolism also constitute the most abundant gene groups [11,26]. Collectively, these characteristics indicate that strain YIM B08401 has potential advantages in functional expression, environmental survival, and competitive nutrient acquisition.
The KEGG database annotated 3196 genes across six categories: metabolism, genetic information processing, environmental information processing, human diseases, organismal systems, and cellular processes [35], representing 49.14% of all annotated genes (Figure 3B). Despite overlapping annotations, the “Metabolism” category (2732 genes, 65.74%) harbored the largest gene set, consistent with COG annotation results. Among the six categories, excluding 1074 genes assigned to “Global and overview maps”, genes associated with membrane transport (345 genes, 8.30%), amino acid metabolism (344 genes, 8.28%), and carbohydrate metabolism (313 genes, 7.53%) were the most prevalent. These findings align with GO and COG annotations, further validating the strain’s high abundance of genes related to energy transport and biosynthesis.
Using the GO database, 3990 genes were annotated in strain YIM B08401, accounting for 61.35% of the total annotated genes (Figure 3C). The database classified all annotated genes into three main categories, with partial genes assigned to multiple categories: “Cellular Component” (1682 genes, 24.57%), “Molecular Function” (3349 genes, 48.92%), and “Biological Process” (1815 genes, 26.51%) [36]. Notably, nearly half of the annotated genes fell under “Molecular Function”, indicating the strain’s rich functional expression and strong potential for growth promotion. Among all annotated subcategories, the most abundant were “integral component of membrane” (14.78%), “DNA binding” (7.21%), “ATP binding” (5.57%), “cytoplasm” (4.78%), “plasma membrane” (4.5%), and “DNA-binding transcription factor activity” (4.47%). A comparison with known plant growth-promoting rhizobacteria revealed that strain YIM B08401 exhibits significantly higher abundances of genes associated with integral components of membrane, ATP binding, and DNA-binding transcription factor activity compared to strains such as Bacillus velezensis SH-1471 and Bacillus subtilis MG-1 [26,37]. These characteristics further confirm that strain YIM B08401 possesses remarkable functional versatility and metabolic activity, with distinct advantages particularly in membrane-related functions, molecular interactions, and transcriptional regulation.

3.3. CAZyme Database Analysis

A total of 196 CAZyme-related enzymes were identified in the genome of YIM B08401, including 64 Glycoside Hydrolases (GH), 54 GlycosylTransferases (GT), 1 Polysaccharide Lyase (PL), 46 Carbohydrate Esterases (CE), 30 Auxiliary Activities (AA), and 1 Carbohydrate-Binding Module (CBM). Among these, families associated with chitin degradation, starch hydrolysis, and cellulose degradation were detected, including GH18, GH15, GH54, GH39, and GH3. Genomic mining further revealed the presence of the chitinase synthesis gene chiA, which enables the conversion of exogenous chitin into N-acetylglucosamine (GlcNAc) and GlcNAc monomer polymers, subsequently transported into bacterial cells [38]. GlcNAc is phosphorylated to GlcNAc-6P by NagK (N-acetylglucosamine kinase encoded by nagK), then converted to glucosamine-6P and acetate by NagA (N-acetylglucosamine-6-phosphate deacetylase encoded by nagA), where acetate serves as a carbon source for bacterial growth. Additionally, glucosamine-6P is transformed into fructose-6-phosphate by NagB (glucosamine-6-phosphate deaminase encoded by nagB), with released NH3 utilized as a nitrogen source by the bacteria [39]. Qualitative assays confirmed the production of chitinase and xylanase by strain YIM B08401 (Figure S2), highlighting its potential for carbohydrate metabolism and utilization in ecological niches.

3.4. antiSMASH Database Analysis

Burkholderia species typically possess large and complex genomes with numerous secondary metabolite biosynthesis clusters [40]. Using the antiSMASH database (with the MIBiG database as the reference dataset and stringent cluster detection), strain YIM B08401 was analyzed for potential biosynthetic gene clusters (BGCs) (Table S1). KnownClusterBlast identified 21 secondary metabolite biosynthesis gene clusters, of which only 5 showed >85% similarity to known compound clusters, 10 exhibited <85% similarity, and 6 had no homology [41]. Studies indicate that BGCs with >85% similarity likely encode the same compound as their closest known cluster, while those with <85% similarity may harbor novel metabolites [42]. The five BGCs with >85% similarity include fragin (with antifungal activity) [43]; ornibactin C8/C4/C6 (siderophores with pathogen-antagonistic capabilities) [44]; icosalide A/B (antibiotics inhibiting insect pathogens) [45]; and rhizomide A/B/C (with potential antibacterial activity) [46,47]. These predicted secondary metabolites are all reported to inhibit pathogen growth, consistent with the strain’s antibacterial results in previous studies [24], indicating a strong potential for YIM B08401 to synthesize these compounds. Additionally, the clusters were predicted to contain homoserine lactones (hserlactone), signaling molecules of the quorum-sensing system, aligning with the universal quorum-sensing capability of Burkholderia [48]. BGCs with <85% similarity represent promising targets for discovering novel natural products. Heterologous expression could be employed to further characterize its functional expression and uncover novel natural secondary metabolites.

3.5. Plant Growth Promotion Potential

3.5.1. Phosphorus Transformation

Phosphorus is an essential element for plant growth, but large amounts of insoluble phosphorus in soil cannot be absorbed by plant roots. Bacteria can leverage their microbial characteristics to convert insoluble phosphorus into forms absorbable by plants. Phosphorus is also a vital nutrient for microbes, participating in the synthesis of cellular structures (e.g., nucleic acids, lipids) and energy-supplying processes (e.g., the tricarboxylic acid cycle). To ensure long-term phosphorus acquisition, microbes have evolved diverse regulatory systems for phosphate uptake and utilization, with three well-characterized mechanisms: inorganic phosphorus solubilization and organic phosphorus mineralization, phosphate uptake and transport, and phosphorus starvation response regulation. A primary mechanism of bacterial inorganic phosphorus solubilization involves secreting low-molecular-weight organic acids to dissolve insoluble phosphorus by reducing pH, chelating cations bound to phosphate, and competing for phosphorus absorption sites [49]. Examples of such organic acids include gluconic acid (GA), oxalic acid, malic acid, and citric acid [50]. Goldstein et al. proposed that gluconic acid is the main agent for inorganic phosphorus solubilization in Gram-negative bacteria [51]. Gluconic acid synthesis requires glucose dehydrogenase (GDH encoded by gcd) and the redox cofactor pyrroloquinoline quinone (PQQ encoded by pqqABCDEF), which together convert glucose to gluconic acid. Genomic annotation of YIM B08401 identified genes involved in gluconic acid synthesis (pqqBCDF, gcd, gdh), indicating the strain’s potential to secrete gluconic acid-driven organic acids for insoluble phosphate solubilization. Utilization of insoluble organic phosphorus relies on bacterial phosphatases to mineralize organic phosphates. YIM B08401 harbors phoA and phnCDEFGHIJKLMN genes, conferring the potential to secrete alkaline phosphomonoesterase (EC: 3.1.3.1) and phosphonatases/carbon-phosphorus (C-P) lyases. C–P lyases enable microbes to utilize phosphonates as the sole phosphorus source under phosphorus starvation [52]. Additionally, YIM B08401 possesses phosphate uptake-related genes (pit, pitA, PhoR-PhoB, pstSCAB, PhoU), forming a low-affinity constitutive Pit system and a high-affinity phosphate starvation-induced Pst system. Details of phosphate-solubilizing genes are listed in Table S2. Previous experiments showed that YIM B08401 solubilized 455.63 ± 59.65 mg/L of phosphorus from tricalcium phosphate in a phosphorus-solubilizing medium after 2 days and 18.46 ± 1.71 mg/L from lecithin after 3 days [24], confirming its phosphorus solubilization capacity.

3.5.2. Nitrogen Fixation

In studies on whether the strain can participate in the nitrogen cycle, preliminary experiments verified that strain YIM B08401 could grow on Ashby nitrogen-fixing bacteria medium, demonstrating biological nitrogen fixation capacity [24]. Gene annotation revealed genes related to the nitrogen cycle in the strain (Table S3), including nirB, which encodes nitrite reductase involved in nitrate reduction. However, the genome of YIM B08401 lacks genes directly associated with nitrogen fixation, though it possesses a gene (iscU) with primary structural similarity to nifU. This gene may be involved in synthesizing iron-sulfur (Fe-S) clusters required for nitrogenase [53,54].

3.5.3. Sulfur Metabolism

Multiple studies have demonstrated that hydrogen sulfide (H2S) acts as a gaseous signaling molecule in various plant physiological processes, including promoting seed germination, alleviating heavy metal toxicity, and mitigating effects of abiotic stresses (e.g., high salinity, drought, and extreme temperatures) [55,56,57,58]. However, direct exogenous supplementation of H2S in agricultural practice is challenging, making microbial-mediated H2S production a promising research direction. Experimental validation confirmed that strain YIM B08401 can utilize thiosulfate and convert it into H2S.
Genomic annotation of YIM B08401 revealed a gene pathway for assimilatory sulfate reduction (Figure 4). Sulfate is first converted to adenosine 5′-phosphosulfate (APS) by sulfate adenylyltransferase (encoded by cysN), followed by transformation to 3′-phosphoadenosine-5′-phosphosulfate (PAPS) via adenylylsulfate kinase (encoded by cysC). PAPS is then reduced to sulfite by phosphoadenosine phosphosulfate reductase (encoded by cysH), and finally converted to H2S by sulfite reductase (NADPH) flavoprotein alpha-component (EC: 1.8.1.2, encoded by cysJ) [34]. Additionally, the sqr gene, a marker for sulfide oxidation, encodes sulfide: quinone oxidoreductase, which catalyzes the oxidation of sulfide and reduction of ubiquinone [59]. YIM B08401 harbors a highly homologous sqr gene, suggesting its potential for sulfur oxidation. Details of sulfur metabolism-related genes are listed in Table S4.

3.5.4. Zinc Solubilization

Zinc, a trace element essential for living organisms, is the second most important transition metal ion after iron. Its divalent ion form (Zn2+) serves as a cofactor for metalloproteins, participating in structural, catalytic, and regulatory functions. Zinc in soil predominantly exists in insoluble forms, making it inaccessible to plants. Microbial zinc solubilization can convert insoluble zinc into plant-available Zn2+. Burkholderia species are Gram-negative bacteria that utilize multiple systems for zinc uptake, including the ZnuABC transporter, ZIP protein family, and TonB system. zur, a key regulator of zinc homeostasis, controls zinc uptake by activating high-affinity transporters under zinc-limiting conditions. When zinc is abundant, low-affinity ZIP (ZRT, IRT-like proteins) family members like ZupT mediate zinc uptake [60]. Under zinc deficiency, zur senses low zinc levels and activates the high-affinity ABC transporter znuABC, which specifically imports extracellular zinc for bacterial utilization. Genomic annotation of YIM B08401 identified znuA and znuC genes involved in forming the zinc-uptake ABC transporter, but znuB was absent, suggesting this may not be the primary zinc uptake pathway for the strain. Additionally, the genome harbors TonB system genes (tonB, exbB, exbD) associated with zinc uptake. Collectively, YIM B08401 possesses a suite of genes related to zinc uptake and utilization (Table S5), indicating its zinc solubilization potential. Experimental validation showed that the strain solubilized 18.60 ± 4.19 mg/kg of zinc after 7 days [24], confirming its capacity to convert insoluble zinc into bioavailable forms.

3.5.5. Siderophore Production

Iron, the most critical transition metal ion for living organisms, is an essential nutrient for microbial growth. Siderophores, with their high affinity for Fe3+, chelate insoluble iron into plant-available soluble forms. They also compete with pathogens for Fe3+, indirectly reducing pathogen abundance. Previous studies have confirmed that strain YIM B08401 produces siderophores [24], though the specific type remains uncharacterized. Genomic annotation revealed genes involved in synthesizing catechol-type siderophores Bacillibactin and Enterochelin. These siderophores, which are encoded by entABCEF and dhbF genes, function not only as potential antimicrobial agents but also as iron-chelating agents to supply iron for bacterial growth. Details of the relevant genes are listed in Table S6.

3.5.6. Indole-3-Acetic Acid (IAA) Production

The genome of strain YIM B08401 harbors a complete pathway for tryptophan synthesis encoded by trpABCDEFG genes (Figure 5), indicating the strain’s potential to produce IAA without exogenous tryptophan supplementation. Genes involved in the second and third steps of the indole pyruvic acid (IPA) pathway were identified, including ipdC (encoding indolepyruvate decarboxylase [EC: 4.1.1.74]) and aldh (encoding aldehyde dehydrogenase [NAD+] [EC: 1.2.1.3]). Additionally, genes governing the final step of the indoleacetamide (IAM) pathway, specifically amiE and iaaH, were annotated. These genes encode amidase [EC: 3.5.1.4] and indoleacetamide hydrolase [EC: 3.5.1.-], respectively. Both enzymes specifically hydrolyze indole-3-acetamide (IAM) into IAA and ammonia. Details of IAA biosynthesis-related genes annotated in YIM B08401 are listed in Table S7.

3.5.7. Ethylene Regulation

Ethylene is a key phytohormone regulating plant growth and development, orchestrating physiological processes and coordinating with other signaling pathways to mediate responses including fruit ripening, organ senescence, flowering, seed dormancy and germination, root hair development, and biotic/abiotic stress responses. However, excessive ethylene accelerates plant senescence, detrimentally affecting crop yield and storage. One strategy to mitigate ethylene production involves the acdS-encoded enzyme 1-aminocyclopropane-1-carboxylate deaminase (ACCD), which catalyzes the conversion of 1-aminocyclopropane-1-carboxylate (ACC, the immediate precursor of ethylene) into ammonia and α-ketobutyrate. This not only reduces ethylene biosynthesis but also provides ammonia as a nitrogen source for plant growth [61,62].
Genomic annotation of strain YIM B08401 using the Swiss-Prot database identified the presence of the acdS gene (Table S8). Blastp analysis of the translated protein revealed highest homology (89.35%) to ACCD from Paraburkholderia guartelaensis. Structural alignment with functionally verified ACCD sequences highlighted conserved residues E295 (glutamic acid) and L322 (leucine), which are critical for catalytic activity. These findings strongly suggest that YIM B08401 harbors a functional ACCD enzyme. Experimental validation demonstrated that YIM B08401 maintained viability when repeatedly subcultured on ADF (ACC Deaminase Activity Assay Medium) [24], confirming its ability to utilize ACC as a nitrogen source and further supporting its role in ethylene modulation. This mechanism likely contributes to plant growth promotion and stress tolerance under adverse conditions.

3.5.8. Degradation of Phenolic Acids

Continuous monocropping in agriculture often leads to the accumulation of phenolic acids (e.g., benzoic acid, p-hydroxybenzoic acid, salicylic acid, ferulic acid) secreted by plant roots, which inhibit both plant growth and soil microbial activity, thereby contributing to replant disease. Microbial degradation of these compounds represents a promising strategy to alleviate such obstacles. The genome of strain YIM B08401 harbors a complete benzoate degradation pathway (Figure S1). Benzoic acid is sequentially converted to catechol by the actions of benzoate 1,2-dioxygenase (encoded by benA-xylX) and dihydrodiol dehydrogenase (encoded by benD-xylL). Through the ortho-cleavage pathway, catechol is further metabolized via enzymes encoded by catB, catC, pcaD, pcaI, and fadA, ultimately generating succinyl-CoA and acetyl-CoA, which enter the citric acid cycle to provide energy for microbial growth. Additional genes involved in this degradation process that are present in the genome of strain YIM B08401 are listed in Table S9.

3.5.9. Root Colonization

The ability of plant growth-promoting microorganisms to colonize the rhizosphere is a critical prerequisite for their effectiveness in promoting plant growth. Bacterial chemotaxis serves as the primary driver of colonization; bacteria must first recognize chemical signals from root exudates and exhibit chemotactic responses to migrate toward the rhizosphere and aggregate for colonization. This process relies on bacterial motility, primarily mediated by flagella, which enable movement and adhesion in response to chemotactic cues [63,64]. Genomic analysis of strain YIM B08401 identified a suite of genes associated with chemotaxis, including tar, tsr, trg, and aer (encoding chemotactic signal sensory proteins) and cheABCDRWYZ (encoding regulatory proteins). Genes involved in flagellar assembly, including flgABCDEEEFGHIKLMN, flhABCD, fliACDDEFGHIJKMNOPQRST, and motAB, were also annotated. Collectively, these genes suggest that YIM B08401 possesses the genetic machinery for rhizosphere colonization (Figure 6, Table S10). To validate this potential, colonization assays were conducted, demonstrating that YIM B08401 successfully colonized the roots of tomato seedlings (Figure S3). This phenotypic result aligns with genomic predictions, providing robust evidence for the strain’s chemotactic and motile capabilities essential for root association.

3.5.10. Heavy Metal Adsorption

Heavy metal ions are typical inorganic pollutants, with cadmium (Cd) recognized as one of the most toxic, posing lethal threats to humans and ecosystems [65,66]. Microbial-based remediation leveraging metal tolerance and adsorption capabilities has emerged as a research hotspot in environmental restoration due to its cost-effectiveness, minimal ecological disturbance, and sustainability. Microorganisms employ diverse strategies to counteract heavy metal stress, including biotransformation (e.g., valence alteration), complexation-precipitation (e.g., extracellular polymeric substance binding), transmembrane transport (e.g., efflux pumps), and intracellular detoxification (e.g., thiol compound chelation) [67,68]. Genomic annotation of strain YIM B08401 revealed numerous genes associated with tolerance, resistance, and transport of multiple heavy metals (e.g., Cd, Cu, Cr, Hg) (Table S11). Key genetic determinants include glutathione (GSH) biosynthesis genes gshA (encoding glutamate-cysteine ligase) and gshB (glutathione synthetase), which mediate intracellular detoxification by forming low-toxicity complexes with heavy metal ions (e.g., Cd2+, Hg2+) via thiol (-SH) groups [69,70]. Phytochelatin (PCs) synthesis gene pcs-1 encodes enzymes that chelate heavy metals through multiple thiol groups, thereby reducing their bioavailability and toxicity [71]. The copper resistance system involves the two-component regulatory system cusBR (sensing Cu2+ and activating downstream responses) and copA (encoding a Cu-CPx type ATPase for active copper efflux), which collaboratively maintain intracellular copper homeostasis [72,73]. The RND (Resistance–Nodulation–Division) transporter complex czcCBA mediates the efflux of divalent cations (Cd2+, Zn2+, Co2+) and represents a critical resistance mechanism in Gram-negative bacteria [74,75]. Heavy metal adsorption assays confirmed that live cells of strain YIM B08401 can reduce Cd2+ concentrations. The underlying mechanisms may involve not only direct cellular adsorption but also the gene-mediated transport and detoxification processes described above.

3.6. Cd2+ Adsorption Efficiency and Characteristics of Strain YIM B08401

Heavy metal tolerance tests revealed that strain YIM B08401 could grow on NA medium supplemented with 500 mg/L of Cd2+, Zn2+, or Cu2+, and adsorption experiments further demonstrated the strain effectively reduced Cd2+ concentrations in solution within two days, with adsorption efficiencies of 20.76% (100 mg/L initial Cd2+) and 38.49% (200 mg/L) as measured by atomic absorption spectroscopy (AAS).
Scanning electron microscopy–energy dispersive spectroscopy (SEM-EDS) analysis of cells exposed to 0, 100, and 200 mg/L Cd2+ showed that precipitates in the 0 mg/L group appeared as large, smooth aggregates (Figure 7A) likely formed by extracellular polymeric substances (EPS) secreted during normal growth [76], while those in the 100 mg/L group fragmented into smaller particles (Figure 7C), possibly due to interactions between Cd2+ and cell surface functional groups (e.g., carboxyl, hydroxyl, amino) disrupting EPS structure via complexation or ion exchange [77,78]. When the Cd2+ concentration reaches 200 mg/L, the precipitate exhibits a rough and porous surface (Figure 7E), potentially resulting from high-concentration Cd2+-induced cell lysis. In this scenario, the released intracellular substances react with Cd2+ and extracellular polymeric substances (EPS) to form irregular complexes [79,80,81].
EDS detected characteristic Cd peaks accounting for 1.78% and 14.75% of total elemental composition in the 100 and 200 mg/L groups, respectively (Figure 7D,F), indicating multiple Cd2+ removal mechanisms including surface adsorption and biomineralization [77,81]. The absence of distinct bacterial structures in SEM images could be attributed to surface masking by EPS-Cd2+ complexes or Cd precipitates, or cell damage and lysis from high Cd2+ toxicity mixing cellular debris with other components [80,82].

3.7. FTIR Spectroscopy of Strain YIM B08401

To further clarify the adsorption mechanism of Cd2+ by strain YIM B08401, Fourier transform infrared spectroscopy (FTIR) was used to characterize the functional groups on the cell surface of YIM B08401 before and after cadmium adsorption, revealing multiple characteristic absorption peaks within the wavenumber range of 397–4003 cm−1 (Figure 8). Specifically, a peak near 1055 cm−1 corresponded to stretching vibrations of C-O, C-C, C-O-C, and C-O-P bonds in polysaccharides [83], while the peak at 1231 cm−1 represented P=O vibrations of phosphodiester bonds in nucleic acids and phospholipids [84]. The absorption peak at 1390 cm−1 reflected C-H vibrations of CH3/CH2 groups and C-O vibrations of carboxylate (COO−), confirming the presence of extracellular polymeric substances (EPS) secreted by bacteria that can effectively chelate metal ions through cation exchange to reduce toxicity [85,86]. A characteristic absorption peak at 1534 cm−1 was likely attributed to bending vibrations of N-H bonds and stretching vibrations of C-N bonds in amide groups, potential structural components of the bacterial cell wall [87], and the broad absorption peak at 3281 cm−1 was assigned to stretching vibrations of hydroxyl (O-H) groups [81]. These results indicate that under Cd2+ stress, strain YIM B08401 interacts with Cd2+ through multiple cell surface functional groups (e.g., C-O-C, P=O, O-H), with groups associated with proteins, polysaccharides, and lipids (such as phospholipids) potentially involved in Cd assimilation and metabolic processes.

4. Conclusions

In this study, whole-genome sequencing and annotation of Burkholderia alba YIM B08401 were performed to identify genes and metabolic pathways associated with plant growth promotion, biocontrol, and abiotic stress tolerance. The strain exhibited a G+C content of 66.39% and harbored 6504 annotated genes, including those involved in nutrient conversion, indole-3-acetic acid (IAA) secretion, and siderophore production. KEGG pathway annotation revealed metabolic pathways related to nutrient utilization, such as ABC transporter genes (pstABCS, phnDEC, cysPUWA, znuABC), two-component systems (PhoR-PhoB, cheWARYB), and complete pathways for tryptophan synthesis and benzoic acid degradation. AntiSMASH annotation identified 21 secondary metabolism gene clusters, including those for terpenoids, non-ribosomal peptides (NRPS), polyketides (PKS), and homoserine lactones (hserlactone). CAZy annotation further confirmed the presence of enzymes involved in chitin, starch, cellulose, and xylan degradation. FTIR and SEM-EDS analyses demonstrated that YIM B08401 specifically binds Cd2+ through cell surface functional groups (e.g., C-O-C, P=O, O-H), enabling biosorption of heavy metal ions. Collectively, Burkholderia alba YIM B08401 harbors genetically encoded potentials for plant growth promotion, biocontrol of plant diseases, and abiotic stress resistance, warranting further molecular investigations to unlock its full genetic repertoire and expand its application potential in agricultural and environmental biotechnology.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy15081780/s1, Figure S1: Schematic diagram of the benzoic acid degradation gene pathway (blue-bordered region). Red boxes indicate genes present in strain YIM B08401; Figure S2. Photographs of qualitative enzyme activity assays for strain YIM B08401. (A) Chitinase; (B) Xylanase. Figure S3. Photographs of tomato seedling root colonization by strain YIM B08401. Table S1: Results of secondary metabolite prediction for YIM B08401 by antiSMASH; Table S2: Phosphate solubilization related genes; Table S3: Nitrogen cycle related genes; Table S4: Sulfur metabolism related genes; Table S5: Zinc solubilization related genes; Table S6: Iron carrier production related genes; Table S7: Indole acetic acid (IAA) secretion related genes; Table S8: Ethylene regulation related genes; Table S9: Benzoic acid degradation related genes; Table S10: Root colonization related genes; Table S11: Heavy metal related genes.

Author Contributions

Conceptualization, L.F., X.L., N.W., Z.S. (Zhuli Shi), Y.W., J.J., Z.S. (Zhufeng Shi), T.P. and P.Y.; methodology, P.Y.; software, N.W.; formal analysis, X.L.; investigation, Z.S. (Zhuli Shi), Y.W. and J.J.; resources, Z.S. (Zhufeng Shi) and T.P.; writing—original draft, L.F. and X.L.; writing—review and editing, L.F., X.L. and P.Y.; funding acquisition, P.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Yunnan Province “Xingdian Talent” Support Program (XDYC-CYCX-2002-0071) and the Central Government Guided Local Science and Technology Development Fund (202407AC110006).

Data Availability Statement

Genome sequences were deposited in the GenBank database under BioProject accession number PRJNA1027102 under accession number JAWJWL000000000 (https://www.ncbi.nlm.nih.gov/nuccore/JAWJWL000000000, accessed on 16 October 2023).

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Figure 1. Phylogenetic trees of strain YIM B08401 based on 16S rDNA gene sequences. (A) Neighbor-joining (NJ) method; (B) maximum likelihood (ML) method; (C) maximum parsimony (MP) method.
Figure 1. Phylogenetic trees of strain YIM B08401 based on 16S rDNA gene sequences. (A) Neighbor-joining (NJ) method; (B) maximum likelihood (ML) method; (C) maximum parsimony (MP) method.
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Figure 2. Circos genome map of strain YIM B08401. Note: The outermost circle indicates the genome size. The second and third circles represent the coding sequences (CDS) on the positive and negative strands, respectively, with different colors corresponding to different COG (Clusters of Orthologous Groups) functional categories of the CDS. The fourth circle shows rRNA and tRNA. The fifth circle denotes the GC content. The innermost circle represents the GC-Skew values.
Figure 2. Circos genome map of strain YIM B08401. Note: The outermost circle indicates the genome size. The second and third circles represent the coding sequences (CDS) on the positive and negative strands, respectively, with different colors corresponding to different COG (Clusters of Orthologous Groups) functional categories of the CDS. The fourth circle shows rRNA and tRNA. The fifth circle denotes the GC content. The innermost circle represents the GC-Skew values.
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Figure 3. Functional annotation results of the YIM B08401 strain genome across databases. (A) COG database; (B) KEGG database; (C) GO database (showing highly abundant categories among the three classifications).
Figure 3. Functional annotation results of the YIM B08401 strain genome across databases. (A) COG database; (B) KEGG database; (C) GO database (showing highly abundant categories among the three classifications).
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Figure 4. Schematic diagram of the assimilatory sulfate reduction gene pathway. Red boxes indicate genes possessed by strain YIM B08401.
Figure 4. Schematic diagram of the assimilatory sulfate reduction gene pathway. Red boxes indicate genes possessed by strain YIM B08401.
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Figure 5. Schematic diagram of the tryptophan biosynthesis gene pathway. Red boxes indicate genes possessed by strain YIM B08401.
Figure 5. Schematic diagram of the tryptophan biosynthesis gene pathway. Red boxes indicate genes possessed by strain YIM B08401.
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Figure 6. Schematic diagram of flagellar assembly genes. Red boxes indicate genes present in strain YIM B08401.
Figure 6. Schematic diagram of flagellar assembly genes. Red boxes indicate genes present in strain YIM B08401.
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Figure 7. SEM images and EDS elemental analysis of YIM B08401 under non-Cd and Cd stress conditions. (A,B) SEM image and EDS spectrum of YIM B08401 without Cd stress; (C,D) SEM image and EDS spectrum of YIM B08401 under 100 mg/L Cd2+ stress; (E,F) SEM image and EDS spectrum of YIM B08401 under 200 mg/L Cd2+ stress. Red circles indicate the selected points for spectral analysis.
Figure 7. SEM images and EDS elemental analysis of YIM B08401 under non-Cd and Cd stress conditions. (A,B) SEM image and EDS spectrum of YIM B08401 without Cd stress; (C,D) SEM image and EDS spectrum of YIM B08401 under 100 mg/L Cd2+ stress; (E,F) SEM image and EDS spectrum of YIM B08401 under 200 mg/L Cd2+ stress. Red circles indicate the selected points for spectral analysis.
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Figure 8. FTIR spectra of YIM B08401 before and after Cd2+ adsorption.
Figure 8. FTIR spectra of YIM B08401 before and after Cd2+ adsorption.
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Table 1. The genome characterization of YIM B08401.
Table 1. The genome characterization of YIM B08401.
The CharacterizationValue
Assembly information
The total length (bp)7,322,157
Total scaffold No204
Scaffold N50(bp)201,844
Contigs193
Conting N50 (bp)143,587
G + C content (%)66.39
Annotation information
CDSs (total)6504
rRNA3
tRNA63
Mobile Genetic Element (MGE)
Gene island15
Prophage regions2
CRISPR-Cas22
Insertion sequence9
Tns62
NCBI
BioProject IDPRJNA1027102
BioSample IDSAMN37776913
GeneBank accession numberJAWJWL000000000
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MDPI and ACS Style

Feng, L.; Liu, X.; Wang, N.; Shi, Z.; Wang, Y.; Jia, J.; Shi, Z.; Pu, T.; Yang, P. Genomic Analysis of Cadmium-Resistant and Plant Growth-Promoting Burkholderia alba Isolated from Plant Rhizosphere. Agronomy 2025, 15, 1780. https://doi.org/10.3390/agronomy15081780

AMA Style

Feng L, Liu X, Wang N, Shi Z, Wang Y, Jia J, Shi Z, Pu T, Yang P. Genomic Analysis of Cadmium-Resistant and Plant Growth-Promoting Burkholderia alba Isolated from Plant Rhizosphere. Agronomy. 2025; 15(8):1780. https://doi.org/10.3390/agronomy15081780

Chicago/Turabian Style

Feng, Luyao, Xin Liu, Nan Wang, Zhuli Shi, Yu Wang, Jianpeng Jia, Zhufeng Shi, Te Pu, and Peiwen Yang. 2025. "Genomic Analysis of Cadmium-Resistant and Plant Growth-Promoting Burkholderia alba Isolated from Plant Rhizosphere" Agronomy 15, no. 8: 1780. https://doi.org/10.3390/agronomy15081780

APA Style

Feng, L., Liu, X., Wang, N., Shi, Z., Wang, Y., Jia, J., Shi, Z., Pu, T., & Yang, P. (2025). Genomic Analysis of Cadmium-Resistant and Plant Growth-Promoting Burkholderia alba Isolated from Plant Rhizosphere. Agronomy, 15(8), 1780. https://doi.org/10.3390/agronomy15081780

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