Burkholderia glumae

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1. Classification

a. Higher order taxa

Bacteria; Pseudomonadota; Betaproteobacteria; Burkholderiales; Burkholderiaceae; Burkholderia

Species

NCBI: [1]

Burkholderia glumae

2. Description and significance

Burkholderia glumae, formerly known as Pseudomonas glumae, is a bacterial species recognized primarily for causing bacterial panicle blight (BPB) of rice (Oryza sativa) in tropical and subtropical rice-growing countries. BPB can reduce rice yields by as much as 75% [2] and can also cause wilting in tomato, eggplant, pepper, and sesame plants [3]. Recognized as an emerging threat to global rice production [4], B. glumae grows optimally at elevated temperature and humidity, suggesting that its prevalence will increase as global temperatures rise [5]. While B. glumae is not considered a human pathogen, one case of infection was reported in an immunodeficient infant in 2007, suggesting the potential for opportunistic pathogenicity in humans [10]. B. glumae also secretes the lipase LipA, which is used in the pharmaceutical industry to produce enantiopure compounds [7]. Despite advances in understanding B. glumae’s genome and virulence factors, gaps remain in understanding regulation of its pathogenicity, as well as mitigation strategies in the context of evolving climate conditions.

3. Genome structure

There are complete genomes of several B. glumae strains available. These include BGR1 [6], PG1 [7], BD_21G [8], and Chinese strains HN1/HN2 [9]. The genome size is roughly 6.7 to 7.0 Mbp (million base pairs) across strains, with a relatively high G+C % (approximately 68%), which is typical for the genus Burkholderia. B. glumae’s genomic structure is usually multipartite, with the genome of strain BGR1 containing two chromosomes and four plasmids, though these numbers often vary between strains [6], [25]. Protein-coding genes range from 6,000-7,000 per genome. Non-coding regions, including regulatory RNAs and intergenic spacers, are less well-characterized [6], [25].

Some genes of interest include quorum sensing (QS) regulons. All strains of B. glumae possess at least one QS system mediated by acyl-homoserine lactone (AHL). In particular, strain BGR1 uses a LuxI/LuxR homolog (designated TofI/TofR) with an AHL synthase encoded by the tofI gene, while strain BGPG1 is the only known strain of B. glumae to possess three distinct AHL synthase genes [10].

The toxoflavin biosynthetic gene cluster houses genes that are responsible for producing the phytotoxin toxoflavin. This compound plays a crucial role in BPB, as it is one of the main virulence factors in B. glumae [12]. The toxABCDE operon (consisting of genes toxA to E) codes for toxoflavin biosynthesis, while the toxFGHI operon (genes toxF to I) codes for a system of resistance-nodulation-division (RND)-like efflux transporters [20]. Both operons are regulated by the LysR-type regulatory protein ToxR, which uses toxoflavin as a coinducer, and by the transcriptional activator ToxJ, which is regulated by TofI/TofR quorum sensing [20].

B. glumae also has secretion systems important to its function. Multiple type VI secretion systems (T6SS) have distinct roles in inter-bacterial competition and plant virulence that enhance B. glumae’s ability to colonize and compete within the rice phyllosphere. The tssD1 gene found within a T6SS gene cluster in B. glumae is responsible for antibacterial effects; tssD1 expression levels increase in the presence of other bacterial taxa and will outcompete E. coli in vitro and pre-existing endophytic bacterial populations in Oryza sativa plants, driving down diversity and resulting in domination of B. glumae within the plant upon infection [13].

Genes coding for flagella are also present in B. glumae’s genome. Quorum sensing can activate flhDC, which is the master regulator of polar flagellum biosynthesis in B. glumae, allowing for swimming and swarming motilities [14].

4. Cell structure

Burkholderia glumae is a Gram-negative, rod-shaped, motile bacterium with two to four polar flagella [4]. Cells typically range from 0.5 to 0.7 µm in width and 1.5 to 2.5µm in length. B. glumae does not form spores [16] but produces surface structures such as pili and flagella, regulated in part by quorum sensing [10]. Scanning electron microscopy studies demonstrate cytoplasmic leakage and cell lysis due to increased permeability of the cell membrane upon exposure to ginger essential oil, despite the presence of lipopolysaccharides in the outer membrane, which provide increased protection against hydrophobic molecules such as essential oils [17].

5. Metabolic processes

B. glumae is a chemoorganoheterotroph, utilizing organic compounds for carbon and energy. It produces energy primarily via aerobic respiration using oxidative phosphorylation, a process that is moderated by quorum sensing, which will act as a metabolic brake through the transcriptional regulator QsmR when cells overproliferate and conditions become crowded [24]. Additionally, B. glumae performs glutamate uptake, which is vital for osmoregulation, especially in hypertonic environments [18]. Oxalic acid secretion maintains acidic conditions beneficial for quorum-sensing-mediated regulation of virulence. This is because an acidic pH is needed for the buildup of acyl-homoserine lactones, which act as signaling molecules in B. glumae’s quorum sensing system [15]. B. glumae also produces toxoflavin, a phytotoxin that induces reactive oxygen species, aiding in nutrient acquisition through disruption of rice cell components [12]. Additionally, B. glumae secretes the LipA lipase, which is important for pathogenicity [23] and is used in the pharmaceutical industry to generate enantiopure products [7]. B. glumae also synthesizes factors that enable biofilm formation and surface motility, such as rhamnolipids and type IV pili, respectively [10].

6. Ecology

B. glumae is predominantly found in rice-growing regions of tropical and subtropical Asia, including Thailand, India, South Korea, and parts of Southeast Asia [11], [16]. It has also been reported in the Americas and other rice cultivation areas. B. glumae primarily colonizes rice plants (Oryza sativa), initially in the floral structures’ spikelets, glumes, stamens and the gynoecium [19].

B. glumae grows optimally at warm temperatures (30–35 °C) and high humidity, conditions which occur during the rice-growing season [4], [19]. It is sensitive to environmental pH changes, relying on oxalic acid secretion to maintain acidification conducive to quorum sensing and toxin production [15]. Experimentally, agitation and nutrient-rich media (e.g., LB broth) support in vitro growth of B. glumae. However, B. glumae exhibits glutamate uptake to cope with osmotic fluctuations in its surroundings [18].

7. Pathology

B. glumae infection is the primary cause of bacterial panicle blight (BPB) of rice plants (Oryza sativa), symptoms of which include seedling rot, grain rot, leaf-sheath browning, spikelet sterility, and inhibition of seed germination [3], [19]. B. glumae is a seed-borne pathogen that can live endophytically within rice plants for up to a year [19].

B. glumae initiates infection by colonizing glume hairs at the base of the rice spikelet and subsequently invades the palea and lemma, allowing for bacterial cells to spread across the stamens and gynoecium [19]. Under conditions associated with rice-growing season, i.e. high temperatures and moisture, B. glumae infection can cause gynoecium wilt and pollen deformity and abortion in 10 days [19].

Virulence Factors

Toxoflavin is the principal toxin produced by B. glumae that is responsible for tissue damage and disease symptoms associated with BPB. Toxoflavin is an electron carrier between NADH and oxygen and induces oxidative stress in plant cells through hydrogen peroxide formation [15]. Genes for toxoflavin biosynthesis and transport are encoded in the toxABCDE and toxFGHI operons, respectively; these operons are regulated by ToxR, a LysR-type regulator that uses toxoflavin as a coinducer, and ToxJ, a transcriptional activator controlled by TofR/TofI quorum sensing [20].

Additional virulence factors associated with quorum sensing include:

• Motility: Quorum sensing controls the transcriptional regulator QsmR, which regulates flhDC, the master regulator of polar flagellum genes in B. glumae. Flagellum-deficient B. glumae mutants lose swimming and swarming motility and fail to induce disease in rice plants despite being able to produce toxoflavin, suggesting that flagellum formation and motility are essential for B. glumae virulence [21].
• Oxalic Acid Secretion: Oxalic acid maintains an acidic microenvironment, which is essential for quorum sensing and toxoflavin synthesis. If oxalic acid biosynthesis is disrupted, B. glumae becomes unable to neutralize alkaline pH and therefore cannot accumulate AHLs during growth, which in turn disrupts quorum sensing and associated processes such as toxoflavin synthesis [15].
• Lipase: B. glumae secretes a lipase encoded by the lipA gene, a process that is regulated by quorum sensing. Mutants lacking lipA show drastic loss of ability to induce disease symptoms, though the mechanisms of QS regulation and phytopathogenicity associated with the gene remain unknown [23].
• CRISPR-Cas: A few B. glumae isolates contain CRISPR-Cas systems, hypothesized to assist with virulence, biofilm formation, and cell immunity, though their actual function remains unknown. AHL synthase mutants showed notable decreases in transcription of CRISPR clusters, indicating that the regulation of these systems is linked to quorum sensing [10].

Other virulence factors include type III secretion systems (T3SSs), type VI secretion systems (T6SSs), and polygalacturonases [4], [10]. B. glumae also exhibits high genetic diversity within populations due to prophage-driven horizontal gene transfer, potentially complicating mitigation strategies [11].

Human Pathogenicity

B. glumae is not considered a human pathogen. However, in 2007, it was isolated from lung lesions in an immunodeficient infant, demonstrating its potential to act as an opportunistic pathogen in humans [22].

8. Current Research

Recent research on B. glumae has focused on understanding molecular mechanisms of virulence, quorum sensing, and exploring disease management options.

Molecular Insights into Quorum Sensing and Virulence Regulation

Genome-wide RNA-seq was used to determine the functions of the three QS systems in the B. glumae PG1 strain. Researchers created mutants lacking each of the three Al-1 synthase genes, ΔbgaI1, ΔbgaI2, and ΔbgaI3, and compared their transcriptomes to the wild-type strain during the transition to stationary phase [10]. They found that each mutant showed extensive changes in gene expression with most differences involving motility, secretion systems, and metabolic pathways. This work marked an advance in understanding the mechanisms that govern pathogenicity. Other research found that the membrane protein ΔdbcA is essential for maintaining the acidic conditions that B. glumae needs for proper quorum sensing and toxoflavin production [15]. When ΔdbcA was deleted, the mutant could not secrete oxalic acid, causing the environment to become too alkaline. The high pH inactivated AHL quorum sensing signals and reduced the expression of regulation genes [15]. This demonstrates that dbcA and the oxalic acid pathway are specific targets for disrupting virulence.

Advances in Disease Control

Biological and chemical management strategies are being tested to combat BPB. Ginger essential oil has been identified as an antibacterial against B. glumae, with the ability to disrupt its cell membrane, inhibit biofilms, and create bactericidal effects [17]. Results suggest a potential eco-friendly alternative to pesticides. Other research studied the use of nano copper and biocontrol agents, such as Bacillus amyloliquefaciens and Pseudomonas fluorescens, to suppress B. glumae [5]. Nano copper treatment resulted in enzymatic antioxidant activity and upregulation of defense-related genes OsPR2 and OsPAL1 in O. sativa plants, while showing greater inhibition of B. glumae than the biocontrol agents [5]. In another study, transgenic rice plants engineered to express the enzyme TxeA demonstrated increased resistance to BPB by degrading toxoflavin produced by B. glumae [12]. Although other virulence factors of B. glumae remained unaffected, this finding suggests a possible step towards developing B. glumae resistance in crops.

References

[1] Schoch, C.L., et al. (2020). Taxonomy Browser (Burkholderia glumae). National Center for Biotechnology Information. U.S. National Library of Medicine.

[2] Shew, A. M., Durand-Morat, A., Nalley, L.L., Zhou, X.G., Rojas, C., & Thoma, G. (2019). Warming increases Bacterial Panicle Blight (Burkholderia glumae) occurrences and impacts on USA rice production. PLoS One, 14(7). https://doi.org/10.1371/journal.pone.0219199

Edited by students of Jennifer Bhatnagar for BI 311 General Microbiology, 2025, Boston University.