Burkholderia gladioli

Burkholderia gladioli is a species of aerobic gram-negative rod-shaped bacteria[1] that causes disease in both humans and plants. It can also live in symbiosis with plants and fungi[2] and is found in soil, water, the rhizosphere, and in many animals. It was formerly known as Pseudomonas marginata.

Burkholderia gladioli
Scientific classification
Domain: Bacteria
Phylum: Pseudomonadota
Class: Betaproteobacteria
Order: Burkholderiales
Family: Burkholderiaceae
Genus: Burkholderia
Species:
B. gladioli
Binomial name
Burkholderia gladioli
(Zopf 1885)
Yabuuchi et al. 1993
Type strain
ATCC 10248
CCUG 1782
CFBP 2427
CIP 105410
DSM 4285
HAMBI 2157
ICMP 3950
JCM 9311
LMG 2216
NBRC 13700
NCCB 38018
NCPPB 1891
NCTC 12378
NRRL B-793
Synonyms

Pseudomonas gladioli Severini 1913
Burkholderia cocovenerans (van Damme et al. 1960) Gillis et al..
Pseudomonas cocovenenans van Damme et al. 1960
Pseudomonas antimicrobica Attafuah and Bradbury 1990
Pseudomonas marginata (McCulloch) Stapp
Pseudomonas farinofermentans Naixin
Pseudomonas alliicola (Burkholder 1942) Starr and Burkholder 1942

Burkholderia gladioli synthesizes several inhibitory substances, among them gladiolin, bongkrek acid, enaxyloxin, and toxoflavin.[3][4][5][6] Those molecules might participate in antagonistic interactions with other microbes in the environment where they grow.[7] One pathovariety, growing on coconut pulp, produces the respiratory toxin bongkrek acid which can cause fatal poisoning in humans.

Nomenclature

The members of the genus Burkholderia were formerly classified as Pseudomonas, but Burkholderia was one of the seven genera that arose when Pseudomonas was divided based on rRNA differences.[8] Burkholderia gladioli is closely related to, and often mistaken for, a member of the Burkholderia cepacia complex. This includes ten closely related species, which are all plant pathogens.

Burkholderia gladioli is divided into several pathovars:[9]

  • B. gladioli pv. gladioli causes gladiolus rot
  • B. g. pv. alliicola causes onion bulb rot
  • B. g. pv.agaricicola causes soft rot in mushrooms
  • B. g. pv. cocovenerans (sometimes written as cocovenenans) spoils coconut pulp[10]

Etymology

Burkholderia - Named after the scientist (bacteriologist) that discovered an organism linked to disease in the skin of onions.[11]

Gladioli - Small sword, of a lily; used within botany.[12]

Identification

Burkholderia are motile, Gram negative rods that may be straight or slightly curved. They are aerobic, catalase positive, urease positive, nonsporeformers. They grow on MacConkey agar, but do not ferment the lactose. Burkholderia gladioli can be distinguished from the other Burkholderia because it is oxidase negative [1] B. gladioli is indole negative, nitrate negative, and lysine decarboxylation negative.[13]

On the molecular level, PCR can be used to distinguish between the different Burkholderia species. According to Furuya et al., the ribosomal RNA gene is highly conserved and universally distributed in all living things, and therefore difference in the DNA sequences between 16S and 23S rRNA genes can be used to differentiate between the species.[14]

The primers used for the amplification of the 16S to 23S region in the B. gladioli genome are as follows: GLA-f 5'-(CGAGCTAATACCGCGAAA)-3' and GLA-r 5'-(AGACTCGAGTCAACTGA)-3' Using these primers for PCR results in an amplicon of approximately 300bp.[14]

All members of the genus Burkholderia have multireplicon genomes. They are able to keep "essential housekeeping" genes on the largest chromosome. This largest chromosome has a single origin of replication. The gene order and GC composition is conserved as well. Members of Burkholderia are able to capture and retain foreign DNA. The foreign DNA can be detected by looking for atypical GC context areas. One of the first foreign DNA segments detected this way encoded for virulence.[1]

The B. gladioli genome consists of 6 major holders of genetic information: two chromosomes and four plasmids. The entire genome amounts to 9.06 Mb (Million Bases) with 89.64% of the genome - including non-coding regions - on the two chromosomes.[15]

Characteristics

All species of the genus Burkholderia - except for B. mallei - display a form of motility when suspended within liquid. Being Gram-Negative, B. gladioli will not be stained by the Crystal Violet - Iodine complex, but will be counter stained red by Safranin. The optimal growth temperature on a Nutrient Agar plate is 30-35 degree Celsius. The Genus Burkholderia (including B. gladioli) shows a remarkable amount of diversity of metabolism of carbohydrates and other organic compounds. B. gladioli is able to more acids than is typical for its genus.

Test type Test Characteristics
Colony characters Size
Type Round
Color Pale Yellow
Shape
Morphological characters Shape Slightly Bent Rods
Physiological characters Motility +
Growth at 6.5% NaCl
Biochemical characters Gram staining -
Oxidase d
Catalase
Oxidative-Fermentative
Motility +
Methyl Red
Voges-Proskauer
Indole
H2S Production
Urease
Nitrate reductase
β-Galactosidase
Hydrolysis of Gelatin +
Starch -
Casein
Utilization of Glycerol
Galactose +
D-Glucose +
D-Fructose +
D-Mannose +
Mannitol +

Pathology

In plants
Gladiolus plant inoculated with B. gladioli

B. gladioli has been identified as a plant pathogen in onions, gladiolus, iris, and together with Burkholderia glumae affect the rice. It was originally described to have caused rot of gladiolus corms. The bulbs can become water soaked and decay.

Some other common symptoms of infected plants can be seen in the leaves. The leaves contain brown lesions, and they may become watersoaked. Other symptoms are the wilting and/or rot of roots, stems, and petals. B. gladioli has also been identified as the causative agent in leaf-sheath browning in gladiolas and onions. Sometimes, the whole plant decays.[2]

One widespread plant disease caused by B. gladioli is called scab. It can be seen on gladiolus corms as water-soaked brown spots, outlined in yellow. Eventually, they can become hollow and surrounded by scabs. If the scabs fall off, they leave behind cavities or lesions.[16]

In humans

B. gladioli in humans is an opportunistic pathogen that is an important agent for hospital-associated infections. It has recently appeared as a severe pathogen in patients with cystic fibrosis, causing severe pulmonary infections.[2] Though it is still a fairly uncommon pathogen, its presence is associated with a poor prognosis. It has also colonized the respiratory tracts of patients with granulomatous disease. In lung transplant patients, infection can be fatal as patients have developed bacteremia and sterile wound infections as a result.[17]

Tempe bongkrèk, a variation of tempeh prepared with coconut, is susceptible to B. gladioli pathovar. cocovenenans contamination. Contaminated tempe bongkrèk can contain lethal amounts of highly toxic bongkrek acid and toxoflavin.

B. gladioli was implicated in the 2015 deaths of 75 people, in Mozambique, who had consumed a home-brewed beer made from corn flour that was contaminated with the bacterium.[18]

A 3-year long study period of neonatal and nosocomial sepsis yielded 14 patients (out of approximately 3784) with isolated positive colonies of B. gladioli from blood cultures. During this time, symptoms of the sepsis caused by the B. gladioli infection included congenital leukemia, pneumonia, and several other respiratory malfunctions. A mortality rate of 7% is linked to the B. gladioli infections present during the time of study.[19]

Systems of Pathology

The primary system responsible for the disease caused by B. gladioli sp. is a type two secretion pathway.[20] An experiment performed by Chowdhury and Heinemann revealed that six strains of Burkholderia gladioli that were avirulent still contained the capacity for mushroom growth inhibition without having the characteristics of mushroom tissue degradations. This led the two to believe the genetic factors that cause the microbe to have the ability to generate the cavity disease within an organism can be separated from the factors that inhibit mycelium growth within said mushrooms.[20]

References
  1. Coenye T, Vandamme P (2007). Burkholderia: Molecular Microbiology and Genomics. Horizon Bioscience. ISBN 978-1-904933-28-1.
  2. Stoyanova M, Pavlina I, Moncheva P, Bogatzevska N (March 2007). "Biodiversity and Incidence of Burkholderia Species". Biotechnol. & Biotechnol. Eq. 21 (3): 306–310. doi:10.1080/13102818.2007.10817465.
  3. Song L, Jenner M, Masschelein J, Jones C, Bull MJ, Harris SR, et al. (June 2017). "Discovery and Biosynthesis of Gladiolin: A Burkholderia gladioli Antibiotic with Promising Activity against Mycobacterium tuberculosis". Journal of the American Chemical Society. 139 (23): 7974–7981. doi:10.1021/jacs.7b03382. PMID 28528545.
  4. Subík J, Behún M (April 1974). "Effect of bongkrekic acid on growth and metabolism of filamentous fungi". Archiv für Mikrobiologie. 97 (1): 81–88. doi:10.1007/BF00403048. PMID 4857952. S2CID 11639700.
  5. Ross C, Opel V, Scherlach K, Hertweck C (December 2014). "Biosynthesis of antifungal and antibacterial polyketides by Burkholderia gladioli in coculture with Rhizopus microsporus". Mycoses. 57 Suppl 3: 48–55. doi:10.1111/myc.12246. PMID 25250879.
  6. Furuya N, Iiyama K, Shiozaki N, Matsuyama N (1997). "Phytotoxin produced by Burkholderia gladioli". Journal of the Faculty of Agriculture, Kyushu University. 42: 33–37. doi:10.5109/24188.
  7. Marín-Cevada V, Muñoz-Rojas J, Caballero-Mellado J, Mascarúa-Esparza MA, Castañeda-Lucio M, Carreño-López R, et al. (2012). "Antagonistic interactions among bacteria inhabiting pineapple". Applied Soil Ecology. 61: 230–235. doi:10.1016/j.apsoil.2011.11.014.
  8. Prescott LM, Harley JP, Klein DA (2005). "Bacteria: The Proteobacteria". Microbiology (6th ed.). New York: McGraw-Hill. pp. 482–483. ISBN 978-0-07-295175-2.
  9. Jiao Z, Kawamura Y, Mishima N, Yang R, Li N, Liu X, Ezaki T (2003). "Need to differentiate lethal toxin-producing strains of Burkholderia gladioli, which cause severe food poisoning: description of B. gladioli pathovar cocovenenans and an emended description of B. gladioli". Microbiology and Immunology. 47 (12): 915–925. doi:10.1111/j.1348-0421.2003.tb03465.x. PMID 14695441.
  10. NCBI: Burkholderia gladioli pv. cocovenerans (no rank)
  11. "Genus burkholderia". LPSN - List of Prokaryotic names with Standing in Nomenclature. DSMZ-German Collection of Microorganisms and Cell Cultures GmbH. Retrieved 26 February 2022.
  12. "Species burkholderia gladioli". LPSN - List of Prokaryotic names with Standing in Nomenclature. DSMZ-German Collection of Microorganisms and Cell Cultures GmbH. Retrieved 22 February 2022.
  13. Graves M, Robin T, Chipman AM, Wong J, Khashe S, Janda JM (October 1997). "Four additional cases of Burkholderia gladioli infection with microbiological correlates and review". Clinical Infectious Diseases. 25 (4): 838–842. doi:10.1086/515551. PMID 9356798.
  14. Furuya N, Ura H, Iiyama K, Matsumoto M, Takeshita M, Takanami Y (2002). "Specific Oligonucleotide Primers Based on Sequences of the 16S-23S rDNA Spacer Region for the Detection of Burkholderia gladioli by PCR". J. Gen. Plant Pathol. 68 (3): 220–224. doi:10.1007/PL00013080. S2CID 20789383.
  15. Seo YS, Lim J, Choi BS, Kim H, Goo E, Lee B, et al. (June 2011). "Complete genome sequence of Burkholderia gladioli BSR3". Journal of Bacteriology. 193 (12): 3149. doi:10.1128/JB.00420-11. PMC 3133191. PMID 21478339.
  16. "Page has moved, College of ACES :: University of Illinois" (PDF). Archived from the original (PDF) on 2006-09-01. Retrieved 2008-04-19.
  17. Khan SU, Arroglia AC, Gordon SM (August 1998). "Significance of airway colonization by Burkholderia gladioli in lung transplant candidates". Chest. 114 (2): 658. doi:10.1378/chest.114.2.658. PMID 9726771.
  18. "Mozambique: Mass Poisoning Caused By Bacterial Contamination". allafrica.com. 4 November 2015. Retrieved 7 February 2016.
  19. Dursun A, Zenciroglu A, Karagol BS, Hakan N, Okumus N, Gol N, Tanir G (October 2012). "Burkholderia gladioli sepsis in newborns". European Journal of Pediatrics. 171 (10): 1503–1509. doi:10.1007/s00431-012-1756-y. PMID 22648018. S2CID 12429995.
  20. Chowdhury PR, Heinemann JA (May 2006). "The general secretory pathway of Burkholderia gladioli pv. agaricicola BG164R is necessary for cavity disease in white button mushrooms". Applied and Environmental Microbiology. 72 (5): 3558–65. Bibcode:2006ApEnM..72.3558C. doi:10.1128/AEM.72.5.3558-3565.2006. PMC 1472315. PMID 16672503.
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