Burkholderia gladioli explained

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 the microbiome of many animals. It was formerly known as Pseudomonas marginata.

Burkholderia gladioli synthesizes several inhibitory substances, among them gladiolin, bongkrek acid, enacyloxin, 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 mitochondria disrupting 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]

Etymology

The genus Burkholderia is named after scientist Walter H. Burkholder, who discovered an organism linked to disease in the skin of onions.[11]

Gladioli refers to the plant genus Gladiolus, which is grown ornamentally around the world, and where the fungus can cause rot.[12] The flower is named gladiolus "little sword" from gladius "sword", due to the shape of the leaves.

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 300 bp.

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.

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 °C. 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 typeTestCharacteristics
Colony charactersSize
TypeRound
ColorPale Yellow
Shape
Morphological charactersShapeSlightly Bent Rods
Physiological charactersMotility+
Growth at 6.5% NaCl
Biochemical charactersGram staining-
Oxidased
Catalase
Oxidative-Fermentative
Motility+
Methyl Red
Voges-Proskauer
Indole
H2S Production
Urease
Nitrate reductase
β-Galactosidase
Hydrolysis ofGelatin+
Starch-
Casein
Utilization ofGlycerol
Galactose+
D-Glucose+
D-Fructose+
D-Mannose+
Mannitol+

Pathology

In plants

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.

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. 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]

Virulence factors

The primary system responsible for the disease caused by Burkholderia gladioli is a type two secretion pathway.[20]  An experiment performed by Chowdhury and Heinemann revealed that six strains of B. gladioli that were avirulent still contained the capacity for mushroom growth inhibition without having the characteristics of mushroom tissue degradation. 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.

External links

Notes and References

  1. Book: Coenye T, Vandamme P . 2007 . Burkholderia: Molecular Microbiology and Genomics. Horizon Bioscience . Horizon Bioscience . 978-1-904933-28-1.
  2. Stoyanova M, Pavlina I, Moncheva P, Bogatzevska N . March 2007 . Biodiversity and Incidence of Burkholderia Species . Biotechnology & Biotechnological Equipment. 21 . 3 . 306–310 . 10.1080/13102818.2007.10817465 . free .
  3. Song L, Jenner M, Masschelein J, Jones C, Bull MJ, Harris SR, Hartkoorn RC, Vocat A, Romero-Canelon I, Coupland P, Webster G, Dunn M, Weiser R, Paisey C, Cole ST, Parkhill J, Mahenthiralingam E, Challis GL . 6 . 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 . June 2017 . 28528545 . 10.1021/jacs.7b03382 . free .
  4. Subík J, Behún M . Effect of bongkrekic acid on growth and metabolism of filamentous fungi . Archiv für Mikrobiologie . 97 . 1 . 81–88 . April 1974 . 4857952 . 10.1007/BF00403048 . 1974ArMic..97...81S . 11639700 .
  5. Ross C, Opel V, Scherlach K, Hertweck C . Biosynthesis of antifungal and antibacterial polyketides by Burkholderia gladioli in coculture with Rhizopus microsporus . Mycoses . 57 . 48–55 . December 2014 . Suppl 3 . 25250879 . 10.1111/myc.12246 . free .
  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. 10.5109/24188. free.
  7. Marín-Cevada V, Muñoz-Rojas J, Caballero-Mellado J, Mascarúa-Esparza MA, Castañeda-Lucio M, Carreño-López R, Estrada-De Los Santos P, Fuentes-Ramírez LE . 6 . 2012. Antagonistic interactions among bacteria inhabiting pineapple. Applied Soil Ecology. 61. 230–235. 10.1016/j.apsoil.2011.11.014. 2012AppSE..61..230M .
  8. Book: Prescott LM, Harley JP, Klein DA . 2005 . Bacteria: The Proteobacteria . Microbiology . 6th . 482–483 . New York . McGraw-Hill . 978-0-07-295175-2.
  9. Jiao Z, Kawamura Y, Mishima N, Yang R, Li N, Liu X, Ezaki T . 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 . 2003 . 14695441 . 10.1111/j.1348-0421.2003.tb03465.x . free .
  10. [NCBI]
  11. Web site: Genus burkholderia . 26 February 2022 . LPSN - List of Prokaryotic names with Standing in Nomenclature . DSMZ-German Collection of Microorganisms and Cell Cultures GmbH .
  12. Web site: Species burkholderia gladioli . 22 February 2022 . LPSN - List of Prokaryotic names with Standing in Nomenclature . DSMZ-German Collection of Microorganisms and Cell Cultures GmbH.
  13. Graves M, Robin T, Chipman AM, Wong J, Khashe S, Janda JM . Four additional cases of Burkholderia gladioli infection with microbiological correlates and review . Clinical Infectious Diseases . 25 . 4 . 838–842 . October 1997 . 9356798 . 10.1086/515551 . free .
  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 . 10.1007/PL00013080. 2002JGPP...68..220F . 20789383 .
  15. Seo YS, Lim J, Choi BS, Kim H, Goo E, Lee B, Lim JS, Choi IY, Moon JS, Kim J, Hwang I . 6 . Complete genome sequence of Burkholderia gladioli BSR3 . Journal of Bacteriology . 193 . 12 . 3149 . June 2011 . 21478339 . 3133191 . 10.1128/JB.00420-11 .
  16. Web site: Page has moved, College of ACES :: University of Illinois. 2008-04-19. https://web.archive.org/web/20060901064134/http://web.aces.uiuc.edu/vista/pdf_pubs/651.pdf. 2006-09-01. dead.
  17. Khan SU, Arroglia AC, Gordon SM . Significance of airway colonization by Burkholderia gladioli in lung transplant candidates . Chest . 114 . 2 . 658 . August 1998 . 9726771 . 10.1378/chest.114.2.658 .
  18. News: Mozambique: Mass Poisoning Caused By Bacterial Contamination . . 4 November 2015 . 7 February 2016.
  19. Dursun A, Zenciroglu A, Karagol BS, Hakan N, Okumus N, Gol N, Tanir G . Burkholderia gladioli sepsis in newborns . European Journal of Pediatrics . 171 . 10 . 1503–1509 . October 2012 . 22648018 . 10.1007/s00431-012-1756-y . 12429995 . free .
  20. Chowdhury PR, Heinemann JA . 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 . May 2006 . 16672503 . 1472315 . 10.1128/AEM.72.5.3558-3565.2006 . 2006ApEnM..72.3558C .