Burkholderia gladioli

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Burkholderia gladioli
Scientific classification OOjs UI icon edit-ltr.svg
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 gladioliSeverini 1913
Burkholderia cocovenerans(van Damme et al. 1960) Gillis et al..
Pseudomonas cocovenenansvan Damme et al. 1960
Pseudomonas antimicrobicaAttafuah and Bradbury 1990
Pseudomonas marginata(McCulloch) Stapp
Pseudomonas farinofermentansNaixin
Pseudomonas alliicola(Burkholder 1942) Starr and Burkholder 1942

Contents

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. [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 °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

Gladiolus plant inoculated with B. gladioli Gladiolus plant inoculated with B. gladioli.JPG
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.[ citation needed ]

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]

Gladiolin, a novel macrolide produced by B. gladioli strain BCC0238, was found to have promising antibiotic activity against Mycobacterium tuberculosis in a 2017 study; the compound, which inhibits RNA polymerase, is structurally and functionally similar to etnangien, a macrolide synthesised by the bacterium Sorangium cellulosum which has also demonstrated potency against Mycobacterium, but is more unstable than gladiolin. In the study, gladiolin was found to have low mammalian cytotoxicity and good activity against M. tuberculosis isolates, suggesting that it may be a useful starting point in developing new antibiotics to treat multidrug resistant tuberculosis infections. [19]

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. [20]

Virulence factors

The primary system responsible for the disease caused by Burkholderia gladioli is a type two secretion pathway. [21]  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. [21]

Related Research Articles

<i>Pseudomonas</i> Genus of Gram-negative bacteria

Pseudomonas is a genus of Gram-negative bacteria belonging to the family Pseudomonadaceae in the class Gammaproteobacteria. The 313 members of the genus demonstrate a great deal of metabolic diversity and consequently are able to colonize a wide range of niches. Their ease of culture in vitro and availability of an increasing number of Pseudomonas strain genome sequences has made the genus an excellent focus for scientific research; the best studied species include P. aeruginosa in its role as an opportunistic human pathogen, the plant pathogen P. syringae, the soil bacterium P. putida, and the plant growth-promoting P. fluorescens, P. lini, P. migulae, and P. graminis.

<i>Mycobacterium tuberculosis</i> Species of pathogenic bacteria that causes tuberculosis

Mycobacterium tuberculosis, also known as Koch's bacillus, is a species of pathogenic bacteria in the family Mycobacteriaceae and the causative agent of tuberculosis. First discovered in 1882 by Robert Koch, M. tuberculosis has an unusual, waxy coating on its cell surface primarily due to the presence of mycolic acid. This coating makes the cells impervious to Gram staining, and as a result, M. tuberculosis can appear weakly Gram-positive. Acid-fast stains such as Ziehl–Neelsen, or fluorescent stains such as auramine are used instead to identify M. tuberculosis with a microscope. The physiology of M. tuberculosis is highly aerobic and requires high levels of oxygen. Primarily a pathogen of the mammalian respiratory system, it infects the lungs. The most frequently used diagnostic methods for tuberculosis are the tuberculin skin test, acid-fast stain, culture, and polymerase chain reaction.

<i>Mycobacterium</i> Genus of bacteria

Mycobacterium is a genus of over 190 species in the phylum Actinomycetota, assigned its own family, Mycobacteriaceae. This genus includes pathogens known to cause serious diseases in mammals, including tuberculosis and leprosy in humans. The Greek prefix myco- means 'fungus', alluding to this genus' mold-like colony surfaces. Since this genus has cell walls with a waxy lipid-rich outer layer containing high concentrations of mycolic acid, acid-fast staining is used to emphasize their resistance to acids, compared to other cell types.

Nontuberculous mycobacteria (NTM), also known as environmental mycobacteria, atypical mycobacteria and mycobacteria other than tuberculosis (MOTT), are mycobacteria which do not cause tuberculosis or leprosy/Hansen's disease. NTM are able to cause pulmonary diseases that resemble tuberculosis. Mycobacteriosis is any of these illnesses, usually meant to exclude tuberculosis. They occur in many animals, including humans and are commonly found in soil and water.

Mycobacterium avium subspecies paratuberculosis (MAP) is an obligate pathogenic bacterium in the genus Mycobacterium. It is often abbreviated M. paratuberculosis or M. avium ssp. paratuberculosis. It is the causative agent of Johne's disease, which affects ruminants such as cattle, and suspected causative agent in human Crohn's disease and rheumatoid arthritis. The type strain is ATCC 19698.

<i>Burkholderia</i> Genus of bacteria

Burkholderia is a genus of Pseudomonadota whose pathogenic members include the Burkholderia cepacia complex, which attacks humans and Burkholderia mallei, responsible for glanders, a disease that occurs mostly in horses and related animals; Burkholderia pseudomallei, causative agent of melioidosis; and Burkholderia cepacia, an important pathogen of pulmonary infections in people with cystic fibrosis (CF). Burkholderia species is also found in marine environments. S.I. Paul et al. (2021) isolated and characterized Burkholderia cepacia from marine sponges of the Saint Martin's Island of the Bay of Bengal, Bangladesh.

<i>Burkholderia cepacia</i> complex Species of bacterium

Burkholderia cepacia complex (BCC) is a species complex consisting of Burkholderia cepacia and at least 20 different biochemically similar species of Gram-negative bacteria. They are catalase-producing and lactose-nonfermenting. Members of BCC are opportunistic human pathogens that most often cause pneumonia in immunocompromised individuals with underlying lung disease. Patients with sickle-cell haemoglobinopathies are also at risk. The species complex also attacks young onion and tobacco plants, and displays a remarkable ability to digest oil.

<i>Dickeya dadantii</i> Disease-causing Gram Negative Bacillus

Dickeya dadantii is a Gram-negative bacillus that belongs to the family Pectobacteriaceae. It was formerly known as Erwinia chrysanthemi but was reassigned as Dickeya dadantii in 2005. Members of this family are facultative anaerobes, able to ferment sugars to lactic acid, have nitrate reductase, but lack oxidases. Even though many clinical pathogens are part of the order Enterobacterales, most members of this family are plant pathogens. D. dadantii is a motile, nonsporing, straight rod-shaped cell with rounded ends, much like the other members of the genus, Dickeya. Cells range in size from 0.8 to 3.2 μm by 0.5 to 0.8 μm and are surrounded by numerous flagella (peritrichous).

<i>Burkholderia pseudomallei</i> Species of bacterium

Burkholderia pseudomallei is a Gram-negative, bipolar, aerobic, motile rod-shaped bacterium. It is a soil-dwelling bacterium endemic in tropical and subtropical regions worldwide, particularly in Thailand and northern Australia. It was reported in 2008 that there had been an expansion of the affected regions due to significant natural disasters, and it could be found in Southern China, Hong Kong, and countries in the Americas. B. pseudomallei, amongst other pathogens, has been found in monkeys imported into the United States from Asia for laboratory use, posing a risk that the pathogen could be introduced into the country.

<i>Burkholderia mallei</i> Species of bacterium

Burkholderia mallei is a Gram-negative, bipolar, aerobic bacterium, a human and animal pathogen of genus Burkholderia causing glanders; the Latin name of this disease (malleus) gave its name to the species causing it. It is closely related to B. pseudomallei, and by multilocus sequence typing it is a subspecies of B. pseudomallei.B. mallei evolved from B. pseudomallei by selective reduction and deletions from the B. pseudomallei genome. Unlike B. pseudomallei and other genus members, B. mallei is nonmotile; its shape is coccobacillary measuring some 1.5–3.0 μm in length and 0.5–1.0 μm in diameter with rounded ends.

<i>Burkholderia cenocepacia</i> Species of bacterium

Burkholderia cenocepacia is a Gram-negative, rod-shaped bacterium that is commonly found in soil and water environments and may also be associated with plants and animals, particularly as a human pathogen. It is one of over 20 species in the Burkholderia cepacia complex (Bcc) and is notable due to its virulence factors and inherent antibiotic resistance that render it a prominent opportunistic pathogen responsible for life-threatening, nosocomial infections in immunocompromised patients, such as those with cystic fibrosis or chronic granulomatous disease. The quorum sensing systems CepIR and CciIR regulate the formation of biofilms and the expression of virulence factors such as siderophores and proteases. Burkholderia cenocepacia may also cause disease in plants, such as in onions and bananas. Additionally, some strains serve as plant growth-promoting rhizobacteria.

<i>Xanthomonas campestris</i> Species of bacterium

Xanthomonas campestris is a gram-negative, obligate aerobic bacterium that is a member of the Xanthomonas genus, which is a group of bacteria that are commonly known for their association with plant disease. This species includes Xanthomonas campestris pv. campestris, the cause of black rot in brassicas, one of the most important diseases of brassicas worldwide.

<i>Mycobacteroides abscessus</i> Species of bacterium

Mycobacteroides abscessus is a species of rapidly growing, multidrug-resistant, nontuberculous mycobacteria (NTM) that is a common soil and water contaminant. Although M. abscessus most commonly causes chronic lung infection and skin and soft tissue infection (SSTI), it can also cause infection in almost all human organs, mostly in patients with suppressed immune systems. Amongst NTM species responsible for disease, infection caused by M. abscessus complex are more difficult to treat due to antimicrobial drug resistance.

<i>Pseudomonas syringae</i> Species of bacterium

Pseudomonas syringae is a rod-shaped, Gram-negative bacterium with polar flagella. As a plant pathogen, it can infect a wide range of species, and exists as over 50 different pathovars, all of which are available to researchers from international culture collections such as the NCPPB, ICMP, and others.

<i>Ralstonia</i> Genus of bacteria

Ralstonia is a genus of bacteria, previously included in the genus Pseudomonas. It is named after the American bacteriologist Ericka Ralston. Ericka Ralston was born in 1944 in Saratoga, California, and died in 2015 in Sebastopol, California. While in graduate school at the University of California at Berkeley, she identified 20 strains of Pseudomonas which formed a phenotypical homologous group, and named them Pseudomonas pickettii, after M.J. Pickett in the Department of Bacteriology at the University of California at Los Angeles, from whom she had received the strains. Later, P. pickettii was transferred to the new genus Ralstonia, along with several other species. She continued her research into bacterial pathogenesis under the name of Ericka Barrett while a professor of microbiology at the University of California at Davis from 1977 until her retirement in 1996.

<i>Xanthomonas</i> Genus of bacteria

Xanthomonas is a genus of bacteria, many of which cause plant diseases. There are at least 27 plant associated Xanthomonas spp., that all together infect at least 400 plant species. Different species typically have specific host and/or tissue range and colonization strategies.

Curtobacterium flaccumfaciens is a Gram-positive bacterium that causes disease on a variety of plants. Gram-positive bacteria characteristics include small irregular rods, lateral flagella, the ability to persist in aerobic environments, and cells containing catalase. In the interest of studying pathogenicity in plants, this species is broken down further into pathovars, which help to better describe the pathogen.

<span class="mw-page-title-main">Pathogenic bacteria</span> Disease-causing bacteria

Pathogenic bacteria are bacteria that can cause disease. This article focuses on the bacteria that are pathogenic to humans. Most species of bacteria are harmless and are often beneficial but others can cause infectious diseases. The number of these pathogenic species in humans is estimated to be fewer than a hundred. By contrast, several thousand species are part of the gut flora present in the digestive tract.

Black rot, caused by the bacterium Xanthomonas campestris pv. campestris (Xcc), is considered the most important and most destructive disease of crucifers, infecting all cultivated varieties of brassicas worldwide. This disease was first described by botanist and entomologist Harrison Garman in Lexington, Kentucky, US in 1889. Since then, it has been found in nearly every country in which vegetable brassicas are commercially cultivated.

In biology, a pathogen, in the oldest and broadest sense, is any organism or agent that can produce disease. A pathogen may also be referred to as an infectious agent, or simply a germ.

References

  1. 1 2 3 Coenye T, Vandamme P (2007). Burkholderia: Molecular Microbiology and Genomics. Horizon Bioscience. Horizon Bioscience. ISBN   978-1-904933-28-1.
  2. 1 2 3 Stoyanova M, Pavlina I, Moncheva P, Bogatzevska N (March 2007). "Biodiversity and Incidence of Burkholderia Species". Biotechnology & Biotechnological Equipment. 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. Bibcode:1974ArMic..97...81S. 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. Bibcode:2012AppSE..61..230M. 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. 1 2 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. Bibcode:2002JGPP...68..220F. 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. ↑ Song, Lijiang; Jenner, Matthew; Masschelein, Joleen; Jones, Cerith; Bull, Matthew J.; Harris, Simon R.; Hartkoorn, Ruben C.; Vocat, Anthony; Romero-Canelon, Isolda; Coupland, Paul; Webster, Gordon; Dunn, Matthew; Weiser, Rebecca; Paisey, Christopher; Cole, Stewart T. (2017-06-14). "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. ISSN   1520-5126. PMID   28528545.
  20. ↑ 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.
  21. 1 2 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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