Basidiobolus

The wonderful world of Basidiobolus

Hello, and welcome to my blog about this very interesting fungus; Basidiobolus. My name is Michelle Austin, and I am currently working on my masters in biology at Western Illinois University. My research focuses on Geomyces destructans and other keratinophilic fungi species but I have a passion for all fungi. I am currently taking medical mycology and have become quite interested in fungal pathogens such as Basidiobolus. I hope you enjoy reading about this fungus as much as I have.
  

General Description of Basidiobolus

Taxonomic Classification:

Kingdom: Fungi
Phylum: Zygomycota
Subphylum: Zygomycotina
Class: Zygomycetes
Order: Entomophthorales
Family: Basidiobolaceae
Genus: Basidiobolus 

Zygomycota fungi make up about 1% of the total number of fungi inhabiting the world yet these fungi are the primary colonizers of most substrates. Basidiobolus is a member of this phylum and is a filamentous fungus that is most commonly found in soil, decaying organic matter, and the gastrointestinal tracts of amphibians, reptiles, fish and bats.  Basidiobolus is the sole genus of the family Basidiobolaceae which has classically been the second family recognized in the order Entomophthorales [12]. The two most common species are B. ranarum and B. haptosporus [12]. Although this fungus can be found worldwide, human infections caused by this fungus are most commonly reported from Africa, South America and tropical Asia [1]. This could be due to the fact that only pathogenic species of this fungus are found in those regions or maybe the environmental conditions in these areas are more favorable to the pathogenic species. 

Basidiobolus ranarum is an an example of a pathogenic species in Basidiobolus fungi.  This species is an opportunistic pathogen which means it occasionally causes disease in humans (immunocompromised individuals or young children).  Since it is often found in soil and in vertebrate guts and dung especially of amphibians and reptiles [10], it would be very easy for children to come in contact with this fungus. Basidiobolus is dimorphic meaning it can grow as hyphae and/or yeast depending upon the environmental conditions. An important feature of hyphal growth of this species is the cytoplasm migrates with the growing tip. This growth causes mycelium that consists of mostly empty cells and a collection of individual growing tip cells with no internal sharing of resources or genetic material. One unique characteristic of Basidiobolus is that it has extremely large nuclei (25–50 µm) [10] compared to most filamentous fungi which have nuclei with a diameter of 1-3µm [11]. The nucleoli of Basidiobolus can fill nearly the entire nucleus [10]. *See diagram below*

Diagram of a fungal cell
http://www.peteducation.com/article.cfm?c=16+2160&aid=2956

Rate of Growth: Since this fungus is a Zygomycota fungus, growth is rapid and the fungus matures within 5 days. Maturity can be determined by whether or not the fungus is producing spores [1].

Colony Morphology: Colonies of this fungus are flat, thin, waxy in appearance and can vary in color buff to gray. Later growth of the fungus can be characterized by its heaped up or radially folded appearance and grayish brown color. This later growth of the fungus is covered by fine, white, powdery surface mycelium. If you reverse the plate, the colony looks white or pale. An important note: some strains have an earthy odor typical for Streptomyces spp (a bacteria) [2].

Culture of Basidiobolus ranarum http://www.mycology.adelaide.edu.au/Fungal_Descriptions/Zygomycetes/Basidiobolus/

*Important note: Basidiobolus species lose their sporulation ability after relatively short periods of time in culture. The use of media which incorporates glucosamine hydrochloride and casein hydrolysate seems to help overcome this problem [7]. The media also appears to be suitable for culturing Conidiobolus species, which is interesting considering the two fungal species are considered lookalikes.

Microscopic features:  The hyphae of Basidiobolus are large (8 to 20 µm in diameter) and septate. Having large hyphae/thick fungal walls are a common characteristic of fungi in the phylum Zygomycota. The more spores the fungus produces, the greater the number of septa are present. Basidiobolus spp. produce sexual spores called zygospores that are thick-walled and can be smooth or have undulating outer cell walls. This fungus can also produce two different types of asexual spores or conidia called: ballistospores and capilliconidia [2].

Zygospores of Basidiobolus ranarum http://www.mycology.adelaide.edu.au/Fungal_Descriptions/Zygomycetes/Basidiobolus/

Asexual spores of Basidiobolus ranarum
http://www.mycology.adelaide.edu.au/Fungal_Descriptions/Zygomycetes/Basidiobolus/

Definitions:

hyphae: the branching filaments of a fungus

mycelium: a collection of hyphae

zygospores:sexual spores of fungi within the Zygomycota phylum

septate fungi: fungal hyphae that have partitions (septations)

sporangiophore: asexual stalk which a sporangium is attached

sporangium: asexual structure that holds sporangiospores

sporangiospores: asexual spores 

Life Cycle of Zygomycota fungi

Life Cycle of a typical Zygomycota fungus http://micro-organic-world.blogspot.com/2009/11/identification-of-medically-important.html

An interesting feature of the life cycle of Basidiobolus is that it has the ability to produce several types of spores; usually, depending on its microhabitat. The first type of spore are ballistospores which is forcibly discharged to stick to substrate. The second type of spore are capilliconidia which is not forcibly discharged, but it has a weak spot in the conidiophore so that upon contact the spore is released, and capilliconidium with a sticky blob on glue on the tube-like haptor at its distal (outward) end can attach to anything it contacts, often a passing insect or even a growing fungal hypha. These capilliconidia may develop directly from a hypha or from a mature ballistospore [8].

Clinical Cases 

Pathogenicity: Basidiobolus ranarum is the causative agent of subcutaneous zygomycosis, which is a chronic inflammatory or granulomatous disease. It is generally restricted to the limbs, chest, back or buttocks. The lesions are very large in size, hard, palpable, nonulcerating subcutaneous masses. This pathogenic fungus can also cause gastrointestinal infections on occasion [3] This disease occurs usually in children, occasionally in adolescents and rarely in adults. It more frequently affects males than females [3].

Below are links to clinical cases associated with this fungus:

Case 1: http://jcm.asm.org/content/39/6/2360.full

Case 2: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2893432/

Case 1: describes a 41 year old male with a gastrointestinal infection caused by Basidiobolus ranarum. The patient was admitted to the hospital after complaining of abdominal pain. An ultrasound revealed a thick mass in the right iliac fossa and showed a marked thickening of the ascending colon and cecum and an increased echogenicity of the renal cortex. His prostate was enlarged and he also had a fecal impaction [4].  After an intestinal biopsy, their original diagnosis was intestinal tuberculosis but when it was cultured, there was no growth of mycobacterium. A tissue biopsy was not performed to check for a fungal infection, however his urine cultures came back with fungal growth positive for Basidiobolus ranarum. The patient was treated with Amphotericin B, however his condition did not improve and they later realized that his strain of B. ranarum was resistant to Amphotericin B. After 4 weeks, the patient decided to return home to his family. Since there have only been 10 reported cases in literature, surgical resection of the infected tissue and prolonged treatment with itraconazole appear to be the best available options for treatment [4].

Case 2: describes a 42 year old diabetic male with suspected lung abscesses and multiple organ damage. He is a smoker, works on a farm, and has had diabetes since he was 20. He had generalized hyperkeratotic skin lesions with central necrosis located on his lower limbs and back of chest. Some of these lesions were simulating diabetic kyrle and some healed pyoderma [5]. An examination of the respiratory system revealed a diagnosis of non-resolving pneumonia right upper lobe. Since the X ray appearance was not typical of a lung abscess, there were multiple possibilities for diagnosis such as: fungal infection, mycobacterial infection or hydatid cyst. A CT of the thorax revealed fluid and solid attenuation areas that were mimicking a fungal ball as well as double layered cyst wall as in hydatid cyst. He was initially treated with a broad spectrum of antibiotics and his condition did not improve. Blood heart infusion broth revealed growth of B. ranarum and the patient was started on treatment right away. His treatment consisted of potassium iodide which was considered the drug of choice for this fungus. He was started on oral potassium iodide with 1 drop 3 times a day and gradually increased to 10 drops 3 times a day. He was also given cotrimoxazole. Since the patient's condition did not permit the use of the specific agent-KI, they had to perform surgery to remove the fungus. He was taken to cardio-thoracic surgery for resection after control of diabetes and renal function where a right upper lobectomy was done. The patient completely recovered after this [5].

Below is an image of the destruction caused by B. ranarum

Cutaneous lesions caused by B. ranarum
http://www.mold.ph/basidiobolus.htm

Geographic Distribution

Distribution: Basidiobolus is a ubiquitous fungus and the majority of cases have been reported in South America, Africa and tropical Asia [1]. However, recently (2012) this fungus has been classified as an emerging invasive fungal infection in desert regions of the US Southwest causing gastrointestinal basidiobolomycosis [9]. 

Map of the world showing areas where human infections are reported
www.ezilon.com 

How do people acquire this fungal infection? Traumatic implantation or insect bite are the most likely way for B. ranarum to enter the body [5].

Habitat: Basidiobolus can be found in the feces of amphibians, reptiles, and insectivorous bats as well as in wood lice, on decaying fruits and organic matter and soil [2].

Look Alikes: Conidiobolus is quite similar to Basidiobolus however, Conidiobolus have sporangiophores that are not swollen at their apices and zygospores that do not contain beaks [6].

Asexual spores of Basidiobolus ranarum http://www.mycology.adelaide.edu.au/Fungal_Descriptions/Zygomycetes/Basidiobolus/

     

Asexual spores of Condiobolus
http://www.mold.ph/conidiobolus.htm

Websites you should check out: http://www.doctorfungus.org/thefungi/Basidiobolus.php  http://www.mycology.adelaide.edu.au/Fungal_Descriptions/Zygomycetes/Basidiobolus/  References [1] Gugnani H.C. 1999. A review of zygomycosis due to Basidiobolus ranarum. European Journal of Epidemiology 15: 923-929 [2] Rex J.H., McGinnis M., Arikan S., Rodriquez-Adrian L., Kirsch M. 2011 Basidiobolus Species www.drfungus.org/thefungi/Basidiobolus.php (March 29th 2012) [3] Larone D.H. 2002. Medically important fungi A guide to identification 4th edition. ASM Press page 176 [4] Kahn Z.U., Khoursheed M., Makar R., Al-Waheeb S., Al-Bader I., Al-Muzaini A., Chandy R., Mustafa A.S. 2001. Basidiobolus ranarum as an Etiologic Agent of Gastrointestinal Zygomycosis. Journal of Clinical Microbiology vol 39 no. 6: 2360-2363 [5] Chetambath R., Deepa Sarma M.S., Suraj K.P., Jyothi E., Mohammed S., Philomina B.J., Ramadevi S. 2010. Basidiobolus: An unusual case of lung abscess. Lung India 27(2): 89-92 [6] Rex J.H., McGinnis M., Arikan S., Rodriquez-Adrian L., Kirsch M. 2011 Conidiobolus Species http://www.doctorfungus.org/thefungi/Conidiobolus.php (March 29th 2012)] [7] Shipton W.A., Zahari P., 1987 Sporulation Media for Basidiobolus species Journal Med Vet Mycology 25(5):323-327  [8] Blackwell M., 2001 Fungi that fly: A two part laboratory study Mycology laboratory manual: LSU [9] Vikram H.R., Smilack J.D., Leighton J.A., Crowell M.D., De Petris G. 2012 Emergence of       Gastrointestinal Basidiobolomycosis in the United States, With a Review of Worldwide Cases Clinical           Infectious Diseases [10] Henk D.A., Fisher M.C., 2012The Gut Fungus Basidiobolus ranarum Has a Large Genome and Different Copy Numbers of Putatively Functionally Redundant Elongation Factor Genes PLoS ONE 7(2): e31268. doi:10.1371/journal.pone.0031268 [11] Gow N.A., Gadd G.M., 1994 The Growing Fungus. Chapman & Hall pgs: 75-76 [12] Howard D.H., 1983 Pathogenic Fungi in Humans and Animals. Library of Congress pgs 130-132