Chapter 104

Bulleribasidium Sampaio, Weiss & Bauer(2002)

Jose Paulo Sampaio

DIAGNOSIS OF THE GENUS

Asexual reproduction: Yeast cells are ovoid and budding is polar. Ballistoconidia are formed and are rotationally symmetrical. Cultures areyellowish-cream in color.Sexual reproduction: The sexual structures are formed in the filamentous state. The hyphae have incomplete clamp connections but formhaustorial branches. The sexual state has only been observed in culture, and basidiocarps are not formed. Basidia are typically transverselyseptate, occasionally longitudinally septate, and are arranged in small clusters or occur in isolation. The basidiospores are produced at theapex of tubular sterigmata and are forcibly discharged. They are globose, rotationally symmetrical, and germinate by budding or repetition.The septal pore is a dolipore with poorly developed parenthesome-like elements.Physiology/biochemistry: Fermentation is absent. myo-Inositol and D-glucuronate are utilized, but nitrate is not. Starch-like compounds areformed. The diazonium blue B reaction and production of urease are positive.Phylogenetic placement: Subphylum Agaricomycotina, Class Tremellomycetes, Order Tremellales (Fig. 104.1).

Filobasidium floriforme CBS 6241 / AF075498100

73100

6973

60 100

8468

91

56

97

98

99

100100

10099

Filobasidium capsuligenum CBS 4736 / AF075501Filobasidiella neoformans CBS 132 / AF075484

Sirobasidium magnum CCJ 1289 / AF042240Cryptococcus flavus CBS 331T / AF075497Tremella encephala CBS 6968 / AF189867

Tremella aurantia CBS 6965 / AF189842Fellomyces polyborus CBS 6072T / AF189859

Kockovaella thailandica CBS 7552T / AF075516Cuniculitrema polymorpha PYCC 5647 / AY032662

Bulleromyces albus CBS 500 / AF416643Tremella nivalis CCJ 1191 / AF042232Tremella moriformis CBS 7810 / AF075493

Cryptococcus laurentii CBS 139T / AF075469Cryptococcus aureus CBS 318T / AB035041Auriculibuller fuscus PYCC 5690T / AF444762Papiliotrema bandonii CBS 9107T / AF416642

Tremella mycophaga RJB 6539-4 / AF042249Fibulobasidium inconspicuum CBS 8238 / AF416649

Trimorphomyces papilionaceus CBS 444.92 / AF416645Cryptococcus dimennae CBS 5770T / AF075489Tremella mesenterica CBS 6973 / AF444433

Bullera miyagiana CBS 7526T / AF189858Bulleribasidium oberjochense CBS 9110T / AF416646

Bulleribasidium

Bullera variabilis CBS 7347T / AF189855Bullera pseudovariabilis AS 2.2092T / AF544247

Bullera siamensis JCM 11822T / AY188391Bullera begoniae JCM 12155T / AB119462Bullera panici JCM 11819T / AY188387

Cryptococcus nemorosus VKM Y-2906T / AF472625

10 changes

FIGURE 104.1 Phylogenetic placement of Bulleribasidium oberjochense within the Tremellales. Maximum parsimony analysis (consensus tree)of an alignment of the D1/D2 regions of LSU rRNA gene sequences. The topology was rooted with members of the Filobasidiales. Numbers onthe branches are bootstrap values (1000 replicates; values below 50% are not shown; T5 type strain).

1387The Yeasts, a Taxonomic Study© 2011 Elsevier B.V. All rights reserved.

TYPE SPECIES

Bulleribasidium oberjochense Sampaio, Gadanho, Weiss & Bauer

SPECIES ACCEPTED

1. Bulleribasidium oberjochense Sampaio, Gadanho, Weiss & Bauer (2002)

SYSTEMATIC DISCUSSION OF THE SPECIES

104.1. Bulleribasidium oberjochense Sampaio,Gadanho, Weiss & Bauer (2002)

Growth on 5% malt extract agar: After 6 days at 20�C, the cells areovoid to pyriform, 4�63 6�10 μm, occur singly or in pairs, and bud-ding is multilateral (Fig. 104.2A). Ballistoconidia are formed at theend of 5 to 8-μm long sterigmata. Mature ballistoconidia are globose,2�4 μm, to subglobose, 3�43 4�5 μm (Fig. 104.2B). The streak cul-ture is yellowish-cream, smooth to slightly verrucose, dull and butyr-ous, with hyphae developing from the margin.Dalmau plate culture on corn meal agar: Pseudohyphae and truehyphae are formed.Sexual state: The sexual state is formed by self-fertile strains.Hyphae develop from single yeast cells (Fig. 104.2C) and have

incomplete clamp connections. The presence of culture contaminantslike Cladosporium spp. stimulates the formation of haustoria(Fig. 104.2D). Haustorial cells are globose or elongated, and the haus-torial filaments can be branched or unbranched. Basida are formedafter approximately 2 months on corn meal agar plates incubated at20�22�C. Basidia are arranged in small clusters, or occur alone.Transfer of agar blocks with mycelium and basidial initials to 2%water agar enhances basidial development. Approximately 10 daysafter transfer, septate basidia can be observed. When mature, thebasidia are two-celled, normally transversely septate and cylindrical,occasionally globose and longitudinally septate, measuring4�8310�20 μm (Fig. 104.2E). The basidiospores are globose,5�7 μm, thin walled, ejected from sterigmata, 1�338�20 μm, andgerminate by budding or repetition (Fig. 104.2F).

Fermentation: Absent.

Growth (in Liquid Media)1

Glucose 1

Inulin 2

Sucrose 1

Raffinose 1

Melibiose 1

Galactose 1

Lactose vTrehalose 1/sMaltose 1

Melezitose 1

Methyl-α-D-glucoside 1

Soluble starch 1

Cellobiose 1

Salicin 1

L-Sorbose 2

L-Rhamnose 1

D-Xylose 1

L-Arabinose 1

D-Arabinose 1

D-Ribose sMethanol 2

Ethanol 2

Glycerol vErythritol 2

Ribitol sGalactitol 1

D-Mannitol sD-Glucitol 1

myo-Inositol 1

DL-Lactate vSuccinate 1

Citrate 1/sD-Gluconate 1

D-Glucosamine sN-Acetyl-D-glucosamine nHexadecane nNitrate 2

Vitamin-free 2

1Based on CBS 9110 and PYCC 5742.

Additional Growth Tests and Other Characteristics1

Nitrite 2

D-Glucuronate 1

Xylitol 1

L-Tartaric acid 1

Saccharic acid sProtocatechuic acid 2

p-Hydroxybenzoic acid 2

m-Hydroxybenzoic acid 2

Gallic acid 2

Gentisic acid 2

Vanillic acid 2

Ethylamine 2

L-Lysine 1

Cadaverine 2

Creatine 2

Creatinine 2

Cycloheximide 0.01% 1

Cycloheximide 0.1% vGrowth at 25�C 1

Growth at 30�C vGrowth at 35�C 2

Starch formation 1

DBB 1

1Based on CBS 9110 and PYCC 5742.

(A) (B)

(C) (D)

(E) (F)

FIGURE 104.2 Bulleribasidium oberjochense CBS 9110. (A) Buddingcells on 5% malt extract agar after 6 days at 20�C. (B)Ballistoconidiogenic cells and ballistoconidia formed on corn mealagar. (C) Initial stages of development of mycelium. (D) Haustoriaand interaction with hyphae of Cladosporium spp. (E) Different devel-opmental stages of basidia. (F) Basidiospore. Bar510 μm.

1388 PART | VB Descriptions of Teleomorphic Basidiomycetous Genera and Species

CoQ: Not determined.Mol% G1C: Not determined.Gene sequence accession number, type strain: D1/D2 LSUrRNA5AF416646.Cell carbohydrates: Not determined.Origin of the strains studied: CBS 9110 and PYCC 5742, isolatedfrom fruitbodies of Tulasnella helicospora collected in Oberjoch,Bavarian Alps, Germany (Sampaio et al. 2002).Type strain: CBS 9110.Systematics: Bulleribasidium, Auriculibuller and Bulleromyces are thegenera that currently accommodate the sexual states of the mitospo-ric ballistoconidial genus Bullera. The phylogenetic tree depicted inFig. 104.1 indicates that Bulleribasidium is evolutionarily well sepa-rated from both Auriculibuller and Bulleromyces. The transverselyseptate basidium of Bulleribasidium (Fig. 104.2E) is more similarto the basidium of Auriculibuller (see Chapter 102), which is alsotransversely septate, than to the basidium of Bulleromyces (seeChapter 105), which has a Tremella-type basidium.

The closest relatives of B. oberjochense are Bullera variabilisand Bullera pseudovariabilis, and these three species, together withBullera begoniae, Bullera panici and Bullera siamensis constitutethe Bulleribasidium clade (Fig. 104.1). It is expected that additionalsexual states uncovered in this group will resemble that ofB. oberjochense. B. oberjochense, Bullera variabilis and Bullera pseudo-variabilis, share similar nutritional profiles and cannot be distin-guished based on physiological data. Bai et al. (2003) mentioned thatthe sole test that gives different results in Bullera variabilis andBullera pseudovariabilis is lactose utilization, but this test is variablefor B. oberjochense. The occurrence of mating among strains ofBullera variabilis, including the type strain of this species, wasreported by Boekhout et al. (1991), but, besides production of hyphae

with clamp connections and haustoria, basidial development was notobserved. Sampaio et al. (2002) compared B. oberjochense and Bulleravariabilis. Because the LSU rRNA gene sequences of the type strainsof the two species differed by five substitutions and nuclearDNA�DNA reassociation experiments yielded low values, it wasconcluded that B. oberjochense does not represent the sexual state ofBullera variabilis. Bullera pseudovariabilis differs from B. oberjochenseby four substitutions in the D1/D2 domains of the LSU rRNA gene.Ecology: In culture, hyphae of B. oberjochense form haustoria thatattach to hyphae of Cladosporium (Sampaio et al. 2002), which sug-gests that mycoparasitism may play a role in the life strategy of thisyeast. Another argument pointing to associations with other fungi isthe type of substrate on which B. oberjochense was found. The twoavailable strains of this species were isolated from the basidiocarp ofTulasnella helicospora, a jelly fungus.Biotechnology: Unknown.Agriculture and food: Unknown.Clinical importance: Unknown.Additional comments: Fruiting bodies are not known in B. oberjo-chense. At the sub-cellular level, B. oberjochense has dolipores withpoorly developed parenthesome-like elements in the vicinity of theseptal pore (Sampaio et al. 2002).

COMMENTS ON THE GENUS

The salient features of Bulleribasidium are the formation of a trans-versely septate and two-celled basidium, combined with the forma-tion of ballistoconidia in the yeast state. A Bulleribasidium-like lifecycle might be hypothesized for the closest asexual relatives ofB. oberjochense presently classified in Bullera (see Fig. 104.1).

1389Chapter | 104 Bulleribasidium Sampaio, Weiss & Bauer (2002)