The Yeasts || Kurtzmanomyces Y. Yamada, M. Itoh, Kawasaki, Banno & Nakase (1988)

Chapter 146

Kurtzmanomyces Y. Yamada, M. Itoh,Kawasaki, Banno & Nakase (1988)

Jose Paulo Sampaio

DIAGNOSIS OF THE GENUS

Asexual reproduction: Cells are globose to ovoid and small, and rarely exceed 9 μm in length. Reproduction is by budding and by productionof blastoconidia at the end of a stalk-like conidiophore. The stalked blastoconidia are freed without forceful ejection at the distal end of thestalk-like conidiophore. Each conidiophore can produce sequential multiple blastoconidia, thus becoming branched or elongated.Ballistoconidia can be formed in some species. Cultures are light orange in color.Sexual reproduction: Although the sexual state of the three species in Kurtzmanomyces is not known, a fourth (and sexual) species,Mycogloea nipponica, is closely related to Kurtzmanomyces (Fig. 146.1) and produces a Kurtzmanomyces-like anamorph. In nature, M. nipponicaproduces minute, light orange basidiocarps. Basidia arise from thin-walled cylindrical probasidia and detach easily from the probasidia.Basidia, but not basidiocarps, are produced in culture.Physiology/biochemistry: Fermentative ability is absent. Nitrate is assimilated. D-Glucuronate, myo-inositol and aromatic compounds are notassimilated. Starch-like compounds are not formed. The dominant CoQ system has 10 isoprenologues. The DBB reaction is positive.Phylogenetic placement: Kurtzmanomyces belongs to the family Chionosphaeraceae, class Agaricostilbomycetes, subphylum Pucciniomycotina(Fig. 146.1).

TYPE SPECIES

Kurtzmanomyces nectairei (Rodrigues de Miranda) Y. Yamada, M. Itoh, Kawasaki, Banno & Nakase

SPECIES ACCEPTED

1. Kurtzmanomyces insolitus Sampaio & Fell (1999)2. Kurtzmanomyces nectairei (Rodrigues de Miranda) Y. Yamada, M. Itoh, Kawasaki, Banno & Nakase (1988)3. Kurtzmanomyces tardus Giménez-Jurado & van Uden (1990)4. Kurtzmanomyces-like stage of Mycogloea nipponica Bandoni (1998)

1795The Yeasts, a Taxonomic Study© 2011 Elsevier B.V. All rights reserved.

KEY TO SPECIES INCLUDING MYCOGLOEA NIPPONICA

1. a. L-Arabinose and D-arabinose are assimilated................................................................................................................................K. insolitus:b. L-Arabinose and D-arabinose are not assimilated............................................................................................................................................2

p. 1797

2(1). a. Trehalose is assimilated ............................................................................................................................................................................................3b. Trehalose is not assimilated ....................................................................................................................................................................K. tardus: p. 1798

3(2). a. Sucrose is assimilated........................................................................................................................................................Mycogloea nipponica:b. Sucrose is not assimilated ...................................................................................................................................................................K. nectairei:

p. 1799p. 1797

Kurtzmanomyces insolitus CBS 8377T / AF177408

Kurtzmanomyces tardus CBS 7421T / AF177410

Kurtzmanomyces nectairei CBS 6405T / AF177409

Mycogloea nipponica PYCC 5754 / AY159650

Chionosphaera apobasidialis F93 / AF393470

Chionosphaera cuniculicola PYCC 5686 / AF393472

Sporobolomyces lactophilus CBS 7527T / AF177411

Sporobolomyces xanthus CBS 7513T / AF177414

Agaricostilbum hyphaenes CBS 7811T / AF177406

Agaricostilbum pulcherrimum RJB 6859-3 / EU085531

Sterigmatomyces elviae CBS 5922T / AF177415

Sterigmatomyces halophilus CBS 4609T / AF177416

Kondoa aeria CBS 8352T / AF189901

Kondoa malvinella CBS 6082T / AF189903

Mixia osmundae IAM14324 / AY512867

Kondoaceae

Agaricostilbaceae

Ag

ari

co

sti

lba

les

Chionosphaeraceae

10 changes

100

100

100

97

97

93

95

96

80

91

FIGURE 146.1 Phylogenetic placement of Kurtzmanomyces within the Agaricostilbomycetes. Maximum parsimony analysis (consensus tree)of an alignment of the D1/D2 region of the LSU rRNA gene sequence. The topology was rooted with Mixia osmundae. Numbers on the branchesare bootstrap values (1000 replicates; values below 50% are not shown). GenBank accession numbers of the sequences are indicated afterstrain numbers. Dotted lines indicate the nodes that correspond to the delimitation of each family.

TABLE 146.1 Relevant Physiological Tests for the Discrimination of Species in the Genus Kurtzmanomyces

K. nectairei K. tardus K. insolitus M. nipponica

D-Xylose 2 2 1 sL-Arabinose 2 2 1 2

D-Arabinose 2 2 1 2

Cellobiose 2 2 1 1

Lactose 2 2 1 2

Raffinose 2 2 1 1

Melezitose 2 2 1 1

Cadaverine 2 2 1 2

Cycloheximide 0.01% 2 2 1 2

Cycloheximide 0.1% 2 2 1 2

Ballistoconidia 2 2 1 2

Trehalose 1 2 1 1

Ribitol 1 2 1 1

Succinate 1 2 1 1

L-Malic acid 1 2 2 sD-Glucitol 1 1 2 2

Sucrose 2 1 1 1

Growth at 30�C 2 1 1 1

K., Kurtzmanomyces; M., Mycogloea.

1796 PART | VC Descriptions of Anamorphic Basidiomycetous Genera and Species

SYSTEMATIC DISCUSSION OF THE SPECIES

146.1. Kurtzmanomyces insolitus Sampaio &Fell (Sampaio et al. 1999b)

Growth on 5% malt extract agar: After 6 days at 20�C, the cells aresubglobose to ellipsoid, 2�334�6 μm (Fig. 146.2A). The conidiogen-ous stalks, normally one per cell, measure 1�5 μm. More than oneconidium can be produced sympodially on each stalk-like conidio-phore. Ovoid to reniform ballistoconidia, 2�435�8 μm, can be pro-duced (Fig. 146.2B). Streak cultures are pale orange, smooth,butyrous and glossy, and have an entire margin. Growth is slow.Dalmau plate culture on corn meal agar: Pseudohyphae are absent.

Fermentation: Absent.

Growth (in Liquid Media)*

Glucose 1

Inulin 2

Sucrose 1

Raffinose 1

Melibiose 2

Galactose 2

Lactose 1

Trehalose 1

Maltose 2

Melezitose 1

Methyl-α-D-glucoside 2

Soluble starch 2

Cellobiose 1

Salicin sL-Sorbose 2

L-Rhamnose 2

D-Xylose 1

L-Arabinose 1

D-Arabinose 1

D-Ribose sMethanol 2

Ethanol 1

Glycerol sErythritol sRibitol sGalactitol 2

D-Mannitol 1

D-Glucitol 2

Inositol 2

DL-Lactate sSuccinate 1

Citrate 2

D-Gluconate sD-Glucosamine 2

N-Acetyl-D-glucosamine nHexadecane nNitrate 1

Vitamin-free 2

*Based on CBS 8377.

Additional Growth Tests and Other Characteristics

Nitrite 1 Vanillic acid 2

D-Glucuronate 2 Ferulic acid 2

Xylitol 1 Veratric acid 2

L-Malic acid 2 Cycloheximide 0.01% 1

L-Tartaric acid 2 Cycloheximide 0.1% 1

Saccharic acid 2 Growth at 25�C 1

p-Hydroxybenzoic acid 2 Growth at 30�C 1

m-Hydroxybenzoic acid 2 Growth at 35�C 2

Gallic acid 2 Starch formation 2

Gentisic acid 2 DBB 1

CoQ: Not determined.Mol% G1C: 49.1 (Tm: Sampaio et al. 1999b).Gene sequence accession number, type strain: D1/D2 LSU rRNA5AF177408, ITS 5AF444594.Cell carbohydrates: Not determined.Origin of the strain studied: CBS 8377 (JCM 10409), isolated fromthe basidiocarp of an unidentified species of Exidiopsis, Sesimbra,Portugal.Type strain: CBS 8377.Systematics: Kurtzmanomyces insolitus shows a peculiar combinationof characteristics. In addition to the typical features of the genus, it isalso able to form ballistoconidia (Sampaio et al. 1999). Table 146.1shows the phenotypic properties that allow the discrimination ofK. insolitus from the other Kurtzmanomyces species. This speciesseems to be nutritionally more versatile than the other species in thegenus as it grows on more carbon compounds than K. nectairei orK. tardus (Table 146.1).Ecology: Since only a single strain of this species is available in cul-ture collections, the ecological niche of K. insolitus is unknown.Biotechnology: Unknown.Agriculture and food: Unknown.Clinical importance: Unknown.

146.2. Kurtzmanomyces nectairei (Rodriguesde Miranda) Y. Yamada, M. Itoh, Kawasaki,Banno & Nakase (1988a)

Synonyms:

Sterigmatomyces nectairei Rodrigues de Miranda (1975)Fellomyces nectairei (Rodrigues de Miranda) Y. Yamada & Banno

(1984a)

Growth on 5% malt extract agar: After 6 days at 20�C, the cellsare spherical to ovoid, 3�63 4�10 μm, with one to 10 short stalk-like conidiophores (Fig. 146.3). Conidia develop laterally or termi-nally on stalk-like conidiophores and branching of the conidiophorecan occur. Ballistoconidia are not produced. Streak cultures are paleorange, butyrous, smooth and semi-dull, and have an entire margin.Dalmau plate culture on corn meal agar: Pseudohyphae are notformed. Short and sparse strands of narrow hyphae can beformed.

FIGURE 146.2 Kurtzmanomyces insolitus CBS 8377. (A) Yeast cells on5% malt extract agar after 6 days at 20�C. (B) Ballistoconidia andballistoconidia-forming cells. Bar 510 μm.

FIGURE 146.3 Kurtzmanomyces nectairei CBS 6405. Yeast cells on 5%malt extract agar after 6 days at 20�C. Bar 510 μm.

1797Chapter | 146 Kurtzmanomyces Y. Yamada, M. Itoh, Kawasaki, Banno & Nakase (1988)



Glucose 1

Inulin 2

Sucrose 2

Raffinose 2

Melibiose 2

Galactose 2

Lactose 2

Trehalose 1

Maltose 2

Melezitose 2


Soluble starch 2

Cellobiose 2

Salicin 2

L-Sorbose 2

L-Rhamnose 2

D-Xylose 2

L-Arabinose 2

D-Arabinose 2

D-Ribose 2

Methanol 2

Ethanol wGlycerol 2

Erythritol 2

Ribitol 1

Galactitol 2

D-Mannitol 1

D-Glucitol 1

myo-Inositol 2

DL-Lactate 2

Succinate 1

Citrate 2

D-Gluconate 2

D-Glucosamine 2


Vitamin-free 2

*Based on CBS 6405.


Nitrite 1

D-Glucuronate 2

Xylitol 2

L-Malic acid 1

L-Tartaric acid 2

Saccharic acid 2

p-Hydroxybenzoic acid 2

m-Hydroxybenzoic acid 2

Gallic acid 2

Gentisic acid 2

Vanillic acid 2

Ferulic acid 2

Veratric acid 2

Cycloheximide 0.01% 2


Growth at 25�C 1

Growth at 30�C 2

Starch formation 2

DBB 1

CoQ: 10 (Yamada et al. 1988a).Mol% G1C: 52.5 (BD: Kurtzman 1990).Gene sequence accession number, type strain: D1/D2 LSUrRNA5AF177409, ITS 5AF444494.Cell carbohydrates: Xylose is absent in whole-cell hydrolysates.Origin of the strain studied: CBS 6405 (JCM 6906), isolated fromcheese of St. Nectaire, France.Type strain: CBS 6405.Systematics: Table 146.1 shows the phenotypic properties that allowthe discrimination of K. nectairei from the other Kurtzmanomycesspecies. In terms of the ability to utilize different carbon sources,K. nectairei occupies an intermediate position as it grows on fewercarbon compounds than K. insolitus, but more than K. tardus.Ecology: Since only a single strain of this species is known(Rodrigues de Miranda 1975), the ecological preferences of K. nec-tairei remain unknown.Biotechnology: Unknown.Agriculture and food: The single strain of this species was isolatedfrom St. Nectaire's cheese (France).Clinical importance: Unknown.

146.3. Kurtzmanomyces tardus Gimenez-Jurado & van Uden (Gimenez-Jurado et al.1990)

Growth on 5% malt extract agar: After 6 days at 20�C, the cells aresubglobose to ellipsoid, 3�534�8 μm (Fig. 146.4). The conidiogenous

stalks, normally one to four per cell, are short, 0.4�2 μm.Ballistoconidia are not produced. Streak cultures are pale orange,smooth, butyrous and glossy, and have an entiremargin. Growth is slow.Dalmau plate culture on corn meal agar: Pseudohyphae are absent.Slender, septate hyphae without clamp connections can be formed.



Glucose 1

Inulin 2

Sucrose 1

Raffinose 2

Melibiose 2

Galactose 2

Lactose 2

Trehalose 2

Maltose 2

Melezitose 2


Soluble starch 2

Cellobiose 2

Salicin 2

L-Sorbose 2

L-Rhamnose 2

D-Xylose 2

L-Arabinose 2

D-Arabinose 2

D-Ribose 2

Methanol 2

Ethanol 1

Glycerol 2

Erythritol 2

Ribitol 2

Galactitol 2

D-Mannitol 1

D-Glucitol w, smyo-Inositol 2

DL-Lactate 2

Succinate 2

Citrate 2

D-Gluconate 2

D-Glucosamine 2


Vitamin-free 2

*Based on CBS 7241.


Nitrite 1

D-Glucuronate 2

Xylitol 2

L-Malic acid 2

L-Tartaric acid 2

Saccharic acid 2



Gallic acid 2

Gentisic acid 2

Vanillic acid 2

Ferulic acid 2

Veratric acid 2



Growth at 25�C 1

Growth at 30�C 1

Growth at 35�C 2

Starch formation 2

DBB 1

CoQ: 10 (Giménez-Jurado et al. 1990).Mol% G1C: 58.2 (Tm: Giménez-Jurado et al. 1990).Gene sequence accession number, type strain: D1/D2 LSU rRNA5AF177410, ITS 5AF444566.Cell carbohydrates: Xylose is absent in whole-cell hydrolysates(Giménez-Jurado et al. 1990).Origin of the strain studied: CBS 7421 (JCM 10490), isolated fromcontaminated demineralized water, Oeiras, Portugal (Giménez-Jurado et al. 1990).Type strain: CBS 7421.Systematics: Besides its slow growth rate, K. tardus grows on fewercarbon compounds than the other species in the genus. Table 146.1

FIGURE 146.4 Kurtzmanomyces tardus CBS 7421. Yeast cells on 5%malt extract agar after 6 days at 20�C. Bar 510 μm.


shows the phenotypic properties that allow the discrimination ofK. tardus from the other Kurtzmanomyces species.Ecology: Since only a single strain of this species is known, the eco-logical niche of K. tardus remains uncertain.Biotechnology: Unknown.Agriculture and food: Unknown.Clinical importance: Unknown.

146.4. Kurtzmanomyces-like state ofMycogloea nipponica Bandoni (1998b)

Growth on 5% malt extract agar: After 6 days at 20�C, the yeastcells are subglobose to ellipsoidal, 2�533�7 μm (Fig. 146.5A). Theconidiogenous stalks are short and numerous (up to 10) per cell.More than one conidium can be produced sympodially on each stalk-like conidiophore. Ballistoconidia are not produced. Streak culturesare pale orange, smooth, butyrous and semi-glossy, and have anentire margin.

Dalmau plate culture on corn meal agar: Pseudohyphae are absent.Slender, septate hyphae without clamp connections are formed.Sexual stage: Hyphae are devoid of clamp connections and developfrom unconjugated yeast cells (Fig. 146.5B). The hyphae are 1.5�2μmin diameter (Fig. 146.5C). Probasidia are thin-walled, long andnarrow, 3�4314�19 μm, and basidia are cylindrical, 2.5�4.5335�55 μm, three-septate and tend to detach (Fig. 146.5D,E).Basidiospores are thin-walled, ovoid or ellipsoid, 2�43 4�7 μm.



Glucose 1

Inulin 2

Sucrose 1

Raffinose 1

Melibiose 2

Galactose 1

Lactose 2

Trehalose 1

Maltose 1

Melezitose 1


Soluble starch 2

Cellobiose 1

Salicin sL-Sorbose 2

L-Rhamnose 2

D-Xylose sL-Arabinose 2

D-Arabinose 2

D-Ribose sMethanol 2

Ethanol 1

Glycerol sErythritol 1

Ribitol 1

Galactitol 2

D-Mannitol 1

D-Glucitol 2

myo-Inositol 2

DL-Lactate sSuccinate 1

Citrate sD-Gluconate 2

D-Glucosamine 2


Vitamin-free 2

*Based on PYCC 5754.


Nitrite 1

D-Glucuronate 2

Xylitol 2

L-Malic acid sL-Tartaric acid 2

Saccharic acid 2



Gallic acid 2

Gentisic acid 2

Vanillic acid 2

Ferulic acid 2

Veratric acid 2



Growth at 25�C 1

Growth at 30�C 1

Growth at 35�C 2

Starch formation 2

DBB 1

CoQ: Not determined.Mol% G1C: Not determined.Gene sequence accession number, PYCC 5754: D1/D2 LSU rRNA5AY159650.Cell carbohydrates: Not determined.Origin of the strain studied: PYCC 5754, obtained by Dr RolandKirschner from basidiospores discharged from a basidiocarp ofM. nipponica developing in a rotting branch lying on the ground inYangmingsham, Taipei, Taiwan (Kirschner et al. 2003).Type strain: No living culture was derived from the type material,which is deposited at the Mycological Herbarium of the NationalScience Museum (TNS) in Tokyo, Japan.Systematics: Olive (1950) created the genus Mycogloea, which hebased on M. carnosa. According to the last update (Bandoni 1998b),the genus contains six species that have been rarely found, and formost of them living cultures have not been obtained. Molecular datafor this genus are scarce and sequence data have only been obtainedfor M. macrospora (U41848, partial sequence of the SSU rRNA gene)

FIGURE 146.5 Mycogloea nipponica PYCC 5754. (A) Yeast cells on 5%malt extract agar after 6 days at 20�C. (B) Yeast cell forming a hyphawithout cell-to-cell conjugation. (C) Hypha without clamp connec-tions. (D) Basidia in different developmental stages (note one basid-iospore in the basidium on the right side). (E) Typical Mycogloeabasidium, which is completely detached from the hypha where itwas formed. Bar 510 μm.

1799Chapter | 146 Kurtzmanomyces Y. Yamada, M. Itoh, Kawasaki, Banno & Nakase (1988)

and M. nipponica (partial sequence of the LSU rRNA gene). The mainphenotypic characteristics of the genus are the gasteroid basidia (i.e.,basidiospores are passively released), the presence of a yeast stateand the deciduous nature of basidia that normally are detached fromthe hyphae.

The original description of M. nipponica was based on a Japanesecollection and did not include the isolation of a living culture(Bandoni 1998b). The culture upon which this review is based wasisolated from a collection made in Taiwan (Kirschner et al. 2003).The connection between Kurtzmanomyces and M. nipponica raises afew questions to be answered in the future: Do the Kurtzmanomycesspecies have a sexual Mycogloea-like stage? Do the remainingMycogloea species have a Kurtzmanomyces yeast stage? Does theentire Mycogloea group represent a single lineage?Ecology: In nature, M. nipponica seems to be mycoparasitic on asco-mycetes. This species has been found in Asia, in Japan and Taiwan(Bandoni 1998b, Kirschner et al. 2003).Biotechnology: Unknown.Agriculture and food: Unknown.Clinical importance: Unknown.

COMMENTS ON THE GENUS

Yamada et al. (1988a) erected the genus Kurtzmanomyces for asexual,stalk-producing yeasts with coenzyme CoQ-10 and that did not havexylose in whole-cell hydrolysates. Subsequent studies using molecularphylogenetic analyses validated this arrangement (Fell et al. 2000).An updated molecular analysis of Kurtzmanomyces is presented inFig. 146.1. It includes Mycogloea nipponica, a sexual species that has ayeast stage that fits the morphological, physiological and molecularconcept of Kurtzmanomyces (Kirschner et al. 2003). The sister clade ofKurtzmanomyces is the teleomorphic genus Chionosphaera. The buddingof cells through minute stalks is present in C. apobasidialis (J.P. Sampaio,unpublished data) and in C. cuniculicola (Kirschner et al. 2001b) andis similar, and probably homologous, to the mode of reproductiondescribed for members of Kurtzmanomyces. According to Bauer et al.(2006), both genera belong to the family Chionosphaeraceae of theorder Agaricostilbales. Another remarkable feature of Kurtzmanomycesis the apparent rarity of these organisms. Each species is known onlyfrom the type strain and therefore the entire genus is based on threestrains.


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The Yeasts || Kurtzmanomyces Y. Yamada, M. Itoh, Kawasaki, Banno & Nakase (1988)