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Geotrichum Link: Fries (1832)
Chapter 91
Geotrichum Link: Fries (1832) G. Sybren de Hoog and Maudy Th. Smith
DIAGNOSIS OF THE GENUS Asexual reproduction: Colonies are white, farinose or hairy, usually dry, and consist of true hyphae, which branch at broad or right angles, have rounded apices, and disarticulate into arthroconidia. Sympodially produced blastoconidia may also be present. Budding is absent. Chlamydospores may be formed. Septa have micropores. Sexual reproduction: Dipodascus and Galactomyces represent the teleomorphic states of Geotrichum. Physiology/biochemistry: Fermentation is often absent. D-Xylose is assimilated. Nitrate is not assimilated. Extracellular starch is not produced. The diazonium blue B reaction is negative. Small subunit rRNA gene sequences are without deletions. Phylogenetic placement: Saccharomycetales. Geotrichum and its teleomorphic states Dipodascus and Galactomyces are sister genera to Magnusiomyces and its anamorphic state Saprochaete (Figs 13.1, 91.1).
TYPE SPECIES Geotrichum candidum Link: Fries
Dipodascus aggregatus CBS 175.53T / AY788294
99
Geotrichum restrictum CBS 111234T / EF126738 Geotrichum klebahnii CBS 179.30T / AY788298
85
Dipodascus armillariae CBS 817.71T / AY788348 Dipodascus macrosporus CBS 259.82T / AY788310 Dipodascus albidus CBS 766.85 / AY788342 Dipodascus geniculatus CBS 184.80T / AY788301
88
Dipodascus australiensis CBS 372.83 / AY788314 Geotrichum fermentans CBS 439.83T / AY788318 Galactomyces citri-aurantii CBS 175.89T / AY788295 Galactomyces reessii CBS 179.60T / AY788299 97
Galactomyces pseudocandidus CBS 626.83T / AY788334 84
Geotrichum europaeum CBS 866.68T / AY788351 90
Galactomyces geotrichum CBS 773.71 / AY788343 Galactomyces candidus CBS 178.71 / AY788297
0.05 substitutions/site FIGURE 91.1 Phylogenetic tree showing the relationship of species of the genus Geotrichum and its teleomorphic genera Dipodascus and Galactomyces determined from maximum likelihood analysis of ITS sequences using RaxML (Stamatakis et al. 2008). Bootstrap values (.80%) are from 1000 replicates. GenBank accession numbers follow strain numbers.
SPECIES ACCEPTED 1. 2. 3. 4. 5.
Geotrichum candidum Link: Fries (1832) Geotrichum carabidarum S.-O. Suh & M. Blackwell (2006) Geotrichum citri-aurantii (Ferraris) E.E. Butler (1988) Geotrichum cucujoidarum S.-O. Suh & M. Blackwell (2006) Geotrichum decipiens (L.R. Tulasne & C. Tulasne) W. Gams (1983)
The Yeasts, a Taxonomic Study © 2011 Elsevier B.V. All rights reserved.
1279
1280 6. 7. 8. 9. 10. 11.
PART | IVC
Descriptions of Anamorphic Ascomycetous Genera and Species
Geotrichum europaeum de Hoog & M.Th. Smith (2004) Geotrichum fermentans (Diddens & Lodder) von Arx (1977a) Geotrichum histeridarum S.-O. Suh & M. Blackwell (2006) Geotrichum klebahnii (Stautz) Morenz (1964) Geotrichum pseudocandidum Saëz (1968b) Geotrichum restrictum de Hoog & M.Th. Smith (2004)
KEY TO SPECIES 1. 2 (1). 3 (2). 4(3). 5(1). 6(5). 7(6). 8(5).
9(8).
a. b. a. b. a. b. a. b. a. b. a. b. a. b. a. b.
Vitamins are required for growth .............................................................................................................................................................................2 Vitamins are not required for growth .....................................................................................................................................................................5 Growth occurs at 30 C ..................................................................................................................................................................................................3 Growth is absent at 30 C......................................................................................................................................................................G. restrictum: D-Galactose is assimilated ............................................................................................................................................................................................4 D-Galactose is not assimilated .......................................................................................................................................................G. carabidarum: Growth radius at 25 C . 20 mm/7 days ...................................................................................................................................G. citri-aurantii: Growth radius at 25 C , 20 mm/7 days ...................................................................................................................................G. histeridarum: Cellobiose is assimilated ...............................................................................................................................................................................................6 Cellobiose is not assimilated .......................................................................................................................................................................................8 Growth occurs at 30 C ..................................................................................................................................................................................................7 Growth is absent at 30 C........................................................................................................................................................................G. decipiens: L-Sorbose is assimilated .......................................................................................................................................................................G. fermentans: L-Sorbose is not assimilated ..........................................................................................................................................................G. cucujoidarum: Mannitol is assimilated .................................................................................................................................................................................................9 Mannitol is not assimilated ....................................................................................................................................................G. pseudocandidum: G. europaeum: a. Growth occurs at 35 C; growth radius at 25 C . 15 mm/7 days ..........................................................................................G. candidum: b. Growth is absent at 35 C; growth radius at 25 C , 15 mm/7 days.......................................................................................G. klebahnii:
p. 1285 p. 1280 p. 1281 p. 1283
p. 1281 p. 1282 p. 1281 p. 1285 p. 1282 p. 1280 p. 1284
TABLE 91.1 Key Characters of Species Assigned to the Genus Geotrichum Species
G. candidum G. carabidarum G. citri-aurantii G. cucujoidarum G. decipiens G. europaeum G. fermentans G. histeridarum G. klebahnii G. pseudocandidum G. restrictum 1
Growth with
Growth at
D-Galactose
L-Sorbose
Cellobiose
D-Mannitol
30 C
35 C
1 2 1 1 1 1 1 1 1 1 1
1 d/w 1 2 2 1 1 d/w 1 1 1
2 2 2 1 1/w 2 1 2 2 2 2
1 w/2 1 1 1 2 1 1 1 2 1
1 1 1 1 2 1 1 1 v 1 2
1 2 2 1 2 2 1 2 2 v 2
Growth without Vitamins 1 2 2 1 1 1 1 2 1 1 2
Range of Growth, Radius (mm/7d)1 15 4 24 6 4 21 11 7 5 20 2
43 5 64 8 9 25 21 9 11 32 3
Growth on glucose-peptone-yeast extract agar.
SYSTEMATIC DISCUSSION OF THE SPECIES 91.1. Geotrichum candidum Link : Fries (1832) See under teleomorph Galactomyces candidus: p. 414
91.2. Geotrichum carabidarum S.-O. Suh & M. Blackwell (2006)
Growth in YM broth: After 7 days at 25 C, septate hyphae with cylindrical arthroconidia, 2 3 3 3 6 μm, are abundantly formed. Budding cells are absent.
Dalmau plate culture on corn meal agar: After 10 days at 25 C, septate hyphae are present. Aerial growth is off-white with a filamentous margin. Growth radius on glucose-peptone-yeast extract agar: 4 5 mm after 7 days at 25 C (one strain, M.Th. Smith, unpublished data).
Fermentation Glucose Galactose Sucrose Maltose
d 2 2 2
Lactose Raffinose Trehalose
2 2 2
Chapter | 91
Geotrichum Link: Fries (1832)
1281
Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 2 2 2 2 2 2 2 2 2 d/w 2 1/d 2 2
D-Ribose
Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
2 2 1/d 1 2 2 2 w/2 w 2 d d/w d 2 2 n n 2 2
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
2 2 w/2
Growth at 30 C Growth at 35 C
1 2
CoQ: Not determined. Mol% G 1 C: Not determined. Gene sequence accession numbers, type strain: D1/D2 LSU rRNA 5 AY520292, SSU rRNA rDNA 5 AY520162, ITS 5 DQ143888. Cell carbohydrates: Not determined. Origin of the strain studied: CBS 9891 (NRRL Y-27727), isolated from the gut of Lelis sp. (Carabidae: Coleoptera), on a basidiocarp of Thelephora sp., Barro Colorado Island, Panama. Type strain: CBS 9891. Systematics: Suh and Blackwell (2006) isolated various arthroconidial ascomycetous yeast strains from the gut content of different insect species. On the basis of comparisons of rRNA gene sequences, these isolates differed from recognized Geotrichum species and represented three new taxa. To accommodate these taxa, Suh and Blackwell (2006) introduced G. carabidarum, G. cucujoidarum and G. histeridarum. Ecology: Geotrichum carabidarum has been found in the guts of Coleoptera and Lepidoptera species (Suh and Blackwell 2006). Biotechnology: Unknown. Agriculture and food: Unknown. Clinical importance: Unknown.
91.3. Geotrichum citri-aurantii (Ferraris) E.E. Butler (Butler et al. 1988) See under teleomorph Galactomyces citri-aurantii: p. 416
91.4. Geotrichum cucujoidarum S.-O. Suh & M. Blackwell (2006) Growth in YM broth: After 7 days at 25 C, septate hyphae disarticulate into cylindrical arthroconidia that measure 1 2 3 2 11 μm. Budding cells are absent.
Dalmau plate culture on corn meal agar: After 10 days at 25 C, septate hyphae with arthroconidia are present. Aerial growth is offwhite with a filamentous margin. Growth radius on glucose-peptone-yeast extract agar: 628 mm after 7 days at 25 C (one strain, M.Th. Smith, unpublished data). Fermentation: Absent.
Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 1 2 2 2 2 2 v 1 w 2 2 v 2 2
D-Ribose
Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
2 2 1 1 2 1 2 1 1 2 d/w 1/d v w/2 2 n n 2 1
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
1 2 w/2
Growth at 37 C Growth at 40 C
1 2
CoQ: Not determined. Mol% G 1 C: Not determined. Gene sequence accession numbers, type strain: D1/D2 LSU rRNA 5 AY520305, SSU rRNA 5 AY520175, ITS 5 DQ143890. Cell carbohydrates: Not determined. Origin of the strain studied: CBS 9893 (NRRL Y-27731), isolated from the gut of an unidentified cucujoid beetle (Cucujoidae: Coleoptera), Athens, Georgia, USA. Type strain: CBS 9893. Systematics: Suh and Blackwell (2006) isolated various arthroconidial ascomycetous yeast strains from the gut content of different insect species. On the basis of comparisons of rRNA gene sequences, these isolates differed from recognized Geotrichum species and represented three new taxa. To accommodate these taxa, Suh and Blackwell (2006) introduced G. carabidarum, G. cucujoidarum and G. histeridarum. Ecology: The species has been found in the gut of different species of Coleoptera (Suh and Blackwell 2006). Biotechnology: Unknown. Agriculture and food: Unknown. Clinical importance: Unknown.
91.5. Geotrichum decipiens (L.R. Tulasne & C. Tulasne) W. Gams (1983) See under teleomorph Dipodascus armillariae: p. 388
1282
PART | IVC
Descriptions of Anamorphic Ascomycetous Genera and Species
91.6. Geotrichum europeum de Hoog & M.Th. Smith (2004) Growth on 4% malt extract/0.5% yeast extract agar: After 10 days at 20 22 C, colonies are 50 80 mm in diameter, white, flat, dry, and powdery to finely hairy. Expanding hyphae up to 8 μm wide with rounded apices are present and give rise to much narrower hyphae that branch at nearly right angles. These narrower hyphae soon disarticulate into rectangular arthroconidia (Fig. 91.2). Ellipsoidal, hyaline chlamydospore-like cells may be present. Growth radius on glucose-peptone-yeast extract agar: 21 25 mm after 7 days at 25 C (one strain, Smith et al. 1995c).
Fermentation: Absent. Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
D-Ribose
Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
2 2 1 1 2 2 2 2 1 2 1 1 1 2 2 n n 2 1
91.7. Geotrichum fermentans (Diddens & Lodder) von Arx (1977a)
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
2 2 2
Growth at 30 C Growth at 35 C
FIGURE 91.2 Geotrichum europaeum CBS 866.68. Hyphae with branching at more or less right angles, which disarticulate into rectangular arthroconidia, MEYA, 22 C. Bar 5 10 μm. Reproduced from from de Hoog and Smith (2004), with permission.
Synonyms: 1 2
CoQ: Not determined. Mol% G 1 C: low value: 36.6; high value: 43.0, CBS 866.68 (from derivative graph of Tm: Smith et al. 1995c). Gene sequence accession number, type strain: ITS 5 AY788351. Cell carbohydrates: Not determined. Origin of the strain studied: CBS 866.68, isolated from soil of wheat field, Germany, W. Gams. Type strain: CBS 866.68. Systematics: This species was described by de Hoog and Smith (2004) to validate homology group C of the G. candidum complex, which was recognized from DNA reassociation experiments (Smith et al. 1995c). Ecology: Unknown, because the species is based on a single strain isolated from wheat field soil. Biotechnology: Unknown. Agriculture and food: Unknown. Clinical importance: Unknown.
Trichosporon fermentans Diddens & Lodder (1942) Fermentotrichon fermentans (Diddens & Lodder) Novák & Zsolt (1961) Growth on 4% malt extract/0.5% yeast extract agar: After 10 days at 20 22 C, colonies are 35 40 mm in diameter, whitish, moist and somewhat raised with straight and sharp margins that later become fimbriate. Expanding hyphae are straight, initially infrequently septate, later showing septa every 20 60 μm; the main branches are 5 7 μm wide, lateral branches are 2.5 4 μm wide and disarticulate into arthroconidia, 2.8 4 3 8 30 μm. Hyphae that form later often remain intact and develop short, loose clusters of ellipsoidal cells (Fig. 91.3). Growth radius on glucose-peptone-yeast extract agar: 11 21 mm after 7 days at 25 C (five strains, Smith et al. 2000).
Fermentation Glucose Galactose Sucrose Maltose
1 1 2 2
Lactose Raffinose Trehalose
2 2 n
Chapter | 91
Geotrichum Link: Fries (1832)
1283 Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
FIGURE 91.3 Geotrichum fermentans CBS 2529. Expanding hyphae, blastoconidia and arthroconidia, MEYA, 22 C. Reproduced from de Hoog et al. (1998c), with permission.
1 v 2
Growth at 35 C Growth at 37 C Growth at 40 C
1 v 2
CoQ: Not determined. Mol% G 1 C: 42, CBS 439.83 (Tm: Guého 1979); 46.1 46.2, CBS 409.34, CBS 439.83 (BD: Guého et al. 1985); 44.9 46.7, CBS 409.34, CBS 439.83, CBS 451.83, CBS 452.83 (from derivative graph of Tm: Smith et al. 2000). Gene sequence accession numbers, type strain: D1/D2 LSU rRNA 5 U40117, SSU rRNA 5 AB000651, ITS 5 AY788351. Cell carbohydrates: Glucose, mannose and galactose are present (Gorin and Spencer 1968, Weijman 1979b). Origin of the strains studied: CBS 409.34 (CBS 5057), isolated from woodpulp mill, E. Melin; CBS 439.83 (CBS 2529, NRRL Y-1492, IFO 1199, ATCC 10675), from wood pulp, E. Rennerfelt, Sweden; CBS 451.83 (CBS 2143), CBS 452.83 (CBS 2264), from tanned sheep skin; IGC 3556, from a California black oak (Quercus kelloggii, Fagaceae). Type strain: CBS 439.83. Systematics: Because of the presence of relatively long and narrow blastoconidia, which do not inflate after detachment, and the occurrence of local, lateral branchlets with small clusters of ellipsoidal cells, this species was accepted as a distinct Geotrichum taxon by de Hoog et al. (1986). This status was confirmed by DNA reassociation experiments (Smith et al. 2000). The phylogenetic relatedness of G. fermentans to species of Geotrichum and related arthroconidial ascosporic species was examined by Kurtzman and Robnett (1995) and Ueda-Nishimura and Mikata (2000). Ecology: The species has been reported on grapes, cherries and oranges (Lugauskas et al. 2006). Biotechnology: Chen et al. (1994) reported on the production of two types of extracellular lipases by G. fermentans (cited as Trichosporon fermentans). Agriculture and food: Omemu et al. (2007) demonstrated the significance of the species as a lipase producer in the fermentation of maize for ogi, a popular breakfast gruel in West African countries. Clinical importance: Unknown.
Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 1 2 2 2 2 2 2 1 v 1 2 1 v v
D-Ribose
Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
w 2 1 1 2 v 2 1 1 2 1 1 1 2 2 n n 2 1
91.8. Geotrichum histeridarum S.-O. Suh & M. Blackwell (2006) Growth in YM broth: After 7 days at 25 C, septate hyphae with cylindrical arthroconidia, 1 2 3 3 8 μm, are formed abundantly. Budding cells are absent. Dalmau plate culture on corn meal agar: After 10 days at 25 C, septate hyphae are present. Aerial growth is off-white with a filamentous margin. Growth radius on glucose-peptone-yeast extract agar: 7 9 mm after 7 days at 25 C (one strain, M.Th. Smith, unpublished data).
Fermentation Glucose Galactose Sucrose Maltose
d/w 2 2 2
Lactose Raffinose Trehalose
2 2 2
1284
PART | IVC
Descriptions of Anamorphic Ascomycetous Genera and Species
Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 1 2 2 2 2 2 2 2 2 d/w 2 1 2 2
D-Ribose Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
2 2 1/w 1/w 2 w/2 2 1 1/d 2 1/d 1/d/w 1/d w/2 2 n n 2 2
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
2 w/2 v
Growth at 30 C Growth at 35 C
1 2
CoQ: Not determined. Mol% G 1 C: Not determined. Gene sequence accession numbers, type strain: D1/D2 LSU rRNA 5 AY520357, SSU rRNA 5 AY520227, ITS 5 DQ143889. Cell carbohydrates: Not determined. Origin of the strain studied: CBS 9892 (NRRL Y-27729), isolated from the gut of a histerid beetle (Plagiogramma schmidti, Histeridae: Coleoptera), on a basidiocarp of Coriolus sp., Barro Colorado Island, Panama. Type strain: CBS 9892. Systematics: Suh and Blackwell (2006) isolated various arthroconidial ascomycetous yeast strains from the gut content of different insect species. On the basis of comparisons of rRNA gene sequences, these isolates differed from recognized Geotrichum species and represented three new taxa. To accommodate these taxa, Suh and Blackwell (2006) introduced G. carabidarum, G. cucujoidarum and G. histeridarum. Ecology: The species has been found in the gut of Coleoptera and Lepidoptera species in Panama (Suh and Blackwell 2006). Biotechnology: Unknown. Agriculture and food: Unknown. Clinical importance: Unknown.
91.9. Geotrichum klebahnii (Stautz) Morenz (1964)
1
Growth on 4% malt extract/0.5 % yeast extract agar: After 10 days at 20 22 C, colonies are 25 30 mm in diameter, glassy-white, moist, somewhat raised and slightly veined, with margins that are fimbriate, and finally hairy. Expanding hyphae are septate every 40 80 μm, 3.5 5 μm in width, with a slight differentiation of main and lateral branches. Hyphae locally disarticulate into cubic arthroconidia measuring 2.8 3.2 3 4.5 9 μm (Fig. 91.4). Growth radius on glucose-peptone-yeast extract-agar: 5 10 mm after 7 days at 25 C (six strains, Smith et al. 2000).
Fermentation Glucose Galactose Sucrose Maltose
v w/2 2 2
Lactose Raffinose Trehalose
2 2 n
Growth (in Liquid Media)
Synonyms: Trichosporon klebahnii Stautz (1931) Endomyces lactis (Fresenius) Windisch var. klebahnii Windisch (1951) Trichosporon penicillatum do Carmo-Sousa (1965)1 Geotrichum penicillatum (do Carmo-Sousa) von Arx (1977a)
FIGURE 91.4 Geotrichum klebahnii CBS 179.30 and CBS 627.74. Expanding hyphae and arthroconidia, MEYA, 22 C. Reproduced from from de Hoog et al. (1998c), with permission.
(Stautz)
Synonymy based on DNA reassociation experiments (Smith et al. 2000).
Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose
1 2 2 2 2 1 2 2 2
D-Ribose
Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol
2 2 1 1 2 v 2 1 1
Chapter | 91
Geotrichum Link: Fries (1832)
Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
2 2 2 2 2 1 2 1 2 2
myo-Inositol DL-Lactate
Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
1285 2 1 1 v 2 2 n n 2 1
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
1 2 2
Growth at 25 C Growth at 30 C Growth at 35 C
1 v 2
CoQ: Not determined. Mol% G 1 C: 40.1 40.7, CBS 179.30, CBS 627.74 (BD: Guého et al. 1984); 41.5 42.1, CBS 179.30, CBS 196.35, CBS 627.74, CBS 511.83 (from derivative graph of Tm: Smith et al. 2000). Gene sequence accession numbers, type strain: D1/D2 LSU rRNA 5 U40114, SSU rRNA 5 AB000641, ITS 5 AY788298. Cell carbohydrates: Glucose, mannose and galactose are present in whole cell hydrolysates (Weijman 1979b). Origin of the strains studied: CBS 179.30 (NRRL Y-17568, IFO 10826), isolated from slime flux of a yew (Taxus baccata, Taxaceae), W. Stautz; CBS 196.35, from wood pulp, E. Rennerfelt; CBS 627.74 (CBS 5586, ATCC 18019), type strain of Trichosporon penicillatum, from slime flux of an elm (Ulmus sp., Ulmaceae), H.J. Phaff; CBS 511.83 (CBS 2463), from sewage filter, T.G. Tomlinson. Type strain: CBS 179.30. Systematics: On the basis of minor phenotypic differences with Dipodascus aggregatus and Geotrichum clavatum, G. klebahnii was recognized as a distinct taxon (de Hoog et al. 1986, von Arx 1977a), and this was confirmed by DNA reassociation experiments (Smith et al. 2000). The separation from D. aggregatus is supported by a difference in mol% G 1 C. The phylogenetic relatedness to species of the genus Geotrichum and its teleomorph states was studied by Kurtzman and Robnett (1995) and Ueda-Nishimura and Mikata (2000). Species distinction was examined by de Hoog and Smith (2004) on the basis of ITS sequences. Ecology: This species frequently occurs in slime fluxes of trees, and is probably selected by high concentrations of sugars in this substrate. Biotechnology: Geotrichum klebahnii was reported to degrade lignin rapidly from corn stover (Glanser and Ban 1983) and to show good growth on hemicelluloses from sugar-cane bagasse (Pou et al. 1985a, 1985b). The secretion of protopectinases with polygalacturonase activity was published in various studies (Cavalitto et al. 2000, Iguchi et al. 1996, Sakai and Okushima 1982, Sakai et al. 1989). Agriculture and food: Unknown. Clinical importance: Unknown.
91.10. Geotrichum pseudocandidum Sae¨z (1968b) See under teleomorph Galactomyces pseudocandidus: p. 418
91.11. Geotrichum restrictum de Hoog & M. Th. Smith (2004) Growth on 4% malt extract/0.5% yeast extract agar: After 10 days at 20 22 C, colonies are 25 30 mm in diameter, transparent white,
FIGURE 91.5 Geotrichum restrictum CBS 111234. Disarticulating hyphae, MEYA, 22 C. Bar 5 10 μm. Reproduced from de Hoog and Smith (2004), with permission. moist, somewhat raised and slightly veined, with margins that are fimbriate, and finally hairy. Expanding hyphae are septate and measure up to 5 μm in width, have rounded apices, and are poorly branched. Hyphae soon disarticulate into cylindrical arthroconidia, which are mostly inflated after liberation (Fig. 91.5). Growth radius on glucose-peptone-yeast extract agar: 2 3 mm after 7 days at 25 C (one strain, Smith et al. 2000).
Fermentation: Absent. Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
D-Ribose Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
2 2 1 1 2 2 2 1 1 2 2 n n 2 2 n n 2 2
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
n n n
Growth at 25 C Growth at 30 C
1 2
1286
PART | IVC
CoQ: Not determined. Mol% G 1 C: 42.7, CBS 111234 (from derivative graph of Tm: de Hoog and Smith 2004). Gene sequence accession number, type strain: ITS 5 EF126738. Cell carbohydrates: Not determined. Origin of the strain studied: CBS 111234, endophyte isolated from a Norway spruce (Picea abies, Pinaceae), Sweden, isolated by R. Vasiliauskas. Type strain: CBS 111234. Systematics: The species was described by de Hoog and Smith (2004) in their study to determine the phylogenetic relatedness of species of Geotrichum and its teleomorphic genera from ITS sequence divergence and DNA reassociation. Biotechnology: Unknown. Ecology: The only strain available was isolated as an endophyte of Picea abies in Sweden. Agriculture and food: Unknown. Clinical importance: Unknown.
COMMENTS ON THE GENUS The genus Geotrichum was originally maintained for filamentous, arthroconidial Hemiascomycetes with Galactomyces and Dipodascus as the teleomorphic genera. Kurtzman and Robnett (1995) demonstrated from D1/D2 LSU rRNA gene sequence analysis that the genus Dipodascus included two genetically distinct groups of species. De Hoog and Smith (2004) used additional rRNA gene sequence analyses as the basis for transferring Dipodascus species not related to the type species clade to the genus Magnusiomyces and its anamorph Saprochaete. The anamorphic genera Geotrichum and Saprochaete are distinguishable from the numerous arthroconidial basidiomycetous anamorphs by having soft, somewhat buttery colonies, whereas anamorphs of mushrooms are dry and cottony. From transmission electron microscopy, the hyphal septa of arthroconidial ascomycetes and basidiomycetes are differentiated by showing micropores and dolipores, respectively.
Descriptions of Anamorphic Ascomycetous Genera and Species Most Geotrichum species have restricted ecological niches. Several species occur in wound saps of trees or are found on fruits or have been isolated from guts of Coleoptera species. One species, G. decipiens (teleomorph Dipodascus armillariae) is strictly associated with one species of mushroom, i.e., the honey mushroom (Armillaria sp.). Since the study of de Hoog and Smith (2004), a few more Geotrichum species have been described. Geotrichum silvicola was introduced by Pimenta et al. (2005), and G. vulgare by Wuczkowski et al. (2006). From D1/D2 LSU rRNA gene analyses, each species was recognized as a distinct taxon, closely related to Galactomyces geotrichum. However, both analyses did not include three taxa, Gal. candidus, Gal. pseudocandidus and G. europaeum, that were closely related to Gal. geotrichum (de Hoog and Smith 2004). Since the morphological and physiological properties of G. silvicola could be identified with Gal. Candidus, and those of G. vulgare with Gal. pseudocandidus (M.Th. Smith, unpublished data), further molecular examination is needed to support the species status of G. silvicola and of G. vulgare. Consequently, these species are not included in this study. The species G. carabidarum, G. histeridarum and G. cucujoidarum introduced by Suh and Blackwell (2006) are accepted because sequence analyses of the ribosomal RNA genes demonstrated that these species are distantly related to the species of the Galactomyces and Dipodascus subclades.
SPECIES RECEIVED TOO LATE FOR INCLUSION IN THIS CHAPTER 1. Geotrichum bryndzae Sulo, Laurenc ík, Poláková, Minárik & Sláviková (2009) 2. Geotrichum ghanense Nielsen, Jakobsen & Jespersen (2010a) 3. Geotrichum phurueaensis Limtong, Kaewwichian, Yongmanitchai, Srisuk & Fujjiyama (Kaewwichian et al. 2010) 4. Geotrichum siamensis Limtong, Kaewwichian, Yongmanitchai, Srisuk & Fujjiyama (Kaewwichian et al. 2010)
Geotrichum Link: Fries (1832) G. Sybren de Hoog and Maudy Th. Smith
DIAGNOSIS OF THE GENUS Asexual reproduction: Colonies are white, farinose or hairy, usually dry, and consist of true hyphae, which branch at broad or right angles, have rounded apices, and disarticulate into arthroconidia. Sympodially produced blastoconidia may also be present. Budding is absent. Chlamydospores may be formed. Septa have micropores. Sexual reproduction: Dipodascus and Galactomyces represent the teleomorphic states of Geotrichum. Physiology/biochemistry: Fermentation is often absent. D-Xylose is assimilated. Nitrate is not assimilated. Extracellular starch is not produced. The diazonium blue B reaction is negative. Small subunit rRNA gene sequences are without deletions. Phylogenetic placement: Saccharomycetales. Geotrichum and its teleomorphic states Dipodascus and Galactomyces are sister genera to Magnusiomyces and its anamorphic state Saprochaete (Figs 13.1, 91.1).
TYPE SPECIES Geotrichum candidum Link: Fries
Dipodascus aggregatus CBS 175.53T / AY788294
99
Geotrichum restrictum CBS 111234T / EF126738 Geotrichum klebahnii CBS 179.30T / AY788298
85
Dipodascus armillariae CBS 817.71T / AY788348 Dipodascus macrosporus CBS 259.82T / AY788310 Dipodascus albidus CBS 766.85 / AY788342 Dipodascus geniculatus CBS 184.80T / AY788301
88
Dipodascus australiensis CBS 372.83 / AY788314 Geotrichum fermentans CBS 439.83T / AY788318 Galactomyces citri-aurantii CBS 175.89T / AY788295 Galactomyces reessii CBS 179.60T / AY788299 97
Galactomyces pseudocandidus CBS 626.83T / AY788334 84
Geotrichum europaeum CBS 866.68T / AY788351 90
Galactomyces geotrichum CBS 773.71 / AY788343 Galactomyces candidus CBS 178.71 / AY788297
0.05 substitutions/site FIGURE 91.1 Phylogenetic tree showing the relationship of species of the genus Geotrichum and its teleomorphic genera Dipodascus and Galactomyces determined from maximum likelihood analysis of ITS sequences using RaxML (Stamatakis et al. 2008). Bootstrap values (.80%) are from 1000 replicates. GenBank accession numbers follow strain numbers.
SPECIES ACCEPTED 1. 2. 3. 4. 5.
Geotrichum candidum Link: Fries (1832) Geotrichum carabidarum S.-O. Suh & M. Blackwell (2006) Geotrichum citri-aurantii (Ferraris) E.E. Butler (1988) Geotrichum cucujoidarum S.-O. Suh & M. Blackwell (2006) Geotrichum decipiens (L.R. Tulasne & C. Tulasne) W. Gams (1983)
The Yeasts, a Taxonomic Study © 2011 Elsevier B.V. All rights reserved.
1279
1280 6. 7. 8. 9. 10. 11.
PART | IVC
Descriptions of Anamorphic Ascomycetous Genera and Species
Geotrichum europaeum de Hoog & M.Th. Smith (2004) Geotrichum fermentans (Diddens & Lodder) von Arx (1977a) Geotrichum histeridarum S.-O. Suh & M. Blackwell (2006) Geotrichum klebahnii (Stautz) Morenz (1964) Geotrichum pseudocandidum Saëz (1968b) Geotrichum restrictum de Hoog & M.Th. Smith (2004)
KEY TO SPECIES 1. 2 (1). 3 (2). 4(3). 5(1). 6(5). 7(6). 8(5).
9(8).
a. b. a. b. a. b. a. b. a. b. a. b. a. b. a. b.
Vitamins are required for growth .............................................................................................................................................................................2 Vitamins are not required for growth .....................................................................................................................................................................5 Growth occurs at 30 C ..................................................................................................................................................................................................3 Growth is absent at 30 C......................................................................................................................................................................G. restrictum: D-Galactose is assimilated ............................................................................................................................................................................................4 D-Galactose is not assimilated .......................................................................................................................................................G. carabidarum: Growth radius at 25 C . 20 mm/7 days ...................................................................................................................................G. citri-aurantii: Growth radius at 25 C , 20 mm/7 days ...................................................................................................................................G. histeridarum: Cellobiose is assimilated ...............................................................................................................................................................................................6 Cellobiose is not assimilated .......................................................................................................................................................................................8 Growth occurs at 30 C ..................................................................................................................................................................................................7 Growth is absent at 30 C........................................................................................................................................................................G. decipiens: L-Sorbose is assimilated .......................................................................................................................................................................G. fermentans: L-Sorbose is not assimilated ..........................................................................................................................................................G. cucujoidarum: Mannitol is assimilated .................................................................................................................................................................................................9 Mannitol is not assimilated ....................................................................................................................................................G. pseudocandidum: G. europaeum: a. Growth occurs at 35 C; growth radius at 25 C . 15 mm/7 days ..........................................................................................G. candidum: b. Growth is absent at 35 C; growth radius at 25 C , 15 mm/7 days.......................................................................................G. klebahnii:
p. 1285 p. 1280 p. 1281 p. 1283
p. 1281 p. 1282 p. 1281 p. 1285 p. 1282 p. 1280 p. 1284
TABLE 91.1 Key Characters of Species Assigned to the Genus Geotrichum Species
G. candidum G. carabidarum G. citri-aurantii G. cucujoidarum G. decipiens G. europaeum G. fermentans G. histeridarum G. klebahnii G. pseudocandidum G. restrictum 1
Growth with
Growth at
D-Galactose
L-Sorbose
Cellobiose
D-Mannitol
30 C
35 C
1 2 1 1 1 1 1 1 1 1 1
1 d/w 1 2 2 1 1 d/w 1 1 1
2 2 2 1 1/w 2 1 2 2 2 2
1 w/2 1 1 1 2 1 1 1 2 1
1 1 1 1 2 1 1 1 v 1 2
1 2 2 1 2 2 1 2 2 v 2
Growth without Vitamins 1 2 2 1 1 1 1 2 1 1 2
Range of Growth, Radius (mm/7d)1 15 4 24 6 4 21 11 7 5 20 2
43 5 64 8 9 25 21 9 11 32 3
Growth on glucose-peptone-yeast extract agar.
SYSTEMATIC DISCUSSION OF THE SPECIES 91.1. Geotrichum candidum Link : Fries (1832) See under teleomorph Galactomyces candidus: p. 414
91.2. Geotrichum carabidarum S.-O. Suh & M. Blackwell (2006)
Growth in YM broth: After 7 days at 25 C, septate hyphae with cylindrical arthroconidia, 2 3 3 3 6 μm, are abundantly formed. Budding cells are absent.
Dalmau plate culture on corn meal agar: After 10 days at 25 C, septate hyphae are present. Aerial growth is off-white with a filamentous margin. Growth radius on glucose-peptone-yeast extract agar: 4 5 mm after 7 days at 25 C (one strain, M.Th. Smith, unpublished data).
Fermentation Glucose Galactose Sucrose Maltose
d 2 2 2
Lactose Raffinose Trehalose
2 2 2
Chapter | 91
Geotrichum Link: Fries (1832)
1281
Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 2 2 2 2 2 2 2 2 2 d/w 2 1/d 2 2
D-Ribose
Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
2 2 1/d 1 2 2 2 w/2 w 2 d d/w d 2 2 n n 2 2
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
2 2 w/2
Growth at 30 C Growth at 35 C
1 2
CoQ: Not determined. Mol% G 1 C: Not determined. Gene sequence accession numbers, type strain: D1/D2 LSU rRNA 5 AY520292, SSU rRNA rDNA 5 AY520162, ITS 5 DQ143888. Cell carbohydrates: Not determined. Origin of the strain studied: CBS 9891 (NRRL Y-27727), isolated from the gut of Lelis sp. (Carabidae: Coleoptera), on a basidiocarp of Thelephora sp., Barro Colorado Island, Panama. Type strain: CBS 9891. Systematics: Suh and Blackwell (2006) isolated various arthroconidial ascomycetous yeast strains from the gut content of different insect species. On the basis of comparisons of rRNA gene sequences, these isolates differed from recognized Geotrichum species and represented three new taxa. To accommodate these taxa, Suh and Blackwell (2006) introduced G. carabidarum, G. cucujoidarum and G. histeridarum. Ecology: Geotrichum carabidarum has been found in the guts of Coleoptera and Lepidoptera species (Suh and Blackwell 2006). Biotechnology: Unknown. Agriculture and food: Unknown. Clinical importance: Unknown.
91.3. Geotrichum citri-aurantii (Ferraris) E.E. Butler (Butler et al. 1988) See under teleomorph Galactomyces citri-aurantii: p. 416
91.4. Geotrichum cucujoidarum S.-O. Suh & M. Blackwell (2006) Growth in YM broth: After 7 days at 25 C, septate hyphae disarticulate into cylindrical arthroconidia that measure 1 2 3 2 11 μm. Budding cells are absent.
Dalmau plate culture on corn meal agar: After 10 days at 25 C, septate hyphae with arthroconidia are present. Aerial growth is offwhite with a filamentous margin. Growth radius on glucose-peptone-yeast extract agar: 628 mm after 7 days at 25 C (one strain, M.Th. Smith, unpublished data). Fermentation: Absent.
Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 1 2 2 2 2 2 v 1 w 2 2 v 2 2
D-Ribose
Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
2 2 1 1 2 1 2 1 1 2 d/w 1/d v w/2 2 n n 2 1
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
1 2 w/2
Growth at 37 C Growth at 40 C
1 2
CoQ: Not determined. Mol% G 1 C: Not determined. Gene sequence accession numbers, type strain: D1/D2 LSU rRNA 5 AY520305, SSU rRNA 5 AY520175, ITS 5 DQ143890. Cell carbohydrates: Not determined. Origin of the strain studied: CBS 9893 (NRRL Y-27731), isolated from the gut of an unidentified cucujoid beetle (Cucujoidae: Coleoptera), Athens, Georgia, USA. Type strain: CBS 9893. Systematics: Suh and Blackwell (2006) isolated various arthroconidial ascomycetous yeast strains from the gut content of different insect species. On the basis of comparisons of rRNA gene sequences, these isolates differed from recognized Geotrichum species and represented three new taxa. To accommodate these taxa, Suh and Blackwell (2006) introduced G. carabidarum, G. cucujoidarum and G. histeridarum. Ecology: The species has been found in the gut of different species of Coleoptera (Suh and Blackwell 2006). Biotechnology: Unknown. Agriculture and food: Unknown. Clinical importance: Unknown.
91.5. Geotrichum decipiens (L.R. Tulasne & C. Tulasne) W. Gams (1983) See under teleomorph Dipodascus armillariae: p. 388
1282
PART | IVC
Descriptions of Anamorphic Ascomycetous Genera and Species
91.6. Geotrichum europeum de Hoog & M.Th. Smith (2004) Growth on 4% malt extract/0.5% yeast extract agar: After 10 days at 20 22 C, colonies are 50 80 mm in diameter, white, flat, dry, and powdery to finely hairy. Expanding hyphae up to 8 μm wide with rounded apices are present and give rise to much narrower hyphae that branch at nearly right angles. These narrower hyphae soon disarticulate into rectangular arthroconidia (Fig. 91.2). Ellipsoidal, hyaline chlamydospore-like cells may be present. Growth radius on glucose-peptone-yeast extract agar: 21 25 mm after 7 days at 25 C (one strain, Smith et al. 1995c).
Fermentation: Absent. Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
D-Ribose
Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
2 2 1 1 2 2 2 2 1 2 1 1 1 2 2 n n 2 1
91.7. Geotrichum fermentans (Diddens & Lodder) von Arx (1977a)
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
2 2 2
Growth at 30 C Growth at 35 C
FIGURE 91.2 Geotrichum europaeum CBS 866.68. Hyphae with branching at more or less right angles, which disarticulate into rectangular arthroconidia, MEYA, 22 C. Bar 5 10 μm. Reproduced from from de Hoog and Smith (2004), with permission.
Synonyms: 1 2
CoQ: Not determined. Mol% G 1 C: low value: 36.6; high value: 43.0, CBS 866.68 (from derivative graph of Tm: Smith et al. 1995c). Gene sequence accession number, type strain: ITS 5 AY788351. Cell carbohydrates: Not determined. Origin of the strain studied: CBS 866.68, isolated from soil of wheat field, Germany, W. Gams. Type strain: CBS 866.68. Systematics: This species was described by de Hoog and Smith (2004) to validate homology group C of the G. candidum complex, which was recognized from DNA reassociation experiments (Smith et al. 1995c). Ecology: Unknown, because the species is based on a single strain isolated from wheat field soil. Biotechnology: Unknown. Agriculture and food: Unknown. Clinical importance: Unknown.
Trichosporon fermentans Diddens & Lodder (1942) Fermentotrichon fermentans (Diddens & Lodder) Novák & Zsolt (1961) Growth on 4% malt extract/0.5% yeast extract agar: After 10 days at 20 22 C, colonies are 35 40 mm in diameter, whitish, moist and somewhat raised with straight and sharp margins that later become fimbriate. Expanding hyphae are straight, initially infrequently septate, later showing septa every 20 60 μm; the main branches are 5 7 μm wide, lateral branches are 2.5 4 μm wide and disarticulate into arthroconidia, 2.8 4 3 8 30 μm. Hyphae that form later often remain intact and develop short, loose clusters of ellipsoidal cells (Fig. 91.3). Growth radius on glucose-peptone-yeast extract agar: 11 21 mm after 7 days at 25 C (five strains, Smith et al. 2000).
Fermentation Glucose Galactose Sucrose Maltose
1 1 2 2
Lactose Raffinose Trehalose
2 2 n
Chapter | 91
Geotrichum Link: Fries (1832)
1283 Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
FIGURE 91.3 Geotrichum fermentans CBS 2529. Expanding hyphae, blastoconidia and arthroconidia, MEYA, 22 C. Reproduced from de Hoog et al. (1998c), with permission.
1 v 2
Growth at 35 C Growth at 37 C Growth at 40 C
1 v 2
CoQ: Not determined. Mol% G 1 C: 42, CBS 439.83 (Tm: Guého 1979); 46.1 46.2, CBS 409.34, CBS 439.83 (BD: Guého et al. 1985); 44.9 46.7, CBS 409.34, CBS 439.83, CBS 451.83, CBS 452.83 (from derivative graph of Tm: Smith et al. 2000). Gene sequence accession numbers, type strain: D1/D2 LSU rRNA 5 U40117, SSU rRNA 5 AB000651, ITS 5 AY788351. Cell carbohydrates: Glucose, mannose and galactose are present (Gorin and Spencer 1968, Weijman 1979b). Origin of the strains studied: CBS 409.34 (CBS 5057), isolated from woodpulp mill, E. Melin; CBS 439.83 (CBS 2529, NRRL Y-1492, IFO 1199, ATCC 10675), from wood pulp, E. Rennerfelt, Sweden; CBS 451.83 (CBS 2143), CBS 452.83 (CBS 2264), from tanned sheep skin; IGC 3556, from a California black oak (Quercus kelloggii, Fagaceae). Type strain: CBS 439.83. Systematics: Because of the presence of relatively long and narrow blastoconidia, which do not inflate after detachment, and the occurrence of local, lateral branchlets with small clusters of ellipsoidal cells, this species was accepted as a distinct Geotrichum taxon by de Hoog et al. (1986). This status was confirmed by DNA reassociation experiments (Smith et al. 2000). The phylogenetic relatedness of G. fermentans to species of Geotrichum and related arthroconidial ascosporic species was examined by Kurtzman and Robnett (1995) and Ueda-Nishimura and Mikata (2000). Ecology: The species has been reported on grapes, cherries and oranges (Lugauskas et al. 2006). Biotechnology: Chen et al. (1994) reported on the production of two types of extracellular lipases by G. fermentans (cited as Trichosporon fermentans). Agriculture and food: Omemu et al. (2007) demonstrated the significance of the species as a lipase producer in the fermentation of maize for ogi, a popular breakfast gruel in West African countries. Clinical importance: Unknown.
Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 1 2 2 2 2 2 2 1 v 1 2 1 v v
D-Ribose
Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
w 2 1 1 2 v 2 1 1 2 1 1 1 2 2 n n 2 1
91.8. Geotrichum histeridarum S.-O. Suh & M. Blackwell (2006) Growth in YM broth: After 7 days at 25 C, septate hyphae with cylindrical arthroconidia, 1 2 3 3 8 μm, are formed abundantly. Budding cells are absent. Dalmau plate culture on corn meal agar: After 10 days at 25 C, septate hyphae are present. Aerial growth is off-white with a filamentous margin. Growth radius on glucose-peptone-yeast extract agar: 7 9 mm after 7 days at 25 C (one strain, M.Th. Smith, unpublished data).
Fermentation Glucose Galactose Sucrose Maltose
d/w 2 2 2
Lactose Raffinose Trehalose
2 2 2
1284
PART | IVC
Descriptions of Anamorphic Ascomycetous Genera and Species
Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 1 2 2 2 2 2 2 2 2 d/w 2 1 2 2
D-Ribose Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
2 2 1/w 1/w 2 w/2 2 1 1/d 2 1/d 1/d/w 1/d w/2 2 n n 2 2
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
2 w/2 v
Growth at 30 C Growth at 35 C
1 2
CoQ: Not determined. Mol% G 1 C: Not determined. Gene sequence accession numbers, type strain: D1/D2 LSU rRNA 5 AY520357, SSU rRNA 5 AY520227, ITS 5 DQ143889. Cell carbohydrates: Not determined. Origin of the strain studied: CBS 9892 (NRRL Y-27729), isolated from the gut of a histerid beetle (Plagiogramma schmidti, Histeridae: Coleoptera), on a basidiocarp of Coriolus sp., Barro Colorado Island, Panama. Type strain: CBS 9892. Systematics: Suh and Blackwell (2006) isolated various arthroconidial ascomycetous yeast strains from the gut content of different insect species. On the basis of comparisons of rRNA gene sequences, these isolates differed from recognized Geotrichum species and represented three new taxa. To accommodate these taxa, Suh and Blackwell (2006) introduced G. carabidarum, G. cucujoidarum and G. histeridarum. Ecology: The species has been found in the gut of Coleoptera and Lepidoptera species in Panama (Suh and Blackwell 2006). Biotechnology: Unknown. Agriculture and food: Unknown. Clinical importance: Unknown.
91.9. Geotrichum klebahnii (Stautz) Morenz (1964)
1
Growth on 4% malt extract/0.5 % yeast extract agar: After 10 days at 20 22 C, colonies are 25 30 mm in diameter, glassy-white, moist, somewhat raised and slightly veined, with margins that are fimbriate, and finally hairy. Expanding hyphae are septate every 40 80 μm, 3.5 5 μm in width, with a slight differentiation of main and lateral branches. Hyphae locally disarticulate into cubic arthroconidia measuring 2.8 3.2 3 4.5 9 μm (Fig. 91.4). Growth radius on glucose-peptone-yeast extract-agar: 5 10 mm after 7 days at 25 C (six strains, Smith et al. 2000).
Fermentation Glucose Galactose Sucrose Maltose
v w/2 2 2
Lactose Raffinose Trehalose
2 2 n
Growth (in Liquid Media)
Synonyms: Trichosporon klebahnii Stautz (1931) Endomyces lactis (Fresenius) Windisch var. klebahnii Windisch (1951) Trichosporon penicillatum do Carmo-Sousa (1965)1 Geotrichum penicillatum (do Carmo-Sousa) von Arx (1977a)
FIGURE 91.4 Geotrichum klebahnii CBS 179.30 and CBS 627.74. Expanding hyphae and arthroconidia, MEYA, 22 C. Reproduced from from de Hoog et al. (1998c), with permission.
(Stautz)
Synonymy based on DNA reassociation experiments (Smith et al. 2000).
Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose
1 2 2 2 2 1 2 2 2
D-Ribose
Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol
2 2 1 1 2 v 2 1 1
Chapter | 91
Geotrichum Link: Fries (1832)
Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
2 2 2 2 2 1 2 1 2 2
myo-Inositol DL-Lactate
Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
1285 2 1 1 v 2 2 n n 2 1
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
1 2 2
Growth at 25 C Growth at 30 C Growth at 35 C
1 v 2
CoQ: Not determined. Mol% G 1 C: 40.1 40.7, CBS 179.30, CBS 627.74 (BD: Guého et al. 1984); 41.5 42.1, CBS 179.30, CBS 196.35, CBS 627.74, CBS 511.83 (from derivative graph of Tm: Smith et al. 2000). Gene sequence accession numbers, type strain: D1/D2 LSU rRNA 5 U40114, SSU rRNA 5 AB000641, ITS 5 AY788298. Cell carbohydrates: Glucose, mannose and galactose are present in whole cell hydrolysates (Weijman 1979b). Origin of the strains studied: CBS 179.30 (NRRL Y-17568, IFO 10826), isolated from slime flux of a yew (Taxus baccata, Taxaceae), W. Stautz; CBS 196.35, from wood pulp, E. Rennerfelt; CBS 627.74 (CBS 5586, ATCC 18019), type strain of Trichosporon penicillatum, from slime flux of an elm (Ulmus sp., Ulmaceae), H.J. Phaff; CBS 511.83 (CBS 2463), from sewage filter, T.G. Tomlinson. Type strain: CBS 179.30. Systematics: On the basis of minor phenotypic differences with Dipodascus aggregatus and Geotrichum clavatum, G. klebahnii was recognized as a distinct taxon (de Hoog et al. 1986, von Arx 1977a), and this was confirmed by DNA reassociation experiments (Smith et al. 2000). The separation from D. aggregatus is supported by a difference in mol% G 1 C. The phylogenetic relatedness to species of the genus Geotrichum and its teleomorph states was studied by Kurtzman and Robnett (1995) and Ueda-Nishimura and Mikata (2000). Species distinction was examined by de Hoog and Smith (2004) on the basis of ITS sequences. Ecology: This species frequently occurs in slime fluxes of trees, and is probably selected by high concentrations of sugars in this substrate. Biotechnology: Geotrichum klebahnii was reported to degrade lignin rapidly from corn stover (Glanser and Ban 1983) and to show good growth on hemicelluloses from sugar-cane bagasse (Pou et al. 1985a, 1985b). The secretion of protopectinases with polygalacturonase activity was published in various studies (Cavalitto et al. 2000, Iguchi et al. 1996, Sakai and Okushima 1982, Sakai et al. 1989). Agriculture and food: Unknown. Clinical importance: Unknown.
91.10. Geotrichum pseudocandidum Sae¨z (1968b) See under teleomorph Galactomyces pseudocandidus: p. 418
91.11. Geotrichum restrictum de Hoog & M. Th. Smith (2004) Growth on 4% malt extract/0.5% yeast extract agar: After 10 days at 20 22 C, colonies are 25 30 mm in diameter, transparent white,
FIGURE 91.5 Geotrichum restrictum CBS 111234. Disarticulating hyphae, MEYA, 22 C. Bar 5 10 μm. Reproduced from de Hoog and Smith (2004), with permission. moist, somewhat raised and slightly veined, with margins that are fimbriate, and finally hairy. Expanding hyphae are septate and measure up to 5 μm in width, have rounded apices, and are poorly branched. Hyphae soon disarticulate into cylindrical arthroconidia, which are mostly inflated after liberation (Fig. 91.5). Growth radius on glucose-peptone-yeast extract agar: 2 3 mm after 7 days at 25 C (one strain, Smith et al. 2000).
Fermentation: Absent. Growth (in Liquid Media) Glucose Inulin Sucrose Raffinose Melibiose Galactose Lactose Trehalose Maltose Melezitose Methyl-α-D-glucoside Soluble starch Cellobiose Salicin L-Sorbose L-Rhamnose D-Xylose L-Arabinose D-Arabinose
1 2 2 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
D-Ribose Methanol Ethanol Glycerol Erythritol Ribitol Galactitol D-Mannitol D-Glucitol myo-Inositol DL-Lactate Succinate Citrate D-Gluconate D-Glucosamine N-Acetyl-D-glucosamine Hexadecane Nitrate Vitamin-free
2 2 1 1 2 2 2 1 1 2 2 n n 2 2 n n 2 2
Additional Growth Tests and Other Characteristics Arbutin Xylitol 2-Keto-D-gluconate
n n n
Growth at 25 C Growth at 30 C
1 2
1286
PART | IVC
CoQ: Not determined. Mol% G 1 C: 42.7, CBS 111234 (from derivative graph of Tm: de Hoog and Smith 2004). Gene sequence accession number, type strain: ITS 5 EF126738. Cell carbohydrates: Not determined. Origin of the strain studied: CBS 111234, endophyte isolated from a Norway spruce (Picea abies, Pinaceae), Sweden, isolated by R. Vasiliauskas. Type strain: CBS 111234. Systematics: The species was described by de Hoog and Smith (2004) in their study to determine the phylogenetic relatedness of species of Geotrichum and its teleomorphic genera from ITS sequence divergence and DNA reassociation. Biotechnology: Unknown. Ecology: The only strain available was isolated as an endophyte of Picea abies in Sweden. Agriculture and food: Unknown. Clinical importance: Unknown.
COMMENTS ON THE GENUS The genus Geotrichum was originally maintained for filamentous, arthroconidial Hemiascomycetes with Galactomyces and Dipodascus as the teleomorphic genera. Kurtzman and Robnett (1995) demonstrated from D1/D2 LSU rRNA gene sequence analysis that the genus Dipodascus included two genetically distinct groups of species. De Hoog and Smith (2004) used additional rRNA gene sequence analyses as the basis for transferring Dipodascus species not related to the type species clade to the genus Magnusiomyces and its anamorph Saprochaete. The anamorphic genera Geotrichum and Saprochaete are distinguishable from the numerous arthroconidial basidiomycetous anamorphs by having soft, somewhat buttery colonies, whereas anamorphs of mushrooms are dry and cottony. From transmission electron microscopy, the hyphal septa of arthroconidial ascomycetes and basidiomycetes are differentiated by showing micropores and dolipores, respectively.
Descriptions of Anamorphic Ascomycetous Genera and Species Most Geotrichum species have restricted ecological niches. Several species occur in wound saps of trees or are found on fruits or have been isolated from guts of Coleoptera species. One species, G. decipiens (teleomorph Dipodascus armillariae) is strictly associated with one species of mushroom, i.e., the honey mushroom (Armillaria sp.). Since the study of de Hoog and Smith (2004), a few more Geotrichum species have been described. Geotrichum silvicola was introduced by Pimenta et al. (2005), and G. vulgare by Wuczkowski et al. (2006). From D1/D2 LSU rRNA gene analyses, each species was recognized as a distinct taxon, closely related to Galactomyces geotrichum. However, both analyses did not include three taxa, Gal. candidus, Gal. pseudocandidus and G. europaeum, that were closely related to Gal. geotrichum (de Hoog and Smith 2004). Since the morphological and physiological properties of G. silvicola could be identified with Gal. Candidus, and those of G. vulgare with Gal. pseudocandidus (M.Th. Smith, unpublished data), further molecular examination is needed to support the species status of G. silvicola and of G. vulgare. Consequently, these species are not included in this study. The species G. carabidarum, G. histeridarum and G. cucujoidarum introduced by Suh and Blackwell (2006) are accepted because sequence analyses of the ribosomal RNA genes demonstrated that these species are distantly related to the species of the Galactomyces and Dipodascus subclades.
SPECIES RECEIVED TOO LATE FOR INCLUSION IN THIS CHAPTER 1. Geotrichum bryndzae Sulo, Laurenc ík, Poláková, Minárik & Sláviková (2009) 2. Geotrichum ghanense Nielsen, Jakobsen & Jespersen (2010a) 3. Geotrichum phurueaensis Limtong, Kaewwichian, Yongmanitchai, Srisuk & Fujjiyama (Kaewwichian et al. 2010) 4. Geotrichum siamensis Limtong, Kaewwichian, Yongmanitchai, Srisuk & Fujjiyama (Kaewwichian et al. 2010)