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MALDI-ToF MS: Matrix Assisted Laser Desorption Ionization-Time of Flight mass spectrometry (MALDI-
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ToF MS) has emerged as the method of choice for rapid, highly accurate and cost-effective routine identification of yeast species. There are two commercially available MALDI-ToF MS systems, the Bruker Biotyper
(Bruker Daltonics, Bremen, Germany) and Vitek MS (bioMerieux). The identification rate of most common
and uncommon yeast isolates is comparable using both systems (Lee et al., 2017; Patel, 2019), although
studies have reported more misidentifications with the VITEK MS when the microorganism analysed was
not present in the database compared to Bruker Biotyper (Levesque et al., 2015). The Vitek MS has been
reported to misidentify some yeasts, notably Candida metapsilosis as Candida parapsilosis (Nobrega de
Almeida et al., 2014).
Molecular identification: ITS sequencing is useful for the identification of most clinical yeasts.
References: Barnett et al. (1983); Kurtzman et al. (2011); de Hoog et al. (2015).
15.1. Candida albicans (Robin) Berkhout
Candida albicans is a commensal of mucous membranes and the gastrointestinal tract. Environmental isolations have been made from sources contaminated by human or animal excreta, such as polluted water, soil,
air and plants. C. albicans is the most common cause of candidiasis in humans.
RG-2 organism
Culture: Colonies (SDA) white to cream coloured, smooth, glabrous, yeast-like.
Microscopy: Spherical to subspherical budding blastoconidia, 2-7 × 3-8 m in size.
India ink preparation: Negative - no capsules present.
Dalmau plate culture: Branched pseudohyphae with dense verticils of blastoconidia. Spherical chlamydo-
spores, mostly terminal, often on a slightly swollen subtending cell are formed near the edge of the cover slip.
Germ tube formation: Positive.
Physiological tests: (+ Positive, - Negative, v Variable, w Weak, s Slow).
Fermentation:
Glucose + Sucrose v Lactose –
Galactose v Maltose + Trehalose v
Growth reactions:
Glucose + L-Sorbose v myo-Inositol –
Sucrose v L-Rhamnose – DL-Lactate +
Raffinose – D-Xylose + D-Gluconate v
Melibiose – L-Arabinose v 2-Keto-D-gluconate +
Galactose + D-Arabinose v D-Glucosamine v
Lactose – D-Ribose v N-Acetyl-D-glucosamine v
Trehalose v Glycerol v D-Glucuronate –
Maltose + Erythritol – Nitrate –
Melezitose v Ribitol v Urease –
Methyl-α-D-glucoside v Galactitol – 0.1% Cycloheximide +
Soluble starch + D-Mannitol + Growth at 37oC +
Cellobiose – D-Glucitol v Growth at 42oC +
Descriptions of Medical Fungi 46
Key features: Germ tube positive, production of chlamydospores on Dalmau plate culture, fermentation of
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glucose, sugar assimilation profile and a distinctive green colour on CHROMagar™ Candida. Note: Germ
tube negative variants (previously known as C. claussenii), and sucrose-negative variants (previously
described as C. stellatoidea) may occur.
Antifungal susceptibility: (Table 15.1).
Table 15.1. Candida albicans (Australian national data with additional ISAV data from Pfaller et al., 2013a); MIC μg/mL.
Antifungal No. ≤0.016 0.03 0.06 0.125 0.25 0.5 1 2 4 8 16 32 ≥64
AmB 2635 2 16 164 648 645 875 283 2
FLU 2638 2 2 3 100 840 110 4 378 82 22 17 31 14 43
ISAV 800 733 51 5 5 2 2 1 1
VORI 2354 1936 217 84 30 28 26 12 10 2 3 6
POSA 2005 876 809 193 63 30 18 13 1 2
ITRA 2638 165 74 9 111 4 467 60 46 15 3 1 18
ANID 1731 526 656 403 137 6 1 1 1
MICA 1730 16 14 96 12 5 2 1
5FC 2638 4 207 11 96 541 273 260 88 23 12 8 3 3 20
15.2. Candida auris Satoh and Makimura
Candida auris is an emerging multidrug resistant yeast that causes invasive infections, that was first
described in 2009 in Japan and has since been reported from numerous countries (Lockhart et al., 2017a,b;
Jeffery-Smith et al., 2018; Spivak and Hanson, 2018; Heath et al., 2019; Zhu et al., 2020). Infections and
outbreaks caused by C. auris in hospital settings have been rising over the past several years. Difficulty in
its identification, multidrug resistance properties, associated high mortality rates, and long-term survival
on surfaces in the environment make C. auris particularly problematic in clinical settings (Du et al., 2020).
Candida auris is now a notifiable infection under public health regulations in many countries including
Australia.
Candida auris may be misidentified as C. haemuloni or other yeast species using conventional phenotypic
and biochemical methods (Kathuria et al., 2015; Jeffery-Smith et al., 2018). However, unlike these other
Candida species, C. auris grows at 42
et al., 2019). Candida auris is best identified by MALDI-ToF MS or by molecular methods (Du et al., 2020;
Zhu et al., 2020).
o
C, and this has become a useful differential characteristic (Casadevall
MALDI-ToF MS: Can accurately differentiate Candida auris from other fungal species; however, accurate
identification is dependent on the reference database being used (Kathuria et al., 2015; Jeffery-Smith et al.,
2018; Zhu et al., 2020).
Molecular identification: ITS and D1/D2 sequencing provide accurate species identification (Kathuria et al.,
2015; Kordalewska et al., 2017; Leach et al., 2018; Du et al., 2020; Zhu et al., 2020).
RG-2 organism
Culture: Colonies (SDA) white to cream coloured, smooth, glabrous, yeast-like.
Microscopy: Spherical to subspherical budding blastoconidia, 2-3 x 2-5 m in size.
India ink preparation: Negative - no capsules present.
Dalmau plate culture: Ovoid budding yeast cells only. No pseudohyphae produced.
Germ tube formation: Negative.
Descriptions of Medical Fungi 47
Physiological tests: (+ Positive, – Negative, v Variable, w Weak, s Slow).
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Fermentation:
Glucose + Sucrose w,+ Lactose –
Galactose – Maltose – Trehalose w,+
Growth reactions:
Glucose + L-Sorbose – myo-Inositol –
Sucrose + L-Rhamnose – DL-Lactate –
Raffinose + D-Xylose – D-Gluconate –
Melibiose – L-Arabinose – 2-Keto-D-gluconate –
Galactose – D-Arabinose – D-Glucosamine –
Lactose – D-Ribose – N-Acetyl-D-glucosamine +
Trehalose + Glycerol – D-Glucuronate –
Maltose + Erythritol – Nitrate –
Melezitose + Ribitol w,+ Urease –
Methyl-α-D-glucoside – Galactitol + 0.1% Cycloheximide –
Soluble starch + D-Mannitol + Growth at 37oC +
Cellobiose – D-Glucitol + Growth at 42oC +,w,s
Key features: Candida auris is difficult to identify using conventional phenotypic and biochemical methods
and has often been misidentified as Candida haemuloni or Saccharomyces cerevisiae. Growth at 42
o
C on
CHROMagar™ Candida produces white, pink, or dark purple colonies (Kumar et al., 2017), however on
CHROMagar™ Candida Plus, C. auris colonies display a differential light blue colour with a blue halo
(Mulet Bayona et al., 2022). Reliable identification methods are MALDI-ToF MS or ITS and D1/D2
sequencing.
Fig. 15.5. Candida auris grown on CHROMagar™ Candida Plus agar showing characteristic blue halo.
Descriptions of Medical Fungi 48
Antifungal susceptibility: (Table 15.2).
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Table 15.2. Candida auris (Chowdhary et al., 2018; and Australian national data); MIC g/mL.
Antifungal No. ≤0.016 0.03 0.06 0.125 0.25 0.5 1 2 4 8 16 32 ≥64
AmB 369 4 27 129 174 22 11 2
FLU 369 5 1 5 2 25 62 269
ISAV 353 44 138 53 35 37 23 10 8 5
VORI 369 21 23 94 91 43 36 28 19 4 10
POSA 369 97 90 85 48 31 8 3 3 2 2
ITRA 369 1 66 70 10 4 72 28 16 8 1 3
ANID 369 3 28 99 75 11 2 37 5 1 1 8
MICA 369 26 109 140 61 17 5 1 1 5 4
5FC 369 213 44 5 24 2 11 6 5 9 50
15.3. Candida bracarensis Correia et al.
Candida bracarensis is recognised as part of the Candida glabrata species complex (Correia et al., 2006). It
is phenotypically indistinguishable from C. glabrata and is best identified by MALDI-ToF or molecular
methods. C. bracarensis was described based on PCR-fingerprints and sequence divergence in the D1/D2
domains (Correia et al., 2006).
RG-2 organism
Culture: Colonies (SDA) white to cream coloured, smooth, glabrous, yeast-like.
Microscopy: Ellipsoidal budding blastoconidia, 3.9-6 x 2-4 m in size. No pseudohyphae or chlamydospores
produced.
India ink preparation: Negative - no capsules present.
Dalmau plate culture: No pseudohyphae produced.
Germ tube formation: Negative.
Physiological tests: (+ Positive, – Negative, v Variable, w Weak, s Slow, n not done).
Fermentation:
Glucose + Sucrose – Lactose –
Galactose – Maltose – Trehalose s
Growth reactions:
Glucose + L-Sorbose – myo-Inositol –
Sucrose – L-Rhamnose – DL-Lactate –
Raffinose – D-Xylose – D-Gluconate +
Melibiose – L-Arabinose – 2-Keto-D-gluconate –
Galactose – D-Arabinose – D-Glucosamine –
Lactose – D-Ribose – N-Acetyl-D-glucosamine n
Trehalose + Glycerol v D-Glucuronate –
Maltose – Erythritol – Nitrate –
Melezitose – Ribitol – Urease –
Methyl-α-D-glucoside – Galactitol – 0.1% Cycloheximide –
Soluble starch – D-Mannitol – Growth at 37oC +
Cellobiose – D-Glucitol – Growth at 42oC +
Descriptions of Medical Fungi 49
Key features: Candida bracarensis has variable API 20C patterns that overlap with C. nivariensis and some
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C. glabrata isolates and has variable results with a rapid trehalose assay. Note: C. glabrata produces mauve
coloured colonies on CHROMagar™ Candida, whereas isolates of C. bracarensis and C.nivariensis produce
white colonies on CHROMagar™ Candida (Alcoba-Florez et al., 2005; Bishop et al., 2008).
Antifungal susceptibility: (Table 15.3).
Table 15.3. Candida bracarensis (Australian national data); MIC μg/mL.
Antifungal No. ≤0.016 0.03 0.06 0.125 0.25 0.5 1 2 4 8 16 32 ≥64
AmB 12 1 3 4 3 1
FLU 12 1 4 4 2 1
ISAV 3 3 1
VORI 12 1 1 4 5 1
POSA 12 1 3 6 2
ITRA 12 1 1 7 3
ANID 12 3 3 5 1
MICA 12 11 1
5FC 12 2 2 4 3 1
15.4. Candida dubliniensis Sullivan et al.
Candida dubliniensis is an occasional cause of candidaemia and mucosal infection, especially in HIV patients.
RG-2 organism
Culture: Colonies (SDA) white to cream coloured, smooth, glabrous, yeast-like.
Microscopy: Spherical to subspherical budding blastoconidia, 3-8 x 2-7 m in size.
India ink preparation: Negative - no capsules present.
Dalmau plate culture: Branched pseudohyphae with dense verticils of blastoconidia and spherical, mostly
terminal chlamydospores.
Germ tube formation: Positive.
Physiological tests: (+ Positive, – Negative, v Variable, w Weak, s Slow).
Fermentation:
Glucose + Sucrose – Lactose –
Galactose +,s Maltose + Trehalose v
Growth reactions:
Glucose + L-Sorbose – myo-Inositol –
Sucrose + L-Rhamnose – DL-Lactate +
Raffinose – D-Xylose s,+ D-Gluconate –
Melibiose – L-Arabinose – 2-Keto-D-gluconate +
Galactose + D-Arabinose – D-Glucosamine v
Lactose – D-Ribose – N-Acetyl-D-glucosamine +
Trehalose s,+ Glycerol w,s,+ D-Glucuronate –
Maltose + Erythritol – Nitrate –
Descriptions of Medical Fungi 50
Melezitose w,+ Ribitol + Urease –
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Methyl-α-D-glucoside +,s Galactitol – 0.1% Cycloheximide s
Soluble starch w,+ D-Mannitol + Growth at 37oC +
Cellobiose – D-Glucitol + Growth at 42oC v
Key features: Germ tube positive, similar to C. albicans, except for absence of growth at 45oC (Pinjon et al.,
1998); glycerol (mostly +), methyl-α--glucoside (-), trehalose (-), and -xylose (-). Initial colonies dark green
colour on CHROMagar™ Candida and producing rough colonies on bird seed agar. ITS sequencing and
MALDI-ToF can reliably distinguish Candida dubliniensis from C. albicans.
Antifungal susceptibility: (Table 15.4).
Table 15.4. Candida dubliniensis (Australian national data with additional ISAV data from Pfaller et al., 2013a);
MIC μg/mL.
Antifungal N o. ≤0.016 0.03 0.06 0.125 0.25 0.5 1 2 4 8 16 32 ≥64
AmB 196 1 1 3 37 82 66 6
FLU 196 90 75 26 5
ISAV 54 49 4 1
VORI 193 193
POSA 185 99 63 20 3
ITRA 196 77 49 54 12 4
ANID 170 24 36 45 56 3 6
MICA 170 81 70 11 2 6
5FC 196 12 160 17 4 2 1
15.5. Candida glabrata (Anderson) S.A. Meyer & Yarrow
Synonymy: Torulopsis glabrata (Anderson) Lodder & de Vries.
Recently Candida glabrata has been recognised as a species complex consisting of C. glabrata, C. bracarensis
(Correia et al., 2006) and C. nivariensis (Alcoba-Florez et al., 2005). These three species are phenotypically
indistinguishable and are best identified by molecular methods or MALDI-ToF MS. C. bracarensis was
described based on PCR-fingerprints and sequence divergence in the D1/D2 domains (Correia et al., 2006).
C. nivariensis was differentiated from other yeasts based on ITS sequences (Borman et al., 2008).
Candida glabrata is one of the most common yeast species to be found on the body surface and is often
isolated as an incidental finding from skin and urine. It has been implicated as an “opportunistic” cause of
both superficial and systemic infections, especially in immunocompromised patients, and it has been isolated
from patients with septicaemia, pyelonephritis, pulmonary infections, endocarditis and hyperalimentation.
Approximately 10% of clinical isolates exhibit azole cross-resistance.
RG-2 organism
Culture: Colonies (SDA) white to cream coloured, smooth, glabrous, yeast-like.
Microscopy: Ovoid to ellipsoidal budding blastoconidia, 3.4 × 2.0 m in size. No pseudohyphae or
chlamydospores produced.
India ink preparation: Negative - no capsules present.
Dalmau plate culture: Ovoid budding yeast cells only. No pseudohyphae produced.
Germ tube formation: Negative.
Descriptions of Medical Fungi 51
Physiological tests: (+ Positive, – Negative, v Variable, w Weak, s Slow).
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Fermentation:
Glucose + Sucrose – Lactose –
Galactose – Maltose – Trehalose s
Growth reactions:
Glucose + L-Sorbose – myo-Inositol –
Sucrose – L-Rhamnose – DL-Lactate v
Raffinose – D-Xylose – D-Gluconate +
Melibiose – L-Arabinose – 2-Keto-D-gluconate v
Galactose – D-Arabinose – D-Glucosamine –
Lactose – D-Ribose – N-Acetyl-D-glucosamine –
Trehalose v Glycerol v D-Glucuronate –
Maltose – Erythritol – Nitrate –
Melezitose – Ribitol – Urease –
Methyl-α-D-glucoside – Galactitol – 0.1% Cycloheximide –
Soluble starch – D-Mannitol – Growth at 37oC +
Cellobiose – D-Glucitol –
Key features: Germ tube negative yeast and sugar assimilation pattern. Candida bracarensis (Correia et al.,
2006) and C. nivariensis (Alcoba-Florez et al., 2005) are recently identified cryptic species.
Antifungal susceptibility: (Table 15.5).
Table 15.5. Candida glabrata complex (Australian national data); MIC μg/mL.
Antifungal No. ≤0.016 0.03 0.06 0.125 0.25 0.5 1 2 4 8 16 32 ≥64
AmB 1763 2 8 25 280 393 594 441 19 1
FLU 1766 1 4 8 29 183 271 236 417 343 274
ISAV 503 9 26 61 74 105 129 62 16 13 8
VORI 1658 20 68 181 305 390 359 157 59 87 31 1
POSA 1563 2 11 17 71 178 361 454 289 7 146
ITRA 1766 6 19 126 358 485 395 123 33 7 214
ANID 1395 103 566 462 225 9 5 8 15 1 1
MICA 1394 1214 132 13 5 8 3 7 4 3 5
5FC 1764 3 308 1362 37 11 10 8 11 3 1 10
15.6. Candida haemuloni (Uden & Kolip.) Meyer & Yarrow
Synonymy: Candida haemuloni var. vulneris Cendejas-Bueno et al.
Note: Candida haemuloni and C. haemulonis are orthographic variants, but C. haemuloni is considered the
correct name.
Candida haemuloni has recently been reclassified as a complex of three phenotypically identical but genotypically distinct entities: C. haemuloni, C. duobushaemulonis and C. haemuloni var. vulneris, based on ITS
and D1/D2 sequencing (Cendejas-Bueno et al., 2012; Ramos et al., 2015). Candida haemuloni has been
reported from a few cases of fungaemia but clinical isolations remain rare.
Descriptions of Medical Fungi 52
RG-1 organism
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Culture: Colonies (SDA) white to cream coloured, smooth, glabrous, yeast-like.
Microscopy: Ovoid to globose, budding yeast-like cells or blastoconidia, 2-7 x 2-7 m. No pseudohyphae produced.
India ink preparation: Negative - no capsules present.
Dalmau plate culture: No pseudohyphae produced.
Germ tube formation: Negative.
Physiological tests: (+ Positive, – Negative, v Variable, w Weak, s Slow).
Fermentation:
Glucose + Sucrose + Lactose –
Galactose – Maltose – Trehalose +,s
Growth reactions:
Glucose + L-Sorbose – myo-Inositol –
Sucrose + L-Rhamnose +,w DL-Lactate –
Raffinose +,s D-Xylose – D-Gluconate +
Melibiose – L-Arabinose – 2-Keto-D-gluconate +
Galactose +,w D-Arabinose – D-Glucosamine +,s
Lactose – D-Ribose – N-Acetyl-D-glucosamine +
Trehalose + Glycerol +,s D-Glucuronate –
Maltose + Erythritol – Nitrate –
Melezitose +,w Ribitol +,s Urease –
Methyl-α-D-glucoside – Galactitol – 0.1% Cycloheximide –
Soluble starch – D-Mannitol + Growth at 30oC +
Cellobiose – D-Glucitol + Growth at 37oC –
Key features: Germ tube negative yeast and sugar assimilation pattern. C. haemuloni may be difficult to
distinguish from Debaryomyces hansenii (previously C. famata) using some commercial yeast identification
systems due to database limitations. Molecular identification may be required.
Antifungal susceptibility: (Table. 15.6).
Table 15.6. Candida haemuloni complex (Australian national data); MIC μg/mL.
Antifungal N o. ≤0.016 0.03 0.06 0.125 0.25 0.5 1 2 4 8 16 32 ≥64
AmB 30 2 10 7 7 1 2
FLU 30 1 3 1 25
VORI 28 1 1 1 1 20 4
POSA 23 1 2 1 1 3 16
ITRA 30 2 1 2 1 24
ANID 21 13 1 3 1 1 2
MICA 21 2 10 3 2 4
5FC 25 2 4 7 6 2 3 1
Descriptions of Medical Fungi 53
15.7. Candida inconspicua (Lodder & Kreger-van Rij) Meyer & Yarrow
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Synonymy: Torulopsis inconspicua Lodder & Kreger-van Rij.
Candida inconspicua is a rare cause of candidaemia.
RG-1 organism
Culture: Colonies (SDA) white to cream coloured, smooth, glabrous, yeast-like.
Microscopy: Ovoidal budding blastoconidia, 2.0-5 × 5.0-11.0 m.
India ink preparation: Negative - no capsules present.
Dalmau plate culture: Spherical to ovoid budding yeast cells only. Primitive pseudohyphae may be produced
after 14 days.
Germ tube formation: Negative.
Physiological tests: (+ Positive, – Negative, v Variable, w Weak, s Slow).
Fermentation:
Glucose + Sucrose – Lactose –
Galactose – Maltose – Trehalose –
Growth reactions:
Glucose + L-Sorbose – myo-Inositol –
Sucrose – L-Rhamnose – DL-Lactate +
Raffinose – D-Xylose – D-Gluconate –
Melibiose – L-Arabinose – 2-Keto-D-gluconate –
Galactose – D-Arabinose – D-Glucosamine +
Lactose – D-Ribose – N-Acetyl-D-glucosamine v
Trehalose – Glycerol + D-Glucuronate –
Maltose – Erythritol – Nitrate –
Melezitose – Ribitol – Urease –
Methyl-α-D-glucoside – Galactitol – 0.1% Cycloheximide –
Soluble starch – D-Mannitol – Growth at 37oC +
Cellobiose – D-Glucitol –
Key features: Germ tube negative yeast, sugar assimilation pattern, colonies are white on Candida
CHROMagar™ Candida.
Antifungal susceptibility: (Table 15.7).
Table 15.7. Candida inconspicua (Australian national data); MIC μg/mL.
Antifungal No. ≤0.016 0.03 0.06 0.125 0.25 0.5 1 2 4 8 16 32 ≥64
AmB 16 4 1 1 3 6 1
FLU 16 2 4 10
VORI 13 2 4 3 2 1
POSA 13 2 3 5 2 1
ITRA 15 2 6 6 1
ANID 2 2
MICA 2 2
5FC 14 1 1 2 4 3 1 1 1
Descriptions of Medical Fungi 54
15.8. Candida metapsilosis Tavanti et al.
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Candida metapsilosis is recognised as part of the Candida parapsilosis species complex (Tavanti et al., 2005).
It is phenotypically indistinguishable from C. parapsilosis, C. orthopsilosis and Lodderomyces elongisporus
and is best identified by ITS sequencing or MALDI-ToF MS.
RG-2 organism
Culture: Colonies (SDA) white to cream coloured, smooth, glabrous, yeast-like.
Microscopy: Ellipsoid, subglobose to fusiform budding blastoconidia, 4 x 3-6 m, with some larger
India ink preparation: Negative - no capsules present.
Dalmau plate culture: Abundant, much branched pseudohyphae produced.
Germ tube formation: Negative.
Physiological tests: (+ Positive, – Negative, v Variable, w Weak, s Slow).
Fermentation:
Glucose + Sucrose - Lactose –
Galactose + Maltose - Trehalose –
Growth reactions:
Glucose + L-Sorbose + myo-Inositol –
Sucrose + L-Rhamnose – DL-Lactate –
Raffinose – D-Xylose + D-Gluconate +
Melibiose – L-Arabinose + 2-Keto-D-gluconate +
Galactose + D-Arabinose – D-Glucosamine –
Lactose – D-Ribose + N-Acetyl-D-glucosamine +
Trehalose + Glycerol + D-Glucuronate –
Maltose + Erythritol – Nitrate –
Melezitose + Ribitol + Urease –
Methyl-α-D-glucoside + Galactitol – 0.1% Cycloheximide –
Soluble starch v D-Mannitol + Growth at 37oC +
Cellobiose – D-Glucitol + Growth at 42oC +
Key features: Candida metapsilosis cannot be distinguished phenotypically from C. parapsilosis and
C.orthopsilosis, but can be reliably identified by ITS sequencing (Tavanti et al., 2005; Borman et al., 2008;
Asadzadeh et al., 2009) and MALDI-ToF MS.
Antifungal susceptibility: (Table 15.8).
Table 15.8. Candida metapsilosis (Australian national data); MIC μg/mL.
Antifungal No. ≤0.016 0.03 0.06 0.125 0.25 0.5 1 2 4 8 16 32 ≥64
AmB 58 2 9 21 22 3 1
FLU 58 1 4 17 22 4
ISAV 7 5 1 1
VORI 58 13 31 10 4
POSA 58 6 3 15 27 5 1 1
ITRA 28 2 3 4 9 9 1
ANID 39 1 11 12 12 2 1
MICA 39 6 15 17 1
5FC 27 16 6 4 1
Descriptions of Medical Fungi 55
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