Medical Mycology Month 2012, Early Online: 1–12

The taxonomic status of Trichophyton quinckeanum

and T. interdigitale revisited: a multigene phylogenetic
approach
HUGUES BEGUIN, NANCY PYCK, MARIJKE HENDRICKX, CHANTAL PLANARD, DIRK STUBBE &
MONIQUE DETANDT
Scientific Institute of Public Health, Section of Mycology & Aerobiology, Brussels, Belgium

Trichophyton quinckeanum, known as the causative agent of mouse favus, has been a
subject of controversy since its discovery, 125 years ago. The purpose of this study
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was to examine the phylogenetic relationships between this fungus and related taxa. To
achieve this objective, the ITS rDNA region, as well as actin and β-tubulin gene regions
of various isolates were sequenced. Bayesian inference and maximum likelihood analy-
ses were conducted with T. rubrum as outgroup. Our study showed that strains identified
as T. quinckeanum and others identified as T. schoenleinii are part of the complex T.
mentagrophytes, and that their genotype cannot be confused with any other dermato-
phytes. Furthermore, this study demonstrates that the choice of the neotype of T. menta-
grophytes was inappropriate. The beta-tubulin topology also revealed that isolates of T.
interdigitale form a genetically distinct population from the type strains of Arthroderma
vanbreuseghemii. Therefore, contrary to what is generally accepted, the anthropophilic
For personal use only.

species T. interdigitale cannot be considered as the anamorph associated with the latter.
Keywords Trichophyton schoenleinii, Arthroderma vanbreuseghemii, ITS rDNA,
β -tubulin, actin

Introduction remains that all extensive studies on the agent of mouse

Since its description, Trichophyton quinckeanum (Zopf)
D.M. MacLeod & Muende, the fungus causing favus of
mice, has been the subject of controversies. First, its original
description was based on an isolate from the neck of a man
who carried flour bags [1]. The involvement of this fungus
as infectious agent has therefore been questioned, especially
since, at that time, Achorion schoenleinii (Lebert) Remak
(currently referred to as T. schoenleinii (Lebert) Langeron
& Miloch.) was considered to be the only etiologic agent of
favus in both man and animals. Second, this fungus’ taxo-
nomic status has been challenged over time as it has been
assigned to each of the following genera; Oidium, Achorion,
Sabouraudites, and Microsporum, and then finally recog-
nized as a representative of the genus Trichophyton. The fact
Received 16 January 2012; Received in final revised form 5 March 2012;
Accepted 7 April 2012
Correspondence: Hugues Beguin, Scientific Institute of Public Health,
Juliette Wytsmanstreet 14; B-1050 Brussels, Belgium. Tel: ⫹32 (0)2 642
56 31; Fax: ⫹32 (0)2 642 55 19. E-mail: hugues.beguin@wiv-isp.be
© 2012 ISHAM
favus never denied its existence [2–6].
Initially, the species delineation of the dermatophytes
was based primarily on clinical features. Emmons’ 1934
classification [7], based solely on fungal morphological
characteristics, proposed that several alleged species
including the ‘trichophytons microides’ of Sabouraud [3],
as well as T. interdigitale Priestley [8], were conspecific
with T. mentagrophytes (Robin) Blanchard. Although these
fungi have indeed microscopically similar morphologies,
the appearance of their thalli was quite variable. Therefore,
many mycologists continued to consider the downy and
granular types of T. mentagrophytes cultures as separate
taxa. The downy type cultures, commonly isolated from
chronic infections of human feet and nails, were identified
mainly as T. mentagrophytes var. interdigitale or T. inter-
digitale. The species name T. mentagrophytes was retained
for those isolates which had granular type colonies in cul-
tures, most frequently isolated from suppurative lesions of
tinea capitis, tinea corporis, tinea unguium, and tinea bar-
bae acquired from animals.
DOI: 10.3109/13693786.2012.684153
 2 Beguin et al.
In 1939, Emmons isolated a strain identical to that
described by Pinoy as Epidermophyton simii (currently T.
simii (Pinoy) Stockdale, D.W.R. Mack. & Austwick).
Emmons considered it was clearly a Trichophyton species
that fell within the limits of the variable species T. menta-
grophytes [9]. Similarly, whereas some mycologists viewed
T. quinckeanum as a distinct species [1–7,10], others
reduced it to synonymy under T. mentagrophytes [11] or
to be a variant of the latter, because of its special patho-
genic properties. Indeed, this taxon is clearly distinguish-
able from the other members of the T. mentagrophytes
group due to its ability to produce favic lesions in small
animals and occasionally in man, and, by the green fluo-
rescence of infected animal hair under the Wood’s light
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[12–15].
What follows will show that T. mentagrophytes is actu-
ally a name covering several distinct species.
Since the discovery in 1965 of the ascomycetous state
of T. simii, Arthroderma simii Stockdale, Mackenzie &
Austwick, this fungus has been considered as a separate
species (T. mentagrophytes and T. simii closely resemble
each other in morphology but fail to mate together) [16].
Two years later, Arthroderma benhamiae Ajello & S.L.
Cheng, the perfect state of some strains identified as T.
mentagrophytes var. granulosum (Sabour.) Neveu-Lem.
For personal use only.
(i.e., the granular type of T. mentagrophytes) was in turn
described [17].
However, due to the successful crossing of strains of T.
quinckeanum with tester strains of A. benhamiae, the posi-
tion of T. quinckeanum as a distinct species could not be
maintained [18].
Eight years later, while the crosses between T. simii and
T. mentagrophytes resulted only in the development of
ascocarp initials or in the production of sterile ascocarps,
Weitzman and Padhye obtained fertile ascocarps from
crosses between T. mentagrophytes var. quinckeanum and
T. simii [19]. These authors concluded that T mentagro-
phytes var. quinckeanum was more closely related to A.
simii than T. mentagrophytes, but also stated that their
results were characteristic of interspecific crosses rather
than intraspecific matings. Not long before, the A. van-
breuseghemii state was reported by Takashio to be the
teleomorph of granular isolates considered by many authors
as the most representative of T. mentagrophytes [20].
Therefore T. mentagrophytes represented a genetical com-
plex including more than one teleomorph.
The introduction of molecular methods started another
era of species delineation of the dermatophytes of the T.
mentagrophytes complex. Contrary to the view of Weitz-
man and Padhye, these molecular studies proposed that T.
mentagrophytes (but not the variety quinckeanum) would
be the taxon closest to A. simii [21–23]. In addition, accord-
ing to these studies, T. interdigitale would be considered
as the anamorph of A. vanbreuseghemii. This is inconsis-
tent with the observations of Takashio who claimed from
mating experiments that T. interdigitale was known only
by its conidial state [20].
Given all these taxonomical uncertainties, our study
therefore aimed to re-evaluate the position of the causative
agent of mouse favus and its relationships with all fungi
listed above. To do this, three unlinked DNA regions were
sequenced, i.e., the ITS rDNA region as well as a fragment
of the β -tubulin and actin genes. Bayesian inference and
maximum likelihood analyses were used to investigate
phylogenetic relationships.
Material and methods
Fungal strains
A total of 45 dermatophyte strains from the BCCM/IHEM
Collection, Brussels, Belgium (http://bccm.belspo.be/
about/ihem.php) were characterized (see Table 1). They
were originally isolated from various sources and geo-
graphical locations. Sequences of the strains CBS 106.67
(T. mentagrophytes var. quinckeanum), CBS 433.63 and
CBS 855.71 (T. schoenleinii) and CBS 318.56 (designated
as the neotype of T. mentagrophytes), used as references in
other studies [21,24], were downloaded from GenBank and
included in the ITS data set.
DNA extraction, PCR and sequencing
Genomic DNA was extracted from the strains cultivated for
at least 5 days in Sabouraud dextrose broth by using the
Invisorb Spin Plant Mini Kit for DNA extraction (Invitek),
according to the manufacturer’s instructions. Some adapta-
tions made to the protocol included the fungal material
bring lyophilized prior to lysis, and time of lysis augmented
to at least 2 hours. The following three loci were amplified
and sequenced; (1) the internal transcribed spacer region of
the ribosomal DNA (ITS), which includes spacer regions
ITS1 and ITS2 and the ribosomal gene 5.8S, (2) a fragment
of the β -tubulin gene, and (3) a part of the actin gene. The
ITS region was amplified and sequenced using the ITS5
and IT2 (5′-CCTCCGCTTATTGATATGCTTAGG-3′, mo-
dified from ITS4) primers [25]. The primers Bt2b and Bt2a
described by Glass and Donaldson [26] were used for
amplification and sequencing of the partial β-tubulin gene.
Amplification and sequencing of a fragment of actin was
done using primer pair actin5 and actin3 [27]. PCR prod-
ucts were purified using the Wizard PCR Preps DNA Puri-
fication System (Promega). Sequencing was performed
using ABI 3130xl Genetic Analyser and ABI Prism BigDye
Terminator 3.1 chemistry, according to the manufacturer’s
instruction. To resolve undetermined sites as much as
© 2012 ISHAM, Medical Mycology, Early Online: 1–12
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For personal use only.

Table 1 Isolates of dermatophytes used in this study.

GenBank accession number

Taxon Isolate Source ITS Actin β-tubulin

A. benhamiae_afr IHEM 4032 ⫽ RV 25293 Human dermatomycosis; Mozambique JQ407180 JQ407089 JQ407134
A. benhamiae_afr IHEM 4033 ⫽ RV 27926 Human dermatomycosis; South Africa JQ407181 JQ407090 JQ407135
A. benhamiae_ameu T IHEM 4710 ⫽ ATCC 16781 SA : TM-17 (a); Ajello & Cheng [17] JQ407182 JQ407092 JQ407137
A. benhamiae_ameu T IHEM 24908 ⫽ ATCC 16782 SA : TM-20 (A); Ajello & Cheng [17] JQ407183 JQ407091 JQ407136
A. simii T IHEM 4420 ⫽ IMI 101695 SA (-) from IMI 98944 (poultry, India); Stockdale et al. [16] JQ407210 JQ407093 JQ407138
A. simii T IHEM 4421 ⫽ IMI 101693 SA (⫹) from IMI 98944 (poultry, India; Stockdale et al. [16] JQ407209 JQ407094 JQ407139
A. vanbreuseghemii IHEM 4028 ⫽ RV 24720 Human; Mozambique JQ407190 JQ407101 JQ407146
A. vanbreuseghemii IHEM 4412 ⫽ RV27436 Human circinate herpes; France JQ407187 JQ407102 JQ407147
A. vanbreuseghemii T IHEM 14193 ⫽ RV 27960 SA-181 (⫹); Takashio [20] JQ407185 JQ407096 JQ407141
A. vanbreuseghemii IHEM 19643 ⫽ RV 27438 Human foot; France JQ407184 JQ407097 JQ407142
A. vanbreuseghemii IHEM 19644 ⫽ RV28833 Tinea corporis on a human leg JQ407191 JQ407098 JQ407143
A. vanbreuseghemii IHEM 19645 ⫽ RV 28834 Human scalp; UK JQ407188 JQ407099 JQ407144
A. vanbreuseghemii T IHEM 19701 ⫽ RV 27961 SA -187 (-); Takashio [20] JQ407189 JQ407100 JQ407145

© 2012 ISHAM, Medical Mycology, Early Online: 1–12

A. vanbreuseghemii IHEM 10162 Chinchilla with ringworm; Belgium JQ407186 JQ407095 JQ407140
T. mentagrophytes NT CBS 318.56 Deep human trichophytosis; The Netherlands Z97995
T. mentagrophytes s.l. IHEM 4268 Tinea corporis (on a human face); Belgium JQ407193 JQ407118 JQ407163
T. mentagrophytes s.l. IHEM 4270 Tinea corporis (on a human face); Belgium JQ407194 JQ407119 JQ407164
T. mentagrophytes s.l. IHEM 19024 Ringworm on a Pudu puda; Belgium JQ407192 JQ407117 JQ407162
T.interdigitale IHEM 584 Tinea pedis; Belgium JQ407200 JQ407114 JQ407159
T.interdigitale IHEM 620 Tinea pedis; Belgium JQ407196 JQ407115 JQ407160
T.interdigitale IHEM 1104 Floor swimming pool; Belgium JQ407208 JQ407103 JQ407148
T.interdigitale IHEM 1210 Floor swimming pool; Belgium JQ407202 JQ407104 JQ407149
T.interdigitale IHEM 1237 Floor swimming pool; Belgium JQ407201 JQ407105 JQ407150
T.interdigitale IHEM 1723 Floor swimming pool; Belgium JQ407204 JQ407107 JQ407152
T.interdigitale IHEM 2497 Tinea pedis; Belgium JQ407205 JQ407108 JQ407153
T.interdigitale IHEM 2562 Tinea pedis; Belgium JQ407195 JQ407109 JQ407154
T.interdigitale IHEM 2792 Tinea pedis; Belgium JQ407198 JQ407110 JQ407155
T.interdigitale IHEM 3227 Human dermatomycosis; Belgium JQ407197 JQ407111 JQ407156
T.interdigitale IHEM 3290 Tinea pedis; Belgium JQ407199 JQ407112 JQ407157
T.interdigitale IHEM 3720 Floor swimming pool; Belgium JQ407207 JQ407113 JQ407158
T.interdigitale IHEM 7493 Floor tropical swimming pool; Belgium JQ407203 JQ407116 JQ407161
T.interdigitale IHEM 13244 Onychomycosis; Belgium JQ407206 JQ407106 JQ407151
T. quinckeanum CBS 106.67 Human hand, skin; The Netherlands Z98000
T. quinckeanum IHEM 13570 ⫽ RV 32629 ⫽ Dog favus; USA JQ407222 JQ407120 JQ407165
CDC X-395 ⫽ Blank’s isolate T19
T. quinckeanum IHEM 13571 ⫽ RV 32627 ⫽ Human favus; USA JQ407217 JQ407121 JQ407166
CDC X-396 ⫽ Blank’s isolate T24
T. quinckeanum IHEM 13572 ⫽ RV 28111 Mouse favus; Australia JQ407216 JQ407122 JQ407167
T. quinckeanum IHEM 13573 ⫽ RV 28110 Mouse favus; Australia JQ407223 JQ407123 JQ407168
T. quinckeanum IHEM 13574 ⫽ RV 28109 Mouse favus; Australia JQ407218 JQ407124 JQ407169
T. quinckeanum IHEM 13575 ⫽ RV 28108 Mouse favus; Australia JQ407220 JQ407125 JQ407170
Taxonomic status of T. quinckeanum and T. Interdigitale

T. quinckeanum IHEM 13576 ⫽ RV 28107 Mouse favus; Australia JQ407214 JQ407126 JQ407171
T. quinckeanum IHEM 13577 ⫽ RV7234 Rivalier’s collection JQ407215 JQ407127 JQ407172
3

(Continued)
 4 Beguin et al.

possible, both forward and reverse sequences were obtained

Abbreviations used: ATCC, American Type Culture Collection; B, Janssens Pharmaceutica Collection (integrated in the BCCM/IHEM Collection); CBS, Centraalbureau voor Schimmelcultures,
Baarn; IHEM, BCCM/IHEM Biomedical fungi and yeasts collection, Brussels, Belgium; IMI, CABI Fungal Reference Collection; RV, Raymond Vanbreuseghem Collection (integrated in the
JQ407173

JQ407174
JQ407175

JQ407178
JQ407176
JQ407177
β-tubulin
for all three loci and multiple repeats of the sequences were
made when undetermined sites remained. Sequences were

BCCM/IHEM Collection); CDC, Centers for Disease Control, Atlanta, Georgia. SA, single ascospore; T, ex-type strain; ameu, American-European race; afr, African race; s.l. sensu lato.
assembled and edited using DNASTAR Lasergene 8. All
GenBank accession number

DNA sequences determined for this study were deposited

in GenBank, with the accession numbers given in Table 1.
JQ407128

JQ407129
JQ407130

JQ407133
JQ407131
JQ407132
Actin

Phylogenetic analyses
MAFFT v6.814b [28] was used for initial sequence align-
ment with manual optimization in MacClade 4.04 [29]. An
ambiguously aligned region in the β-tubulin alignment was
JQ407219

JQ407221
JQ407179

JQ407211
JQ407213
JQ407212
ITS

Z98010
Z98011

excluded for analysis.

Data for each gene were analyzed separately and
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together as a combined multilocus sequence (MLS). Based

on previous studies [21,23], T. rubrum was selected as the
outgroup. All three datasets were analyzed using Bayesian
inference (BI) and Maximum likelihood (ML). All analy-
ses were performed multiple times.
A model of evolution was determined for each dataset
using MrModeltest v. 2.3 [30]. This resulted in the GTR ⫹ G
model for ITS and the K80 ⫹ G model for actin and β-tubu-
lin. Bayesian analyses were carried out using MrBayes v3.1.2
[31] with two independent runs for 2 million generations,
Source

sampling every 100 generations. Four Markov chains per

For personal use only.

Human hair; The Netherlands

Human hair; The Netherlands

run, one cold and three heated, were initiated from a random
Tinea corporis; New Guinea
Onychomycosis; Belgium

starting tree. The number of generations was considered suf-

Human favus; Morocco
Tinea capitis; Belgium
Human favus; Algeria

ficient when the log likelihood values of the cold chain were
Mouse favus; USA

stationary and the average standard deviation of split fre-

quencies had dropped below 0.01. Based on convergence of
likelihood scores, the first 2000 sampled trees (10%) were
treated as burnin and discarded. Additionally, convergence of
the chains was checked using TRACER 1.5 [32], confirming
acceptable mixing and sufficient sampling. The majority-rule
consensus tree and posterior probabilities (PP) were deter-
mined from the remaining trees. In the combined analysis,
CDC X-393 ⫽ Blank’s isolate T10

each marker was placed in a separate partition and all parti-

IHEM 13697 ⫽ RV 32626 ⫽

tions were unlinked. The same models were assigned to

IHEM 13800 ⫽ RV 25851

IHEM 13512 ⫽ RV 35443

IHEM 13515 ⫽ RV 19356
IHEM 19665 ⫽ B 63668

separate partitions as selected for single analyses.

Isolate

ML analyses were conducted using the rapid hill-climb-

ing algorithm in RAxML-VI-HPC v2.2.3 [33]. Each anal-
ysis included 1000 inferences with a random initial starting
CBS 433.63
CBS 855.71
IHEM 5232

tree for each inference and GTRMIX set as the nucleotide

substitution model. After the completion of 1000 infer-
ences, the topology with the highest likelihood was selected.
Non-parametric bootstrapping was carried out by comput-
ing 2000 replicates with the same substitution model. The
Table 1 (Continued )

bootstaps support values (BSS) were plotted onto the pre-

viously chosen topology with the best likelihood. Data for
T. quinckeanum

T. quinckeanum

T. schoenleinii
T. schoenleinii
T. schoenleinii
T. schoenleinii
T. schoenleinii

each marker were analyzed separately and the concatenated

T. rubrum

dataset was partitioned.

Taxon

Significant incongruence between the single-gene matri-

ces was assessed with the incongruence length difference
© 2012 ISHAM, Medical Mycology, Early Online: 1–12

test of Farris et al. [34]. One thousand replicates were con-
ducted in WinClada 1.00.08 [35] with NONA [36] invoked
as a daughter process for cladistic analysis.
Results
ITS data set
The aligned ITS data set consisted of 627 characters. The
ML and BI analyses resulted in highly similar phylogenies.
Therefore only the ML tree is shown, with the addition of
the PP of the BI analysis (Fig. 1). In the phylogeny, four
well-separated clades could be recognized. Three of them,
namely the clades of A. benhamiae, A. vanbreuseghemii/T.
interdigitale, and T. quinckeanum/T. schoenleinii), received
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high support in both the ML as well as the BI analyses.
The clade of A. simii was strongly supported by the BI
analysis (PP 0.96) but not by the ML analysis.
Within the A. benhamiae clade, American-European
and African races were clearly distinguished based on their
characteristic ITS sequence.
Trichophyton quinckeanum and T. schoenleinii formed
a highly supported monophyletic group (BSS 94/PP 0.98)
as sister taxa, differing only by three nucleotides in their
ITS sequence. No intraspecific variability was encountered
in these two subgroups. The strains identified as T. quinck-
For personal use only.
eanum or T. schoenleinii were therefore phylogenetically
different from other members of the T. mentagrophytes
complex represented here.
The remaining well-supported clade showed that T.
interdigitale grouped strongly together with representa-
tives of A. vanbreuseghemii and strains identified morpho-
logically as T. mentagrophytes sensu lato. However, the 14
ITS sequences of T. interdigitale formed a separate group,
since they were all identical, and different from those of
both latter taxa.
The downloaded sequences from GenBank of T. quinck-
eanum CBS 106.67) and T. schoenleinii (CBS 855.71 and
CBS 433.63) grouped with conspecific sequences (although
the downloaded sequences of T. schoenleinii differed from
their counterparts by two nucleotides); this was not the
case for the neotype of T. mentagrophytes (CBS 318.56),
which fell into the T. quinckeanum clade.
Actin data set
A total of 521 characters were present in the aligned actin
data set. The ML and BI analyses produced similar phy-
logenies (Fig. 2).
Similar clades could be distinguished in this tree as in
the tree based on ITS sequences. However, unlike the ITS
matrix, the actin-based phylogeny showed that A. simii iso-
lates formed a sister clade to that holding T. quinckeanum
and T. schoenleinii.
© 2012 ISHAM, Medical Mycology, Early Online: 1–12
Taxonomic status of T. quinckeanum and T. Interdigitale 5
b-tubulin data set
The data set consisted of 432 characters. The ML and BI
analyses produced similar phylogenies. Trichophyton
quinckeanum, T. schoenleinii and A. simii were grouped to
form a well-supported monophyletic group, and all, except
IHEM 4421, had identical β-tubulin sequences (Fig. 3).
Most interesting was that some (but not all) strains of A.
vanbreuseghemii, including the type strains, formed a
robust separate clade (BSS 94/PP 1).
Combined data set
The partition homogeneity test demonstrated that the
three loci sequence datasets were congruent (P ⫽ 0.08711)
and could therefore be combined and analyzed as MLS.
The concatenated matrix consisted of 1579 characters.
The ML and BI analyses resulted in similar phylogenies
(Fig. 4). It was completely congruent with the ITS phylog-
eny, except that now, the clade of A. simii was supported
by both the ML and the BI analyses. The clade holding
T. schoenleinii/T. quinckeanum also received strong sup-
port values (BSS 98/PP 1). As in the β-tubulin dataset,
some A. vanbreuseghemii isolates formed a well-supported,
separate group (BSS 81/PP 1). But what was most striking
was that all strains of T. interdigitale were grouped in
another clade which received high support in the BI analy-
sis (PP 0.95).
Discussion
Vanbreuseghem believed that T. quinckeanum was a sepa-
rate species and he was sceptical about the successful
crossing between this species and A. benhamiae. There-
fore, he considered that true strains of T. quinckeanum were
only those isolated from rodent favus, or which experimen-
tally produced yellow, cup-shaped crusts, known as scutula
[15]. The T. quinckeanum strains used in our study are
from the RV collection (Raymond Vanbreuseghem), and
since some were isolated from mouse favus, their identity
can be regarded as indisputable. Note should be taken that
Vanbreuseghem received three strains from Blank under
the name of Microsporum quinckeanum.
With the new system of classification for the dermato-
phytes proposed by Ajello in 1968 [37], which focused on
the appearance of the macroconidial wall surface, there
could no longer be any doubt about the generic placement
of T. quinckeanum. However, since previously this mor-
phological feature had no taxonomic significance, some
mycologists had treated it as a Microsporum species, as did
Blank (Blank’s illustrations show a fungus with smooth-
walled macroconidia corresponding exactly to the current
definition of the genus Trichophyton) [5,6]. Nevertheless,
 6 Beguin et al.

A. vanbreuseghemii IHEM10162
A. vanbreuseghemii IHEM14193 T
A. vanbreuseghemii IHEM19701 T
A. vanbreuseghemii IHEM19643
T. interdigitale IHEM1723
T. interdigitale IHEM2497
T. interdigitale IHEM3227
T. interdigitale IHEM1210
T. interdigitale IHEM1237
T. interdigitale IHEM584
87 T. interdigitale IHEM620
T. interdigitale IHEM2562
T. interdigitale IHEM13244
T. interdigitale IHEM2792
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T. interdigitale IHEM7493
T. interdigitale IHEM3720
T. interdigitale IHEM3290
T. interdigitale IHEM1104
84 A. vanbreuseghemii IHEM4028
A. vanbreuseghemii IHEM19644
A. vanbreuseghemii IHEM4412
A. vanbreuseghemii IHEM19645
T. mentagrophytes s.l. IHEM4270
T. mentagrophytes s.l. IHEM19024
T. mentagrophytes s.l. IHEM4268
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T. quinckeanum IHEM13697
T. quinckeanum IHEM13572
T. quinckeanum IHEM13570
T. quinckeanum IHEM13574
T. quinckeanum IHEM13575
T. quinckeanum IHEM13576
T. quinckeanum IHEM13571
T. quinckeanum IHEM13573
96 74
T. quinckeanum IHEM19665
T. quinckeanum IHEM13577
T. mentagrophytes var. mentagrophytes CBS318.56
94
T. mentagrophytes var. quinckeanum CBS106.67
T. schoenleinii IHEM5232
T. schoenleinii IHEM13515
T. schoenleinii IHEM13512
T. schoenleinii CBS855.71
76
T. schoenleinii CBS433.63
A. simii IHEM4421 T
A. simii IHEM4420 T

89 A. benhamiae _ afr IHEM4032

98 A. benhamiae _ afr IHEM4033

100 A. benhamiae _ ameur IHEM4710 T

A. benhamiae _ ameur IHEM24908 T

T. rubrum IHEM13800

0.0080

Fig. 1 Maximum likelihood tree based on ITS sequences. Bootstrap support values exceeding 70% are shown above the branches. T ⫽ ex-type strain.
The scale indicates the number of expected substitutions accumulated per nucleotide site. Branches in bold face indicate Bayesian posterior probability
greater than 0.95.

© 2012 ISHAM, Medical Mycology, Early Online: 1–12

 Taxonomic status of T. quinckeanum and T. Interdigitale 7

A. vanbreuseghemii IHEM19644
T. mentagrophytes s.l. IHEM4270
A. vanbreuseghemii IHEM14193 T
T. mentagrophytes s.l. IHEM19024
A. vanbreuseghemii IHEM19645
A. vanbreuseghemii IHEM19701 T
A. vanbreuseghemii IHEM4412
A. vanbreuseghemii IHEM10162
T. mentagrophytes s.l. IHEM4268
98
T. interdigitale IHEM2562
T. interdigitale IHEM3227
T. interdigitale IHEM620
T. interdigitale IHEM584
T. interdigitale IHEM1104
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T. interdigitale IHEM7493
T. interdigitale IHEM1237
T. interdigitale IHEM3720
T. interdigitale IHEM1210
T. interdigitale IHEM13244
T. interdigitale IHEM3290
T. interdigitale IHEM2497
T. interdigitale IHEM2792
A. vanbreuseghemii IHEM4028
For personal use only.

T. interdigitale IHEM1723
A. vanbreuseghemii IHEM19643
T. schoenleinii IHEM5232
T. quinckeanum IHEM13570
77 T. quinckeanum IHEM13573
T. quinckeanum IHEM13575
T. quinckeanum IHEM13576
T. quinckeanum IHEM13697
T. quinckeanum IHEM13577
T. quinckeanum IHEM13571
84
T. quinckeanum IHEM13572
T. quinckeanum IHEM19665
T. schoenleinii IHEM13515
T. schoenleinii IHEM13512
T. quinckeanum IHEM13574
A. simii IHEM4421 T
A. simii IHEM4420 T
A. benhamiae_afr IHEM4033
92
A. benhamiae_afr IHEM4032
100
A. benhamiae_ameur IHEM4710 T
90
A. benhamiae_ameur IHEM24908 T
T. rubrum IHEM13800

0.0040

Fig. 2 Maximum likelihood tree based on actin sequences. Bootstrap support values exceeding 70% are shown above branches. T ⫽ ex-type strain.
The scale indicates the number of expected substitutions accumulated per nucleotide site. Branches in bold face indicate Bayesian posterior probability
greater than 0.95.

© 2012 ISHAM, Medical Mycology, Early Online: 1–12

 8 Beguin et al.

A. vanbreuseghemii IHEM19643
T. interdigitale IHEM3720
T. interdigitale IHEM7493
A. vanbreuseghemii IHEM4028
T. interdigitale IHEM584
T. interdigitale IHEM1237
T. interdigitale IHEM2562
T. interdigitale IHEM1104
T. interdigitale IHEM2497
T. interdigitale IHEM13244
98 T. interdigitale IHEM3290
T. interdigitale IHEM2792
T. interdigitale IHEM1210
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T. interdigitale IHEM620
T. interdigitale IHEM1723
T. interdigitale IHEM3227
T. mentagrophytes s.l. IHEM19024
A. vanbreuseghemii IHEM10162
94 A. vanbreuseghemii IHEM19644
73
76 T. mentagrophytes s.l. IHEM4270
T. mentagrophytes s.l. IHEM4268
A. vanbreuseghemii IHEM14193 T
A. vanbreuseghemii IHEM19645
For personal use only.

A. vanbreuseghemii IHEM19701 T
A. vanbreuseghemii IHEM4412
A. simii IHEM4421 T
T. quinckeanum IHEM13572
T. quinckeanum IHEM13571
T. quinckeanum IHEM13573
99
T. quinckeanum IHEM13576
T. quinckeanum IHEM19655
T. quinckeanum IHEM13574
T. quinckeanum IHEM13570
T. quinckeanum IHEM13697
A. simii IHEM4420 T
T. schoenleinii IHEM13515
T. quinckeanum IHEM13577
T. schoenleinii IHEM13512
T. schoenleinii IHEM5232
T. quinckeanum IHEM13575
A. benhamiae_afr IHEM4033
94
94 A. benhamiae_afr IHEM4032
A. benhamiae_ameur IHEM 24908 T
98
A. benhamiae_ameur IHEM4710 T
T. rubrum IHEM13800

0.0050

Fig. 3 Maximum likelihood tree based on β-tubulin sequences. Bootstrap support values exceeding 70% are shown above branches. T ⫽ ex-type strain.
The scale indicates the number of expected substitutions accumulated per nucleotide site. Branches in bold face indicate Bayesian posterior probability
greater than 0.95.

© 2012 ISHAM, Medical Mycology, Early Online: 1–12

 Taxonomic status of T. quinckeanum and T. Interdigitale 9

T. mentagrophytes s.l. IHEM19024

T. mentagrophytes s.l. IHEM4270
A. vanbreuseghemii IHEM4412
70
A. vanbreuseghemii IHEM19645
A. vanbreuseghemii IHEM19644
81
T. mentagrophytes s.l. IHEM4268
A. vanbreuseghemii IHEM10162
77
A. vanbreuseghemii IHEM19701 T
A. vanbreuseghemii IHEM14193 T
A. vanbreuseghemii IHEM4028
T. interdigitale IHEM2497
100
T. interdigitale IHEM3720
T. interdigitale IHEM1723
T. interdigitale IHEM1237
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T. interdigitale IHEM3290
95
T. interdigitale IHEM1210
T. interdigitale IHEM584
T. interdigitale IHEM2792
T. interdigitale IHEM7493
T. interdigitale IHEM13244
T. interdigitale IHEM3227
T. interdigitale IHEM620
T. interdigitale IHEM2562
T. interdigitale IHEM1104
For personal use only.

96
A. vanbreuseghemii IHEM19643
T. quinckeanum IHEM13574
T. quinckeanum IHEM13571
T. quinckeanum IHEM13572
T. quinckeanum IHEM13570
T. quinckeanum IHEM19665
T. quinckeanum IHEM13697
T. quinckeanum IHEM13573
T. quinckeanum IHEM13577
T. quinckeanum IHEM13575
98 T. quinckeanum IHEM13576
T. schoenleinii IHEM5232

73 76 T. schoenleinii IHEM13515
T. schoenleinii IHEM13512
A. simii IHEM4421 T
87
A. simii IHEM4420 T
A. benhamiae_ameur IHEM4710 T
100
100 A. benhamiae_ameur IHEM24908 T
A. benhamiae_afr IHEM4033
99
A. benhamiae_afr IHEM4032
T. rubrum IHEM13800

0.0040

Fig. 4 Maximum likelihood tree based on the combined dataset. Bootstrap support values exceeding 70% are shown above branches. T = ex-type
strain. The scale indicates the number of expected substitutions accumulated per nucleotide site. Branches in bold face indicate Bayesian posterior
probability greater than 0.95.

© 2012 ISHAM, Medical Mycology, Early Online: 1–12

 10 Beguin et al.
it was already considered correctly as a Trichophyton spe-
cies by most mycologists. This generic affiliation was also
confirmed by successful mating between this fungus and
some strains belonging to the genus Trichophyton [18,19].
Next to that, Weitzman and Padhye [19], like La Touche
[12], also mentioned a series of morphological arguments
to reject Blank’s classification of T. quinckeanum in the
genus Microsporum.
The results of mating between the geophilic species
A. simii and T. quinckeanum obtained by Weitzman and
Padhye in 1976 [19] were rather characteristic of an inter-
specific cross and therefore that genetical analysis of prog-
eny was essential to clarify the relationship between the
parental strains. However, because Stockdale et al. [16] did
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not obtain crosses between T. mentagrophytes and A. simii,
Weitzman and Padhye concluded that T. quinckeanum was
closer to A. simii than the T. mentagrophytes strains tested
by Stockdale. Therefore, these findings were inconsistent
with the view of Ajello et al., who incorrectly considered
T. quinckeanum as a synonym of T. mentagrophytes [18,37].
However, this synonymy continues to persist, which
explains that today the correct designation of T. quinck-
eanum is still the subject of disagreements. The fact remains
that these mating studies suggested the existence of a link
between T. quinckeanum and A. simii, and that T. quinck-
For personal use only.
eanum was part of the T. mentagrophytes complex. Our
phylogenetic study indeed confirms this view.
Gräser and co-authors included a specimen originally
identified as T. mentagrophytes var. quinckeanum (CBS
106.67) in their study but, based on Blank’s interpretation
that this taxon belongs to Microsporum, they considered it
as a misidentification and concluded that the epithet should
be abandoned as a nomen dubium [21]. Indeed, Quincke’s
first description of this fungus [1], isolated from a human,
and not from a mouse, looked like what at that time could
be interpreted as a Microsporum. However, Bodin described
in 1902 that isolates recovered from favic lesions of five
mice and one child should be placed under the name Acho-
rion quinckeanum (an epithet assigned in 1890). The fun-
gus was undoubtedly the causative agent of mouse favus,
and Bodin recognized his cultures as identical to Quincke’s
fungus [2]. Blank also stated that the isolated dermato-
phytes from scutula of the mice resembled Quincke’s fun-
gus in all respects [5].
Our phylogenetic analyses on the actin gene data sepa-
rately and in combination with β-tubulin and ITS sequences
showed A. simii as a sister group of the clade containing
T. quinckeanum isolates, thus confirming the observations
obtained by the experimental matings mentioned above. A
similar result was also obtained in the molecular study of
Kawasaki et al. [38] who showed that T. quinckeanum (as
the variety quinckeanum) was intermingled with A. simii.
This contrasted with the conclusions of other molecular
studies which found that T. mentagrophytes was close to
A. simii [21,23]. In fact, in the complex T. mentagrophytes
proposed by Gräser and co-workers [21], the strain CBS
106.67, identified as T. mentagrophytes var. quinckeanum,
nested in the clade that the authors ultimately labelled as
T. mentagrophytes. However, as CBS 106.67 was a
Trichophyton isolated from human skin (and not from a
mouse, the natural habitat of T. quinckeanum), they regarded
this strain as a probable misidentification. For them, refer-
ring to the description of Blank [5], this strain should look
like a Microsporum which was not the case. As noted
above, this controversy should no longer exist. It is now
clear that CBS 106.67 had initially been correctly identi-
fied: it was found among our representatives of the
T. quinckeanum species in our tree (Fig. 1). In contrast, the
strain CBS 318.56, designated by these authors as the neo-
type of T. mentagrophytes is a misidentification, since it
was also found in our tree among the T. quinckeanum
strains. There are at least two reasons to consider the des-
ignation of this neotype, close to A. simii, not to be the best
choice. The first is that it originated from confusion between
two morphologically very similar but genetically different
taxa: the two CBS isolates mentioned above are represen-
tatives of T. quinckeanum. The second is that the term
‘mentagrophytes’ was created by Gruby, in 1842, to des-
ignate the fungus with an ectothrix parasitism (spores
forming a sheath around the hair) causing tinea barbae
(‘une espèce de cryptogame de la mentagre’) [39], that
corresponds essentially to the ‘trichophytons microides’ of
Sabouraud [3]. By contrast, hairs invaded by T. quinck-
eanum show an endothrix infection [15,40,41]. Therefore,
one may regard it a mistake not to have selected the neo-
type of T. mentagrophytes from among these ‘trichophy-
tons microides’ (precisely those that had been synonymized
with T. mentagrophytes by Emmons [7]), and which – for
most isolates – have as teleomorph A. vanbreuseghemii or
A. benhamiae [20].
All this explains why, among 48 human and animal iso-
lates, Sun et al. [42] found no genotype corresponding to
the neotype of T. mentagrophytes, whereas this cosmopoli-
tan taxon would normally be the most commonly isolated
dermatophyte from man and animals [43]. In the light of our
results, this is understandable, given the fact that this neo-
type actually represents another taxon, i.e., T. quinckeanum.
Similarly, Ninet et al. [44] found no sequence of this neo-
type from 63 strains of human and animal origins docu-
mented as ‘T. mentagrophytes’ on the basis of morphology.
She and her co-authors already suggested that the neotype
of T. mentagrophytes likely belonged to another taxon. This
taxon must be rare since it has not been found in either of
these studies. This is indeed the case for T. quinckeanum. In
any case, it rarely causes infections. In his detailed study of
this fungus, Bodin said that he had indeed recognized the
© 2012 ISHAM, Medical Mycology, Early Online: 1–12

fungus only 6 times in 10 years (5 times in mice and once
in man) among hundreds of animal and human lesions [2].
It is reasonable to think that this fungus is even rarer today
because of improved living conditions.
It is not surprising to find T. quinckeanum and T. schoen-
leinii in the same clade in our analyses. This is in agree-
ment with an earlier study from Makimura et al. [45].
Although T. schoenleinii principally creates lesions of the
scalp, whereas symptoms caused by T quinckeanum in man
are mainly localized to the glabrous skin, both cause the
production of scutula. However, T. schoenleinii is now con-
sidered as an anthropophilic species but outside of that,
these fungi are morphologically very different. Trichophy-
ton quinckeanum produces numerous microconidia and
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sometimes macroconidia, whereas T. schoenleinii virtually
never produces macro- and microconidia. Moreover antler-
like terminal hyphae with swollen hyphal tips (nail-head
hyphae) are characteristic in culture of the latter species.
From a taxonomic point of view, these two binomials have
always been regarded as different entities and our study
does not contradict this vision: the isolates representing
these two taxa have indeed different ITS rDNA sequences,
which appear to be specific for each of them. Trichophyton
quinckeanum and T. schoenleinii are two distinct patho-
genic fungi, which probably share a common saprophytic
For personal use only.
ancestor with the geophilic species A. simii.
The species status of T. interdigitale is also ambiguous,
with some even seeing it as the anamorph of A. van-
breuseghemii. However, our study showed that the T. inter-
digitale strains formed a distinct group of the latter. Indeed,
the apparent homogenous ITS genotype in T. interdigitale
contrasted with the genetic variability of the strains identi-
fied as A. vanbreuseghemii and T. mentagrophytes sensu
lato present in our phylogenetic analysis. Among the 11
sequences of both of the latter taxa, one differed from those
of T. interdigitale by six nucleotides, three others by four
nucleotides, another by three nucleotides, five others by
two nucleotides and the last by a single nucleotide. All the
A. vanbreuseghemii and T. mentagrophytes ITS sequences
differed from that of T. interdigitale by at least a single
nucleotide polymorphism at position 9 (A ⬎ G) across the
ITS rDNA sequence alignment. Therefore, this transition
was verified in all strains available in the BCCM/IHEM
collection, i.e., all 110 strains of T. interdigitale had an A
at position 9. Of the granular type of T. mentagrophytes
sensu lato and A. vanbreuseghemii, 85 (out 86) and 28 (out
of 29) respectively had a G instead of an A in 9th position
(data not shown). So, all the T. interdigitale isolates dis-
played a characteristic ITS sequence and could be readily
differentiated (with more than 99% certainty) by the nucle-
otide found at position 9 of the ITS sequence. This result
corresponds to that obtained by Heideman et al. [46]: iso-
lates of T. interdigitale characterized by this substitution in
© 2012 ISHAM, Medical Mycology, Early Online: 1–12
Taxonomic status of T. quinckeanum and T. Interdigitale 11
the ITS region (position 8) were the etiological agents of
tinea pedis and onychomycosis in 88% and 97% of cases,
respectively. The above suggested that some isolates of A.
vanbreuseghemii might have evolved from wild strains to
form a homogenous population of T. interdigitale. How-
ever, in our study, there is evidence from the β-tubulin phy-
logeny that strains of T. interdigitale belong to another
group, because the type strains of A. vanbreuseghemii were
strongly supported in a separate clade. A similar result was
obtained by phylogenetic analysis based on the combined
dataset: the T. interdigitale isolates were grouped in a well-
supported clade that excluded the tester strains of A. van-
breuseghemii. Therefore, it seems hard to believe that T.
interdigitale is the anamorph of A. vanbreuseghemii.
According to the mating behaviour and geographical origin
of some strains belonging to A. benhamiae, Takashio
showed the existence of races and varieties in this species,
and he thought that subspecific groups were also possible
in A. vanbreuseghemii [20]. Our beta-tubulin topology also
suggests the same, because, like our anthropophilic strains
of T. interdigitale, two strains identified as ‘A. van-
breuseghemii’ following a successful mating with a tester
strain (-) of A. vanbreuseghemii were outside the clade
formed by both tester strains of A. vanbreuseghemii.
Altogether, our thorough phylogenetic analysis showed
(i) that T. quinckeanum is not a variety of T. mentagro-
phytes and should be considered as a different taxon, (ii)
that T. quinckeanum and T. schoenleinii are part of the com-
plex T. mentagrophytes, (iii) that the neotype of T. menta-
grophytes is actually a T. quinckeanum isolate, and (iv) that
the genotype of the anthropophilic T. interdigitale strains
is different from that of A. vanbreuseghemii sensu stricto,
and therefore the former cannot be treated as the conidial
state of the latter.
Declaration of interest: The authors report no conflicts of
interest. The authors alone are responsible for the content
and writing of the paper.
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