Taxonomy

Computational and Structural Biotechnology Journal 16 (2018) 197–210
Contents lists available at ScienceDirect
journal homepage: www.elsevier.com/locate/csbj
Taxonomy and evolution of Aspergillus, Penicillium and Talaromyces in the

omics era – Past, present and future
Chi-Ching Tsang a, James Y.M. Tang a, Susanna K.P. Lau a,b,c,d,e,⁎, Patrick C.Y. Woo a,b,c,d,e,⁎
a
Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong
b
Research Centre of Infection and Immunology, The University of Hong Kong, Hong Kong
c
State Key Laboratory of Emerging Infectious Diseases, The University of Hong Kong, Hong Kong
d
Carol Yu Centre for Infection, The University of Hong Kong, Hong Kong
e
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, The University of Hong Kong, Hong Kong
a r t i c l e i n f o a b s t r a c t
Article history: Aspergillus, Penicillium and Talaromyces are diverse, phenotypically polythetic genera encompassing species im-
Received 25 October 2017 portant to the environment, economy, biotechnology and medicine, causing significant social impacts. Taxo-
Received in revised form 12 March 2018 nomic studies on these fungi are essential since they could provide invaluable information on their
Accepted 23 May 2018
evolutionary relationships and define criteria for species recognition. With the advancement of various biological,
Available online 31 May 2018
biochemical and computational technologies, different approaches have been adopted for the taxonomy of Asper-
Keywords:
gillus, Penicillium and Talaromyces; for example, from traditional morphotyping, phenotyping to chemotyping
Aspergillus (e.g. lipotyping, proteotypingand metabolotyping) and then mitogenotyping and/or phylotyping. Since different
Penicillium taxonomic approaches focus on different sets of characters of the organisms, various classification and identifica-
Talaromyces tion schemes would result. In view of this, the consolidated species concept, which takes into account different
Classification types of characters, is recently accepted for taxonomic purposes and, together with the lately implemented
Evolution ‘One Fungus – One Name’ policy, is expected to bring a more stable taxonomy for Aspergillus, Penicillium and
Omics Talaromyces, which could facilitate their evolutionary studies. The most significant taxonomic change for the
three genera was the transfer of Penicillium subgenus Biverticillium to Talaromyces (e.g. the medically important
thermally dimorphic ‘P. marneffei’ endemic in Southeast Asia is now named T. marneffei), leaving both Penicillium
and Talaromyces as monophyletic genera. Several distantly related Aspergillus-like fungi were also segregated
from Aspergillus, making this genus, containing members of both sexual and asexual morphs, monophyletic as
well. In the current omics era, application of various state-of-the-art omics technologies is likely to provide com-
prehensive information on the evolution of Aspergillus, Penicillium and Talaromyces and a stable taxonomy will
hopefully be achieved.
© 2018 The Authors. Published by Elsevier B.V. on behalf of Research Network of Computational and Structural
Biotechnology. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
1. Introduction Many Aspergillus, Penicillium and Talaromyces species are economi-

cally, biotechnologically and medically important with huge social im-
Aspergillus, Penicillium and Talaromyces are diverse genera which be- pacts. For example, these species are vital to the food industry and
long to the Order Eurotiales and contain a large number of species quite a number of them are exploited to produce fermented food such
possessing a worldwide distribution and a huge range of ecological hab- as cheeses (e.g. P. roqueforti), sausages (e.g. P. nalgiovense) and soy
itats. They are ubiquitous and can be found in the air, soil, vegetation sauce (e.g. A. oryzae and A. sojae). These fungi are also important bio-
and indoor environments [1,2]. Some members are able to grow in ex- technologically for their strong degradative abilities which have been
treme environments such as those with high/low temperatures, high utilised for the production of enzymes [5,6]. In addition, they are robust
salt/sugar concentrations, low acidities or low oxygen levels [3,4]. Spe- producers of a diverse spectrum of secondary metabolites (or extrolites)
cies of the three genera are mainly environmental saprobes [3,4] and some of which could be used as drugs and antibiotics or as the lead com-
the primary contribution of these microorganisms to nature is the de- pounds of potential drug candidates with pharmaceutical or biological
composition of organic materials [1]. activities [7]. On the other hand, many of these species, such as
A. chevalieri, A. flavipes, P. citreonigrum and T. macrosporus, are food
spoiling decomposers which cause pre- and post-harvest devastation
⁎ Corresponding authors at: Department of Microbiology, Li Ka Shing Faculty of
Medicine, The University of Hong Kong, 4/F, University Pathology Building, Queen Mary
of food crops; and many of these food-spoiling species are also
Hospital Compound, Hong Kong. mycotoxin-producers [8]. Even worse, some of them are infectious
E-mail addresses: [email protected], (S.K.P. Lau), [email protected] (P.C.Y. Woo). agents and cause diseases in humans and animals. The most notorious
https://doi.org/10.1016/j.csbj.2018.05.003
2001-0370/© 2018 The Authors. Published by Elsevier B.V. on behalf of Research Network of Computational and Structural Biotechnology. This is an open access article under the CC BY
license (http://creativecommons.org/licenses/by/4.0/).
198 C.-C. Tsang et al. / Computational and Structural Biotechnology Journal 16 (2018) 197–210
pathogenic species on a global sense is A. fumigatus [9], which is the a b c

aetiological agent for the majority of aspergillosis cases [10]. Other com-
monly encountered pathogenic Aspergillus species include A. flavus,
A. nidulans, A. niger and A. terrus. Although Penicillium and Talaromyces
species are less commonly associated with human or veterinary infec-
tions, the thermally dimorphic fungus T. marneffei, previously known
as P. marneffei, is an exception. This notorious fungus is endemic in
Southeast Asia and it is able to cause systemic infections particularly
in immunocompromised individuals such as HIV-positive patients [11]
d e f
or patients with impaired cell-mediated immunity [12].
Aspergillus, Penicillium and Talaromyces were traditionally classified
according to their morphologies. As technologies capable of
characterising biological macromolecules advanced, various approaches
focusing on the profiles of different cellular constituents such as lipids,
proteins and exometabolites have emerged to supplement the taxon-
omy of these fungi. The availability of DNA sequencing technology in g h i
the past two-to-three decades has generated an enormous amount of
DNA sequence data, allowing fungal taxonomy through phylogenetics,
including genealogical concordance. The currently accepted consoli-
dated species concept [13], or informally known as the ‘polyphasic tax-
onomic approach’, has revolutionised fungal taxonomy, and the
classification scheme for a vast number of fungi has been revised. In par-
ticular, significant changes have been made to reclassify Aspergillus, Pen- j k l
icillium and Talaromyces species in the past seven years. Such revision
on the classification of these fungi results in redefined species concepts
for Aspergillus, Penicillium and Talaromyces, providing new insights on
the evolution of these important filamentous fungi. In this article, the
development of various taxonomic approaches as well as species recog-
nition and identification schemes for Aspergillus, Penicillium and
Talaromyces is reviewed. These include the traditional morphological/ m n o
phenotypic approach, the supplementary lipidomic, proteomic and
metabolomic approaches, as well as the currently widely used phyloge-
netic/consolidated approach. The clinical implications of this evolving
taxonomy are also discussed.
2. Classification and nomenclature: a brief history and recent

development
Fig. 1. Morphological features of Aspergillus, Penicillium and Talaromyces species.
(a) Colony morphology after 7 days of incubation on dichloran 18% glycerol agar, (b) a
The name Aspergillus was first introduced by Micheli in 1729 to de- conidiophore (magnification 400×) and (c) ascomata (Eurotium-like sexual stage,
scribe asexual fungi whose conidiophores resembled an aspergillum, a magnification 200×) of A. glaucus NRRL 116T. (d) Colony morphology after 7 days of
device used to sprinkle holy water [14] (Fig. 1a–f). Later in 1768 von incubation on malt extract agar (MEA), (e) a conidiophore (magnification 400×) and
Haller validated the genus [15] and in 1832 Fries sanctioned the generic (f) an ascocarp (Emericella-like sexual stage, magnification 100×) of A. nidulans NRRL
187T. (g) Colony morphology after 7 days of incubation on MEA and (h and
name [16]. Similarly, the genus Penicillium was erected by Link in 1809
i) conidiophores (magnification 400×) of P. expansum NRRL 976T. (j) Colony
[17] to accommodate asexual fungi which bore penicillum (painter’s morphology after 7 days of incubation on MEA, (k) conidiophores (magnification 400×)
brush)-like fruiting bodies (Fig. 1g–l). and (l) an ascocarp (Eupenicillium-like sexual stage, magnification 100×) of P. kewense
Although both Aspergillus and Penicillium were originally described NRRL 3332T. (m) Colony morphology after 7 days of incubation on MEA,
as anamorphic (asexual), some species of the two genera were subse- (n) conidiophores (magnification 400×) and (o) an ascocarp (magnification 100×) of
T. flavus NRRL 2098T.
quently found to be ascocarp-forming (Fig. 1c, f and l). For example,
the sexual genus Eurotium was first firmly connected to Aspergillus by
de Bary in 1854 [18] whereas the ascomycetous genus Eupenicillium names of the ‘perfect states’ (sexual morphs) of fungi took precedence
has been used to describe Penicillium species capable of producing [26], Benjamin assigned Aspergillus species which possess sexual life cy-
sclerotoid cleistothecia from as early as 1892 [19]. Since the discovery cles into the sexual genera Eurotium, Emericella and Sartorya [27]. In ad-
of the various sexual states of Aspergillus and Penicillium species, it has dition, he transferred Penicillium species with sexual life cycles to the
been controversial as to whether separate sexual generic names should ascomycetous genus Carpenteles (later synonym of Eupenicillium)
be used to describe species able to produce ascospores. In spite of the [27,28]. During his assignment, Benjamin also established the novel
fact that several sexual genera had already been established to accom- genus Talaromyces to describe Penicillium species which, in their sexual
modate the sexual morphs of some Aspergillus and Penicillium species, life cycles, possessed soft ascocarps exhibiting indeterminate growth
Thom, Church, Raper and Fennell, in their monographic masterpieces and whose walls were composed of interwoven hyphae [27] (Fig. 1m–o).
on the taxonomy of these two genera, neglected the use of sexual As the number of species of the genera Aspergillus, Penicillium and
names. This was because, in their opinions, this would cause unneces- Talaromyces increased, closely related species were grouped into
sary nomenclatural confusion, especially for strains which were in sex- subgroups [29–32]. Such infrageneric classification system underwent
ual stages at first and then lost their ascospore-forming ability under vigorous changes since different authors focused on different morpho-
laboratory maintenance. In addition, this would also lead to the frag- logical features when establishing their subgrouping schemes
mentation of the large and obviously cohesive Aspergillus/Penicillium (Table 1). For example, Blochwitz as well as Thom and his co-workers
groups [20–25]. Nevertheless, in order to abide by the then International were the first to divide Aspergillus species into seven and 18 subgeneric
Code of Botanical Nomenclature (Stockholm Code), where the first valid ‘groups’, respectively, based on their phenotypes [21,24,30,31]. The
C.-C. Tsang et al. / Computational and Structural Biotechnology Journal 16 (2018) 197–210 199
subgrouping by Thom and associates formed the foundation of Aspergil- Talaromyces species were also split into four sections based on the struc-
lus subgeneric classification which had been largely followed by other tures of their conidial states [32] (Table 1c).
mycologists working on this genus in the last century. However, since As the species concept for fungi migrates from morphological, phys-
these subgeneric ‘groups’ did not possess any nomenclatural status, iological, or phenotypic to genetic, phylogenetic (including genealogical
Gams et al., in 1986, established six subgenera and 18 sections to ac- concordance) and even consolidated, further changes have been made
commodate these ‘groups’, formalising the subgeneric classification of to the infrageneric classification of Aspergillus, Penicillium and
Aspergillus species [33] (Table 1a). As for Penicillium, Dierckx and Talaromyces (Table 1). The adoption of the consolidated species concept,
Biourge firstly subdivided the genus into the subgenera Aspergilloides with reduced emphasis on morphological properties, in classifying spe-
(synonym: Monoverticillium) as well as Eupenicillium, which was further cies of these genera resulted in the fact that fungi with aspergillum-
separated into sections Biverticillium and Bulliardium (synonym: shaped conidiophores no longer necessarily are Aspergillus species,
Asymmetrica) [29,34]. Subsequently, Thom and his co-workers did not while fungi with penicillum-shaped conidiophores no longer necessar-
follow Dierckx’s and Biourge’s grouping and proposed a new subgeneric ily are Penicillium species [37]. One notable change in relation to these
classification scheme for Penicillium composed of four main divisions/ genera, also as a result of the recent implementation of the single-
sections, where species were grouped according to features of their col- naming system(‘One Fungus – One Name’ [1F1N] principle) [38–40],
onies and branching patterns of their conidiophores [20,22]. The system was the transfer of fungi belonging to Penicillium subgenus Biverticillium
established by Thom and associates for Penicillium was adopted by other to the genus Talaromyces [41], whose close chemotaxonomic relation-
mycologists for the next 30 years until Pitt as well as Stolk and Samson ship [42] and phylogenetic connection [43–45] have been recognised
in the 1980s proposed two other subgeneric classification schemes since the 1990s, leaving both the genera Penicillium and Talaromyces
based on features of conidiophores, morphology of phialides and as monophyletic clades [41] (Fig. 2). Interestingly, during this transfer
growth characteristics, as well as branching patterns of conidiophores the species P. aureocephalum (synonym for sexual morph: Lasioderma
and phialide morphology, respectively [35,36] (Table 1b). Similarly, flavovirens) [46] was also accommodated in the Talaromyces clade.
Table 1a
Overview of major subgeneric classifications of Aspergillus species.
Blochwitz Thom & Church [30], Gams et al. [33] Peterson [168] Peterson et al. [169] Houbraken & Samson Houbraken et al. [4] Jurjević et al. [170],
[31] Thom & Raper [21], [3] Kocsubé et al. [60],
Raper & Fennell [24] Sklenář et al. [171]
f
Euglobosi Group A. candidus Subgenus Aspergillus Subgenus Subgenus Aspergillus Subgenus Aspergillus Subgenus Aspergillus Subgenus Aspergillus
Aspergillus
Flavi Group A. cervinus Section Aspergillus Section Aspergillus Section Aspergillus Section Aspergillus Section Aspergillus Section Aspergillus
Fulvi Group A. clavatus Section Restricti Section Candidi Section Restricti Section Restricti Section Restricti Section Restricti
Glauci Group A. cremeus Subgenus Section Cervini Subgenus Candidi Subgenus Circumdati Subgenus Circumdati Subgenus Circumdati
Circumdati
Nidulantes Group A. flavipes Section Candidi Section Circumdati Section Candidi Section Candidi Section Candidi Section Candidi
g
Nigroides Group A. flavus Section Circumdati Section Cremei Subgenus Circumdati Section Circumdati Section Circumdati Section Circumdati
h
Phaei Group A. fumigatus Section Cremei Section Flavi Section Circumdati Section Flavi Section Flavi Section Flavi
i
Group A. glaucus Section Flavi Section Flavipedes Section Cremei Section Flavipedes Section Flavipedes Section Flavipedes
Group A. nidulans Section Nigri Section Nigri Section Flavi Section Nigri Section Nigri Section Jani
Group A. niger Section Sparsi Section Restricti Section Nigri Section Terrei Section Terrei Section Nigri
c
Group A. ochraceus Section Wentii Section Terrei Subgenus Fumigati Subgenus Fumigati Subgenus Fumigati Section Petersonii
a
Group A. ornatus Subgenus Clavati Subgenus Fumigati Section Cervini Section Cervini Section Cervini Section Robusti
Group A. restrictus Section Clavati Section Clavati Section Clavati Section Clavati Section Clavati Section Tanneri
Group A. sparsus Subgenus Fumigati Section Fumigati Section Fumigati Section Fumigati Section Fumigati Section Terrei
a j
Group A. terreus Section Cervini Subgenus Nidulantes Subgenus Ornati Subgenus Nidulantes Subgenus Nidulantes Subgenus Cremei
a a
Group A. ustus Section Fumigati Section Ornati Section Ornati Section Aenei Section Aenei Subgenus Fumigati
b a
Group A. versicolor Subgenus Ornati Section Nidulantes Subgenus Nidulantes Section Ochraceorosei Section Bispori Section Cervini
c a k
Group A. wentii Section Ornati Section Sparsi Section Bispori Section Nidulantes Section Cremei Section Clavati
l
Subgenus Nidulantes Section Ochraceorosei Section Sparsi Section Ochraceorosei Section Fumigati
Section Flavipedes Section Nidulantes Section Usti Section Nidulantes Subgenus Nidulantes
m
Section Nidulantes Section Raperi Unassigned section Section Silvati Section Aenei
Section Terrei Section Silvati Section Cremei Section Sparsi Section Bispori
Section Usti Section Sparsi Section Usti Section Cavernicolus
b
Section Versicolores Section Usti Section Ochraceorosei
m
Subgenus Terrei Section Nidulantes
Section Flavipedes Section Raperi
Section Terrei Section Silvati
Subgenus Warcupi Section Sparsi
d m
Section Warcupi Section Usti
e
Section Zonati Subgenus
Polypaecilum
a
Transferred to genus Sclerocleista and excluded from Aspergillus [3,53]
b
Merged with section Nidulantes [168]
c
Merged with section Cremei [172]
d
Transferred to genus Warcupiella and excluded from Aspergillus [3,53]
e
Trasnferred to genus Penicilliopsis and excluded from Aspergillus [3,60]
f
Sexual synonym = Eurotium [4]
g
Sexual synonym = Neopetromyces [4]
h
Sexual synonym = Petromyces [4]
i
Sexual synonym = Fennellia [4]
j
Sexual synonym = Chaetosartorya [4]
k
Sexual synonym = Dichotomomyces and Neocarpenteles [4]
l
Sexual synonym = Neosartorya [4]
m
Sexual synonym = Emericella [4]
200
Table 1b
Overview of major subgeneric classifications of Penicillium species.
Dierckx [29] Biourge [34] Thom [20] Raper et al. [22] Pitt [35] Stolk & Samson [36] Houbraken & Samson [3], Houbraken
et al.
[173]
a
Subgenus Subgenus Eupenicillium Division Asymmetrica Section Asymmetrica Subgenus Aspergilloides Section Aspergilloides Subgenus Aspergilloides
C.-C. Tsang et al. / Computational and Structural Biotechnology Journal 16 (2018) 197–210
Aspergilloides
a b b b
Subgenus Section Biverticillium Section Brevi-compacta Section Biverticillata-symmetrica Section Aspergilloides Section Biverticillium Section Aspergilloides
Eupenicillium
Section Bulliardium Section Fasciculata Section Monoverticillata Section Exilicaulis Section Coremigenum Section Charlesii
(=Section Asymmetrica)
b
Subgenus Monoverticillium Section Funiculosa Section Polyverticillata-symmetrica Subgenus Section Divaricatum Section Cinnamopurpurea
Biverticillium
Section Lanata-divaricata Section Coremigenum Section Eladia Section Citrina
Section Lanata-typica Section Simplicium Section Geosmithia Section Exilicaulis
Section Velutina Subgenus Furcatum Section Inordinate Section Fracta
b
Division Biverticillata-symmetrica Section Divaricatum Section Ramosum Section Gracilenta
Section Ascogena Section Furcatum Section Penicillium Section Lanata-divaricata
Section Coremigena Subgenus Penicillium Section Torulomyces Section Ochrosalmonea
Section Luteo-virida Section Coronatum Section Ramigena
Section Miscellanea Section Cylindrosporum Section Sclerotiora
Division Monoverticillata Section Inordinate Section Stolkia
Section Monoverticillata-stricta Section Penicillium Section Torulomyces
Section Monoverticillata-Ramigena Section Thysanophora
Division Subgenus Penicillium
Polyverticillata-symmetrica
Section Brevicompacta
Section Canescentia
Section Chrysogena
Section Digitata
Section Eladia
Section Fasiculata
Section Osmophila
Section Paradoxa
Section Penicillium
Section Ramosa
Section Robsamsonia
Section Roquefortorum
Section Turbata
a
Not referring to the sexual genus Eupenicillium Ludwig
b
Transferred to genus Talaromyces and excluded from Penicillium
Table 1c hand, the main problem for the narrow Aspergillus concept rests in the
Overview of major subgeneric classifications of Talaromyces species retypification by conservation of the genus. This is because under the
Stolk & Samson [32] Yaguchi et al. [174] Yilmaz et al. [63] narrow Aspergillus concept, the type of the genus Aspergillus, A. glaucus
a
Section Emersonii a
Section Emersonii Section Bacillispori
of subgenus Aspergillus, would fall in the genus Eurotium instead. Since
Section Purpurea Section Purpurea Section Helici taxonomic properties of the type and related species determine the cir-
Section Talaromyces Section Talaromyces Section Islandici cumscription of the genus, if the name Aspergillus is to be applied to sub-
b b
Section Thermophila Section Thermophila Section Purpurei genus Circumdati, the type of the genus has to be changed to one of the
Section Trachyspermus Section Talaromyces
species within this subgenus, for example, A. niger as suggested by Pitt
Section Subinflati
Section Trachyspermi and Taylor because of its more frequent use in literatures and databases
a
[58]. However, in the eyes of the wide Aspergillus concept advocates,
Transferred to genus Rasamsonia and excluded from Talaromyces [175]
b
Transferred to genus Thermomyces and excluded from Talaromyces [4]
such generic retypification is debatable since the new type of choice
would depend on the interest of different fields. For instance, A. flavus
would be the type of choice for food mycology and mycotoxicology,
Inclusion of this species, which is also the type and only species of the A. fumigatus for medical mycology, whereas A. nidulans for fungal mo-
genus Lasioderma [47], necessitated the renaming of the Talaromyces lecular genetics [2]. Recently, regarding the narrow Aspergillus proposal
clade as Lasioderma, since this is an older sexual name with nomencla- which considers Aspergillus to be non-monophyletic and recommends
tural priority [48]. However, such renaming would require many to apply the name Aspergillus only to members of the subgenus
name changes (from Talaromyces species to Lasioderma species) and Circumdati through retypification by conservation while maintaining
several species are better scientifically and economically well-known the sexual names for other supported clades [58,59], Kocsubé et al., sup-
with their Talaromyces names. Also, even though using identical porters of the wide Aspergillus concept, demonstrated in their phyloge-
names for botanical/mycological and zoological genera is not forbidden netic analyses, based on six and nine genetic markers using both
by the Melbourne Code, the name Lasioderma [Ascomycota] is a later maximum likelihood and Bayesian approaches as well as extrolite pro-
homonym to Lasioderma [Arthropoda] currently in use for one of the filing, that Aspergillus represents a well-supported monophyletic clade
beetle genera and this might cause confusion to non-taxonomists. sister to the monophyletic Penicillium clade (Fig. 2) [60], rejecting Pitt
Hence, it was proposed to conserve the generic name Talaromyces et al.’s hypotheses and proposal. They also established the subgenus
over Lasioderma (Ascomycota) [49]. Recently, this proposal was ap- Polypaecilum to encompass species previously assigned to the genera
proved by both the Nomenclature Committee for Fungi (NCF) [50] and Phialosimplex and Polypaecilum (Fig. 2), whereas the species
General Committee for Nomenclature [51] of the International Associa- A. clavatoflavus and A. zonatus, which are actually phylogenetically dis-
tion for Plant Taxonomy, retaining the generic name Talaromyces. tantly related to Aspergillus, were transferred to the novel genera
Despite the fact that the taxonomy of Penicillium and Talaromyces Aspergillago as Aspergillago clavatoflava and Penicilliopsis as Penicilliopsis
seems straight-forward now since both of them clearly represent two zonata, respectively [60]. Nevertheless, Pitt and Taylor have submitted a
separate monophyletic groups [41], the scenario for Aspergillus is formal proposal to the NCF to retypify Aspergillus with A. niger to rede-
much more complicated, involving two opposing generic concepts, fine the genus to members of subgenus Circumdati only, with sexual
namely the wide and narrow Aspergillus concepts. Early work by Benja- names taken up to replace other subgeneric names of Aspergillus [61].
min summarised the links between Aspergillus and the sexual genera In response to Pitt and Taylor, Samson et al. urged the NCF to reject
Emericella, Eurotium and Neosartorya (erroneously as Sartorya by Benja- the conservation proposal based on their arguments that Aspergillus is
min which was later found that the original description of Sartorya was monophyletic as well as clearly-defined by phenotypic synapomorphies
based on a contaminant in an A. fumigatus culture receiving radium ra- and secondary metabolite chemistry; that the size of the genus Aspergil-
diation) [24,27,52]. Following other subsequent changes in Aspergillus lus is irrelevant; and that conservation with a different generic type
classification, seven additional sexual genera, including Chaetosartorya (A. niger) would lead to unpredictable name changes and would not re-
[53], Cristaspora [2], Dichotomomyces [2,54], Fennellia [55], sult in a more stable nomenclature [62]. Recently, voting was held by
Neocarpenteles [56], Neopetromyces [57] and Petromyces [52], are further the NCF and the proposal by Pitt and Taylor could not obtain a 60% ma-
connected to Aspergillus. Remarkably, each of these sexual genera only jority for the ‘yes’ vote after two rounds of ballots. Although the ‘no’ vote
associates with a particular Aspergillus subgenus or section (Table 1a). was also one vote short of reaching 60%, it was in the majority. Since
Subsequent to the adoption of 1F1N, there have been disputes as to there is no definite recommendation from the NCF, this proposal will
whether the generic name Aspergillus should be retained for the large be referred to the General Committee on Nomenclature for final deci-
monophyletic clade, although weakly supported (~50–70% bootstrap sion (Dr Tom May, personal communication).
only) by maximum likelihood analyses [3,4], of classical Aspergillus spe-
cies (broad/wide Aspergillus concept) [2]; or to adopt sexual names for 3. Species recognition/identification and current advances
those well-supported clades containing both pleomorphic species and
asexual species with Aspergillus morphologies (narrow Aspergillus con- Since the establishment of Aspergillus, Penicillium and Talaromyces,
cept; i.e. subgenus Aspergillus = Eurotium, subgenus Cremei = species in these genera had been recognised by their morphological fea-
Chaetosartorya, subgenus Fumigati = Neosartorya and subgenus tures until the dawn of molecular systematics. In particular, morphology
Nidulantes = Emericella), leaving the weakly supported (b50% boot- of conidial structures, especially their branching patterns as discussed
strap) [3] subgenus Circumdati as Aspergillus sensu stricto, even though above, has played an important role in species recognition and identifi-
this group does include several less well-known sexual genera cation. Other important morphological properties useful for diagnosing
(Fennellia, Neopetromyces and Petromyces) [58]. The latter proposal a species include cleistothecium and ascus/ascospore (when present)
was advocated based on the fact that the sexual genera Chaetosartorya, characters [1,2]. Macroscopically, characteristics of the colony, such as
Emericella, Eurotium and Neosartorya differ significantly in their mor- texture, growth rate, degree of sporulation, conidial and mycelial col-
phologies, physiologies, enzymologies, as well as toxicologies [59]. ours, as well as production of diffusing pigments, exudates, acids and
Also, Pitt, Taylor and Göker, proposers of the narrow Aspergillus concept, other secondary metabolites, are also used for species differentiation
found in their phylogenetic analyses that classical Aspergillus was [1,2,63]. The need for standardisation of culture media and incubation
paraphyletic, encompassing the monophyletic Penicillium clade. As a re- condition for reproducible species identification was recognised as
sult, according to Pitt et al. if the wide Aspergillus concept is to be early as Biourge's and Dierckx's time [64]. This is because variations in
adopted then Pencillium would also need to be synonymised under As- the immediate cultural environment, such as nutrient availability, tem-
pergillus to make the whole clade monophyletic [58,59]. On the other perature, light intensity (including ultraviolet light), water activity,
Subgenus Aspergilloides
Penicillium
Subgenus Penicillium
Subgenus Nidulantes
Subgenus Circumdati
Subgenus Fumigati
Aspergillus
Subgenus Cremei
Subgenus Aspergillus
Subgenus Polypaecilum
Hamigera, Warcupiella
Aspergillaceae Penicilliopsis
Monascus, Xeromyces, Leiothecium
Aspergillago
Phialomyces
Sclerocleista
Thermoascus
Thermoascaceae Byssochlamys/Paecilomyces
Section Talaromyces
Eurotiales Section Helici
Section Purpurei
Section Trachyspermi Talaromyces
Section Bacillispori
Section Subinflati
Section Islandici
Thermomyces
Sagenomella
Trichocomaceae Rasamsonia
Trichocoma
Coccidioides immitis
Fig. 2. Schematic representation of the phylogenetic relationship, as inferred by Houbraken & Samson [3], Yilmaz et al. [63] and Kocsubé et al. [60], amongst members of the order
Eurotiales. Aspergillus and Penicillium are sister genera of the family Aspergillaceae whereas Talaromyces is more distantly related to those two genera and belongs to a separate family,
Trichocomaceae.
humidity and/or other environmental factors, regardless how subtle quite a number of Talaromyces species were considered and
these discrepancies are, could change the appearance of the organism characterised as Penicillium species.
since morphology is one of the way in which an organism adapts to With the availability of newer techniques, such as gas–liquid chro-
and survives in its environment [1]. The effects of these changes in incu- matography and electrophoresis, for the characterisation of biomole-
bation condition have been exemplified by the work by Okura et al. cules in the 20th century, chemotaxonomy has gained popularity in
[65,66]. As such, standardised working techniques for morphological Aspergillus, Penicillium and Talaromyces taxonomy, especially since the
characterisation have been recommended for Aspergillus and Penicillium 1980s. One of the approaches for chemotaxonomy is zymogram profil-
species [1,2]. Although no standard is proposed for Talaromyces, these ing, where species are differentiated based on the polyacrylamide gel-
methods should also be applicable to this genus since by tradition electrophoretic patterns of certain isoenzymes [67]. This technique has
been demonstrated to be highly successful in differentiating species of chromatography (UHPLC/HPLC) coupled with diode array detection
Penicillium subgenus Penicillium, where the isozyme patterns showed (DAD) and mass spectrometry (MS) is the method of choice for detailed
a high correlation with morphological species [68,69]. However, when chemotaxonomic characterisation of Aspergillus, Penicillium and
species from other Penicillium subgenera were also included in the anal- Talaromyces [1,2,63,88]. With about 350 accepted species each in Asper-
ysis it was found that correlation between zymogram grouping and gillus [2,60] and Penicillium [1] and more than 100 accepted species in
morphological species only existed in some cases [70], rendering the Talaromyces [63,89], qualitative databases equipped with a large vol-
utility of this technique for the identification of Penicillium species ques- ume of verified data on the production of secondary metabolites by var-
tionable. On the other hand, zymogram profiling has also been applied ious Aspergillus, Penicillium and Talaromyces species is needed for
to Aspergillus species and this identification method was found to be accurate species identification [2]. In view of this, an Aspergillus Second-
practical especially for members of the subgenera Circumdati, Fumigati ary Metabolites Database (A2MDB) was established last year [90]. Re-
and Nidulantes [71–73], in spite of the fact that some closely related spe- cently, metabolic fingerprinting has also been demonstrated as a
cies, such as the wild type A. flavus and the domesticated counterpart potentially successful tool for differentiating closely related Aspergillus
A. oryzae or the wild type A. parasiticus and the domesticated A. sojae, species, without the need of investigating the actual identities of the
produced very similar isoenzyme patterns and could not be well differ- metabolites. For example, utilising this technique Tam et al. showed
entiated [71]. Nonetheless, fingerprinting of isozymes has not been that A. nomius and A. tamarii could be distinguished from their morpho-
widely employed as a practical identification system since the enzyme logically similar sibling A. flavus [91]. In addition, hierarchical cluster
profiles for the vast majority of Aspergillus, Penicillium and Talaromyces analysis by Tsang et al. also showed that except for A. austroafricanus,
species remained uncharacterised. Also, there is no consensus as to the metabolic fingerprints of species in the same Aspergillus section
which isoenzymes should be used for comparison. clustered together and those of infraspecific strains also formed smaller
Another approach for chemotaxonomy is extrolite profiling. The subclades [92].
exometabolome reflects the physiology of an organism in response to Fatty acid profiling is another increasingly used method in diagnos-
its biotic and abiotic environment [74] and profiling of the ing filamentous fungal species. Although characterisation of fatty acid
exometabolome is particularly useful for the chemotaxonomy of Asper- composition and relative concentration has long been utilised for bacte-
gillus, Penicillium and Talaromyces species since these genera are the rial and yeast chemotaxonomy [93,94] and there is even a commercial
best known exometabolite producers, having the most diverse spectra fatty acid methyl ester (FAME)-based bacterial/yeast identification sys-
of exometabolites amongst 26 different groups of ascomycetes tem containing profiles from more than 1,500 different species devel-
analysed, which represented four different Classes (Dothideomycetes, oped [95], there are only a few studies making use of this technique to
Eurotiomycetes, Leotiomycetes and Sordariomycetes) [37]. Amongst the characterise the chemotaxonomy of filamentous fungi [96]. This is be-
various kinds of exometabolites, such as excessive organic acids, extra- cause filamentous fungi do not produce fatty acids in the quantity and
cellular enzymes and accumulated carbohydrates, the one that gener- diversity that bacteria do [97] and therefore, traditionally fatty acid pro-
ally displays more pronounced chemoconsistency and higher species filing had been regarded to have little taxonomic value for filamentous
specificity is secondary metabolites [74]. The first insight of the taxo- fungi [98]. Blomquist et al. [99] first examined the utility of this tech-
nomic value of secondary metabolite profiling was gained when Ciegler nique on the identification of filamentous fungi. They characterised
et al. attempted to divide P. viridicatum into three subgroups, in which the fatty acid contents of conidia and found that fatty acid profiling,
the production of the mycotoxins citrinin, ochratoxin, viomellein and even though performed at different times, could potentially be used to
xanthomegnin was characterised as one of the classification criteria identify Aspergillus and Penicillium species in a reproducible way [99].
[75,76]. However, Ciegler et al.’s method required complicated and te- In 1996, Stahl and Klug performed a large-scale study to characterise
dious pre-treatment of the samples. As a result, their approach was the composition and relative concentration of fatty acids in the mycelia
only popularised after the development of simpler techniques which of a number of filamentous fungi from across different phyla [98]. Seven
only involve direct spotting of small agar plugs from fungal cultures species of Penicillium and one of Aspergillus were included in their study.
on thin-layer chromatography plates without the need of any preceding It was revealed that four fatty acids, namely palmitic acid (C16:0),
extraction or purification procedures [77,78]. Since then, extrolite data stearic acid (C18:0), oleic acid (C18:1Δ9[cis]) and linoleic acid
have contributed much to species recognition of Aspergillus, Penicillium (C18:2Δ9,12[cis]), represented more than 95% of the total cellular fatty
and Talaromyces species. For example, using secondary metabolite pro- acid content. These four fatty acids were also common to all the filamen-
filing Frisvad and Filtenborg classified more than 4,000 isolates of tous fungi characterised. In spite of this, discriminant analysis showed
terverticillate penicillia into 38 taxa and chemotypes, where infrataxon that the fatty acid profiles for these species are significantly different.
strains exhibited chemoconsistency in terms of the production of myco- Notably, all the seven Penicillium species characterised were found to
toxins [79]. They also reidentified a large number of misidentified Peni- possess unique fatty acid profiles [98]. Later in 1998, Da Silva et al. ex-
cillium strains based on their profiles of secondary metabolites [79–81]. panded the characterisation to 18 Penicillium species [100]; and they
Frisvad and Filtenborg, together with Samson and Stolk, also pioneered found that different Penicillium subgenera could be readily differenti-
the chemotaxonomy of Talaromyces. Again, their analysis demonstrated ated by fatty acid profiling. Moreover, in some cases, species of the
that the production of secondary metabolites by members of this genus same subgenus such as Furcatum could be separated based on their
was taxon-specific and they also recognised T. macrosporus and T. luteus fatty acid profiles, which mainly differed in the relative concentration
as separate species from T. flavus and T. udagawae, respectively, because rather than the composition of fatty acids; although difficulties existed
of their different metabolic profiles [42]. In fact, this chemotaxonomic for the subgenus Penicillium [100]. The fact that the species differentia-
work offered one of the very first indications of the connection between tion power relied on the variation in fatty acid relative concentration
Talaromyces and Penicillium subgenus Biverticillium [42]. An overview of was observed by Mahmoud et al. as well [101]. Fatty acid profiling has
the extrolite profiles for various Talaromyces species was given in the also been successfully used to differentiate Aspergillus species [102,103].
latest monograph on the genus by Yilmaz et al. [63]. The same also ap- A recent chemotaxonomic approach for rapid identification of Asper-
plies to Aspergillus species [82–86]. Notably, different Aspergillus gillus, Penicillium and Talaromyces is matrix-assisted laser desorption/
subgenera produce different unique extrolites, as summarised by ionisation–time-of-flight (MALDI–TOF) MS. The technology compares
Frisvad and Larsen [87]. Thus, the production of a certain secondary me- the cellular protein profiles of different organisms to achieve identifica-
tabolite by an Aspergillus isolate would serve as a practical hint for iden- tion at the species level [104]. The advantage of this technique is that the
tification at the sectional level, whereas the identification of several methodology is simple, rapid and inexpensive, requiring a specialised
secondary metabolites of the organism would be an effective tool for bench-top MALDI–TOF mass spectrometer only. Also, since the majority
species recognition [2]. Currently, (ultra) high-performance liquid of proteins analysed by MALDI–TOF MS are constitutively expressed
Table 2
Novel Aspergillus, Penicillium and Talaromyces species/taxonomic entities described during January, 2013 to December, 2017 sampled from human or non-human vertebrate specimens
Species Synonym(s) Associated human infections or clinical Associated non-human vertebrates Molecular Year of Reference(s)
specimensa markersb valid
publication
Aspergillus
A. aurantiopurpureus Novel species Kangaroo rat cheek pouch ITS, benA, cmdA 2016 [86]
and rpb2
A. caninus ≡ Phialosimplex Bone marrow aspirate of a dog rpb2 2014 [2,176,177]
caninus,
A. capsici ≡ Scopulariopsis Fur and skin of hibernating bat 2014 [2,178]
capsica
= Leuconeurospora
capsica
A. chlamydosporus ≡ Sagenomella Disseminated infection in a dog rpb2 2014 [2,176,179,180]
chlamydospore
= Phialosimplex
chlamydosporus
A. citrinoterreus Novel species Nails, various respiratory specimen, benA and cmdA 2015 [181]
wound and biopsy
A. contaminans Novel species Fingernail (probably as a contaminant) ITS, benA, cmdA 2017 [182]
and rpb2
A. europaeus Novel species Toenail ITS, benA and 2016 [183]
cmdA
A. felis Novel species Chronic invasive pulmonary Invasive fungal rhinosinusitis in ITS, benA and 2013 [184–187]
aspergillosis and onychomycosis; BAL, domestic cats and disseminated cmdA
oropharyngeal exudate and sputum invasive aspergillosis in a dog
A. hongkongensis Novel species Onychomycosis ITS, benA, cmdA, 2016 [92]
rpb2, mcm7 and
tsr1
A. insolitus ≡ Polypaecilum Onychomycosis; ear cct8, rpb2 and 2014 [2,188]
insolitum tsr1
A. keratitidis ≡ Sagenomella Keratitis ITS and 28S 2017 [189,190]
keratitidis nrDNA
A. latilabiatus Novel species Sheep dung ITS, benA, cmdA 2016 [86]
and rpb2
A. latus ≡ Aspergillus nidulans Invasive pulmonary aspergillosis ITS, benA, cmdA 2016 [53,86,191–195]
var. latus and rpb2
= Aspergillus
montenegroi
= Aspergillus
sublatus
= Emericella
montenegroi
= Emericella nidulans
var. lata
= Emericella sublata
A. magnivesiculatus Novel species Child carriers ITS, benA, cmdA 2017 [171]
and rpb2
A. mallochii Novel species Pack rat dung benA, cmdA and 2017 [196]
rpb2
A. microperforatus Novel species Lymph node and toenail ITS, benA, cmdA 2017 [151]
and rpb2
A. pallidofulvus ≡ Aspergillus Invasive pulmonary aspergillosis and ITS, benA, cmdA 2014 [122,197]
sulphureus var. disseminated aspergillosis
minimus
A. parafelis Novel species Invasive aspergillosis; oropharyngeal Cats benA, cmdA, 2014 [198,199]
exudate and sputum rpb2, mcm7 and
tsr1
A. pragensis Aspergillus section Onychomycosis ITS, benA and 2014 [200]
Candidi cmdA
A. pseudofelis Novel species Invasive aspergillosis; sputum and nail benA, cmdA, 2014 [198]
rpb2, mcm7 and
tsr1
A. pseudogracilis Novel species Child carrier ITS, benA, cmdA 2017 [171]
and rpb2
A. Novel species BAL, lung and sputum ITS, benA, cmdA 2017 [149]
pseudosclerotiorum and rpb2
A. Novel species Invasive aspergillosis; mediastinal benA, cmdA, 2014 [198]
pseudoviridinutans lymph node rpb2, mcm7 and
tsr1
A. reticulatus Novel species Lung biopsy, child carrier ITS, benA, cmdA 2017 [171]
and rpb2
A. sclerotialis ≡ Sagenomella Dog rpb2 2014 [2,176,201]
sclerotialis
= Phialosimplex
sclerotialis
A. spinulosporus ≡ Aspergillus nidulans Recurrent prosthetic valve endocarditis ITS, benA, cmdA 2016 [2,202–208]
Table 2 (continued)
Species Synonym(s) Associated human infections or clinical Associated non-human vertebrates Molecular Year of Reference(s)
specimensa markersb valid
publication
var. echinulatus and invasive pulmonary aspergillosis and rpb2

= Emericella = Aspergillus
echinulate delacroixii (Samson,
Visagie &
Houbraken)
= Emericella
nidulans var.
echinulata
A. stercorarius Novel species Lizard (Uromastix acanthinurus) ITS, benA, cmdA 2016 [86]
dung and rpb2
A. wyomingensis Novel species Cat benA and cmdA 2014 [134,209]
Penicillium
P. canis Novel species Bone lesion of spayed Rhodesian ITS, benA and 2014 [210]
ridgeback dog with osteomyelitis cmdA
P. fimorum Novel species Mouse dung ITS, benA, cmdA 2016 [173]
and rpb2
P. paradoxum ≡ Aspergillus Dung of dog and opossum ITS, benA, cmdA 2014 [1,202,211,212]
paradoxus and rpb2
= Aspergillus
ingratus
= Hemicarpenteles
paradoxus
P. robsamsonii Novel species Mouse dung ITS, benA, cmdA 2016 [173]
and rpb2
Talaromyces
T. alveolaris Novel species BAL ITS, benA, cmdA 2017 [150]
and rpb2
T. atroroseus Novel species Mouse dung ITS, benA and 2013 [213]
rpb1
T. columbinus Novel species Fungaemia and pulmonary nodule and ITS, benA, cmdA, 2013 [214–216]
adjacent rib osteomyelitis rpb1, rpb2,
mcm7 and tsr1
T. georgiensis Novel species Animal joint fluid ITS, benA and 2017 [150]
rpb2
T. kabodanensis Novel species BAL ITS, benA, cmdA 2016 [150,217]
and rpb2
T. minnesotensis Novel species Ear ITS, benA, cmdA 2017 [150]
and rpb2
T. rapidus Novel species BAL ITS, benA, cmdA 2017 [150]
and rpb2
T. siglerae Novel species Tinea capitis ITS, benA, cmdA 2017 [218]
and rpb2
a
BAL, bronchoalveolar lavage
b
benA, β-tubulin gene; cct8, chaperonin-containing T-complex protein 1 subunit theta gene; cmdA, calmodulin gene; ITS, internal transcribed spacer; mcm7, mini-chromosome
maintenance complex component 7 gene; nrDNA, nuclear ribosomal rRNA gene; rpb1, RNA polymerase II largest subunit gene; rpb2, RNA polymerase II second largest subunit gene; tsr1,
ribosome maturation factor for 20S rRNA accumulation gene
ribosomal proteins, microorganisms can be successfully identified even well as A. sydowii (formerly section Versicolores) as A. versicolor
though varying culture media and incubation conditions are used [92,122]. A probable reason for this is that the mass spectra for many
[104,105]. More importantly, databases consisting of protein mass spec- of these rare species are lacking in the commercial libraries. It should
tra from over 2,400 microbial species are commercially available be noted that the Bruker MBT MSP 6903 Library, Bruker MBT Filamen-
[106,107], making the identification of a wide range of microorganisms tous Fungi Library and Vitek MS V3.0 Knowledge Base only include ref-
possible. Given its numerous advantages, MALDI–TOF MS has been erence mass spectra for 42, 127 and 82 filamentous fungal species,
gaining popularity for identification of pathogenic microorganisms, in- respectively [106,117,123]. Of these, only up to 22 Aspergillus, 21 Penicil-
cluding bacteria [108,109], yeasts [108–115] and even filamentous lium and 6 Talaromyces, which are still named with their previous Peni-
fungi [109,116–118], in clinical microbiology laboratories. The potential cillium synonyms, species are included [107,123]. However, the
of this technology in diagnosing Aspergillus, Penicillium and Talaromyces numbers of accepted Aspergillus, Penicillium and Talaromyces species
species has also been evaluated by numerous studies. In general, greatly outnumber those included in the MALDI–TOF MS databases,
MALDI–TOF MS is successful in identifying the more commonly found with both Aspergillus and Penicillium having approximately 350 species
aspergilli/penicillia, such as A. flavus, A. fumigatus, A. nidulans, A. niger, [1,2,60] and Talaromyces having more than 100 species [63,89]. Despite
A. sydowii, A. unguis, P. chrysogenum, P. aurantiogriseum and this, MALDI–TOF MS has still been demonstrated as a potential tool to
P. purpurogenum, with correct identification rates of ≥78% [117–121]. differentiate members of the three genera by hierarchical cluster analy-
Yet, for other rare species misidentification is often encountered. Nota- sis of the mass spectra of various species [91,124,125]. As a result, theo-
bly, these uncommon species could usually be identified to the sectional retically if more reference mass spectra for different species, especially
level. For example, A. tritici (section Candidi) was misidentified as the rare ones, are generated for inclusion in the databases the species di-
A. candidus; A. oryzae (section Flavi) as A. flavus; A. fischeri (section agnosis power of MALDI–TOF MS would be greatly enhanced and it has
Fumigati) as A. fumigatus; A. tubingensis and A. welwitschiae (section already been exemplified by previous studies that the correct identifica-
Nigri) as A. niger, A. hortai and A. niveus (section Terrei) as A. terreus; as tion rates could be improved by the expansion of reference libraries
using inhouse generated mass spectra [118,122,125]. To overcome the Nucleotide Sequence Database Collaboration (INSDC) [135] contains a
limitation of small reference data volume of the commercial databases, vast number of sequences, the reliability of the sequence annotation is
several organisations have self-established online supplementary data- questionable [136,137]. Notably, ≥10% of the fungal ITS sequences in
bases. For example, the Spectra database (freely available at https:// these databases were found to be misannotated [136]. As such, the Fun-
spectra.folkhalsomyndigheten.se/spectra/) by the Public Health Agency gal ITS RefSeq Targeted Loci Project has been initiated by the National
of Sweden (Folkhälsomyndigheten) is a platform for MALDI–TOF MS Center for Biotechnology Information (NCBI) to improve the quality
users to deposit and exchange user-generated mass spectra which are and accuracy of the sequences deposited to INSDC [138,139]. Similarly,
curated and continuously updated. Another such complementary data- the UNITE database was developed to include high-quality type or rep-
base is the MSI Platforme which serves as a webtool for MALDI–TOF MS- resentative sequences for fungi or fungal species hypothesis with cor-
based fungal identification. This platform contains more than 11,800 rect or up-to-date taxonomic annotations [140]. The International
reference mass spectra of more than 900 fungal species, aiming at Society for Human and Animal Mycology (ISHAM) ITS database,
supplementing the insufficient spectral diversity of the commercial da- specialised in the ITS-based identification of medical fungi, has also
tabases so as to improve species identification [126]. been recently established [141] and it contains quite a number of
With the current adoption of consolidated species recognition high-quality ITS sequences for Aspergillus, Penicillium and Talaromyces
where molecular characters play a predominant role, DNA sequencing species, which are commonly encountered in the clinical settings.
and phylogenetic analysis have become the gold standard for accurate While curated databases for benA, cmdA and rpb2 have not been created,
fungal identification. As in other fungi, early molecular work on Asper- reliable sequences for all the ex-type strains of Aspergillus, Penicillium
gillus, Penicillium and Talaromyces involved the comparison of large and Talaromyces accepted species have been listed in the recent mono-
and small subunit ribosomal nucleic acid (mitochondrial and/or nu- graphs on the three genera [1,2,63] or online at http://www.
clear) as well as internal transcribed spacer (ITS) sequences aspergilluspenicillium.org/. In addition to nuclear genes, attempts
[43–45,127]. However, subsequent analysis showed that ribosomal have also been made to understand the evolution (and thus species rec-
genes are too conserved to separate these groups of fungi [128,129]. In ognition) of Aspergillus, Penicillium and Talaromyces by sequencing of
addition, although ITS is now accepted as the official DNA barcode for mitogenomes [142–145]. Yet, only a handful of mitogenomes are avail-
fungi [130], it has also been recognised as an extremely conserved re- able for these groups of fungi currently and the utility of mitogenomes
gion for Aspergillus, Penicillium and Talaromyces [1,2,63]. Despite the for species diagnosis awaits further examination.
fact that its sequence variability could be used to distinguish species be-
longing to different sections or series [128], very often it is not useful for 4. Clinical perspectives
the differentiation of species within the same section or series. In view
of this and also to better reflect the genealogy of this group of organ- A stable taxonomy is important to the study of Aspergillus, Penicil-
isms, sequencing of multiple genetic markers, in particular the β- lium and Talaromyces in every aspect including medical mycology.
tubulin (benA) and calmodulin (cmdA or CaM) genes, to define species First of all, the nomenclature of pathogenic fungi should be steady
boundaries has been advocated [131]. The exons of these genes are over time, without frequent vigorous name changes. The recently im-
highly conserved and are therefore good locations for primer binding, plemented 1F1N scheme, where one fungus shall only possess one
whereas introns in between the exons act as the major source of se- name, drastically simplified fungal nomenclature. The accepted use of
quence variation. As a result, sequences of these genes containing Aspergillus and Penicillium names over their respective ‘sexual names’
both exons and introns are able to provide variations at different levels is particularly important to the medical community. This is because
for species delimitation [131]. With the majority of Aspergillus, Penicil- most clinical fungi are isolated in the asexual forms and these fungi
lium and Talaromyces species clearly defined nowadays, sequencing of are traditionally named with their asexual names. Use of the ‘sexual
benA and/or cmdA can be utilised to identify most of these species. In names’ would confuse clinicians since they would not be aware of
fact, benA and cmdA have been proposed as the secondary identification what Eupenicillium, Neosartorya and Emericella are, thus hindering treat-
markers for Penicillium and Aspergillus species, respectively [1,2]. This is ment and patient care. This could be exemplified by the recent transfer
because there are universal primers available for these two genes and of P. marneffei to T. marneffei, where the well-known disease name
both of them are easy to amplify. In the case of Aspergillus, although ‘penicilliosis’ also has to be changed to the unfamiliar ‘talaromycosis’.
benA could be easily amplified, the presence of paralogous genes (e.g. A stable taxonomy also clearly defines species and their identification
tubC) in some species which could also be amplified by the universal methods. Therefore, the clinical spectrum of pathogenic species could
primers could be confusing and complicate species identification also be better studied. In particular, rare and new aetiological agents
[132,133]. In contrast, although a similar problem has also been noted could be revealed (Table 2) [92,146–151]. Accurate identification of
for cmdA, amplification of a pseudogene only occurred for one Aspergil- the causative pathogen is crucial to epidemiological studies. Correct
lus strain [134]. Moreover, cmdA is also easy to amplify and its sequence species diagnosis could also help predict antifungal susceptibility,
is available for nearly all accepted species. Therefore, cmdA was chosen which varies across different species and this could significantly affect
over benA as secondary identification marker for Aspergillus [2]. On the patient treatment, disease management and prognosis. For example, it
other hand, as for Penicillium, amplification of benA paralogues has not has been shown that A. tubingensis and A. unguis possessed elevated
been reported and since a complete cmdA sequence database is lacking, minimum inhibitory concentrations (MICs) to itraconazole [92]. The
benA became the secondary identification marker of choice [1]. Al- fact that triazole agents exhibit various activities against different
though a third option, RNA polymerase II second-largest subunit gene Aspergillus species has also been demonstrated by other studies
(rpb2), also exists and its lack of introns allows robust and easy align- [148,149,151]. Also, although triazoles showed moderate activities
ment for phylogenetic analysis, it was not selected over benA or cmdA against Penicillium species, their effectiveness against some Talaromyces
because rpb2 is sometimes difficult to amplify and a database with suf- species are poor [147].
ficient volume is lacking [1,2]. Nonetheless, when resources are avail-
able it is recommended to sequence all the four genetic markers (ITS, 5. Summary and outlook
benA, cmdA and rpb2) to aid identification, especially when new species
are diagnosed [1,2]. Although a recommendation of identification With a consistent taxonomy, understanding on the epidemiology
markers has not been put forward for Talaromyces species, they gener- and clinical spectrum of diseases caused by Aspergillus, Penicillium and
ally follow those for Aspergillus and Penicillium species [63]. In order to Talaromyces could be enhanced. This in turn facilitates laboratory diag-
achieve accurate identification, sequences from reliable databases nosis of these important mycotic pathogens and establishment of pa-
should be compared against. Despite the fact that the International tient treatment strategies. The transition from morphological/
phenotypic to chemotaxonomic, genetic/phylogenetic, or consolidated References

species recognition results in the reclassification of these groups of
fungi and enables sexual-asexual connection. In the current omics era, [1] Visagie CM, Houbraken J, Frisvad JC, Hong SB, Klaassen CHW, Perrone G, et al. Iden-
tification and nomenclature of the genus Penicillium. Stud Mycol 2014;78(Supple-
advancement in different omics technologies makes characterisation ment C):343–71.
of the complete set of a particular group of characters possible, allowing [2] Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CHW, et al. Phy-
more thorough analyses and therefore, a more stable taxonomy. For ex- logeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 2014;
78:141–73.
ample, comparison of mitogenomes supported the transfer of [3] Houbraken J, Samson R. Phylogeny of Penicillium and the segregation of
‘P. marneffei’ to Talaromyces and demonstrated that Aspergillus and Pen- Trichocomaceae into three families. Stud Mycol 2011;70(:1):1–51.
icillium are more closely related to each other than to Talaromyces [4] Houbraken J, de Vries RP, Samson RA. Modern taxonomy of biotechnologically im-
portant Aspergillus and Penicillium species. In: Sariaslani S, Gadd GM, editors. Adv
[142,144,145]. The availability of contemporary advanced techniques, Appl Microbiol.San Diego: Academic Press; 2014. p. 199–249.
such as MALDI–TOF MS as well as UHPLC/HPLC–DAD–MS, significantly [5] Chávez R, Bull P, Eyzaguirre J. The xylanolytic enzyme system from the genus Pen-
improves proteomic and metabolic fingerprinting of fungi, respectively, icillium. J Biotechnol 2006;123(4):413–33.
[6] Ichishima E. Development of enzyme technology for Aspergillus oryzae, A. sojae, and
thus aiding chemotaxonomy. As the cost for second-generation se- A. luchuensis, the national microorganisms of Japan. Biosci Biotechnol Biochem
quencing is getting lower and the emerging third-generation sequenc- 2016;80(9):1681–92.
ing is becoming more widely accessible, more and more complete/ [7] Frisvad JC, Smedsgaard J, Larsen TO, Samson RA. Mycotoxins, drugs and other
extrolites produced by species in Penicillium subgenus Penicillium. Stud Mycol
almost complete fungal genomes become available. These genome se-
2004;49:201–41.
quences could advance our knowledge on these fungi, such as [8] Pitt JI, Hocking AD. Fungi and Food Spoilage. Boston: Springer; 2009.
T. marneffei [144,152–158], and taxonomy on them could thus be facil- [9] Kwon-Chung KJ, Sugui JA. Aspergillus fumigatus—What makes the species a ubiqui-
itated. With such additional novel data, further reclassification on Asper- tous human fungal pathogen? PLoS Pathog 2013;9(12):e1003743.
[10] Latgé J-P. Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 1999;12(2):
gillus, Penicillium and Talaromyces is expected. Application of all these 310–50.
state-of-the-art omics technologies is likely to provide comprehensive [11] Vanittanakom N, Cooper CR, Fisher MC, Sirisanthana T. Penicillium marneffei infec-
information on the evolution of the three related genera, and a more tion and recent advances in the epidemiology and molecular biology aspects. Clin
Microbiol Rev 2006;19(1):95–110.
stable taxonomy for them will hopefully be achieved. Yet, it should be [12] Chan JFW, Lau SKP, Yuen K-Y, Woo PCY. Talaromyces (Penicillium) marneffei infec-
noted that even though these advanced methodologies are becoming tion in non-HIV-infected patients. Emerg Microbes Infect 2016;5:e19.
more readily available for the identification and classification of fungi, [13] Quaedvlieg W, Binder M, Groenewald JZ, Summerell BA, Carnegie AJ, Burgess TI,
et al. Introducing the consolidated species concept to resolve species in the
it is equally important for mycologists to apply standard or best prac- Teratosphaeriaceae. Persoonia 2014;33:1–40.
tices when studying fungal taxonomic relationships. In particular, fun- [14] Micheli PA. Nova Plantarum Genera. Florence: Typis Bernardi Paperinii; 1729.
gal taxonomists should always keep themselves up-to-date with [15] von Haller A. Historia Stirpium Indigenarum Helvetiae Inchoata. Tomus Secundus.
Bernae: Sumptibus Societatis; 1768.
recent trends, tools, standards, recommendations and practices in the
[16] Fries EM. Systema Mycologicum: Sistens Fungorum Ordines, Genera Et Species,
field, especially when describing new species [159–163]. When depos- Huc Usque Cognitas, Quas Ad Normam Methodi Naturalis Determinavit. Lundae:
iting DNA sequence data to public databases, the sequences should be Ex Officina Berlingiana; 1832.
[17] Link HF. Observationes in ordines plantarum naturales. Ges Naturf Freunde Berlin
well checked for authenticity as well as reliability [164], and they should
Mag Neuesten Entdeck Gesammten Naturk 1809;3(1):3–42.
be richly annotated as far as possible [165]. Also, multiple genetic [18] de Bary A. Ueber die entwickelung und den zusammenhang von Aspergillus glaucus
markers and proper analytical tools should be used for the inference und Eurotium. Bot Zeitung (Berlin) 1854;12(25–27):425–34 441–451, 465–471.
of phylogenetic relationships [166]. As nowadays taxonomy has entered [19] Ludwig F. Lehrbuch der Niederen Kryptogamen. Stuttgart: von Ferdinand Enke;
1892.
a deep crisis where descriptive taxonomic studies are not encouraged, it [20] Thom C. The Penicillia. London: Baillière, Tindall and Cox; 1930.
is important for taxonomists to keep the pace for re-growth, to partici- [21] Thom C, Raper KB. A Manual of the Aspergilli. Baltimore: Williams & Wilkins; 1945.
pate actively and to form a good ‘taxonomic culture’ so that the scientific [22] Raper KB, Thom C, Fennel DI. A Manual of the Penicillia. Baltimore: Williams & Wil-
kins; 1949.
community would value taxonomic work higher [167]. This could also [23] Thom C. The evolution of species concepts in Aspergillus and Penicillium. Ann N Y
help attract more research funding for more expensive technology or Acad Sci 1954;60(1):24–34.
equipment for more detailed taxonomic characterisation. All these ef- [24] Raper KB, Fennell DI. The Genus Aspergillus. Baltimore: Williams & Wilkins; 1965.
[25] Raper KB. Nomenclature in Aspergillus and Penicillium. Mycologia 1957;49(5):
forts could help speed up taxonomic and molecular ecology progress 644–62.
on Aspergillus, Penicillium and Talaromyces significantly. [26] Lanjouw J, Baehni C, Merrill ED, Rickett HW, Robyns W, Sprague TA, et al. Interna-
tional Code of Botanical Nomenclature, Adopted by the Seventh International Bo-
tanical Congress, Stockholm. Waltham: Chronica Botanica; July 1950; 1952.
Acknowledgement
[27] Benjamin CR. Ascocarps of Aspergillus and Penicillium. Mycologia 1955;47(5):
669–87.
This work is supported by the Health and Medical Research Fund [28] Stolk AC, de Scott B. Studies on the genus Eupenicillium Ludwig I. Taxonomy and
nomenclature of Penicillia in relation to their sclerotioid ascocarpic states.
(No. HKM-15-M07 [commissioned project]), Food and Health Bureau,
Persoonia 1967;4(4):391–405.
Government of the Hong Kong Special Administrative Region, Hong [29] Dierckx RP. Un Essai de revision du genre Penicillium Link. Ann Soc Sci Bruxelles
Kong. We are grateful to the Agricultural Research Service (ARS) Culture 1901;25:83–9.
Collection (NRRL), Department of Agriculture, USA for providing the ref- [30] Thom C, Church M. The Aspergilli. Baltimore: Williams & Wilkins; 1926.
[31] Blochwitz A. Die Aspergillaceen. System und Phylogenie. Ann Mycol 1929;27:
erence strains A. glaucus NRRL 116T, A. nidulans NRRL 187T, P. kewense 185–204.
NRRL 3332T, P. expansum NRRL 976T and T. flavus NRRL 2098T for free. [32] Stolk AC, Samson RA. The genus Talaromyces. Studies on Talaromyces and related
We also thank Mr Jordan Y. H. Fong, Department of Microbiology, The genera II. Stud Mycol 1972;2:1–65.
[33] Gams W, Christensen M, Onions AH, Pitt JI, Samson RA. Infrageneric taxa of Asper-
University of Hong Kong, for his assistance in taking macroscopic photos gillus. In: Samson RA, Pitt JI, editors. Advances in Penicillium and Aspergillus System-
for these reference fungal strains. atics. Boston: Springer; 1986. p. 55–62.
[34] Biourge P. Les moisissures du groupe Penicillium Link. Cellule 1923;33:7–331.
[35] Pitt JI. The Genus Penicillium and Its Teleomorphic States Eupenicillium and
Conflict of interest Talaromyces. London: Academic Press; 1979.
[36] Stolk AC, Samson RA. A new taxonomic scheme for Penicillium anamorphs. In:
Patrick C.Y. Woo has provided scientific advisory/laboratory services Samson RA, Pitt JI, editors. Advances in Penicillium and Aspergillus Systematics. Bos-
ton: Springer; 1986. p. 163–92.
for Gilead Sciences, Incorporated; International Health Management As- [37] Frisvad JC. Taxonomy, chemodiversity, and chemoconsistency of Aspergillus, Peni-
sociates, Incorporated; Merck & Corporation, Incorporated and Pfizer, cillium, and Talaromyces species. Front Microbiol 2015;5:773.
Incorporated. The other authors report no conflicts of interest. The [38] Hawksworth DL, Crous PW, Redhead SA, Reynolds DR, Samson RA, Seifert KA, et al.
The Amsterdam declaration on fungal nomenclature. IMA Fungus 2011;2(1):
funding sources had no role in study design, data collection, analysis, in-
105–12.
terpretation or writing of the report. The authors alone are responsible [39] Norvell LL. Fungal nomenclature. 1. Melbourne approves a new code. Mycotaxon
for the content and the writing of the manuscript. 2011;116(1):481–90.
[40] Flann C, Turland N, Turland NJ, Monro M. A. Report on botanical nomenclature— [73] Balali GR, Minaiefar AA, Sharifnabi B. Pectic zymogram variation and morphological
Melbourne 2011. XVIII International Botanical Congress, Melbourne: nomenclature identification of Aspergillus species. Rostaniha 2010;11(2):163–74.
section, 18–22 July 2011. PhytoKeys 2014;41:1–289. [74] Frisvad JC, Larsen TO, de Vries R, Meijer M, Houbraken J, Cabañes FJ, et al. Secondary
[41] Samson RA, Yilmaz N, Houbraken J, Spierenburg H, Seifert KA, Peterson SW, et al. metabolite profiling, growth profiles and other tools for species recognition and
Phylogeny and nomenclature of the genus Talaromyces and taxa accommodated important Aspergillus mycotoxins. Stud Mycol 2007;59:31–7.
in Penicillium subgenus Biverticillium. Stud Mycol 2011;70(1):159–83. [75] Ciegler A, Fennell DI, Sansing GA, Detroy RW, Bennett GA. Mycotoxin-producing
[42] Frisvad JC, Filtenborg O, Samson RA, Stolk AC. Chemotaxonomy of the genus strains of Penicillium viridicatum: classification into subgroups. Appl Microbiol
Talaromyces. Antonie Van Leeuwenhoek 1990;57(3):179–89. 1973;26(3):271–8.
[43] LoBuglio KF, Taylor JW. Molecular phylogeny of Talaromyces and Penicillium species [76] Ciegler A, Lee LS, Dunn JJ. Production of naphthoquinone mycotoxins and taxon-
in subgenus Biverticillium. The Fungal Holomorph: Mitotic, Meiotic And Pleomor- omy of Penicillium viridicatum. Appl Environ Microbiol 1981;42(3):446–9.
phic Speciation In Fungal Systematics. Wallingford: CAB International; 1993. [77] Filtenborg O, Frisvad JC. A simple screening method for toxigenic moulds in pure
p. 115–28. cultures. Lebenson Wiss Technol 1980;13(3):128–30.
[44] LoBuglio KF, Pitt JI, Taylor JW. Phylogenetic analysis of two ribosomal DNA regions [78] Filtenborg O, Frisvad JC, Svendsen JA. Simple screening method for molds produc-
indicates multiple independent losses of a sexual Talaromyces state among asexual ing intracellular mycotoxins in pure cultures. Appl Environ Microbiol 1983;45(2):
Penicillium species in subgenus Biverticillium. Mycologia 1993;85(4):592–604. 581–5.
[45] Berbee ML, Yoshimura A, Sugiyama J, Taylor JW. Is Penicillium monophyletic? An [79] Frisvad JC, Filtenborg O. Terverticillate penicillia: chemotaxonomy and mycotoxin
evaluation of phylogeny in the family Trichocomaceae from 18S, 5.8S and ITS ribo- production. Mycologia 1989;81(6):837–61.
somal DNA sequence data. Mycologia 1995;87(2):210–22. [80] Frisvad JC. Profiles of primary and secondary metabolites of value in classification
[46] Visagie CM, Llimona X, Vila J, Louis-Seize G, Seifert KA. Phylogenetic relationships of Penicillium viridicatum and related species. In: Samson RA, Pitt JI, editors. Ad-
and the newly discovered sexual state of Talaromyces flavovirens, comb. nov. vances in Penicillium and Aspergillus systematics. Boston: Springer; 1986.
Mycotaxon 2013;122(1):399–411. p. 311–25.
[47] Montagne J. Cinquième centurie. De plantes cellulaires exotiques nouvelles. Ann [81] Frisvad JC. The connection between the Penicillia and Aspergilli and mycotoxins
Sci Nat Bot 1845;4:346–67. with special emphasis on misidentified isolates. Arch Environ Contam Toxicol
[48] McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, et al. Inter- 1989;18(3):452–67.
national Code of Nomenclature for algae, fungi, and plants (Melbourne Code), [82] Frisvad JC. Secondary metabolites as an aid to Emericella classification. In: Samson
Adopted by the Eighteenth International Botanical Congress Melbourne, RA, Pitt JI, editors. Advances in Penicillium and Aspergillus systematics. Boston:
Australia, July 2011. Königstein: Koeltz Scientific Books; 2012. Springer; 1986. p. 437–44.
[49] Seifert KA, Frisvad JC, Houbraken J, Llimona X, Peterson SW, Samson RA, et al. Pro- [83] Frisvad JC, Samson RA. Chemotaxonomy and morphology of Aspergillus fumigatus
posal to conserve the name Talaromyces over Lasioderma (Ascomycota). Taxon and related taxa. In: Samson RA, Pitt JI, editors. Modern concepts in Penicillium
2012;61(2):461–2. and Aspergillus classification. Boston: Springer; 1990. p. 201–8.
[50] May TW. Report of the nomenclature committee for fungi: 20. Taxon 2017;66(2): [84] Samson RA, Noonim P, Meijer M, Houbraken J, Frisvad J, Varga J. Diagnostic tools to
483–95. identify black aspergilli. Stud Mycol 2007;59:129–45.
[51] Wilson KL. Report of the general committee: 18. Taxon 2017;66(3):742–4. [85] Samson RA, Peterson SW, Frisvad JC, Varga J. New species in Aspergillus section
[52] Malloch D, Cain RF. The Trichocomataceae: ascomycetes with Aspergillus, Terrei. Stud Mycol 2011;69:39–55.
Paecilomyces, and Penicillium imperfect states. Can J Bot 1972;50(12):2613–28. [86] Chen AJ, Frisvad JC, Sun BD, Varga J, Kocsubé S, Dijksterhuis J, et al. Aspergillus sec-
[53] Subramanian CV. The perfect states of Aspergillus. Curr Sci 1972;41(21):755–61. tion Nidulantes (formerly Emericella): polyphasic taxonomy, chemistry and biology.
[54] Varga J, Due M, Frisvad JC, Samson RA. Taxonomic revision of Aspergillus section Stud Mycol 2016;84(Supplement C):1–118.
Clavati based on molecular, morphological and physiological data. Stud Mycol [87] Frisvad JC, Larsen TO. Chemodiversity in the genus Aspergillus. Appl Microbiol
2007;59:89–106. Biotechnol 2015;99(19):7859–77.
[55] Wiley BJ, Simmons EG. New species and a new genus of plectomycetes with Asper- [88] Frisvad JC, Andersen B, Thrane U. The use of secondary metabolite profiling in che-
gillus states. Mycologia 1973;65(4):934–8. motaxonomy of filamentous fungi. Mycol Res 2008;112(2):231–40.
[56] Udagawa S-i, Uchiyama S. Neocarpenteles: a new ascomycete genus to accommo- [89] Chen AJ, Sun BD, Houbraken J, Frisvad JC, Yilmaz N, Zhou YG, et al. New Talaromyces
date Hemicarpenteles acanthosporus. Mycoscience 2002;43(1):3–6. species from indoor environments in China. Stud Mycol 2016;84:119–44.
[57] Frisvad JC, Samson RA. Neopetromyces gen. nov and an overview of teleomorphs of [90] Vadlapudi V, Borah N, Yellusani KR, Gade S, Reddy P, Rajamanikyam M, et al. Asper-
Aspergillus subgenus Circumdati. Stud Mycol 2000;45:201–7. gillus Secondary Metabolite Database, a resource to understand the secondary me-
[58] Pitt JI, Taylor JW. Aspergillus, its sexual states and the new International Code of No- tabolome of Aspergillus genus. Sci Rep 2017;7(1):7325.
menclature. Mycologia 2014;106(5):1051–62. [91] Tam EWT, Chen JHK, Lau ECL, Ngan AHY, Fung KSC, Lee K-C, et al. Misidentification
[59] Taylor JW, Göker M, Pitt JI. Choosing one name for pleomorphic fungi: The example of Aspergillus nomius and Aspergillus tamarii as Aspergillus flavus: characterization
of Aspergillus versus Eurotium, Neosartorya and Emericella. Taxon 2016;65(3): by internal transcribed spacer, β-tubulin, and calmodulin gene sequencing, meta-
593–601. bolic fingerprinting, and matrix-assisted laser desorption ionization–time of flight
[60] Kocsubé S, Perrone G, Magistà D, Houbraken J, Varga J, Szigeti G, et al. Aspergillus is mass spectrometry. J Clin Microbiol 2014;52(4):1153–60.
monophyletic: evidence from multiple gene phylogenies and extrolites profiles. [92] Tsang C-C, Hui TWS, Lee K-C, Chen JHK, Ngan AHY, Tam EWT, et al. Genetic diver-
Stud Mycol 2016;85(Supplement C):199–213. sity of Aspergillus species isolated from onychomycosis and Aspergillus
[61] Pitt JI, Taylor JW. Proposal to conserve the name Aspergillus (Fungi: Eurotiales: hongkongensis sp. nov., with implications to antifungal susceptibility testing.
Trichocomaceae) with a conserved type to maintain also the name Eurotium. Diagn Microbiol Infect Dis 2016;84(2):125–34.
Taxon 2016;65(3):631–2. [93] Vasyurenko ZP, Frolov AF. Fatty acid composition of bacteria as a chemotaxonomic
[62] Samson RA, Hubka V, Varga J, Houbraken J, Hong S-B, Klaassen CHW, et al. Re- criterion. J Hyg Epidemiol Microbiol Immunol 1986;30(3):287–93.
sponse to Pitt & Taylor 2016: conservation of Aspergillus with A. niger as the con- [94] Welch DF. Applications of cellular fatty acid analysis. Clin Microbiol Rev 1991;4(4):
served type is unnecessary and potentially disruptive. Taxon 2017;66(6):1439–46. 422–38.
[63] Yilmaz N, Visagie CM, Houbraken J, Frisvad JC, Samson RA. Polyphasic taxonomy of [95] Kunitsky C, Osterhout G, Sasser M. Identification of microorganisms using fatty acid
the genus Talaromyces. Stud Mycol 2014;78:175–341. methyl ester (FAME) analysis and the MIDI Sherlock® microbial identification sys-
[64] Hennebert GL. Dierckx’ contribution to the genus Penicillium. In: Samson RA, Pitt JI, tem. In: Miller MJ, editor. Encyclopedia of Rapid Microbiological Methods. River
editors. Advances in Penicillium and Aspergillus systematics. Boston: Springer; Grove: Davis Healthcare International Publishing; 2006. p. 1–17.
1986. p. 9–21. [96] Zain ME, Bahkali AH, Al-Othman MR. Developments in using fatty acids in fungal
[65] Okuda T. Variation in colony characteristics of Penicillium strains resulting from chemotaxonomy. Afr J Microbiol Res 2013;7(38):4638–45.
minor variations in culture conditions. Mycologia 1994;86(2):259–62. [97] Lechevalier H, Lechevalier MP. Chemotaxonomic use of lipids—an overview. In:
[66] Okuda T, Klich MA, Seifert KA, Ando K. Media and incubation effects on morpholog- Ratledge C, Wilkinson SG, editors. Microbial Lipids. London: Academic Press;
ical characteristics of Penicillium and Aspergillus. In: Samson RA, Pitt JI, editors. Inte- 1988. p. 869–902.
gration of modern taxonomic methods for Penicillium and Aspergillus Classification. [98] Stahl PD, Klug MJ. Characterization and differentiation of filamentous fungi based
Amsterdam: Harwood Academic Publishers; 2000. p. 83–100. on fatty acid composition. Appl Environ Microbiol 1996;62(11):4136–46.
[67] Pitt JI. Chemotaxonomy of Penicillium and related teleomorphs. Jpn J Med Mycol [99] Blomquist G, Andersson B, Andersson K, Brondz I. Analysis of fatty acids. A new
1991;32(Supplement 2):31–8. method for characterization of moulds. J Microbiol Methods 1992;16(1):59–68.
[68] Cruickshank RH, Pitt JI. The zymogram technique: isoenzyme patterns as an aid in [100] da Silva TL, de Sousa E, Pereira PT, Ferrão AM, Roseiro JC. Cellular fatty acid profiles
Penicillium classification. Microbiol Sci 1987;4(1):14–7. for the differentiation of Penicillium species. FEMS Microbiol Lett 1998;164(2):
[69] Cruickshank RH, Pitt JI. Identification of species in Penicillium subgenus Penicillium 303–10.
by enzyme electrophoresis. Mycologia 1987;79(4):614–20. [101] Mahmoud MA, Abd-El-Aziz ARM, Al-Othman MR. Molecular and biochemical tax-
[70] Paterson RRM, Bridge PD, Crosswaite MJ, Hawksworth DL. A reappraisal of the onomic tools for the identification and classification of plant-pathogenic Penicillium
terverticillate penicillia using biochemical, physiological and morphological fea- species. Biotechnol Biotechnol Equip 2016;30(6):1090–6.
tures III. An evaluation of pectinase and amylase isoenzymes for species character- [102] Nemec T, Jernejc K, Cimerman A. Sterols and fatty acids of different Aspergillus spe-
ization. Microbiology 1989;135(11):2979–91. cies. FEMS Microbiol Lett 1997;149(2):201–5.
[71] Cruickshank RH, Pitt JI. Isoenzyme patterns in Aspergillus flavus and closely related [103] Fraga ME, Santana DM, Gatti MJ, Direito GM, Cavaglieri LR, Rosa CA. Characteriza-
species. In: Samson RA, Pitt JI, editors. Modern concepts in Penicillium and Aspergil- tion of Aspergillus species based on fatty acid profiles. Mem Inst Oswaldo Cruz
lus classification. Boston: Springer; 1990. p. 259–65. 2008;103(6):540–4.
[72] Varga J, Yu E, Kiss I, Botos B, Kozakiewicz Z. Carbon source utilization and isoen- [104] Singhal N, Kumar M, Kanaujia PK, Virdi JS. MALDI-TOF mass spectrometry: an
zyme analysis as taxonomic aids for toxigenic Neosartorya species and their rela- emerging technology for microbial identification and diagnosis. Front Microbiol
tives. Acta Microbiol Immunol Hung 1997;44(1):1–11. 2015;6:791.
[105] Valentine N, Wunschel S, Wunschel D, Petersen C, Wahl K. Effect of culture condi- [129] Demİrel R. Comparison of rDNA regions (ITS, LSU, and SSU) of some Aspergillus,
tions on microorganism identification by matrix-assisted laser desorption ioniza- Penicillium, and Talaromyces spp. Turk J Bot 2016;40:576–83.
tion mass spectrometry. Appl Environ Microbiol 2005;71(1):58–64. [130] Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, et al. Nuclear
[106] Bruker Corporation. MBT 6903 MSP Library (#1829023). Release Notes. Bremen: ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode
Bruker Corporation; 2016. marker for Fungi. Proc Natl Acad Sci U S A 2012;109(16):6241–6.
[107] bioMérieux SA. Vitek MS™ V3.0 Knowledge Base. Clinical Use. 161150-556-B. [131] Geiser DM, Harbinski FM, Taylor JW. Molecular and analytical tools for characteriz-
Marcy-l’Etoile: bioMérieux; 2016. ing Aspergillus and Penicillium species at the intra- and interspecific levels. In:
[108] Deak E, Charlton CL, Bobenchik AM, Miller SA, Pollett S, McHardy IH, et al. Compar- Samson RAP, editor. Integration of modern taxonomic methods for Penicillium
ison of the Vitek MS and Bruker Microflex LT MALDI-TOF MS platforms for routine and Aspergillus classification. Amsterdam: Harwood Acadmic Publishers; 2000.
identification of commonly isolated bacteria and yeast in the clinical microbiology p. 381–94.
laboratory. Diagn Microbiol Infect Dis 2015;81(1):27–33. [132] Peterson SW. Phylogenetic analysis of Aspergillus species using DNA sequences
[109] Lévesque S, Dufresne PJ, Soualhine H, Domingo M-C, Bekal S, Lefebvre B, et al. A from four loci. Mycologia 2008;100(2):205–26.
side by side comparison of Bruker Biotyper and VITEK MS: utility of MALDI-TOF [133] Hubka V, Kolarik M. β-tubulin paralogue tubC is frequently misidentified as the
MS technology for microorganism identification in a public health reference labo- benA gene in Aspergillus section Nigri taxonomy: primer specificity testing and tax-
ratory. PLoS One 2015;10(12):e0144878. onomic consequences. Persoonia 2012;29:1–10.
[110] Mancini N, De Carolis E, Infurnari L, Vella A, Clementi N, Vaccaro L, et al. Compara- [134] Nováková A, Hubka V, Dudová Z, Matsuzawa T, Kubátová A, Yaguchi T, et al. New
tive evaluation of the Bruker Biotyper and Vitek MS matrix-assisted laser desorp- species in Aspergillus section Fumigati from reclamation sites in Wyoming (U.S.A.)
tion ionization–time of flight (MALDI-TOF) mass spectrometry systems for and revision of A. viridinutans complex. Fungal Divers 2014;64(1):253–74.
identification of yeasts of medical importance. J Clin Microbiol 2013;51(7):2453–7. [135] Cochrane G, Karsch-Mizrachi I, Takagi T, International Nucleotide Sequence
[111] Pence MA, McElvania TeKippe E, Wallace MA, Burnham C-AD. Comparison and op- Database Collaboration. The International Nucleotide Sequence Database Collabo-
timization of two MALDI-TOF MS platforms for the identification of medically rel- ration. Nucleic Acids Res 2016;44(D1):D48–50.
evant yeast species. Eur J Clin Microbiol Infect Dis 2014;33(10):1703–12. [136] Nilsson RH, Ryberg M, Kristiansson E, Abarenkov K, Larsson K-H, Kõljalg U. Taxo-
[112] Jamal WY, Ahmad S, Khan ZU, Rotimi VO. Comparative evaluation of two matrix- nomic reliability of DNA sequences in public sequence databases: a fungal perspec-
assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI- tive. PLoS One 2006;1(1):e59.
TOF MS) systems for the identification of clinically significant yeasts. Int J Infect [137] Bidartondo MI, Bruns TD, Blackwell M, Edwards I, Taylor AFS, Horton T, et al. Pre-
Dis 2014;26:167–70. serving accuracy in GenBank. Science 2008;319(5870):1616.
[113] Zhao Y, Chan JFW, Tsang C-C, Wang H, Guo D, Pan Y, et al. Clinical characteristics, [138] Schoch CL, Robbertse B, Robert V, Vu D, Cardinali G, Irinyi L, et al. Finding needles in
laboratory identification, and in vitro antifungal susceptibility of Yarrowia haystacks: linking scientific names, reference specimens and molecular data for
(Candida) lipolytica isolates causing fungemia: a multicenter, prospective surveil- Fungi. Database 2014. https://doi.org/10.1093/database/bau061.
lance study. J Clin Microbiol 2015;53(11):3639–45. [139] National Center for Biotechnology Information. Fungal Internal Transcribed Spacer
[114] Wang H, Xiao M, Chen SC-A, Kong F, Sun Z-Y, Liao K, et al. In vitro susceptibilities of RNA (ITS) RefSeq Targeted Loci Project. Undated; Available from: http://www.ncbi.
yeast species to fluconazole and voriconazole as determined by the 2010 National nlm.nih.gov/bioproject/PRJNA177353/.
China Hospital Invasive Fungal Surveillance Net (CHIF-NET) study. J Clin Microbiol [140] Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, et al. To-
2012;50(12):3952–9. wards a unified paradigm for sequence-based identification of fungi. Mol Ecol
[115] Cassagne C, Normand A-C, Bonzon L, L'Ollivier C, Gautier M, Jeddi F, et al. Routine 2013;22(21):5271–7.
identification and mixed species detection in 6,192 clinical yeast isolates. Med [141] Irinyi L, Serena C, Garcia-Hermoso D, Arabatzis M, Desnos-Ollivier M, Vu D, et al. In-
Mycol 2016;54(3):256–65. ternational Society of Human and Animal Mycology (ISHAM)-ITS reference DNA
[116] Karabıçak N, Karatuna O, İlkit M, Akyar I. Evaluation of the Bruker matrix-assisted barcoding database—the quality controlled standard tool for routine identification
laser desorption–ionization time-of-flight mass spectrometry (MALDI-TOF MS) of human and animal pathogenic fungi. Med Mycol 2015;53(4):313–37.
system for the identification of clinically important dermatophyte species. [142] Woo PCY, Zhen H, Cai JJ, Yu J, Lau SKP, Wang J, et al. The mitochondrial genome of
Mycopathologia 2015;180(3):165–71. the thermal dimorphic fungus Penicillium marneffei is more closely related to those
[117] McMullen AR, Wallace MA, Pincus DH, Wilkey K, Burnham C-AD. Evaluation of the of molds than yeasts. FEBS Lett 2003;555(3):469–77.
Vitek MS matrix-assisted laser desorption ionization–time of flight mass spectrom- [143] Joardar V, Abrams NF, Hostetler J, Paukstelis PJ, Pakala S, Pakala SB, et al. Sequenc-
etry system for identification of clinically relevant filamentous fungi. J Clin ing of mitochondrial genomes of nine Aspergillus and Penicillium species identifies
Microbiol 2016;54(8):2068–73. mobile introns and accessory genes as main sources of genome size variability.
[118] Sleiman S, Halliday CL, Chapman B, Brown M, Nitschke J, Lau AF, et al. Performance BMC Genomics 2012;13(1):698.
of matrix-assisted laser desorption ionization−time of flight mass spectrometry [144] Tam EWT, Tsang C-C, Lau SKP, Woo PCY. Comparative mitogenomic and phyloge-
for identification of Aspergillus, Scedosporium, and Fusarium spp. in the Australian netic characterization on the complete mitogenomes of Talaromyces (Penicillium)
clinical setting. J Clin Microbiol 2016;54(8):2182–6. marneffei. Mitochondrial DNA B Resour 2016;1(1):941–2.
[119] Bille E, Dauphin B, Leto J, Bougnoux ME, Beretti JL, Lotz A, et al. MALDI-TOF MS [145] Lau SKP, Tsang C-C, Woo PCY. Talaromyces marneffei genomic, transcriptomic, pro-
Andromas strategy for the routine identification of bacteria, mycobacteria, yeasts, teomic and metabolomic studies reveal mechanisms for environmental adapta-
Aspergillus spp. and positive blood cultures. Clin Microbiol Infect 2012;18(11): tions and virulence. Toxins 2017;9(6):192.
1117–25. [146] Hubka V, Kubatova A, Mallatova N, Sedlacek P, Melichar J, Skorepova M, et al. Rare
[120] Ranque S, Normand A-C, Cassagne C, Murat J-B, Bourgeois N, Dalle F, et al. MALDI- and new etiological agents revealed among 178 clinical Aspergillus strains obtained
TOF mass spectrometry identification of filamentous fungi in the clinical labora- from Czech patients and characterized by molecular sequencing. Med Mycol 2012;
tory. Mycoses 2014;57(3):135–40. 50(6):601–10.
[121] Park JH, Shin JH, Choi MJ, Choi JU, Park Y-J, Jang SJ, et al. Evaluation of matrix- [147] Guevara-Suarez M, Sutton DA, Cano-Lira JF, García D, Martin-Vicente A, Wiederhold
assisted laser desorption/ionization time-of-fight mass spectrometry for identifica- N, et al. Identification and antifungal susceptibility of Penicillium-like fungi from
tion of 345 clinical isolates of Aspergillus species from 11 Korean hospitals: compar- clinical samples in the United States. J Clin Microbiol 2016;54(8):2155–61.
ison with molecular identification. Diagn Microbiol Infect Dis 2017;87(1):28–31. [148] Siqueira JPZ, Sutton DA, García D, Gené J, Thomson P, Wiederhold N, et al. Species
[122] Masih A, Singh PK, Kathuria S, Agarwal K, Meis JF, Chowdhary A. Identification by diversity of Aspergillus section Versicolores in clinical samples and antifungal sus-
molecular methods and matrix-assisted laser desorption ionization–time of flight ceptibility. Fungal Biol 2016;120(11):1458–67.
mass spectrometry and antifungal susceptibility profiles of clinically significant [149] Siqueira JPZ, Sutton DA, Gené J, García D, Wiederhold N, Peterson SW, et al.
rare Aspergillus species in a referral chest hospital in Delhi, India. J Clin Microbiol Multilocus phylogeny and antifungal susceptibility of Aspergillus section Circumdati
2016;54(9):2354–64. from clinical samples and description of A. pseudosclerotiorum sp. nov. J Clin
[123] Bruker Corporation. MALDI Biotyper Filamentous Fungi Library (1838971). Bre- Microbiol 2017;55(3):947–58.
men: Bruker Corporation; 2015. [150] Guevara-Suarez M, Sutton DA, Gené J, García D, Wiederhold N, Guarro J, et al. Four
[124] Hettick JM, Green BJ, Buskirk AD, Kashon ML, Slaven JE, Janotka E, et al. Discrimina- new species of Talaromyces from clinical sources. Mycoses 2017;60(10):651–62.
tion of Penicillium isolates by matrix-assisted laser desorption/ionization time-of- [151] Siqueira JPZ, Sutton DA, Gené J, García D, Wiederhold N, Guarro J. Species of Asper-
flight mass spectrometry fingerprinting. Rapid Commun Mass Spectrom 2008;22 gillus section Aspergillus from clinical samples in the United States. Med Mycol
(16):2555–60. 2018;56(5):541–50.
[125] Lau SKP, Lam CSK, Ngan AHY, Chow W-N, Wu AKL, Tsang DNC, et al. Matrix- [152] Woo PCY, Lau SKP, Liu B, Cai JJ, Chong KTK, Tse H, et al. Draft genome sequence of
assisted laser desorption ionization time-of-flight mass spectrometry for rapid Penicillium marneffei strain PM1. Eukaryot Cell 2011;10(12):1740–1.
identification of mold and yeast cultures of Penicillium marneffei. BMC Microbiol [153] Woo PCY, Tam EWT, Chong KTK, Cai JJ, Tung ETK, Ngan AHY, et al. High diversity of
2016;16(1):1–9. polyketide synthase genes and the melanin biosynthesis gene cluster in Penicillium
[126] Normand AC, Becker P, Gabriel F, Cassagne C, Accoceberry I, Gari-Toussaint M, et al. marneffei. FEBS J 2010;277(18):3750–8.
Validation of a new web application for identification of fungi by use of matrix- [154] Woo PCY, Lam C-W, Tam EWT, Leung CKF, Wong SSY, Lau SKP, et al. First discovery
assisted laser desorption ionization–time of flight mass spectrometry. J Clin of two polyketide synthase genes for mitorubrinic acid and mitorubrinol yellow
Microbiol 2017;55(9):2661–70. pigment biosynthesis and implications in virulence of Penicillium marneffei. PLoS
[127] Logrieco A, Peterson SW, Wicklow DT. Ribosomal RNA comparisons among taxa of Negl Trop Dis 2012;6(10):e1871.
the terverticillare Penicillia. In: Samson RA, Pitt JI, editors. Modern Concepts in Pen- [155] Lau SKP, Chow W-N, Wong AYP, Yeung JMY, Bao J, Zhang N, et al. Identification of
icillium and Aspergillus Classification. New York: Plenum Press; 1990. p. 343–55. microRNA-like RNAs in mycelial and yeast phases of the thermal dimorphic fungus
[128] Skouboe P, Taylor JW, Frisvad JC, Lauritsen D, Larsen L, Albœk C, et al. Molecular Penicillium marneffei. PLoS Negl Trop Dis 2013;7(8):e2398.
methods for differentiation of closely related Penicillium species. In: Samson RA, [156] Yang E, Wang G, Woo PCY, Lau SKP, Chow W-N, Chong KTK, et al. Unraveling the
Pitt JI, editors. Integration of Modern Taxonomic Methods for Penicillium and Asper- molecular basis of temperature-dependent genetic regulation in Penicillium
gillus Classification. Amsterdam: Harwood Academic Publishers; 2000. marneffei. Eukaryot Cell 2013;12(9):1214–24.
[157] Yang E, Chow W-N, Wang G, Woo PCY, Lau SKP, Yuen K-Y, et al. Signature gene ex- [187] Barrs VR, van Doorn TM, Houbraken J, Kidd SE, Martin P, Pinheiro MD, et al. Asper-
pression reveals novel clues to the molecular mechanisms of dimorphic transition gillus felis sp. nov., an emerging agent of invasive aspergillosis in humans, cats, and
in Penicillium marneffei. PLoS Genet 2014;10(10):e1004662. dogs. PLoS One 2013;8(6):e64871.
[158] Woo PCY, Lau SKP, Lau CCY, Tung ETK, Chong KTK, Yang F, et al. Mp1p is a virulence [188] Tanney JB, Visagie CM, Yilmaz N, Seifert KA. Aspergillus subgenus Polypaecilum from
factor in Talaromyces (Penicillium) marneffei. PLoS Negl Trop Dis 2016;10(8): the built environment. Stud Mycol 2017;88:237–67.
e0004907. [189] Hsieh H-M, Ju Y-M, Hsueh P-R, Lin H-Y, Hu F-R, Chen W-L. Fungal keratitis caused by a
[159] Seifert KA, Rossman AY. How to describe a new fungal species. IMA Fungus 2010;1 new filamentous hyphomycete Sagenomella keratitidis. Botanical Stud 2009;50:331–5.
(2):109–16. [190] Martinelli L, Zalar P, Gunde-Cimerman N, Azua-Bustos A, Sterflinger K, Piñar G. Asper-
[160] Ariyawansa HA, Hawksworth DL, Hyde KD, Jones EBG, Maharachchikumbura SSN, gillus atacamensis and A. salisburgensis: two new halophilic species from hypersaline/
Manamgoda DS, et al. Epitypification and neotypification: guidelines with appro- arid habitats with a phialosimplex-like morphology. Extremophiles 2017;21(4):
priate and inappropriate examples. Fungal Divers 2014;69(1):57–91. 755–73.
[161] Crous PW, Hawksworth DL, Wingfield MJ. Identifying and naming plant- [191] Thom C, Raper KB. The Aspergillus nidulans group. Mycologia 1939;31(6):653–69.
pathogenic fungi: past, present, and future. Annu Rev Phytopathol 2015;53(1): [192] Horie Y. New or interesting Emericella from herbal drugs. Trans Mycol Soc Jpn
247–67. 1979;20:481–91.
[162] Tedersoo L, Ramirez KS, Nilsson RH, Kaljuvee A, Kõljalg U, Abarenkov K. Standard- [193] Horie Y, Miyaji M, Nishimura K, Franco MF, KlR Coelho. New and interesting species
izing metadata and taxonomic identification in metabarcoding studies. GigaScience of Emericella from Brazilian soil. Mycoscience 1996;37(2):137–44.
2015;4(1):34. [194] Fontbrune FS, Denis B, Meunier M, Garcia-Hermoso D, Bretagne S, Alanio A. Itera-
[163] Schoch CL, Aime MC, de Beer W, Crous PW, Hyde KD, Penev L, et al. Using standard tive breakthrough invasive aspergillosis due to TR(34)/L98H azole-resistant Asper-
keywords in publications to facilitate updates of new fungal taxonomic names. IMA gillus fumigatus and Emericella sublata in a single hematopoietic stem cell
Fungus 2018;8(2):70–3. transplant patient. Transpl Infect Dis 2014;16(4):687–91.
[164] Nilsson RH, Tedersoo L, Abarenkov K, Ryberg M, Kristiansson E, Hartmann M, et al. [195] Chrenkova V, Hubka V, Cetkovsky P, Kouba M, Weinbergerova B, Lyskova P, et al.
Five simple guidelines for establishing basic authenticity and reliability of newly Proven invasive pulmonary aspergillosis in stem cell transplant recipient due to Asper-
generated fungal ITS sequences. MycoKeys 2012;4:37–63. gillus sublatus, a cryptic species of A. nidulans. Mycopathologia 2018;183(2):423–9.
[165] Tedersoo L, Abarenkov K, Nilsson RH, Schüssler A, Grelet G-A, Kohout P, et al. Tidy- [196] Visagie CM, Yilmaz N, Renaud JB, Sumarah MW, Hubka V, Frisvad JC, et al. A survey
ing up international nucleotide sequence databases: ecological, geographical and of xerophilic Aspergillus from indoor environment, including descriptions of two
sequence quality annotation of ITS sequences of mycorrhizal fungi. PLoS One new section Aspergillus species producing eurotium-like sexual states. MycoKeys
2011;6(9):e24940. 2017;19:1–30.
[166] Hyde KD, Udayanga D, Manamgoda DS, Tedersoo L, Larsson E, Abarenkov K, et al. [197] Visagie CM, Varga J, Houbraken J, Meijer M, Kocsubé S, Yilmaz N, et al. Ochratoxin
Incorporating molecular data in fungal systematics: a guide for aspiring re- production and taxonomy of the yellow aspergilli (Aspergillus section Circumdati).
searchers. Curr Res Environm Appl Mycol 2013;3(1):1–32. Stud Mycol 2014;78:1–61.
[167] Kotov AA, Gololobova MA. Traditional taxonomy: Quo vadis? Integr Zool 2016;11 [198] Sugui JA, Peterson SW, Figat A, Hansen B, Samson RA, Mellado E, et al. Genetic re-
(6):500–5. latedness versus biological compatibility between Aspergillus fumigatus and related
[168] Peterson SW. Phylogenetic relationships in Aspergillus based on rDNA sequence species. J Clin Microbiol 2014;52(10):3707–21.
analysis. In: Samson RA, Pitt JI, editors. Integration of Modern Taxonomic Methods [199] Chong GM, Vonk AG, Meis JF, Dingemans GJH, Houbraken J, Hagen F, et al. Interspe-
for Penicillium and Aspergillus Classification. Amsterdam: Harwood Academic Pub- cies discrimination of A. fumigatus and siblings A. lentulus and A. felis of the Asper-
lishers; 2000. p. 323–56. gillus section Fumigati using the AsperGenius® assay. Diagn Microbiol Infect Dis
[169] Peterson SW, Varga J, Frisvad JC, Samson RA. Phylogeny and subgeneric taxonomy 2017;87(3):247–52.
of Aspergillus. In: Varga J, Samson RA, editors. Aspergillus in the genomic era. [200] Hubka V, Lyskova P, Frisvad JC, Peterson SW, Skorepova M, Kolarik M. Aspergillus
Wageningen: Wageningen Academic Publishers; 2008. p. 33–56. pragensis sp. nov. discovered during molecular reidentification of clinical isolates
[170] Jurjević Ž, Kubátová A, Kolařík M, Hubka V. Taxonomy of Aspergillus section belonging to Aspergillus section Candidi. Med Mycol 2014;52(6):565–76.
Petersonii sect. nov. encompassing indoor and soil-borne species with predominant [201] Gams W. Connected and disconnected chains of phialoconidia and Sagenomella
tropical distribution. Plant Syst Evol 2015;301(10):2441–62. gen. nov. segregated from Acremonium. Persoonia 1978;10(1):97–112.
[171] Sklenář F, Jurjević Ž, Zalar P, Frisvad JC, Visagie CM, Kolařík M, et al. Phylogeny of [202] Fennell DI, Raper KB. New species and varieties of Aspergillus. Mycologia 1955;47
xerophilic aspergilli (subgenus Aspergillus) and taxonomic revision of section (1):68–89.
Restricti. Stud Mycol 2017:161–236. [203] Godeas AM. Micoflora del suelo de la argentina. I algunas formas ascosporicas de la
[172] Peterson SW. Phylogenetic analysis of Aspergillus sections Cremei and Wentii, based region chaqueña. Mycopathol Mycol Appl 1972;46(3):189–204.
on ribosomal DNA sequences. Mycol Res 1995;99(11):1349–55. [204] Horie Y. Ascospores ornamentation and its application to the taxonomic re-
[173] Houbraken J, Wang L, Lee HB, Frisvad JC. New sections in Penicillium containing evaluation in Emericella. Trans Mycol Soc Jpn 1980;21:483–93.
novel species producing patulin, pyripyropens or other bioactive compounds. [205] Yu J, Mu X, Li R. Invasive pulmonary aspergillosis due to Emericella nidulans var.
Persoonia 2016;36(1):299–314. echinulata, successfully cured by voriconazole and micafungin. J Clin Microbiol
[174] Yaguchi T, Someya A, S-i Udagawa. A reappraisal of intrageneric classification of 2013;51(4):1327–9.
Talaromyces based on the ubiquinone systems. Mycoscience 1996;37(1):55–60. [206] Uhrin GB, Jensen RH, Korup E, Grønlund J, Hjort U, Moser C, et al. Recurrent pros-
[175] Houbraken J, Spierenburg H, Frisvad JC. Rasamsonia, a new genus comprising thetic valve endocarditis caused by Aspergillus delacroxii (formerly Aspergillus
thermotolerant and thermophilic Talaromyces and Geosmithia species. Antonie nidulans var. echinulatus). Med Mycol Case Rep 2015;10:21–3.
Van Leeuwenhoek 2012;101(2):403–21. [207] Ishiwada N, Takeshita K, Yaguchi T, Nagasawa K, Takeuchi N, Hishiki H, et al. The
[176] Sigler L, Sutton DA, Gibas CFC, Summerbell RC, Noel RK, Iwen PC. Phialosimplex, a first case of invasive mixed-mold infections due to Emericella nidulans var.
new anamorphic genus associated with infections in dogs and having phylogenetic echinulata and Rasamsonia piperina in a patient with chronic granulomatous dis-
affinity to the Trichocomaceae. Med Mycol 2010;48(2):335–45. ease. Mycopathologia 2016;181(3):305–9.
[177] Armstrong PF, Sigler L, Sutton DA, Grooters AM, Hitt M. Fungal myelitis caused by [208] Hubka V, Nováková A, Peterson SW, Frisvad JC, Sklenář F, Matsuzawa T, et al. A re-
Phialosimplex caninus in an immunosuppressed dog. Med Mycol 2012;50(5): appraisal of Aspergillus section Nidulantes with descriptions of two new
509–12. sterigmatocystin-producing species. Plant Syst Evol 2016;302(9):1267–99.
[178] Malloch D, Sigler L, Hambleton S, Vanderwolf KJ, Gibas CFC, McAlpine DF. Fungi as- [209] Barrs VR, Beatty JA, Dhand NK, Talbot JJ, Bell E, Abraham LA, et al. Computed tomo-
sociated with hibernating bats in New Brunswick caves: the genus graphic features of feline sino-nasal and sino-orbital aspergillosis. Vet J 2014;201
Leuconeurospora. Botany 2016;94(12):1171–81. (2):215–22.
[179] GM E, C J, T P, G I, MdM E, R E, et al. Disseminated mycoses in a dog by Paecilomyces [210] Langlois DK, Sutton DA, Swenson CL, Bailey CJ, Wiederhold NP, Nelson NC, et al.
sp. J Vet Med A 2000;47(4):243–9. Clinical, morphological, and molecular characterization of Penicillium canis sp.
[180] Gené J, Blanco JL, Cano J, García ME, Guarro J. New filamentous fungus Sagenomella nov., isolated from a dog with osteomyelitis. J Clin Microbiol 2014;52(7):2447–53.
chlamydospora responsible for a disseminated infection in a dog. J Clin Microbiol [211] Sarbhoy AK, Elphick JJ. Hemicarpenteles paradoxus gen. & sp.nov.: the perfect state
2003;41(4):1722–5. of Aspergillus paradoxus. Trans Br Mycol Soc 1968;51(1):155–7.
[181] Guinea J, Sandoval-Denis M, Escribano P, Peláez T, Guarro J, Bouza E. Aspergillus [212] Yaguchi T, Someya A, Miyadoh S, Udagawa S. Aspergillus ingratus, a new species in
citrinoterreus, a new species of section terrei isolated from samples of patients with Aspergillus section Clavati. Trans Mycol Soc Jpn 1993;34:305–10.
nonhematological predisposing conditions. J Clin Microbiol 2015;53(2):611–7. [213] Frisvad JC, Yilmaz N, Thrane U, Rasmussen KB, Houbraken J, Samson RA.
[182] Crous PW, Wingfield MJ, Burgess TI, Carnegie AJ, Hardy GE, Smith D, et al. Fungal Talaromyces atroroseus, a new species efficiently producing industrially relevant
planet description sheets: 625–715. Persoonia 2017;39(1):270–467. red pigments. PLoS One 2013;8(12):e84102.
[183] Hubka V, Nováková A, Samson RA, Houbraken J, Frisvad JC, Sklenář F, et al. Asper- [214] Horré R, Gilges S, Breig P, Kupfer B, De Hoog GS, Hoekstra E, et al. Case Report.
gillus europaeus sp. nov., a widely distributed soil-borne species related to Fungaemia due to Penicillium piceum, a member of the Penicillium marneffei com-
A. wentii (section Cremei). Plant Syst Evol 2016;302(6):641–50. plex. Mycoses 2001;44(11-12):502–4.
[184] Katz ME, Dougall AM, Weeks K, Cheetham BF. Multiple genetically distinct groups [215] Santos PE, Piontelli E, Shea YR, Galluzzo ML, Holland SM, Zelazko ME, et al. Penicil-
revealed among clinical isolates identified as atypical Aspergillus fumigatus. J Clin lium piceum infection: diagnosis and successful treatment in chronic granuloma-
Microbiol 2005;43(2):551–5. tous disease. Med Mycol 2006;44(8):749–53.
[185] Coelho D, Silva S, Vale-Silva L, Gomes H, Pinto E, Sarmento A, et al. Aspergillus [216] Peterson SW, Jurjević Ž. Talaromyces columbinus sp. nov., and genealogical concor-
viridinutans: an agent of adult chronic invasive aspergillosis. Med Mycol 2011;49 dance analysis in Talaromyces clade 2a. PLoS One 2013;8(10):e78084.
(7):755–9. [217] Crous PW, Wingfield MJ, Burgess TI, Hardy GE, Crane C, Barrett S, et al. Fungal
[186] Peláez T, Álvarez-Pérez S, Mellado E, Serrano D, Valerio M, Blanco JL, et al. Invasive Planet description sheets: 469–557. Persoonia 2016;37:218–403.
aspergillosis caused by cryptic Aspergillus species: a report of two consecutive epi- [218] Peterson SW, Jurjević Ž. New species of Talaromyces isolated from maize, indoor air,
sodes in a patient with leukaemia. J Med Microbiol 2013;62(3):474–8. and other substrates. Mycologia 2017;109(4):537–56.

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Computational and Structural Biotechnology Journal 16 (2018) 197–210

Contents lists available at ScienceDirect

journal homepage: www.elsevier.com/locate/csbj

Taxonomy and evolution of Aspergillus, Penicillium and Talaromyces in the

1. Introduction Many Aspergillus, Penicillium and Talaromyces species are economi-

pathogenic species on a global sense is A. fumigatus [9], which is the a b c

2. Classiﬁcation and nomenclature: a brief history and recent

Monascus, Xeromyces, Leiothecium

Eurotiales Section Helici

Section Trachyspermi Talaromyces

var. echinulatus and invasive pulmonary aspergillosis and rpb2

phenotypic to chemotaxonomic, genetic/phylogenetic, or consolidated References

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