microorganisms

Article
The Protean Acremonium. A. sclerotigenum/egyptiacum:
Revision, Food Contaminant, and Human Disease
Richard C. Summerbell 1,2, *, Cecile Gueidan 3 , Josep Guarro 4 , Akif Eskalen 5 , Pedro W. Crous 6 ,
Aditya K. Gupta 7,8 , Josepa Gené 4 , Jose F. Cano-Lira 4 , Arien van Iperen 6 , Mieke Starink 6 and
James A. Scott 2 ID
1 Sporometrics, 219 Dufferin St. Ste. 20C, Toronto, ON M6K 1Y9 Canada
2 Dalla Lana School of Public Health, University of Toronto, Toronto, ON M5T 3M7, Canada;
[Link]@[Link]
3 Australian National Herbarium, National Research Collections Australia, CSIRO-NCMI, Canberra,
ACT 2601, Australia; [Link]@[Link]
4 Unitat de Micologia, Facultat de Medicina i Ciencies de la Salut and IISPV, Universitat Rovira i Virgili, Reus,
43201 Tarragona, Spain; [Link]@[Link] (J.G.); [Link]@[Link] (J.G.); [Link]@[Link] (J.F.C.-L.)
5 Department of Plant Pathology, University of California Davis, Davis, CA 95616, USA;
aeskalen@[Link]
6 Westerdijk Fungal Biodiversity Institute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands;
[Link]@[Link] (P.W.C.); [Link]@[Link] (A.v.I.);
[Link]@[Link] (M.S.)
7 Division of Dermatology, Department of Medicine, University of Toronto, Toronto, ON M5G 2C4, Canada;
agupta@[Link]
8 Mediprobe Research Inc., London, ON N5X 2P1, Canada
* Correspondence: rsummerbell@[Link]; Tel.: +1-416-516-1660




Received: 2 June 2018; Accepted: 13 August 2018; Published: 16 August 2018


Abstract: Acremonium is known to be regularly isolated from food and also to be a cause of human
disease. Herein, we resolve some sources of confusion that have strongly hampered the accurate
interpretation of these and other isolations. The recently designated type species of the genus Acremonium,
A. alternatum, is known only from a single isolate, but it is the closest known relative of what may be
one of the planet’s most successful organisms, Acremonium sclerotigenum/egyptianum, shown herein to be
best called by its earliest valid name, A. egyptiacum. The sequencing of ribosomal internal transcribed
spacer (ITS) regions, actin genes, or both for 72 study isolates within this group allowed the full range of
morphotypes and ITS barcode types to be elucidated, along with information on temperature tolerance
and habitat. The results showed that nomenclatural confusion and frequent misidentifications facilitated
by morphotaxonomy, along with misidentified early sequence deposits, have obscured the reality that this
species is, in many ways, the definitive match of the historical concept of Acremonium: a pale orange or
dull greenish-coloured monophialidic hyphomycete, forming cylindrical, ellipsoidal, or obovoid conidia
in sticky heads or obovoid conidia in dry chains, and acting ecologically as a soil organism, marine
organism, plant pathogen, plant endophyte, probable insect pathogen, human opportunistic pathogen,
food contaminant, probable dermatological communicable disease agent, and heat-tolerant spoilage
organism. Industrially, it is already in exploratory use as a producer of the antibiotic ascofuranone, active
against trypanosomes, cryptosporidia, and microsporidia, and additional applications are in development.
The genus-level clarification of the phylogeny of A. egyptiacum shows other historic acremonia belong to
separate genera, and two are here described, Parasarocladium for the Acremonium radiatum complex and
Kiflimonium for the Acremonium curvulum complex.

Keywords: Hypocreales; biodeterioration; Bionectriaceae; Acremonium; Acremonium sclerotigenum;

Acremonium egyptianum

Microorganisms 2018, 6, 88; doi:10.3390/microorganisms6030088 [Link]/journal/microorganisms

Microorganisms 2018, 6, 88 2 of 21

1. Introduction
Acremonium is one of the genera selected for this Special Issue, as it is well established as a
potentially food-borne organism that also plays a role in infectious diseases of humans and animals [1].
The study of overlapping biotypes commonly isolated from food and cases of human disease soon led
to a focus on one particular group of Acremonium species as significant in these areas. The sequence
analysis of DNA loci was needed to clarify the circumscription of the group of interest.
Molecular phylogeny is particularly revelatory in the case of simply structured organisms, which
produce few morphological clues to their natural affinities. Phylogenetic revisions [2–4] of the species
grouped in the morphogenus Acremonium by Gams [5] contained at least two major surprises. One
surprise was that multiple families and orders of fungi were encompassed in the concept. Indeed,
species of radically different phylogenetic affinity could look almost indistinguishable; an example is
the convergence of the Hypocrealean Acremonium sclerotigenum (particularly mucoid-conidial isolates
not forming sclerotia) and its distant relative Acremonium (now Sarocladium) strictum, as well as the
far-removed Plectosphaerellaceous Acremonium cucurbitacearum, now Plectosphaerella melonis. The other
surprise was that conidiogenesis was strongly pleomorphic within some species. Different morphs
with identical or near-identical sequences at standard biosystematically used loci had sometimes been
described as separate species. In the especially dramatic case of Acremonium sclerotigenum/egyptiacum,
conidiogenesis, though always phialidic, differed markedly among isolates. Some mainly produced
cylindrical to long-ellipsoidal conidia in mucoid heads, while others produced broadly ellipsoidal
conidia in heads. There were also many isolates producing obclavate to obovoid conidia in dry
chains. The different conidial morphs had distinct colours: the mucoid morphs were pale to medium
salmonaceous, while the catenate morphs matured as dull greenish grey. This unexpected plasticity
helped to inform a revised view of the taxonomic informativeness of fungal conidiogenesis [6].
The long-standing practical consequence of this sort of plasticity was that very few historic
identifications of the Acremonium species from substrates of practical interest, like food, could be
trusted. The exceptions were a few cases where voucher isolates were retained and could later
be sequence-identified. The small number of such isolates in collections indicated that the name
Acremonium sclerotigenum was sometimes isolated from contaminated food [7]. The species concepts
had to be redefined, however, in order to be certain which isolates, if any, should truly bear this name,
particularly as early sequencing had deposited many reference sequences under names known to be
incorrect. The phylogenetic analysis used to clarify species definitions also frequently brought the
names of genera into question, and further biosystematic decisions had to be made at that level.
The morphological convergence among Acremonium types was so extensive that, prior to 2011,
there were at least five major, phylogenetically distinct contenders among sequence types for the role
of epitype of Acremonium alternatum, the type species. This typification was only substantiated by a
scant dried type specimen and illustrations. The choice of epitype would root the future phylogenetic
concept of Acremonium. Even when the contenders were vetted by exact morphological comparison
with Gams’ illustrations of dried type material [8], as well as habitat considerations (leaf litter, near
Rostock, Germany), the name could not be narrowed down to a single phylogenetic species. At the
time, the most economically, medically, and industrially important species in Acremonium were (a)
those related to A. kiliense and A. strictum (two closely related species), (b) the antibiotic producers
A. chrysogenum and Emericellopsis salmosynnemata (which had an Acremonium asexual mvorph), and
(c) Acremonium sclerotigenum. The importance of A. sclerotigenum was masked by circumstance: its
morphological diversity meant that most isolates had been identified under other names, usually
A. strictum or A. potronii for isolates with mucoid conidia and A. egyptiacum or A. alternatum for isolates
with catenate conidia. Sequence evidence revealed that the importance of A. strictum as an opportunistic
human pathogen was based on misidentification: all such identifications that could be definitively
traced were A. sclerotigenum or A. kiliense [7]. A. kiliense was closely related to the type species
of a valid genus, Sarocladium, originally distinguished by a minor apomorphy, slightly penicillate
Microorganisms 2018, 6, 88 3 of 21

conidiophore branching. It was not especially closely related to any candidate for A. alternatum, nor
were A. chrysogenum or E. salmosynnemata.
Meanwhile, sequenced isolates revealed that A. sclerotigenum was going unrecognised in many
important roles and microhabitats that were typical of existing concepts of Acremonium. Though not
infrequently identified as A. alternatum itself when catenate, it had a distinct grey-green tone in chained
conidial masses that was not mentioned in the description of the type. It was, however, closely related
to an isolate that was an excellent candidate for ‘the real’ A. alternatum in every way, CBS 407.66
(CBS = Westerdijk Institute, Utrecht, the Netherlands). For all these reasons (and others), A. kiliense
and A. strictum were recombined into Sarocladium, and A. alternatum was epitypified with CBS 407.66
with the express aim of including A. sclerotigenum in the core group of the revised genus Acremonium.
The object of the present paper is to document the intrinsic phylogenetic biodiversity, protean
ecology, multifaceted anthropic significance, and complex nomenclature of this archetypical
Acremonium species. For practical purposes, in reference to the theme of this Special Issue, this
clarification is expected to provide an essential underpinning for interpreting Acremonium isolations, as
well as nucleic acid and secondary metabolite data, from food-related and biomedical sources. Without
such a study, given the prevalence of misidentified reference sequences in public databases and the
many known reports already marred by use of these inappropriate names [7], authors remain at risk of
inadvertently generating data that are misleading or arduous to interpret.

2. Materials and Methods

Isolates were obtained from the collections of the Westerdijk Institute (previously called the CBS
Fungal Biodiversity Centre; herbarium designation still CBS) and the FMR collection (Facultad de
Medicina, Reus, Tarragona, Spain). Many of the latter isolates had originally been received from the
University of Texas Health Science Center at San Antonio, TX, USA, and had UTHSC (University of
Texas Health Science Center) numbers. Several isolates from the Ontario Ministry of Health (OMH)
were tested, and while most were deposited into CBS and listed under those numbers, a few have only
OMH numbers.
The isolates were grown for microscopic observation and temperature growth tests on malt extract
agar (MEA; 3% malt extract, Oxoid, Basingstoke, Hampshire, UK) and oatmeal agar (OA; [9]). Growth
at human body temperature (37 ◦ C) was monitored at 7 and 14 days for selected isolates considered to
represent the range of morphological diversity seen in the isolates.
The DNA for the isolates handled at the Westerdijk Institute was extracted with a FastDNA kit
(Qbiogene, Heidelberg, Germany) from mycelium grown for 5–14 days in liquid complete medium [10].
One mL of each DNA sample (containing 50–100 ng DNA mL–1 ) was subjected to PCR amplification.
The nuclear ribosomal internal transcribed spacer (ITS) region was amplified (ITS1 spacer, 5.8S
ribosomal region, ITS2 spacer) using primers ITS1 and ITS4 as described by White et al. [11].
The amplicons were cleaned using the GFX PCR DNA Purification Kit (Amersham Pharmacia,
Little Chalfont, UK) as per the kit’s instructions. The cleaned DNA was subjected to cycle sequencing
using the same primers used for PCR. The cycle sequencing program was as follows: 25 cycles of 95 ◦ C
(20 s), 50 ◦ C (15 s), and 60 ◦ C (60 s). The cycle sequencing PCR products were purified using Sephadex
G-50 (Amersham Pharmacia) and sequenced at the Westerdijk Institute using BigDye chemistry and
an ABI 3730xl sequencer (Applied Biosystems, Carlsbad, CA, USA).
At FMR, total genomic DNA was extracted from colonies grown on potato dextrose agar (PDA;
4 g of potato infusion, 20 g dextrose, 15 g of agar-agar, 1 L tap water) after 7 days of incubation
at 20 ± 1 ◦ C, using the FastDNA kit protocol (per Bio101, Vista, CA, USA), with a FastPrep FP120
instrument (Thermo Savant, Holbrook, NY, USA) following the manufacturer’s protocol. The DNA
was quantified using the Nanodrop 2000 (Thermo Scientific, Madrid, Spain). The ITS region and a
fragment of the actin gene were amplified with the primer pairs ITS1/ITS4 [11] and ACT1/ACT4R [12],
respectively. The amplicons were sequenced in both directions with the same primer pair used for
amplification at Macrogen Europe (Macrogen Inc., Amsterdam, The Netherlands). The consensus
Microorganisms 2018, 6, 88 4 of 21

sequences were obtained using the SeqMan software version 7.0.0 (DNAStar Lasergene, Madison,
WI, USA).
At the Australian National Herbarium, the Lasergene SeqMan and EditSeq software modules
(DNAstar Lasergene) were used to assemble and edit the sequence files. The sequences were then
aligned manually in Mesquite version 3.40 [13]. The two gene regions were analysed separately.
The ITS dataset included a total of 72 isolates, and six of these (four species of Emericellopsis, one
species of Stilbella, and the ex-type strain of Acremonium tubakii) were used to root the tree. The actin
dataset included a total of 49 taxa, with Acremonium curvulum, Acremonium spinosum, and Emericellopsis
glabra as outgroup taxa. A GTRCAT model was applied to the two markers, and the two datasets
were analysed using maximum likelihood (ML) with the software RAxML VI-HPC v.8.2.9; [14,15]), as
implemented on the CIPRES Web Portal ([Link] [16]). Support values were obtained
using a fast bootstrap analysis of 1000 pseudoreplicates. The trees were visualised in PAUP* [17] and
edited with Illustrator (Adobe Systems, San Jose, CA, USA). The datasets were deposited in TreeBase
(accession 22890), sequences in GenBank, and nomenclature in MycoBank.

3. Results
DNA sequencing at both the ITS and actin loci showed that isolates with a range of morphologies
were grouped into a cohesive sequence group. Within this group, ITS sequences were consistently
subdivided into three minimally delimited genetic variants. The sequence differences for these ITS
barcode variants are shown in Table 1. A small number of sequences within each barcode type had
other minor divergences, not consistent from strain to strain.

Table 1. Major variants in internal transcribed spacer (ITS) sequences among isolates identified as
conspecific with the type of Acremonium sclerotigenum.

Position 33 after Common Startpoint

ITS Group Position 106 Position 388
‘ATCATTA’
Ex-type strains 1 group
C C C
(Group 1)
Group 2 T C C
Group 3 T T A
1 Contains sequences from ex-type isolates of Acremonium sclerotigenum and A. egyptiacum.

A select group of isolates at CBS and at FMR were studied to analyse morphological characters.
A smaller group of isolates held at CBS were tested for growth at 37 ◦ C. Figure 1A–C,E,F show the
range of morphologies seen: catenate conidia of CBS 545.89 (Figure 1A) consistent with Gams’ concept
of A. alternatum, ellipsoidal, mucoid conidia of CBS 251.95 (Figure 1C) consistent with Gams’ concept
of A. potronii, and cylindrical, mucoid conidia of CBS 113276 (Figure 1E) consistent with the original
description of A. sclerotigenum. Sclerotia are shown both for the catenate-conidial 545.89 (Figure 1B)
and at lower magnification for the mucoid-conidial Zare 60-#3. The original 1910 line-drawing of
Acremonium potronii (Figure 1D), reproduced here for comparison, is described in the Discussion.
In Table 2, the characteristics of the isolates studied in detail are listed with the identification and
isolation details of all the other isolates in this study for which ITS sequences were obtained. Table 3
lists isolation details for isolates included in actin sequencing but not elsewhere in the study. It also
lists details for outgroup isolates used in analysis in the ITS and actin studies.
Microorganisms 2018, 6, 88 5 of 21

Table 2 shows that among the three common ITS barcode types, only the first one, 33C/106C/388C,
was predominantly seen in isolates obtained outside clinical (including medical and veterinary)
environments. Of 32 such isolates, 23 were from environmental sources, eight from clinical sources,
and one of unrecorded origin. In contrast, for ITS barcode 2 (33T/106C/388C), six of 11 isolates were
Microorganisms 2018, 6, x FOR PEER REVIEW 5 of 20
from clinical sources. For barcode type 3, (33T/106T/388A), only two of 19 isolates were known to be
from environmental
were known to be from sources, while just one
environmental was from
sources, whileanjust
unrecorded
one wassource,
from anleaving the remaining
unrecorded source,
16 clinical. Each barcode type contained an isolate involved in a published medical
leaving the remaining 16 clinical. Each barcode type contained an isolate involved in a published or veterinary case:
lethal infection
medical of an ostrich
or veterinary case: egg in barcode
lethal infection1 of
[18],
andialysis-related
ostrich egg in peritonitis
barcode 1 in[18],
barcode 2 [19], and
dialysis-related
systemic infection of an immunocompromised patient in barcode 3 [20]. Most isolates
peritonitis in barcode 2 [19], and systemic infection of an immunocompromised patient in barcode obtained from 3
humans were from infected toenails. Many were from repetition-confirmed infections
[20]. Most isolates obtained from humans were from infected toenails. Many were from repetition- as described
by Gupta etinfections
confirmed al. [21]; the
as 32 “Acremonium
described sp.”et
by Gupta isolates listed
al. [21]; in “Acremonium
the 32 that publication
sp.”asisolates
confirmed causes
listed of
in that
onychomycosis were all later identified as A. sclerotigenum.
publication as confirmed causes of onychomycosis were all later identified as A. sclerotigenum.

Figure 1. Morphological diversity of Acremonium sclerotigenum/egyptiacum plus a comparison with an

Figure 1. Morphological diversity of Acremonium sclerotigenum/egyptiacum plus a comparison with
illustration of the original Acremonium potronii. (A–E) ×1000, (F) ×400. Blue structures stained in lactic-
an illustration of the original Acremonium potronii. (A–E) ×1000, (F) ×400. Blue structures stained in
acid-cotton-blue stain, reddish in lactofuchsin: (A) CBS 545.89, catenate-conidial isolate originally
lactic-acid-cotton-blue stain, reddish in lactofuchsin: (A) CBS 545.89, catenate-conidial isolate originally
identified as A. alternatum; (B) CBS 545.89 sclerotia; (C) CBS 251.95 mucoid-conidial isolate with
identified as A. alternatum; (B) CBS 545.89 sclerotia; (C) CBS 251.95 mucoid-conidial isolate with
ellipsoidal conidia, originally
ellipsoidal conidia, originallyidentified
[Link];
potronii;(D)
(D)original
original Vuillemin
Vuillemin drawing
drawing of potronii;
of A. A. potronii;
(E)
(E)
CBS 113276, typical mucoid-conidial A. sclerotigenum isolate with cylindrical conidia; and (F) and
CBS 113276, typical mucoid-conidial A. sclerotigenum isolate with cylindrical conidia; (F)
heavily
heavily
sclerotialsclerotial IranianZare
Iranian isolate isolate Zare 60-#3.
60-#3.

Table 2. Isolates in the Acremonium sclerotigenum/egyptiacum complex typed by ITS barcode type.
Isolate # (CBS
Original
Unless Otherwise
Identification (as ITS
Indicated) and
Received by Us; Geno- Morphology Habitat Origin Remarks
GenBank
Nomenclature Not Group
Numbers: ITS,
Updated)
(Actin)
sand dune France, region
124.42 Acremonium slow 37 °C
1 mucoid under Pays de la
MH424620 sclerotigenum (T) growth
Ammophila Loire
114785 Acremonium
Microorganisms 2018, 6, 88 6 of 21

Table 2. Isolates in the Acremonium sclerotigenum/egyptiacum complex typed by ITS barcode type.

Isolate # (CBS
Original
Unless Otherwise
Identification (as
Indicated) and ITS
Received by Us; Morphology Habitat Origin Remarks
GenBank Geno-Group
Nomenclature
Numbers: ITS,
Not Updated)
(Actin)
124.42 Acremonium sand dune under France, region
1 mucoid slow 37 ◦ C growth
MH424620 sclerotigenum (T) Ammophila Pays de la Loire
114785 Acremonium
MH424616, egyptiacum (T) as 1 catenate soil Cairo, Egypt
(MH427920) Oospora egyptiaca
474.67 Acremonium banana leaf in
1 mucoid Netherlands slow growth 37 ◦ C
MH424661 strictum greenhouse
734.69 survives 37 ◦ C,
Acremonium Izmir Prov.,
MH424615, 1 catenate tomato root does not grow.
egyptiacum Turkey
(MH427921) Forms sclerotia
319.70D
Acremonium survives 37 ◦ C,
MH424660, 1 mucoid chamois dung Tyrol, Austria
strictum does not grow
(MH427955)
526.93 Acremonium Muskmelon
1 mucoid Spain slow growth 37 ◦ C
MH424614 cucurbitacearum (Cucumis melo)
223.70 Acremonium survives 37 ◦ C,
1 catenate wall France
U57674 alternatum does not grow
100816
Acremonium Illustrated by
MH424640, 1 mucoid ostrich egg Piedmont, Italy
sclerotigenum Isaia et al. [18]
(MH427956)
384.65 Acremonium
1 mucoid human toenail Québec, Canada
MH424635 sclerotigenum
113276 Acremonium survives 37 ◦ C,
1 mucoid human Germany
MH424641 sclerotigenum does not grow
OMH F3691.97 Acremonium
1 mucoid human toenail Ontario, Canada
MH424648 sclerotigenum
Eskalen ST2 Acremonium Madera Cty.,
1 mucoid grapevine
MH424646 alternatum California, USA
Eskalen SRLH9 Acremonium Madera Cty.,
1 mucoid grapevine
MH424612 alternatum California, USA
Eskalen SRLH5 Acremonium Madera Cty.,
1 mucoid grapevine
MH424611 alternatum California, USA
Eskalen SRLH14 Acremonium Madera Cty.,
1 mucoid grapevine
MH729059 alternatum California, USA
human
UTHSC 04-3176 Acremonium
1 mucoid cerebro-spinal Minnesota, USA
MH424653 sclerotigenum
fluid
UTHSC 06-1454
Acremonium
MH424656, 1 mucoid human toenail Florida, USA
sclerotigenum
(MH427916)
UTHSC 05-104
Acremonium human, unknown
MH424654, 1 catenate California, USA
egyptiacum site
(MH427917)
786.69
Acremonium xylem of
MH424639, 1 mucoid Iran
sclerotigenum Gossypium
(MH427931)
134.58 Acremonium
1 mucoid Cucumis sativus Netherlands
MH424621 sclerotigenum
135.56
Acremonium
MH424622, 1 mucoid Anthurium leaf Netherlands
sclerotigenum
(MH427934)
281.80
Acremonium
MH424625, 1 mucoid human toenail Netherlands
sclerotigenum
(MH427940)
Microorganisms 2018, 6, 88 7 of 21

Table 2. Cont.

Isolate # (CBS
Original
Unless Otherwise
Identification (as
Indicated) and ITS
Received by Us; Morphology Habitat Origin Remarks
GenBank Geno-Group
Nomenclature
Numbers: ITS,
Not Updated)
(Actin)
119482
Acremonium Madera Cty.,
MH424643, 1 mucoid grapevine
sclerotigenum California, USA
(MH427923)
119483
Acremonium Yolo Cty.,
MH424644, 1 mucoid grapevine
sclerotigenum California, USA
(MH427922)
286.70H
Acremonium
MH424633, 1 mucoid haversack Florida, USA
sclerotigenum
(MH427924)
286.70G
Acremonium grapefruit juice
MH424632, 1 mucoid Florida, USA
sclerotigenum can
(MH427925)
121405 Acremonium
1 catenate grapevine Syria
MH424645 egyptiacum
149.55 Puccinia
Acremonium
MH424623, 1 mucoid rubigo-vera Germany
sclerotigenum
(MH427933) uredinium
343.64
Acremonium Finistère Dept.,
MH424634, 1 mucoid lenticel in apple
sclerotigenum France
(MH427936)
286.70E
Acremonium
MH424630, 1 mucoid ND 1 Louisiana, USA
sclerotigenum
(MH427927)
740.69
Acremonium France, Nord
MH424638, 1 mucoid fishmeal
sclerotigenum Dept.
(MH427932)
286.70A
Acremonium Pteridium
MH424626, 1 mucoid Ischia, Italy
sclerotigenum aquilinum petiole
(MH427930)
270.86
Acremonium
MH424624, 2 mucoid human toenail Nancy, France
sclerotigenum
(MH427911)
112783
Acremonium Thessaloniki,
MH424670, 2 mucoid peritoneal fluid
strictum Greece
(MH427947)
251.95 Acremonium Limburg,
2 mucoid human nail slow growth 37 ◦ C
MH424617 potronii Netherlands
545.89 Acremonium South Holland, survives 37 ◦ C,
2 catenate human, blood
MH424636 alternatum Netherlands does not grow
379.70D Acremonium North Holland,
2 mucoid human foot skin
MH424618 potronii Netherlands
Eskalen SRLH17 Acremonium Madera Cty.,
2 mucoid grapevine
MH424613 alternatum California, USA
UTHSC 03-2 Acremonium
2 mucoid human sinus California, USA
MH424652 sclerotigenum
286.70F
Acremonium
MH424631, 2 mucoid ND Florida, USA
sclerotigenum
(MH427926)
114320
Acremonium Hordeum vulgare
MH424642, 2 ND Iran
sclerotigenum leaf
(MH427937)
739.69
Acremonium
MH424637, 2 mucoid humus-rich soil Netherlands
sclerotigenum
(MH427938)
Microorganisms 2018, 6, 88 8 of 21

Table 2. Cont.

Isolate # (CBS
Original
Unless Otherwise
Identification (as
Indicated) and ITS
Received by Us; Morphology Habitat Origin Remarks
GenBank Geno-Group
Nomenclature
Numbers: ITS,
Not Updated)
(Actin)
286.70D
Acremonium air in penicillin
MH424629, 2 mucoid Pakistan
sclerotigenum factory
(MH427928)
soft contact lens
109041 Acremonium
3 mucoid from inflamed Ontario, Canada slow growth 37 ◦ C
MH424619 potronii
human eye
287.70O
Acremonium moderate growth
MH424659, 3 mucoid soil Egypt
strictum 37 ◦ C (9 mm/14 d)
(MH427954)
Acremonium
Novicki UW836 Washington State,
strictum genogroup 3 mucoid human blood ND
AY138844 USA
II
114224
Acremonium
MH424668, 3 mucoid human nail Ontario, Canada
sclerotigenum
(MH427943)
114225
Acremonium
MH424669, 3 mucoid human nail Ontario, Canada
sclerotigenum
(MH427942)
114226
Acremonium
MH424666, 3 mucoid human nail Ontario, Canada
sclerotigenum
(MH427941)
114227 Acremonium
3 mucoid human nail Ontario, Canada slow growth 37 ◦ C
MH424662 sclerotigenum
114229
Acremonium
MH424667, 3 mucoid human nail Ontario, Canada
sclerotigenum
(MH427951)
OMH F1648.97 Acremonium
3 mucoid human nail Ontario, Canada
MH424663 sclerotigenum
OMH F2629.97 Acremonium
3 mucoid human nail Ontario, Canada
MH424665 sclerotigenum
UTHSC 01-194
Acremonium Washington state,
MH424649, 3 mucoid human blood
strictum USA
(MH427912)
UTHSC 07-3739
Acremonium
MH424657, 3 mucoid human toenail Minnesota, USA
alternatum
(MH427918)
UTHSC 05-2270 Acremonium
3 mucoid human blood Utah, USA
MH424655 strictum
UTHSC 02-2890
Acremonium human olecranon
MH424651, 3 mucoid Wisconsin, USA
strictum bursa
(MH427914)
UTHSC 02-2054
Acremonium human tracheal
MH424650, 3 mucoid Ohio, USA
alternatum aspirate
(MH427913)
UTHSC 08-3294
Acremonium
MH424658, 3 mucoid human sputum California, USA
strictum
(MH427915)
149.55
Acremonium diseased Dianthus
MH424623, 3 mucoid Netherlands
sclerotigenum caryophyllus
(MH427933)
FMR 10587
Acremonium Tarragona Prov.,
MH424647, 3 mucoid human nail
sclerotigenum Spain
(MH427919)
286.70B
Acremonium
MH424627, 3 mucoid ND Germany
sclerotigenum
(MH427929)
1 ND = no data.
Microorganisms 2018, 6, 88 9 of 21

Table 3. Additional isolates included in actin sequencing only or as outgroups.

Species and GenBank Isolate # (CBS

Record (Actin Accession Number Habitat Origin
Unless Noted) Unless Noted)
Acremonium sclerotigenum
159.61 1 ND 2 USA
MH427935
A. sclerotigenum
113719 ND Iran
MH427944
A. sclerotigenum
395.70B human toenail Florida, USA
MH427945
A. sclerotigenum
114228 1 human toenail Ontario, Canada
MH427946
A. sclerotigenum
101572 Endophyte in grapevine California, USA
MH427948
A. sclerotigenum
476.96 stony coastal soil Madang Prov., Papua New Guinea
MH427949
A. sclerotigenum
692.86 ND Isère Dept., France
MH427950
A. sclerotigenum
120606 grapevine Madera Cty., California, USA
MH427952
A. sclerotigenum
120819 grapevine Madera Cty., California, USA
MH427953
Ovicillium attenuatum
112092 Theobroma Ecuador
KU382189 ITS
Ovicillium oosporum
101236 Lepidoptera larva Brazil
KU382203 ITS
Emericellopsis terricola (T)
120.40 soil Netherlands
U57676 ITS
Acremonium tubakii (T)
790.69 seacoast Wakayama Pref., Japan
MH424671 ITS
Emericellopsis maritima
NR_144919 ITS
Emericellopsis pallida 491.71 seawater Crimea
NR_145052 ITS 490.71 seawater Crimea
Emericellopsis alkalina 127350 ND ND
NR_145051 ITS AUMC 11023 salt lake Behira Gov., Egypt
Stilbella fimetaria
KX446764 ITS
Acremonium spinosum (T)
136.33 human nail Argentina
HE608629
Acremonium curvulum (T)
HE608630 430.66 soil Schleswig-Holstein, Germany
MH424698 ITS
1 CBS 159.61 and 114228 cluster with members of ITS barcode group 3 in actin analysis. 2 ND = no data.
Microorganisms 2018, 6, 88 10 of 21

The isolates from plant sources were diverse and mostly not ecologically interpretable, but barcode
types 1 and 2, particularly the former, were regularly isolated as endophytes of grapevines, including
numerous isolates from California vine arms obtained by one of us (A.E.).
The isolates derived from food-related sources were all of barcode type 1 and were obtained
from fishmeal, cucumber, muskmelon, and a grapefruit juice can. Whether the many isolates from
grapevines have any connection to the quality of grapes as food was not investigated.
Studies of growth at 37 ◦ C revealed that many of the isolates in barcode types 1 and 2 could
survive 14 days at body temperature but could not grow. In each barcode type, at least one isolate was
seen that could grow minimally off the inoculum plug into the surrounding MEA during 14 days at
37 ◦ C. All three test isolates of barcode group 3 grew at least minimally at 37 ◦ C, and isolate 287.70O
from Egyptian soil grew 9 mm in diameter in 14 days.
The majority of the catenate-conidial isolates conforming to the prototype Acremonium egyptiacum
morphology belonged to barcode type 1, but one such isolate, CBS 545.89, transpired to belong to
barcode type 2. Perdomo et al. [4] reported that an isolate consistent with barcode type 3, UTHSC
05-1172, formed conidia in chains, but that isolate was subsequently lost, and no similar isolate has
been detected so far.
Alignments of the ITS and actin regions showed that ITS barcode types were minimally resolved,
although in the ITS dendrogram itself (Figure 2), the barcode type 2 isolates tended to cluster together,
and the barcode type 3 isolates made up a distinct branch. In the actin dendrogram (Figure 3), the
ITS barcode type 3 isolates again mostly clustered together on a unique branch, but there were two
anomalies. The branch containing the type 3 isolates also consistently contained, on a short side-branch,
CBS 734.69, an ITS type 1 strain with catenate conidiation isolated from tomato roots in Turkey. Also,
CBS 287.70O, an ITS type 3 isolate from Egyptian soil, did not cluster with other type 3 isolates in actin
analysis but instead clustered among the type 1 and 2 isolates.
Figures 2 and 3 also show that the genus Acremonium sensu stricto (s. str.), as represented by
its apparently rare type species, A. alternatum, and the common A. sclerotigenum/egyptiacum group,
is well demarcated from the most closely situated genus in ITS analysis, the recently described
Ovicillium, composed of isolates conforming to the outdated Verticillium sect. Albo-Erecta. Also
distinctly delimited is the cluster containing Stilbella s. str. and Emericellopsis (along with the closely
associated Stanjemonium, not shown). Other related genera, Geosmithia and Clonostachys, are too
distant to align reliably in the ITS analyses used here, and few compatible actin sequences exist for
related fungi.
 Microorganisms 2018, 6, x FOR PEER REVIEW 10 of 20

distinctly delimited is the cluster containing Stilbella s. str. and Emericellopsis (along with the closely
associated Stanjemonium, not shown). Other related genera, Geosmithia and Clonostachys, are too
distant to align
Microorganisms reliably
2018, 6, 88 in the ITS analyses used here, and few compatible actin sequences exist for
11 of 21
related fungi.

[Link]
Figure Phylogeneticdisposition
dispositionofofthe
theAcremonium
Acremoniumsclerotigenum/egyptiacum
sclerotigenum/egyptiacumcomplex
complexasasshown
shownby by
complete ribosomal internal transcribed spacer (ITS) sequences analysed using maximum
complete ribosomal internal transcribed spacer (ITS) sequences analysed using maximum likelihood likelihood
(ML)with
(ML) withRAxML
RAxMLVI-HPC.
[Link]
Supportvalues
valueswere
wereobtained
obtainedusing
usinga afast
fastbootstrap
bootstrapanalysis
analysisofof1000
1000
pseudoreplicates. Members of the Emericellopsis-Stilbella complex are used as an outgroup.
pseudoreplicates. Members of the Emericellopsis-Stilbella complex are used as an outgroup.
Microorganisms 2018, 6, 88 12 of 21
Microorganisms 2018, 6, x FOR PEER REVIEW 11 of 20

Figure
Figure 3. [Link]
Phylogeneticdisposition
disposition of
of the
the Acremonium
Acremonium sclerotigenum/egyptiacum
sclerotigenum/egyptiacum complex
complexas asshown
shownby
bya afragment
fragmentof of the
the actin
actin gene amplified using
gene amplified using the
theprimers
primersACT1
ACT1and
andACT4R,
ACT4R,andandanalysed
analysedusing
using
maximum
maximum likelihood
likelihood (ML)
(ML) with
with RAxML
RAxML VI-HPC.
VI-HPC. Support
Support values
values were
were obtained
obtained using
using a fast
a fast bootstrap
bootstrap
analysis
analysis ofof 1000
1000 pseudoreplicates.
pseudoreplicates. Acremonium
Acremonium spinosum,
spinosum, A.A. curvulum,
curvulum, and
and Emericellopsis
Emericellopsis glabra
glabra appear
appear
asas outgroups.
outgroups.
Microorganisms 2018, 6, 88 13 of 21

4. Discussion

4.1. Taxonomy and Nomenclature of the Acremonium sclerotigenum/egyptiacum Cluster

As Perdomo et al. [4] noted, there is a need to settle the matter of the correct naming of the
unexpectedly phenotypically diverse group of isolates encompassed in the A. sclerotigenum/egyptiacum
cluster. The balance of the Discussion will be most comprehensible if this matter is settled before other
matters are addressed.
We conclude that the ITS and actin sequences used do not support the naming of additional
species or infraspecific taxa in this group. Apparent contradictions between ITS and actin placements of
a few strains suggest that a sexual or hybridisation process may be shuffling markers within the isolates
studied and their conspecifics. Although this re-assortment might well indicate linkage disequilibrium
within a sexual species, the differences are small enough that chance alone may also be a factor.
Despite their morphological differences, the isolates ex-type of the original species names
Cephalosporium sclerotigenum Moreau and R. Moreau ex Valenta 1948 (validation of an invalid name
from 1941) and Oospora egyptiaca J.F.H. Beyma 1933 are very closely related, both belonging to ITS
barcode type 1. The earlier valid name, in its modern generic combination, is thus Acremonium
egyptiacum (J.F.H. Beyma) W. Gams. Both names are underutilised in the literature, because isolates
are so frequently misidentified as Sarocladium (Acremonium) strictum or A. alternatum, and there is
no eminent economic or cultural momentum that would argue for the junior name being formally
conserved against the senior.
The main outstanding question, then, is whether another of the names frequently found in
use for this group, Acremonium potronii Vuill. 1910, might be the true earliest name. Although the
isolate ex-type, illustrated by Vuillemin [22] and later in more detail by Pollacci and Nannizzi [23],
has not survived to be analysed genetically, the illustrations show a superficially plausible,
Acremonium sclerotigenum-like form with ellipsoidal to obovate conidia in mucoid heads (Figure 1D).
The isolation is from a medical case possibly involving systemic dissemination (see detailed synopsis
by Summerbell [24]). Very few Acremonium-like species are confirmed as causing such cases or growing
at 37 ◦ C, usually a prerequisite for human infection, but members of the A. sclerotigenum group have
been shown to do both. Close examination of Vuillemin’s illustrations and descriptions, however,
reveal that nearly all of the phialides he drew for A. potronii were adelophialides—that is, they lacked
a basal septum. Some of them were foreshortened to minute phialidic necks protruding laterally along
hyphae, while others were fully developed aculeate structures, frequently somewhat swollen between
the basal region and the mid-region. The drawings were of impeccable accuracy; Vuillemin, in the same
publication [22], coined and defined the term ‘phialide’ for the first time, giving diverse well-scrutinised
examples, and he specifically excluded the structures seen in A. potronii from that term because they
were not delimited from the subtending hypha [25]. Gams [5] accepted A. potronii as a name for
Acremonium types whose phialides all had basal septa, and he identified several A. sclerotigenum-group
isolates with this name (e.g., CBS 251.95), although none of the three A. potronii isolates illustrated
in his 1971 monograph is a member of this group. Based on current research findings, it appears
likely that A. potronii was a Phialemonium-, Phialemoniopsis-, or Coniochaeta-like fungus [26,27]. Its exact
identity is unclear, and we consider it a nomen dubium.
The correct name for the species studied by us, then, is Acremonium egyptiacum (J.F.H. Beyma)
W. Gams.

4.2. Ecology and Medical and Economic Significance of A. egyptiacum

As detailed by Summerbell and Scott [7], most published medical cases historically attributed to
“Acremonium strictum” turned out to be caused by A. egyptiacum in cases where sequence identification
or re-identification became available. Members of ITS barcode group 3 appear to be the most important,
causing, to begin with, two well-documented cases of disseminated infection in immunocompromised
patients, one attributed by Novicki et al. [20] to ‘Acremonium strictum genogroup 2’, and a more
Microorganisms 2018, 6, 88 14 of 21

recent case attributed by Guitard et al. [28] to ‘Acremonium sclerotigenum/egyptiacum’. Numerous

onychomycosis cases studied by Gupta et al. [21] also can now be attributed to this subclade [6], and
there are many isolates obtained from infected toenails in other regions (Tables 2 and 3), though not all
are repetition-confirmed as true etiologic agents [29]. This subclade is isolated so regularly from toenail
onychomycosis, mostly in the elderly, that it may be hypothesised to have developed an ongoing niche
as a communicable disease of the nails. If it were environmentally common, as are other nail infecting
non-dermatophyte fungi like Scopulariopsis brevicaulis, it could be interpreted as a regular invader of
nails from other environmental substrates; but, its relatively rare environmental isolation suggests
that it may instead be transmitted from person to person via transient environmental inoculum as
are dermatophytes. This would make its ecology comparable to that of Neoscytalidium dimidiatum,
which has wild-type subtypes that are seen both in woody plant infections and in human skin and
nail infections, as well as divergent subtypes, featuring slow growth or loss of melanisation, which are
only known from dermatological infections [30].
The presence of A. egyptiacum in the nails may become a systemic hazard if the patient becomes
immunocompromised: the case of blood-borne disseminated infection studied by Guitard et al. [28]
appeared to arise from a toenail with a prior A. egyptiacum infection.
A case of prosthetic mitral heart valve infestation documented by Guarro et al. [31] can now be
attributed to A. egyptiacum ITS barcode type 3, based on its sequence, in GenBank as AM990178.
The relative virulence of two ITS barcode type 3 isolates, UTHSC 01-194 and 05-2270,
both originally from blood, was studied in an immunocompromised mouse model by
Fernández-Silva et al. [32]. The isolates proved only to infect the immunosuppressed mice, but
not immunocompetent controls, and killed 70% of the susceptible animals within 16 days even when
low inoculum levels were used.
Barcode type 2 can be credited with a case of kidney dialysis-related peritonitis in a Greek
patient [19]. The isolate was kindly forwarded to CBS and is included in this study as CBS 112783.
Barcode type 1 isolates have been isolated from toenails, and there is an isolate, UTHSC 04-3176,
listed as derived from cerebrospinal fluid. This is a normally sterile bodily material, but even though
microorganisms are normally absent in it, medical significance cannot automatically be attributed
to common environmental fungi isolated from it. Process contamination, such as microscopic-scale
exposure of syringe needle interiors to contaminant fungal spores from room air or alcohol-swabbed
skin, cannot be entirely excluded in the making of clinical isolations from normally sterile bodily
materials. Confirmation of pathogenicity requires not just isolation alone, but also supportive case
information, such as pathology findings or repeated isolations. Thus, UTHSC 04-3176 is of uncertain
medical significance. The one well-confirmed case of clinical significance caused by an isolate of this
barcode type (specifically, CBS 100816) is an infection of a farm-produced ostrich egg investigated in
Italy because it failed to hatch [18].
A. egyptiacum, as seen in Tables 2 and 3, occurs regularly in many areas as an endophyte of
grapevines; one of us (R.C.S.) has identified many isolates from this habitat sent in to the CBS
identification service but not retained in the collection. The species was also found, as A. sclerotigenum,
to be a year-round endophyte of Quercus ilex in north-central Spain [33]. Barcode type 1 isolates, listed
as Acremonium sp., were obtained in Korea as an endophyte of the medicinal Chinese boxwood, Lycium
chinense [34]. A. egyptiacum was a moderately prevalent isolate from diseased or dead larvae of the
rose stem girdler beetle Agrilus aurichalcenus in the Kerman Province of south-eastern Iran [35]. Here,
the identifications were not stated as having been confirmed by sequencing, but a photograph shows
the recognisable pale greyish green of catenulate isolates of A. egyptiacum, and the authors were aware
of our as yet unpublished findings about this name. Most isolations from plants are of unknown
significance: for example, scattered isolations from the phylloplane of barley (CBS 114320; [36]) may
reflect growth in situ or sedimentation from air spora.
A phytopathogenic role for A. egyptiacum (as A. sclerotigenum) was documented by Li et al. [37],
who fulfilled Koch’s postulates after discovering the fungus caused a spot disease on bagged apples.
Microorganisms 2018, 6, 88 15 of 21

The sequences obtained were likely of barcode type 1, because CBS 384.65 (GenBank HQ232129) was
cited as the reference used in identification. Both a morph with mucoid heads and a morph with long
conidial chains were involved; they had identical sequences at three loci. This finding may connect
with the isolation of CBS 343.64 from lenticel of an apple tree.
Koch’s postulates were again fulfilled for A. egyptiacum as a causal agent of rose dieback in Iran’s
Fars province [38]. Both isolates sequenced in the study (GenBank KU532330, KU532331) conformed
to ITS barcode type 1 and had conidia in mucoid heads. Evidence of significant aerial transmission
of inoculum was obtained by spore trapping, possibly indicating that some chains were also formed
in situ.
Sequences obtained via denaturing gradient gel electrophoresis (DGGE) from the root zone of the
Scrophulariaceous medicinal plant Rehmannia glutinosa (‘sheng di huang’ approximately transcribes
the common-name 生地黄) in Henan Province, China, were compatible with ITS barcode type 1,
with a GenBank ITS sequence of A. sclerotigenum ex-type CBS 124.42 (HQ232209) cited as a reference
comparison [39]. The authors interpreted these sequences as indications of a potential pathogenic
contribution from A. egyptiacum (as A. sclerotigenum) in a toxic-soil replant problem with the plant.
The correction via sequencing of a long-standing misidentification of an A. egyptiacum barcode
type 1 isolate (GenBank LC063776) as Ascochyta viciae allowed this species (as A. sclerotigenum) to
be identified as the producer of the meroterpenoid compound ascofuranone, a cyanide-insensitive
alternative-oxidase inhibitor with proven efficacy against rodent infections of African trypanosomiasis
and cryptosporidiosis [40], as well as laboratory-demonstrated potential against microsporidia [41].
A. egyptiacum also produces the related compounds ascochlorin and ascofuranol [42]. Other industrial
explorations have shown that the species can affect some potentially useful transformations of
pharmaceutically produced steroids [43]. A recent study has stated that an A. egyptiacum (identified
as A. sclerotigenum) isolate obtained from Flabellia petiolata marine alga produces amyloidogenic
hydrophobin proteins that may be of interest in the manufacture of ‘green’ bio-coatings [44]. However, a
search in GenBank for sequences from this study yielded only accession KR014351 for strain MUT-4872;
this sequence matches a known undescribed species related to Acremonium hennebertii. It may have
BLASTed most closely to A. egyptiacum sequences.
Correctly identified marine isolates with ITS sequences 99% similar to those of CBS 114785,
the ex-type of A. egyptiacum, were cited from seawater near the Northern Antarctic Peninsula by
Gonçalves et al. [45]. Examination of the sequences showed they were of barcode type 3. “Acremonium
alternatum” isolates listed as having 99% similarity to GenBank record U57674.1, the ITS sequence
of CBS 223.70, were obtained from marine sediments associated with coal deposits [46]. The exact
sequences obtained were not deposited. A. egyptiacum barcode type 1 was found repeatedly in
petroleum-contaminated soils of the Khuzestan Province, southern Iran [47]. Note that GenBank
accession KY039283, the first of four sequences listed by these authors as A. sclerotigenum, is actually
diagnostic of an Emericellopsis species, with a characteristic ACAAAACTTT motif at the beginning of
the 5.8S rDNA.
Certain isolations, such as that of CBS 149.55 from a rust fungus lesion, raise the possibility
that A. egyptiacum may be a facultative mycoparasite. There is little evidence for this as yet, but
because closely related species, especially Ovicillium oosporum Zare and W. Gams, are well-established
fungicolous fungi, evidence of this role in A. egyptiacum should be watched for. Plant endophytism, for
example, may in some cases include or be based upon parasitism of other fungal endophytes.
It is likely that A. egyptiacum will be found to be one of the major Acremonium-like organisms
associated with food spoilage, if not the most important. The species’ association with multiple
plant and animal sources, and its ability to grow at relatively high temperatures, in combination
with its general morphological compatibility with Acremonium sp. contaminants described at the
genus level in food-related textbooks, makes this seem likely. There may be medical implications,
because the intestine can be a portal of entry for infection in severely immunocompromised patients.
A disseminated infection attributed to an untraceable “Acremonium strictum” isolate by Schell and
Microorganisms 2018, 6, 88 16 of 21

Perfect [48] appeared to start in the gut, thus probably originating from food. This isolate was probably
either A. egyptiacum or A. kiliense but was most likely the former, because the latter could generally be
distinguished easily in pre-molecular identification by the formation of chlamydospores, and also was
well known to produce distinctive melanoid pigment on Sabouraud agar. A. egyptiacum has elevated
heat tolerance: it is able to survive 90 ◦ C heat treatment for 50 min [49]. Its production of sclerotia
probably significantly increases its ability to survive under adverse conditions [38]. This sort of heat
tolerance may facilitate the contamination of heat-disinfected foods.
Recently, one of us (R.C.S.) curated the alignment of 170 A. egyptiacum sequences assembled in the
Plutof Biodiversity Platform ([Link] [50]. Many of these sequences were deposited
under incorrect names or as unknown sequences obtained in molecular community studies. Study
of the origins of these sequences, and tracking of any published material involved, could shed
considerable further light on the ecology of this fungal group. A preliminary survey of the first
few items listed yields variously identified barcode type 1 isolates in a wide range of substrata.
There are colonisers of Peniophora basidiomycetes in Texan attine ant nests (GenBank HQ607928;
sequence misidentified as Peniophora sp.), as well as endophytes of Bletilla ochracea (Chinese butterfly
orchid) (HM751796) and Atractylodes lancea (Asteraceae) (KC172079) in China. Other isolates are
from Taxus globosa bark in Mexico (JF773645), and from human nails in China (KT878342, KT878343).
Barcode 3 isolates appear as colonisers of human nail (KC254088, MITS56|KP132613) and blood
(KC254089|MITS52) in Greece. Others appear as endophytes of Gossypium in China (KF999020) and as
colonisers of marine macroalgae (HQ914912) and deep-sea materials (KM274118). Already, combined
with the results of Gonçalves et al. [45], mentioned above, a possible trend for barcode type 3 to be
isolated from marine materials can be perceived.

4.3. Broader Taxonomic Situation of the Genus Acremonium

The compilation of information on the biodiversity within A. egyptiacum shows that this organism’s
range of ecological, clinical, and economic roles epitomises most of the generalities assigned to the
genus Acremonium in general textbooks, such as the Introduction to Food- and Airborne Fungi [51]. Thus,
prior concepts of Acremonium as a genus are preserved in this phylogenetic nomenclature even though
the great majority of species historically given this genus name will be excised. There may be some
additional species related to A. sordidulum and A. brachypenium that will remain within Acremonium, but
the close phylogenetic proximity of a very different genus, Ovicillium, effectively barricades extension
of the name beyond the point where Acremonium and Ovicillium diverge. The next proximal major clade,
the Emericellopsis-Stanjemonium-Stilbella one, now incorporates a venerable (1900) and famous genus
name, Stilbella, and potentially unites this generic name with several heretofore excluded organisms
forming synnemata, such as Emericellopsis salmosynnemata and E. synnematicola.
Most of the groups currently containing Acremonium names are in clades that need revision to
clarify their unity and extension. There are, however, two highly distinct and isolated genus-level
clades, as shown by Summerbell et al. [3], that could be rescued immediately from anachronistic
nomenclature. The highly distinct nature of these groups extends to the possession of variant forms of
the usual AAACTTT motif that begins the 5.8 ribosomal DNA segment throughout the filamentous
Ascomycota in fungi ranging from Acremonium egyptiacum to Fusarium, Chaetomium, Aspergillus, and
Ochroconis. The Acremonium radiatum clade has CAACTTT, while the Acremonium curvulum clade has
AAACCTT. These groups are sufficiently distinct that their ITS sequences cannot be meaningfully
aligned with those of other groups. Their current taxonomic situation has been determined via the
18S ribosomal and 28S LSU sequences published previously [3], after updating showed no recently
deposited sequences have altered their positions of isolation. Both groups require revision to deal with
undescribed species in their midst, but we believe that a good beginning would be to focus interest on
these orphaned Acremonium clades by giving them working generic names.
Microorganisms 2018, 6, 88 17 of 21

A. Parasarocladium Summerbell, Scott, Guarro, and Crous, gen. nov. (MYCOBANK 826815).
Etymology: name derived from ancient Greek παρά (beside, juxtaposed to) and the genus name
Sarocladium.
Type species: Parasarocladium radiatum (Sukap. and Thirum.) Summerbell, Scott, Guarro,
and Crous.
Ascomatal morph not observed. Mycelium consisting of hyaline, septate, branched hyphae.
Colonies smooth to thinly floccose, with salmonaceous, orange, yellow, or greenish-black reverse
colouration. Conidiophores arising laterally from somatic hyphae, erect, cylindrical to subcylindrical,
unbranched or less commonly branched, aseptate or septate, smooth, hyaline. Conidiogenous cells
phialidic, arising laterally from hyphae or in terminal pairs, or verticils of three, or small monopodially
branched tufts of up to four from conidiophores, monophialidic, hyaline, smooth, mostly aseptate but
up to two-septate, elongate-ampulliform to subcylindrical, with inconspicuous collarettes. Conidia
aseptate, smooth-walled or with chromophilic roughening, ellipsoidal, ovate, bacilliform or fusiform,
sometimes slightly curved, forming slimy heads on the phialides. Chlamydospores absent but hyphal
swellings may be present. Characteristic CAACTTT motif at 50 end of 5.8S rDNA.
1. Parasarocladium radiatum (Sukap. and Thirum.) Summerbell, Scott, Guarro, and Crous, comb. et
stat. nov., MYCOBANK 826816.
Basionym: Cephalosporium acremonium Corda var. radiatum Sukapure and Thirum. in Sydowia 19:
172 (1966).
Acremonium radiatum (Sukap. and Thirum.) W. Gams, Cephalosporium-artige Schimmelpilze:
125 (1971).
Type: CBS 142.62, ITS accession MH424699.
2. Parasarocladium breve (W. Gams) Summerbell, Scott, Guarro, and Crous, comb. et stat. nov.,
MYCOBANK 826817.
Basionym: Cephalosporium roseum var. breve Sukap. and Thirum. in Sydowia 19: 174, 1966.
≡ Acremonium breve W. Gams, Cephalosporium-artige Schimmelpilze: 60 (1971).
Type: CBS 150.62, ITS accession MH424706.
3. Parasarocladium gamsii (Tichelaar) Summerbell, Scott, Guarro, and Crous, comb. nov.
MYCOBANK MB 826818.
Basionym: Acremonium gamsii Tichelaar, Acta Botanica Neerlandica 21: 197 (1972).
Type: CBS 726.71, ITS accession MH424707.
Known members of this genus have been almost exclusively isolated from soil or from possible
conidial dispersal media such as air. B. Kiflimonium Summerbell, Scott, Guarro, and Crous, gen. nov.,
MYCOBANK 826819.
Etymology: Named for the resemblance of the curved shapes of the conidia to crescent-shaped
pastries known in many areas by the originally Hungarian name kifli (singular noun form), which is
adopted as English in some extended dictionaries such as [Link]; also known by the cognate
Serbian, Bosnian, Macedonian, and Bulgarian name kifla and the Austrian kipfel. (The basic Latin
and Greek roots for ‘curved,’ ‘crescent-shaped,’and so forth, are overused in other fungal names, and
members of this group of simply structured organisms share no distinctive visible feature other than
their curved conidia). -Monium, meaning ‘little singularity,’ derives from Acremonium.
Type species: Kiflimonium curvulum (W. Gams) Summerbell, Scott, Guarro, and Crous.
Ascomatal morph not observed. Mycelium consisting of hyaline, septate, branched hyphae.
Colonies pale to yellow-orange, sometimes producing brown reverse pigments. Conidiophores
mostly short side branches arising laterally from somatic hyphae, subcylindrical, unbranched, or
branched and bearing mostly 1–4 conidiogenous cells, smooth, hyaline. Conidiogenous cells phialidic,
arising laterally and singly from hyphae or on conidiophores in subverticillate clusters of mostly 2–4,
mostly monophialidic, hyaline, smooth, generally aseptate, elongate-subcylindrical to aciculate, gently
Microorganisms 2018, 6, 88 18 of 21

tapered, with inconspicuous collarettes; short, adelophialidic side-branches may be present. Conidia
0–1 septate, smooth-walled, lunate to falcate with rounded or acute ends, or in some cases ellipsoidal;
in all cases, forming slimy heads on the phialides. Chlamydospores absent. Characteristic AAACCTT
motif at 50 end of 5.8S rDNA.
1. Kiflimonium curvulum (W. Gams) Summerbell, Scott, Guarro, and Crous, comb. nov.
MYCOBANK MB 826820
Basionym: Acremonium curvulum W. Gams, Cephalosporium-artige Schimmelpilze: 57, 1971.
No Kiflimonium isolate studied so far has been found to grow at 37 ◦ C. Some of the features in the
generic description are only known from as yet undescribed organisms stored at CBS.
Members of this genus are mostly isolated from soil; CBS 214.70, distinct by possessing many
septate conidia [5], was isolated from rust-infected Lolium ryegrass. Isolates accepted as K. curvulum ss.
str. include (with ITS sequence accessions as substantiation) CBS 430.66 (ex-type; MH424698), CBS
229.75 (MH424700), CBS 101442 (MH424701), CBS 333.92 (MH424702), CBS 898.85 (MH424703), CBS
384.70A (MH424704), and CBS 761.69 (MH424705).
There are at least 10 other major clades of Acremonium species that will require new generic
names or will need to be recombined into genera originally erected for ascomatal species or for
‘charismatic apomorphs’ (i.e., groups drawing attention with distinctive, evolutionarily derived
conidiophore types [3]—cf. Ovicillium, Stilbella, Trichothecium, Sarocladium). Species that will be
affected by name changes include some very recently described taxa, such as Acremonium asperulatum
and A. variecolor [52], which may belong to Bulbithecium or an as yet unnamed neighbour-genus,
and A. pilosum, A. parvum, and A. citrinum, which are situated in the phylogenetically isolated
Acremonium fusidioides clade [53]. We would encourage authors not to hesitate to give simply structured,
phylogenetically distinct organisms generic names; hesitation to await discovery of distinctive phenetic
features would be an error in scientific strategy. The ecological and biochemical significance of the
phylogenetically unified, morphologically flexible concept of Acremonium egyptiacum illustrates an
important reality: the impact of Acremonium-like taxa can only be obscured if biosystematists place too
great a focus on morphological delimitation.

Author Contributions: Conceptualisation, R.C.S., J.G. (Josep Guarro), J.F.C.-L., and C.G.; Methodology, R.C.S.,
J.G. (Josep Guarro), J.F.C.-L., and C.G.; Software, C.G., J.F.C.-L., R.C.S., and J.G. (Josepa Gené); Validation, R.C.S.,
J.G. (Josep Guarro), J.F.C.-L., and C.G.; Formal Analysis, C.G.; Investigation R.C.S., C.G., J.G. (Josep Guarro), A.E.,
A.K.G., J.G. (Josepa Gené), J.F.C.-L., A.v.I., M.S., and J.A.S.; Resources, P.W.C., J.G. (Josep Guarro), A.K.G., C.G., and
A.E.; Data Curation, R.C.S., C.G., and J.F.C.-L.; Original Draft Preparation, R.C.S., C.G., J.F.C.-L., and J.A.S.; Review
and Editing of Manuscript, R.C.S., C.G., J.G. (Josep Guarro), J.F.C.-L., J.A.S., and P.W.C.; Visualisation, R.C.S., C.G.,
and J.A.S.; Supervision, R.C.S., J.G. (Josep Guarro), J.G. (Josepa Gené), and J.F.C.-L.; Project Administration, R.C.S.
J.A.S., J.G. (Josep Guarro), J.F.C.-L., J.G. (Josepa Gené), A.K.G., A.E., and C.G.; Funding Acquisition, R.C.S., J.G.
(Josep Guarro), C.G., J.A.S., A.K.G., and P.W.C.
Funding: This project of 18-years duration was funded by many pockets. The Dutch component was mostly from
the core budget of the Westerdijk Institute. The Spanish component was partly from the Spanish Ministerio de
Educación y Ciencia, notably grants CGL 2009-08698/BOS and CGL 2008-04226/BOS. In Canada, A.K. Gupta
provided funding from Mediprobe Laboratories, and J.A. Scott provided funding from Sporometrics. In Australia,
the Australian National Herbarium supported C. Gueidan.
Acknowledgments: The late Walter Gams provided immensely valuable consultation. The Collection staff of
the Westerdijk Institute also played an invaluable role, as did Saleh Albreish and his staff at OMH. The late
Deanna Sutton and her colleagues at the University of Texas Health Science Center sent many isolates from
medical sources that were re-used in this project. Administratively, the late Dirk van der Mei was the key sponsor
of this study’s beginning, and he, along with the other departed crew of this deceptively colossal enterprise,
is remembered with great affection.
Conflicts of Interest: The authors declare no conflicts of interest.

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