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Antonie van Leeuwenhoek 83: 351–360, 2003.
351
2003 Kluwer Academic Publishers. Printed in the Netherlands.
A new meristematic fungus, Pseudotaeniolina globosa
1 1 2,3,
*
`
F. De Leo , C. Urzı and G.S. de Hoog
1
`
Dipartimento di Scienze Microbiologiche
,
Genetiche e Molecolari
,
Universita di Messina
,
Salita Sperone
2
31,
I-
98166
Messina
,
Italy
;
Centraalbureau voor Schimmelcultures
,
P
.
O
.
Box
85167,
NL-
3508
AD Utrecht
,
3
The Netherlands
;
Institute for Biodiversity and Ecosystem Dynamics
,
University of Amsterdam
,
Kruislaan
*
318,
NL-
1098
SM Amsterdam
,
The Netherlands
;
Author for correspondence
Received 10 July 2002; accepted in revised form 21 October 2002
Key words
:
Black yeasts, Coniosporium, Epiphyte, MCF, Meristematic fungi, Rock-inhabiting fungi, Taxonomy,
Trimmatostroma
Abstract
A new species of Pseudotaeniolina, a genus of anamorphic, melanized fungi with meristematic development, is
described. The species is compared to morphologically similar taxa among which are Trimmatostroma and
Coniosporium. Its novelty is supported by SSU (small subunit) and ITS (internal transcribed spacer) rDNA
sequence data.
Introduction sumoto et al. 1984). Meristematic growth seems to be
suitable for divergent types of environmental stress
Meristematic fungi are characterized by isodiametric including those encountered during the infection of
cell wall expansion concomitant with ongoing cyto- warm-blooded animals.
kinesis and arbitrarily oriented septation (Zalar et al. About 25 genera of melanized meristematic, sur-
1999a). Additional polarized growth featuring hyphae face-inhabiting fungi have been described. Many of
or budding cells may or may not be present. Bipolar them have few distinctive morphological features, but
growth is occasionally observed (Butin et al. 1996). others exhibit striking features when observed on the
Most species grow slowly, have very thick cell walls natural substrate. Some show a bewildering phenetic
and are densely melanized. The fungi are often found polymorphism (Figueras et al. 1996; Yoshida et al.
as epilithic or epiphytic saprobes on exposed surfaces 1996). Over the last decades, several genera of epi-
such as desert rock, outdoor statues or leathery plant endolithic fungi have been revealed on and in native
leaves; or they may thrive in Antarctic rock or in rock (Staley et al. 1982) and stone monuments, espe-
hypersaline coastal ponds. Melanization and meri- cially in the Mediterranean Basin (Sterflinger et al.
``
stematic growth are therefore regarded to render the 1999; Urzı and Realini 1998; Urzı et al. 2000). These
fungus’ phenotype suitable for survival under extreme species entirely lack structures enabling identification.
conditions, including low and high temperatures, low In situ on rock they mostly consist of extremely small
water activity and intense solar irradiation (Sterflinger clumps of black cells and have therefore been referred
1998). In the Chaetothyrialean species Cla- to as microcolonial fungi (MCF; Staley et al. 1982).
dophialophora carrionii (Trejos) de Hoog et al., a In culture some are preponderantly single-celled and
meristematic ecotype that occurs inside dry cactus have been classified in Sarcinomyces (Wollenzien et
spines (Zeppenfeldt et al. 1994) is also produced al. 1997), while others produce muriform cells and are
when the fungus is traumatically inoculated into assigned to Trimmatostroma (Zalar et al. 1999b) if
human tissue. This tissue form, known as the they produce branched conidial chains, or to Conios-
muriform cell, is the characteristic hallmark of a porium (Sterflinger et al. 1997; De Leo et al. 1999) if
distinctive skin disease, chromoblastomycosis (Mat- they produce unbranched chains (Ellis 1971, 1976). A
352
superficially similar, monotypic genus, Pseudo- Morphology
taeniolina, has been introduced by Crane and Schok-
necht (1986) for species from plant material. In these Cell-morphology was studied using light and phase-
species, meristematic development is followed by contrast microscopy. Daily growth rates and morphol-
arthric secession leading preponderantly to the forma- ogy of colonies were recorded on PDA, 2% Malt
tion of single cells. Extract Agar (MEA, Oxoid), Oatmeal Agar (OA), and
Only very few species of MCF have as yet been Czapek Dox Agar (CzA, Oxoid) in culture plates
cultured. Judging from ribosomal sequence data, the incubated at 25 8C. Hyphal maturation and
MCF are polyphyletic, being anamorphs of conidiogenesis were studied in slide cultures on
Chaetothyriales and Dothideales (Ascomycetes) MEA; slides were mounted in lactophenol with or
(Sterflinger et al. 1997). Currently available ribosom- without cotton blue.
al sequences have revealed that this subdivision does
not correspond with morphological generic cir-
cumscriptions. Facing the lack of congruity between Molecular biology
morphology and phylogeny, we have chosen in the
present article to take broad phylogenetic lines into DNA isolation. DNA extraction was done according
consideration, but to refrain from introducing a new to Gerrits van den Ende and De Hoog (1999). In brief,
2
taxonomic system for the meristematic fungi. For about 1 cm mycelium of 30-day-old cultures was
Pseudotaeniolina, neither cultures nor sequence data ground and extracted in 200 ml CTAB (cetyltri-
are available. The aims of this study are to describe a methylammonium bromide) buffer with 500 ml chlo-
new species of Pseudotaeniolina on the basis of roform. DNA was precipitated in 96% ethanol at
phenetic and genetic data and to compare this entity 220 8C. The pellet was washed with cold 70% etha-
with existing meristematic taxa. nol. After drying at room temperature, DNA was
resuspended in 97.5 ml TE-buffer with 2.5 ml RNAse
21
(20 U ml ) and incubated for 5 min at 37 8C.
Material and methods DNA amplification. The internal transcribed spacer
(ITS) rDNA was sequenced for each strain; the small
Strains subunit (SSU) was sequenced for one strain of each
species recognized. PCR was performed in 100 ml
Strain MC 769 was isolated from a sandstone sample volumes of a reaction mixture containing 60 ml dis-
taken from the outside wall of the church of ‘‘Santa tilled water, 10 ml PCR buffer, 20 ml N-buffer, 2 mlof
Maria di Mili’’ (Mili San Pietro, Messina, Italy; Plate each primer, 2 ml Amplitherm DNA polymerase and 4
1). The surface of the stone was characterized by the ml fungal DNA. Primers NS1, NS24, Oli1, Oli5, Oli9,
presence of green patina attributed to the growth of Oli10, BF951, BF963, Oli2, Oli3, Oli13, Oli14, BF
green chlorococcal algae associated with a few 1419, BF 1438, Oli15, V9G, ITS1, ITS4, ITS5 and
sporogenous bacteria and numerous black fungi. Sam- LS266 (De Hoog et al. 2000) were employed. Forty
ples were processed according to recommendations of amplification cycles were performed: 94 8C, 30 s;
the Italian Normal Commission (Commissione Nor- 58 8C, 1 min; 72 8C, 30 s, with initial and terminal
mal 1990). The rock sample was powdered in a delay of 1 min in a Biomed thermocycler (type 60).
mortar and suspended (1:10) in saline with 0.001% Alignment and tree reconstruction. Sequences were
Tween 80 and stirred continuously for 1 h. One ml- adjusted using Seqman II of Lasergene software
volumes of suspension were inoculated in duplicate (DNAStar, Madison, U.S.A.). ITS sequences were
on Dichloran Rose Bengal Chloramphenicol agar aligned in BioNumerics v. 2.5 (Applied Maths, Kor-
`
(DRBC; King et al. 1979; Urzı et al. 1992) and trijk, Belgium) and 18S sequences with DCSE (De
incubated at 28 8C for one month. Colonies were Rijk and De Wachter 1993). Trees were reconstructed
transferred to culture plates with Potato Dextrose using the TREECON software package (Van de Peer
Agar (PDA, Oxoid) and incubated at 25 8C for one and De Wachter 1994) using the neighbor-joining
month. Strains for comparison were selected on the algorithm with Kimura-2 correction with 100 boot-
basis of morphological and sequence similarities. strap replications and were verified with parsimony in
Strains are listed in Table 1. BioNumerics.
353
Plate
1.
A) View of the church of Santa Maria di Mili (Mili San Pietro, Messina Italy). B) Sandstone sample (11b) from the outside wall of the
church from which strain MC 769 was isolated. Algal colonization is visible on the surface. C) Small black colonies isolated from sample 11b
growing on DRBC agar after 20 days of incubation at 28 8C.
Results further analysis. A Dothideales-biased neighbor-join-
ing tree based on 45 near-complete SSU rDNA se-
The near-complete SSU sequence of strain MC 769 quences and, as an outgroup, Capronia villosa
was compared with 115 sequences of black yeasts and Samuels (Chaetothyriales) is presented in Figure 1.
relatives of the ascomycete orders Chaetothyriales Strain MC 769 clustered amidst a group of meri-
and Dothideales present at CBS (data not shown); stematic species. The nearest teleomorph species was
nearest neighbours were verified in the public domain Coccodinium bartschii Massal. (Coccodiniaceae,
using BLASTn. Most of the Chaetothyriales proved Dothideales). Trimmatostroma salinum Zalar et al.
only distantly related and were therefore omitted from was found at considerable distance (Figure 1), close
354
Table
1.
List of strains studied.
Strain number GenBank Species name Source Geography
CBS 116.90 (5ATCC 526815UAMH 5389) AJ238471 Hortaea werneckii Fish, eye Italy
CBS 373.92 AJ238474 Hortaea werneckii Soil, beach Gran Canaria
CBS 107.67NT AJ238468 Hortaea werneckii Man, tinea nigra Portugal
CBS 111.31 AJ238679 Hortaea werneckii Man, tinea nigra Brazil
CBS 359.66 AJ244249 Hortaea werneckii Man, tinea nigra Surinam
CBS 117.90 (5UAMH 4978) AJ238472 Hortaea werneckii Salted fish Brazil
MZKI B-987 Hortaea werneckii Hypersaline water Spain
CBS 122.32 AJ238473 Hortaea werneckii Man, tinea nigra –
CBS 115.90 (5UAMH 4985) AJ238470 Hortaea werneckii Frog, kidney Brazil
CBS 100496 AY128703 Hortaea werneckii Seawater-sprayed marble Greece
CBS 100455 (5MZKI B-675) AY128704 Hortaea werneckii Coral, seawater Croatia
CBS 110353 (5DH 12843 5VPCI 176) Hortaea werneckii Hollow tree Sudan
DH 12719 (5Onofri 976-21a) Trimmatostroma sp. Sandstone Antarctica
CBS 109863 (5MC 662) AY128701 Mycocalicium victoriae Soil Italy
CBS 109862 (5MC 633) AY128702 Mycocalicium victoriae Soil Italy
Sterflinger NH7-7 AJ312123 Mycocalicium victoriae Limestone Austria
CBS 214.90T AJ244238 Capnobotryella renispora Capnobotrys neesii, subiculum Japan
CBS 618.84 AY128696 Trimmatostroma abietis Ilex sp. –
CBS 290.90 AY128698 Trimmatostroma abietis Man –
CBS 459.93 Trimmatostroma abietis Abies sp. Germany
CBS 300.81 AY128697 Trimmatostroma abietis Juniperus communis, needle Switzerland
CBS 145.97 AY128699 Trimmatostroma abietis Sandstone Germany
CBS 109889T (5MC 769) AY128700 Pseudotaeniolina globosa Rock Italy
CBS 303.84 AJ244268 Pseudotaeniolina globosa Wood –
CBS 110352 (5DH 12840) Pseudotaeniolina globosa Human aorta at autopsy Germany
CBS 486.80 AF362066 Stenella araguata Paepalanthus columbianus, dead leaf Colombia
MZKI B-994 AJ238677 Phaeotheca triangularis Hypersaline water Spain
MZKI B-950 AJ238674 Phaeotheca triangularis Hypersaline water Slovenia
CBS 471.90T AJ244256 Phaeotheca triangularis Humidifier Belgium
MZKI B-810 AJ238673 Phaeotheca triangularis Hypersaline water Slovenia
CBS 100458 (5MZKI B-733) AJ238671 Phaeotheca triangularis Hypersaline water Slovenia
AF291707 Cercospora sorghi Sorghum bicolor –
AF291708 Cercospora kikuchii Glycine max –
AF291709 Cercospora zeae-maydis Zea mays –
AF222827 Cercospora beticola ––
CBS 544.71 Cercospora dulcamarae Solanum dulcamara Romania
CBS 119.25 AF163085 Cercospora apii Apium graveolens Romania
AF385611 Coniothyrium zuluense Eucalyptus sp. Mexico
Abbreviations used: ATCC 5 American Type Culture Collection, Manassas, VA, U.S.A.; CBS 5 Centraalbureau voor Schimmelcultures,
Utrecht, The Netherlands; DH 5 G.S. de Hoog private collection; MC 5 Collection of Istituto di Microbiologia, Messina, Italy; MZKI 5
Microbiological Culture Collection, National Institute of Chemistry, Ljubljana, Slovenia; UAMH 5 University of Alberta Microfungus
Herbarium and Collection, Edmonton, AB, Canada; VPCI 5 Vallabhbhai Patel Chest Institute, Delhi, India. NT 5 ex-neotype strain; T 5
ex-type strain.
to Capnodium and Scorias (Capnodiaceae, strains were found to share a main clade with Tri-
Dothideales) (based on partial sequences; data not mmatostroma abietis Butin et al., which showed
shown). In general the Dothideales proved to be infraspecific heterogeneity (Figure 2). A strain iden-
heterogeneous, most branches being unresolved. tified as T
.
salicis Corda, CBS 300.81, clustered
Results of sequencing of the ITS rDNA domain are amidst T
.
abietis strains. This strain was isolated from
presented in Figure 2. Strains MC 769, CBS 303.84 Juniperus (Table 1), and as T
.
abietis is particularly
and dH 12840 were found to be nearly identical. They found on conifers it is likely that a misidentification
were clearly separate from the remaining fungi, form- for that species was concerned. The group was
ing a distinct entity at high bootstrap support. The paraphyletic to Stenella araguata Syd., CBS 486.80.
355
Figure
1.
Consensus tree of 45 members of black yeasts and relatives with accent on Dothideales, constructed with the neighbor-joining
algorithm in the TREECON package with Kimura (2) correction and 100 bootstrap replicates (values . 90 are shown with the branches).
Families to which teleomorphs are assigned are listed at the right hand side; species not classified in the Dothideales are in brackets. The new
species is indicated with an arrow. Capronia villosa, CBS 616.96 is taken as outgroup.
Alignment with species such as Mycocalicium vic- Hortaea werneckii (Horta) Nishimura and Miyaji and
toriae (C. Knight ex F. Wilson) Tibell (Caliciales; some Cercospora species was ambiguous in parts of
Tibell 1987), Capnobotryella renispora Sugiyama, the ITS1 and 2 domains.
356
`
Pseudotaeniolina globosa De Leo
,
Urzı and De Conidia terminalia, meristematica, 1–2 3 0–1 sep-
Hoog
,
sp
.
nov
.
– Plate
2
tata, 12–20 mm. Typus: MC 769.
Coloniae nigrae, butyreae, 28 diebus 25 mm diametro.
Mycelium immersum, ramosum, torulosum, Cultural characteristics at
25 8
C
olivaceum, ex cellulis 6–7 3 8–15 mm compositum. Colonies on MEA black and glistening, buttery, flat,
Figure
2.
Consensus tree of 35 strains of meristematic melanized fungi with accent on species potentially growing in environments with low
water activity, constructed with the neighbor-joining algorithm in the TREECON package with Kimura (2) correction and 100 bootstrap
replicates (values . 90 are shown with the branches). Capnobotryella renispora, CBS 214.90 is taken as outgroup.
357
slightly raised at the centre, radially folded, attaining The species fits the genus Pseudotaeniolina. Pseu-
up to 25 mm diam in 4 weeks. Aerial mycelium dotaeniolina convolvuli (Esfandiari) Crane and
absent. Stroma and setae absent. Colonies on OA flat, Schoknecht is the only species known to date in this
with sharp, regular margin, attaining up to 21 mm genus (Crane and Schoknecht 1986). P
.
globosa, like
diam in 4 weeks. Colonies on CzA flat, with fimbriate P
.
convolvuli, develops series of arthric, mostly one-
margin, attaining up to 10 mm diam in 4 weeks. celled conidia from meristematically ripening hyphae.
Colonies on PDA flat, with regular margin, slightly The liberated conidia finally swell and take on a
raised at the centre, cerebriform, radially folded, yeast-like appearance. Occasionally the spherical
attaining up to 28 mm diam in 4 weeks. cells of P
.
convolvuli have asymmetrical septation, as
observed in P
.
globosa. P
.
globosa has larger, more
coarsely ornamented cells, and it frequently sheds
parts of the outer cell wall. This phenomenon is also
Description based on cultures grown on MEA at
known in Phaeotheca triangularis De Hoog and
25 8
C
Beguin (Zalar et al. 1999a), but the ITS domain of this
Mycelium initially consisting of regular, dark olivace-
species was aligned to that of P
.
globosa with difficul-
ous hyphae, moderately thick- and smooth-walled;
ty (Figure 2), as holds true for other Phaeotheca and
hyphal cells 8–15 mm long and 6–7 mm wide. Termi-
also Hyphospora species (De Hoog et al. 1999). P
.
nal and lateral, holoblastic budding cells are frequent-
convolvuli was described from rotten stems of Con-
ly produced in cultures older than 2 weeks. Some-
volvulus.
times terminal conidia, 10–12 mm diam are observed,
Classification of meristematic anamorphs is proble-
these are (sub)spherical and one-celled when young,
matic because of their mostly poorly developed but
later becoming septate up to muriform with 1(22)
highly variable morphology. Our species grows with
septa, 12–20 mm diam. Mature hyphae fall apart into
pale olivaceous, branched hyphae which gradually
separate cells. Older cells at the centre of the colony
convert into clumps of cells by isodiametric inflation
swell and may become transversely septate, septa
of intercalary and terminal cells. This is observed in
often being asymmetrical and cleaving the original
many genera of meristematic fungi. Only the sub-
cell into a large cell and a very small cell which
sequent disarticulation into preponderantly one-celled
occasionally has 1(22) septa. The cells or cell clumps
conidia is characteristic for Pseudotaeniolina. A large
are thick-walled, spherical, 7–17 mm in diam, smoot-
number of meristematic species have been described
h-walled, verrucose or coarsely punctate; frequently
on the basis of morphology alone (Ellis 1971, 1976).
local parts of the outer mother cell wall is shed off.
None of these have single cells or aymmetrically
Yeast cells absent. Teleomorph unknown.
septate cells as a final product of conidiogenesis, so in
Type strain (living and dried): MC 769, ex sand-
this respect P
.
globosa is unique. Taeniolella is also
stone of outside wall of the church of ‘‘Santa Maria di
distinctive: while it forms mostly unbranched cells
Mili’’ (Mili San Pietro, Messina, Italy).
similar to those of Pseudotaeniolella, it also shows
terminal, holoblastic elongation of chains.
Ellis (1971, 1976) regarded the combination of
branched chains of meristematically developing,
Discussion muriform conidia as diagnostic for the genus Tri-
mmatostroma, while Coniosporium had unbranched
Pseudotaeniolina globosa is characterized by melan- chains. Taeniolella had conidia only with transverse
ized hyphae that are converted rapidly into chains of septa. Only a limited number of meristematic taxa and
spherical cells which after liberation frequently are sooty moulds have thus far been investigated in SSU
asymmetrically one-septate (Plate 2). The cells often rDNA sequence studies (Sterflinger et al. 1997;
aggregate in dense clumps. The exact moment of Reynolds 1998), and thus the mono- or polyphyly of
transition is difficult to follow. Strain DH 12840 genera like Trimmatostroma
,
Coniosporium or
remained sterile on MEA, showing densely parallel Taeniolella can as yet not be specified.
hyphae consisting of short cells. Large multicellular Micromorphologically P
.
globosa is similar to Sar-
bodies were observed locally on the colony surface; cinomyces petricola Wollenzien and De Hoog (Wol-
these possibly represented abortive fruit bodies. On lenzien et al. 1997), but the cultures of P
.
globosa are
PCA the same strain rapidly converted to spherical slimy and yeast-like after 4–5 d growth, while those
clumps of cells. of S
.
petricola are dry. In addition, the ITS domains of
358
Plate
2.
A) Colonies of P
.
globosa, MC 769, after one month incubation. Media tested: 1. MEA; 2. OA; 3. PDA; 4. CzA. B–F) Slide culture on
MEA. B and C) Hyphal structure. E) Mature hyphae. D and F) Mature spheerical conidia. Bars represent 10 mm in all micrographs.
359
the two species differed strongly and could be aligned Acknowledgements
only with difficulty. Judging from ribosomal sequence
data, S
.
petricola is closer to the Chaetothyriales than K.F. Luijsterburg is thanked for technical assistance.
to Dothideales (data not shown). The same holds true This work was carried out with the financial contribu-
for the stone-inhabiting Coniosporium species tion of the European Community through the Re-
Coniosporium perforans Sterflinger, C
.
apollinis search Project CATS (project nr. EVK4-CT-2000-
Sterflinger (Sterflinger et al. 1997) and C
.
uncinatum 00028) and the Network COALITION (project nr.
De Leo et al. (De Leo et al. 1999). C
.
uncinatum is EVK4-1999-20001), the Italian C.N.R. (project Nr.
morphologically unique in having curved hyphal 01.00654.PF36) and P.R.A. (Progetti ordinari e
ends. The similarly rock-inhabiting C
.
aeroalgicola giovani ricercatori).
Turian (Turian 1977) is not known to have been
preserved; its conidia were multicellular. Sar-
cinomyces crustaceus Lindner forms conidial packets
References
with longitudinal and transverse septation (Sigler et
al. 1981) and, judging from rDNA sequence data, is
Butin H., Pehl L., De Hoog G.S. and Wollenzien U. 1996. Trim-
remote from Trimmatostroma-like fungi. matostroma abietis sp. nov. (hyphomycetes) and related species.
A. van Leeuw. J. Microb. 69: 203–209.
Phylogenetically, the taxa related to P
.
globosa are
Commissione Normal 1990. Raccomandazioni Normal: 9 /88 Mi-
in the Dothideales (Figure 1), but most branches
croflora autotrofa ed eterotrofa: tecniche di isolamento in coltura.
within this order are poorly supported. In the ITS
C.N.R. - I.C.R, Roma.
comparison (Figure 2) of taxa with substantial se-
Crane J.L. and Schoknecht J.D. 1986. Revision of Torula and
quence similarity to P
.
globosa, we note that the Hormiscium species, new names for Hormiscium undulatum
,
Torula equina, and Torula convolvuli. Mycologia 78: 86–91.
results reflect an ecological commonality. Most
´
De Hoog G.S., Guarro J., Gene J. and Figueras M.J. 2000. Atlas of
species clustering with P
.
globosa are associated with
Clinical Fungi. 2nd edn. Centraalbureau voor
low water activity, being either epilithic, epiphytic or
Schimmelcultures / Universitat Rovira i Virgili, Utrecht / Reus,
halophilic. Trimmatostroma abietis, the Trimmatos-
1126 pp.
`
troma species with an ITS sequence closest to that of De Hoog G.S., Zalar P., Urzı C., De Leo F., Yurlova N.A. and
Sterflinger K. 1999. Relationships of dothideaceous black yeasts
P
.
globosa, is an epiphyte on leathery plant leaves and
and meristematic fungi based on 5.8S and ITS2 rDNA sequence
is occasionally seen on inert surfaces such as rock
comparison. Stud. Mycol. 43: 31–37.
(Butin et al. 1996). The ITS domain of T
.
salinum,a
`
De Leo F., Urzı C. and De Hoog G.S. 1999. Two Coniosporium
species inhabiting hypersaline environments (Zalar et
species from rock surfaces. Stud. Mycol. 43: 70–79.
al. 1999b) could not be aligned with confidence to any De Rijk P. and De Wachter R. 1993. DCSE, an interactive tool for
sequence alignment and secondary structure research. Comput.
of these species (data not shown). It has muriform
Appl. Biosci. 9: 735–740.
rather than one-celled mature conidia. Surprisingly,
Ellis M.B. 1971. Dematiaceous Hyphomycetes. Commonwealth
one of the strains of P
.
globosa was isolated from an
Mycological Institute, Kew, 608 pp.
aorta of a deceased human patient in which fungal
Ellis M.B. 1976. More Dematiaceous Hyphomycetes. Common-
growth was not observed in vivo (O. Kurzai, pers. wealth Mycological Institute, Kew, 507 pp.
Figueras M.J., De Hoog G.S., Takeo K. and Guarro J. 1996.
comm.). The isolate was recovered from a male adult
Stationary phase development of Trimmatostroma abietis. A. van
who was admitted for aortic aneurysm and died
Leeuw. J. Microb. 69: 217–222.
during surgery. The pathogenic potential of P
.
globosa
Gerrits van den Ende A.H.G. and De Hoog G.S. 1999. Variability
remains unclear. Given that the two other strains of P
.
and molecular diagnostics of the neurotropic species
globosa, as well as some close relatives of the species Cladophialophora bantiana. Stud. Mycol. 43: 151–162.
King A.D., Hocking A.D. and Pitt J.I. 1979. Dichloran rose bengal
have a tendency to be oligotrophic, adhering to inert
medium for enumeration and isolation of moulds from foods.
surfaces such as rock, metal, leathery leaves or
Appl. Environ. Microbiol. 37: 959–964.
painted wood, it is reasonable to speculate that the
Matsumoto T., Padhye A.A., Ajello L., Standard P.G. and McGin-
fungus had contaminated a medical device. The strain
nis M.R. 1984. Critical review of human isolates of Wangiella
from aorta proved to be unable to grow at 37 8C. One dermatitidis. Mycologia 76: 232–249.
Reynolds D.R. 1998. Capnodiaceous sooty mold phylogeny. Can. J.
of the strains of Trimmatostroma abietis, with an
Bot. 76: 2125–2130.
ecological spectrum similar to that of P
.
globosa,
Sigler L., Tsuneda A. and Carmichael J.W. 1981. Phaeotheca and
originated from a human (Butin et al. 1996; Table 1),
Phaeosclera, two new genera of dematiaceous hyphomycetes,
but unfortunately no case report is available of that
and a redescription of Sarcinomyces Lindner. Mycotaxon 17:
isolate. 449–467.
360
Staley J.T., Palmer F.E. and Adams J.B. 1982. Microcolonial fungi: Greek quarried marbles associated to specific alteration. In:
th
common inhabitants on desert rocks? Science 215: 1093–1095. Monte M. (ed.), Proc. 8 Workshop Eurocare Euromarble
Sterflinger K. 1998. Temperature and NaCl-tolerance of rock- EU496. CNR, Rome, pp. 35–42.
inhabiting meristematic fungi. A. van Leeuw. J. Microb. 74: Van de Peer Y. and De Wachter R. 1994. TREECON for Windows:
271–281. a software package for the construction and drawing of
Sterflinger K., De Baere R., De Hoog G.S., De Wachter R., evolutionary trees for the Microsoft Windows environment.
Krumbein W.E. and Haase G. 1997. Coniosporium perforans and Comput. Appl. Biosci. 10: 569–570.
C
.
apollinis, two new rock inhabiting fungi isolated from marble Yoshida S., Takeo K., De Hoog G.S., Nishimura K. and Miyaji M.
in the Sanctuary of Delos (Cyclades, Greece). A. van Leeuw. J. 1996. A new type of growth exhibited by Trimmatostroma
Microb. 72: 349–363. abietis. A. van Leeuw. J. Microb. 69: 211–215.
Sterflinger K., De Hoog G.S. and Haase G. 1999. Phylogeny and Wollenzien U., De Hoog G.S., Krumbein W. and Uijthof J.M.J.
ecology of meristematic ascomycetes. Stud. Mycol. 43: 5–22. 1997. Sarcinomyces petricola, a new microcolonial fungus from
Tibell L. 1987. Australasian Caliciales. Symb. Bot. Upsal. 27: marble in the Mediterranean basin. A. van Leeuw. J. Microb. 71:
1–279. 281–288.
Turian G. 1977. Coniosporium aeroalgicolum sp. nov., moisissure Zalar P., De Hoog G.S. and Gunde-Cimerman N. 1999a. Taxonomy
´´ ´
dematiee semi-lichenisante. Ber. Schweiz. Bot. Ges. 87: 19–24. of the endoconidial black yeast genera Phaeotheca and Hy-
`
Urzı C., Lisi S., Criseo G. and Zagari M. 1992. Comparazione di phospora. Stud. Mycol. 43: 49–56.
terreni per l’enumerazione e l’isolamento di funghi deteriogeni Zalar P., De Hoog G.S. and Gunde-Cimerman N. 1999b. Trim-
isolati da materiali naturali. Ann. Microbiol. Enzimol. 42: 185– matostroma salinum, a new species from hypersaline water.
193. Stud. Mycol. 43: 61–67.
` ´
Urzı C. and Realini M. 1998. Colour changes of Noto’s calcareous Zeppenfeldt G., Richard-Yegres N., Yegres F. and Hernandez R.
´
sandstone as related to its colonisation by microorganisms. Int. 1994. Cladosporium carrionii: hongo dimorfo en cactaceas de la
´
Biodet. Biodegr. 42: 45–54. zona endemica para la cromomicosis en Venezuela. Revta
`
Urzı C., De Leo F. and Salamone P. 2000. Microbial diversity of Iberoam. Micol. 11: 61–63.
