Abstract. The new Tremella umbilicariae, lichenicolous on Umbilicaria, is described from Peru. It is characterized by large, dark brown, convex basidiomatal galls, long and narrow basidia, and relatively large basidiospores

Diederich, P.

Millanes, A.M.

Wedin, Mats

Digitala Vetenskapliga Arkivet - Academic Archive On-line

Tremella umbilicariae (Tremellomycetes, Basidiomycota), a new lichenicolous species on Umbilicaria from Peru

Swedish Museum of Natural History

Paul Diederich

Ana M Millanes

Mats Wedin

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Bull. Soc. Nat. luxemb. 115 (2014) 167
Tremella umbilicariae (Tremellomycetes, Basidiomycota),  
a new lichenicolous species on Umbilicaria from Peru
Paul Diederich1, Ana M. Millanes2 & Mats Wedin3
1 Musée national d’histoire naturelle, 25 rue Munster, L–2160 Luxembourg (paul.diederich@education.lu)
2 Departamento de Biología y Geología, Universidad Rey Juan Carlos, C/ Tulipán s.n., E–28933 Móstoles, Spain 
(ana.millanes@urjc.es)
3 Department of Botany, Swedish Museum of Natural History, P. O. Box 50007, SE–104 05 Stockholm, Sweden 
(mats.wedin@nrm.se)
Diederich, P., A. M. Millanes & M. Wedin, 2014. Tremella umbilicariae (Tremellomycetes, 
Basidiomycota), a new lichenicolous species on Umbilicaria from Peru. Bulletin de la Société 
des naturalistes luxembourgeois 115 : 167–172.
Abstract. The new Tremella umbilicariae, lichenicolous on Umbilicaria, is described from 
Peru. It is characterized by large, dark brown, convex basidiomatal galls, long and narrow 
basidia, and relatively large basidiospores.
1. Introduction
The genus Tremella Pers. includes mainly 
mycoparasitic species, most of them being 
highly host-specific and confined to a single 
fungal genus or species. Over fifty licheni-
colous species have been recognized so far 
growing exclusively on lichenized fungi 
(Diederich 1986, 1996, 2003, Sérusiaux 
et al. 2003, Diederich 2007, Zamora et al. 
2011, Millanes et al. 2012, Millanes et al. 
2014). The lichenicolous Tremella species 
often induce the formation of conspicuous 
galls on their host thalli or ascomata, whilst 
some intrahymenial taxa do not produce 
any external symptoms (Diederich 1996, 
Zamora et al. 2011). The phylogenetic posi-
tion of the lichen-inhabiting representatives 
has been tested by molecular methods by 
Millanes et al. (2011), who confirmed that 
they are nested within the genus Tremella. 
In this paper we will describe a new lichen-
inhabiting species of Tremella inducing large 
galls on the thallus of Umbilicaria.
2. Material and Methods
2.1. Molecular studies
In addition to the specimen studied, 18 speci-
mens representing 12 Tremella species were 
included in the molecular study (Table 1). 
The sampling included the type of the genus 
Tremella (T. mesenterica), terminals of the 
Fuciformis and Foliacea groups distin-
guished by Chen (1998) and terminals rep-
resenting three groups of lichenicolous spe-
cies distinguished by Millanes et al. (2011), 
in particular, lichenicolous species with a 
micro-morphology similar to that of the 
specimen growing on Umbilicaria. Filoba-
sidium floriforme and F. uniguttulatum were 
used as outgroup. Species names, voucher 
information, and GenBank accession num-
bers are given in Table 1.
DNA extraction and PCR amplifications 
were achieved following protocols in Mil-
lanes et al. (2012), except that in this case 
we used the primers ITS1F (Gardes & 
Bruns 1993) and BasidLSU3-3 (Millanes et 
al. 2011), to amplify only the internal tran-
scribed spacer I, the 5.8 rDNA gene, the 
internal transcribed spacer II and a small 
fragment of approximately 120 bp in the 
nLSU rDNA gene.
Bayesian analyses were conducted following 
Millanes et al. (2012). Maximum likelihood 
analyses were achieved in RAxMLGUI 1.3, a 
graphical front-end for RAxML (Stamatakis, 
2006), using the GTRCAT model of nucleo-
tide substitution. We performed a total of 
100 runs and assessed node support via 1000 
bootstrap replicates.
168 Bull. Soc. Nat. luxemb. 115 (2014)
2.2. Morphological examination
Dry herbarium specimens were examined 
and measured under a binocular micro-
scope Leica MZ 7.5. Macroscopic pho-
tographs were done using a Canon 40D 
camera with a Canon MP-E 65 mm lens, 
StackShot (Cognisys) and Helicon Focus 
(HeliconSoft) for increasing the depth 
of field. Hand-made sections and squash 
preparations of basidiomata were studied 
in a mixture of Phloxin B, Congo Red and 
10% KOH. Microscopic photographs were 
prepared using a Leica DMLB microscope 
with DIC optics at a magnification of 
1000× and a Leica EC3 camera. Measure-
ments of basidia and basidiospores are 
indicated as (minimum–) X-σx – X+σx 
(–maximum), followed by the number of 
measurements (N); the ratio length/width 
of ascospores is indicated as l/w and given 
in the same way.
3. Results
3.1. Phylogenetic results
One ITS sequence of Tremella umbilicariae, 
including also ca. 120 nucleotides of the 
nuLSU, was aligned together with sequences 
already available in GenBank (Table 1). We 
produced a combined data matrix of the ITS 
and nLSU rDNA sequences, which com-
prised 1212 characters. A majority rule con-
sensus tree was constructed from the 2500 
trees of the stationary tree sample from the 
Bayesian analysis. Convergence among runs 
was assessed following Millanes et al. (2012). 
The best tree obtained from the ML analysis 
had an ln-likelihood value of -4569.7999. 
The new species Tremella umbilicariae is 
included within the so-called “Clade II” in 
Millanes et al. (2011), together with T. cla-
doniae, T. lobariacearum and T. phaeophys-
ciae (Fig. 1), although the relationships with 
these species is not resolved with support.
Species names Specimen data / culture references ITS nLSU
Tremella caloplacae France, Sérusiaux s.n. ( S-F102489) JN053469 JN043574
Tremella candelariellae Luxembourg, Diederich 12808 (S-F102492) JN053470 JN043575
Tremella cetrariicola-a Finland, Suija s.n. ( S-F102413) JN053490 JN043596
Tremella cetrariicola-b Latvia, 2005, Suija s.n. (TU) JN053491 JN043597
Tremella cladoniae-a France, Diederich 16031 (S-F102550) JN053478 JN043584
Tremella cladoniae-b Estonia, Suija 872 (TU-45019) JN053477 JN043583
Tremella coppinsii-a UK, Diederich 15628 (S-F102414) JN053495 JN043601
Tremella coppinsii-b Estonia, Suija 38a (TU-38637) JN053496 JN043602
Tremella dendrographae USA, Tehler 7068 (S-F102415) JN053471 JN043576
Tremella foliacea Sweden, Wiklund 018 (S-F102409) JN053502 JN043609
Tremella hypogymniae-a Sweden, Wedin 6892 (UPS) JN053484 JN043590
Tremella hypogymniae-b Estonia, Suija s.n. (TU-39402) JN053485 JN043591
Tremella lobariacearum-a (Type) Madeira, Diederich 4935 (S-F102418) JN053473 JN043579
Tremella lobariacearum-b Canary Islands, Diederich 16468 (S-F102419) JN053474 JN043580
Tremella mesenterica-a Sweden, Ryman 9146 (S-F102411) JN053463 JN043568
Tremella phaeophysciae-a Luxembourg, Diederich 12429 (S-F102505) JN053479 JN043585
Tremella phaeophysciae-b Estonia, Suija s.n. (TU-55041) JN053480 JN043586
Tremella umbilicariae (Type) Peru, Santesson & Moberg P62:55 (UPS) KM507564 -
Outgroup
Filobasidium floriforme CBS 6241 AF190007 AF075498
Filobasidium uniguttulatum CBS 1730 AF444302 AF075468 
Table 1. Sequence newly produced corresponding to the type of the new species (bold), and 
sequences downloaded from GenBank, with specimen data or culture references.
Bull. Soc. Nat. luxemb. 115 (2014) 169
Fig. 1. Fifty per cent majority rule Bayesian consensus tree with average branch lengths from the combined analyses 
of ITS and nnLSU datasets. PP values ≥ 0.95, obtained in the Bayesian analysis, are indicated over the branches, 
and maximum likelihood bootstrap values ≥ 70%, below the branches. Branch lengths are scaled to the expected 
number of nucleotide substitutions per site. The new species Tremella umbilicariae is highlighted in bold and bigger 
font. The clade corresponding to “Clade II” in Millanes et al. (2011) is indicated to the right.
0 . 0 2
T .  cetrariicola-a
F.  uniguttulatum
T .  lobariacearum -b
T .  um bilicariae
T .  cetrariicola-b
T .  lobariacearum -a
T .  caloplacae
T .  m es enterica
T .  dendrographae
T.  hypogym niae-b
T .  cladoniae-b
F.  floriform e
T .  fuciform is
T.  candelariellae
T .  hypogym niae-a
T .  phaeophys ciae-b
T .  cladoniae-a
T .  phaeophys ciae-a
T .  foliacea
97
100
99
100
100
88
100
100
100
100
95
100
100
1 .00
1 .00
1 .00
1 .00
1 .00
1 .00
0.99
1 .00
1 .00
1 .00
1 .00
1 .00
“Clade II”
1 .00
170 Bull. Soc. Nat. luxemb. 115 (2014)
3.2. Taxonomy
Tremella umbilicariae Diederich & Millanes 
sp. nov. (Figs. 2–3)
Mycobank MB 810174
Characterized by large, dark brown, convex 
basidiomatal galls, long and narrow, 
1-transseptate basidia, 19.7–25.2 × 7.2–7.8 µm, 
and relatively large basidiospores, 7.6–9.4 × 6.1–
7.6 µm.
Fig. 2. Tremella umbilicariae on Umbilicaria (holotypus). Scale bar = 1 mm (the same for both photographs).
Bull. Soc. Nat. luxemb. 115 (2014) 171
Type: Peru, dept. Ancash, prov. Huaraz, pass W of 
Conococha (road Huaraz-Pativilca), 10°7’ S, 77°23’ W, 
alt. 3900 m, on Umbilicaria, 1 iii 1981, R. Santesson & 
R. Moberg P62:55 (UPS–holotype; herb. Diederich–
isotype).
Basidiomata inducing the formation of dis-
tinct convex galls on the host thallus, base not 
or slightly constricted, dark brown to blackish, 
relatively smooth, matt, frequently pruinose 
near the base, 0.6–2.5 mm diam., when very 
old sometimes almost tuberculate and with a 
cracked surface. Context hyphae thin-walled, 
often with clamp connections, 2.5–3 µm 
diam.; haustorial branches present, mother 
cells subspherical, 3–5 × 3–4 µm, haustorial 
filament 1–1.5 µm diam. Hymenium hyaline, 
containing numerous probasidia; hyphidia 
present, but not abundant, thick-walled, 
with numerous septa and ramifications, 
2.5–5.0 µm diam.; probasidial initials clavate, 
proliferations occurring through the basal 
clamp. Basidia, when mature, 2-celled, with 
one transverse septum, slightly constricted 
Fig. 3. Tremella umbilicariae (holotypus, in a mixture of Phloxin B, Congo Red and 10% KOH, using DIC optics). 
A, Basidiospores. B, Young, mature and old basidia, and epibasidia (right). C, Hymenium, showing basidia and 
numerous context hyphae. D, Context hyphae and clamp (arrow). E, Hyphae with haustorial branches (arrows). 
Scale bar = 10 µm (the same for all photos).
172 Bull. Soc. Nat. luxemb. 115 (2014)
at the septum, (19.0–)19.7–25.2(–28.0) × 
(6.7-)7.2–7.8(–8.0) µm (excl. epibasidia), 
ratio l/w (2.5–)2.6–3.4(–3.7) (N=15), rarely 
with an attenuated stalk-like base; epibasidia 
subcylindrical, up to 45 µm long, 2.5–4 µm 
diam. Basidiospores ellipsoid to subspherical, 
with a distinct apiculus, (6.5–)7.6–9.4(–10.0) 
× (5.5–)6.1–7.6(–8.3) µm, ratio l/w (1.1–)1.2–
1.3(–1.4) (N=15). Anamorph not observed. 
Distribution and host. Known only from the 
type locality in Peru at 3900 m, gall-induc-
ing on the thallus of Umbilicaria sp.
Discussion. Tremella umbilicariae has to be 
compared with the other species with 1-trans-
septate, narrow basidia, relatively long epi-
basidia and relatively large basidiospores 
described by Diederich (1996). T. cladoniae 
Diederich & M. S. Christ. is distinguished by 
pinkish brown to reddish brown basidiomatal 
galls, the absence of hyphidia, often longer and 
narrower basidia, 20–30 × 4.5–8 µm, and the 
presence of asteroconidia in some specimens. 
T. lobariacearum Diederich & M. S. Christ. is 
distinguished by the absence of hyphidia, much 
broader basidia, 14–23 × 7–11 µm, with trans-
verse, oblique or longitudinal septa, and the 
presence of asteroconidia in some specimens. 
T. phaeophysciae Diederich & M. S. Christ. is 
distinguished by more flat to slightly convex, 
olivaceous galls, the absence of hyphidia, often 
narrower basidia, 4.5–8 µm diam., shorter epi-
basidia, 25–30 µm long, more roundish basidi-
ospores, ratio l/w c. 1.1, and the frequency of 
asteroconidia, which are absent in the type 
specimen of the new species. T. psoromicola 
Diederich is distinguished by smaller basidi-
omata, 0.2–0.8 mm diam., not inducing galls, 
and much broader basidia, 17–24 × 8.5–11.5 
µm. T. santessonii Diederich has much smaller, 
reddish brown basidiomata, 0.2-0.3 mm diam. 
T. hypogymniae Diederich & M. S. Christ. has 
shorter and broader basidia, 11–16 × 7–12 µm.
Acknowledgments
We thank the curator of UPS for the loan of 
the type material, and Javier Etayo for drawing 
our attention to this material. Sequencing was 
supported by a grant from the Spanish Ministry 
of Economy and Competitiveness (CGL2012–
40123) to A.M. and M.W.
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Tremella umbilicariae (Tremellomycetes, Basidiomycota), a new lichenicolous species on Umbilicaria from Peru

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