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Citation: Silva-Filho, A.G.S.;
Mombert, A.; Nascimento, C.C.;
Nóbrega, B.B.; Soares, D.M.M.;
Martins, A.G.S.; Domingos, A.H.R.;
Santos, I.; Della-Torre, O.H.P.; Perry,
B.A.; et al. Eoscyphella luciurceolata
gen. and sp. nov. (Agaricomycetes)
Shed Light on Cyphellopsidaceae
with a New Lineage of
Bioluminescent Fungi. J. Fungi 2023,
9, 1004. https://doi.org/10.3390/
jof9101004
Academic Editor: Samantha
C. Karunarathna
Received: 17 July 2023
Revised: 22 August 2023
Accepted: 6 October 2023
Published: 12 October 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
Fungi
Journal of
Article
Eoscyphella luciurceolata gen. and sp. nov. (Agaricomycetes)
Shed Light on Cyphellopsidaceae with a New Lineage of
Bioluminescent Fungi
Alexandre G. S. Silva-Filho 1, Andgelo Mombert 2, Cristiano C. Nascimento 1, Bianca B. Nóbrega 3,4,
Douglas M. M. Soares 4, Ana G. S. Martins 5, Adão H. R. Domingos 5, Isaias Santos 5, Olavo H. P. Della-Torre 5,
Brian A. Perry 6, Dennis E. Desjardin 7, Cassius V. Stevani 3,4 ,* and Nelson Menolli, Jr. 1,*
1IFungiLab, Departamento de Ciências da Natureza e Matemática (DCM), Subárea de Biologia (SAB),
Instituto Federal de Educação, Ciência e Tecnologia de São Paulo (IFSP), Campus São Paulo (SPO),
São Paulo 01109-010, SP, Brazil; silvafilhoags@gmail.com (A.G.S.S.-F.);
cristiano.nascimento@ifpi.edu.br (C.C.N.)
2Independent Researcher, 25640 Corcelle-Mieslot, France; mombertan@gmail.com
3Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo,
São Paulo 05508-000, SP, Brazil; bianca.barros.nobrega@usp.br
4Departamento de Química Fundamental, Instituto de Química, Universidade de São Paulo,
São Paulo 05508-000, SP, Brazil; douglas@iq.usp.br
5Instituto de Pesquisa da Biodiversidade (IPBio), Iporanga 18330-000, SP, Brazil;
anaglaucia@ipbio.org.br (A.G.S.M.); henrique.domingos@ipbio.org.br (A.H.R.D.);
tatubio@hotmail.com (I.S.); olavopetrucci@gmail.com (O.H.P.D.-T.)
6Department of Biological Sciences, California State University, East Bay, Hayward, CA 94542, USA;
brian.perry@csueastbay.edu
7Department of Biology, San Francisco State University, San Francisco, CA 94132, USA; ded@sfsu.edu
*Correspondence: stevani@iq.usp.br (C.V.S.); menollijr@yahoo.com.br (N.M.J.)
Abstract:
During nocturnal field expeditions in the Brazilian Atlantic Rainforest, an unexpected
bioluminescent fungus with reduced form was found. Based on morphological data, the taxon
was first identified as belonging to the cyphelloid genus Maireina, but in our phylogenetic analyses,
Maireina was recovered and confirmed as a paraphyletic group related to genera Merismodes and
Cyphellopsis.Maireina filipendula,Ma. monacha, and Ma. subsphaerospora are herein transferred to
Merismodes. Based upon morphological and molecular characters, the bioluminescent cyphelloid
taxon is described as the new genus Eoscyphella, characterized by a vasiform to urceolate basidiomata,
subglobose to broadly ellipsoid basidiospores, being pigmented, weakly to densely encrusted external
hyphae, regularly bi-spored basidia, unclamped hyphae, and an absence of both conspicuous long
external hairs and hymenial cystidia. Phylogenetic analyses based on ITS rDNA and LSU rDNA
support the proposal of the new genus and confirm its position in Cyphellopsidaceae. Eoscyphella
luciurceolata represents a new lineage of bioluminescent basidiomycetes with reduced forms.
Keywords: Agaricales; Basidiomycota; Brazilian biodiversity; bioluminescence; Niaceae
1. Introduction
Agaricomycetes forms a large and diverse group that includes the mushroom-forming
fungi and produces the most complex basidiomata forms, such as gilled mushrooms, bo-
letes, polypores, and puffballs [
1
]. Some species of gilled mushroom are well known and
stand out for their natural light emission with a luciferin/luciferase chemical reaction [
2
,
3
].
The bioluminescent fungi are morphologically well characterized and typically known for
their gilled or poroid basidiomata within the order Agaricales [
4
]. The known biolumines-
cent mushrooms are distributed in tropical and temperate regions, where they grow on
moist decaying wood or leaves [4].
J. Fungi 2023,9, 1004. https://doi.org/10.3390/jof9101004 https://www.mdpi.com/journal/jof
J. Fungi 2023,9, 1004 2 of 23
The first reports describing light emission with fungi were written in the 19th century
by J. F. Heller [
5
]. In the 20th century, approximately 50 species of fungi related to light
emission were described [
6
–
21
]. These species were evaluated and revised by Desjardin
et al. [
4
], who recovered 64 valid names of bioluminescent mushrooms. In recent years,
the number of known species has increased substantially [
22
–
29
], with approximately
110 bioluminescent fungi currently recognized [30].
Desjardin et al. [
4
,
24
] proposed four molecular lineages to accommodate the biolumi-
nescent species: Armillaria, Mycenoid, Omphalotus, and Lucentipes. The Armillaria lineage
is represented by species of the genus Armillaria (Fr.) Staude, which is phylogenetically
positioned in the Physalacriaceae Corner [
31
]. These species are popularly called Honey
Mushrooms and represent saprotrophic or forest tree root pathogens [
32
]. The Mycenoid is
the most diverse lineage, with species known in the genus Mycena (Pers.) Roussel sensu
lato,Filoboletus Henn. (manipularis group), Panellus P. Karst. (Panellus/Dictyopanus species),
Roridomyces Rexer, and Resinomycena Redhead & Singer, all anchored in the family Myce-
naceae Overeem [
4
,
25
]. Bioluminescent species of the Mycenoid lineage exhibit wide phe-
notypic variation; the majority produce small mushrooms with lamellate hymenophores,
like most Mycena species, whilst other have poroid hymenophores like those in Filoboletus,
and pleurotoid species with poroid or lamellate hymenophores are represented by the
genus Panellus [
4
]. The Omphalotus lineage is well represented by species of the genera
Neonothopanus R.H. Petersen & Krisai and Omphalotus Fayod plus Nothopanus eugrammus
(Mont.) Singer [=Pleurotus eugrammus (Mont.) Dennis] and Pleurotus decipiens Corner [
4
].
Omphalotus and Neonothopanus are phylogenetically positioned in Omphalotaceae Bresin-
sky, while the phylogenetic position of N. eugrammus and P. decipiens has not yet been
confirmed [
4
,
33
]. Omphalotus and Neonothopanus are saprobic, forming large and conspicu-
ous agaricoid mushrooms, some popularly known as jack-o’-lantern mushrooms in Europe
and North America [
34
]. Gerronema viridilucens Desjardin, Capelari & Stevani and Mycena
lucentipes Desjardin, Capelari & Stevani (the Lucentipes clade) form an independent lineage
of bioluminescent fungi with uncertain phylogenetic position at the family level [24,35].
Agaricomycetes also includes species that produce reduced forms such as the cyphel-
loid fungi, comprised primarily of saprobic species, producing minute barrel-, cup-, bowl-,
or tube-shaped basidiomata with smooth and even hymenophores [
36
–
40
]. The cyphel-
loid fungi were first grouped in the artificial family Cyphellaceae Burnett [
41
]. The name
Porotheleaceae Murrill was later related to tubular and discoid Hymenomycetes [
42
]. Some
authors, including Cooke [
43
], used this classification for the reduced forms. However, the
polyphyletic status of the cyphelloid fungi, with multiple lineages in the order Agaricales,
has already been elucidated in previous molecular phylogenetic studies [31,44–50].
The diversity of cyphelloid fungi includes roughly 120 taxa that have been classified
in approximately 40 widely accepted genera [
44
,
51
], with additional new taxa recently
described [
50
,
52
–
56
]. It is estimated that the number of cyphelloid fungi distributed
worldwide could reach nearly 400 to 500 species [45,53,57].
Currently, Cyphellopsidaceae Jülich and Niaceae Jülich are the names related to the
Nia clade [
45
,
58
]. Cyphellopsidaceae is the most diverse family and the largest lineage
of cyphelloid forms confirmed with molecular data [
45
]. The genera Calathella D.A.Reid.
Cyphellopsis Donk, Merismodes Earle (abbreviated here as Me.), and Woldmaria W.B. Cooke
were previously classified in Cyphellopsidaceae [
58
] and typified with Cyphellopsis anomala
(Pers.) Donk. Niaceae was erected in the same work [
58
] to accommodate the genus Nia
R.T. Moore & Meyers, typified by the marine species Nia vibrissa R.T. Moore & Meyers.
Binder et al. [
59
] placed N. vibrissa in the euagaric clade and Hibbett and Binder [
60
]
confirmed its placement in the euagaric clade along with two additional marine basid-
iomycetes, Calathella mangrovei E.B.G. Jones & Agerer and Halocyphina villosa Kohlm. &
E. Kohlm. Bodensteiner et al. [
45
] recognized in the Nia clade the cyphelloid genera Ca-
lathella,Cyphellopsis,Flagelloscypha Donk, Halocyphina Kohlm. & E. Kohlm., Lachnella Fr.,
Merismodes, and Woldmaria, as well as the corticioid genus Dendrothele Höhn. & Litschn.
Finally, Maireina W.B. Cooke (abbreviated here as Ma.) has had its phylogenetic position
J. Fungi 2023,9, 1004 3 of 23
confirmed in the Nia clade (=Cyphellopsidaceae) [
54
,
55
]. In the Mycobank and the Index
Fungorum databases, the names Digitatispora Doguet, Flagelloscypha,Halocyphina,Lachnella,
Maireina,Merismodes,Nia,Peyronelina P.J. Fisher, J. Webster & D.F. Kane, and Woldmaria are
still classified in the family Niaceae. The name Cyphellopsidaceae was legitimized over
Niaceae by Knudsen and Vesterholt [
61
], although the name Niaceae is still being used by
some authors (e.g., [62]).
During one of many nocturnal expeditions into the Atlantic Rainforest in the state
of São Paulo (Brazil), in the same area where 12 bioluminescent species have already
been described or recorded [
22
–
25
], an unusual bioluminescent fungus with cyphelloid
form was discovered by co-authors of this work. The aims of this study are as follows:
(i) confirm the phylogenetic position and classification of all known bioluminescent fungi
based on molecular data; (ii) identify, based on morphology and molecular data, the new
bioluminescent fungi with reduced form; and (iii) provide the phylogenetic placement
of Maireina monacha to better understand its relationship with related genera. Based on
molecular analyses, Maireina is considered a synonym of Merismodes and is herein amended.
Maireina filipendula Læssøe, Ma. monacha (Speg.) W.B. Cooke, and Ma. subsphaerospora
Mombert are transferred to Merismodes, and the new bioluminescent cyphelloid taxon
from Brazil is described in the new genus Eoscyphella gen. nov., within Cyphellopsidaceae.
Eoscyphella luciurceolata represents a new lineage of bioluminescent basidiomycetes with
cyphelloid form.
2. Materials and Methods
2.1. Collecting Area
2.1.1. Brazilian Site of the New Luminescent Taxon
Basidiomata of the new bioluminescent taxon were collected during expeditions to
the Atlantic Rainforest in the municipality of Eldorado, state of São Paulo, Brazil. More
specifically, at a 546 m altitude and 500 m west of the entrance to the “Caverna do Diabo”
(Devil’s Cave) State Park at coordinates 24
◦
38
0
14.0100
00
S and 48
◦
24
0
37.6812
00
W. The climate
there is classified as humid subtropical, and the mean annual temperatures are usually
between 20 and 22
◦
C and have a high pluviometric index, with average annual rainfall
ranging from 1500 to 2000 mm [
63
]. The forest type is Dense Ombrophilous Forest, which
is mainly composed of the Angiosperm families Annonaceae Juss., Euphorbiaceae Juss.,
Lauraceae Juss., Melastomataceae Juss., Moraceae Gaudich., Myrtaceae Juss., Rubiaceae
Juss., and Sapotaceae Juss. [64,65].
2.1.2. French Site of Maireina monacha
The Butte de la Garenne is located in the Cantal department in Southern-Central
France. The site is covered with a calcareous beech forest of approximately one hectare,
and a pubescent oak forest in the remaining area [66].
2.2. Morphological Analyses
Macroscopic features were recorded from fresh material. Color names and codes follow
Kornerup and Wanscher [
67
]. Micromorphological analyses were performed using the
methodology of Bodensteiner [
53
]. Basidiospores were measured in lateral view using 5%
KOH. Basidiospore statistics include the following: xm = arithmetic mean of basidiospore
length
×
basidiospore width (
±
standard deviation) for nbasidiospores measured in a
single specimen; xr = range of basidiospore means; Q = quotient of basidiospore length
by basidiospore width in any one basidiospore, indicated as a range of variation in n
basidiospores measured; Qm = mean of Q-values in a single specimen; n= number of
basidiospores measured per specimen; and s = number of specimens studied. Distilled
water was used in order to visualize crystals in skeletal hyphae, whilst Melzer’s reagent
was used to test amyloid/dextrinoid reactions. The Brazilian specimens were deposited at
the Fungarium IFungi (FIFUNGI) from the IFungiLab at the “Instituto Federal de Educação,
J. Fungi 2023,9, 1004 4 of 23
Ciência e Tecnologia de São Paulo (IFSP)”, Brazil, and the European specimens are housed at
the “Muséum National d’Histoire Naturelle” (P), France ([
68
], 2023, continuously updated).
2.3. Molecular Methods
Entire basidiomata were homogenized in lysis tubes with magnetic beads for three
cycles of 2 min in SpeedMill Plus (Analytik, Jena, Germany) in an AP1 buffer, and the
genomic DNA was extracted using the Qiagen Dneasy
®
Plant Mini Kit (Germantown,
MD, USA) according to the manufacturer’s instructions. Primer pairs ITS1-F/ITS4 and
LR0R/LR5 were used to amplify and sequence the ITS rDNA region and the LSU rDNA
gene, respectively [
44
,
69
]. Sequencing reactions were conducted at Macrogen (Seoul,
Republic of Korea).
2.4. Phylogenetic Analyses
The newly generated sequences were assembled and edited in Sequencher TM v5.0
software (Gene Codes Corporation, Ann Arbor, MI, USA) and were deposited in GenBank
(codes in the tree and in Supplementary Table S1). Three new ITS rDNA and two novel LSU
r DNA sequences were generated in this study. Three distinct datasets were constructed:
one composed only of the LSU rDNA sequences, one only with ITS rDNA sequences, and a
third including the ITS rDNA + LSU rDNA sequences. To assemble the LSU rDNA dataset,
our generated sequences were submitted to the BLASTn algorithm at NCBI (GenBank,
https://blast.ncbi.nlm.nih.gov/Blast.cgi, accessed on 1 May 2023) to retrieve similar se-
quences. Other sequences of cyphelloid basidiomycetes, including those generated by
Bodensteiner et al. [
45
], Læssøe et al. [
54
], Baltazar et al. [
48
], Karasi´nski et al. [
56
], and
Vizzini et al. [
70
], were downloaded and included in the dataset. Existing sequences of
known bioluminescent fungi were also downloaded from GenBank to compose a final
dataset that includes all known bioluminescent and cyphelloid lineages. The LSU rDNA
sequence most likely misnamed G. viridilucens (EF514207), which is available on GenBank
and was used in the phylogenetic analyses by Vizzini et al. [
70
] and Na et al. [
71
], is 99.7%
identical to sequence M. lucentipes (DED7828) [
72
]. For this reason, we excluded the se-
quence EF514207 from our phylogenetic analyses and included a new one of G. viridilucens
(DED7822), originally from type locality and morphologically described and confirmed [
22
].
For the ITS rDNA dataset, sequences of species belonging to Cyphellopsidaceae were
retrieved from GenBank and then used to recover similar sequences using the BLASTn
algorithm. The combined ITS+LSU rDNA dataset was constructed to focus primarily on
the Merismodes clade. Boletus griseiceps B. Feng, Y.Y. Cui, J.P. Xu & Zhu L. Yang; Boletus sub-
violaceofuscus B. Feng, Y.Y. Cui, J.P. Xu & Zhu L. Yang; and Fistulinella ruschii Magnago were
used as an outgroup in the LSU rDNA dataset. Two sequences of Cunninghammyces Stalpers
were used as an outgroup in the ITS rDNA dataset, and sequences of Acanthocorticium
brueggemannii Baltazar, Gorjón & Rajchenb were used for the combined analyses.
Our datasets were aligned using MAFFT v.7 under the E-INS-i criteria [
73
]. Seaview
v.4 was used to visualize the alignment [
74
]. To compute the best-fit model of nucleotide
evolution, the ITS rDNA alignment was subdivided into three partitions: ITS1, 5.8S, and
ITS2. Maximum Likelihood analyses were performed in RAxML v8.2.X [
75
]. The most
appropriate nucleotide substitution models were selected with BIC (Bayesian Information
Criterion) using jModelTest 2v.1.6 [
76
]. Bayesian inferences (BI) were performed using
MrBayes 3.1.2, performing 2
×
10
7
MCMC generations, sampling one tree every 1
×
10
3
generations [
77
]. The jModelTest 2v.1.6, RAxML v8.2.X, and MrBayes 3.1.2 software were
implemented in CIPRES Science Gateway 3.1 [
78
]. Trees were visualized and rooted in
FigTree v.1.4.4 and the final tree figures were completed in CorelDRAW Grafics Suit 2021.
A node was considered significantly supported if it received bootstrap (BS)
≥
70% and
Bayesian posterior probability (BPP) ≥0.95.
J. Fungi 2023,9, 1004 5 of 23
3. Results
3.1. Phylogenetic Results
3.1.1. LSU rDNA Dataset
The final LSU rDNA dataset contains 206 sequences (including 2 that are newly
generated), consisting of 1051 nucleotide sites, including gaps. The most appropriate
evolutionary model estimated was TrN+I+G. The bootstrapping criteria from the ML
analyses stopped after 350 replicates. Both the RAxML analysis and Bayesian inference
yielded similar tree topologies. The LSU rDNA tree generated from the ML analysis,
including bootstrap values and posterior probabilities, is shown in four parts (Figure 1a–d).
The family Cyphellopsidaceae, represented by 52 sequences, forms a well-supported
clade (100% BS, 1.0 BPP) (Figure 1a) that harbors the largest number of cyphelloid genera
hitherto confirmed with molecular data: Akenomyces G. Arnaud, Calathella (represented by
Calathella gayana (Lév.) Agerer), Flagelloscypha,Halocyphina,Lachnella,Maireina,Merismodes,
Nia,Eoscyphella gen. nov., Pseudolasiobolus Agerer, and Woldmaria.
The new proposed genus Eoscyphella formed a well-supported clade (100% BS, 1.0 BPP)
sister to the cyphelloid genus Woldmaria. The LSU rDNA sequences of Eoscyphella and
Woldmaria are from 92.6% to 92.7% similar. Sequences of taxa of the genus Maireina were
represented in our analyses by Ma. filipendula, Ma. subsphaerosphora, and Ma. monacha (type
species of Maireina), with the latter sampled, sequenced, and identified by Mombert [
55
]
and fully described and epityfied in this study. Maireina formed a paraphyletic group, but
represents a monophyletic clade when including sequences of Merismodes anomala (Pers.)
Singer (as = Cyphellopsis anomala) and Me. fasciculata (Schwein.) Earle, with the latter being
the type species of the genus. The clade formed with Maireina and Merismodes is well
supported (75% BS, 0.99 BPP).
In addition to Cyphellopsidaceae, our LSU rDNA analyses recovered another
11 lineages of cyphelloid fungi (Figure 1a–d). Several cyphelloid genera are recovered in
distinct well-supported clades that correspond to at least five well-delimited families: in
Cyphellaceae (96% BS, 1.0 BPP), the genus Cyphella Fr. (100% BS, 1.0 BPP); in Crepido-
taceae (S. Imai) Singer (77% BS, 0.99 BPP), the genus Pellidiscus Donk (100% BS, 1.0 BPP);
in Marasmiaceae Roze ex Kühner (98% BS, 1.0 BPP), the genus Amyloflagellula Singer; in
Phyllotopsidaceae Locquin ex Olariaga, Huhtinen, Læssøe, J.H. Petersen & K. Hansen
(94% BS, 1.0 BPP), the genus Cyphelloporia Karasi´nski, L. Nagy, Szarkándi, Holec & Kolaˇrík
(100% BS, 1.0 BPP); and in Porotheleaceae (94% BS, 0.99 BPP), the genus Stromatoscypha
Donk (100% BS, 1.0 BPP). The cyphelloid genus Stigmatolemma Kalchbr. clusters with
sequences of Resupinatus alboniger (Pat.) Singer (MK278432) and Resupinatus conspersus
(Pers.) Thorn, Moncalvo & Redhead (AY570994) in a well-supported clade (91% BS, 1.0 BPP)
that is sister (unsupported) to the well-supported clade (78% BS, 0.99 BP) formed with
sequences of the cyphelloid genus Calyptella Quél. (Figure 1b).
Additionally, sequences of the cyphelloid genera Henningsomyces Kuntze and Rectipilus
Agerer are resolved in two phylogenetically distant clades: the Henningsomyces/Rectipilus/
Acanthocorticium clade (100% BS, 1.0 BPP) that is sister (86% BS, 1.0 BPP) to Cyphellop-
sidaceae (Figure 1a), and in the clade of Phyllotopsidaceae sensu Olariaga et al. [
77
] and
Karasi´nski et al. [
56
], forming a well-supported clade (99% BS, 1.0 BPP) with Cyphelloporia
representatives (Figure 1b). Other cyphelloid taxa, such as Calathella columbiana Agerer
(AY570993), Chromocyphella lamellata G. Moreno & Olariaga (MF623831), and Phaeosolenia
densa (Berk.) W.B. Cooke (AY571018, AY571019) formed independent lineages with no clear
relationship to other known lineages (Figure 1c).
J. Fungi 2023,9, 1004 6 of 23
J.Fungi2023,9,xFORPEERREVIEW6of23
(a)
Figure 1. Cont.
J. Fungi 2023,9, 1004 7 of 23
J.Fungi2023,9,xFORPEERREVIEW7of23
(b)
Figure 1. Cont.
J. Fungi 2023,9, 1004 8 of 23
J.Fungi2023,9,xFORPEERREVIEW8of23
(c)
Figure 1. Cont.
J. Fungi 2023,9, 1004 9 of 23
J.Fungi2023,9,xFORPEERREVIEW9of23
(d)
Figure1.(a–d)TheMLphylogenyofrepresentativecollectionsofAgaricomycetesbasedon
completeLSUrDNA.Voucher/strain/cloneorherbariumnumberaswellasGenBankaccession
numbersandcountryoforiginfollowtaxonname.Cyphelloidspeciesarenotedwiththesymbol◆
andbioluminescentspecieswiththesymbol
⚫
.Thenewspeciesishighlightedinred,andthe
luminescentlineagesareingray.Thickerlinesrepresentbrancheswithmaximumbootstrapvalues
andposteriorprobabilities(100%BS,1.0BPP).BootstrapvaluesandBayesianposteriorprobabilities
areindicatediftheyareequaltoorgreaterthan70%,and0.95,respectively.Thescalebarrepresents
theexpectednumberofnucleotidechangespersite.
Additionally,sequencesofthecyphelloidgeneraHenningsomycesKuntzeand
RectipilusAgererareresolvedintwophylogeneticallydistantclades:the
Henningsomyces/Rectipilus/Acanthocorticiumclade(100%BS,1.0BPP)thatissister(86%BS,
1.0BPP)toCyphellopsidaceae(Figure1a),andinthecladeofPhyllotopsidaceaesensu
Olariagaetal.[77]andKarasińskietal.[56],formingawell‐supportedclade(99%BS,1.0
BPP)withCyphelloporiarepresentatives(Figure1b).Othercyphelloidtaxa,suchas
CalathellacolumbianaAgerer(AY570993),ChromocyphellalamellataG.Moreno&Olariaga
(MF623831),andPhaeosoleniadensa(Berk.)W.B.Cooke(AY571018,AY571019)formed
independentlineageswithnoclearrelationshiptootherknownlineages(Figure1c).
ThefourbioluminescentlineagessensuDesjardinetal.[4]arerepresented(Figure
1a–d).TheMycenoidlineageisthelargestandformsamonophyleticgroupinawell‐
supported(99%BS,1.0BPP)clade(familyMycenaceae)representedinouranalyses
(Figure1c)by25speciesofthegeneraFiloboletus,Mycena,Panellus,andRoridomyces.The
Armillarialineage(Figure1d)ishererepresentedbyfivespeciesofthegenusArmillaria
thatclusteredinawell‐supported(92%BS,1.0BPP)cladesistertosequencesofCyptotrama
asprata(Berk.)Redhead&Ginns(KY418873)andXerulastrigosaZhuL.Yang,L.Wang&
G.M.Muell.(KF305680)withinPhysalacriaceae(97%BS,1.0BPP).TheOmphalotuslineage
isrepresented(Figure1d)bysixspeciesofOmphalotusandNeonothopanusthatformawell‐
Figure 1.
(
a
–
d
) The ML phylogeny of representative collections of Agaricomycetes based on complete
LSU rDNA. Voucher/strain/clone or herbarium number as well as GenBank accession numbers
and country of origin follow taxon name. Cyphelloid species are noted with the symbol
J.Fungi2023,9,xFORPEERREVIEW9of23
(d)
Figure1.(a–d)TheMLphylogenyofrepresentativecollectionsofAgaricomycetesbasedon
completeLSUrDNA.Voucher/strain/cloneorherbariumnumberaswellasGenBankaccession
numbersandcountryoforiginfollowtaxonname.Cyphelloidspeciesarenotedwiththesymbol◆
andbioluminescentspecieswiththesymbol
⚫
.Thenewspeciesishighlightedinred,andthe
luminescentlineagesareingray.Thickerlinesrepresentbrancheswithmaximumbootstrapvalues
andposteriorprobabilities(100%BS,1.0BPP).BootstrapvaluesandBayesianposteriorprobabilities
areindicatediftheyareequaltoorgreaterthan70%,and0.95,respectively.Thescalebarrepresents
theexpectednumberofnucleotidechangespersite.
Additionally,sequencesofthecyphelloidgeneraHenningsomycesKuntzeand
RectipilusAgererareresolvedintwophylogeneticallydistantclades:the
Henningsomyces/Rectipilus/Acanthocorticiumclade(100%BS,1.0BPP)thatissister(86%BS,
1.0BPP)toCyphellopsidaceae(Figure1a),andinthecladeofPhyllotopsidaceaesensu
Olariagaetal.[77]andKarasińskietal.[56],formingawell‐supportedclade(99%BS,1.0
BPP)withCyphelloporiarepresentatives(Figure1b).Othercyphelloidtaxa,suchas
CalathellacolumbianaAgerer(AY570993),ChromocyphellalamellataG.Moreno&Olariaga
(MF623831),andPhaeosoleniadensa(Berk.)W.B.Cooke(AY571018,AY571019)formed
independentlineageswithnoclearrelationshiptootherknownlineages(Figure1c).
ThefourbioluminescentlineagessensuDesjardinetal.[4]arerepresented(Figure
1a–d).TheMycenoidlineageisthelargestandformsamonophyleticgroupinawell‐
supported(99%BS,1.0BPP)clade(familyMycenaceae)representedinouranalyses
(Figure1c)by25speciesofthegeneraFiloboletus,Mycena,Panellus,andRoridomyces.The
Armillarialineage(Figure1d)ishererepresentedbyfivespeciesofthegenusArmillaria
thatclusteredinawell‐supported(92%BS,1.0BPP)cladesistertosequencesofCyptotrama
asprata(Berk.)Redhead&Ginns(KY418873)andXerulastrigosaZhuL.Yang,L.Wang&
G.M.Muell.(KF305680)withinPhysalacriaceae(97%BS,1.0BPP).TheOmphalotuslineage
isrepresented(Figure1d)bysixspeciesofOmphalotusandNeonothopanusthatformawell‐
and
bioluminescent species with the symbol
J.Fungi2023,9,xFORPEERREVIEW9of23
(d)
Figure1.(a–d)TheMLphylogenyofrepresentativecollectionsofAgaricomycetesbasedon
completeLSUrDNA.Voucher/strain/cloneorherbariumnumberaswellasGenBankaccession
numbersandcountryoforiginfollowtaxonname.Cyphelloidspeciesarenotedwiththesymbol◆
andbioluminescentspecieswiththesymbol
⚫
.Thenewspeciesishighlightedinred,andthe
luminescentlineagesareingray.Thickerlinesrepresentbrancheswithmaximumbootstrapvalues
andposteriorprobabilities(100%BS,1.0BPP).BootstrapvaluesandBayesianposteriorprobabilities
areindicatediftheyareequaltoorgreaterthan70%,and0.95,respectively.Thescalebarrepresents
theexpectednumberofnucleotidechangespersite.
Additionally,sequencesofthecyphelloidgeneraHenningsomycesKuntzeand
RectipilusAgererareresolvedintwophylogeneticallydistantclades:the
Henningsomyces/Rectipilus/Acanthocorticiumclade(100%BS,1.0BPP)thatissister(86%BS,
1.0BPP)toCyphellopsidaceae(Figure1a),andinthecladeofPhyllotopsidaceaesensu
Olariagaetal.[77]andKarasińskietal.[56],formingawell‐supportedclade(99%BS,1.0
BPP)withCyphelloporiarepresentatives(Figure1b).Othercyphelloidtaxa,suchas
CalathellacolumbianaAgerer(AY570993),ChromocyphellalamellataG.Moreno&Olariaga
(MF623831),andPhaeosoleniadensa(Berk.)W.B.Cooke(AY571018,AY571019)formed
independentlineageswithnoclearrelationshiptootherknownlineages(Figure1c).
ThefourbioluminescentlineagessensuDesjardinetal.[4]arerepresented(Figure
1a–d).TheMycenoidlineageisthelargestandformsamonophyleticgroupinawell‐
supported(99%BS,1.0BPP)clade(familyMycenaceae)representedinouranalyses
(Figure1c)by25speciesofthegeneraFiloboletus,Mycena,Panellus,andRoridomyces.The
Armillarialineage(Figure1d)ishererepresentedbyfivespeciesofthegenusArmillaria
thatclusteredinawell‐supported(92%BS,1.0BPP)cladesistertosequencesofCyptotrama
asprata(Berk.)Redhead&Ginns(KY418873)andXerulastrigosaZhuL.Yang,L.Wang&
G.M.Muell.(KF305680)withinPhysalacriaceae(97%BS,1.0BPP).TheOmphalotuslineage
isrepresented(Figure1d)bysixspeciesofOmphalotusandNeonothopanusthatformawell‐
. The new species is highlighted in red, and the luminescent
lineages are in gray. Thicker lines represent branches with maximum bootstrap values and posterior
probabilities (100% BS, 1.0 BPP). Bootstrap values and Bayesian posterior probabilities are indicated
if they are equal to or greater than 70%, and 0.95, respectively. The scale bar represents the expected
number of nucleotide changes per site.
The four bioluminescent lineages sensu Desjardin et al. [
4
] are represented (Figure 1a–d).
The Mycenoid lineage is the largest and forms a monophyletic group in a well-supported
(99% BS, 1.0 BPP) clade (family Mycenaceae) represented in our analyses (Figure 1c) by
25 species of the genera Filoboletus,Mycena,Panellus, and Roridomyces. The Armillaria lineage
(Figure 1d) is here represented by five species of the genus Armillaria that clustered in a well-
supported (92% BS, 1.0 BPP) clade sister to sequences of Cyptotrama asprata (Berk.) Redhead &
Ginns (KY418873) and Xerula strigosa Zhu L. Yang, L. Wang & G.M. Muell. (KF305680) within
Physalacriaceae (97% BS, 1.0 BPP). The Omphalotus lineage is represented (Figure 1d) by six
species of Omphalotus and Neonothopanus that form a well-supported (98% BS, 1.0 BPP) clade
corresponding to Omphalotaceae. The Lucentipes clade forms a well-supported (0.99 BPP)
independent lineage (Figure 1b) that contains, in addition to Gerronema viridilucens (EF514207)
and Mycena lucentipes (OR343215), sequences identified as Atheniela rutila Q. Na & Y.P. Ge,
(NG153951), Mycopan scabripes (Murrill) Redhead, Moncalvo & Vilgalys (MK278154), Hydropus
trichoderma (Joss.) Singer (MK278158), and Mycena cf. quiniaultensis Kauffman (EU681183). A
fifth bioluminescent lineage is composed of the proposed new genus Eoscyphella, represented
by two sequences of Eoscyphella luciurceolata sp. nov. (Figure 1a).
J. Fungi 2023,9, 1004 10 of 23
3.1.2. ITS rDNA Dataset
The final ITS rDNA dataset has 44 sequences (including 3 that are newly generated),
consisting of 1051 nucleotide sites, including gaps. The best evolutionary models estimated
for each part of the alignments were ITS1: TPM2uf+G, 5.8S: TPM2+G, and ITS2: HKY+G. The
bootstrapping criteria from the ML analysis stopped after 300 replicates. Both the RAxML
analysis and Bayesian inference yielded similar tree topologies. The ITS rDNA tree generated
from the ML analysis, including bootstrap and posterior probabilities, is shown in Figure 2.
J.Fungi2023,9,xFORPEERREVIEW11of23
Figure2.MLphylogenyofcollectionsofCyphellopsidaceaerepresentativesbasedoncompleteITS
rDNA.Thenewspeciesishighlightedinred.Voucher/strain/cloneorherbariumnumberaswellas
GenBankaccessionnumbersandcountryoforiginfollowtaxonname.Thickerlinesrepresent
brancheswithmaximumbootstrapvaluesandposteriorprobabilities(100%BS,1.0BPP).Bootstrap
valuesandBayesianposteriorprobabilitiesareindicatediftheyareequaltoorgreaterthan70%,
and0.95,respectively.Thescalebarrepresentstheexpectednumberofnucleotidechangespersite.
ThebootstrappingcriteriafromtheMLanalysisstoppedafter50replicates.Themost
likelytreegeneratedwiththeMLanalysisisshowninFigure3.Thefamily
Cyphellopsidaceae(100%BS,1.0BPP)isrepresentedby19terminals,withemphasison
theMerismodesclade(100%BS,1.0BBP),representedby12terminalsofMaireinaand
Figure 2.
ML phylogeny of collections of Cyphellopsidaceae representatives based on complete ITS
rDNA. The new species is highlighted in red. Voucher/strain/clone or herbarium number as well
as GenBank accession numbers and country of origin follow taxon name. Thicker lines represent
branches with maximum bootstrap values and posterior probabilities (100% BS, 1.0 BPP). Bootstrap
values and Bayesian posterior probabilities are indicated if they are equal to or greater than 70%, and
0.95, respectively. The scale bar represents the expected number of nucleotide changes per site.
J. Fungi 2023,9, 1004 11 of 23
The family Cyphellopsidaceae (100% BS, 1.0 BPP) is represented by 42 sequences,
with no representatives of Woldmaria nor Peyronelina due to lack of available sequences.
Eoscyphella luciurceolata sp. nov. and the non-bioluminescent Eoscyphella sp. formed a
well-supported clade (84% BS, 1.0 BPP), sister to (but not supported) a clade that contains
sequences of Dendrothele microspora (H.S. Jacks. & P.A. Lemke) P.A. Lemke, Dendrothele
incrustans (P.A. Lemke) P.A. Lemke, and Dendrothele griseocana (Bres.) Bourdot & Galzin
(Figure 2). The genus Maireina, represented by the same species as in the LSU rDNA
analyses, is again confirmed as paraphyletic with the ITS rDNA data. However, as in the
nLSU analyses, the included Maireina sequences form a monophyletic and well-supported
clade (91% BS, 1.9 BPP) when including sequences of Merismodes anomala,Me. fasciculata,
and Merismodes sp. (MZ919217).
3.1.3. Combined LSU rDNA + ITS rDNA Dataset
The final combined LSU rDNA plus ITS rDNA dataset contains 20 ITS rDNA and
16 LSU rDNA sequences (including 5 generated as part of this study) for 21 terminals,
and consists of 1806 nucleotide sites, including gaps. The most appropriate evolutionary
models estimated for each part of the alignments were ITS1: TPM2uf+G, 5.8S: TPM2, ITS2:
TPM2uf+G, and LSU: TIM3+G.
The bootstrapping criteria from the ML analysis stopped after 50 replicates. The most
likely tree generated with the ML analysis is shown in Figure 3. The family Cyphellopsi-
daceae (100% BS, 1.0 BPP) is represented by 19 terminals, with emphasis on the Merismodes
clade (100% BS, 1.0 BBP), represented by 12 terminals of Maireina and Merismodes. Consis-
tent with the other previous analyses, both the Bayesian inference and ML analysis recover
Maireina as a paraphyletic group (Figure 3).
J.Fungi2023,9,xFORPEERREVIEW12of23
Merismodes.Consistentwiththeotherpreviousanalyses,boththeBayesianinferenceand
MLanalysisrecoverMaireinaasaparaphyleticgroup(Figure3).
Figure3.MLphylogenyofCyphellopsidaceaefocusingoncollectionsofMerismodesrepresentatives
basedoncombinedITSrDNAandLSUrDNA.Thenewspeciesishighlightedinred.
Voucher/strain/cloneorherbariumnumberaswellasGenBankaccessionnumbersandcountryof
originfollowtaxonname.Thickerlinesrepresentbrancheswithmaximumbootstrapvaluesand
posteriorprobabilities(100%BS,1.0BPP).BootstrapvaluesandBayesianposteriorprobabilitiesare
indicatediftheyareequaltoorgreaterthan70%,and0.95,respectively.Thescalebarrepresents
theexpectednumberofnucleotidechangespersite.
3.2.TaxonomicPart
Frommolecularphylogeneticresults,weconsiderMaireinaasynonymofMerismodes
(=Cyphellopsis),supportingthetaxonomicconceptofKnudsenandVesterholt[61],who
consideredMaireina,Cyphellopsis,andPhaeocyphellopsisW.B.Cookesynonymsof
Merismodes.WehereinproposethecombinationofMa.monacha,Ma.filipendula,andMa.
subsphaerophoraintoMerismodes,aswellasthedescriptionofthegenusEoscyphellato
accommodatethenovelbioluminescentcyphelloidspeciesfromBrazil.
MerismodesEarle,BulletinoftheNewYorkBotanicalGarden5:406(1909)emend.Silva‐
Filho&Menolli
=CyphellopsisDonk,MededelingenvandeNederlandseMycologischeVereeniging
18–20:128(1931).
=MaireinaW.B.Cooke,BeiheftezurSydowia4:83(1961).
Figure 3.
ML phylogeny of Cyphellopsidaceae focusing on collections of Merismodes representatives
based on combined ITS rDNA and LSU rDNA. The new species is highlighted in red. Voucher/strain/clone
J. Fungi 2023,9, 1004 12 of 23
or herbarium number as well as GenBank accession numbers and country of origin follow taxon
name. Thicker lines represent branches with maximum bootstrap values and posterior probabilities
(100% BS, 1.0 BPP). Bootstrap values and Bayesian posterior probabilities are indicated if they are
equal to or greater than 70%, and 0.95, respectively. The scale bar represents the expected number of
nucleotide changes per site.
3.2. Taxonomic Part
From molecular phylogenetic results, we consider Maireina a synonym of Merismodes
(=Cyphellopsis), supporting the taxonomic concept of Knudsen and Vesterholt [
61
], who
considered Maireina, Cyphellopsis, and Phaeocyphellopsis W.B. Cooke synonyms of Merismodes.
We herein propose the combination of Ma. monacha,Ma. filipendula, and Ma. subsphaerophora
into Merismodes, as well as the description of the genus Eoscyphella to accommodate the
novel bioluminescent cyphelloid species from Brazil.
Merismodes
Earle, Bulletin of the New York Botanical Garden 5: 406 (1909) emend.
Silva-Filho & Menolli
=Cyphellopsis Donk, Mededelingen van de Nederlandse Mycologische Vereeniging
18–20: 128 (1931).
=Maireina W.B. Cooke, Beihefte zur Sydowia 4: 83 (1961).
=Phaeocyphellopsis W.B. Cooke, Beihefte zur Sydowia 4: 119 (1961).
=Pseudodasyscypha Velen., Novitates mycologicae: 167 (1939).
Original diagnosis [
79
]: Not pultrecent, densely connate-cespitose: pileus fleshy, irregu-
lar: lamellae reduced to obscure folds: spores white or hyaline: veil none: stipe irregular,
the bases fused.
Emended description: Basidiomata gregarious or scattered. Receptacle cyphelloid,
cupulate to tubular, sessile or pendant; outside covered with yellow brown to brown
hairs, hymenium pale, whitish. Subiculum absent or developed. External hyphae thick-
walled, not branched, straight, attenuated to spiraled towards the distal end, yellow
to brown pigmented, sometimes with apical ends colorless, tips incrusted or smooth,
obtuse to inflated, inamyloid to slightly dextrinoid. Trama gelatinous or non-gelatinous.
Basidiospores subglobose, ellipsoid, cylindrical, allantoid or subfusiform, smooth, thin-
walled, hyaline, inamyloid. Basidia cylindrical to clavate, four-spored, occasionally two-
spored. Cystidia absent or rarely present. Clamp connections present or absent.
Notes: After the very brief protologue, Knudsen and Vesterholt [
61
] included in
their description of Merismodes include some morphological characteristics of the genera
Maireina,Cyphellopsis, and Phaeocyphellopsis. In our emendation, we include additional
distinctive morphological characteristics of the species recently described [
52
–
54
] and of
Maireina based on Bodensteiner [
57
]. In all our analyses, the genus Maireina is resolved
as paraphyletic, forming a well-supported monophyletic lineage with the sequences of
Mersimodes included. Based on these results and those of previous investigators [
61
],
we consider Maireina a synonym of the latter genus and propose an amendment. The
name Merismodes, proposed in 1909 [
79
], has priority against Maireina erected in 1961 [
43
].
Thus, to better accommodate the Maireina species sampled in our analyses (which includes
sequences from holotype material), we propose the combination of Ma. filipendula and Ma.
subsphaerosphora in Merismodes. Additionally, a recently collected sample of Ma. monacha
(type species of Maireina) from France (same country locality of the holotype) was also
included in our analyses. The taxon is herein re-analyzed and confirmed in Merismodes and
an epitype is designated.
Merismodes monacha (Speg.) Silva-Filho, Mombert & Menolli comb. nov.
MycoBank: MB 849402
Figure 4a–d
Basionym:Cyphella monacha Speg., Michelia 2 (7): 303 (1881).
≡Cyphellopsis monacha (Speg.) D.A. Reid, Kew Bulletin 17: 297 (1963).
≡Maireina monacha (Speg.) W.B. Cooke, Beihefte zur Sydowia 4: 90 (1961).
J. Fungi 2023,9, 1004 13 of 23
=Cyphella bresadolae Grélet, Bulletin de la SociétéMycologique de France 38: 174 (1922).
=Cyphella bresadolae var. gregaria (Syd. & P. Syd.) Pilát, Annales Mycologici 23: 162
(1925).
=Cyphella bresadolae var. leochroma (Bres.) Grélet, Bulletin de la SociétéMycologique de
France 38: 174 (1922).
=Cyphella bresadolae var. tephroleuca (Bres.) Grélet, Bulletin de la SociétéMycologique
de France 38: 174 (1922).
=Merismodes bresadolae (Grélet) Singer, The Agaricales in modern taxonomy. 3rd ed. J.
Cramer, Lehre, Vaduz: 665 (1975).
=Cyphella gregaria Syd. & P. Syd., Hedwigia 39(3): 116 (1900).
=Cyphella leochroma Bres., Fungi Tridentini II (fasc. 14): 99, Table 211, f. 1 (1900).
=Cyphella obscura Roum., Fungi selecti gallici exsiccati. Michelia II, Cent. 20, no. 1905
(1882).
=Cyphella sydowii Bres., in SYDOW H, Mycotheca Marchica. Cent. 38, no. 3706 (1892).
=Cyphella tephroleuca Bres., Fungi Tridentini II (fasc. 11–13): 57, Table 166, f. 2 (1898).
=Maireina marginata (McAlpine) W.B. Cooke, Sydowia, Annales Mycologici, Beiheft 4:
89 (1962).
J.Fungi2023,9,xFORPEERREVIEW14of23
Figure4.Merismodesmonacha(ALV30536,Epitype–PC0142589).(a)Basidiomatainsitu;(b)
basidiospores;(c)basidium;(d)externalhyphae.PhotosbyAndgeloMombert.
Macro‐andmicro‐morphologicaldescription:Cooke[43].
Materialexamined:FRANCE,Cantal.St‐Santin‐de‐Maurs,onastill‐attacheddead
twigofCornussanguineaL.,28June2021.Leg.A.Mombert.,ALV30536[PC0142589,
Epitypeheredesignated!(validatedidentifier:MBT204394)].
Habitatandknowndistribution:OnbarkofdeadbranchofCornussanguineainoak
forestinFrance,butalsoAcercampestreL.(Aceraceae),BerberisvulgarisL.(Berberidaceae),
BupleurumfruticosumL.(Apiacaceae),HieraciumumbellatumL.(Asteraceae),Cytisussp.,
GenistatinctoriaL.,Sarothamnusscoparius(L.)Link(Fabaceae),Lonicerasp.(Caprifoliaceae),
PrunusamygdalusBatsch,P.persica(L.)Batsch(Rosaceae),QuercusmongolicaFisch.ex
Ledeb.(Fagaceae)[57].DistributedinEuropeandOceania[43].
Notes:OurspecimenagreeswiththedescriptionofMe.monachapresentedbyCooke
([43],asMa.monacha),whoanalyzedauthenticmaterialofallnamesincludedhereas
synonyms,includingthetypesofCyphellaobscuraRoum.andCyphellasydowiiBres.
AccordingtoCooke[43],Me.monachaischaracterizedbybrownreceptacleswithlonghairs
aroundthecupedgeandatthehymenialsurface,elongatetocylindricalbasidiospores,
four‐sporedbasidia,andcylindrical,yellowishbrowntobrownexternalhyphaewithpaler
apices.Althoughourmaterialhashadslightlybroaderreceptacles(1.5–3mmdiam.)and
basidia(9.0–110μmdiam.)thanreportedbyCooke[43](receptacles,0.5–1mmdiam.;
basidia,5.5–8.0μmdiam.),othermacro‐ andmicromorphologicalcharacteristicsare
sufficientfortheidentificationofthissampleasMa.monachasensuCooke[43]and
Bodensteiner[57].Merismodesmonachawasoriginallydescribedfromsamplescollectedin
FrancebutithasadistributionrecordedinmanyEuropeancountries,includingGermany,
Austria,Italy,theCzechRepublic,Hungary,theUnitedKingdom,andonerecordfrom
Australia[43].TheholotypeofCyphellamonachaSpeg.[anon.s.n.(Fung.Gall.768)
Figure 4.
Merismodes monacha (ALV30536, Epitype–PC0142589). (
a
) Basidiomata in situ; (
b
) basid-
iospores; (c) basidium; (d) external hyphae. Photos by Andgelo Mombert.
Macro- and micro-morphological description: Cooke [43].
Material examined: FRANCE, Cantal. St-Santin-de-Maurs, on a still-attached dead
twig of Cornus sanguinea L., 28 June 2021. Leg. A. Mombert., ALV30536 [PC0142589, Epitype
here designated! (validated identifier: MBT 204394)].
Habitat and known distribution: On bark of dead branch of Cornus sanguinea in oak
forest in France, but also Acer campestre L. (Aceraceae), Berberis vulgaris L. (Berberidaceae),
Bupleurum fruticosum L. (Apiacaceae), Hieracium umbellatum L. (Asteraceae), Cytisus sp.,
J. Fungi 2023,9, 1004 14 of 23
Genista tinctoria L., Sarothamnus scoparius (L.) Link (Fabaceae), Lonicera sp. (Caprifoliaceae),
Prunus amygdalus Batsch, P. persica (L.) Batsch (Rosaceae), Quercus mongolica Fisch. ex Ledeb.
(Fagaceae) [57]. Distributed in Europe and Oceania [43].
Notes: Our specimen agrees with the description of Me.monacha presented by Cooke
(ref. [
43
], as Ma. monacha), who analyzed authentic material of all names included here
as synonyms, including the types of Cyphella obscura Roum. and Cyphella sydowii Bres.
According to Cooke [
43
], Me. monacha is characterized by brown receptacles with long hairs
around the cup edge and at the hymenial surface, elongate to cylindrical basidiospores,
four-spored basidia, and cylindrical, yellowish brown to brown external hyphae with paler
apices. Although our material has had slightly broader receptacles (1.5–3 mm diam.) and
basidia (9.0–110
µ
m diam.) than reported by Cooke [
43
] (receptacles, 0.5–1 mm diam.; ba-
sidia, 5.5–8.0
µ
m diam.), other macro- and micromorphological characteristics are sufficient
for the identification of this sample as Ma. monacha sensu Cooke [
43
] and Bodensteiner [
57
].
Merismodes monacha was originally described from samples collected in France but it has
a distribution recorded in many European countries, including Germany, Austria, Italy,
the Czech Republic, Hungary, the United Kingdom, and one record from Australia [
43
].
The holotype of Cyphella monacha Speg. [anon. s.n. (Fung. Gall. 768) Spegazzini s.n.] was
deposited at the New York Botanical Garden Herbarium (NY). Considering the complete
morphological and molecular data recovered from our sample that is from a region close to
the type locality, we decided to designate the voucher ALV30536 as epitypus.
Merismodes filipendula (Læssøe) Silva-Filho & Menolli comb. nov.
MycoBank: MB 849405
Basionym: Maireina filipendula Læssøe, Karstenia 56 (1): 40 (2016).
Macro- and micro-morphological description: see Læssøe et al. [54].
Merismodes subsphaerospora (Mombert) Silva-Filho, Mombert & Menolli comb. nov.
MycoBank: MB 849406
Basionym: Maireina subsphaerospora Mombert, Bulletin Mycologique et Botanique
Dauphiné-Savoie 246: 38 (2022).
Macro- and micro-morphological description: see Mombert [55].
Eoscyphella Silva-Filho, Stevani & Menolli gen. nov.
MycoBank: MB 849403
Etymology: Eos = light of day; the goddess of dawn (Greek); cyphella (from kyfos in
Greek) = shape of a cup, something hollow. The prefix “Eos” is in reference to the light
emitted by the bioluminescent basidiomata of the type species. Additionally, the Roman
equivalent refers to Eosforos as Lucifer, which is the entity’s name that was later considered
into Christianity as the devil, and it also refers to the name of the protected area (Devil’s
Cave State Park) near where the specimens of the type species were found. The name
cyphella is a reference to the genus Cyphella and to the cyphelloid body form.
Type species: Eoscyphella luciurceolata Silva-Filho, Stevani & Desjardin (described below).
Diagnosis: Eoscyphella is morphologically similar to Merismodes and Woldmaria but
differs from Woldmaria in lacking conspicuous long hairs in the receptacle, subglobose
to broadly ellipsoid basidiospores, regularly bi-spored basidia, and unclamped hyphae;
and from Merismodes by the absence of conspicuous hairs in the receptacle, absence of
cystidia, regularly bi-spored basidia, and the characteristic external hyphae that are always
pigmented and encrusted at the tips.
Notes: Eoscyphella, typified here using Eoscyphella luciurceolata sp. nov., represents a new
lineage of bioluminescent fungi. It is supported with phylogenetic data
(Figures 1a, 2and 3)
and morphological characteristics, including the absence of conspicuous long hairs on the
receptacle, subglobose to broadly ellipsoid basidiospores, regularly bi-spored basidia, the
absence of clamp connections, and the consistent presence of pigmented and encrusted exter-
nal hyphae. An additional collection (FIPBIO 01) of a related non-bioluminescent cyphelloid
species was found in the same region of the type species. The ITS rDNA sequence data
J. Fungi 2023,9, 1004 15 of 23
(OR260255) resolves this taxon as sister to E. luciurceolata and suggests that it represents an
additional species of Eoscyphella (Figures 2and 3). The presence of a second species indicates
that Eoscyphella is likely a non-monospecific genus that includes both bioluminescent and
non-bioluminescent members. Until additional material of the non-bioluminescent taxon can
be collected to confirm these initial observations, we prefer to leave it undescribed.
Eoscyphella luciurceolata Silva-Filho, Stevani & Desjardin sp. nov. Figures 5–8.
J.Fungi2023,9,xFORPEERREVIEW16of23
and48°24′37.6812″W,alt.546m,22March2023,FBIPBio96.20230322,leg.IsaiasSantos,
AdãoHenriqueRosaDomingos,OlavoH.P.Della‐Torre(FIFUNGI0001,holotype!)
GenBank[ITSrDNA]:OR230671,[LSUrDNA]:OR230673.
Diagnosis:Eoscyphellaluciurceolatadiffersfromotherknownspeciesofcyphelloidfungi
bythefollowingcombinationofcharacters:receptaclevasiformtourceolatewithout
conspicuouslonghairs;externalhyphaecylindrical,sinuous,coiledtoconspicuouslyspiraled,
pigmented,weaklytodenselyincrustedoverall,lesssoneartheirtips,withsmallglobular
crystals;basidiosporessubglobosetoovoidorbroadlyellipsoid;basidiacylindricalto
subclavate,2‐spored(rarely4‐spored);hymenialcystidiaabsent;clampconnectionsabsent.
Figure5.Eoscyphellaluciurceolatabasidiomatainlight(above)anddark(below).(a–c)Onthebarkof
“fumeiro”tree(Solanumswartzianum).Notethatonlydrymushrooms,whosemarginisadornedwith
waterdroplets,emitlight.FBIPBio93.20220802(Paratype–FIFUNGI00249).PhotosbyAdãoHenrique
RosaDomingos.
Figure6.Eoscyphellaluciurceolatabasidiomatainlight(above)anddark(below)onremovedbarkof
“fumeiro”tree(Solanumswartzianum).Notethatmushroomsareinwetterconditionsandallofthem
emitlight.(a)Adriedmushroomisshownnexttoascalpelbladetodemonstrateitssize;(b)FBIPBio
93.20220802(Paratype–FIFUNGI00249).PhotosbyAdãoHenriqueRosaDomingosandIsaiasSantos.
Figure 5.
Eoscyphella luciurceolata basidiomata in light (above) and dark (below). (
a
–
c
) On the bark
of “fumeiro” tree (Solanum swartzianum). Note that only dry mushrooms, whose margin is adorned
with water droplets, emit light. FBIPBio 93.20220802 (Paratype–FIFUNGI00249). Photos by Adão
Henrique Rosa Domingos.
J.Fungi2023,9,xFORPEERREVIEW16of23
and48°24′37.6812″W,alt.546m,22March2023,FBIPBio96.20230322,leg.IsaiasSantos,
AdãoHenriqueRosaDomingos,OlavoH.P.Della‐Torre(FIFUNGI0001,holotype!)
GenBank[ITSrDNA]:OR230671,[LSUrDNA]:OR230673.
Diagnosis:Eoscyphellaluciurceolatadiffersfromotherknownspeciesofcyphelloidfungi
bythefollowingcombinationofcharacters:receptaclevasiformtourceolatewithout
conspicuouslonghairs;externalhyphaecylindrical,sinuous,coiledtoconspicuouslyspiraled,
pigmented,weaklytodenselyincrustedoverall,lesssoneartheirtips,withsmallglobular
crystals;basidiosporessubglobosetoovoidorbroadlyellipsoid;basidiacylindricalto
subclavate,2‐spored(rarely4‐spored);hymenialcystidiaabsent;clampconnectionsabsent.
Figure5.Eoscyphellaluciurceolatabasidiomatainlight(above)anddark(below).(a–c)Onthebarkof
“fumeiro”tree(Solanumswartzianum).Notethatonlydrymushrooms,whosemarginisadornedwith
waterdroplets,emitlight.FBIPBio93.20220802(Paratype–FIFUNGI00249).PhotosbyAdãoHenrique
RosaDomingos.
Figure6.Eoscyphellaluciurceolatabasidiomatainlight(above)anddark(below)onremovedbarkof
“fumeiro”tree(Solanumswartzianum).Notethatmushroomsareinwetterconditionsandallofthem
emitlight.(a)Adriedmushroomisshownnexttoascalpelbladetodemonstrateitssize;(b)FBIPBio
93.20220802(Paratype–FIFUNGI00249).PhotosbyAdãoHenriqueRosaDomingosandIsaiasSantos.
Figure 6.
Eoscyphella luciurceolata basidiomata in light (above) and dark (below) on removed bark of
“fumeiro” tree (Solanum swartzianum). Note that mushrooms are in wetter conditions and all of them
emit light. (
a
) A dried mushroom is shown next to a scalpel blade to demonstrate its size; (
b
) FBIPBio
93.20220802 (Paratype–FIFUNGI00249). Photos by Adão Henrique Rosa Domingos and Isaias Santos.
J. Fungi 2023,9, 1004 16 of 23
J.Fungi2023,9,xFORPEERREVIEW17of23
Figure7.Eoscyphellaluciurceolata(FBIPBio96.20230322,holotype–FIFUNGI0001).(a)Basidiospores;
(b)basidia;(c)hymeniumandexternalsurface;(d,e)externalhyphae.PhotosbyAlexandreG.S.
Silva‐FilhoandCristianoC.Nascimento.
Figure8.Eoscyphellaluciurceolata(FBIPBio96.20230322,holotype‐FIFUNGI0001.(a)Basidiospores;
(b)hymeniumwithbasidiaandbasidioles;(c)basidia;(d,e)externalhyphae.Drawings:originalby
AlexandreG.S.Silva‐FilhoandinkedbyK.Sousa.
Figure 7.
Eoscyphella luciurceolata (FBIPBio 96.20230322, holotype–FIFUNGI0001). (
a
) Basidiospores;
(
b
) basidia; (
c
) hymenium and external surface; (
d
,
e
) external hyphae. Photos by Alexandre G. S.
Silva-Filho and Cristiano C. Nascimento.
J.Fungi2023,9,xFORPEERREVIEW17of23
Figure7.Eoscyphellaluciurceolata(FBIPBio96.20230322,holotype–FIFUNGI0001).(a)Basidiospores;
(b)basidia;(c)hymeniumandexternalsurface;(d,e)externalhyphae.PhotosbyAlexandreG.S.
Silva‐FilhoandCristianoC.Nascimento.
Figure8.Eoscyphellaluciurceolata(FBIPBio96.20230322,holotype‐FIFUNGI0001.(a)Basidiospores;
(b)hymeniumwithbasidiaandbasidioles;(c)basidia;(d,e)externalhyphae.Drawings:originalby
AlexandreG.S.Silva‐FilhoandinkedbyK.Sousa.
Figure 8.
Eoscyphella luciurceolata (FBIPBio 96.20230322, holotype-FIFUNGI0001. (
a
) Basidiospores;
(b) hymenium with basidia and basidioles; (c) basidia; (d,e) external hyphae. Drawings: original by
Alexandre G. S. Silva-Filho and inked by K. Sousa.
J. Fungi 2023,9, 1004 17 of 23
MycoBank: MB 849404
Etymology: Luci = light (Latin); urceolus = diminutive of urceus “pitcher” (Latin), in
reference to urceolate shape of the receptacle. Since bioluminescent and non-bioluminescent
species occur in the genus, the prefix “Luci” is here applied to differentiate this new species
from putative non-bioluminescent ones.
Holotype: BRAZIL, São Paulo state, Eldorado, approximately 500 m west of the
entrance to the “Caverna do Diabo” (Devil’s Cave) State Park, but still in the buffered
conservation area, on a single “fumeiro” tree (Solanum swartzianum Roem. & Schult.),
24
◦
38
0
14.0100
00
S and 48
◦
24
0
37.6812
00
W, alt. 546 m, 22 March 2023, FBIPBio 96.20230322,
leg. Isaias Santos, Adão Henrique Rosa Domingos, Olavo H. P. Della-Torre (FIFUNGI0001,
holotype!) GenBank [ITS rDNA]: OR230671, [LSU rDNA]: OR230673.
Diagnosis: Eoscyphella luciurceolata differs from other known species of cyphelloid
fungi by the following combination of characters: receptacle vasiform to urceolate without
conspicuous long hairs; external hyphae cylindrical, sinuous, coiled to conspicuously
spiraled, pigmented, weakly to densely incrusted overall, less so near their tips, with
small globular crystals; basidiospores subglobose to ovoid or broadly ellipsoid; basidia
cylindrical to subclavate, 2-spored (rarely 4-spored); hymenial cystidia absent; clamp
connections absent.
Basidiomata scattered (Figures 5and 6). Receptacle 0.3–0.5 mm tall, 0.2–0.3 mm
diam, vasiform to urceolate, sessile (astipitate), with distinct opening; external surface
dull, dry, felted to appressed-pubescent, conspicuous long hairs absent, pale yellow (2A3)
to greyish yellow (2B3, 4B5) or greyish orange (5B4), white (1A–B1) near the distal open-
ing
(Figures 5c and 6b;
subiculum absent; hymenial surface greyish yellow (2C4), smooth.
External hyphae 60–128
×
2.0–4.0
µ
m, cylindrical, sinuous to coiled, yellowish brown to
brownish orange in water or KOH, weakly to densely incrusted overall, less so near the tips,
with small globular crystals, thick-walled (0.5–1.5 um thick), thinner near the tip, inamy-
loid, non-gelatinous, unclamped; terminal cells narrowed towards the tip to
1.5–2.0 µm
diam, tips hyaline to pale yellowish brown, obtuse to subacute, those at the margin of the
pore hyaline and conspicuously spiraled (Figures 7c–e and 8d–e); dendrohyphidia absent.
Trama composed of an interwoven layer of irregularly cylindrical to inflated, short-celled
hyphae 3.0–9.5
µ
m diam, hyaline to pale yellowish brown, much-branched, non-incrusted,
non-gelatinous, thin- to thick-walled (0–0.5
µ
m thick), unclamped (Figure 7c). Subhy-
menial layer composed of cylindrical hyphae 3.0–4.0
µ
m diam, hyaline, thin- to thick-
walled (
0.5–1.5 µm
thick), unclamped. Basidiospores
(6.5–)7.5–9.5 ×(5.5–)6.5–8(–9.5) µm
[xm = 8.56
±
0.13
×
7.35
±
0.29
µ
m, xr = 8.5–8.7
×
7.1–7.6
µ
m, Q = 1.0–1.6,
Qm = 1.18 ±0.05,
n = 60, s = 3], subglobose to ovoid or broadly ellipsoid, predominantly subglobose, smooth,
hyaline, inamyloid, sometimes one- or two-guttulate, hilar appendix up to 1
µ
m long, thin-
or thick-walled (0.5–1.0
µ
m) at maturity (Figures 7a and 8a). Basidia
22–32 ×7.0–10.0 µm,
cylindrical to subclavate, two-spored, rarely four-spored, hyaline, sometimes with refrin-
gent contents, unclamped; sterigmata up to 12
µ
m long (Figures 7b and 8b). Basidioles
subclavate (Figures 7c and 8b). Hymenial cystidia absent (Figure 7c). Clamp connections
absent in all tissues examined. Bioluminescence: emitting yellowish green light only in a
narrow band around the pore margin of the receptacle; water droplets likely magnify the
light (Figures 5and 6).
Additional specimens examined: BRAZIL, São Paulo state, Eldorado, exact same
location, and tree described above, 2 August 2023, FBIPBio 93.20220802, leg. Isaias Santos,
Adão Henrique Rosa Domingos, Olavo H. P. Della-Torre (FIFUNGI00249, Paratype!); ibid,
20 September 2022, FBIPBio 94.20220920 (FIFUNGI00250, Paratype!) GenBank [ITS rDNA]:
OR230672, [LSU rDNA] OR230674.
Habitat and known distribution: On bark of “fumeiro” tree (Solanum swartzianum) in
the Atlantic Rainforest, southern Brazil. Known only from the type locality.
Notes: When morphologically compared with other cyphelloid species, Maireina
spiralis (Coker) W.B. Cooke has external hyphae with spiral tips, differing from E. luciurceo-
lata in the clamped hyphae and with longer (11–15
µ
m long) ellipsoid basidiospores [
43
].
J. Fungi 2023,9, 1004 18 of 23
Maireina afibulata Bodensteiner and Ma. pseudochracea W.B. Cooke do not produce clamp
connection, but the first has smaller basidiospores (5–6(–6.5)
×
3–4
µ
m) and both have
straight external hyphae and produce smaller basidia (6–23
×
5–6.5
µ
m in Ma. afibulata;
17.5 ×5.8 µm in Ma. pseudochracea) with four sterigma [43,53].
4. Discussion
The morphological delimitation of Merismodes,Cyphellopsis, and Maireina has been
the cause of debates about the morphological limits of these genera [
43
,
51
,
57
,
62
,
80
–
83
].
Reid [
81
] considered Cyphellopsis and Maireina as synonyms and suggested that the depth
of the cavity that lined the hymenium is a character insufficient for the separation of
Cyphellopsis
(=Maireina) and Merismodes. Singer [
83
] synonymized the genus
Cyphellopsis
and Maireina with Merismodes and listed both Maireina and Cyphellopsis as sections. The
first broad research on cyphelloid fungi based on molecular phylogenetic analyses re-
solved Merismodes and Cyphellopsis as a monophyletic group, recognizing them as a
single genus [
45
]. Another broad study of Maireina without molecular data led Boden-
sterner [
53
,
57
] to recognize the genus Maireina as an independent lineage from Merismodes
and Cyphellopsis. Knudsen and Vesterholt [
61
] recognized Cyphellopsis,Maireina, and Phaeo-
cyphellopsis as synonyms of Merismodes, providing a broad description for the genus. The
first works to describe new species of Maireina based in-part on molecular data are those
of Læssøe et al. [
54
] and Mombert [
55
]. In both, the sequences of Maireina clustered with
Merismodes and Cyphellopsis in a large clade, making it possible to determine the phylo-
genetic position within Cyphellopsidaceae. Our phylogenetic analyses in separate and
combined LSU rDNA and ITS rDNA recognized Merismodes,Cyphellopsis, and Maireina as a
monophyletic group, supporting the proposal of Knudsen and Vesterholt [
61
] for a broad
morphological concept of Merismodes. The samples and sequences of Me. monacha, type
species of Maireina, first studied by Mombert [
55
] were extremely important for the recog-
nition and the phylogenetic positioning of the genus Maireina. Although the sequences are
not of the holotype specimen, the collection is from a region very close to the type locality,
and the morphological description agrees with the complete redescription presented by
Cooke [43].
Our cyphelloid bioluminescent samples were initially identified within the mor-
phological concept of Maireina sensu Bodensteiner [
53
,
57
]. However, our phylograms
(Figures 1a, 2and 3)
showed a phylogenetic distance between E. luciurceolata and Me.
monacha, which are only 90.6% to 90.7% similar in the LSU rDNA and 64.6% to 65.9%
similar in the ITS rDNA. Eoscyphella is closely related to the genus Woldmaria in our analy-
ses, but the included taxa are 7.3% to 7.4% divergent in their LSU rDNA sequences, a high
value considering a similarity threshold of around 96.91% to discriminate genera using
LSU rDNA in Basidiomycota [
84
]. These data and results support the proposition of a
new cyphelloid genus and distinct molecular lineage. Additionally, Eoscyphella is also mor-
phologically well delimited with receptacles that lack conspicuous long hairs, subglobose
to broadly ellipsoid basidiospores, frequently bi-spored basidia, unclamped hyphae, and
weakly to densely incrusted overall external hyphae, which are always pigmented and
encrusted at the tips.
Regarding the cyphelloid genera within Agaricomycetes, our LSU rDNA analyses
retrieved 11 lineages of cyphelloid fungi and the phylogenetic relationship of the cyphel-
loid genera agrees with recent phylogenetic studies [
45
,
50
,
56
]. However, we highlight
that sequences of the collection PB327 named as Calathella columbiana appear in different
positions and for this reason were excluded from the combined analyses: in the ITS rDNA
tree within Cyphellopsidaceae (Figure 2), and in the LSU rDNA tree (Figure 1c) in a clade
close to representatives of Entolomataceae. Additionally, Phaeosolenia densa (Berk.) W.B.
Cooke was shown by Bodensteiner et al. [
45
] to be close to the genus Tubaria (W.G. Sm.)
Gillet, whilst in our analyses, it forms an isolated clade without support (Figure 1c).
Desjardin et al. [4] performed the second review of bioluminescent fungi worldwide,
referring 64 luminescent species into three lineages, Armillaria, Mycenoid, and Omphalotus,
J. Fungi 2023,9, 1004 19 of 23
indicating that Gerronema viridilucens and Mycena lucentipes do not belong to the Mycenoid
lineage. Later, Desjardin et al. [
24
] referred G. viridilucens and M. lucentipes to a new and
unnamed lineage, which was later named the Lucentipes lineage by Oliveira et al. [
35
]. Our
LSU rDNA phylogram (Figure 1b) shows and confirms G. viridilucens plus M. lucentipes as
a separate bioluminescent lineage. The Eoscyphella lineage is here recognized as a new and
fifth bioluminescent lineage in Cyphellopsidaceae (Figure 1a).
From previous phylogenetic analyses, G. viridilucens has been proposed within Porothe-
leaceae [
70
,
71
]. However, our LSU rDNA phylogram (Figure 1b) showed Porotheleaceae,
represented by type species of the genus Hydropus [Hydropus fuliginarius (Batsch) Singer,
AF261368], forming a well-supported clade (94%, BS, 0.99 BPP) that harbors most of the
species of Gerronema Singer, except G. viridilucens, which clustered with sequences of M.
lucentipes,Atheniella rutilla (NG153951), Hydropus trichoderma (MK278154), Mycena cf. quini-
aultensis (EU681183), and Mycopan scabripes (MK278154) in a clade phylogenetically distant
from Porotheleaceae. Vizzini et al. [
70
] showed the genera Acanthocorticium Baltazar, Gorjón
& Rajchenb.; Athelia Pers.; Atheniella Redhead, Moncalvo, Vilgalys, Desjardin & B.A. Perry;
Baeospora Singer; Calyptella;Campanophyllum Cifuentes & R.H. Petersen; Cheimonophyllum
Singer; Chondrostereum Pouzar; Cyphella;Granulobasidium Jülich; Gloeostereum S. Ito & S.
Imai; Mycopan Redhead, Moncalvo & Vilgalys; Pleurella E. Horak; Henningsomyces; and
Rectipilus as part of the Henningsomyces/Rectipius/Acanthocorticium clade, with all accommo-
dated in Cyphellaceae. Due to the close relationship between Atheniella and Mycopan, most
of the genera of Cyphellaceae sensu Vizzini et al. [
70
] were included in our phylogeny in
order to confirm the phylogenetic position of G. viridilucens plus Mycena lucentipes. How-
ever, in our LSU rDNA analyses (Figure 1a,b), Cyphellaceae sensu Vizzini et al. [
70
] was
retrieved as a polyphyletic group, with representatives grouped into five different clades.
In the LSU rDNA phylogram (Figure 1b) Cyphellaceae can be well represented by the clade
with sequences of Cyphella digitalis (Alb. & Schwein.) Fr. (AY29293175 and AY635771), Chei-
monophyllum candidissimum (Sacc.) Singer (DQ457654), and Campanophyllum proboscideum
(Fr.) Cifuentes & R.H. Petersen (AY230866). Thus, it is confirmed that G. viridilucens and
Mycena lucentipes are positioned neither in Porothelleaceae nor in Cyphellaceae.
5. Conclusions
Our systematic study confirms the findings of previous studies regarding the existence
of multiple bioluminescent lineages in Agaricales. All bioluminescent fungi have currently
been described in suborder Marasmiineae Aime, Dentinger & Gaya. The newly described
Eoscyphella luciurceolata was confirmed from molecular phylogenies in the family Cyphel-
lopsidaceae, currently accepted within the suborder Schizophyllineaeae Aime, Dentinger &
Gaya [
62
]. Additionally, our study reveals a new lineage within a group primarily consist-
ing of reduced forms. Fungal bioluminescence engages in a cyclical process of biosynthesis
known as the Caffeic Acid Cycle (CAC), which relies on a sequence of four consecutive
enzymes: hispidin synthase (HispS), hispidin-3-hydroxylase (H3H), luciferase (Luz), and
caffeylpyruvate hydrolase (CPH) [
3
]. At present, there are limited genomic data concerning
bioluminescent fungi in the existing literature [85], with the majority originating from the
Mycenoid and Armillaria lineages. By identifying this recently discovered bioluminescent
lineage and uncovering the sequences of the hisps,h3h,luz, and cph genes, there is potential
for enhancing our understanding of the evolutionary progression of the bioluminescent
trait within the fungal kingdom.
A high diversity of bioluminescent fungi has been discovered in Brazil, with 23 species
(including our new described species) reported theretofore, see [
86
]. In the Brazilian
Atlantic Rainforest, new species of bioluminescent fungi have been described or reported,
e.g., [
87
], with emphasis to the southwestern portion of the state of São Paulo, the same
area where E. luciurceolata was found and where another 12 species of Mycenoid and
Lucentipes lineage taxa have already been described or reported [
22
–
25
]. Even so, new
bioluminescent samples collected at the same area are currently in the process of molecular
and morphological characterization and may represent taxonomic novelties, demonstrating
J. Fungi 2023,9, 1004 20 of 23
that the Atlantic Rainforest in the southwestern region of the São Paulo state is one of the
most studied areas of bioluminescent fungi and may represent a biodiversity hot spot for
these organisms.
Supplementary Materials:
The following supporting information can be downloaded at: https://
www.mdpi.com/article/10.3390/jof9101004/s1, Table S1: List of specimens; culture, herbarium access
number, isolate, strain, or voucher collection (V); and GenBank accession numbers.
Author Contributions:
Conceptualization, A.G.S.S.-F., C.V.S. and N.M.J.; Resource, A.M., B.B.N.,
B.A.P., C.C.N., D.E.D., D.M.M.S., A.G.S.M., A.H.R.D., I.S. and O.H.P.D.-T.; Writing: A.G.S.S.-F., C.V.S.,
D.E.D., B.A.P. and N.M.J.; and Funding, C.V.S. and N.M.J. All authors have read and agreed to the
published version of the manuscript.
Funding:
This work was supported by “Fundação de Amparo àPesquisa do Estado de São Paulo”
(FAPESP) under grant numbers 2018/15677-0 (N.M.J.), 2021/09109-1 (A.G.S.S.-F.), 2020/16000-3
(B.B.N.), 2019/12605-0 and 2022/14964-0 (D.M.M.S.), and 2017/22501-2 (C.V.S.), and by the Brazil-
ian National Council for Scientific and Technological Development (CNPq) under grant numbers
314236/2021-0 (N.M.J.) and 303525/2021-5 (C.V.S.). This work was also supported with funding from
the Office of Naval Research Global through grant ONRG N62909-17-1-2023 to C.V.S. and D.E.D.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement:
The DNA sequence data obtained in this study were deposited at
GenBank. The accession numbers can be found in the trees and in Supplementary Table S1. This
study is according to the Brazilian legislation on access to biodiversity and is registered in the “Sistema
Nacional de Gestão do Patrimônio Genético e do Conhecimento Tradicional Associado” (SisGen
#A5A80A7).
Acknowledgments:
The authors thank Alexandro Andrade and Jefferson Góis for the initial taxo-
nomic support, Suzana Ehlin Martins for the taxonomic identification of the host plant, Dimitrios
Floudas for suggesting the Greek prefix of the new generic name and also for helping to compose
the etymology of the new genus, and the anonymous reviewers for improvements to the original
manuscript. We are also grateful to “Fundação Florestal” and “Secretaria do Meio Ambiente do
Estado de São Paulo” for the collection licenses (process #260108-010.245/2017).
Conflicts of Interest: The authors declare no conflict of interest.
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