This paper is published in a part-themed issue of

Photochemical & Photobiological Sciences containing

papers on

Bioluminescence

Guest edited by Vadim Viviani

Published in issue 2, 2008 of Photochemical &

Photobiological Sciences.

Other papers in this issue:

Firefly luminescence: A historical perspective and recent developments

Hugo Fraga, Photochem. Photobiol. Sci., 2008, 146 (DOI: 10.1039/b719181b)

The structural origin and biological function of pH-sensitivity in firefly luciferases

V. R. Viviani, F. G. C. Arnoldi, A. J. S. Neto, T. L. Oehlmeyer, E. J. H. Bechara and Y.
Ohmiya, Photochem. Photobiol. Sci., 2008, 159 (DOI: 10.1039/b714392c)

Fungi bioluminescence revisited

Dennis E. Desjardin, Anderson G. Oliveira and Cassius V. Stevani , Photochem. Photobiol.
Sci., 2008, 170 (DOI: 10.1039/b713328f)

Activity coupling and complex formation between bacterial luciferase and flavin
reductases
Shiao-Chun Tu, Photochem. Photobiol. Sci., 2008, 183 (DOI: 10.1039/b713462b)

Coelenterazine-binding protein of Renilla muelleri: cDNA cloning, overexpression, and

characterization as a substrate of luciferase
Maxim S. Titushin, Svetlana V. Markova, Ludmila A. Frank, Natalia P. Malikova, Galina A.
Stepanyuk, John Lee and Eugene S. Vysotski, Photochem. Photobiol. Sci., 2008, 189 (DOI:
10.1039/b713109g)

The reaction mechanism for the high quantum yield of Cypridina (Vargula)
bioluminescence supported by the chemiluminescence of 6-aryl-2-methylimidazo[1,2-
a]pyrazin-3(7H)-ones (Cypridina luciferin analogues)
Takashi Hirano, Yuto Takahashi, Hiroyuki Kondo, Shojiro Maki, Satoshi Kojima, Hiroshi
Ikeda and Haruki Niwa, Photochem. Photobiol. Sci., 2008, 197 (DOI: 10.1039/b713374j)

C-terminal region of the active domain enhances enzymatic activity in dinoflagellate

luciferase
Chie Suzuki-Ogoh, Chun Wu and Yoshihiro Ohmiya, Photochem. Photobiol. Sci., 2008, 208
(DOI: 10.1039/b713157g)

Combining intracellular and secreted bioluminescent reporter proteins for multicolor

cell-based assays
Elisa Michelini, Luca Cevenini, Laura Mezzanotte, Danielle Ablamsky, Tara Southworth,
Bruce R. Branchini and Aldo Roda, Photochem. Photobiol. Sci., 2008, 212 (DOI:
10.1039/b714251j)

Interaction of firefly luciferase with substrates and their analogs: a study using
fluorescence spectroscopy methods
Natalia N. Ugarova, Photochem. Photobiol. Sci., 2008, 218 (DOI: 10.1039/b712895a)
PERSPECTIVE www.rsc.org/pps | Photochemical & Photobiological Sciences

Fungi bioluminescence revisited†

Dennis E. Desjardin,a Anderson G. Oliveirab and Cassius V. Stevani*b
Received 3rd September 2007, Accepted 3rd January 2008
First published as an Advance Article on the web 24th January 2008
DOI: 10.1039/b713328f

A review of the research conducted during the past 30 years on the distribution, taxonomy, phylogeny,
ecology, physiology and bioluminescence mechanisms of luminescent fungi is presented. We recognize
64 species of bioluminescent fungi belonging to at least three distinct evolutionary lineages, termed
Omphalotus, Armillaria and mycenoid. An accounting of their currently accepted names, distributions,
citations reporting luminescence and whether their mycelium and/or basidiomes emit light are
provided. We address the physiological and ecological aspects of fungal bioluminescence and provide
data on the mechanisms responsible for bioluminescence in the fungi.

Introduction Historia Naturalis that bioluminescent white fungi, sweet in taste

and with pharmacological properties, could be found in France
Harvey’s A History of Bioluminescence covers the physics, chem- on decaying trees. Interestingly, G. E. Rumph (1637–1706), a
istry, and biology of diverse luminescence phenomena, including Dutch physician, merchant and consul of Amboine (Moluccas,
a detailed description of bioluminescence.1 Therein we learn Indonesia), reported in his Herbarium Amboiense that natives
that light emission by living organisms has been noticed and were able to illuminate their path in the dark forest carrying
documented since ancient times by many philosophers and bioluminescent fruiting bodies in their hands. Harvey pointed out
scientists.1 According to Harvey, Aristotle (384–322 BC) first uncommon uses of luminous mushrooms 200 hundred years later
described light emission from rotten wood and distinguished this in Micronesia, where natives used them on their head as ornaments
living light from fire.1 Pliny the Elder (23–79) mentioned in his in ritual dances or crushed them on their face in order to scare their
enemies. Curiously, these mushrooms were frequently destroyed as
a
San Francisco State University, Dept. of Biology, 1600 Holloway Ave., San they were considered a bad omen.1
Francisco, CA 94132, USA
b
Instituto de Quı́mica da Universidade de São Paulo, Caixa Postal 26077, Despite Aristotle’s and Pliny’s writings on bioluminescent
05599-970, São Paulo, SP, Brazil. E-mail: [email protected] mushrooms and reports by botanists on the distribution of
† This paper was published as part of the themed issue on bioluminescence. luminous mushrooms, early attention was focused mainly on

Dennis E. Desjardin studied

with Prof. Harry D. Thiers at
San Francisco State University
(SFSU) from 1981–1985 (BSc
1983, MSc 1985) and completed
his PhD in 1989 at University
of Tennessee under supervision of
Prof. Ron Petersen. He is Biology
Professor at SFSU concentrating
in the area of fungi taxonomy and
being responsible for the identi-
fication of more than 150 new
species worldwide. He is currently
Dennis E. Desjardin Anderson G. Oliveira Cassius V. Stevani Director of the H. D. Thiers
Herbarium at SFSU.
Anderson Garbuglio de Oliveira was born in Agudos, São Paulo. He received his BSc in Chemistry in 2004 from the Universidade Federal
de Santa Catarina in Florianópolis (UFSC). In 2005 he moved to São Paulo to study the mechanism of fungi bioluminescence under the
supervision of Prof. Cassius Vinicius Stevani at IQ-USP.
Cassius Vinicius Stevani received his BSc in Chemistry in 1992 from the Chemistry Institute of University of São Paulo (IQ-USP). He
completed his PhD in Organic Chemistry in 1997 at IQ-USP under supervision of Prof. Josef W. Baader studying the mechanism involved in
the chemiluminescent reaction of light-sticks. Between 1998–2000 he was a post-doctoral fellow working with Prof. Etelvino J. H. Bechara
at IQ-USP. Currently, he lectures in Organic and Environmental Organic Chemistry at IQ-USP as Assistant Professor.

170 | Photochem. Photobiol. Sci., 2008, 7, 170–182 This journal is © The Royal Society of Chemistry and Owner Societies 2008
the light emitted from rotten wood instead on the fungi. Light influenced by environmental factors, comprehensive descriptions
emission was only directly linked to the fungi in the first half that include data on all cell and tissue types that comprise the
of the nineteenth century.1 J. F. Heller (1813–1871), professor reproductive structures of individuals from numerous populations
at Vienna University, was the first to correlate cause and effect are necessary for accurate species diagnoses. These micro-data are
attributing to fungi and bacteria the light exhibited by decaying usually absent from most descriptions published prior to the 1950s.
wood and animals, respectively. A modern appraisal of this Consequently, many synonyms have been published and many
subject was provided by W. Pfeffer (1845–1920),1 who applied of the species listed by Wassink4 remained poorly known until
to bioluminescent fungi the terms luciferin and luciferase coined recently. Concerted efforts by a number of fungal taxonomists to
by Dubois for the thermo-stable (substrate) and labile (enzyme) study exsiccati (type or authentic specimens) and to recollect and
factors.2,3 redescribe luminescent species has lead to the clarification of many
In this work we revisit, expand and update Wassink’s 19784 species concepts.10–13 In addition, Desjardin and colleagues14–16
review of the taxonomy and bioluminescence mechanisms in have discovered a number of new species and new luminescence
fungi. The number of reported bioluminescent fungus species in accounts of species from Brazil to add to the growing list of
the world is reevaluated to include the many new species that luminescent fungi (Fig. 1).
we discovered since 2005. In addition, we discuss evolutionary
aspects of bioluminescence in the fungi and raise hypotheses on
the molecular mechanisms underlying the bioluminescent pathway
based on the literature and our own observations. Our revision is
focused on fungi bioluminescence defined as a chemical reaction
that occurs in fungi leading to constant light emission with max-
imum intensity in the range 520–530 nm whose chemiexcitation
step is catalyzed by an enzyme generally called luciferase. This
phenomenon should not be confused with transient, low-level or
ultraweak chemiluminescence that often increases in response to
oxidative stress (e.g., elevated O2 concentrations or introduction
of ROS-generating compounds) wherein light may be emitted
from singlet oxygen, triplet excited states, reactions of ONOO− ,
lipoxygenase activity, heme protein-peroxide reactions and Fenton
chemistry.5 The latter phenomenon, reported from some yeasts
and other fungi,4 will not be treated herein.

Taxonomy and evolutionary aspects of fungi

bioluminescence
In 1978,4 Wassink updated his review of luminescent fungi
published in 19486 and that of Harvey,7 wherein he treated 42
taxa with verified or questionable luminescent properties. His
review included a reevaluation of the taxonomic status, synonymy,
and luminescent characteristics of all species reported before
1945 (19 species), and detailed accounts of newly described or
rediscussed luminous species reported between 1946 and 1978
(23 species). In addition he provided lists of species of uncertain
taxonomic position (16 epithets) and of doubtful bioluminescent
capabilities (17 epithets). Many of the new accounts represented
species described from Malaysia, Japan and the South Pacific, but
unfortunately many of these epithets were invalidly published.8,9
In addition, the protologues provided only limited morphological
data making identification of subsequent collections difficult, and
consequently, vouchered reports of most of the Asian species have
not been published since.
Significant strides have been made in the past 30 years Fig. 1 Images of bioluminescent fungi taken in natural light (left) and
in the dark (right). (A) Culture of Mycena aff. euspeirea on agar isolated
in augmenting our knowledge of the occurrence, distribution,
from basidiomes collected in the El Verde Research Area, Puerto Rico.
ecology, taxonomy and phylogeny of luminescent fungi. For
(B) Naturally bioluminescent twigs inhabited by mycelium of undeter-
most fungi, populations are delimited into species based on a mined basidiomycetous fungi collected in Parque Estadual Turı́stico do
suite of shared morphological features, with distinctions between Alto Ribeira (PETAR), São Paulo State, Brazil. (C) Filoboletus manipularis
species often being subtle differences in the macro- and micromor- collected in Negeri Sembilan Prov., Malaysia. (D) Gerronema viridilucens
phological characteristics of their sexual reproductive structures. collected in PETAR, São Paulo State, Brazil. (E) Mycena lucentipes
Because macromorphological features are quite plastic and easily collected in PETAR, São Paulo State, Brazil.

This journal is © The Royal Society of Chemistry and Owner Societies 2008 Photochem. Photobiol. Sci., 2008, 7, 170–182 | 171
 A biological species concept can be applied to species that species Nothopanus noctilucens, Pleurotus decipiens and Pleurotus
cooperate in vitro. For many saprotrophic fungal species, single eugrammus var. radicicolus, and the Brazilian species Pleurotus
spores can be isolated, mated on select media, and their ability gardneri. In the most current and comprehensive phylogeny of
to dikaryotize and develop into new individuals can be evaluated. euagaric lineages,28 the luminescent Omphalotus lineage is sister to
Hence, interbreedability and genetic exchange can be tested. An the non-luminescent gymnopoid fungi (Gymnopus, Marasmiellus,
evolutionary species concept may be applied when molecular Lentinula and others sensu Wilson and Desjardin)34 and distantly
sequences datasets are generated and clades of terminal taxa in related to any of the other known luminescent fungi.
resultant phylogenetic analyses are used to inform taxonomic
decisions. The application of these new techniques of mating Armillaria lineage
system studies17–21 and phylogenetic analyses22–26 are helpful in
delimiting the taxonomic boundaries of species and have been Armillaria species, commonly called the Honey Mushroom, are
used to clarify species concepts in a number of luminescent fungi. well-known edible fungi that are saprotrophs or problematical
Phylogenetic analyses of multiple loci datasets have greatly forest tree root pathogens. They form creamy-white mycelial
advanced our understanding of relationships amongst the fungi fans and coarse black rhizomorphs as infection, exploratory
and have allowed a first glimpse at the phylogenetic placement and transport organs. It is the mycelium, mycelial fans and
of bioluminescent fungi. After extensive searches of pertinent rhizomorphs that are luminescent as first proven by Guyot in
literature, examination of numerous exsiccati specimens, fieldwork 1927.35 The luminous phenomenon of these asexual hyphae,
throughout the world, and analyses of the nomenclature, taxon- known as “foxfire”, has been known for millennia and the
omy and phylogeny of reported species, we recognize no fewer earliest accounts of glowing wood probably document the effects
than 64 species of luminescent fungi (Table 1). If we couple these of Armillaria mycelia. It has been shown that the mycelia
data with the seminal research published by Moncalvo et al.27 and in vitro can sustain bright luminescence for up to 10 weeks.36
Matheny et al.28 it is clear that all known bioluminescent fungi are Interestingly, the basidiomes of Armillaria species have never
Basidiomycetes and represent white-spored euagarics once placed been reported as luminescent. Currently, the taxonomy of the
in the polyphyletic family Trichomolataceae sensu Singer.29 They worldwide members of Armillaria is well-known with ca. 40 species
are mushroom-forming, saprotrophic or rarely plant pathogenic recognized based on morphological,12,37 intercompatibility20,21 and
species belonging to three distinct lineages. Twelve species belong molecular datasets.24–26 Because many species are serious forest
to the Omphalotus lineage (Omphalotaceae), five species to the tree pathogens, much is known about their biology, genetics and
Armillaria lineage (Physalacriaceae), and the majority 47 species ecology,38,39 although only five species have been verified as being
belong to the mycenoid lineages (mostly Mycenaceae). We will luminescent (Table 1). It must be remembered, however, that
address each of these lineages separately. until the late 1970s when mating studies and genetic research
intensified, most currently recognized species of Armillaria were
Omphalotus lineage lumped into an admittedly morphologically variable A. mellea.
Hence, the many early reports of luminescent mycelium from
The luminescent properties of the large and conspicuous mush- around the world that were attributed to A. mellea most likely
rooms in this lineage have been documented at least since represent different species currently accepted in the A. mellea
the time of Pliny the Elder. The group includes the Jack-o- species complex. We suspect that the mycelium of most (if not
Lantern mushrooms of Europe and eastern North America all) Armillaria species is luminescent. In the most current and
(Omphalotus olearius and O. illudens), the Western Jack-o-Lantern comprehensive phylogeny of euagaric lineages,28 the luminescent
mushroom of western North America (O. olivascens), the Moon Armillaria lineage is sister to the remainder of the Physalacriaceae,
Night mushroom or Tsukiyotake of Japan (O. japonicus), and all of which are non-luminescent, and distantly related to any of
the Ghost Fungus of Australasia (O. nidiformis). Most species the other known luminescent fungi
in this group are well-characterized by morphological and One final note, it was a species of Armillaria (reported as A.
chemotaxonomical,13,30 intercompatibility,17 restriction enzyme,22 bulbosa, now known as A. gallica) that received headlines and the
and molecular datasets,24–26 and are currently accepted in the nickname “humungous fungus” for being one of the world’s largest
genera Omphalotus and Neonothopanus. Historically they were organisms. A single individual (i.e., mycelial genet) in Michigan
placed in the genera Clitocybe, Omphalotus, Lampteromyces, covered 15 hectares and was estimated to weigh at least 9 700 kg
Pleurotus, Panus, and Nothopanus. A recent phylogeny of Om- and be 1 500 years old!40 This discovery stimulated the search
phalotus based on sequences from the ITS1-5.8S-ITS2 rDNA for even larger Armillaria individuals and in 2003 researchers in
region included worldwide coverage of eight species, five of which Oregon reported a single individual of A. ostoyae covering 900
are known as luminescent, and confirmed that Lampteromyces hectares (9 km2 ) and estimated to be between 2 000 and 8 500 years
is a synonym of Omphalotus.23 Omphalotus mangensis and old.41 One wonders if the entire forest floor is aglow at night?
Lampteromyces luminescens were not included in the analyses
although they have been verified as luminescent.31,32 We suspect Mycenoid lineages
that all species of Omphalotus form luminescent basidiomes
(fruit bodies). Luminescent mycelium has been confirmed only Most known luminescent fungi were described in the genus
in three species (O. illudens, O. japonicus, O. olearius), whereas the Mycena or in closely allied genera and belong to what we have
mycelium of O. olivascens has been reported as non-luminescent termed the mycenoid lineages. They are nearly all saprotrophic,
(Table 1).33 Although reported as forming luminescent basidiomes, white-rot decomposers that form small mushrooms with lamellate
very little is currently known about the biology of the Malesian (gills) or poroid (tubes) spore-bearing surfaces. A few are plant

172 | Photochem. Photobiol. Sci., 2008, 7, 170–182 This journal is © The Royal Society of Chemistry and Owner Societies 2008
Table 1 Species of fungi reported as bioluminescent in the literature

Taxona Mycelium Basidiomes Distributionb Citationsc

Omphalotus lineage
Lampteromyces luminescens M. Zang ? + CH Zang 197931
Neonothopanus nambi (Speg.) Petersen & Krisai-Greilhuber ? + SA, CA, MS, AU Corner 198186
= Nothopanus eugrammus (Mont.) Singer sensu Corner non sensu Singer
Nothopanus noctilucens (Lév.) Singer ? + JP Léveillé 1844;87 Haneda 19558
= Pleurotus noctilucens Lév.
Omphalotus illudens (Schwein.) Bresinsky & Besl. + + EU, NA Wassink 1948,6 1978;4 Berliner 196136
= Clitocybe illudens Schwein.
= Panus illudens (Schwein.) Fr.
= Pleurotus facifer Berk. & M. A. Curtis
Omphalotus japonicus (Kawam.) Kirchm. & O. K. Mill. + + JP Kawamura 1915;88 Bermudes et al.
1992;44 Singer 194789
= Lampteromyces japonicus (Kawam.) Singer Singer 194789
= Pleurotus japonicus Kawam.
Omphalotus mangensis (J. Li & X. Hu) Kirchm. & O. K. Mill. ? + CH Li and Hu 199332
= Lampteromyces mangensis J. Li & X. Hu
Omphalotus nidiformis (Berk.) O. K. Mill. ? + AU Berkeley 1844;90 Miller 199462
= Pleurotus nidiformis (Berk.) Sacc.
= Pleurotus candescens (F. Muell. & Berk.) Sacc.
= Pleurotus illuminans (Berk.) Sacc.
= Pleurotus lampas (Berk.) Sacc.
= Pleurotus phosphorus (Berk.) Sacc.
Omphalotus olearius (DC.: Fr.) Singer + + EU Wassink 19486
= Pleurotus olearius (DC.) Gillet
Omphalotus olivascens H. E. Bigelow, O. K. Mill. & Thiers — + NA Bigelow et al. 197633
Pleurotus decipiens Corner ? + MS Corner 198186
Pleurotus eugrammus var. radicicolus Corner ? + MS, JP Corner 198186
= Pleurotus lunaillustris Kawam. nom. inval.
Pleurotus gardneri (Berk.) Sacc. ? + SA Saccardo 188791
[Predicted to have luminescent basidiomes: Omphalotus mexicanus Guzmán & V. Mora - CA; Omphalotus olivascens var. indigo Moreno, Esteve-Rav.,
Pöder & Ayala - CA; Omphalotus subilludens (Murrill) Bigelow - NA; Pleurotus olivascens Corner - MS]

Armillaria lineage
Armillaria fuscipes Petch + — MS Wassink 1948,6 1978;4 Berliner 196136
Armillaria gallica Marxm. & Romagn. + — EU, NA Mihail and Bruhn 200763
Armillaria mellea (Valh.) P. Kumm. sensu stricto + — EU, NA Mihail and Bruhn 200763
= Armillariella mellea (Valh.) P. Karst.
Armillaria ostoyae (Romagn.) Henrik + — EU, NA Risbeth 198664
Armillaria tabescens (Scop. ) Emel + — EU, NA Mihail and Bruhn 200763
= Collybia tabescens (Scop.) Fr.

Mycenoid lineages
Gerronema species
Gerronema viridilucens Desjardin, Capelari & Stevani + + SA Desjardin et al. 200514

Mycena species
Sect. Aspratiles
M. lacrimans Singer ? + SA Desjardin and Braga-Neto 200716
Sect. Basipedes
M. illuminans Henn. ? + MS, JP Haneda 1939;92 Corner 1954,9 199493
= M. bambusa Kawam. nom. inval.
M. stylobates (Pers.: Fr.) P. Kumm. + — EU, NA, JP, AF Bothe 193194
= M. dilitata (Fr.: Fr.) Gillet
Sect. Calodontes
M. pura (Pers.: Fr.) P. Kumm. + — EU, NA, SA, JP Treu and Agerer 199046
M. rosea (Bull.) Gramberg + — EU Treu and Agerer 199046
Sect. Citricolores
M. citricolor (Berk. & M. A. Curtis) Sacc. + — SA, CA Buller 1934;48 Berliner 196136
= Omphalia flavida Maubl. & Rangel
Sect. Diversae
M. lucentipes Desjardin, Capelari & Stevani + + SA, CA Desjardin et al. 200715
Sect. Euspeireae
M. species + + SA Desjardin et al. 2007;15 unpublished
data
Sect. Exornatae
M. chlorophos (Berk. & M. A. Curtis) Sacc. + + MS, JP, PA Corner 19549
= M. cyanophos (Berk. & M. A. Curtis) Sacc.
M. discobasis Métrod ? + SA, AF Desjardin et al. 200715

This journal is © The Royal Society of Chemistry and Owner Societies 2008 Photochem. Photobiol. Sci., 2008, 7, 170–182 | 173
Table 1 (Contd.)

Taxona Mycelium Basidiomes Distributionb Citationsc

Sect. Fragilipedes
M. polygramma (Bull.: Fr.) S. F. Gray + — EU, NA, JP, AF Bothe 1931;94 Berliner 1961;36 Treu and
Agerer 199046
= M. parabolica (Fr.) Quél. sensu Ricken
M. zephirus (Fr.: Fr.) P. Kumm. + — EU Bothe 1931;94 Treu and Agerer 199046
Sect. Galactopoda
M. haematopus (Pers.: Fr.) P. Kumm. + + EU, NA, JP Treu and Agerer 1990;46 Bermudes et al.
199244
Sect. Hygrocyboideae
M. epipterygia (Scop.: Fr.) S. F. Gray + — EU, NA, JP Bothe 193194
Sect. Lactipedes
M. galopus (Pers.: Fr.) P. Kumm. + — EU, NA, JP Bothe 1931;94 Berliner 1961;36 Treu
andAgerer 199046
Sect. Mycena
M. inclinata (Fr.) Quél. + — EU, NA, AF Wassink 19486
= M. galericulata var. calopus (Fr.) P. Karst.
M. maculata P. Karst. + EU, NA, AF Treu and Agerer 199046
M. tintinnabulum (Fr.) Quél. + — EU Bothe 193095
Sect. Roridae (= Roridomyces Rexer 199496 )
M. irritans E. Horak — + AU Horak 197845
M. lamprospora (Corner) E. Horak — + (spores) MS, AU Corner 1950,97 1994;93 Horak 197845
= M. rorida var. lamprospora Corner
M. pruinoso-viscida Corner ? + MS Corner 1954,9 199493
M. pruinoso-viscida var. rabaulensis Corner ? + (spores) AU Corner 1954,9 199493
M. rorida (Fr.) Quél. + — EU, NA, SA, JP Josserand 195398
M. sublucens Corner — + MS Corner 19549
Sect. Rubromarginatae
M. lux-coeli Corner ? + JP Corner 19549
M. noctilucens Kawam. ex Corner ? + MS, PA Corner 1954,9 199493
M. noctilucens var. magnispora Corner ? + PA Corner 199493
M. olivaceomarginata (Massee apud Cooke) + — EU, NA Wassink 19486
Massee
= M. avenacea (Fr.) Quél.
M. singeri Lodge ? + SA, CA Desjardin et al. 200715
M. species ? + SA Desjardin et al. 200715
Sect. Sacchariferae
M. asterina Desjardin, Capelari & Stevani + + SA Desjardin et al. 2007;15 unpublished data
Sect. Sanguinolentae
M. sanguinolenta (Alb. & Schwein.: Fr.) P. Kumm. + — EU, NA, JP Bothe 193194
Sect. Supinae
M. fera Maas Geest. & de Meijer ? + SA Desjardin et al. 200715

Incertae Sedis
Mycena daisyogunensis Kobayasi ? + JP Kobayasi 195199
Mycena pseudostylobates Kobayasi + ? JP Kobayasi 195199

Manipularis-group
Filoboletus pallescens (Boedijn) Maas. Geest. ? + MS Maas Geesteranus 199242
Poromycena pallescens Boedijn
Filoboletus yunnanensis P. G. Liu ? + CH Liu and Yang 1994100
Mycena manipularis (Berk.) Métrod nom. inval. [non + + MS, PA, AU Corner 19549
M. manipularis (Berk.) Sacc.]
= Poromycena manipularis (Berk.) Heim
= Filoboletus manipularis (Berk.) Singer
= Polyporus mycenoides Pat.
Mycena manipularis var. microporus Kawam. ? + PA Corner 19549
ex Corner nom. inval.
= Polyporus microporus Kawam. nom. inval.
Poromycena hanedai Kobayasi ? + JP Kobayasi 195199
= Polyporus hanedai Kawam. sensu Kobayasi nom. inval. (not Polyporus hanedai A. Kawam. )

Panellus/dictyopanus species
Dictyopanus foliicolus Kobayasi + + JP Kobayasi 1951,99 1963101
Dictyopanus pusillus var. sublamellatus Corner ? + SA Corner 19549
Panellus gloeocystidiatus (Corner) Corner ? + JP, MS Corner 1954,9 1986;102 Kobayasi 1963101
= Dictyopanus gloeocystidiatus Corner
Panellus luminescens (Corner) Corner ? + MS Corner 1950,97 1986102
= Dictyopanus luminescens Corner
Panellus pusillus (Pers. ex Lév.) Burdsall & O. K. Mill. + + NA, SA, MS, AU, AF Haneda 1955;8 Burdsall and Miller 1975103
= Dictyopanus pusillus (Pers. ex Lév.) Singer
= Polyporus rhipidium Berk.

174 | Photochem. Photobiol. Sci., 2008, 7, 170–182 This journal is © The Royal Society of Chemistry and Owner Societies 2008
Table 1 (Contd.)

Taxona Mycelium Basidiomes Distributionb Citationsc

Panellus stipticus (Bull.: Fr.) Karst. + + EU, NA, SA, JP, AU, AF Buller 1924;50 Berliner 1961;36
Wassink 19486
= Panus stipticus (Bull.) Fr.

Excluded, doubtful or insufficiently known taxa

Collybia cirrhata (Schumach.) P. Kumm. ? + EU, NA, JP Wassink 19486
Collybia tuberosa (Bull.) P. Kumm. ? + EU, NA, JP Wassink 19486
Flammulina velutipes (Curtis) Singer + — EU, NA, JP Airth and Foerster 1964104
= Collybia velutipes (Curtis) P. Kumm. [a non-luminescent species]
Fungus igneus Rumph. nom. inval. ? + MS Wassink 19486
Gerronema glutinipes Pegler ? + AF Liu 1995105
Locellina illuminans Henn. (not Mycena illuminans Henn.) ? + MS Hennings 1900;106 Wassink 19486
Locellina noctilucens Henn. (not Mycena noctilucens Henn.) ? + AU Hennings 1898;107 Wassink 19486
Marasmius phosphorus Kawam. nom. inval. ? + JP Haneda 1939108
Mycena bambusa Kawam. nom. inval. ? + JP Haneda 1939108
Mycena citrinella var. illumina Kawam. nom. inval. ? + JP Haneda 19558
Mycena microillumina Kawam. nom. inval. ? + JP Haneda 1939108
Mycena phosphora Kawam. nom. inval. ? + JP Haneda 1939,108 19558
Mycena photogena Komin. nom. inval. ? + JP Haneda 19558
Mycena yapensis Kawam. nom. inval. ? + JP Haneda 1939108
Omphalia martensii Henn. ? + MS Wassink 19486
Omphalia noctilucens Rick ? + SA Rick 1930109
Panus incandescens Berk. & Broome ? + AU Wassink 19486
Pleurotus emerci Berk. nom. inval. ? + ? Wassink 19486
Pleurotus lux Hariot ? + PA Wassink 19486
Pleurotus prometheus Berk. & M. A. Curtis ? + CH Wassink 19486
= Pleurotus djamor (Rumph. ex Fr.) Boedijn [a non-luminescent species]
Polyporus noctilucens Lagerh. ? + AF Wassink 19486
All brown-spored agarics, boletes, polypores, corticioid fungi, gasteromycetes and ascomycetes reported in Table III of Wassink 1948,6 and parts A.2–A.3
of Wassink 1978.4
a
Taxonomic synonyms are listed only if they were reported as luminescent in published literature. b Distributions reported in the literature. If we consider
a report unreliable we have not included it. Europe (EU), North America (NA), South America (SA), Central America and the Caribbean region (CA),
Pacific islands (PA), China (CH), Japan (JP), Malaysia, South Asia and Southeastern Asia (MS), Australasia including Papua New Guinea and New
Caledonia (AU), Africa (AF). c Citations where bioluminescence was reported. These are not necessarily the first or only reports of luminescence.

pathogens, such as M. citricolor (syn. Omphalia flavida) that causes lacrimans from Amazonas State.16 Nocturnal collecting protocols
the American Leaf Spot disease of coffee. There are currently over and the use of photometers and digital cameras to capture light
500 species of Mycena sensu lato and the genus has been subdivided emitted at intensities not visible by dark-adapted human eyes
into 60 sections.10,11,42,43 Out of this tremendous diversity, only have also increased the number of known luminescent mycenoid
35 Mycena species have been reported as luminescent, but these fungi. We contend that many of the described Mycena species
belong to 17 different sections of the genus (Table 1). Additional have bioluminescent properties that are currently undetected.
bioluminescent mycenoid fungi include five species traditionally For example, most literature classifies M. haematopus as non-
placed in Filoboletus or Poromycena that form putrescent poroid luminescent, but when studied photometrically, both the mycelium
basidiomes, and six species traditionally placed in Panellus or and basidiomes emit light.44
Dictyopanus that form tough and persistent, lamellate or poroid The components of the life cycle that luminesce are variable in
basidiomes. Phylogenetic analyses reveal that Mycena s.l. is the mycenoid lineages and this surely influences the ecological roles
not monophyletic, although which infrageneric groups represent and adaptive significance of bioluminescence. In many species,
distinct genus-rank lineages remains uncertain.27,28 Multiple loci only the mycelium is luminescent (Table 1), whereas in others
molecular sequences datasets are currently being generated in both the mycelium and basidiomes emit light. Very rarely has the
the Desjardin lab to help elucidate phylogenetic relationships basidiome been reported as luminescent while the mycelium is
in the mycenoid fungi. We can state that all but two of the non-luminescent (M. irritans, M. lamprospora, M. sublucens).9,45
luminescent mycenoid species listed in Table 1 belong to the Myce- Treu and Agerer46 confirmed earlier reports of luminescent
naceae (excluded: Gerronema viridilucens, Mycena lucentipes), that mycelium in Mycena spp. and added several more species to the
Panellus is the correct name for taxa once named Dictyopanus, list. For many species, however, pure cultures have not been studied
and that the luminescent species listed under Manipularis-group so no data are available documenting the luminescent properties
represent a distinct lineage that requires a new generic name of their mycelia. There is also variability in which components
(none are closely related to the type species of Filoboletus or of the basidiomes glow. For example, in M. lamprospora and M.
Poromycena). Most of the Mycena epithets added to the list pruinoso-viscida var. raboulensis only the spores are known to emit
after Wassink4 were the result of our recent fieldwork in Brazil light,9,45 in G. viridilucens only the lamellae glow,14 in M. chlorophos
where we discovered eight luminescent taxa from a single site in and M. asterina the pilei and lamellae are luminescent,15,47 whereas
primary Atlantic Forest habitat in São Paulo State,14,15 and M. in M. lucentipes only the stipes glow.15 Clearly more qualitative

This journal is © The Royal Society of Chemistry and Owner Societies 2008 Photochem. Photobiol. Sci., 2008, 7, 170–182 | 175
observations of fresh basidiomes and mycelia in situ and in vitro and that luminescence in the basidiomes was restricted primarily
are needed to clarify the bioluminescent properties of mycenoid to the pileus margin and lamellar edges. In addition it was shown
fungi. that in both cultures and basidiomes, the wavelength of maximum
One of the more interesting luminescent mycenoid fungi is the bioluminescence was at 525 nm.56 In in vitro antagonism studies,
coffee leaf pathogen M. citricolor. Its mycelium produces asexual it was shown that bioluminescence emissions in P. stipticus and O.
reproductive structures called gemmifers that are tiny (2 mm olearius were reduced over six orders of magnitude when grown
tall), mushroom-shaped structures with a sterile (non-sporulating) with the mycopathogenic fungus Trichoderma harzianum.57
cap that disarticulates and acts as a dispersal propagule.48 These Some early work was published on laboratory cultivation
modified sterile caps are the primary infecting inoculum of of Omphalotus japonicus (syn. Lampteromyces japonicus)58 as a
new Coffea host plants and they are luminescent. Whether the prelude to investigations on the mechanism of bioluminescence,
luminous propagules attract arthropod dispersal vectors thereby and subsequent research resulted in the proposition of riboflavin
aiding the fungus in infecting new hosts is unknown. To avoid as the putative light emitter.59,60 Other than a few papers elu-
confusion in the use of the misapplied name Stilbum flavida for this cidating the cultural conditions for optimal mycelial growth,61
stage in the life cycle, Redhead et al.49 created the name Decapitatus and the production of degradative enzymes, toxins (illudoids),
for the anamorphic dispersal stage of M. citricolor. nematophagous compounds, and biomedically active (antibiotic,
In the most current and comprehensive phylogeny of euagaric antitumor) compounds (not cited here), only limited research has
lineages,28 the luminescent mycenoid fungi in the Mycenaceae been published on the biology of the Moon Night mushroom, O.
belong to the Tricholomatoid clade whose other members are all japonicus.
non-luminescent. The Tricholomatoid clade is distantly related to In Miller’s62 redescription on the Australian Ghost Fungus,
the Marasmioid clade in which the Omphalotaceae (Omphalotus O. nidiformis, he noted different color-morphs that had variable
lineage) and Physalacriaceae (Armillaria lineage) belong. luminescent properties, with a dark form that luminesced rather
In summary, recent multi-gene molecular sequences datasets weakly and a light form with very strong luminescence. Culture
suggest at least 3 independent origins of bioluminescence in analyses and interfertility studies amongst the two forms indicated
the fungi: in the Omphalotaceae, the Physalacriaceae and the that they belong to a single morphologically and physiologically
Mycenaceae. The phylogenetic placement of G. viridilucens and variable species.
M. lucentipes outside of the Mycenaceae (unpublished data) may The dynamics of bioluminescence in three sympatric species
indicate a fourth independent origin but more work needs to be of Armillaria (A. gallica, A. mellea, A. tabescens) was exam-
done to support this contention. Within the Mycenaceae, the 45 ined in response to environmental illumination and mechanical
recognized luminescent taxa belong to 18 different taxonomic disturbance.63 The data revealed consistent differences in expres-
groups (genera or sections within Mycena). Whether this indicates sion of bioluminescence among the three species, confirming
a single early origin of luminescence in the family followed earlier work,64 and among intragenet cultures. They found no
by multiple losses, or multiple independent origins is currently evidence in support of diurnal periodicity of bioluminescence
unknown but under investigation in our labs. in the mycelial cultures in vitro. Similar results indicating that
bioluminescence does not vary between night and day were
Physiology of luminescent fungi reported recently from mycelia of an undetermined tropical fungus
inhabiting natural wood substrate in situ.65 Earlier reports sug-
Wassink provided an excellent review of the literature on the gested a diurnal–nocturnal oscillation66,67 and seasonal variation68
physiology and biochemical aspects of luminescent fungi up of light emissions in A. mellea and P. stipticus. Weitz et al.69 studied
to 1978.4 Since then, limited research has been conducted on the effects of temperature, light and pH on mycelial growth and
luminescent fungi in pure culture and none in situ. A few examples luminescence in A. mellea, O. olearius, M. citricolor and P. stipticus
are presented here. and found that temperature and pH had a significant effect on both
As early as 19244 it was known that there are luminescent and aspects but that light did not.
non-luminescent strains of Panellus stipticus, and interfertility Bermudes and colleagues44 were some of the first to systemati-
studies by Macrae51,52 confirmed that non-luminescent popula- cally use photometers to measure light emission from fungi, and
tions from Europe were sexually compatible with luminescent as a consequence discovered that Mycena haematopus, previously
populations from eastern North America. More recent research thought to be non-luminescent, actually emitted light but at
by Petersen and Bermudes18,19 indicated that populations of P. intensity not perceived by the human eye. Measurements of total
stipticus from eastern Russia, Japan, New Zealand, and eastern luminescence of single-spore (monokaryon) or dikaryon cultures
North America were all sexually compatible, and they confirmed of six species of fungi revealed a significant difference in lumi-
with photometric analyses that the species is non-luminescent in nescence between different species and between monokaryon and
Eurasia, but that both non-luminescent and luminescent strains of dikaryon cultures of the same species (P. stipticus, O. japonicus).
P. stipticus occur in eastern North America. The effects of various Recently, the optimal conditions for the growth of mycelia
environmental and nutritional conditions on the growth and and the production of basidiomes in Mycena chlorophos have
bioluminescence of mycelia of P. stipticus indicated that optimal been published.47,70 Optimal temperature for mycelial growth and
conditions included: darkness; 28 ◦ C; pH 3.8; cellobiose, glucose, primordium formation were 27 ◦ C and 21 ◦ C respectively, optimal
maltose, pectin, or trehalose as the carbon source; and ammonia or pH of the medium was 4.0, and light was required for primordium
asparagine as the nitrogen source.53 Studies on the localization of initiation. Basidiomes of this species are typically short-lived, but
bioluminescent tissues in P. stipticus54,55 indicated a 10- to 50-fold luminescence at a maximum wavelength of 522 nm was emitted
increase in luminescence emission during basidiome development continuously for three days. In an unpublished report, basidiomes

176 | Photochem. Photobiol. Sci., 2008, 7, 170–182 This journal is © The Royal Society of Chemistry and Owner Societies 2008
of M. lux-coeli emitted relatively strong light for 2–3 days in situ the luminous reaction involves a readily available by-product
in Japan.71 The mechanism of luminescence in M. chlorophos has compound or secondary metabolite.39,65,73 This has been ob-
not been elucidated although it was assumed by those authors70 to served in luminous bacteria where reduced flavin mononucleotide
be the same as that reported by Shimomura72 for other mycenoid (FMNH2 ), a continuously available by-product of respiration, is
fungi (M. citricolor, M. lux-coeli P. stipticus). the substrate of the luminous reaction.65 Luminous fungi may be
To summarize, most of the published research on the physiology emitting light instead of heat as an energy by-product of enzyme
of bioluminescent fungi has focused on determining the conditions mediated oxidation reactions.74 Bioluminescence is an oxygen-
for optimal mycelial growth and basidiome production, the con- dependant metabolic process. Lingle84,85 and Bermudes et al.44
ditions for maximum light emission, the effects of environmental have hypothesized that fungal bioluminescence is involved in lignin
conditions and mechanical disturbance on bioluminescence, and degradation through the detoxification of peroxides formed during
the variability in the quality and quantity of light emission ligninolysis. As far as we know, all luminescent basidiomycetes
amongst different luminescent species under different growth con- are white-rot fungi capable of lignin degradation. We favor the
ditions. Nearly all of the published research has been conducted hypothesis that fungal bioluminescence is an advantageous process
on fungi grown in pure culture. There is considerable variability that provides antioxidant protection against deleterious effects of
amongst luminescent fungi in the optimal growth conditions for reactive oxygen species (ROS) produced mainly by mitochondria
maximum light emission and in the various environmental factors during respiration.15
that impact bioluminescence. All reports agree that luminescent
fungi have a bioluminescence emission peak in the range 520–
530 nm. Bioluminescence mechanism
Early accounts
Ecological functions of luminescent fungi
Although significant advances have occurred in the past 30 years to
The potential ecological functions and adaptive significance of augment our knowledge of the occurrence, taxonomy, phylogeny
bioluminescence in the fungi have been reviewed recently,44,73,74 and ecology of bioluminescent fungi, only limited progress have
reiterating the ideas of numerous earlier workers.75–78 It has been been made in understanding the biochemistry involved in fungal
suggested that bioluminescent basidiomes attract invertebrates light emission. Mechanistic studies of fungal bioluminescence
to aid in fungal spore dispersal.79,80 In an elegant experiment, reported until now are incomplete and often misleading. A
Sivinski79 showed that more arthropods were attracted at night to chronological and critical compilation of published data is here
luminous forest litter containing mycelia of a Mycena species en- presented.
capsulated in closed glass test tubes (to allow visual recognition but The first attempts to elucidate the chemistry of fungal biolu-
practically eliminate olfactory detection) than to glass test tubes minescence were based on the classic “cold” and “hot” extract
containing non-luminous forest litter. In addition, subsequent procedure proposed by Dubois in 1885.110 Dubois reported that
research has confirmed that fungivorous insects are positively light emission in vitro could be observed as soon as the “cold”
phototactic to relatively low light emissions of wavelengths in the and the “hot” extracts prepared from either luminous organs
range 300–650 nm.81 Hence, for those fungal species that form of the bivalve mollusk Pholas dactylus or from an Indian click-
luminous basidiomes that sporulate at night, emitting light may beetle, Pyrophorus sp., were mixed. Dependence of light emission
have a selective advantage over non-luminous species in attracting on molecular oxygen was already known. Usually light emission
potential spore-dispersing arthropods, especially in areas where from extracts is too dim to be perceived by the naked eye
wind dispersal is inhibited (e.g., dense, closed canopy tropical and a sensitive photometer or photocounter must be employed.
forests). Given that luminous and non-luminous basidiomes can Perhaps this explains the unsuccessful attempts by Ewart in
each produce millions of spores per night that are easily wind- 1907 and by Kawamura in 1915 to detect light using “cold”
dispersed, the significance of supplemental insect dispersal is and “hot” extracts from the fungi Pleurotus candescens and
unknown. O. japonicus, respectively.76,111 Some years later, Harvey applied
Bioluminescence as an adaptation to enhance spore dispersal, Dubois’ procedure to A. mellea, O. olearius and P. stipticus,7,112
however, cannot be used to explain the ecological function of light but did not observe any light emission, which was then attributed
emissions from mycelia. In most luminescent fungi, the mycelium to a low concentration and instability of luciferin or luciferase in
does not form dispersal propagules, except for the enigmatic the extracts.
M. citricolor (see above). Fungal mycelia are a major or sole Buller tried to extract the luciferin/luciferase system from
source of nutrition for myriad invertebrates, and the fungi have P. stipticus by pressing basidiomes between two glass slides.50
evolved a number of ways to counter predation, including the As the mushrooms were gradually squeezed, the light emission
production of noxious compounds.82,83 Sivinski79 also suggested diminished until total extinction. Light could be visually detected
that luminescence might serve as a warning signal to repel if water was dripped onto dried and whole mushrooms; however,
nocturnal fungivores, or might attract predators or parasitoids if dried mushrooms had been pulverized, light could not be
of fungivores. These hypotheses are worthy of further study. observed upon water addition. Buller interpreted these results to
As pointed out by Weitz,74 luminescence may not confer represent a chemical inactivation of the substances involved in
selective advantage because there are both luminescent and non- the bioluminescent reaction, such as oxidation of luciferin and/or
luminescent sympatric strains of the same species,19 and may luciferase by substances previously confined in cell compartments.
have no ecological value. Some published data indicate that In 1959, Airth and McElroy113,114 finally accomplished a suc-
light emission involves little energy expenditure, implying that cessful experiment using the “cold” and “hot” extract procedure.

This journal is © The Royal Society of Chemistry and Owner Societies 2008 Photochem. Photobiol. Sci., 2008, 7, 170–182 | 177
These authors ascribed the failure of prior attempts to a low Moreover, the maximum wavelength emission observed for fungi
concentration of luciferase in the extracts, eventual presence bioluminescence is around 530 nm15,56 whereas for bacteria,
of inhibitors, and/or the lability of luciferin in “hot” extracts. it is ca. 490 nm.114 In addition, Airth and Foerster repeated
Importantly, light emission could only be detected if NAD(P)H successfully their experiment with any possible enzyme/substrate
was added to the reactive medium, suggesting reversibility of any combinations of extracts obtained from A. mellea, “C. velutipes”,
oxidation process that affected the native components. and the North American bioluminescent variety of P. stipticus,
suggesting that both enzyme and substrate are essentially the same
Airth and Foerster’s proposal for all bioluminescent fungi species.104
The structural characterization of the chemical components
Airth and Foerster performed several experiments using the “hot” remained to be accomplished. All efforts conducted to purify
extract of A. mellea (source of luciferin) and the “cold” extract protein fractions using ammonium sulfate precipitation, dialysis,
of Collybia velutipes (source of luciferase).115 Clearly, the authors different types of chromatography and differential centrifugation
used a luminous culture identified erroneously as C. velutipes, resulted in loss of activity and protein degradation.116 With regard
because that species has been shown to be non-luminescent.4 to the luciferin purification, its lability especially in basic medium
Some modifications to the classic Dubois’s procedure were also and the presence of oxygen complicate the adoption of purification
introduced by the authors. The “hot” extract was obtained from procedures and consequent structural characterization.
dried mycelium cultures of A. mellea by prior preparation of fun- In 1966, Kuwabara and Wassink were able to isolate 12 mg
gus homogenate in phosphate buffer and centrifugation, followed of a crystalline fluorescent substance from 15 kg of Mycena
by heating the supernatant in boiling water. The homogenate citricolor cultivated mycelium.117 The compound was unstable in
of “cold” extract, obtained from dried mycelium cultures of basic conditions, in the presence of light and oxygen, and at high
“C. velutipes”, was first separated by centrifugation at 3 000 g, temperatures, similar to what has been reported for other luciferins
followed by ultracentrifugation of the supernatant at 198 000 g, isolated from different bioluminescent organisms (Scheme 3).118–123
yielding a soluble protein fraction and a membrane protein Additionally, a visible green light emission with a spectrum similar
fraction (pellet). Light emission was observed as the hot extract to that of the fungal bioluminescence was observed in the presence
(luciferin/oxiluciferin) was mixed with the soluble protein fraction of NaOH and H2 O2 or when the substance was subjected to the
in the presence of NADPH, followed by addition of the pellet Airth and Foerster’s procedure. Unfortunately, these authors never
(re-suspended in buffer) some minutes after incubation. The reported any structural or physical properties of the fluorescent
protein nature of both ultracentrifugation fractions was suggested crystalline substance.
by the fact that they precipitated upon addition of ammonium Between the early 1970s and middle 1990s, some authors
sulfate, were non-dialyzable, and became inactive under heating. claimed to be able to isolate and characterize the chemical struc-
The experiment also provided clear-cut evidence that the soluble ture of fungal luciferin.58–60,124–126 Several molecules were then as-
protein fraction contained a NADPH-dependent reductase while signed as the actual luciferins, among them: lampterol (illudin S),
the membrane protein fraction contained the fungal luciferase. ergosta-4,6,8(14),22-tetraen-3-one, riboflavin and lampteroflavin,
Based on this experiment, Airth and Foerster proposed a two- all extracted and purified from O. japonicus (Scheme 4). Notwith-
step bioluminescent mechanism involving (i) an initial reduction standing the similarity of their fluorescent spectra to the fungal
of the luciferin precursor (X) present in the “hot” extract by a bioluminescence, no further evidence has ever been provided
NADPH-dependent reductase, leading to the formation of the to support the involvement of any of these molecules in the
fungal luciferin (XH2 ), and (ii) the reaction of reduced luciferin mechanism of fungal light emission in vivo.
with luciferase in the presence of molecular oxygen yielding light
and oxyluciferin (X
) (Scheme 1).
Shimomura’s proposal

During that same period, Shimomura isolated a sesquiterpene

from fruiting bodies of P. stipticus possibly involved in the
bioluminescent pathway, which was named panal. In fact, panal is
present in that fungus in the form of its decanoic and dodecanoic
esters, PS-A and PS-B, respectively (Scheme 4).127,128 When panal
Scheme 1 was incubated with ammonium salts or primary amines for 1 to
24 h, the putative pyrrolic derivative that formed (our assumption)
Although Airth and Foerster’s proposal resembles the mecha- exhibited light emission upon Fe2+ /H2 O2 addition at pH 7–8. The
nism of bacterial bioluminescence (Scheme 2), the fungal system emission maximum wavelength (485–585 nm) was dependent on
is not stimulated by the addition of reduced flavin mononucleotide added surfactant.129 The author did not observe any light emission
(FMNH2 ), flavin adenine dinucleotide (FADH2 ) or dodecanal.114 from the fungus P. stipticus128 using the procedure of Airth and
Foerster.104
Based on these findings, Shimomura proposed a non-enzymatic
mechanism to account for the fungal bioluminescence, where no
luciferase was involved and panal (in fact PS-A and PS-B) was
the luciferin precursor. It must be emphasized that there is no
report of in vivo reactions of panal with nitrogen compounds. This
Scheme 2 idea was conceived with basis on the reaction between polygodial,

178 | Photochem. Photobiol. Sci., 2008, 7, 170–182 This journal is © The Royal Society of Chemistry and Owner Societies 2008
 Scheme 3

Scheme 4

a phytoalexin obtained from the plant Polygonum hydropiper, We have been able to observe light emission using the classic
and nitrogen compounds.130 Actually, panal is endowed with low “cold” and “hot” extract procedure in the presence of either
conjugation and high flexibility requiring a cyclization reaction NADH or NADPH with cultures of the recently described Brazil-
in order to become more rigid and consequently to increase its ian bioluminescent species G. viridilucens and M. lucentipes.14,15
fluorescence quantum yield (Scheme 5). Moreover, it is widely To our knowledge, aside from Kuwabara117 and Kamzolkina’s
known that the hydroxyl radical produced by the Fenton’s reaction group,131 we are the only ones to successfully observe light with
(Fe2+ in the presence of H2 O2 ) is a highly oxidizing reagent, which the aid of a photometer using either Dubois’s or Airth and
argues against its use in model studies of bioluminescence, in Foerster’s procedure carried out with cultivated mycelium extracts
which the main objective is to resemble physiological plausible under physiologically plausible conditions. Moreover, we were also
conditions. The hypothesis of a non-enzymatic pathway involved able to detect light emission with any possible enzyme/substrate
in fungal bioluminescence requires further investigations to be combinations of extracts obtained from G. viridilucens and M.
seriously considered. lucentipes as performed earlier with other bioluminescent fungi

This journal is © The Royal Society of Chemistry and Owner Societies 2008 Photochem. Photobiol. Sci., 2008, 7, 170–182 | 179
 Scheme 5

(i.e., A. mellea and P. stipticus).104 Based on our own findings we are 9 E. J. H. Corner, Further descriptions of luminous agarics, Trans. Br.
very much inclined to favor Airth and Foerster’s proposal against Mycol. Soc., 1954, 37, 256.
10 R. A. Maas Geesteranus, Mycenas of the Northern Hemisphere,
Shimomura’s mechanism. We are currently employing Dubois’s vol. II, Verh. Kon. Ned. Akad. Wetensch. Afd. Natuurk. Tweede Reeks,
and Airth and Foerster’s procedure to guide us in the isolation of 1992, 90, 1.
the luciferin and enzymes involved in fungi bioluminescence. 11 G. Robich, Mycena d’Europa, Centro Studi Micologici, Trento, Italy,
2003.
12 D. N. Pegler, Taxonomy, nomenclature and description of Armillaria,
Acknowledgements in Armillaria Root Rot: Biology and Control of Honey-Fungus, ed.
R. T. V. Fox, Intercept Ltd., Andover, 2000.
We would like to thank Prof. Dr Etelvino J. H. Bechara (Chemistry 13 M. Kirchmair, R. Pöder, C. G. Huber and O. K. Miller Jr., Chemotax-
onomical and morphological observations in the genus Omphalotus
Institute, University of São Paulo) for helpful discussions and Fayod (Omphalotaceae), Persoonia, 2002, 17, 583.
for a critical reading of the manuscript. We are grateful to Dr 14 D. E. Desjardin, M. Capelari and C. V. Stevani, A new bioluminescent
Rubin Walleyn and Dr Brian Perry for the use of photographic agaric from São Paulo, Brazil, Fung. Div., 2005, 18, 9.
images of Filoboletus manipularis and Mycena aff. euspeirea, 15 D. E. Desjardin, M. Capelari and C. V. Stevani, Bioluminescent
Mycena species from São Paulo, Brazil, Mycologia, 2007, 99, 317.
respectively. Finally, we would also like to thank Dr Vadim Viviani 16 D. E. Desjardin and R. Braga-Neto, Mycena lacrimans, a rare species
(Universidade Federal de São Carlos, Campus de Sorocaba, SP) from Amazonia, is bioluminescent, Edinburgh J. Bot., 2007, 64, 275.
for the kind invitation to write this article. Partial funding for this 17 R. H. Petersen and K. W. Hughes, Mating systems in Omphalotus
(Paxillaceae, Agaricales), Plant Syst. Evol., 1998, 211, 217.
project was provided by FAPESP (grant #06/53628-3 to C. V. S.) 18 R. H. Petersen and D. Bermudes, Panellus stypticus: geographically
and the US National Science Foundation (grant # DEB-0542445 separated interbreeding populations, Mycologia, 1992, 84, 209.
to D. E. D.). 19 R. H. Petersen and D. Bermudes, Intercontinental compatibility in
Panellus stypticus with a note on bioluminescence, Persoonia, 1992,
14, 457.
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