Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
A review on bioluminescent fungus Neonothopanus gardneri
Uma revisão sobre o fungo bioluminescente Neonothopanus gardneri
Revisión sobre el hongo bioluminiscente Neonothopanus gardneri
Received: 03/13/2022 | Reviewed: 03/20/2022 | Accept: 03/26/2022 | Published: 04/02/2022
Maycon Bruno Barbosa Vieira
ORCID: https://orcid.org/0000-0002-1849-0541
Federal Institute of Piaui, Brazil
E-mail: mayconbr6@gmail.com
Iago Cavalcante Oliveira
ORCID: https://orcid.org/0000-0003-4739-509X
Federal Institute of Piaui, Brazil
E-mail: iagooliverc12@gmail.com
Maria das Dores Alves de Oliveira
ORCID: https://orcid.org/0000-0002-2847-6567
Federal University of Piaui, Brazil
E-mail: maralves013@gmail.com
Joaquim Soares da Costa Júnior
ORCID: https://orcid.org/0000-0002-9849-201X
Federal Institute of Piaui, Brazil
E-mail: jquimjr@gmail.com
Teresinha de Jesus Aguiar dos Santos Andrade
ORCID: https://orcid.org/0000-0002-2415-9222
Federal Institute of Maranhão, Brazil
E-mail: teresinha.andrade@ifma.edu.br
Chistiane Mendes Feitosa
ORCID: https://orcid.org/0000-0001-8013-1761
Federal University of Piaui, Brazil
E-mail: chistiane@ufpi.edu.br
Mahendra Rai
ORCID: https://orcid.org/0000-0003-0291-0422
Nicolaus Copernicus University, Poland
E-mail: mahendra.rai@v.umk.pl
Nerilson Marques Lima
ORCID: https://orcid.org/0000-0001-9669-0306
Federal University of Goias, Brazil
E-mail: nerilsonmarques@gmail.com
Danielle da Costa Silva
ORCID: https://orcid.org/0000-0003-2706-9588
Federal Institute of Piaui, Brazil
E-mail: dcsdanielle@gmail.com
Abstract
Neonothopanus gardneri (N. gardneri) is a species of bioluminescent fungus belonging to the order Agaricales
(Marasmiaceae) found in South America. Its existence was first reported in 1840 by George Gardner in his travels to
Brazil, where it is popularly called "coco flower". Found mainly in decaying leaves and in the trunk of dwarf palm
trees called "pindoba" (Attalea oleifera) or babaçu (Orbignya phalerata), recently N. gardneri had some of its bioactives
isolated and their respective structures elucidated. Thus, this paper aims to present and discuss the findings of the works
produced involving this theme. Thus, for the development of this literature review, books and scientific articles were
searched in the following databases: Scopus, PubMed, Science Direct, web of science, Royal Society of Chemistry
(RSC) Publishing and Google Scholar (1990-2021). The following keywords were used to filter the productions:
"Neonothopanus", "Neonothopanus gardneri", "Bioactivities", "Bioprospecting", "Secondary metabolite",
"Endophytic" and "bioluminescence". Finally, it is possible to observe that studies involving this species of
bioluminescent fungus have focused on explaining the mechanism of light production and its potential biological
activities, among them, antitumor, antioxidant, antimicrobial and antileishmanial effects.
Keywords: Bioluminescence fungus; Neonothopanus gardneri; Flor de coco; Agaricales.
Resumo
A Neonothopanus gardneri (N. gardneri) é uma espécie de fungo bioluminescente pertencente à ordem Agaricales
(Marasmiaceae) encontrada na América do Sul. Sua existência foi reportada pela primeira vez em 1840 por George
1
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
Gardner em suas viagens ao Brasil, onde é popularmente chamada de "flor de coco". Encontrada principalmente em
folhas em decomposição e no tronco de palmeiras-anãs chamadas “pindoba” (Attalea oleifera) ou babaçu (Orbignya
phalerata), recentemente a N. gardneri teve alguns de seus bioativos isolados e suas respectivas estruturas elucidadas.
Sendo assim, este trabalho tem como objetivo apresentar e discutir os achados das obras produzidas envolvendo este
tema. Sendo assim, para desenvolvimento dessa revisão da literatura foram realizadas buscas de livros e artigos nas
seguintes bases de dados: Scopus, PubMed, Science Direct, web of science, Royal Society of Chemistry (RSC)
Publishing e Google Scholar (1990-2021). Para filtragem das produções utilizou-se as seguintes palavras-Chaves:
“Neonothopanus”, “Neonothopanus gardneri”, “Bioatividades”, “Bioprospecção”, “Metabolito secundário”,
“Endofitico” e “bioluminescência”. Por fim, é possível observar que os estudos envolvendo essa espécie de fungo
bioluminescente tem se concentrado em explicar o mecanismo de produção de luz e seus potenciais atividades
biológicas, dentre elas, os efeitos antitumorais, antioxidantes, antimicrobianos e antileishmania.
Palavras-chave: Fungo de bioluminescência; Neonothopanus gardneri; Flor de coco; Agaricales.
Resumen
Neonothopanus gardneri (N. gardneri) es una especie de hongo bioluminiscente perteneciente al orden Agaricales
(Marasmiaceae) que se encuentra en Sudamérica. Su existencia fue reportada por primera vez en 1840 por George
Gardner en sus viajes a Brasil, donde se le llama popularmente "flor de coco". Encontrada principalmente en las hojas
en descomposición y en el tronco de las palmeras enanas llamadas "pindoba" (Attalea oleifera) o babaçu (Orbignya
phalerata), recientemente se han aislado algunos de sus bioactivos y se han dilucidado sus respectivas estructuras. Así,
este trabajo tiene como objetivo presentar y discutir las conclusiones de los trabajos realizados en torno a este tema.
Así, para el desarrollo de esta revisión bibliográfica, se buscaron libros y artículos en las siguientes bases de datos:
Scopus, PubMed, Science Direct, web of science, Royal Society of Chemistry (RSC) Publishing y Google Scholar
(1990-2021). Se han utilizado las siguientes palabras clave para filtrar las producciones: "Neonothopanus",
"Neonothopanus gardneri", "Bioactividades", "Bioprospección", "Metabolito secundario", "Endofítico" y
"bioluminiscencia". Por último, es posible observar que los estudios sobre esta especie de hongo bioluminiscente se han
centrado en explicar el mecanismo de producción de luz y sus potenciales actividades biológicas, entre ellas, los efectos
antitumorales, antioxidantes, antimicrobianos y antileishmania.
Palabras clave: Hongo de la bioluminiscencia; Neonothopanus gardneri; Flor de coco; Agaricales.
1. Introduction
Living organisms that emit light, such as plants and animals, have long attracted the interest and curiosity of man (Olivei
et all., 2013). There are mentions of some descriptions that corroborate with this statement, such as Chinese songs and poetry
that quote “night travelers”, which is credited treat of fireflies (Lee, 2008). Although in this period records on the luminescence
of these beings are fragmented and scarce, partly attributed to technologies and rustic writing techniques, it was from the time
of Aristotle (384-322), who recognized and recorded observations about the self-luminosity of these organisms. In recent years,
there has been a growing interest of the researchers in the light emitted by organic beings (Shimomura, 2006; Lee, 2008; Oliveira
et al., 2013; Puzyr et al., 2019).
The term luminescence was proposed by Wiedemann (1888), who felt the need of a uniform designation for bodies with
cold light emission. The use of the word “bioluminescence”, refers to the living beings that emit this type of light as a result of
chemical reactions, may have been used for the first time by Harvey (1916) and is present in several species of bacteria,
dinoflagellates, fungi, marine and land animals (Shimomura, 2006).
Bioluminescence has been observed mainly in aquatic marine organisms. It is present in around 700 genera of
eukaryotes and prokaryotes of 16 phyla (Stevani et al., 2013). Although much less common in terrestrial environment, this
phenomenon is confirmed almost exclusively in animals, reported in the genera of Nematoda and Arthropoda, and in fungi,
present in about 71 species of the order Agaricales (Kahlke & Umbers, 2016). In spite of the fact that there is no apparent specific
relationship for its distribution, fungi are one of the few taxa by which it is believed to have a conserved system of this
characteristic (Shimomura, 2006; Oliveira et al., 2013; Stevani et al., 2013; Kahlke & Umbers, 2016).
Until recently, there were some controversies about the green light emanated by bioluminescent fungi due to the ultraweak emission of photons. However, oxygen is fundamental and extremely important in the process, it should not be confused
with the emission of light generated from oxidative stress, that is, with chemiluminescence (Sivinski et al., 1998; Oliveira et al.,
2
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
2013; Kahlke & Umbers, 2016). A justification for the production of light in fungi can be directly linked to communication,
predation, mating, repulsion, etc. It is believed that light works as a way for the body to get rid of reactive oxygen species (ROS)
and attract spore-dispersing insects (Paley & Prescher, 2014; Waldenmaier et al., 2015).
In 2013, there were approximately 71 species of known terrestrial bioluminescent fungi belonging to four bloodlines
evolutionary found in different parts of the world: Micenoide (Asia, Europe, Americas, Africa, Caribbean, Australia and Pacific
Islands), Omphalotus (Asia, Europe, Americas, Caribbean and Australia), Armillaria (one native from South / Southeast Asia
and four from Europe / North America) Lucentipes (Brazil) (Lloyd & Gentry, 2009; Oliveira et al., 2012, 2013).
Bioluminescent fungi, in general, are saprophytes, that is, they feed on decomposing organic matter, “white rot”
agaricus, and due to the high humidity and hot climate, are found mainly in tropical areas. The emission of light by these
organisms is not evenly distributed throughout their structure and may be present in the mycelium, fruiting body or both.
Although popular for their continuous brightness, they are much less studied than other bioluminescent organisms. Among the
slightly more than 71 species reported, 12 of them can be found in Brazilian territory (Deheyn & Latz, 2007; Oliveira et al.,
2013; Stevani et al., 2013). This review describes an interesting fungal species Neonothopanus gardneri; the largest
bioluminescent mushroom in Brazil and one of the largest reported to date (Waldenmaier, 2015).
2. Methodology
As stated by Gonçalves (2021), the methodology is the detailed, rigorous and exact explanation of every action
developed in the research work. In the case of literature review articles, their data collection is based on the search for descriptors
that make up the topic addressed in database, books and scientific articles. Thus, in order to achieve the objective of the work,
an integrative review was chosen because it allows a broader investigation and considers a diverse sample of studies with
different approaches and methodologies, resulting in a diversified and understandable panorama of the investigated study object.
Thus, this integrative review article is a qualitative bibliographical study that aims to discuss what has been reported
and studied about the bioluminescent fungus of the species Neonothopanus gardneri in studies published between 1990 to 2021.
For this purpose, searches were made for books and articles scientific in the following databases: Scopus, PubMed,
ScienceDirect, web of science, Royal Society of Chemistry (RSC) Publishing and Google Scholar. For filtering the productions,
the following keywords were used: “Neonothopanus”, “Neonothopanus gardneri”, “Bioactivities”, “Bioprospection”,
“Secondary Metabolite”, “Endophytic” “Bioluminescence”. We used as inclusion criteria the works in Portuguese and English
that presented in the title or abstract at least one of the used descriptors. As exclusion criteria those that did not fit the theme
(Figure 1).
3
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
Figure 1. Flowchart of identification and selection of found.
Source: Authors (2022).
3. Results and Discussion
As shown in the flowchart (figure 1), after the search, screening and selection of records, 42 studies were considered
relevant to the discussion of the theme. Thus, after reading them in their entirety, we collected those exposed in chart 1.
Chart 1. Studies located in the databases Scopus, PubMed, ScienceDirect, web of science, Royal Society of Chemistry (RSC)
Publishing and Google Scholar (1990-2021).
Reference
(Baker &
Dunlap, 2012).
Title
The circadian clock of
Neurospora crassa
(Blunt, 2006)
Marine natural products.
Natural
The luminescent system of
the luminous fungus
Neonothopanus nambi
(Bondar et al.,
2011)
Objective
It presents a review focused on
the contributions to the field of
chronobiology obtained from
the study of the circadian system
in Neurospora crassa.
Literature review on marine
natural products.
Investigate the luminescent
system of the luminous fungus
Neonothopanus nambi, which
was found in the rainforests of
South Vietnam.
(Bondar et al.,
2013)
On the mechanism of
luminescence of the
fungus Neonothopanus
nambi
Investigate the luminescent
system of the luminous fungus
Neonothopanus nambi, which
was found in the rainforests of
South Vietnam.
(Bondar et al.,
2014)
Isolation of Luminescence
System from the
Luminescent Fungus
Neonothopanus nambi
Investigate the luminescent
system of the
luminous fungus
Neonothopanus nambi, which
was
found in the rainforests of South
Vietnam.
4
Results
Introduces the fundamentals of circadian
rhythms, the filamentous fungus model
Neurospora crassa, and provides an overview
of the molecular components and regulation
of the circadian clock.
review of the literature for 2007 and describes
961 new compounds from 350 articles
in this study, primary data were obtained
on the structural and functional organization
and
physical-chemical properties of the
luminescence system has the superior tropical
luminous fungus N. nambi.
It has been shown that the mycelial globules
transferred to a measuring cuvette from the
nutrient medium display no luminescence;
that is, the luminescence level does not
significantly differ from the background noise
of the measurement system. the incubation of
N. nambi mycelial globules in DI water for
12–24 h leads to a considerable increase in
the luminescence.
It was found that supernatants isolated from
the mycelium of the luminous fungus N.
nambi by the method described emitted long
luminescence. This fact allowed us to
conclude that a selfsufficient luminescent
system that ensures luminescence in vitro was
isolated from this fungal species.
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
(Capelari et al.,
2011).
(Desjardin et al.,
2008)
(Dubois, 1885)
(Dunlap, 1999)
Neonothopanus gardneri:
A new combination for a
bioluminescent agaric
from Brazil
Fungi bioluminescence
revisited
Note sur la physiologic
des pyrophores
Molecular bases for
circadian clocks
(Fagg et al.,
2015).
Useful Brazilian plants
listed in the manuscripts
and publications of the
Scottish medic and
naturalist George Gardner
(1812-1849)
(Gomes, 2019).
Toxicogenética e os
efeitos antitumorais de
extratos obtidos do
neonothopanus gardneri:
potencial biotecnológico e
farmacêutico
(Hevia et al.,
2016).
Circadian clocks and the
regulation of virulence in
fungi: Getting up to speed
(Ilondu & Okiti,
2016)
Bioluminescence in
Mushroom and Its
Application Potentials
(Jayakumar et
al., 2009)
In-vitro antioxidant
activities of an ethanolic
extract of the oyster
mushroom, Pleurotus
ostreatus
Bioluminescence in
Progress
(Johnson &
Haneda, 1966).
(Kanokmedhakul
et al., 2012)
Cytotoxic sesquiterpenes
from luminescent
mushroom Neonothopanus
nambi
(Kaskova et al.,
2017)
Mechanism and color
modulation of fungal
bioluminescence
Re-evaluation of its taxonomic
affinities.
Agaricus gardneri was transferred to the
genus Neonothopanus based on a combination
of morphological and molecular data.
To present a review of the
research carried out during the
last 30 years on the distribution,
taxonomy, phylogeny, ecology,
physiology and mechanisms of
bioluminescence of luminescent
fungi.
Verified the chemical nature of
the bioluminescence reaction.
Detail the molecular basis of
circadian systems
We recognized 64 species of bioluminescent
fungi belonging to at least different
evolutionary lineages, named Omphalotus,
Armillaria and mycenoid.
To present data recorded by
Gardner in his
manuscript Catalogue of
Brazilian Plants regarding the
use of native plants by Brazilian
people and evaluate the extent to
which they have been explored.
Iwdentify some of the chemical
compounds by phytochemistry,
liquid chromatography and
magnetic resonance; in addition
to evaluating the toxicogenetic
and antitumor effects of
methanolic and ethyl acetate
extracts obtained from N.
gardneri, in Saccharomyces
cerevisiae, murine models for
Sarcoma 180 and for breast
cancer.
Comment on the overall
importance of clocks, what is
known in Neurospora and what
has been described in other
fungi including new insights on
the evolution of fungal clock
components.
Compile information on fungal
bioluminescence.
To investigate the antioxidant
potential of an ethanolic extract
of the oyster mushroom,
Pleurotus ostreatus.
Identification of enzymes generically called
luciferase and the substrate as luciferin
Described central aspects of the circadian
basis
time in at least four of these groups cyanobacteria, fungi, insects and mammals.
A total of 63 useful plants was recorded from
the Catalogue and a further 30 from Gardner׳s
book Travels in the Interior of
Brazil (Gardner, 1846). Of the recorded
names in the Catalogue, 46 (73%) could be
identified to species by consulting specimens
collected by Gardner and held at Kew.
Antitumor effects of the extract were
observed by mechanisms associated with
DNA damage and induction of apoptosis,
possibly with the inclusion of oxidative
damage induced by its bioactives.
Showed the molecular description of the
fungal circadian system, general importance
of clocks, what is known in Neurospora and
what has been described in other fungi,
including new insights into the evolution of
fungal clock components.
It presented bases to assist among
biochemists, chemists and physicists in the
isolation and purification of Luciferin
compounds present in these mushrooms and
other possible potentials in the production of
light.
The data generated by this study strongly
suggest that an ethanolic extract of the oyster
mushroom, P. ostreatus, has potent
antioxidant activity.
To isolate, characterize, and
synthesize the reactants that are
involved directly and indirectly
in the light-emitting process; to
understand the kinetics and
mechanism of their reactions;
and to interpret the action of
various factors that influence
light emission
isolation and characterization of
substances from the
bioluminescent fungus
Neonothopanus nambi
lists the types of bioluminescence systems
that have been extracted from various kinds of
luminescent organisms, together with the
minimal requirements for a light-emitting
reaction in vitro, and some of the
spectrographic properties of the systems
Report the structure of fungal
oxyluciferin, investigate the
mechanism of fungal
bioluminescence, and describe
the use of simple synthetic αpyrones as luciferins to produce
multicolor enzymatic
chemiluminescence
Provides insight into the mechanism of fungal
bioluminescence by characterizing the
oxyluciferin of 3-hydroxyhispidin and
expanding the knowledge on how styryl-3hydroxy-α-pyrones are chemiexcited in vivo.
5
Isolation of six new compounds along with a
known compound, aurisin A.
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
(Kirk, 2008)
Dictionary of the Fungi
Present taxonomic data.
(Lee, 2008)
Bioluminescence: The
First 3000 Years (Review)
(Love &
Prescher, 2020)
Seeing (and using) the
Light: Recent
Developments in
Bioluminescence
Technology
Describes the many
investigations of animal
luminescence up to the end of
the 19th Century.
Highlights recent advance in
bioluminescent probe
development that are driving
new directions in biomedical
research.
(Menolli et al.,
2014)
The genus Pleurotus in
Brazil: A molecular and
taxonomic overview
(Min et al.,
2017)
Theoretically obtained
insight into the mechanism
and dioxetanone species
responsible for the singlet
chemiexcitation of
Coelenterazine
(MontenegroMontero et al.,
2015)
Aro und the Fungal Clock:
Recent Advances in the
Molecular Study of
Circadian Clocks in
Neurospora and Other
Fungi
Identification of hispidin
as a bioluminescent active
compound and its
recycling biosynthesis in
the luminous fungal
fruiting body
(Oba et al.,
2017).
Present for the first time a
discussion on the recognition of
at least five species of Pleurotus
in Brazil
Determine what the dioxetanone
species responsible for efficient
chemiexcitation are, in the
luminescent reactions of
Coelenterazine.
discuss the circadian system of
the filamentous fungus
Neurospora crassa
Check the presence of hispidin
as a bioluminescent active
compound at 25-1000 pmol g-1
in the fruiting bodies of Mycena
chlorophos, Omphalotus
japonicus, and Neonothopanus
gardneri.
To discuss the distribution of
bioluminescent fungi on Earth,
attempts to elucidate the
mechanism involved in light
emission, and presents
preliminary results on the
evolution and ecological role of
fungal bioluminescence.
verify if the bioluminescence
mechanism is the same in all
four evolutionary lineages
suggesting a single origin of
luminescence in fungi, or if each
lineage has a unique light
emission mechanism implying
independent origins.
Enzymatically obtain in vitro
light emission from the assay of
cold and hot extracts using
different species of fungi.
Influence and relationship of
circadian control on fungal
bioluminescence
(Olivei et all.,
2013).
Bioluminescência de
fungos: Distribuição,
função e mecanismo de
emissão de luz.
(Olivei et all.,
2012).
Evidence that a single
bioluminescent system is
shared by all known
bioluminescent fungal
lineages
(Oliveira &
Stevani, 2009).
The enzymatic nature of
fungal bioluminescence
(Oliveira &
Stevani, 2015).
Circadian control sheds
light on fungal
bioluminescence
(Pegler, 1988)
Agaricales of Brazil
Described by M. J.
Berkeley
To evaluate fifty-five species of
agaricoid fungi described from
Brazil by M. J. Berkeley
between 1840 and 1876.
(Petersen &
KrisaiGreilhuber,
1999)
Type specimen studies in
Pleurotus
to identify the epithets of the
Pleurotus species that did not
have their type specimens
documented
6
Contains the consensus on the fungal
taxonomic hierarchy to the rank of genus.
Presents relevant aspects in 300 years of
research on bioluminescence.
Show how new luciferins and engineered
luciferases are expanding the scope of optical
imaging. also highlight how bioluminescent
systems are being leveraged not just for
sensing-but also controlling-biological
processes.
Presents a list of all epithets that have been
recorded for Brazil and the current update of
their taxonomic status.
Efficient chemiexcitation of Coelenterazine
results from a neutral dioxetanone; is
achieved without significant electron/charge
transfer;The thermolysis of anionic
dioxetanones leads to less efficient
chemiexcitation occurs albeit significant
electron and charge transfers.
Provided additional insights into the
physiological impact of the clock and
potential additional functions of clock
proteins in fungi and speculate on the
presence of FRQ or FRQ-like proteins in
diverse fungal lineages.
The results suggest that luminous mushrooms
contain hispidin as a luciferin precursor and
the non-luminous "young" fruiting bodies
exhibited luminescence by hispidin treatment.
It contributes to the discussion about the
bioluminescence mechanism in fungi for new
perspectives of academic and applied studies.
The results support the hypothesis that all four
lineages of luminescent fungi share the same
type of luciferin and luciferase, that there is a
single luminescent mechanism in the Fungi,
and that fungal luciferin is not a ubiquitous
molecule in fungal metabolism.
Kinetic data suggest a consecutive two-step
enzymatic mechanism and corroborate the
enzymatic proposal of Airth and Foerster.
Report that bioluminescence from the
mycelium of Neonothopanus gardneri is
controlled by a temperature compensated
circadian clock, the result of cycles in
content/activity of the luciferase, reductase,
and the luciferin that comprise the
luminescent system.
He following new combinations are proposed:
Eccilia vespertilio (Berk.) Pegler (Agaricus
vespertilio Berk.), Gymnopilus panurensis
(Berk.) Pegler (Agaricus panurensis Berk.),
G. psamminus (Berk.) Pegler (Agaricus
psamminus Berk.), and Pleurotus
submembranaceus (Berk.) Pegler (Lentinus
submembranaceus Berk.).
Report on three additional species, P.
cornucopiae, P. eugrammus.and P. opuntiae
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
(Petushkov et al.,
2014)
A novel type of luciferin
from the Siberian
luminous earthworm
Fridericia heliota:
structure elucidation by
spectral studies and total
synthesis
The structure elucidation and
synthesis of the luciferin from
the recently discovered
luminous earthworm Fridericia
heliota.
(Petushkov et al.,
2018)
Isolation and Purification
of Fungal Luciferase from
Neonothopanus nimbi.
(Petushkov et al.,
2015)
Components of the
luminescent system of the
luminous fungus
Neonothopanus nambi.
(Queiroz, 2017)
Composição fitoquímica e
atividades antileishmania,
citotóxica,
imunomoduladora e
genotóxica de
Neonothopanus gardneri:
um cogumelo
bioluminescente
Extracellular Oxidases of
Basidiomycete
Neonothopanus nambi:
Isolation and Some
Properties
The aim of this study was to
isolate and purify the luciferase
of the luminous fungus
Neonothopanus nambi for its
subsequent sequencing.
The aim of this work was to
separate the protein and
nonprotein components of the
light emitting system of the
fungus Neonothopanus nambi
and to study some of their
properties.
Identify bioactive compounds
and their respective biological
activity, in addition to
elucidating their chemical
structures.
(Ronzhin, 2020)
(Samuel et al.,
2011)
Antibacterial activity of
marine derived fungi
collected from South East
Coast of Tamilnadu, India
(Shimomura,
2006)
Bioluminescence:
Chemical principles and
methods.
(Smetanina et
al., 2007)
Indole Alkaloids Produced
by A Marine Fungus
Isolate Of Penicillium
Janthinellum Biourge.
(Stevani et al.,
2013)
Current status of research
on fungal
bioluminescence:
Biochemistry and
prospects for
ecotoxicological
application
Toxicity of metal cations
and phenolic compounds
to the bioluminescent
fungus Neonothopanus
gardneri
(Ventura, 2021)
(Waldenmaier et
al., 2015)
(Wilson &
Hastings, 1998)
Circadian rhythm in
fungal bioluminescence:
nature’s bright idea
Bioluminescence
Isolate extracellular oxidases
from the mycelium of the
basidiomycete Neonothopanus
nambi by treating its biomass
with β-glucosidase and to the
study of some of their
properties.
To study the antibacterial
activity of the marine fungi,
collected
from the south east coastal area
of Tamilnadu, India.
Provide a comprehensive
overview of the biochemical
aspects of all currently known
luminous organisms
To describe the isolation and
structural elucidation of new
alkaloids produced by the
marine fungus P. janthinellum.
To present an overview of the
current state of the study of
fungal luminescence and the
application of bioluminescent
fungi as versatile tool in
ecotoxicology.
To describe a toxicological
bioassay that relies on a 24-h
variation of total light emitted
by the mycelium of the
bioluminescent fungus
Neonothopanus gardneri when
exposed to a toxicant.
Present a mini review on the
circadian rhythm in fungal
bioluminescence.
To present a broad overview of
the chemistry and cellular
control of bioluminescence with
deeper discussions of selected
topics.
Source: Authors (2022).
7
The novel luciferin was found to have an
unusual extensively modified peptidic nature,
thus implying an unprecedented mechanism
of action. UV, fluorescence, NMR, and
HRMS spectroscopy studies were performed
in the isolated substance and revealed four
isomeric structures that conform to spectral
data.
Have for the first time obtained a high-purity
fungal luciferase suitable for Edman
sequencing (N-terminal sequencing) and mass
spectrometric sequencing.
The results obtained in this study indicate that
the luminescent system of luminous fungus N.
nambi includes at least four components that
ensure light emission in vitro.
He obtained positive results for metabolites
such as alkaloids, reducing sugars, tannins,
depsides, among others. Antileishmanial,
cytotoxic and immunomodulatory activity
were found.
Two protein fractions were isolated from the
extracts, which contained enzymes with
oxidase activity conventionally called F1 and
F2.
Among the used fungal species, Geotrichum
candidum was found to be active against all
human pathogenic bacterial strains.
It is the first book to provide chemical
information on all known bioluminescence
systems.
Three new indole alkaloids, shearinines D, E,
and F, together with the known shearinine A
were isolated from the marine-derived strain
of the fungus Penicillium janthinellum
Biourge.
It contributes to studies related to fungal
bioluminescence, presenting a recent
overview of research in the area.
Among the compounds tested, found that N.
gardneri presents a predictable
bioluminescence and growth pattern, and is
highly sensitive to these compounds.
Contributes to studies related to the chemical
basis of bioluminescence and reports about N.
gardneri.
Contributes to interest and importance of
bioluminescence to a reader unfamiliar with
the field.
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
3.1 Discovery and classifications attributed to Neonothopanus gardneri
George Gardner, a Scottish naturalist and surgeon, is among the scientists who traveled the most in Brazil cataloging
information about biodiversity in the early 19th century. Although the Brazilian flora has already been extensively studied, few
ventured into the interior of the country as Gardner did, mainly in the northeast region (Fagg et al., 2015). In 1840, in his work
‘‘Description of a new phosphorescent species of Agaricus’’ the naturalist, after observing children playing with a luminous
object and performing a careful inspection, first identified an Agaricus species belonging to the required tribe Pleurotus of Fries
(Capelari et al., 2011).
It is popularly known as "coconut flower" (flor de coco) because of its resemblance to a flower growing at the base of
a palm tree. The species was formally named in 1840 in an article written by G. Gardner as Agaricus gardneri Berk. Later
Berkeley, in his 1843 work titled ‘‘Notices of some Brazilian fungi’’, refers to the species as Agaricus (Omphalia) gardneri.
Shortly thereafter, in 1887, Saccardo reclassified it as Pleurotus gardneri. However, Pegler (1988), after carrying out an analysis,
found that although it had characteristics typical of Omphalotus olearius, it was one of its variants, but to distinguish A. gardneri
as a different species, it required to study with fresh material in which it had no access (Capelari et al., 2011).
More recently, after studies of molecular and morphological data of material collected in the states of Tocantins and
Piauí (Brazil), the species of Agaricus gardneri was transferred to Neonothopanus gardneri. This mushroom has greater
incidence in the North and Northeast regions of Brazil. It is distributed in coconuts forests, a transitional biome between the
Amazon Forest and the Caatinga, in the states of Maranhão, Piauí, Tocantins and Goiás. They are found mainly in decomposing
leaves and in the trunk dwarf palms popularly called “pidomba” (Attalea oleifera) or babassu (Orbignya phalerata) (Capelari et
al., 2011; Menolli et al., 2014).
3.2 Taxonomic classification
In the order Agaricales, most of the bioluminescent fungi belong to the families Mycenaceae and Marasmiaceae. This
last one is characterized by the presence of basidiomycetes which in general presents resistant stems (stipe) and, during dry
periods, have the ability to collect, wither, as a way to cross the drought and recover later (Kaskova et all., 2019; Johnson &
Haneda, 1966).
The genus Neonothopanus was proposed in 1999 after the need for a new classification for Lentinus (Pleurotus)
eugrammus once the categorization of Nothopanus was based on a misinterpretation, given that not match the type specimen of
that species. In addition, the term was attributed a taxonomically distinct concept, although later it was found to be correct.
Horak, in 1968, classified the specimen as Pleurotus using Nothopanus with a synonym of that genus. The impasse between
such concepts arose the need for a new nomenclature: Neonothopanus (Kirk, 2008).
In Latin America the main representative of the Neonothopanus (Marasmiaceae) is Neonothopanus gardneri species,
found mainly in Brazilian ecotones territory, the cocal forests. A molecular study carried out by Capelari et al. (2011)
demonstrated that the species did not present in any analysis a monophyletic lineage with any of the Omphalotus family, but that
it resembled Neonothopanus nambi, differing mainly in size of the basidiospore, stature and its pigmentation (Waldenmaier,
2015).
Although N. nambi has been relatively more studied in recent years (Bondar et al., 2011, 2013, 2014; Purtov, 2015,
2018; Ronzhin, 2020), presenting itself as a rich source of cytotoxic sesquiterpenes used against cancer cells. The studies have
rarely gone deeper to investigate the metabolites and possible biological activities of N. gardneri that can be observed by a few
reports present in the literature (Kanokmedhakul et al., 2012).
Among the main characteristics of the fungus Neonothopanus gardneri is the presence of strong bioluminescent
basidiomas, omphalotoid basidiomes with a coloration strain ranging from white to yellow and size around 10 - 90 mm, wide
8
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
lamellae, well-developed stipe, hyaline basidospores, smooth and globular as well as elongated - fusoid to sinuous-cylindrical
cheilocystidia (Johnson & Haneda, 1966).
Recently, a study was published describing a toxicological bioassay based on a 24-hour variation of the total light
emitted by the mycelium of the bioluminescent fungus Neonothopanus gardneri when exposed to a toxicant. It was found that
N. gardneri has a predictable bioluminescence and growth pattern, and is highly sensitive to the compounds Cd (II), 4nitrophenol, phenol and Cu (II). According to the authors, these characteristics offer valuable advantages and make N. gardneri
the ideal candidate for toxicological studies with basidiomycetes (Ventura, 2021).
3.3 Light emission mechanism
With the discovery of the organic nature of the reactions of mixtures outside living organisms that resulted in
luminescence and the oxidation reaction of lophine, the first chemiluminescent reaction discovered in 1877, the idea was born
that bioluminescence is reaction chemistry that occurs within these organisms. Raphael Dubois was the first to study
bioluminescence based on this idea in addition to trying to elucidate the chemical nature of light emission by fungi (Lee, 2008).
In his classic experiments, Dubois used “hot” and “cold” extracts obtained from organs of the beetle Pyrophorus
noctilucus or bivalve mollusc Pholas dactylus to study the luminescence of these organisms, and observed that the extract
prepared in cold water produced a brilliant solution that it gradually lost its intensity, while the preparation in hot water had its
shine extinguished. When the two solutions were mixed, the light emission was restored and Dubois thus verified the chemical
nature of the bioluminescence reaction. In addition, he observed that the cold extract contained thermolabile enzymes necessary
for light emission, while the hot extract contained heat-stable enzymes. These enzymes were generically called luciferase and
the substrate as luciferin (Dubois, 1885; Desjardin et al., 2008; Oliveira, 2012, 2013).
An experiment carried out by Airth and Foerster (Desjardin et al., 2008) using hot (A. mellea) and cold (Collybia
velutipes) extracts, that is, sources of luciferase and luciferin confirmed that the fungal bioluminescence process depends on two
enzymes: a soluble substrate dependent on nicotinamide adenine dinucleotide (NADPH) or nicotinamide adenine dinucleotide
reduced (NADH), responsible for the reduction of luciferin. When reacting with luciferase in the presence of molecular oxygen,
light emission is produced. That is, in synthesis, bioluminescence occurs through the oxidation of a substrate (luciferin) by
luciferase (enzyme) generating an excited by-product where the emission of light occurs, similar to the mechanism present in
bacteria, although they are distinguished by the lack of stimulation in the presence of reduced flavin mononucleotide (FMNH 2)
or adenine flavin dinucleotide (FADH 2) (Figure 2) (Wilson & Hastings, 1998; Desjardin et al., 2008; Oliveira et al., 2013;
Stevani et al., 2013).
9
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
Figure 2: Light emission mechanism in fungi and bacteria.
Source: Adapted from Oliveira et al., (2013).
In a bioluminescent reaction, the enzyme (luciferase) requires the presence of oxygen in the system with luciferin (a
small molecule that generates light), acting as a catalyst and can be recycled. The total amount of light produced in the reaction
is directly linked to the amount of substrate (luciferin) available. Looking at the chemical level, the vast majority of light
emissions by living organisms occur as a result of the decomposition of a four-membered dioxetone ring. Thus, although these
peroxides require little energy to break the bonds and open the ring, they result in a molecule in the electronically excited state
that seeks stability, returning to its fundamental state and the energy is released in the form of light in the visible range (Min et
al., 2017; Waldenmaier et al., 2015).
Oliveira et al. (2012), when studying bioluminescence in four different strains of fungi obtained results that corroborate
the idea of a common mechanism for light emission by these organisms, where it is believed to share the same luciferin /
luciferase or a similar one. Furthermore, when performing cross tests with hot / cold extracts on seven species that represented
the four bioluminescent strains, including N. gardneri, and comparing them with non-bioluminescent species, the emission of
light was observed only in the first, suggesting a single pathway bioluminescent in the evolution of the order Agaricales.
At different stages of their life cycle, bioluminescent fungi emit greenish tint light in a wavelength range (λ) between
520 to 530 nanometers (Shimomura, 2006; Ilondu & Okiti, 2016). This emission occurs mainly in certain periods of its
development. In 2009, a study reported based on in vitro tests that the light emission of the fungus species Neonothopanus
gardneri occurs continuously with λ max = 533 nanometers (Oliveira & Stevani, 2009). Bioluminescence in this species is mainly
governed by a circadian clock, that is, a molecular mechanism with a rhythm around 24 hours that allows organisms to perform
an infinite number of biological processes in sync with the daily cycles of the environment (Waldenmaier, 2015).
This species of central clock has been described in several organisms, having in common an internal, autonomous
negative feedback oscillator with rhythms that is basically the same at different temperatures, in addition to responding according
to information it receives from the environment, such as light and light (Dunlap, 1999; Montenegro-Montero et al., 2015).
N. gardneri, as described by Oliveira et al. (2015) in a study with agar plates freshly inoculated with the mycelium of
the species, the light emission oscillates in a circadian rhythm of approximately 22 hours, reaching its peak at night. A curious
fact lies in Neurospora crassa, a species of non-bioluminescent fungus from the phylum Ascomycota, present a circadian period
10
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
also less than 24 hours (22.5 hours) (Baker & Dunlap, 2012). Furthermore, the establishment of rhythmic bioluminescence, that
is, a circadian clock, provided for the first time a basis for explaining the presence of luminescence in these organisms. Although
unknown, bioluminescence can have a range of biological and ecological functions, not only as an improbable metabolic byproduct but with an adaptive meaning, such as attracting insects and thus dispensing spores providing an evolutionary advantage
compared to non-luminescent fungi (Hevia et al., 2016).
Knowing the basic pillars of the bioluminescent chemical reaction in living organisms, that occurs in the presence of
a substrate (luciferin), a reductase dependent on soluble NAD(P)H, membrane-bound oxygen (luciferase) and oxygen (Petersen
& Krisai-Greilhuber, 1999; Wilson & Hastings, 1998; Oliveira et al. 2015) the light emission in N. gardneri was explained by
hydrolysis catalyzed by the oxyluciferin (caffeylpyruvic acid), which emits light in this system from enzymatic hydrolysis
resulting in the production of caffeic acid (Figure 3) (Hevia et al., 2016).
Figure 3: Chemical reaction of fungal bioluminescence.
Source: Adapted from Oba et al. (2017).
Purtov et al. (2015), while studying the mechanism of bioluminescence in fungi using the mycelium N. nambi, reported
hispidin as a precursor of fungal luciferin, 3 - hydroxyspidine, and in this way, has turned to isolation, elucidation and
characterization of luciferin structures. Although it is present in nature, few of these molecules had their chemical structure
determined and many of them are still unknown.
In 2014, Petushkov et al. (2014) reported the chemical structure of a luciferin present in a bioluminescent earthworm
Fridericia heliota and thus elucidates the eighth structure of bioluminescent molecules present in organisms (Figure 4), as well
as coelenterazine and its derivatives (used by many taxonomically unrelated species), firefly luciferins, crustacean
(Dinoflagellata) (Cypridina and Latia lapa) and a worm (Diplocardia longa). However, it is worth noting the fact that N. gardneri
11
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
has not yet had its luciferin structure elucidated.
Figure 4: Chemical structures of luciferins identified in different species of organisms so far in literature.
Source: Authors (2022).
3.4 Biological activity
Fungi belonging to the phylum Basidiomycota are among the sources of obtaining new natural products most used by
the industry in recent years, mainly due to their wide range of biological activities due to the bioactive compounds isolated from
these organisms such as alkaloids, terpenoids, steroids, phenolic compounds, and flavonoids. Investigations on the bioactive
compounds and secondary metabolites present in the species that make up the genus Neonothopanus are mainly focused on N.
gardneri and N. nambi, with almost all studies focused on the latter - N. nambi (Blunt, 2006; Smetanina et al., 2007; Jayakumar
et al., 2009: Samuel et al., 2011; Love & Prescher, 2020).
In an attempt to identify bioactive compounds that are responsible for biological activity, in addition to elucidating their
respective chemical structures, some scholars have dedicated themselves to studying N. gardneri extensively, mainly due to its
promising characteristics against some neglected diseases (Queiroz, 2017; Gomes, 2019).
Queiroz (2017) evaluated cytotoxicity, genotoxicity, immunomodulatory, and antileishmania activity in extracts of N.
gardneri and became one of the pioneers in the search to identify the bioactivities. of this species. In this study, by performing
qualitative phytochemical characterization with ethyl acetate extract (AcOEt), methanolic extract (MeOH) and ethanolic extract
(EtOH) from N. gardneri, he obtained positive results for metabolites such as alkaloids, reducing sugars, tannins and depsides
among others as shown in Table 1.
12
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
Table 1: Phytochemical screening of the extracts AcOEt, MeOH and EtOH of N. gardneri.
Extracts
MeOH EtOH
present present
Metabolites
Alkaloids
AcOEt
present
Reducing sugars
Proteins/ amino
acids
catechins
Tannins
present
absent
present
present
present
present
absent
absent
present
present
present
Absent
Depsídeos/
depsidonas
absent
present
present
Main biological activities
anticholinergic, antihypertensive, antimalarial, antitumor,
antitussive, antiviral, among others.
showed antitumor effects by inducing apoptosis
antioxidant
antioxidant activity, astringent properties,potencial citotóxico
contra parasita.
antioxidants, antivirals, antitumor, analgesics and antipyretics.
Reference
(QUEIROZ,
2017)
Source: Adapted from (Gomes, 2019).
The analysis of antileishmanial, cytotoxic and immunomodulatory activity justified mainly by virtue of natural products,
such as the tannins found in the extracts of N. gardneri as shown in Table 1, present potential biological activities mentioned
before. Queiroz (2017) while evaluating extracts and isolates of N. gardneri in vitro, observed a significant potential
antileishmanial activity causing death of promastigote forms of Leishmania amazonenses in approximately 80, 91 and 81% in
the concentration of 3,200 μg / mL and 74; 85; 59% at 1,600 μg / mL of the EtOH, MeOH and AcOEt extracts. While assessing
cytotoxicity, antileishmanial activity must have greater selectivity in relation to the parasite and less toxicity to host cells, Queiroz
(2017) described how the extracts obtained from N. gardneri have been shown to be more selective for the parasite than for
mammalian cells, to be able to increase the phagocytosis capacity of murine peritoneal macrophages in addition to their
lysosomal volume and to induce nitric oxide synthesis (NO).
When evaluating for the first time the cytotoxic, genotoxic and mutagenic potential of N. gardneri ethyl acetate and
methanolic extracts in meristematic cells of Allium cepa, an ability to reduce the mitotic index was observed, resulting in a
cytotoxic effect. Furthermore, the extracts did not cause a significant increase in the frequency of chromosomal changes, that is,
they did not result in genotoxicity (Queiroz, 2017).
Recently, Gomes (2019) studied the antitumor activity of methanolic extracts and ethyl acetate from N. gardneri in
Sarcoma 180 cells and breast cancer using murine models, in addition to possible toxicogenic effects. The extracts showed
antioxidant effects in Saccharomyces cerevisiae at low concentrations (500 and 1000 μg / mL). Furthermore, the author was able
to isolate and evaluate two natural substances with antitumoral potential, 7,8-Dihydroxy-13-oxo-heneicosa-9,11-dienamide (2)
and 7,8-Di-hydroxy-13-oxo- octadeca-9,11-dienamide isolated from the methanolic extract of N. gardneri.
In the analysis of the extracts, it was observed that the methanolic extract significantly interfered in the cell viability in
cells of the ascitic liquid of Sarcoma 180, presenting cytotoxic effects in the concentrations of 1000, 1500 and 2000μg / mL.
Furthermore, the extracts also showed genotoxicity at all concentrations tested (Gomes, 2019). According to Gomes (2019)
genotoxic damage may be directly linked to the N. gardneri bioluminescence mechanism, since it occurs under oxidative stress
due to the production of hydrogen peroxide (H 2O2), which also causes damage to DNA.
Moreover, Gomes (2019) reported for the first time the antitumor effect in breast carcinoma, obtaining reduction in the
breasts of female mice, after treatment with N. gardneri methanolic extract (10 mg / kg). In addition, characterized by
mechanisms associated with DNA damage, the methanolic extract showed a cytotoxic effect on breast carcinoma cells
culminating in a percentage increase in aptitude, due to nuclear dissolution and fragmentation, in neoplastic breast cells. The
tests of mutagenic tests in liver cells and bone marrow, according to the author's data, did not induce mutagenicity due to the
formation of micronuclei.
13
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
4. Final Considerations
Reports on the metabolites and biological activities of Neonothopanus gardneri are rare in the literature. The reported
bioactivities, such as: antitumor and antileishmania effect investigated by some researchers, show the importance and the need
to carry out more detailed studies for this species of bioluminescent fungus, since Basidiomycota is a source of compounds with
different applications and important pharmacological activities. The few in-depth reports on the species described here aim to
study its bioluminescent mechanism to identify luciferin. In addition, it is extremely important to carefully analyze the extracts
to understand the bioactive substances and their respective biological activities.
Based on our results, it is observed that most of the studies have been dedicated to the elucidation of the substances
involved in the bioluminescence mechanism of N. gardneri. Only in the last few years some interest in its biological activities
has been observed, resulting in a promising field of studies that should be explored. Therefore, studies for this purpose are
necessary.
Conflict of Interest
The authors declare that there are no conflicts of interest.
Acknowledgments
The authors are grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de
Amparo à Pesquisa do Estado do Piauí (FAPEPI) Individual Process No. 313038/2019-8, Institutional Process No. 680002/20138/ DCR-PI Program and Instituto Federal do Piauí (IFPI), Brazil.
References
Baker, C. L., Loros, J. J., & Dunlap, J. C. (2012). The circadian clock of Neurospora crassa. FEMS microbiology reviews, 36(1), 95–110.
Blunt, J. W., Copp, B. R., Munro, M. H. G., Northcote, P. T., & Prinsep, M. R. (2006). Marine natural products. Natural Product Reports, 23, 26-78.
Bondar, V. S., Puzyr, A. P., Purtov, K. V., Petunin, A. I., Burov, A. E., Rodicheva, E. K., Medvedeva, S. E., Shpak, B. A., Tyaglik, A. B., Shimomura, O., &
Gitel’zon, I. I. (2014). Isolation of luminescence system from the luminescent fungus Neonothopanus nambi. Doklady Biochemistry and Biophysics, 455 (1),
56–58.
Bondar, V. S., Puzyr, A. P., Purtov, K. V., Medvedeva, S. E., Rodicheva, E. K., & Gitelson, J. I. (2011). The luminescent system of the luminous fungus
Neonothopanus nambi. Doklady Biochemistry and Biophysics, 438 (1), 138–140.
Bondar, V. S., Rodicheva, E. K., Medvedeva, S. E., Tyulkova, N. A., Tyaglik, A. B., Shpak, B. A., & Gitelson, J. I. (2013) On the mechanism of luminescence
of the fungus Neonothopanus nambi. Doklady Biochemistry and Biophysics, 449 (1), 80–83.
Capelari, M., Desjardin, D. E., Perry, B. A., Asai, T., & Stevani, C. V. (2011) Neonothopanus gardneri: A new combination for a bioluminescent agaric from
Brazil. Mycologia, 103 (6), 1433–1440.
Deheyn, D. D., & Latz, M. I. (2007). Bioluminescence characteristics of a tropical terrestrial fungus (Basidiomycetes). Luminescence, 22 (5), 462–467.
Desjardin, D. E., Oliveira, A. G., & Stevani, C. V. (2008). Fungi bioluminescence revisited. Photochemical and Photobiological Sciences, 7, 170-182.
DUBOIS, R. (1885). Note sur la physiologic des pyrophores C. R. Séanc. Soc. Biol, 2, 559.
Dunlap J. C. (1999). Molecular bases for circadian clocks. Cell, 96 (2), 271–290.
Fagg, C. W., Lughadha, E. N., Milliken, W., Hind, D. J. N., & Brandão, M. G. L. (2015). Useful Brazilian plants listed in the manuscripts and publications of
the Scottish medic and naturalist George Gardner (1812-1849). Journal of Ethnopharmacology, 161, 18–29.
Gomes, D. C. V. (2019). Toxicogenética e os efeitos antitumorais de extratos obtidos do neonothopanus gardneri: potencial biotecnológico e farmacêutico (Tese
de Doutorado) - UFPI. Teresina.
Gonçalves, J. R. (2021). Manual de artigo de revisão de literatura. Processus, 2021.
Hevia, M. A., Canessa, P., & Larrondo, L. F. (2016). Circadian clocks and the regulation of virulence in fungi: Getting up to speed. Seminars in cell &
developmental biology, 57, 147–155.
14
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
Harvey, E. N. (1916). The mechanism of light production in animals. Science, 44 (1128), 208-209.
Ilondu, E. M., & And Okiti, A. A. (2016). Bioluminescence in Mushroom and Its Application Potentials. Nigerian Journal of Science and Environment, 14 (1),
132–139.
Jayakumar, T., Thomas, P. A., & Geraldine, P. (2009). In-vitro antioxidant activities of an ethanolic extract of the oyster mushroom, Pleurotus ostreatus.
Innovative Food Science and Emerging Technologies, 10 (2), 228–234.
Johnson, F. H., & Haneda, Y. (Eds.). (1966). Bioluminescence in Progress. Princeton University Press.
Kahlke, T., & Umbers, K. D. L. (2016). Bioluminescence. Current Biology, 26 (8), 313-314.
Kanokmedhakul, Somdej; Lekphrom, Ratsami; Kanokmedhakul, Kwanjai; Hahnvajanawong, Chariya; Bua-Art, Sureeporn; Saksirirat, Weerasak; Prabpai,
Samran; Kongsaeree, Palangpon. (2012). Cytotoxic sesquiterpenes from luminescent mushroom Neonothopanus nambi. Tetrahedron, 68 (39), 8261–8266.
Kaskova, Z. M., Dörr, F. A., Petushkov, V. N., Purtov, K. V., Tsarkova, A. S., Rodionova, N. S., Mineev, K. S., Guglya, E. B., Kotlobay, A., Baleeva, N. S.,
Baranov, M. S., Arseniev, A. S., Gitelson, J. I., Lukyanov, S., Suzuki, Y., Kanie, S., Pinto, E., Di Mascio, P., Waldenmaier, H. E., Pereira, T. A., & Yampolsky,
I. V. (2017). Mechanism and color modulation of fungal bioluminescence. Science advances, 3 (4), e1602847.
Kirk, P. M., Cannon, P. F., Minter, D. W., & Stalpers, J. A. (2008) Dictionary of the Fungi. 10th Edition, Wallingford, CABI.
Lee, J. (2008). Bioluminescence: The First 3000 Years (Review). Journal of Siberian Federal University. Biology, 1 (3), 194–205.
Lloyd, J. E., & Gentry, E. C. (2009). Bioluminescence. In: Encyclopedia of Insects. Elsevier Inc., 101–105
Love, A. C., & Prescher, J. A. (2020). Seeing (and using) the Light: Recent Developments in Bioluminescence Technology. Cell Chemical Biology Elsevier Ltd,
27 (8), 904-920.
Menolli, N., Breternitz, B. S., & Capelari, M. (2014). The genus Pleurotus in Brazil: A molecular and taxonomic overview. Mycoscience, 55 (5), 378–389.
Min, C. G., Ferreira, P. J. O., & Da Silva, L. P. (2017). Theoretically obtained insight into the mechanism and dioxetanone species responsible for the singlet
chemiexcitation of Coelenterazine. Journal of Photochemistry and Photobiology B: Biology, 174, 18–26.
Montenegro-Montero, A., Canessa, P., & Larrondo, L. F. (2015). Around the Fungal Clock: Recent Advances in the Molecular Study of Circadian Clocks in
Neurospora and Other Fungi. Advances in Genetics, 92, 107–184.
Oba, Y., Suzuki, Y., Martins, G. N. R., Carvalho, R. P., Pereira, Tatiana A., Waldenmaier, H. E., Kanie, S., Naito, M., Oliveira, A. G., Dörr, F. A., Pinto, E.,
Yampolskygh, I. V., & Stevani, C. V. (2017). Identification of hispidin as a bioluminescent active compound and its recycling biosynthesis in the luminous
fungal fruiting body. Photochemical and Photobiological Sciences, 16 (9), 1435–1440.
Oliveira, A. G., Carvalho, R. P., Waldenmaier, H. E., & Stevani, C. V. (2013). Bioluminescência de fungos: Distribuição, função e mecanismo de emissão de
luz. Química Nova, 36 (2), 314-319.
Oliveira, A. G., Desjardin, D. E., Perry, B. A., & Stevani, C. V. (2012). Evidence that a single bioluminescent system is shared by all known bioluminescent
fungal lineages. Photochemical and Photobiological Sciences, 11 (5), 848–852.
Oliveira, A. G., Stevani, C. V. (2009). The enzymatic nature of fungal bioluminescence. Photochemical and Photobiological Sciences, 8 (10), 1416–1421.
Oliveira, A. G., Stevani, C. V., Waldenmaier, H. E., Viviani, V., Emerson, J. M., Loros, J. J., & Dunlap, J. C. (2015). Circadian control sheds light on fungal
bioluminescence. Current biology: CB, 25 (7), 964–968.
Paley, M. A., & Prescher, J. A. (2014). Bioluminescence: A versatile technique for imaging cellular and molecular features. MedChemComm, 5 (3), 255-267.
Pegler, D. N. (1988). Agaricales of Brazil Described by M. J. Berkeley. Kew Bulletin, 43 (3), 453.
Petersen, R. H., & Krisai-Greilhuber, I. (1999). Type specimen studies in Pleurotus. In: Persoonia - Molecular Phylogeny and Evolution of Fungi.
Petushkov, V. N., Dubinnyi, M. A., Tsarkova, A. S., Rodionova, N. S., Baranov, M. S., Kublitski, V. S., Shimomura, O., & Yampolsky, I. V. (2014). A novel
type of luciferin from the Siberian luminous earthworm Fridericia heliota: structure elucidation by spectral studies and total synthesis. Angewandte Chemie
(International ed. in English), 53(22), 5566–5568.
Purtov, K. V., Gorokhovatsky, A. Y., Kotlobay, A. A., Osipova, Z. M., Petushkov, V.N., Rodionova, N. S., Tsarkova, A.S., Chepurnykh, T. V., Yampolsky, I.
V., & Gitelson, J. I. (2018) Isolation and Purification of Fungal Luciferase from Neonothopanus nimbi. Doklady Biochemistry and Biophysics, 480 (1), 177–
180.
Purtov, K. V., Petunin, A. I., Rodicheva, E. K., Bondar, V. S., & Gitelson, J. I. (2015). Components of the luminescent system of the luminous fungus
Neonothopanus nambi. Doklady Biochemistry and Biophysics, 461 (1), 65–68.
Puzyr, A. P., Burov, A. E., Medvedeva, S. E., Burova, O. G., & Bondar, V. S. (2019). Two forms of substrate for the bioluminescent reaction in three species of
basidiomycetes. Mycology, 10 (2), 84–91.
Queiroz, B. C. S. H. (2017). Composição fitoquímica e atividades antileishmania, citotóxica, imunomoduladora e genotóxica de Neonothopanus gardneri : um
cogumelo bioluminescente (Dissertação de Mestrado) - UFPI. Teresina.
Ronzhin, N. O., Mogilnaya, O. A., Artemenko, K. S., Posokhina, E. D., & Bondar, V. S. (2020). Extracellular Oxidases of Basidiomycete Neonothopanus nambi:
Isolation and Some Properties. Doklady Biochemistry and Biophysics, 490 (1), 38–42.
15
Research, Society and Development, v. 11, n. 5, e16811528009, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i5.28009
Samuel, P., Prince, L., & Prabakaran, P. (2011). Antibacterial activity of marine derived fungi collected from South East Coast of Tamilnadu, India. Journal of
Microbiology and Biotechnology Research, 1 (4), 86-94.
Shimomura, O. (2006) Bioluminescence: Chemical principles and methods. World Scientific.
Sivinski, J., Aluja, M., Holler, T., & Eitam, A. (1998). Phenological Comparison of Two Braconid Parasitoids of the Caribbean Fruit Fly (Diptera: Tephritidae).
Environmental Entomology, 27 (2), 360–365.
Smetanina, O. F., Kalinovsky, A. I., Khudyakova, Y. V., Pivkin, M. V., Dmitrenok, P. S., Fedorov, S. N., Ji, H., Kwak, J. Y., & Kuznetsova, T. A. (2007). Indole
Alkaloids Produced by A Marine Fungus Isolate Of Penicillium Janthinellum Biourge. Journal Of Natural Products, 70 (6), 906–909.
Stevani, C. V., Oliveira, A. G., Mendes, L. F., Ventura, F. F., Waldenmaier, H. E., Carvalho, R. P., & Pereira, T. A. (2013) Current status of research on fungal
bioluminescence: Biochemistry and prospects for ecotoxicological application. Photochemistry and Photobiology, 89 (6), 1318–1326.
Ventura, F. F., Soares, D. M. M., Bayle, K., Oliveira, A. G., Bechara, E. J. H., Freire, R. S., Stevani, C. V. (2021). Toxicity of metal cations and phenolic
compounds to the bioluminescent fungus Neonothopanus gardneri. Environmental Advances, 4, 1-7.
Waldenmaier, H. E., Oliveira, A. G., Loros, J. J., Dunlap J. C. & Stevani, C. V. (2015). Circadian rhythm in fungal bioluminescence: nature’s bright idea.
Microbiology Today: Light, 98-101.
Wiedemann, E. (1888). Ueber Fluorescenz und Phosphorescenz I. Abhandlung. Annalen der Physik, 270 (7), 446–463.
Wilson, T., & Hastings, J. W. (1998). Bioluminescence. Annual Review of Cell and Developmental Biology,14 (1), 197–230.
16
Mahendra Rai