FULL PAPER
DOI: 10.1002/ejoc.201200757
Epicolactone – Natural Product Isolated from the Sugarcane Endophytic
Fungus Epicoccum nigrum
Francisca Diana da Silva Araújo,
[a]
Léia Cecilia de Lima Fávaro,
[b]
Welington Luiz Araújo,
[c]
Fábio Lazzarotto de Oliveira,
[a]
Ricardo Aparicio,
[a]
and Anita Jocelyne Marsaioli*
[a]
Keywords: Natural products / Bioorganic chemistry / Mutagenesis / Epicoccum nigrum
The endophytic fungus Epicoccum nigrum was isolated from
sugarcane and the bioguided fractionation of the ethyl acet-
ate extract led to the isolation of epicolactone, mellein, and
4,5-dimethylresorcinol. Characterization of epicolactone by
MS, NMR and X-ray crystallography revealed a new natural
Introduction
Fungi are important in biotechnological processes ap-
plied in the food, cosmetic, and pharmaceutical indus-
tries.
[1]
Notwithstanding, the relevance of the predicted
fungi species (1.5 million), only 5.7% have been described,
and of these only a few have actually been investigated for
the production of bioactive metabolites.
[2]
Among these, en-
dophytic fungi living in association with plants are a rich
source of biologically active compounds.
[3]
Epicoccum nigrum Link (syn. E. purpurascens Ehrenb. ex
Schlecht) is an ascomycete fungus distributed worldwide,
which colonizes different types of soils and host plants.
[4]
By 1959 about 70 species of the Epicoccum genus had been
described, which were evaluated and combined into a single
variable species, the E. nigrum Link.
[5]
However, recently
Fávaro et al.
[6]
developed an analysis based on the poly-
phasic approach, which suggested the occurrence of cryptic
species within E. nigrum and that many of the sequences
deposited as E. nigrum in GenBank and culture collections
of microbial strains should be reclassified, including the ref-
erence strain CBS 161.73.
E. nigrum has been used as a biological control agent
for plant pathogens
[7]
and produces a variety of bioactive
secondary metabolites such as flavipin,
[8]
epicorazins A-B,
[9]
epirodin,
[10]
triornicin,
[11]
orevactaene,
[12]
epicoccamide,
[13]
[a] Chemistry Institute, University of Campinas,
POB 6154, 13084-971, Campinas, SP, Brazil
Fax: +55-19-35213023
E-mail: anita@iqm.unicamp.br
Homepage: http://anita.iqm.unicamp.br/
[b] Brazilian Agricultural Research Corporation, Embrapa
Agroenergia,
Brasília, Distrito Federal, Brazil
[c] Biomedical Sciences Institute, University of São Paulo,
São Paulo, SP, Brazil
Supporting information for this article is available on the
WWW under http://dx.doi.org/10.1002/ejoc.201200757.
Eur. J. Org. Chem. 2012, 5225–5230 © 2012 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim 5225
product with an unusual carbon skeleton. The production of
this secondary metabolite decreased in mutants of Epi-
coccum nigrum transformed by Agrobacterium tumefaciens.
Additionally, these mutants produced 4-hydroxymellein.
epicocconone,
[14]
D8646-2-6,
[15]
and epicoccins A–D,
[16]
among others. However, little is known regarding the genes
related to the synthesis of the metabolites produced by Ep-
icoccum nigrum. Herein we report the isolation and struc-
tural elucidation of secondary metabolites from E. nigrum
wild type P16, and using three E. nigrum agrotransformants
P16–17, P16–47set, and P16–91, we identify genes related
to the synthesis of a new natural compound produced by
E. nigrum P16.
Results and Discussion
The culture broth from E. nigrum fermentation was ex-
tracted with ethyl acetate and subjected to successive frac-
tionations with open silica gel column chromatography.
Further purification of the selected bioactive fractions (an-
timicrobial) afforded a unique natural product, here named
epicolactone (1), as white crystals. Based on HRMS (ESI)
in negative mode, combined with
1
H and
13
C 2D NMR
spectroscopic data, the epicolactone molecular formula is
C
17
H
16
O
8
(10 degrees of unsaturation). Analysis of the
1
H,
13
C{
1
H}, DEPT 135°, and gradient heteronuclear single
quantum coherence (gHSQC) 2D NMR spectroscopic data
of 1 showed the occurrence of three singlets at δ
H
= 6.07,
8.50, and 8.61 ppm with no correlations to carbon atoms,
which are thus assigned to OH, two methyl groups, three
oxymethylenes with diastereotopic hydrogen atoms, one
methane group, and eleven carbon atoms nonbonded to hy-
drogen atoms, three of which resonated at δ
C
= 176.0, 192.8,
and 190.1 ppm, characteristic of carbonyl carbon atoms
(Table 1). The gradient COSY (gCOSY) spectrum con-
firmed the presence of three two-spin systems assigned to
diastereotopic oxymethylene hydrogen atoms. The remain-
ing nine hydrogen atoms showed neither scalar coupling
nor homonuclear
1
H,
1
H correlations. This information