Resistoflavine, cytotoxic compound from a marine actinomycete, Streptomyces chibaensis AUBN1/7

Article (PDF Available)inMicrobiological Research 162(4):322-7 · February 2007with62 Reads
DOI: 10.1016/j.micres.2006.01.012 · Source: PubMed
In our systematic screening programme for marine actinomycetes, a bioactive Streptomycete was isolated from marine sediment samples of Bay of Bengal, India. The taxonomic studies indicated that the isolate belongs to Streptomyces chibaensis and it was designated as S. chibaensis AUBN1/7. The isolate yielded a cytotoxic compound. It was obtained by solvent extraction followed by the chromatographic purification. Based on the spectral data of the pure compound, it was identified as quinone-related antibiotic, resistoflavine (1). It showed a potent cytotoxic activity against cell lines viz. HMO2 (Gastric adenocarcinoma) and HePG2 (Hepatic carcinoma) in vitro and also exhibited weak antibacterial activities against Gram-positive and Gram-negative bacteria.


Microbiological Research 162 (2007) 322327
Resistoflavine, cytotoxic compound from a marine
actinomycete, Streptomyces chibaensis AUBN
Adinarayana Gorajana
, Venkatesan M
, Saisha Vinjamuri,
Bapiraju V.V.S.N. Kurada
, Sujatha Peela
, Premkumar Jangam
Ellaiah Poluri
, Axel Zeeck
School of Pharmacy, International Medical University, Sesama Center, Plaza, Komanwel, Bukit jalil,
57000 Kuala Lumpur, Malaysia
Institut fur Organische Chemie, George-August Universitat, Tammannstrasse 2, D-37077 Gottingen, Germany
Biotechnology Division, Department of Pharmaceutical Sciences, Andhra University, Visakhapatnam 530003, India
Accepted 27 January 2006
In our systematic screening programme for marine actinomycetes, a bioactive
Streptomycete was isolated from marine sediment samples of Bay of Bengal, India.
The taxonomic studies indicated that the isolate belongs to Streptomyces chibaensis
and it was designated as S. chibaensis AUBN
/7. The isolate yielded a cytotoxic
compound. It was obtained by solvent extraction followed by the chromatographic
purification. Based on the spectral data of the pure compound, it was identified
as quinone-related antibiotic, resistoflavine (1). It showed a potent cytotoxic
activity against cell lines viz. HMO2 (Gastric adenocarcinoma) and HePG2 (Hepatic
carcinoma) in vitro and also exhibited weak antibacterial activities against Gram-
positive and Gram-negative bacteria.
& 2006 Elsevier GmbH. All rights reserved.
Marine microorganisms are of considerable cur-
rent interest as a new and promising source of
biologically active compounds. They produce a
variety of metabolites, some of which can be used
for drug development (Pietra, 1997). These micro-
organisms (bacteria and actinomycetes) are vir-
tually unlimited sources of novel compounds with
many therapeutic applications. Actinomycetes,
among them, hold a prominent position due to
their diversity and proven ability to produce
new compounds. Further, the discovery of novel
antibiotic and non-antibiotic lead molecules
through microbial secondary metabolite screening
0944-5013/$ - see front matter & 2006 Elsevier GmbH. All rights reserved.
Corresponding author.
E-mail address: (A. Gorajana).
is becoming increasingly important. However, a
well-defined taxonomic study of actinomycetes is
important to ascertain the correct species that
produces novel secondary metabolites. Actinomy-
cetes are the potent sources of antibiotics, besides
vitamins and enzymes, and such antagonistic
actinomycetes of marine origin are being regularly
reported (Krasil’nikov, 1962; Okami et al., 1976;
Pisano et al., 1986 ; Weyland and Helmke, 1988;
Do et al., 1991; Farooq Biabani et al., 1997;
Pusecker et al., 1997; Romero et al., 1997; Williams
et al., 1999). The present study is aimed for the
isolation of cytotoxic compound, i.e. resistoflavine,
from the strain of S. chibaensis, which was isolated
in the laboratory of Pharmaceutical Sciences,
Andhra University. In this paper, we describe the
taxonomy of the producing strain, fermentation,
isolation, physico-chemical properties, structure
determination, and biological activities of resisto-
Materials and methods
Isolation and maintenance
Strain AUBN
/7 was isolated from a marine
sediment sample colleted at a depth of 30 m at a
distance of 8 km off Machilipatnam coast of Bay of
Bengal. For the isolation, starch casein agar with
the addition of rifampicin (Pisano et al., 1989)
(2.5 mg/ml) and flucanozole (75 mg/ml) was used to
minimize bacterial and fungal contaminations,
respectively. The strain was sub-cultured onto
starch casein agar (Weyland, 1981) slant (medium
with 50% sea water), incubated at 28 1 C for 57
days to achieve good sporulation and was preserved
in 20% glycerol at 80 1C.
Taxonomic characteristics of the isolate were
determined by cultivation on various media as
described by Shirling and Gottlieb (1966), Waksman
(1961) and Arai (1975). Morphological character-
istics were observed after incubation of the culture
at 28 1C for 14 days on Oatmeal agar (ISP med 3).
Cultural characteristics were determined after
growing the culture at 28 1C for 14 days. The
carbon source utilization pattern was determined
as per the ISP protocol (Shirling and Gottlieb,
1966). Cell wall composition was analyzed by the
method of Lechevalier and Lechevalier (1975),
using thin layer chromatography plates as de-
scribed by Staneck and Roberts (1974).
A full grown slant culture of the strain AUBN
on starch casein agar (composition: soluble starch
1.0%, casein 0.03%, KNO
0.2%, NaCl 0.2%, K
0.005%, CaCO
0.002%, FeSO
O 0.001%, and
agar 2.0%) was transferred into Erlenmeyer flasks
(2 250 ml) containing 50 ml of seed medium
(composition: Soyabean meal 1.0%, corn steep
solids 1.0%, glucose 0.5% and CaCO
0.5% with pH
7.0) and incubated for 2 days at 28 1C on a rotary
shaker (220 rpm). A 10% level of this inoculum was
transferred into 200 ml of production medium
contained in 1 l EM flasks (30 in number). The
medium composition is: soyabean meal 1.0%, corn
steep solids 0.5%, soluble starch 1.0%, glucose 0.5%
and calcium carbonate 0.7% with pH 7.0. The
inoculated production flasks were incubated for
56 h at 28 1C on a rotary shaker (220 rpm).
The culture broth (6 l) was centrifuged at
4000 rpm for 10 min, at 10 1C and clear culture
filtrate was separated. It was extracted twice with
ethyl acetate (2 1.2 l) and washed with 500 ml
water at pH 7.0. The mycelium was extracted with
acetone (1.0 l) and then centrifuged (4000 rpm,
10 min, 10 1C). The ethyl acetate phase was
concentrated in vacuum at 35 1C to give 5.0 g of
the crude ethyl acetate extract, while the acetone
extract was concentrated in vacuum and kept for
lyophilization to obtain 4.5 g of mycelium extract.
The mycelium extract (4.5 g) was chromato-
graphed on silica gel column (22 5 cm) and eluted
with dichloromethane/methanol (95:5, 1 l) to give
eight major fractions (Fr IVIII). Finally, the silica
gel column was washed with methanol (500 ml) to
obtain two more major fractions IX and X (Fig. 1).
The dried residues of all 10 major fractions were
dissolved, each in a specified volume of dichlor-
omethane to give 1 mg/ml concentration and
tested for their antimicrobial activities using
Bacillus subtilis as test organism by disc-plate
method. Among 10 fractions, fraction No. VII
exhibited good activity, fractions No. III, IV, V, VI
and IX showed moderate activities and fraction I, II,
VIII and X did not exhibit any activity. The active
fraction VII (41.8 mg) was purified by chromatogra-
phy on Sephadex LH20 (methanol) to obtain
fractions VII a, VII b, VII c, VII d, VII e and VII f.
The fraction VII d was found to possess good
antimicrobial activity while others hav e no or
negligible activities. The active fraction VII d was
further purified by chromatography on Sephadex
Resistoflavine, cytotoxic compound from a Streptomyces chibaensis 323
LH20 (acetone) which resulted in two distinct
fractions VII d.I (4.9 mg) and VII d.II (6.3 mg).
Fraction VII d.II had good antimicrobial activity
(100 mg/ml) but negligible activity was observed
with VIId.I. The fraction VII d. II was found to be
pure and was pale yellow in color. Regarding the
extra cellular metabolite of the isolate, polymer
was obtained which does not possess any antimi-
crobial activity.
Instrumental analysis
Melting points were determined on a Fisher–-
Johns apparatus. NMR experiments were performed
on Bruker DRX-500 (500 MHz) and Bruker AMX 300
(300 MHz). The chemical shifts were expressed in d
(ppm) using CDCl
as solvent and TMS as internal
reference. The MS spectra were measured on
Varian MAT 731 and Finnigan MAT 311 A. UV spectra
were recorded on a Kontron Uvikon 860. IR
spectrum was measured on a Perkin Elmen Model
298 (KBr discs). TLC was carried out on silica gel 60
plates (Merck, 0.25 mm) and Column chroma-
tography on silica gel (Macherey & Nagel,
o0.08 mm) or Sephadex LH-20 (Pharmacia). R
values were determined on 20 20 cm plates, the
evaluation length being 10 cm. Compounds were
viewed under UV lamp at 254 nm and sprayed with
followed by heating.
Cytotoxic activity
The cytotoxicities of 1 were assessed based on
their effects on the growth of tumor cells in vitro
according to the NCI guide lines (Grever et al.,
1992).The cell lines used were HMO2 (gastric
adenocarcinoma) and HePG2 (hepatic carcinoma).
Cells were grown in 96-well microtitre plates of
RPMI 1640 tissue culture medium supplemented
with 10% fetal calf serum at 37 1C in a humified
atmosphere of 50% CO
in air. After 24 h of
incubation 1 (0.110.0 mg/ml) was added to the
cells. After 48 h incubation, the cells were fixed by
addition of trichloracetic acid and cell protein was
assayed with sulforhodamineB (Skehan et al.,
1990). For each concentration tested, the GI
(drug concentration causing 50% growth inhibition),
TGI values (drug concentration causing 100% growth
inhibition) and LC
(minimum concentration which
reduces the initial cell number to half were
determined; Table 3).
Antimicrobial activity
The minimum inhibitory concentrations (MIC) of
the purified antibiotic (1) against different test
organisms were determined by the broth dilution
Compound I
Sephadex LH 20
Sephadex LH 20
: MeOH
Silica gel
Culture filtrate extract
ethyl acetate
Mycelium extract
Culture filtrate
Mycelium cake
Culture Broth
Figure 1. Scheme for the isolation of pure fractions.
A. Gorajana et al.324
The sporophores occurred as short closed spirals
with 24 turns, arranged in groups and formed
spiral spore chains which belong to section Spira
(S). The cultural characteristics of the strain are
summarized in Table 1. Color of aerial mycelium
was medium gray and color of reverse side was
brown. Diffusible pigments were not formed. It
utilized glucose,
L-arabinose, sucrose, xylose,
inositol, mannitol and fructose. The analysis of cell
wall hydrolysates showed the presence
pimelic acid and glycine without any characteristic
sugar pattern. Taxonomic studies indicated that it
belongs to the Streptomyces genus. A detailed
survey of literature revealed that it is closely
related to Streptomyces chibaensis.
The physico-chemical properties of resistoflavine
(1) are summarized in Table 2. The molecular
formula was determined as C
on the basis of
the EI-MS (70 eV), which gave a ([M
], 100) ion at
m/z 392.0.
] DMSO, 200 MHz): d ¼ 13.33 (br. s, 1H,
chel.OH), 12.62 (br. s, 1H, chel.OH), 12.37 (br. s, 1H,
1.61 (s, 3H, 13-CH
) 1.54 (s, 3H, 12-CH
]DMSO,75.5MHz):d ¼ 203.6 (Cq, C-2,
CQO), 189.3 (Cq, C-6, CQO), 183.7 (Cq, C-10,
CQO), 168.4 (2Cq, C-7, C-5), 164.0 (Cq, C-3), 156.6
(Cq, C-11a), 150.1 (Cq, C-9), 149.5 (Cq, C-11c), 148.4
(Cq, C-11d), 127.7 (CH, C-11), 121.2 (CH, C-8), 120.6
(Cq, C-9a), 111.6 (Cq, C-6a), 108.5 (Cq, C-5a), 107.6
(Cq, C-2a), 104.1 (CH, C-4), 61.9 (Cq, C-11b), 46.6
(Cq, C-1), 31.1 (CH
, C-12), 24.4 (CH
,C-13), 23.5
A cytotoxic compound of producing isolate
/7 from marine sediment of Bay of Bengal
Ocean has been characterized and identified as
Table 1. Cultural characteristics of strain AUBN
Medium Growth Aerial mycelium Substrate mycelium Diffusible pigment
Yeast extractmalt extract agar (ISP2) Good Gray Yellow brown None
Oatmeal agar (ISP3) Poor Gray Yellowish brown None
Inorganic saltsstarch agar (ISP4) Good Grayish white Brown None
Glycerol asparagine agar (ISP5) Good Reddish gray Reddish brown None
Tyrosine agar ((ISP7) Poor Light gray Brownish gray None
Table 2. Physico-chemical properties of resistoflavine (1)
State Pale yellow colored powder (solid)
Molecular formula C
Melting point (MP) 239.0 1C
Soluble in Dichloromethane, methanol
Insoluble in n-Hexane, H
EI-MS 392.0[M
], 100
(Mol.Ellip.) 214.2 (+155744), 226.2 (7089), 243.8 (+30995), 262.6 (8468), 273.6
(1064), 322.2 (19029), 395.0 (+7923) nm
(KBr) 3440,1604,1648,1667,1569,1376 and 1284 cm
Silicagel TLC (Merck, 0.25 mm); (CHCl
: MeOH ¼ 9:1).
Figure 2. Structure of resistoflavine (1).
Resistoflavine, cytotoxic compound from a Streptomyces chibaensis 325
S. chibaensis. The results indicated that the
spectrum of compound showed a broad singlets at
d ¼ 13:33, 12.62 and 12.37 with intensities of 1
proton each. These indicate the presence of 3
chelated hydroxyl groups in the molecule. In the
aromatic region three singlets at d ¼ 7:00, 6.55 and
6.49 with relative intensity of one proton each
were observed. This indicates the presence of
three differen t protons. A broad singlet of one
proton intensity appeared at d ¼ 7:26, this indi-
cates the presen ce of hydroxyl group attached
to alicyclic compound. The chemical shift of the
signal at d ¼ 2:69 indicated for the pre sence of
methyl group either on an aromatic ring or on
heteroatom. The singlet of three proton intensity
peak at d ¼ 1:61 and another singlet of intensity
three protons at d ¼ 1:54, indicated the presence
of two methyl groups in aliphatic or cyclic environ-
C-NMR spectrum exhibited three signals at
d ¼ 203 : 6, 189.3 and 183.7 and these peaks
indicated the presence of three carbonyl groups.
In addition to this 15 signals are in the aromatic
region and three signals in the aliphatic region
were observed. The above spectral data suggest
the following structure for the resistoflavine.
The spectral information of the 1 was searched in
different databases like Chapman and Hall, SciFin-
der, Beilstein and Antibase and no hints were
observed in any of the databases (Dictionary of
Natural Products on CD-ROM, 2002). This indicated
that resistoflavine (1,AUBN
/7,VI1 d.I1,3,5,7,11b-
Tetrahydroxy-1,1,9-trimethyl-2H-benzo [cd] pyren-,
6,10-(1H,11bH)-trion) is a known compound which
was earlier reported from terrestrial actinos (Eck-
ardt et al., 1970a, b, 1972; Haupt and Eckardt,
1972; Hofle and Wolf, 1983) but not reported so far
from marine sources (Fig. 2). Resistoflavine is a
cytotoxic compound (Table 3) with a weak anti-
bacterial activity (Table 4).
The authors gratefully acknowledge Andhra Uni-
versity and University of Gottingen for providing
necessary infrastructural facilities for carrying out
the work.
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Compound Cell line HMO2 Cell line HePG2
I 0.007 0.009 0.013 0.010 0.013 0.016
All the concentrations are in mg/ml; GI
¼ Concentration which produces half of the maximum cell growth inhibition;
TGI ¼ Concentration which produces complete growth inhibition; LC
¼ Minimum concentration which reduces the initial cell
number to half (24 h growth).
Table 4. Antimicrobial activities of resistoflavine (1)
Test organism MIC (mg/ml)
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B. pumilus (ATCC 19164) 464
S. aureus (ATCC 29213) 432
E. coli (ATCC 26) 128
P. aeruginosa (ATCC 27853) 4128
P. vulgaris (ATCC 6897) 464
A. Gorajana et al.326
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Resistoflavine, cytotoxic compound from a Streptomyces chibaensis 327
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