ORIGINAL ARTICLE/ARTICLE ORIGINAL

Antimicrobial activity from the extracts of fungal

isolates of soil and dung samples from Kaziranga
National Park, Assam, India
Activite antimicrobienne dextraits disolats fongiques du sol et du
fumier du parc national de Kaziranga, Assam, Inde
C. Ganesh Kumar, P. Mongolla, J. Joseph, Y.V.D. Nageswar, A. Kamal
*
Chemical Biology Laboratory, Division of Organic Chemistry, Indian Institute of Chemical Technology, Hyderabad 500607, India
Received 18 June 2010; received in revised form 13 August 2010; accepted 20 August 2010
Available online 23 October 2010
KEYWORDS
Antimicrobial activity;
Fungi;
Kaziranga National Park;
Secondary metabolites
Summary One hundred and thirty fungal strains were isolated from soil and dung samples
collected from the biodiversity hotspot, the Kaziranga National Park, Assam, India. These were
then characterized by conventional methods and assessed for their antimicrobial activity against
test microorganisms. From the 130 isolates, 42 organisms showed antimicrobial activity; 15 of
them were exclusively anti-bacterial and 20 isolates showed both antibacterial and anti-Candida
activity and seven isolates showed exclusive anti-Candida activity. The inhibition was higher
against Gram-positive bacteria, while Gram-negative bacteria were less inhibited. The potent
antibiotic producing strains isolated belong mainly to the genera Aspergillus, followed by
Scopulariopsis, Curvularia, Phoma, Lasiodiplodia theobromae, Fusarium, Acremonium and
Aureobasidium pullulans. This is the rst report on the antimicrobial activity of fungal isolates
from the Kaziranga National Park biosphere of India.
# 2010 Elsevier Masson SAS. All rights reserved.
Activit
antimicrobienne;
Fungi;
Parc national de
Kaziranga;
Mtabolites secondaires
Rsum Cent trente souches fongiques ont t isoles dans des chantillons de sol et de
fumier au point nvralgique de biodiversit du parc national de Kaziranga, Assam, Inde. Elles ont
t alors caractrises par des mthodes conventionnelles et values pour leur activit
antimicrobienne contre des microorganismes tests. partir des 130 isolats, 42 montrent une
activit antimicrobienne, 15 sont exclusivement antibactriens, 20 sont antibactriens et
antifongiques et sept sont exclusivement antifongiques. Linhibition est la plus forte contre
les bactries Gram positives, alors que des bactries Gram ngatives moins sont moins sensibles.
Les espces produisant des mtabolites antimicrobiens appartiennent principalement aux
genres Aspergillus, Scopulariopsis, Curvularia, Phoma, Lasiodiplodia theobromae, Fusarium,
Journal de Mycologie Mdicale (2010) 20, 283289
* Corresponding author.
E-mail address: ahmedkamal@iict.res.in (A. Kamal).
1156-5233/$ see front matter # 2010 Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.mycmed.2010.08.002
Acremoniumet Aureobasidiumpullulans. Cest le premier rapport sur lactivit antimicrobienne
des isolats fongiques de la biosphre du parc national de Kaziranga (Inde).
# 2010 Elsevier Masson SAS. Tous droits rservs.
Introduction
Microbial metabolites are rich sources for new potential
therapeutic drugs [22]. Over 5000 antibiotics have been
identied from the cultures of Gram-positive, Gram-nega-
tive and lamentous fungi; but only about hundred antibio-
tics alone have been used commercially to treat the human,
animal and plant diseases [2]. Industrial antibiotic produc-
tion mainly focuses on screening programmes for identica-
tion of new potent antibiotic producing organisms either
from natural sources or from established cultures [4]. Selec-
tive procedures which allow detection and isolation of only
those microorganisms of interest from a large population
were developed for screening [9]. The need for less toxic,
more potent antibiotics from non-infective organisms, which
overcome the resistance exhibited against the existing anti-
biotics are some of the challenges to the evolving therapeu-
tics against microbial infections.
Soil, in particular, is an extensively explored ecological
niche for microorganisms that produce useful biologically
active natural products including antibiotics [34]. Majority of
antibiotics so far isolated were produced by Streptomycetes
and fungi, which are common inhabitants of the soil [15].
Modern researchers emphasize on the need to explore novel
unexplored niches like rain forests [28], marine sponges [12],
mangroves [16] and endophytes [25,29] for pharmacologi-
cally active compounds. The expanding list of novel micro-
organisms and the products derived from poorly explored
areas of the world like Australia [19], Jordan [21] and
Antarctica [18] suggests that a careful exploration of new
habitats might continue to be useful. The biopharmaceutical
industry has become increasingly interested in novel anti-
biotics to meet the challenge of resistance. By employing
strategic screening programmes of microbes, it is feasible to
increase the number of potential products for therapeutic
use [13,27]. In the present paper, we present the report on
fungal isolates showing antimicrobial activity from the
hitherto unexplored soil and dung samples collected from
the Kaziranga National Park, declared as one of the World
Heritage site by UNESCO in 1985. The park is a unique natural
landscape of sheer forest, tall elephant grass, rugged reeds,
marshes and shallow pools [31].
Materials and methods
Target strains
The target strains used for screening antimicrobial activity
were procured frommicrobial type culture collection (MTCC)
and Gene Bank of the Institute of microbial technology,
Chandigarh, India and are: Micrococcus luteus MTCC 2470,
Staphylococcus aureus MTCC 96, S. aureus MLS16 MTCC 2940,
Bacillus subtilis MTCC 121, Escherichia coli MTCC 739, Pseu-
domonas aeruginosa MTCC 2453, Klebsiella planticola MTCC
530 and Candida albicans MTCC 3017.
Collection of soil and dung samples
Soil samples and dung samples of elephant, tiger and one-
horned rhinoceros were obtained from different locations
of Kaziranga National Park, Assam, India. From each of
these locations, soil samples were collected from 10
15 cm below the surface in small prelabelled sterile plastic
containers, which were tightly sealed and transported to
the laboratory.
Isolation, growth conditions and storage
One gram of each of these soil and dung samples was
suspended in 100 ml sterile water and vortexed on a
shaker. Dilutions of the suspensions (1:10 and 1:100) were
prepared and 1 ml of these dilutions was used for sam-
pling. Each sample was cultivated on two different sterile
media in Petri dishes containing 1518 ml of potato dex-
trose agar (PDA) or Rose Bengal Chloramphenicol agar
(HiMedia Laboratories Pvt. Ltd, Mumbai, India). The petri
dishes were incubated at 28 8C for 45 days until fungal
growth of the colonies was fully formed. Use of antibiotics
for PDA medium was avoided as some fungal species was
found to be sensitive to antibiotics. The fungi were pur-
ied by repeated sub-culturing to get axenic cultures,
which were maintained on PDA slants. Fungal stocks of
the puried cultures were prepared in the same medium as
above and overlaid with mineral oil and stored at 4 8C in
the culture collection of the laboratory for further iden-
tication and screening for antimicrobial activity. The
isolates were identied up to the level of the genus based
on cultural and morphological characteristics of spore and
hyphae under lactophenol staining and deposited in the
laboratory culture collection.
Growth and production of antimicrobial activity
The spore suspension fromdifferent fungal isolates (96 h old)
was prepared and inoculated in 50 ml of potato dextrose
broth in 250 ml Erlenmeyer ask and incubated at 28 8C for 5
days. After incubation, the culture broth was ltered through
lter paper (Whatman No. 3) to remove the fungal cell mass
and the cell-free supernatant was stored in vials at 4 8C until
further use. The resulting ltrates were used to evaluate
antimicrobial activity.
Screening of antibiotic activity by agar well
diffusion method
Antibacterial activity was assayed in duplicate by agar well
diffusion method. Wells of 5 mm diameter were punched
in nutrient agar plates seeded with test bacterial organ-
isms, which corresponded to a 0.5 McFarland turbidity
standard solution. Yeast extract, peptone and dextrose
(YEPD) medium instead of nutrient agar was used for
284 C. Ganesh Kumar et al.
Candida. Plates were incubated for 96 h at optimal tem-
perature for the test organism. The inhibition zones
around the disks were measured. Crude cell free super-
natant (20 ml) of overnight fungal culture of 1618 h
growth was added in each well. Plates were then incu-
bated overnight at 37 8C for 24 h. The inhibitory activity
was detected as a zone of clearing in the turbid medium
around the wells containing antibacterial activity (positive
samples). The diameter of the clearing zones in (mm)
formed a semi-quantitative method of determination of
the inhibition effect at specic concentration of the anti-
bacterial compound.
Results
A total of 38 samples were collected in and around Kaziranga
National Park which included 23 forest soil samples, nine
dung samples (three each of elephant, tiger and one-horned
rhinoceros), four rhizosphere soil samples and one sample
each from termite hills and tree bark (epiphytes). After
processing these samples in our laboratory, 130 fungi were
isolated as pure cultures on PDA plates. Extracts from all
these isolates were tested for antimicrobial activities by
well diffusion method and 42 of them showed positive
Table 1 Identication of the fungal isolates from Kaziranga National Park exhibiting antimicrobial activity.
Identication des isolats fongiques du parc national de Kaziranga montrant une activite antimicrobienne.
S. No. Isolate No.
*
Sample source Identication
1 KZR 001 Forest soil Aspergillus sp.
2 KZR 002 Forest soil Scopulariopsis sp.
3 KZR 003 Forest soil (Munna beel) Aspergillus versicolor
4 KZR 005 Pennisetum sp. rhizosphere soil Aspergillus versicolor
5 KZR 006 Forest soil Aureobasidium pullulans
6 KZR 007 Forest soil Aspergillus sp.
7 KZR 008 Forest soil Aspergillus avus
8 KZR 009 Forest soil Curvularia sp.
9 KZR 028 Forest soil Aspergillus sp.
10 KZR 047 Elephant dung Lasiodiplodia theobromae
11 KZR 048 Anthurium sp. rhizosphere soil Aspergillus avus
12 KZR 049 Rhino dung Aspergillus avus
13 KZR 053 Anthurium sp. rhizosphere soil Scopulariopsis spp
14 KZR 054 Elephant dung Aspergillus avus
15 KZR 059 Elephant dung Curvularia sp.
16 KZR 061 Forest soil Aspergillus niger
17 KZR 063 Elephant dung Aspergillus niger
18 KZR 065 Elephant dung Aspergillus avus
19 KZR 069 Anthurium sp. rhizosphere soil Fusarium sp.
20 KZR 070 Forest soil Aspergillus terreus
21 KZR 071 Elephant dung Aspergillus niger
22 KZR 079 Elephant dung Aspergillus avus
23 KZR 080 Forest soil Aspergillus avus
24 KZR 084 Anthurium sp. rhizosphere soil Aspergillus fumigatus
25 KZR 085 Forest soil Aspergillus nidulans
26 KZR 087 Forest soil Phoma sp.
27 KZR 088 Crispa sp. rhizosphere soil Aspergillus avus
28 KZR 090 Rhino dung Aspergillus avus
29 KZR 091 Rhino dung Aspergillus fumigatus
30 KZR 095 Forest soil Aspergillus niger
31 KZR 100 Termite hill Acremonium spp
32 KZR 101 Crispa sp. rhizosphere soil Aspergillus niger
33 KZR 110 Termite hill Phoma sp.
34 KZR 117 Elephant dung Aspergillus niger
35 KZR 118 Forest soil Aspergillus niger
36 KZR 121 Elephant dung Aspergillus versicolor
37 KZR 124 Rhino dung Aspergillus avus
38 KZR 125 Elephant dung Aspergillus avus
39 KZR 126 Elephant dung Aspergillus versicolor
40 KZR 127 Tiger dung Aspergillus fumigatus
41 KZR 129 Tree bark scrapings Aspergillus fumigatus
42 KZR 130 Termite hill Aspergillus avus
*KZR Kaziranga.
Antimicrobial activity from the extracts of fungal isolates of soil 285
Table 2 Antimicrobial activity of fungal isolates from Kaziranga National Park against pathogen test strains.
Activite antimicrobienne des isolats fongiques du parc national de Kaziranga contre des souches tests pathoge `nes.
S. No Isolate No. Micrococcus
luteus
MTCC 2470
Escherichia
coli MTCC 739
Pseudomonas
aeruginosa
MTCC 2453
Staphylococcus
aureus MLS-16
MTCC 2940
Staphylococcus
aureus MTCC 96
Bacillus
subtilis
MTCC 121
Klebsiella
planticola
MTCC 530
Candida
albicans
MTCC 3017
1 KZR 001 +++
2 KZR 002 ++ ++ ++
3 KZR 003 ++ ++ +++
4 KZR 005 ++ +++
5 KZR 006 +++
6 KZR 007 ++ +++
7 KZR 008 ++ +++
8 KZR 009 + ++ +++
9 KZR 028 +++ ++ ++ +++ +++ +
10 KZR 047 ++
11 KZR 048 ++ ++
12 KZR 049 ++
13 KZR 053 ++ ++
14 KZR 054 ++ ++ ++
15 KZR 059 ++ ++
16 KZR 061 ++ +++ +++
17 KZR 063 ++ ++ ++ ++ ++
18 KZR 065 ++ ++ ++
19 KZR 069 ++ ++ ++ + ++
20 KZR 070 ++ ++ ++ ++ ++
21 KZR 071 ++ ++ ++ ++ ++ ++
22 KZR 079 ++ ++
23 KZR 080 ++ ++ +
24 KZR 084 ++ +
25 KZR 085 +
26 KZR 087 +
27 KZR 088 + ++
28 KZR 090 ++ +
29 KZR 091 ++ ++
30 KZR 095 ++ ++ ++ ++ ++ ++ ++
31 KZR 100 ++
32 KZR 101 +
33 KZR 110 ++ ++ ++ ++ ++
34 KZR 117 ++ ++ ++ ++
35 KZR 118 ++ ++ ++
36 KZR 121 ++ ++ ++
2
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antimicrobial activity. The details of the positive isolates
including their source and culture characteristics along with
their identication are described in Table 1. The identica-
tion of the potent antibiotic producing strains reveals that
most of them belong to the genus Aspergillus (32 isolates)
followed by Scopulariopsis (two isolates), Curvularia (two
isolates), Phoma (two isolates) and one each of Lasiodiplodia
theobromae, Fusarium, Acremonium and Aureobasidium
pullulans. Among the 42 isolates, 15 isolates showed only
antibacterial activity, 20 isolates showed both antibacterial
and anti-Candida activities, but seven were exclusive for
anti-Candida in their activity (Table 2). While maximum
isolates showed activity against C. albicans and S. aureus
MLS16, only two isolates showed activity against E. coli.
Discussion
Microorganisms had been the source of most important
medicines ever developed; some of the key antibiotics from
microorganisms developed as drugs include penicillin [8],
streptomycin [23], chloramphenicol [6], erythromycin [17],
gentamicin [35,14], rapamycin [33], etc. Some of these
drugs, for example, rapamycin produced by Streptomyces
hygroscopicus, were later developed as potent immunosup-
pressant [11] and anticancer [3] agents. The increasing
number of cases of resistance and the growing demand for
new lead structures in pharmacology necessitated the need
to search for novel metabolites in developing them as med-
icines against new targets or as new compounds against the
established targets. Discovery of bioactives mainly depends
on the knowledge of habitats where the fungi are abundant
and the strength of culture collections [13]. Microorganisms
isolated from hitherto unexplored areas and/or from
extreme environments is the obvious choice for development
of potential novel bioactive metabolites [7,20]. The high
proportion of strains producing antimicrobials from such
environments may be associated with defensive or aggressive
roles of the organisms for maintaining their ecological niche
in such environments. Further, the thriving of fungi in such
competitive environments is assumed that their metabolic
compatibility is strongly inuenced by natural selection [10].
In connection with our ongoing screening activities for
biological active secondary metabolites from fungi, the
present study was undertaken to screen for novel microbes
and for selecting strains with antibacterial and anti-Candida
activities from hitherto unexplored areas of Kaziranga
National Park, Assam, India, which has soils very rich in
moisture content and provide excellent conditions for fungal
growth. The results of the screening revealed that a total of
42 from 130 isolates exhibited antimicrobial activity with 15
as antibacterials, 20 with antibacterial and anti-Candida
activity and seven with exclusive activity against the Candida
albicans. Thirteen of the isolates producing antibacterials
were active against Gram-positive bacteria (B. subtilis and S.
aureus); only two of the isolates were active against Gram-
negative bacteria. The reason for differential sensitivity
between Gram-positive and Gram-negative bacteria could
be ascribed to the morphological differences between these
microorganisms; Gram-negative bacteria have an outer poly-
saccharide membrane carrying the structural lipopolysac-
charide components. This makes the cell wall impermeable
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Antimicrobial activity from the extracts of fungal isolates of soil 287
to lipophilic compounds; the Gram-positive bacteria, on the
other hand, will be more susceptible as they have only an
outer peptidoglycan layer which is not an effective perme-
ability barrier [24].
In our study, among the 42 short-listed isolates (Tables 1
and 2) exhibiting antimicrobial activity, the culture ltrates
of about 32 isolates belonging to the genus Aspergillus and
one Fusarium isolate (KZR 069) showed a wide spectrum of
antimicrobial activity, which supports the observations that
fungal genera like Acremonium, Aspergilllus, Fusarium and
Penicillium are considered as creative species based on
their ability to produce several bioactive metabolites [5].
Similarly, several secondary metabolites from a marine iso-
late, Aspergilllus niger exhibited diverse antibacterial and
antifungal potential [1]. In our study, we observed two
species of Curvularia (KZR 009 and KZR 059) and one Aur-
eobasidium pullulans (KZR 006) showed antimicrobial activ-
ity. Similarly, in some earlier studies, 4-epiradicinol
produced by Curvularia lunata [32], aureobasidins produced
by Aureobasidium pullulans [30] and botryodiplodin pro-
duced by Lasiodiplodia theobromae (the synonym of Botryo-
diplodia theobromae) [26] are reported to exhibit
antimicrobial activity. To the best of our knowledge there
are no reports on Scopulariopsis and Phoma exhibiting anti-
microbial activity. Our investigation suggests that bioactive
fungal constituents are possibly a rich source of novel meta-
bolites with antimicrobial activity. The broad-spectrum
activity exhibited by some of the isolates is possibly due
to the production of diverse antimicrobial compounds, which
may represent a potential for pharmaceutical and/or agri-
cultural applications. Further investigations on purication
and structure elucidation of the compounds are in progress.
To the best of our knowledge this is a rst study on the
antimicrobial activity of fungal isolates from Kaziranga
National Park biosphere of India.
Conict of Interest
None.
Acknowledgements
The authors are thankful to Dr. T.C. Bora, Scientist, NEIST,
Jorhat and Mr. Dharnidhar Boro, Forest Range Ofcer, Kazir-
anga National Park, for their help and providing the necessary
logistics during the expedition of sample collection in Kazir-
anga National Park, Assam, India. The authors are also thank-
ful to Prof. V. Lakshmipati for his kind help in providing
editing, and valuable comments during the preparation of
the manuscript. The nancial support extended by Council
of Scientic and Industrial Research (CSIR), New Delhi,
Government of India in the form of a Network Project on
Exploitation of Microbial Wealth of India is gratefully
acknowledged.
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