Sharma et al

Tropical Journal of Pharmaceutical Research December 2011; 10 (6): 801-808

© Pharmacotherapy Group,
Faculty of Pharmacy, University of Benin,
Benin City, 300001 Nigeria.
.
All rights reserved

Available online at http://www.tjpr.org

http://dx.doi.org/10.4314/tjpr.v10i6.14

Research Article

Antimicrobial Activity of Actinomycetes Against

Multidrug Resistant Staphylococcus aureus, E. coli
and Various Other Pathogens
Deepika Sharma, Talwinder Kaur, BS Chadha and Rajesh Kumari Manhas*
Department of Microbiology, Guru Nanak Dev University, Amritsar 143005, India

Abstract

Purpose: The rapid emergence of drug resistance among pathogenic bacteria, especially multidrug-
resistant bacteria, underlines the need to look for new antibiotics.
Methods: In the present study, 134 different actinomycetes, isolated from the soil samples collected
from different localities of Punjab and Himachal Pradesh, were screened for antimicrobial activity
against various test organisms including multidrug-resistant methicillin-resistant Staphylococcus aureus
(MRSA) and Escherichia coli in order to identify potential antibiotic producers.
Results: Among these isolates, 51 (38 %) showed antimicrobial activity against one or more test
organisms and six exhibited promising broad-spectrum activity against all the tested organisms. The
observed cultural, morphological, physiological and biochemical characteristics confirmed that these
isolates are species of the genus, Streptomyces.
Conclusion: Further studies on the bioactive metabolites from these cultures will be useful for
discovering novel compounds of clinical and agricultural use.

Keywords: Actinomycetes, Broad spectrum antibiotics, Multidrug-resistant Staphylococcus aureus,

Streptomyces.

Received: 5 March 2011 Revised accepted: 22 November, 2011

*Corresponding author: Email: [email protected]; Tel: +91-183-2258802-09 Ext 3450; Fax: +91-183-
2258819-20.

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 Sharma et al

INTRODUCTION broad-spectrum antibiotic-producing action-

mycetes.
Since man started suffering from diseases
caused by infectious microorganisms, the
EXPERIMENTAL
quest for their remedies started and led to the
discovery of a large number of antibiotics
Isolation of actinomycetes
from microorganisms including actinomy-
cetes. Microorganisms have made an
The soil samples from different localities of
outstanding contribution to the health and
Punjab and Himachal Pradesh (India) were
well-being of people throughout the world [1].
collected in sterile polyethylene bags, sealed
Actinomycetes are filamentous gram-positive
tightly and stored in a refrigerator. Soil
bacteria with high G + C content and are the
samples were given three different
most widely distributed group of micro-
pretreatments: dry heat (heating at 100 ºC for
organisms in nature which primarily inhabit
1 h), wet heat (heating at 70 ºC in a water
the soil [2-3]. Among actinomycetes, the
bath for 15 min) and 1.5 % phenol treatment.
genus Streptomyces has long been
Each pretreated soil sample was serially
recognized as a rich source of useful -6
diluted to 10 – fold and then 0.1 ml aliquot
secondary metabolites and continues to be a
from each dilution was spread on starch-
major source of new bioactive molecules [4-
casein medium containing (g/l): starch 10.0,
6]. They are the origin of a good number of
casein 0.3, KNO3 2.0, NaCl 2.0, K2HPO4 2.0,
marketed antibiotics [7].
MgSO4.7H2O 0.05, CaCO3 0.02, FeSO4.7H2O
0.01 and agar 18.0, which was supplemented
However, rapid emergence of antimicrobial
with cycloheximide (50 µg/ml) and nystatin
resistance among pathogenic micro-
(25 µg/ml, HiMedia). The plates were
organisms has led to a renewed search for
incubated at 28 ºC for 28 days. The colonies
new antimicrobial agents from Streptomyces.
of actinomycetes were recognized according
Severe infections caused by bacteria that are
to their rough and chalky macroscopic
resistant to commonly used antibiotics have
characteristics, and were then purified,
become a major global healthcare problem in
st transferred to starch casein nitrate agar
the 21 century [8]. The most resistant
slants (without any antifungal and
bacteria causing important community-
antibacterial) and preserved at 4 °C. The
acquired infections include methicillin-
isolates were maintained as spore
resistant Staphylococcus aureus (MRSA),
suspensions and mycelia fragments in 20
vancomycin-resistant Staphyloco-ccus
%v/v glycerol at -70 ºC in an ultra-low
aureus (VRSA), vancomycin-resistant
temperature freezer.
Enterococcus (VRE), extended spectrum β-
lactamase (ESBL) producing bacteria such
Test organisms
as E. coli and Klebsiella spp and multiple
drug resistant Mycobacterium tuberculosis
Various test organisms used in this study
(MDR-MTB). Therefore, it is imperative to
include: Bacillus megaterium (MTCC 428),
search for new, efficacious and safe
Bacillus subtilis (MTCC 619), Enterobacter
antibiotics from natural sources to combat the
aerogenes (MTCC 111), Escherichia coli
menace of drug-resistant infections.
(MTCC 1885), Klebsiella pneumoniae sub sp.
pneumoniae (MTCC 109), Proteus mirabilis
In view of the foregoing, the objective of the
(MTCC 1429), Salmonella typhi (MTCC 733),
present investigation was to screen soil
Candida albicans (MTCC 3017), Rhodotorula
samples collected from different localities of
rubra (MTCC 248); clinical isolates (provided
Punjab and Himachal Pradesh, which are
by Postgraduate Institute of Medical
large, diverse and largely unscreened
Sciences, Chandigarh, India) Enterococcus
ecosystems, for the isolation of potent and
sp., two multidrug resistant E. coli strains

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 Sharma et al

(S1-LF and R65-LF, both resistant to temperature and zone of inhibition was
cephotaxime, ciprofloxacin, rifampicin, recorded.
clindamycin and cefoperzone; R65-LF is also
resistant to trimethoprim) and three Extraction of antibiotic
methicillin-resistant Staphylococcus aureus
strains (MRSA P-169, MRSA C-67 and For the isolation of antimicrobial compound,
MRSA C-97, which are also resistant to five days old culture broths were extracted
erythromycin, cefepime, gentamicin, co- twice with six different solvents of a wide
trimoxazole, netilimycin, amikacin and range of polarity, namely, n-butanol,
imipenem). chloroform, diethyl ether, ethyl acetate,
hexane: methanol (20:50) and hexane. The
Antimicrobial screening and selection of solvent extracts were concentrated to
isolates dryness using rotavapour and tested for their
antimicrobial activity against various test
Primary screening was carried out using the organisms.
modified method of Kirby Bauer antibiotic
susceptibility test [9]. Antibiotic activity was Characterization of selected isolates
determined on Mueller Hinton agar and Yeast using polyphasic approaches Morpholo-
malt agar media (Hi-Media) inoculated with gical, cultural, physiological and bioche-
bacteria and yeasts, respectively. The mical characterization
actinomycetes isolates were lawn-cultured by
dense streaking on starch casein nitrate The six selected isolates (2A, A26, A27, A13,
medium plates and incubated at 30 ºC for N23 and R3YS which showed promising
seven days. Six mm agar discs were broad spectrum activity) were characterized
prepared using sterile cork borer from well- morphologically and physiologically according
grown culture and placed on fresh lawn to International Streptomyces Project [10-11].
culture of test organisms. The plates were The morphological characteristics were
then kept at 4 ºC for 30 min for the diffusion examined by culturing isolates on different
of the culture broth, and then incubated at ISP media (ISP-2, ISP-3, ISP-4, ISP-5, ISP-
their respective optimum temperature (37 ºC 7) and Bennett’s agar. The plates were
for bacteria and 25 ºC for the yeasts). The incubated at 28 ºC for one week.
zones of inhibition for bacteria were
Physiological tests - growth at various
determined after 18 - 24 h and for yeasts
temperatures (20 – 37 ºC) and NaCl
after 2 -3 days.
concentrations (2 - 10 %) were examined by
Isolates which showed broad spectrum growing the strains on starch casein nitrate
activity against test organisms in primary (SCN) agar medium. Starch hydrolysis was
screening were subjected to secondary investigated after 7 days on starch casein
screening by Kirby Bauer agar well diffusion nitrate agar by flooding the plates with a 1
method. Erlenmeyer flasks (250 ml)
%w/v iodine solution [12]. To check esculin
containing 50 ml of starch casein nitrate broth hydrolysis, isolates were grown on esculin
were inoculated with 7 days old culture and hydrolysis medium for 7 days and observed
incubated at 28 °C for 5 days at 180 rpm. The for appearance of dark brown to black
culture broth was centrifuged and the activity coloration [12]. Gelatin hydrolysis was tested
of the supernatant was determined against after growing isolates for 7 days on gelatin
test organisms by adding 50 µl to wells containing medium. To examine for
(6mm) bored into freshly inoculated plates. hydrolysis, culture tubes were chilled in ice
The plates were then kept at 4 °C for 30 min water and checked for solidification.
for diffusion of the antibiotic, they were then Hydrolysed gelatin remained fluid [12]. For
incubated at their respective optimum nitrate reduction, isolates were grown in

Trop J Pharm Res, December 2011;10 (6): 803

 Sharma et al

nitrate containing medium for a week and a significance level of p < 0.05 using Sigma
thereafter, nitrate reduction was investigated Stat 3.5.
by addition of Griess- Illosvay’s reagent [13].
For urea hydrolysis, 2 % urea was added to RESULTS
basal medium. After a week, change in color
from yellow to red was recorded [14]. In this isolation and screening programme,
Assimilation of sugars as carbon sources and 134 different actinomycete isolates (based on
acid production were studied by adding 1 % colony morphology) were obtained from the
filter-sterilized sugars to the basal medium soil samples collected. Out of these, 51
(ISP-9). D-glucose containing medium was isolates (38.0 %) exhibited antimicrobial
considered as a positive control while activity during primary screening. All 51
medium without sugar was negative control. isolates exhibited antibacterial activity against
Growth on other sugars (sucrose, xylose, B. megaterium while only three (2.23 %)
inositol, D-Mannitol, D-fructose, L-Rhamnose, exhibited antiyeast activity (against C.
D-raffinose and cellulose) was compared to albicans and R. rubra). The isolates
positive control after 2 weeks of incubation exhibiting antimicrobial activity in primary
[10]. screening were subjected to secondary
screening by agar well method to confirm
Chemotaxonomic characterization their activity in culture broth. Forty four
isolates exhibited antimicrobial activity (32.8
Analysis of the isomer of diaminopimelic acid %) in culture broth.
in the cell wall and sugars in the whole-cell
Six isolates - 2A, R3YS, N23, A26, A27 and
hydrolysate was done according to Kutzner
A13 - showing promising broad spectrum
[15]. For sugar determination, dried cells (50
activity against different test organisms were
mg) were hydrolyzed in 1 ml of H2SO4 at 100 selected for further study. All the isolates
°C for 2 h and neutralized with saturated when grown on starch casein nitrate broth
solution of Ba(OH)2. The supernatant was showed maximal antibiotic production on the
dried, dissolved in distilled water and spotted fifth day (Table 1). R3YS showed maximum
(5µl) on a thin-layer plate coated with silica inhibition zone against all the tested
gel along with reference sugars (xylose, organisms followed by 2A isolate. Statistical
galactose, arabinose and glucose 5mg/ml analysis of the antimicrobial activity of
each). For the determination of actinomycete isolates against various test
diaminopimelic acid (DAP), dried cells (1 mg) organisms showed significant interaction
were hydrolyzed with 6M HCl at 100 °C for 18 between actinomycete isolates and test
h. The sample was dried and dissolved in organisms (Table 1).
distil water and spotted (5 µl) on thin layer
plate along with 2 µl DAP acid (0.01M) as Extraction of antibiotic
reference standard.
The antimicrobial compounds from the
Statistical analysis culture filtrates of the isolates 2A, R3YS,
N23, A27 and A13 were extractable in n-
To analyze the antimicrobial activity of the butanol (1: 2 v/v) whereas from A26 was
different actinomycete isolates against the extracted in diethyl ether. This suggests the
various test organisms, the data (expressed polar nature of antimicrobial substances from
the culture filtrates of 2A, R3YS, A27, A13
as the mean ± standard error of mean (SEM)
and N23 while non polar nature of compound
of three replicates) were subjected to two-
from A26.
way analysis of variance (ANOVA) and the
means were compared using Tukey’s HSD at

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 Sharma et al

Table 1: Antimicrobial activity of actinomycete isolates

Test organism Zone of inhibition (mm)

2A R3YS N23 A26 A27 A13
abu av aw acx aw aw
MRSA-97 21.6 ± 0.5 24 ± 1.0 17 ± 1.0 18.3 ± 0.5 17 ± 1.0 17 ± 0.0
acfu bv bw bfwx abwx abx
MRSA-67 19.3 ± 0.5 21 ± 0.5 14.6 ± 0.5 15.6 ± 0.5 15.6 ± 0.5 16 ± 1.0
acfu av bwx befw bwx bcx
MRSA P-169 19.3 ± 0.5 24 ± 0.0 15 ± 0.5 15.6 ± 0.5 15 ± 0.0 14.6 ± 0.5
bgu adv cw cw ax acy
B. megaterium 21.6 ± 0.5 23.3 ± 0.5 20.3 ± 0.5 19.3 ± 0.8 17.3 ± 0.5 16 ± 0.0
cfu bev aw adw bcx bcx
B. subtilis 21.0 ± 1.0 20.3 ± 0.5 17.3 ± 0.5 17.6 ± 0.5 14.6 ± 0.5 14.6 ± 0.5
acfu cev dw eiw bx dx
R-6SLF 19.3 ± 0.5 19.3 ± 0.5 10 ± 0.0 14.6 ± 1.0 15 ± 0.0 0
du bdv bw bdx bw dy
SI-LF 12.6 ± 0.5 22.3 ± 0.5 14.3 ± 0.5 16.3 ± 0.5 15 ± 1.0 0
cefu bev bw bfxy bwx ay
E. coli 17.6 ± 0.5 20.3 ± 0.5 14.6 ± 0.5 16 ± 0.0 15± 1.0 16.3 ± 0.5
fu av au efiw dx dy
S. typhi 19 ± 1.0 24.6 ± 0.8 18.0 ± 0.0 14.6 ± 0.5 13 ± 0.0 0
du gv w gx ew dw
P. mirabilis 12.3 ± 0.5 15 ± 0.0 0 11.6 ± 0.5 0 0
dhu fhkv dw gw fw ew
K. pneumoniae 11.3 ± 0.5 12.6 ± 0.5 9.3 ± 0.5 9.3 ± 0.5 10 ± 0.0 10 ± 0.0
ijhu iu ew gu ew dw
Enterococcus 10 ± 1.5 10.6 ± 0.5 0 10 ± 0.0 0 0
eu ju bw hx cdx cfx
E. aerogenes 16.3 ± 0.5 17.3 ± 0.5 15 ± 0.5 12.3 ± 0.5 13.3± 0.5 13.3 ± 0.5
eu cev ew ix ew dw
R. rubra 16.3 ± 0.5 19 ± 0.5 0 14 ± 0.0 0 0
ku gku ev ghw ev dv
C. albicans 14.6 ± 0.5 13.6 ± 0.5 0 11.6 ± 0.5 0 0
iu ifv ew jw ew dw
P. syringe 9.6 ± 0.5 12 ± 0.0 0 0 0 0
gu av cw jx ex dx
M. smegmatis 23 ± 1.0 25 ± 1.0 20.3 ± 0.5 0 0 0
ju cv fw ju eu du
X. campestris 0 18.3 ± 0.5 12.6 ± 0.5 0 0 0
Note: Results are mean ± SEM of three independent experiments. The same letters (a, b, c, d, e, f, g, h, i, j, k) within a
row are not significantly different (Tukey’s HSD, p < 0.05). The effect of different actinomycete isolates on antimicrobial
activity. The same letters (u, v, w, x, y) within a column are not significantly different (Tukey’s HSD, p < 0.05) and signify
the effect of various test organism on antimicrobial activity of actinomycete isolates

Characterization of selected isolates Cultural characteristics of isolates on different

using polyphasic approaches: Morpholo- media are presented in Table 2. They grew
gical, cultural, physiological and well on most of the organic and synthetic
biochemical characterization media but the best growth of all the cultures
was observed on starch casein nitrate agar.
All the isolates formed stable aerial and No soluble pigment was produced by 2A,
substrate mycelia when examined under R3YS, N23, A26 and A27 on any of the
phase contrast microscopy (slide culturing media used. However, isolate A13 produced
technique). The spore chain morphology of yellow-colored soluble pigment in all the
2A and A26 belongs to straight chain section, tested media except glycerol asparagine agar
while in R3YS, N23, A27 and A13, most of and tyrosine agar.
the spore chains were rectus flexibilis, and
very few formed loops on the tips of the spore The various physiological characteristics of
chain. The mature spores of A26 and A13 the isolates are presented in Table 3. All the
were round in shape and the number of isolates grew over a temperature range of 20
spores varied from 25 - 45 per spore chain. - 37 ºC with the optimum conditions at 28 ºC
However, in R3YS, A27, N23 and 2A, spores and 2 % NaCl concentration. All the isolates
were oval and there were more than 20 per were capable of hydrolyzing starch and
spore chain. esculin but not gelatin (only N23 and A27
hydrolyzed gelatin). R3YS, N23 and A27

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 Sharma et al

Table 2: Cultural characteristics of active isolates on different media

Medium Charac- Isolate

terstic 2A R3YS N23 A26 A27 A13
a
Starch G Abundant Adundant Abundant Abundant Abundant Abundant
b
casein AM Pinkish white Peach Whitish green Pinkish white Whitish green Grey
c
nitrate agar SM White Light peach Light yellow Pinkish white Whitish green Grey
d
SP None None None None None Mustard
e
S Pinkish white Light peach Pastal green Pinkish white Whitish green Grey
Yeast G Abundant Adundant Abundant Abundant Abundant Abundant
extract malt AM White Light peach Whitish green White Whitish green Dark Grey
extract SM White Peach Cream White Whitish green Grey
agar (ISP2) SP None None None None None Mustard
S White Light peach Pastal green White Whitish green Dark Grey
Oat meal G Abundant Abundant Abundant Abundant Abundant Abundant
agar (ISP3) AM Pinkish white Grey Pastal green Pinkish white Whitish green Grey
SM White Grey Cream White Whitish green Grey
SP None None None None None Mustard
S Pinkish white Grey Pastal green Pinkish white Pastal green Grey
Inorganic G Abundant Adundant Abundant Abundant Abundant Good
salts agar AM Pinkish white Peach Whitish green Pinkish white Whitish green Yellow
(ISP4) SM Pinkish white Peach Cream Pinkish white Whitish green Light yellow
SP None None None None None Light yellow
S Pinkish white Peach Greenish Pinkish white Pastal green Light yellow
Glycerol G Poor Abundant Abundant Poor Good Abundant
asparagine AM White White Whitish green White Pastal green Creamish
agar (ISP5) SM White White Cream White Pastal green Creamish
SP None None None None None None
S White White Whitish green White Whitish green Whitish grey
Tyrosine G Abundant Adundant Abundant Abundant Abundant Good
agar (ISP7) AM Pinkish white Peach Whitish green Pinkish white Pastal green Grey
SM White Light peach Cream White Pastal green Grey
SP None None None None None None
S Pinkish white Peach Pastal green Pinkish white Whitish green Grey
Bennett’s G Abundant Abundant Abundant Abundant Abundant Good
agar AM White Grey Whitish green White Whitish green Light yellow
SM White Grey Cream White Whitish green Light yellow
SP None None None None None Light yellow
S White Grey Pastal green White Whitish green Light yellow
a
G = Growth, bAM = Aerial mycelium, cSM = Substrate mycelium, dSP = Soluble pigment, eS = Sporulation

reduced nitrate to nitrite and hydrolyzed urea. chemotaxonomic characteristics indicated

None of the isolates produced melanin on that all six active isolates belonged to the
tyrosine agar. Assimilation of sugars as genus Streptomyces.
carbon sources and acid production by
isolates were studied and the results are DISCUSSION
shown in Table 4.
Actinomycetes are the most
Chemotaxonomic characterization biotechnologically valuable prokaryotes
responsible for the production of about half of
All the six isolates possess LL-DAP and the discovered bioactive secondary
glycine in their cell wall but no characteristic metabolites including antibiotics [3,4,6]. They
sugar. Phenotypic characteristics and

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 Sharma et al

Table 3: Physiological characteristics of isolates

Characteristic Medium Response of isolates

2A R3YS N23 A26 A27 A13
Hydrolysis of starch Starch casein nitrate agar + + + + + +
Hydrolysis of urea Urea broth - + + - + -
Reduction of nitrate Nitrate broth - + + - + -
Melanin formation Tyrosine agar - - - - - -
Hydrolysis of esculin Esculin hydrolysis medium + + + + + +
Hydrolysis of gelatin Gelatin hydrolysis medium - - + - + -
NaCl resistance Yeast extract-malt extract
2% agar with NaCl + + + + + +
5% + + +/- +/- + +/-
7% + +/- - - + -
10% - - - - - -
Temperature range Starch casein nitrate agar 20-37°C 20- 20- 20- 20- 20-
40°C 37°C 35°C 37°C 37°C
Positive = (+), negative = (-), doubtful = (+/-)

Table 4: Utilization of sugars and acid production by different isolates

Sugar Isolate
2A R3YS N23 A26 A27 A13
a b
U A U A U A U A U A U A
D-glucose + + + + + + + +/- + + + +
Sucrose - - + - +/- - + - - - - -
Xylose - - + - +/- - +/- - + - + -
Inositol - - + - - - - - +/- - + +
D-Mannitol - - + + + + - - + + + +
D-fructose + + +/- + + +/- - - + + + +/-
L-Rhaminose - - + + + +/- - - + - + +
D-Raffinose - - + - +/- - +/- - - - - -
Cellulose - - + - +/- - +/- - - - - -
a
U = utilization of sugar as sole carbon source, bA = acid production from sugar Positive = (+), negative = (-), doubtful = (+/-)

are the main source of clinically important line with results reported earlier by some
antibiotics, most of which are too complex to researchers [16,17]. On the basis of primary
be synthesized by combinatorial chemistry; and secondary screenings, six potent
thus, microbial natural products still appear antibiotic producers exhibiting broad-
as the most promising sources for developing spectrum activity were selected and studied
future antibiotics. in detail. All the six isolates grew well on most
of the media tested. When grown on starch
In the present investigation actinomycetes casein nitrate broth, the maximal antibiotic
were isolated from soil samples collected production was displayed on the 5th day. A
from different unscreened ecosystems of broad-spectrum antifungal compound
Punjab and Himachal Pradesh (India) which producing Streptomyces isolate, 1DA-28,
are large and diverse, for the isolation of from Indian soil, which was characterized and
potent and broad-spectrum antibiotic- identified as Streptomyces aburaviensis var.
producing actinomycetes. Out of the total 134 ablastmyceticus (MTCC 2469) has previously
isolates, 51 isolates showed good activity in been found also to exhibit maximum antibiotic
primary screening but failed to manifest production on the 5th day of incubation at 30
activity in secondary screening, which is in ºC [18].

Trop J Pharm Res, December 2011;10 (6): 807

 Sharma et al

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