J. Eco. Heal. Env. Vol. 3, No.

1, 7-13 (2015) 7

Journal of Ecology of Health & Environment

An International Journal

http://dx.doi.org/10.12785/jehe/030102

Screening of Antimicrobial Activity of Selected Egyptian

Cyanobacterial Species

Mervat A. M. Abo-State1, Sanaa M. M. Shanab2, Hamdy E. A. Ali1 and Mohd A. Abdullah3,*

1
Department of Microbiology, National Center for Radiation Research and Technology (NCRRT), Atomic Energy Authority,
Egypt.
2
Department of Botany and Microbiology, Faculty of Science, Cairo University, 12613 Giza, Egypt.
3
Department of Chemical Engineering, Universiti Teknologi PETRONAS, Bandar Seri Iskandar, 31750 Tronoh, Perak, Malaysia.

Received: 7Jun. 2014, Revised: 21Sep. 2014, Accepted: 23Sep. 2014.

Published online: 1 Jan. 2015.

Abstract: The present study aimed to evaluate the antimicrobial activity (against selected bacterial, fungal and yeast strains) of
successive extracts from different blue green algae. Aqueous and organic extracts of seven cyanobacterial species were screened against
in vitro eight human bacterial pathogens and five fungal strains. Chloroform extract of the seven cyanobacterial species showed largest
antibacterial inhibition zone diameter against the pathogenic bacterial strains. The chloroform extracts showed a broad spectrum against
Gram- negative bacteria (Escherichia coli, Aeromonas hydrophila , Salmonella enterica S 1180, Klebsiella pneumonia K 51 , Vibrio
cholera V116 and Salmonella paratyphi) and Gram-positive bacteria (Staphylococcus aureus S 1426, Listeria monocytogenes L 49 ).
However, the chloroformic extracts displayed also antifungal activity against Aspergillus terreus F98, while, none of the extracts of the
seven cyanobacterial species demonstrated any activity against Tirchoderma viride F94. Meanwhile, the ethanolic extracts of four of
cyanobacterial species showed antifungal activity against both yeast strains of Candida tropicalis Y26 and Saccharomyces cerevisiae
Y39. On the other hand, ethyl acetate extracts of all cyanobacterial species showed antifungal activity against Saccharomyces cerevisiae
YH.
Keywords: Antibacterial activity, Antifungal activity, Blue green algae, Human pathogens, Successive extracts.

nutrients, including vitamin B, vitamin E, beta-carotene,

1.Introduction manganese, zinc, copper, iron, selenium, and essential fatty
acid such as γ linolenic acid (Gupta et al., 2013). Moreover,
Cyanobacteria( blue green algae) are Gram they included the potential sources of new polymers,
negative autotrophic bacteria, exhibiting a variety of carbohydrates (as glucosyl glycerol, trehalose and sucrose)
metabolic capabilities and adaptive mechanisms, including which are synthesized by cyanobacteria under different
chromatic adaptation, nitrogen fixation (occurs in osmotic stresses (Santillan, 1982). They have potential
specialised cells called heterocytes/under microaerobic applications in diverse areas, especially in agriculture (as
conditions/through temporal spatiation), and the ability to biofertilizer, plant growth promoting rhizobacteria and as
form symbiotic associations with several eukaryotic hosts biocontrol agents).
such as plants, fungi, and protists (Bergman and Ran 2008).
Their role as food supplements/nutraceuticals and
They mainly have chlorophyll a, moreover accessory
in bioremediation and wastewater treatment is an emerging
pigments such as phycobilins, carotenoids (Hedges et al.,
area of interest. In addition, they are known to produce
2001). Cyanobacterial phycobiliproteins (phycocyanin,
wide array of bioactive compounds (secondary metabolites)
phycoerythrin and allophycocyanin). All these pigments
with different biological activities including antibacterial,
have different pharmaceutical applications, as antioxidants,
antifungal, antiviral, antimalarial, antitumoral and anti-
boost the immune system and possibly decrease the risk of
inflammatory properties, having industrial, therapeutic and
heart disease, prevent onset of cancers and protect against
agricultural significance (Gupta et al., 2013). Screening of
age related diseases as cataracts and multiple sclerosis, etc.
cyanobacteria for antibiotics and other pharmacologically
(Larsson et al., 2007). Blue green algae also, contain
*
Corresponding author e-mail: [email protected]
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Natural Sciences Publishing Cor.
8 M. A. M. Abo-State et al.: Screening of antimicrobial activity …

active compounds, has received ever-increasing interest as Salmonella enterica S 1180, Klebsiella pneumonia K 51 ,
a potential source for new drugs (Browitzka, 1995; Schlegel Vibrio cholera V116 and Salmonella paratyphi, were
et al.,1999).The important compounds identified as kindly provided by Institute of Medical Research (IMR),
antimicrobial are fatty acids, acrylic acid, halogenated Kuala Lumpur, Malaysia. These strains were cultured and
aliphatic compounds, terpenes, sulphur containing hetero maintained on L.B agar medium (Martin et al.,1981).
cyclic compounds, carbohydrates and phenols (Kannan et Bacterial strains were inoculated in L.B broth medium
al., 2010). A couple of biologically active compounds were overnight (16 hours) in shaking incubator at 37 oC. the
identified among exometabolites, e.g. certain antibacterial grown culture (2x108 CFU/ml) were used to seed L.B agar
diterpenoids in Nostoc commune (Jaki et al., 2000) and plates (by medical swaps) the seeded plates were left for 1
antifungal peptides in Tolypotrix byssoidea (Jaki et al., hr, then filter paper discs ( 10 mm diameter) were loaded
2001). The present study aimed to evaluate the by 50 µl of tested extract from each algal species against
antimicrobial potential of successive extracts from seven each bacterial strain . Three replicates were used for each
cyanobacterial species against human pathogenic bacteria, extract. The plates were incubated up right for 24 hrs at
fungi, and yeast. 37oC. Amoxicillin was used as standard commercial
antibacterial agent (positive control) and dimethyl sulfoxide
2. Materials and methods (DMSO (1%)) as (negative control). The inhibition zones
2.1 Algal species and culture conditions around discs were determined (mm).
2.3.2. Antifungal activity
Seven Cyanobacteria species (Oscillatoria sp., Nostoc sp.,
Nostoc muscorum, Nostoc piscinale, Phormidium sp.,
The yeast strains Saccharomyces cerevisiae Y39; Candida
Anabaena flos-aquae and Spirulina platensis) were
tropicalis Y26 and Saccharomyces cerevisiae YH. Fungal
obtained from the Microbiology Department, Soils, Water
strains Tirchoderma viride F94 and Aspergillus terreus F98
and Environment Res. Inst. (SWERI), Agric. Res., Center
were kindly provided by Dr. Abo-State (National Center for
(ARC), Giza, Egypt. Cyanobacterial species were
Radiaition Research and Technology (NCRRT), Cairo,
maintained on BG11 medium (Rippka, 1988) except
Egypt).Yeast strains were cultured and maintained on
Spirulina platensis which was cultured on Zarrouk medium
Wickersham’s medium (Wickersham´s. 1951).Yeast strains
(Zarrouk, 1966). Cultures of these species were incubated at
were inoculated in Wickersham’s broth medium and
temperature 25±1°C under illumination of natural light
incubated for 24 hrs at 30 oC, (2x105 CFU/ml). These yeast
intensity of 30 µE/m2/s and photoperiod 12/12 h. At the
cultures were used to seed the Wickersham’s agar plates for
late exponential growth phase, algae were harvested by
testing biological activity of algal extracts. Fungal strains
centrifugation at 3500 rpm for 10 min and the pellets were
were cultured and maintained on Saubouraud agar medium
subjected to extraction by different solvents of increasing
(Oxoid, 1982). and spore suspension were carried out
polarity.
according to Abo-State 2003 , flasks (250ml) containing
2.2. Successive extract preparation 100ml Saubouraud agar medium were inoculated and
incubated at 27 oC for 7 days. The spores of each strain
A known weight (2g) of each algal species was extracted were collected by 0.1 % Tween 80 in sterile saline solution
two times by hexane for 30 min.at room temperature (30ml). The collected spore suspensions (2x107spores/ml)
(25±1°C) followed by centrifugation at 4500 rpm for 10 were used to seed Saubouraud agar plates. The seeded
min. and the supernatants were combined. The subsequent plates were left for 1 hr and then sterile filter paper discs
successive extraction of each algal pellet was performed by (10 mm diameter), loaded by 50 µl of each algal extract
the same pervious procedure with the following solvents, were placed on the surface of seeded plates and incubated
chloroform, ethyl acetate, ethanol (70%) and dist. water. So at 27 oC for three days. Three replicates were used for each
each algal species have five extracts (Fig 1). Solvents were extract. Ultragriseofulvin was used as standard antifungal
evaporated using rotary evaporator at 40-45oC, while those activity agent (positive control) and dimethyl sulfoxide
of ethanol (70%) and water were freeze-dried. Dried solvent (DMSO (1%)) as (negative control).The clear
residues of extracts belonging to each algal species were inhibition zones around discs were determined (mm) which
dissolved in DMSO (1%) and used for determination of were used as a measure of antifungal activity of algal
their antimicrobial activities. extracts.

2.3. Determination of antimicrobial activity 2.4. Statistical analysis

2.3.1. Antibacterial activity The experiments were carried out in triplicates and the
results were expressed as the means values and standard
deviations. The statistical analyses were performed using
The Bacterial strains (Gram- positive) Staphylococcus
SPSS version 16.0 for windows.
aureus S 1426, Listeria monocytogenes L 49, (Gram-
negative) Escherichia coli, Aeromonas hydrophila ,

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J. Eco. Heal. Env. Vol. 3, No. 1, 7-13 (2015) / http://www.naturalspublishing.com/Journals.asp 9

3. Result and discussion Ethyl acetate extracts of Nostoc sp., A. flos-aquae and S.
platensis showed slight inhibition zones (11.0 , 12.0 and
The extracts of seven cyanobacterial species were tested for 11.5 mm) against S. paratyphi and that of N. musorum
their antibacterial activity against eight human pathogenic showed similar slight inhibition zone with S. enterica S
bacteria and antifungal activity against three yeast and two 1180 (11.0 mm) . While, ethanolic extract of all
fungal strains. cyanobacterial species demonstrated inhibition zones of
variable diameters (11.0 - 15.5 mm) against E. coli accept
that N. piscinale which showed no activity. Ethanolic
3.1. Antibacterial activity extracts of both N. Piscinale and S. platensis showed
slight and moderate inhibition zones (11.0 , 17.0 mm
Table (1) and Fig (1, 2) recorded the antibacterial activity
respectively) against A. hydrophila. Also slight inhibition
of successive extracts of the tested pathogenic bacterial
zones were recorded against S. aureus S 1426 by ethanolic
species. The most remarkable results was that of
extracts of both N. piscinale and A. flos-aquae (11.0 mm).
chloroform extracts of all the seven used bacteria showed
In addition, ethanolic extract of N. musorum illustrated
inhibition zones of variable diameters (11.0 -30.0 mm),
slight antibacterial activity against V. cholera V116
while hexane and water extracts recorded negative results.
(12.0mm).

Table (1): Antibacterial activity of different successive extracts from seven blue green algae

Results are the means of diameter values ± standard deviation. (-): No activity

© 2015 NSP
Natural Sciences Publishing Cor.
10 M. A. M. Abo-State et al.: Screening of antimicrobial activity …

extracts of all the investigated cyanobacterial species

showed no activities with the tested fungal and yeast
species except hexane extract of S. platensis which
exhibited very weak activity against A. terreus F98.
The cyanobacteria such as Nostoc commune (Jaki et al.,
2000), Scytonema hofmanni (Pignatello et al., 1983),
Anabaena spp. (Frankmolle et al., 1992), Nostoc
spongiaeforme (Hirata et al.,1996), Phormidium sp. (Fish
and Codd 1994), have been reported as the main
cyanobacterial species producing antimicrobial substances.
Investigations aimed to identify antimicrobial
agents in cyanobacteria showed the occurrence of many
promising compounds. Some of these substances were
Figure (1): Successive extracts of different cyanobacterial identified including Nostocyclyne A (Ploutno and Carmeli,
species acquire various colours, Oscillatoria sp. (A), and 2000), Nostofungicidine (Kajiyama et al.,1998),
Phormidium sp. (B). Kawaguchipeptin B (Ishida et al.,1997), Nostocin A (Hirata
et al.,1996), Ambigol A and B (Falch et al.,1995),
Hapalindoles (Moore et al.,1987) and Scytophycins
(Ishibashi et al.,1986). Studies have only done as in vitro
assays and, it is likely that most of these compounds will
have little or no clinical application as they are either too
toxic or inactive in vivo . However, they may be useful
compounds for the synthesis of antibiotics or may be used
in agriculture applications. For example Tjipanazoles which
was isolated from the cyanobacterium, Tolypothrix
tjipanensis, demonstrated appreciable fungicidal activity
against rice blast and leaf rust wheat infections (Browitzka,
1995). The obtained results (antibacterial and antifungal) i n
this study were confirmed by the results of other
investigators. Ghasemi et al. (2003) found that methanolic
Figure (2): Antibacterial activity: zone of inhibition extracts and culture supernatants of 21 species of
exhibited by different extracts of cyanobacterial species: cyanobacteria exhibited significant antibacterial activity
Nostoc sp. (1: V. cholera V116) and N. piscinale (2: and 13 species showed antifungal effects. No antimicrobial
Salmonella enterica S 1180). activity was detected in the hexane extracts of the
cyanobacteria under investigation which may be probably
3.2. Antifungal activity due to the polar nature of the active components. Also,
Bhateja et al. (2006) studied the effect of different extracts of
None of the tested seven cyanobacterial extracts showed nine cyanobacteria against different strains of
any antifungal activity against T. viride. However, the Staphylococcus aureus. Aqueous extract of all the tested
chloroform extract of five cyanobacterial species out of the blue green microalgal were found to be inactive against in
seven demonstrated antifungal activity against A. vitro generated vancomycin intermediate resistant
terreus.While three ethanolic extracts also showed Staphylococcus aureus (VISA). While, Kreitlow et al. (1999)
antifungal activity against the same fungus as showed in evaluated the antimicrobial activities of twelve
(Table 2). On contrast C. tropicalis Y26 was sensitive cyanobacterial species against seven microorganisms.
against four ethanolic extracts (of N. musorum (17.5 mm), However, no inhibitory effects were recorded against the
S. platensis (13.5 mm), Phormidium sp (11.5 mm) and three Gram- negative bacteria, E. coli, Proteus mirabilis
Oscillatoria sp. (11.0 mm)). However ethyl acetate extracts and Serratia marcescens and the yeast Candida maltosa.
of the seven cyanobacterial species was effective in Different results have been reported by many authors in this
inducing weak activities (11.0 -12.5 mm) against S. context. For example, Falch et al. (1995) and Hirata et al.
cerevicieae YH. In case of S. cerevisiae Y39 the ethanolic (1996) reported active compounds against E. coli in the
extracts of the four cyanobacterial species (N. musorum , N. petroleum ether fraction of Fischerella ambigua and
piscinale, Phormidium sp. and S. platensis) showed supernatant of Nostoc spongiaeforme. However, Plazaa et
antifungal activities against this organism (13.0, 13.5, 12.0 al.(2010) found that ethanol was selected as the most
and 12.5 mm respectively). Extracts of Oscillatoria sp., appropriate solvent to extract bioactive compounds from
Nostoc sp. and A. flos-aquae showed no activity with the two macro and microalgal species with antimicrobial
most tested fungal and yeast strains. Hexane and water

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J. Eco. Heal. Env. Vol. 3, No. 1, 7-13 (2015) / http://www.naturalspublishing.com/Journals.asp 11

activities against four microorganisms (E. coli, inhibition). Also, Chauhan et al. (1992) reported that ether
Staphylococcus aureus, Candida albicans and Aspergillus extract of Oscillatoria sp. demonstrated antibiotic activity
niger). But, Bhagavathy et al. (2011) used the green algal, which may be due to the isolated and identified saturated
chlorococcum humicola extracts of various organic fatty acids( C14:0, C16:0 and C18:0). In the same context,
solvents against seven pathogenic bacteria, one yeast and Shanab (2007) studied the antibiotic efficiency of three
two fungal strains. From all the investigated organic Oscillatoria species (O. hameli, O. rubescens and O.
extracts, only benzene and ethyl acetate extracts showed platensis).
greatest activity (reached nearly 80% of microbial growth

Table (2): Antifungal activity of different successive extracts from seven blue green algae

Results are the means of diameter values ± standard deviation. (-): No activity
The results revealed that the active compounds antimicrobial substances on different microorganisms. It
isolated and identified by GC/MS and TLC contained fatty was reported that Gram – negative bacteria are more
acids (saturated and unsaturated), the tetramine spermine resistant to the inactivation by medium and long chain fatty
and piperazine derivatives which may be responsible for acids than the Gram – positive bacteria which are more
the pronounced antimicrobial activity against the Gram- susceptible; this may result from impermeability of the
positive , Gram- negative bacteria and pathogenic fungi. outer membrane of Gram –negative bacteria which is
The antimicrobial activity manifested by either Oscillatoria considered as an effective barrier against hydrophobic
species in the previous study or by the seven selected substances (Sheu and Freese, 1973). The inhibitory effect of
cyanobacteria species in the present investigation was in antifungal compounds may be due to the inhibition of spore
accordance with reported antibiotic activities manifested by germination or the inhibition of synthesis of B- (1,3)-D-
different cyanobacterial bioactive compounds as glucan or inhibition of integral component of fungal cell
Hapalindoles alkaloids, cyanobacterin, Nostocyclamide, wall and their effect on fungal cell membrane which alter
Fischerellin A&B and Norhamane which were produced by its permeability (Gupta et al., 2001). In the same context, it
various cyanobacteria species (Volk, 2005). Antimicrobial was also reported that, antifungal compounds may inhibit
activities of Spermine, Piperazine and fatty acids were lipid synthesis in the tested fungal species. This may be due
reported in many studies (Cushion et al., 2004; Shanab, to a decrease in the ratio of unsaturated to saturated fatty
2007). Fatty acids (non-polar) are recognized to have acids or inhibition of ergosterol biosynthesis
antibacterial and antifungal activities against broad (Georgopapadakou et al.,1987).
spectrum of bacterial and fungal species (McGaw et
Further studies are needed concerning the analysis of the
al.,2002; Barbour et al.,2004 ; Agoramoorthy et al., 2007).
promising extracts of the tested cyanobacterial species,
Many authors suggested the mechanism of action of
comparing between their contents and identifying the active

© 2015 NSP
Natural Sciences Publishing Cor.
12 M. A. M. Abo-State et al.: Screening of antimicrobial activity …

substance which may be the responsible agent(s) for the 875, (1973).
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[9] C. Zarrouk, Contribution á l’étude d’une cyanophycée.
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