ANTIMICROBIAL ACTIVITIES OF SPIRULINA PLATENSIS EXTRACTS AND NANOPARTICLES MATERIAL AGAINST SOME PATHOGENIC BACTERIAL ISOLATES

ANTIMICROBIAL ACTIVITIES OF SPIRULINA
PLATENSIS EXTRACTS AND NANOPARTICLES
MATERIAL AGAINST SOME PATHOGENIC
BACTERIAL ISOLATES
Omayma A. Awadalla1 ; Nanis G. Allam1 ; Yehia M. Mokhtar2 ;
Eslam Baklola 2 ; Wagih A. El-Shouny1 and M. El-Shetehy 1
1 Microbiology and plant pathology, Botany Department, Faculty of Science, Tanta
University
2 Central Laboratory of Environmental Quality monitoring – National Water Research
Center
Eslam_baklola@hotmail.com
ABSTRACT
The algal species Spirulina platensis have the potential to produce
a large number of antimicrobial substances that considered as suitable
bio-control agents for plant pathogenic bacteria. The present study aimed
to synthesize nano- material of S. platensis, use anti-bacteria material of
S. platensis using solvent extracts and tested them against pathogenic
bacteria by Standard well diffusion method for antibacterial activity.
Mullor Hinton Agar (MHA) plates and pure cultures of bacterial
pathogens were grown in Nutrient broth at 37OC for 18-24 hours. In the
present, the tested positive and negative gram bacteria were isolated from
water Omar Bek drainage water-Damietta branch of Nile River
The data of sodium-citrate extraction showed maximum zone of
inhibition against all the bacterial isolated while extraction of S. platensis
showed minimum inhibition zone against bacterial pathogens in
comparison to other solvent extracts. Nano material recorded the highest
zone of inhibition against Yersinia pestis (45mm) in comparison with Nacitrate
against Staphylococcus aureus (20mm) as an organic solvent
extract. The research concluded and recommended S. platensis should be
considered as an economic antibacterial agent than using medical
antimicrobials against pathogenic bacteria.
1. INTRODUCTION
Spirulina, a blue green alga is now becoming a health food along
worldwide. It is an edible, microscopic, multi-cellular, filamentous,
alkalophilic, photo auto trophiccyano bacterium that belonging to micro
algae of the class Cyanophyta. It consists of a larger cell size for ease of
cultivation, for ease of harvest and an easily digestible cell wall. They are
considered as rich source of protein, vitamins, and minerals than any
Egypt. J. of Appl. Sci., 36 (5-6) 2021 20-33
other single cell protein. Dominating the micro-flora of alkaline saline
waters with pH of up to 11.0 and they can exist in various types of
habitats, namely soils; marches, thermal springs uses, fresh water,
seawater and brackish, domestic, industrial wastewaters (Jensen and
Knutsen, 1993 and Marcello Nicoletti, 2016).
They have been a nature source of medicinal agents for thousands
of years. Modern drugs have been isolated from natural sources based on
their uses in traditional medicine. Recently many screening of
cyanobacteria, antibiotics and other pharmacologically active compounds
have received considerable attention (Haidan et al, 2016).
Spirulina as many other cyanobacteria species have the potential to
produce a large number of antimicrobial substances that they are
considered as bio-control agents of plant pathogenic bacteria and fungi.
Algal organisms are rich source of structurally novel and biologically
active metabolites that primary or secondary metabolites produced by
these organisms may be potential bioactive compounds of
pharmaceutical industry (Yuliani et al., 2021).
S. platensis produce a diverse range of bioactive molecules, making
them a rich source of different types of medicines, (Kapoor and Mehta
1993; Nasima, et al., 2012). The Spirulina, as a whole, has been known
only for its nutritional value but their antimicrobial property of the Cphycocyanin
has not been studied in detail in Indian context.
Antimicrobial compounds found in cyanobacterial exudates include
polyphenols, fatty acids, glycolipids, terpenoids, alkaloids and a variety
of yet to be described bacteriocins (Sherif et al., 2021).
Secondary metabolites from cyanobacteria are associated with
toxic, hormonal, anti-neoplastic and antimicrobial effects. The
antimicrobial substances involved may target various kinds of microorganisms,
prokaryotes as well as eukaryotes. The properties of
secondary metabolites in nature are not completely understood.
Secondary metabolites influence other organisms in the vicinity and are
thought to be of phylo-genetic importance. The methods that commonly
applied for extraction are based on the agar diffusion principle using
pour-plate or spread plate (Seeded plates) techniques. Antimicrobial
effects are shown as visible zones of growth inhibition (Inhibition halos)
(McGill and Hardy, 1992). The research aimed to synthesize nanomaterial
of S. platensis, use anti-bacteria material of S. platensis algae
using solvent extracts and tested them against pathogenic bacteria by
Standard well diffusion method for antibacterial activity.
21 Egypt. J. of Appl. Sci., 36 (5-6) 2021
2. MATERIALS AND METHODS
2.1 Study area and Sample Collection
The study area includes about 119 km (73.94 miles) of the
Damietta branch and extended from upstream of the Omar-Bek drain to
Faraskour City as shown in Fig.(1). It receives the outlet of three
agricultural main drains (Omar Bek, Upper Serw and Drain No.1) where
they uploaded with untreated sewage water from many villages. Omar
Bek drain is about 130 km far away from Cairo. It serves about 43,000
feddan (one feddan=0.42 ha) of fertile lands and has a discharge rate of
about 12,000 m /h. These wastewaters are collected from industrial,
domestic, and agricultural effluents along this drain path from Zefta to
Samanoud cities. Omar Bek was initially built as an agricultural drain by
the 1980s, and its water quality was in normal ranges till the 1990s. After
the 1990s, many environmental issues related to this drain started to be
raised (Ezzat and Elkorasey, 2020; Mostafa and Peters, 2016).
Fig.(1): Map of Study Area Location and Water Samples along Omar
Bek Drain and Damietta Branch-Nile River
In this study, area under investigation ten water samples along
Omar Bek drain and from Damietta branch of Nile River, during autumn
(on 26 September 2016- from 8.00 a.m. to 10.00 a.m.- air temperature was
31oC) as shown in Fig.(1). Sampling procedures were carried out
according to Standard Methods for Examination of Water and
Wastewater (APHA, 2012). All collected samples were stored in an iced
cooler box and delivered immediately to the Central Laboratory for
Environmental Quality Monitoring, National Water Research Center
“CLEQM-NWRC” where it has been analyzed.
Egypt. J. of Appl. Sci., 36 (5-6) 2021 22
2.2 Isolation, purification and characterization of bacteria
isolates
2.2.1 Identification of Bacterial isolates:
For all wastewater samples, a volume of 100ml was filtered
through 0.47μm pore sized filter using water pump. All selective media
used were prepared according to Bergeys Manual (1957) in order to
isolate and identify bacteria spp.
2.2.2. Morphological characteristics of Bacterial isolates:
Morphological characteristics of colonies color, Gram reaction.
Cell Shape, Spore formation, and Motility and Diffusible pigment were
investigated. Physiological and biochemical characteristics of pathogenic
bacteria isolates were conducted according to tests in Bergeys Manual
(1957). Table (1) illustrates the Morphological and biochemical
characteristics of identified bacteria isolates from water of Omar bek
drain.
2.2.3 Collection of Pathogenic Bacteria:
Eleven different bacterial cultures of Gram positive and Gram
negative bacteria were isolated from water samples along Omar Bek
drain that were:
Gram positive bacteria: Staphylococcus aureus and Enterococcus
faecalis.
Gram negative bacteria: Pseudomonas aeruginosa; Serratia liquefaciens;
Enterobacter aerogenes; Klebsiella pneumonia; Shigella sonnei;
Legionella pneumophila; Yersinia pestis; Moraxella catarrhalis and
Hafnia alvei
2.3 Determination of Antimicrobial Activity of S. platensis
2.3.1 Preparation of S. platensis extract:
Cells of S. platensis were cultivated in Zarrouk growth media (Fig.2a)
(Zarrouk, 1966) at constant shaking at 30°C±2°C and pH 10 in
light/dark conditions (16/8 hrs) with shaking of culture manually twice a
day. Bacterial cells were harvested after 5-6 days and then washed twice
in distilled water. The collected cells were preserved and the supernatant
was discarded. The cells of S. platensis were stored at -20 until be used.
2.3.2 Phyto-chemical Extraction:
About 2 gm of algae fresh weight were added to 10 ml of the
desired organic solvent (Na citrate; Ethanol; Hexane; DMSO and
acetone) (Fig. 2b, c), mixed well per each organic solvent and then the
mixture was exposed to Sonication (Cycle 5 min on, 5min off, 1min on,
power 100% on Ice). After Sonication the volume was completed into
100ml with worm water were add to the sonicated solution. Then, the
solution was incubated for 16 hours at 30°C with shaking at 150 rpm.
Water and methanol extraction were performed according to
(Tsibakhashvili, et al., 2011).
23 Egypt. J. of Appl. Sci., 36 (5-6) 2021
Table (1). Morphological and biochemical characteristics of identified bacteria isolates from water of
Omar bek drain.
Test
L.
pneumophila
Y.
pestis
H.
alvei
S. liquefaciens
P.
aeruginosa
S.
aureus
M.
Catarrhalis
E.
faecalis
E.
aerogenes
K.
pneumoniae
S.
sonnei
Temp. Limits of
growth
36°C 35-37°C 2.6°C-42°C 30-37°C
37°C, -/4°C and
+/-41°C
15 - 45°C 28-37°C 10-45°C 40°C 36°C 35-37°C
Shape of colony
Rods and
filaments
Raised
irrigular
Straight Straight rods straight rods
Raised, circular
and entire
large and kidney
Small-raised
and entire
Rod Rod Short rods
Texture Smooth Smooth Smooth Smooth Smooth Smooth Smooth Smooth Smooth Smooth Smooth
Pigmentation - - - -
Blue-green
exopigment
Golden yellow - - Yellow - -
Motility + - + + + - - - + - -
O2 requirements Aerobic
facultatively
anaerobic
facultatively
anaerobic
Aerobic
Facultatively
anaerobic
Facultatively
anaerobic
Aerobic
Facultatively
anaerobic
Aerobic/
anerobic
Facultatively
anaerobic
Facultatively
anaerobic
Gram reaction - - - - - + - + - - -
Cell Shape Rods Rods Rod Rods Straight rods
Cocci in clusters
and pairs
Kidney
Cocci in pairs
short chains
Rod Rods Rod
Sporulation - - - - - - - - - - -
Capsule - + - - - - - - + + -
Catalase + + + + + + + - + + +
Coagulase - + + + - + NA - + +
Oxidase + - - - + - + - - - -
Urease - - - + - + - - - + -
Gelatin
liquefaction
- - - + + + + + - - -
Starch hydrolysis + + - + - - + - - - -
Phyenl amine
deaminase
+ - - - - - + - - - -
H2S production - - - - - - + - - - -
Heamolysis blood
agar
β-Heamolysis - β-Heamolysis β-Heamolysis β-Heamolysis β-Heamolysis - β-Heamolysis β-Heamolysis - -
Nitrate reduction - + + + - + + - + + +
Indol formation - - - - - - - - - - -
Methyl red - + + - - + + - - - +
Tween 80
hydrolysis
+ + - - - + - - - - -
Voges-Proskauer + - + + - + - + + + -
Citrate utilization + - - + + + - - + + -
D-glucose + + + A/G -/- A/- - A/- A/G A/G +
Sucrose + - - + -/- A/- - A/- + + -
Mannose + + + + -/- A/- - A/- + + +
Lactose + - - - -/- A/- - A/- + + -
Mannitol + + + + A/- A/- - A/- + + -
(+), positive result; (-), negative result; (A), (NA), Not Applicable; (A), acidproduction and (G), gas production.
Egypt. J. of Appl. Sci., 36 (5-6) 2021 24
2.3.4 Antimicrobial activity of the obtained algae nano silver
In vitro antimicrobial activities had been examined for 11
pathogenic bacteria using the agar disk diffusion method according to
(Attaie, et al., 1987). Inhibition zones of growth around the disks were
measured after 24 hours of incubation at 37°C. The nano-particle activity
was compared with some other of generic antibiotics.
(a) (b) (c)
Figure (2): (a) S. platensis cultivation; (b) Extracting antibiotics from S.
platensis cultivation; (c) antibacterial agents test of S. platensis
against pathogenic bacteria.
2.3.5 Determination of Antibacterial Activity by Well Diffusion
Method
The wet biomass of S. platensis (1g) was re-suspended in 500 ml
Erlenmeyer flask with 100ml of 10−3 M aqueous silver nitrate (preparing
1mM of Silver nitrate (AgNO3) solution: dissolving 0.169g of AgNO3
(Sigma, 99%, 169.87g/mol) in 1 liter of de-ionized water.) by using deionized
water (pH7) incubated at room temperature for different time
intervals (1–5 days). (Kalabegishvili et al., 2012; Devina et al., 2010).
The AgNPs synthesized from S. platensis was tested for its
antibacterial activity against pathogenic bacteria by standard well
diffusion method in Mullor Hinton Agar (MHA) plates. Pure cultures of
bacterial pathogens were grown in Nutrient broth at 37OC for 18-24
hours.
25 Egypt. J. of Appl. Sci., 36 (5-6) 2021
Wells were done on Moller-Hinton agar plates by using gel
puncture and plates were inoculated by scavenging bacterial pathogens in
order to create a confluent turf of the bacterial growth. After incubation
at 37OC for 24 hours, diameter of zone of inhibition in millimeter around
each well was measured (Thomas et al., 2012).
In this study, we used S. platensis algae as natural antibacterial
through phytochemical extraction with other organic solvents, against
pathogenic bacteria. We used S. platensis as natural nano material
through mixing algae with AgNO3 solution, against pathogenic bacteria
3. RESULTS AND DISCUSSION
3.1 Antibacterial Activity of Organic Antibacterial Solvents of S.
platensis
The antibacterial activity of S. platensis was determined against
bacteria and the findings were furnished in the Table (2), Figures (3 and
4). The zone of inhibition of S. platensis extracts against bacteria was
ranged between 5 mm to 45 mm at 200 μl. The Na-citrate extract of S.
platensis showed the highest mean zone of inhibition (20 mm) against the
Gram positive cocci Staphylococcus aureus, followed by Enterococcus
faecalis (15 mm), in comparison to other organic solvents. The minimum
zone of inhibition obtained from the acetone extract of S. platensis
against bacterial pathogens was comparatively very less when compared
to the other solvent extracts (Saranraj, 2015).
For Gram negative bacteria, the maximum zone of inhibition was
recorded also in Na-citrate extract of S. platensis against Yersinia pestis
(17mm) followed by Serratia liquefaciens (16mm), Klebsiella
pneumoniae (15mm), Legionella pneumophila (13mm), Moraxella
catarrhalis (11mm), both Pseudomonas aeruginosa and Shigella sonnei
were recorded (10mm), Hafnia alvei (7mm) and Enterobacter aerogenes
(5mm). No zone of inhibition was seen in DMSO and ethanol with both
gram positive and negative bacteria, in agreement with data of Saranraj,
et al., (2015). Kaushik and Chauhan (2008) reported that extracts of S.
platensis inhibited the growth diameter of Staphylococcus aureus,
Escherichia coli, Pseudomonas aeruginosa, Salmonella typhi and
Klebsiella pneumoniae. They used hexane, ethyl acetate,
dichloromethane and methanol to obtain the phenolic extracts and the
methanolic extracts had the best results. The methane extract of
Staphylococcus aureus and Escherichia coli minimum inhibitory
concentrations (MIC) were 128μg/ml and 256μg/ml respectively.
Egypt. J. of Appl. Sci., 36 (5-6) 2021 26
(a) (b)
(c) (d)
(e) (f)
Figure (3) Resistance of (a) Staphylococcus aureus; (b) Pseudomonas aeruginosa; (c)
Serratia liquefaciens; (d) Enterobacter aerogenes ; (e) Klebsiella
27 Egypt. J. of Appl. Sci., 36 (5-6) 2021
pneumonia; (f) Shigella sonnei isolates against nature antibacterial solvents
and nano material extract synthesized from S. platensis solution.
(a) (b)
(c) (d)
(e)
Figure (4) Resistance of (a) Legionella pneumophila; (b) Yersinia pestis; (c)
Moraxella catarrhalis; (d) Hafnia alvei ; (e) Klebsiella pneumonia; (f)
Enterococcus faecalis isolates against nature antibacterial solvents and
nano material extract synthesized from S. platensis solution.
Parisi et al., (2009) also found high antimicrobial activity of
phenolic compounds extracted with methanol from S. platensis against
Gram positive Staphylococcus aureus. Vinay Kumar et al., (2011)
examined the algal extracts in vitro for their antibacterial effects against
(Staphylococcus aureus and Salmonella typhimurium) using Agar well
Egypt. J. of Appl. Sci., 36 (5-6) 2021 28
diffusion method and Paper disc diffusion method with concentration
from 250ppm to 7000ppm and it noticed that all of these bacteria showed
inhibition in the growth of these extracts.
Table (2): Antibacterial Activity of Organic Solvents and Nano
Mmaterial Synthesized by S. platensis
Isolates Organic Solvents + Algae Algae as Nano Material
Na citrate Ethanol Hexane DMSO Acetone
Nano Material
only
Nano Material
+ Water
+DMSO
Staphylococcus aureus 20 -ve -ve -ve -ve 30 15
Pseudomonas aeruginosa 10 -ve -ve -ve -ve 12 -ve
Serratia liquefaciens 16 -ve -ve -ve -ve 20 30
Enterobacter aerogenes 5 -ve -ve -ve -ve 10 -ve
Klebsiella pneumoniae 15 -ve 10 -ve 10 11 -ve
Shigella sonnei 10 -ve -ve -ve -ve 13 -ve
Legionella pneumophila 13 -ve -ve -ve -ve 40 5
Yersinia pestis 17 -ve -ve -ve -ve 45 10
Moraxella catarrhalis 11 -ve -ve -ve -ve 20 10
Hafnia alvei 7 -ve 15 -ve 7 8 10
Enterococcus faecalis 15 -ve 15 -ve 20 6 -ve
(-ve), negative result
Antibacterial activity of AgNPs synthesized by S. platensis
The antibacterial activity of biosynthesized silver nano-particle was
performed against both gram positive bacteria as mentioned before by
well diffusion method. The zone of inhibition of S. platensis extracts
against bacteria was ranged between 5 mm to 45 mm at 200 μl/well. The
nano material extract of S. platensis showed the highest mean zone of
inhibition (30mm) against the gram positive cocci Staphylococcus
aureus, followed by Enterococcus faecalis (6mm), in comparison to nano
material + water + DMSO.
For Gram negative bacteria, the maximum zone of inhibition was
recorded also in nano material extracts of S. platensis against Yersinia
pestis (45mm) followed by Legionella pneumophila (40mm), both
Moraxella catarrhalis and Serratia liquefaciens (20mm), Shigella sonnei
(13mm), Pseudomonas aeruginosa (12mm), Klebsiella pneumoniae
(11mm), Enterobacter aerogenes (10mm), and Hafnia alvei (8mm).
By increasing the volume of AgNPs synthesized S. platensis to 100
μL/well the zone of inhibition increases for both gram positive and
negative bacteria. However, a Silver Nano particle has showed
antibacterial activities more than Na-citrate solvent. This study in
agreement with Theivasanthi and Alagar (2011) that reported Silver
nano particles material have showed high antibacterial activities in
comparison with other extracts.
The efficiency of the biosynthesized nano-material against the
tested bacteria could be attributed to the adherence of small sized nano-
29 Egypt. J. of Appl. Sci., 36 (5-6) 2021
material to the bacterial cell membrane surface and thus disturbing its
permeability and respiration functions (Jagtap and Bapat, 2013).
The utilization of S. platensis as antibacterial reagents or as nano
material solution has various advantages like easy cultivation and
availability. This biological method approach toward the synthesis of
nano-material has numerous benefits, that is, non-toxicity, cost
effectiveness, rapid reduction, and economic viability. Future prospects
of this research would be large scale production of nano material using S.
platensis and ascertaining its effectiveness against a broad spectrum of
microbial populations. In addition to other investigations that will
coverage of the S. Platensis effectiveness to synthesis silver nanoparticles.
4. CONCLUSION
Synthesis of S. platensis algae as nano-material using organic
solvents was carried out and tested for its antibacterial activity against
pathogenic bacteria. It was clear that Na-citrate extract showed maximum
zone of inhibition against all the bacterial while hexane extract of S.
platensis showed minimum inhibition zone against bacterial pathogens.
Nano material recorded the highest zone of inhibition against Yersinia
pestis (45mm) in comparison with organic solvent extract (Na-citrate)
against Staphylococcus aureus (20mm). S. platensis should be considered
as an economic antibacterial agent than using medical antimicrobials
against pathogenic bacteria. Other Future prospects of this research
would be large scale production of AgNPs using S. platensis and at
different concentrations in order to explore more benefits of S. platensis
as bio-antibacterial for pathogenic bacteria.
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الأنشطة الميکروبية لمسبيرولينا بلاتنيس کمضاد حيوي وکمادة نانونية لبعض
عزلات البکتيريا المسببة للأم ا رض
، أميمة عوض الله 1، نانيس علام 1، مختار يحيي 2 ، اسلام بقمولة 1
وجيه الشوني، محمد الشتيحي 1
1 قسم الأحياء الدقيقة وأم ا رض النبات ، کمية العموم ، جامعة طنطا
2 المعامل المرکزية لمرصد البيئي – المرکز القومي لبحوث المياة
تتمتع السبيرولينا مثل العديد من أنواع البکتيريا الزرقاء الأخرى بالقدرة عمى إنتاج عدد
کبير من المواد المضادة لمميکروبات وخاصة الممرضة منيا، لذلک فيي تعتبر کائنات حية
مناسبة تماماً للاستغلال کعوامل لممکافحة الحيوية لمبکتيريا المسببة للأم ا رض. في ىذه الد ا رسة ،
تم اختبار عدد من مستخمصات المذيبات العضوية المختمفة وخمطيا مع المواد المضادة من
الطحمب وکذا المواد النانوية المُصنعة من طحمب سبيرولينا بلاتنسيس ويرجع ذلک لنشاطيا
المضاد لمبکتيريا وخاصة ضد البکتيريا المسببة للأم ا رض. حيث تم استخدام طريقة انتشار البئر
القياسية لقياس الأنشطة المضادة لمبکتيريا من خلال تنمية الطحمب في أطباق مولمر ىينتون
أجار وتمت ز ا رعتو بم ا زرع الطحالب النقية من مسببات الأم ا رض البکتيرية في آجار مغذي عند
24 ساعة. - 37 درجة مئوية لمدة 18
تم جمع عدد عشر عينات مياه بمحاذاة مصرف عمر بک ومن فرع دمياط لنير النيل
خلال الخريف )سبتمبر 2116 ( ، ثم تم عزل عدة أنواع من البکتيريا الممرضة موجبة ج ا رم
وسالبة ج ا رم. ظيرت نتيجة مستخمص سيت ا رت الصوديوم أقصى منطقة من التثبيط ضد کل
أنواع البکتيريا الممرضة. في حين أظير مستخمص اليکسان من سبيرولينا بلاتنسيس الحد
الأدنى من منطقة التثبيط ضد مسببات الأم ا رض البکتيرية وذلک عند مقارنتيا بمستخمصات
المذيبات العضوية الأخرى. سجمت مادة النانو المُصنعة من الطحمب أعمى منطقة تثبيط ضد
اليرسينيا الطاعونية ) 45 مم( مقارنة مع ست ا رت الصوديوم ضد المکو ا رت العنقودية الذىبية ) 21
مم( کمستخمص مذيب عضوي. ينبغي الأخذ في الاعتبار أن سبيرولينا بلاتنسيس يعتبر بمثابة
مضاداً اقتصاديًا لمبکتيريا بدلاً من استخدام مضادات الميکروبات الطبية ضد البکتيريا المسببة
للأم ا رض.
33 Egypt. J. of Appl. Sci., 36 (5-6) 2021