Antimicrobial activity of some Macrophytes from Lake Manzalah (Egypt)
The antimicrobial activities of aqueous and organic
solvents (chloroform, ethanol and methanol) extracts of four plants Ceratophyllum
demersum L., Eichhornia crassipes, Potamogeton crispus
and Potamogeton pectinatus were tested in vitro against
seventeen different microorganisms including Gram-positive and Gram-negative
bacteria and fungi. Nine of these identified organisms were obtained from
different sources, Bacillus subtilis 1020, Bacillus cereus
1080, Staphylococcus aureus, Erwinia carotovora NCPPB 312,
Candida albicans, Candida tropicalis, Aspergillus niger,
Fusarium oxysporum and Penicillium italicum. The other eight
organisms were isolated from Manzalah lake water and identified using
API 20E strip system (BioMereux). One hundred pathogenic bacterial isolates
representing eight genera were identified to species level. These organisms
are Escherichia coli (20%), Pseudomonas aeruginosa (16%),
Klebsiella pneumoniae (14%), Salmonella colerasuis (13%),
Shigella sp. (11%), Serratia liquefaciens (10%), Proteus
vulgaris (9%) and Brenneria nigrifluens (7%). The extracts
of all tested plants demonstrated antimicrobial activity against the used
organisms. The efficiency of the extracts varied with, solvent used in
the extraction as well as plant species and the part of plant used. The
aqueous extract appeared to be the highly effective extract against all
tested organisms especially Fusarium oxysporum causing inhibition
zone 48 ± 0.01 mm, Pseudomonas aeruginosa 59 ± 0.02
mm and Salmonella cholerasuis 55 ± 0.01 mm when using P.
crispus, P. pectinatus and C. demersum, respectively.
Ethanol extracts of C. demersum, P. crispus and E. crassipes
root showed antimicrobial activities against all tested organisms except
Aspergillus niger. At the same time the extract of P. pectinatus
had no effect also on Fusarum oxysparum and the extract of E.
crassipes leaves have no effect on Penicillium italicum. On
using chloroform extracts Esherichia coli, Aspergillus niger
and Penicillium italicum showed resistance. Comparing the effect
of different plants extracts C. demersum appeared to be the most
effective followed by P. pectinatus. Furthermore, the extracts
of E. crassipes leaves being more effective than that, of its roots.
Elemental analysis were also takes place in water and plant samples and
the results revealed the presence of Mn and Pb in higher concentration
in P. pectinatus (Mn 603 ± 4.243 ppm and Pb 44 ±
2.828 ppm), at the same time the highest values of Fe 1680 ± 2.2
ppm, Zn 31.5 ± 2.1 ppm and Cu 26.5 ± 2.1 ppm were recorded
for C. demersum. Comparing the two parts of E. crassipes
(leaves and roots), the roots have the highest values of all studied metals.
One of the most important factors of water pollution is the microbial
contamination; especially with pathogenic microorganisms. Enteric pathogens
are typically responsible for waterborne sickness (Karaboze et al.,
2003). Pathogens are a serious concern for managers of water resources,
because excessive amounts of faecal bacteria in sewage and urban run-off
have been known to indicate risk of pathogen-induced illnesses in humans
(Fleisher et al., 1998). The need for new antimicrobial agents
and strategies for their use in the treatment of serious Gram-positive
infections is evident (Menichetti, 2005). Furthermore, several species
of Gram-negative bacteria present in municipal wastewater are pathogenic.
Thus, identification of these pathogenic agents in water resources is
beneficial for controlling and prevention planning of the infectious diseases
Bacterial diseases results in major economic losses to fish and animals
production, moreover, it represents a potential hazard to human health.
Since the advert of antibiotics in the 1950s, bacteria and fungi have
been relied upon for sources of antimicrobial agents (Cowan, 1999). For
treatment of bacterial disease antibiotics are sometimes used. The misuse
of antibacterial agents increase the incidence of resistant strains. One
of the solutions to solve antibiotic resistant incident problem among
pathogenic bacteria is to develop new drug from natural sources such as
plant. Moreover, most antimicrobial agents have many side effects. However,
herbal therapy if effective serves both as synergistic and corrective
factors (Diab, 2002). Traditionally, plants are used as source of treatment
of diseases in different parts of the world (Cowan, 1999; Eisenberge et
al., 1993; Hostettmann et al., 2000; Stock Well, 1988).
The plant is widely used in Angola against diarrhea and dysentery, especially
amoebic dysentery. In Nigeria, extracts or exudates of the plant are used
as ear drops and in the treatment of boils, sore and promoting wound healing
(Igoli et al., 2005).
Interest in plants with antimicrobial properties has revived as a result
of current problems associated with the use of antibiotics (Shiota et
al., 2004; Abu-Shanab et al., 2004). The plant compounds were
used to treat infections in age-old practice in a large part of the world,
especially in developing countries, where there is dependence on traditional
medicine for a verity of diseases (Gangoue-Pieboji et al., 2006;
Shiba et al., 2005). Plants remain a common source of antimicrobial
agents which is reported to have minimal side effects (Biobitha et
al., 2002; Maghrani et al., 2005).
The aesthetic, medical and antimicrobial properties of aqueous plants
extracts have been known since ancient times. The extracts of several
wild and medicinal plants have been tested against some bacterial and
fungal growth and for antimicrobial properties (Bilgrami et al.,
1980; Arora and Ohlan, 1997; Shatter, 2001; Diab, 2002; El Anezy et
al., 2006; Erdeny, 2006; Khalil, 2006; Qadir and Hoshyar, 2006). Few
studies were reported on the effect of macrophytes extracts on growth
of some bacterial and fungal organisms (Abd-Alla et al., 2001;
Ballesteros et al.,1992; Bushmann and Stephen, 2006; Haroon, 2006).
Lake Manzalah is the largest Egyptian, costal deltaic lake in Egypt.
It is situated at the Northeast quadrant of the Nile Delta, along Southeastern
Mediterranean coast between Damietta branch of the River Nile and the
Suez Canal. It serves five provinces namely; Damietta, port-said, Ismailia,
Sharkiya and Dakahliy (Zahran and Willis, 1992). This lake is often inhabited
by mixed stands of aquatic plants, some of these plants were selected
for this study. Ceratophyllum demersum L. (family Ceratophyllaceae),
Eichhornia crassipes (family Potederiaceae), Potamogeton crispus
and Potamogeton pectinatus (family Potamogetonacea). Morphologically,
these plants were briefly described by Tackholm (1974), Migahid (1978)
and Pandey (1982).
The present investigation aimed to study the effects of some extracts
obtained from these four macrophytes using different solvent, as well
as its dry powdered samples on growth of some strains of pathogenic bacteria
MATERIALS AND METHODS
Source of plant materials: The macrophytes used in this investigation
were collected during June 2005 from two stations situated at the southern
coast of lake Manzalah (Fig. 1) namely:
El-Raswa: From this place Ceratophyllum demersum L., Potamogeton
pectinatus L. and Potamogeton crispus L. were collected.
El-Shiboh: From this place samples of Eichhornia crassips were
The collected samples washed with tap water, left to dry in shade to
constant weight. Samples of Eichhornia crassips were separated
into leaves and roots where the analysis takes place in each part separately.
For the rest of plants the analysis takes place in the whole plant because
these plants have no true roots and the absorption of elements takes place
through the whole plant. The dry samples were ground to fine powder and
preserved in well stopper sample vessels.
Water analysis: Water samples at a depth of 5-20 cm was taken
from each stand dominated by the studied hydrophytes. Water pH was determined
using a combined pH meter digital (Model 5986). Total alkalinity was determined
according to Welch (1952). Determination of Na+, K+ and
Ca++ in water samples was carried out using a Corning 410 flame
photometer. Microelements were determined by Flame Atomic Absorption Spectrophotometry
(Pertkin Elmer 2100 Flam Atomic Absorption Spectrophotometer with an Autosampler,
Plant analysis: For determination of metals, dried plant tissue
was digested at 80°C for 2 h, using nitric acid (Allen, 1989). Metals
were determined by Flam Atomic Absorption Spectrophotometry (Pertkin Elmer
2100 Flam Atomic Absorption Spectrophotometer with an Autosampler).
|| Map of Manzalah Lake with points of samples collection,
Preparation of plant extracts: The powdered plants samples were
subjected to extraction using different organic solvents (methanol, ethanol
and chloroform) in addition to water according to the method described
by Saber (1976) and Alghalibi (2004). Twenty grams of each plant materials
were soaked in 200 mL solvent (80%), shaken for about 90 min and left
in the laboratory in a sealed container for 24 h. The above steps was
repeated daily throughout five successive days, thereafter the extract
was filtered through Whatman No. 1 filter paper and concentrated under
vacuum at 4°C in a Rota-vapor apparatus to dryness. The residues were
dried to constant weights and kept in a vacuum desiccator for further
Antagonistic organisms: Seventeen different microorganisms
including Gram-positive and Gram-negative bacteria and fungi were used
in this study as indicator organisms. Out of these organisms 9 identified
isolates were obtained from different sources and the other isolated from
Manzlah water samples.
Identified bacteria: Bacillus subtilis 1020, Bacillus
cereus 1080 and Staphylococcus aureus obtained from the culture
collection of the Microbiological Resource Center (MIRCEN), Faculty of
Agriculture, Ain Shams University, Resource, Cairo, Egypt), Erwinia
carotovora NCPPB 312 was kindly provided by Professor Essam Azab.
Candida albicans, Candida tropicalis, Aspergillus niger
and Fusarium oxysporum were kindly provided by Professor Yhya Abd
El-Gleel Mahmood. Penicillium italicum was isolated from disease
of Cirtus sinensis fruits and identified by Azab et al.
Unidentified bacteria: The unidentified bacteria were isolated
from Manzlah water samples.
Isolation and purification of Gram-negative bacteria: Isolation
of Gram-negative bacteria in Lake Manzala water samples were performed
using MacConkey agar supplemented with 0.001 g L-1 crystal
violet (cited in Rabeh and Azab, 2006). One hundred isolates were purified,
screened and the suspected similar ones were grouped for the purpose of
selection and identification processes.
Identification of some Gram-negative pathogens: One hundred isolates
from the examined water samples were subjected to identification by biochemical
characteristics using API 20E strip system (BioMereux). Each API 20E strip
consists of twenty wells containing dehydrated media. The isolate to be
tested was suspended in sterile saline and added to each well. The inoculated
strip was incubated for 16-24 h and the color reactions were noted either
positive or negative.
Inocula preparation: Overnight cultures of the bacterial indicators
were prepared in culture broth and diluted to 1x106 cfu mL-1
while the fungi were grown in PDA and there spore suspension of 5x105
spore mL-1 were prepared and served as inocula.
Antimicrobial assay: The antibacterial activities of the macrophytes
aqueous and organic solvent extracts were determined by paper disc method
described by Dulger (2005). The dried plant extracts were dissolved in
there solvents and sterilized paper discs having a diameter 6 mm (Whatman
No. 1) were impregnated with 40 μL of each extract (130 mg mL-1)
and placed on the surface of previously inoculated petri dishes. Nutrient
agar plates were prepared and 100 μL of 1x106 cfu mL-1
was spread on the surface. The inoculated plates were kept at 4°C
for 2 h and incubated at the suitable temperature (Bacillus subtilis
1020 and Bacillus cereus 1080 at 30°C and the other bacteria
at 37°C) for 24 h. At the end of incubation period, the appearance
of inhibition zones were considered positive results. The antifungal activities
of the studied plant extracts were measured using the well technique described
by Holmalahti et al. (1994). Wells (6 mm diameter) were punched
in the previously inoculated Potato Dextrose Agar (PDA) plates with 50
μL of 5x105 spores mL-1 of each fungus, using
a sterilized cork-borer. One hundred microliter aliquots (300 mg mL-1)
of each sterilized extract inserted into the wells and the plates were
incubated at 30°C for 3 days and the antifungal activities were evaluated
by measuring inhibition zone diameters. This experiment was performed
Table 1 showed the biochemical characteristics of pathogenic
Gram-negative bacteria isolated from Lake Manzalah water. The isolates
of genus 1 were differentiated and confirmed by API 20E as E. coli.
It is the main indicator of faecal pollution, constitute 20% of the identified
Gram-negative bacteria in the examined water. This also indicated that
the water of Lake Manzala is subjected to sewage pollution. Based on morphological
and API 20E biochemical reactions, the members of genus 2 are identified
as Pseudomonas aeruginosa which is an opportunistic pathogen of
humans. In contrast to most enterobacteria, this pathogenic bacterium
is the most significant example of bacteria capable of multiplying in
water. Thus, P. aeruginosa is common (16%) in the tested water
of Lake Manzala.
|| API 20E biochemical characteristics of pathogenic Gram-negative
bacteria isolated from Lake Manzalah water
|According to the biochemical reactions of API 20E eight
G-negative bacteria were identified as follows: E. coli (1)
Pseudomonas aeruginosa (2), Klebsiella pneumoniae (3),
Salmonella cloerasuis (4), Shigella sp. (5),
Serratia liquefaciens (6), Proteus vulgaris (7) and Brenneria
nitrifluens (8).+: Positve, -: Negative
|| Mean values ± SD of water characteristics expressed
as ppm of the two stations from which plants were collected
|| Mean values ± SD of macro and microelements
expressed as % of dry wt. and ppm in the studied plants
The isolates of genus 3 were identified as Klebsiella pneumoniae
according to morphological and biochemical characteristics. Klebsiella
pneumoniae represented 14% of the identified gram-negative bacteria
isolated from Lake Manzala. This pathogenic bacterium has been previously
isolated from surface water (Podschun et al., 2001). The species
of Genus 4 was classified as Salmonella cholerasuis because of
its biochemical characteristics, such pathogenic bacterium constituted
13% of Gram-negative bacteria from the examined water.
On the other hand, isolates of genus 5 were identified as Shigella
sp. and represented 11% of the identified Gram-negative bacteria.
Isolates of genus 6 were identified as Serratia liquefaciens and
represented 10% of Gram-negative bacteria isolated from the tested water
samples. This bacterium is considered a pathogen of fish (McIntosh and
Austin, 1990). Genus 7 (9%) and genus 8 (7%) of Gram-negative bacteria
which were identified as Proteu vulgaris and Brenneria nigrifluens.
Different values of water characteristics were recorded for the stations
of samples collection, with the highest values except Ca++
content and pH value for samples from El-Raswa. The pH values lies in
the alkaline side and ranged from 9.0 at El-Raswa to 9.4 ± 0.141
at El-Shiboh. The values of TSS fluctuated between 1752 ± 1.83
and 1714 ± 1.83 ppm and the water temperature ranged from 29 to
30°C for the two stations, respectively. Low values of micro-elements
were recorded for the two stations (Table 2).
As shown in Table 3 different concentrations of all
studied metals ( Ca, Na, Mg, Fe, Zn, Mn, Cu and Pb) were found in the
different plants as well as in different parts of the same plant. The
submerged macrophyte P. pectinatus has the highest values of Mn
603 ± 4.243 ppm and Pb 44 ± 2.828 ppm followed by P.
crispus (Mn 405 ± 7.07 ppm and Pb 31.5 ± 2.121 ppm),
while the highest values of Zn 234 ± 2.828 ppm and Cu 85 ±
1.414 ppm were recorded for E. crassipes roots.
The free floating plant E. crassipes shows different concentrations
of various elements within its tissues and the highest values were recorded
for its roots.
The antimicrobial activities of C. demersum, P. pectinatus,
P. crispus and E. crassipes (leaves and roots) against previously
isolated strains of bacteria and fungi were investigated. The results
are shown in Table 4-7. As presented
in this study, the extracts of all selected plants displayed some kind
of activity on the tested organisms. The aqueous extract appeared to be
the most effective extract but, being more effective on fungal growth
especially (Aspergillus niger and Fusarum oxysparum) causing
inhibition growth zone ranged from 53 ± 0.02 mm with C. demersum
to 48 ± 0.01 with P. crispus extract.
|| The antimicrobial activities of aqueous, chloroform,
ethanol and methanol extracts of Ceratophyllum demersum
|| The antimicrobial activities of aqueous, ethanol and
methanol extracts of Eichhornia crassipes (leaves and roots)
Regarding to the efficiency of organic solvents used in extracting antimicrobial
substances from the used plants, ethanol and methanol were nearly similar
except in few cases, where, ethanol extracts appeared to be active against
all tested organisms except Aspergillus niger and Fusarum oxysparum
in case of Potamogeton pectinatus, Aspergillus niger using
the extracts of Ceratophyllum demersum, Potamogeton crispus
and Eichhornia crassipes roots, while the extract of E. crassipes
leaves appeared to have no effect also on Penicillium italicum.
Chloroform extract of all tested plants seemed to have no effect against
Escherichia coli, Aspergillus niger and Penicillium italicum.
Aqueous extract of C. demersum exhibited antimicrobial effects
against all tested organisms and being the highly effective extract against
Salmonella cholerasuis and Aspergillus niger causing inhibition
growth zone (55 ± 0.01 and 53 ± 0.02 mm, respectively).
At the same time on using methanol and ethanol extracts Aspergillus
niger showed resistance while, the inhibition growth zone of Salmonella
cholerasuis ranged from 13 ± 0.0 to 16 ± 0.0 mm, respectively
The results in Table 5 showed that the aqueous extract
of E. crassipes (leaves and roots) were effective against all tested
organisms and the leaves extract seem to be the highly effective especially
against Aspergillus niger and Fusarium oxysporum causing
inhibition zones ranged from 47 ± 0.01 to 44 ± 0.01 mm,
respectively. At the same time methanol extract was the highly effective
against Bacillus subtilis 1020 and Bacillus cereus 1080
causing inhibition zone 47 ± 0.02 and 47 ± 0.01 mm for the
two species, respectively. In contrast to this the ethanol extract of
roots was highly effective than that of leaves against these two bacterial
|| The antimicrobial activities of aqueous, chloroform,
ethanol and methanol extracts of Potamogeton crispus
|| The antimicrobial activities of aqueous, chloroform,
ethanol and methanol extracts of Potamogeton pectinatus
The results in Table 6 and 7 showed
that, the aqueous extract of P. crispus was highly effective extract
against Fusarium oxysporum causing inhibition zone 48 ±
0.01 mm while the extract of P. pectinatus was the highly effective
extract against the pathogenic bacteria Pseudomonas aeruginosa
(59 ± 0.02 mm) and Klebsiella pneumoniae (48 ± 0.01
mm). At the same time the methanol extract of P. pectinatus was
also recorded as the most effective extract against Pseudomonas aeruginosa
and Klebsiella pneumoniae.
According to the previously mentioned results, all tested plant materials
used had an variable inhibitory effect on growth of the tested microorganisms.
The distribution of antimicrobial substances which varied from species
to species lead to the variation of antimicrobial activity (Lustigman
and Brown, 1991). The effect of aqueous extract followed by ethanol extract
appeared to be the most effective extract on most tested Gram positive
and Gram negative bacteria. Adomi (2006) reported that the water and ethanol
extracts of the stem bark of some medicinal plants were tested on Gram
positive and Gram negative bacteria, where the aqueous extract was active
while the ethanol extract was not active. The efficiency of the solvent
used in the extraction varied with the plant material, where Potamogeton
pectinatus and Potamogeton crispus appeared to be the most
effective followed by Ceratophyllum demersum and E. crassipes.
As recorded by El-Habibi et al. (1992) and Haroon (2006) the phytochemical
screening of the tested plants (Table 8), revealed the
presence of some important and active substances (tannins, flavonoids,
saponins, alkaloids, terpenes and glycosides) but with a few exceptions,
where, C. demersum was characterized by the presence of all these
substances while tannins were absent from E. crassipes, saponins
were not detected in E. crassipes and terpenes were not found
in P. pectinatus.
||A preliminary phytochmical screening of Ceratophyllum
demersum, Eichhornia crassipes (roots and leaves), Potamogeton
crispus and Potamogeton pectinatus
The presence of the active substances mentioned above in the extracts
of the studied plants caused the inhibiting effect on growth of the tested
organisms. This effect was affected by the concentrations of these active
substances in the plant extract. This could be explain the greatest effect
of P. pectinatus extracts upon the tested organisms, where, it
is extracts contained the highest amount of the active substances among
all tested plants.
The results also showed that, the effect of extract were not only depend
on the type of solvent and plant species used, but was also depend on
the part of plant used, where, the extracts of E. crassipes leaves
being more effective than that, of its roots. Although roots have higher
concentrations of heavy metals compared to the leaves it is antimicrobial
effect is less and this means, that the antimicrobial activity is more
affected by the presence of active substances which present in leaves
in high amount compared by it in roots.
As recorded by Harding (1981), Kantrud (1990), Ali et al. (1999)
and Serag et al. (1999), P. pectinatus was found in abundance
at highly polluted sites, C. demersum and E. crassipes were
characterized by its high level of heavy metals, this may be another reason
describing the antimicrobial activity of these extracts. The effect of
various elements on antimicrobial activity of the extracts could be observed,
where, P. pectinatus was characterized by its high lead content
and the highly effected compared with the rest of other extracts.
The powdered samples of all investigated plants gave negative results,
which coming in agreement with who mentioned that, the negative results
recorded by Azzouz and Bullerman (1982) for the effect of powdered Pomegranate
peel on growth of A. flavus or A. parasiticus may be due
to that, the powdered crude material contains ferrous ion, which bind
with the active substances (tannins and flavonoids) and inhibit its effect
on the cytochrome while, the extracts are characterized by the presence
of these substances in free form.
The water of Lake Manzala is subjected to fecal pollution and monitoring
of microbial quality of water is a must to control the spreading of pathogens
transmitted by contaminated water.
The study confirms that all plants extracts used in this investigation
possess in vitro antibacterial and antifungal activity against
the used organisms. At the same time the powdered plants samples had no
The efficiency of the extracts varied with, solvent used in the extraction
as well as, plant species and the part of plant used. The aqueous extracts
appeared to be the most effective extracts against all tested organisms.
So, it could be conclude to use it for food preservation or medicinal
purposes after some experiments for safety and toxicity.
Comparing the effect of different plants extracts C. demersum
appeared to be the most effective followed by P. pectinatus. Furthermore,
the extracts of E. crassipes leaves being more effective than that,
of its roots.
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