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The Antibiotic Principle of Seeds of Moringa oleifera and Moringa stenopetala

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Abstract

4(α-L-Rhamnosyloxy)benzyl isothiocyanate was identified as an active antimicrobial agent form seeds of Moringa oleifera and M. stenopetala. Roots of M. oleifera only contain this compound and benzyl isothiocyanate, but not pterygospermin as previously suggested. Defatted and shell free seeds of both species contain about 8-10% of 4(α-L-rhamnosyloxy)benzyl isothiocyanate, but this amount is produced from M. oleifera only when asorbic acid is added during water extraction. The compound acts on several bacteria and fungi. The minimal bactericidal concentration in vitro is 40 µmol/l for Mycobacterium phlei and 56 µmol/l for Bacillus subtilis.
1981, Vol. 42, pp. 55—61, © Hippokrates Verlag GmbH Plmta Jotrnot
Ud Reseth
The Antibiotic Principle of Seeds
of Moringa oleifera and Moringa stenopetala1
U. Eilert, B. Wolters and A. Nahrstedt
Institut für Pharmazeutische Biologie der Technischen Universität, Braunschweig,
Federal Republic of Germany
Key Word Index: Moringa oleifera; Moringa stenopetala; Moringaceae; Antimicro-
bial Activity; Mustard Oil; 4 (a-L-rhamnosyloxy)benzyl isothiocyanate.
Abstract Introduction
4(a-L-Rhamnosyloxy)benzyl isothio-
cyanate was identified as an active anti-
microbial agent form seeds of Moringa
oleifera and M. stenopetala. Roots of M.
oleifera only contain this compound and
benzyl isothiocyanate, but not pterygo-
spermin as previously suggested. Defat-
ted and shell free seeds of both species
contain about 8—10 % of 4(u-L-rhamno-
syloxy)benzyl isothiocyanate, but this
amount is produced from M. oleifera on-
ly when asorbic acid is added during wa-
ter extraction. The compound acts on se-
veral bacteria and fungi. The minimal
bactericidal concentration in vitro is 40
tmol/1 for Mycobacterium phlei and 56
tmol/l for Bacillus subtilis.
Part of the projected dissertation of U. Ei-
LERT, also presented as a poster during the Intern.
Res. Congress on Natural Products as Medicinal
Agents, Strasbourg, July 1980 [Planta Medica, 39,
235 (1980)]
Moringa oleifera LAM. andM. stenope-
tala (Bak. f.) Cufod. are native to tropi-
cal Africa and the former is also found in
India, Ceylon and Madagascar. Leaves,
roots and seeds are often used in folk me-
dicine [1]. In rural areas of the Sudan in
particular, the powdered seeds of M.
oleifera are traditionally utilized for wa-
ter purification because of their strong
coagulating properties for sedimentation
of suspended mud and turbidity [1, 2].
During some coagulation experiments a
slight decrease of total bacterial count of
the purified water was observed [2] indi-
cating that the seeds might contain sub-
stances with antimicrobial activity. In-
deed, from roots of M. oleifera (syn. M.
pterygosperma GAERTN.) an antibiotic
substance has been isolated and a surpri-
sing structure (1) was proposed [3, 4].
The present paper describes purification,
elucidation and antimicrobial properties
of the antibiotic principle of seeds of M.
oleifera and M. stenopetala and reinvesti-
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56 ElIert, Wolters, Nahrstedt
gates the antibiotic substance of roots of Results and Discussion
M. oleifera using its antimicrobial activi-
ty for detection [5, 6]. This substance is
an isothiocyanate, already known from
these plants, but which has never been
tested for its antimicrobial activity.
TableI
Bacteria
Bacillus cereus var. rnycoides
Bacillus rnegaterium
Bacillus subtilis 1527
Bacillus subtilis Na
Escherichia coli (gram neg.)
Kiebsiella aerogenes (gram neg.)
Micrococcus aureus (Staphylococcus)
Micrococcus luteus (Sarcina)
Proteus mirabilis (gram neg.)
Salrrionella edinburg (gram neg.)
Serratia marcescens 1534 (gram neg.)
Serratia marcescens Na (gram neg.)
Streptococcus faecalis
Mycobacterium phlei Na
Mycobacterium phlei Wo
FungiAspergillus oryzae
Botr-ytis allii
Candida pseudotropicalis
Candida reukaufli
Coniophora cerebella
Fusarium oxysporum, f. lycopersici
Penicillium expansum
Phytophthora cactorum
Piricularia oryzae
Polystictus versicolor (Polyporus)
Saccharornyces carisbergensis
Zygorrhynchus sp.
Preliminary investigations of aqueous
1:10 extracts of the seeds from M. oleife-
ra and M. stenopetala indicated distinct
antimicrobial effects which are listed in
Antibiotic activity of an aqueous extract (1:10) from seeds of Moringa oleifera tested in the petri plate diffu-
sion assay using the streak-plate method, the cup-test, and the disk-test
(+) = inhibitionzone 1— 2 mm ssaprophytic
+= inhibitionzone 2— 5 mm h = humanpathogen
++ = inhibitionzone 5—10 mm p = phytopathogen
=inhibitionzone 10—15mm s1 = wood decaying fungus
Organism Host
Substrate Inhibition
S
S
S
S5, HS,(H)
HS5, HHS,(H)
S, (H)
S, Hpp
SpS, HS
SIP. (H)
SpP
SISS
++++++
++++
+++++++++(+)(+)+++++
+++++++++++++++++++++
(+)(+)
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Antibiotic Principle of Moringa
table I. The active component was not
extractable with MeOH or EtOH and
seeds boiled for a short time in water
showed greatly decreased activity. Water
extracts from germinated seeds exhibited
a minor activity, whereas extracts from
seed shells were completely inactive.
The active principle was extracted
from defatted seeds by incubation of the
seed powder in water and purified by ex-
traction of the water phase with EtOAc,
column chromatography on silica gel and
HPLC on RP-18. During all steps the
presence of the antimicrobial was moni-
tored by TLC using its antimicrobial ac-
tivity as an indicator [5, 6]. These tests
showed one active substance to be pre-
sent in seeds of both species with an
identical Rf value. This substance was
isolated from the HPLC eluate as a white
crystalline product, m.p. 740 C (substan-
ce A). In the roots of M. oleifera in addi-
tion a second minor active zone was de-
tected with a greater Rf value (substance
B). There was no indication of further
antibiotic substances in the roots.
Substance A showed a M of m/e 311
in the MS and contained sulphur as well
as nitrogen. ?ax in the UV spectrum was
221 (H20) and no bathochromic shift
was observed upon addition of alkali.
The JR spectrum showed a strong and
broad absorption at 2160 cm' and 2080
cm' indicating a N=C=S grouping.
Acidic hydrolysis yielded rhamnose as
the only sugar component. The 'H-
NMR in acetonitrile-d3 exhibited a mul-
tiplet characteristic of a para disubstitu-
ted benzene (7.0—7.5 ppm, 4H), a singlet
of an isolated CH2 group (4.7 ppm, 2H),
multiplets in the sugar region between
3.2 and 4 ppm, a doublet of the anomeric
rhamnose proton (5.5 ppm, 1H, J = 2
Hz) whose shift indicates the a-configu-
ration at C1 [7] and a doublet of the CH3
of the rhamnose (1.2 ppm, 3H, J = 6
Hz). The spectrum is consistent with
4(a-L-rhamnosyloxy)benzyl isothiocy-
anate (2) which has already been isolated
by BADGETr [8] from seeds of M. oleifera
and by KJAER et al. from myrosinase trea-
ted seed extracts of M. peregrina [9]. A
proton noise-decoupled 13C-NMR was
completely compatible with structure 2
and the a-configuration of the sugar was
indicated by the JC1H1 value of 165 2
Hz [7] and the chemical shifts of C-3'
(71.37 ppm) and C-5 (70.01 ppm),
which are shifted to higher field when
compared to 13-rhamnosides [7]. Thus,
the antimicrobial substance of water in-
cubated seeds of M. olesfera and M. sten-
opetala, as well as roots of M. oleifera
has structure 2.
Substance B was isolated by preparati-
ve TLC from water incubated root pow-
der of M. oleifera. The substance had an
identical R1 value with benzyl isothiocy-
anate (TLC, GLC) and an identical 1H-
NMR in CDCI3. Thus, the second com-
pound with antimicrobial activity from
roots of M. oleifera has structure 3.
Table II shows the results of the quan-
titative estimation of 2 and 3 by GLC.
When incubated in water M. stenopetala
seeds released more than twofold the
amount of 2 compared to M. oleifera
seeds, but when incubated with buffer at
pH 6.8, together with a small amount of
ascorbic acid [10] the content of 2 from
M. oleifera increased to give a similar
amount to that of M. stenopetala.
The antimicrobial activity of pure 2
was tested against three species of bacte-
ria and compared to 3: Bacillus subtilis
(gram +), Serratia inarcescens (gram —),
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58 ElIert, Wolters, Nahrstedt
Table II
1J.-CH2—N_0 O—N—CH2--ej.
s—_k'J_ -s
or
(j-CH2-N-Q_ r20
s—c—o 0—c—s
23
CH3 I
Ho7OH
CH2—N—C5
1 f3,LJ
2
3
Contents of 2 and 3 in the defatted seeds without shells of M. oleifera and M. stenopetala and roots of M.
oleif era as obtained by GLC using water, as well as phosphate buffer pH 6.8 with 0.1 % ascorbic acid, for
incubation.
Seed shells are about 20—25 % of the whole seed; whole seeds contain 26—28 % of extractable lipids.
Incubated with
M. oleifera M. stenopetaa
seeds roots seeds
232323
H,O 3.6 % 0.08 % 0.04 % 9.2 %
bufferpH6.8,0.1 %vit.C 8.9% 8.5%
and Mycobacterium phici. The results are
presented in table III. In the range of
concentration used, B. subtilis was com-
pletely inhibited by 56 Jkmol/l of 2 and 90
Rmol/l of 3 and M. phlei by 40 .tmol/l of
2 and 42 i.tmolJl of 3. These values are the
minimal bactericidal concentrations as
proved by plating.
Both substances only partially inhibi-
ted S. marcescens in the range of concen-
trations used. These results indicate that
the antimicrobial properties of 4 (a-L-
rhamnosyloxy) benzyl isothiocyanate,
which at present is the only known gly-
cosidic mustard oil, are similar to or even
better than the medicinally utilized benz-
yl isothiocyanate [11], which is the most
active isothiocyanate of about 250 tested
by KRI5TIAN et al. [13]. As 2 is a solid that
is readily soluble in water ("-'1.3 mmol/l)
and is non volatile, it appears to be a
good substitute for 3 which is a volatile
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>
0
C)
-ci
C)
CD
0
0
-'
(a
Table III
Results from a dilution tube test with 4 (a-L-rhamnosyloxy)
benzyl isothiocyanate (2) and benzyl isothiocyanate (3).
Bacillus subtilis Mycobacteriwn phlei Serratia marcescens
2 3 2 3 2 3
smo1/l ag/ml smol/l sg/ml amol/l ag/mi amo1/l ag/ml amol/l ag/ml amo1/l ag/ml
minimum bactericidal
concentration 56 17.5 90 13.5 40 12.5 42 6.5
minimum bacterio-
static concentration 40 12.5 67 10 40 12.5 42 6.5 —L
50 % inhibition 30
10 % inhibition 4
= final concentration 537 tmol/1
= maximal solubility
of 3: 90 amol/l.
9.5 35 5 25 7.8 16 2.5 80 25 42 6.5
1.5 <3 0.5 3 1.5 10 1.5 30 9.3
(7i
(0
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60 Eilert, Wolters, Nahrstedt
liquid of poor water solubility and acts as
a skin irritant. Table II shows that seeds
of both M. oletfera and M. stenopetala
are good sources of 2, containing up to
about 8—10 % in the defatted shell free
seeds. However, in our seed material the
myrosinase activity in seeds of M. oletfe-
ra is not sufficient for liberation of all of
2 from the parent compound 4 (a-L-
rhamnosyloxy) benzyl glucosinolate
which was obtained as the heptaacetate
after acetylation of M. oleefera seed ex-
tracts by BADGETr [8]. It is known that vi-
tamin C acts as a coenzyme for special
glucosidases which hydrolyze glucosino-
lates [10]. Obviously a glucosidase of this
type completes the cleavage to 2 in M.
oleifera seeds after ascorbic acid has been
added.For water purification normally about
0.2 gIl of the powder made from entire
seeds is utilized and ascorbic acid ob-
viously is not present in these systems.
From these data a concentration of about
15—30 tmol/l of 2 is calculated, which is
on the borderline for a clear antimicro-
bial effect [2]. Applying the same amount
of seeds of M. stenopetala (which also are
very active as a coagulant, S. A. A. JAHN,
pers. comm.), these will be of more value
during water purification as they will al-
so have an effect against any microorga-
nisms in the water.
The results from roots of M. oleifera
indicate 2 and 3 as the only antimicrobial
substances in this part of the plant. No
evidence for pterygospermine (1) was
obtained, at least in the material origina-
ting from the Sudan. In view of the sur-
prising structure 1 and the data from this
paper the present authors assume 1 to be
an artifact of isolation or structural eluci-
dation.
Experimental
Plant material
The air dried plant material was kindly provided
by Dr. S. A. A, JAHN (Khartoum, Sudan). The
seeds were defatted by extraction with petrol. Incu-
bation of the defatted or undefatted seeds was car-
ried out with 10 parts of water normally for two
hours and the filtrate was taken for antimicrobial
tests.
Isolation
For isolation the water phase was extracted with
EtOAc and the concentrated EtOAc solution was
chromatographed on silica gel (3 x 60 cm) with
EtOAc/MeOH/H20 95:4:1. The active principle
was detected by TLC methods [5, 6] in the range
520—900 ml. This fraction was further purified by
HPLC on Lichrosorb RP-18 (0.8 x 25 cm) using
CH3CN/H20/MeOH 40:53:7 as the eluent (1.3
mi/mm, detection at 240 nm, tR = 12 mm). During
concentration of the trapped fractions substance A
was obtained as white crystals, m.p. 74°C recorded
by differential thermo analysis. Another isolation
procedure was carried out by chromatography of
the EtOAc extract on preparative TLC with Me-
OH/HCO2Et 10:90. The same solvent was used
for monitoring the antibiotic activity by TLC [5,
6]. In this system substance A shows an R1 of 0.4;
extracts of roots additionally show an active zone at
R1 0.7 (substance B) which was collected by elution
of this zone with CH2 Cl2.
NMR-spectra
NMR-spectra were recorded on a Varian T 60
('H) and a Varian XL-100 ('3C). The proton spec-
trum is djscussed in Results. '3C-NMR: (a-range,
ppm): aromatic carbons at 157.14 (s, C-I), 117.51
(d, C-2), 129.27 (d, C-3), 129.0! (s, C-4); -CH2-:
48.53 (t); -N = C=5: 129.01 or possibly not ob-
served, broad; rhamnosyl residue: 99.11 (d, C-i ),
72.06 (d, C-2'), 71.37 (d, C-i'), 73.26 (d, C-4'),
70.01 (d, C-5), 18.00 (q, C-6'). The 'Jc,-u, value
was determined from the residual coupling in the
SFORD '3C-spectrum and H-I proton chemical
shift by the use of known procedures [14]. Alt-
hough this method is not as accurate as direct deter-
mination from a 'H coupled '3C-spectrum the va-
lue of 165 + 2 Hz is characteristic of the a sugar
configuration [7].
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Antibiotic Princip'e of Moringa 61
El-MSThe El-MS showed signals at m/e: 311 (8 %),
165 (39 %), 147 (90 %), 146 (100 %), 129 (32 %),
107 (94 %), 85 (83 %), 71(73 %) as published for
2 in [91.
Quantitative determination
For quantitative determination the defatted seed
powder or the pulverized root material (—1 g) was
incubated with 5 ml of water (in some experiments
with 2.5 ml of water, 2.5 ml of phosphate buffer
pH 6.8 containing 0.1 % ascorbic acid) for 12
hours and then kieselgur (Celite 545) and 10 ml
CH2CI2 were added. This wet powder was filled
into a small glass tube and eluted with 100 ml
CH2 Cl2. The CH2 Cl2 was removed carefully under
vacuum, dissolved in 0.2—0.5 ml pyridine and sily-
lated [12]. 100—200 i.tl of a standard solution (100
mg 1, 3, 5-triphenylbenzene in 10 ml Cd4) was ad-
ded and the supematant was used for GLC.
GLC-system: OV-10l, 2 % on Chromosorb
AW-DMCS, 80—100 mesh, 3 m X l/, glass; tem-
perature program: 17 mm isothermally at 90° C,
then 100 C/mm up to 235° C, 235° isothermally.
Detector: FID, 245° C; injector: 225° C; 25 mI/mm
nitrogen as carrier gas. tR of 3: 13 mm, tR of 2: 47
mm, tR of standard: 52 mm.
Both isothiocyanates were estimated against the
internal standard and the correction factor was
measured at 1.64 0.11 for 2 and 1.43 0.12 for
3. Nutrient media. for bacteria: beef extract
0.5 %, meat peptone 0.6 %, glucose 0.4 %, dou-
bly distilled water; pH 7.0 solid medium with 2 %
agar. For fungi: Löflunds malt extract 4 %, casein
peptone 0.5 %, doubly distilled water, agar 2 %;
pH 5.4.Growth conditions: bacteria 37° C; fungi 25° C.
Methods of antimicrobial assays: preliminary
tests: diffusion plate assays; dilution tube test: tur—
bidimetric method (instrument: Trubungsmesser
Dr. B. Lange, Berlin). Incubation time: 48 h. TLC-
stripe-test as described by WOLTERS [5, 6]; test or-
ganisms: Polystictus versicolor, Bacillus subtilis.
Acknowledgement
We are grateful to Dr. S. A. A. JAHN (Khar-
toum, Sudan) who kindly provided us with the
plant material and gave the impulse for this investi-
gation. Prof. Dr. R. NALVEKE (TU Braunschweig)
performed some of the antimicrobial tests, Dr. L.
Wirr (GBF, Braunschweig-Stockheim) recorded
the EI-MS, Dr. V. WRAY (GBF, Braunschweig-
Stöckheim) the NMR-spectra and Prof. Dr. H.
JUNGINGER (TU Braunschweig) the m.p. by DTA;
to all of whom we give our thanks. The linguistic
advice of Dr. V. WRAY is also appreciated.
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Water, the elixir of life, is becoming a scarce and expensive resource in the present era of unmindful exploitation of the resources. With current exploitation of groundwater resources and unchecked pollution on surface water resources, the emphasis is laid on the development of greener solutions for water treatment. With a wide spectrum of biodiversity, nature always offers greener solution for the water problems. One such aspect is the utilization of indigenous natural materials for water treatment. The usage of natural coagulants in water treatment may be primitive, but it is a sustainable solution with a specific scientific approach. The last few decades witnessed a plethora of research in natural coagulants in the treatment of both wastewater and drinking water. Scientific dissemination of the properties of the natural coagulant is utmost important. In light of these challenges, the review paper will collate the natural coagulants explored by the indigenous communities and the scientific fraternity. The review will also address the challenges and limitations with respect to the utilization of these materials in water treatment when compared to its chemical counterpart, viz. alum and ferric chloride. These plants with active coagulant ingredients also have the inherent potential of commercial utility as industrial crops. Large-scale application and commercialization of these natural coagulants would be possible only through continuous exploration of the process and chemistry of these natural coagulants.
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13C NMR spectra for a variety of α and β-anomeric series of d-mannopyranosides and l-rhamnopyranosides are presented and analyzed in comparison with those of D-glucopyranosides. The results obtained in the present study are valuable for the structure studies of plant-glycosides as well as carbohydrates, especially for determination of anomeric configurations of mannosides and rhamnosides which has been extremely difficult by other classical techniques.
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