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Aqueous and organic basidiocarp extracts of the edible mushroom Lactarius indigo were evaluated for their antibacterial and cytotoxic effects. 10, 20 and 30 mg of organic extracts were tested against diarrheagenic Escherichia coli strains (EIEC, EPEC, ETEC-LT and ETEC-ST), Pseudomonas aeruginosa, Enterobacter cloacae, Staphylococcus aureus and Salmonella enterica. 10 mg of hexane extract showed activity against ETEC-LT (18.8 mm zone of inhibition) and P. aeruginosa (10.5 mm). All levels of the ethyl acetate extract inhibited all the strains, with stronger activity against EIEC (19.0 mm) and P. aeruginosa (21.0 mm) at 30 mg. Methanol extract inhibited all bacterial growth, but E. cloacae. 100 µg/ml of aqueous extract showed antiproliferative activity against MCF7 cells, but not on HeLa, A549 and normal bovine mammary epithelium cells. Methanol and ethyl acetate extracts inhibited proliferation of HeLa cells (50 to 1000 ng/ml) but increased proliferation of A549 (100 ng/ml), as did methanol extract (500 ng/ml). Methanol extract did not inhibit normal rabbit serum fibroblast cells, while hexane and ethyl acetate extracts showed an inhibitory effect with 50 and 100 ng/ml, respectively, less than in proliferation of HeLa cells. These results show that L. indigo basidiocarps contain substances with antibacterial and cytotoxic activities.
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African Journal of Pharmacy and Pharmacology Vol. 5(2). pp. 281-288, February 2011
Available online
ISSN 1996-0816 ©2011 Academic Journals
Full Length Research Paper
Antibacterial and cytotoxic activity from basidiocarp
extracts of the edible mushroom Lactarius indigo
(Schw.) Fr. (Russulaceae)
Alejandra Ochoa-Zarzosa1, Ma. Soledad Vázquez-Garcidueñas2, Virginia A. Robinson-
Fuentes2 and Gerardo Vázquez-Marrufo1*
1Centro Multidisciplinario de Estudios en Biotecnología, Facultad de Medicina Veterinaria y Zootecnia.
2División de Estudios de Posgrado, Facultad de Ciencias Médicas y Biológicas “Dr. Ignacio Chávez”, Universidad
Michoacana de San Nicolás de Hidalgo, Morelia, Michoacán, México.
Accepted 18 February, 2011
Aqueous and organic basidiocarp extracts of the edible mushroom Lactarius indigo were evaluated for
their antibacterial and cytotoxic effects. 10, 20 and 30 mg of organic extracts were tested against
diarrheagenic Escherichia coli strains (EIEC, EPEC, ETEC-LT and ETEC-ST), Pseudomonas aeruginosa,
Enterobacter cloacae, Staphylococcus aureus and Salmonella enterica. 10 mg of hexane extract
showed activity against ETEC-LT (18.8 mm zone of inhibition) and P. aeruginosa (10.5 mm). All levels of
the ethyl acetate extract inhibited all the strains, with stronger activity against EIEC (19.0 mm) and P.
aeruginosa (21.0 mm) at 30 mg. Methanol extract inhibited all bacterial growth, but E. cloacae. 100 µg/ml
of aqueous extract showed antiproliferative activity against MCF7 cells, but not on HeLa, A549 and
normal bovine mammary epithelium cells. Methanol and ethyl acetate extracts inhibited proliferation of
HeLa cells (50 to 1000 ng/ml) but increased proliferation of A549 (100 ng/ml), as did methanol extract
(500 ng/ml). Methanol extract did not inhibit normal rabbit serum fibroblast cells, while hexane and ethyl
acetate extracts showed an inhibitory effect with 50 and 100 ng/ml, respectively, less than in
proliferation of HeLa cells. These results show that L. indigo basidiocarps contain substances with
antibacterial and cytotoxic activities.
Key words: Lactarius indigo extracts, antibacterial activity, cytotoxic activity.
Fungi from the division Basidiomycota have been widely
studied as an alternative source of metabolites with
pharmacological properties, including anticancerigenous,
antitumor, immunomodulating, antibacterial and cytotoxic
activities (Wasser, 2002; Daba and Ezeronye, 2003; Fan
et al., 2006; Borchers et al., 2008). Antibiotic resistance
of human pathogenic bacteria has become a major
worldwide public health concern (Finch, 2002; Harbarth
and Samore, 2005), this is why the search for new
substances with antimicrobial activity is a priority
(Livermore, 2005). Antimicrobial activity has already been
documented in extracts from the mycelium (Suay et al.,
2000) and fruiting bodies (Zjawioney, 2004) of differ-
*Corresponding author. E-mail:
mx. Tel/Fax: + 52 443 295 80 29.
rent wild species from Basidiomycota.
Another worldwide public health problem is cancer,
given that it is estimated that approximately 25 million
people suffer one of its different manifestations and 10
million new cases are annually reported (WHO, 2002); for
that reason, there is an increasing demand for more
effective anticancerigenous substances and therapies
(Lord and Ashworth, 2010). In that regard, several
studies have reported cytotoxic activity against cancer
cells of organic extracts of spores (Fukuzawa et al.,
2008), vegetative mycelium (Hu et al., 2002; Choi et al.,
2004) and basidiocarps (Takaku et al., 2001; Hu et al.,
2002) from several species of Basidiomycota. The genus
Lactarius (Russulaceae) includes species reported as
edible in different parts of the world (Boa, 2004) and
reports exist of the antimicrobial activity of methanol
extracts of Lactarius deterrimus, Lactarius sanguifluus,
Lactarius semisanguifluus, Lactarius piperatus, Lactarius
282 Afr. J. Pharm. Pharmacol.
deliciosus and Lactarius salmonicolor (Dulger et al.,
2002; Barros et al., 2007a, b). In addition, the organic
extracts of some Lactarius species have shown immuno-
modulating, cytotoxic, antiviral and antigenotoxic
activities (Krawczyk et al., 2003, 2005, 2006; Mlinaric et
al., 2004).
Lactarius indigo (Schw.) Fr. is an edible mushroom that
distributed from East Asia (China and Japan) (Wu and
Mueller, 1997) to Northeastern and Central America
(Hesler and Smith, 1979; Hutchinson, 1991; Mueller and
Halling, 1995; Montoya and Bandala, 1996; Wu and
Mueller, 1997). In México, L. indigo is associated to
diverse plant communities (Montoya and Bandala, 1996)
and is highly valued as food (Boa, 2004; Pérez et al.,
2006), being sold in local markets (Montoya et al., 2001;
Martínez-Carrera et al., 2005). It is known by the Spanish
common names indigo, hongo azul (blue mushroom) and
the combined Spanish-Nahuatl names tecax azul (blue
tecax) and tecosan morado (purple tecosan) (Montoya et
al., 2001, 2003).
A single report is known about the nutritional value of L.
indigo (León-Guzmán et al., 1997); however, there is not
a single report regarding the pharmacological properties
of this species. In the present work, the antibacterial and
cytotoxic activities of aqueous and organic extracts of L.
indigo are evaluated for the first time and the results are
compared with those from similar reports for other
species of Basidiomycota, mainly for the genus Lactarius.
Basidiocarp collection
Basidiocarps of L. indigo were collected in the Parque Nacional
Insurgente José María Morelos in the municipality of Charo, state of
Michoacán, México (19° 39.918’ N, 101° 00.450’ W) on September
2006, and were authenticated by M.Sc. Marlene Gómez Peralta,
curator of the herbarium of the Facultad de Biología, Universidad
Michoacana de San Nicolás de Hidalgo, where a voucher specimen
(KM03) was deposited. The basidiocarps were frozen at -80°C the
same day of collection and freeze-dried after 24 h. The freeze-dried
material was preserved in the dark at C in a container with silica
gel until processed.
Test microorganisms
Strains of Escherichia coli EPEC, ETEC, and EIEC pathotypes
used for the antibacterial activity assays were purchased from the
Institute of Diagnostic and Epidemic Reference of xico (InDRE,
Table 1). The Children’s Hospital Eva Sámano de López Mateos of
Morelia, Michoacán, Mexico, donated the tested strains of Pseudo-
monas aeruginosa, Enterobacter cloacae, and Salmonella enterica
subsp. enterica. The tested strain of Staphylococcus aureus was
Cell lines
Several cell lines corresponding to human cancers were used for
the cytotoxicity assays: HeLa (cervicouterine cancer), MCF7 (breast
cancer) and A549 (lung cancer). As controls for evaluating the
effect on normal cells, bovine mammary epithelial cells (BME) were
used for assays with aqueous extracts, and rabbit skin fibroblasts
(RSF) for assays with organic extracts. The latter two cell lines were
generated in our laboratory. All cell lines were kept in Dulbecco’s
modified Eagle’s medium (DMEM)-F12K (1:1, Sigma, USA)
supplemented with 30 mM NaHCO3, 15% fetal bovine serum
(Gibco, USA), 50 U/ml of penicillin and 50 U/ml of streptomycin
(Gibco, USA). Cells were cultured at 37°C in an atmosphere with
5% CO2 and 95% humidity.
Extract preparation
For obtaining the aqueous extract 100 g (dry weight) of basidiocarp
mass was boiled in 700 ml of deionized water for 60 min,
continuously replacing the evaporated water during the extraction
time. After extraction was completed the residual biomass was
eliminated by filtration through sterile gauze. The recovered filtrate
was lyophilized and resuspended in deionized water at a
concentration of 500 mg/ml. The resulting solution of aqueous
extract was sterilized by filtering through a 0.25 µm pore size
membrane (Millipore, USA) and stored at 4°C.
Organic extracts were prepared by crushing 50 g of freeze-dried
basidiocarp until a fine powder was obtained; the resulting material
was successively extracted with 100 ml of each hexane, ethyl
acetate, and methanol during 72 h. The extracts were later
centrifuged at 1500 x g at room temperature and filtered. The
solvents were eliminated by rotoevaporation until dryness and the
dry extracts were stored at 4°C. Solutions for the bioassays were
prepared by resuspending the dry extracts in the same solvent used
for the extraction at a concentration of 500 mg/ml.
Antimicrobial activity by disk diffusion method
The antimicrobial assays were performed in vitro using the agar-
disk diffusion method (National Committee for Clinical Laboratory
Standards, 1993). Petri dishes with Mueller-Hinton Agar (Oxoid,
USA) were inoculated massively with a 200 µl suspension of each
of the bacterial cultures and grown to their mid-log phase, after
which the plate’s surfaces were air-dried. Filter paper sensidisks (6
mm in diameter) were impregnated with the necessary volume of
each of the extracts in order to reach the final levels of 10, 20, and
30 mg/disk. The impregnated sensidisks were air-dried before being
placed on the Petri dishes with the test microorganisms. The plates
were incubated for 24 h at 3C and the inhibition areas were
measured in mm using a digital caliper (precision of 0.01 mm,
Model CD-6” C, Mitutoyo Corp., Japan). Controls consisted of
sensidisks impregnated with the corresponding pure solvent and
air-dried. The inhibition diameter of the control disk was subtracted
from the inhibition diameter resulting from the application of the
corresponding extracts of L. indigo. In some tests, control
sensidisks with ampicillin (AM) and carbenicillin (CB) (BioRad,
USA) were used (Table 1). All assays were performed in triplicate
and the results were reported as mean ± standard deviation (SD).
Cytotoxicity assays
For cytotoxicity assays four different concentrations were used of
the organic extracts and the same volume of the corresponding
solvent as a control. All tested cell lines were cultivated to
confluence as described above and were detached from the culture
plate using PBS saline solution at pH 7.4 supplemented with
antibiotics and 0.25% trypsin-EDTA (w/v, Sigma, USA) and agitated
for 10 min. Afterwards, 1 x 106 cells were seeded in OPTIMEM
(Gibco, USA) growth medium without serum or antibiotics in 96-well
microtitration plates. To these cultures the corresponding extract
was added incubating the treated plates during 24 to 48 h at 37°C.
After incubation, 10 µl of a 5 mg/ml solution of tetrazolium bromide
3-(4,5-dimetil-2-tiazol)-2,5-diphenil-2H-tetrazolium salt (MTT,
Sigma, USA) were added and further incubated for 4 h at 37°C.
Finally, 100 µl of 10% SDS were added in order to dissolve the
formazan crystals and the viability of cells was determined by
measuring the reduction of MTT at 595 nm in a microplate reader
(Bio-Rad, USA). Each assay was carried out at least in sextuplicate.
Statistical analysis
In order to evaluate the effect of the extract concentration on the
different studied strains and cell lines, the results were analyzed by
one-way analysis of variance (ANOVA) and Tukey tests (p<0.05),
using StatistiXL ver. 1.8.
Antibacterial activity
The controls showed that hexane alone did not cause
any inhibition to the tested strains whereas the ethyl
acetate and methanol caused a minimal inhibition that
was subtracted as described in Materials and Methods.
The hexane extract caused inhibition of P. aeruginosa
and ETEC-LT (Table 2). For the ETEC-LT strain, 10 and
20 mg of hexane extract did not show significant
differences in the inhibition zone diameter but 30 mg
caused a significantly larger inhibition zone diameter than
that for lower amounts. For P. aeruginosa, the maximum
inhibition was observed at 20 mg of hexane extract, since
no significant differences could be observed with 20 and
30 mg of the extract (Table 2). The compounds present in
the hexane extract had a greater effect on the ETEC-LT
strain than on P. aeruginosa. The inhibition caused by the
hexane extract is comparable with that caused by the
standard antibiotics AM and CB (Table 1).
The ethyl acetate extract inhibited all tested strains
(Table 2). In all strains, except for ETEC-LT and S.
enterica, an apparent dose-response effect could be
observed, since the inhibition increased in relation to the
applied level of ethyl acetate extract. No significant
differences could be observed in E. cloacae and S.
aureus when applying the two lower amounts of the
extract. At 10 mg of ethyl acetate extract, no differences
could be observed in the inhibition of any of the tested
microorganisms. However, at 20 and 30 mg of ethyl
acetate extract, significant differences were observed in
the inhibition of P. aeruginosa, EIEC, ETC-ST, and EPEC
(Table 2). At the highest level, all strains showed different
susceptibilities to the ethyl acetate extract, except for E.
cloacae and S. aureus. The inhibition of the different E.
coli pathotypes caused by 30 mg of the ethyl acetate
extract was comparable to that caused by AM and CB,
except for strain ETEC-LT (Table 1).
Zarzosa et al. 283
The methanol extract caused inhibition in all bacteria
tested. Only E. cloacae did not show susceptibility at 10
mg (Table 2). At this level, S. enterica and P. aeruginosa
were much more susceptible than the other tested
bacteria. With 20 mg of the methanol extract, the
inhibitory effect was greater in the ETEC-LT and EIEC
strains, whereas EPEC was less susceptible. Even
though the inhibition effect caused by the methanol
extract differed little from that caused by the other tested
extracts, the differences were statistically significant.
Using 30 mg of methanol extract, EIEC and E. cloacae
exhibited the greatest inhibition, followed by ETEC-ST
and S. aureus (Table 2). The increase in level of the
methanol extract had different effects among strains. The
strains EIEC, EPEC, E. cloacae, and S. aureus displayed
an apparent dose-response effect, with an increase in the
inhibition zone diameter corresponding to the increment
in amount of extract. ETEC and P. aeruginosa increased
their inhibition zone diameter as the level of methanol
extract augmented from 10 to 20 mg, but their inhibition
zone did not increase when the level was raised to 30 mg
of the extract. Finally, S. enterica showed no variation in
its inhibition zone diameter as the extract level increased.
The different E. coli pathotypes showed inhibition zone
diameters comparable to those caused by AM and CB,
except from ETEC-LT (Table 1).
Cytotoxic activity
The aqueous extract of L. indigo basidiocarp had different
effects on the various cell lines tested. No antiproliferative
effect of the aqueous extract was observed against the
A549 and MCF7 cell lines, but it significantly inhibited the
proliferation of HeLa cells at a concentration of 100 µg/ml
(Figure 1). In the case of primary BME cells, a significant
stimulation of prolife-ration was observed at a concen-
tration of 10 µg/ml and no effect was observed at any
other tested concen-tration.
The organic extracts of L. indigo also showed
contrasting effects between studied cell lines. Thus, in
normal RSF cells only the hexane extract showed an
inhibitory effect of proliferation relative to the control at all
concentrations tested (Figure 2), although the maximum
inhibition value was only of 25.63% compared to the
control at the maximum concentration of 1000 ng/ml. The
ethyl acetate extract showed significant inhibitory values
at the concentrations of 100, 500 and 1000 ng/ml.
Nevertheless, the maximum inhibition percentage was of
only 20.80% relative to the control. The methanolic
extract did not alter the capacity for proliferation of
fibroblasts at any concentration used (Figure 2). In the
case of HeLa cells, the three organic extracts had a
significant inhibitory effect on proliferation at all
concentrations evaluated. Using ethyl acetate extract, the
maximum inhibition was observed at a concentration of
100 ng/ml with a value of 95.74%, while for the metha-
284 Afr. J. Pharm. Pharmacol.
Table 1. Reference strains and clinical isolates used in the present study.
Strain Pathotype/comment Code AM
E. coli Enterotoxigenic with heat-labile toxin (ETEC-LT) H10407 18.0 17.0
Enterotoxaemia with heat-stable toxin (ETEC-ST) 25611 16.0 18.0
Enteroinvasive (EIEC) E11 20.0 12.0
Enteropathogenic (EPEC) O111 15.0 12.0
S. aureus isolated from bovine mastitis ATCC27543 nt nt
P. aeruginosa clinical isolate VGPM01 nt nt
E. cloacae clinical isolate VGEM17 nt nt
S. enterica subsp. enterica clinical isolate VGSM33 nt nt
aInhibition zone diameter (mm) caused by 10 µg of ampicillin (AM) and 100 µg of carbenicillin (CB), nt, not tested.
Table 2. Antibacterial activity of the organic extracts of L. indigo*.
mg/disk of each extract
Hexane Ethyl acetate Methanol
10 20 30 10 20 30 10 20 30
E. coli
EIEC - - - 9.6 (0.58)1,a 14.0 (0.73)1,b 19.0 (0.58)1,c 11.3 (0.53)1,a 16.0 (0.31)1, b 20.6 (0.31)1,c
EPEC - - - 9.3 (0.52)1,a 12.0 (0.50)2,3,b 15.3 (0.15)2,c 11.0 (0.78)1,a 12.3 (0.22)2,b 14.3 (0.58)2,5,c
ETEC-LT 18.8 (0.73)1,a 18.6 (0.30)1,a 21.0 (0.80)1,b 10.5 (0.73)1,a 11.3 (0.53)3,5,a 12.0 (0.78)3,a 11.6 (0.15)1,a 17.0 (0.73)1,b 17.6 (0.15)3,b
ETEC-ST - - - 10.0 (0.19)1,a 13.0 (0.75)1,2,b 17.1 (0.53)4,c 10.7 (0.58)1,a 15.0 (0.31)3,b 16.0 (0.73)3,4,b
P. aeruginosa 10.5 (0.51)2,a 11.2 (0.75)2,ab 12.1 (0.52)2,b 9.6 (0.33)1,a 17.2 (0.25)4,b 21.0 (0.65)5,c 13.3 (0.53)2,a 15.1 (0.53)3,b 15.3 (0.15)4,b
E. cloacae - - - 9.7 (0.36)1,a 10.1 (0.75)5,a 13.5 (0.17)6,b - 13.6 (0.15)4,a 19.0 (0.73)1,b
S. aureus - - - 10.1 (0.29)1,a 11.3 (0.65)3,5,a 13.0 (0.73)3, 6,b 9.6 (0.18)3, a 14.0 (0.78)3,4,b 16.3 (0.29)3,c
S. enterica - - - 9.7 (0.75)1,a 11.0 (0.58)3,5,a 11.0 (0.59)7,a 13.2 (0.38)2,a 13.7 (0.17)4,a 13.6 (0.15)5,a
*The mean radius of the inhibition zone of three independent experiments is shown in mm (±SD). Values in the same row with the same superscript letter have non-significant differences
between them. Values in the same column with the same superscript number have non-significant differences between them. For both rows and columns, the significance test was
evaluated at p < 0.05. This significance analysis was made only for results within the same kind of extract for all levels tested.
-, no inhibition zone.
nolic extract the percentage inhibition value at the
same concentration was of 67.61%. The hexane
extract caused maximum inhibitory activity
(76.51%) at 500 ng/ml. MCF7 cells showed a
significant stimulation of proliferation at different
concentrations of hexane and methanol extracts
(Figure 2), the response was higher for the
hexane extract at a concentration of 100 ng/ml
with a value of 98.08%.
The present work shows that organic extracts
from L. indigo are active against E. coli
diarrheagenic strains and other bacteria that are
pathogenic to humans. This is the first study in
which basidiocarps of the genus Lactarius are
tested against different E. coli diarrheagenic
strains. Some of the tested strains showed
significant differences in their responses to the
extracts. The ETEC-LT pathotype was susceptible
Zarzosa et al. 285
0. 00 1.00 5.00 10.00 50.00 100.00
Optical density
Extract concentration (
BME HeLa A549 MCF7
Figure 1. Effect of aqueous extract of L. indigo basidiocarp on proliferation of the four cell types evaluated. Bars represent the
mean of sextuplicates with its relative standard error. Asterisks indicate extract doses having significant differences relative to
the control (deionized water).
to the hexane extract whereas the EIEC pathotype was
more susceptible to the ethyl acetate and methanol
extracts. Our results agree with those reported by Dulger
et al. (2002), who documented the activity against E. coli
of methanol extracts of different species of Lactarius,
although they used a non-pathogenic strain. There are
some reports about the effect of methanol extracts of
Lactarius deliciosus on E. coli, with very contrasting
results. On one side, extracts of L. deliciosus collected in
Portugal had no activity against non-diarrheagenic E. coli
(Barros et al., 2007a, b); on the other extreme,
basidiocarp extracts of the same species collected in
Turkey gave positive inhibitory results against a different
strain of non-diarrheagenic E. coli (Dulger et al., 2002).
Methanolic extracts of Lactarius piperatus inhibited
growth of E. coli, but its activity was dependent on the
maturity of the basidiocarp used to make the extracts
(Barros et al., 2007b). These results may be due
to differences in the susceptibilities of the different strains
tested, although differences in the chemical composition
of the basidiocarps and in the extraction methods cannot
be discarded. In relation to the other microorganisms
tested, the three extracts showed strong activity against
P. aeruginosa and only the methanol extract exhibited
activity against E. cloacae and S. aureus. These results
agree with other reports stating that P. aeruginosa and S.
aureus can be inhibited by methanol extracts of
basidiocarps of species in the genus Lactarius (Dulger et
al., 2002; Barros et al., 2007a, b). However, the inhibition
activity of the methanol extract of L. indigo on S. aureus
that was observed in the present work seems to be
greater than the activity previously reported for methanol
extracts of other species in the same genus (Dulger et
al., 2002). No previous reports were found about the
inhibition of E. cloacae using extracts of species of the
genus Lactarius.
286 Afr. J. Pharm. Pharmacol.
0 50 100 500 1000
Optical density
Extract concentration (ng/ml)
0 50 100 500 1000
Optical density
Extract concentration (ng/ml)
0 50 100 500 1000
Optical density
Extract concentration (ng/ml)
Figure 2. Effect of hexane (HX), ethyl acetate (EA) and methanolic
(MeOH) extracts of L. indigo basidiocarp on the proliferation of
normal RSF (upper panel), HeLa (middle panel) and MCF7 (bottom
panel) cell lines. Bars represent the mean of sextuplicates with its
relative standard error. Asterisks indicate extract doses with
significant differences relative to the control (pure solvent).
The inhibition caused by the ethyl acetate and
methanol extracts was observed in practically all tested
strains. Therefore, it can be hypothesized that the
basidiocarps from L. indigo contain a wide spectrum of
antibacterial compounds. It has been previously establi-
shed that compounds with antibacterial activity extracted
from species in the genus Lactarius are mainly sesqui-
terpenes (Anke et al., 1989; Vidari et al., 1995). Further
studies are now needed to elucidate the chemical
structure of the antibacterial compounds extracted from
basidiocarps of L. indigo.
In the present work the aqueous extract of L. indigo
significantly inhibited the proliferation of HeLa cells and
showed a significant stimulatory effect on the proliferation
of primary BME cells. These results contrast with reports
for other species of Basidiomycota, although at
significantly higher concentrations of aqueous extract
than those used in the present study. For example, the
aqueous extracts of Coprinellus sp., Flammulina velu-
tipes and Coprinus comatus were capable of inhibi-ting
the proliferation in vitro of MCF7 cells, with IC50 values of
120, 150 and 450 µg/ml, respectively (Gu and Leonard,
2006). Consequently, we cannot discard the possibility
that the aqueous extract of L. indigo may present
antiproliferative activity against the other cell lines
evaluated in the present work at higher concentrations
than those used by us, a possibility that needs to be
evaluated in future works. On the other side, the fact that
low concentrations of the aqueous extract had a
significant stimulatory effect on the proliferation of normal
BME cells is indicative of the possibility that the chemical
compounds in the aqueous extract of L. indigo, which
inhibit the proliferation of HeLa cells may be specific
against certain types of cancerous cells. This fact is
relevant given that not all aqueous extracts of Basidio-
mycota present a specific activity against cancer cells; for
example, the vegetative mycelia of Funalia trogii and of
Trametes (Coriolus) vers-icolor contain water-soluble
metabolites that inhibit the proliferation of both HeLa and
normal fibroblasts (Ünyayar et al., 2006). One possibility
is that the aqueous extract of L. indigo contains active
polysaccharides that are specific against cancer cell
lines. One polysaccharide has been isolated from the
aqueous extract of Pleuotus ostreatus that has an
antiproliferative effect against HeLa cells at
concentrations of 100, 200 and 400 µM, but that has no
significant inhibitory effect on normal human embryonic
kidney cells 293T (Tong et al., 2009). Recently, a polysa-
ccharide enriched with selenium was obtained from an
aqueous extract of vegetative mycelium of Ganoderma
lucidum that displays a high antiproliferative activity in
vitro against HeLa and MCF7 cells with IC50 values of
0.17 and 0.14 µM, respectively (Shang et al., 2009). The
determination and characterization of anticarcinogenic
polysaccharides in aqueous extracts of L. indigo is
certainly an essential task to be carried out.
The organic extracts of the basidiocarp of L. indigo did
not show cytotoxic activity against the MCF7 cell line but
were capable for inhibiting the proliferation of HeLa cells.
While ethyl acetate and methanol extracts showed a
significant inhibitory effect of proliferation on normal RSF,
this was relatively low. Regarding MCF7 cells, the results
of our study contrast with those of several previous
reports about the effect of organic extracts of
Basidiomycota. Thus, methanolic extracts of Pleurotus
ostreatus significantly inhibit the proliferation in vitro of
MCF7 cells at concentrations above 120 µg/ml (Jedinak
and Sliva, 2008). Such extracts induce the arrest of the
cell cycle at the G0/G1 transition by means of induction of
the expression of p53 and p21 proteins, which inhibit the
cyclinkinase complexes (CDK). Analyses have been
made of the antiproliferative effects of the organic
extracts of the Basidiomycota fungus Naematoloma
fasciculare as well as those of the unsaturated aliphatic
acids, ergosterol and ergosterol peroxide, isolated from
such extracts (Yan et al., 2009). The pure chemical
compounds showed an antiproliferative effect against MCF7
cells that is from 10 to 100 times larger than that of the
extracts; while for the former the IC50 values oscillated
between 0.16 and 1.54 µg/ml, in the latter case those values
varied from 13.80 to over 30.0 µg/ml (Yan et al., 2009).
Triterpenoids isolated by means of extraction with ethyl
acetate of basidiocarp of Leucopaxillus gentianeus showed
a high antiproliferative activity against MCF7 cells, some
of these compounds having IC50 values lower than 300
µM (Clericuzio et al., 2004).
In contrast with the case of the MCF7 cells, our results
with HeLa cells agree with a number of literature reports.
Thus, the inhibition of proliferation of HeLa cells by
ethanolic extracts of spores of G. lucidum has been
reported (Fukuzawa et al., 2008), an effect that was
attributed to long chain fatty acids; however, there is a
recent report of triterpenoids of the same species having
high cytotoxic potential against HeLa cells (Cheng et al.,
An interesting observation made during the present
work is the stimulation of the proliferation of the MCF7
cell line, an activity that has been previously reported for
aqueous extracts of Agaricus blazei in the presence of
the estrogenic compound nonylophenol (Talorete et al.,
2002). Such proliferative activity has been associated
with induction of the expression of the c-Jun protein by
the extract, which is synthesized by one of the genes
from the proto-oncogene family c-jun, characterized by
being induced by mitogenic agents (Talorete et al., 2002).
Because the MCF7 cell line is characterized by
presenting estrogen receptors, it is possible that the
organic extracts of L. indigo may contain a substance that
stimuli-tes those receptors, something to be analyzed in
the future.
Both aqueous and organic extracts of L. indigo basidio-
carp posses pharmacological activity; in some cases, due
Zarzosa et al. 287
to inhibition of the proliferation capacity of pathogenic
bacteria, and in others, that of carcinogenic cells, without
significantly affecting normal cells. Our results show that
the basidiocarp of the edible L. indigo is a source of
pharmacological substances having diverse therapeutic
applications, which makes it necessary to perform further
studies in that regard by isolating and characterizing the
molecules responsible for the observed activities.
The authors acknowledge Silvia Martínez Chávez and
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... It is known for its fascinating color and the cultural significance it has in countries such as Mexico [56]. However, research has indicated the mushroom has antibacterial and cytotoxic properties [57]. Bioassays and cytotoxic assays were created to compare the inhibition of strains with only hexane and methanol versus with the Lactarius indigo. ...
... When tested against different bacteria, such as diarrheagenic Escherichia coli strains, the Lactarius indigo inhibited proliferation of certain pathogenic bacteria, the inhibitory effect depended on the bacteria it was tested against and the dosage of Lactarius indigo. Overall, the study indicated possible medicinal properties in L. indigo [57]. Both aqueous and organic extracts of Lactarius indigo basidiocarp have pharmacological activity, Ochoa-Zarzosa, et al., show that the basidiocarp of the edible Lactarius indigo is a source of pharmacological substances having varied therapeutic applications, which makes it necessary to perform further studies in that regard by isolating and characterizing the molecules responsible for the observed activities [58]. ...
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The need to improve the life quality together with the increase in the frequency of treating diseases attracted the attention of many researches to view food as a source of nutritional and therapeutical agents. Since earliest times, several mushrooms have been reported as a nutritious food with valuable medicinal properties. The genus Clitocybe and Lactarius belonging to Basidiomycota fungi, is a potential group of edible mushrooms that are distributed in Europe, North America, Asia, Australia and Mexico. The studies on Clitocybe nuda and Lactarius indigo species have revealed high nutritional and medicinal potentials. This review aims to present Clitocybe and Lactarius genus importance as both food and medicine, and which will offer a new vision to researchers to develop new drugs from natural sources.
... Further, several extracts displayed significant inhibition of carcinogenic cells without impacting healthy cells. These results suggest that L. indigo could be a source of pharmacological substances with diverse therapeutic applications, although the molecules responsible require isolating and characterizing (see: Ochoa-Zarzosa et al., 2011). In this context, it is also interesting to note that L. indigo contains high concentrations of chlorogenic and ascorbic acids, as well as flavonoids (López-Vázquez et al., 2017). ...
Land use conflict is a major contributor to unsustainable deforestation rates, with agriculture being the primary driver. Demand for agricultural output is forecast to increase for years to come and the associated deforestation is a key driver in global declines of biodiversity. Moreover, deforestation is contributing to instability of agricultural production systems and reduces our ability to mitigate anthropogenically driven climate change. There is urgency in reducing this land use conflict and the cultivation of ectomycorrhizal fungi (EMF) may provide a partial solution. As an example, here we focus on Lactarius indigo, an edible and historically appreciated species with distribution in the Neotropics and Nearctic. Exploring the geographic spread and associated climate preferences, we describe how cultivation of this species can be combined with forest-based biodiversity and conservation goals. Detailing a full methodology, including mycelium production and how to create trees that may produce the fungus, we explore potential benefits. Combing data from the emerging field of EMF cultivation with nutritional studies, we show that a protein production of 7.31 kg per hectare should be possible, exceeding that of extensive pastoral beef production. In contrast to commercial agriculture, L. indigo cultivation may enhance biodiversity, contribute to conservational goals and create a net sink of greenhouse gases whilst at the same time producing a similar or higher level of protein per unit area than the most common agriculture use of deforested land. With such startling and clear benefits, we call for urgent action to further the development of such novel food production systems.
... It is known that young fungi of this genus are filled up with latex and, thus, they are practically not damaged by worms, microorganisms or eaten by animals. There is a number of works of different authors showing high antimicrobial activity of substances present in the milky juice of mushrooms [13][14][15]. These authors also noted instability of such substances and the dependence of the antimicrobial activity on the stage of fungi development [14]. ...
... During the last decade, a large number of species of subdivisions Basidiomycotina and some Ascomycotina were tested in various studies which showed their antimicrobial potential (Barros et al. 2008 a, b;Ramesh and Ramesh and Pattar 2010;Ochoa-Zarzosa et al. 2011;Schwan 2012;Alves et al. 2013;Kostić et al. 2017;Soković et al. 2017). Results of these studies indicate that macromycetes are rich with compounds that possess various biological activities (Boucher et al. 2009). ...
The problem of the existence and prevalence of infectious diseases caused by pathogenic microorganisms in human society is persisted. Many studies have endeavoured to highlight the therapeutic potential of mushrooms. They can produce notable primary and secondary metabolites and could be of great benefit for humans. The largest internal vital organ in the human body is liver. It is responsible for many biochemical molecular interactions that are necessary for humankind.
... showed no activity against all the tested bacteria. However, Aqueous and organic (hexane, ethyl acetate and methanol) basidiocarp extracts of the edible mushroom Lactarius indigo were showed varied activity against various diarrheagenic Escherichia coli strains, Pseudomonas aeruginosa, Enterobacter cloacae, Staphylococcus aureus and Salmonella enterica [37]. ...
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The present study is aims to investigate the antibacterial activities of crude methanol extracts of 24 southern Western Ghats wild mushrooms. Crude methanol extracts from 24 mushrooms from southern Western Ghats, India were evaluated for their antibacterial activity against Eggerthella lenta, Vibrio parahaemolyticus and Enterococcus faecalis by agar well diffusion method. The study revealed that about 67% of the mushrooms inhibited growth of all the test bacteria, 29% was active against any of the two test bacteria and 4% were completely inactive. Amoxicillin used as standard reference. 15 mushroom species showed strong antibacterial activity against Eggerthella lenta higher than the standard antibiotic (Amoxicillin). 11 mushrooms showed strong antibacterial activity against Vibrio parahaemolyticus higher than the standard antibiotic (Amoxicillin). The best in vitro antibacterial activity was by Gymnopilus junonius (26.0 mm against Eggerthella lenta; 25.0 mm against Vibrio parahaemolyticus) followed by Tricholoma equestre (21.0 mm against Vibrio parahaemolyticus). Gymnopilus junonius, Tricholoma equestre and Trametes versicolor have higher antibacterial activity than that of standard antibiotic.
... Infundibulicybe geotropa, Lactarius controversus, Lactarius delicious and Phellinus hartigii [29]; Lactarius indigo [30] and Stereum ...
... In a very interesting discovery, Lovy et al. (2000) showed that the EEMs Russula xerampelina (known as the shrimp mushroom), Boletus variipes, and Boletus queletii, showed activity against Plasmodium falciparum , a protozoan parasite that causes malaria in humans. Antimicrobial activities originated by low molecular weight molecules, carbohydrates, or proteins have been studied in EEMs from Portugal (Alves et al. 2012; Barros et al. 2007a), China (Liu et al. 2013a, b; Dai et al. 2009), Turkey (Dog ˘an and Akbas 2013;), Mexico (Ochoa-Zarzosa et al. 2011), Serbia (Heleno et al. 2013; KosanicétKosanicét al. 2012), Korea (Lee et al. 1999; Park et al. 1995), Macedonia (Nedelkoska et al. 2013), Algeria (Gouzi et al. 2011; Dib-Bellahouel and Fortas 2011) and Jordan (Janakat et al. 2005). It is interesting to note that6.5 Mexican market stall selling a mixture of species of the ectomycorrhizal genera Ramaria, Gomphus, Russula and Lactarius, which have a variety of novel bioactive compounds phenolic compounds from wild mushrooms, including some ectomycorrhizal species, with antimicrobial activities have been recently reviewed by Alves et al. (2013)Solak et al. 2006). ...
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Ecologically, edible mushrooms can be: (i) parasites of plants or animals, (ii) saprotrophs, which live and feed on dead organisms, such as the industrially cultivated button, oyster or shiitake mushrooms, or (iii) ectomycorrhizal, which establish mutually beneficial symbiosis with the roots of host plants. Ectomycorrhizal wild mushrooms, which are the subject of this chapter, embrace the most expensive edible fungi, including truffles, porcini, matsutake, chanterelles, Caesar's mushrooms, or saffron milk caps. The international commerce of edible ectomycorrhizal mushrooms (EEMs) annually is worth billions of dollars. However, EEMs have been a largely unexplored source of bioactive compounds. Despite this fact, analgesic, antiallergic, anticarcinogenic, antibacterial, anticoagulant, antifungal, antihypertensive, anti-inflammatory, antinociceptive, antioxidant, antipyretic, antivenom, antiviral (including anti-HIV), cholesterol-lowering, hepatoprotective, and immune enhancement properties have been found in more than 100 species of EEMs. Some bioactive compounds including grifolin, polyozelyn, and novel lectins or ribonucleases produced by Albatrellus, Boletopsis, Hygrophorus, Thelephora, and Polyozellus, respectively, are exclusive of EEMs. Additionally, insecticide, nematicide, and allelophatic compounds with potential application to control agricultural pests and weeds have been found in EEM. Despite the fact that most EEMs have defied cultivation, some advances have been made in cultivation of truffles and broth cultures of species included in the genera Hygrophorus, Lactarius, Morchella, Rhizopogon, Suillus, and Tuber as a potential source of bioactive compounds with medical or nutraceutical importance. In addition, EEMs as a valuable non-timber forest product contributes to rural development and the establishment of truffle plantations contributes to rehabilitation of degraded areas and global carbon sequestration. In the future, advances in the cultivation of EEMs might produce bioactive compounds in industrial amounts. © Springer International Publishing Switzerland 2014. All rights are reserved.
... (Nicholas et al., 2001); Ganoderma lucidum, Navesporus floccosa and Phellinus rimosus (Sheena et al., 2003); Pleurotus tuber-regium (Ezeronye et al., 2005Yamac and Bilgili, 2006); Lactarius deliciosus, Sarcodon imbricatus and Tricholoma portentosum (Barros et al., 2006); Russula delica (Turkoglu et al., 2007); Pleurotus eryngii var. ferulae (Akyuz and Kirbag, 2009); Infundibulicybe geotropa, Lactarius controversus, Lactarius delicious and Phellinus hartigii (Altuner and Akata, 2010); Lactarius indigo (Ochoa-Zarzosa, 2011) and Stereum ostrea (Praveen et al., 2012) contain a wide range of antimicrobial activity. This difference in response of mushroom extracts to test organisms might be due to a number of factors, as studies suggest that the antimicrobial activities of all mushroom extracts are changeable (Iwalokun et al., 2007), depending upon the nature of environment and media in which it was grown. ...
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The antibacterial activities of petroleum ether, chloroform and methanol extract of mushroom H. parvula was analyzed in vitro by agar well diffusion method. The yields of extracts obtained from different solvents were petroleum ether (10.88) gm, chloroform (11.21gm) and methanol (51.16gm). The growth inhibitory effects of crude extracts were tested against three plants and six human pathogenic bacteria. The maximum antibacterial activity of petroleum ether extracts of H. parvula was found against A. tumefaciens (16mm) at 100% concentration and minimum against X. campestris (3mm) at lower concentration of chloroform and methanol extract in plant pathogenic bacteria. Whereas petroleum ether extracts were showed more inhibition zone against P. aeuroginosa (18mm), at 100% concentration in human pathogenic bacteria, the activity was less than the standard Tetracycline and Ciprofloxacin. The extract shows increasing inhibitory activity with increase in concentration (12.5%-100%). The antibacterial activity of all the solvent extracts were calculated by measuring inhibition zone formed around the well.
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The huge land areas in China provide highly diverse habitats for macrofungi. Of these macrofungi, many are directly related to people’s daily life and have been utilized by ancient Chinese for at least 6800 years. In this study, we evaluate the current known resource diversity of Chinese macrofungi. A total of 1662 taxa are summarized, and all species names and their authorities have been checked and corrected according to authentic mycological databases. Among the 1662 taxa, 1020, 692, and 480 are considered to be edible, medicinal and poisonous mushrooms, respectively. A few of edible macrofungi in China are commonly used for commercial production. All known medicinal functions are labeled for medicinal species. The most common medicinal functions possessed by Chinese macrofungi are antitumor or anticancer, followed by antioxidant and antimicrobial. A total of 277 Chinese macrofungi are edible simultaneously with certain medicinal functions and without known toxicity. These species could be treated as “Gold Mushrooms”. Contrarily, 193 edible and/or medicinal species are also recognized as poisonous mushrooms. To avoid poisoning caused by these species, ingestion either in a proper way or in small amounts is important. However, the mycotoxins metabolized by these poisonous species could be a huge wealth of natural products yet to be explored. How to utilize these Chinese macrofungal resources is a critical to benefit humans worldwide.
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Antimicrobial activities of extracts of fruit bodies of Lycoperdon perlatum against Staphylococcus aureus, Pseudomonas aeruginosa, Escherichia coli, Bacillus cereus, Candida albicans and Candida glabrata were investigated. Antimicrobial components from the mushrooms were extracted using ethanol, methanol and water. The antimicrobial activities were examined by agar well diffusion method. The MIC, MBC and MFC were evaluated for each extract of the mushroom. The aqueous extract of Lycoperdon perlatum inhibited the growth of all the tested pathogenic organisms except P. aeruginosa while the methanol and ethanol extracts inhibited all the tested organisms. The phytochemical analysis revealed the presence of varying levels of bioactive compounds. Flavonoids, saponins, protein and carbohydrate were detected in all the extracts while glycosides, alkaloids and tannins were found in some. The results obtained from this study suggest that Lycoperdon perlatum has broad-spectrum of activity against microbial isolates used. Keywords: Lycoperdon perlatum, antimicrobial, phytochemicals, well diffusion
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Comparisons were made of the species composition and distribution of Amanita, Laccaria, Lactarius, and genera in the Boletaceae reported from temperate North America, southern Neotropical Quercus forests (Costa Rica-Colombia), the Lesser Antilles, tropical South America excluding montaine Colombia, and temperate South America. The examined fungi showed discrete rather than cosmopolitan distribution ranges, with little overlap in species composition between these different geographic regions. Potential endemism was high in Neotropical oak forests, with 30-100% of the species in each of the genera studied not reported from outside the region. -from Authors
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One hundred and fourteen species of Agaricales from Sonora were determined. One hundred and four of these are new records of Sonoran mycobiota. Sixteen families were identified, with the highest number of taxa for Pluteaceae (26), Cortinariaceae (17), and Russulaceae (12), in the following types of vegetation: pine-oak forest (54), oak forest (46) and tropical deciduous forest (16). The genus Amanita was the best represented with 22 taxa, including edible, mycorrhizal and toxic species. Amanita daucipes and Entoloma byssisedum are registered for the second time from Mexico.
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Summary There has been a lot of progress in mushroom science and biotechnology in the last decade. The optimization of PFGE separation of fungal chromosomes allowed the study of the molecular karyotype of mushrooms and the assignment of genes to chromosomes. There are 115 genes encoded from different species of mushrooms. Cross breeding contin- ues to be the principal method, but it is accompanied by the analyses of RAPD or RFLPs methods. The genetic makers are used and introduced into commercial large hybrids via introgression breeding. The complex traits such as yield, resistance to disease and quality characteristics, and quantitative traits more than one quantitative trait locus (QTL) are found and used in practice. The transformants or transgenic mutant strains were obtained by Agrobacterium system or particle bombardment. At least 651 species representing 182 genera of hetero- and homobasidiomycetes mushrooms were researched containing anti- tumor or immunostimulating polysaccharides. Ergosterol in the lipid fraction was identi- fied as one of the most active constituents. New sesquiterpenoid hydroquinones, steroids, oxalic acid, triterpenes, water-soluble lignins, sulfated polysaccharides, protein-bound poly- saccharides are researched intensively as antimicrobial or antiviral agents. Many small mo- lecular mass compounds exhibit cytotoxic activities, such as illudins, leaianafulvene, triter- penes (ganoderic acids), acetoxyscirpenediol, ergosterol peroxide, sterols. There are many other compounds or activities found in the mushrooms, such as antioxidative, hypoglyce- mic action, anti-inflammatory effect, hepatoprotective compounds, psychoactive compounds and activities.
Observations of the basidiospores under SEM, as well as new data and critical notes concerning the taxonomy and distribution of Lactarius alnicola A. H. Sm. var. alnicola, L. corrugis Peck, L. deceptivus Peck, L. indigo (Schw.) Fr., L. griseus Peck, L resimus (Fr.) Fr var. resimus, L. resimus var. regalis Peck and L. subpalustris Hesler & A. H. Sm. are presented. The three latter species are reported for first time from Mexican mycobiota.
Anti-tumor activity of mushroom fruit bodies and mycelial extracts evaluated using different cancer cell lines. These polysaccharide extracts showed potent antitumor activity against sarcoma 180, mammary adenocarcinoma 755, leukemia L-1210 and a host of other tumors. The antitumor activity was mainly due to indirect host mediated immunotherapeutic effect. These studies are still in progress in many laboratories and the role of the polysaccharides as immunopotentiators is especially under intense debate. The purpose of the present review is to summarize the available information in this area and to indicate the present status of the research.
Eastern North America and temperate eastern Asia reportedly share a relatively high number of taxa of macrofungi (mushrooms and relatives), including a number of taxa that have putative eastern North America temperate eastern Asia disjunct distributions. These reports have been used to imply an affinity between the mycota (fungal equivalent of flora and fauna) of the two regions. To date, however, this affinity has not been examined in detail. A comparison of north temperate macrofungal mycotas was undertaken to examine the similarity between these regions. We used two methods in this study: (i) direct comparison of taxon lists and (ii) calculation of the Simpson Coefficient of similarity from lists of selected taxa. These analyses were based on field work, herbarium records, and published taxonomic treatments for Amanita, Lactarius, Ramaria, and Boletaceae. Results of these analyses document that taxonomic similarity between eastern North America and temperate eastern Asia mycotas can be quite high. In all cases, the calculated similarity values for eastern North America - temperate eastern Asia comparisons are higher than those between either region of North America and Europe or between western North America and eastern Asia. Furthermore, the eastern North American and temperate eastern Asian disjunct distributions of macrofungi are usually limited to the level of species or lower.
The extracts obtained from six Lactarius species [Lactarius deterrimus Grager, Lactarius sanguifluus (Paul.: Fr.) Fr., Lactarius semisanguifluus Heim et Leclair, Lactarius piperatus Scop. ex Fr., Lactarius deliciosus (L. ex Fr.) S.F. Gray and Lactarius salmonicolor Heim et Leclair] have been investigated for their antimicrobial activity. Growth inhibition using agar disk diffusion assays was determined against: Escherichia coli ATCC 11230, Micrococcus luteus ATCC 2971, Stapylococcus aureus ATCC 6538P, Salmonella thyphi ATCC 19430, Klebsiella pneumoniae UC57, Pseudomonas aeruginosa ATCC 27853, Corynebacterium xerosis CCM 2824, Bacillus cereus ATCC 7064, Bacillus megaterium DSM 32, Mycobacterium smegmatis CCM 2067, Candida albicans ATCC10231 and Saccharomyces cerevisiae ATCC 9763. As a result of this study, we have found that Lactarius species revealed antimicrobial activity against some Gram (+) and Gram (-) bacteria, but showed no antagonistic effect against yeasts used in this study.