Appl Microbiol Biotechnol (2010) 88:9971005
DOI 10.1007/s00253-010-2821-y
ENVIRONMENTAL BIOTECHNOLOGY
Biosorption of Cd, Cu, Pb, and Zn from aqueous solutions
by the fruiting bodies of jelly fungi (Tremella fuciformis
and Auricularia polytricha)
Rong Pan & Lixiang Cao & Haiwei Huang &
Renduo Zhang & Yu Mo
Received: 11 July 2010 / Revised: 31 July 2010 / Accepted: 1 August 2010 / Published online: 18 August 2010
# Springer-Verlag 2010
Abstract In this study, dried and humid fruiting bodies of
Tremella fuciformis and Auricularia polytricha were
examined as cost-effective biosorbents in treatment of heavy
metals (Cd2+, Cu2+, Pb2+, and Zn2+) in aqueous solution. The
humid T. fuciformis showed the highest capacity to adsorb the
four metals in the multi-metal solutions. The Pb2+ adsorption
rates were 85.5%, 97.8%, 84.8%, and 91.0% by dried T.
fuciformis, humid T. fuciformis, dried A. polytricha, and
humid A. polytricha, respectively. The adsorption amount of
Pb2+ by dried and humid T. fuciformis in Cd2+ +Pb2+, Cu2+ +
Pb2+, Pb2+ +Zn2+, Cd2+ +Cu2+ +Pb2+, and Cd2+ +Zn2+ +Pb2+
solutions were not lower than that in Pb2+ solutions. The
results suggested that in humid T. fuciformis, Cd2+, Cu2+, and
Zn2+ promoted the Pb2+ adsorption by the biomass. In the
multi-metal solutions of Cd2+ +Cu2+ +Pb2+ +Zn2+, the adsorp-
tion amount and rates of the metals by all the test biosorbents
were in the order of Pb2+ >Cu2+ >Zn2+ >Cd2+. Compared with
the pseudo first-order model, the pseudo second-order model
described the adsorption kinetics much better, indicating a
two-step biosorption process. The present study confirmed
that fruiting bodies of the jelly fungi should be useful for the
treatment of wastewater containing Cd2+, Cu2+, Pb2+, and
Zn2+.
Keywords Auricularia polytricha . Biosorption
Fruiting bodies . Jelly fungi . Tremella fuciformis
R. Pan : H. Huang : R. Zhang (*) : Y. Mo
School of Environmental Science and Engineering,
Sun Yat-Sen University,
Guangzhou 510275, Peoples Republic of China
e-mail: zhangrd@mail.sysu.edu.cn
L. Cao
School of Life Sciences, Sun Yat-Sen University,
Guangzhou 510275, Peoples Republic of China
Introduction
Contamination of the environment by toxic metals has
been accelerated dramatically with the rapid development
of industry. These metals are difficult to remediate and
adversely affect the ecosystems and human health. The
high costs of traditional remedial approaches have driven
interests in applications of bioremediation technology
(Wu et al. 2009). Many types of microbe biomass have
been reported to be able to remove metals from aqueous
solutions (Chen et al. 2008). Microbes can accumulate
heavy metals by two mechanisms: biosorption and
bioaccumulation. Biosorption is a metabolism-independent
binding process of negatively charged free groups to the
microbial cell wall, while bioaccumulation is an energy-
dependent metal influx (Malik 2004). As a consequence of
metal accumulation, microorganisms have developed different
mechanisms of metal resistance (Raspanti et al. 2009). Among
microorganisms, fungi display a high ability to immobilize
toxic metals by insoluble metal oxalate formation, biosorption,
or chelation onto melanin-like polymers (Baldrian 2003). The
use of fungi for bioremediation of wastewater contaminated
by heavy metals may be more advantageous than bacterial
biosorption.
For the industrial application of biosorption, the use of
freely suspended biomass has several disadvantages, such as
compaction, clogging, and difficulties of post-separation of
suspended biomass from the treated effluent, maintenance of
biosorbent stability, and regeneration of used biosorbents
(Akhtar et al. 2009). Because of absence of the rational
method to predict the biosorption potential of a microorganism,
the only method for identifying and developing new and
efficient biosorbents is through sustained screening of
microbes. Fruiting bodies of macrofungi (mushrooms) are
998
considered to be ideal materials as biosorbents. It has been
demonstrated that many Agaric fungal species exhibit high
biosorptive potentials (Collin-Hansen et al. 2007; Courbot et
al. 2004; Garca et al. 2009). Growing prolifically in many
parts of the world, mushrooms have large biomass, strong
texture, and other characteristics required for the development
into sorbents, which obviate the need for immobilization or
deployment of specialized reactor configurations as required
with other microbial sorbents (Muraleedharan et al. 1995).
It has been shown that, as cost-effective biosorbents,
mushrooms may play an important role in removing heavy
metals from the aqueous environment (Vimala and Das 2009).
However, the heavy metal biosorption and bioaccumulation of
mushrooms need to be thoroughly investigated except for a
few species of Agaricales (Pleurotus spp., Agaricus spp., and
Calocybe spp.). Tremella fuciformis and Auricularia poly-
tricha belong to the so-called jelly fungi, a set of species from
different taxonomical groups of Phragmobasidiomycetes,
which form gelatinous fruiting bodies. They are able to
survive for a long period of drought by drying to a horny
texture. When moisture is available, the fungi absorb water
and become gelatinous. This characteristic of jelly fungi is due
to the presence of specific water absorbing polysaccharides
that compose 6070% of the dry fruiting body. Some
polysaccharides have shown chelating effects on metallic ions
(Mau et al. 2001), and can be applied for effluent treatments
(Levankumar et al. 2009). The potential of jelly fungal
polysaccharides as biosorbents is worthy to be further studied.
Mushroom fruiting bodies have complex structures, both
morphologically and physiologically with undoubted varia-
tions in chemical composition (Smith et al. 2002). Therefore,
the jelly fungi show potentials in biosorption of metals from
wastewater. However, the study on biosorption of metals by
jelly fungi is still limited.
The aim of this study was to characterize the biosorption
of heavy metal ions (Cd2+, Cu2+, Pb2+, and Zn2+) by the
fruiting bodies of jelly fungi (T. fuciformis and A.
polytricha). The adsorption processes were described using
the pseudo first-order model and pseudo second-order
model. The implications of the results on the biosorption
were also addressed.
Materials and methods
Biosorption experiments
Dried fruiting bodies of T. fuciformis (Silver ear, Agricultural
Culture Collection of China, ACCC50546) and A. polytricha
(Red ear, ACCC50140) were used for experiments. Humid
jelly fungi were obtained by immersing the dried fungi into
deionized water for 10 h. Four totally different types of
biosorbents: dried red ear (RD), humid red ear (RH), dried
Appl Microbiol Biotechnol (2010) 88:9971005
silver ear (SD), and humid silver ear (SH), were used in the
study. The humid biosorbents were prepared using the same
amount of dried fungi.
The stock aqueous solutions of 1,000 mg L1 Cd2+, Cu2+,
Pb , and Zn2+ were prepared by dissolving analytical grade
2+
CdCl2, CuCl22H2O, ZnCl2, and Pb(NO3)2 in deionized
water, respectively. The stock solutions were used to prepare
dilute solutions of different working concentrations (10, 50,
and 100 mg L1). The multi-metal solutions were prepared
by mixing different single-metal solutions (100 mg L1 for
each) together.
Biosorption experiments were carried out with 60 treat-
ments, including four biosorbents (RD, RH, SD, and SH)
combined 15 different metal solutions (four single-metal
solutions, six two-metal mixture solutions, four three-metal
mixture solutions, and one four-metal mixture solution).
There were three replicates for each treatment. For each
experiment, in a 100-mL Erlenmeyer flask, a biosorbent
(0.1 g dried fungi, 1.2 g humid silver ear, or 0.8 g humid
red ear: 0.1 g dried biomass became 1.2 g humid silver ear
and 0.8 g humid red ear after immersing with deionized
water for 10 h) was added with 25 mL of a metal solution.
The flask was put on a rotary shaker at 150 rpm and 25 C
for 5, 10, 20, 30, 60, and 120 min for the single-metal
solutions, 30 min for the multi-metal solutions with RD and
RH, and 20 min for the multi-metal solutions with SD and
SH.
The fungal biomass was separated by filtration, then
dried at 80 C for 12 h, and weighted. The filtrate was
digested in 67% HNO3. The solids were redissolved in
0.1 M HCl after the HNO3 solution was evaporated. Then
the metal concentrations were determined using inductively
coupled plasma optical emission spectrometry (Perkinelne
5300dv, Optima, USA).
Batch adsorption experiments were conducted to study
the effects of initial concentration, contact time, and
competitive adsorption of multi-metals on the biosorption
of Cd2+, Cu2+, Pb2+, and Zn2+ by the jelly fungi. For
each metal, three initial concentrations (10, 50, and
100 mg L1) were used and six different contact times
(5, 10, 20, 30, 60, and 120 min) were adopted for each
concentration. In a multi-metal solution, the concentration
of each metal was set as 100 mg L1, and the contact time
of red ear and silver ear was set as 30 and 20 min,
respectively.
Additional experiments were conducted to compare
our biosorbents with Agaricales mushrooms, including
Agaricus bisporus, Lentinu edodes, and Pleurotus ostreatus.
For each Agricales mushroom, 0.1 g dry mass was mixed
with 25 mL of each of Cd2+, Cu2+, Pb2+, and Zn2+ solutions
(10 mg L1) at pH of 5.0 in a 100-mL Erlenmeyer flask.
Other experimental conditions were the same as described
above.
Appl Microbiol Biotechnol (2010) 88:9971005
Methods for data analyses
Metal adsorption amount and rates by the fungi were
calculated using the following equations:
Ci  Cf V
Q 1 Results
W
Ci  Cf
R 100% 2
Ci
1
Here Q is the adsorption amount of fungus (mg g ); R is
the adsorption rate of fungus (%); Ci is the initial
concentration of heavy metal used (mg L1); Cf is the final
concentration of heavy metal after adsorption (mg L1); V is
the volume of the heavy metal solution (25 mL in the
experiments); and W is the dry weight of fungus biomass
(0.1 g in this study).
The following two models were used to characterize the
time-dependent kinetics of metals binding by the biosorb-
ents. The pseudo first-order equation is given by (Galli et
al. 2003):
dqt
k1 qe  qt 3 adsorption rates of the four ions than RD and RH. The four
dt
where qt and qe are the amounts of heavy metal adsorption
of the fungus (mg g1) at time t (min) and the equilibrium,
respectively, and k1 is the pseudo first-order rate constant
for the adsorption process (min1). The integrated form of
Eq. 3 is
lnqe  qt ln qe  k1 t 4
Values of qe and k1 can be determined from the intercept
and slope of Eq. 4, respectively.
The pseudo second-order equation is expressed as
(Gupta and Rastogi 2008):
dqt
k2 qe  qt 2 5 respectively. In general, the metal rates and amount adsorbed
dt
where k2 is the equilibrium rate constant of pseudo second-
order adsorption (g mg1 min1). Integrating Eq. 5 from t=
0 to t with qt =0 to qt yields
t 1 1 Pb2+ solution. In the multi-metal solution of Cd2+ +Cu2+ +
t 6 Pb2+ +Zn2+, the amount and rates of the metals by all the
qt k2 q2e qe
If the second-order kinetics model is applicable for a data
set, the plot of t/qt versus t should show a reasonably good
linear relationship, from which qe and k2 can be determined
from the slope and intercept.
For the adsorption data of multi-metals by the fungi, 2
tests were performed using the statistical analysis software
SAS (SAS Institute, Inc., Cary, NC). Values of the mean
and standard deviations (mean standard deviation) were
999
calculated using the one-way ANOVA. The significance
analyses of different treatments were conducted with a 5%
least significant difference test (p<0.05).
Effects of contact time and initial metal concentrations
on metal biosorption
The biosorption of Cd2+, Cu2+, Pb2+, and Zn2+ by the fungi
reached equilibrium after 30 min of the experiment. The
adsorption amounts of Cd2+, Cu2+, Pb2+, and Zn2+ by the
fungi increased with the initial concentrations up to
100 mg L1. However, the adsorption amount of Zn2+ by
SH increased with the initial concentrations from 10 to
50 mg L1, and then decreased from 50 to 100 mg L1. The
results were attributable to the decrease of the effective pore
diffusivity with increasing initial metal concentrations.
As shown in Fig. 1, the adsorption rates (R) decreased
with the increase of initial concentrations. Among the four
biosorbents, SH demonstrated the highest adsorption rates
in the four-metal solutions. SD and SH showed higher
biosorbents had higher adsorption rates to Pb2+ than those
to Cd2+, Cu2+, and Zn2+ at the concentration of 100 mg L1
(Fig. 1c). Nevertheless, not all the adsorption curves
continuously decreased with the initial metal concentra-
tions. For example, the adsorption rates of the four metals
by RD decreased firstly then increased (Fig. 1ad).
Effects of other heavy metals and fungal physiological
properties on metal biosorption
The adsorption rates and amount of fungal fruiting bodies in
the single and multi-metal solutions with the initial concen-
tration of 100 mg L1 are shown in Tables 1 and 2,
by the fungal biomass decreased with more metals involved.
However, the adsorption amounts of Pb2+ by SD and SH in
Cd2+ +Pb2+, Cu2+ +Pb2+, Pb2+ +Zn2+, Cd2+ +Cu2+ +Pb2+, and
Cd2+ +Zn2+ +Pb2+ solutions were not lower than that in the
biosorbents were in the order of Pb2+ >Cu2+ >Zn2+ >Cd2+.
Nevertheless, the adsorption rates and amount of Cd2+ and
Zn2+ were similar in the Cd2+ +Zn2+ solution.
In the 50-mg L1 single Cd2+, Cu2+, and Zn2+ solutions,
the adsorption rates or the biosorption capacities of the
biosorbents were in the order of SH > SD > RD and RH
(Fig. 1). Although the biosorption capacities of different
sorbents in the 100-mg L1 metal solutions were different
from those in the 50-mg L1 solutions for the four single
1000 Appl Microbiol Biotechnol (2010) 88:9971005

100 metals, the biosorption capacity of SH was significantly

higher than that of RH, the Cd2+ and Cu2+ removal
Adsorption rate (%) 80
capacities of SD were significantly higher than those of
60
RD, and the Zn2+ removal capacity of RD was significantly
higher than that of SD (p<0.05). However, the Pb2+
40 removal capacities by SD and RD were not significantly
RD
RH
different (p<0.05). In most cases, the metal removal
20
SD capacity of SH was significantly higher than that of SD.
A
0
SH
In the single Cd2+, Cu2+, and Zn2+ solutions with the
0 20 40 60 80 100 120
concentration of 100 mg L1, the adsorption rates and
Initial concentration (mg.L-1)
amount of RD was higher than that of RH, while the
adsorption capacities of Pb2+ by RD and RH were not
100 significantly different (p<0.05). In the single Cd2+, Cu2+,
and Pb2+ solutions with the concentration of 100 mg L1,
Adsorption rate (%)

80
the adsorption rates and amount of SH were higher than
60 that of SD, while the difference between the adsorption
capacities of Zn2+ by SD and SH was not significant
40 (Table 2). Therefore, SH showed the highest capacity to
RD adsorb the four metals in the multi-metal solutions and the
20 RH
SD B water holding capacity of the biosorbents affected the
0
SH sorption capacity to the metals.
0 20 40 60 80 100 120
Initial concentration (mg.L-1)
Adsorption kinetics

100 The pseudo first-order kinetic model (Eq. 4) was used to fit
the experimental data of the heavy metal biosorption by the
Adsorption rate (%)

80
jelly fungi. The best fitting parameters of the kinetic model
60 (qe and k1) are listed in Table 3. Values of the coefficients of
determination (R2) were relatively high (R2 >0.80). How-
40
ever, values of the amount of heavy metal adsorption by the
20
RD fungi at the equilibrium calculated from the fitting process
RH
SD C (qe,cal) were significantly different from the experimental
0 SH values (qe,exp). Except one case, the calculated values were
0 20 40 60 80 100 120
Initial concentration (mg.L-1)
much smaller than the experimental values. Compared with
the experimental values, the relative errors of qe,cal were
from 21% to 95%. Therefore, the pseudo first-order model
100
was not satisfactory to describe the adsorption kinetics.
The fitting results of the pseudo second-order model
Adsorption rate (%)

80
(Eq. 6) are summarized in Table 4. For the different heavy
60 metals, initial concentrations, and biosorbents, the pseudo
second-order adsorption model fitted the experimental data
40
very well. The coefficients of determination (R2) were high
RD (>0.95 for most of the cases) and the adsorption capacities
20 RH
SD calculated from the model were close to the experimental
SH D
0 results. The adsorption amount (qe) increased with the
0 20 40 60 80 100 120
initial concentration and the rate constant (k2) decreased
Initial concentration (mg.L-1)
with the increasing initial concentration.
Fig. 1 Effect of initial metal concentrations on adsoption rates of a Under the same experimental conditions, the Cd2+
Cd2+, b Cu2+, c Pb2+, and d Zn2+ by the fungi. RD dried red ear, RH adsorption amounts by SD, SH, and RD were higher than
humid red ear, SD dried silver ear, SH humid silver ear
those by the Agaricales mushrooms (A. bisporus, L.
edodes, and P. ostreatus) (Fig. 2). The Cd2+ adsorption
amounts by SH and RD were more two times than that by
L. edodes (2.60 and 2.28 mg g1 vs. 1.11 mg g1).
Appl Microbiol Biotechnol (2010) 88:9971005 1001

Table 1 Adsorption rates of

Cd2+, Cu2+, Pb2+, and Zn2+ by Treatment Element RD RH SD SH
the jelly fungi (%)
Cd2+ Cd2+ 87.32 37.96 42.92 91.05
Cu2+ Cu2+ 81.76 47.81 52.84 78.10
Pb2+ Pb2+ 84.77 90.98 85.53 97.76
Zn2+ Zn2+ 56.64 31.75 81.47 80.54
Cd2+ +Cu2+ Cd2+ 7.36 7.52 34.12 44.48
Cu2+ 17.16 21.00 49.80 69.12
Cd2+ +Pb2+ Cd2+ 23.56 19.12 76.48 80.08
Pb2+ 56.76 51.52 89.40 99.56
Cd2+ +Zn2+ Cd2+ 15.28 21.00 42.72 66.96
Zn2+ 13.68 20.36 40.56 66.24
Cu2+ +Pb2+ Cu2+ 8.32 35.28 56.36 70.28
Pb2+ 25.12 49.36 85.48 96.12
Cu2+ +Zn2+ Cu2+ 15.88 31.20 43.44 55.52
Zn2+ 4.68 11.64 29.52 38.56
Pb2+ +Zn2+ Pb2+ 40.68 45.00 89.76 99.80
Zn2+ 7.40 17.68 50.16 62.32
2+ 2+ 2+
Cd +Cu +Pb Cd2+ 10.68 7.68 23.48 39.04
Cu2+ 15.32 20.08 38.32 67.32
Pb2+ 28.24 29.44 76.84 97.92
Cd2+ +Cu2+ +Zn2+ Cd2+ 6.68 5.60 11.96 29.92
Cu2+ 17.80 23.32 29.20 58.28
Zn2+ 8.88 7.36 14.96 33.24
Cd2+ +Pb2+ +Zn2+ Cd2+ 9.48 10.76 25.24 40.16
Pb2+ 41.08 45.32 78.60 99.56
Zn2+ 12.72 15.08 27.48 54.32
Cu2+ +Pb2+ +Zn2+ Cu2+ 12.44 21.32 28.52 47.80
Pb2+ 23.04 29.76 62.52 69.60
Zn2+ 7.96 11.08 17.96 28.16
The initial concentrations of the Cd2+ +Cu2+ +Pb2+ +Zn2+ Cd2+ 2.76 5.52 9.68 27.00
metals were 100 mg L1 Cu2+ 13.48 20.56 25.76 46.28
RD dried red ear, RH humid red Pb2+ 23.76 29.64 59.64 69.28
ear, SD dried silver ear, SH Zn2+ 7.40 8.16 13.80 45.68
humid silver ear

Similarly, the Cu2+ and Pb2+ adsorption amounts by SD,
SH, and RD were higher than those by the Agaricales
mushrooms. The Cu2+ adsorption amounts by SD and RD
were two times as that by P. ostreatus (2.10 and
2.03 mg g1 vs. 1.04 mg g1). The Zn2+ adsorption
amounts by SD, SH, RD, and RH were higher than those
by the Agaricales mushrooms (1.97, 2.38, 2.27, and
1.18 mg g1 vs. 0.67, 0.93, and 0.34 mg g1, respectively).
Discussion
The metal adsorption rates and amount by the different
fungal fruiting bodies in the multi-metal solutions were
generally lower than those in the single-metal solutions
under the same experimental conditions. With more
metal types involved, the metal rates and amount
adsorbed by the fungal biomass decreased. The inter-
actions among the different metals may influence the
binding capacity of metals to the adsorption sites.
Therefore, the uptake of metal ions in a competitive
adsorption process would be lower than that for
individual adsorption (Arief et al. 2008). However, the
adsorption amounts of Pb2+ by SD and SH were higher in
the Cd2+ +Pb2+, Cu2+ +Pb2+, Pb2+ +Zn2+, Cd2+ +Cu2+ +
Pb2+, and Cd2+ +Zn2+ +Pb2+ solutions than that in the
single Pb2+ solution. It has been reported that the impact
factors on the order of priority adsorption include
paramagnetism, coordination number, electronegativity,
and the covalent bond index (Mohapatra and Gupta
2005). Nevertheless, the interactions among different
metals are so complicated that further research is needed.
A system for explaining the behavior of metal ions in a
complex solution has been established through the covalent
1002 Appl Microbiol Biotechnol (2010) 88:9971005

Table 2 Adsorption amounts of

Cd2+, Cu2+, Pb2+, and Zn2+ by Treatment Element RD RH SD SH
the jelly fungi (mg g1)
Cd2+ Cd2+ 21.830.72 a 9.490.54 b 10.730.25 b 22.762.46 c
Cu2+ Cu2+ 20.441.62 a 13.390.67 b 13.210.64 b 19.532.54 a
Pb2+ Pb2+ 21.191.32 b 22.751.34 b 21.380.14 b 24.403.43 a
Zn2+ Zn2+ 14.161.56 b 7.940.34 c 20.370.16 a 20.130.84 a
Cd2+ +Cu2+ Cd2+ 1.840.33 c 1.880.34 c 8.530.23 b 11.121.07 a
Cu2+ 4.290.64 c 5.251.63 c 12.450.18 b 17.281.81 a
Cd2+ +Pb2+ Cd2+ 5.890.93 b 4.780.24 b 19.120.65 a 20.021.19 a
Pb2+ 14.190.91 c 12.881.65 c 22.350.91 b 24.893.45 a
Cd2+ +Zn2+ Cd2+ 3.820.68 c 5.251.27 c 10.681.10 b 16.742.03 a
Zn2+ 3.420.77 c 5.091.35 c 10.140.77 b 16.562.25 a
Cu2+ +Pb2+ Cu2+ 2.080.93 d 8.821.89 c 14.090.25 b 17.570.54 a
Pb2+ 6.280.81 d 12.342.45 c 21.370.48 b 24.030.46 a
Cu2+ +Zn2+ Cu2+ 3.970.60 c 7.801.89 b 10.860.66 a 13.882.32 a
Zn2+ 1.170.51 d 2.910.81 c 7.380.53 b 9.641.31 a
Pb2+ +Zn2+ Pb2+ 10.170.51 c 11.251.75 c 22.440.63 b 24.961.95 a
Zn2+ 1.850.93 d 4.421.41 c 12.540.67 b 15.580.79 a
2+ 2+ 2+
Cd +Cu +Pb Cd2+ 2.670.22 c 1.920.16 c 5.870.66 b 9.761.41 a
Cu2+ 3.830.32 c 5.020.18 c 9.580.61 b 16.832.78 a
Pb2+ 7.060.45 c 7.360.31 c 19.210.91 b 24.483.82 a
Cd2+ +Cu2+ +Zn2+ Cd2+ 1.670.62 b 1.400.08 b 2.990.81 b 7.481.48 a
Cu2+ 4.450.79 b 5.830.40 b 7.300.98 b 14.573.37 a
Zn2+ 2.220.47 b 1.840.09 b 3.741.18 b 8.311.69 a
Cd2+ +Pb2+ +Zn2+ Cd2+ 2.370.56 c 2.690.25 c 6.310.47 b 10.041.96 a
Pb2+ 10.270.14 c 11.330.54 c 19.650.50 b 24.681.91 a
Zn2+ 3.180.34 c 3.770.40 c 6.870.45 b 13.582.74 a
The initial concentrations of the Cu2+ Pb2+ Zn2+ Cu2+ 3.111.43 c 5.331.14 bc 7.130.46 b 11.952.77 a
metals were 100 mg L1 . The Pb2+ 5.761.32 b 7.441.23 b 15.630.58 a 17.403.85 a
values are mean standard
Zn2+ 1.991.02 c 2.771.23 bc 4.490.63 b 7.041.82 a
deviation (n=3). Different letters
indicate that the results are Cd2+ +Cu2+ +Pb2+ +Zn2+ Cd2+ 0.690.53 c 1.380.40 bc 2.420.97 b 6.751.33 a
significantly different (p<0.05) Cu2+ 3.370.84 b 5.390.54 b 6.441.04 b 11.575.24 a
RD dried red ear, RH humid red Pb2+ 5.940.72 c 7.410.73 c 14.911.95 b 17.327.24 a
ear, SD dried silver ear, SH Zn2+ 1.850.56 b 2.040.53 b 3.450.96 b 11.424.24 a
humid silver ear

Table 3 Parameters of the pseudo first-order kinetic model fitting to the data of heavy metal biosorption by the jelly fungi

Treatment Ci (mgL1) Biosorbent qe exp

a
(mgg1) qe cal
a
(mgg1) Relative error of qe (%) k1 (min1) R

Cd2+ 10 RD 2.145 1.149 46 0.029 0.978

50 RD 8.074 6.411 21 0.049 0.863
100 RH 9.579 6.619 31 0.022 0.949
Cu2+ 10 RD 1.933 0.915 53 0.026 0.949
Pb2+ 10 RD 1.521 0.233 85 0.017 0.956
50 RD 11.342 5.089 55 0.033 0.931
Zn2+ 10 RD 2.132 1.188 44 0.034 0.917
50 SD 10.500 2.872 73 0.058 0.998
100 RH 4.017 7.745 93 0.076 0.947
100 SH 12.882 7.652 41 0.074 0.880

RD dried red ear, RH humid red ear, SD dried silver ear, SH humid silver ear
a
The amounts of heavy metal adsorption of the fungus at the equilibrium based on the experimental data and the fitting procedure, respectively
Appl Microbiol Biotechnol (2010) 88:9971005 1003

Table 4 Parameters of the pseudo second-order kinetic model fitting to the data of heavy metals biosorption by jelly fungi

Ci RD RH SD SH

qe k2 R2 qe k2 R2 qe k2 R2 qe k2 R2

Cd2+ 10 2.278 0.055 0.996 1.319 2.736 0.997 1.890 0.204 0.998 2.597 0.082 0.988
50 8.929 0.010 0.988 7.752 0.010 0.993 10.000 0.116 0.997 14.925 0.128 0.987
100 25.000 0.001 0.870 10.753 0.005 0.986 10.753 0.127 0.975 14.493 0.017 0.961
Cu2+ 10 2.028 0.071 0.996 1.445 0.184 0.985 2.096 0.125 0.996 1.855 0.210 0.964
50 6.944 0.013 0.966 8.065 0.009 0.979 8.621 0.129 0.997 17.857 0.008 0.994
100 17.241 0.004 0.925 8.621 0.016 0.989 9.524 0.021 0.996 16.393 0.155 0.987
Pb2+
10 1.504 0.522 0.999 1.253 0.245 0.973 1.427 0.051 0.960 2.058 0.187 0.992
50 11.905 0.014 0.998 9.091 0.083 0.966 11.236 0.014 0.997 16.949 0.018 0.994
100 19.608 0.010 0.989 14.085 0.025 0.969 19.608 0.021 0.999 29.412 0.064 0.938
Zn2+ 10 2.268 0.054 0.999 1.181 0.434 0.934 1.972 0.201 0.996 2.381 0.356 0.979
50 8.696 0.010 0.984 6.757 0.008 0.919 10.753 0.052 0.999 15.873 0.027 0.993
100 10.000 0.016 0.965 5.618 0.004 0.850 10.204 0.343 0.988 13.333 0.019 0.997

RD dried red ear, RH humid red ear, SD dried silver ear, SH humid silver ear

bond index for the classification of metal ions (Nieboer and
Mcbryde 1973). The covalent bond index is defined as:
Xm2 r 0:85a 7 kinetic model (Mata et al. 2009). The pseudo second-order
where Xm is the electronegativity of ion, r is the ionic
radius, 0.85 is the constant of reflection ionic radius, and a
is the bond index. In this system, Pb2+ belongs to the b-
type ion, while Cd2+, Cu2+, Zn2+ belong to the border ions.
In general, the b group ions are characterized by larger
covalent bond index values, which have greater ability to
form covalent bonds with the biological ligand (Mohapatra
and Gupta 2005). Based on Eq. 7, the electronegatiivity
values of Pb2+, Cu2+, Zn2+, and Cd2+ are 2.33, 1.90, 1.65,
and 1.69, respectively. In addition, the antagonism between
Cd2+ and Zn2+ (Akhtar et al. 1996), and hydrolysis constant
series (Pagnanelli et al. 2003) make the adsorption
capacities in the multi-metal system be in the order of
Cu2+ >Zn2+ >Cd2+. Similar results were demonstrated in
consisting of the dissociation of these complexes and the
interaction of metals with active sites in the biosorbents, can
explain the better applications of the pseudo second-order
model has been successfully used to describe chemisorptions
involving valency forces through sharing or exchanging
electrons between the adsorbent and adsorbate, and through
exchanging electrons among the particles involved (Klc et
al. 2009). The good fitting results using the pseudo second-
order model suggested that the metals be adsorbed by the
jelly fungi through these mechanisms.
Metal adsorption by other biomaterials, such as the
Agaricales mushrooms (A. bisporus, L. edodes, and P.
ostreatus), have been reported in the literature. The adsorption
3.0
RD RH SD SH
Adsorption amount (mg.g-1)

2.5 AB LE PO

mutli-metal system biosorption of Mucor rouxii (Yan and

2.0
Viraraghavan 2003).
In general, the pseudo first-order kinetic model does not fit 1.5
well to the whole range of an adsorption process and is usually
applicable over the initial stage of the process, whereas the 1.0

pseudo second-order model fits experimental results better 0.5

(Bulut et al. 2008; Gupta and Rastogi 2008; Klc et al.
2009). The poorer fitting results of the pseudo first-order 0.0
Cd2+ Cu2+ Pb2+ Zn2+
model indicated that biosorption was not occurring exclu- Heavy metal
sively onto one site per ion, and more than one mechanism
were involved in the adsorption process (Nuhoglu and Fig. 2 Adsorption amounts of Cu2+, Cd2+, Pb2+, and Zn2+ on the jelly
fungi and Agaricales mushrooms. RD dried red ear, RH humid red ear,
Malkoc 2009). Cadmium, lead, and copper are mainly
SD dried silver ear, SH humid silver ear, AB Agaricus bisporus, LE
existed as hydrated complexes in solutions rather than as Lentinu edodes, PO Pleurotus ostreatus. These data are calculated
dissociated ions. Therefore, a two-step biosorption process, from pseudo second-order model, so there is no error bar in Fig. 2
1004
amounts of Cd2+ and Pb2+ by A. bisporus were 29.67 and
33.78 mg g1, respectively (Vimala and Das 2009). The
maximum adsorption amounts of Cd2+ by A. bisporus and
L. edodes were 2.08 and 0.716 mg g1, respectively
(Mathialagan et al. 2003). The maximum adsorption rates of
Cu2+and Pb2+ by mushroom A. macrosporus were 96% and
89%, respectively (Melgar et al. 2007). In our case, the
adsorption rates of Pb2+, Cd2+, Cu2+, and Zn2+ by SH reached
97.8%, 91.1%, 78.1%, and 80.5%, respectively. However,
it must be cautious to compare the results in the literature
because the experimental conditions used (metal concentra-
tions, solution volumes, pH, temperature, amount of
biosorbent, etc.) can be widely different. The absence of a
uniform methodology often makes quantitative comparisons
almost impossible (Melgar et al. 2007). Therefore, we
compared the adsorption amounts of Cd2+, Cu2+, Pb2+, and
Zn2+ by the jelly fungi with those by the Agaricales
mushrooms under the same experimental conditions. The
higher Cd2+, Cu2+, Zn2+, and Pb2+ removal efficiency of the
jelly fungi was attributable to the polysaccharide gel matrixes,
such as glucuronoxylomannan, in the jelly fungi. The
polysaccharide glucuronoxylomannan of jelly fungi is
consisted of a linear backbone of 1,3-linked alpha-D-mannose
with mainly xylose and glucuronic acid in side chains
(Khondkar et al. 2002; Sun et al. 2010). It is known that
polysaccharide gel matrixes such as alginate is responsible for
the high metal uptakes of brown algae when compared with
other algae, bacteria and fungi (Mata et al. 2009). Alginates are
linear polysaccharides composed of (1,4)-linked mannuronic
acid and guluronic acid (Cao et al. 2007). Probably, the
glucuronic acid residues are responsible for the metal
adsorption by the jelly fungi.
The conventional treatment processes for industrial effluents
are neither effective nor economical (Amini et al. 2008).
Chemical precipitation of heavy metals produces large amount
of sludge and is ineffective when metal ion concentrations are
lower than 100 mg L1 (Wang and Chen 2006). Solvent
extraction techniques are not suitable for effluents with low
heavy metal concentrations (Mameri et al. 1999). In addition,
multi-metal contamination is a common problem in the
industrial effluents (Gikas 2008). The humid silver ear
presents excellent capacity to remove metals from single-
metal and mixed-metal solutions. In addition, dried silver ear
can survive a long period of drought. When moisture is
available, the fungi absorb water and become gelatinous.
Compared with other Agaricales, jelly fungi show higher
growth rates, higher yields and lower prices (Huang 1982).
Therefore, T. fuciformis should be useful for the treatment of
wastewaters containing Cd2+, Cu2+, Pb2+, and Zn2+.
Acknowledgements This work was partly supported by grants from
the Fundamental Research Funds for the Central Universities, the
Natural Science Foundation of Guangdong Province (No. 06202438),
Appl Microbiol Biotechnol (2010) 88:9971005
and the Chinese National Natural Science Foundation (No.
50779080).
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