Biosorption of lead(II) and copper(II) from aqueous solutions by

pre-treated biomass of Australian marine algae

Jose T. Matheickal, Qiming Yu
*
School of Environmental Engineering, Grith University, Nathan, Brisbane, 4111 Queensland, Australia
Received 15 October 1997; revised 11 December 1998; accepted 12 December 1998
Abstract
Chemically modied biomass of marine algae can eectively remove heavy metals from waste water. Australian marine algae
(Durvillaea potatorum and Ecklonia radiata) based biosorbents (DP95Ca and ER95Ca) were developed and studied for their heavy
metal removal properties from aqueous solutions. A two stage modication process substantially improved the leaching charac-
teristics of the biomass. Batch equilibrium experiments showed that the maximum adsorption capacities of DP95Ca for lead and
copper were 1.6 and 1.3 mmol/g, respectively. The corresponding values for ER95Ca were 1.3 and 1.1 mmol/g. These capacities are
comparable with those of commercial ion exchange resins and are much higher than those of natural zeolites and powdered acti-
vated carbon. The heavy metal uptake process was found to be rapid with 90% of the adsorption completed in about 10 min in batch
conditions. Heavy metal adsorption was observed at pH values as low as 2.0 and maximum adsorption was obtained approximately
at a pH of 4.5. Both biosorbents were eective in removing lead and copper in the presence of chelating agents and other light metal
ions in waste water. 1999 Elsevier Science Ltd. All rights reserved.
Keywords: Biosorbent; Biosorption; Lead; Copper; Marine algae; Durvillaea potatorum; Ecklonia radiata
1. Introduction
Pollution of the environment by toxic heavy metals
arises as a result of many activities, largely industrial,
although sources such as agriculture and sewage dis-
posal also contribute. A number of methods exist for the
removal of heavy metal pollutants from liquid wastes
when they are present in high concentrations. These
include methods such as precipitation, evaporation,
electroplating, ion exchange and membrane processes.
However, identifying practical and cost-eective
means of removing such contaminants at very low
concentrations is much more dicult. Processes that are
otherwise suitable at high concentrations are often either
ineective or cost prohibitive when applied to dilute
wastes with heavy metal concentrations of less than 100
mg/l (Volesky, 1990). This has led to a growing interest
in the application of biosorption technology for the re-
moval of trace amounts of toxic metals from dilute
aqueous solutions.
Biosorption utilises the ability of biological materials
to accumulate heavy metals from waste water by either
metabolically mediated, or physico-chemical pathways
of uptake (Fourest and Roux, 1992). It has been known
that heavy metal ions are accumulated by micro-or-
ganisms, and a number of investigators have shown that
micro-organisms are valuable tools in removing and
recovering heavy metals from waste streams (Cheng
et al., 1975; Higham et al., 1985; Darnall et al., 1986;
Huang et al., 1988; Xue et al., 1988).
Because of the many problems inherent in maintain-
ing active microbial populations under highly variable
conditions of waste waters, living systems are often
unreliable. However, certain types of microbial biomass,
even in non-living form, can serve as a basis for devel-
opment of biosorbent materials for the ecient removal
of heavy metals (Volesky, 1987; Niu et al., 1993; Mur-
aleedharan et al., 1995; Matheickal and Yu, 1996a). A
number of workers investigated the feasibility of using
cheaply available marine or fresh water algae for heavy
metal removal (Darnall et al., 1986; Holan et al., 1993).
These studies revealed an interesting potential associat-
ed with certain algal species such as Sargassam natans,
Ascophyllum nodosum and Chlorella vulgaris. The
mechanism of biosorption has been identied as
Bioresource Technology 69 (1999) 223229
*
Corresponding author. Tel:. 00 61 7 3875 5289; fax: 00 61 7 3875
7459; e-mail: jimmy.yu@mailbox.gu.edu.au
0960-8524/99/$ see front matter 1999 Elsevier Science Ltd. All rights reserved.
PII: S 0 9 6 0 - 8 5 2 4 ( 9 8 ) 0 0 1 9 6 - 5
predominantly one of ion exchange although other
mechanisms such as precipitation could contribute to
the overall metal uptake marginally (Kuyucak and Vo-
lesky, 1989). The non-living biosorbents can be re-used
after regenerating the exhausted biosorbent using a
suitable eluent. This avoids the problems associated with
disposal of the metal-loaded biosorbent into a landll or
burning the biomass for recovering the metals.
Recently, Aderhold et al. (1996) reported the use of
biomass of a brown marine alga (Durvillaea potatorum)
for heavy metal removal. However, the applications of
the native biomass were found to be limited due to
leaching of alginate into the solution and subsequent
blocking of the columns packed with native biomass. It
is known that alginates play a signicant role in heavy
metal uptake by algal biomass (Kuyucak and Volesky,
1989) and the leaching of alginate out of the biomass
may lead to a loss of adsorption capacity of the biomass
(Fourest and Volesky, 1996). Hence, chemical modi-
cation of the biomass to increase the stability of the
native biomass materials will signicantly facilitate the
application of biosorbent materials for metal recovery.
Studies on heavy metal uptake properties of two
marine algae based biosorbents (DP95Ca and ER95Ca)
that were developed by chemically modifying the bio-
mass of the marine algae Durvillaea potatorum and
Ecklonia radiata are presented in this paper. Both
D. potatorum and E. radiata are ubiquitous marine algae
in the high wave-exposed areas of Australia and New
Zealand. They support a high biomass yield relative to
many other marine and terrestrial ecosystems. For ex-
ample, 273,000 ton (wet wt) of D. potatorum is exported
yearly from King Island, Tasmania (Virtue and Nichols,
1994).
The biosorbents were obtained by a two-stage process
of thermal and chemical modication of the raw bio-
mass. The pre-treatment process prevents leaching of
alginate from the biomass and increases the stability of
the biosorbent material. This work showed that the bi-
osorbents (ER95Ca and DP95Ca) developed can accu-
mulate high amounts of lead and copper from aqueous
solutions.
2. Materials and methods
Sun-dried samples of D. potatorum (DP) in the
ground form was supplied by Kelp Industries, King Is-
land, Tasmania, Australia. These algal samples were
harvested in the month of June from the coast of King
Island. Samples of E. radiata (ER) were collected in the
same period, from the coast of Hastings Point, northern
New South Wales, Australia. Pre-treatment of the bio-
mass samples was carried out as follows: A sample of 20
g of native biomass (300600 lm) was treated with 400
ml of 0.2 M CaCl
2
solution for 24 h under slow stirring.
The solution pH was kept constant at pH 5.0 using 0.1
M HNO
3
. The calcium treated biomass was washed
several times with deionised water to remove excess
calcium ions from the biomass. The biomass was then
dried in an oven at 100C for 24 h. The biosorbents
developed from D. potatorum and E. radiata were des-
ignated as DP95Ca and ER95Ca, respectively.
For equilibrium studies, a series of asks were pre-
pared containing heavy metal solutions (100 ml) of
known concentrations, varying from 0.4 to 4.5 mM.
Amounts (200 mg) of pre-treated biomass were added to
the asks and the mixtures agitated on a rotary shaker
for 24 h. The pH controlled experiments were conducted
by adjusting the pH of the solutions using 0.1 M HNO
3
or 0.1 M NaOH before and after the addition of bio-
mass and also during the equilibrium period. The ex-
periments were performed at room temperature
(21 2C). The biomass was removed by ltration
through a 0.45 lm membrane lter (Millipore), and the
ltrates analysed for heavy metal concentrations by
atomic absorption spectrometry (Spectra AA-20Plus,
Varian, Australia).
The eects of light metal ions and anionic ligands
were studied by using 2g/l of biosorbent and 1 mM
heavy metal solution containing the respective light
metal or anionic ligand and agitating the mixture on a
rotary shaker until equilibrium. Blank samples without
light metals or anions were used as controls.
The leaching characteristics of native and modied
biomass (DP95Ca and ER95Ca) were studied in the
presence of dierent concentrations of heavy metal ions
and at dierent pH values. The total organic carbon
(TOC) of the aqueous phase, which was in contact with
the biosorbent for 24 h under dierent experimental
conditions, was taken as the measure of the total
strength of organic leachate. The TOC was measured
using a total organic carbon analyser (DC-190, Rose-
mount-Dohrmann, Germany) tted with an autosam-
pler.
Kinetic experiments were conducted for dierent
initial heavy metal concentrations. Pre-wetted bi-
osorbent samples (1 g) were added to continuously
stirred beakers (200 rpm) containing 500 ml of heavy
metal solution. Samples of 1 ml solution were with-
drawn at pre-determined time intervals using a syringe
tted with a membrane lter and analysed for residual
heavy metal.
Packed bed experiments were conducted at room
temperature (21 2C) in a 1 cm ID glass column,
packed with pre-wetted biomass granules (2 g). Heavy
metal solution (2.4 mM of lead) was pumped through
the column by a peristaltic pump (Gilson Miniplus-3,
France) at a ow rate of 1.5 ml/min. Euent samples
for analysis were collected for every bed volume (6.6 ml)
by a programmable fraction collector (Gilson FC-204,
France) and analysed for heavy metal concentration.
224 J.T. Matheickal, Q. Yu / Bioresource Technology 69 (1999) 223229
All batch experiments were carried out in triplicate to
ensure statistical quality control and the values given are
mean of the experimental results. In addition, a separate
experiment was carried out using 24 lots of 0.2 g of bi-
osorbent samples in 100 ml of 2.5 mM metal solution, to
determine the reproducibility of metal adsorption by the
biosorbents and to determine the homogeneity of the
biosorbent samples. The results presented in describing
packed-bed experiments are those obtained from single
column runs as the number of variables involved made
averaging results from separate runs of little value.
However, the results are typical of three column runs.
3. Results and discussion
3.1. Homogeneity of biomass samples
The homogeneity of the biosorbent samples was in-
vestigated by using 24 lots of biosorbent samples. Each
lot (200 mg) was equilibrated with the same initial
concentration (2 mM) of the metal. The nal concen-
tration of the solution was measured after equilibrating
for 24 h. The relative standard deviations for the sam-
ples (l) were around 3.4 and 2.8 for lead and copper,
respectively, showing that the biosorbent samples were
rather homogeneous.
3.2. Adsorption equilibrium
The adsorption isotherms for DP95Ca and ER95Ca
for lead and copper individually present in the aqueous
phase at a solution pH of 4.0 are shown in Fig. 1. The
isotherms are rather steep at lower equilibrium concen-
trations implying the suitability of both biosorbents to
treat dilute heavy metal solutions. The adsorption iso-
therm plots have a typical shape of L-2 isotherms, in-
dicating a reduction in the number of active sites on the
adsorbents at a high residual heavy metal concentration
in the solution phase. Our earlier studies (Matheickal
and Yu, 1997) have shown that ion exchange with cell
wall-bound counter ions is the predominant mechanism
involved in heavy metal uptake by brown algae. The
isotherm can be described by the Langmuir equation:
q
bQ
max
c
1 bc
;
where q is the amount of heavy metal adsorbed per unit
weight (dry) of adsorbent, c the solution phase equilib-
rium concentration, Q
max
the maximum amount of ad-
sorption and b a constant. The Langmuir parameters
(Q
max
and b) were obtained for dierent equilibrium pH
values and listed in Table 1.
A comparison of the heavy metal uptake capacities
(Q
max
at pH 5.0) of DP95Ca and ER95Ca with those of
other adsorbents reported in the literature is given in
Table 2. Many of these adsorbents such as activated
carbon, natural zeolite and ion exchange resins have
been used in many practical metal recovery applications
(Blanchard et al., 1984; Arulanantham et al., 1989).
Although a direct comparison of DP95Ca and ER95Ca
with other reported biosorbents is dicult due to the
varying experimental conditions employed in those
studies, in general, the heavy metal uptake capacities of
DP95Ca and ER95Ca far exceeded the uptake capacities
of activated carbon, zeolite and other biosorbents and
are comparable with those of the commercial ion ex-
change resin.
3.3. Eect of pH on heavy metal uptake by biosorbents
It can be seen from Table 1 that the maximum ad-
sorption capacity (Q
max
) of the biosorbents increases
with solution pH. The eect of pH on heavy metal ad-
sorption is shown in Fig. 2. The sharpest increase in
Q
max
is obtained between pH 2 and 3, while around pH
4.5 a plateau is reached. Experiments were not con-
ducted beyond pH 5 to avoid heavy metal precipitation.
These results show the suitability of the biosorbent for
treatment of acidic waste waters.
In explaining the pH dependence of algal biosorbents
in heavy metal adsorption, it is important to consider
the ionic states of cell wall functional groups as well as
the heavy metal solution chemistry at various pH values.
However, both lead and copper are present in their free
ionic forms (Pb
2
and Cu
2
) at pH values less than 5.0.
This implies that the metal biosorption depends on the
protonation or deprotonation of the cell wall polymer
functional groups, relative to their pKa. The cell walls of
brown algae are chiey composed of three kinds of
polymer: cellulose, alginic acid and the heterogeneous
fucose-containing sulphated polysaccharides called fu-
cans (Clayton, 1981). These polymers can provide vari-
ous functional groups as binding sites for the metal ions.
Fig. 1. Lead and copper adsorption isotherms for modied biomass
(pH, 4.0; equilibrium time, 24 h; biomass dose, 2g/l; temperature,
21 2C).
J.T. Matheickal, Q. Yu / Bioresource Technology 69 (1999) 223229 225
At low pH, the protonation of the functional groups
gives an overall positive charge to the polymer molecules
unable to adsorb positively charged heavy metal ions.
The adsorption is reduced. Increasing the pH reduces
the electrostatic repulsion, exposing more ligands car-
rying negative charges. The adsorption is hence in-
creased at high pH.
3.4. Eect of light metal ions on biosorption
Industrial euents often contain large amounts of
light metal ions such as calcium, magnesium, sodium
and potassium along with the heavy metal ions. These
light metal ions often reduce the binding capacity of
commercial ion exchange resins. This eect can be less
signicant in biosorption systems. The eects of light
metal ions on lead and copper (initial concentration 1
mM) adsorption capacity of ER95Ca and DP95Ca were
studied and the results are shown in Figs. 3 and 4. The
eect of Na

and K

on copper uptake was marginal

even at a 10 mM concentration of these ions. Calcium
ions, at 10 mM concentration, reduced the removal
Fig. 3. Lead and copper removal eciencies of ER95Ca in the pres-
ence of light metal ions. (biomass dose, 2g/l; initial Cu
2
and Pb
2
concentrations, 1 mM; solution pH, 4.0; A Pb
2
; B Cu
2
).
Table 2
Comparison of lead and copper uptake capacities (Q
max
, mmol/g) of various adsorbents
Adsorbent Pb
2
Cu
2
Reference
Australian natural zeolite 0.08 Matheickal and Yu, 1996a
Powdered activated carbon 0.10 Matheickal and Yu, 1996b
Pseudomonas aeruginosa 0.33 0.29 Chang et al., 1997
Rhizopus arrhizus 0.50 0.25 Volesky, 1990
Granular activated carbon, F-400 0.15 0.03 Muraleedharan et al., 1995
Ion exchange resin (Duolite GT-73) 1.37 Volesky, 1994
DP95Ca (marine algae based) 1.55 1.30 This study
ER95Ca (marine algae based) 1.26 1.11 This study
Table 1
Langmuir parameters (Q
max
, mmol/g and b, 1/mM) for lead and copper adsorption onto pre-treated biomass
pH DP95Ca ER95Ca
Lead Copper Lead Copper
Q
max
b Q
max
b Q
max
b Q
max
b
(mmol/g) (1/mM) (mmol/g) (1/mM) (mmol/g) (1/mM) (mmol/g) (1/mM)
1 0.02 0.00 0.04 0.00 0.05 0.89 0.07 0.62
2 0.76 2.62 0.18 0.02 0.42 9.25 0.45 0.40
3 1.29 90.50 0.99 7.28 0.99 25.97 0.95 4.00
4 1.47 247.2 1.21 11.11 1.17 35.89 1.06 8.19
5 1.55 496.6 1.30 16.68 1.26 38.88 1.11 13.15
Fig. 2. Maximum heavy metal uptake capacity (Q
max
, mmol/g) of
ER95Ca and DP95Ca as a function of solution pH (Q
max
data from
Table 1).
226 J.T. Matheickal, Q. Yu / Bioresource Technology 69 (1999) 223229
eciency by around 1018%, while Mg
2
reduced the
eciency by around 510%. The results show that the
biosorbents have much higher relative anities for the
heavy metal ions than for the light metal ions studied.
3.5. Eect of anionic ligands on heavy metal adsorption
A number of anionic ligands are often found along
with heavy metals in industrial waste waters. The eects
of four types of anions, commonly encountered in ef-
uent streams, on copper uptake capacity of ER95Ca
(Fig. 5) were studied. For all the anions, sodium ion was
used as the cationic component, as it was observed
earlier that sodium ion did not inuence the biosorption
of copper ion. The pH of the solution was kept constant
at 5.0 during these studies.
The ligands exhibited only marginal inhibition even
at 20 mM concentration of these ions, except for EDTA.
At 1 mM concentration, EDTA inhibited copper uptake
substantially and at 5 mM concentration of EDTA the
copper uptake by ER95Ca was reduced to almost zero,
indicating strong association of the copper ions with
EDTA. On the other hand, it is possible that EDTA can
be used as an eective recovering agent for the copper
ions from the loaded biosorbent.
3.6. Organic leaching from biomass
Leaching of organics from biomass into the aqueous
phase has been reported in many biosorption studies
(Carvalho et al., 1994; Aderhold et al., 1996). Figs. 6
and 7 show the leaching of organics from native as well
as modied D. potatorum and E. radiata, respectively.
The organic leaching was high from the raw biomass in
all cases. However, the modied biomass showed low to
negligible leaching of organics even at low pH values
Fig. 5. Copper removal eciencies of ER95Ca in the presence of an-
ionic ligands (biomass dose, 2g/l; initial copper ion concentration, 1
mM; solution pH, 5.0).
Fig. 6. Organic leaching from raw and modied biomass (ER95Ca) at
dierent pH values and at dierent initial metal concentrations (bio-
mass dose, 2g/l; agitation time, 24 h; raw; - - - - - - modied).
Fig. 7. Organic leaching from raw and modied biomass (DP95Ca) at
dierent pH values and at dierent initial metal concentrations (bio-
mass dose, 2g/l; agitation time, 24 h; raw; - - - - - - modied).
Fig. 4. Lead and copper removal eciencies of DP95Ca in the pres-
ence of light metal ions. (biomass dose, 2g/l; initial Cu
2
and Pb
2
concentrations, 1 mM; solution pH, 4.0; A Pb
2
; B Cu
2
).
J.T. Matheickal, Q. Yu / Bioresource Technology 69 (1999) 223229 227
indicating stabilisation of the biomass attained through
the modication process.
Marine algae contain a high content of alginate
constituting 1440% of the dry weight of the biomass
(Percival and McDowell, 1967). The decreased solubility
after calcium treatment is mainly due to the crosslinking
reaction taking place in the alginate polymers. The
major component of the alginate is alginic acid, a
polymer composed of unbranched chains of 1,4-linked
b-D-mannuronic acid and a-L-guluronic acids. It is
known that the addition of calcium to alginate results in
a co-operative association of long regions of polymer
chains, leading to an ``egg box'' structure (Grant et al.,
1973). Such a structure will improve the stability of the
polymers. In addition, the improvement in stability can
be partially attributed to the heat treatment given to the
biomass. Such stability improvement has been previ-
ously reported for pure alginate treated with calcium
ions wherein an irreversible shrinkage of calcium cross-
linked polymers within the biomass was observed
(Vorlop and Klein, 1981).
3.7. Kinetics of biosorption and packed bed studies
From the kinetic experiment, a plot of heavy metal
concentration in the biosorbents versus time (Figs. 8
and 9) showed that rate of heavy metal uptake was
rather fast and 90% of the total uptake occurred in 30
min. However, after 30 min, there was a slower rate of
uptake to about 1 h and no further signicant adsorp-
tion was noted beyond the 1 h period. This was the same
for all the initial metal concentrations and for both bi-
osorbents studied.
Packed bed studies conducted with 2.4 mM lead so-
lution showed that both biosorbents were able to reduce
the metal concentration in aqueous phase to parts per
billion (ppb) levels. The typical euent history from a
column packed with 2 g of the biosorbent is shown in
Fig. 10. The concentration of lead in the euent was
below the detection limits (0.02 mg/l) of the AA spec-
trophotometer until column breakthrough. A total of
about 1000 ml of lead solution (2.4 mM) was passed
through the column before breakthrough. The total
adsorption capacities of the column for DP95Ca and
ER95Ca were calculated by graphically integrating the
column breakthrough curve until the saturation points.
The adsorption capacities were calculated to be 1.6 and
1.3 mmol/g, respectively, for DP95Ca and ER95Ca.
These values were very close to the values obtained for
batch equilibrium experiments (1.55 and 1.26 mmol/g,
respectively).
An important aspect about biosorption technology is
that the biosorbent can be regenerated using suitable
chemical eluents and the regenerated biomass can be re-
used in a number of cycles. In the case of DP95Ca and
ER95Ca, it was possible to regenerate the column using
nitric acid as an eluent and the biosorbents could be re-
used for subsequent metal removal. The regeneration
and recovery aspects are discussed elsewhere (Math-
eickal and Yu, 1997).
Fig. 8. Kinetics of lead adsorption by DP95Ca at dierent initial lead
concentrations, biomass dose 2g/l; temperature, 21 2C; agitation
rate, 200 rpm).
Fig. 9. Kinetics of copper adsorption by ER95Ca at dierent initial
copper concentrations, biomass dose 2g/l; temperature, 21 2C; ag-
itation rate, 200 rpm).
Fig. 10. Fixed bed breakthrough curves for lead removal by DP95Ca
and ER95Ca (biomass dose, 2 g; ow rate, 1.5 ml/min; column di-
ameter, 1 cm; packed bed height, 5 cm).
228 J.T. Matheickal, Q. Yu / Bioresource Technology 69 (1999) 223229
4. Conclusions
The study indicated that abundantly and cheaply
available brown marine algae from the Australian ma-
rine environment can be used for the development of
ecient biosorbent materials for heavy metal recovery
from wastewater. The modication of raw biomass
substantially improved the stability of the biomaterial.
The heavy metal adsorption capacities of DP95Ca and
ER95Ca are comparable with those of commercial ion-
exchange resins. Kinetic studies revealed that the rate of
metal uptake by the modied biomass was high even at
low initial concentrations. In contrast to some of the ion
exchange resins, the ions of hard water (Ca
2
and Mg
2
)
or monovalent cations (Na

and K

) do not signi-
cantly interfere with the binding of heavy metal ions.
The biosorbent appears to be well suited for treatment
of dilute waste streams, where extremely low levels of
euent standards are to be met. The biosorbent can be
used in packed bed operations and current facilities used
for adsorption and ion exchange process can be utilised
for its applications.
Acknowledgements
This work was supported in part by the Australian
Research Council (Small Grant Scheme) and an AusAid
Scholarship.
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